Escape from X inactivation in mice and humans

Genome Biology

Volumn 11, Issue 6, 2010, Pages

  Berletch, Joel B ^a   Yang, Fan ^a   Disteche, Christine M ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; EPIGENETICS; GENE DOSAGE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE REPRESSION; GENE SILENCING; GENOME IMPRINTING; HUMAN; NONHUMAN; REVIEW; SEX DIFFERENCE; SPECIES DIFFERENCE; X CHROMOSOME INACTIVATION; ANIMAL; GENERAL ASPECTS OF DISEASE; GENETICS; MEIOSIS; MOUSE; SEX CHROMOSOME;

MAMMALIA; MUS;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DISEASE; GENOMIC IMPRINTING; HUMANS; MEIOSIS; MICE; SEX CHROMOSOMES; X CHROMOSOME INACTIVATION;

EID: 77958197135     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2010-11-6-213     Document Type: Review

References (58)

1. Nguyen DK, Disteche CM. Dosage compensation of the active X chromosome in mammals. Nat Genet 2006, 38:47-53. 10.1038/ng1705, 16341221.
2. Gupta V, Parisi M, Sturgill D, Nuttall R, Doctolero M, Dudko OK, Malley JD, Eastman PS, Oliver B. Global analysis of X-chromosome dosage compensation. J Biol 2006, 5:3. 10.1186/jbiol30, 1414069, 16507155.
3. Lyon MF. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 1961, 190:372-373. 10.1038/190372a0, 13764598.
4. Birchler JA, Fernandez HR, Kavi HH. Commonalities in compensation. BioEssays 2006, 28:565-568. 10.1002/bies.20408, 16700062.
5. Lahn BT, Page DC. Four evolutionary strata on the human X chromosome. Science 1999, 286:964-967. 10.1126/science.286.5441.964, 10542153.
6. Ross MT, Grafham DV, Coffey AJ, Scherer S, McLay K, Muzny D, Platzer M, Howell GR, Burrows C, Bird CP, Frankish A, Lovell FL, Howe KL, Ashurst JL, Fulton RS, Sudbrak R, Wen G, Jones MC, Hurles ME, Andrews TD, Scott CE, Searle S, Ramser J, Whittaker A, Deadman R, Carter NP, Hunt SE, Chen R, Cree A, Gunaratne P, et al. The DNA sequence of the human X chromosome. Nature 2005, 434:325-337. 10.1038/nature03440, 2665286, 15772651.
7. Heard E, Disteche CM. Dosage compensation in mammals: fine-tuning the expression of the X chromosome. Genes Dev 2006, 20:1848-1867. 10.1101/gad.1422906, 16847345.
8. Brown CJ, Ballabio A, Rupert JL, Lafreniere RG, Grompe M, Tonlorenzi R, Willard HF. A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 1991, 349:38-44. 10.1038/349038a0, 1985261.
9. Zhao J, Sun BK, Erwin JA, Song JJ, Lee JT. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 2008, 322:750-756. 10.1126/science.1163045, 2748911, 18974356.
10. Brockdorff N, Ashworth A, Kay GF, McCabe VM, Norris DP, Cooper PJ, Swift S, Rastan S. The product of the mouse Xist gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus. Cell 1992, 71:515-526. 10.1016/0092-8674(92)90519-I, 1423610.
11. Brown CJ, Hendrich BD, Rupert JL, Lafreniere RG, Xing Y, Lawrence J, Willard HF. The human XIST gene: analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell 1992, 71:527-542. 10.1016/0092-8674(92)90520-M, 1423611.
12. Carrel L, Willard HF. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 2005, 434:400-404. 10.1038/nature03479, 15772666.
13. Yang F, Babak T, Shendure J, Disteche CM. Global survey of escape from X inactivation by RNA-sequencing in mouse. Genome Res 2010, 20:614-622. 10.1101/gr.103200.109, 20363980.
