Identification of Spen as a crucial factor for Xist function through forward genetic screening in haploid embryonic stem cells

Cell Reports

Volumn 12, Issue 4, 2015, Pages 554-561

  Monfort, Asun ^a   Di Minin, Giulio ^a   Postlmayr, Andreas ^a   Freimann, Remo ^a   Arieti, Fabiana ^b   Thore, Stéphane ^c,d   Wutz, Anton ^a  

^a ETH ZURICH   (Switzerland)

^b MASARYK UNIVERSITY   (Czech Republic)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d INSERM U869   (France)

Author keywords

[No Author keywords available]

Indexed keywords

POLYCOMB GROUP PROTEIN; PROTEIN SPEN; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG; UNTRANSLATED RNA; XIST RNA; EZH2 PROTEIN, MOUSE; LONG UNTRANSLATED RNA; NUCLEAR PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2; SPEN PROTEIN, MOUSE; XIST NON-CODING RNA;

ANIMAL CELL; ARTICLE; CHROMATIN; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; EPIGENETICS; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOCATION; GENE REPRESSION; GENE SILENCING; GENETIC ENGINEERING; GENETIC SCREENING; HAPLOIDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN RNA BINDING; X CHROMOSOME INACTIVATION; ANIMAL; CELL CULTURE; GENETICS; METABOLISM;

ANIMALS; CELLS, CULTURED; EMBRYONIC STEM CELLS; ENHANCER OF ZESTE HOMOLOG 2 PROTEIN; GENE SILENCING; HAPLOIDY; MICE; NUCLEAR PROTEINS; POLYCOMB REPRESSIVE COMPLEX 2; RNA, LONG NONCODING;

EID: 84947018503     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.06.067     Document Type: Article

References (37)

