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Lin B, Shi W, Lu Q, Shito TT, Yu H, Dong B. Establishment of a developmental atlas and transgenetic tools in the ascidian Styela clava. MARINE LIFE SCIENCE & TECHNOLOGY 2023; 5:435-454. [PMID: 38045543 PMCID: PMC10689645 DOI: 10.1007/s42995-023-00200-2] [Citation(s) in RCA: 2] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 01/23/2023] [Accepted: 09/28/2023] [Indexed: 12/05/2023]
Abstract
The ascidian Styela clava is an ecologically important species that is distributed along coastal regions worldwide. It has a long history as a model animal for evolutionary and developmental biology research owing to its phylogenetic position between vertebrates and invertebrates, and its classical mosaic expression patterns. However, the standard developmental atlas and protocols and tools for molecular manipulation of this organism are inadequate. In this study, we established a standard developmental table and provided a web-based digital image resource for S. clava embryogenesis at each developmental stage from fertilized eggs to hatching larvae by utilizing confocal laser microscopy and 3D reconstruction images. It takes around 10 h for fertilized eggs to develop into swimming larvae and 20-30 min to complete the tail regression processes at the metamorphic stage. We observed that the notochord cells in S. clava embryos did not produce an extracellular lumen like Ciona robusta, but showed polarized elongation behaviors, providing us an ideal comparative model to study tissue morphogenesis. In addition, we established a chemical-washing procedure to remove the chorion easily from the fertilized eggs. Based on the dechorionation technique, we further realized transgenic manipulation by electroporation and successfully applied tissue-specific fluorescent labeling in S. clava embryos. Our work provides a standard imaging atlas and powerful genetic tools for investigating embryogenesis and evolution using S. clava as a model organism. Supplementary Information The online version contains supplementary material available at 10.1007/s42995-023-00200-2.
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Affiliation(s)
- Boyan Lin
- Fang Zongxi Center, College of Marine Life Sciences, Ocean University of China, Qingdao, 266003 China
| | - Wenjie Shi
- Fang Zongxi Center, College of Marine Life Sciences, Ocean University of China, Qingdao, 266003 China
| | - Qiongxuan Lu
- Fang Zongxi Center, College of Marine Life Sciences, Ocean University of China, Qingdao, 266003 China
| | - Takumi T. Shito
- Department of Bioscience and Informatics, Faculty of Science and Technology, Keio University, Yokohama, 223-8522 Japan
| | - Haiyan Yu
- Fang Zongxi Center, College of Marine Life Sciences, Ocean University of China, Qingdao, 266003 China
| | - Bo Dong
- Fang Zongxi Center, College of Marine Life Sciences, Ocean University of China, Qingdao, 266003 China
- Laoshan Laboratory, Qingdao, 266237 China
- MoE Key Laboratory of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, 266003 China
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Zhang Y, Zeng F, Han X, Weng J, Gao Y. Lineage tracing: technology tool for exploring the development, regeneration, and disease of the digestive system. Stem Cell Res Ther 2020; 11:438. [PMID: 33059752 PMCID: PMC7559019 DOI: 10.1186/s13287-020-01941-y] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/16/2020] [Accepted: 09/17/2020] [Indexed: 12/15/2022] Open
Abstract
Lineage tracing is the most widely used technique to track the migration, proliferation, and differentiation of specific cells in vivo. The currently available gene-targeting technologies have been developing for decades to study organogenesis, tissue injury repairing, and tumor progression by tracing the fates of individual cells. Recently, lineage tracing has expanded the platforms available for disease model establishment, drug screening, cell plasticity research, and personalized medicine development in a molecular and cellular biology perspective. Lineage tracing provides new views for exploring digestive organ development and regeneration and techniques for digestive disease causes and progression. This review focuses on the lineage tracing technology and its application in digestive diseases.
