#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Xist RNA in action: Past, present, and future


Autoři: Agnese Loda aff001;  Edith Heard aff001
Působiště autorů: Directors’ research, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany aff001;  Collège de France, Paris, France aff002
Vyšlo v časopise: Xist RNA in action: Past, present, and future. PLoS Genet 15(9): e32767. doi:10.1371/journal.pgen.1008333
Kategorie: Review
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1008333

Souhrn

In mammals, dosage compensation of sex chromosomal genes between females (XX) and males (XY) is achieved through X-chromosome inactivation (XCI). The X-linked X-inactive-specific transcript (Xist) long noncoding RNA is indispensable for XCI and initiates the process early during development by spreading in cis across the X chromosome from which it is transcribed. During XCI, Xist RNA triggers gene silencing, recruits a plethora of chromatin modifying factors, and drives a major structural reorganization of the X chromosome. Here, we review our knowledge of the multitude of epigenetic events orchestrated by Xist RNA to allow female mammals to survive through embryonic development by establishing and maintaining proper dosage compensation. In particular, we focus on recent studies characterizing the interaction partners of Xist RNA, and we discuss how they have affected the field by addressing long-standing controversies or by giving rise to new research perspectives that are currently being explored. This review is dedicated to the memory of Denise Barlow, pioneer of genomic imprinting and functional long noncoding RNAs (lncRNAs), whose work has revolutionized the epigenetics field and continues to inspire generations of scientists.

Klíčová slova:

Biology and life sciences – Cell biology – Chromosome biology – Chromatin – Genetics – Epigenetics – Gene expression – Genomics – Heredity – Biochemistry – Nucleic acids – Computational biology – Gene regulation – Medicine and health sciences – RNA – Non-coding RNA – DNA transcription – Clinical genetics – Genome complexity – Gene silencing – Dosage compensation – X chromosome inactivation – Silencer elements – Genetic linkage – Sex linkage – X-linked traits – Non-coding RNA sequences – Long non-coding RNAs


Zdroje

1. Brown SDM. XIST and the mapping of the X chromosome inactivation centre [Internet]. BioEssays. 1991. pp. 607–612. doi: 10.1002/bies.950131112 1772416

2. Brown CJ, Hendrich BD, Rupert JL, Lafrenière RG, Xing Y, Lawrence J, et al. 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. doi: 10.1016/0092-8674(92)90520-m 1423611

3. Borsani G, Tonlorenzi R, Simmler MC, Dandolo L, Arnaud D, Capra V, et al. Characterization of a murine gene expressed from the inactive X chromosome. Nature. 1991;351: 325–329. doi: 10.1038/351325a0 2034278

4. Brockdorff N, Ashworth A, Kay GF, Cooper P, Smith S, McCabe VM, et al. Conservation of position and exclusive expression of mouse Xist from the inactive X chromosome. Nature. 1991;351: 329–331. doi: 10.1038/351329a0 2034279

5. Brockdorff N, Ashworth A, Kay GF, McCabe VM, Norris DP, Cooper PJ, et al. 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. doi: 10.1016/0092-8674(92)90519-i 1423610

6. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, et al. 2001. Initial sequencing and analysis of the human genome. Nature. 409: 860. doi: 10.1038/35057062 11237011

7. Brannan CI, Dees EC, Ingram RS. The product of the H19 gene may function as an RNA. Molecular and cellular. Am Soc Microbiol; 1990; Available: https://mcb.asm.org/content/10/1/28.short

8. Bartolomei MS, Zemel S, Tilghman SM. Parental imprinting of the mouse H19 gene. Nature. 1991;351: 153–155. doi: 10.1038/351153a0 1709450

9. Wutz A, Smrzka OW, Schweifer N, Schellander K, Wagner EF, Barlow DP. Imprinted expression of the Igf2r gene depends on an intronic CpG island. Nature. 1997. pp. 745–749. doi: 10.1038/39631 9338788

10. Sleutels F, Zwart R, Barlow DP. The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature. 2002. pp. 810–813. doi: 10.1038/415810a 11845212

11. Okazaki Y, Furuno M, Kasukawa T, Adachi J, Bono H, Kondo S, et al. RIKEN Genome Exploration Research Group Phase I & II Team Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature. 2002;420: 563–573. doi: 10.1038/nature01266 12466851

12. Katayama S, Tomaru Y, Kasukawa T, Waki K, Nakanishi M, Nakamura M, et al. RIKEN Genome Exploration Research Group; Genome Science Group (Genome Network Project Core Group); FANTOM Consortium. Antisense transcription in the mammalian transcriptome. Science. 2005;309: 1564–1566. doi: 10.1126/science.1112009 16141073

