Differentiation-dependent requirement of Tsix long non-coding RNA in imprinted X-chromosome inactivation

Nature Communications

Volumn 5, Issue , 2014, Pages

  Maclary, Emily ^a   Buttigieg, Emily ^a   Hinten, Michael ^a   Gayen, Srimonta ^a   Harris, Clair ^a   Sarkar, Mrinal Kumar ^a   Purushothaman, Sonya ^b   Kalantry, Sundeep ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b EAST CAROLINA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; LONG UNTRANSLATED RNA; TSIX; UNCLASSIFIED DRUG; XIST; TSIX TRANSCRIPT, MOUSE; XIST NON-CODING RNA;

CHROMOSOME; EMBRYO; GENE EXPRESSION; GENETIC VARIATION; GENOME; MAMMAL; RNA;

ALLELE; ANIMAL CELL; ARTICLE; BLASTOCYST; CELL DIFFERENTIATION; CONTROLLED STUDY; ECTODERM; EMBRYO; FEMALE; GENE EXPRESSION; GENE LOCUS; MALE; MOLECULAR IMPRINTING; MOUSE; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WILD TYPE; X CHROMOSOME; X CHROMOSOME INACTIVATION; ANIMAL; CYTOLOGY; EMBRYOLOGY; GENETICS; GENOME IMPRINTING; METABOLISM; STEM CELL; TROPHOBLAST;

ANIMALS; CELL DIFFERENTIATION; FEMALE; GENOMIC IMPRINTING; MALE; MICE; RNA, LONG NONCODING; STEM CELLS; TROPHOBLASTS; X CHROMOSOME; X CHROMOSOME INACTIVATION;

EID: 84903703837     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5209     Document Type: Article

References (59)

