Nucleome programming is required for the foundation of totipotency in mammalian germline development.

Szczegóły
Abstrakt

Tytuł:: Nucleome programming is required for the foundation of totipotency in mammalian germline development.
Autorzy:: Nagano M; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.; Department of Anatomy and Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
Hu B; Department of Anatomy and Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan.; Department of Human Genetics, McGill University, Montreal, QC, Canada.
Yokobayashi S; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.; Department of Anatomy and Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan.; Center for iPS Cell Research and Application (CiRA), Kyoto University, Kyoto, Japan.
Yamamura A; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.; Department of Anatomy and Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
Umemura F; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.; Department of Anatomy and Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
Coradin M; Department of Biochemistry and Biophysics, University of Pennsylvania, Philadelphia, PA, USA.; Penn Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.; Department of Molecular, Cellular, and Developmental Biology, University of Colorado Boulder, Boulder, CO, USA.
Ohta H; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.; Department of Anatomy and Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
Yabuta Y; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.; Department of Anatomy and Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
Ishikura Y; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.; Department of Anatomy and Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
Okamoto I; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.; Department of Anatomy and Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
Ikeda H; Center for iPS Cell Research and Application (CiRA), Kyoto University, Kyoto, Japan.; Department of Embryology, Nara Medical University, Nara, Japan.
Kawahira N; Department of Molecular Cell Developmental Biology, School of Life Science, University of California, Los Angeles, CA, USA.; Laboratory for Developmental Morphogeometry, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan.
Nosaka Y; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.; Department of Anatomy and Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
Shimizu S; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.; Department of Anatomy and Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
Kojima Y; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.; Department of Anatomy and Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan.; Center for iPS Cell Research and Application (CiRA), Kyoto University, Kyoto, Japan.
Mizuta K; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.; Department of Anatomy and Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
Kasahara T; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.; RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.
Imoto Y; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.
Meehan K; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.
Stocsits R; Research Institute of Molecular Pathology, Vienna BioCenter, Vienna, Austria.
Wutz G; Research Institute of Molecular Pathology, Vienna BioCenter, Vienna, Austria.
Hiraoka Y; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.
Murakawa Y; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.; RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.
Yamamoto T; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.; Center for iPS Cell Research and Application (CiRA), Kyoto University, Kyoto, Japan.; Medical-risk Avoidance based on iPS Cells Team, RIKEN Center for Advanced Intelligence Project, Kyoto, Japan.
Tachibana K; Institute of Molecular Biotechnology of the Austrian Academy of Sciences, Vienna BioCenter, Vienna, Austria.; Department of Totipotency, Max Planck Institute of Biochemistry, Martinsried, Germany.
Peters JM; Research Institute of Molecular Pathology, Vienna BioCenter, Vienna, Austria.
Mirny LA; Institute for Medical Engineering and Science, and Department of Physics, Massachusetts Institute of Technology, Cambridge, MA, USA.
Garcia BA; Department of Biochemistry and Biophysics, University of Pennsylvania, Philadelphia, PA, USA.; Penn Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.; Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine, St. Louis, MO, USA.
Majewski J; Department of Human Genetics, McGill University, Montreal, QC, Canada.
Saitou M; Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan.; Department of Anatomy and Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan.; Center for iPS Cell Research and Application (CiRA), Kyoto University, Kyoto, Japan.
Źródło:: The EMBO journal [EMBO J] 2022 Jul 04; Vol. 41 (13), pp. e110600. Date of Electronic Publication: 2022 Jun 15.