13. ENCODE Project Consortium, Birney E, Stamatoyannopoulos JA, Dutta A, Guigó R, Gingeras TR, et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature. 2007;447: 799–816. doi: 10.1038/nature05874 17571346

14. Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature. 2009;458: 223–227. doi: 10.1038/nature07672 19182780

15. Ponting CP, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell. 2009;136: 629–641. doi: 10.1016/j.cell.2009.02.006 19239885

16. Delás MJ, Sabin LR, Dolzhenko E, Knott SR, Munera Maravilla E, Jackson BT, et al. lncRNA requirements for mouse acute myeloid leukemia and normal differentiation. Elife. 2017;6. doi: 10.7554/eLife.25607 28875933

17. Pauli A, Valen E, Lin MF, Garber M, Vastenhouw NL, Levin JZ, et al. Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res. 2012;22: 577–591. doi: 10.1101/gr.133009.111 22110045

18. Nam J-W, Bartel DP. Long noncoding RNAs in C. elegans. Genome Res. 2012;22: 2529–2540. doi: 10.1101/gr.140475.112 22707570

19. Barr ML, Bertram EG. A morphological distinction between neurones of the male and female, and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis. Nature. 1949;163: 676. doi: 10.1038/163676a0 18120749

20. Balaton BP, Brown CJ. Escape Artists of the X Chromosome. Trends Genet. 2016;32: 348–359. doi: 10.1016/j.tig.2016.03.007 27103486

21. 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. Springer; 1983;64: 24–27.

22. Cockwell A, MacKenzie M, Youings S, Jacobs P. A cytogenetic and molecular study of a series of 45,X fetuses and their parents [Internet]. Journal of Medical Genetics. 1991. pp. 151–155. doi: 10.1136/jmg.28.3.151 1675683

23. Schurz H, Salie M, Tromp G, Hoal EG, Kinnear CJ, Möller M. The X chromosome and sex-specific effects in infectious disease susceptibility. Hum Genomics. 2019;13: 2. doi: 10.1186/s40246-018-0185-z 30621780

24. Libert C, Dejager L, Pinheiro I. The X chromosome in immune functions: when a chromosome makes the difference. Nat Rev Immunol. 2010;10: 594–604. doi: 10.1038/nri2815 20651746

25. Lee JT, Davidow LS, Warshawsky D. Tsix, a gene antisense to Xist at the X-inactivation centre. Nat Genet. 1999;21: 400–404. doi: 10.1038/7734 10192391

26. Lee JT. Disruption of imprinted X inactivation by parent-of-origin effects at Tsix. Cell. 2000;103: 17–27. doi: 10.1016/s0092-8674(00)00101-x 11051544

27. Sado T, Wang Z, Sasaki H, Li E. Regulation of imprinted X-chromosome inactivation in mice by Tsix. Development. 2001;128: 1275–1286. 11262229

28. Luikenhuis S, Wutz A, Jaenisch R. Antisense Transcription through theXist Locus Mediates Tsix Function in Embryonic Stem Cells. Mol Cell Biol. American Society for Microbiology Journals; 2001;21: 8512–8520.

29. Shibata S, Lee JT. Tsix transcription- versus RNA-based mechanisms in Xist repression and epigenetic choice. Curr Biol. 2004;14: 1747–1754. doi: 10.1016/j.cub.2004.09.053 15458646

30. Ohhata T, Hoki Y, Sasaki H, Sado T. Crucial role of antisense transcription across the Xist promoter in Tsix-mediated Xist chromatin modification [Internet]. Development. 2007. pp. 227–235. doi: 10.1242/dev.008490 18057104

31. Sado T, Hoki Y, Sasaki H. Tsix silences Xist through modification of chromatin structure. Dev Cell. 2005;9: 159–165. doi: 10.1016/j.devcel.2005.05.015 15992549

32. Debrand E, Chureau C, Arnaud D. Functional Analysis of the DXPas34Locus, a 3′ Regulator of Xist Expression. Molecular and cellular. Am Soc Microbiol; 1999; Available: https://mcb.asm.org/content/19/12/8513.short

33. Anguera MC, Ma W, Clift D, Namekawa S, Kelleher RJ 3rd, Lee JT. Tsx produces a long noncoding RNA and has general functions in the germline, stem cells, and brain. PLoS Genet. 2011;7: e1002248. doi: 10.1371/journal.pgen.1002248 21912526

34. Ogawa Y, Lee JT. Xite, X-inactivation intergenic transcription elements that regulate the probability of choice. Mol Cell. 2003;11: 731–743. 12667455