14. Song R, Ro S, Michaels JD, Park C, McCarrey JR, Yan W. Many X-linked microRNAs escape meiotic sex chromosome inactivation. Nat Genet 2009, 41:488-493. 10.1038/ng.338, 2723799, 19305411.
15. Prothero KE, Stahl JM, Carrel L. Dosage compensation and gene expression on the mammalian X chromosome: one plus one does not always equal two. Chromosome Res 2009, 17:637-648. 10.1007/s10577-009-9063-9, 19802704.
16. Deakin JE, Chaumeil J, Hore TA, Marshall Graves JA. Unravelling the evolutionary origins of X chromosome inactivation in mammals: insights from marsupials and monotremes. Chromosome Res 2009, 17:671-685. 10.1007/s10577-009-9058-6, 19802707.
17. Duret L, Chureau C, Samain S, Weissenbach J, Avner P. The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science 2006, 312:1653-1655. 10.1126/science.1126316, 16778056.
18. Disteche CM. Escapees on the X chromosome. Proc Natl Acad Sci USA 1999, 96:14180-14182. 10.1073/pnas.96.25.14180, 33938, 10588671.
19. Tsuchiya KD, Greally JM, Yi Y, Noel KP, Truong JP, Disteche CM. Comparative sequence and x-inactivation analyses of a domain of escape in human Xp11.2 and the conserved segment in mouse. Genome Res 2004, 14:1275-1284. 10.1101/gr.2575904, 442142, 15197169.
20. Sudbrak R, Wieczorek G, Nuber UA, Mann W, Kirchner R, Erdogan F, Brown CJ, Wöhrle D, Sterk P, Kalscheuer VM, Berger W, Lehrach H, Ropers HH. X chromosome-specific cDNA arrays: identification of genes that escape from X-inactivation and other applications. Hum Mol Genet 2001, 10:77-83. 10.1093/hmg/10.1.77, 11136717.
21. Yang X, Schadt EE, Wang S, Wang H, Arnold AP, Ingram-Drake L, Drake TA, Lusis AJ. Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res 2006, 16:995-1004. 10.1101/gr.5217506, 1524872, 16825664.
22. Johnston CM, Lovell FL, Leongamornlert DA, Stranger BE, Dermitzakis ET, Ross MT. Large-scale population study of human cell lines indicates that dosage compensation is virtually complete. PLoS Genet 2008, 4:e9. 10.1371/journal.pgen.0040009, 2213701,2213701, 18208332.
23. Bondy CA. Turner syndrome 2008. Horm Res 2009, 71(Suppl 1):52-56. 10.1159/000178039, 19153507.
24. Hook EB, Warburton D. The distribution of chromosomal genotypes associated with Turner's syndrome: livebirth prevalence rates and evidence for diminished fetal mortality and severity in genotypes associated with structural X abnormalities or mosaicism. Hum Genet 1983, 64:24-27. 10.1007/BF00289473, 6683706.
25. Zinn AR, Ross JL. Molecular analysis of genes on Xp controlling Turner syndrome and premature ovarian failure (POF). Semin Reprod Med 2001, 19:141-146. 10.1055/s-2001-15394, 11480911.
26. Clement-Jones M, Schiller S, Rao E, Blaschke RJ, Zuniga A, Zeller R, Robson SC, Binder G, Glass I, Strachan T, Lindsay S, Rappold GA. The short stature homeobox gene SHOX is involved in skeletal abnormalities in Turner syndrome. Hum Mol Genet 2000, 9:695-702. 10.1093/hmg/9.5.695, 10749976.
27. Urbach A, Benvenisty N. Studying early lethality of 45,XO (Turner's syndrome) embryos using human embryonic stem cells. PLoS One 2009, 4:e4175. 10.1371/journal.pone.0004175, 2613558, 19137066.
