Physical and functional interaction between PML and TBX2 in the establishment of cellular senescence

EMBO Journal

Volumn 31, Issue 1, 2012, Pages 95-109

  Martin, Nadine ^a,b,d   Benhamed, Moussa ^a,b   Nacerddine, Karim ^a,b,c   Demarque, Maud D ^a,b   Van Lohuizen, Maarten ^c   Dejean, Anne ^a,b   Bischof, Oliver ^a,b  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

^d HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

cellular senescence; chromatin; gene repression; PML; TBX2

Indexed keywords

PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEIN P130; T BOX TRANSCRIPTION FACTOR 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E2F4; UNCLASSIFIED DRUG;

ARTICLE; CELL AGING; CHROMATIN; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION PROFILING; GENE REPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION;

ANIMALS; CELL AGING; FIBROBLASTS; HUMANS; MICE; NIH 3T3 CELLS; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; T-BOX DOMAIN PROTEINS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84855344619     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.370     Document Type: Article

References (51)

1. Abrahams A, Parker MI, Prince S (2010) The T-box transcription factor Tbx2: its role in development and possible implication in cancer. IUBMB Life 62: 92-102
2. Agulnik SI, Bollag RJ, Silver LM (1995) Conservation of the T-box gene family from Mus musculus to Caenorhabditis elegans. Genomics 25: 214-219
3. Bernardi R, Pandolfi PP (2007) Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat Rev Mol Cell Biol 8: 1006-1016 (Pubitemid 350174636)
4. Bischof O, Kirsh O, Pearson M, Itahana K, Pelicci PG, Dejean A (2002) Deconstructing PML-induced premature senescence. EMBO J 21: 3358-3369 (Pubitemid 34760568)
5. Bischof O, Nacerddine K, Dejean A (2005) Human papillomavirus oncoprotein E7 targets the promyelocytic leukemia protein and circumvents cellular senescence via the Rb and p53 tumor suppressor pathways. Mol Cell Biol 25: 1013-1024 (Pubitemid 40165809)
6. Bischof O, Schwamborn K, Martin N, Werner A, Sustmann C, Grosschedl R, Dejean A (2006) The E3 SUMO ligase PIASy is a regulator of cellular senescence and apoptosis. Mol Cell 22: 783-794
7. Block GJ, Eskiw CH, Dellaire G, Bazett-Jones DP (2006) Transcriptional regulation is affected by subnuclear targeting of reporter plasmids to PML nuclear bodies. Mol Cell Biol 26: 8814-8825 (Pubitemid 44851941)
8. Cam H, Balciunaite E, Blais A, Spektor A, Scarpulla RC, Young R, Kluger Y, Dynlacht BD (2004) A common set of gene regulatory networks links metabolism and growth inhibition. Mol Cell 16: 399-411 (Pubitemid 39504794)
9. Campisi J, d'Adda di Fagagna F (2007) Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol 8: 729-740 (Pubitemid 47312822)
10. Carreira S, Liu B, Goding CR (2000) The gene encoding the T-box factor Tbx2 is a target for the microphthalmia-associated transcription factor in melanocytes. J Biol Chem 275: 21920-21927 (Pubitemid 30621764)
11. Chen Z, Trotman LC, Shaffer D, Lin HK, Dotan ZA, Niki M, Koutcher JA, Scher HI, Ludwig T, Gerald W, Cordon-Cardo C, Pandolfi PP (2005) Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature 436: 725-730 (Pubitemid 41117277)
12. Chicas A, Wang X, Zhang C, McCurrach M, Zhao Z, Mert O, Dickins RA, Narita M, Zhang M, Lowe SW (2010) Dissecting the unique role of the retinoblastoma tumor suppressor during cellular senescence. Cancer Cell 17: 376-387
13. Courtois-Cox S, Genther Williams SM, Reczek EE, Johnson BW, McGillicuddy LT, Johannessen CM, Hollstein PE, MacCollin M, Cichowski K (2006) A negative feedback signaling network underlies oncogene-induced senescence. Cancer Cell 10: 459-472 (Pubitemid 44872980)
