X-chromosome inactivation: Counting, choice and initiation

Nature Reviews Genetics

Volumn 2, Issue 1, 2001, Pages 59-67

  Avner, Philip ^a   Heard, Edith ^a,b  

^a U Genet Molec Murine Inst P   (France)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIA;

RNA; TRANSCRIPTION FACTOR; UNTRANSLATED RNA; X (INACTIVE) SPECIFIC TRANSCRIPT (XIST); X (INACTIVE)-SPECIFIC TRANSCRIPT (XIST);

ANIMAL; CHROMOSOME MAP; DROSOPHILA MELANOGASTER; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; REVIEW; X CHROMOSOME;

ANIMALS; CHROMOSOME MAPPING; DOSAGE COMPENSATION, GENETIC; DROSOPHILA MELANOGASTER; FEMALE; MALE; RNA; RNA, UNTRANSLATED; TRANSCRIPTION FACTORS; X CHROMOSOME;

EID: 0035228079     PISSN: 14710056     EISSN: None     Source Type: Journal    
DOI: 10.1038/35047580     Document Type: Review

References (71)

1. Heard, E., Clerc, P. & Avner, P. X-chromosome inactivation in mammals. Annu. Rev. Genet. 31, 571-610 (1997).
2. Courtier, B., Heard, E. & Avner, P. Xce haplotypes show modified methylation in a region of the active X chromosome lying 3′ to Xist. Proc. Natl Acad. Sci USA 92, 3531-3535 (1995).
3. Lee, J. T., Davidow, L. S. & Warshawsky, D. TsiX, a gene antisense to Xist at the X-inactivation centre. Nature Genet. 21, 400-404 (1999).
4. Keohane, A. M., O'Neill, L. P., Belyaev, N. D., Lavender, J. S. & Turner, B. M. X-inactivation and H4 acetylation in embryonic stem cells. Dev. Biol. 180, 618-630 (1996).
5. Mermoud, J. E., Costanzi, C., Pehrson, J. R. & Brockdorff, N. Histone MacroH2A relocates to the inactive X chromosome after initiation and propagation of X-inactivation. J. Cell Biol. 147, 1399-1408 (1999).
6. Sado, T. et al. X inactivation in the mouse embryo deficient for Dnmt1: distinct effect of hypomethylation on imprinted and randon X inactivation. Dev. Biol. 225, 294-303 (2000).
7. Lyon, M. F. Some milestones in the history of X-chromosome inactivation. Annu. Rev. Genet 26, 15-27 (1992).
8. Panning, B., Dausman, J. & Jaenisch, R. X chromosome inactivation is mediated by Xist RNA stabilisation. Cell 90, 907-916 (1997).
9. Sheardown, S. A. et al. Stabilisation of Xist RNA mediates initiation of X chromosome inactivation. Cell 91, 99-107 (1997).
10. Johnston, C. M. et al. Developmentally regulated Xist promoter switch mediates initiation of X inactivation. Cell 94, 809-817 (1998).
11. Warshawsky, D., Stavropoulos, N. & Lee, J. T. Further examination of the Xist promoter-switch hypothesis in X inactivation: evidence against the existence and function of a PO promoter. Proc. Natl Acad. Sci. USA 96, 14424-14429 (1999).
12. Romer, J. T. & Ashworth, A. The upstream region of the mouse xist gene contains two ribosomal protein pseudogenes. Mamm. Genome. 11, 461-463 (2000).
13. O'Neill, L. P. et al. A developmental switch in H4 acetylation upstream of Xist plays a role in X chromosome inactivation. EMBO J. 18, 2897-2907 (1999).
14. Wutz, A. & Jaenisch, R. A shift from reversible to irreversible X inactivation is triggered during ES cell differentiation. Mol. Cell 5, 695-705 (2000).
15. Heard, E. et al. Human XIST yeast artificial chromosome transgenes show partial X inactivation center function in mouse embryonic stem cells. Proc. Natl Acad. Sci. USA 96, 6841-6846 (1999).
16. Penny, G. D., Kay, G. F., Sheardown, S. A., Rastan, S. & Brockdorff, N. Requirement for Xist in X chromosome inactivation. Nature 379, 131-137 (1996).