1. Agrelo, R., Souabni, A., Novatchkova, M., Haslinger, C., Leeb, M., Komnenovic, V., Kishimoto, H., Gresh, L., Kohwi-Shigematsu, T., Kenner, L., and Wutz, A. (2009). SATB1 defines the developmental context for gene silencing by Xist in lymphoma and embryonic cells. Dev. Cell 16, 507-516.
2. Arieti, F., Gabus, C., Tambalo, M., Huet, T., Round, A., and Thore, S. (2014). The crystal structure of the Split End protein SHARP adds a new layer of complexity to proteins containing RNA recognition motifs. Nucleic Acids Res. 42, 6742-6752.
3. Blewitt, M.E., Gendrel, A.V., Pang, Z., Sparrow, D.B., Whitelaw, N., Craig, J.M., Apedaile, A.,Hilton, D.J.,Dunwoodie, S.L., Brockdorff, N., et al. (2008).SmcHD1, containing a structural-maintenance-of-chromosomes hinge domain, has a critical role in X inactivation. Nat. Genet. 40, 663-669.
4. Borsani, G., Tonlorenzi, R., Simmler, M.C., Dandolo, L., Arnaud, D., Capra, V., Grompe, M., Pizzuti, A., Muzny, D., Lawrence, C., et al. (1991). Characterization of a murine gene expressed from the inactive X chromosome. Nature 351, 325-329.
5. Brockdorff, N., Ashworth, A., Kay, G.F., Cooper, P., Smith, S., McCabe, V.M., Norris, D.P., Penny, G.D., Patel, D., and Rastan, S. (1991). Conservation of position and exclusive expression of mouse Xist from the inactive X chromosome. Nature 351, 329-331.
6. Brown, C.J., and Willard, H.F. (1994). The human X-inactivation centre is not required for maintenance of X-chromosome inactivation. Nature 368, 154-156.
7. Brown, C.J., Ballabio, A., Rupert, J.L., Lafreniere, R.G., Grompe, M., Tonlorenzi, R., and Willard, H.F. (1991a). A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 349, 38-44.
8. Brown, C.J., Lafreniere, R.G., Powers, V.E., Sebastio, G., Ballabio, A., Pettigrew, A.L., Ledbetter, D.H., Levy, E., Craig, I.W., and Willard, H.F. (1991b). Localization of the X inactivation centre on the human X chromosome in Xq13. Nature 349, 82-84.
9. Carette, J.E., Guimaraes, C.P., Varadarajan, M., Park, A.S., Wuethrich, I., Godarova, A., Kotecki, M., Cochran, B.H., Spooner, E., Ploegh, H.L., and Brummelkamp, T.R. (2009). Haploid genetic screens in human cells identify host factors used by pathogens. Science 326, 1231-1235.
10. Chu, C., Zhang, Q.C., da Rocha, S.T., Flynn, R.A., Bharadwaj, M., Calabrese, J.M., Magnuson, T., Heard, E., and Chang, H.Y. (2015). Systematic discovery of Xist RNA binding proteins. Cell 161, 404-416.
11. Costanzi, C., and Pehrson, J.R. (1998). Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 393, 599-601.
12. Doudna, J.A., and Charpentier, E. (2014). Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346, 1258096.
13. Elling, U., Taubenschmid, J., Wirnsberger, G., O'Malley, R., Demers, S.P., Vanhaelen, Q., Shukalyuk, A.I., Schmauss, G., Schramek, D., Schnuetgen, F., et al. (2011). Forward and reverse genetics through derivation of haploid mouse embryonic stem cells. Cell Stem Cell 9, 563-574.
14. Helbig, R., and Fackelmayer, F.O. (2003). Scaffold attachment factor A (SAF-A) is concentrated in inactive X chromosome territories through its RGG domain. Chromosoma 112, 173-182.
15. Jae, L.T., Raaben, M., Herbert, A.S., Kuehne, A.I., Wirchnianski, A.S., Soh, T.K., Stubbs, S.H., Janssen, H., Damme, M., Saftig, P., et al. (2014). Virus entry. Lassa virus entry requires a trigger-induced receptor switch. Science 344, 1506-1510.
16. Jeon, Y., and Lee, J.T. (2011). YY1 tethers Xist RNA to the inactive X nucleation center. Cell 146, 119-133.
17. Jiang, J., Jing, Y., Cost, G.J., Chiang, J.C., Kolpa, H.J., Cotton, A.M., Carone, D.M., Carone, B.R., Shivak, D.A., Guschin, D.Y., et al. (2013). Translating dosage compensation to trisomy 21. Nature 500, 296-300.
18. Kohlmaier, A., Savarese, F., Lachner, M., Martens, J., Jenuwein, T., and Wutz, A. (2004). A chromosomal memory triggered by Xist regulates histone methylation in X inactivation. PLoS Biol. 2, E171.
19. Koike-Yusa, H., Li, Y., Tan, E.P., Velasco-Herrera, Mdel.C., and Yusa, K. (2014). Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library. Nat. Biotechnol. 32, 267-273.
20. Kuroda, K., Han, H., Tani, S., Tanigaki, K., Tun, T., Furukawa, T., Taniguchi, Y., Kurooka, H., Hamada, Y., Toyokuni, S., and Honjo, T. (2003). Regulation of marginal zone B cell development by MINT, a suppressor of Notch/RBP-J signaling pathway. Immunity 18, 301-312.
21. 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.
22. Leeb, M., and Wutz, A. (2011). Derivation of haploid embryonic stem cells from mouse embryos. Nature 479, 131-134.
23. Leeb, M., Dietmann, S., Paramor, M., Niwa, H., and Smith, A. (2014). Genetic exploration of the exit from self-renewal using haploid embryonic stem cells. Cell Stem Cell 14, 385-393.
24. Lyon, M.F. (1961). Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190, 372-373.
25. Makhlouf, M., Ouimette, J.F., Oldfield, A., Navarro, P., Neuillet, D., and Rougeulle, C. (2014). A prominent and conserved role for YY1 in Xist transcriptional activation. Nat. Commun. 5, 4878.
26. 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.
27. McHugh, C.A., Chen, C.K., Chow, A., Surka, C.F., Tran, C., McDonel, P., Pandya- Jones, A., Blanco, M., Burghard, C., Moradian, A., et al. (2015). The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature 521, 232-236.
28. Nechanitzky, R., Dávila, A., Savarese, F., Fietze, S., and Grosschedl, R. (2012). Satb1 and Satb2 are dispensable for X chromosome inactivation in mice. Dev. Cell 23, 866-871.
29. Penny, G.D., Kay, G.F., Sheardown, S.A., Rastan, S., and Brockdorff, N. (1996). Requirement for Xist in X chromosome inactivation. Nature 379, 131-137.
30. Pullirsch, D., Härtel, R., Kishimoto, H., Leeb, M., Steiner, G., and Wutz, A. (2010). The Trithorax group protein Ash2l and Saf-A are recruited to the inactive X chromosome at the onset of stable X inactivation. Development 137, 935-943.
31. Savarese, F., Flahndorfer, K., Jaenisch, R., Busslinger, M., and Wutz, A. (2006). Hematopoietic precursor cells transiently reestablish permissiveness for X inactivation. Mol. Cell. Biol. 26, 7167-7177.
32. Shi, Y., Downes, M., Xie, W., Kao, H.Y., Ordentlich, P., Tsai, C.C., Hon, M., and Evans, R.M. (2001). Sharp, an inducible cofactor that integrates nuclear receptor repression and activation. Genes Dev. 15, 1140-1151.
33. Wang, J., Mager, J., Chen, Y., Schneider, E., Cross, J.C., Nagy, A., and Magnuson, T. (2001). Imprinted X inactivation maintained by a mouse Polycomb group gene. Nat. Genet. 28, 371-375.
34. Wutz, A., and Jaenisch, R. (2000). A shift from reversible to irreversible X inactivation is triggered during ES cell differentiation. Mol. Cell 5, 695-705.
35. 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.
36. Yabe, D., Fukuda, H., Aoki, M., Yamada, S., Takebayashi, S., Shinkura, R., Yamamoto, N., and Honjo, T. (2007). Generation of a conditional knockout allele for mammalian Spen protein Mint/SHARP. Genesis 45, 300-306.
37. Yildirim, E., Kirby, J.E., Brown, D.E., Mercier, F.E., Sadreyev, R.I., Scadden, D.T., and Lee, J.T. (2013). Xist RNA is a potent suppressor of hematologic cancer in mice. Cell 152, 727-742.