MDC1 and RNF8 function in a pathway that directs BRCA1-dependent localization of PALB2 required for homologous recombination

Journal of Cell Science

Volumn 125, Issue 24, 2012, Pages 6049-6057

  Zhang, Fan ^a   Bick, Gregory ^a   Park, Jung Young ^a   Andreassen, Paul R ^a,b  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

BRCA1; BRCT repeats; DNA repair; Homologous recombination; PALB2

Indexed keywords

BRCA1 PROTEIN; BRCT PALB2 PROTEIN; HETERODIMER; HOMODIMER; HYBRID PROTEIN; MDC 1 PROTEIN; MITOMYCIN; NUCLEIC ACID BINDING PROTEIN; PALB 2 PROTEIN; RAD51 PROTEIN; RNF 8 PROTEIN; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; MDC1 PROTEIN, HUMAN; NUCLEAR PROTEIN; PALB2 PROTEIN, HUMAN; RNF8 PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; BREAST TUMOR; GENETICS; MALE; METABOLISM; TUMOR CELL LINE;

BRCA1 PROTEIN; BREAST NEOPLASMS; CELL LINE, TUMOR; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; HOMOLOGOUS RECOMBINATION; HUMANS; MALE; NUCLEAR PROTEINS; TRANS-ACTIVATORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84871566041     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.111872     Document Type: Article

References (47)

