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X-Chromosome Inactivation: A Complex Circuits regulated by Non-coding RNAs and Pluripotent Factors

  • Hwang, Jae Yeon (Department of Agricultural Biotechnology, Animal Biotechnology Major, Seoul National University) ;
  • Lee, Chang-Kyu (Department of Agricultural Biotechnology, Animal Biotechnology Major, Seoul National University)
  • Received : 2017.05.11
  • Accepted : 2017.05.31
  • Published : 2017.05.31

Abstract

X-chromosome inactivation is one of the most complex events observed in early embryo developments. The epigenetic changes occurred in female X-chromosome is essential to compensate dosages of X-linked genes between males and females. Because of the relevance of the epigenetic process to the normal embryo developments and stem cell studies, X-chromosome inactivation has been focused intensively for last 10 years. Initiation and regulation of the process is managed by diverse factors. Especially, proteins and non-coding RNAs encoded in X-chromosome inactivation center, and a couple of transcription factors have been reported to regulate the event. In this review, we introduce the reported factors, and how they regulate epigenetic inactivation of X-chromosomes.

Keywords

References

  1. Barakat TS, Gunhanlar N, Pardo CG, Achame EM, Ghazvini M, Boers R, Kenter A, Rentmeester E, Grootegoed JA, Gribnau J (2011): RNF12 activates Xist and is essential for X chromosome inactivation. PLoS Genet 7:e1002001. https://doi.org/10.1371/journal.pgen.1002001
  2. Barakat TS, Loos F, van Staveren S, Myronova E, Ghazvini M, Grootegoed JA, Gribnau J (2014): The trans-activator RNF12 and cis-acting elements effectuate X chromosome inactivation independent of Xpairing. Molecular Cell 53:965-978. https://doi.org/10.1016/j.molcel.2014.02.006
  3. Brockdorff N, Ashworth A, Kay GF, McCabe VM, Norris DP, Cooper PJ, Swift S, Rastan S (1992): 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 71:515-526. https://doi.org/10.1016/0092-8674(92)90519-I
  4. Brons IGM, Smithers LE, Trotter MW, Rugg-Gunn P, Sun B, de Sousa Lopes SMC, Howlett SK, Clarkson A, Ahrlund-Richter L, Pedersen RA (2007): Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448:191-195. https://doi.org/10.1038/nature05950
  5. Brown CJ, Hendrich BD, Rupert JL, Lafreniere RG, Xing Y, Lawrence J, Willard HF (1992): 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 71:527-542. https://doi.org/10.1016/0092-8674(92)90520-M
  6. Brown CJ, Lafreniere RG (1991): Localization of the X inactivation centre on the human X chromosome in Xq13. Nature 349:82. https://doi.org/10.1038/349082a0
  7. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A (2003): Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113:643-655. https://doi.org/10.1016/S0092-8674(03)00392-1
  8. Chao W, Huynh KD, Spencer RJ, Davidow LS, Lee JT (2002): CTCF, a candidate trans-acting factor for X-inactivation choice. Science 295:345-347. https://doi.org/10.1126/science.1065982
  9. Chureau C, Chantalat S, Romito A, Galvani A, Duret L, Avner P, Rougeulle C (2010): Ftx is a non-coding RNA which affects Xist expression and chromatin structure within the X-inactivation center region. Human molecular genetics. pp 516.
  10. Chureau C, Prissette M, Bourdet A, Barbe V, Cattolico L, Jones L, Eggen A, Avner P, Duret L (2002): Comparative sequence analysis of the X-inactivation center region in mouse, human, and bovine. Genome Research 12:894-908.
