Ubiquitin-specific proteases 7 and 11 modulate Polycomb regulation of the INK4a tumour suppressor

EMBO Journal

Volumn 29, Issue 15, 2010, Pages 2553-2565

  Maertens, Goedele N ^a,d   El Messaoudi Aubert, Selma ^a,e   Elderkin, Sarah ^b   Hiom, Kevin ^c   Peters, Gordon ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b BABRAHAM INSTITUTE   (United Kingdom)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e INSTITUT PASTEUR   (France)

Author keywords

chromatin; INK4a; Polycomb; transcription; ubiquitination

Indexed keywords

HISTONE H2A; POLYCOMB GROUP PROTEIN; POLYCOMB REPRESSIVE COMPLEX 1; TUMOR SUPPRESSOR PROTEIN; TUMOR SUPPRESSOR PROTEIN INK4A; UBIQUITIN SPECIFIC PROTEASE 11; UBIQUITIN SPECIFIC PROTEASE 7; UNCLASSIFIED DRUG;

ARTICLE; CELL PROLIFERATION; FIBROBLAST; GENE LOCUS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; SENESCENCE; TURNOVER TIME; UBIQUITINATION;

CELL PROLIFERATION; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P16; HISTONES; HUMANS; NUCLEAR PROTEINS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; REPRESSOR PROTEINS; RNA INTERFERENCE; THIOLESTER HYDROLASES; UBIQUITIN THIOLESTERASE; UBIQUITINATION;

EID: 77955419051     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.129     Document Type: Article

References (69)