1. Akbari, M. R., Ghadirian, P., Robidoux, A., Foumani, M., Sun, Y., Royer, R., Zandvakili, I., Lynch, H. and Narod, S. A. (2009). Germline RAP80 mutations and susceptibility to breast cancer. Breast Cancer Res. Treat. 113, 377-381.
2. Brodie, K. M. and Henderson, B. R. (2010). Differential modulation of BRCA1 and BARD1 nuclear localisation and foci assembly by DNA damage. Cell. Signal. 22, 291-302.
3. Buisson, R., Dion-Côté, A. M., Coulombe, Y., Launay, H., Cai, H., Stasiak, A. Z., Stasiak, A., Xia, B. and Masson, J. Y. (2010). Cooperation of breast cancer proteins PALB2 and piccolo BRCA2 in stimulating homologous recombination. Nat. Struct. Mol. Biol. 17, 1247-1254.
4. Chen, L., Nievera, C. J., Lee, A. Y. and Wu, X. (2008). Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J. Biol. Chem. 283, 7713-7720.
5. Coleman, K. A. and Greenberg, R. A. (2011). The BRCA1-RAP80 complex regulates DNA repair mechanism utilization by restricting end resection. J. Biol. Chem. 286, 13669-13680.
6. Dray, E., Etchin, J., Wiese, C., Saro, D., Williams, G. J., Hammel, M., Yu, X., Galkin, V. E., Liu, D., Tsai, M. S. et al. (2010). Enhancement of RAD51 recombinase activity by the tumor suppressor PALB2. Nat. Struct. Mol. Biol. 17, 1255-1259.
7. Erkko, H., Xia, B., Nikkilä, J., Schleutker, J., Syrjäkoski, K., Mannermaa, A., Kallioniemi, A., Pylkäs, K., Karppinen, S. M., Rapakko, K. et al. (2007). A recurrent mutation in PALB2 in Finnish cancer families. Nature 446, 316-319.
8. Ganesan, S., Silver, D. P., Greenberg, R. A., Avni, D., Drapkin, R., Miron, A., Mok, S. C., Randrianarison, V., Brodie, S., Salstrom, J. et al. (2002). BRCA1 supports XIST RNA concentration on the inactive X chromosome. Cell 111, 393-405.
9. Gayther, S. A., Harrington, P., Russell, P., Kharkevich, G., Garkavtseva, R. F., Ponder, B. A.; UKCCCR Familial Ovarian Cancer Study Group (1996). Rapid detection of regionally clustered germ-line BRCA1 mutations by multiplex heteroduplex analysis. Am. J. Hum. Genet. 58, 451-456.
10. Hu, Y., Scully, R., Sobhian, B., Xie, A., Shestakova, E. and Livingston, D. M. (2011). RAP80-directed tuning of BRCA1 homologous recombination function at ionizing radiation-induced nuclear foci. Genes Dev. 25, 685-700.
11. Huang, J., Huen, M. S., Kim, H., Leung, C. C., Glover, J. N., Yu, X. and Chen, J. (2009). RAD18 transmits DNA damage signalling to elicit homologous recombination repair. Nat. Cell Biol. 11, 592-603.
12. Huen, M. S., Grant, R., Manke, I., Minn, K., Yu, X., Yaffe, M. B. and Chen, J. (2007). RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131, 901-914.
13. Huen, M. S., Sy, S. M. and Chen, J. (2010). BRCA1 and its toolbox for the maintenance of genome integrity. Nat. Rev. Mol. Cell Biol. 11, 138-148.
14. Kim, H., Chen, J. and Yu, X. (2007a). Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 316, 1202-1205.
15. Kim, H., Huang, J. and Chen, J. (2007b). CCDC98 is a BRCA1-BRCT domainbinding protein involved in the DNA damage response. Nat. Struct. Mol. Biol. 14, 710-715.
16. Kolas, N. K., Chapman, J. R., Nakada, S., Ylanko, J., Chahwan, R., Sweeney, F. D., Panier, S., Mendez, M., Wildenhain, J., Thomson, T. M. et al. (2007). Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318, 1637-1640.
17. Liu, Z., Wu, J. and Yu, X. (2007). CCDC98 targets BRCA1 to DNA damage sites. Nat. Struct. Mol. Biol. 14, 716-720.
18. Lou, Z., Chini, C. C., Minter-Dykhouse, K. and Chen, J. (2003). Mediator of DNA damage checkpoint protein 1 regulates BRCA1 localization and phosphorylation in DNA damage checkpoint control. J. Biol. Chem. 278, 13599-13602.
19. Mailand, N., Bekker-Jensen, S., Faustrup, H., Melander, F., Bartek, J., Lukas, C. and Lukas, J. (2007). RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131, 887-900.
20. Martin, R. W., Orelli, B. J., Yamazoe, M., Minn, A. J., Takeda, S. and Bishop, D. K. (2007). RAD51 up-regulation bypasses BRCA1 function and is a common feature of BRCA1-deficient breast tumors. Cancer Res. 67, 9658-9665.
21. Moynahan, M. E. and Jasin, M. (2010). Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat. Rev. Mol. Cell Biol. 11, 196- 207.
22. Moynahan, M. E., Cui, T. Y. and Jasin, M. (2001). Homology-directed dna repair, mitomycin-c resistance, and chromosome stability is restored with correction of a Brca1 mutation. Cancer Res. 61, 4842-4850.
23. Nikkilä, J., Coleman, K. A., Morrissey, D., Pylkäs, K., Erkko, H., Messick, T. E., Karppinen, S. M., Amelina, A., Winqvist, R. and Greenberg, R. A. (2009). Familial breast cancer screening reveals an alteration in the RAP80 UIM domain that impairs DNA damage response function. Oncogene 28, 1843-1852.
24. Oliver, A. W., Swift, S., Lord, C. J., Ashworth, A. and Pearl, L. H. (2009). Structural basis for recruitment of BRCA2 by PALB2. EMBO Rep. 10, 990-996.
