Bypass of senescence by the polycomb group protein CBX8 through direct binding to the INK4A-ARF locus

EMBO Journal

Volumn 26, Issue 6, 2007, Pages 1637-1648

  Dietrich, Nikolaj ^a   Bracken, Adrian P ^a   Trinh, Emmanuelle ^a   Schjerling, Charlotte K ^b   Koseki, Haruhiko ^c   Rappsilber, Juri ^d   Helin, Kristian ^a   Hansen, Klaus H ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Mental Health Services CPH   (Denmark)

^c RIKEN Center for Integrative Medical Sciences   (Japan)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

ARF; CBX8; INK4A; Polycomb; Senescence

Indexed keywords

PROTEIN; PROTEIN CBX8; UNCLASSIFIED DRUG;

ARTICLE; CELL FATE; CELL GROWTH; CELL IMMORTALIZATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; FIBROBLAST; GENE EXPRESSION; GENE LOCATION; GENE LOCUS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ANIMALS; CELL AGING; CELL PROLIFERATION; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CYCLIN-DEPENDENT KINASE INHIBITOR P16; FIBROBLASTS; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; MICE; MICROSCOPY, FLUORESCENCE; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 33947576177     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601632     Document Type: Article

References (55)

1. Attardi LD, Reczek EE, Cosmas C, Demicco EG, McCurrach ME, Lowe SW, Jacks T (2000) PERP, an apoptosis-associated target of p53, is a novel member of the PMP-22/gas3 family. Genes Dev 14: 704-718
2. Bardos JI, Saurin AJ, Tissot C, Duprez E, Freemont PS (2000) HPC3 is a new human polycomb orthologue that interacts and associates with RING1 and Bmi1 and has transcriptional repression properties. J Biol Chem 275: 28785-28792
3. Bea S, Tort F, Pinyol M, Puig X, Hernandez L, Hernandez S, Fernandez PL, van Lohuizen M, Colomer D, Campo E (2001) BMI-1 gene amplification and overexpression in hematological malignancies occur mainly in mantle cell lymphomas. Cancer Res 61: 2409-2412
4. Ben-Porath I, Weinberg RA (2005) The signals and pathways activating cellular senescence. Int J Biochem Cell Biol 37: 961-976
5. Bernstein E, Duncan EM, Masui O, Gil J, Heard E, Allis CD (2006) Mouse polycomb proteins bind differentially to methylated histone H3 and RNA and are enriched in facultative heterochromatin. Mol Cell Biol 26: 2560-2569
6. Bracken AP, Dietrich N, Pasini D, Hansen KH, Helin K (2006) Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev 20: 1123-1136
7. Bracken AP, Pasini D, Capra M, Prosperini E, Colli E, Helin K (2003) EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. EMBO J 22: 5323-5335
8. Bruggeman SW, Valk-Lingbeek ME, van der Stoop PP, Jacobs JJ, Kieboom K, Tanger E, Hulsman D, Leung C, Arsenijevic Y, Marino S, van Lohuizen M (2005) Ink4a and Arf differentially affect cell proliferation and neural stem cell self-renewal in Bmi1-deficient mice. Genes Dev 19: 1438-1443
9. Brummelkamp TR, Bernards R, Agami R (2002) A system for stable expression of short interfering RNAs in mammalian cells. Science 296: 550-553
10. Campisi J (2000) Cancer, aging and cellular senescence. In Vivo 14: 183-188
11. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298: 1039-1043
12. Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, Pirrotta V (2002) Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111: 185-196
13. Dirac AM, Bernards R (2003) Reversal of senescence inmouse fibroblasts through lentiviral suppression of p53. J Biol Chem 278: 11731-11734
14. Drayton S, Brookes S, Rowe J, Peters G (2004) The significance of p16INK4a in cell defenses against transformation. Cell Cycle 3: 611-615
15. Fischle W, Wang Y, Jacobs SA, Kim Y, Allis CD, Khorasanizadeh S (2003) Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev 17: 1870-1881
