|
1
|
King MR, Colla S. Muscle Rehabilitation Techniques and Prevention of Injury. Vet Clin North Am Equine Pract 2025; 41:193-211. [PMID: 39788826 DOI: 10.1016/j.cveq.2024.11.010] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/12/2025] Open
Abstract
Rehabilitation following muscle injury is critical in restoring the equine athlete to full function. Rehabilitation protocols should be tailored to each patient's global functional assessment, taking into account sports-specific demands, goals for return-to-performance, and overall prognosis. Rehabilitation protocols are often designed to modulate pain, enhance repair, improve proprioception, increase flexibility, restore muscle strength, joint range-of-motion, and neuromotor control. This article will review mechanisms of muscle injury, various physical modalities commonly employed in the rehabilitation period following muscle injury, and injury prevention.
Collapse
Affiliation(s)
- Melissa R King
- Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Colorado State University Veterinary Teaching Hospital, Equine Orthopaedic Research Center, 2250 Gillette Drive, Fort Collins, CO 80523, USA.
| | - Sandro Colla
- Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Colorado State University Veterinary Teaching Hospital, Equine Orthopaedic Research Center, 2250 Gillette Drive, Fort Collins, CO 80523, USA
| |
Collapse
|
|
2
|
Rastogi M, Sahu K, Majumder SK. Light assisted modulation of stem cell function and secretome production: a systematic review on current status and new avenues for regenerative medicine. Lasers Med Sci 2025; 40:83. [PMID: 39934459 PMCID: PMC11814041 DOI: 10.1007/s10103-025-04339-5] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/29/2024] [Accepted: 01/29/2025] [Indexed: 02/13/2025]
Abstract
Stem cells (SC) based therapies are proving to be the mainstay of regenerative medicine. Despite the significant potential, direct grafting or implantation of SCs for regenerative therapy encounters various translational roadblocks such as paucity of implantable cells, decreased potency, cell death post-implantation, cell damage caused by the pre-existing inflammation and immune rejection. Hence, an emerging avenue is cell-free approach; use of SC secretome. Although priming approaches based on pharmacological molecules/chemicals, cytokines and growth factors are being explored to elicit enhanced secretome production, the potential concerns include the need for continuous replenishment and potential chemical contamination during secretome isolation. To alleviate these concerns, various non-pharmacological approaches for invigorating SCs are also being investigated and among these, use of photobiomodulation (PBM) has garnered considerable interest. Notwithstanding the positive outcomes, standardized parameters are yet to be established for reproducible results. Moreover, the mechanisms of PBM based SC stimulation and secretome production are poorly elucidated and significant knowledge gaps exist on influence of cell type, culture conditions on PBM. This review aims to provide insight into the current status of this emerging field emphasizing on novel avenues and potential challenges for clinical translation. We also summarize the studies on PBM based proliferation, differentiation and secretome production according to SC cell type and culture conditions. Further, as a fixed PBM based protocol for SC proliferation, differentiation and secretome is lacking, the knowledge on functional targets and pathways in PBM based SC stimulation needs upgradation. Consequently, putative mechanisms for PBM based SC secretome have been proposed.
Collapse
Affiliation(s)
- Mahima Rastogi
- Laser Biomedical Applications Division, Raja Ramanna Centre for Advanced Technology, Indore, Madhya Pradesh, 452013, India
- Homi Bhabha National Institute, Training School Complex, Anushakti Nagar, Mumbai, 400094, India
| | - Khageswar Sahu
- Laser Biomedical Applications Division, Raja Ramanna Centre for Advanced Technology, Indore, Madhya Pradesh, 452013, India.
- Homi Bhabha National Institute, Training School Complex, Anushakti Nagar, Mumbai, 400094, India.
| | - Shovan Kumar Majumder
- Laser Biomedical Applications Division, Raja Ramanna Centre for Advanced Technology, Indore, Madhya Pradesh, 452013, India
- Homi Bhabha National Institute, Training School Complex, Anushakti Nagar, Mumbai, 400094, India
| |
Collapse
|
|
3
|
Roets B, Abrahamse H, Crous A. The Application of Photobiomodulation on Mesenchymal Stem Cells and its Potential Use for Tenocyte Differentiation. Curr Stem Cell Res Ther 2025; 20:232-245. [PMID: 38847377 DOI: 10.2174/011574888x295488240319111911] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/28/2023] [Revised: 02/23/2024] [Accepted: 03/02/2024] [Indexed: 05/13/2025]
Abstract
Tendinopathy is a prevalent and debilitating musculoskeletal disorder. Uncertainty remains regarding its pathophysiology, but it is believed to be a combination of inflammation, damage, degenerative changes, and unsuccessful repair mechanisms. Cell-based therapy is an emerging regenerative medicine modality that uses mesenchymal stem cells (MSCs), their progeny or exosomes to promote tendon healing and regeneration. It is based on the fact that MSCs can be differentiated into tenocytes, the major cell type within tendons, and facilitate tendon repair. Photobiomodulation (PBM) is a non-invasive and potentially promising therapeutic technique that utilizes low-level light to alter intracellular processes and promote tissue healing and regeneration. Recent studies have examined the potential for PBM to improve MSC therapy use in tendinopathy by promoting viability, proliferation, and differentiation. As well as enhance tendon regeneration. This review focuses on Photobiomodulation and MSC therapy applications in regenerative medicine and their potential for tendon tissue engineering.
Collapse
Affiliation(s)
- Brendon Roets
- Laser Research Centre, Faculty of Health Science, University of Johannesburg, P.O. Box 17011, Doornfontein, Johannesburg, 2028, South Africa
| | - Heidi Abrahamse
- Laser Research Centre, Faculty of Health Science, University of Johannesburg, P.O. Box 17011, Doornfontein, Johannesburg, 2028, South Africa
| | - Anine Crous
- Laser Research Centre, Faculty of Health Science, University of Johannesburg, P.O. Box 17011, Doornfontein, Johannesburg, 2028, South Africa
| |
Collapse
|
|
4
|
Uysal BS, Sarıkaya B, Dizakar SÖA, Kaplanoğlu GT, Gümüşderelioğlu M. Investigation of healing strategies in a rat corneal opacity model with polychromatic light and stem cells injection. JOURNAL OF PHOTOCHEMISTRY AND PHOTOBIOLOGY. B, BIOLOGY 2024; 253:112874. [PMID: 38422971 DOI: 10.1016/j.jphotobiol.2024.112874] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 12/25/2023] [Revised: 02/13/2024] [Accepted: 02/22/2024] [Indexed: 03/02/2024]
Abstract
Corneal opacities are a major cause of vision loss worldwide. However, the current therapies are suboptimal to manage the corneal wound healing process. Therefore, there is an obvious need to develop new treatment strategies that are efficient in promoting wound healing in patients with severe corneal disorders. In this study, we investigated and compared the efficacy of adipose-derived mesenchymal stem cells (ADMSCs) and photobiomodulation (PBM) with polychromatic light in the NIR (600-1200 nm) alone and in combination, on corneal opacity, inflammatory response, and tissue architecture in a rat corneal opacity model created by mechanical injury. All animals were divided into four groups randomly following the injury: injury only (no treatment), ADMSCs treatment, PBM treatment and combined (ADMSCs+PBM) treatment (n = 12 eyes per group). At the 10th and 30th day following injury, corneal opacity formation, neovascularization, and corneal thickness were assessed. On the 30th day the harvested corneas were analyzed by transmission electron microscopy (TEM), histological evaluation, immunohistochemical (IHC) staining and real-time polymerase chain reaction (RT-PCR). On day 30, the corneal opacity score, neovascularization grade, and corneal thickness in all treatment groups were significantly lower in comparison with the untreated injured corneas. The TEM imaging and H&E staining together clearly revealed a significant enhancement in corneal regeneration with improved corneal microenvironment and reduced vascularization in the combined administration of PBM and ADMSCs compared to treatment of PBM and ADMSCs alone. In addition, the IHC staining, and RT-PCR analysis supported our hypothesis that combining ADMSCs therapy with PBM alleviated the inflammatory response, and significantly decreased scar formation compared to either ADMSCs or PBM alone during the corneal wound healing.
