NIPP1 maintains EZH2 phosphorylation and promoter occupancy at proliferation-related target genes

Nucleic Acids Research

Volumn 41, Issue 2, 2013, Pages 842-854

  Minnebo, Nikki ^a   Görnemann, Janina ^a   O'Connell, Nichole ^b   Van Dessel, Nele ^a   Derua, Rita ^a   Vermunt, Marit Willemijn ^c   Page, Rebecca ^c   Beullens, Monique ^a   Peti, Wolfgang ^c,d   Van Eynde, Aleyde ^a   Bollen, Mathieu ^a  

^a LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

^b BROWN UNIVERSITY   (United States)

^c BROWN UNIVERSITY   (United States)

^d BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE; FORKHEAD TRANSCRIPTION FACTOR; MUTANT PROTEIN; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN NIPP1; THREONINE; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG;

ARTICLE; CELL CULTURE; CELL PROLIFERATION; CONTROLLED STUDY; DEPHOSPHORYLATION; GENE LOCUS; GENE TARGETING; GENETIC ASSOCIATION; HELA CELL; HISTONE MODIFICATION; HUMAN; HUMAN CELL; HYPOPHOSPHORYLATION; MOLECULAR DOCKING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; CELL PROLIFERATION; ENDORIBONUCLEASES; HEK293 CELLS; HELA CELLS; HUMANS; MICE; MODELS, MOLECULAR; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; POLYCOMB REPRESSIVE COMPLEX 2; PROMOTER REGIONS, GENETIC; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN PHOSPHATASE 1; RNA-BINDING PROTEINS; THREONINE;

EID: 84875446516     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1255     Document Type: Article

References (41)