35. Stavropoulos N, Rowntree RK, Lee JT. Identification of developmentally specific enhancers for Tsix in the regulation of X chromosome inactivation. Mol Cell Biol. 2005;25: 2757–2769. doi: 10.1128/MCB.25.7.2757-2769.2005 15767680

36. Chureau C, Chantalat S, Romito A, Galvani A, Duret L, Avner P, et al. Ftx is a non-coding RNA which affects Xist expression and chromatin structure within the X-inactivation center region [Internet]. Human Molecular Genetics. 2011. pp. 705–718. doi: 10.1093/hmg/ddq516 21118898

37. Sun S, Del Rosario BC, Szanto A, Ogawa Y, Jeon Y, Lee JT. Jpx RNA activates Xist by evicting CTCF. Cell. 2013;153: 1537–1551. doi: 10.1016/j.cell.2013.05.028 23791181

38. Tian D, Sun S, Lee JT. The long noncoding RNA, Jpx, is a molecular switch for X chromosome inactivation. Cell. 2010;143: 390–403. doi: 10.1016/j.cell.2010.09.049 21029862

39. Furlan G, Gutierrez Hernandez N, Huret C, Galupa R, van Bemmel JG, Romito A, et al. The Ftx Noncoding Locus Controls X Chromosome Inactivation Independently of Its RNA Products. Mol Cell. 2018;70: 462–472.e8. doi: 10.1016/j.molcel.2018.03.024 29706539

40. Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I, Servant N, et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature. 2012;485: 381–385. doi: 10.1038/nature11049 22495304

41. Gendrel A-V, Heard E. Noncoding RNAs and epigenetic mechanisms during X-chromosome inactivation. Annu Rev Cell Dev Biol. 2014;30: 561–580. doi: 10.1146/annurev-cellbio-101512-122415 25000994

42. Galupa R, Heard E. X-Chromosome Inactivation: A Crossroads Between Chromosome Architecture and Gene Regulation. Annu Rev Genet. 2018;52: 535–566. doi: 10.1146/annurev-genet-120116-024611 30256677

43. Furlan G, Rougeulle C. Function and evolution of the long noncoding RNA circuitry orchestrating X-chromosome inactivation in mammals. Wiley Interdiscip Rev RNA. Wiley Online Library; 2016;7: 702–722.

44. Galupa R, Heard E. X-chromosome inactivation: new insights into cis and trans regulation. Curr Opin Genet Dev. 2015;31: 57–66. doi: 10.1016/j.gde.2015.04.002 26004255

45. Penny GD, Kay GF, Sheardown SA, Rastan S, Brockdorff N. Requirement for Xist in X chromosome inactivation. Nature. 1996;379: 131–137. doi: 10.1038/379131a0 8538762

46. Marahrens Y, Panning B, Dausman J, Strauss W, Jaenisch R. Xist-deficient mice are defective in dosage compensation but not spermatogenesis. Genes Dev. 1997;11: 156–166. doi: 10.1101/gad.11.2.156 9009199

47. Wutz A, Jaenisch R. A shift from reversible to irreversible X inactivation is triggered during ES cell differentiation. Mol Cell. 2000;5: 695–705. 10882105

48. Chow JC, Hall LL, Baldry SEL, Thorogood NP, Lawrence JB, Brown CJ. Inducible XIST-dependent X-chromosome inactivation in human somatic cells is reversible. Proc Natl Acad Sci U S A. 2007;104: 10104–10109. doi: 10.1073/pnas.0610946104 17537922

49. Tang YA, Huntley D, Montana G, Cerase A, Nesterova TB, Brockdorff N. Efficiency of Xist-mediated silencing on autosomes is linked to chromosomal domain organisation. Epigenetics Chromatin. 2010;3: 10. doi: 10.1186/1756-8935-3-10 20459652

50. Loda A, Brandsma JH, Vassilev I, Servant N, Loos F, Amirnasr A, et al. Genetic and epigenetic features direct differential efficiency of Xist-mediated silencing at X-chromosomal and autosomal locations. Nat Commun. 2017;8: 690. doi: 10.1038/s41467-017-00528-1 28947736

51. Wutz A, Rasmussen TP, Jaenisch R. Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat Genet. 2002;30: 167–174. doi: 10.1038/ng820 11780141

52. Nesterova TB, Slobodyanyuk SY, Elisaphenko EA, Shevchenko AI, Johnston C, Pavlova ME, et al. Characterization of the genomic Xist locus in rodents reveals conservation of overall gene structure and tandem repeats but rapid evolution of unique sequence. Genome Res. 2001;11: 833–849. doi: 10.1101/gr.174901 11337478

