BRCA1 is required for common-fragile-site stability via its G2/M checkpoint function

Molecular and Cellular Biology

Volumn 24, Issue 15, 2004, Pages 6701-6709

  Arlt, Martin F ^a   Xu, Bo ^b   Durkin, Sandra G ^a   Casper, Anne M ^a   Kastan, Michael B ^c   Glover, Thomas W ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATR PROTEIN; BRCA1 PROTEIN; DNA; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CANCER CELL; CELL CYCLE G2 PHASE; CELL CYCLE PHASE; CHROMOSOME FRAGILE SITE; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; DNA SYNTHESIS INHIBITION; GENE MUTATION; HUMAN; HUMAN CELL; MITOSIS; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; RNA INTERFERENCE; TUMOR SUPPRESSOR GENE;

ANIMALS; BINDING SITES; BRCA1 PROTEIN; CELL LINE, TUMOR; CHROMOSOME FRAGILE SITES; CHROMOSOME FRAGILITY; DNA DAMAGE; FLOW CYTOMETRY; G2 PHASE; GENES, BRCA1; HUMANS; MICE; MICROSCOPY, FLUORESCENCE; MITOSIS; MUTATION; NEOPLASMS; PRECIPITIN TESTS; RNA INTERFERENCE; TRANSFECTION;

ANIMALIA;

EID: 3242712112     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.15.6701-6709.2004     Document Type: Article

References (48)

