Common fragile sites as targets for chromosome rearrangements

DNA Repair

Volumn 5, Issue 9-10, 2006, Pages 1126-1135

  Arlt, Martin F ^a   Durkin, Sandra G ^a   Ragland, Ryan L ^a   Glover, Thomas W ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Cancer; Common fragile site; Replication stress; Translocations

Indexed keywords

CANCER GENETICS; CELL CYCLE; CHROMOSOMAL INSTABILITY; CHROMOSOME CONDENSATION; CHROMOSOME REARRANGEMENT; CHROMOSOME STRUCTURE; CHROMOSOME TRANSLOCATION; DNA REPAIR; DNA STRAND BREAKAGE; GENE ACTIVATION; GENE EXPRESSION; GENE REPLICATION; GENE SEQUENCE; HUMAN; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; STATISTICAL SIGNIFICANCE; TUMOR CELL;

CHROMOSOME FRAGILE SITES; CHROMOSOME FRAGILITY; CHROMOSOMES, HUMAN; GENOMIC INSTABILITY; HUMANS; MODELS, GENETIC; NEOPLASMS; TRANSLOCATION, GENETIC; TUMOR CELLS, CULTURED;

EID: 33748623634     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2006.05.010     Document Type: Review

References (96)

1. Kremer E.J., Pritchard M., Lynch M., Yu S., Holman K., Baker E., Warren S.T., Schlessinger D., Sutherland G.R., and Richards R.I. Mapping of DNA instability at the fragile X to a trinucleotide repeat sequence p(CCG)n. Science 252 (1991) 1711-1714
2. Sutherland G.R., Baker E., and Richards R.I. Fragile sites still breaking. Trends Genet. 14 (1998) 501-506
3. Glover T.W., Berger C., Coyle J., and Echo B. DNA polymerase α inhibition by aphidicolin induces gaps and breaks at common fragile sites in human chromosomes. Hum. Genet. 67 (1984) 136-142
4. Arlt M.F., Miller D.E., Beer D.G., and Glover T.W. Molecular characterization of FRAXB and comparative common fragile site instability in cancer cells. Genes Chromosomes Cancer 33 (2002) 82-92
5. Bednarek A.K., Laflin K.J., Daniel R.L., Liao Q., Hawkins K.A., and Aldaz C.M. WWOX, a novel WW domain-containing protein mapping to human chromosome 16q23.3-24.1, a region frequently affected in breast cancer. Cancer Res. 60 (2000) 2140-2145
6. Callahan G., Denison S.R., Phillips L.A., Shridhar V., and Smith D.I. Characterization of the common fragile site FRA9E and its potential role in ovarian cancer. Oncogene 22 (2003) 590-601
7. Denison S.R., Callahan G., Becker N.A., Phillips L.A., and Smith D.I. Characterization of FRA6E and its potential role in autosomal recessive juvenile parkinsonism and ovarian cancer. Genes Chromosomes Cancer 38 (2003) 40-52
8. Huang H., Qian J., Proffit J., Wilber K., Jenkins R., and Smith D.I. 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 (1998) 2311-2319
9. Limongi M.Z., Pelliccia F., and Rocchi A. Characterization of the human common fragile site FRA2G. Genomics 81 (2003) 93-97
10. 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. 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. U.S.A. 95 (1998) 8141-8146
11. Morelli C., Karayianni E., Magnanini C., Mungall A.J., Thorland E., Negrini M., Smith D.I., and Barbanti-Brodano G. Cloning and characterization of the common fragile site FRA6F harboring a replicative senescence gene and frequently deleted in human tumors. Oncogene 21 (2002) 7266-7276
12. 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. The FHIT gene, spanning the chromosome 3pl4.2 fragile site and renal carcinoma-associated t(3;8) breakpoint, is abnormal in digestive tract cancers. Cell 84 (1996) 587-597
13. 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. 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 (2000) 1651-1663
