Epigenetic regulation of autosomal gene expression by sex chromosomes

Trends in Genetics

Volumn 27, Issue 4, 2011, Pages 132-140

  Wijchers, Patrick J ^a   Festenstein, Richard J ^b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b IMPERIAL COLLEGE SCHOOL OF MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOSOME; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEX CHROMOSOME; SEX DIFFERENCE; X CHROMOSOME; Y CHROMOSOME;

ANEUPLOIDY; ANIMALS; EPIGENESIS, GENETIC; HUMANS; SEX CHARACTERISTICS; SEX CHROMOSOMES; TRANSCRIPTION, GENETIC;

EID: 79953043998     PISSN: 01689525     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tig.2011.01.004     Document Type: Review

References (100)

1. Ellegren H., Parsch J. The evolution of sex-biased genes and sex-biased gene expression. Nat. Rev. Genet. 2007, 8:689-698.
2. Ober C., et al. Sex-specific genetic architecture of human disease. Nat. Rev. Genet. 2008, 9:911-922.
3. Isensee J., Ruiz Noppinger P. Sexually dimorphic gene expression in mammalian somatic tissue. Gend. Med. 2007, 4(Suppl. B):S75-95.
4. Rinn J.L., Snyder M. Sexual dimorphism in mammalian gene expression. Trends Genet. 2005, 21:298-305.
5. Blekhman R., et al. Sex-specific and lineage-specific alternative splicing in primates. Genome Res. 2010, 20:180-189.
6. Su W.L., et al. Exon and junction microarrays detect widespread mouse strain- and sex-bias expression differences. BMC Genomics 2008, 9:273.
7. Yang X., et al. Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res. 2006, 16:995-1004.
8. Wijchers P.J., et al. Sexual dimorphism in mammalian autosomal gene regulation is determined not only by Sry but by sex chromosome complement as well. Dev. Cell 2010, 19:477-484.
9. Wilhelm D., Koopman P. The makings of maleness: towards an integrated view of male sexual development. Nat. Rev. Genet. 2006, 7:620-631.
10. Jazin E., Cahill L. Sex differences in molecular neuroscience: from fruit flies to humans. Nat. Rev. Neurosci. 2010, 11:9-17.
11. Wilson C.A., Davies D.C. The control of sexual differentiation of the reproductive system and brain. Reproduction 2007, 133:331-359.
12. McCombe P.A., et al. Sexual dimorphism in autoimmune disease. Curr. Mol. Med. 2009, 9:1058-1079.
13. van Nas A., et al. Elucidating the role of gonadal hormones in sexually dimorphic gene coexpression networks. Endocrinology 2009, 150:1235-1249.
14. Burgoyne P.S. A Y-chromosomal effect on blastocyst cell number in mice. Development 1993, 117:341-345.
15. Burgoyne P.S., et al. The genetic basis of XX-XY differences present before gonadal sex differentiation in the mouse. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 1995, 350:253-260. discussion 260-251.
16. Thornhill A.R., Burgoyne P.S. A paternally imprinted X chromosome retards the development of the early mouse embryo. Development 1993, 118:171-174.
17. Bermejo-Alvarez P., et al. Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:3394-3399.
18. Kobayashi S., et al. Comparison of gene expression in male and female mouse blastocysts revealed imprinting of the X-linked gene, Rhox5/Pem, at preimplantation stages. Curr. Biol. 2006, 16:166-172.
19. Arnold A.P., Chen X. What does the " four core genotypes" mouse model tell us about sex differences in the brain and other tissues?. Front. Neuroendocrinol. 2009, 30:1-9.
20. Mahadevaiah S.K., et al. Tdy-negative XY,XXY and XYY female mice: breeding data and synaptonemal complex analysis. J. Reprod. Fertil. 1993, 97:151-160.
21. Gatewood J.D., et al. Sex chromosome complement and gonadal sex influence aggressive and parental behaviors in mice. J. Neurosci. 2006, 26:2335-2342.
