Different flavors of X-chromosome inactivation in mammals

Current Opinion in Cell Biology

Volumn 25, Issue 3, 2013, Pages 314-321

  Dupont, Cathérine ^a   Gribnau, Joost ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; KRUPPEL LIKE FACTOR 4; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR GATA 6; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2;

BLASTOCYST; ECTODERM; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; ENDODERM; GENE EXPRESSION; MARSUPIAL; NIDATION; NONHUMAN; PLACENTAL MAMMALS; PRIORITY JOURNAL; REVIEW; TRANSCRIPTION INITIATION SITE; X CHROMOSOME; X CHROMOSOME INACTIVATION;

ANIMALS; BIOLOGICAL EVOLUTION; GENES, X-LINKED; MAMMALS; MICE; MODELS, ANIMAL; SEX DETERMINATION PROCESSES; SPECIES SPECIFICITY; X CHROMOSOME INACTIVATION;

ANIMALIA; EUTHERIA; MAMMALIA; METATHERIA; THERIA;

EID: 84879249750     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2013.03.001     Document Type: Review

References (107)

1. Koopman P., et al. Expression of a candidate sex-determining gene during mouse testis differentiation. Nature 1990, 348:450-452.
2. Lovell-Badge R. The role of Sry in mammalian sex determination. Ciba Found Symp 1992, 165:162-179. discussion 179-82.
3. Wallis M.C., Waters P.D., Graves J.A. Sex determination in mammals-before and after the evolution of SRY. Cell Mol Life Sci 2008, 65:3182-3195.
4. Nguyen D.K., Disteche C.M. Dosage compensation of the active X chromosome in mammals. Nat Genet 2006, 38:47-53.
5. Gribnau J., Grootegoed J.A. Origin and evolution of X chromosome inactivation. Curr Opin Cell Biol 2012, 24:397-404.
6. Lyon M.F. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 1961, 190:372-373.
7. Brown C.J., et al. A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 1991, 349:38-44.
8. Borsani G., et al. Characterization of a murine gene expressed from the inactive X chromosome. Nature 1991, 351:325-329.
9. Brockdorff N., et al. Conservation of position and exclusive expression of mouse Xist from the inactive X chromosome. Nature 1991, 351:329-331.
10. Grant J., et al. Rsx is a metatherian RNA with Xist-like properties in X-chromosome inactivation. Nature 2012, 487:254-258.
11. Okamoto I., Tan S., Takagi N. X-chromosome inactivation in XX androgenetic mouse embryos surviving implantation. Development 2000, 127:4137-4145.
12. Brown S.D. XIST and the mapping of the X chromosome inactivation centre. Bioessays 1991, 13:607-612.
13. Lee J.T., Davidow L.S., Warshawsky D. Tsix, a gene antisense to Xist at the X-inactivation centre. Nat Genet 1999, 21:400-404.
14. Lee J.T., Lu N. Targeted mutagenesis of Tsix leads to nonrandom X inactivation. Cell 1999, 99:47-57.
15. Penny G.D., et al. Requirement for Xist in X chromosome inactivation. Nature 1996, 379:131-137.
16. Okamoto I., Heard E. Lessons from comparative analysis of X-chromosome inactivation in mammals. Chromosome Res 2009, 17:659-669.
17. Patrat C., et al. Dynamic changes in paternal X-chromosome activity during imprinted X-chromosome inactivation in mice. Proc Natl Acad Sci USA 2009, 106:5198-5203.
18. Kalantry S., et al. Evidence of Xist RNA-independent initiation of mouse imprinted X-chromosome inactivation. Nature 2009, 460:647-651.
19. Namekawa S.H., et al. Two-step imprinted X inactivation: repeat versus genic silencing in the mouse. Mol Cell Biol 2010, 30:3187-3205.
20. Okamoto I., et al. Evidence for de novo imprinted X-chromosome inactivation independent of meiotic inactivation in mice. Nature 2005, 438:369-373.
21. Kay G.F., et al. Expression of Xist during mouse development suggests a role in the initiation of X chromosome inactivation. Cell 1993, 72:171-182.
22. Hartshorn C., Rice J.E., Wangh L.J. Developmentally-regulated changes of Xist RNA levels in single preimplantation mouse embryos, as revealed by quantitative real-time PCR. Mol Reprod Dev 2002, 61:425-436.
23. Nesterova T.B., et al. Loss of Xist imprinting in diploid parthenogenetic preimplantation embryos. Dev Biol 2001, 235:343-350.
