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Liu K, Han H, Xiong K, Zhai S, Yang X, Yu X, Chen B, Liu M, Dong Q, Meng H, Gu Y. Single-cell landscape of intratumoral heterogeneity and tumor microenvironment remolding in pre-nodal metastases of breast cancer. J Transl Med 2024; 22:804. [PMID: 39210391 PMCID: PMC11363495 DOI: 10.1186/s12967-024-05625-6] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/04/2024] [Accepted: 08/15/2024] [Indexed: 09/04/2024] Open
Abstract
BACKGROUND The metastasis of cancer cells is influenced by both their intrinsic characteristics and the tumor microenvironment (TME). However, the molecular mechanisms underlying pre-nodal metastases of breast cancer remain unclear. METHODS We integrated a total of 216,963 cells from 54 samples across 6 single-cell datasets to profile the cellular landscape differences between primary tumors and pre-nodal metastases. RESULTS We revealed three distinct metastatic epithelial cell subtypes (Epi1, Epi2 and Epi3), which exhibited different metastatic mechanisms. Specifically, the marker gene KCNK15 of the Epi1 subtype exhibited increased gene expression along the cell differentiation trajectory and was specifically regulated by the transcription factor ASCL1. In the Epi3 subtype, we highlighted NR2F1 as a regulator targeting the marker gene MUCL1. Additionally, we found that the Epi2 and Epi3 subtypes shared some regulons, such as ZEB1 and NR2C1. Similarly, we identified specific subtypes of stromal and immune cells in the TME, and discovered that vascular cancer-associated fibroblasts might promote capillary formation through CXCL9+ macrophages in pre-nodal metastases. All three subtypes of metastatic epithelial cells were associated with poor prognosis. CONCLUSIONS In summary, this study dissects the intratumoral heterogeneity and remodeling of the TME in pre-nodal metastases of breast cancer, providing novel insights into the mechanisms underlying breast cancer metastasis.
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Affiliation(s)
- Kaidong Liu
- Department of Systems Biology, College of Bioinformatics Science and Technology, Harbin Medical University, Harbin, China
| | - Huiming Han
- Department of Systems Biology, College of Bioinformatics Science and Technology, Harbin Medical University, Harbin, China
| | - Kai Xiong
- Department of Systems Biology, College of Bioinformatics Science and Technology, Harbin Medical University, Harbin, China
| | - Songmei Zhai
- Department of Systems Biology, College of Bioinformatics Science and Technology, Harbin Medical University, Harbin, China
| | - Xiuqi Yang
- Department of Systems Biology, College of Bioinformatics Science and Technology, Harbin Medical University, Harbin, China
| | - Xinmiao Yu
- Department of Human Anatomy, Harbin Medical University, Harbin, China
| | - Bo Chen
- Department of Systems Biology, College of Bioinformatics Science and Technology, Harbin Medical University, Harbin, China
| | - Mingyue Liu
- Department of Systems Biology, College of Bioinformatics Science and Technology, Harbin Medical University, Harbin, China
| | - Qi Dong
- Department of Systems Biology, College of Bioinformatics Science and Technology, Harbin Medical University, Harbin, China
| | - Hongxue Meng
- Department of Pathology, Harbin Medical University Cancer Hospital, Harbin, China.
| | - Yunyan Gu
- Department of Systems Biology, College of Bioinformatics Science and Technology, Harbin Medical University, Harbin, China.
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Deng Z, Feng Q, Zhao D, Huang Z. A degradome-related signature for predicting the prognosis and immunotherapy benefit in stomach adenocarcinoma based on machine learning procedure. Medicine (Baltimore) 2024; 103:e37728. [PMID: 38608069 PMCID: PMC11018154 DOI: 10.1097/md.0000000000037728] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/04/2024] [Accepted: 03/05/2024] [Indexed: 04/14/2024] Open
Abstract
Stomach adenocarcinoma (STAD) is one of the subtype of gastric cancer with high invasiveness, extreme heterogeneity, high morbidity, and high mortality. The degradome is the most abundant class of cellular enzymes that play an essential role in regulating cellular activity and carcinogenesis. An integrative machine learning procedure including 10 methods was performed to develop a prognostic degradome-based prognostic signature (DPS) in TCGA, GSE15459, GSE26253, and GSE62254 datasets. Investigations of the DPS concerning immune infiltration, immunotherapy benefits, and drug priority were orchestrated. The DPS developed by Enet [alpha = 0.3] method was regarded as the optimal prognostic model. The DPS had a stable and powerful performance in predicting the clinical outcome of STAD and served as an independent risk factor in training and testing cohorts. The C-index of DPS was higher than that of age, sex, and clinical stage. STAD patients with low DPS scores had a higher abundance of B cells, CD8+ T cells, higher cytolytic scores, and T cell co-stimulation scores. Moreover, low DPS score indicated a lower tumor immune dysfunction and exclusion score, lower T cell dysfunction and exclusion score, higher PD1&CTLA4 immunophenoscore, and higher tumor mutation burden score in STAD, demonstrating a better immunotherapy response. STAD patients with a high DPS score had a lower IC50 value of common chemotherapy and targeted therapy regimens (Cisplatin, Docetaxel, Gefitinib, etc). Our study developed an optimal DPS for STAD. The DPS could predict the prognosis, risk stratification and guide treatment for STAD patients.