22. Wagner C.K., et al. Neonatal mice possessing an Sry transgene show a masculinized pattern of progesterone receptor expression in the brain independent of sex chromosome status. Endocrinology 2004, 145:1046-1049.
23. Palaszynski K.M., et al. A yin-yang effect between sex chromosome complement and sex hormones on the immune response. Endocrinology 2005, 146:3280-3285.
24. Kaminsky Z., et al. Complex disease, gender and epigenetics. Ann. Med. 2006, 38:530-544.
25. McCarthy M.M., et al. The epigenetics of sex differences in the brain. J. Neurosci. 2009, 29:12815-12823.
26. Heard E., Disteche C.M. Dosage compensation in mammals: fine-tuning the expression of the X chromosome. Genes. Dev. 2006, 20:1848-1867.
27. Lyon M.F. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 1961, 190:372-373.
28. Davies W., et al. Xlr3b is a new imprinted candidate for X-linked parent-of-origin effects on cognitive function in mice. Nat. Genet. 2005, 37:625-629.
29. Raefski A.S., O'Neill M.J. Identification of a cluster of X-linked imprinted genes in mice. Nat. Genet. 2005, 37:620-624.
30. Zvetkova I., et al. Global hypomethylation of the genome in XX embryonic stem cells. Nat. Genet. 2005, 37:1274-1279.
31. Ooi S.K., et al. Dynamic instability of genomic methylation patterns in pluripotent stem cells. Epigenetics Chromatin 2010, 3:17.
32. Durcova-Hills G., et al. Analysis of sex differences in EGC imprinting. Dev. Biol. 2004, 268:105-110.
33. Durcova-Hills G., et al. Influence of sex chromosome constitution on the genomic imprinting of germ cells. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:11184-11188.
34. Maherali N., et al. Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell 2007, 1:55-70.
35. Festenstein R., et al. Locus control region function and heterochromatin-induced position effect variegation. Science 1996, 271:1123-1125.
36. Sekido R., Lovell-Badge R. Sex determination and SRY: down to a wink and a nudge?. Trends Genet. 2009, 25:19-29.
37. Lahr G., et al. Transcription of the Y chromosomal gene, Sry, in adult mouse brain. Brain Res. Mol. Brain Res. 1995, 33:179-182.
38. Mayer A., et al. Developmental profile of Sry transcripts in mouse brain. Neurogenetics 2000, 3:25-30.
39. Dewing P., et al. Direct regulation of adult brain function by the male-specific factor SRY. Curr. Biol. 2006, 16:415-420.
40. Wu J.B., et al. Regulation of monoamine oxidase A by the SRY gene on the Y chromosome. FASEB J. 2009, 23:4029-4038.
41. Oh H.J., et al. Sry associates with the heterochromatin protein 1 complex by interacting with a KRAB domain protein. Biol. Reprod. 2005, 72:407-415.
42. Peng H., et al. Epigenetic gene silencing by the SRY protein is mediated by a KRAB-O protein that recruits the KAP1 co-repressor machinery. J. Biol. Chem. 2009, 284:35670-35680.
43. De Vries G.J. Minireview: sex differences in adult and developing brains: compensation, compensation, compensation. Endocrinology 2004, 145:1063-1068.
44. Graves J.A. Sex chromosome specialization and degeneration in mammals. Cell 2006, 124:901-914.
45. Skaletsky H., et al. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 2003, 423:825-837.
46. Toure A., et al. Identification of novel Y chromosome encoded transcripts by testis transcriptome analysis of mice with deletions of the Y chromosome long arm. Genome Biol. 2005, 6:R102.
47. Cocquet J., et al. The multicopy gene Sly represses the sex chromosomes in the male mouse germline after meiosis. PLoS Biol. 2009, 7:e1000244.