24. Matsui J., Goto Y., Takagi N. Control of Xist expression for imprinted and random X chromosome inactivation in mice. Hum Mol Genet 2001, 10:1393-1401.
25. Takagi N., Sasaki M. Preferential inactivation of the paternally derived X chromosome in the extraembryonic membranes of the mouse. Nature 1975, 256:640-642.
26. Mak W., et al. Reactivation of the paternal X chromosome in early mouse embryos. Science 2004, 303:666-669.
27. Okamoto I., et al. Epigenetic dynamics of imprinted X inactivation during early mouse development. Science 2004, 303:644-649.
28. Lee J.T. Disruption of imprinted X inactivation by parent-of-origin effects at Tsix. Cell 2000, 103:17-27.
29. Sado T., et al. Regulation of imprinted X-chromosome inactivation in mice by Tsix. Development 2001, 128:1275-1286.
30. Marahrens Y., et al. Xist-deficient mice are defective in dosage compensation but not spermatogenesis. Genes Dev 1997, 11:156-166.
31. Tada T., et al. Imprint switching for non-random X-chromosome inactivation during mouse oocyte growth. Development 2000, 127:3101-3105.
32. Navarro P., Avner P. When X-inactivation meets pluripotency: an intimate rendezvous. FEBS Lett 2009, 583:1721-1727.
33. Ambrosetti D.C., Basilico C., Dailey L. Synergistic activation of the fibroblast growth factor 4 enhancer by Sox2 and Oct-3 depends on protein-protein interactions facilitated by a specific spatial arrangement of factor binding sites. Mol Cell Biol 1997, 17:6321-6329.
34. Ambrosetti D.C., et al. Modulation of the activity of multiple transcriptional activation domains by the DNA binding domains mediates the synergistic action of Sox2 and Oct-3 on the fibroblast growth factor-4 enhancer. J Biol Chem 2000, 275:23387-23397.
35. Niwa H., et al. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 2005, 123:917-929.
36. Jonkers I., et al. RNF12 is an X-encoded dose-dependent activator of X chromosome inactivation. Cell 2009, 139:999-1011.
37. Barakat T.S., et al. RNF12 activates Xist and is essential for X chromosome inactivation. PLoS Genet 2011, 7:e1002001.
38. Gontan C., et al. RNF12 initiates X-chromosome inactivation by targeting REX1 for degradation. Nature 2012, 485:386-390.
39. Shin J., et al. Maternal Rnf12/RLIM is required for imprinted X-chromosome inactivation in mice. Nature 2010, 467:977-981.
40. Rossant J., Tam P.P. Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 2009, 136:701-713.
41. Plusa B., et al. Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 2008, 135:3081-3091.
42. Chazaud C., et al. Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev Cell 2006, 10:615-624.
43. Navarro P., et al. Molecular coupling of Xist regulation and pluripotency. Science 2008, 321:1693-1695.
44. Navarro P., et al. Molecular coupling of Tsix regulation and pluripotency. Nature 2010, 468:457-460.
45. Navarro P., et al. The X-inactivation trans-activator Rnf12 is negatively regulated by pluripotency factors in embryonic stem cells. Hum Genet 2011, 130:255-264.
46. Nesterova T.B., et al. Pluripotency factor binding and Tsix expression act synergistically to repress Xist in undifferentiated embryonic stem cells. Epigenetics Chromatin 2011, 4:17.
47. Tesar P.J., et al. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 2007, 448:196-199.
48. Guo G., et al. Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 2009, 136:1063-1069.
49. Strumpf D., et al. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 2005, 132:2093-2102.
50. Monkhorst K., et al. X inactivation counting and choice is a stochastic process: evidence for involvement of an X-linked activator. Cell 2008, 132:410-421.
51. Barakat T.S., et al. X-changing information on X inactivation. Exp Cell Res 2010, 316:679-687.
52. Bacher C.P., et al. Transient colocalization of X-inactivation centres accompanies the initiation of X inactivation. Nat Cell Biol 2006, 8:293-299.