16. Frigola J, Munoz M, Clark SJ, Moreno V, Capella G, Peinado MA (2005) Hypermethylation of the prostacyclin synthase (PTGIS) promoter is a frequent event in colorectal cancer and associated with aneuploidy. Oncogene 24: 7320-7326
17. Gil J, Peters G (2006) Regulation of the INK4b-ARF-INK4a tumour suppressor locus: all for one or one for all. Nat Rev Mol Cell Biol 7: 667-677
18. Gil J, Bernard D, Martinez D, Beach D (2004) Polycomb CBX7 has a unifying role in cellular lifespan. Nat Cell Biol 6: 67-72
19. Grignani F, Kinsella T, Mencarelli A, Valtieri M, Riganelli D, Grignani F, Lanfrancone L, Peschle C, Nolan GP, Pelicci PG (1998) High-efficiency gene transfer and selection of human hematopoietic progenitor cells with a hybrid EBV/retroviral vector expressing the green fluorescence protein. Cancer Res 58: 14-19
20. Hake SB, Allis CD (2006) Histone H3 variants and their potential role in indexing mammalian genomes: the "H3 barcode hypothesis". Proc Natl Acad Sci USA 103: 6428-6435
21. Haupt Y, Alexander WS, Barri G, Klinken SP, Adams JM (1991) Novel zinc finger gene implicated as myc collaborator by retrovirally accelerated lymphomagenesis in E mu-myc transgenic mice. Cell 65: 753-763
22. Hildebrandt T, Preiherr J, Tarbe N, Klostermann S, Van Muijen GN, Weidle UH (2000) Identification of THW, a putative new tumor suppressor gene. Anticancer Res 20: 2801-2809
23. Isono K, Fujimura Y, Shinga J, Yamaki M, Wang OJ, 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
24. 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
25. 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
26. Jin J, Cai Y, Li B, Conaway RC, Workman JL, Conaway JW, Kusch T (2005) In and out: histone variant exchange in chromatin. Trends Biochem Sci 30: 680-687
27. Kim H, Lapointe J, Kaygusuz G, Ong DE, Li C, van de Rijn M, Brooks JD, Pollack JR (2005) The retinoic acid synthesis gene ALDH1a2 is a candidate tumor suppressor in prostate cancer. Cancer Res 65: 8118-8124
28. Kleer CG, Cao Q, Varambally S, Shen R, Ota I, Tomlins SA, Ghosh D, Sewalt RG, Otte AP, Hayes DF, Sabel MS, Livant D, Weiss SJ, Rubin MA, Chinnaiyan AM (2003) EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc Natl Acad Sci USA 100: 11606-11611
29. Klose RJ, Kallin EM, Zhang Y (2006) JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet 7: 715-727
30. Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D (2002) Histone methyltransferase activity associated with a human multiprotein complex containing the enhancer of Zeste protein. Genes Dev 16: 2893-2905
31. Levine SS, Weiss A, Erdjument-Bromage H, Shao Z, Tempst P, Kingston RE (2002) The core of the polycomb repressive complex is compositionally and functionally conserved in flies and humans. Mol Cell Biol 22: 6070-6078
32. Liu L, Andrews LG, Tollefsbol TO (2006) Loss of the human polycomb group protein BMI1 promotes cancer-specific cell death. Oncogene 25: 4370-4375
33. Lundberg AS, Hahn WC, Gupta P, Weinberg RA (2000) Genes involved in senescence and immortalization. Curr Opin Cell Biol 12: 705-709
34. Mesnil M, Crespin S, Avanzo JL, Zaidan-Dagli ML (2005) Defective gap junctional intercellular communication in the carcinogenic process. Biochim Biophys Acta 1719: 125-145
35. Miyamoto K, Fukutomi T, Akashi-Tanaka S, Hasegawa T, Asahara T, Sugimura T, Ushijima T (2005) Identification of 20 genes aberrantly methylated in human breast cancers. Int J Cancer 116: 407-414
36. Molofsky AV, Pardal R, Iwashita T, Park IK, Clarke MF, Morrison SJ (2003) Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 425: 962-967