Typ publikacji:: Journal Article; Research Support, Non-U.S. Gov't; Research Support, N.I.H., Extramural
Język:: English
Imprint Name(s):: Publication: 2014- : London : Wiley Blackwell
Original Publication: Eynsham, Oxford, England : Published for the European Molecular Biology Organization by IRL Press, [c1982-
MeSH Terms:: Epigenesis, Genetic*
Germ Cells*/metabolism
Animals ; Chromatin/genetics ; Chromatin/metabolism ; DNA Methylation ; Epigenomics ; Female ; Male ; Mammals/genetics ; Mice ; Spermatogonia
References:: Science. 2020 Mar 6;367(6482):. (PMID: 32054698)
EMBO J. 2017 Jul 3;36(13):1888-1907. (PMID: 28559416)
Cell Rep. 2016 Dec 6;17(10):2789-2804. (PMID: 27926879)
F1000Res. 2015 Dec 30;4:1521. (PMID: 26925227)
Genome Biol. 2017 Jan 30;18(1):21. (PMID: 28137286)
Nat Genet. 2019 Sep;51(9):1369-1379. (PMID: 31477927)
Cell. 2014 Nov 6;159(4):800-13. (PMID: 25417157)
Nat Commun. 2021 Dec 2;12(1):7020. (PMID: 34857746)
Genome Biol. 2018 Aug 10;19(1):109. (PMID: 30097049)
Methods. 2017 Jul 1;123:56-65. (PMID: 28435001)
F1000Res. 2020 Jul 15;9:. (PMID: 33564394)
Nature. 2017 Sep 13;549(7671):219-226. (PMID: 28905911)
iScience. 2020 Apr 24;23(4):101034. (PMID: 32315832)
Nucleic Acids Res. 2022 Apr 8;50(6):e35. (PMID: 34928367)
Science. 2021 Oct;374(6563):eaaz6830. (PMID: 34591639)
Commun Biol. 2021 May 13;4(1):571. (PMID: 33986449)
Cell. 2007 Feb 23;128(4):747-62. (PMID: 17320511)
J Proteome Res. 2018 Jul 6;17(7):2533-2541. (PMID: 29790754)
Cell Stem Cell. 2011 Jun 3;8(6):676-87. (PMID: 21624812)
Nucleic Acids Res. 2016 Jul 8;44(W1):W160-5. (PMID: 27079975)
Nature. 2012 Jan 04;481(7381):389-93. (PMID: 22217937)
Nat Genet. 2019 May;51(5):835-843. (PMID: 31011212)
Cell. 2014 Dec 18;159(7):1665-80. (PMID: 25497547)
Nat Commun. 2020 Feb 6;11(1):747. (PMID: 32029740)
Nucleic Acids Res. 2020 Apr 17;48(7):e39. (PMID: 32083658)
Nat Genet. 2018 Feb;50(2):238-249. (PMID: 29335546)
Cell Syst. 2016 Jul;3(1):95-8. (PMID: 27467249)
Nature. 2020 Jul;583(7818):744-751. (PMID: 32728240)
Genome Res. 2008 Nov;18(11):1752-62. (PMID: 18682548)
Nucleus. 2014 Mar-Apr;5(2):163-72. (PMID: 24637835)
Nat Genet. 2019 Sep;51(9):1380-1388. (PMID: 31427791)
Biophys J. 2017 Feb 7;112(3):473-490. (PMID: 28131315)
J Cell Biol. 2015 Jan 5;208(1):33-52. (PMID: 25559185)
Nature. 2019 Nov;575(7782):390-394. (PMID: 31618757)
Nat Rev Genet. 2016 Oct;17(10):585-600. (PMID: 27573372)
Epigenetics. 2014 Nov;9(11):1439-45. (PMID: 25482057)
Mol Cell. 2020 Feb 20;77(4):825-839.e7. (PMID: 31837995)
Genome Biol. 2014;15(12):550. (PMID: 25516281)
Mol Cell. 2019 Oct 17;76(2):320-328. (PMID: 31563431)
Bioinformatics. 2021 Feb 11;:. (PMID: 33576390)
Elife. 2019 Oct 01;8:. (PMID: 31573510)
Biol Reprod. 2003 Aug;69(2):612-6. (PMID: 12700182)
Biol Reprod. 2021 Feb 11;104(2):344-360. (PMID: 33079185)
Physiol Rev. 2016 Jan;96(1):1-17. (PMID: 26537427)
Cell. 2020 Sep 17;182(6):1474-1489.e23. (PMID: 32841603)
Nature. 2005 Nov 17;438(7066):369-73. (PMID: 16227973)
Dev Cell. 2016 Oct 10;39(1):87-103. (PMID: 27642137)
Nat Commun. 2020 Nov 16;11(1):5795. (PMID: 33199682)
Cell. 2011 Aug 19;146(4):519-32. (PMID: 21820164)
Nat Struct Mol Biol. 2019 Mar;26(3):164-174. (PMID: 30778236)
Bioinformatics. 2012 Feb 15;28(4):573-80. (PMID: 22247279)
Bioinformatics. 2016 Feb 15;32(4):587-9. (PMID: 26508757)
Bioinformatics. 2021 Mar 03;:. (PMID: 33681991)