53. Hoki Y, Kimura N, Kanbayashi M, Amakawa Y, Ohhata T, Sasaki H, et al. A proximal conserved repeat in the Xist gene is essential as a genomic element for X-inactivation in mouse. Development. 2009;136: 139–146. doi: 10.1242/dev.026427 19036803

54. Beletskii A-K. Hong Y, Pehrson J, Egholm M, Strauss WM. PNA interference mapping demonstrates functional domains in the noncoding RNA Xist [Internet]. Proceedings of the National Academy of Sciences. 2001. pp. 9215–9220. doi: 10.1073/pnas.161173098 11481485

55. Sarma K, Levasseur P, Aristarkhov A, Lee JT. Locked nucleic acids (LNAs) reveal sequence requirements and kinetics of Xist RNA localization to the X chromosome. Proc Natl Acad Sci U S A. 2010;107: 22196–22201. doi: 10.1073/pnas.1009785107 21135235

56. Yamada N, Hasegawa Y, Yue M, Hamada T, Nakagawa S, Ogawa Y. Xist Exon 7 Contributes to the Stable Localization of Xist RNA on the Inactive X-Chromosome [Internet]. PLoS Genetics. 2015. p. e1005430. doi: 10.1371/journal.pgen.1005430 26244333

57. Sunwoo H, Colognori D, Froberg JE, Jeon Y, Lee JT. Repeat E anchors Xist RNA to the inactive X chromosomal compartment through CDKN1A-interacting protein (CIZ1). Proc Natl Acad Sci U S A. 2017;114: 10654–10659. doi: 10.1073/pnas.1711206114 28923964

58. Ridings-Figueroa R, Stewart ER, Nesterova TB, Coker H, Pintacuda G, Godwin J, et al. The nuclear matrix protein CIZ1 facilitates localization of Xist RNA to the inactive X-chromosome territory. Genes Dev. 2017;31: 876–888. doi: 10.1101/gad.295907.117 28546514

59. Jeon Y, Lee JT. YY1 tethers Xist RNA to the inactive X nucleation center. Cell. 2011;146: 119–133. doi: 10.1016/j.cell.2011.06.026 21729784

60. Colognori D, Sunwoo H, Kriz AJ, Wang C-Y, Lee JT. Xist Deletional Analysis Reveals an Interdependency between Xist RNA and Polycomb Complexes for Spreading along the Inactive X [Internet]. Molecular Cell. 2019. pp. 101–117.e10. doi: 10.1016/j.molcel.2019.01.015 30827740

61. Hasegawa Y, Brockdorff N, Kawano S, Tsutui K, Tsutui K, Nakagawa S. The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Dev Cell. 2010;19: 469–476. doi: 10.1016/j.devcel.2010.08.006 20833368

62. Bousard A, Raposo AC, Zylicz JJ, Picard C, Pires VB, Qi Y, et al. Exploring the role of Polycomb recruitment in Xist-mediated silencing of the X chromosome in ES cells [Internet].

63. Pintacuda G, Wei G, Roustan C, Kirmizitas BA, Solcan N, Cerase A, et al. hnRNPK Recruits PCGF3/5-PRC1 to the Xist RNA B-Repeat to Establish Polycomb-Mediated Chromosomal Silencing. Mol Cell. 2017;68: 955–969.e10. doi: 10.1016/j.molcel.2017.11.013 29220657

64. Almeida M, Pintacuda G, Masui O, Koseki Y, Gdula M, Cerase A, et al. PCGF3/5–PRC1 initiates Polycomb recruitment in X chromosome inactivation [Internet]. Science. 2017. pp. 1081–1084. doi: 10.1126/science.aal2512 28596365

65. Zhao J, Sun BK, Erwin JA, Song J-J, Lee JT. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science. 2008;322: 750–756. doi: 10.1126/science.1163045 18974356

66. de Napoles M, Nesterova T, Brockdorff N. Early loss of Xist RNA expression and inactive X chromosome associated chromatin modification in developing primordial germ cells. PLoS One. 2007;2: e860. doi: 10.1371/journal.pone.0000860 17848991

67. Mak W, Baxter J, Silva J, Newall AE, Otte AP, Brockdorff N. Mitotically stable association of polycomb group proteins eed and enx1 with the inactive x chromosome in trophoblast stem cells. Curr Biol. 2002;12: 1016–1020. doi: 10.1016/s0960-9822(02)00892-8 12123576

68. Plath K, Fang J, Mlynarczyk-Evans SK, Cao R, Worringer KA, Wang H, et al. Role of histone H3 lysine 27 methylation in X inactivation. Science. 2003;300: 131–135. doi: 10.1126/science.1084274 12649488