14. Rozier L., El-Achkar E., Apiou F., and Debatisse M. Characterization of a conserved aphidicolin-sensitive common fragile site at human 4q22 and mouse 6C1: possible association with an inherited disease and cancer. Oncogene 23 (2004) 6872-6880
15. Savelyeva L., Sagulenko E., Schmitt J.G., and Schwab M. The neurobeachin gene spans the common fragile site FRA13A. Hum. Genet. 118 (2006) 551-558
16. Zlotorynski E., Rahat A., Sakaug J., Ben-Porat N., Ozeri E., Herschberg R., Levi A., Scherer S.W., Margalit H., and Kerem B. Molecular basis for expression of common and rare fragile sites. Mol. Cell. Biol. 23 (2003) 7143-7151
17. Smith D.I., Zhu Y., McAvoy S., and Kuhn R. Common fragile sites, extremely large genes, neural development and cancer. Cancer Lett. 232 (2006) 48-57
18. Cohen A.J., Li F.P., Berg S., Marchetto D.J., Tsai S., Jacobs S.C., and Brown R.S. Hereditary renal-cell carcinoma associated with a chromosomal translocation. N. Engl. J. Med. 301 (1979) 592-595
19. Fang J.M., Arlt M.F., Burgess A.C., Dagenais S.L., Beer D.G., and Glover T.W. Translocation breakpoints in FHIT and FRA3B in both homologs of chromosome 3 in an esophageal adenocarcinoma. Genes Chromosomes Cancer 30 (2001) 292-298
20. Gemmill R.M., West J.D., Boldog F., Tanaka N., Robinson L.J., Smith D.I., Li F., and Drabkin H.A. The hereditary renal cell carcinoma 3;8 translocation fuses FHIT to a patched-related gene, TRC8. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 9572-9577
21. Geurts J.M.W., Schoenmakers E.F.P.M., Roijer E., Stenman G., and Van de Ven W.J.M. Expression of reciprocal hybrid transcripts of HMGIC and FHIT in a pleomorphic adenoma of the parotid gland. Cancer Res. 57 (1997) 13-17
22. Glover T.W., and Stein C.K. Chromosome breakage and recombination at fragile sites. Am. J. Hum. Genet. 43 (1988) 265-273
23. Keck C.L., Zimonjic D.B., Yuan B.-Z., Thorgeirsson S.S., and Popescu N.C. Nonrandom breakpoints of unbalanced chromosome translocations in human hepatocellular carcinoma cell lines. Cancer Genet. Cytogenet. 111 (1999)
24. Popovici C., Basset C., Bertucci F., Orsetti B., Adelaide J., Mozziconacci M.-J., Conte N., Murati A., Ginestier C., Charafe-Jauffret E., Ethier S.P., Lafage-Pochitaloff M., Theillet C., Birnbaum D., and Chaffanet M. Reciprocal translocations in breast tumor cell lines: cloning of a t(3;20) that targets the FHIT gene. Genes Chromosomes Cancer 35 (2002) 204-218
25. Krummel K.A., Roberts L.R., Kawakami M., Glover T.W., and Smith D.I. The characterization of the common fragile site FRA16D and its involvement in multiple myeloma translocations. Genomics 69 (2000) 37-46
26. Druck T., Podolski J., Byrski T., Wyrwicz L., Zajaczek S., Kata G., Borowka A., Lubinski J., and Huebner K. The DIRC1 gene at chromosome 2q33 spans a familial RCC-associated t(2;3)(q33;q21) chromosome translocation. J. Hum. Genet. 46 (2001) 583-589
27. Podolski J., Byrski T., Zajaczek S., Druck T., Zimonjic D.B., Popescu N.C., Kata G., Borowka A., Gronwal J., Lubinski J., and Huebner K. Characterization of a familial RCC-associated t(2;3)(q33;q21) chromosome translocation. J. Hum. Genet. 46 (2001) 685-693
28. Ferber M.J., Eilers P., Schuuring E., Fenton J.A.L., Fleuren G.J., Renter G., Szuhai S., Smith D.I., Raap A.K., and Brink A.A.T.P. Positioning of cervical carcinoma and Burkitt lymphoma translocation breakpoints with respect to the human papillomavirus integration cluster in FRA8C at 8q24.13. Cancer Genet. Cytogenet. 154 (2004) 1-9