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Affiliation(s)
- Ziqing Deng
- Department of General Surgery, Nanchang People’s Hospital, Nanchang, China
| | - Qian Feng
- Department of Emergency, The Second Affiliated Hospital of Nanchang University, Nanchang, China
| | - Dan Zhao
- Department of Critical Care Medicine, The Affiliated Hospital of Jiangxi University of Traditional Chinese Medicine, Nanchang, China
| | - Zhihao Huang
- Department of General Surgery, The Second Affiliated Hospital of Nanchang University, Nanchang, China
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Sheng G, Li F, Jin W, Wang K. Pan-caner analysis identifies PSMA7 as a targets for amplification at 20q13.33 in tumorigenesis. Sci Rep 2024; 14:3034. [PMID: 38321088 PMCID: PMC10847487 DOI: 10.1038/s41598-024-53585-0] [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: 08/07/2023] [Accepted: 02/02/2024] [Indexed: 02/08/2024] Open
Abstract
The chromosome 20 long arm (20q) is one of the genomic hotspots where copy number alterations frequently occur in multiple types of tumors. However, it remains elusive which genes are implicated in 20q-related tumorigenesis. Here, by querying TCGA and GEO databases, we observed frequent copy number amplification at 20q and the chromosome subband 20q13.33 was amplificated in multiple cancers. Among those genes at 20q13.33, PSMA7 was found with the strongest correlation with cancers. Further analysis revealed that PSMA7 amplification was the most frequent genetic alteration event conferring adverse prognosis in various cancers. Consistent with the strong positive correlation between PSMA7 amplification and gene expression, elevated PSMA7 expression was observed in 20 of 33 types of cancers with a close link to adverse outcomes in certain tumors. In addition, PSMA7 was essential for the growth of almost 1095 cancer lines. Mechanistically, aberrant PSMA7 most probably influenced the proteasome and protease-related pathways to promote tumorigenesis and might be antagonized by several compounds, e.g., Docetaxel in relevant cancers. The current in-depth pan-cancer analysis refines our understanding of the crucial oncogenic role of copy number amplifications at PSMA7 loci at the novel chromosome amplicon 20q13.33 across different tumors.
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Affiliation(s)
- Guangying Sheng
- State Key Laboratory of Medical Genomics, Ruijin Hospital Shanghai Institute of Hematology, National Research Center for Translational Medicine at Shanghai, Shanghai Jiao Tong University School of Medicine, 197 Ruijin Er Rd, Shanghai, 200025, China
- Ruijin Hospital, Sino-French Research Center for Life Sciences and Genomics, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Fuyu Li
- State Key Laboratory of Medical Genomics, Ruijin Hospital Shanghai Institute of Hematology, National Research Center for Translational Medicine at Shanghai, Shanghai Jiao Tong University School of Medicine, 197 Ruijin Er Rd, Shanghai, 200025, China
- Ruijin Hospital, Sino-French Research Center for Life Sciences and Genomics, Shanghai Jiao Tong University School of Medicine, Shanghai, China
- School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China
| | - Wen Jin
- State Key Laboratory of Medical Genomics, Ruijin Hospital Shanghai Institute of Hematology, National Research Center for Translational Medicine at Shanghai, Shanghai Jiao Tong University School of Medicine, 197 Ruijin Er Rd, Shanghai, 200025, China
| | - Kankan Wang
- State Key Laboratory of Medical Genomics, Ruijin Hospital Shanghai Institute of Hematology, National Research Center for Translational Medicine at Shanghai, Shanghai Jiao Tong University School of Medicine, 197 Ruijin Er Rd, Shanghai, 200025, China.