  11. Clerc P, Avner P (1998): Role of the region 3' to Xist exon 6 in the counting process of X-chromosome inactivation. Nature Genetics 19:249-253. https://doi.org/10.1038/924
  12. Donohoe ME, Silva SS, Pinter SF, Xu N, Lee JT (2009): The pluripotency factor Oct4 interacts with Ctcf and also controls X-chromosome pairing and counting. Nature 460:128-132. https://doi.org/10.1038/nature08098
  13. Donohoe ME, Zhang LF, Xu N, Shi Y, Lee JT (2007): Identification of a Ctcf cofactor, Yy1, for the X chromosome binary switch. Molecular Cell 25:43-56. https://doi.org/10.1016/j.molcel.2006.11.017
  14. Duret L, Chureau C, Samain S, Weissenbach J, Avner P (2006): The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science 312:1653-1655. https://doi.org/10.1126/science.1126316
  15. Elisaphenko EA, Kolesnikov NN, Shevchenko AI, Rogozin IB, Nesterova TB, Brockdorff N, Zakian SM (2008): A dual origin of the Xist gene from a protein-coding gene and a set of transposable elements. PLoS One 3:e2521. https://doi.org/10.1371/journal.pone.0002521
  16. Escamilla-Del-Arenal M, da Rocha ST, Heard E (2011): Evolutionary diversity and developmental regulation of X-chromosome inactivation. Human Genetics 130:307-327. https://doi.org/10.1007/s00439-011-1029-2
  17. Finestra TR, Gribnau J (2017): X chromosome inactivation: silencing, topology and reactivation. Current Opinion in Cell Biology 46:54-61. https://doi.org/10.1016/j.ceb.2017.01.007
  18. Gontan C, Achame EM, Demmers J, Barakat TS, Rentmeester E, van IJcken W, Grootegoed JA, Gribnau J (2012): RNF12 initiates X-chromosome inactivation by targeting REX1 for degradation. Nature 485:386-390. https://doi.org/10.1038/nature11070
  19. Grutzner F, Rens W, Tsend-Ayush E, El-Mogharbel N, O'brien PC, Jones RC, Ferguson-Smith MA, Graves JAM (2004): In the platypus a meiotic chain of ten sex chromosomes shares genes with the bird Z and mammal X chromosomes. Nature 432:913-917. https://doi.org/10.1038/nature03021
  20. Graves JA (2015): Evolution of vertebrate sex chromosomes and dosage compensation. Nature Reviews Genetics.
  21. Hore TA, Koina E, Wakefield MJ, Graves JAM (2007): The region homologous to the X-chromosome inactivation centre has been disrupted in marsupial and monotreme mammals. Chromosome Research 15:147. https://doi.org/10.1007/s10577-007-1119-0
  22. Hwang JY, Kim EB, Ka H, Lee CK (2013): Identification of the porcine XIST gene and its differential CpG methylation status in male and female pig cells. PloS One 8:e73677. https://doi.org/10.1371/journal.pone.0073677
  23. Hwang JY, Oh JN, Park CH, Lee DK, Lee CK (2015): Dosage compensation of X-chromosome inactivation center-linked genes in porcine preimplantation embryos: Non-chromosome-wide initiation of X-chromosome inactivation in blastocysts. Mechanisms of Development 138:246-255. https://doi.org/10.1016/j.mod.2015.10.005
  24. Inoue K, Kohda T, Sugimoto M, Sado T, Ogonuki N, Matoba S, Shiura H, Ikeda R, Mochida K, Fujii T (2010): Impeding Xist expression from the active X chromosome improves mouse somatic cell nuclear transfer. Science 330:496-499. https://doi.org/10.1126/science.1194174
  25. Johnston CM, Newall AE, Brockdorff N, Nesterova TB (2002): Enox, a novel gene that maps 10 kb upstream of Xist and partially escapes X inactivation. Genomics 80:236-244. https://doi.org/10.1006/geno.2002.6819
  26. Jonkers I, Barakat TS, Achame EM, Monkhorst K, Kenter A, Rentmeester E, Grosveld F, Grootegoed JA, Gribnau J (2009): RNF12 is an X-Encoded dosedependent activator of X chromosome inactivation. Cell 139:999-1011. https://doi.org/10.1016/j.cell.2009.10.034
  27. Kalantry S, Purushothaman S, Bowen RB, Starmer J Magnuson T (2009): Evidence of Xist RNA-independent initiation of mouse imprinted X-chromosome inactivation. Nature 460:647-651. https://doi.org/10.1038/nature08161
  28. Kurimoto K, Yamaji M, Seki Y, Saitou M (2008): Specification of the germ cell lineage in mice: a process orchestrated by the PR-domain proteins, Blimp1 and Prdm14. Cell Cycle 7:3514-3518. https://doi.org/10.4161/cc.7.22.6979
  29. Lee J, Davidow LS, Warshawsky D (1999): Tsix, a gene antisense to Xist at the X-inactivation centre. Nature genetics 21:400-404. https://doi.org/10.1038/7734
  30. Lee JT (2005): Regulation of X-chromosome counting by Tsix and Xite sequences. Science 309:768-771. https://doi.org/10.1126/science.1113673
  31. Lee JT, Lu N (1999): Targeted mutagenesis of Tsix leads to nonrandom X inactivation. Cell 99:47-57. https://doi.org/10.1016/S0092-8674(00)80061-6
  32. Lyon MF (1961): Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190:372-373. https://doi.org/10.1038/190372a0
  33. Ma Z, Swigut T, Valouev A, Rada-Iglesias A, Wysocka J (2011): Sequence-specific regulator Prdm14 safeguards mouse ESCs from entering extraembryonic endoderm fates. Nature Structural, Molecular Biology 18:120-127. https://doi.org/10.1038/nsmb.2000
  34. Marahrens Y, Panning B, Dausman J, Strauss W, Jaenisch R (1997): Xist-deficient mice are defective in dosage compensation but not spermatogenesis. Genes & Development 11:156-166. https://doi.org/10.1101/gad.11.2.156
  35. Masui S, Nakatake Y, Toyooka Y, Shimosato D, Yagi R, Takahashi K, Okochi H, Okuda A, Matoba R, Sharov AA (2007): Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nature Cell Biology 9:625-635. https://doi.org/10.1038/ncb1589
  36. Matoba S, Inoue K, Kohda T, Sugimoto M, Mizutani E, Ogonuki N, Nakamura T, Abe K, Nakano T, Ishino F (2011): RNAi-mediated knockdown of Xist can rescue the impaired postimplantation development of cloned mouse embryos. Proceedings of the National Academy of Sciences 108:20621-20626. https://doi.org/10.1073/pnas.1112664108