17. 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).
18. Heard, E. et al. Transgenic mice carrying an Xist-containing YAC. Hum. Mol. Genet. 5, 441-450 (1996).
19. Matsuura, S., Episkopou, V., Hamvas, R. & Brown, S. D. M. Xist expression from an Xist transgene carried on the mouse Y chromosome. Hum. Mol. Genet. 5, 451-459 (1996)
20. Lee, J. T., Strauss, W. M., Dausman, J. A. & Jaenisch, R. A 450 kb transgene displays properties of the mammalian X-inactivation center. Cell 86, 83-94 (1996).
21. Heard, E., Mongelard, F., Arnaud, D. & Avner, P. Xist Yeast artificial chromosome transgenes functions as X-inactivation centers only in multicopy arrays and not as single copies. Mol. Cell. Biol. 19, 3156-3166 (1999). A transgenic analysis suggesting that additional, as-yet-undefined functions, other than those covered by the Xist gene and its immediate flanking regions, are necessary for counting and choice to occur.
22. Stuckenholz, C. Kageyama, Y. & Kuroda, M. I. Guilt by association: non-coding RNAs, chromosome-specific proteins and dosage compensation in Drosophila. Trends Genet. 15, 454-458 (1999).
23. Akhtar, A., Zink, D. & Becker, P. B. A chromodomain-RNA interaction targets MOF to the Drosophila X chromosome. Nature 407, 405-409 (2000). Interesting data on the role of non-coding RNAs in anchoring members of the dosage compensation complex in Drosophila (including the MOF protein, which has acetyltransferase activity) to the male X chromosome.
24. Gilbert, S. L., Pehrson, J. R. & Sharp, P. A. XIST RNA associates with specific regions of the inactive X chromatin. J. Biol. Chem. 275, 36491-36494 (2000).
25. Jeppesen, P. & Turner, B. M. 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).
26. Boggs, B. A., Connors, B., Sobel, R. E. Chinault, A. C. & Allis, C. D. Reduced levels of histone H3 acetylation on the inactive X chromosome in human females. Chromosoma 105, 303-309 (1996).
27. Gilbert, S. L. & Sharp, P. A Promoter-specific hypoacetylation of X-inactivated genes. Proc. Natl Acad. Sci USA 96, 13825-13830 (1999).
28. Costanzi, C. & Pehrson, J. R. Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 393, 599-601 (1998).
29. Rasmussen, T. P. et al. Dynamic relocalization of histone macroH2A1 from centrosomes to inactive X chromosomes during X inactivation. J. Cell Biol. 150, 1189-1198 (2000).
30. Perche, P.-Y. Concentrations of histone MacroH2A in the Barr body are correlated with higher nucleosome density. Curr. Biol. 10, 1581-1534 (2000).
31. Csankovski, G., Panning, B., Bates, B., Pehrson, J. R. & Jaenisch, R. Deletion of Xist disrupts histone macroH2A localization but not maintenance of X inactivation. Nature Genet. 22, 323-324 (1999). Shows that Xist RNA coating is necessary for macroH2A accumulation on the inactive X in somatic cells, but neither Xist RNA nor macroH2A are necessary for the maintenance of the inactive state.
32. Costanzi, C., Stein, P., Worrad, D. M., Schultz, R. M. & Pehrson, J. R. Histone macroH2A is concentrated in the inactive X chromosome of female preimplantation mouse embryos. Development 127, 2283-2289 (2000). This paper describes the unexpectedly early association of macroH2A with the X chromosome during imprinted X inactivation, which contrasts with its much later association during random X inactivation.
