Gene regulation and tumor suppression by the bromodomain-containing protein BRD7

Cell Cycle

Volumn 9, Issue 14, 2010, Pages 2849-2853

  Mantovani, Fiamma ^a,b   Drost, Jarno ^c   Voorhoeve, P Mathijs ^d   Del Sal, Giannino ^a,b   Agami, Reuven ^c,e  

^a Laboratorio Nazionale CIB   (Italy)

^b UNIVERSITY OF TRIESTE   (Italy)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

^d DUKE NUS MEDICAL SCHOOL   (Singapore)

^e Center for Biomedical Genetics   (Netherlands)

Author keywords

BRD7; Chromatin remodeling; p53; Senescence; Transcription; Tumor suppressor gene

Indexed keywords

PROTEIN P53;

BREAST TUMOR; BROMODOMAIN CONTAINING 7 GENE; CANCER INHIBITION; CELL PROLIFERATION; CYTOLOGY; DNA REPAIR; GENE CONTROL; GENE LOCUS; HUMAN; REVIEW; STEM CELL; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE;

EID: 77956813033     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.14.12309     Document Type: Review

References (62)

1. Michaloglou C, Vredeveld LC, Soengas MS, Denoyelle C, Kuilman T, van der Horst CM, et al. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature 2005; 436:720-4.
2. Chen Z, Trotman LC, Shaffer D, Lin HK, Dotan ZA, Niki M, et al. Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature 2005; 436:725-30.
3. Collado M, Gil J, Efeyan A, Guerra C, Schuhmacher AJ, Barradas M, et al. Tumour biology: senescence in premalignant tumours. Nature 2005; 436:642.
4. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, Luise C, et al. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 2006; 444:638-42.
5. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N, et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 2006; 444:633-7.
6. Kortlever RM, Higgins PJ, Bernards R. Plasminogen activator inhibitor-1 is a critical downstream target of p53 in the induction of replicative senescence. Nat Cell Biol 2006; 8:877-84.
7. Christophorou MA, Ringshausen I, Finch AJ, Swigart LB, Evan GI. The pathological response to DNA damage does not contribute to p53-mediated tumour suppression. Nature 2006; 443:214-7.
8. Ventura A, Kirsch DG, McLaughlin ME, Tuveson DA, Grimm J, Lintault L, et al. Restoration of p53 function leads to tumour regression in vivo. Nature 2007; 445:661-5.
9. Xue W, Zender L, Miething C, Dickins RA, Hernando E, Krizhanovsky V, et al. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007; 445:656-60.
10. Tang Y, Zhao W, Chen Y, Zhao Y, Gu W. Acetylation is indispensable for p53 activation. Cell 2008; 133:612-26.
11. Sykes SM, Mellert HS, Holbert MA, Li K, Marmorstein R, Lane WS, et al. Acetylation of the p53 DNA-binding domain regulates apoptosis induction. Mol Cell 2006; 24:841-51.
12. Tang Y, Luo J, Zhang W, Gu W. Tip60-dependent acetylation of p53 modulates the decision between cell cycle arrest and apoptosis. Mol Cell 2006; 24:827-39.
13. Knights CD, Catania J, Di Giovanni S, Muratoglu S, Perez R, Swartzbeck A, et al. Distinct p53 acetylation cassettes differentially influence gene-expression patterns and cell fate. J Cell Biol 2006; 173:533-44.
14. Zhao Y, Lu S, Wu L, Chai G, Wang H, Chen Y, et al. Acetylation of p53 at lysine 373/382 by the histone deacetylase inhibitor depsipeptide induces expression of p21(Waf1/Cip1). Mol Cell Biol 2006; 26:2782-90.
15. Vousden KH, Prives C. Blinded by the Light: The Growing Complexity of p53. Cell 2009; 137:413-31.
16. Drost J, Mantovani F, Tocco F, Elkon R, Comel A, Holstege H, et al. BRD7 is a candidate tumour suppressor gene required for p53 function. Nat Cell Biol 2010; 12:380-9.
17. Peng C, Zhou J, Liu HY, Zhou M, Wang LL, Zhang QH, et al. The transcriptional regulation role of BRD7 by binding to acetylated histone through bromodomain. J Cell Biochem 2006; 97:882-92.
18. Kaeser MD, Aslanian A, Dong MQ, Yates JR, 3rd, Emerson BM. BRD7, a novel PBAF-specific SWI/SNF subunit, is required for target gene activation and repression in embryonic stem cells. J Biol Chem 2008; 283:32254-63.