28. Burgoyne PS, Baker TG. Perinatal oocyte loss in XO mice and its implications for the aetiology of gonadal dysgenesis in XO women. J Reprod Fertil 1985, 75:633-645.
29. Speed RM. Oocyte development in XO foetuses of man and mouse: the possible role of heterologous X-chromosome pairing in germ cell survival. Chromosoma 1986, 94:115-124. 10.1007/BF00286989, 3757617.
30. Keitges E, Rivest M, Siniscalco M, Gartler SM. X-linkage of steroid sulphatase in the mouse is evidence for a functional Y-linked allele. Nature 1985, 315:226-227. 10.1038/315226a0, 3858674.
31. Perry J, Palmer S, Gabriel A, Ashworth A. A short pseudoautosomal region in laboratory mice. Genome Res 2001, 11:1826-1832. 311143, 11691846.
32. Wareham KA, Lyon MF, Glenister PH, Williams ED. Age related reactivation of an X-linked gene. Nature 1987, 327:725-727. 10.1038/327725a0, 3600770.
33. Schoeftner S, Blanco R, de Silanes IL, Munoz P, Gomez-Lopez G, Flores JM, Blasco MA. Telomere shortening relaxes X chromosome inactivation and forces global transcriptome alterations. Proc Natl Acad Sci USA 2009, 106:19393-19398. 10.1073/pnas.0909265106, 2772818, 19887628.
34. Lyon MF. X-chromosome inactivation: a repeat hypothesis. Cytogenet Cell Genet 1998, 80:133-137. 10.1159/000014969, 9678347.
35. Bailey JA, Carrel L, Chakravarti A, Eichler EE. Molecular evidence for a relationship between LINE-1 elements and X chromosome inactivation: the Lyon repeat hypothesis. Proc Natl Acad Sci USA 2000, 97:6634-6639. 10.1073/pnas.97.12.6634, 18684, 10841562.
36. Carrel L, Park C, Tyekucheva S, Dunn J, Chiaromonte F, Makova KD. Genomic environment predicts expression patterns on the human inactive X chromosome. PLoS Genet 2006, 2:e151. 10.1371/journal.pgen.0020151, 1584270, 17009873.
37. Wang Z, Willard HF, Mukherjee S, Furey TS. Evidence of influence of genomic DNA sequence on human X chromosome inactivation. PLoS Comput Biol 2006, 2:e113. 10.1371/journal.pcbi.0020113, 1557588,1557588, 16948528.
38. Murakami K, Ohhira T, Oshiro E, Qi D, Oshimura M, Kugoh H. Identification of the chromatin regions coated by non-coding Xist RNA. Cytogenet Genome Res 2009, 125:19-25. 10.1159/000207514, 19617692.
39. Changolkar LN, Pehrson JR. macroH2A1 histone variants are depleted on active genes but concentrated on the inactive X chromosome. Mol Cell Biol 2006, 26:4410-4420. 10.1128/MCB.02258-05, 1489112, 16738309.
40. Marks H, Chow JC, Denissov S, Francoijs KJ, Brockdorff N, Heard E, Stunnenberg HG. High-resolution analysis of epigenetic changes associated with X inactivation. Genome Res 2009, 19:1361-1373. 10.1101/gr.092643.109, 2720191, 19581487.
41. Goto Y, Kimura H. Inactive X chromosome-specific histone H3 modifications and CpG hypomethylation flank a chromatin boundary between an X-inactivated and an escape gene. Nucleic Acids Res 2009, 37:7416-7428. 10.1093/nar/gkp860, 2794193, 19843608.
42. Khalil AM, Driscoll DJ. Trimethylation of histone H3 lysine 4 is an epigenetic mark at regions escaping mammalian X inactivation. Epigenetics 2007, 2:114-118. 10.4161/epi.2.2.4612, 17965609.