1. Banito A, Rashid ST, Acosta JC, Li S, Pereira CF, Geti I, Pinho S, Silva JC, Azuara V, Walsh M, Vallier L, Gil J (2009) Senescence impairs successful reprogramming to pluripotent stem cells. Genes Dev 23: 2134-2139
2. Ben-Saadon R, Zaaroor D, Ziv T, Ciechanover A (2006) The polycomb protein Ring1B generates self atypical mixed ubiquitin chains required for its in vitro histone H2A ligase activity. Mol Cell 24: 701-711
3. Bouwmeester T, Bauch A, Ruffner H, Angrand PO, Bergamini G, Croughton K, Cruciat C, Eberhard D, Gagneur J, Ghidelli S, Hopf C, Huhse B, Mangano R, Michon AM, Schirle M, Schlegl J, Schwab M, Stein MA, Bauer A, Casari G et al (2004) A physical and functional map of the human TNF-alpha/NF-kappa B signal transduction pathway. Nat Cell Biol 6: 97-105
4. Bracken AP, Kleine-Kohlbrecher D, Dietrich N, Pasini D, Gargiulo G, Beekman C, Theilgaard-Monch K, Minucci S, Porse BT, Marine JC, Hansen KH, Helin K (2007) The Polycomb group proteins bind throughout the INK4A-ARF locus and are disassociated in senescent cells. Genes Dev 21: 525-530
5. Brookes S, Rowe J, Gutierrez Del Arroyo A, Bond J, Peters G (2004) Contribution of p16(INK4a) to replicative senescence of human fibroblasts. Exp Cell Res 298: 549-559
6. Brookes S, Rowe J, Ruas M, Llanos S, Clark PA, Lomax M, James MC, Vatcheva R, Bates S, Vousden KH, Parry D, Gruis N, Smit N, Bergman W, Peters G (2002) INK4a-deficient human diploid fibroblasts are resistant to RAS-induced senescence. EMBO J 21: 2936-2945
7. Brooks CL, Li M, Hu M, Shi Y, Gu W (2007) The p53\Mdm2\HAUSP complex is involved in p53 stabilization by HAUSP. Oncogene 26: 7262-7266
8. Buchwald G, Van Der Stoop P, Weichenrieder O, Perrakis A, Van Lohuizen M, Sixma TK (2006) Structure and E3-ligase activity of the ring-ring complex of polycomb proteins Bmi1 and Ring1b. EMBO J 25: 2465-2474
9. Cales C, Roman-Trufero M, Pavon L, Serrano I, Melgar T, Endoh M, Perez C, Koseki H, Vidal M (2008) Inactivation of the polycomb group protein Ring1B unveils an antiproliferative role in hematopoietic cell expansion and cooperation with tumorigenesis associated with Ink4a deletion. Mol Cell Biol 28: 1018-1028
10. Campisi J, d'Adda di Fagagna F (2007) Cellular senescence: when bad things happen to good cells. Nat Rev 8: 729-740
11. Cao R, Tsukada Y, Zhang Y (2005) Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol Cell 20: 845-854
12. Cao R, Zhang Y (2004) The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr Opin Genet Dev 14: 155-164
13. Cherepanov P (2007) LEDGF/p75 interacts with divergent lentiviral integrases and modulates their enzymatic activity in vitro. Nucleic Acids Res 35: 113-124
14. Collado M, Blasco MA, Serrano M (2007) Cellular senescence in cancer and aging. Cell 130: 223-233
15. Collado M, Serrano M (2006) The power and the promise of oncogene-induced senescence markers. Nat Rev Cancer 6: 472-476
16. Cummins JM, Rago C, Kohli M, Kinzler KW, Lengauer C, Vogelstein B (2004) Tumour suppression: disruption of HAUSP gene stabilizes p53. Nature 428: 1 p following 486
17. Cummins JM, Vogelstein B (2004) HAUSP is required for p53 destabilization. Cell Cycle 3: 689-692.
18. De Napoles M, Mermoud JE, Wakao R, Tang YA, Endoh M, Appanah R, Nesterova TB, Silva J, Otte AP, Vidal M, Koseki H, Brockdorff N (2004) Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev Cell 7: 663-676
19. Dietrich N, Bracken AP, Trinh E, Schjerling CK, Koseki H, Rappsilber J, Helin K, Hansen KH (2007) Bypass of senescence by the polycomb group protein CBX8 through direct binding to the INK4A-ARF locus. EMBO J 26: 1637-1648
20. Elderkin S, Maertens GN, Endoh M, Mallery DL, Morrice N, Koseki H, Peters G, Brockdorff N, Hiom K (2007) A phosphorylated form of Mel-18 targets the Ring1B histone H2A ubiquitin ligase to chromatin. Mol Cell 28: 107-120
21. El Messaoudi-Aubert S, Nicholls J, Maertens GN, Brookes S, Bernstein E, Peters G (2010) Role for the MOV10 RNA helicase in Polycomb-mediated repression of the INK4a tumor suppressor. Nat Struct Molec Biol (advance online publication 13 June 2010)
22. Everett RD, Meredith M, Orr A, Cross A, Kathoria M, Parkinson J (1997) A novel ubiquitin-specific protease is dynamically associated with the PML nuclear domain and binds to a herpesvirus regulatory protein. EMBO J 16: 1519-1530 (Pubitemid 27151947)
