RYBP, a new repressor protein that interacts with components of the mammalian Polycomb complex, and with the transcription factor YY1

EMBO Journal

Volumn 18, Issue 12, 1999, Pages 3404-3418

  Garcia, Emiliano ^a   Marcos Gutiérrez, Camelia ^a,b   Del Mar Lorente, Maria ^a   Moreno, Juan Carlos ^a   Vidal, Miguel ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

M33; Polycomb; Ring1; Transcriptional repression; YY1

Indexed keywords

REPRESSOR PROTEIN; TRANSCRIPTION FACTOR; ZINC FINGER PROTEIN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DROSOPHILA; EMBRYO DEVELOPMENT; GENE REPRESSION; GENETIC TRANSFECTION; HOMEOBOX; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CELL NUCLEUS; CENTRAL NERVOUS SYSTEM; CLONING, MOLECULAR; CYTOPLASM; DNA-BINDING PROTEINS; EMBRYO; ERYTHROID-SPECIFIC DNA-BINDING FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; HUMANS; MICE; MOLECULAR SEQUENCE DATA; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; RNA, MESSENGER; SEQUENCE DELETION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; UBIQUITIN-PROTEIN LIGASES; YEASTS; YY1 TRANSCRIPTION FACTOR; ZINC FINGERS;

EID: 0344223442     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.12.3404     Document Type: Article

References (85)