Collapse
Affiliation(s)
- Betül Seher Uysal
- Gazi University, Faculty of Medicine, Department of Ophthalmology, Ankara, Turkey
| | - Burcu Sarıkaya
- Balıkesir University, Faculty of Medicine, Department of Medical Genetics, Balıkesir, Turkey
| | | | - Gülnur Take Kaplanoğlu
- Gazi University, Faculty of Medicine, Department of Histology and Embryology, Ankara, Turkey
| | - Menemşe Gümüşderelioğlu
- Hacettepe University, Graduate School of Science and Engineering, Bioengineering Division, Ankara, Turkey.
| |
Collapse
|
|
5
|
Pasternak-Mnich K, Szwed-Georgiou A, Ziemba B, Pieszyński I, Bryszewska M, Kujawa J. Effect of photobiomodulation therapy on the morphology, intracellular calcium concentration, free radical generation, apoptosis and necrosis of human mesenchymal stem cells-an in vitro study. Lasers Med Sci 2024; 39:75. [PMID: 38383862 DOI: 10.1007/s10103-024-04008-z] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/14/2023] [Accepted: 01/30/2024] [Indexed: 02/23/2024]
Abstract
The aim of the study was to investigate the impact of multiwave locked system (MLS M1) emitting synchronized laser radiation at 2 wavelength simultaneous (λ = 808 nm, λ = 905 nm) on the mesenchymal stem cells (MSCs). Human MSCs were exposed to MLS M1 system laser radiation with the power density 195-318 mW/cm2 and doses of energy 3-20 J, in continuous wave emission (CW) or pulsed emission (PE). After irradiation exposure in doses of energy 3 J, 10 J (CW, ƒ = 1000 Hz), and 20 J (ƒ = 2000 Hz), increased proliferation of MSCs was observed. Significant reduction of Fluo-4 Direct™ Ca2+ indicator fluorescence over controls after CW and PE with 3 J, 10 J, and 20 J was noticed. A decrease in fluorescence intensity after the application of radiation with a frequency of 2000 Hz in doses of 3 J, 10 J, and 20 J was observed. In contrary, an increase in DCF fluorescence intensity after irradiation with laser radiation of 3 J, 10 J, and 20 J (CW, ƒ = 1000 Hz and ƒ = 2000 Hz) was also shown. Laser irradiation at a dose of 20 J, emitted at 1000 Hz and 2000 Hz, and 3 J emitted at a frequency of 2000 Hz caused a statistically significant loss of MSC viability. The applied photobiomodulation therapy induced a strong pro-apoptotic effect dependent on the laser irradiation exposure time, while the application of a sufficiently high-energy dose and frequency with a sufficiently long exposure time significantly increased intracellular calcium ion concentration and free radical production by MSCs.
Collapse
Affiliation(s)
- Kamila Pasternak-Mnich
- Department of Medical Rehabilitation, Faculty of Health Sciences, Medical University of Lodz, 251 Pomorska St., 92-213, Lodz, Poland.
| | - Aleksandra Szwed-Georgiou
- Department of General Biophysics, University of Lodz, 141/143 Pomorska St., 90-236, Lodz, Poland
- Department of Immunology and Infectious Biology, University of Lodz, 12/16 Banacha St., 90-236, Lodz, Poland
| | - Barbara Ziemba
- Department of Clinical Genetic, Medical University of Lodz, 251 Pomorska St., 92-213, Lodz, Poland
| | - Ireneusz Pieszyński
- Department of Medical Rehabilitation, Faculty of Health Sciences, Medical University of Lodz, 251 Pomorska St., 92-213, Lodz, Poland
| | - Maria Bryszewska
- Department of General Biophysics, University of Lodz, 141/143 Pomorska St., 90-236, Lodz, Poland
| | - Jolanta Kujawa
- Department of Medical Rehabilitation, Faculty of Health Sciences, Medical University of Lodz, 251 Pomorska St., 92-213, Lodz, Poland
| |
Collapse
|
|
6
|
Zhang F, Li Q, Qin W, Ren W, Zhu P, Jin Q, Li M. A study of the biological effects of low-level light. Lasers Med Sci 2024; 39:74. [PMID: 38383895 DOI: 10.1007/s10103-024-04018-x] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/30/2023] [Accepted: 02/10/2024] [Indexed: 02/23/2024]
Abstract
Low-level light therapy (LLLT), also known as photo biomodulation (PBM), is a type of optical therapy that uses red or near-infrared lasers or light-emitting diodes (LEDs) for medical treatment. The laser wavelengths involved in PBM typically range between 600-700 nm and 780-1100 nm, with power densities ranging between 5 mW/cm2 and 5 W/cm2. PBM is a series of biochemical cascades exhibited by biological tissues after absorbing a certain amount of energy from light. PBM has been widely used in clinical practice in the past 20 years, and numerous clinical trials have demonstrated its biological efficacy. However, the underlying mechanisms have not yet been fully explored. In this paper, we have summarized the research into PBM over the past two decades, to identify the important mechanisms of the biological effects of PBM from the perspective of molecular mechanisms, cellular levels, and tissue changes. We hope our study provide a theoretical basis for future investigations into the underlying mechanisms.
Collapse
Affiliation(s)
- Fan Zhang
- Hair Medical Research Center, Department of Dermatology and Venereology, Beijing Jishuitan Hospital, Capital Medical University, No. 31 of Xinjiekou East Street, Xicheng District, Beijing, 100035, China.
| | - Qiaoyu Li
- School of Clinical Medicine, Peking University School of Medicine, Beijing, 100191, China
| | - Wenxin Qin
- School of Clinical Medicine, Peking University School of Medicine, Beijing, 100191, China
| | - Wei Ren
- School of Clinical Medicine, Peking University School of Medicine, Beijing, 100191, China
| | - Peiqiu Zhu
- Hair Medical Research Center, Department of Dermatology and Venereology, Beijing Jishuitan Hospital, Capital Medical University, No. 31 of Xinjiekou East Street, Xicheng District, Beijing, 100035, China
| | - Qiuzi Jin
- Hair Medical Research Center, Department of Dermatology and Venereology, Beijing Jishuitan Hospital, Capital Medical University, No. 31 of Xinjiekou East Street, Xicheng District, Beijing, 100035, China
| | - Man Li
- Hair Medical Research Center, Department of Dermatology and Venereology, Beijing Jishuitan Hospital, Capital Medical University, No. 31 of Xinjiekou East Street, Xicheng District, Beijing, 100035, China
| |
Collapse
|
|
7
|
He L, Zheng Y, Liu M, Dong X, Shen L, He Y, An J, Zhang Y. Nd:YAG-photobiomodulation enhanced ADSCs multilineage differentiation and immunomodulation potentials. Lasers Med Sci 2023; 38:190. [PMID: 37608016 PMCID: PMC10444653 DOI: 10.1007/s10103-023-03818-x] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/04/2022] [Accepted: 06/17/2023] [Indexed: 08/24/2023]
Abstract
To investigate the effects of Nd: YAG (1064 nm) photobiomodulation on multilineage differentiation and immunomodulation potentials of adipose tissue-derived stem cells (ADSCs) in vitro and in vivo. For in vitro experiments, cells were divided into the control group (non-irradiated control ADSCs) and photobiomodulation groups. 0.5 J/cm2, 1 J/cm2, 2 J/cm2, and 4 J/cm2 were used for proliferation assays; for ADSCs adipogenic differentiation assays, 0.5 J/cm2, 1 J/cm2 were applied; 1 J/cm2 was used for migration and immunomodulation assays. The differentiation abilities were assessed by qPCR, Oil Red O staining, and Alizarin Red staining. The immunomodulation potential was assessed by qPCR and human cytokine array. DSS-induced colitis model. was used to test the effect of photobiomodulation on ADSCs immunomodulation potentials in vivo. Nd:YAG-based photobiomodulation dose-dependently promoted ADSCs proliferation and migration; 1 J/cm2 showed the best promotion effect on proliferation. Moreover, Nd:YAG photobiomodulation promoted ADSCs osteogenic differentiation and brown adipose adipogenic differentiation. The potential immunomodulation assays showed Nd:YAG photobiomodulation improved Anti-inflammation capacity of ADSCs and photobiomodulation irradiated ADSCs effectively alleviated DSS-induced colitis severity in vivo. Our study suggests Nd:YAG photobiomodulation might enhance the ADSCs multilineage differentiation and immunomodulation potentials. These results might help to enhance ADSCs therapeutic effects for clinical application. However, further studies are needed to explore the mechanisms of Nd:YAG photobiomodulation promoting multilineage differentiation and immunomodulation potentials of ADSCs.
