The long noncoding RNA Gm15055 represses Hoxa gene expression by recruiting PRC2 to the gene cluster

Nucleic Acids Research

Volumn 44, Issue 6, 2015, Pages 2613-2627

  Liu, Guo You ^a   Zhao, Guang Nian ^a   Chen, Xiao Feng ^a   Hao, De Long ^a   Zhao, Xiang ^a   Lv, Xiang ^a   Liu, De Pei ^a  

^a PEKING UNION MEDICAL COLLEGE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; LONG UNTRANSLATED RNA; OCTAMER TRANSCRIPTION FACTOR 4; POLYCOMB REPRESSIVE COMPLEX 2; RNA; CHROMATIN; HISTONE; HOMEODOMAIN PROTEIN; HOXA PROTEIN; POU5F1 PROTEIN, MOUSE; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CHROMOSOME ANALYSIS; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; GENE; GENE ACTIVATION; GENE CLUSTER; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOCUS; GENE REPRESSION; GENE SILENCING; GM15055 GENE; HISTONE METHYLATION; HOXA GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY SEQUENCE; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CHEMISTRY; CHROMATIN; CYTOLOGY; GENETICS; METABOLISM; MOUSE EMBRYONIC STEM CELL; MULTIGENE FAMILY; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; CHROMATIN; GENE EXPRESSION REGULATION; HISTONES; HOMEODOMAIN PROTEINS; MICE; MOUSE EMBRYONIC STEM CELLS; MULTIGENE FAMILY; OCTAMER TRANSCRIPTION FACTOR-3; POLYCOMB REPRESSIVE COMPLEX 2; PROMOTER REGIONS, GENETIC; RNA, LONG NONCODING; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84963829073     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1315     Document Type: Article

References (48)