1. Adler, P.N., Martin, E.C., Charlton, J. and Jones, K. (1991) Phenotypic consequences and genetic interactions of a null mutation in the Drosophila Posterior Sex Combs gene. Dev. Genet., 12, 349-361.
2. Akasaka, T., Kanno, M., Balling, R., Mieza, M.A., Taniguchi, M. and Koseki, H. (1996) A role for mel-18, a Polycomb group-related vertebrate gene, during the anteroposterior specification of the axial skeleton. Development, 122, 1513-1522.
3. Alkema, M.J., van der Lugt, N.M., Bobeldijk, R.C., Berns, A. and van Lohuizen, M. (1995) Transformation of axial skeleton due to overexpression of bmi-1 in transgenic mice. Nature, 374, 724-727.
4. Alkema, M.J., Bronk, M., Verhoeven, E., Otte, A., van't Veer, L.J., Berns, A. and van Lohuizen, M. (1997a) Identification of Bmil-interacting proteins as constituents of a multimeric mammalian polycomb complex. Genes Dev., 11, 226-240.
5. Alkema, M.J., Jacobs, J., Voncken, J.W., Jenkins, N.A., Copeland, N.G., Satijn, D.P., Otte, A.P., Berns, A. and van Lohuizen, M. (1997b) MPc2, a new murine homolog of the Drosophila polycomb protein is a member of the mouse polycomb transcriptional repressor complex. J. Mol. Biol., 273, 993-1003.
6. Bienz, M. and Muller, J. (1995) Transcriptional silencing of homeotic genes in Drosophila. BioEssays, 17, 775-784.
7. Bornemann, D., Miller, E. and Simon, J. (1996) The Drosophila Polycomb group gene Sex comb on midleg (Scm) encodes a zinc finger protein with similarity to polyhomeotic protein. Development, 122, 1621-1630.
8. Brown, J.L., Mucci, D., Whiteley, M., Dirksen, M.L. and Kassis, J.A. (1998) The Drosophila Polycomb group gene pleiohomeotic encodes a DNA binding protein with homology to the transcription factor YY1. Mol. Cell, 1, 1057-1064.
9. Buchenau, P., Hodgson, J., Strutt, H. and Arndt-Jovin, D.J. (1998) The distribution of polycomb-group proteins during cell division and development in Drosophila embryos: impact on models for silencing. J. Cell Biol., 141, 469-481.
10. Bunker, C.A. and Kingston, R.E. (1994) Transcriptional repression by Drosophila and mammalian Polycomb group proteins in transfected mammalian cells. Mol. Cell. Biol., 14, 1721-1732.
11. Busturia, A. and Bienz, M. (1993) Silencers in abdominal-B, a homeotic Drosophila gene. EMBO J., 12, 1415-1425.
12. Chatton, B., Bahr, A., Acker, J. and Kedinger, C. (1995) Eukaryotic GST fusion vector for the study of protein-protein association in vivo: application to interaction of ATFa with Jun and Fos. Biotechniques, 18, 142-145.
13. Cheng, N.N., Sinclair, D.A., Campbell, R.B. and Brock, H.W. (1994) Interactions of polyhomeotic with Polycomb group genes of Drosophila melanogaster. Genetics. 138, 1151-1162.
14. Chiang, A., O'Connor, M.B., Paro, R., Simon, J. and Bender, W. (1995) Discrete Polycomb-binding sites in each parasegmental domain of the bithorax complex. Development, 121, 1681-1689.
15. Cohen, K.J., Hanna, J.S., Prescott, J.E. and Dang, C.V. (1996) Transformation by the Bmi-1 oncoprotein correlates with its subnuclear localization but not its transcriptional suppression activity. Mol. Cell. Biol., 16, 5527-5535.
16. Coré, N., Bel, S., Gaunt, S.J., Aurrand-Lions, M., Pearce, J., Fisher, A. and Djabali, M. (1997) Altered cellular proliferation and mesoderm patterning in Polycomb-M33-deficient mice. Development, 124, 721-729.
17. Coulson, M., Robert, S., Eyre, H.J. and Saint, R. (1998) The identification and localization of a human gene with sequence similarity to Polycomblike of Drosophila melanogaster. Genomics, 48, 381-383.
18. DeCamillis, M., Cheng, N.S., Pierre, D. and Brock, H.W. (1992) The polyhomeotic gene of Drosophila encodes a chromatin protein that shares polytene chromosome-binding sites with Polycomb. Genes Dev., 6, 223-232.
19. Denisenko, O.N. and Bomsztyk, K. (1997) The product of the murine homolog of the Drosophila extra sex comb gene displays transcriptional repressor activity. Mol. Cell. Biol., 17, 4707-4717.
20. Duncan, I.M. (1982) Polycomblike: a gene that appears to be required for the normal expression of the bithorax and antennapedia gene complexes of Drosophila melanogaster. Genetics, 102, 49-70.
21. Evan, G.I., Lewis, G.K., Ramsay, G. and Bishop, J.M. (1985) Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol., 5, 3610-3616.