29. Sinclair P.B., Harrison C.J., Jarosova M., and Foroni L. Analysis of balanced rearrangements of chromosome 6 in acute leukemia: clustered breakpoints in q22-q23 and possible involvement of c-MYB in a new recurrent translocation, t(6;7)(q23;q32-36). Haematologica 90 (2005)
30. Boldog F.L., Waggoner B., Glover T.W., Chumakov I., Le Paslier D., Cohen D., Gemmill R.M., and Drabkin H.A. Integrated YAC contig containing the 3pl4.2 hereditary renal carcinoma 3;8 translocation breakpoint and the fragile site FRA3B. Genes Chromosomes Cancer 11 (1994) 216-221
31. Wilke C.M., Guo S.W., Hall B.K., Boldog F., Gemmill R.M., Chandrasekharappa S.C., Barcroft C.L., Drabkin H.A., and Glover T.W. Multicolor FISH mapping of YAC clones in 3pl4 and identification of a YAC spanning both FRA3B and the t(3;8) associated with hereditary renal cell carcinoma. Genomics 22 (1994) 319-326
32. Zanesi N., Fidanza V., Fong L.Y., Mancini R., Druck T., Valtieri M., Rudiger T., McCue P.A., Croce C.M., and Huebner K. The tumour spectrum in Fhit-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 10250-10255
33. Siprashvili Z., Sozzi G., Barnes L.D., McCue P., Robinson A.K., Eryomin V., Sard L., Tagliabue E., Greco A., Fusetti L., Schwartz G., Pierotti M.C., Croce C.M., and Huebner K. Replacement of Fhit in cancer cells suppresses tumorigenicity. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 13771-13776
34. Wilke C.M., Hall B.K., Hoge A., Paradee W., Smith D.I., and Glover T.W. FRA3B extends over a broad region and contains a spontaneous HPVI6 integration site: direct evidence for the coincidence of viral integration sites and fragile sites. Hum. Mol. Genet. 5 (1996) 187-195
35. Thorland E.C., Myers S.L., Persing D.H., Sarkar G., McGovern R.M., Gostout B.S., and Smith D.I. Human papillomavirus type 16 integrations in cervical tumors frequently occur in common fragile sites. Cancer Res. 60 (2000) 5916-5921
36. Bednarek A., Keek-Waggoner C.L., Daniel R.L., Laflin K.J., Bergsagel P.L., Kiguchi K., Brenner A.W., and Aldaz C.M. WWOX, the FRA16D gene, behaves as a suppressor of tumor growth. Cancer Res. 61 (2001) 8068-8073
37. Mangelsdorf M., Ried K., Woollatt E., Dayan S., Eyre H., Finnis M., Hobson L., Nancarrow J., Venter D., Baker E., and Richards R.I. Chromosomal fragile site FRA16D and DNA instability in cancer. Cancer Res. 60 (2000) 1683-1689
38. Paige A.J.W., Taylor K.J., Taylor C., Hillier S.G., Farrington S., Scott D., Porteous D.J., Smyth J.F., Gabra H., and Watson J.E.V. WWOX: a candidate tumor suppressor gene involved in multiple tumor types. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 11417-11422
39. Glover T.W., Arlt M.F., Casper A.M., and Durkin S.G. Mechanisms of common fragile site instability. Hum. Mol. Genet. 14 (2005) R197-R205
40. Paradee W., Wilke C.M., Wang L., Shridhar R., Mullins C.M., Hoge A., Glover T.W., and Smith D.I. A 350-kb cosmid contig in 3pl4.2 that crosses the t(3;8) hereditary renal cell carcinoma translocation breakpoint and 17 aphidicolin-induced FRA3B breakpoints. Genomics 35 (1996) 87-93
41. Wang N.D., Testa J.R., and Smith D.I. Determination of the specificity of aphidicolin-induced breakage of the human 3pl4.2 fragile site. Genomics 17 (1993) 341-347
42. Glover T.W., and Stein C.K. Induction of sister chromatid exchanges at common fragile sites. Am. J. Hum. Genet. 41 (1987) 882-890
43. Rassool F.V., McKeithan T.W., and Neilly M.E. E. van Melle, R. Espinosa III, M. M. Le Beau, Preferential integration of marker DNA into the chromosomal fragile site at 3pl4: an approach to cloning fragile sites. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 6657-6661