19. Staal A, Enserink JM, Stein JL, Stein GS, van Wijnen AJ. Molecular characterization of celtix-1, a bromodomain protein interacting with the transcription factor interferon regulatory factor 2. J Cell Physiol 2000; 185:269-79.
20. Sun H, Liu J, Zhang J, Shen W, Huang H, Xu C, et al. Solution structure of BRD7 bromodomain and its interaction with acetylated peptides from histone H3 and H4. Biochem Biophys Res Commun 2007; 358:435-41.
21. Oh J, Sohn DH, Ko M, Chung H, Jeon SH, Seong RH. BAF60a interacts with p53 to recruit the SWI/SNF complex. J Biol Chem 2008; 283:11924-34.
22. Lee D, Kim JW, Seo T, Hwang SG, Choi EJ, Choe J. SWI/SNF complex interacts with tumor suppressor p53 and is necessary for the activation of p53-mediated transcription. J Biol Chem 2002; 277:22330-7.
23. Peterson CL, Workman JL. Promoter targeting and chromatin remodeling by the SWI/SNF complex. Curr Opin Genet Dev 2000; 10:187-92.
24. Hendricks KB, Shanahan F, Lees E. Role for BRG1 in cell cycle control and tumor suppression. Mol Cell Biol 2004; 24:362-76.
25. Kang H, Cui K, Zhao K. BRG1 controls the activity of the retinoblastoma protein via regulation of p21CIP1/WAF1/SDI. Mol Cell Biol 2004; 24:1188-99.
26. Xu Y, Zhang J, Chen X. The activity of p53 is differentially regulated by Brm- and Brg1-containing SWI/SNF chromatin remodeling complexes. J Biol Chem 2007; 282:37429-35.
27. Naidu SR, Love IM, Imbalzano AN, Grossman SR, Androphy EJ. The SWI/SNF chromatin remodeling subunit BRG1 is a critical regulator of p53 necessary for proliferation of malignant cells. Oncogene 2009; 28:2492-501.
28. Gevry N, Chan HM, Laflamme L, Livingston DM, Gaudreau L. p21 transcription is regulated by differential localization of histone H2A.Z. Genes Dev 2007; 21:1869-81.
29. Adams PD. Remodeling of chromatin structure in senescent cells and its potential impact on tumor suppression and aging. Gene 2007; 397:84-93.
30. Narita M, Nunez S, Heard E, Lin AW, Hearn SA, Spector DL, et al. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 2003; 113:703-16.
31. Ye X, Zerlanko B, Zhang R, Somaiah N, Lipinski M, Salomoni P, et al. Definition of pRB- and p53-dependent and -independent steps in HIRA/ASF1a-mediated formation of senescence-associated heterochromatin foci. Mol Cell Biol 2007; 27:2452-65.
32. Strobeck MW, Knudsen KE, Fribourg AF, DeCristofaro MF, Weissman BE, Imbalzano AN, et al. BRG-1 is required for RB-mediated cell cycle arrest. Proc Natl Acad Sci USA 2000; 97:7748-53.
33. Zhang HS, Gavin M, Dahiya A, Postigo AA, Ma D, Luo RX, et al. Exit from G1 and S phase of the cell cycle is regulated by repressor complexes containing HDAC-Rb-hSWI/SNF and Rb-hSWI/SNF. Cell 2000; 101:79-89.
34. Zhou J, Ma J, Zhang BC, Li XL, Shen SR, Zhu SG, et al. BRD7, a novel bromodomain gene, inhibits G1-S progression by transcriptionally regulating some important molecules involved in ras/MEK/ERK and Rb/E2F pathways. J Cell Physiol 2004; 200:89-98.
35. Peng C, Liu HY, Zhou M, Zhang LM, Li XL, Shen SR, et al. BRD7 suppresses the growth of Nasopharyngeal Carcinoma cells (HNE1) through negatively regulating beta-catenin and ERK pathways. Mol Cell Biochem 2007; 303:141-9.
36. Harte MT, O'Brien GJ, Ryan NM, Gorski JJ, Savage KI, Crawford NT, et al. BRD7, a subunit of SWI/SNF complexes, binds directly to BRCA1 and regulates BRCA1-dependent transcription. Cancer Res 2010; 70:2538-47.
37. Park JH, Park EJ, Lee HS, Kim SJ, Hur SK, Imbalzano AN, et al. Mammalian SWI/SNF complexes facilitate DNA double-strand break repair by promoting gamma-H2AX induction. EMBO J 2006; 25:3986-97.
38. Lee HS, Park JH, Kim SJ, Kwon SJ, Kwon J. A cooperative activation loop among SWI/SNF, gamma-H2AX and H3 acetylation for DNA double-strand break repair. EMBO J 2010; 29:1434-45.
39. Zhao Q, Wang QE, Ray A, Wani G, Han C, Milum K, et al. Modulation of nucleotide excision repair by mammalian SWI/SNF chromatin-remodeling complex. J Biol Chem 2009; 284:30424-32.