69. Silva J, Mak W, Zvetkova I, Appanah R, Nesterova TB, Webster Z, et al. Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes. Dev Cell. 2003;4: 481–495. 12689588

70. Wang L, Brown JL, Cao R, Zhang Y, Kassis JA, Jones RS. Hierarchical recruitment of polycomb group silencing complexes. Mol Cell. 2004;14: 637–646. doi: 10.1016/j.molcel.2004.05.009 15175158

71. Fang J, Chen T, Chadwick B, Li E, Zhang Y. Ring1b-mediated H2A ubiquitination associates with inactive X chromosomes and is involved in initiation of X inactivation. J Biol Chem. 2004;279: 52812–52815. doi: 10.1074/jbc.C400493200 15509584

72. Sarma K, Cifuentes-Rojas C, Ergun A, Del Rosario A, Jeon Y, White F, et al. ATRX directs binding of PRC2 to Xist RNA and Polycomb targets. Cell. 2014;159: 869–883. doi: 10.1016/j.cell.2014.10.019 25417162

73. Chu C, Zhang QC, da Rocha ST, Flynn RA, Bharadwaj M, Calabrese JM, et al. Systematic discovery of Xist RNA binding proteins. Cell. 2015;161: 404–416. doi: 10.1016/j.cell.2015.03.025 25843628

74. McHugh CA, Chen C-K, Chow A, Surka CF, Tran C, McDonel P, et al. The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature. 2015;521: 232–236. doi: 10.1038/nature14443 25915022

75. Minajigi A, Froberg J, Wei C, Sunwoo H, Kesner B, Colognori D, et al. Chromosomes. A comprehensive Xist interactome reveals cohesin repulsion and an RNA-directed chromosome conformation. Science. 2015;349. doi: 10.1126/science.aab2276 26089354

76. Moindrot B, Cerase A, Coker H, Masui O, Grijzenhout A, Pintacuda G, et al. A Pooled shRNA Screen Identifies Rbm15, Spen, and Wtap as Factors Required for Xist RNA-Mediated Silencing. Cell Rep. 2015;12: 562–572. doi: 10.1016/j.celrep.2015.06.053 26190105

77. Monfort A, Di Minin G, Postlmayr A, Freimann R, Arieti F, Thore S, et al. Identification of Spen as a Crucial Factor for Xist Function through Forward Genetic Screening in Haploid Embryonic Stem Cells. Cell Rep. 2015;12: 554–561. doi: 10.1016/j.celrep.2015.06.067 26190100

78. Nesterova TB, Wei G, Coker H, Pintacuda G. Systematic Allelic Analysis Defines the Interplay of Key Pathways in X Chromosome Inactivation. bioRxiv. biorxiv.org; 2018; https://www.biorxiv.org/content/10.1101/477232v1.abstract

79. Shi Y, Downes M, Xie W, Kao HY, Ordentlich P, Tsai CC, et al. Sharp, an inducible cofactor that integrates nuclear receptor repression and activation. Genes Dev. 2001;15: 1140–1151. doi: 10.1101/gad.871201 11331609

80. You S-H, Lim H-W, Sun Z, Broache M, Won K-J, Lazar MA. Nuclear receptor co-repressors are required for the histone-deacetylase activity of HDAC3 in vivo. Nat Struct Mol Biol. 2013;20: 182–187. doi: 10.1038/nsmb.2476 23292142

81. Guenther MG, Barak O, Lazar MA. The SMRT and N-CoR corepressors are activating cofactors for histone deacetylase 3. Mol Cell Biol. 2001;21: 6091–6101. doi: 10.1128/MCB.21.18.6091-6101.2001 11509652

82. Mikami S, Kanaba T, Mishima M. Structural insights into the recruitment of SMRT by the co-repressor SHARP under phosphorylative regulation [Internet]. 2013.

83. Żylicz JJ, Bousard A, Žumer K, Dossin F, Mohammad E, da Rocha ST, et al. The Implication of Early Chromatin Changes in X Chromosome Inactivation. Cell. 2019;176: 182–197.e23. doi: 10.1016/j.cell.2018.11.041 30595450

84. Kohlmaier A, Savarese F, Lachner M, Martens J, Jenuwein T, Wutz A. A chromosomal memory triggered by Xist regulates histone methylation in X inactivation. PLoS Biol. 2004;2: E171. doi: 10.1371/journal.pbio.0020171 15252442

85. Schoeftner S, Sengupta AK, Kubicek S, Mechtler K, Spahn L, Koseki H, et al. Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing. EMBO J. 2006;25: 3110–3122. doi: 10.1038/sj.emboj.7601187 16763550