44. De Braekeleer M., Sreekantaiah C., and Haas O. Herpes simplex virus and human papillomavirus sites correlate with chromosomal breakpoints in human cervical carcinoma. Cancer Genet. Cytogenet. 59 (1992) 135-137
45. Popescu N.C., and DiPaolo J.A. Preferential sites for viral integration on mammalian genome. Cancer Genet. Cytogenet. 42 (1989) 157-171
46. Smith P.P., Friedman C., Bryant E.M., and McDougall J.K. Viral integration and fragile sites in human papillomavirus-immortalized human keratinocyte cell lines. Genes Chromosomes Cancer 5 (1992) 150-157
47. Coquelle A., Pipiras E., Toledo F., Buttin G., and Debatisse M. Expression of fragile sites triggers intrachromosomal mammalian gene amplification and sets boundaries to early amplicons. Cell 89 (1997) 215-225
48. Kuo M.T., Vyas R.C., Jiang L.X., and Hittelman W.N. Chromosome breakage at a major fragile site associated with P-glycoprotein gene amplification in multidrug-resistant CHO cells. Mol. Cell. Biol. 14 (1994) 5202-5211
49. Elder F.F.B., and Robinson T.J. Rodent fragile sites: are they conserved? Evidence from mouse and rat. Chromosoma 97 (1989) 459-464
50. McAllister B.F., and Greenbaum I.F. How common are common fragile sites: variation of aphidicolin-induced chromosomal fragile sites in a population of the deer mouse (Peromyscus maniculatus). Hum. Genet. 100 (1997) 182-188
51. Ruiz-Herrera A., Garcia F., Fronicke L., Ponsa M., Egozcue J., Caldes M.G., and Stanyon R. Conservation of aphidicolin-induced fragile sites in Papionini (Primates) species and humans. Chromosome Res. 12 (2004) 683-690
52. Smeets D.F.C.M., and van de Klundert F.A.J.M. Common fragile sites in man and three closely related primate species. Cytogenet. Cell Genet. 53 (1990) 8-14
53. Soulie J., and De Grouchy J. A cytogenetic survey of 110 baboons (Papio cynocephalus). Am. J. Phys. Anthrop. 56 (1981) 107-113
54. Stone D.M., Jacky P.B., Hancock D.D., and Prieur D.J. Chromosomal fragile site expression in dogs. Am. J. Med. Genet. 40 (1991) 214-222
55. Stone D.M., Stephens K.E., and Doles J. Folate-sensitive and aphidicolin-inducible fragile sites are expressed in the genome of the domestic cat. Cancer Genet. Cytogenet. 65 (1993) 130-134
56. Yang M.Y., and Long S.E. Folate sensitive common fragile sites in chromosomes of the domestic pig (Sus scrofa). Res. Vet. Sci. 55 (1993) 231-235
57. 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. The murine Fhit gene is highly similar to its human orthologue and maps to a common fragile site region. Cancer Res. 58 (1998) 3409-3414
58. Krummel K.A., Denison S.R., Calhoun E., Phillips L.A., and Smith D.I. The common fragile site FRA16D and its associated gene WWOX are highly conserved in the mouse at Fra8El. Genes Chromosomes Cancer 34 (2002) 154-167
59. Matsuyama A., Shiraishi T., Trapasso F., Kuroki T., Alder H., Mori M., Huebner K., and Croce C.M. Fragile site orthologs FHIT/FRA3B and Fhit/Fra 14A2: evolutionarily conserved but highly recombinogenic. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 14988-14993
60. Shiraishi T., Druck T., Mimori K., Flomenberg J., Berk L., Alder H., Miller W., Huebner K., and Croce C.M. Sequence conservation at human and mouse orthologous common fragile regions, FRA3B/FHIT and Fra14A2/Fhit. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 5722-5727
61. Cha R.S., and Kleckner N. ATR homolog Mecl promotes fork progression, thus averting breaks in replication slow zones. Science 297 (2002) 602-606