14. Davis E, Teng H, Bilican B, Parker MI, Liu B, Carriera S, Goding CR, Prince S (2008) Ectopic Tbx2 expression results in polyploidy and cisplatin resistance. Oncogene 27: 976-984 (Pubitemid 351225380)
15. De Stanchina E, Querido E, Narita M, Davuluri RV, Pandolfi PP, Ferbeyre G, Lowe SW (2004) PML is a direct p53 target that modulates p53 effector functions. Mol Cell 13: 523-535 (Pubitemid 38299380)
16. Dyson N (1998) The regulation of E2F by pRB-family proteins. Genes Dev 12: 2245-2262 (Pubitemid 28371346)
17. Everett RD, Chelbi-Alix MK (2007) PML and PML nuclear bodies: implications in antiviral defence. Biochimie 89: 819-830 (Pubitemid 47008945)
18. Ferbeyre G, de Stanchina E, Querido E, Baptiste N, Prives C, Lowe SW (2000) PML is induced by oncogenic ras and promotes premature senescence. Genes Dev 14: 2015-2027 (Pubitemid 30637352)
19. Frolov MV, Dyson NJ (2004) Molecular mechanisms of E2F-dependent activation and pRB-mediated repression. J Cell Sci 11 7 (Part 11): 2173-2181 (Pubitemid 38807486)
20. Gabai VL, Yaglom JA, Waldman T, Sherman MY (2009) Heat shock protein Hsp72 controls oncogene-induced senescence pathways in cancer cells. Mol Cell Biol 29: 559-569
21. Gurrieri C, Capodieci P, Bernardi R, Scaglioni PP, Nafa K, Rush LJ, Verbel DA, Cordon-Cardo C, Pandolfi PP (2004a) Loss of the tumor suppressor PML in human cancers of multiple histologic origins. J Natl Cancer Inst 96: 269-279 (Pubitemid 38256272)
22. Gurrieri C, Nafa K, Merghoub T, Bernardi R, Capodieci P, Biondi A, Nimer S, Douer D, Cordon-Cardo C, Gallagher R, Pandolfi PP (2004b) Mutations of the PML tumor suppressor gene in acute promyelocytic leukemia. Blood 103: 2358-2362 (Pubitemid 38326258)
23. He M, Wen L, Campbell CE, Wu JY, Rao Y (1999) Transcription repression by Xenopus ET and its human ortholog TBX3, a gene involved in ulnar-mammary syndrome. Proc Natl Acad Sci USA 96: 10212-10217 (Pubitemid 29422538)
24. Helmbold H, Deppert W, Bohn W (2006) Regulation of cellular senescence by Rb2/p130. Oncogene 25: 5257-5262 (Pubitemid 44299085)
25. Ismail A, Bateman A (2009) Expression of TBX2 promotes anchorage-independent growth and survival in the p53-negative SW13 adrenocortical carcinoma. Cancer Lett 278: 230-240
26. Jackson JG, Pereira-Smith OM (2006) Primary and compensatory roles for RB family members at cell cycle gene promoters that are deacetylated and downregulated in doxorubicin-induced senescence of breast cancer cells. Mol Cell Biol 26: 2501-2510
27. Jacobs JJ, Keblusek P, Robanus-Maandag E, Kristel P, Lingbeek M, Nederlof PM, van Welsem T, van de Vijver MJ, Koh EY, Daley GQ, van Lohuizen M (2000) Senescence bypass screen identifies TBX2, which represses Cdkn2a (p19(ARF)) and is amplified in a subset of human breast cancers. Nat Genet 26: 291-299
28. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M (1999) The oncogene and Polycomb-group gene bmi-1 regu lates cell proliferation and senescence through the ink4a locus. Nature 397: 164-168 (Pubitemid 29050921)
29. Jensen K, Shiels C, Freemont PS (2001) PML protein isoforms and the RBCC/TRIM motif. Oncogene 20: 7223-7233 (Pubitemid 33105011)
30. Jenuwein T (2006) The epigenetic magic of histone lysine methyla-tion. FEBS J 273: 3121-3135
31. Kumar PP, Bischof O, Purbey PK, Notani D, Urlaub H, Dejean A, Galande S (2007) Functional interaction between PML and SATB1 regulates chromatin-loop architecture and transcription of the MHC class I locus. Nat Cell Biol 9: 45-56 (Pubitemid 46024196)
32. Lin AW, Barradas M, Stone JC, van Aelst L, Serrano M, Lowe SW (1998) Premature senescence involving p53 and p16 is activated in response to constitutive MEK/MAPK mitogenic signaling. Genes Dev 12: 3008-3019 (Pubitemid 28469303)
