Bloom syndrome, genomic instability and cancer: the SOS-like hypothesis

Cancer Letters

Volumn 236, Issue 1, 2006, Pages 1-12

  Amor Guéret, Mounira ^a  

^a INSTITUT CURIE   (France)

Author keywords

Apoptosis; Bloom's syndrome; Cancer; Genetic instability; Recombination dependent replication; SOS response; Stalled replication forks

Indexed keywords

BLEOMYCIN; BLM PROTEIN; DOXORUBICIN; ETOPOSIDE; MITOMYCIN C; NUCLEAR PROTEIN; RAD51 PROTEIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; BLOOM SYNDROME PROTEIN; HELICASE;

APOPTOSIS; BACTERIUM; BLOOM SYNDROME; CANCER RISK; CARCINOGENESIS; CELL CYCLE; CHROMOSOMAL INSTABILITY; CORRELATION ANALYSIS; DNA DAMAGE; DNA REPAIR; GENE INTERACTION; GENE REPLICATION; GENETIC DISORDER; GENETIC RECOMBINATION; GENOMIC INSTABILITY; GENOTOXICITY; HUMAN; LETHALITY; MALIGNANT NEOPLASTIC DISEASE; MISMATCH REPAIR; MULTIGENE FAMILY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SHORT SURVEY; ANIMAL; GENETIC PREDISPOSITION; GENETICS; METABOLISM; MUTATION; NEOPLASM; REVIEW; SISTER CHROMATID EXCHANGE;

BACTERIA (MICROORGANISMS);

ADENOSINE TRIPHOSPHATASES; ANIMALS; APOPTOSIS; BLOOM SYNDROME; CELL CYCLE; DNA HELICASES; GENETIC PREDISPOSITION TO DISEASE; GENOMIC INSTABILITY; HUMANS; MUTATION; NEOPLASMS; SISTER CHROMATID EXCHANGE; SOS RESPONSE (GENETICS);

EID: 33745398364     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2005.04.023     Document Type: Review

References (100)