43. Filippova GN, Cheng MK, Moore JM, Truong JP, Hu YJ, Nguyen DK, Tsuchiya KD, Disteche CM. Boundaries between chromosomal domains of X inactivation and escape bind CTCF and lack CpG methylation during early development. Dev Cell 2005, 8:31-42. 10.1016/j.devcel.2004.10.018, 15669143.
44. Ciavatta D, Kalantry S, Magnuson T, Smithies O. A DNA insulator prevents repression of a targeted X-linked transgene but not its random or imprinted X inactivation. Proc Natl Acad Sci USA 2006, 103:9958-9963. 10.1073/pnas.0603754103, 1479543, 16777957.
45. Li N, Carrel L. Escape from X chromosome inactivation is an intrinsic property of the Jarid1c locus. Proc Natl Acad Sci USA 2008, 105:17055-17060. 10.1073/pnas.0807765105, 2579377, 18971342.
46. Heard E, Bickmore W. The ins and outs of gene regulation and chromosome territory organisation. Curr Opin Cell Biol 2007, 19:311-316. 10.1016/j.ceb.2007.04.016, 17467967.
47. Brown CJ, Greally JM. A stain upon the silence: genes escaping X inactivation. Trends Genet 2003, 19:432-438. 10.1016/S0168-9525(03)00177-X, 12902161.
48. Rougeulle C, Navarro P, Avner P. Promoter-restricted H3 Lys 4 di-methylation is an epigenetic mark for monoallelic expression. Hum Mol Genet 2003, 12:3343-3348. 10.1093/hmg/ddg351, 14570711.
49. Lingenfelter PA, Adler DA, Poslinski D, Thomas S, Elliott RW, Chapman VM, Disteche CM. Escape from X inactivation of Smcx is preceded by silencing during mouse development. Nat Genet 1998, 18:212-213. 10.1038/ng0398-212, 9500539.
50. Hong S, Cho YW, Yu LR, Yu H, Veenstra TD, Ge K. Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc Natl Acad Sci USA 2007, 104:18439-18444. 10.1073/pnas.0707292104, 2141795, 18003914.
51. Agger K, Cloos PA, Christensen J, Pasini D, Rose S, Rappsilber J, Issaeva I, Canaani E, Salcini AE, Helin K. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 2007, 449:731-734. 10.1038/nature06145, 17713478.
52. Lan F, Bayliss PE, Rinn JL, Whetstine JR, Wang JK, Chen S, Iwase S, Alpatov R, Issaeva I, Canaani E, Roberts TM, Chang HY, Shi Y. A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 2007, 449:689-694. 10.1038/nature06192, 17851529.
53. Patrat C, Okamoto I, Diabangouaya P, Vialon V, Le Baccon P, Chow J, Heard E. Dynamic changes in paternal X-chromosome activity during imprinted X-chromosome inactivation in mice. Proc Natl Acad Sci USA 2009, 106:5198-5203. 10.1073/pnas.0810683106, 2653561, 19273861.
54. Kalantry S, Purushothaman S, Bowen RB, Starmer J, Magnuson T. Evidence of Xist RNA-independent initiation of mouse imprinted X-chromosome inactivation. Nature 2009, 460:647-651. 2754729, 19571810.
55. Turner JM. Meiotic sex chromosome inactivation. Development 2007, 134:1823-1831. 10.1242/dev.000018, 17329371.
56. Namekawa SH, Park PJ, Zhang LF, Shima JE, McCarrey JR, Griswold MD, Lee JT. Postmeiotic sex chromatin in the male germline of mice. Curr Biol 2006, 16:660-667. 10.1016/j.cub.2006.01.066, 16581510.
57. Huynh KD, Lee JT. Inheritance of a pre-inactivated paternal X chromosome in early mouse embryos. Nature 2003, 426:857-862. 10.1038/nature02222, 14661031.
58. Mueller JL, Mahadevaiah SK, Park PJ, Warburton PE, Page DC, Turner JM. The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression. Nat Genet 2008, 40:794-799. 10.1038/ng.126, 2740655, 18454149.