1. Arlt, M. F., D. E. Miller, D. G. Beer, and T. W. Glover. 2002. Molecular characterization of FRAXB and comparative common fragile site instability in cancer cells. Genes Chromosomes Cancer 33:82-92.
2. Brown, E. J., and D. Baltimore. 2003. Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes Dev. 17:615-628.
3. Casper, A. M., P. Nghiem, M. F. Arit, and T. W. Glover. 2002. ATR regulates fragile site stability. Cell 111:779-789.
4. Cha, R. S., and N. Kleckner. 2002. ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 297:602-606.
5. Cliby, W. A., C. J. Roberts, K. A. Cimprich, C. M. Stringer, J. R. Lamb, S. L. Schreiber, and S. H. Friend. 1998. Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints. EMBO J. 17:159-169.
6. Coquelle, A., E. Pipiras, F. Toledo, G. Buttin, and M. Debatisse. 1997. Expression of fragile sites triggers intrachromosomal mammalian gene amplification and sets boundaries to early amplicons. Cell 89:215-225.
7. Cortez, D., S. Guntuku, J. Qin, and S. J. Elledge. 2001. ATR and ATRIP: partners in checkpoint signaling. Science 294:1713-1716.
8. Cortez, D., Y. Wang, J. Qin, and S. J. Elledge. 1999. Requirement of ATM-dependent phosphorylation of Brca1 in the DNA damage response to double-strand breaks. Science 286:1162-1166.
9. Feijoo, C., C. Hall-Jackson, R. Wu, D. Jenkins, J. Leitch, D. M. Gilbert, and C. Smythe. 2001. Activation of mammalian Chk1 during DNA replication arrest: a role for Chk1 in the intra-S phase checkpoint monitoring replication origin firing. J. Cell Biol. 154:913-923.
10. Gatei, M., B.-B. Zhou, K. Hobson, S. Scott, D. Young, and K. K. Khanna. 2001. Ataxia telangiectasia mutated (ATM) kinase and ATM and Rad3 related kinase mediate phosphorylation of Brca1 at distinct and overlapping sites. J. Biol. Chem. 276:17276-17280.
11. Glover, T. W., C. Berger, J. Coyle, and B. Echo. 1984. DNA polymerase α inhibition by aphidicolin induces gaps and breaks at common fragile sites in human chromosomes. Hum. Genet. 67:136-142.
12. Glover, T. W., J. F. Coyle-Morris, F. P. Li, R. S. Brown, C. S. Berger, R. M. Gemmill, and F. Hecht. 1988. Translocation t(3;8)(p14.2;q24.1) in renal cell carcinoma affects expression of the common fragile site at 3p14(FRA3B) in lymphocytes. Cancer Genet. Cytogenet. 31:69-73.
13. Glover, T. W., A. W. Hoge, D. E. Miller, J. E. Ascara-Wilke, A. N. Adam, S. L. Dagenais, C. M. Wilke, H. A. Dierick, and D. G. Beer. 1998. The murine Fhit gene is highly similar to its human orthologue and maps to a common fragile site region. Cancer Res. 58:3409-3414.
14. Glover, T. W., and C. K. Stein. 1987. Induction of sister chromatid exchanges at common fragile sites. Am. J. Hum. Genet. 41:882-890.
15. Guo, Z., A. Kumagai, S. X. Wang, and W. G. Dunphy. 2000. Requirement for Atr in phosphorylation of Chk1 and cell cycle regulation in response to DNA replication blocks and UV-damaged DNA in Xenopus egg extracts. Genes Dev. 14:2745-2756.
16. Huang, H., J. Qian, J. Proffit, K. Wilber, R. Jenkins, and D. I. Smith. 1998. FRA7G extends over a broad region: coincidence of human endogenous retroviral sequences (HERV-H) and small polydispersed circular DNAs (spcDNA) and fragile sites. Oncogene 16:2311-2319.
17. Huang, H., C. P. Reed, A. Mordi, G. Lomberk, L. Wang, V. Shridhar, L. Hartmann, R. Jenkins, and D. I. Smith. 1999. Frequent deletions within FRA7G at 7q31.2 in invasive epithelial ovarian cancer. Genes Chromosomes Cancer 24:48-55.
18. Lallas, T. A., T. E. Buekers, and R. E. Buller. 1999. BRCA1 mutations in familial ovarian cancer. Mol. Gen. Metabol. 67:357-363.
19. Le Beau, M. M., F. V. Rassool, M. E. Neilly, R. Espinosa III, T. W. Glover, D. I. Smith, and T. W. McKeithan. 1998. Replication of a common fragile site, FRA3B, occurs late in S phase and is delayed further upon induction: implications for the mechanism of fragile site induction. Hum. Mol. Genet. 7:755-761.
20. 2/M DNA damage checkpoint. Genes Dev. 14:1448-1459.
21. Mangeisdorf, M., K. Ried, E. Woollatt, S. Dayan, H. Eyre, M. Finnis, L. Hobson, J. Nancarrow, D. Venter, E. Baker, and R. I. Richards. 2000. Chromosomal fragile site FRA16D and DNA instability in cancer. Cancer Res. 60:1683-1689.
22. Matsuyama, A., T. Shiraishi, F. Trapasso, T. Kuroki, H. Alder, M. Mori, K. Huebner, and C. M. Croce. 2003. Fragile site orthologs FH1T/FRA3B and Fhit/Fra14A2: evolutionarily conserved but highly recombinogenic. Proc. Natl. Acad. Sci. USA 100:14988-14993.
23. Michael, D., D. G. Beer, C. W. Wilke, D. E. Miller, and T. W. Glover. 1997. Frequent deletions of FHIT and FRA3B in Barrett's metaplasia and esophageal adenocarcinomas. Oncogene 15:1653-1659.
24. Mimori, K., T. Druck, H. Inoue, H. Alder, L. Berk, M. Mori, K. Huebner, and C. M. Croce. 1999. Cancer-specific chromosome alterations in the constitutive fragile region FRA3B. Proc. Natl. Acad. Sci. USA 96:7456-7461.
25. Mishmar, D., Y. Mandel-Gutfreund, H. Margalit, A. Rahat, and B. Kerem. 1999. Common fragile sites: G-band characteristics within an R-band. Am. J. Hum. Genet. 64:908-910.