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Affiliation(s)
- Yue Zhang
- Department of Hepatobiliary Surgery II, Guangdong Provincial Research Center for Artificial Organ and Tissue Engineering, Guangzhou Clinical Research and Transformation Center for Artificial Liver, Institute of Regenerative Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou, Guangdong Province, China.,State Key Laboratory of Organ Failure Research, Southern Medical University, Guangzhou, China
| | - Fanhong Zeng
- Department of Hepatobiliary Surgery II, Guangdong Provincial Research Center for Artificial Organ and Tissue Engineering, Guangzhou Clinical Research and Transformation Center for Artificial Liver, Institute of Regenerative Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou, Guangdong Province, China.,State Key Laboratory of Organ Failure Research, Southern Medical University, Guangzhou, China
| | - Xu Han
- Department of Hepatobiliary Surgery II, Guangdong Provincial Research Center for Artificial Organ and Tissue Engineering, Guangzhou Clinical Research and Transformation Center for Artificial Liver, Institute of Regenerative Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou, Guangdong Province, China.,State Key Laboratory of Organ Failure Research, Southern Medical University, Guangzhou, China
| | - Jun Weng
- Department of Hepatobiliary Surgery II, Guangdong Provincial Research Center for Artificial Organ and Tissue Engineering, Guangzhou Clinical Research and Transformation Center for Artificial Liver, Institute of Regenerative Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou, Guangdong Province, China. .,State Key Laboratory of Organ Failure Research, Southern Medical University, Guangzhou, China.
| | - Yi Gao
- Department of Hepatobiliary Surgery II, Guangdong Provincial Research Center for Artificial Organ and Tissue Engineering, Guangzhou Clinical Research and Transformation Center for Artificial Liver, Institute of Regenerative Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou, Guangdong Province, China. .,State Key Laboratory of Organ Failure Research, Southern Medical University, Guangzhou, China.
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Gómez-Villafuertes R, Paniagua-Herranz L, Gascon S, de Agustín-Durán D, Ferreras MDLO, Gil-Redondo JC, Queipo MJ, Menendez-Mendez A, Pérez-Sen R, Delicado EG, Gualix J, Costa MR, Schroeder T, Miras-Portugal MT, Ortega F. Live Imaging Followed by Single Cell Tracking to Monitor Cell Biology and the Lineage Progression of Multiple Neural Populations. J Vis Exp 2017. [PMID: 29286427 PMCID: PMC5755616 DOI: 10.3791/56291] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/23/2023] Open
Abstract
Understanding the mechanisms that control critical biological events of neural cell populations, such as proliferation, differentiation, or cell fate decisions, will be crucial to design therapeutic strategies for many diseases affecting the nervous system. Current methods to track cell populations rely on their final outcomes in still images and they generally fail to provide sufficient temporal resolution to identify behavioral features in single cells. Moreover, variations in cell death, behavioral heterogeneity within a cell population, dilution, spreading, or the low efficiency of the markers used to analyze cells are all important handicaps that will lead to incomplete or incorrect read-outs of the results. Conversely, performing live imaging and single cell tracking under appropriate conditions represents a powerful tool to monitor each of these events. Here, a time-lapse video-microscopy protocol, followed by post-processing, is described to track neural populations with single cell resolution, employing specific software. The methods described enable researchers to address essential questions regarding the cell biology and lineage progression of distinct neural populations.