1. Bernstein, B.E., Mikkelsen, T.S., Xie, X., Kamal, M., Huebert, D.J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K., et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell, 125, 315-326.
2. Noordermeer, D., Leleu, M., Schorderet, P., Joye, E., Chabaud, F. and Duboule, D. (2014) Temporal dynamics and developmental memory of 3D chromatin architecture at Hox gene loci. Elife, 3, e02557.
3. Soshnikova, N. and Duboule, D. (2009) Epigenetic temporal control of mouse Hox genes in vivo. Science, 324, 1320-1323.
4. Noordermeer, D., Leleu, M., Splinter, E., Rougemont, J., De Laat, W. and Duboule, D. (2011) The dynamic architecture of Hox gene clusters. Science, 334, 222-225.
5. Boyer, L.A., Plath, K., Zeitlinger, J., Brambrink, T., Medeiros, L.A., Lee, T.I., Levine, S.S., Wernig, M., Tajonar, A., Ray, M.K., et al. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature, 441, 349-353.
6. Lee, T.I., Jenner, R.G., Boyer, L.A., Guenther, M.G., Levine, S.S., Kumar, R.M., Chevalier, B., Johnstone, S.E., Cole, M.F., Isono, K., et al. (2006) Control of developmental regulators by Polycomb in human embryonic stem cells. Cell, 125, 301-313.
7. Brockdorff, N. (2013) Noncoding RNA and Polycomb recruitment. RNA, 19, 429-442.
8. Zhao, J., Sun, B.K., Erwin, J.A., Song, J.J. and Lee, J.T. (2008) Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science, 322, 750-756.
9. Pandey, R.R., Mondal, T., Mohammad, F., Enroth, S., Redrup, L., Komorowski, J., Nagano, T., Mancini-Dinardo, D. and Kanduri, C. (2008) Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol. Cell, 32, 232-246.
10. Rinn, J.L., Kertesz, M., Wang, J.K., Squazzo, S.L., Xu, X., Brugmann, S.A., Goodnough, L.H., Helms, J.A., Farnham, P.J., Segal, E., et al. (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell, 129, 1311-1323.
11. Tsai, M.C., Manor, O., Wan, Y., Mosammaparast, N., Wang, J.K., Lan, F., Shi, Y., Segal, E. and Chang, H.Y. (2010) Long noncoding RNA as modular scaffold of histone modification complexes. Science, 329, 689-693.
12. Li, L., Liu, B., Wapinski, O.L., Tsai, M.C., Qu, K., Zhang, J., Carlson, J.C., Lin, M., Fang, F., Gupta, R.A., et al. (2013) Targeted Disruption of Hotair Leads to Homeotic Transformation and Gene Derepression. Cell Rep., 5, 3-12.
13. Bhan, A. and Mandal, S.S. (2015) LncRNA HOTAIR: a master regulator of chromatin dynamics and cancer. Biochim. Biophys. Acta, 1856, 151-164.
14. Batista, P.J. and Chang, H.Y. (2013) Long noncoding RNAs: cellular address codes in development and disease. Cell, 152, 1298-1307.
15. Zhao, J., Ohsumi, T.K., Kung, J.T., Ogawa, Y., Grau, D.J., Sarma, K., Song, J.J., Kingston, R.E., Borowsky, M. and Lee, J.T. (2010) Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol. Cell, 40, 939-953.
16. Guttman, M., Amit, I., Garber, M., French, C., Lin, M.F., Feldser, D., Huarte, M., Zuk, O., Carey, B.W., Cassady, J.P., et al. (2009) Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature, 458, 223-227.
17. Guttman, M., Garber, M., Levin, J.Z., Donaghey, J., Robinson, J., Adiconis, X., Fan, L., Koziol, M.J., Gnirke, A., Nusbaum, C., et al. (2010) Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat. Biotechnol., 28, 503-510.
18. Maamar, H., Cabili, M.N., Rinn, J. and Raj, A. (2013) linc-HOXA1 is a noncoding RNA that represses Hoxa1 transcription in cis. Genes Dev., 27, 1260-1271.
19. Sauvageau, M., Goff, L.A., Lodato, S., Bonev, B., Groff, A.F., Gerhardinger, C., Sanchez-Gomez, D.B., Hacisuleyman, E., Li, E., Spence, M., et al. (2013) Multiple knockout mouse models reveal lincRNAs are required for life and brain development. Elife, 2, e01749.
20. Moffat, J., Grueneberg, D.A., Yang, X., Kim, S.Y., Kloepfer, A.M., Hinkle, G., Piqani, B., Eisenhaure, T.M., Luo, B., Grenier, J.K., et al. (2006) A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell, 124, 1283-1298.
21. Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Wu, X., Jiang, W., Marraffini, L.A., et al. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science, 339, 819-823.
22. Wang, K.C., Yang, Y.W., Liu, B., Sanyal, A., Corces-Zimmerman, R., Chen, Y., Lajoie, B.R., Protacio, A., Flynn, R.A., Gupta, R.A., et al. (2011) A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature, 472, 120-124.
23. Xu, M., Zhao, G.N., Lv, X., Liu, G., Wang, L.Y., Hao, D.L., Wang, J., Liu, D.P. and Liang, C.C. (2014) CTCF controls HOXA cluster silencing and mediates PRC2-repressive higher-order chromatin structure in NT2/D1 cells. Mol. Cell. Biol., 34, 3867-3879.
24. Naumova, N., Smith, E.M., Zhan, Y. and Dekker, J. (2012) Analysis of long-range chromatin interactions using Chromosome Conformation Capture. Methods, 58, 192-203.