62. Lemoine F.J., Degtyareva N.P., Lobcchev K., and Petes T.D. Chromosomal translocations in yeast induced by low levels of DNA polymerase a model for chromosome fragile sites. Cell 120 (2005) 587-598
63. Admire A., Shanks L., Danzl N., Wang M., Weier U., Stevens W., Hunt E., and Weinert T. Cycles of chromosome instability are associated with a fragile site and are increased by defects in DNA replication and checkpoint controls in yeast. Genes Dev. 20 (2006) 159-173
64. Druck T., Hadaczek P., Fu T.-B., Ohta M., Siprashvili Z., Baffa R., Negrini M., Kastury K., Veronese M.L., Rosen D., Rothstein J., McCue P., Cotticelli M.G., Inoue H., Croce C.M., and Huebner K. Structure and expression of the human FHIT gene in normal and tumor cells. Cancer Res. 57 (1997) 504-512
65. Michael D., Beer D.G., Wilke C.W., Miller D.E., and Glover T.W. Frequent deletions of FHIT and FRA3B in Barrett's metaplasia and esophageal adenocarcinomas. Oncogene 15 (1997) 1653-1659
66. Mimori K., Druck T., Inoue H., Alder H., Berk L., Mori M., Huebner K., and Croce C.M. Cancer-specific chromosome alterations in the constitutive fragile region FRA3B. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 7456-7461
67. Corbin S., Neilly M.E., Espinosa III R., Davis E.M., McKeithan T.W., and Le Beau M.M. Identification of unstable sequences within the common fragile site at 3pl4.2:implications for the mechanism of deletions within fragile histidine triad gene/common fragile site at 3pl4.2 in tumors. Cancer Res. 62 (2002) 3477-3484
68. Finnis M., Dayan S., Hobson L., Chenevix-Trench G., Friend K., Ried K., Venter D., Woollatt E., Baker E., and Richards R.I. Common chromosomal fragile site FRA16D mutation in cancer cells. Hum. Mol. Genet. 14 (2005) 1341-1349
69. Huang H., Qian C., Jenkins R.B., and Smith D.I. FISH mapping of YAC clones at human chromosomal band 7q31.2: identification of YACs spanning FRA7G within the common region of LOH in breast and prostate cancer. Genes Chromosomes Cancer 21 (1998) 152-159
70. Chesi M., Bergsagel P.L., Shonukan O.O., Martelli M.L., Brents L.A., Chen T., Schrock E., Ried T., and Kuehl W.M. Frequent dysregulation of the c-maf proto-oncogene at 16q23 by translocation to an Ig locus in multiple myeloma. Blood 91 (1998) 4457-4463
71. Hellman A., Zlotorynski E., Scherer S.W., Cheung J., Vincent J.B., Smith D.I., Trakhtenbrot L., and Kerem B. A role for common fragile site induction in amplification of human oncogenes. Cancer Cell 1 (2002) 89-97
72. Miller C.T., Lin L., Casper A.M., Lim J., Thomas D.G., Orringer M.B., Chang A.C., Chambers A.F., Giordano T.J., Glover T.W., and Beer D.G. Genomic amplification of MET with boundaries within fragile site FRA7G and upregulation of MET signaling pathways in esophageal adenocarcinoma. Oncogene 25 (2006) 409-418
73. Boldog F., Gemmill R., West J., Robinson M., and Li E. Chromosome 3pl4 homozygous deletions and sequence analysis of FRA3B. Hum. Mol. Genet. 6 (1997) 193-203
74. Le Beau M.M., Rassool F.V., Neilly M.E., Espinosa III R., Glover T.W., Smith D.I., and McKeithan T.W. 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 (1998) 755-761
75. Hellman A., Rahat A., Scherer S.W., Darvasi A., Tsui L.-C., and Kerem S. Replication delay along FRA7H, a common fragile site on human chromosome 7, leads to chromosomal instability. Mol. Cell. Biol. 20 (2000) 4420-4427
76. Palakodeti A., Han Y., Jiang Y., and Le Beau M.M. The role of late/slow replication of the FRA16D in common fragile site induction. Genes Chromosomes Cancer 39 (2004) 71-76
