BRCA1 Is Required for Common-Fragile-Site Stability via Its G₂/M Checkpoint Function

REFERENCES

• Arlt, M. F., Miller D. E., Beer D. G., and Glover T. W.. 2002. Molecular characterization of FRAXB and comparative common fragile site instability in cancer cells. Genes Chromosomes Cancer 33:82–92.
   PubMed Web of Science ®Google Scholar
• Brown, E. J., and Baltimore D.. 2003. Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes Dev. 17:615–628.
   PubMed Web of Science ®Google Scholar
• Casper, A. M., Nghiem P., Arlt M. F., and Glover T. W.. 2002. ATR regulates fragile site stability. Cell 111:779–789.
   PubMed Web of Science ®Google Scholar
• Cha, R. S., and Kleckner N.. 2002. ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 297:602–606.
   PubMed Web of Science ®Google Scholar
• Cliby, W. A., Roberts C. J., Cimprich K. A., Stringer C. M., Lamb J. R., Schreiber S. L., and Friend S. H.. 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.
   PubMed Web of Science ®Google Scholar
• Coquelle, A., Pipiras E., Toledo F., Buttin G., and Debatisse M.. 1997. Expression of fragile sites triggers intrachromosomal mammalian gene amplification and sets boundaries to early amplicons. Cell 89:215–225.
   PubMed Web of Science ®Google Scholar
• Cortez, D., Guntuku S., Qin J., and Elledge S. J.. 2001. ATR and ATRIP: partners in checkpoint signaling. Science 294:1713–1716.
   PubMed Web of Science ®Google Scholar
• Cortez, D., Wang Y., Qin J., and Elledge S. J.. 1999. Requirement of ATM-dependent phosphorylation of Brca1 in the DNA damage response to double-strand breaks. Science 286:1162–1166.
   PubMed Web of Science ®Google Scholar
• Feijoo, C., Hall-Jackson C., Wu R., Jenkins D., Leitch J., Gilbert D. M., and Smythe C.. 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.
   PubMed Web of Science ®Google Scholar
• Gatei, M., Zhou B.-B., Hobson K., Scott S., Young D., and Khanna K. K.. 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.
   PubMed Web of Science ®Google Scholar
• Glover, T. W., Berger C., Coyle J., and Echo B.. 1984. DNA polymerase α inhibition by aphidicolin induces gaps and breaks at common fragile sites in human chromosomes. Hum. Genet. 67:136–142.
   PubMed Web of Science ®Google Scholar
• Glover, T. W., Coyle-Morris J. F., Li F. P., Brown R. S., Berger C. S., Gemmill R. M., and Hecht F.. 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.
   PubMedGoogle Scholar
• Glover, T. W., Hoge A. W., Miller D. E., Ascara-Wilke J. E., Adam A. N., Dagenais S. L., Wilke C. M., Dierick H. A., and Beer D. G.. 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.
   PubMed Web of Science ®Google Scholar
• Glover, T. W., and Stein C. K.. 1987. Induction of sister chromatid exchanges at common fragile sites. Am. J. Hum. Genet. 41:882–890.
   PubMedGoogle Scholar
• Guo, Z., Kumagai A., Wang S. X., and Dunphy W. G.. 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.
   PubMed Web of Science ®Google Scholar
• Huang, H., Qian J., Proffit J., Wilber K., Jenkins R., and Smith D. I.. 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.
   PubMedGoogle Scholar
• Huang, H., Reed C. P., Mordi A., Lomberk G., Wang L., Shridhar V., Hartmann L., Jenkins R., and Smith D. I.. 1999. Frequent deletions within FRA7G at 7q31.2 in invasive epithelial ovarian cancer. Genes Chromosomes Cancer 24:48–55.
   PubMed Web of Science ®Google Scholar
• Lallas, T. A., Buekers T. E., and Buller R. E.. 1999. BRCA1 mutations in familial ovarian cancer. Mol. Gen. Metabol. 67:357–363.
   PubMedGoogle Scholar
• Le Beau, M. M., Rassool F. V., Neilly M. E., Espinosa III R., Glover T. W., Smith D. I., and McKeithan T. W.. 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.