Collapse
Affiliation(s)
- Linhai He
- First Clinical Division, Peking University School and Hospital of Stomatology & National Center for Stomatology & National Clinical Research Center for Oral Diseases & National Engineering Research Center of Oral Biomaterials and Digital Medical Devices, Beijing, People's Republic of China
| | - Yi Zheng
- Department of Oral and Maxillofacial Surgery, Peking University School and Hospital of Stomatology & National Center for Stomatology & National Clinical Research Center for Oral Diseases & National Engineering Research Center of Oral Biomaterials and Digital Medical Devices, 22 Zhongguancun Nandajie, Haidian District, Beijing, 100081, People's Republic of China
| | - Meng Liu
- Laser and Cosmetic Surgery Division, Peking University School and Hospital of Stomatology & National Center for Stomatology & National Clinical Research Center for Oral Diseases & National Engineering Research Center of Oral Biomaterials and Digital Medical Devices, Beijing, People's Republic of China
| | - Xian Dong
- Department of Oral and Maxillofacial Surgery, Peking University School and Hospital of Stomatology & National Center for Stomatology & National Clinical Research Center for Oral Diseases & National Engineering Research Center of Oral Biomaterials and Digital Medical Devices, 22 Zhongguancun Nandajie, Haidian District, Beijing, 100081, People's Republic of China
| | - Lihang Shen
- Department of Oral and Maxillofacial Surgery, Peking University School and Hospital of Stomatology & National Center for Stomatology & National Clinical Research Center for Oral Diseases & National Engineering Research Center of Oral Biomaterials and Digital Medical Devices, 22 Zhongguancun Nandajie, Haidian District, Beijing, 100081, People's Republic of China
| | - Yang He
- Department of Oral and Maxillofacial Surgery, Peking University School and Hospital of Stomatology & National Center for Stomatology & National Clinical Research Center for Oral Diseases & National Engineering Research Center of Oral Biomaterials and Digital Medical Devices, 22 Zhongguancun Nandajie, Haidian District, Beijing, 100081, People's Republic of China
| | - Jingang An
- Department of Oral and Maxillofacial Surgery, Peking University School and Hospital of Stomatology & National Center for Stomatology & National Clinical Research Center for Oral Diseases & National Engineering Research Center of Oral Biomaterials and Digital Medical Devices, 22 Zhongguancun Nandajie, Haidian District, Beijing, 100081, People's Republic of China
| | - Yi Zhang
- Department of Oral and Maxillofacial Surgery, Peking University School and Hospital of Stomatology & National Center for Stomatology & National Clinical Research Center for Oral Diseases & National Engineering Research Center of Oral Biomaterials and Digital Medical Devices, 22 Zhongguancun Nandajie, Haidian District, Beijing, 100081, People's Republic of China.
| |
Collapse
|
|
8
|
Carr BJ. Regenerative Medicine and Rehabilitation Therapy in the Canine. Vet Clin North Am Small Anim Pract 2023; 53:801-827. [PMID: 36997410 DOI: 10.1016/j.cvsm.2023.02.011] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 03/30/2023]
Abstract
Regenerative medicine is used in the canine to optimize tissue healing and treat osteoarthritis and soft tissue injuries. Rehabilitation therapy is also often implemented in the treatment and management of musculoskeletal conditions in the canine. Initial experimental studies have shown that regenerative medicine and rehabilitation therapy may work safely and synergistically to enhance tissue healing. Although additional study is required to define optional rehabilitation therapy protocols after regenerative medicine therapy in the canine, certain fundamental principles of rehabilitation therapy still apply to patients treated with regenerative medicine.
Collapse
|
|
9
|
Chen X, Yu W, Zhang J, Fan X, Liu X, Liu Q, Pan S, Dixon RAF, Li P, Yu P, Shi A. Therapeutic angiogenesis and tissue revascularization in ischemic vascular disease. J Biol Eng 2023; 17:13. [PMID: 36797776 PMCID: PMC9936669 DOI: 10.1186/s13036-023-00330-2] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/08/2022] [Accepted: 02/06/2023] [Indexed: 02/18/2023] Open
Abstract
Ischemic vascular disease is a major healthcare problem. The keys to treatment lie in vascular regeneration and restoration of perfusion. However, current treatments cannot satisfy the need for vascular regeneration to restore blood circulation. As biomedical research has evolved rapidly, a variety of potential alternative therapeutics has been explored widely, such as growth factor-based therapy, cell-based therapy, and material-based therapy including nanomedicine and biomaterials. This review will comprehensively describe the main pathogenesis of vascular injury in ischemic vascular disease, the therapeutic function of the above three treatment strategies, the corresponding potential challenges, and future research directions.
Collapse
Affiliation(s)
- Xinyue Chen
- grid.412455.30000 0004 1756 5980The Second Clinical Medical College of Nanchang University, The Second Affiliated Hospital of Nanchang University, Nanchang, 330006 Jiangxi China
| | - Wenlu Yu
- grid.260463.50000 0001 2182 8825School of Ophthalmology and Optometry of Nanchang University, Nanchang, 330006 China
| | - Jing Zhang
- grid.412455.30000 0004 1756 5980Department of Anesthesiology, The Second Affiliated Hospital of Nanchang University, Nanchang, 330006 Jiangxi China
| | - Xiao Fan
- grid.412455.30000 0004 1756 5980Department of Anesthesiology, The Second Affiliated Hospital of Nanchang University, Nanchang, 330006 Jiangxi China
| | - Xiao Liu
- grid.412536.70000 0004 1791 7851Department of Cardiovascular Medicine, The Second Affiliated Hospital of Sun Yat Sen University, Guangzhou, 51000 Guangdong China
| | - Qi Liu
- grid.416470.00000 0004 4656 4290Wafic Said Molecular Cardiology Research Laboratory, The Texas Heart Institute, Houston, TX USA
| | - Su Pan
- grid.416470.00000 0004 4656 4290Wafic Said Molecular Cardiology Research Laboratory, The Texas Heart Institute, Houston, TX USA
| | - Richard A. F. Dixon
- grid.416470.00000 0004 4656 4290Wafic Said Molecular Cardiology Research Laboratory, The Texas Heart Institute, Houston, TX USA
| | - Pengyang Li
- grid.224260.00000 0004 0458 8737Division of Cardiology, Pauley Heart Center, Virginia Commonwealth University, Richmond, VA USA
| | - Peng Yu
- The Second Clinical Medical College of Nanchang University, The Second Affiliated Hospital of Nanchang University, Nanchang, 330006, Jiangxi, China. .,Department of Endocrinology and Metabolism, The Second Affiliated Hospital of Nanchang University, Nanchang, Jiangxi Province, 330006, China.
| | - Ao Shi
- School of Medicine, St. George University of London, London, UK. .,School of Medicine, University of Nicosia, Nicosia, Cyprus.
| |
Collapse
|
|
10
|
Zafari J, Jouni FJ, Nikzad F, Esmailnasab S, Javan ZA, Karkehabadi H. Combination of Dental-Capping Agents with Low Level Laser Therapy Promotes Proliferation of Stem Cells from Apical Papilla. Photobiomodul Photomed Laser Surg 2023; 41:3-9. [PMID: 36577035 DOI: 10.1089/photob.2022.0072] [Citation(s) in RCA: 2] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/29/2022] Open
Abstract
Background: Direct pulp capping is a vital pulp therapy, which stimulates differentiation of stem cells from apical papilla (SCAPs). SCAPs have multipotential capacity to differentiate into types of cells, contributing to the regeneration of tissues. Objective: Considering the promising effects of dental-capping materials, we aim to investigate the effect of dental dressing materials combined with laser therapy on the percentage of SCAP viability and the consequent dental regeneration capacity. Methods: We collected two immature third molar teeth and isolated SCAPs through collagenase type I enzymatic activity. Isolated SCAPs were then cultured with Dulbecco's modified Eagle's medium and α-minimum essential medium enriched with 15% and 10% fetal bovine serum, respectively. After reaching 70-80% confluency, cells were seeded in a 96-well plate and then treated with mineral trioxide aggregate (MTA), enamel matrix derivative (EMD), biodentine, and low level laser therapy (LLLT) alone and in combination for 24, 48, and 168 h. After that, cell survival rate was assessed using (3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide) (MTT) assay. Results: We found that combination of MTA, EMD, and LLLT as well as that of biodentine, EMD, and LLLT could lead to significant increase of SCAP viability as compared with other treatment groups. Combination of MTA and biodentine with EMD could also show increased level of SCAP proliferation and viability. However, MTA and biodentine alone reduced SCAP survival rate in all time points. Conclusions: Our conclusion is that LLLT can serve as an enhancer of SCAP proliferation and differentiation rate when added to dental-capping agents such as MTA, EMD, and biodentine. Thus, LLLT combination with effective capping materials will serve as a promising option for dental tissue repair.