48. Reynard L.N., et al. The multi-copy mouse gene Sycp3-like Y-linked (Sly) encodes an abundant spermatid protein that interacts with a histone acetyltransferase and an acrosomal protein. Biol. Reprod. 2009, 81:250-257.
49. Skuse D.H., et al. Evidence from Turner's syndrome of an imprinted X-linked locus affecting cognitive function. Nature 1997, 387:705-708.
50. Mak W., et al. Reactivation of the paternal X chromosome in early mouse embryos. Science 2004, 303:666-669.
51. Okamoto I., et al. Epigenetic dynamics of imprinted X inactivation during early mouse development. Science 2004, 303:644-649.
52. Eggan K., et al. X-chromosome inactivation in cloned mouse embryos. Science 2000, 290:1578-1581.
53. Carrel L., Willard H.F. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 2005, 434:400-404.
54. Johnston C.M., et al. Large-scale population study of human cell lines indicates that dosage compensation is virtually complete. PLoS Genet. 2008, 4:e9.
55. Nguyen D.K., Disteche C.M. Dosage compensation of the active X chromosome in mammals. Nat. Genet. 2006, 38:47-53.
56. Yang F., et al. Global survey of escape from X inactivation by RNA-sequencing in mouse. Genome Res. 2010, 20:614-622.
57. Xu J., et al. Sex differences in sex chromosome gene expression in mouse brain. Hum. Mol. Genet. 2002, 11:1409-1419.
58. Xu J., et al. Sex-specific expression of the X-linked histone demethylase gene Jarid1c in brain. PLoS ONE 2008, 3:e2553.
59. Xu J., et al. Sex-specific differences in expression of histone demethylases Utx and Uty in mouse brain and neurons. J. Neurosci. 2008, 28:4521-4527.
60. Ditton H.J., et al. The AZFa gene DBY (DDX3Y) is widely transcribed but the protein is limited to the male germ cells by translation control. Hum. Mol. Genet. 2004, 13:2333-2341.
61. Hong S., et al. Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:18439-18444.
62. Lan F., et al. A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 2007, 449:689-694.
63. Christensen J., et al. RBP2 belongs to a family of demethylases, specific for tri-and dimethylated lysine 4 on histone 3. Cell 2007, 128:1063-1076.
64. Iwase S., et al. The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 2007, 128:1077-1088.
65. Buggy J.J., et al. Cloning and characterization of a novel human histone deacetylase, HDAC8. Biochem J. 2000, 350(Pt 1):199-205.
66. Hu E., et al. Cloning and characterization of a novel human class I histone deacetylase that functions as a transcription repressor. J. Biol. Chem. 2000, 275:15254-15264.
67. Van den Wyngaert I., et al. Cloning and characterization of human histone deacetylase 8. FEBS Lett. 2000, 478:77-83.
68. Smith E.R., et al. A human protein complex homologous to the Drosophila MSL complex is responsible for the majority of histone H4 acetylation at lysine 16. Mol. Cell. Biol. 2005, 25:9175-9188.
69. Cai Y., et al. Identification of new subunits of the multiprotein mammalian TRRAP/TIP60-containing histone acetyltransferase complex. J. Biol. Chem. 2003, 278:42733-42736.
70. Weiler K.S., Wakimoto B.T. Heterochromatin and gene expression in Drosophila. Annu. Rev. Genet. 1995, 29:577-605.
71. Eissenberg J.C., et al. Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:9923-9927.
72. Eissenberg J.C., et al. The heterochromatin-associated protein HP-1 is an essential protein in Drosophila with dosage-dependent effects on position-effect variegation. Genetics 1992, 131:345-352.
73. Festenstein R., et al. Heterochromatin protein 1 modifies mammalian PEV in a dose- and chromosomal-context-dependent manner. Nat. Genet. 1999, 23:457-461.
74. Gowen J.W.A.E.H.G. Chromosome constitution and behavior in eversporting and mottling in Drosophila melanogaster. Genetics 1934, 19:189-208.