37. Muller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, Wild B, Miller EL, O'Connor MB, Kingston RE, Simon JA (2002) Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111: 197-208
38. Narita M, Nunez S, Heard E, Narita M, Lin AW, Hearn SA, Spector DL, Hannon GJ, Lowe SW (2003) Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 113: 703-716
39. 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
40. Park YB, Park MJ, Kimura K, Shimizu K, Lee SH, Yokota J (2002) Alterations in the INK4a/ARF locus and their effects on the growth of human osteosarcoma cell lines. Cancer Genet Cytogenet 133: 105-111
41. Pasini D, Bracken AP, Jensen MR, Lazzerini Denchi E, Helin K (2004) Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. EMBO J 23: 4061-4071
42. Sanchez-Beato M, Sanchez E, Gonzalez-Carrero J, Morente M, Diez A, Sanchez-Verde L, Martin MC, Cigudosa JC, Vidal M, Piris MA (2006) Variability in the expression of polycomb proteins in different normal and tumoral tissues. A pilot study using tissue microarrays. Mod Pathol 19: 684-694
43. Satijn DP, Olson DJ, van der Vlag J, Hamer KM, Lambrechts C, Masselink H, Gunster MJ, Sewalt RG, van Driel R, Otte AP (1997) Interference with the expression of a novel human polycomb protein, hPc2, results in cellular transformation and apoptosis. Mol Cell Biol 17: 6076-6086
44. Saurin AJ, Shiels C, Williamson J, Satijn DP, Otte AP, Sheer D, Freemont PS (1998) The human polycomb group complex associates with pericentromeric heterochromatin to form a novel nuclear domain. J Cell Biol 142: 887-898
45. Seibold S, Rudroff C, Weber M, Galle J, Wanner C, Marx M (2003) Identification of a new tumor suppressor gene located at chromosome 8p21.3-22. FASEB J 17: 1180-1182
46. Serrano M, Blasco MA (2001) Putting the stress on senescence. Curr Opin Cell Biol 13: 748-753
47. Thiebault K, Mazelin L, Pays L, Llambi F, Joly MO, Scoazec JY, Saurin JC, Romeo G, Mehlen P (2003) The netrin-1 receptors UNC5H are putative tumor suppressors controlling cell death commitment. Proc Natl Acad Sci USA 100: 4173-4178
48. Todaro GJ, Green H (1963) Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J Cell Biol 17: 299-313
49. Valk-Lingbeek ME, Bruggeman SW, van Lohuizen M (2004) Stem cells and cancer; the polycomb connection. Cell 118: 409-418
50. van Kemenade FJ, Raaphorst FM, Blokzijl T, Fieret E, Hamer KM, Satijn DP, Otte AP, Meijer CJ (2001) Coexpression of BMI-1 and EZH2 polycomb-group proteins is associated with cycling cells and degree of malignancy in B-cell non-Hodgkin lymphoma. Blood 97: 3896-3901
51. van Lohuizen M, Verbeek S, Scheijen B, Wientjens E, van der Gulden H, Berns A (1991) Identification of cooperating oncogenes in E mu-myc transgenic mice by provirus tagging. Cell 65: 737-752
52. Vanaja DK, Ballman KV, Morlan BW, Cheville JC, Neumann RM, Lieber MM, Tindall DJ, Young CY (2006) PDLIM4 repression by hypermethylation as a potential biomarker for prostate cancer. Clin Cancer Res 12: 1128-1136
53. Voncken JW, Schweizer D, Aagaard L, Sattler L, Jantsch MF, van Lohuizen M (1999) Chromatin-association of the Polycomb group protein BMI1 is cell cycle-regulated and correlates with its phosphorylation status. J Cell Sci 112 (Part 24): 4627-4639
54. Vonlanthen S, Heighway J, Altermatt HJ, Gugger M, Kappeler A, Borner MM, van Lohuizen M, Betticher DC (2001) The bmi-1 oncoprotein is differentially expressed in non-small cell lung cancer and correlates with INK4A-ARF locus expression. Br J Cancer 84: 1372-1376
55. Ying J, Srivastava G, Hsieh WS, Gao Z, Murray P, Liao SK, Ambinder R, Tao Q (2005) The stress-responsive gene GADD45G is a functional tumor suppressor, with its response to environmental stresses frequently disrupted epigenetically in multiple tumors. Clin Cancer Res 11: 6442-6449