Activation of BRCA1/BRCA2-associated helicase BACH1 is required for timely progression through S phase

Molecular and Cellular Biology

Volumn 27, Issue 19, 2007, Pages 6733-6741

  Kumaraswamy, Easwari ^a   Shiekhattar, Ramin ^a,b  

^a WISTAR INSTITUTE   (United States)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; BRCA2 PROTEIN; HELICASE; PROTEIN BACH1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL STRAIN MCF 7; CONTROLLED STUDY; DEPHOSPHORYLATION; DNA DAMAGE; ENZYME ACTIVATION; ENZYME INACTIVATION; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; LONG TERMINAL REPEAT; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; BRCA1 PROTEIN; BRCA2 PROTEIN; CAENORHABDITIS ELEGANS; CHROMATIN; DNA DAMAGE; ENZYME ACTIVATION; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; HUMANS; MULTIPROTEIN COMPLEXES; RNA, SMALL INTERFERING; S PHASE; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES;

CAENORHABDITIS ELEGANS;

EID: 34748890424     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00961-07     Document Type: Article

References (44)

1. Alberg, A. J., A. P. Lam, and K. J. Helzlsouer. 1999. Epidemiology, prevention, and early detection of breast cancer. Curr. Opin. Oncol. 11:435-441.
2. Bork, P., K. Hofmann, P. Bucher, A. F. Neuwald, S. F. Altschul, and E. V. Koonin. 1997. A superfamily of conserved domains in DNA damage-responsive cell cycle checkpoint proteins. FASEB J. 11:68-76.
3. Bridge, W. L., C. J. Vandenberg, R. J. Franklin, and K. Hiom. 2005. The BRIP1 helicase functions independently of BRCA1 in the Fanconi anemia pathway for DNA crosslink repair. Nat. Genet. 37:953-957.
4. Callebaut, I., and J. P. Mornon. 1997. From BRCA1 to RAP1: a widespread BRCT module closely associated with DNA repair. FEBS Lett. 400:25-30.
5. Cantor, S. B., D. W. Bell, S. Ganesan, E. M. Kass, R. Drapkin, S. Grossman, D. C. Wahrer, D. C. Sgroi, W. S. Lane, D. A. Haber, and D. M. Livingston. 2001. BACH1, a novel helicase-like protein, interacts directly with BRCA1 and contributes to its DNA repair function. Cell 105:149-160.
6. Chen, Y., C. F. Chen, D. J. Riley, D. C. Allred, P. L. Chen, D. Von Hoff, C. K. Osborne, and W. H. Lee. 1995. Aberrant subcellular localization of BRCA1 in breast cancer. Science 270:789-791.
7. Cheung, I., M. Schertzer, A. Rose, and P. M. Lansdorp. 2002. Disruption of dog-1 in Caenorhabditis elegans triggers deletions upstream of guanine-rich DNA. Nat. Genet. 31:405-409.
8. Dong, Y., M. A. Hakimi, X. Chen, E. Kumaraswamy, N. S. Cooch, A. K. Godwin, and R. Shiekhattar. 2003. Regulation of BRCC, a holoenzyme complex containing BRCA1 and BRCA2, by a signalosome-like subunit and its role in DNA repair. Mol. Cell 12:1087-1099.
9. Futreal, P. A., Q. Liu, D. Shattuck-Eidens, C. Cochran, K. Harshman, S. Tavtigian, L. M. Bennett, A. Haugen-Strano, J. Swensen, Y. Miki, et al. 1994. BRCA1 mutations in primary breast and ovarian carcinomas. Science 266:120-122.
10. Hand, R., and J. German. 1975. A retarded rate of DNA chain growth in Bloom's syndrome. Proc. Natl. Acad. Sci. USA 72:758-762.
11. Hickson, I. D. 2003. RecQ helicases: caretakers of the genome. Nat. Rev. Cancer 3:169-178.