Genome Biol. 2015 Apr 14;16:77. (PMID: 25886366)
Bioinformatics. 2018 Sep 1;34(17):i884-i890. (PMID: 30423086)
Nucleic Acids Res. 2016 Mar 18;44(5):e45. (PMID: 26578583)
Sci Rep. 2018 Jun 25;8(1):9588. (PMID: 29942049)
Dev Growth Differ. 2000 Apr;42(2):105-12. (PMID: 10830433)
EMBO J. 2017 Nov 2;36(21):3100-3119. (PMID: 28928204)
Proc Natl Acad Sci U S A. 2013 Apr 9;110(15):6037-42. (PMID: 23530188)
J Cell Biol. 2004 Aug 16;166(4):493-505. (PMID: 15302854)
EMBO J. 2017 Dec 15;36(24):3573-3599. (PMID: 29217591)
Cell. 2004 Dec 29;119(7):1001-12. (PMID: 15620358)
Nature. 2008 May 22;453(7194):519-23. (PMID: 18497825)
BMC Bioinformatics. 2021 Apr 10;22(1):183. (PMID: 33838653)
Nat Commun. 2021 Jun 7;12(1):3366. (PMID: 34099725)
Nature. 2008 Jun 12;453(7197):948-51. (PMID: 18463634)
Nucleic Acids Res. 2015 Apr 30;43(8):e51. (PMID: 25653163)
Cold Spring Harb Perspect Biol. 2011 Jun 01;3(6):. (PMID: 21555407)
Nature. 1977 Jun 2;267(5610):430-1. (PMID: 559943)
BMC Bioinformatics. 2019 Oct 4;20(1):487. (PMID: 31585526)
Nucleic Acids Res. 2016 Apr 20;44(7):e70. (PMID: 26704975)
Nature. 2009 Nov 19;462(7271):315-22. (PMID: 19829295)
Mol Cell. 2012 Dec 28;48(6):849-62. (PMID: 23219530)
Cell Stem Cell. 2014 Jun 5;14(6):710-9. (PMID: 24905162)
J Cell Biol. 2013 Dec 9;203(5):767-83. (PMID: 24297746)
Cell. 2017 Jul 13;170(2):367-381.e20. (PMID: 28709003)
Neurochem Res. 2020 Mar;45(3):606-619. (PMID: 32020491)
Mol Cell. 2019 Feb 7;73(3):547-561.e6. (PMID: 30735655)
BMC Bioinformatics. 2011 Mar 17;12:77. (PMID: 21414208)
Bioinformatics. 2021 May 17;37(7):951-955. (PMID: 32866221)
Bioinformatics. 2010 Jan 1;26(1):139-40. (PMID: 19910308)
Nature. 2017 Apr 6;544(7648):110-114. (PMID: 28355183)
Nature. 2017 Jul 12;547(7662):232-235. (PMID: 28703188)
Methods Mol Biol. 2014;1164:67-85. (PMID: 24927836)
Nat Methods. 2013 Dec;10(12):1213-8. (PMID: 24097267)
Cell Stem Cell. 2015 May 7;16(5):517-32. (PMID: 25800778)
Genome Biol. 2008;9(9):R137. (PMID: 18798982)
Nat Methods. 2012 Mar 04;9(4):357-9. (PMID: 22388286)
Cell. 2012 Apr 27;149(3):590-604. (PMID: 22541430)
Bioinformatics. 2013 Jan 1;29(1):15-21. (PMID: 23104886)
Annu Rev Genet. 2017 Nov 27;51:265-285. (PMID: 28853925)
Stem Cells. 2008 Feb;26(2):339-47. (PMID: 18024419)
Mol Cell. 2010 May 28;38(4):603-13. (PMID: 20513434)
Nat Struct Mol Biol. 2019 Mar;26(3):175-184. (PMID: 30778237)
Nat Protoc. 2006;1(2):729-48. (PMID: 17406303)
BMC Bioinformatics. 2020 Jul 20;21(1):319. (PMID: 32689928)
Mol Cell. 2016 Jun 16;62(6):834-847. (PMID: 27264872)
Sci Rep. 2019 Jun 27;9(1):9354. (PMID: 31249361)
Genome Biol. 2019 Dec 18;20(1):282. (PMID: 31847870)
Bioinformatics. 2020 May 1;36(10):2980-2985. (PMID: 32003791)
Cell Rep. 2019 Jul 9;28(2):352-367.e9. (PMID: 31291573)
Bioinformatics. 2020 Jan 1;36(1):311-316. (PMID: 31290943)
Cell. 2017 Oct 19;171(3):573-587.e14. (PMID: 29033129)
Nat Rev Mol Cell Biol. 2019 Sep;20(9):535-550. (PMID: 31197269)
Bioinformatics. 2011 Jun 1;27(11):1571-2. (PMID: 21493656)
Nucleic Acids Res. 2020 Apr 6;48(6):e31. (PMID: 32009147)
Bioinformatics. 2014 Sep 1;30(17):i386-92. (PMID: 25161224)
F1000Res. 2015 Nov 20;4:1310. (PMID: 26835000)
Nat Commun. 2021 Feb 26;12(1):1307. (PMID: 33637709)
Nat Genet. 2019 Dec;51(12):1664-1669. (PMID: 31784727)
Nat Methods. 2017 Oct;14(10):959-962. (PMID: 28846090)
Bioinformatics. 2009 Aug 15;25(16):2078-9. (PMID: 19505943)
