The Zscan4-Tet2 Transcription Nexus Regulates Metabolic Rewiring and Enhances Proteostasis to Promote Reprogramming
Summary: Evolutionarily conserved SCAN (named after SRE-ZBP, CTfin51, AW-1, and Number 18 cDNA)-domain-containing zinc finger transcription factors (ZSCAN) have been found in both mouse and human genomes. Zscan4 is transiently expressed during zygotic genome activation (ZGA) in preimplantation embry...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2020-07-01
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| Series: | Cell Reports |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124720308585 |
| _version_ | 1819059650672197632 |
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| author | Zhou-Li Cheng Meng-Li Zhang Huai-Peng Lin Chao Gao Jun-Bin Song Zhihong Zheng Linpeng Li Yanan Zhang Xiaoqi Shen Hao Zhang Zhenghui Huang Wuqiang Zhan Cheng Zhang Xu Hu Yi-Ping Sun Lubing Jiang Lei Sun Yanhui Xu Chen Yang Yuanlong Ge Yong Zhao Xingguo Liu Hui Yang Pengyuan Liu Xing Guo Kun-Liang Guan Yue Xiong Mingliang Zhang Dan Ye |
| author_facet | Zhou-Li Cheng Meng-Li Zhang Huai-Peng Lin Chao Gao Jun-Bin Song Zhihong Zheng Linpeng Li Yanan Zhang Xiaoqi Shen Hao Zhang Zhenghui Huang Wuqiang Zhan Cheng Zhang Xu Hu Yi-Ping Sun Lubing Jiang Lei Sun Yanhui Xu Chen Yang Yuanlong Ge Yong Zhao Xingguo Liu Hui Yang Pengyuan Liu Xing Guo Kun-Liang Guan Yue Xiong Mingliang Zhang Dan Ye |
| author_sort | Zhou-Li Cheng |
| collection | DOAJ |
| description | Summary: Evolutionarily conserved SCAN (named after SRE-ZBP, CTfin51, AW-1, and Number 18 cDNA)-domain-containing zinc finger transcription factors (ZSCAN) have been found in both mouse and human genomes. Zscan4 is transiently expressed during zygotic genome activation (ZGA) in preimplantation embryos and induced pluripotent stem cell (iPSC) reprogramming. However, little is known about the mechanism of Zscan4 underlying these processes of cell fate control. Here, we show that Zscan4f, a representative of ZSCAN proteins, is able to recruit Tet2 through its SCAN domain. The Zscan4f-Tet2 interaction promotes DNA demethylation and regulates the expression of target genes, particularly those encoding glycolytic enzymes and proteasome subunits. Zscan4f regulates metabolic rewiring, enhances proteasome function, and ultimately promotes iPSC generation. These results identify Zscan4f as an important partner of Tet2 in regulating target genes and promoting iPSC generation and suggest a possible and common mechanism shared by SCAN family transcription factors to recruit ten-eleven translocation (TET) DNA dioxygenases to regulate diverse cellular processes, including reprogramming. |
| first_indexed | 2024-12-21T14:14:28Z |
| format | Article |
| id | doaj.art-49b552f6eee04c049922b1fa4b9cd396 |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-12-21T14:14:28Z |
| publishDate | 2020-07-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-49b552f6eee04c049922b1fa4b9cd3962022-12-21T19:00:57ZengElsevierCell Reports2211-12472020-07-01322107877The Zscan4-Tet2 Transcription Nexus Regulates Metabolic Rewiring and Enhances Proteostasis to Promote ReprogrammingZhou-Li Cheng0Meng-Li Zhang1Huai-Peng Lin2Chao Gao3Jun-Bin Song4Zhihong Zheng5Linpeng Li6Yanan Zhang7Xiaoqi Shen8Hao Zhang9Zhenghui Huang10Wuqiang Zhan11Cheng Zhang12Xu Hu13Yi-Ping Sun14Lubing Jiang15Lei Sun16Yanhui Xu17Chen Yang18Yuanlong Ge19Yong Zhao20Xingguo Liu21Hui Yang22Pengyuan Liu23Xing Guo24Kun-Liang Guan25Yue Xiong26Mingliang Zhang27Dan Ye28Huashan Hospital, Fudan University, and Molecular and Cell Biology Lab, the Shanghai Key Laboratory of Medical Epigenetics, Institutes of Biomedical Sciences, Fudan University, and the Key Laboratory of Metabolism and Molecular, Ministry of Education, Shanghai, China; The International Co-laboratory of Medical Epigenetics and Metabolism, Ministry of Science and Technology, Beijing, ChinaHuashan Hospital, Fudan University, and Molecular and Cell Biology Lab, the Shanghai Key Laboratory of Medical Epigenetics, Institutes of Biomedical Sciences, Fudan University, and the Key Laboratory of Metabolism and Molecular, Ministry of Education, Shanghai, China; Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai 200040, ChinaMedical College of Xiamen University, Xiamen 361102, ChinaHuashan Hospital, Fudan University, and Molecular and Cell Biology Lab, the Shanghai Key Laboratory of Medical Epigenetics, Institutes of Biomedical Sciences, Fudan University, and the Key Laboratory of Metabolism and Molecular, Ministry of Education, Shanghai, China; The International Co-laboratory of Medical Epigenetics and Metabolism, Ministry of Science and Technology, Beijing, ChinaHuashan Hospital, Fudan University, and Molecular and Cell Biology Lab, the Shanghai Key Laboratory of Medical Epigenetics, Institutes of Biomedical Sciences, Fudan University, and the Key Laboratory of Metabolism and Molecular, Ministry of Education, Shanghai, China; The International Co-laboratory of Medical Epigenetics and Metabolism, Ministry of Science and Technology, Beijing, ChinaDepartment of Gynecologic Oncology, Women’s Hospital and Institute of Translational Medicine, School of Medicine, Zhejiang University, Hangzhou, Zhejiang 310029, ChinaThe Key Laboratory of Regenerative Biology, Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, South China Institute for Stem Cell Biology and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou 510530, ChinaLife Sciences Institute, Zhejiang University, Hangzhou 310058, ChinaLife Sciences Institute, Zhejiang University, Hangzhou 310058, ChinaKey Laboratory of Synthetic Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, ChinaInstitute Pasteur of Shanghai, Chinese Academy of Sciences, Shanghai 200031, ChinaHuashan Hospital, Fudan University, and Molecular and Cell Biology Lab, the Shanghai Key Laboratory of Medical Epigenetics, Institutes of Biomedical Sciences, Fudan University, and the Key Laboratory of Metabolism and Molecular, Ministry of Education, Shanghai, China; The International Co-laboratory of Medical Epigenetics and Metabolism, Ministry of Science and Technology, Beijing, ChinaHuashan Hospital, Fudan University, and Molecular and Cell Biology Lab, the Shanghai Key Laboratory of Medical Epigenetics, Institutes of Biomedical Sciences, Fudan University, and the Key Laboratory of Metabolism and Molecular, Ministry of Education, Shanghai, China; The International Co-laboratory of Medical Epigenetics and Metabolism, Ministry of Science and Technology, Beijing, ChinaDepartment of Histoembryology, Genetics and Developmental Biology, Shanghai Jiao Tong University School of Medicine, Shanghai Key Laboratory of Reproductive Medicine, Shanghai, ChinaHuashan Hospital, Fudan University, and Molecular and Cell Biology Lab, the Shanghai Key Laboratory of Medical Epigenetics, Institutes of Biomedical Sciences, Fudan University, and the Key Laboratory of Metabolism and Molecular, Ministry of Education, Shanghai, China; The International Co-laboratory of Medical Epigenetics and Metabolism, Ministry of Science and Technology, Beijing, ChinaInstitute Pasteur of Shanghai, Chinese Academy of Sciences, Shanghai 200031, ChinaHuashan Hospital, Fudan University, and Molecular and Cell Biology Lab, the Shanghai Key Laboratory of Medical Epigenetics, Institutes of Biomedical Sciences, Fudan University, and the Key Laboratory of Metabolism and Molecular, Ministry of Education, Shanghai, China; The International Co-laboratory of Medical Epigenetics and Metabolism, Ministry of Science and Technology, Beijing, ChinaHuashan Hospital, Fudan University, and Molecular and Cell Biology Lab, the Shanghai Key Laboratory of Medical Epigenetics, Institutes of Biomedical Sciences, Fudan University, and the Key Laboratory of Metabolism and Molecular, Ministry of Education, Shanghai, China; The International Co-laboratory of Medical Epigenetics and Metabolism, Ministry of Science and Technology, Beijing, ChinaKey Laboratory of Synthetic Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, ChinaMOE Key Laboratory of Gene Function and Regulation, State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou 510006, ChinaMOE Key Laboratory of Gene Function and Regulation, State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou 510006, ChinaThe Key Laboratory of Regenerative Biology, Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, South China Institute for Stem Cell Biology