26. Mishmar, D., A. Rahat, S. W. Scherer, G. Nyakatura, B. Hinzmann, Y. Kohwi, Y. Mandel-Gutfroint, J. R. Lee, B. Drescher, D. E. Sas, H. Margalit, M. Platzer, A. Weiss, L. C. Tsui, A. Rosenthal, and B. Kerem. 1998. Molecular characterization of a common fragile site (FRA7H) on human chromosome 7 by the cloning of a simian virus 40 integration site. Proc. Natl. Acad. Sci. USA 95:8141-8146.
27. Morelli, C., E. Karayianni, C. Magnanini, A. J. Mungall, E. Thorland, M. Negrini, D. I. Smith, and G. Barbanti-Brodano. 2002. Cloning and characterization of the common fragile site FRA6F harboring a replicative senescence gene and frequently deleted in human tumors. Oncogene 21:7266-7276.
28. Negrini, M., C. Monaco, I. Vorechovsky, M. Ohta, T. Druck, R. Baffa, K. Huebner, and C. M. Croce. 1996. The FHIT gene at 3p14.2 is abnormal in breast carcinomas. Cancer Res. 56:3173-3179.
29. 1 checkpoint-deficient cells to lethal premature chromatin condensation. Proc. Natl. Acad. Sci. USA 98:9092-9097.
30. Ohta, M., H. Inoue, M. G. Cotticelli, K. Kastury, R. Baffa, J. Palazzo, Z. Siprashvili, M. Mori, P. McCue, T. Druck, C. M. Croce, and K. Huebner. 1996. The FHITgene, spanning the chromosome 3p14.2 fragile site and renal carcinoma-associated t(3;8) breakpoint, is abnormal in digestive tract cancers. Cell 84:587-597.
31. Okada, S., and T. Ouchi. 2003. Cell cycle differences in DNA damage-induced BRCA1 phosphorylation affect its subcellular localization. J. Biol. Chem. 278:2015-2020.
32. Rassool, F. V., T. W. McKeithan, M. E. Neilly, E. van Melle, R. Espinosa III, and M. M. Le Beau. 1991. Preferential integration of marker DNA into the chromosomal fragile site at 3p14: an approach to cloning fragile sites. Proc. Natl. Acad. Sci. USA 88:6657-6661.
33. Ried, K., M. Finnis, L. Hobson, M. Mangelsdorf, S. Sayan, J. K. Nancarrow, E. Woollatt, G. Kremmidiotis, A. Gardner, D. Venter, E. Baker, and R. I. Richards. 2000. Common chromosomal fragile site FRA16D sequence: identification of the FOR gene spanning FRA16D and homozygous deletions and translocation breakpoints in cancer cells. Hum. Mol. Genet. 9:1651-1663.
34. 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.
35. Scully, R., S. Ganesan, M. Brown, J. A. De Caprio, S. A. Cannistra, J. Feunteun, S. Schnitt, and D. M. Livingston. 1996. Location of BRCA1 in human breast and ovarian cancer cells. Science 272:123-126.
36. Tibbetts, R. S., D. Cortez, K. M. Brumbaugh, R. Scully, D. Livingston, S. J. Elledge, and R. T. Abraham. 2000. Functional interactions between BRCA1 and the checkpoint kinase ATR during genotoxic stress. Genes Dev. 14:2989-3002.
37. Tomlinson, G. E., T. T.-L. Chen, V. A. Stastny, A. K. Virmani, M. A. Spillman, V. Tonk, J. L. Blum, N. R. Schneider, I. I. Wistuba, J. W. Shay, J. D. Minna, and A. F. Gazdar. 1998. Characterization of a breast cancer cell line derived from a germ-line BRCA1 mutation carrier. Cancer Res. 58:3237-3242.
38. Turner, B. C., M. Ottey, D. B. Zimonjic, M. Potoczek, W. W. Hauck, E. Pequignot, C. L. Keck-Waggoner, C. Devignani, C. M. Aldaz, P. A. McCue, J. Palazzo, K. Huebner, and N. C. Popescu. 2002. The fragile histidine triad/common chromosome fragile site 3B locus and repair-deficient cancers. Cancer Res. 62:4054-4060.
39. Wang, L., J. Darling, J.-S. Zhang, H. Huang, W. Liu, and D. I. Smith. 1999. Allele-specific late replication and fragility of the most active common fragile site, FRA3B. Hum. Mol. Genet. 8:431-437.
40. Wang, L., W. Paradee, C. Mullins, R. Shridhar, R. Rosati, C. M. Wilke, T. W. Glover, and D. I. Smith. 1997. Aphidicolin-induced FRA3B breakpoints cluster in two distinct regions. Genomics 41:485-488.
41. Wilke, C. M., B. K. Hall, A. Hoge, W. Paradee, D. I. Smith, and T. W. Glover. 1996. FRA3B extends over a broad region and contains a spontaneous HPV16 integration site: direct evidence for the coincidence of viral integration sites and fragile sites. Hum. Mol. Genet. 5:187-195.
42. Wilson, C. A., L. Ramos, M. R. Villaseñor, K. H. Anders, M. F. Press, K. Clarke, B. Karlan, Chen-Jun-Jie, R. Scully, D. Livingston, R. H. Zuch, M. H. Kanter, S. Cohen, F. J. Calzone, and D. J. Slamon. 1999. Localization of human BRCA1 and its loss in high-grade, non-inherited breast carcinomas. Nat. Genet. 21:236-240.
43. 2-phase checkpoints after ionizing irradiation. Mol. Cell. Biol. 21:3445-3450.
44. Xu, B., A. H. O'Donnell, S. T. Kim, and M. B. Kastan. 2002. Phosphorylation of serine 1387 in Brca1 is specifically required for the Atm-mediated S-phase checkpoint after ionizing irradiation. Cancer Res. 62:4588-4591.
45. Yamane, K., J. Chen, and T. J. Kinsella. 2003. Both DNA topoisomerase II-binding protein 1 and BRCA1 regulate the G2-M cell cycle checkpoint. Cancer Res. 63:3049-3053.
46. Yarden, R. I., S. Pardo-Reoyo, M. Sgagias, K. H. Cowan, and L. C. Brody. 2002. BRCA1 regulates the G2/M checkpoint by activating Chk1 kinase upon DNA damage. Nat. Genet. 30:285-289.
47. Zhao, H., and H. Piwnica-Worms. 2001. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol. Cell. Biol. 21:4129-4139.
48. Zhong, Q., T. G. Boyer, P.-L. Chen, and W.-H. Lee. 2002. Deficient nonhomologous end-joining activity in cell-free extracts from Brca1-null fibroblasts. Cancer Res. 62:3966-3970.