Cell Rep. 2021 Feb 23;34(8):108769. (PMID: 33626351)
J Vis Exp. 2016 May 17;(111):. (PMID: 27286567)
Nat Methods. 2017 Apr;14(4):417-419. (PMID: 28263959)
Genome Biol. 2018 Sep 28;19(1):150. (PMID: 30266094)
Nat Genet. 2011 Jun 26;43(8):768-75. (PMID: 21706001)
Cell Rep. 2019 Jun 18;27(12):3500-3510.e4. (PMID: 31216471)
Cell Stem Cell. 2021 Dec 2;28(12):2167-2179.e9. (PMID: 34496297)
Cell. 2017 Oct 19;171(3):557-572.e24. (PMID: 29053968)
Bioinformatics. 2010 Mar 15;26(6):841-2. (PMID: 20110278)
Genome Res. 2012 Feb;22(2):246-58. (PMID: 22156296)
Nature. 2017 Nov 2;551(7678):51-56. (PMID: 29094699)
Nat Genet. 2020 Oct;52(10):1088-1098. (PMID: 32929285)
Genome Biol. 2020 Dec 17;21(1):303. (PMID: 33334380)
Nat Cell Biol. 2019 Oct;21(10):1179-1190. (PMID: 31548608)
PLoS Genet. 2012;8(3):e1002575. (PMID: 22438826)
Nat Genet. 2010 Dec;42(12):1093-100. (PMID: 21057502)
Cell Stem Cell. 2015 Aug 6;17(2):178-94. (PMID: 26189426)
Nat Commun. 2021 May 10;12(1):2439. (PMID: 33972523)
EMBO J. 2022 Jul 4;41(13):e110600. (PMID: 35703121)
BMC Genomics. 2015 Aug 20;16:624. (PMID: 26290333)
Bioinformatics. 2019 Nov 1;35(21):4392-4393. (PMID: 30923821)
Nucleic Acids Res. 2014 Jun;42(11):e92. (PMID: 24782521)
Nat Cell Biol. 2014 Jun;16(6):516-28. (PMID: 24859004)
Grant Information:: P01 CA196539 United States CA NCI NIH HHS; R01 AI118891 United States AI NIAID NIH HHS; R01 NS111997 United States NS NINDS NIH HHS
Contributed Indexing:: Keywords: 3D genome organization; epigenetic reprogramming; germ cells; lamina-associated domains; nucleome
Molecular Sequence:: GEO GSE183828
Substance Nomenclature:: 0 (Chromatin)
Entry Date(s):: Date Created: 20220615 Date Completed: 20220707 Latest Revision: 20230617
Update Code:: 20240105
PubMed Central ID:: PMC9251848
DOI:: 10.15252/embj.2022110600
PMID:: 35703121
: Czasopismo naukowe

Full Text Finder

Germ cells are unique in engendering totipotency, yet the mechanisms underlying this capacity remain elusive. Here, we perform comprehensive and in-depth nucleome analysis of mouse germ-cell development in vitro, encompassing pluripotent precursors, primordial germ cells (PGCs) before and after epigenetic reprogramming, and spermatogonia/spermatogonial stem cells (SSCs). Although epigenetic reprogramming, including genome-wide DNA de-methylation, creates broadly open chromatin with abundant enhancer-like signatures, the augmented chromatin insulation safeguards transcriptional fidelity. These insulatory constraints are then erased en masse for spermatogonial development. Notably, despite distinguishing epigenetic programming, including global DNA re-methylation, the PGCs-to-spermatogonia/SSCs development entails further euchromatization. This accompanies substantial erasure of lamina-associated domains, generating spermatogonia/SSCs with a minimal peripheral attachment of chromatin except for pericentromeres-an architecture conserved in primates. Accordingly, faulty nucleome maturation, including persistent insulation and improper euchromatization, leads to impaired spermatogenic potential. Given that PGCs after epigenetic reprogramming serve as oogenic progenitors as well, our findings elucidate a principle for the nucleome programming that creates gametogenic progenitors in both sexes, defining a basis for nuclear totipotency.
(© 2022 The Authors.)

Informacja