- Ruijin Hospital, Sino-French Research Center for Life Sciences and Genomics, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
- School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China.
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Jiao QH, Wang Y, Zhang AN, Liu QQ, Zhou QB. PSMA7 promotes the malignant proliferation of esophageal cancer. Heliyon 2024; 10:e23173. [PMID: 38173490 PMCID: PMC10761361 DOI: 10.1016/j.heliyon.2023.e23173] [Citation(s) in RCA: 2] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/16/2023] [Revised: 11/20/2023] [Accepted: 11/28/2023] [Indexed: 01/05/2024] Open
Abstract
Background It is important to explore novel molecules that play a key role in esophageal cancer (ESCA) progression. Methods Two ESCA tissue expression profile microarrays (GSE92396 and GSE17351) data from GEO were downloaded, and differentially expressed genes (DEGs) were analyzed using GEO2R. The DEGs common to both microarrays were analyzed for protein-protein interactions, KEGG and GO. The altered expression of proteasome 20S subunit α 7 (PSMA7) in ESCA tissues was analyzed using information from publicly available databases (GEO, TCGA, TNMplot). PSMA7 was overexpressed or knocked down in Eca109 and KYSE150 cells using transfection, and the effects on cell proliferation, migration, invasion and apoptosis were examined using CCK-8, Transwell, and flow cytometry experiments. Results 284 common DEGs were identified, and 10 core proteins, HSP90AA1, AURKA, CDC6, PCNA, MCM5, KAT2B, GRB2, MYBL2, PSMA7, and CKAP5, involved in ESCA progression were identified. PSMA7 mRNA level was significantly increased in ESCA tissues. PSMA7 overexpression significantly promoted the proliferation, migration and invasion of Eca109 and KYSE150 cells, and significantly promoted apoptosis. In contrast, PSMA7 knockdown inhibited their proliferation and motility, and significantly suppressed apoptosis. Conclusion This study analyzed multiple proteins that may play a key role in ESCA progression, and identified the pro-cancer role of PSMA7.
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Affiliation(s)
- Qing-hua Jiao
- Department of Geriatrics, The Second Hospital Cheeloo College of Medicine Shandong University, Jinan 250000, Shandong, China
| | - Yan Wang
- Department of Geriatrics, The Second Hospital Cheeloo College of Medicine Shandong University, Jinan 250000, Shandong, China
| | - An-na Zhang
- Department of Geriatrics, The Second Hospital Cheeloo College of Medicine Shandong University, Jinan 250000, Shandong, China
| | - Qian-qian Liu
- Department of Geriatrics, The Second Hospital Cheeloo College of Medicine Shandong University, Jinan 250000, Shandong, China
| | - Qing-bo Zhou
- Department of Geriatrics, The Second Hospital Cheeloo College of Medicine Shandong University, Jinan 250000, Shandong, China
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Li Q, Yin LK. Comprehensive analysis of disulfidptosis related genes and prognosis of gastric cancer. World J Clin Oncol 2023; 14:373-399. [PMID: 37970110 PMCID: PMC10631345 DOI: 10.5306/wjco.v14.i10.373] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/30/2023] [Revised: 09/07/2023] [Accepted: 09/18/2023] [Indexed: 10/24/2023] Open
Abstract
BACKGROUND Gastric cancer (GC) is a common malignant tumor of the digestive system. Disulfidptosis is a new programmed cell death mechanism, although its specific mechanism in GC is incompletely understood. AIM In this study, we used bioinformatics analysis to explore a disulfidptosis-based predictive model related to GC prognosis and to identify potential therapeutic targets and sensitive drugs for GC. METHODS We extracted GC-related data from The Cancer Genome Atlas and Gene Expression Omnibus databases. R software (version 4.2.1) was used for correlation analysis. RESULTS Through the above analysis, we found that the disulfidptosis related gene may be related to the prognosis of GC. Six genes, namely, PLS3, GRP, APOD, SGCE, COL8A1, and VAMP7, were found to constitute a predictive model for GC prognosis. APOD is a potential therapeutic target for treating GC. Bosutinib and other drugs are sensitive for the treatment of GC. CONCLUSION The results of this study indicate that disulfidptosis is related to the prognosis and treatment of GC, while APOD represents a potential therapeutic target for GC.
