Tsix transcription across the Xist gene alters chromatin conformation without affecting Xist transcription: Implications for X-chromosome inactivation

Genes and Development

Volumn 19, Issue 12, 2005, Pages 1474-1484

  Navarro, Pablo ^a   Pichard, Sylvain ^a   Ciaudo, Constance ^a   Avner, Philip ^a   Rougeulle, Claire ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

Antisense transcription; Histone methylation; Noncoding RNAs; Preinitiation complex of transcription; X chromosome inactivation

Indexed keywords

HISTONE H3; RNA POLYMERASE II;

ALLELE; ANIMAL CELL; ARTICLE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONFORMATION; DOWN REGULATION; EMBRYONIC STEM CELL; EPIGENETICS; FEMALE; GENE; GENE ACTIVITY; GENE CONTROL; GENE EXPRESSION; GENE LOCUS; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; GENOME IMPRINTING; INNER CELL MASS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN METHYLATION; TSIX GENE; X CHROMOSOME; X CHROMOSOME INACTIVATION; XIST GENE;

ALLELES; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DOSAGE COMPENSATION, GENETIC; EMBRYONIC DEVELOPMENT; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONES; MALE; MICE; MODELS, GENETIC; MOLECULAR CONFORMATION; RNA, UNTRANSLATED; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 22344451854     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.341105     Document Type: Article

References (49)