1. Morey, C. & Avner, P. The demoiselle of X-inactivation: 50 years old and as trendy and mesmerising as ever. PLoS Genet. 7, e1002212 (2011).
2. Plath, K., Mlynarczyk-Evans, S., Nusinow, D. A. & Panning, B. Xist RNA and the mechanism of X chromoso (Pubitemid 36109190)
3. Lee, J. T. Gracefully ageing at 50, X-chromosome inactivation becomes a paradigm for RNA and chromatin control. Nat. Rev. Mol. Cell Biol. 12, 815-826 (2011).
4. Rastan, S. Non-random X-chromosome inactivation in mouse X-autosome translocation embryos-location of the inactivation centre. J. Embryol. Exp. Morphol. 78, 1-22 (1983). (Pubitemid 14215355)
5. Rastan, S. & Robertson, E. J. X-chromosome deletions in embryo-derived (EK) cell lines associated with lack of X-chromosome inactivation. J. Embryol. Exp. Morphol. 90, 379-388 (1985). (Pubitemid 16149379)
6. Marahrens, Y., Loring, J. & Jaenisch, R. Role of the Xist gene in X chromosome choosing. Cell 92, 657-664 (1998). (Pubitemid 28141514)
7. 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). (Pubitemid 26020194)
8. Payer, B. & Lee, J. T. X chromosome dosage compensation: how mammals keep the balance. Annu. Rev. Genet. 42, 733-772 (2008).
9. Kalantry, S. Recent advances in X-chromosome inactivation. J. Cell Physiol. 226, 1714-1718 (2011).
10. Plath, K. et al. Role of histone H3 lysine 27 methylation in X inactivation. Science 300, 131-135 (2003). (Pubitemid 36423045)
11. Plath, K. et al. Developmentally regulated alterations in Polycomb repressive complex 1 proteins on the inactive X chromosome. J. Cell Biol. 167, 1025-1035 (2004). (Pubitemid 40066619)
12. Silva, J. et al. Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes. Dev. Cell 4, 481-495 (2003). (Pubitemid 36437556)
13. Mak, W. et al. Mitotically stable association of polycomb group proteins eed and enx1 with the inactive x chromosome in trophoblast stem cells. Curr. Biol. 12, 1016-1020 (2002). (Pubitemid 34703333)
14. Lee, J. T. & Lu, N. Targeted mutagenesis of Tsix leads to nonrandom X inactivation. Cell 99, 47-57 (1999). (Pubitemid 29468629)
15. Lee, J. T. Disruption of imprinted X inactivation by parent-of-origin effects at Tsix. Cell 103, 17-27 (2000).
16. Sado, T., Wang, Z., Sasaki, H. & Li, E. Regulation of imprinted X-chromosome inactivation in mice by Tsix. Development 128, 1275-1286 (2001). (Pubitemid 32409650)
17. Sado, T., Hoki, Y. & Sasaki, H. Tsix silences Xist through modification of chromatin structure. Dev. Cell 9, 159-165 (2005). (Pubitemid 40903668)
18. Navarro, P., Pichard, S., Ciaudo, C., Avner, P. & Rougeulle, C. Tsix transcription across the Xist gene alters chromatin conformation without affecting Xist transcription: implications for X-chromosome inactivation. Genes Dev. 19, 1474-1484 (2005). (Pubitemid 41003014)
19. Okamoto, I., Otte, A. P., Allis, C. D., Reinberg, D. & Heard, E. Epigenetic dynamics of imprinted X inactivation during early mouse development. Science 303, 644-649 (2004). (Pubitemid 38141624)
20. Patrat, C. et al. Dynamic changes in paternal X-chromosome activity during imprinted X-chromosome inactivation in mice. Proc. Natl Acad. Sci. USA 106, 5198-5203 (2009).
21. Kalantry, S., Purushothaman, S., Bowen, R. B., Starmer, J. & Magnuson, T. Evidence of Xist RNA-independent initiation of mouse imprinted X-chromosome inactivation. Nature 460, 647-651 (2009).
22. Namekawa, S. H., Payer, B., Huynh, K. D., Jaenisch, R. & Lee, J. T. Two-step imprinted X inactivation: repeat versus genic silencing in the mouse. Mol. Cell Biol. 30, 3187-3205 (2010).
23. Lee, J. T. & Bartolomei, M. S. X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell 152, 1308-1323 (2013).
24. Lyon, M. F. & Rastan, S. Parental source of chromosome imprinting and its relevance for X chromosome inactivation. Differentiation 26, 63-67 (1984). (Pubitemid 14170578)
25. Goto, Y. & Takagi, N. Maternally inherited X chromosome is not inactivated in mouse blastocysts due to parental imprinting. Chromosome Res. 8, 101-109 (2000). (Pubitemid 30182181)
26. Tada, T. et al. Imprint switching for non-random X-chromosome inactivation during mouse oocyte growth. Development 127, 3101-3105 (2000). (Pubitemid 30611902)
27. Kay, G. F., Barton, S. C., Surani, M. A. & Rastan, S. Imprinting and X chromosome counting mechanisms determine Xist expression in early mouse development. Cell 77, 639-650 (1994). (Pubitemid 24175601)
28. Okamoto, I., Tan, S. & Takagi, N. X-chromosome inactivation in XX androgenetic mouse embryos surviving implantation. Development 127, 4137-4145 (2000).
29. Mak, W. et al. Reactivation of the paternal X chromosome in early mouse embryos. Science 303, 666-669 (2004). (Pubitemid 38141631)
30. Williams, L. H., Kalantry, S., Starmer, J. & Magnuson, T. Transcription precedes loss of Xist coating and depletion of H3K27me3 during X-chromosome reprogramming in the mouse inner cell mass. Development 138, 2049-2057 (2011).