22. Gindhart, J.G.,Jr and Kaufman, T.C. (1995) Identification of Polycomb and trithorax group responsive elements in the regulatory region of the Drosophila homeotic gene Sex combs reduced. Genetics, 139, 797-814.
23. Goodrich, J. (1998) Plant development: Medea's maternal instinct. Curr. Biol., 8, R480-R484.
24. Green, S., Issemann, I., and Sheer, E. (1988) A versatile in vivo and in vitro eukaryotic expression vector for protein engineering. Nucleic Acids Res., 16, 369.
25. Grossniklaus, U., Vielle-Calzada, J.P., Hoeppner, M.A. and Gagliano, W.B. (1998) Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science, 280, 446-450.
26. Gunning, P., Leavitt, J., Muscat, G., Ng, S.Y. and Kedes, L. (1987) A human β-actin expression vector system directs high-level accumulation of antisense transcripts. Proc. Natl Acad. Sci. USA, 84, 4831-4835.
27. Gunster, M.J., Satijn, D.P., Hamer, K.M., den Blaauwen, J.L., de Bruijn, D., Alkema, M.J., van Lohuizen, M., van Driel, R. and Otte, A.P. (1997) Identification and characterization of interactions between the vertebrate polycomb-group protein BMI1 and human homologs of polyhomeotic. Mol. Cell. Biol., 17, 2326-2335.
28. Hashimoto, N., Brock, H.W., Nomura, M., Kyba, M., Hodgson, J., Fujita, Y., Takihara, Y., Shimada, K. and Higashinakagawa, T. (1998) RAE28, BMI1 and M33 are members of heterogeneous multimeric mammalian Polycomb group complexes. Biochem. Biophys. Res. Commun., 245, 356-365.
29. Hemenway, C.S., Halligan, B.W. and Levy, L.S. (1998) The Bmi-1 oncoprotein interacts with dinG and MPh2: the role of RING finger domains. Oncogene, 16, 2541-2547.
30. Hobert, O., Jallal, B. and Ullrich, A. (1996a) Interaction of Vav with ENX-1, a putative transcriptional regulator of homeobox gene expression. Mol. Cell. Biol., 16, 3066-3073.
31. Hobert, O., Sures, I., Ciossek, T., Fuchs, M. and Ullrich, A. (1996b) Isolation and developmental expression analysis of Enx-1, a novel mouse Polycomb group gene. Mech. Dev., 55, 171-184.
32. Holdeman, R., Nehrt, S. and Strome, S. (1998) MES-2, a maternal protein essential for viability of the germline in Caenorhabditis elegans, is homologous to a Drosophila Polycomb group protein. Development, 125, 2457-2467.
33. Hollenberg, S.M., Sternglanz, R., Cheng, P.F. and Weintraub, H. (1995) Identification of a new family of tissue-specific basic helix-loop-helix proteins with a two-hybrid system. Mol. Cell. Biol., 15, 3813-3822.
34. Ishida, A., Asano, H., Hasegawa, M., Koseki, H., Ono, T., Yoshida, M.C., Taniguchi, M. and Kanno, M. (1993) Cloning and chromosome mapping of the human Mel-18 gene which encodes a DNA-binding protein with a new 'RING-finger' motif. Gene, 129, 249-255.
35. Jürgens, G. (1985) A group of genes controlling the spatial expression of the bithorax complex in Drosophila. Nature, 316, 153-155.
36. Kalenik, J.L., Chen, D., Bradley, M.E., Chen, S.-J. and Lee, T.-C. (1997) Yeast two-hybrid cloning of a novel zinc finger protein that interacts with the multifunctional transcription factor YY1. Nucleic Acids Res., 25, 843-849.
37. Kanno, M., Hasegawa, M., Ishida, A., Isono, K. and Taniguchi, M. (1995) mel-18, a Polycomb group-related mammalian gene, encodes a transcriptional negative regulator with tumor suppressive activity. EMBO J., 14, 5672-5678.
38. Kehle, J., Beuchle, D., Treuheit, S., Christen, B., Kennison, J.A., Bienz, M. and Muller, J. (1998) dMi-2, a hunchback-interacting protein that functions in polycomb repression. Science, 282, 1897-1900.
39. Kennison, J.A. (1995) The Polycomb and trithorax group proteins of Drosophila: trans-regulators of homeotic gene function. Anna. Rev. Genet., 29, 289-303.
40. Korf, I., Fan, Y. and Strome, S. (1998) The Polycomb group in Caenorhabditis elegans and maternal control of germline development. Development, 125, 2469-2478.
41. Kyba, M. and Brock, H.W. (1998a) The Drosophila polycomb group protein Psc contacts ph and Pc through specific conserved domains. Mol. Cell. Biol., 18, 2712-2720.
42. Kyba, M. and Brock, H.W. (1998b) The SAM domain of polyhomeotic, RAE28 and scm mediates specific interactions through conserved residues. Dev. Genet., 22, 74-84.