   PubMedGoogle Scholar
• Liu, Q., Guntuku S., Cui X.-S., Matsuoka S., Cortez D., Tamai K., Luo G., Carattini-Rivera S., DeMayo F., Bradley A., Donehower L. A., and Elledge S. J.. 2000. Chk1 is an essential kinase that is regulated by Atr and required for the G2/M DNA damage checkpoint. Genes Dev. 14:1448–1459.
   PubMedGoogle Scholar
• Mangelsdorf, M., Ried K., Woollatt E., Dayan S., Eyre H., Finnis M., Hobson L., Nancarrow J., Venter D., Baker E., and Richards R. I.. 2000. Chromosomal fragile site FRA16D and DNA instability in cancer. Cancer Res. 60:1683–1689.
   PubMedGoogle Scholar
• Matsuyama, A., Shiraishi T., Trapasso F., Kuroki T., Alder H., Mori M., Huebner K., and Croce C. M.. 2003. Fragile site orthologs FHIT/FRA3B and Fhit/Fra14A2: evolutionarily conserved but highly recombinogenic. Proc. Natl. Acad. Sci. USA 100:14988–14993.
   PubMedGoogle Scholar
• Michael, D., Beer D. G., Wilke C. W., Miller D. E., and Glover T. W.. 1997. Frequent deletions of FHIT and FRA3B in Barrett's metaplasia and esophageal adenocarcinomas. Oncogene 15:1653–1659.
   PubMedGoogle Scholar
• Mimori, K., Druck T., Inoue H., Alder H., Berk L., Mori M., Huebner K., and Croce C. M.. 1999. Cancer-specific chromosome alterations in the constitutive fragile region FRA3B. Proc. Natl. Acad. Sci. USA 96:7456–7461.
   PubMedGoogle Scholar
• Mishmar, D., Mandel-Gutfreund Y., Margalit H., Rahat A., and Kerem B.. 1999. Common fragile sites: G-band characteristics within an R-band. Am. J. Hum. Genet. 64:908–910.
   PubMedGoogle Scholar
• Mishmar, D., Rahat A., Scherer S. W., Nyakatura G., Hinzmann B., Kohwi Y., Mandel-Gutfroint Y., Lee J. R., Drescher B., Sas D. E., Margalit H., Platzer M., Weiss A., Tsui L. C., Rosenthal A., and Kerem B.. 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.
   PubMedGoogle Scholar
• Morelli, C., Karayianni E., Magnanini C., Mungall A. J., Thorland E., Negrini M., Smith D. I., and Barbanti-Brodano G.. 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.
   PubMedGoogle Scholar
• Negrini, M., Monaco C., Vorechovsky I., Ohta M., Druck T., Baffa R., Huebner K., and Croce C. M.. 1996. The FHIT gene at 3p14.2 is abnormal in breast carcinomas. Cancer Res. 56:3173–3179.
   PubMedGoogle Scholar
• Nghiem, P., Park P. K., Kim Y.-S., Vaziri C., and Schreiber S. L.. 2001. ATR inhibition selectively sensitizes G1 checkpoint-deficient cells to lethal premature chromatin condensation. Proc. Natl. Acad. Sci. USA 98:9092–9097.
   PubMed Web of Science ®Google Scholar
• Ohta, M., Inoue H., Cotticelli M. G., Kastury K., Baffa R., Palazzo J., Siprashvili Z., Mori M., McCue P., Druck T., Croce C. M., and Huebner K.. 1996. The FHIT gene, 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.
   PubMed Web of Science ®Google Scholar
• Okada, S., and Ouchi T.. 2003. Cell cycle differences in DNA damage-induced BRCA1 phosphorylation affect its subcellular localization. J. Biol. Chem. 278:2015–2020.
   PubMedGoogle Scholar
• Rassool, F. V., McKeithan T. W., Neilly M. E., van Melle E., Espinosa III R., and Le Beau M. M.. 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.
   PubMedGoogle Scholar
• Ried, K., Finnis M., Hobson L., Mangelsdorf M., Sayan S., Nancarrow J. K., Woollatt E., Kremmidiotis G., Gardner A., Venter D., Baker E., and Richards R. I.. 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.
   PubMedGoogle Scholar
• Scully, R., Chen J., Ochs R. L., Keegan K., Hoekstra M., Feunteun J., and Livingston D. M.. 1997. Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 90:425–435.