33. Clerc, P. & Avner, P. Role of the region 3′ to Xist exon 6 in the counting process of X chromosome inactivation. Nature Genet. 19, 249-253 (1998). Provides the first molecular evidence for counting element(s) that are localized in a region lying 3′ to the mouse Xist gene.
34. Debrand, E., Chureau, E. Arnaud, D., Avner, P. & Heard, E. Functional analysis of the DXPas34 locus: A 3′ regulator of Xist expression. Mol. Cell. Biol. 19, 8513-8525 (1999).
35. Lu, N. & Lee, J. T. Targeted mutagenesis of Tsix leads to nonrandom X inactivation. Cell 99, 47-57 (1999).
36. Gribnau, J., Diderich, K., Pruzina, S., Calzolari, R. & Fraser, P. Intergenic transcription and developmental remodeling of chromatin subdomains in the human β-globin locus. Mol. Cell 5, 377-386 (2000).
37. Travers, A. Chromatin modification by DNA tracking. Proc. Natl Acad. Sci USA 96, 13634-13637 (1999).
38. Simmler, M. C., Cattanach, B. M., Rasberry, C., Rouguelle, C. & Avner, P. Mapping the murine Xce locus with (CA)n repeats. Mamm. Genome 4, 523-530 (1993)
39. Plenge, R. M. et al. A promoter mutation in the XIST gene in two unrelated families with skewed X-chromosome inactivation. Nature Genet. 14, 353-356 (1997)
40. Marahrens, Y., Loring, J. & Jaenisch, R. Role of the Xist gene in X chromosome choosing, Cell 92, 657-664 (1998).
41. Graves, J. A. Mammals that break the rules: genetics of marsupials and monotremes. Annu. Rev. Genet 30, 233-260 (1996).
42. Richler, C., Dhara, S. K. & Wahrman, J. Histone macroH2A 1.2 is concentrated in the XY compartment of mammalian male meiotic nuclei. Cytogenet. Cell. Genet. 89, 118-120 (2000).
43. Hoyer-Fender, S., Costanzi, C. & Pehrson, J. R. Histone macroH2A1.2 is concentrated in the XY-body by the early pachytene stage of spermatogenesis. Exp. Cell Res. 258, 254-260 (2000).
44. Mayer, W., Niveleau, A., Walter, J., Fundele, R. & Haaf, T. Demethylation of the zygotic paternal genome. Nature 403, 501-502 (2000).
45. Ferreira, J. & Carmo-Fonseca, M. Genome replication in early mouse embryos follows a defined temporal and spatial order. J. Cell Sci. 110, 889-897 (1997).
46. Mayer, W., Smith, A., Fundele, R. & Haaf, T. Spatial separation of parental genomes in preimplantation mouse embryos. J. Cell Biol. 148, 629-634 (2000).
47. Eggan, K. et al. Non-random and random X chromosome inactivation in cloned embryos. Science 290, 1578-1581 (2000). The first use of somatic nuclear transfer to explore facets of the biology of X inactivation.
48. Okamoto, I., Tan, S. S. & Takagi, N. X chromosome inactivation in XX androgenetic mouse embryos surviving implantation. Development 127, 4137-4145 (2000).
49. Goto, Y. & Takagi, N. Maternally inherited X chromosome is not inactivated in mouse blastocysts due to parental imprinting. Chromosome Res. 7, 101-109 (1999).
50. Tada, T. et al. Imprint switching for non random X-chromosome inactivation during mouse oocyte growth. Development 127, 3101-3103 (2000).
51. McDonald, L. E., Paterson, C. A. & Kay, G. F. Bisulfite genomic sequencing-derived methylation profile of the Xist gene throughout early mouse development. Genomics 54, 379-386 (1998).
52. Lee, J. T. Disruption of imprinted X inactivation by parent-of-origin effects at TsiX. Cell 103, 17-27 (2000).