and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou 510530, ChinaDepartment of Neurosurgery, Huashan Hospital, Fudan University, Shanghai 200040, ChinaDepartment of Respiratory Medicine, Sir Run Run Shaw Hospital and Institute of Translational Medicine, School of Medicine, Zhejiang University, Hangzhou, Zhejiang 310016, ChinaLife Sciences Institute, Zhejiang University, Hangzhou 310058, ChinaDepartment of Pharmacology and Moores Cancer Center, University of California San Diego, La Jolla, CA 92093, USADepartment of Biochemistry and Biophysics, Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USADepartment of Histoembryology, Genetics and Developmental Biology, Shanghai Jiao Tong University School of Medicine, Shanghai Key Laboratory of Reproductive Medicine, Shanghai, China; Corresponding authorHuashan Hospital, Fudan University, and Molecular and Cell Biology Lab, the Shanghai Key Laboratory of Medical Epigenetics, Institutes of Biomedical Sciences, Fudan University, and the Key Laboratory of Metabolism and Molecular, Ministry of Education, Shanghai, China; The International Co-laboratory of Medical Epigenetics and Metabolism, Ministry of Science and Technology, Beijing, China; Department of General Surgery, Huashan Hospital, Fudan University, Shanghai 200040, China; Corresponding authorSummary: Evolutionarily conserved SCAN (named after SRE-ZBP, CTfin51, AW-1, and Number 18 cDNA)-domain-containing zinc finger transcription factors (ZSCAN) have been found in both mouse and human genomes. Zscan4 is transiently expressed during zygotic genome activation (ZGA) in preimplantation embryos and induced pluripotent stem cell (iPSC) reprogramming. However, little is known about the mechanism of Zscan4 underlying these processes of cell fate control. Here, we show that Zscan4f, a representative of ZSCAN proteins, is able to recruit Tet2 through its SCAN domain. The Zscan4f-Tet2 interaction promotes DNA demethylation and regulates the expression of target genes, particularly those encoding glycolytic enzymes and proteasome subunits. Zscan4f regulates metabolic rewiring, enhances proteasome function, and ultimately promotes iPSC generation. These results identify Zscan4f as an important partner of Tet2 in regulating target genes and promoting iPSC generation and suggest a possible and common mechanism shared by SCAN family transcription factors to recruit ten-eleven translocation (TET) DNA dioxygenases to regulate diverse cellular processes, including reprogramming.http://www.sciencedirect.com/science/article/pii/S2211124720308585ZSCAN4TET2SCAN domaininduced pluripotent stem cellsiPSCsmetabolic rewiring |
| spellingShingle | Zhou-Li Cheng Meng-Li Zhang Huai-Peng Lin Chao Gao Jun-Bin Song Zhihong Zheng Linpeng Li Yanan Zhang Xiaoqi Shen Hao Zhang Zhenghui Huang Wuqiang Zhan Cheng Zhang Xu Hu Yi-Ping Sun Lubing Jiang Lei Sun Yanhui Xu Chen Yang Yuanlong Ge Yong Zhao Xingguo Liu Hui Yang Pengyuan Liu Xing Guo Kun-Liang Guan Yue Xiong Mingliang Zhang Dan Ye The Zscan4-Tet2 Transcription Nexus Regulates Metabolic Rewiring and Enhances Proteostasis to Promote Reprogramming Cell Reports ZSCAN4 TET2 SCAN domain induced pluripotent stem cells iPSCs metabolic rewiring |
| title | The Zscan4-Tet2 Transcription Nexus Regulates Metabolic Rewiring and Enhances Proteostasis to Promote Reprogramming |
| title_full | The Zscan4-Tet2 Transcription Nexus Regulates Metabolic Rewiring and Enhances Proteostasis to Promote Reprogramming |
| title_fullStr | The Zscan4-Tet2 Transcription Nexus Regulates Metabolic Rewiring and Enhances Proteostasis to Promote Reprogramming |
| title_full_unstemmed | The Zscan4-Tet2 Transcription Nexus Regulates Metabolic Rewiring and Enhances Proteostasis to Promote Reprogramming |
| title_short | The Zscan4-Tet2 Transcription Nexus Regulates Metabolic Rewiring and Enhances Proteostasis to Promote Reprogramming |
| title_sort | zscan4 tet2 transcription nexus regulates metabolic rewiring and enhances proteostasis to promote reprogramming |
| topic | ZSCAN4 TET2 SCAN domain induced pluripotent stem cells iPSCs metabolic rewiring |
| url | http://www.sciencedirect.com/science/article/pii/S2211124720308585 |
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