Collapse
Affiliation(s)
- Jaber Zafari
- Laser Application in Medical Sciences Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran.,Department of Pharmacology and Toxicology, Faculty of Pharmacy, Tehran Medical Sciences, Islamic Azad University, Tehran, Iran
| | - Fatemeh Javani Jouni
- Department of Biochemistry and Biophysics, Faculty of Advanced Sciences and Technology, Tehran Medical Sciences, Islamic Azad University, Tehran, Iran
| | - Forough Nikzad
- Department of Endodontics, Dental School, Hamadan University of Medical Science, Hamadan, Iran
| | - Sogand Esmailnasab
- Department of Endodontics, Dental School, Hamadan University of Medical Science, Hamadan, Iran
| | - Zahra Abbasi Javan
- Department of Endodontics, Dental School, Hamadan University of Medical Science, Hamadan, Iran
| | - Hamed Karkehabadi
- Department of Endodontics, Dental School, Hamadan University of Medical Science, Hamadan, Iran
| |
Collapse
|
|
11
|
Ebrahimi-Kia Y, Noori-Zadeh A, Rajaei F, Darabi S, Darabi L, Ghasemi Hamidabadi H. The Effect of bisphenol A and Photobiomodulation Therapy on Autophagy-Related Genes Induction in Adipose Tissue-Derived Stem Cells. J Lasers Med Sci 2022; 13:e15. [DOI: 10.34172/jlms.2022.15] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/11/2021] [Accepted: 12/18/2021] [Indexed: 11/09/2022]
Abstract
Introduction: As adipose tissue-derived stem cells (ADSCs) can divide rapidly and be prepared non-invasively, they have extensively been used in regenerative medicine. On the other hand, a new method of therapy, known as photobiomodulation (PHT), has been used to treat many diseases, such as inflammatory conditions, wound healing and pain. Besides, exposure to chemical substances such as bisphenol A (BPA), at low levels, can lead to autophagy. This study investigated the effects of BPA and PHT on the expression of autophagy-related genes, including LC3, NRF2, P62, in rat ADSCs as a model. Methods: ADSCs isolation and purification were confirmed by immunocytochemistry (ICC). The cells were then treated with different concentrations of BPA and also subjected to PHT. Reverse transcription polymerase chain reaction (RT-PCR) was used for the evaluation of LC3, NRF2 and P62 gene expressions. Oil red O staining was used for adipogenic vacuole formation. Result: ICC showed that the isolated cells were CD 49-positive but CD 31 and CD 34-negative. The viability test indicated that the number of live cells after 24 hours in the BPA groups at concentrations of 0, 1, 50, 100 and 200 μM was 100%, 93%, 81%, 72%, and 43% respectively. The difference in cell viability between groups 50, 100 and 200 μM was significant as compared with the control groups (P<0.05). Moreover, in the group with 1 μM concentration of BPA, the expressions of LC3, NRF2 and P62 genes were upregulated. However, in the treatment group at the concentration of 200 μM of BPA, the LC3 gene was expressed, but NRF2 and P62 genes were downregulated. Conclusion: BPA and PHT induce autophagy and adiposeness in ADSCs in a dose-dependent manner.
Collapse
Affiliation(s)
| | - Ali Noori-Zadeh
- Department of Clinical Biochemistry, Faculty of Medicine, Ilam University of Medical Sciences, Ilam, Iran
- Student Research Committee, Ilam University of Medical Sciences, Ilam, Iran
| | - Farzad Rajaei
- Cellular and Molecular Research Center, Research Institute for Non-Communicable Diseases, Qazvin University of Medical Sciences, Qazvin, Iran
| | - Shahram Darabi
- Cellular and Molecular Research Center, Research Institute for Non-Communicable Diseases, Qazvin University of Medical Sciences, Qazvin, Iran
| | - Leila Darabi
- Department of Neurology, Islamic Azad University Tehran Medical branch (IAUTMU), Tehran, Iran
| | - Hatef Ghasemi Hamidabadi
- Department of Anatomy & Cell Biology, Faculty of Medicine, Mazandaran University of Medical Sciences, Sari, Iran
| |
Collapse
|
|
12
|
Effectiveness of preconditioned adipose-derived mesenchymal stem cells with photobiomodulation for the treatment of diabetic foot ulcers: a systematic review. Lasers Med Sci 2021; 37:1415-1425. [PMID: 34697696 DOI: 10.1007/s10103-021-03451-6] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/30/2021] [Accepted: 10/19/2021] [Indexed: 10/20/2022]
Abstract
The primary goal of this systematic review article was to provide an outline of the use of diabetic autologous adipose-derived mesenchymal stem cells (DAAD-MSCs) in the treatment of wounds and ulcers in animal models and patients with diabetes mellitus (DM). The secondary goal was to present the outcomes of pretreatment of diabetic adipose-derived mesenchymal stem cells (DAD-MSCs) with probable different agents in the treatment of diabetic foot ulcers (DFUs) and wounds. In view of possible clinical applications of AD-MSC-mediated cell therapy for DFUs, it is essential to evaluate the influence of DM on AD-MSC functions. Nevertheless, there are conflicting results about the effects of DAAD-MSCs on accelerating wound healing in animals and DM patients. Multistep research of the MEDLINE, PubMed, Embase, Clinicaltrials.gov, Scopus database, and Cochrane databases was conducted for abstracts and full-text scientific papers published between 2000 and 2020. Finally, 5 articles confirmed that the usage of allogeneic or autologous AD-MSCs had encouraging outcomes on diabetic wound healing. One study reported that DM changes AD-MSC function and therapeutic potential, and one article recommended that the pretreatment of diabetic allogeneic adipose-derived mesenchymal stem cells (DAlD-MSCs) was more effective in accelerating diabetic wound healing. Recently, much work has concentrated on evolving innovative healing tactics for hastening the repair of DFUs. While DM alters the intrinsic properties of AD-MSCs and impairs their function, one animal study showed that the pretreatment of DAlD-MSCs in vitro significantly increased the function of DAlD-MSCs compared with DAlD-MSCs without any treatment. Preconditioning diabetic AD-MSCs with pretreatment agents like photobiomodulation (PBM) significantly hastened healing in delayed-healing wounds. It is suggested that further animal and human studies be conducted in order to provide more documentation. Hopefully, these outcomes will help the use of DAAD-MSCs plus PBM as a routine treatment protocol for healing severe DFUs in DM patients.
Collapse
|
|
13
|
Gazor R, Asgari M, Abdollajhifar MA, Kiani P, Zare F, Fadaei Fathabady F, Norouzian M, Amini A, Khosravipour A, Atashgah RB, Kazemi M, Chien S, Bayat M. Simultaneous Treatment of Photobiomodulation and Demineralized Bone Matrix With Adipose-Derived Stem Cells Improve Bone Healing in an osteoporotic bone defect. J Lasers Med Sci 2021; 12:e41. [PMID: 34733764 PMCID: PMC8558716 DOI: 10.34172/jlms.2021.41] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/30/2020] [Accepted: 09/23/2020] [Indexed: 12/28/2022]
Abstract
Introduction: The ability of simultaneous treatment of critical-sized femoral defects (CSFDs) with photobiomodulation (PBM) and demineralized bone matrix (DBM) with or without seeded adipose-derived stem cells (ASCs) to induce bone reconstruction in ovariectomized induced osteoporotic (OVX) rats was investigated. Methods: The OVX rats with CSFD were arbitrarily separated into 6 groups: control, scaffold (S, DBM), S + PBM, S + alendronate (ALN), S + ASCs, and S + PBM + ASCs. Each group was assessed by cone beam computed tomography (CBCT) and histological examinations. Results: In the fourth week, CBCT and histological analyses revealed that the largest volume of new bone formed in the S + PBM and S + PBM + ASC groups. The S + PBM treatment relative to the S and S + ALN treatments remarkably reduced the CSFD (Mann-Whitney test, P = 0.009 and P = 0.01). Furthermore, S + PBM + ASCs treatment compared to the S and S + ALN treatments significantly decreased CSFD (Mann Whitney test, P = 0.01). In the eighth week, CBCT analysis showed that extremely enhanced bone regeneration occurred in the CSFD of the S + PBM group. Moreover, the CSFD in the S + PBM group was substantially smaller than S, S + ALN and S + ASCs groups (Mann Whitney test, P = 0.01, P = 0.02 and P = 0.009). Histological observations showed more new bone formation in the treated CSFD of S + PBM + ASCs and S + PBM groups. Conclusion: The PBM plus DBM with or without ASCs significantly enhanced bone healing in the CSFD in OVX rats compared to control, DBM alone, and ALN plus DBM groups. The PBM plus DBM with or without ASCs significantly decreased the CSFD area compared to either the solo DBM or ALN plus DBM treatments.