1. Bernstein, B.E., Humphrey, E.L., Erlich, R.L., Schneider, R., Bouman, P., Liu, J.S., Kouzarides, T., and Schreiber, S.L. 2002. Methylation of histone H3 Lys 4 in coding regions of active genes. Proc. Natl. Acad. Sci. 99: 8695-8700.
2. Borsani, B., Tonlorenzi, R., Simmler, M.-C., Dandolo, L., Arnaud, D., Capra, V., Grompe, M., Pizzuti, A., Muzni, D., Lawrence, C., et al. 1991. Characterization of a murine gene expressed from the inactive X chromosome. Nature 351: 325-329.
3. Clemson, C.M., McNeil, J.A., Willard, H.F., and Lawrence, J.B. 1996. XIST RNA paints the inactive X chromosome at interphase: Evidence for a novel RNA involved in nuclear/chromosome structure. J. Cell. Biol. 132: 259-275.
4. Debrand, E., Chureau, C., Arnaud, D., Avner, P., and Heard, E. 1999. Functional analysis of the DXPas34 locus, a 3′ regulator of Xist expression. Mol. Cell. Biol. 19: 8513-8525.
5. Fournier, C., Goto, Y., Ballestar, E., Delaval, K., Hever, A.M., Esteller, M., and Feil, R. 2002. Allele-specific histone lysine methylation marks regulatory regions at imprinted mouse genes. EMBO J. 21: 6560-6570.
6. Heard, E. 2004. Recent advances in X-chromosome inactivation. Curr. Opin. Cell Biol. 16: 247-255.
7. Heard, E., Rougeulle, C., Arnaud, D., Avner, P., Allis, C.D., and Spector, D.L. 2001. Methylation of histone H3 at Lys-9 is an early mark on the X chromosome during X inactivation. Cell 107: 727-738.
8. Huynh, K.D. and Lee, J.T. 2003. Inheritance of a pre-inactivated paternal X chromosome in early mouse embryos. Nature 426: 857-862.
9. Johnston, C.M., Nesterova, T.B., Formstone, E.J., Newall, A.E., Duthie, S.M., Sheardown, S.A., and Brockdorff, N. 1998. Developmentally regulated Xist promoter switch mediates initiation of X inactivation. Cell 94: 809-817.
10. Kay, G.F., Barton, S.C., Surani, M.A., and Rastan, S. 1994. Imprinting and X chromosome counting mechanisms determine Xist expression in early mouse development. Cell 77: 639-650.
11. Kimura, H., Tada, M., Hatano, S., Yamazaki, M., Nakatsuji, N., and Tada, T. 2002. Chromatin reprogramming of male somatic cell-derived Xist and Tsix in ES hybrid cells. Cytogenet. Genome Res. 99: 106-114.
12. Kimura, H., Tada, M., Nakatsuji, N., and Tada, T. 2004. Histone code modifications on pluripotential nuclei of reprogrammed somatic cells. Mol. Cell Biol. 24: 5710-5720.
13. Krogan, N.V., Dover, J., Wood, A., Schneider, J., Heidt, J., Boateng, M.A., Dean, K., Ryan, O.W., Golshani, A., Johnston, M., et al. 2003. The Paf1 complex is required for Histone H3 methylation by COMPASS and Dot1p: Linking transcriptional elongation to histone methylation. Mol. Cell 11: 721-729.
14. Lee, J.T. 2000. Disruption of imprinted X inactivation by parent-of-origin effects at Tsix. Cell 103: 17-27.
15. Lee, J.T. and Lu, N. 1999. Targeted mutagenesis of Tsix leads to nonrandom X inactivation. Cell 99: 47-57.
16. Lee, T.I. and Young, R.A. 2000. Transcription of eukaryotic protein-coding genes. Annu. Rev. Genet. 34: 77-137.
17. Lee, J.T., Strauss, W.M., Dausman, J.A., and Jaenisch, R. 1996. A 450 kb transgene displays properties of the mammalian X-inactivation center. Cell 86: 83-94.
18. Lee, J.T., Davidow, L.S., and Warshawsky, D. 1999. Tsix, a gene antisense to Xist at the X-inactivation centre. Nat. Genet. 21: 400-404.
19. Lewis, A., Mitsuya, K., Umlauf, D., Smith, P., Dean, W., Walter, J., Higgins, M., Feil, R., and Reik, W. 2004. Imprinting on distal chromosome 7 in the placenta involves repressive histone methylation independent of DNA methylation. Nat. Genet. 36: 1291-1295.
20. Luikenhuis, S., Wutz, A., and Jaenisch, R. 2001. Antisense transcription through the Xist locus mediates Tsix function in embryonic stem cells. Mol. Cell. Biol. 21: 8512-8520.
21. MacDonald, L.E., Paterson, C.A., and Kay, G.F. 1998. Bisulfite genomic sequencing-derived methylation profile of the Xist gene throughout early mouse development. Genomics 54: 379-386.
22. Mak, W., Baxter, J., Silva, J., Newall, A.E., Otte, A.P., and Brockdorff, N. 2002. Mitotically stable association of polycomb group proteins Eed and Enx1 with the inactive X chromosome in trophoblast stem cells. Curr. Biol. 12: 1016-1020.
23. Mak, W., Nesterova, T.B., de Napoles, M., Appanah, R., Yamanaka, S., Otte, A.P., and Brockdorff, N. 2004. Reactivation of the paternal X chromosome in early mouse embryos. Science 303: 666-669.
24. Marahrens, Y., Panning, B., Dausman, J., Strauss, W., and Jaenisch, R. 1997. Xist-deficient mice are defective in dosage compensation but not spermatogenesis. Genes & Dev. 11: 156-166.