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Affiliation(s)
- Rosa Gómez-Villafuertes
- Biochemistry and Molecular Biology Department, Faculty of Veterinary medicine, Complutense University; University Institute for Neurochemistry Research (IUIN); Instituto de Investigación Sanitaria del Hospital Clínico San Carlos (IdISSC)
| | - Lucía Paniagua-Herranz
- Biochemistry and Molecular Biology Department, Faculty of Veterinary medicine, Complutense University; University Institute for Neurochemistry Research (IUIN); Instituto de Investigación Sanitaria del Hospital Clínico San Carlos (IdISSC)
| | - Sergio Gascon
- Institute of Stem Cell Research, Helmholtz Center Munich, Neuherberg/Munich, Germany Physiological Genomics, Biomedical Center, Ludwig-Maximilians University Munich; Toxicology and Pharmacology Department, Faculty of Veterinary medicine, Complutense University
| | - David de Agustín-Durán
- Biochemistry and Molecular Biology Department, Faculty of Veterinary medicine, Complutense University; University Institute for Neurochemistry Research (IUIN); Instituto de Investigación Sanitaria del Hospital Clínico San Carlos (IdISSC)
| | - María de la O Ferreras
- Biochemistry and Molecular Biology Department, Faculty of Veterinary medicine, Complutense University; University Institute for Neurochemistry Research (IUIN); Instituto de Investigación Sanitaria del Hospital Clínico San Carlos (IdISSC)
| | - Juan Carlos Gil-Redondo
- Biochemistry and Molecular Biology Department, Faculty of Veterinary medicine, Complutense University; University Institute for Neurochemistry Research (IUIN); Instituto de Investigación Sanitaria del Hospital Clínico San Carlos (IdISSC)
| | - María José Queipo
- Biochemistry and Molecular Biology Department, Faculty of Veterinary medicine, Complutense University; University Institute for Neurochemistry Research (IUIN); Instituto de Investigación Sanitaria del Hospital Clínico San Carlos (IdISSC)
| | - Aida Menendez-Mendez
- Biochemistry and Molecular Biology Department, Faculty of Veterinary medicine, Complutense University; University Institute for Neurochemistry Research (IUIN); Instituto de Investigación Sanitaria del Hospital Clínico San Carlos (IdISSC)
| | - Ráquel Pérez-Sen
- Biochemistry and Molecular Biology Department, Faculty of Veterinary medicine, Complutense University; University Institute for Neurochemistry Research (IUIN); Instituto de Investigación Sanitaria del Hospital Clínico San Carlos (IdISSC)
| | - Esmerilda G Delicado
- Biochemistry and Molecular Biology Department, Faculty of Veterinary medicine, Complutense University; University Institute for Neurochemistry Research (IUIN); Instituto de Investigación Sanitaria del Hospital Clínico San Carlos (IdISSC)
| | - Javier Gualix
- Biochemistry and Molecular Biology Department, Faculty of Veterinary medicine, Complutense University; University Institute for Neurochemistry Research (IUIN); Instituto de Investigación Sanitaria del Hospital Clínico San Carlos (IdISSC)
| | - Marcos R Costa
- Brain Institute, Federal University of Rio Grande do Norte
| | - Timm Schroeder
- Department of Biosystems Science and Engineering, Eidgenössische Technische Hochschule (ETH) Zurich
| | - María Teresa Miras-Portugal
- Biochemistry and Molecular Biology Department, Faculty of Veterinary medicine, Complutense University; University Institute for Neurochemistry Research (IUIN); Instituto de Investigación Sanitaria del Hospital Clínico San Carlos (IdISSC)
| | - Felipe Ortega
- Biochemistry and Molecular Biology Department, Faculty of Veterinary medicine, Complutense University; University Institute for Neurochemistry Research (IUIN); Instituto de Investigación Sanitaria del Hospital Clínico San Carlos (IdISSC);
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Mukherjee S, Brat DJ. Molecular Programs Underlying Asymmetric Stem Cell Division and Their Disruption in Malignancy. Results Probl Cell Differ 2017; 61:401-421. [PMID: 28409315 DOI: 10.1007/978-3-319-53150-2_18] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 06/07/2023]
Abstract
Asymmetric division of stem cells is a highly conserved and tightly regulated process by which a single stem cell produces two unequal daughter cells. One retains its stem cell identity while the other becomes specialized through a differentiation program and loses stem cell properties. Coordinating these events requires control over numerous intra- and extracellular biological processes and signaling networks. In the initial stages, critical events include the compartmentalization of fate determining proteins within the mother cell and their subsequent passage to the appropriate daughter cell in order to direct their destiny. Disturbance of these events results in an altered dynamic of self-renewing and differentiation within the cell population, which is highly relevant to the growth and progression of cancer. Other critical events include proper asymmetric spindle assembly, extrinsic regulation through micro-environmental cues, and non-canonical signaling networks that impact cell division and fate determination. In this review, we discuss mechanisms that maintain the delicate balance of asymmetric cell division in normal tissues and describe the current understanding how some of these mechanisms are deregulated in cancer.
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Affiliation(s)
- Subhas Mukherjee
- Departments of Pathology and Laboratory Medicine, Emory University, Atlanta, GA, USA
| | - Daniel J Brat
- Departments of Pathology and Laboratory Medicine, Emory University, Atlanta, GA, USA.