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Affiliation(s)
- Qian Li
- Department of Oncology, Fushun Hospital of Traditional Chinese Medicine, Zigong 643200, Sichuan Province, China
| | - Long-Kuan Yin
- Department of Gastrointestinal Surgery, Fushun People’s Hospital, Zigong 643200, Sichuan Province, China
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Luo QW, Yao L, Li L, Yang Z, Zhao MM, Zheng YZ, Zhuo FF, Liu TT, Zhang XW, Liu D, Tu PF, Zeng KW. Inherent Capability of Self-Assembling Nanostructures in Specific Proteasome Activation for Cancer Cell Pyroptosis. SMALL (WEINHEIM AN DER BERGSTRASSE, GERMANY) 2023; 19:e2205531. [PMID: 36549896 DOI: 10.1002/smll.202205531] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 09/07/2022] [Revised: 11/23/2022] [Indexed: 06/17/2023]
Abstract
Understanding the direct interaction of nanostructures per se with biological systems is important for biomedical applications. However, whether nanostructures regulate biological systems by targeting specific cellular proteins remains largely unknown. In the present work, self-assembling nanomicelles are constructed using small-molecule oleanolic acid (OA) as a molecular template. Unexpectedly, without modifications by functional ligands, OA nanomicelles significantly activate cellular proteasome function by directly binding to 20S proteasome subunit alpha 6 (PSMA6). Mechanism study reveals that OA nanomicelles interact with PSMA6 to dynamically modulate its N-terminal domain conformation change, thereby controlling the entry of proteins into 20S proteasome. Subsequently, OA nanomicelles accelerate the degradation of several crucial proteins, thus potently driving cancer cell pyroptosis. For translational medicine, OA nanomicelles exhibit a significant anticancer potential in tumor-bearing mouse models and stimulate immune cell infiltration. Collectively, this proof-of-concept study advances the mechanical understanding of nanostructure-guided biological effects via their inherent capacity to activate proteasome.
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Affiliation(s)
- Qian-Wei Luo
- State Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking University, Beijing, 100191, China
| | - Lu Yao
- State Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking University, Beijing, 100191, China
| | - Ling Li
- State Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking University, Beijing, 100191, China
| | - Zhuo Yang
- State Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking University, Beijing, 100191, China
| | - Mei-Mei Zhao
- State Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking University, Beijing, 100191, China
| | - Yong-Zhe Zheng
- State Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking University, Beijing, 100191, China
| | - Fang-Fang Zhuo
- State Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking University, Beijing, 100191, China
| | - Ting-Ting Liu
- State Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking University, Beijing, 100191, China
| | - Xiao-Wen Zhang
- State Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking University, Beijing, 100191, China
| | - Dan Liu
- Proteomics Laboratory, Medical and Healthy Analytical Center, Peking University Health Science Center, Beijing, 100191, China
| | - Peng-Fei Tu
- State Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking University, Beijing, 100191, China
| | - Ke-Wu Zeng
- State Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking University, Beijing, 100191, China
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Lou J, Lv JX, Zhang YP, Liu ZJ. OSI-027 inhibits the tumorigenesis of colon cancer through mediation of c-Myc/FOXO3a/PUMA axis. Cell Biol Int 2022; 46:1204-1214. [PMID: 35293663 DOI: 10.1002/cbin.11792] [Citation(s) in RCA: 7] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/22/2021] [Revised: 01/16/2022] [Accepted: 03/13/2022] [Indexed: 11/07/2022]
Abstract
Colon cancer is a gastrointestinal malignancy which is one of the leading causes of tumor-associated deaths. It has been reported that mTOR can lead to the progression of colon cancer. However, the mechanism by which mTOR inhibitor (OSI-027) mediates the tumorigenesis of colon cancer remains largely unknown. Cell function of colon cancer was investigated by CCK-8 flow cytometry and TUNEL staining. In addition, qRT-PCR and western blot were used to investigate the mechanism underlying the function of OSI-027 in colon cancer. OSI-027 dose-dependently reduced colon cancer cell viability through inducing the cell apoptosis. In addition, OSI-027 induced the apoptosis of colon cancer cells via upregulation of PUMA. OSI-027 promoted the expression of PUMA by activation of FOXO3a, and c-Myc knockdown partially increased FOXO3a and PUMA level. Moreover, OSI-027 attenuated the tumor growth of colon cancer through mediation of mTOR/c-Myc/FOXO3a axis. OSI-027 attenuates colon cancer progression through mediation of c-Myc/FOXO3a/PUMA axis. Thereby, this research might shed new insights on exploring the strategies against colon cancer. This article is protected by copyright. All rights reserved.
