Dynamic regulation of human endogenous retroviruses mediates factor-induced reprogramming and differentiation potential
Pluripotency can be induced in somatic cells by overexpressing transcription factors, including POU class 5 homeobox 1 (OCT3/4), sex determining region Y-box 2 (SOX2), Krüppel-like factor 4 (KLF4), and myelocytomatosis oncogene (c-MYC). However, some induced pluripotent stem cells (iPSCs) exhibit de...
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| Vydáno v: | Proceedings of the National Academy of Sciences - PNAS Ročník 111; číslo 34; s. 12426 |
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| Hlavní autoři: | , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
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United States
26.08.2014
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| ISSN: | 1091-6490, 1091-6490 |
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| Abstract | Pluripotency can be induced in somatic cells by overexpressing transcription factors, including POU class 5 homeobox 1 (OCT3/4), sex determining region Y-box 2 (SOX2), Krüppel-like factor 4 (KLF4), and myelocytomatosis oncogene (c-MYC). However, some induced pluripotent stem cells (iPSCs) exhibit defective differentiation and inappropriate maintenance of pluripotency features. Here we show that dynamic regulation of human endogenous retroviruses (HERVs) is important in the reprogramming process toward iPSCs, and in re-establishment of differentiation potential. During reprogramming, OCT3/4, SOX2, and KLF4 transiently hyperactivated LTR7s--the long-terminal repeats of HERV type-H (HERV-H)--to levels much higher than in embryonic stem cells by direct occupation of LTR7 sites genome-wide. Knocking down LTR7s or long intergenic non-protein coding RNA, regulator of reprogramming (lincRNA-RoR), a HERV-H-driven long noncoding RNA, early in reprogramming markedly reduced the efficiency of iPSC generation. KLF4 and LTR7 expression decreased to levels comparable with embryonic stem cells once reprogramming was complete, but failure to resuppress KLF4 and LTR7s resulted in defective differentiation. We also observed defective differentiation and LTR7 activation when iPSCs had forced expression of KLF4. However, when aberrantly expressed KLF4 or LTR7s were suppressed in defective iPSCs, normal differentiation was restored. Thus, a major mechanism by which OCT3/4, SOX2, and KLF4 promote human iPSC generation and reestablish potential for differentiation is by dynamically regulating HERV-H LTR7s. |
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| AbstractList | Pluripotency can be induced in somatic cells by overexpressing transcription factors, including POU class 5 homeobox 1 (OCT3/4), sex determining region Y-box 2 (SOX2), Krüppel-like factor 4 (KLF4), and myelocytomatosis oncogene (c-MYC). However, some induced pluripotent stem cells (iPSCs) exhibit defective differentiation and inappropriate maintenance of pluripotency features. Here we show that dynamic regulation of human endogenous retroviruses (HERVs) is important in the reprogramming process toward iPSCs, and in re-establishment of differentiation potential. During reprogramming, OCT3/4, SOX2, and KLF4 transiently hyperactivated LTR7s--the long-terminal repeats of HERV type-H (HERV-H)--to levels much higher than in embryonic stem cells by direct occupation of LTR7 sites genome-wide. Knocking down LTR7s or long intergenic non-protein coding RNA, regulator of reprogramming (lincRNA-RoR), a HERV-H-driven long noncoding RNA, early in reprogramming markedly reduced the efficiency of iPSC generation. KLF4 and LTR7 expression decreased to levels comparable with embryonic stem cells once reprogramming was complete, but failure to resuppress KLF4 and LTR7s resulted in defective differentiation. We also observed defective differentiation and LTR7 activation when iPSCs had forced expression of KLF4. However, when aberrantly expressed KLF4 or LTR7s were suppressed in defective iPSCs, normal differentiation was restored. Thus, a major mechanism by which OCT3/4, SOX2, and KLF4 promote human iPSC generation and reestablish potential for differentiation is by dynamically regulating HERV-H LTR7s.Pluripotency can be induced in somatic cells by overexpressing transcription factors, including POU class 5 homeobox 1 (OCT3/4), sex determining region Y-box 2 (SOX2), Krüppel-like factor 4 (KLF4), and myelocytomatosis oncogene (c-MYC). However, some induced pluripotent stem cells (iPSCs) exhibit defective differentiation and inappropriate maintenance of pluripotency features. Here we show that dynamic regulation of human endogenous retroviruses (HERVs) is important in the reprogramming process toward iPSCs, and in re-establishment of differentiation potential. During reprogramming, OCT3/4, SOX2, and KLF4 transiently hyperactivated LTR7s--the long-terminal repeats of HERV type-H (HERV-H)--to levels much higher than in embryonic stem cells by direct occupation of LTR7 sites genome-wide. Knocking down LTR7s or long intergenic non-protein coding RNA, regulator of reprogramming (lincRNA-RoR), a HERV-H-driven long noncoding RNA, early in reprogramming markedly reduced the efficiency of iPSC generation. KLF4 and LTR7 expression decreased to levels comparable with embryonic stem cells once reprogramming was complete, but failure to resuppress KLF4 and LTR7s resulted in defective differentiation. We also observed defective differentiation and LTR7 activation when iPSCs had forced expression of KLF4. However, when aberrantly expressed KLF4 or LTR7s were suppressed in defective iPSCs, normal differentiation was restored. Thus, a major mechanism by which OCT3/4, SOX2, and KLF4 promote