   PubMed Web of Science ®Google Scholar
• Scully, R., Ganesan S., Brown M., De Caprio J. A., Cannistra S. A., Feunteun J., Schnitt S., and Livingston D. M.. 1996. Location of BRCA1 in human breast and ovarian cancer cells. Science 272:123–126.
   PubMed Web of Science ®Google Scholar
• Tibbetts, R. S., Cortez D., Brumbaugh K. M., Scully R., Livingston D., Elledge S. J., and Abraham R. T.. 2000. Functional interactions between BRCA1 and the checkpoint kinase ATR during genotoxic stress. Genes Dev. 14:2989–3002.
   PubMed Web of Science ®Google Scholar
• Tomlinson, G. E., Chen T. T.-L., Stastny V. A., Virmani A. K., Spillman M. A., Tonk V., Blum J. L., Schneider N. R., Wistuba I. I., Shay J. W., Minna J. D., and Gazdar A. F.. 1998. Characterization of a breast cancer cell line derived from a germ-line BRCA1 mutation carrier. Cancer Res. 58:3237–3242.
   PubMedGoogle Scholar
• Turner, B. C., Ottey M., Zimonjic D. B., Potoczek M., Hauck W. W., Pequignot E., Keck-Waggoner C. L., Devignani C., Aldaz C. M., McCue P. A., Palazzo J., Huebner K., and Popescu N. C.. 2002. The fragile histidine triad/common chromosome fragile site 3B locus and repair-deficient cancers. Cancer Res. 62:4054–4060.
   PubMedGoogle Scholar
• Wang, L., Darling J., Zhang J.-S., Huang H., Liu W., and Smith D. I.. 1999. Allele-specific late replication and fragility of the most active common fragile site, FRA3B. Hum. Mol. Genet. 8:431–437.
   PubMedGoogle Scholar
• Wang, L., Paradee W., Mullins C., Shridhar R., Rosati R., Wilke C. M., Glover T. W., and Smith D. I.. 1997. Aphidicolin-induced FRA3B breakpoints cluster in two distinct regions. Genomics 41:485–488.
   PubMedGoogle Scholar
• Wilke, C. M., Hall B. K., Hoge A., Paradee W., Smith D. I., and Glover T. W.. 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.
   PubMedGoogle Scholar
• Wilson, C. A., Ramos L., Villaseñor M. R., Anders K. H., Press M. F., Clarke K., Karlan B., Chen-Jun-Jie, Scully R., Livingston D., Zuch R. H., Kanter M. H., Cohen S., Calzone F. J., and Slamon D. J.. 1999. Localization of human BRCA1 and its loss in high-grade, non-inherited breast carcinomas. Nat. Genet. 21:236–240.
   PubMed Web of Science ®Google Scholar
• Xu, B., Kim S.-T., and Kastan M. B.. 2001. Involvement of Brca1 in S-phase and G2-phase checkpoints after ionizing irradiation. Mol. Cell. Biol. 21:3445–3450.
   PubMed Web of Science ®Google Scholar
• Xu, B., O'Donnell A. H., Kim S. T., and Kastan M. B.. 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.
   PubMed Web of Science ®Google Scholar
• Yamane, K., Chen J., and Kinsella T. J.. 2003. Both DNA topoisomerase II-binding protein 1 and BRCA1 regulate the G2-M cell cycle checkpoint. Cancer Res. 63:3049–3053.
   PubMedGoogle Scholar
• Yarden, R. I., Pardo-Reoyo S., Sgagias M., Cowan K. H., and Brody L. C.. 2002. BRCA1 regulates the G2/M checkpoint by activating Chk1 kinase upon DNA damage. Nat. Genet. 30:285–289.
   PubMed Web of Science ®Google Scholar
• Zhao, H., and Piwnica-Worms H.. 2001. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol. Cell. Biol. 21:4129–4139.
   PubMed Web of Science ®Google Scholar
• Zhong, Q., Boyer T. G., Chen P.-L., and Lee W.-H.. 2002. Deficient nonhomologous end-joining activity in cell-free extracts from Brca1-null fibroblasts. Cancer Res. 62:3966–3970.
   PubMed Web of Science ®Google Scholar