1. Margueron, R. and Reinberg, D. (2011) The Polycomb complex PRC2 and its mark in life. Nature, 469, 343-349.
2. Bracken, A.P. and Helin, K. (2009) Polycomb group proteins: navigators of lineage pathways led astray in cancer. Nat. Rev. Cancer, 9, 773-784.
3. Sparmann, A. and van, L.M. (2006) Polycomb silencers control cell fate, development and cancer. Nat. Rev. Cancer, 6, 846-856. (Pubitemid 44629896)
4. Cha, T.L., Zhou, B.P., Xia, W., Wu, Y., Yang, C.C., Chen, C.T., Ping, B., Otte, A.P. and Hung, M.C. (2005) Akt-mediated phosphorylation of EZH2 suppresses methylation of lysine 27 in histone H3. Science, 310, 306-310. (Pubitemid 41457195)
5. Palacios, D., Mozzetta, C., Consalvi, S., Caretti, G., Saccone, V., Proserpio, V., Marquez, V.E., Valente, S., Mai, A., Forcales, S.V. et al. (2010) TNF/p38alpha/polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration. Cell Stem Cell, 7, 455-469.
6. Wu, S.C. and Zhang, Y. (2011) Cyclin-dependent kinase 1 (CDK1)-mediated phosphorylation of enhancer of zeste 2 (Ezh2) regulates its stability. J. Biol. Chem., 286, 28511-28519.
7. Chen, S., Bohrer, L.R., Rai, A.N., Pan, Y., Gan, L., Zhou, X., Bagchi, A., Simon, J.A. and Huang, H. (2010) Cyclin-dependent kinases regulate epigenetic gene silencing through phosphorylation of EZH2. Nat. Cell Biol., 12, 1108-1114.
8. Kaneko, S., Li, G., Son, J., Xu, C.F., Margueron, R., Neubert, T.A. and Reinberg, D. (2010) Phosphorylation of the PRC2 component Ezh2 is cell cycle-regulated and up-regulates its binding to ncRNA. Genes Dev., 24, 2615-2620.
9. Wei, Y., Chen, Y.H., Li, L.Y., Lang, J., Yeh, S.P., Shi, B., Yang, C.C., Yang, J.Y., Lin, C.Y., Lai, C.C. et al. (2011) CDK1-dependent phosphorylation of EZH2 suppresses methylation of H3K27 and promotes osteogenic differentiation of human mesenchymal stem cells. Nat. Cell Biol., 13, 87-94.
10. Van Dessel, N., Beke, L., Gornemann, J., Minnebo, N., Beullens, M., Tanuma, N., Shima, H., Van Eynde, A. and Bollen, M. (2010) The phosphatase interactor NIPP1 regulates the occupancy of the histone methyltransferase EZH2 at Polycomb targets. Nucleic Acids Res., 38, 7500-7512.
11. Nuytten, M., Beke, L., Van Eynde, A., Ceulemans, H., Beullens, M., Van Humelen, P., Fuks, F. and Bollen, M. (2008) The transcriptional repressor NIPP1 is an essential player in EZH2-mediated gene silencing. Oncogene, 27, 1449-1460. (Pubitemid 351317463)
12. Roy, N., Van Eynde, A., Beke, L., Nuytten, M. and Bollen, M. (2007) The transcriptional repression by NIPP1 is mediated by Polycomb group proteins. Biochim. Biophys. Acta, 1769, 541-545. (Pubitemid 47411592)
13. Jin, Q., Van Eynde, A., Beullens, M., Roy, N., Thiel, G., Stalmans, W. and Bollen, M. (2003) The protein phosphatase-1 (PP1) regulator, nuclear inhibitor of PP1 (NIPP1), interacts with the polycomb group protein, embryonic ectoderm development (EED), and functions as a transcriptional repressor. J. Biol. Chem., 278, 30677-30685. (Pubitemid 36994573)
14. Van Eynde, A., Nuytten, M., Dewerchin, M., Schoonjans, L., Keppens, S., Beullens, M., Moons, L., Carmeliet, P., Stalmans, W. and Bollen, M. (2004) The nuclear scaffold protein NIPP1 is essential for early embryonic development and cell proliferation. Mol. Cell Biol., 24, 5863-5874. (Pubitemid 38787971)
15. Martin-Granados, C., Prescott, A.R., Van Dessel, N., Van Eynde, A., Arocena, M., Klaska, I., Goernemann, J., Beullens, M., Bollen, M. et al. (2012) A role for PP1/NIPP1 in steering migration of human cancer cells. PLoS One, 7, e40769.
16. Ibrahimi, A., Vande, V.G., Reumers, V., Toelen, J., Thiry, I., Vandeputte, C., Vets, S., Deroose, C., Bormans, G., Baekelandt, V. et al. (2009) Highly efficient multicistronic lentiviral vectors with peptide 2A sequences. Hum. Gene Ther., 20, 845-860.
17. Jagiello, I., Van Eynde, A., Vulsteke, V., Beullens, M., Boudrez, A., Keppens, S., Stalmans, W. and Bollen, M. (2000) Nuclear and subnuclear targeting sequences of the protein phosphatase-1 regulator NIPP1. J. Cell Sci., 113(Pt 21), 3761-3768.
18. Chng, K.R., Chang, C.W., Tan, S.K., Yang, C., Hong, S.Z., Sng, N.Y. and Cheung, E. (2012) A transcriptional repressor co-regulatory network governing androgen response in prostate cancers. EMBO J., 31, 2810-2823.
19. Pasini, D., Bracken, A.P., Jensen, M.R., Lazzerini, D.E. and Helin, K. (2004) Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. EMBO J., 23, 4061-4071. (Pubitemid 39472427)
