Histone H3 lysine 4 dimethylation is enriched on the inactive sex chromosomes in male meiosis but absent on the inactive X in female somatic cells (original) (raw)
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Research Articles| November 03 2005
aDivision of Pediatrics Genetics and Center for Mammalian Genetics;
bDepartment of Molecular Genetics and Microbiology, and the Genetics Institute, University of Florida College of Medicine, Gainesville, FL (USA)
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aDivision of Pediatrics Genetics and Center for Mammalian Genetics;
bDepartment of Molecular Genetics and Microbiology, and the Genetics Institute, University of Florida College of Medicine, Gainesville, FL (USA)
Search for other works by this author on:
Cytogenet Genome Res (2006) 112 (1-2): 11–15.
Abstract
Inactivation of the X chromosome occurs in female somatic cells and in male meiosis. In both cases, the inactive X chromosome undergoes changes in histone modifications including deacetylation of core histone proteins and enrichment with histone H3 lysine 9 (H3-K9) dimethylation. In this study we show that while the inactive X in female somatic cells is largely devoid of H3-K4 dimethylation, the inactive X in male meiosis is enriched with this modification. However, the inactive X chromosome in female somatic cells and the inactive X and Y in male meiosis are devoid of H3-K4 trimethylation. Further, trimethylation of H3-K4 is present at discrete regions along most of the autosomes, while H3-K4 dimethylation shows a more homogenous staining. Also, the Y chromosome is largely devoid of H3-K4 di- and trimethylation in somatic cells of both humans and mice, however, the Y chromosome is enriched with H3-K4 di- but not trimethylation throughout spermatogenesis. Our results provide insights into the differences between female somatic cells and male germ cells in inactivating the X chromosome, and suggest that trimethylation, and not dimethylation, of H3-K4 is a more robust indicator of the active regions of the genome.
References
Avner P, Heard E: X-chromosome inactivation: counting choice and initiation. Nat Rev Genet 2:59–67 (2001).
Bannister AJ, Schneider R, Kouzarides T: Histone methylation: dynamic or static? Cell 109:801–806 (2002).
Boggs BA, Cheung P, Heard E, Spector DL, Chinault AC, Allis CD: Differentially methylated forms of histone H3 show unique association patterns with inactive human X chromosomes. Nat Genet 30:73–76 (2002).
Chaumeil J, Okamoto I, Heard E: X-chromosome inactivation in mouse embryonic stem cells: analysis of histone modifications and transcriptional activity using immunofluorescence and FISH. Meth Enzymol 376:405–419 (2004).
Cheng MK, Disteche CM: Silence of the fathers: early X inactivation Bioessays 26:821–824 (2004).
Gartler SM, Goldman MA: Biology of the X chromosome. Curr Opin Pediatr 13:340–345 (2001).
Hawley RS: The human Y chromosome: rumors of its death have been greatly exaggerated. Cell 113:825–828 (2003).
Heard E: Recent advances in X-chromosome inactivation. Curr Opin Cell Biol 16:247–255 (2004).
Heard E, Rougeulle C, Arnaud D, Avner P, Allis CD, Spector DL: Methylation of histone H3 at Lys-9 is an early mark on the X chromosome during X inactivation. Cell 107:727–738 (2001).
Jenuwein T, Allis CD: Translating the histone code. Science 293:1074–1080 (2001).
Jeppesen P, Turner BM: The inactive X chromosome in female mammals is distinguished by a lack of histone H4 acetylation a cytogenetic marker for gene expression. Cell 74:281–289 (1993).
Khalil AM, Boyar FZ, Driscoll DJ: Dynamic histone modifications mark sex chromosome inactivation
and reactivation during mammalian spermatogenesis. Proc Natl Acad Sci USA 101:16583–16587 (2004).
Kouzarides T: Histone methylation in transcriptional control. Curr Opin Genet Dev 12:198–209 (2002).
Litt MD, Simpson M, Gaszner M, Allis CD, Felsenfeld G: Correlation between histone lysine methylation and developmental changes at the chicken beta-globin locus. Science 293:2453–2455 (2001).
Lyon MF: Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190:372–373 (1961).
Marahrens Y, Panning B, Dausman J, Strauss W, Jaenisch R: _Xist_-deficient mice are defective in dosage compensation but not spermatogenesis. Genes Dev 11:156–166 (1997).
McCarrey JR, Dilworth DD: Expression of Xist in mouse germ cells correlates with X-chromosome inactivation. Nat Genet 2:200–203 (1992).
McCarrey JR, Watson C, Atencio J, Ostermeier GC, Marahrens Y, Jaenisch R, Krawetz SA: X-chromosome inactivation during spermatogenesis is regulated by an _Xist/Tsix_-independent mechanism in the mouse. Genesis 34:257–266 (2002).
Mermoud JE, Popova B, Peters AH, Jenuwein T, Brockdorff N: Histone H3 lysine 9 methylation occurs rapidly at the onset of random X chromosome inactivation. Curr Biol 12:247–251 (2002).
Migeon BR: X chromosome inactivation: theme and variations. Cytogenet Genome Res 99:8–16 (2002).
Okamoto I, Otte AP, Allis CD, Reinberg D, Heard E: Epigenetic dynamics of imprinted X inactivation during early mouse development. Science 303:644–649 (2004).
Peters AH, Mermoud JE, O’Carroll D, Pagani M, Schweizer D, Brockdorff N, Jenuwein T: Histone
H3 lysine 9 methylation is an epigenetic imprint of facultative heterochromatin. Nat Genet 30:77–80 (2002).
Plath K, Mlynarczyk-Evans S, Nusinow DA, Panning B: Xist RNA and the mechanism of X chromosome inactivation. Annu Rev Genet 36:233–278 (2002).
Rougeulle C, Navarro P, Avner P: Promoter-restricted H3 Lys 4 di-methylation is an epigenetic mark for monoallelic expression. Hum Mol Genet 12:3343–3348 (2003).
Salido EC, Yen PH, Mohandas TK, Shapiro LJ: Expression of the X-inactivation-associated gene XIST during spermatogenesis. Nat Genet 2:196–199 (1992).
Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, Emre NC, Schreiber SL, Mellor J, Kouzarides T: Active genes are tri-methylated at K4 of histone H3. Nature 419:407–411 (2002).
Schneider R, Bannister AJ, Myers FA, Thorne AW, Crane-Robinson C, Kouzarides T: Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat Cell Biol 6:73–77 (2004).
Strahl BD, Allis CD: The language of covalent histone modifications. Nature 403:41–45 (2000).
Turner BM: Histone acetylation and an epigenetic code. Bioessays 22:836–845 (2000).
Turner BM: Cellular memory and the histone code. Cell 111:285–291 (2002).
Turner JM, Mahadevaiah SK, Elliott DJ, Garchon HJ, Pehrson JR, Jaenisch R, Burgoyne PS: Meiotic sex chromosome inactivation in male mice with targeted disruptions of Xist. J Cell Sci 115:4097–4105 (2002).
Zhang Y, Reinberg D: Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev 15:2343–2360 (2001).
© 2006 S. Karger AG, Basel
2005
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