25. Whyte, W.A., Orlando, D.A., Hnisz, D., Abraham, B.J., Lin, C.Y., Kagey, M.H., Rahl, P.B., Lee, T.I. and Young, R.A. (2013) Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell, 153, 307-319.
26. Buecker, C., Srinivasan, R., Wu, Z., Calo, E., Acampora, D., Faial, T., Simeone, A., Tan, M., Swigut, T. and Wysocka, J. (2014) Reorganization of enhancer patterns in transition from naive to primed pluripotency. Cell Stem Cell, 14, 838-853.
27. Niwa, H., Miyazaki, J. and Smith, A.G. (2000) Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet., 24, 372-376.
28. Grant, C.E., Bailey, T.L. and Noble, W.S. (2011) FIMO: scanning for occurrences of a given motif. Bioinformatics, 27, 1017-1018.
29. Yin, Y., Yan, P., Lu, J., Song, G., Zhu, Y., Li, Z., Zhao, Y., Shen, B., Huang, X., Zhu, H., et al. (2015) Opposing Roles for the lncRNA Haunt and Its Genomic Locus in Regulating HOXA Gene Activation during Embryonic Stem Cell Differentiation. Cell Stem Cell, 16, 504-516.
30. Rosenbloom, K.R., Sloan, C.A., Malladi, V.S., Dreszer, T.R., Learned, K., Kirkup, V.M., Wong, M.C., Maddren, M., Fang, R., Heitner, S.G., et al. (2013) ENCODE data in the UCSC Genome Browser: year 5 update. Nucleic Acids Res., 41, D56-D63.
31. Engreitz, J.M., Pandya-Jones, A., McDonel, P., Shishkin, A., Sirokman, K., Surka, C., Kadri, S., Xing, J., Goren, A., Lander, E.S., et al. (2013) The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science, 341, 1237973.
32. Hsu, P.D., Scott, D.A., Weinstein, J.A., Ran, F.A., Konermann, S., Agarwala, V., Li, Y., Fine, E.J., Wu, X., Shalem, O., et al. (2013) DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol., 31, 827-832.
33. Mathelier, A., Zhao, X., Zhang, A.W., Parcy, F., Worsley-Hunt, R., Arenillas, D.J., Buchman, S., Chen, C.Y., Chou, A., Ienasescu, H., et al. (2014) JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res., 42, D142-D147.
34. Zabidi, M.A., Arnold, C.D., Schernhuber, K., Pagani, M., Rath, M., Frank, O. and Stark, A. (2014) Enhancer-core-promoter specificity separates developmental and housekeeping gene regulation. Nature, 518, 556-559.
35. Boyer, L.A., Lee, T.I., Cole, M.F., Johnstone, S.E., Levine, S.S., Zucker, J.P., Guenther, M.G., Kumar, R.M., Murray, H.L., Jenner, R.G., et al. (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell, 122, 947-956.
36. Ng, H.H. and Surani, M.A. (2011) The transcriptional and signalling networks of pluripotency. Nat. Cell Biol., 13, 490-496.
37. Orkin, S.H. and Hochedlinger, K. (2011) Chromatin connections to pluripotency and cellular reprogramming. Cell, 145, 835-850.
38. Loh, Y.H., Wu, Q., Chew, J.L., Vega, V.B., Zhang, W., Chen, X., Bourque, G., George, J., Leong, B., Liu, J., et al. (2006) The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat. Genet., 38, 431-440.
39. Woo, C.J., Kharchenko, P.V., Daheron, L., Park, P.J. and Kingston, R.E. (2010) A region of the human HOXD cluster that confers polycomb-group responsiveness. Cell, 140, 99-110.
40. Jermann, P., Hoerner, L., Burger, L. and Schubeler, D. (2014) Short sequences can efficiently recruit histone H3 lysine 27 trimethylation in the absence of enhancer activity and DNA methylation. Proc. Natl. Acad. Sci. U.S.A., 111, E3415-E3421.
41. Davidovich, C., Zheng, L., Goodrich, K.J. and Cech, T.R. (2013) Promiscuous RNA binding by Polycomb repressive complex 2. Nat. Struct. Mol. Biol., 20, 1250-1257.
42. Cifuentes-Rojas, C., Hernandez, A.J., Sarma, K. and Lee, J.T. (2014) Regulatory interactions between RNA and polycomb repressive complex 2. Mol. Cell, 55, 171-185.
43. Davidovich, C., Wang, X., Cifuentes-Rojas, C., Goodrich, K.J., Gooding, A.R., Lee, J.T. and Cech, T.R. (2015) Toward a Consensus on the Binding Specificity and Promiscuity of PRC2 for RNA. Mol. Cell, 57, 552-558.
44. Phillips, J.E. and Corces, V.G. (2009) CTCF: master weaver of the genome. Cell, 137, 1194-1211.
45. Bassett, A.R., Akhtar, A., Barlow, D.P., Bird, A.P., Brockdorff, N., Duboule, D., Ephrussi, A., Ferguson-Smith, A.C., Gingeras, T.R., Haerty, W., et al. (2014) Considerations when investigating lncRNA function in vivo. Elife, 3, e03058.
46. Li, L. and Chang, H.Y. (2014) Physiological roles of long noncoding RNAs: insight from knockout mice. Trends Cell Biol., 24, 594-602.
47. Chen, C.Y., Morris, Q. and Mitchell, J.A. (2012) Enhancer identification in mouse embryonic stem cells using integrative modeling of chromatin and genomic features. BMC Genomics, 13, 152.
48. Kagey, M.H., Newman, J.J., Bilodeau, S., Zhan, Y., Orlando, D.A., van Berkum, N.L., Ebmeier, C.C., Goossens, J., Rahl, P.B., Levine, S.S., et al. (2010) Mediator and cohesin connect gene expression and chromatin architecture. Nature, 467, 430-435.