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Affiliation(s)
- Jie Lou
- Department of Gastroenterology, Shanghai Tenth People's Hospital, School of Medicine, Tongji University, Shanghai, 200072, China.,Department of Gastroenterology, HwaMei Hospital, University of Chinese Academy of Sciences, Ningbo, 315000, Zhejiang Province, China
| | - Jian-Xin Lv
- Department of Gastroenterology, HwaMei Hospital, University of Chinese Academy of Sciences, Ningbo, 315000, Zhejiang Province, China
| | - You-Ping Zhang
- Department of Gastroenterology, HwaMei Hospital, University of Chinese Academy of Sciences, Ningbo, 315000, Zhejiang Province, China
| | - Zhan-Ju Liu
- Department of Gastroenterology, Shanghai Tenth People's Hospital, School of Medicine, Tongji University, Shanghai, 200072, China
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Chiao CC, Liu YH, Phan NN, An Ton NT, Ta HDK, Anuraga G, Minh Xuan DT, Fitriani F, Putri Hermanto EM, Athoillah M, Andriani V, Ajiningrum PS, Wu YF, Lee KH, Chuang JY, Wang CY, Kao TJ. Prognostic and Genomic Analysis of Proteasome 20S Subunit Alpha (PSMA) Family Members in Breast Cancer. Diagnostics (Basel) 2021; 11:diagnostics11122220. [PMID: 34943457 PMCID: PMC8699889 DOI: 10.3390/diagnostics11122220] [Citation(s) in RCA: 26] [Impact Index Per Article: 6.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/18/2021] [Revised: 11/21/2021] [Accepted: 11/22/2021] [Indexed: 12/14/2022] Open
Abstract
The complexity of breast cancer includes many interacting biological processes, and proteasome alpha (PSMA) subunits are reported to be involved in many cancerous diseases, although the transcriptomic expression of this gene family in breast cancer still needs to be more thoroughly investigated. Consequently, we used a holistic bioinformatics approach to study the PSMA genes involved in breast cancer by integrating several well-established high-throughput databases and tools, such as cBioPortal, Oncomine, and the Kaplan–Meier plotter. Additionally, correlations of breast cancer patient survival and PSMA messenger RNA expressions were also studied. The results demonstrated that breast cancer tissues had higher expression levels of PSMA genes compared to normal breast tissues. Furthermore, PSMA2, PSMA3, PSMA4, PSMA6, and PSMA7 showed high expression levels, which were correlated with poor survival of breast cancer patients. In contrast, PSMA5 and PSMA8 had high expression levels, which were associated with good prognoses. We also found that PSMA family genes were positively correlated with the cell cycle, ubiquinone metabolism, oxidative stress, and immune response signaling, including antigen presentation by major histocompatibility class, interferon-gamma, and the cluster of differentiation signaling. Collectively, these findings suggest that PSMA genes have the potential to serve as novel biomarkers and therapeutic targets for breast cancer. Nevertheless, the bioinformatic results from the present study would be strengthened with experimental validation in the future by prospective studies on the underlying biological mechanisms of PSMA genes and breast cancer.
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Affiliation(s)
- Chung-Chieh Chiao
- Ph.D. Program for Cancer Molecular Biology and Drug Discovery, College of Medical Science, Taipei Medical University, Taipei 11031, Taiwan; (C.-C.C.); (H.D.K.T.); (G.A.); (K.-H.L.)
- Graduate Institute of Cancer Biology and Drug Discovery, College of Medical Science and Technology, Taipei Medical University, Taipei 11031, Taiwan; (Y.-H.L.); (D.T.M.X.)
| | - Yen-Hsi Liu
- Graduate Institute of Cancer Biology and Drug Discovery, College of Medical Science and Technology, Taipei Medical University, Taipei 11031, Taiwan; (Y.-H.L.); (D.T.M.X.)
| | - Nam Nhut Phan
- NTT Institute of Hi-Technology, Nguyen Tat Thanh University, Ho Chi Minh City 700000, Vietnam; (N.N.P.); (N.T.A.T.)
| | - Nu Thuy An Ton
- NTT Institute of Hi-Technology, Nguyen Tat Thanh University, Ho Chi Minh City 700000, Vietnam; (N.N.P.); (N.T.A.T.)
| | - Hoang Dang Khoa Ta
- Ph.D. Program for Cancer Molecular Biology and Drug Discovery, College of Medical Science, Taipei Medical University, Taipei 11031, Taiwan; (C.-C.C.); (H.D.K.T.); (G.A.); (K.-H.L.)
