RAP80 is critical in maintaining genomic stability and suppressing tumor development

Cancer Research

Volumn 72, Issue 19, 2012, Pages 5080-5090

  Yin, Zhengyu ^a   Menendez, Daniel ^a   Resnick, Michael A ^a   French, John E ^a   Janardhan, Kyathanahalli S ^b   Jetten, Anton M ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; MEMBRANE PROTEIN; RECEPTOR ASSOCIATED PROTEIN 80; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CARCINOGENESIS; CELL CYCLE ARREST; CELL CYCLE REGULATION; CONTROLLED STUDY; FEMALE; GENOMIC INSTABILITY; LYMPHOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RADIOSENSITIVITY; THYMOCYTE;

ANIMALS; BENZ(A)ANTHRACENES; CELL AGING; CELL CYCLE PROTEINS; CELLS, CULTURED; EMBRYO, MAMMALIAN; FEMALE; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOMIC INSTABILITY; KAPLAN-MEIER ESTIMATE; LYMPHOMA; MALE; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THYMOCYTES; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 84867119889     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-1484     Document Type: Article

References (47)

1. Lukas J, Lukas C, Bartek J. More than just a focus: the chromatin response to DNA damage and its role in genome integrity maintenance. Nat Cell Biol 2011;13:1161-9.
2. Bohgaki T, Bohgaki M, Cardoso R, Panier S, Zeegers D, Li L, et al. Genomic instability, defective spermatogenesis, immunodeficiency, and cancer in a mouse model of the RIDDLE syndrome. PLoS Genet 2011;7:e1001381.
3. McKinnon PJ, Caldecott KW. DNA strand break repair and human genetic disease. Ann Rev Genomics Human Genetics 2007;8:37-55.
4. Moraes MC, Neto JB, Menck CF. DNA repair mechanisms protect our genome from carcinogenesis. Front Biosci 2012;17:1362-88.
5. Rebbeck TR, Mitra N, Domchek SM, Wan F, Friebel TM, Tran TV, et al. Modification of BRCA1-associated breast and ovarian cancer risk by BRCA1-interacting genes. Cancer Res 2011;71:5792-805.
6. Polo SE, Jackson SP. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev 2011;25:409-33.
7. Yan J, Jetten AM. RAP80 and RNF8, key players in the recruitment of repair proteins to DNA damage sites. Cancer Lett 2008;271:179-90.
8. Huen MS, Chen J. The DNA damage response pathways: at the crossroad of protein modifications. Cell Res 2008;18:8-16.
9. Kastan MB, Bartek J. Cell-cycle checkpoints and cancer. Nature 2004;432:316-23. (Pubitemid 39551659)
10. Roy R, Chun J, Powell SN. BRCA1 and BRCA2: different roles in a common pathway of genome protection. Nat Rev Cancer 2012;12:68-78.
11. Bekker-Jensen S, Mailand N. Assembly and function of DNA double-strand break repair foci in mammalian cells. DNA Repair (Amst) 2010;9:1219-28.
12. Greenberg RA. Histone tails: directing the chromatin response to DNA damage. FEBS Lett 2011;585:2883-90.
13. Yan J, Kim YS, Yang XP, Albers M, Koegl M, Jetten AM. Ubiquitin-interaction motifs of RAP80 are critical in its regulation of estrogen receptor alpha. Nucleic Acids Res 2007;35:1673-86. (Pubitemid 46592886)
14. Yan J, Kim YS, Yang XP, Li LP, Liao G, Xia F, et al. The ubiquitin-interacting motif containing protein RAP80 interacts with BRCA1 and functions in DNA damage repair response. Cancer Res 2007;67:6647-56. (Pubitemid 47105510)
15. Liu Z, Wu J, Yu X. CCDC98 targets BRCA1 to DNA damage sites. Nat Struct Mol Biol 2007;14:716-20. (Pubitemid 47220064)
16. Sobhian B, Shao G, Lilli DR, Culhane AC, Moreau LA, Xia B, et al. RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 2007;316:1198-202. (Pubitemid 46877483)
17. Wang B, Matsuoka S, Ballif BA, Zhang D, Smogorzewska A, Gygi SP, et al. Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 2007;316:1194-8. (Pubitemid 46877482)
18. Yan J, Menendez D, Yang XP, Resnick MA, Jetten AM. A regulatory loop composed of RAP80-HDM2-p53 provides RAP80-enhanced p53 degradation by HDM2 in response to DNA damage. J Biol Chem 2009;284:19280-9.
19. Kim H, Chen J, Yu X. Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 2007;316:1202-5. (Pubitemid 46877484)
20. Strauss C, Halevy T, Macarov M, Argaman L, Goldberg M. MDC1 is ubiquitylated on its tandem BRCT domain and directly binds RAP80 in a UBC13-dependent manner. DNA Repair (Amst) 2011;10:806-14.
21. Nikkila J, Coleman KA, Morrissey D, Pylkas K, Erkko H, Messick TE, et al. Familial breast cancer screening reveals an alteration in the RAP80 UIM domain that impairs DNA damage response function. Oncogene 2009;28:1843-52.
22. Medina D, Butel JS, Socher SH, Miller FL. Mammary tumorigenesis in 7,12-dimethybenzanthracene-treated C57BL x DBA/2f F1 mice. Cancer Res 1980;40:368-73. (Pubitemid 10140165)