33. Lingbeek ME, Jacobs JJ, van Lohuizen M (2002) The T-box repres-sors TBX2 and TBX3 specifically regulate the tumor suppressor gene p14ARF via a variant T-site in the initiator. J Biol Chem 277: 26120-26127 (Pubitemid 34967096)
34. Mallette FA, Goumard S, Gaumont-Leclerc MF, Moiseeva O, Ferbeyre G (2004) Human fibroblasts require the Rb family of tumor suppressors, but not p53, for PML-induced senescence. Oncogene 23: 91-99 (Pubitemid 38142243)
35. Mann KK, Shao W, Miller Jr WH (2001) The biology of acute promyelocytic leukemia. Curr Oncol Rep 3: 209-216
36. Minucci S, Nervi C, Lo Coco F, Pelicci PG (2001) Histone deacety-lases: a common molecular target for differentiation treatment of acute myeloid leukemias? Oncogene 20: 3110-3115 (Pubitemid 32553566)
37. Narita M, Nunez S, Heard E, 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 (Pubitemid 36724935)
38. Pearson M, Carbone R, Sebastiani C, Cioce M, Fagioli M, Saito S, Higashimoto Y, Appella E, Minucci S, Pandolfi PP, Pelicci PG (2000) PML regulates p53 acetylation and premature senescence induced by oncogenic Ras. Nature 406: 207-210 (Pubitemid 30469006)
39. Prince S, Carreira S, Vance KW, Abrahams A, Goding CR (2004) Tbx2 directly represses the expression of the p21(WAF1) cyclin-dependent kinase inhibitor. Cancer Res 64: 1669-1674 (Pubitemid 38428688)
40. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW (1997) Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88: 593-602 (Pubitemid 27152402)
41. Takahashi Y, Rayman JB, Dynlacht BD (2000) Analysis of promoter binding by the E2F and pRB families in vivo: distinct E2F proteins mediate activation and repression. Genes Dev 14: 804-816 (Pubitemid 30215000)
42. Tarutani M, Cai T, Dajee M, Khavari PA (2003) Inducible activation of Ras and Raf in adult epidermis. Cancer Res 63: 319-323 (Pubitemid 36152487)
43. Teng H, Davis E, Abrahams A, Mowla S, Parker MI, Prince S (2007) A role for Tbx2 in the regulation of the alpha2(1) collagen gene in human fibroblasts. J Cell Biochem 102: 618-625 (Pubitemid 47557416)
44. Trimarchi JM, Lees JA (2002) Sibling rivalry in the E2F family. Nat Rev Mol Cell Biol 3: 11-20 (Pubitemid 135709914)
45. Vance KW, Carreira S, Brosch G, Goding CR (2005) Tbx2 is over-expressed and plays an important role in maintaining proliferation and suppression of senescence in melanomas. Cancer Res 65: 2260-2268 (Pubitemid 40490135)
46. Vernier M, Bourdeau V, Gaumont-Leclerc MF, Moiseeva O, Begin V, Saad F, Mes-Masson AM, Ferbeyre G (2011) Regulation of E2Fs and senescence by PML nuclear bodies. Genes Dev 25: 41-50
47. Villa R, Pasini D, Gutierrez A, Morey L, Occhionorelli M, Vire E, Nomdedeu JF, Jenuwein T, Pelicci PG, Minucci S, Fuks F, Helin K, Di Croce L (2007) Role of the polycomb repressive complex 2 in acute promyelocytic leukemia. Cancer Cell 11 : 513-525 (Pubitemid 46863505)
48. Wang J, Shiels C, Sasieni P, Wu PJ, Islam SA, Freemont PS, Sheer D (2004) Promyelocytic leukemia nuclear bodies asso-ciate with transcriptionally active genomic regions. J Cell Biol 164: 515-526 (Pubitemid 38233313)
49. Wang ZG, Delva L, Gaboli M, Rivi R, Giorgio M, Cordon-Cardo C, Grosveld F, Pandolfi PP (1998) Role of PML in cell growth and the retinoic acid pathway. Science 279: 1547-1551 (Pubitemid 28217080)
50. Xu ZX, Zhao RX, Ding T, Tran TT, Zhang W, Pandolfi PP, Chang KS (2004) Promyelocytic leukemia protein 4 induces apoptosis by inhibition of survivin expression. J Biol Chem 279: 1838-1844 (Pubitemid 38084451)
51. Zhong S, Salomoni P, Pandolfi PP (2000) The transcriptional role of PML and the nuclear body. Nat Cell Biol 2: E85-E90