  37. Meyer B (2000): Sex and death of a worm: assessing and repressing X chromosomes. Harvey Lectures 95:85-105.
  38. Migeon BR, Chowdhury AK, Dunston JA, McIntosh I (2001): Identification of TSIX, encoding an RNA antisense to human XIST, reveals differences from its murine counterpart: implications for X inactivation. The American Journal of Human Genetics 69:951-960. https://doi.org/10.1086/324022
  39. Migeon BR, Lee CH, Chowdhury AK, Carpenter H (2002): Species differences in TSIX/Tsix reveal the roles of these genes in X-chromosome inactivation. The American Journal of Human Genetics 71:286-293. https://doi.org/10.1086/341605
  40. Minkovsky A, Barakat TS, Sellami N, Chin MH, Gunhanlar N, Gribnau J, Plath K (2013): The pluripotency factor-bound intron 1 of Xist is dispensable for X chromosome inactivation and reactivation in vitro and in vivo. Cell Reports 3:905-918. https://doi.org/10.1016/j.celrep.2013.02.018
  41. Navarro P, Chambers I, Karwacki-Neisius V, Chureau C, Morey C, Rougeulle C, Avner P (2008): Molecular coupling of Xist regulation and pluripotency. Science 321:1693-1695. https://doi.org/10.1126/science.1160952
  42. Navarro P, Moffat M, Mullin NP, Chambers I (2011): The X-inactivation trans-activator Rnf12 is negatively regulated by pluripotency factors in embryonic stem cells. Human Genetics 130:255-264. https://doi.org/10.1007/s00439-011-0998-5
  43. Navarro P, Oldfield A, Legoupi J, Festuccia N, Dubois A, Attia M, Schoorlemmer J, Rougeulle C, Chambers I, Avner P (2010): Molecular coupling of Tsix regulation and pluripotency. Nature 468:457-460. https://doi.org/10.1038/nature09496
  44. Navarro P, Page DR, Avner P, Rougeulle C (2006): Tsix-mediated epigenetic switch of a CTCF-flanked region of the Xist promoter determines the Xist transcription program. Genes & Development 20:2787-2792. https://doi.org/10.1101/gad.389006
  45. Nichols J, Smith A (2009): Naive and primed pluripotent states. Cell Stem Cell 4:487-492. https://doi.org/10.1016/j.stem.2009.05.015
  46. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, Scholer H, Smith A (1998): Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95:379-391. https://doi.org/10.1016/S0092-8674(00)81769-9
  47. Niwa H, Miyazaki JI, Smith AG (2000): Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nature genetics 24:372-376. https://doi.org/10.1038/74199
  48. Ogawa Y, Lee JT (2003): Xite, X-inactivation intergenic transcription elements that regulate the probability of choice. Molecular Cell 11:731-743. https://doi.org/10.1016/S1097-2765(03)00063-7
  49. Ohhata T, Wutz A (2013): Reactivation of the inactive X chromosome in development and reprogramming. Cellular and Molecular Life Sciences 70: 2443-2461. https://doi.org/10.1007/s00018-012-1174-3
  50. Okamoto I, Patrat C, Thepot D, Peynot N, Fauque P, Daniel N, Diabangouaya P, Wolf JP, Renard JP, Duranthon V (2011): Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development. Nature 472:370-374. https://doi.org/10.1038/nature09872
  51. Park CH, Jeong YH, Jeong YI, Lee SY, Jeong YW, Shin T, Kim NH, Jeung EB, Hyun SH, Lee CK (2012): X-linked gene transcription patterns in female and male in vivo, in vitro and cloned porcine individual blastocysts. PLoS One 7:e51398. https://doi.org/10.1371/journal.pone.0051398
  52. Park Y, Kuroda MI (2001): Epigenetic aspects of Xchromosome dosage compensation. Science 293:1083-1085. https://doi.org/10.1126/science.1063073
  53. Payer B, Rosenberg M, Yamaji M, Yabuta Y, Koyanagi-Aoi M, Hayashi K, Yamanaka S, Saitou M, Lee JT (2013): Tsix RNA and the germline factor, PRDM14, link X reactivation and stem cell reprogramming. Molecular Cell 52:805-818. https://doi.org/10.1016/j.molcel.2013.10.023
  54. Penny GD, Kay GF, Sheardown SA, Rastan S, Brockdorff N (1996): Requirement for Xist in X chromosome inactivation. Nature 379:131. https://doi.org/10.1038/379131a0
  55. Postlmayr A, Wutz A (2017): Insights into the establishment of chromatin states in pluripotent cells from studies of X inactivation. Journal of Molecular Biology.