43. Luckow, B. and Schütz, G. (1987) CAT constructions with multiple unique restriction sites for the functional analysis of eukaryotic promoters and regulatory elements. Nucleic Acids Res., 15, 5490.
44. Martin, E.C. and Adler, P.N. (1993) The Polycomb group gene Posterior Sex Combs encodes a chromosomal protein. Development, 117, 641-655.
45. Mihaly, J., Mishra, R.K. and Karch, F. (1998) A conserved sequence motif in Polycomb-response elements. Mol. Cell, 1, 1065-1066.
46. Niman, H.L., Houghten, R.A., Walker, L.E., Reisfeld, R.A., Wilson, I.A., Hogle, J.M. and Lerner, R.A. (1983) Generation of protein-reactive antibodies by short peptides is an event of high frequency: implication for the structural basis of immune recognition. Proc. Natl Acad. Sci. USA, 80, 4949-4953.
47. Nomura, M., Takihara, Y. and Shimada, K. (1994) Isolation and characterization of retinoic acid-inducible cDNA clones in F9 cells: one of the early inducible clones encodes a novel protein sharing several highly homologous regions with a Drosophila Polyhomeotic protein. Differentiation, 57, 39-50.
48. Orlando, V., Jane, E.P., Chinwalla, V., Harte, P.J. and Paro, R. (1998) Binding of Trithorax and Polycomb proteins to the bithorax complex: dynamic changes during early Drosophila embryogenesis. EMBO J., 17, 5141-5150.
49. Ou, S.K.-H., Hwang, J.M.-C. and Patterson, P.H. (1993) A modified method for obtaining large amounts of high titer polyclonal ascites. J. Immunol. Methods, 165, 75-80.
50. Pearce, J.J., Singh, P.B. and Gaunt, S.J. (1992) The mouse has a Polycomblike chromobox gene. Development. 114, 921-929.
51. Pirrotta, V. (1997) Chromatin-silencing mechanisms in Drosophila maintain patterns of gene expression. Trends Genet., 13, 314-318.
52. Pirrotta, V. (1998) Polycombing the genome: PcG. trxG and chromatin silencing. Cell, 93, 333-336.
53. Pirrotta, V., Chan, C.S., McCabe, D. and Qian, S. (1995) Distinct parasegmental and imaginal enhancers and the establishment of the expression pattern of the Ubx gene. Genetics, 141, 1439-1450.
54. Rastelli, L., Chan, C.S. and Pirrotta, V. (1993) Related chromosome binding sites for zeste, suppressors of zeste and Polycomb group proteins in Drosophila and their dependence on Enhancer of zeste function. EMBO J., 12, 1513-1522.
55. Reijnen, M.J., Hamer, K.M., den Blaauwen, J.L., Lambrechts, C., Schoneveld, I., van Driel, R. and Otte, A.P. (1995) Polycomb and bmi-1 homologs are expressed in overlapping patterns in Xenopus embryos and are able to interact with each other. Mech. Dev., 53, 35-46.
56. Rupp, R.A.W., Snider, L. and Weintraub, H. (1994) Xenopus embryos regulate the nuclear localization of XMyoD. Genes Dev., 8, 1311-1323.
57. Sadowski, I. and Ptashne, M. (1989) A vector for expressing GAL4 (1-147) fusions in mammalian cells. Nucleic Acids Res., 17, 7539.
58. Satijn, D.P. and Otte, A.P. (1999) RING1 interacts with multiple Polycomb-group proteins and displays tumorigenic activity. Mol. Cell. Biol., 19, 57-68.
59. Satijn, D.P. et al. (1997a) RING1 is associated with the polycomb group protein complex and acts as a transcriptional repressor. Mol. Cell. Biol., 17, 4105-4113.
60. Satijn, D.P. et al. (1997b) Interference with the expression of a novel human polycomb protein, hPc2, results in cellular transformation and apoptosis. Mol. Cell. Biol., 17, 6076-6086.
61. Saurin, A.J., Shiels, C., Williamson, J., Satijn, D.P.E., Otte, A.P. Sheer, D. and Freemont, P.S. (1998) The human polycomb group complex associates with pericentromeric heterochromatin to form a novel nuclear domain. J. Cell Biol., 142, 887-898.
62. Schoorlemmer, J., Marcos-Gutierrez, C. Were, F., Martinez, R., Garcia, E., Satijn, D.P., Otte, A.P. and Vidal, M. (1997) Ring1A is a transcriptional repressor that interacts with the Polycomb-M33 protein and is expressed at rhombomere boundaries in the mouse hindbrain. EMBO J., 16, 5930-5942.
63. Sewalt, R.G., van der Vlag, J., Gunster, MJ., Hamer, K.M., den Blaauwen, J.L., Satijn, D.P., Hendrix, T. van Driel, R. and Otte, A.P. (1998) Characterization of interactions between the mammalian polycomb-group proteins Enx1/EZH2 and EED suggests the existence of different mammalian polycomb-group protein complexes. Mol. Cell. Biol., 18, 3586-3595.