75. Lemos B., et al. Epigenetic effects of polymorphic Y chromosomes modulate chromatin components, immune response, and sexual conflict. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:15826-15831.
76. Dimitri P., Pisano C. Position effect variegation in Drosophila melanogaster: relationship between suppression effect and the amount of Y chromosome. Genetics 1989, 122:793-800.
77. Lemos B., et al. Polymorphic Y chromosomes harbor cryptic variation with manifold functional consequences. Science 2008, 319:91-93.
78. Heard E. Delving into the diversity of facultative heterochromatin: the epigenetics of the inactive X chromosome. Curr. Opin. Genet. Dev. 2005, 15:482-489.
79. Barrionuevo F., et al. Homozygous inactivation of Sox9 causes complete XY sex reversal in mice. Biol. Reprod. 2006, 74:195-201.
80. Chaboissier M.C., et al. Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development 2004, 131:1891-1901.
81. Lee J.T., Jaenisch R. Long-range cis effects of ectopic X-inactivation centres on a mouse autosome. Nature 1997, 386:275-279.
82. Gregg C., et al. High-resolution analysis of parent-of-origin allelic expression in the mouse brain. Science 2010, 329:643-648.
83. Gregg C., et al. Sex-specific parent-of-origin allelic expression in the mouse brain. Science 2010, 329:682-685.
84. Muller H.J. Types of visible variations induced by X-rays in Drosophila. J. Genet. 1930, 22:299-334.
85. Allshire R.C., et al. Position effect variegation at fission yeast centromeres. Cell 1994, 76:157-169.
86. Festenstein R., Kioussis D. Locus control regions and epigenetic chromatin modifiers. Curr. Opin. Genet. Dev. 2000, 10:199-203.
87. de Krom M., et al. Stochastic patterns in globin gene expression are established prior to transcriptional activation and are clonally inherited. Mol. Cell. 2002, 9:1319-1326.
88. Sybert V.P., McCauley E. Turner's syndrome. N. Engl. J. Med. 2004, 351:1227-1238.
89. Ross J.L., et al. The Turner syndrome-associated neurocognitive phenotype maps to distal Xp. Am. J. Hum. Genet. 2000, 67:672-681.
90. Lanfranco F., et al. Klinefelter's syndrome. Lancet 2004, 364:273-283.
91. Visootsak J., Graham J.M. Klinefelter syndrome and other sex chromosomal aneuploidies. Orphanet J. Rare Dis. 2006, 1:42.
92. Tuttelmann F., Gromoll J. Novel genetic aspects of Klinefelter's syndrome. Mol. Hum. Reprod. 2010, 16:386-395.
93. Lue Y., et al. XXY male mice: an experimental model for Klinefelter syndrome. Endocrinology 2001, 142:1461-1470.
94. Arps S., et al. Isochromosome Xq in Klinefelter syndrome: report of 7 new cases. Am. J. Med. Genet. 1996, 64:580-582.
95. Hockner M., et al. Unravelling the parental origin and mechanism of formation of the 47,XY,i(X)(q10) Klinefelter karyotype variant. Fertil. Steril. 2008, 90:2009. e2013-2007.
96. De Vries G.J., et al. A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. J. Neurosci. 2002, 22:9005-9014.
97. Burgoyne P.S., et al. The Y* rearrangement in mice: new insights into a perplexing PAR. Cytogenet. Cell Genet. 1998, 80:37-40.
98. Eicher E.M., et al. The mouse Y* chromosome involves a complex rearrangement, including interstitial positioning of the pseudoautosomal region. Cytogenet. Cell Genet. 1991, 57:221-230.
99. Burgoyne P.S., Evans E.P. A high frequency of XO offspring from X(Paf)Y* male mice: evidence that the Paf mutation involves an inversion spanning the X PAR boundary. Cytogenet. Cell Genet. 2000, 91:57-61.
100. Evans E.P., Phillips R.J. Inversion heterozygosity and the origin of XO daughters of Bpa/+female mice. Nature 1975, 256:40-41.