- Winship Cancer Institute, Emory University, 1701 Uppergate Drive, Building C, Rm#C5038, Atlanta, GA, USA.
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Jumabay M, Boström KI. Dedifferentiated fat cells: A cell source for regenerative medicine. World J Stem Cells 2015; 7:1202-1214. [PMID: 26640620 PMCID: PMC4663373 DOI: 10.4252/wjsc.v7.i10.1202] [Citation(s) in RCA: 33] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/22/2015] [Revised: 04/02/2015] [Accepted: 10/13/2015] [Indexed: 02/06/2023] Open
Abstract
The identification of an ideal cell source for tissue regeneration remains a challenge in the stem cell field. The ability of progeny cells to differentiate into other cell types is important for the processes of tissue reconstruction and tissue engineering and has clinical, biochemical or molecular implications. The adaptation of stem cells from adipose tissue for use in regenerative medicine has created a new role for adipocytes. Mature adipocytes can easily be isolated from adipose cell suspensions and allowed to dedifferentiate into lipid-free multipotent cells, referred to as dedifferentiated fat (DFAT) cells. Compared to other adult stem cells, the DFAT cells have unique advantages in their abundance, ease of isolation and homogeneity. Under proper condition in vitro and in vivo, the DFAT cells have exhibited adipogenic, osteogenic, chondrogenic, cardiomyogenc, angiogenic, myogenic, and neurogenic potentials. In this review, we first discuss the phenomena of dedifferentiation and transdifferentiation of cells, and then dedifferentiation of adipocytes in particular. Understanding the dedifferentiation process itself may contribute to our knowledge of normal growth processes, as well as mechanisms of disease. Second, we highlight new developments in DFAT cell culture and summarize the current understanding of DFAT cell properties. The unique features of DFAT cells are promising for clinical applications such as tissue regeneration.
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Mukherjee S, Kong J, Brat DJ. Cancer stem cell division: when the rules of asymmetry are broken. Stem Cells Dev 2014; 24:405-16. [PMID: 25382732 DOI: 10.1089/scd.2014.0442] [Citation(s) in RCA: 48] [Impact Index Per Article: 4.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/12/2022] Open
Abstract
Asymmetric division of stem cells is a highly conserved and tightly regulated process by which a single stem cell produces two daughter cells and simultaneously directs the differential fate of both: one retains its stem cell identity while the other becomes specialized and loses stem cell properties. Coordinating these events requires control over numerous intra- and extracellular biological processes and signaling networks. In the initial stages, critical events include the compartmentalization of fate determining proteins within the mother cell and their subsequent passage to the appropriate daughter cell. Disturbance of these events results in an altered dynamic of self-renewing and differentiation within the cell population, which is highly relevant to the growth and progression of cancer. Other critical events include proper asymmetric spindle assembly, extrinsic regulation through micro-environmental cues, and noncanonical signaling networks that impact cell division and fate determination. In this review, we discuss mechanisms that maintain the delicate balance of asymmetric cell division in normal tissues and describe the current understanding how some of these mechanisms are deregulated in cancer. The universe is asymmetric and I am persuaded that life, as it is known to us, is a direct result of the asymmetry of the universe or of its indirect consequences. The universe is asymmetric. -Louis Pasteur.
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Affiliation(s)
- Subhas Mukherjee
- 1 Department of Pathology and Laboratory Medicine, Emory University , Atlanta, Georgia
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Three-dimensional anatomy of the Ciona intestinalis tailbud embryo at single-cell resolution. Dev Biol 2012; 372:274-84. [DOI: 10.1016/j.ydbio.2012.09.007] [Citation(s) in RCA: 41] [Impact Index Per Article: 3.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/23/2012] [Revised: 08/10/2012] [Accepted: 09/13/2012] [Indexed: 11/17/2022]
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Atkinson JW. E. G. Conklin on evolution: the popular writings of an embryologist. JOURNAL OF THE HISTORY OF BIOLOGY 1985; 18:31-50. [PMID: 11611748 DOI: 10.1007/bf00127956] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 05/23/2023]
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