77. Freudenreich C.H., Kantrow S.M., and Zakian V.A. Expansion and length-dependent fragility of CTG repeats in yeast. Science 279 (1998) 853-856
78. Gordenin D.A., Lobachev K.S., Degtyareva N.P., Malkova A.L., Perkins E., and Resnick M.A. Inverted DNA repeats: a source of eukaryotic genomic instability. Mol. Cell. Biol. 13 (1993) 5315-5322
79. Ruskin B., and Fink G.R. Mutations in POL1 increase the mitotic instability of tandem inverted repeats in Saccharomyces cerevisiae. Genetics 133 (1993) 43-56
80. Cliby W.A., Roberts C.J., Cimprich K.A., Stringer C.M., Lamb J.R., Schreiber S.L., and Friend S.H. Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints. EMBO J. 17 (1998) 159-169
81. Cortez D., Guntuku S., Qin J., and Elledge S.J. ATR and ATRIP: partners in checkpoint signaling. Science 294 (2001) 1713-1716
82. Hammond E.M., Denko N.C., Dorie M.J., Abraham R.T., and Giaccia A.J. Hypoxia links ATR and p53 through replication arrest. Mol. Cell. Biol. 22 (2002) 1834-1843
83. 1 checkpoint-deficient cells to lethal premature chromatin condensation. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 9092-9097
84. Casper A.M., Nghiem P., Arlt M.F., and Glover T.W. ATR regulates fragile site stability. Cell 111 (2002) 779-789
85. Casper A.M., Durkin S.G., Arlt M.F., and Glover T.W. Chromosomal instability at common fragile sites in Seckel syndrome. Am. J. Hum. Genet. 75 (2004) 654-660
86. Arlt M.F., Xu B., Durkin S.G., Casper A.M., Kastan M.B., and Glover T.W. BRCA1 is required for common fragile-site stability via its G2/M checkpoint function. Mol. Cell. Biol. 24 (2004) 6701-6709
87. Howlett N.G., Taniguchi T., Durkin S.G., D'Andrea A.D., and Glover T.W. The Fanconi anemia pathway is required for the DNA replication stress response and for the regulation of common fragile site stability. Hum. Mol. Genet. 14 (2005) 693-701
88. Taniguchi T., and D'Andrea A.D. The Fanconi anemia protein, FANCE, promotes the nuclear accumulation of FANCC. Blood 100 (2002) 2457-2462
89. Andreassen P.R., D'Andrea A.D., and Taniguchi T. ATR couples FANCD2 monoubiquitination to the DNA-damage response. Genes Dev. 18 (2004) 1958-1963
90. S.G. Durkin, M.F. Arlt, N.G. Howlett, T.W. Glover, Depletion of CHK1, but not CHK2, induces chromosomal instability and common fragile site breakage, Oncogene, in press.
91. Musio A., Montagna C., Mariani T., Tilenni M., Focarelli M.L., Brait L., Indino E., Benedetti P.A., Chessa L., Albertini A., Ried T., and Vezzoni P. SMC1 involvement in fragile site expression. Hum. Mol. Genet. 14 (2005) 525-533
92. Losada A., and Hirano T. Dynamic molecular linkers of the genome: the first decade of SMC proteins. Genes Dev. 19 (2005) 1269-1287
93. Kitagawa R., Bakkenist C.J., McKinnon P.J., and Kastan M.B. Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev. 18 (2004) 1423-1438
94. Schwartz M., Zlotorynski E., Goldberg M., Ozeri E., Rahat A., le Sage C., Chen B.P., Chen D.J., Agami R., and Kerem B. Homologous recombination and nonhomologous end-joining repair pathways regulate fragile site stability. Genes Dev. 19 (2005) 2715-2726
95. Gorgoulis V.G., Vassiliou L.V., Karakaidos P., Zacharatos P., Kotsinas A., Liloglou T., Venere M., Ditullio Jr. R.A., Kastrinakis N.G., Levy B., Kletsas D., Yoneta A., Herlyn M., Kittas C., and Halazonetis T.D. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434 (2005) 907-913
96. Bartkova J., Horejsi Z., Koed K., Kramer A., Tort F., Zieger K., Guldberg P., Sehested M., Nesland J.M., Lukas C., Orntoft T., Lukas J., and Bartek J. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434 (2005) 864-870