25. Mise, N., Goto, Y., Nakajima, N., and Takagi, N. 1999. Molecular cloning of antisense transcripts of the mouse Xist gene. Biochem. Biophys. Res. Comm. 258: 537-541.
26. Morey, C., Navarro, P., Debrand, E., Avner, P., Rougeulle, C., and Clerc, P. 2004. The region 3′ to Xist mediates X chromosome counting and H3 Lys-4 dimethylation within the Xist gene. EMBO J. 23: 594-604.
27. Ng, H.H., Robert, F., Young, R.A., and Struhl, K. 2003. Targeted recruitment of Set1 histone methylase by elongating pol II provides a localized mark and memory of recent transcriptional activity. Mol. Cell 11: 709-719.
28. Norris, D.P., Patel, D., Kay, G.F., Penny, G.D., Brockdorff, N., Sheardown, S.A., and Rastan, S. 1994. Evidence that random and imprinted Xist expression is controlled by pre-emptive methylation. Cell 77: 41-51.
29. Okamoto, I., Otte, A.P., Allis, C.D., Reinberg, D., and Heard, E. 2004. Epigenetic dynamics of imprinted X inactivation during early mouse development. Science 303: 644-649.
30. Panning, B., Dausman, J., and Jaenisch, R. 1997. X chromosome inactivation is mediated by Xist RNA stabilization. Cell 90: 907-916.
31. Penny, G.D., Kay, G.F., Sheardown, S.A., Rastan, S., Brockdorff, N., Avner, P., and Turner, B.M. 1996. Requirement for Xist in X chromosome inactivation. Nature 379: 131-137.
32. Proudfoot, N. 2000. Connecting transcription to messenger RNA processing. Trends Biochem. Sci. 25: 290-293.
33. Rougeulle, C. and Avner, P. 2003. Controlling X-inactivation in mammals: What does the centre hold? Sem. Cell Dev. Biol. 14: 331-340.
34. -. 2004. The role of antisense transcription in the regulation of X-inactivation. Curr. Top. Dev. Biol. 63: 61-89.
35. Rougeulle, C., Navarro, P., and Avner, P. 2003. Promoter-restricted H3 Lys 4 di-methylation is an epigenetic mark for monoallelic expression. Hum. Mol. Genet. 12: 3343-3348.
36. Rougeulle, C., Chaumeil, J., Sarma, K., Allis, C.D., Reinberg, D., Avner, P., and Heard, E. 2004. Differential histone H3 Lys-9 and Lys-27 methylation profiles on the X chromosome. Mol. Cell. Biol. 24: 5475-5484.
37. Sado, T., Tada, T., and Takagi, N. 1996. Mosaic methylation of Xist gene before chromosome inactivation in undifferentiated female mouse embryonic stem and embryonic germ cells. Dev. Dyn. 205: 421-434.
38. Sado, T., Wang, Z., Sasaki, H., and Li, E. 2001. Regulation of imprinted X-chromosome inactivation in mice by Tsix. Development 128: 1275-1286.
39. Sheardown, S.A., Duthie, S.M., Johnston, C.M., Newall, A.E., Formstone, E.J., Arkell, R.M., Nesterova, T.B., Alghisi, G.C., Rastan, S., and Brockdorff, N. 1997. Stabilization of Xist RNA mediates initiation of X chromosome inactivation. Cell 91: 99-107.
40. Shibata, S. and Lee, J.T. 2003. Characterization and quantitation of differential Tsix transcripts: Implications for Tsix function. Hum. Mol. Genet. 12: 125-136.
41. -. 2004. Tsix transcription- versus RNA-based mechanisms in Xist repression and epigenetic choice. Curr. Biol. 14: 1747-1754.
42. Sims III, R.J., Nishioka, K., and Reinberg, D. 2003. Histone lysine methylation: A signature for chromatin function. Trends Genet. 19: 629-639.
43. Takagi, N. and Sasaki, M. 1975. Preferential inactivation of the paternally derived X chromosome in the extraembryonic membranes of the mouse. Nature 256: 640-642.
44. Tanaka, S., Kunath, T., Hadjantonakis, A.K., Nagy, A., and Rossant, J. 1998. Promotion of trophoblast stem cell proliferation by FGF4. Science 282: 2072-2075.
45. Umlauf, D., Goto, Y., Cao, R., Cerqueira, F., Wagschal, A., Zhang, Y., and Feil, R. 2004. Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes. Nat. Genet. 36: 1296-1300.
46. Verdel, A., Jia, S., Gerber, S., Sugiyama, T., Gygi, S., Grewal, S.I., and Moazed, D. 2004. RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303: 672-676.
47. Vu, T.H., Li, T., and Hoffman, A.R. 2004. Promoter-restricted histone code, not the differentially methylated DNA regions or antisense transcripts, marks the imprinting status of IGF2R in human and mouse. Hum. Mol. Genet. 13: 2233-2245.
48. Wutz, A., Rasmussen, T.P., and Jaenisch, R. 2002. Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat. Genet. 30: 167-174.
49. Xin, Z., Allis, C.D., and Wagstaff, J. 2001. Parent-specific complementary patterns of histone H3 lysine 9 and H3 lysine 4 methylation at the Prader-Willi syndrome imprinting center. Am. J. Hum. Genet. 69: 1389-1394.