23. McElroy SL, Reijo Pera RA. Preparation of mouse embryonic fibroblast feeder cells for human embryonic stem cell culture. CSH Protoc 2008;2008:pdb prot5041.
24. Takeda Y, Kang HS, Angers M, Jetten AM. Retinoic acid-related orphan receptor gamma directly regulates neuronal PAS domain protein 2 transcription in vivo. Nucleic Acids Res 2011;39:4769-82.
25. Yan J, Yang XP, Kim YS, Jetten AM. RAP80 responds to DNA damage induced by both ionizing radiation and UV irradiation and is phosphorylated at Ser205. Cancer Res 2008;68:4269-76.
26. Lu LY, Wu J, Ye L, Gavrilina GB, Saunders TL, Yu X. RNF8-dependent histone modifications regulate nucleosome removal during spermatogenesis. Dev Cell 2010;18:371-84.
27. Santos MA, Huen MS, Jankovic M, Chen HT, Lopez-Contreras AJ, Klein IA, et al. Class switching and meiotic defects in mice lacking the E3 ubiquitin ligase RNF8. J Exp Med 2010;207:973-81.
28. Cao L, Li W, Kim S, Brodie SG, Deng CX. Senescence, aging, and malignant transformation mediated by p53 in mice lacking the Brca1 full-length isoform. Genes Dev 2003;17:201-13. (Pubitemid 36105893)
29. Wang YA, Elson A, Leder P. Loss of p21 increases sensitivity to ionizing radiation and delays the onset of lymphoma in atm-deficient mice. Proc Natl Acad Sci U S A 1997;94:14590-5. (Pubitemid 28041418)
30. Hu Y, Scully R, Sobhian B, Xie A, Shestakova E, Livingston DM. RAP80-directed tuning of BRCA1 homologous recombination function at ionizing radiation-induced nuclear foci. Genes Dev 2011;25:685-700.
31. Levine AJ, Oren M. The first 30 years of p53: growing ever more complex. Nat Rev Cancer 2009;9:749-58.
32. Toledo F, Wahl GM. Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat Rev Cancer 2006;6:909-23. (Pubitemid 44862676)
33. Celeste A, Petersen S, Romanienko PJ, Fernandez-Capetillo O, Chen HT, Sedelnikova OA, et al. Genomic instability in mice lacking histone H2AX. Science 2002;296:922-7. (Pubitemid 34464900)
34. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998;273:5858-68. (Pubitemid 28124064)
35. Donehower LA, Godley LA, Aldaz CM, Pyle R, Shi YP, Pinkel D, et al. The role of p53 loss in genomic instability and tumor progression in a murine mammary cancer model. Prog Clin Biol Res 1996;395:1-11.
36. Narod SA, Foulkes WD. BRCA1 and BRCA2: 1994 and beyond. Nat Rev Cancer 2004;4:665-76. (Pubitemid 39215065)
37. Backlund MG, Trasti SL, Backlund DC, Cressman VL, Godfrey V, Koller BH. Impact of ionizing radiation and genetic background on mammary tumorigenesis in p53-deficient mice. Cancer Res 2001;61:6577-82. (Pubitemid 32783267)
38. Argov S, Cochran AJ, Karre K, Klein GO, Klein G. Incidence and type of tumors induced in C57BL bg/bg mice and +/bg littermates by oral administration of DMBA. Int J Cancer. 1981;28:739-46. (Pubitemid 12245899)
39. Shao G, Lilli DR, Patterson-Fortin J, Coleman KA, Morrissey DE, Greenberg RA. The Rap80-BRCC36 de-ubiquitinating enzyme complex antagonizes RNF8-Ubc13-dependent ubiquitination events at DNA double strand breaks. Proc Natl Acad Sci U S A 2009;106:3166-71.
40. Coleman KA, Greenberg RA. The BRCA1-RAP80 complex regulates DNA repair mechanism utilization by restricting end resection. J Biol Chem 2011;286:13669-80.
41. Wu J, Liu C, Chen J, Yu X. RAP80 protein is important for genomic stability and is required for stabilizing BRCA1-A complex at DNA damage sites in vivo. J Biol Chem 2012;287:22919-26.
42. Chang F, Syrjanen S, Tervahauta A, Syrjanen K. Tumourigenesis associated with the p53 tumour suppressor gene. Br J Cancer 1993;68:653-61. (Pubitemid 23301263)
43. McAllister KA, Houle CD, Malphurs J, Ward T, Collins NK, Gersch W, et al. Spontaneous and irradiation-induced tumor susceptibility in BRCA2 germline mutant mice and cooperative effects with a p53 germline mutation. Toxicol Pathol 2006;34:187-98.
44. Hollestelle A, Wasielewski M, Martens JW, Schutte M. Discovering moderate-risk breast cancer susceptibility genes. Curr Opin Genet Dev 2010;20:268-76.
45. Osorio A, Barroso A, Garcia MJ, Martinez-Delgado B, Urioste M, Benitez J. Evaluation of the BRCA1 interacting genes RAP80 and CCDC98 in familial breast cancer susceptibility. Breast Cancer Res Treat 2009;113:371-6.
46. Novak DJ, Sabbaghian N, Maillet P, Chappuis PO, Foulkes WD, Tischkowitz M. Analysis of the genes coding for the BRCA1-interacting proteins, RAP80 and Abraxas (CCDC98), in high-risk, non-BRCA1/2, multiethnic breast cancer cases. Breast Cancer Res Treat 2009;117:453-9.
47. Akbari MR, Ghadirian P, Robidoux A, Foumani M, Sun Y, Royer R, et al. Germline RAP80 mutations and susceptibility to breast cancer. Breast Cancer Res Treat 2009;113:377-81.