12. Ishimi, Y., Y. Komamura-Kohno, Z. You, A. Omori, and M. Kitagawa. 2000. Inhibition of Mcm4, 6, 7 helicase activity by phosphorylation with cyclin A/Cdk2. J. Biol. Chem. 275:16235-16241.
13. Karmakar, P., J. Piotrowski, R. M. Brosh, Jr., J. A. Sommers, S. P. Miller, W. H. Cheng, C. M. Snowden, D. A. Ramsden, and V. A. Bohr. 2002. Werner protein is a target of DNA-dependent protein kinase in vivo and in vitro, and its catalytic activities are regulated by phosphorylation. J. Biol. Chem. 277:18291-18302.
14. Koonin, E. V., S. F. Altschul, and P. Bork. 1996. BRCA1 protein products. Functional motifs. Nat. Genet. 13:266-268.
15. Levitus, M., Q. Waisfisz, B. C. Godthelp, Y. Vries, S. Hussain, W. W. Wiegant, E. Elghalbzouri-Maghrani, J. Steltenpool, M. A. Rooimans, G. Pals, F. Arwert, C. G. Mathew, M. Z. Zdzienicka, K. Hiom, J. P. De Winter, and H. Joenje. 2005. The DNA helicase BRIP1 is defective in Fanconi anemia complementation group J. Nat. Genet. 37:934-935.
16. Levran, O., C. Attwooll, R. T. Henry, K. L. Milton, K. Neveling, P. Rio, S. D. Batish, R. Kalb, E. Velleuer, S. Barrai, J. Ott, J. Petrini, D. Schindler, H. Hanenberg, and A. D. Auerbach. 2005. The BRCA1-interacting helicase BRIP1 is deficient in Fanconi anemia. Nat. Genet. 37:931-933.
17. Lomonosov, M., S. Anand, M. Sangrithi, R. Davies, and A. R. Venkilaraman. 2003. Stabilization of stalled DNA replication forks by the BRCA2 breast cancer susceptibility protein. Genes Dev. 17:3017-3022.
18. Lonn, U., S. Lonn, U. Nylen, G. Winblad, and J. German. 1990. An abnormal profile of DNA replication intermediates in Bloom's syndrome. Cancer Res 50:3141-3145.
19. Ludwig, T., P. Fisher, S. Ganesan, and A. Efstratiadis. 2001. Tumorigenesis in mice carrying a truncating Brca1 mutation. Genes Dev. 15:1188-1193.
20. Marmorstein, L. Y., A. V. Kinev, G. K. Chan, D. A. Bochar, H. Beniya, J. A. Epstein, T. J. Yen, and R. Shiekhattar. 2001. A human BRCA2 complex containing a structural DNA binding component influences cell cycle progression. Cell 104:247-257.
21. Mendez, J., and B. Stillman. 2000. Chromatin association of human origin recognition complex, Cdc6, and minichromosome maintenance proteins during the cell cycle: assembly of prereplication complexes in late mitosis. Mol. Cell. Biol. 20:8602-8612.
22. Menichini, P., and M. Linial. 2001. SUVi and BACH1: a new subfamily of mammalian helicases? Mutat. Res. 487:67-71.
23. Miki, Y., J. Swensen, D. Shattuck-Eidens, P. A. Futreal, K. Harshman, S. Tavtigian, Q. Liu, C. Cochran, L. M. Bennett, W. Ding, et al. 1994. A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science 266:66-71.
24. Moynahan, M. E., J. W. Chiu, B. H. Koller, and M. Jasin. 1999. Brca1 controls homology-directed DNA repair. Mol. Cell 4:511-518.
25. Nathanson, K. L., R. Wooster, B. L. Weber, and K. N. Nathanson. 2001. Breast cancer genetics: what we know and what we need. Nat. Med. 7:552-556.
26. Nuesch, J. P., S. Dettwiler, R. Corbau, and J. Rommelaere. 1998. Replicative functions of minute virus of mice NS1 protein are regulated in vitro by phosphorylation through protein kinase C. J. Virol. 72:9966-9977.
27. Poot, M., H. Hoehn, T. M. Runger, and G. M. Martin. 1992. Impaired S-phase transit of Werner syndrome cells expressed in lymphoblastoid cell lines. Exp. Cell. Res. 202:267-273.
