MacroH2A in stem cells: a story beyond gene repression.

Animals; Cell Differentiation; Cellular Reprogramming; Chromatin/metabolism; Embryonic Development; Epigenesis, Genetic; Histones/antagonists & inhibitors/genetics/metabolism; Humans; Mice; Mutation; RNA Interference; RNA, Small Interfering/metabolism; Stem Cells/cytology/metabolism; Zebrafish

Abstract :

[en] The importance of epigenetic mechanisms is most clearly illustrated during early development when a totipotent cell goes through multiple cell fate transitions to form the many different cell types and tissues that constitute the embryo and the adult. The exchange of a canonical H2A histone for the 'repressive' macroH2A variant is one of the most striking epigenetic chromatin alterations that can occur at the level of the nucleosome. Here, we discuss recent data on macroH2A in zebrafish and mouse embryos, in embryonic and adult stem cells and also in nuclear reprogramming. We highlight the role of macroH2A in the establishment and maintenance of differentiated states and we discuss its still poorly recognized function in transcriptional activation.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Creppe, Catherine ; IMPPC - Badalona > Chromatin and Cell Fate

Posavec, Melanija

Douet, Julien

Buschbeck, Marcus

Language :

English

Title :

MacroH2A in stem cells: a story beyond gene repression.

Publication date :

2012

Journal title :

Epigenomics

ISSN :

1750-1911

eISSN :

1750-192X

Publisher :

Future Medicine, London, United Kingdom

Volume :

Issue :

Pages :

221-7

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 26 January 2016

Statistics

Number of views

111 (0 by ULiège)