- Graduate Institute of Cancer Biology and Drug Discovery, College of Medical Science and Technology, Taipei Medical University, Taipei 11031, Taiwan; (Y.-H.L.); (D.T.M.X.)
| | - Gangga Anuraga
- Ph.D. Program for Cancer Molecular Biology and Drug Discovery, College of Medical Science, Taipei Medical University, Taipei 11031, Taiwan; (C.-C.C.); (H.D.K.T.); (G.A.); (K.-H.L.)
- Graduate Institute of Cancer Biology and Drug Discovery, College of Medical Science and Technology, Taipei Medical University, Taipei 11031, Taiwan; (Y.-H.L.); (D.T.M.X.)
- Department of Statistics, Faculty of Science and Technology, Universitas PGRI Adi Buana, Surabaya 60234, Indonesia; (F.F.); (E.M.P.H.); (M.A.)
| | - Do Thi Minh Xuan
- Graduate Institute of Cancer Biology and Drug Discovery, College of Medical Science and Technology, Taipei Medical University, Taipei 11031, Taiwan; (Y.-H.L.); (D.T.M.X.)
| | - Fenny Fitriani
- Department of Statistics, Faculty of Science and Technology, Universitas PGRI Adi Buana, Surabaya 60234, Indonesia; (F.F.); (E.M.P.H.); (M.A.)
| | - Elvira Mustikawati Putri Hermanto
- Department of Statistics, Faculty of Science and Technology, Universitas PGRI Adi Buana, Surabaya 60234, Indonesia; (F.F.); (E.M.P.H.); (M.A.)
| | - Muhammad Athoillah
- Department of Statistics, Faculty of Science and Technology, Universitas PGRI Adi Buana, Surabaya 60234, Indonesia; (F.F.); (E.M.P.H.); (M.A.)
| | - Vivin Andriani
- Department of Biological Science, Faculty of Science and Technology, Universitas PGRI Adi Buana, Surabaya 60234, Indonesia; (V.A.); (P.S.A.)
| | - Purity Sabila Ajiningrum
- Department of Biological Science, Faculty of Science and Technology, Universitas PGRI Adi Buana, Surabaya 60234, Indonesia; (V.A.); (P.S.A.)
| | - Yung-Fu Wu
- Department of Medical Research, Tri-Service General Hospital, School of Medicine, National Defense Medical Center, Taipei 11490, Taiwan;
| | - Kuen-Haur Lee
- Ph.D. Program for Cancer Molecular Biology and Drug Discovery, College of Medical Science, Taipei Medical University, Taipei 11031, Taiwan; (C.-C.C.); (H.D.K.T.); (G.A.); (K.-H.L.)
- Graduate Institute of Cancer Biology and Drug Discovery, College of Medical Science and Technology, Taipei Medical University, Taipei 11031, Taiwan; (Y.-H.L.); (D.T.M.X.)
- Cancer Center, Wan Fang Hospital, Taipei Medical University, Taipei 11031, Taiwan
- TMU Research Center of Cancer Translational Medicine, Taipei Medical University, Taipei 11031, Taiwan;
| | - Jian-Ying Chuang
- TMU Research Center of Cancer Translational Medicine, Taipei Medical University, Taipei 11031, Taiwan;
- Ph.D. Program for Neural Regenerative Medicine, Taipei Medical University, Taipei 11031, Taiwan
- Research Center of Neuroscience, Taipei Medical University, Taipei 11031, Taiwan
| | - Chih-Yang Wang
- Ph.D. Program for Cancer Molecular Biology and Drug Discovery, College of Medical Science, Taipei Medical University, Taipei 11031, Taiwan; (C.-C.C.); (H.D.K.T.); (G.A.); (K.-H.L.)
- Graduate Institute of Cancer Biology and Drug Discovery, College of Medical Science and Technology, Taipei Medical University, Taipei 11031, Taiwan; (Y.-H.L.); (D.T.M.X.)
- Correspondence: (C.-Y.W.); (T.-J.K.)
| | - Tzu-Jen Kao
- TMU Research Center of Cancer Translational Medicine, Taipei Medical University, Taipei 11031, Taiwan;
- Ph.D. Program for Neural Regenerative Medicine, Taipei Medical University, Taipei 11031, Taiwan
- Research Center of Neuroscience, Taipei Medical University, Taipei 11031, Taiwan
- Correspondence: (C.-Y.W.); (T.-J.K.)
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