86. Chaumeil J. A novel role for Xist RNA in the formation of a repressive nuclear compartment into which genes are recruited when silenced [Internet]. Genes & Development. 2006. pp. 2223–2237. doi: 10.1101/gad.380906 16912274

87. Kuroda K, Han H, Tani S, Tanigaki K, Tun T, Furukawa T, et al. Regulation of marginal zone B cell development by MINT, a suppressor of Notch/RBP-J signaling pathway. Immunity. 2003;18: 301–312. 12594956

88. Horiuchi K, Kawamura T, Iwanari H, Ohashi R, Naito M, Kodama T, et al. Identification of Wilms’ tumor 1-associating protein complex and its role in alternative splicing and the cell cycle. J Biol Chem. 2013;288: 33292–33302. doi: 10.1074/jbc.M113.500397 24100041

89. Roignant J-Y, Soller M. m 6 A in mRNA: An Ancient Mechanism for Fine-Tuning Gene Expression [Internet]. Trends in Genetics. 2017. pp. 380–390. doi: 10.1016/j.tig.2017.04.003 28499622

90. Zhao BS, Roundtree IA, He C. Post-transcriptional gene regulation by mRNA modifications. Nat Rev Mol Cell Biol. 2017;18: 31–42. doi: 10.1038/nrm.2016.132 27808276

91. Liao S, Sun H, Xu C. YTH Domain: A Family of N6-methyladenosine (m6A) Readers. Genomics Proteomics Bioinformatics. 2018;16: 99–107. doi: 10.1016/j.gpb.2018.04.002 29715522

92. Patil DP, Chen C-K, Pickering BF, Chow A, Jackson C, Guttman M, et al. m6A RNA methylation promotes XIST-mediated transcriptional repression [Internet]. Nature. 2016. pp. 369–373. doi: 10.1038/nature19342 27602518

93. Wang X, Zhao BS, Roundtree IA, Lu Z, Han D, Ma H, et al. N(6)-methyladenosine Modulates Messenger RNA Translation Efficiency. Cell. 2015;161: 1388–1399. doi: 10.1016/j.cell.2015.05.014 26046440

94. Wang X, Lu Z, Gomez A, Hon GC, Yue Y, Han D, et al. N6-methyladenosine-dependent regulation of messenger RNA stability. Nature. 2014;505: 117–120. doi: 10.1038/nature12730 24284625

95. Gruenbaum Y, Margalit A, Goldman RD, Shumaker DK, Wilson KL. The nuclear lamina comes of age. Nat Rev Mol Cell Biol. 2005;6: 21–31. doi: 10.1038/nrm1550 15688064

96. Chen C-K, Blanco M, Jackson C, Aznauryan E, Ollikainen N, Surka C, et al. Xist recruits the X chromosome to the nuclear lamina to enable chromosome-wide silencing. Science. 2016;354: 468–472. doi: 10.1126/science.aae0047 27492478

97. Dyer KA, Canfield TK, Gartler SM. Molecular cytological differentiation of active from inactive X domains in interphase: implications for X chromosome inactivation. Cytogenet Cell Genet. 1989;50: 116–120. doi: 10.1159/000132736 2776476

98. Shultz LD, Lyons BL, Burzenski LM, Gott B, Samuels R, Schweitzer PA, et al. Mutations at the mouse ichthyosis locus are within the lamin B receptor gene: a single gene model for human Pelger—Huet anomaly. Hum Mol Genet. Oxford University Press; 2003;12: 61–69.

99. Cohen TV, Klarmann KD, Sakchaisri K, Cooper JP, Kuhns D, Anver M, et al. The lamin B receptor under transcriptional control of C/EBPε is required for morphological but not functional maturation of neutrophils. Hum Mol Genet. Narnia; 2008;17: 2921–2933.

100. Jonkers I, Monkhorst K, Rentmeester E, Grootegoed JA, Grosveld F, Gribnau J. Xist RNA is confined to the nuclear territory of the silenced X chromosome throughout the cell cycle. Mol Cell Biol. 2008;28: 5583–5594. doi: 10.1128/MCB.02269-07 18625719

101. Clemson CM, McNeil JA, Willard HF, Lawrence JB. XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J Cell Biol. 1996;132: 259–275. doi: 10.1083/jcb.132.3.259 8636206

102. Ng K, Daigle N, Bancaud A, Ohhata T, Humphreys P, Walker R, et al. A system for imaging the regulatory noncoding Xist RNA in living mouse embryonic stem cells. Mol Biol Cell. 2011;22: 2634–2645. doi: 10.1091/mbc.E11-02-0146 21613549