28. Rodriguez, J. A., W. W. Au, and B. R. Henderson. 2004. Cytoplasmic mislocalization of BRCA1 caused by cancer-associated mutations in the BRCT domain. Exp. Cell. Res. 293:14-21.
29. Rodriguez, M., X. Yu, J. Chen, and Z. Songyang. 2003. Phosphopeptide binding specificities of BRCA1 COOH-terminal (BRCT) domains. J. Biol. Chem. 278:52914-52918.
30. Ruffner, H., and I. M. Verma. 1997. BRCA1 is a cell cycle-regulated nuclear phosphoprotein. Proc. Natl. Acad. Sci. USA 94:7138-7143.
31. Schultz, L. B., N. H. Chehab, A. Malikzay, and T. D. Halazonetis. 2000. p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J. Cell Biol. 151:1381-1390.
32. Scully, R., J. Chen, R. L. Ochs, K. Keegan, M. Hoekstra, J. Feunteun, and D. M. Livingston. 1997. Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 90:425-435.
33. Scully, R., S. Ganesan, K. Vlasakova, J. Chen, M. Socolovsky, and D. M. Livingston. 1999. Genetic analysis of BRCA1 function in a defined tumor cell line. Mol. Cell 4:1093-1099.
34. Sedelnikova, O. A., D. R. Pilch, C. Redon, and W. M. Bonner. 2003. Histone H2AX in DNA damage and repair. Cancer Biol Ther. 2:233-235.
35. Skibbens, R. V. 2004. Chl1p, a DNA helicase-like protein in budding yeast, functions in sister-chromatid cohesion. Genetics 166:33-42.
36. Sobhian, B., G. Shao, D. R. Lilli. A. C. Culhane, L. A. Moreau, B. Xia, D. M. Livingston, and R. A. Greenberg. 2007. RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 316:1198-1202.
37. Tavtigian, S. V., J. Simard, J. Rommens, F. Couch, D. Shattuck-Eidens, S. Neuhausen, S. Merajver, S. Thorlacius, K. Offit, D. Stoppa-Lyonnet, C. Belanger, R. Bell, S. Berry, R. Bogden, Q. Chen, T. Davis, M. Dumont, C. Frye, T. Hattier, S. Jammulapati, T. Janecki, P. Jiang, R. Kehrer, J. F. Leblanc, D. E. Goldgar, et al. 1996. The complete BRCA2 gene and mutations in chromosome 13q-linked kindreds. Nat. Genet. 12:333-337.
38. Weber, C. A., E. P. Salazar, S. A. Stewart, and L. H. Thompson. 1990. ERCC2: cDNA cloning and molecular characterization of a human nucleotide excision repair gene with high homology to yeast RAD3. EMBO J. 9:1437-1447.
39. Williams, R. S., D. I. Chasman, D. D. Hau, B. Hui, A. Y. Lau, and J. N. Glover. 2003. Detection of protein folding defects caused by BRCA1-BRCT truncation and missense mutations. J. Biol. Chem. 278:53007-53016.
40. Williams, R. S., R. Green, and J. N. Glover. 2001. Crystal structure of the BRCT repeat region from the breast cancer-associated protein BRCA1. Nat. Struct. Biol. 8:838-842.
41. Yu, X., C. C. Chini, M. He, G. Mer, and J. Chen. 2003. The BRCT domain is a phospho-protein binding domain. Science 302:639-642.
42. Zdzienicka, M. Z., and F. Arwert. 2002. Breast cancer and Fanconi anemia: what are the connections? Trends Mol. Med. 8:458-460.
43. Zgheib, O., Y. Huyen, R. A. Ditullio, Jr., A. Snyder, M. Venere, E. S. Stavridi, and T. D. Halazonetis. 2005. ATM signaling and 53BP1. Radiother Oncol. 76:119-122.
44. Zhong, Q., C. F. Chen, S. Li, Y. Chen, C. C. Wang, J. Xiao, P. L. Chen, Z. D. Sharp, and W. H. Lee. 1999. Association of BRCA1 with the hRad50-hMre11-p95 complex and the DNA damage response. Science 285:747-750.