53. Prissette, M., El-Maarri, O., Arnaud, D., Walter, J. & Avner, P. Methylation profiles of the DXPas34 locus during the onset of X-inactivation. Hum. Mol. Genet. (in the press).
54. White, W. M., Willard, H. F., Van Dyke, D. L. & Wolff, D. J. The spreading of X inactivation into autosomal material of an X;autosome translocation: evidence for a difference between autosomal and X-chromosomal DNA. Am. J. Hum. Genet. 63, 20-28 (1998)
55. Duthie, S. M. et al. Xist RNA exhibits a banded localization on the inactive X chromosome and is excluded from autosomal material in cis. Hum. Mol. Genet. 8, 195-204 (1999).
56. Riggs, A. D. Marsupials and mechanisms of X chromosome inactivation. Aust. J. Zool. 37, 419-441 (1990)
57. Bailey, J. A., Carrel, L., Chakravarti, A. & Eichler, E. E. Molecular evidence for a relationship between LINE-1 elements and X chromosome inactivation: the Lyon repeat hypothesis. Proc. Natl Acad. Sci. USA 97, 6634-6639 (2000).
58. Carrel, L., Cottle, A. A., Goglin, K. C. & Willard, H. F. A first generation X-inactivation profile of the human X chromosome. Proc. Natl Acad. Sci. USA 96, 14440-14444 (1999).
59. Watanabe, Y., Tenzen, T., Nagasaka, Y., Inoko, H. & Ikemura, T. Replication timing of the human X-inactivation center (XIC) region: correlation with chromosome bands. Gene 252, 163-172 (2000).
60. Keohane, A. M., Barlow, A. L., Waters, J., Bourn, D. & Turner, B. M. H4 acetylation, XIST RNA and replication timing are coincident and define X; autosome boundaries in tow abnormal X chromosomes. Hum. Mol. Genet. 8, 377-383 (1999).
61. Disteche, C. M. Escapees on the X chromosome. Proc. Natl Acad. Sci. USA 96, 14180-14182 (1999).
62. DeBerardinis, R. J., Goodier, J. L., Ostertag, E. M. & Kazazian, H. H. Jr Rapid amplification of a retrotransposon subfamily is evolving the mouse genome. Nature Genet. 20, 288-290 (1998).
63. Lingenfelter, P. A. et al. Escape from X inactivation is preceded by silencing during development. Nature Genet. 18, 212-213 (1999).
64. Sanford, J. P., Clark, H. J., Chapman, V. M. & Rossant, J. Differences in DNA methylation during oogenesis and spermatogenesis and their persistence during early embryogenesis in the mouse. Genes Dev. 1, 1039-1046 (1987)
65. Xu, G. L. et al. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402, 187-190 (1999).
66. Amir, R. E. et al. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyt-CpG-binding protein 2. Nature Genet. 23, 185-188 (1999).
67. Simmler, M. C. et al. Localisation and expression analysis of a novel conserved brain expressed sequence, Brx/BRX, lying within the Xic/XIC candidate region. Mamm. Genome 8, 760-766 (1997).
68. Cunningham, D. B., Segretain, D., Arnaud, D., Rogner, U. C. & Avner, P. The Mouse Tsx gene is expressed in Sertoli cells of the adult testis and transiently in premeiotic germ cells during puberty. Dev. Biol. 204, 345-360 (1998).
69. Horn, J. H. & Ashworth, A. A member of the caudal family of homeobox genes maps to the X-inactivation centre region of the mouse and human X chromosomes. Hum. Mol. Genet. 4, 1041-1047 (1995).
70. Rougeulle, C. & Avner, P. Identification of an S19 pseudogene lying close to the Xist sequence in the mouse. Mamm. Genome 7, 606-607 (1996)
71. Lyon, M. F. X-chromosome inactivation: a repeat hypothesis. Cytogenet. Cell Genet. 80, 133-137 (1998).