Number of downloads

269 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Waddington CH. The Epigenetics of Birds. Cambridge University Press, Cambridge, UK (1952).
Bird A. Perceptions of epigenetics. Nature 447(7143), 396-398 (2007).
Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 21(3), 381-395 (2011).
Evans M. Discovering pluripotency: 30 years of mouse embryonic stem cells. Nat. Rev. Mol. Cell Biol. 12(10), 680-686 (2011).
Smith AG. Embryo-derived stem cells: of mice and men. Annu. Rev. Cell Dev. Biol. 17, 435-462 (2001).
Boyer LA, Lee TI, Cole MF et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122(6), 947-956 (2005). Leading work among the manuscripts that reported the identification of the trancriptional circuit that maintains pluripotency.
Chew JL, Loh YH, Zhang W et al. Reciprocal transcriptional regulation of Pou5f1 and Sox2 via the Oct4/Sox2 complex in embryonic stem cells. Mol. Cell Biol. 25(14), 6031-6046 (2005).
Loh YH, Wu Q, Chew JL et al. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat. Genet. 38(4), 431-440 (2006).
Chen X, Xu H, Yuan P et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133(6), 1106-1117 (2008).
Kim J, Chu J, Shen X, Wang J, Orkin SH. An extended transcriptional network for pluripotency of embryonic stem cells. Cell 132(6), 1049-1061 (2008).
Niwa H. How is pluripotency determined and maintained? Development 134(4), 635-646 (2007).
Hake SB, Xiao A, Allis CD. Linking the epigenetic 'language' of covalent histone modifications to cancer. Br. J. Cancer 96(Suppl.), R31-R39 (2007).
Kouzarides T. Chromatin modifications and their function. Cell 128(4), 693-705 (2007).
Williams K, Christensen J, Helin K. DNA methylation: TET proteins-guardians of CpG islands? EMBO Rep. 13(1), 28-35 (2011).
Boulard M, Bouvet P, Kundu TK, Dimitrov S. Histone variant nucleosomes: structure, function and implication in disease. Subcell Biochem. 41, 71-89 (2007).
Banaszynski LA, Allis CD, Lewis PW. Histone variants in metazoan development. Dev. Cell 19(5), 662-674 (2011).
Pehrson JR, Fried VA. MacroH2A, a core histone containing a large nonhistone region. Science 257(5075), 1398-1400 (1992).
Buschbeck M, Di Croce L. Approaching the molecular and physiological function of macroH2A variants. Epigenetics 5(2), 118-123 (2010).
Rasmussen TP, Huang T, Mastrangelo MA, Loring J, Panning B, Jaenisch R. Messenger RNAs encoding mouse histone macroH2A1 isoforms are expressed at similar levels in male and female cells and result from alternative splicing. Nucleic Acids Res. 27(18), 3685-3689 (1999).
Chadwick BP, Willard HF. Histone H2A variants and the inactive X chromosome: identification of a second macroH2A variant. Hum. Mol. Genet. 10(10), 1101-1113 (2001).
Costanzi C, Pehrson JR. MACROH2A2, a new member of the MARCOH2A core histone family. J. Biol. Chem. 276(24), 21776-21784 (2001).
Chang CC, Ma Y, Jacobs S, Tian XC, Yang X, Rasmussen TP. A maternal store of macroH2A is removed from pronuclei prior to onset of somatic macroH2A expression in preimplantation embryos. Dev. Biol. 278(2), 367-380 (2005).
Nashun B, Yukawa M, Liu H, Akiyama T, Aoki F. Changes in the nuclear deposition of histone H2A variants during pre-implantation development in mice. Development 137(22), 3785-3794 (2010). Provides evidence that a tight regulation of macroH2A levels is essential at the premorula stage of early development.
Pehrson JR, Costanzi C, Dharia C. Developmental and tissue expression patterns of histone macroH2A1 subtypes. J. Cell Biochem. 65(1), 107-113 (1997).
Dai B, Rasmussen TP. Global epiproteomic signatures distinguish embryonic stem cells from differentiated cells. Stem Cells 25(10), 2567-2574 (2007).
Mietton F, Sengupta AK, Molla A et al. Weak but uniform enrichment of the histone variant macroH2A1 along the inactive X chromosome. Mol. Cell Biol. 29(1), 150-156 (2009).
Creppe C, Janich P, Cantariño N et al. MacroH2A regulates the commitment to differentiation of embryonic and adult stem cells. Mol. Cell Biol. doi:10.1128/MCB.06323-11 (2012) (Epub ahead of print). Demonstrates that the proactivating function of macroH2A contributes to the regulation of embryonic stem cell differentiation.
Buschbeck M, Uribesalgo I, Wibowo I et al. The histone variant macroH2A is an epigenetic regulator of key developmental genes. Nat. Struct. Mol. Biol. 16(10), 1074-1079 (2009). This study provided the first proof for a role of macroH2A in development and differentiation.
Changolkar LN, Costanzi C, Leu NA, Chen D, McLaughlin KJ, Pehrson JR. Developmental changes in histone macroH2A1-mediated gene regulation. Mol. Cell Biol. 27(7), 2758-2764 (2007). Together with [30], this work provides the description of the metabolic phenotype of macroH2A1-deficient mice.
Boulard M, Storck S, Cong R, Pinto R, Delage H, Bouvet P. Histone variant macroH2A1 deletion in mice causes female-specific steatosis. Epigenetics Chromatin 3(1), 8 (2010). Together with [29], this work provides the description of the metabolic phenotype of macroH2A1-deficient mice.