53. Xu N., Tsai C.L., Lee J.T. Transient homologous chromosome pairing marks the onset of X inactivation. Science 2006, 311:1149-1152.
54. Masui O., et al. Live-cell chromosome dynamics and outcome of X chromosome pairing events during ES cell differentiation. Cell 2011, 145:447-458.
55. Tian D., Sun S., Lee J.T. The long noncoding RNA Jpx, is a molecular switch for X chromosome inactivation. Cell 2010, 143:390-403.
56. Augui S., Nora E.P., Heard E. Regulation of X-chromosome inactivation by the X-inactivation centre. Nat Rev Genet 2011, 12:429-442.
57. Chow J.C., et al. LINE-1 activity in facultative heterochromatin formation during X chromosome inactivation. Cell 2010, 141:956-969.
58. Chaumeil J., et al. A novel role for Xist RNA in the formation of a repressive nuclear compartment into which genes are recruited when silenced. Genes Dev 2006, 20:2223-2237.
59. Jeon Y., Lee J.T. YY1 tethers Xist RNA to the inactive X nucleation center. Cell 2011, 146:119-133.
60. Wutz A., Rasmussen T.P., Jaenisch R. Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat Genet 2002, 30:167-174.
61. Pinter S.F., et al. Spreading of X chromosome inactivation via a hierarchy of defined Polycomb stations. Genome Res 2012, 22:1864-1876.
62. Marks H., et al. High-resolution analysis of epigenetic changes associated with X inactivation. Genome Res 2009, 19:1361-1373.
63. Gebhard C., et al. General transcription factor binding at CpG islands in normal cells correlates with resistance to de novo DNA methylation in cancer cells. Cancer Res 2010, 70:1398-1407.
64. Nora E.P., et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 2012, 485:381-385.
65. Dixon J.R., et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012, 485:376-380.
66. Moreira de Mello J.C., et al. Random X inactivation and extensive mosaicism in human placenta revealed by analysis of allele-specific gene expression along the X chromosome. PLoS ONE 2010, 5:e10947.
67. Wang X., et al. Random X inactivation in the mule and horse placenta. Genome Res 2012, 22:1855-1863.
68. Tachibana M., et al. X-chromosome inactivation in monkey embryos and pluripotent stem cells. Dev Biol 2012, 371:146-155.
69. Xue F., et al. Aberrant patterns of X chromosome inactivation in bovine clones. Nat Genet 2002, 31:216-220.
70. Dindot S.V., et al. Conservation of genomic imprinting at the XIST, IGF2, and GTL2 loci in the bovine. Mamm Genome 2004, 15:966-974.
71. Dindot S.V., et al. Epigenetic and genomic imprinting analysis in nuclear transfer derived Bos gaurus/Bos taurus hybrid fetuses. Biol Reprod 2004, 71:470-478.
72. Wake N., Takagi N., Sasaki M. Non-random inactivation of X chromosome in the rat yolk sac. Nature 1976, 262:580-581.
73. Flach G., et al. The transition from maternal to embryonic control in the 2-cell mouse embryo. EMBO J 1982, 1:681-686.
74. Schultz R.M. Regulation of zygotic gene activation in the mouse. Bioessays 1993, 15:531-538.
75. Frei R.E., Schultz G.A., Church R.B. Qualitative and quantitative changes in protein synthesis occur at the 8-16-cell stage of embryogenesis in the cow. J Reprod Fertil 1989, 86:637-641.
76. Viuff D., et al. Transcriptional activity in in vitro produced bovine two- and four-cell embryos. Mol Reprod Dev 1996, 43:171-179.
77. Braude P., Bolton V., Moore S. Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature 1988, 332:459-461.
78. Manes C. The participation of the embryonic genome during early cleavage in the rabbit. Dev Biol 1973, 32:453-459.
79. Jarrell V.L., Day B.N., Prather R.S. The transition from maternal to zygotic control of development occurs during the 4-cell stage in the domestic pig, Sus scrofa: quantitative and qualitative aspects of protein synthesis. Biol Reprod 1991, 44:62-68.
80. Peippo J., et al. Sex-chromosome linked gene expression in in-vitro produced bovine embryos. Mol Hum Reprod 2002, 8:923-929.