23. Fernandez-Montalvan A, Bouwmeester T, Joberty G, Mader R, Mahnke M, Pierrat B, Schlaeppi JM, Worpenberg S, Gerhartz B (2007) Biochemical characterization of USP7 reveals post-translational modification sites and structural requirements for substrate processing and subcellular localization. FEBS J 274: 4256-4270
24. Gil J, Bernard D, Martinez D, Beach D (2004) Polycomb CBX7 has a unifying role in cellular lifespan. Nat Cell Biol 6: 67-72
25. Gil J, Peters G (2006) Regulation of the INK4b-ARF-INK4a tumour suppressor locus: all for one or one for all. Nat Rev 7: 667-677
26. Hernandez-Munoz I, Lund AH, Van Der Stoop P, Boutsma E, Muijrers I, Verhoeven E, Nusinow DA, Panning B, Marahrens Y, Van Lohuizen M (2005) Stable X chromosome inactivation involves the PRC1 Polycomb complex and requires histone MACROH2A1 and the CULLIN3/SPOP ubiquitin E3 ligase. Proc Natl Acad Sci USA 102: 7635-7640
27. Hong H, Takahashi K, Ichisaka T, Aoi T, Kanagawa O, Nakagawa M, Okita K, Yamanaka S (2009) Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 460: 1132-1135
28. Hussain S, Zhang Y, Galardy PJ (2009) DUBs and cancer: the role of deubiquitinating enzymes as oncogenes, non-oncogenes and tumor suppressors. Cell Cycle 8: 1688-1697
29. Ideguchi H, Ueda A, Tanaka M, Yang J, Tsuji T, Ohno S, Hagiwara E, Aoki A, Ishigatsubo Y (2002) Structural and functional characterization of the USP11 deubiquitinating enzyme, which interacts with the RanGTP-associated protein RanBPM. Biochem J 367 (Part 1): 87-95
30. Isono K, Fujimura Y, Shinga J, Yamaki M, O-Wang J, Takihara Y, Murahashi Y, Takada Y, Mizutani-Koseki Y, Koseki H (2005) Mammalian polyhomeotic homologues Phc2 and Phc1 act in synergy to mediate polycomb repression of Hox genes. Mol Cell Biol 25: 6694-6706
31. Itahana K, Zou Y, Itahana Y, Martinez JL, Beausejour C, Jacobs JJ, Van Lohuizen M, Band V, Campisi J, Dimri GP (2003) Control of the replicative life span of human fibroblasts by p16 and the polycomb protein Bmi-1. Mol Cell Biol 23: 389-401
32. Jacobs JJ, Kieboom K, Marino S, DePinho RA, Van Lohuizen M (1999) The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397: 164-168
33. Kawamura T, Suzuki J, Wang YV, Menendez S, Morera LB, Raya A, Wahl GM, Belmonte JC (2009) Linking the p53 tumour suppressor pathway to somatic cell reprogramming. Nature 460: 1140-1144
34. Kotake Y, Cao R, Viatour P, Sage J, Zhang Y, Xiong Y (2007) pRB family proteins are required for H3K27 trimethylation and Polycomb repression complexes binding to and silencing p16INK4alpha tumor suppressor gene. Genes Dev 21: 49-54
35. Lessard J, Sauvageau G (2003) Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 423: 255-260
36. Li H, Collado M, Villasante A, Strati K, Ortega S, Canamero M, Blasco MA, Serrano M (2009) The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 460: 1136-1139
37. Li M, Brooks CL, Kon N, Gu W (2004) A dynamic role of HAUSP in the p53-Mdm2 pathway. Mol Cell 13: 879-886
38. Li M, Chen D, Shiloh A, Luo J, Nikolaev AY, Qin J, Gu W (2002) Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 416: 648-653
39. Li Z, Cao R, Wang M, Myers MP, Zhang Y, Xu RM (2006) Structure of a Bmi-1-Ring1B polycomb group ubiquitin ligase complex. J Biol Chem 281: 20643-20649
40. Lin CH, Chang HS, Yu WC (2008) USP11 stabilizes HPV-16E7 and further modulates the E7 biological activity. J Biol Chem 283: 15681-15688
41. Maertens GN, Cherepanov P, Engelman A (2006) Transcriptional coactivator p75 binds and tethers the Myc-interacting protein JPO2 to chromatin. J Cell Sci 119(Part 12): 2563-2571
42. Maertens GN, El Messaoudi-Aubert S, Racek T, Stock JK, Nicholls J, Rodriguez-Niedenfuhr M, Gil J, Peters G (2009) Several distinct polycomb complexes regulate and co-localize on the INK4a tumor suppressor locus. PLoS One 4: e6380
43. Marion RM, Strati K, Li H, Murga M, Blanco R, Ortega S, Fernandez-Capetillo O, Serrano M, Blasco MA (2009) A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 460: 1149-1153
44. McConnell BB, Starborg M, Brookes S, Peters G (1998) Inhibitors of cyclin-dependent kinases induce features of replicative senes-cence in early passage human diploid fibroblasts. Curr Biol 8: 351-354