40. MacLachlan TK, Takimoto R, El-Deiry WS. BRCA1 directs a selective p53-dependent transcriptional response towards growth arrest and DNA repair targets. Mol Cell Biol 2002; 22:4280-92.
41. Ongusaha PP, Ouchi T, Kim KT, Nytko E, Kwak JC, Duda RB, et al. BRCA1 shifts p53-mediated cellular outcomes towards irreversible growth arrest. Oncogene 2003; 22:3749-58.
42. Bochar DA, Wang L, Beniya H, Kinev A, Xue Y, Lane WS, et al. BRCA1 is associated with a human SWI/SNF-related complex: linking chromatin remodeling to breast cancer. Cell 2000; 102:257-65.
43. Campisi J. Senescent cells, tumor suppression and organismal aging: good citizens, bad neighbors. Cell 2005; 120:513-22.
44. INK4a. Nature 2006; 443:421-6.
45. INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature 2006; 443:448-52.
46. Argos M, Kibriya MG, Jasmine F, Olopade OI, Su T, Hibshoosh H, et al. Genomewide scan for loss of heterozygosity and chromosomal amplification in breast carcinoma using single-nucleotide polymorphism arrays. Cancer Genet Cytogenet 2008; 182:69-74.
47. Yu Y, Zhang BC, Xie Y, Cao L, Zhou M, Zhan FH, et al. Analysis and Molecular Cloning of Differentially Expressing Genes in Nasopharyngeal Carcinoma. Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao (Shanghai) 2000; 32:327-32.
48. Liu H, Zhang L, Niu Z, Zhou M, Peng C, Li X, et al. Promoter methylation inhibits BRD7 expression in human nasopharyngeal carcinoma cells. BMC Cancer 2008; 8:253.
49. Spruck CH, 3rd, Tsai YC, Huang DP, Yang AS, Rideout WM, 3rd, Gonzalez-Zulueta M, et al. Absence of p53 gene mutations in primary nasopharyngeal carcinomas. Cancer Res 1992; 52:4787-90.
50. Ma Z, Gibson SL, Byrne MA, Zhang J, White MF, Shaw LM. Suppression of insulin receptor substrate 1 (IRS-1) promotes mammary tumor metastasis. Mol Cell Biol 2006; 26:9338-51.
51. Liu X, Holstege H, van der Gulden H, Treur-Mulder M, Zevenhoven J, Velds A, et al. Somatic loss of BRCA1 and p53 in mice induces mammary tumors with features of human BRCA1-mutated basal-like breast cancer. Proc Natl Acad Sci USA 2007; 104:12111-6.
52. Collavin L, Lunardi A, Del Sal G. p53-family proteins and their regulators: hubs and spokes in tumor suppression. Cell Death Differ 2010; In press.
53. Flores ER, Sengupta S, Miller JB, Newman JJ, Bronson R, Crowley D, et al. Tumor predisposition in mice mutant for p63 and p73: evidence for broader tumor suppressor functions for the p53 family. Cancer Cell 2005; 7:363-73.
54. Tomasini R, Tsuchihara K, Wilhelm M, Fujitani M, Rufini A, Cheung CC, et al. TAp73 knockout shows genomic instability with infertility and tumor suppressor functions. Genes Dev 2008; 22:2677-91.
55. Guo X, Keyes WM, Papazoglu C, Zuber J, Li W, Lowe SW, et al. TAp63 induces senescence and suppresses tumorigenesis in vivo. Nat Cell Biol 2009; 11:1451-7.
56. Adorno M, Cordenonsi M, Montagner M, Dupont S, Wong C, Hann B, et al. A Mutant-p53/Smad complex opposes p63 to empower TGFbeta-induced metastasis. Cell 2009; 137:87-98.
57. Reisman D, Glaros S, Thompson EA. The SWI/SNF complex and cancer. Oncogene 2009; 28:1653-68.
58. Reisman DN, Sciarrotta J, Wang W, Funkhouser WK, Weissman BE. Loss of BRG1/BRM in human lung cancer cell lines and primary lung cancers: correlation with poor prognosis. Cancer Res 2003; 63:560-6.
59. Fukuoka J, Fujii T, Shih JH, Dracheva T, Meerzaman D, Player A, et al. Chromatin remodeling factors and BRM/BRG1 expression as prognostic indicators in non-small cell lung cancer. Clin Cancer Res 2004; 10:4314-24.
60. Glaros S, Cirrincione GM, Muchardt C, Kleer CG, Michael CW, Reisman D. The reversible epigenetic silencing of BRM: implications for clinical targeted therapy. Oncogene 2007; 26:7058-66.
61. Versteege I, Sevenet N, Lange J, Rousseau-Merck MF, Ambros P, Handgretinger R, et al. Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer. Nature 1998; 394:203-6.
62. Sansam CG, Roberts CW. Epigenetics and cancer: altered chromatin remodeling via Snf5 loss leads to aberrant cell cycle regulation. Cell Cycle 2006; 5:621-4.