  56. Rastan S (1983): Non-random X-chromosome inactivation in mouse X-autosome translocation embryoslocation of the inactivation centre. Development 78:1-22.
  57. Sado T, Hoki Y, Sasaki H (2005): Tsix silences Xist through modification of chromatin structure. Developmental cell 9:159-165. https://doi.org/10.1016/j.devcel.2005.05.015
  58. Sado T, Wang Z, Sasaki H, Li E (2001): Regulation of imprinted X-chromosome inactivation in mice by Tsix. Development-Cambridge 128:1275-1286.
  59. Sarma K, Levasseur P, Aristarkhov A, Lee JT (2010): Locked nucleic acids (LNAs) reveal sequence requirements and kinetics of Xist RNA localization to the X chromosome. Proceedings of the National Academy of Sciences 107:22196-22201. https://doi.org/10.1073/pnas.1009785107
  60. Shin J, Bossenz M, Chung Y, Ma H, Byron M, Taniguchi-Ishigaki N, Zhu X, Jiao B, Hall LL, Green MR (2010): Maternal Rnf12/RLIM is required for imprinted X-chromosome inactivation in mice. Nature 467:977-981. https://doi.org/10.1038/nature09457
  61. Shin J, Wallingford MC, Gallant J, Marcho C, Jiao B, Byron M, Bossenz M, Lawrence JB, Jones SN, Mager J (2014): RLIM is dispensable for X-chromosome inactivation in the mouse embryonic epiblast. Nature 511:86-89. https://doi.org/10.1038/nature13286
  62. Soma M, Fujihara Y, Okabe M, Ishino F, Kobayashi S (2014): Ftx is dispensable for imprinted X-chromosome inactivation in preimplantation mouse embryos. Scientific Reports 4:5181.
  63. Sun BK, Deaton AM, Lee JT (2006): A transient heterochromatic state in Xist preempts X inactivation choice without RNA stabilization. Molecular Cell 21:617-628. https://doi.org/10.1016/j.molcel.2006.01.028
  64. Sun S, Del Rosario BC, Szanto A, Ogawa Y, Jeon Y, Lee JT (2013): Jpx RNA activates Xist by evicting CTCF. Cell 153:1537-1551. https://doi.org/10.1016/j.cell.2013.05.028
  65. Takahashi K, Yamanaka S (2006): Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676. https://doi.org/10.1016/j.cell.2006.07.024
  66. Tian D, Sun S, Lee JT (2010): The long noncoding RNA, Jpx, is a molecular switch for X chromosome inactivation. Cell 143:390-403. https://doi.org/10.1016/j.cell.2010.09.049
  67. Vigneau S, Augui S, Navarro P, Avner P, Clerc P (2006): An essential role for the DXPas34 tandem repeat and Tsix transcription in the counting process of X chromosome inactivation. Proceedings of the National Academy of Sciences 103:7390-7395. https://doi.org/10.1073/pnas.0602381103
  68. Wutz A, Rasmussen TP, Jaenisch R (2002): Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nature Genetics 30: 167-174. https://doi.org/10.1038/ng820
  69. Yamaji M, Seki Y, Kurimoto K, Yabuta Y, Yuasa M, Shigeta M, Yamanaka K, Ohinata Y, Saitou M (2008): Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nature Genetics 40:1016-1022. https://doi.org/10.1038/ng.186
  70. Yamaji M, Ueda J, Hayashi K, Ohta H, Yabuta Y, Kurimoto K, Nakato R, Yamada Y, Shirahige K, Saitou M (2013): PRDM14 ensures naive pluripotency through dual regulation of signaling and epigenetic pathways in mouse embryonic stem cells. Cell Stem Cell 12:368-382. https://doi.org/10.1016/j.stem.2012.12.012
  71. Zhao J, Sun BK, Erwin JA, Song JJ, Lee JT (2008) Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322:750-756. https://doi.org/10.1126/science.1163045