103. Helbig R, Fackelmayer FO. Scaffold attachment factor A (SAF-A) is concentrated in inactive X chromosome territories through its RGG domain. Chromosoma. 2003;112: 173–182. doi: 10.1007/s00412-003-0258-0 14608463

104. Pullirsch D, Hartel R, Kishimoto H, Leeb M, Steiner G, Wutz A. The Trithorax group protein Ash2l and Saf-A are recruited to the inactive X chromosome at the onset of stable X inactivation [Internet]. Development. 2010. pp. 935–943. doi: 10.1242/dev.035956 20150277

105. Smeets D, Markaki Y, Schmid VJ, Kraus F, Tattermusch A, Cerase A, et al. Three-dimensional super-resolution microscopy of the inactive X chromosome territory reveals a collapse of its active nuclear compartment harboring distinct Xist RNA foci [Internet]. Epigenetics & Chromatin. 2014. p. 8. doi: 10.1186/1756-8935-7-8 25057298

106. Kolpa HJ, Fackelmayer FO, Lawrence JB. SAF-A Requirement in Anchoring XIST RNA to Chromatin Varies in Transformed and Primary Cells. Dev Cell. 2016;39: 9–10. doi: 10.1016/j.devcel.2016.09.021 27728783

107. Sakaguchi T, Hasegawa Y, Brockdorff N, Tsutsui K, Tsutsui KM, Sado T, et al. Control of Chromosomal Localization of Xist by hnRNP U Family Molecules. Dev Cell. 2016;39: 11–12. doi: 10.1016/j.devcel.2016.09.022 27728779

108. Warder DE, Keherly MJ. Ciz1, Cip1 interacting zinc finger protein 1 binds the consensus DNA sequence ARYSR(0–2)YYAC. J Biomed Sci. 2003;10: 406–417. doi: 10.1007/bf02256432 12824700

109. Ainscough JF-X, Ainscough JF, Rahman FA, Sercombe H, Sedo A, Gerlach B, et al. C-terminal domains deliver the DNA replication factor Ciz1 to the nuclear matrix [Internet]. Journal of Cell Science. 2006. pp. 115–124.

110. Yildirim E, Kirby JE, Brown DE, Mercier FE, Sadreyev RI, Scadden DT, et al. Xist RNA is a potent suppressor of hematologic cancer in mice. Cell. 2013;152: 727–742. doi: 10.1016/j.cell.2013.01.034 23415223

111. Chow JC, Ciaudo C, Fazzari MJ, Mise N, Servant N, Glass JL, et al. LINE-1 Activity in Facultative Heterochromatin Formation during X Chromosome Inactivation [Internet]. Cell. 2010. pp. 956–969. doi: 10.1016/j.cell.2010.04.042 20550932

112. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions [Internet]. Nature. 2012. pp. 376–380. doi: 10.1038/nature11082 22495300

113. Deng X, Ma W, Ramani V, Hill A, Yang F, Ay F, et al. Bipartite structure of the inactive mouse X chromosome. Genome Biol. 2015;16: 152. doi: 10.1186/s13059-015-0728-8 26248554

114. Rao SSP, Huntley MH, Durand NC, Stamenova EK, Bochkov ID, Robinson JT, et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell. 2014;159: 1665–1680. doi: 10.1016/j.cell.2014.11.021 25497547

115. Giorgetti L, Lajoie BR, Carter AC, Attia M, Zhan Y, Xu J, et al. Structural organization of the inactive X chromosome in the mouse. Nature. 2016;535: 575–579. doi: 10.1038/nature18589 27437574

116. Darrow EM, Huntley MH, Dudchenko O, Stamenova EK, Durand NC, Sun Z, et al. Deletion of DXZ4 on the human inactive X chromosome alters higher-order genome architecture. Proc Natl Acad Sci U S A. 2016;113: E4504–12. doi: 10.1073/pnas.1609643113 27432957

117. Jansz N, Keniry A, Trussart M, Bildsoe H, Beck T, Tonks ID, et al. Smchd1 regulates long-range chromatin interactions on the inactive X chromosome and at Hox clusters. Nat Struct Mol Biol. 2018;25: 766–777. doi: 10.1038/s41594-018-0111-z 30127357

118. Wang C-Y, Jégu T, Chu H-P, Oh HJ, Lee JT. SMCHD1 Merges Chromosome Compartments and Assists Formation of Super-Structures on the Inactive X. Cell. 2018;174: 406–421.e25. doi: 10.1016/j.cell.2018.05.007 29887375