Collapse
Affiliation(s)
- Rouhallah Gazor
- Department of Anatomy and Cell Biology, Faculty of Medicine, Guilan University of Medical Sciences, Rasht, Iran
| | - Mehrdad Asgari
- Department of Anatomy and Cell Biology, Faculty of Medicine, Guilan University of Medical Sciences, Rasht, Iran
- Department of Biology and Anatomical Sciences, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran; And Department of Maxillofacial Radiology, Guilan University of Medical Sciences, Rasht, Guilan, Iran
| | - Mohammad-Amin Abdollajhifar
- Department of Biology and Anatomical Sciences, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
| | - Pejman Kiani
- Department of Neuroscience and Addiction Studies, School of Advanced Technologies in Medicine, Tehran University of Medical Science, Tehran, Iran
| | - Fatemeh Zare
- Department of Biology and Anatomical Sciences, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
| | - Fatemeh Fadaei Fathabady
- Department of Biology and Anatomical Sciences, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
| | - Mohsen Norouzian
- Department of Biology and Anatomical Sciences, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
| | - Abdollah Amini
- Department of Biology and Anatomical Sciences, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
| | - Armin Khosravipour
- Department of Biology and Anatomical Sciences, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
| | - Rahimeh B. Atashgah
- Department of Pharmaceutical Biomaterials, Faculty of Pharmacy, Tehran University of Medical Sciences, Tehran, 13169- 43551, Iran
| | - Mahsa Kazemi
- Department of Biology and Anatomical Sciences, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
| | - Sufan Chien
- Price Institute of Surgical Research, University of Louisville, and Noveratech LLC, Louisville, Kentucky; USA
| | - Mohammad Bayat
- Department of Biology and Anatomical Sciences, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
- Price Institute of Surgical Research, University of Louisville, and Noveratech LLC, Louisville, Kentucky; USA
| |
Collapse
|
|
14
|
Heo CY, Yoon YS, Min KH, Nam SY, Lee KS, Shin BH, Lee S, Lee M. Effects of low-level laser therapy and adipose-derived stem cells on the viability of autologous fat grafts: a preliminary study. ARCHIVES OF AESTHETIC PLASTIC SURGERY 2021. [DOI: 10.14730/aaps.2021.00080] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/20/2022] Open
Abstract
Background Autologous fat grafts are commonly used in cosmetic and reconstructive surgery, and various methods are used to improve their viability. Low-level laser therapy (LLLT) can enhance the proliferation, growth, and differentiation of various cell lines, including stem cells. Our study investigated and compared the effects of LLLT and the addition of adipose-derived stem cells (ADSCs) on the viability of fat grafts.Methods Twenty nude mice were divided into four groups: control (group 1), LLLT irradiation (group 2), ADSC addition (group 3), and LLLT irradiation+ADSC addition (group 4). ADSCs were combined with the fat tissue. LLLT irradiation was performed once daily for 1 week from the day of grafting. After 8 weeks, the weight, volume, histology, and Western blot findings of the grafted fat tissues were evaluated.Results The retention rate and volume of the fat tissue in groups 2, 3, and 4 were higher than that of group 1, but the difference was not statistically significant. The number of capillaries, histological parameters, and immunofluorescence staining analyses for CD68, CD31, fibroblast growth factor, and vascular endothelial growth factor (VEGF) showed no significant differences among the four groups. The expression level of VEGF was higher in group 2 than in the other groups, but not to a statistically significant level.Conclusions LLLT and ADSCs did not significantly improve the viability of autologous fat grafts. Therefore, further study is necessary to develop safe and effective methods to improve the viability of these grafts for clinical application.
Collapse
|
|
15
|
Eroglu B, Genova E, Zhang Q, Su Y, Shi X, Isales C, Eroglu A. Photobiomodulation has rejuvenating effects on aged bone marrow mesenchymal stem cells. Sci Rep 2021; 11:13067. [PMID: 34158600 PMCID: PMC8219765 DOI: 10.1038/s41598-021-92584-3] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/08/2020] [Accepted: 06/08/2021] [Indexed: 01/06/2023] Open
Abstract
The plasticity and proliferative capacity of stem cells decrease with aging, compromising their tissue regenerative potential and therapeutic applications. This decline is directly linked to mitochondrial dysfunction. Here, we present an effective strategy to reverse aging of mouse bone marrow mesenchymal stem cells (BM-MSCs) by restoring their mitochondrial functionality using photobiomodulation (PBM) therapy. Following the characterization of young and aged MSCs, our results show that a near-infrared PBM treatment delivering 3 J/cm2 is the most effective modality for improving mitochondrial functionality and aging markers. Furthermore, our results unveil that young and aged MSCs respond differently to the same modality of PBM: whereas the beneficial effect of a single PBM treatment dissipates within 7 h in aged stem cells, it is lasting in young ones. Nevertheless, by applying three consecutive treatments at 24-h intervals, we were able to obtain a lasting rejuvenating effect on aged MSCs. Our findings are of particular significance for improving autologous stem cell transplantation in older individuals who need such therapies most.
Collapse
Affiliation(s)
- Binnur Eroglu
- Department of Neuroscience and Regenerative Medicine, Medical College of Georgia, Augusta University, 1120 15th Street, CA-2004, Augusta, GA, 30912, USA
| | - Evan Genova
- Department of Neuroscience and Regenerative Medicine, Medical College of Georgia, Augusta University, 1120 15th Street, CA-2004, Augusta, GA, 30912, USA
| | - Quanguang Zhang
- Department of Neuroscience and Regenerative Medicine, Medical College of Georgia, Augusta University, 1120 15th Street, CA-2004, Augusta, GA, 30912, USA
| | - Yun Su
- Department of Neuroscience and Regenerative Medicine, Medical College of Georgia, Augusta University, 1120 15th Street, CA-2004, Augusta, GA, 30912, USA
| | - Xingming Shi
- Department of Neuroscience and Regenerative Medicine, Medical College of Georgia, Augusta University, 1120 15th Street, CA-2004, Augusta, GA, 30912, USA
| | - Carlos Isales
- Department of Neuroscience and Regenerative Medicine, Medical College of Georgia, Augusta University, 1120 15th Street, CA-2004, Augusta, GA, 30912, USA
- Department of Medicine, Medical College of Georgia, Augusta University, Augusta, GA, 30912, USA
| | - Ali Eroglu
- Department of Neuroscience and Regenerative Medicine, Medical College of Georgia, Augusta University, 1120 15th Street, CA-2004, Augusta, GA, 30912, USA.
- Department of Obstetrics and Gynecology, Medical College of Georgia, Augusta University, Augusta, GA, 30912, USA.
| |
Collapse
|
|
16
|
In Vitro Wound Healing Potential of Photobiomodulation Is Possibly Mediated by Its Stimulatory Effect on AKT Expression in Adipose-Derived Stem Cells. OXIDATIVE MEDICINE AND CELLULAR LONGEVITY 2021; 2021:6664627. [PMID: 33505585 PMCID: PMC7811432 DOI: 10.1155/2021/6664627] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 10/05/2020] [Revised: 12/02/2020] [Accepted: 12/19/2020] [Indexed: 02/07/2023]
Abstract
Increasing evidence suggests that adipose-derived stem cells (ADSCs) serve as a therapeutic approach for wound healing. The aim of this study was to determine the effect of photobiomodulation (PBM) on antioxidant enzymes in ADSCs. Four ADSC cell models, namely, normal, wounded, diabetic, and diabetic wounded, were irradiated with 660 nm (fluence of 5 J/cm2 and power density of 11.2 mW/cm2) or 830 nm (fluence of 5 J/cm2 and power density of 10.3 mW/cm2). Nonirradiated cells served as controls. Cell morphology and wound migration were determined using light microscopy. Cell viability was determined by the trypan blue exclusion assay. The enzyme-linked immunosorbent assay (ELISA) was used to measure the levels of antioxidants (superoxide dismutase (SOD), catalase (CAT), and heme oxygenase (HMOX1)). AKT activation and FOXO1 levels were determined by immunofluorescence and western blotting. The gaps (wound) in PBM-treated wounded and diabetic wounded cell models closed faster than the controls. PBM treatment significantly increased antioxidant levels in all cell models. This reflects that oxidative stress is reduced on the counterpart of increased antioxidant levels. This might be due to the activation of the AKT signaling pathway as evidenced by the increased AKT signals via western blotting and immunofluorescence. This data suggests that PBM promotes wound healing by increasing antioxidant levels by activating AKT signaling.
Collapse
|
|
17
|
Biostimulative effect of laser on growth of mesenchymal stem/stromal cells in vitro. Postepy Dermatol Alergol 2020; 37:771-780. [PMID: 33240019 PMCID: PMC7675089 DOI: 10.5114/ada.2020.100487] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/03/2020] [Accepted: 08/14/2020] [Indexed: 12/23/2022] Open
Abstract
Introduction Human adipose tissue-derived mesenchymal stem/stromal cells (hAT-MSCs) are multipotent stromal cells with a high potential application in tissue engineering and regenerative medicine. Laser irradiation of the place where the cells were implanted can stimulate their proliferation, increase the secretion of growth factors and thus increase the therapeutic effect. Aim To evaluate the influence of two lasers: Er:YAG and diode on the growth of hAT-MSCs in vitro. Material and methods hAT-MSCs were isolated from human subcutaneous adipose tissue. Immunophenotype of hAT-MSCs was confirmed by flow cytometry. Multipotency of hAT-MSCs was confirmed by differentiation into adipogenic, osteogenic and chondrogenic lineages. hAT-MSCs were irradiated with Er:YAG laser (wavelength 2940 nm, frequency 5, 10 Hz, doses: 0.1–1.2 J/cm2) for 2 s and 4 s and diode laser (wavelength 635 nm and doses: 1–8 J/cm2) for 5, 10, 20, 30 and 40 s. Cell viability was analysed 24 h after the exposure using MTT assay. Results Growth stimulation of hAT-MSCs after 5 Hz Er:YAG laser exposure, 0.1 J/cm2 dose for 4 s and 0.3 J/cm2 dose for 4 s was shown in comparison with the control group. Significant growth stimulation of hAT-MSCs after diode laser irradiation in doses of 1–4 J/cm2 was demonstrated compared to the control group. Conclusions The presented results indicate that both lasers, Er:YAG and diode can be used to stimulate stem/stromal cell growth in vitro. The biostimulative effect of laser therapy on stromal cells may be used in the future in aesthetic dermatology in combined laser and cell therapy.