31. Hogan, B., Beddington, R., Costantini, F. & Lacy, E. Manipulating the Mouse Embryo (Cold Spring Harbor Press, 1994).
32. Rastan, S. Timing of X-chromosome inactivation in postimplantation mouse embryos. J. Embryol. Exp. Morphol. 71, 11-24 (1982). (Pubitemid 13233115)
33. Sheardown, S. A. et al. Stabilization of Xist RNA mediates initiation of X chromosome inactivation. Cell 91, 99-107 (1997). (Pubitemid 27431316)
34. Payer, B., Lee, J. T. & Namekawa, S. H. X-inactivation and X-reactivation: epigenetic hallmarks of mammalian reproduction and pluripotent stem cells. Hum. Genet. 130, 265-280 (2011).
35. Minkovsky, A., Patel, S. & Plath, K. Concise review: pluripotency and the transcriptional inactivation of the female mammalian X chromosome. Stem Cells 30, 48-54 (2011).
36. Plath, K. & Lowry, W. E. Progress in understanding reprogramming to the induced pluripotent state. Nat. Rev. Genet. 12, 253-265 (2011).
37. Navarro, P. et al. Molecular coupling of Tsix regulation and pluripotency. Nature 468, 457-460 (2010).
38. Navarro, P. et al. A role for non-coding Tsix transcription in partitioning chromatin domains within the mouse X-inactivation centre. Epigenetics Chromatin 2, 8 (2009).
39. Nesterova, T. B. et al. Pluripotency factor binding and Tsix expression act synergistically to repress Xist in undifferentiated embryonic stem cells. Epigenetics Chromatin 4, 17 (2011).
40. Vigneau, S., Augui, S., Navarro, P., Avner, P. & Clerc, P. An essential role for the DXPas34 tandem repeat and Tsix transcription in the counting process of X chromosome inactivation. Proc. Natl Acad. Sci. USA 103, 7390-7395 (2006). (Pubitemid 43727843)
41. Stavropoulos, N., Rowntree, R. K. & Lee, J. T. Identification of developmentally specific enhancers for Tsix in the regulation of X chromosome inactivation. Mol. Cell Biol. 25, 2757-2769 (2005). (Pubitemid 40381638)
42. Cohen, D. E. et al. The DXPas34 repeat regulates random and imprinted X inactivation. Dev. Cell 12, 57-71 (2007). (Pubitemid 46002600)
43. Kalantry, S. et al. The Polycomb group protein Eed protects the inactive X-chromosome from differentiation-induced reactivation. Nat. Cell Biol. 8, 195-202 (2006).
44. Tanaka, S., Kunath, T., Hadjantonakis, A. K., Nagy, A. & Rossant, J. Promotion of trophoblast stem cell proliferation by FGF4. Science 282, 2072-2075 (1998). (Pubitemid 29001261)
45. Kunath, T. et al. Imprinted X-inactivation in extra-embryonic endoderm cell lines from mouse blastocysts. Development 132, 1649-1661 (2005). (Pubitemid 40575865)
46. Schulz, E. G. & Heard, E. Role and control of X chromosome dosage in mammalian development. Curr. Opin. Genet. Dev. 23, 109-115 (2013).
47. Brockdorff, N. Chromosome silencing mechanisms in X-chromosome inactivation: unknown unknowns. Development 138, 5057-5065 (2012).
48. Schoeftner, S. et al. Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing. EMBO J. 25, 3110-3122 (2006). (Pubitemid 44121103)
49. Wang, J. et al. Imprinted X inactivation maintained by a mouse Polycomb group gene. Nat. Genet. 28, 371-375 (2001). (Pubitemid 32702428)
50. Wutz, A., Rasmussen, T. P. & Jaenisch, R. Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat. Genet. 30, 167-174 (2002).
51. Corbel, C., Diabangouaya, P., Gendrel, A. V., Chow, J. C. & Heard, E. Unusual chromatin status and organization of the inactive X chromosome in murine trophoblast giant cells. Development 140, 861-872 (2013).
52. Rastan, S., Kaufman, M. H., Handyside, A. H. & Lyon, M. F. X-chromosome inactivation in extra-embryonic membranes of diploid parthenogenetic mouse embryos demonstrated by differential staining. Nature 288, 172-173 (1980). (Pubitemid 11212605)
53. Hoki, Y. et al. A proximal conserved repeat in the Xist gene is essential as a genomic element for X-inactivation in mouse. Development 136, 139-146 (2009).
54. Barlow, D. P. Genomic imprinting: a mammalian epigenetic discovery model. Annu. Rev. Genet. 45, 379-403 (2011).
55. Kalantry, S. & Magnuson, T. The Polycomb group protein EED is dispensable for the initiation of random X-chromosome inactivation. PLoS Genet. 2, e66 (2006).
56. Navarro, P. et al. Molecular coupling of Xist regulation and pluripotency. Science 321, 1693-1695 (2008).
57. Donohoe, M. E., Silva, S. S., Pinter, S. F., Xu, N. & Lee, J. T. The pluripotency factor Oct4 interacts with Ctcf and also controls X-chromosome pairing and counting. Nature 460, 128-132 (2009).
58. Pfister, S., Steiner, K. A. & Tam, P. P. Gene expression pattern and progression of embryogenesis in the immediate post-implantation period of mouse development. Gene. Expr. Patterns 7, 558-573 (2007). (Pubitemid 46464655)
59. Hadjantonakis, A. K., Gertsenstein, M., Ikawa, M., Okabe, M. & Nagy, A. Non-invasive sexing of preimplantation stage mammalian embryos. Nat. Genet. 19, 220-222 (1998). (Pubitemid 28309329)