Tanasijevic B, Rasmussen TP. X chromosome inactivation and differentiation occur readily in ES cells doubly-deficient for macroH2A1 and macroH2A2. PLoS ONE 6(6), e21512 (2011).
Epsztejn-Litman S, Feldman N, Abu-Remaileh M et al. De novo DNA methylation promoted by G9a prevents reprogramming of embryonically silenced genes. Nat. Struct. Mol. Biol. 15(11), 1176-1183 (2008).
Feldman N, Gerson A, Fang J et al. G9a-mediated irreversible epigenetic inactivation of Oct-3/4 during early embryogenesis. Nat. Cell Biol. 8(2), 188-194 (2006).
Chang CC, Gao S, Sung LY et al. Rapid elimination of the histone variant MacroH2A from somatic cell heterochromatin after nuclear transfer. Cell Reprogram. 12(1), 43-53 (2010).
Pasque V, Gillich A, Garrett N, Gurdon JB. Histone variant macroH2A confers resistance to nuclear reprogramming. EMBO J. 30(12), 2373-2387 (2011). Demonstrates that macroH2A maintains differentiated states and constitutes a layer of resistance to reprogramming.
Pasque V, Jullien J, Miyamoto K, Halley-Stott RP, Gurdon JB. Epigenetic factors influencing resistance to nuclear reprogramming. Trends Genet. 27(12), 516-525 (2011).
Pasque V, Halley-Stott RP, Gillich A, Garrett N, Gurdon JB. Epigenetic stability of repressed states involving the histone variant macroH2A revealed by nuclear transfer to xenopus oocytes. Nucleus 2(6), 533-539 (2011).
Costanzi C, Pehrson JR. Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 393(6685), 599-601 (1998).
Changolkar LN, Pehrson JR. macroH2A1 histone variants are depleted on active genes but concentrated on the inactive X chromosome. Mol. Cell Biol. 26(12), 4410-4420 (2006).
Changolkar LN, Singh G, Cui K et al. Genome-wide distribution of macroH2A1 histone variants in mouse liver chromatin. Mol. Cell Biol. 30(23), 5473-5483 (2010).
Gamble MJ, Frizzell KM, Yang C, Krishnakumar R, Kraus WI. The histone variant macroH2A1 marks repressed autosomal chromatin, but protects a subset of its target genes from silencing. Genes Dev. 24(1), 21-32 (2010). Together with [42], this article broke the dogma of macroH2A as a sole repressor.
Ouararhni K, Hadj-Slimane R, Ait-Si-Ali S et al. The histone variant mH2A1.1 interferes with transcription by down-regulating PARP-1 enzymatic activity. Genes Dev. 20(23), 3324-3336 (2006). Together with [41], this article broke the dogma of macroH2A as a sole repressor.
Azuara V, Perry P, Sauer S et al. Chromatin signatures of pluripotent cell lines. Nat. Cell Biol. 8(5), 532-538 (2006).
Bernstein BE, Mikkelsen TS, Xie X et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125(2), 315-326 (2006).
Heard E. Delving into the diversity of facultative heterochromatin: the epigenetics of the inactive X chromosome. Curr. Opin. Genet. Dev. 15(5), 482-489 (2005).
Silva J, Smith A. Capturing pluripotency. Cell 132(4), 532-536 (2008). Short review raising and discussing some of the most essential questions in embryonic stem cell biology.
Kustatscher G, Hothorn M, Pugieux C, Scheffzek K, Ladurner AG. Splicing regulates NAD metabolite binding to histone macroH2A. Nat. Struct. Mol. Biol. 12(7), 624-625 (2005).
Timinszky G, Till S, Hassa PO et al. A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat. Struct. Mol. Biol. 16(9), 923-929 (2009).
Bernstein E, Muratore-Schroeder TL, Diaz RL et al. A phosphorylated subpopulation of the histone variant macroH2A1 is excluded from the inactive X chromosome and enriched during mitosis. Proc. Natl Acad. Sci. USA 105(5), 1533-1538 (2008).
Abbott DW, Chadwick BP, Thambirajah AA, Ausio J. Beyond the Xi: macroH2A chromatin distribution and post-translational modification in an avian system. J. Biol. Chem. 280(16), 16437-16445 (2005).
Thambirajah AA, Li A, Ishibashi T, Ausio J. New developments in post-translational modifications and functions of histone H2A variants. Biochem. Cell Biol. 87(1), 7-17 (2009).
Muthurajan UM, McBryant SJ, Lu X, Hansen JC, Luger K. The linker region of macroH2A promotes self-association of nucleosomal arrays. J. Biol. Chem. 286(27), 23852-23864 (2011).
Kapoor A, Goldberg MS, Cumberland LK et al. The histone variant macroH2A suppresses melanoma progression through regulation of CDK8. Nature 468(7327), 1105-1109 (2010). Delivered the first proof that loss of macroH2A is involved in cancer progression.
Strizzi L, Hardy KM, Kirsammer GT, Gerami P, Hendrix MJ. Embryonic signaling in melanoma: potential for diagnosis and therapy. Lab. Invest. 91(6), 819-824 (2011).
Novikov L, Park JW, Chen H, Klerman H, Jalloh AS, Gamble MJ. QKI-mediated alternative splicing of the histone variant macroH2A1 regulates cancer cell proliferation. Mol. Cell Biol. 31(20), 4244-4255 (2011).
Sporn JC, Kustatscher G, Hothorn T et al. Histone macroH2A isoforms predict the risk of lung cancer recurrence. Oncogene 28(38), 3423-3428 (2009).