Collapse
|
|
18
|
Miranda JM, de Arruda JAA, Moreno LMM, Gaião WDC, do Nascimento SVB, Silva EVDS, da Silva MB, Rodrigues CG, de Albuquerque DS, Braz R, Pinheiro ALB, Gerbi MEMDM. Photobiomodulation Therapy in the Proliferation and Differentiation of Human Umbilical Cord Mesenchymal Stem Cells: An In Vitro Study. J Lasers Med Sci 2020; 11:469-474. [PMID: 33425299 DOI: 10.34172/jlms.2020.73] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/01/2023]
Abstract
Introduction: Since photobiomodulation therapy (PBMT) favors in vitro mesenchymal stem cell (MSC) preconditioning before MSC transplantation, increasing the proliferation of these cells without molecular injuries by conserving their characteristics, in the present in vitro study we analyzed the effect of PBMT on the proliferation and osteogenic differentiation of human umbilical cord mesenchymal stem cells (hUCMSCs). Methods: Irradiation with an InGaAIP Laser (660 nm, 10 mW, 2.5 J/cm2 , 0.08 cm2 spot size, and 10 s) was carried out. The cells were divided into four groups: CONTROL [cells grown in Dulbecco's Modified Eagle Medium (DMEM)], OSTEO (cells grown in an osteogenic medium); PBMT (cells grown in DMEM+PBMT), and OSTEO+PBMT (cells grown in an osteogenic medium plus PBMT). The cell proliferation curve was obtained over periods of 24, 48 and 72 hours using the 3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2H-tetrazolium bromide (MTT) assay. Osteogenic differentiation was analyzed by the formation of calcium nodules over periods of 7, 14 and 21 days. Morphometric analysis was performed to quantify the total area of nodular calcification. Results: The highest cell proliferation and cell differentiation occurred in the OSTEO+PBMT group, followed by the PBMT, OSTEO and CONTROL groups respectively, at the observed times (P <0.05). Conclusion: PBMT enhanced the osteogenic proliferation and the differentiation of hUCMSCs during the periods tested, without causing damage to the cells and preserving their specific characteristics, a fact that may represent an innovative pretreatment in the application of stem cells.
Collapse
Affiliation(s)
- Jéssica Meirinhos Miranda
- Laser Center, School of Dentistry, Universidade de Pernambuco, Camaragibe, PE, Brazil.,Department of Restorative Dentistry and Endodontics, School of Dentistry, Universidade de Pernambuco, Camaragibe, PE, Brazil
| | - José Alcides Almeida de Arruda
- Department of Oral Surgery and Pathology, School of Dentistry, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
| | - Lara Marques Magalhães Moreno
- Laser Center, School of Dentistry, Universidade de Pernambuco, Camaragibe, PE, Brazil.,Department of Restorative Dentistry and Endodontics, School of Dentistry, Universidade de Pernambuco, Camaragibe, PE, Brazil
| | | | - Sinval Vinícius Barbosa do Nascimento
- Laser Center, School of Dentistry, Universidade de Pernambuco, Camaragibe, PE, Brazil.,Department of Restorative Dentistry and Endodontics, School of Dentistry, Universidade de Pernambuco, Camaragibe, PE, Brazil
| | - Eduardo Vinícius de Souza Silva
- Laser Center, School of Dentistry, Universidade de Pernambuco, Camaragibe, PE, Brazil.,Department of Restorative Dentistry and Endodontics, School of Dentistry, Universidade de Pernambuco, Camaragibe, PE, Brazil
| | - Márcia Bezerra da Silva
- Department of Biophysics and Radiobiology, Universidade Federal de Pernambuco, Recife, PE, Brazil
| | | | - Diana Santana de Albuquerque
- Department of Restorative Dentistry and Endodontics, School of Dentistry, Universidade de Pernambuco, Camaragibe, PE, Brazil
| | - Rodivan Braz
- Department of Restorative Dentistry and Endodontics, School of Dentistry, Universidade de Pernambuco, Camaragibe, PE, Brazil
| | | | - Marleny Elizabeth Marquez de Martinez Gerbi
- Laser Center, School of Dentistry, Universidade de Pernambuco, Camaragibe, PE, Brazil.,Department of Restorative Dentistry and Endodontics, School of Dentistry, Universidade de Pernambuco, Camaragibe, PE, Brazil
| |
Collapse
|
|
19
|
Chang SY, Carpena NT, Mun S, Jung JY, Chung PS, Shim H, Han K, Ahn JC, Lee MY. Enhanced Inner-Ear Organoid Formation from Mouse Embryonic Stem Cells by Photobiomodulation. MOLECULAR THERAPY-METHODS & CLINICAL DEVELOPMENT 2020; 17:556-567. [PMID: 32258218 PMCID: PMC7118273 DOI: 10.1016/j.omtm.2020.03.010] [Citation(s) in RCA: 15] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 02/04/2020] [Revised: 02/09/2020] [Accepted: 03/10/2020] [Indexed: 12/18/2022]
Abstract
Photobiomodulation (PBM) stimulates different types of stem cells to migrate, proliferate, and differentiate in vitro and in vivo. However, little is known about the effects of PBM on the differentiation of embryonic stem cells (ESCs) toward the otic lineage. Only a few reports have documented the in vitro differentiation of ESCs into inner-ear hair cells (HCs) due to the complexity of HCs compared with other target cell types. In this study, we determined the optimal condition to differentiate the ESCs into the otic organoid using different culture techniques and PBM parameters. The efficiency of organoid formation within the embryoid body (EB) was dependent on the cell density of the hanging drop. PBM, using 630 nm wavelength light-emitting diodes (LEDs), further improved the differentiation of inner-ear hair cell-like cells coupled with reactive oxygen species (ROS) overexpression. Transcriptome analysis showed the factors that are responsible for the effect of PBM in the formation of otic organoids, notably, the downregulation of neural development-associated genes and the hairy and enhancer of split 5 (Hes5) gene, which inhibits the differentiation of prosensory cells to hair cells. These data enrich the current differentiation protocols for generating inner-ear hair cells.
Collapse
Affiliation(s)
- So-Young Chang
- Beckman Laser Institute Korea, Dankook University, 119 Dandae-ro, Cheonan 31116, Republic of Korea
| | - Nathaniel T Carpena
- Department of Otolaryngology-Head & Neck Surgery, College of Medicine, Dankook University, 119 Dandae-ro, Cheonan 31116, Republic of Korea
| | - Seyoung Mun
- Department of Nanobiomedical Science and BK21 PLUS NBM Global Research Center for Regenerative Medicine, Dankook University, 119 Dandae-ro, Cheonan 31116, Republic of Korea.,DKU-Theragen Institute for NGS Analysis (DTiNa), 119 Dandae-ro, Cheonan 31116, Republic of Korea
| | - Jae Yun Jung
- Beckman Laser Institute Korea, Dankook University, 119 Dandae-ro, Cheonan 31116, Republic of Korea.,Department of Otolaryngology-Head & Neck Surgery, College of Medicine, Dankook University, 119 Dandae-ro, Cheonan 31116, Republic of Korea
| | - Phil-Sang Chung
- Beckman Laser Institute Korea, Dankook University, 119 Dandae-ro, Cheonan 31116, Republic of Korea.,Department of Otolaryngology-Head & Neck Surgery, College of Medicine, Dankook University, 119 Dandae-ro, Cheonan 31116, Republic of Korea
| | - Hosup Shim
- Institute of Tissue Regeneration Engineering (ITREN), Dankook University, 119 Dandae-ro, Cheonan 31116, Republic of Korea
| | - Kyudong Han
- Department of Nanobiomedical Science and BK21 PLUS NBM Global Research Center for Regenerative Medicine, Dankook University, 119 Dandae-ro, Cheonan 31116, Republic of Korea.,DKU-Theragen Institute for NGS Analysis (DTiNa), 119 Dandae-ro, Cheonan 31116, Republic of Korea
| | - Jin-Chul Ahn
- Beckman Laser Institute Korea, Dankook University, 119 Dandae-ro, Cheonan 31116, Republic of Korea.,Department of Biomedical Science, Dankook University, 119 Dandae-ro, Cheonan 31116, Republic of Korea
| | - Min Young Lee
- Beckman Laser Institute Korea, Dankook University, 119 Dandae-ro, Cheonan 31116, Republic of Korea.,Department of Otolaryngology-Head & Neck Surgery, College of Medicine, Dankook University, 119 Dandae-ro, Cheonan 31116, Republic of Korea
| |
Collapse
|
|
20
|
Zare F, Moradi A, Fallahnezhad S, Ghoreishi SK, Amini A, Chien S, Bayat M. Photobiomodulation with 630 plus 810 nm wavelengths induce more in vitro cell viability of human adipose stem cells than human bone marrow-derived stem cells. JOURNAL OF PHOTOCHEMISTRY AND PHOTOBIOLOGY B: BIOLOGY 2019; 201:111658. [DOI: 10.1016/j.jphotobiol.2019.111658] [Citation(s) in RCA: 29] [Impact Index Per Article: 4.8] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Received: 04/20/2019] [Revised: 10/04/2019] [Accepted: 10/19/2019] [Indexed: 12/21/2022]
|
|
21
|
Wang L, Wu F, Liu C, Song Y, Guo J, Yang Y, Qiu Y. Low-level laser irradiation modulates the proliferation and the osteogenic differentiation of bone marrow mesenchymal stem cells under healthy and inflammatory condition. Lasers Med Sci 2018; 34:169-178. [PMID: 30456535 DOI: 10.1007/s10103-018-2673-8] [Citation(s) in RCA: 29] [Impact Index Per Article: 4.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/07/2017] [Accepted: 01/12/2018] [Indexed: 10/27/2022]
Abstract
The aim of this in vitro study was to evaluate the effects of low-level laser therapy (LLLT) at different energy intensities on proliferation and osteogenic differentiation of bone marrow mesenchymal stem cells (BMSCs) under healthy and inflammatory microenvironments. Human BMSCs and BMSCs from inflammatory conditions (i-BMSCs, BMSCs treated with tumor necrosis factor α; TNF-α) were subject to LLLT (Nd:YAG;1064 nm) at different intensities. We designed one control group (without irradiation) and four testing groups (irradiation at 2, 4, 8, and 16 J/cm2) for both BMSCs and i-BMSCs. Cell proliferation was measured using colony-forming unit fibroblast assay and 3-(4,5-dimethylthiazol-2yl)-2,5-diphenyltetrazolium bromide assay. Osteogenic capacity of cells was determined by alkaline phosphatase (ALP) staining, ALP activity assay, Alizarin Red S staining and the mRNA transcript levels of genes runt-related transcription factor 2 (Runx2), ALP, and osteocalcin. Moreover, the effects of LLLT on secretion of TNF-α in BMSCs and i-BMSCs were measured by enzyme-linked immunosorbent assay. Our results demonstrated LLLT could significantly promote BMSC proliferation and osteogenesis at densities of 2 and 4 J/cm2. LLLT at density of 8 J/cm2 could promote the proliferation and osteogenesis of i-BMSCs. However, LLLT at 16 J/cm2 significantly suppressed the proliferation and osteogenesis of BMSCs both in healthy and in inflammatory microenvironment. Moreover, we also found that the expression of TNF-α was obviously inhibited by LLLT at 4, 8, and 16 J/cm2, in an inflammatory microenvironment. Considering these findings, LLLT could improve current in vitro methods of differentiating BMSCs under healthy and inflammatory microenvironments prior to transplantation.