119. Gdula MR, Nesterova TB, Pintacuda G, Godwin J, Zhan Y, Ozadam H, et al. The non-canonical SMC protein SmcHD1 antagonises TAD formation and compartmentalisation on the inactive X chromosome. Nat Commun. 2019;10: 30. doi: 10.1038/s41467-018-07907-2 30604745

120. Blewitt ME, Gendrel A-V, Pang Z, Sparrow DB, Whitelaw N, Craig JM, et al. SmcHD1, containing a structural-maintenance-of-chromosomes hinge domain, has a critical role in X inactivation. Nat Genet. 2008;40: 663–669. doi: 10.1038/ng.142 18425126

121. Gendrel A-V, Apedaile A, Coker H, Termanis A, Zvetkova I, Godwin J, et al. Smchd1-dependent and -independent pathways determine developmental dynamics of CpG island methylation on the inactive X chromosome. Dev Cell. 2012;23: 265–279. doi: 10.1016/j.devcel.2012.06.011 22841499

122. Nozawa R-S, Nagao K, Igami K-T, Shibata S, Shirai N, Nozaki N, et al. Human inactive X chromosome is compacted through a PRC2-independent SMCHD1-HBiX1 pathway. Nat Struct Mol Biol. 2013;20: 566–573. doi: 10.1038/nsmb.2532 23542155

123. Denholtz M, Bonora G, Chronis C, Splinter E, de Laat W, Ernst J, et al. Long-Range Chromatin Contacts in Embryonic Stem Cells Reveal a Role for Pluripotency Factors and Polycomb Proteins in Genome Organization [Internet]. Cell Stem Cell. 2013. pp. 602–616. doi: 10.1016/j.stem.2013.08.013 24035354

124. Kundu S, Ji F, Sunwoo H, Jain G, Lee JT, Sadreyev RI, et al. Polycomb Repressive Complex 1 Generates Discrete Compacted Domains that Change during Differentiation. Mol Cell. 2018;71: 191. doi: 10.1016/j.molcel.2018.06.022 29979966

125. Schoenfelder S, Sugar R, Dimond A, Javierre B-M, Armstrong H, Mifsud B, et al. Polycomb repressive complex PRC1 spatially constrains the mouse embryonic stem cell genome. Nat Genet. 2015;47: 1179–1186. doi: 10.1038/ng.3393 26323060

126. Engreitz JM, Pandya-Jones A, McDonel P, Shishkin A, Sirokman K, Surka C, et al. The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science. 2013;341: 1237973. doi: 10.1126/science.1237973 23828888

127. Fox AH, Nakagawa S, Hirose T, Bond CS. Paraspeckles: Where Long Noncoding RNA Meets Phase Separation [Internet]. Trends in Biochemical Sciences. 2018. pp. 124–135. doi: 10.1016/j.tibs.2017.12.001 29289458

128. Tatavosian R, Kent S, Brown K, Yao T, Duc HN, Huynh TN, et al. Nuclear condensates of the Polycomb protein chromobox 2 (CBX2) assemble through phase separation. J Biol Chem. 2019;294: 1451–1463. doi: 10.1074/jbc.RA118.006620 30514760

129. Naganuma T, Nakagawa S, Tanigawa A, Sasaki YF, Goshima N, Hirose T. Alternative 3′-end processing of long noncoding RNA initiates construction of nuclear paraspeckles [Internet]. The EMBO Journal. 2012. pp. 4020–4034. doi: 10.1038/emboj.2012.251 22960638

130. West JA, Mito M, Kurosaka S, Takumi T, Tanegashima C, Chujo T, et al. Structural, super-resolution microscopy analysis of paraspeckle nuclear body organization [Internet]. The Journal of Cell Biology. 2016. pp. 817–830. doi: 10.1083/jcb.201601071 27646274

131. Vance C, Rogelj B, Hortobágyi T, De Vos KJ, Nishimura AL, Sreedharan J, et al. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science. 2009;323: 1208–1211. doi: 10.1126/science.1165942 19251628

132. Strom AR, Emelyanov AV, Mir M, Fyodorov DV, Darzacq X, Karpen GH. Phase separation drives heterochromatin domain formation. Nature. 2017;547: 241–245. doi: 10.1038/nature22989 28636597

133. Larson AG, Elnatan D, Keenen MM, Trnka MJ, Johnston JB, Burlingame AL, et al. Liquid droplet formation by HP1α suggests a role for phase separation in heterochromatin. Nature. 2017;547: 236–240. doi: 10.1038/nature22822 28636604

134. Loda A, Gribnau JH. X chromosome inactivation: Spreading of silencing. Rotterdam: Erasmus University of Rotterdam; 2016

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2019 Číslo 9
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#