human iPSC generation and reestablish potential for differentiation is by dynamically regulating HERV-H LTR7s. Pluripotency can be induced in somatic cells by overexpressing transcription factors, including POU class 5 homeobox 1 (OCT3/4), sex determining region Y-box 2 (SOX2), Krüppel-like factor 4 (KLF4), and myelocytomatosis oncogene (c-MYC). However, some induced pluripotent stem cells (iPSCs) exhibit defective differentiation and inappropriate maintenance of pluripotency features. Here we show that dynamic regulation of human endogenous retroviruses (HERVs) is important in the reprogramming process toward iPSCs, and in re-establishment of differentiation potential. During reprogramming, OCT3/4, SOX2, and KLF4 transiently hyperactivated LTR7s--the long-terminal repeats of HERV type-H (HERV-H)--to levels much higher than in embryonic stem cells by direct occupation of LTR7 sites genome-wide. Knocking down LTR7s or long intergenic non-protein coding RNA, regulator of reprogramming (lincRNA-RoR), a HERV-H-driven long noncoding RNA, early in reprogramming markedly reduced the efficiency of iPSC generation. KLF4 and LTR7 expression decreased to levels comparable with embryonic stem cells once reprogramming was complete, but failure to resuppress KLF4 and LTR7s resulted in defective differentiation. We also observed defective differentiation and LTR7 activation when iPSCs had forced expression of KLF4. However, when aberrantly expressed KLF4 or LTR7s were suppressed in defective iPSCs, normal differentiation was restored. Thus, a major mechanism by which OCT3/4, SOX2, and KLF4 promote human iPSC generation and reestablish potential for differentiation is by dynamically regulating HERV-H LTR7s. |
| Author | Watanabe, Akira Takahashi, Kazutoshi Ohnuki, Mari Yamanaka, Shinya Tanabe, Koji Narita, Megumi Nakamura, Michiko Tokunaga, Yumie Nakamura, Masahiro Sutou, Kenta Teramoto, Ito Sawamura, Yuka |
| Author_xml | – sequence: 1 givenname: Mari surname: Ohnuki fullname: Ohnuki, Mari organization: Center for iPS Cell Research and Application, Kyoto University, Kyoto 606-8507, Japan; and – sequence: 2 givenname: Koji surname: Tanabe fullname: Tanabe, Koji organization: Center for iPS Cell Research and Application, Kyoto University, Kyoto 606-8507, Japan; and – sequence: 3 givenname: Kenta surname: Sutou fullname: Sutou, Kenta organization: Center for iPS Cell Research and Application, Kyoto University, Kyoto 606-8507, Japan; and – sequence: 4 givenname: Ito surname: Teramoto fullname: Teramoto, Ito organization: Center for iPS Cell Research and Application, Kyoto University, Kyoto 606-8507, Japan; and – sequence: 5 givenname: Yuka surname: Sawamura fullname: Sawamura, Yuka organization: Center for iPS Cell Research and Application, Kyoto University, Kyoto 606-8507, Japan; and – sequence: 6 givenname: Megumi surname: Narita fullname: Narita, Megumi organization: Center for iPS Cell Research and Application, Kyoto University, Kyoto 606-8507, Japan; and – sequence: 7 givenname: Michiko surname: Nakamura fullname: Nakamura, Michiko organization: Center for iPS Cell Research and Application, Kyoto University, Kyoto 606-8507, Japan; and – sequence: 8 givenname: Yumie surname: Tokunaga fullname: Tokunaga, Yumie organization: Center for iPS Cell Research and Application, Kyoto University, Kyoto 606-8507, Japan; and – sequence: 9 givenname: Masahiro surname: Nakamura fullname: Nakamura, Masahiro organization: Center for iPS Cell Research and Application, Kyoto University, Kyoto 606-8507, Japan; and – sequence: 10 givenname: Akira surname: Watanabe fullname: Watanabe, Akira organization: Center for iPS Cell Research and Application, Kyoto University, Kyoto 606-8507, Japan; and – sequence: 11 givenname: Shinya surname: Yamanaka fullname: Yamanaka, Shinya email: yamanaka@cira.kyoto-u.ac.jp, takahash@cira.kyoto-u.ac.jp organization: Center for iPS Cell Research and Application, Kyoto University, Kyoto 606-8507, Japan; and Gladstone Institute of Cardiovascular Disease, San Francisco, California 94158 yamanaka@cira.kyoto-u.ac.jp takahash@cira.kyoto-u.ac.jp – sequence: 12 givenname: Kazutoshi surname: Takahashi fullname: Takahashi, Kazutoshi email: yamanaka@cira.kyoto-u.ac.jp, takahash@cira.kyoto-u.ac.jp organization: Center for iPS Cell Research and Application, Kyoto University, Kyoto 606-8507, Japan; and yamanaka@cira.kyoto-u.ac.jp takahash@cira.kyoto-u.ac.jp |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25097266$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Cell Differentiation - genetics Cell Differentiation - physiology Cellular Reprogramming - genetics Cellular Reprogramming - physiology Embryonic Stem Cells - cytology Embryonic Stem Cells - physiology Embryonic Stem Cells - virology Endogenous Retroviruses - genetics Endogenous Retroviruses - physiology Epigenesis, Genetic Gene Expression Gene Knockdown Techniques Humans Induced Pluripotent Stem Cells - cytology Induced Pluripotent Stem Cells - physiology Induced Pluripotent Stem Cells - virology Kruppel-Like Transcription Factors - genetics Kruppel-Like Transcription Factors - physiology Octamer Transcription Factor-3 - genetics Octamer Transcription Factor-3 - physiology Pluripotent Stem Cells - cytology Pluripotent Stem Cells - physiology Pluripotent Stem Cells - virology RNA, Long Noncoding - antagonists & inhibitors RNA, Long Noncoding - genetics RNA, Viral - antagonists & inhibitors RNA, Viral - genetics SOXB1 Transcription Factors - genetics SOXB1 Transcription Factors - physiology |
| Title | Dynamic regulation of human endogenous retroviruses mediates factor-induced reprogramming and differentiation potential |
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