Collapse
Affiliation(s)
- Liying Wang
- Department of Stomatology, Lanzhou General Hospital, Lanzhou Command of PLA, 333 South Binhe Road, Qili River District, Lanzhou, 730050, Gansu, People's Republic of China.,Key Laboratory of Stem Cells and Gene Drugs of Gansu Province, Lanzhou General Hospital, Lanzhou Command of PLA, Lanzhou, Gansu, China
| | - Fan Wu
- Department of Laparoscope Surgery, The 451st Hospital of People's Liberation Army, Xi'an, Shaanxi, China
| | - Chen Liu
- Department of General Dentistry, Stomatological Hospital of Xi'an Jiao Tong University, Xi'an, Shaanxi, China
| | - Yang Song
- Department of Stomatology, The 323rd Hospital of People's Liberation Army, Xi'an, Shaanxi, China
| | - Jiawen Guo
- Department of Stomatology, Lanzhou General Hospital, Lanzhou Command of PLA, 333 South Binhe Road, Qili River District, Lanzhou, 730050, Gansu, People's Republic of China
| | - Yanwei Yang
- Department of Stomatology, Lanzhou General Hospital, Lanzhou Command of PLA, 333 South Binhe Road, Qili River District, Lanzhou, 730050, Gansu, People's Republic of China
| | - Yinong Qiu
- Department of Stomatology, Lanzhou General Hospital, Lanzhou Command of PLA, 333 South Binhe Road, Qili River District, Lanzhou, 730050, Gansu, People's Republic of China.
| |
Collapse
|
|
22
|
Han B, Fan J, Liu L, Tian J, Gan C, Yang Z, Jiao H, Zhang T, Liu Z, Zhang H. Adipose-derived mesenchymal stem cells treatments for fibroblasts of fibrotic scar via downregulating TGF-β1 and Notch-1 expression enhanced by photobiomodulation therapy. Lasers Med Sci 2018; 34:1-10. [DOI: 10.1007/s10103-018-2567-9] [Citation(s) in RCA: 13] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/08/2017] [Accepted: 06/14/2018] [Indexed: 12/23/2022]
|
|
23
|
Priglinger E, Maier J, Chaudary S, Lindner C, Wurzer C, Rieger S, Redl H, Wolbank S, Dungel P. Photobiomodulation of freshly isolated human adipose tissue-derived stromal vascular fraction cells by pulsed light-emitting diodes for direct clinical application. J Tissue Eng Regen Med 2018; 12:1352-1362. [DOI: 10.1002/term.2665] [Citation(s) in RCA: 16] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/09/2017] [Revised: 11/29/2017] [Accepted: 03/21/2018] [Indexed: 01/15/2023]
Affiliation(s)
- E. Priglinger
- Ludwig Boltzmann Institute for Experimental and Clinical Traumatology; AUVA Research Center; Vienna Austria
- Austrian Cluster for Tissue Regeneration; Vienna Austria
- Liporegena GmbH; Breitenfurt Austria
| | - J. Maier
- Ludwig Boltzmann Institute for Experimental and Clinical Traumatology; AUVA Research Center; Vienna Austria
- Austrian Cluster for Tissue Regeneration; Vienna Austria
- Liporegena GmbH; Breitenfurt Austria
| | - S. Chaudary
- Ludwig Boltzmann Institute for Experimental and Clinical Traumatology; AUVA Research Center; Vienna Austria
- Austrian Cluster for Tissue Regeneration; Vienna Austria
- Liporegena GmbH; Breitenfurt Austria
| | - C. Lindner
- Ludwig Boltzmann Institute for Experimental and Clinical Traumatology; AUVA Research Center; Vienna Austria
- Austrian Cluster for Tissue Regeneration; Vienna Austria
- Liporegena GmbH; Breitenfurt Austria
| | - C. Wurzer
- Ludwig Boltzmann Institute for Experimental and Clinical Traumatology; AUVA Research Center; Vienna Austria
- Austrian Cluster for Tissue Regeneration; Vienna Austria
- Liporegena GmbH; Breitenfurt Austria
| | - S. Rieger
- Ludwig Boltzmann Institute for Experimental and Clinical Traumatology; AUVA Research Center; Vienna Austria
- Austrian Cluster for Tissue Regeneration; Vienna Austria
- Liporegena GmbH; Breitenfurt Austria
| | - H. Redl
- Ludwig Boltzmann Institute for Experimental and Clinical Traumatology; AUVA Research Center; Vienna Austria
- Austrian Cluster for Tissue Regeneration; Vienna Austria
- Liporegena GmbH; Breitenfurt Austria
| | - S. Wolbank
- Ludwig Boltzmann Institute for Experimental and Clinical Traumatology; AUVA Research Center; Vienna Austria
- Austrian Cluster for Tissue Regeneration; Vienna Austria
- Liporegena GmbH; Breitenfurt Austria
| | - P. Dungel
- Ludwig Boltzmann Institute for Experimental and Clinical Traumatology; AUVA Research Center; Vienna Austria
- Austrian Cluster for Tissue Regeneration; Vienna Austria
- Liporegena GmbH; Breitenfurt Austria
| |
Collapse
|
|
24
|
Hamblin MR. Mechanisms and Mitochondrial Redox Signaling in Photobiomodulation. Photochem Photobiol 2018; 94:199-212. [PMID: 29164625 PMCID: PMC5844808 DOI: 10.1111/php.12864] [Citation(s) in RCA: 420] [Impact Index Per Article: 60.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/21/2017] [Accepted: 10/31/2017] [Indexed: 12/23/2022]
Abstract
Photobiomodulation (PBM) involves the use of red or near-infrared light at low power densities to produce a beneficial effect on cells or tissues. PBM therapy is used to reduce pain, inflammation, edema, and to regenerate damaged tissues such as wounds, bones, and tendons. The primary site of light absorption in mammalian cells has been identified as the mitochondria and, more specifically, cytochrome c oxidase (CCO). It is hypothesized that inhibitory nitric oxide can be dissociated from CCO, thus restoring electron transport and increasing mitochondrial membrane potential. Another mechanism involves activation of light or heat-gated ion channels. This review will cover the redox signaling that occurs in PBM and examine the difference between healthy and stressed cells, where PBM can have apparently opposite effects. PBM has a marked effect on stem cells, and this is proposed to operate via mitochondrial redox signaling. PBM can act as a preconditioning regimen and can interact with exercise on muscles.