20. DeGuzman, A. and Lee, E.Y. (1988) Preparation of low-molecular-weight forms of rabbit muscle protein phosphatase. Methods Enzymol., 159, 356-368.
21. Brown, N.R., Noble, M.E., Endicott, J.A. and Johnson, L.N. (1999) The structural basis for specificity of substrate and recruitment peptides for cyclin-dependent kinases. Nat. Cell Biol., 1, 438-443. (Pubitemid 129502811)
22. Liu, T., Ortiz, J.A., Taing, L., Meyer, C.A., Lee, B., Zhang, Y., Shin, H., Wong, S.S., Ma, J., Lei, Y. et al. (2011) Cistrome: an integrative platform for transcriptional regulation studies. Genome Biol., 12, R83.
23. Bernstein, B.E., Kamal, M., Lindblad-Toh, K., Bekiranov, S., Bailey, D.K., Huebert, D.J., McMahon, S., Karlsson, E.K., Kulbokas, E.J. III, Gingeras, T.R. et al. (2005) Genomic maps and comparative analysis of histone modifications in human and mouse. Cell, 120, 169-181. (Pubitemid 40174761)
24. 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.
25. Ernst, J., Kheradpour, P., Mikkelsen, T.S., Shoresh, N., Ward, L.D., Epstein, C.B., Zhang, X., Wang, L., Issner, R., Coyne, M. et al. (2011) Mapping and analysis of chromatin state dynamics in nine human cell types. Nature, 473, 43-49.
26. Kumeta, H., Ogura, K., Adachi, S., Fujioka, Y., Tanuma, N., Kikuchi, K. and Inagaki, F. (2008) The NMR structure of the NIPP1 FHA domain. J. Biomol. NMR, 40, 219-224.
27. Boudrez, A., Beullens, M., Groenen, P., Van Eynde, A., Vulsteke, V., Jagiello, I., Murray, M., Krainer, A.R., Stalmans, W. and Bollen, M. (2000) NIPP1-mediated interaction of protein phosphatase-1 with CDC5L, a regulator of pre-mRNA splicing and mitotic entry. J. Biol. Chem., 275, 25411-25417.
28. Qian, J., Lesage, B., Beullens, M., Van Eynde, A. and Bollen, M. (2011) PP1/Repo-man dephosphorylates mitotic histone H3 at T3 and regulates chromosomal aurora B targeting. Curr. Biol., 21, 766-773.
29. Vogel, M.J., Peric-Hupkes, D. and van, S.B. (2007) Detection of in vivo protein-DNA interactions using DamID in mammalian cells. Nat. Protoc., 2, 1467-1478. (Pubitemid 46952325)
30. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S. et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA, 102, 15545-15550. (Pubitemid 41528093)
31. Mootha, V.K., Lindgren, C.M., Eriksson, K.F., Subramanian, A., Sihag, S., Lehar, J., Puigserver, P., Carlsson, E., Ridderstrale, M., Laurila, E. et al. (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet., 34, 267-273. (Pubitemid 36792858)
32. Ben-Porath, I., Thomson, M.W., Carey, V.J., Ge, R., Bell, G.W., Regev, A. and Weinberg, R.A. (2008) An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat. Genet., 40, 499-507. (Pubitemid 351601215)
33. 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. (Pubitemid 44313811)
34. Byeon, I.J., Li, H., Song, H., Gronenborn, A.M. and Tsai, M.D. (2005) Sequential phosphorylation and multisite interactions characterize specific target recognition by the FHA domain of Ki67. Nat. Struct. Mol. Biol., 12, 987-993.
35. Margueron, R., Li, G., Sarma, K., Blais, A., Zavadil, J., Woodcock, C.L., Dynlacht, B.D. and Reinberg, D. (2008) Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mol. Cell, 32, 503-518.
36. Mousavi, K., Zare, H., Wang, A.H. and Sartorelli, V. (2012) Polycomb protein Ezh1 promotes RNA polymerase II elongation. Mol. Cell, 45, 255-262.
37. Ma, H.T. and Poon, R.Y. (2011) How protein kinases co-ordinate mitosis in animal cells. Biochem. J., 435, 17-31.
38. Beullens, M., Van Eynde, A., Vulsteke, V., Connor, J., Shenolikar, S., Stalmans, W. and Bollen, M. (1999) Molecular determinants of nuclear protein phosphatase-1 regulation by NIPP-1. J. Biol. Chem., 274, 14053-14061.
39. Beullens, M., Vulsteke, V., Van Eynde, A., Jagiello, I., Stalmans, W. and Bollen, M. (2000) The C-terminus of NIPP1 (nuclear inhibitor of protein phosphatase-1) contains a novel binding site for protein phosphatase-1 that is controlled by tyrosine phosphorylation and RNA binding. Biochem. J., 352(Pt 3), 651-658. (Pubitemid 32015019)
40. O'Connell, N., Nichols, S.R., Heroes, E., Beullens, M., Bollen, M., Peti, W. and Page, R. (2012) The Molecular Basis for Substrate Specificity of the Nuclear NIPP1:PP1 Holoenzyme. Structure, 20, 1746-1756.
41. Crooks, G.E., Hon, G., Chandonia, J.M. and Brenner, S.E. (2004) WebLogo: a sequence logo generator. Genome Res., 14, 1188-1190. (Pubitemid 38811555)