25. Rahman, N., Seal, S., Thompson, D., Kelly, P., Renwick, A., Elliott, A., Reid, S., Spanova, K., Barfoot, R., Chagtai, T. et al.; Breast Cancer Susceptibility Collaboration (UK) (2007). PALB2, which encodes a BRCA2-interacting protein, is a breast cancer susceptibility gene. Nat. Genet. 39, 165-167.
26. Reid, S., Schindler, D., Hanenberg, H., Barker, K., Hanks, S., Kalb, R., Neveling, K., Kelly, P., Seal, S., Freund, M. et al. (2007). Biallelic mutations in PALB2 cause Fanconi anemia subtype FA-N and predispose to childhood cancer. Nat. Genet. 39, 162-164.
27. Reid, L. J., Shakya, R., Modi, A. P., Lokshin, M., Cheng, J. T., Jasin, M., Baer, R. and Ludwig, T. (2008). E3 ligase activity of BRCA1 is not essential for mammalian cell viability or homology-directed repair of double-strand DNA breaks. Proc. Natl. Acad. Sci. USA 105, 20876-20881.
28. Sartori, A. A., Lukas, C., Coates, J., Mistrik, M., Fu, S., Bartek, J., Baer, R., Lukas, J. and Jackson, S. P. (2007). Human CtIP promotes DNA end resection. Nature 450, 509-514.
29. Scully, R., Ganesan, S., Vlasakova, K., Chen, J., Socolovsky, M. and Livingston, D. M. (1999). Genetic analysis of BRCA1 function in a defined tumor cell line. Mol. Cell 4, 1093-1099.
30. Shakya, R., Reid, L. J., Reczek, C. R., Cole, F., Egli, D., Lin, C. S., deRooij, D. G., Hirsch, S., Ravi, K., Hicks, J. B. et al. (2011). BRCA1 tumor suppression depends on BRCT phosphoprotein binding, but not its E3 ligase activity. Science 334, 525- 528.
31. Sobhian, B., Shao, G., Lilli, D. R., Culhane, A. C., Moreau, L. A., Xia, B., Livingston, D. M. and Greenberg, R. A. (2007). RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 316, 1198-1202.
32. Stewart, G. S., Wang, B., Bignell, C. R., Taylor, A. M. and Elledge, S. J. (2003). MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421, 961- 966.
33. Stucki, M., Clapperton, J. A., Mohammad, D., Yaffe, M. B., Smerdon, S. J. and Jackson, S. P. (2005). MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123, 1213-1226.
34. Sy, S. M., Huen, M. S. and Chen, J. (2009a). PALB2 is an integral component of the BRCA complex required for homologous recombination repair. Proc. Natl. Acad. Sci. USA 106, 7155-7160.
35. Sy, S. M., Huen, M. S., Zhu, Y. and Chen, J. (2009b). PALB2 regulates recombinational repair through chromatin association and oligomerization. J. Biol. Chem. 284, 18302-18310.
36. Wang, B., Matsuoka, S., Ballif, B. A., Zhang, D., Smogorzewska, A., Gygi, S. P. and Elledge, S. J. (2007). Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 316, 1194-1198.
37. Wu, J., Huen, M. S., Lu, L. Y., Ye, L., Dou, Y., Ljungman, M., Chen, J. and Yu, X. (2009). Histone ubiquitination associates with BRCA1-dependent DNA damage response. Mol. Cell. Biol. 29, 849-860.
38. Xia, B., Sheng, Q., Nakanishi, K., Ohashi, A., Wu, J., Christ, N., Liu, X., Jasin, M., Couch, F. J. and Livingston, D. M. (2006). Control of BRCA2 cellular and clinical functions by a nuclear partner, PALB2. Mol. Cell 22, 719-729.
39. Xia, B., Dorsman, J. C., Ameziane, N., de Vries, Y., Rooimans, M. A., Sheng, Q., Pals, G., Errami, A., Gluckman, E., Llera, J. et al. (2007). Fanconi anemia is associated with a defect in the BRCA2 partner PALB2. Nat. Genet. 39, 159-161.
40. Yoo, H. Y., Kumagai, A., Shevchenko, A., Shevchenko, A. and Dunphy, W. G. (2009). The Mre11-Rad50-Nbs1 complex mediates activation of TopBP1 by ATM. Mol. Biol. Cell 20, 2351-2360.
41. Yu, X. and Chen, J. (2004). DNA damage-induced cell cycle checkpoint control requires CtIP, a phosphorylation-dependent binding partner of BRCA1 C-terminal domains. Mol. Cell. Biol. 24, 9478-9486.
42. Yu, X., Wu, L. C., Bowcock, A. M., Aronheim, A. and Baer, R. (1998). The Cterminal (BRCT) domains of BRCA1 interact in vivo with CtIP, a protein implicated in the CtBP pathway of transcriptional repression. J. Biol. Chem. 273, 25388-25392.
43. Yu, X., Chini, C. C., He, M., Mer, G. and Chen, J. (2003). The BRCT domain is a phospho-protein binding domain. Science 302, 639-642.
44. Zhang, J., Ma, Z., Treszezamsky, A. and Powell, S. N. (2005). MDC1 interacts with Rad51 and facilitates homologous recombination. Nat. Struct. Mol. Biol. 12, 902-909.
45. Zhang, F., Fan, Q., Ren, K. and Andreassen, P. R. (2009a). PALB2 functionally connects the breast cancer susceptibility proteins BRCA1 and BRCA2. Mol. Cancer Res. 7, 1110-1118.
46. Zhang, F., Ma, J., Wu, J., Ye, L., Cai, H., Xia, B. and Yu, X. (2009b). PALB2 links BRCA1 and BRCA2 in the DNA-damage response. Curr. Biol. 19, 524-529.
47. Zhang, F., Fan, Q., Ren, K., Auerbach, A. D. and Andreassen, P. R. (2010). FANCJ/ BRIP1 recruitment and regulation of FANCD2 in DNA damage responses. Chromosoma 119, 637-649.