Collapse
Affiliation(s)
- Michael R Hamblin
- Wellman Center for Photomedicine, Massachusetts General Hospital, Boston, MA
- Department of Dermatology, Harvard Medical School, Boston, MA
- Harvard-MIT Division of Health Sciences and Technology, Cambridge, MA
| |
Collapse
|
|
25
|
da Silveira Campos RM, Dâmaso AR, Masquio DCL, Duarte FO, Sene-Fiorese M, Aquino AE, Savioli FA, Quintiliano PCL, Kravchychyn ACP, Guimarães LI, Tock L, Oyama LM, Boldarine VT, Bagnato VS, Parizotto NA. The effects of exercise training associated with low-level laser therapy on biomarkers of adipose tissue transdifferentiation in obese women. Lasers Med Sci 2018; 33:1245-1254. [PMID: 29473115 DOI: 10.1007/s10103-018-2465-1] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/20/2017] [Accepted: 02/07/2018] [Indexed: 02/07/2023]
Abstract
Investigations suggest the benefits of low-level laser therapy (LLLT) to improve noninvasive body contouring treatments, inflammation, insulin resistance and to reduce body fat. However, the mechanism for such potential effects in association with exercise training (ET) and possible implications in browning adiposity processes remains unclear. Forty-nine obese women were involved, aged between 20 and 40 years with a body mass index (BMI) of 30-40 kg/m2. The volunteers were divided into Phototherapy (808 nm) and SHAM groups. Interventions consisted of exercise training and phototherapy applications post exercise for 4 months, with three sessions/week. Body composition, lipid profile, insulin resistance, atrial natriuretic peptide (ANP), WNT5 signaling, interleukin-6 (IL-6), and fibroblast growth factor-21 (FGF-21) were measured. Improvements in body mass, BMI, body fat mass, lean mass, visceral fat, waist circumference, insulin, HOMA-IR, total cholesterol, LDL-cholesterol, triglycerides, and ANP in both groups were demonstrated. Only the Phototherapy group showed a reduction in interleukin-6 and an increase in WNT5 signaling. In addition, it was possible to observe a higher magnitude change for the fat mass, insulin, HOMA-IR, and FGF-21 variables in the Phototherapy group. In the present investigation, it was demonstrated that exercise training associated with LLLT promotes an improvement in body composition and inflammatory processes as previously demonstrated. The Phototherapy group especially presented positive modifications of WNT5 signaling, FGF-21, and ANP, possible biomarkers associated with browning adiposity processes. This suggests that this kind of intervention promotes results applicable in clinical practice to control obesity and related comorbidities.
Collapse
Affiliation(s)
- Raquel Munhoz da Silveira Campos
- Department of Physiotherapy, Therapeutic Resources Laboratory, Universidade Federal de São Carlos (UFSCar), Rodovia Washington Luis, Km 235, São Carlos, São Paulo, 13565-905, Brazil.
| | - Ana Raimunda Dâmaso
- Post Graduated Program of Nutrition Paulista Medicine School, Universidade Federal de São Paulo (UNIFESP), Rua Marselhesa, 650-Vila Clementino, São Paulo, SP, 04020-050, Brazil.
| | | | - Fernanda Oliveira Duarte
- Electrical Engineering Department, Engineering School of São Carlos, Universidade de São Paulo (USP), Av. Trabalhador Sãocarlense 400, São Carlos, SP, 13566-590, Brazil
| | - Marcela Sene-Fiorese
- São Carlos Institute of Physics, Universidade de São Paulo (USP), PO Box 369, São Carlos, SP, 13560-970, Brazil
| | - Antonio Eduardo Aquino
- São Carlos Institute of Physics, Universidade de São Paulo (USP), PO Box 369, São Carlos, SP, 13560-970, Brazil
| | - Filippo Aragão Savioli
- Centro de Traumato-Ortopedia do Esporte (CETE), Universidade Federal de São Paulo (UNIFESP), São Paulo, Brazil
| | | | - Ana Claudia Pelissari Kravchychyn
- Post Graduated Program of Nutrition Paulista Medicine School, Universidade Federal de São Paulo (UNIFESP), Rua Marselhesa, 650-Vila Clementino, São Paulo, SP, 04020-050, Brazil
| | - Liliane Isabel Guimarães
- Centro de Traumato-Ortopedia do Esporte (CETE), Universidade Federal de São Paulo (UNIFESP), São Paulo, Brazil
| | - Lian Tock
- Weight Science, São Paulo, SP, Brazil
| | - Lila Missae Oyama
- Post Graduated Program of Nutrition Paulista Medicine School, Universidade Federal de São Paulo (UNIFESP), Rua Marselhesa, 650-Vila Clementino, São Paulo, SP, 04020-050, Brazil.,Department of Physiology Paulista Medicine School, Universidade Federal de São Paulo, São Paulo, SP, Brazil
| | - Valter Tadeu Boldarine
- Department of Physiology Paulista Medicine School, Universidade Federal de São Paulo, São Paulo, SP, Brazil
| | - Vanderlei Salvador Bagnato
- São Carlos Institute of Physics, Universidade de São Paulo (USP), PO Box 369, São Carlos, SP, 13560-970, Brazil.,Post Graduated Program of Biotechnology, Universidade Federal de São Carlos (UFSCar), São Carlos, SP, 13565-905, Brazil
| | - Nivaldo Antonio Parizotto
- Department of Physiotherapy, Therapeutic Resources Laboratory, Universidade Federal de São Carlos (UFSCar), Rodovia Washington Luis, Km 235, São Carlos, São Paulo, 13565-905, Brazil. .,Post Graduated Program of Biotechnology, Universidade Federal de São Carlos (UFSCar), São Carlos, SP, 13565-905, Brazil.
| |
Collapse
|
|
26
|
Hamblin MR. Mechanisms and Mitochondrial Redox Signaling in Photobiomodulation. Photochem Photobiol 2018. [DOI: 10.1111/php.12864 or not 3194=3194# dgnj] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/26/2022]
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
27
|
Hamblin MR. Mechanisms and Mitochondrial Redox Signaling in Photobiomodulation. Photochem Photobiol 2018. [DOI: 10.1111/php.12864 and (select (case when (5719=8223) then null else ctxsys.drithsx.sn(1,5719) end) from dual) is null] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/30/2022]
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
28
|
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
29
|
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
30
|
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
31
|
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
32
|
Hamblin MR. Mechanisms and Mitochondrial Redox Signaling in Photobiomodulation. Photochem Photobiol 2018. [DOI: 10.1111/php.12864 and make_set(2234=2234,4853)-- tppa] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/28/2022]
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
33
|
Hamblin MR. Mechanisms and Mitochondrial Redox Signaling in Photobiomodulation. Photochem Photobiol 2018. [DOI: 10.1111/php.12864 or updatexml(4295,concat(0x2e,0x717a717671,(select (elt(4295=4295,1))),0x71706a6271),3985)-- bssu] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/25/2022]
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
34
|
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
35
|
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
36
|
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
37
|
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
38
|
Hamblin MR. Mechanisms and Mitochondrial Redox Signaling in Photobiomodulation. Photochem Photobiol 2018. [DOI: 10.1111/php.12864 or not 5169=2257-- ejdi] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/30/2022]
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
39
|
Hamblin MR. Mechanisms and Mitochondrial Redox Signaling in Photobiomodulation. Photochem Photobiol 2018. [DOI: 10.1111/php.12864 and 2019=2019] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/29/2022]
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
40
|
Hamblin MR. Mechanisms and Mitochondrial Redox Signaling in Photobiomodulation. Photochem Photobiol 2018. [DOI: 10.1111/php.12864 and 1705=('qzqvq'||(select case 1705 when 1705 then 1 else 0 end from rdb$database)||'qpjbq')-- qsrj] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/29/2022]
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
41
|
Hamblin MR. Mechanisms and Mitochondrial Redox Signaling in Photobiomodulation. Photochem Photobiol 2018. [DOI: 10.1111/php.12864 and extractvalue(6022,concat(0x5c,0x717a717671,(select (elt(6022=6022,1))),0x71706a6271))# igpm] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/28/2022]
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
42
|
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
43
|
Hamblin MR. Mechanisms and Mitochondrial Redox Signaling in Photobiomodulation. Photochem Photobiol 2018. [DOI: 10.1111/php.12864 or not 8779=2113# mdth] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/30/2022]
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
44
|
Hamblin MR. Mechanisms and Mitochondrial Redox Signaling in Photobiomodulation. Photochem Photobiol 2018. [DOI: 10.1111/php.12864 and 2341=9012# mbxq] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/30/2022]
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
45
|
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
46
|
Hamblin MR. Mechanisms and Mitochondrial Redox Signaling in Photobiomodulation. Photochem Photobiol 2018. [DOI: 10.1111/php.12864 or not 9689=3416#] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/30/2022]
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
47
|
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
48
|
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
49
|
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|
|
50
|
Hamblin MR. Mechanisms and Mitochondrial Redox Signaling in Photobiomodulation. Photochem Photobiol 2018. [DOI: 10.1111/php.12864 or updatexml(4295,concat(0x2e,0x717a717671,(select (elt(4295=4295,1))),0x71706a6271),3985)# pcqv] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/27/2022]
Affiliation(s)
- Michael R. Hamblin
- Wellman Center for Photomedicine Massachusetts General Hospital Boston MA
- Department of Dermatology Harvard Medical School Boston MA
- Harvard‐MIT Division of Health Sciences and Technology Cambridge MA
| |
Collapse
|