81. Merighe G.K., et al. Gene silencing during development of in vitro-produced female bovine embryos. Genet Mol Res 2009, 8:1116-1127.
82. Shevchenko A.I., et al. Variability of sequence surrounding the Xist gene in rodents suggests taxon-specific regulation of X chromosome inactivation. PLoS ONE 2011, 6:e22771.
83. Horvath J.E., et al. Comparative analysis of the primate X-inactivation center region and reconstruction of the ancestral primate XIST locus. Genome Res 2011, 21:850-862.
84. Okamoto I., et al. Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development. Nature 2011, 472:370-374.
85. Ray P.F., Winston R.M., Handyside A.H. XIST expression from the maternal X chromosome in human male preimplantation embryos at the blastocyst stage. Hum Mol Genet 1997, 6:1323-1327.
86. Daniels R., et al. XIST expression in human oocytes and preimplantation embryos. Am J Hum Genet 1997, 61:33-39.
87. Park C.H., et al. Analysis of imprinted gene expression in normal fertilized and uniparental preimplantation porcine embryos. PLoS ONE 2011, 6:e22216.
88. Graves J.A. Sex chromosome specialization and degeneration in mammals. Cell 2006, 124:901-914.
89. Cooper D.W., et al. Phosphoglycerate kinase polymorphism in kangaroos provides further evidence for paternal X inactivation. Nat New Biol 1971, 230:155-157.
90. Sharman G.B. Late DNA replication in the paternally derived X chromosome of female kangaroos. Nature 1971, 230:231-232.
91. Chaumeil J., et al. Evolution from XIST-independent to XIST-controlled X-chromosome inactivation: epigenetic modifications in distantly related mammals. PLoS ONE 2011, 6:e19040.
92. Kaslow D.C., Migeon B.R. DNA methylation stabilizes X chromosome inactivation in eutherians but not in marsupials: evidence for multistep maintenance of mammalian X dosage compensation. Proc Natl Acad Sci USA 1987, 84:6210-6214.
93. Duret L., et al. The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science 2006, 312:1653-1655.
94. Selwood L., Young G.J. Cleavage in vivo and in culture in the Dasyurid marsupial Antechinus stuartii (macleay). J Morphol 1983, 176:43-60.
95. Chen C.H., et al. Spatial and temporal distribution of Oct-4 and acetylated H4K5 in rabbit embryos. Reprod Biomed Online 2012, 24:433-442.
96. Chen C.H., et al. Dynamic profiles of Oct-4 Cdx-2 and acetylated H4K5 in in-vivo-derived rabbit embryos. Reprod Biomed Online 2012, 25:358-370.
97. Alliston C.W., Pardee N.R. Variability of embryonic development in the rabbit at 19 to 168hours after mating. Lab Anim Sci 1973, 23:665-670.
98. Kimber S.J., et al. Expression of genes involved in early cell fate decisions in human embryos and their regulation by growth factors. Reproduction 2008, 135:635-647.
99. Cauffman G., et al. POU5F1 isoforms show different expression patterns in human embryonic stem cells and preimplantation embryos. Stem Cells 2006, 24:2685-2691.
100. Harvey A.J., et al. Inner cell mass localization of NANOG precedes OCT3/4 in rhesus monkey blastocysts. Stem Cells Dev 2009, 18:1451-1458.
101. Mitalipov S.M., et al. Oct-4 expression in pluripotent cells of the rhesus monkey. Biol Reprod 2003, 69:1785-1792.
102. Kuijk E.W., et al. Differences in early lineage segregation between mammals. Dev Dyn 2008, 237:918-927.
103. Kirchhof N., et al. Expression pattern of Oct-4 in preimplantation embryos of different species. Biol Reprod 2000, 63:1698-1705.
104. Hall V.J., et al. Porcine pluripotency cell signaling develops from the inner cell mass to the epiblast during early development. Dev Dyn 2009, 238:2014-2024.
105. Khan D.R., et al. Expression of pluripotency master regulators during two key developmental transitions: EGA and early lineage specification in the bovine embryo. PLoS ONE 2012, 7:e34110.
106. Berg D.K., et al. Trophectoderm lineage determination in cattle. Dev Cell 2011, 20:244-255.
107. King G.J., Atkinson B.A., Robertson H.A. Development of the bovine placentome from days 20 to 29 of gestation. J Reprod Fertil 1980, 59:95-100.