45. Minsky N, Oren M (2004) The RING domain of Mdm2 mediates histone ubiquitylation and transcriptional repression. Mol Cell 16: 631-639
46. Molofsky AV, Pardal R, Iwashita T, Park IK, Clarke MF, Morrison SJ (2003) Bmi-1 dependence distinguishes neural stem cell selfrenewal from progenitor proliferation. Nature 425: 962-967
47. Nijman SM, Luna-Vargas MP, Velds A, Brummelkamp TR, Dirac AM, Sixma TK, Bernards R (2005) A genomic and functional inventory of deubiquitinating enzymes. Cell 123: 773-786 (Pubitemid 41721026)
48. Park IK, Qian D, Kiel M, Becker MW, Pihalja M, Weissman IL, Morrison SJ, Clarke MF (2003) Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 423: 302-305
49. Sanchez C, Sanchez I, Demmers JA, Rodriguez P, Strouboulis J, Vidal M (2007) Proteomics analysis of Ring1B/Rnf2 interactors identifies a novel complex with the Fbxl10/Jhdm1B histone demethylase and the Bcl6 interacting corepressor. Mol Cell Proteomics 6: 820-834
50. Saurin AJ, Shao Z, Erdjument-Bromage H, Tempst P, Kingston RE (2001) A Drosophila Polycomb group complex includes Zeste and dTAFII proteins. Nature 412: 655-660
51. Schnitzler GR (2001) Isolation of histones and nucleosome cores from mammalian cells. Curr Protoc Mol Biol Chapter 21: Unit 21 25
52. Schoenfeld AR, Apgar S, Dolios G, Wang R, Aaronson SA (2004) BRCA2 is ubiquitinated in vivo and interacts with USP11, a deubiquitinating enzyme that exhibits prosurvival function in the cellular response to DNA damage. Mol Cell Biol 24: 7444-7455
53. Schwartz YB, Pirrotta V (2007) Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet 8: 9-22
54. Shao Z, Raible F, Mollaaghababa R, Guyon JR, Wu CT, Bender W, Kingston RE (1999) Stabilization of chromatin structure by PRC1, a Polycomb complex. Cell 98: 37-46
55. Sharpless NE (2005) INK4a/ARF: a multifunctional tumor suppressor locus. Mutat Res 576: 22-38
56. Song MS, Salmena L, Carracedo A, Egia A, Lo-Coco F, Teruya-Feldstein J, Pandolfi PP (2008) The deubiquitinylation and localization of PTEN are regulated by a HAUSP-PML network. Nature 455: 813-817
57. Sowa ME, Bennett EJ, Gygi SP, Harper JW (2009) Defining the human deubiquitinating enzyme interaction landscape. Cell 138: 389-403
58. Sparmann A, Van Lohuizen M (2006) Polycomb silencers control cell fate, development and cancer. Nat Rev Cancer 6: 846-856
59. Treier M, Staszewski LM, Bohmann D (1994) Ubiquitin-dependent c-Jun degradation in vivo is mediated by the delta domain. Cell 78: 787-798
60. Utikal J, Polo JM, Stadtfeld M, Maherali N, Kulalert W, Walsh RM, Khalil A, Rheinwald JG, Hochedlinger K (2009) Immortalization eliminates a roadblock during cellular reprogramming into iPS cells. Nature 460: 1145-1148
61. Van Der Knaap JA, Kumar BR, Moshkin YM, Langenberg K, Krijgsveld J, Heck AJ, Karch F, Verrijzer CP (2005) GMP synthetase stimulates histone H2B deubiquitylation by the epigenetic silencer USP7. Mol Cell 17: 695-707
62. Vissers JH, Nicassio F, Van Lohuizen M, Di Fiore PP, Citterio E (2008) The many faces of ubiquitinated histone H2A: insights from the DUBs. Cell Div 3: 8
63. Wang H, Wang L, Erdjument-Bromage H, Vidal M, Tempst P, Jones RS, Zhang Y (2004) Role of histone H2A ubiquitination in Polycomb silencing. Nature 431: 873-878
64. Weake VM, Workman JL (2008) Histone ubiquitination: triggering gene activity. Mol Cell 29: 653-663
65. West MH, Bonner WM (1980) Histone 2B can be modified by the attachment of ubiquitin. Nucleic Acids Res 8: 4671-4680
66. Whitcomb SJ, Basu A, Allis CD, Bernstein E (2007) Polycomb Group proteins: an evolutionary perspective. Trends Genet 23: 494-502
67. Wu X, Gong Y, Yue J, Qiang B, Yuan J, Peng X (2008) Cooperation between EZH2, NSPc1-mediated histone H2A ubiquitination and Dnmt1 in HOX gene silencing. Nucleic Acids Res 36: 3590-3599
68. Wysocka J, Reilly PT, Herr W (2001) Loss of HCF-1-chromatin association precedes temperature-induced growth arrest of tsBN67 cells. Mol Cell Biol 21: 3820-3829
69. Yamaguchi T, Kimura J, Miki Y, Yoshida K (2007) The deubiquitinating enzyme USP11 controls an IkappaB kinase alpha (IKKalpha)-p53 signaling pathway in response to tumor necrosis factor alpha (TNFalpha). J Biol Chem 282: 33943-33948