64. Sewalt, R.G., Gunster, M.J., van der Vlag, J., Satijn, D.P. and Otte, A.P. (1999) C-terminal binding protein is a transcriptional repressor that interacts with a specific class of vertebrate Polycomb proteins. Mol. Cell. Biol., 19, 777-787.
65. Shi, Y., Seto, E., Chang, L.-S. and Shenk, T. (1991) Transcriptional repression by YY1, a human GLI-Krüppel-related protein and relief of repression by adenovirus E1a protein. Cell, 67, 377-388.
66. Shumacher, A., Faust, C. and Magnuson, T. (1996) Positional cloning of a global regulator of anterior-posterior patterning in mice. Nature, 383, 250-253.
67. Simon, J. (1995) Locking in stable states of gene expression: transcriptional control during Drosophila development. Curr. Opin. Cell Biol., 7, 376-385.
68. Simon, J., Chiang, A., Bender, W., Shimell, M.J. and O'Connor, M. (1993) Elements of the Drosophila bithorax complex that mediate repression by Polycomb group products. Dev. Biol., 158, 131-144.
69. Sinclair, D., Milne, T., Hodgson, J., Shellard, J., Salinas, C., Kyba, M., Randazzo, F. and Brock, H. (1998) The Additional sex combs gene of Drosophila encodes a chromatin protein that binds to shared and unique polycomb group sites on polytene chromosomes. Development, 125, 1207-1216.
70. Soto, M.C., Chou, T.B. and Bender, W. (1995) Comparison of germline mosaics of genes in the Polycomb group of Drosophila melanogaster. Genetics, 140, 231-243.
71. Spanopoulou, E., Zaitseva, F., Wang, F.H., Santagata, S., Baltimore, D. and Panayotou, G. (1996) The homeodomain region of Rag-1 reveals the parallel mechanisms of bacterial and V(D)J recombination. Cell, 87, 263-276.
72. Stankunas, K., Berger, J., Ruse, C., Sinclair, D.A., Randazzo, F. and Brock, H.W. (1998) The Enhancer of Polycomb gene of Drosophila encodes a chromatin protein conserved in yeast and mammals. Development, 125, 4055-4066.
73. Struhl, K. and Akam, M.E. (1985) Altered distributions of Ultrabithorax transcripts in extra sex combs mutant embryos of Drosophila. EMBO J., 4, 3259-3264.
74. Strutt, H. and Paro, R. (1997) The polycomb group protein complex of Drosophila melanogaster has different compositions at different target genes. Mol. Cell. Biol., 17, 6773-6783.
75. Strutt, H., Cavalli, G. and Paro, R. (1997) Co-localization of Polycomb protein and GAGA factor on regulatory elements responsible for the maintenance of homeotic gene expression. EMBO J., 16, 3621-3632.
76. Takihara, Y. et al. (1997) Targeted disruption of the mouse homologue of the Drosophila polyhomeotic gene leads to altered anteroposterior patterning and neural crest defects. Development, 124, 3673-3682.
77. Tetsu, O., Ishihara, H., Kanno, R., Kamiyasu, M., Inoue, H., Tokuhisa, T., Taniguchi, M. and Kanno, M. (1998) mel-18 negatively regulates cell cycle progression upon B cell antigen receptor stimulation through a cascade leading to c-myc/cdc25. Immunity, 9, 439-448.
78. van de Vosse, E. et al. (1998) Characterization of SCML1, a new gene in Xp22, with homology to developmental polycomb genes. Genomics, 49, 96-102.
79. van der Lugt, N.M. et al. (1994) Posterior transformation, neurological abnormalities and severe hematopoietic defects in mice with a targeted deletion of the bmi-1 proto-oncogene. Genes Dev., 8, 757-769.
80. van Lohuizen, M., Frasch, M., Wientjens, E. and Berns, A. (1991) Sequence similarity between the mammalian bmi-1 proto-oncogene and the Drosophila regulatory genes Psc and Su(z)2. Nature, 353, 353-355.
81. van Lohuizen, M., Tijms, M., Voncken, J.W., Schumacher, A., Magnuson, T. and Wientjens, E. (1998) Interaction of mouse polycomb-group (Pc-G) proteins Enx1 and Enx2 with Eed: indication for separate Pc-G complexes. Mol. Cell. Biol., 18, 3572-3579.
82. Vojtek, A.B., Hollenberg, S.M. and Cooper, J.A. (1993) Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell, 74, 205-214.
83. Wedeen, C., Harding, K. and Levine, M. (1986) Spatial regulation of Antennapedia and bithorax gene expression by the Polycomb locus in Drosophila. Cell, 44, 739-748.
84. Wilkinson, D. (1992) Whole mount in situ hybridization of vertebrate embryos. In Wilkinson.D.G. (ed.), In situ Hybridization. IRL Press, Oxford, pp. 75-83.
85. Zink, B. and Paro, R. (1989) In vivo binding pattern of a trans-regulator of homoeotic genes in Drosophila melanogaster. Nature, 337, 468-471.