1. German J., and Ellis N.A. Bloom syndrome. In: Vogelstein B., and Kinzler K.W. (Eds). The Genetic Basis of Human Cancer (1997) 733-751 (Chapter 30)
2. M. Amor-Guéret, Bloom's syndrome, Orphanet Encyclopedia, 2004. URL: http://www.orpha.net/data/patho/GB/uk-Bloomsyndrome.pdf.
3. Chaganti R.S.K., Schonberg S., and German J. A manyfold increase in sister chromatid exchanges in Bloom's syndrome lymphocytes. Proc. Natl Acad. Sci. USA 71 (1974) 4508-4512
4. Ellis N.A., Groden J., Ye T.Z., Straughen J., Lennon D.J., Ciocci S., et al. The Bloom's syndrome gene product is homologous to RecQ helicases. Cell 83 (1995) 655-666
5. Karow J.K., Chakraverty R.K., and Hickson I.D. The Bloom's syndrome gene product is a 3′-5′ DNA helicase. J. Biol. Chem. 49 (1997) 464-469
6. Dutertre S., Sekhri R., Tintignac L.A., Onclercq-Delic R., Chatton B., Jaulin C., et al. Dephosphorylation and subcellular compartment change of the mitotic Bloom's syndrome DNA helicase in response to ionizing radiation. J. Biol. Chem. 277 (2002) 6280-6286
7. Sun H., Karow J.K., Hickson I.D., and Maizels N. The Bloom's syndrome helicase unwinds G4 DNA. J. Biol. Chem. 273 (1998) 27587-27592
8. Mohaghegh P., Karow J.K., Brosh Jr. R.M., Bohr V.A., and Hickson I.D. The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res. 2 (2001) 2843-2849
9. van Brabant A.J., Ye T., Sanz III M., German J.L., Ellis N.A., and Holloman W.K. Binding and melting of D-loops by the Bloom syndrome helicase. Biochemistry 39 (2000) 14617-14625
10. Karow J.K., Constantinou A., Li J.L., West S.C., and Hickson I.D. The Bloom's syndrome gene product promotes branch migration of holliday junctions. Proc. Natl Acad. Sci. USA 97 (2000) 6504-6508
11. Wu L., and Hickson I.D. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426 (2003) 870-874
12. Dutertre S., Ababou M., Onclercq R., Delic J., Chatton B., Jaulin C., et al. Endogenous Bloom's syndrome helicase expression during the cell cycle. Oncogene 19 (2000) 2731-2738
13. Sanz M.M., Proytcheva M., Ellis N.A., Holloman W.K., and German B.L.M. Bloom's syndrome protein, varies during the cell cycle in its amount, distribution, and co-localization with other nuclear proteins. Cytogenet. Cell. Genet. 91 (2000) 217-223
14. Bischof O., Kim S.H., Irving J., Beresten S., Ellis N.A., and Campisi J. Regulation and localization of the Bloom syndrome protein in response to DNA damage. J. Cell Biol. 153 (2001) 367-380
15. Bayart E., Grigorieva O., Leibovitch S., Onclercq-Delic R., and Amor-Guéret M. A major role for mitotic cdc2 kinase inactivation in the establishment of the mitotic DNA damage checkpoint. Cancer Res. 64 (2004) 8954-8959
16. Beamish H., Kedar P., Kaneko H., Chen P., Fukao T., Peng C., et al. Functional link between BLM defective in Bloom's syndrome and the ataxia-telangiectasia-mutated protein, ATM. J. Biol. Chem. 277 (2002) 30515-30523
17. Yin J., Sobeck A., Xu C., Meetei A.R., Hoatlin M., Li L., et al. BLAP75, an essential component of Bloom's syndrome protein complexes that maintain genome integrity. Eur. Mol. Biol. Org. J. (2005) 1-12
18. Ishov A.M., Sotnikov A.G., Negorev D., Vladimirova O.V., Neff N., Kamitani T., et al. PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J. Cell. Biol. 147 (1999) 221-234
19. Zhong S., Hu P., Ye T.Z., Stan R., Ellis N.A., and Pandolfi P.P. A role for PML and the nuclear body in genomic stability. Oncogene 18 (1999) 7941-7947
20. Yankiwski V., Marciniak R.A., Guarente L., and Neff N.F. Nuclear structure in normal and Bloom syndrome cells. Proc. Natl Acad. Sci. USA 97 (2000) 5214-5219
21. Johnson F.B., Lombard D.B., Neff N.F., Mastrangelo M.A., Dewolf W., Ellis N.A., et al. Association of the Bloom syndrome protein with topoisomerase IIIalpha in somatic and meiotic cells. Cancer Res. 60 (2000) 1162-1167
22. Wu L., Davies S.L., North P.S., Goulaouic H., Riou J.F., Turley H., et al. The Bloom's syndrome gene product interacts with topoisomerase III. J. Biol. Chem. 275 (2000) 9636-9644
23. Hu P., Beresten S.F., van Brabant A.J., Ye T.Z., Pandolfi P.P., Johnson F.B., et al. Evidence for BLM and Topoisomerase IIIalpha interaction in genomic stability. Hum. Mol. Genet. 10 (2001) 1287-1298
24. Thacker J. The RAD51 gene family, genetic instability and cancer. Cancer Lett. 219 (2005) 125-135
25. Pedrazzi G., Bachrati C.Z., Selak N., Studer I., Petkovic M., Hickson I.D., et al. The Bloom's syndrome helicase interacts directly with the human DNA mismatch repair protein hMSH6. Biol. Chem. 384 (2003) 1155-1164
26. Davies S.L., North P.S., Dart A., Lakin N.D., and Hickson I.D. Phosphorylation of the Bloom's syndrome helicase and its role in recovery from S-phase arrest. Mol. Cell. Biol. 24 (2004) 279-291
27. Wang Y., Cortez D., Yazdi P., Neff N., Elledge S.J., and Qin J. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev. 14 (2000) 927-939
28. Langland G., Kordich J., Creaney J., Goss K.H., Lillard-Wetherell K., Bebenek K., et al. The Bloom's syndrome protein (BLM) interacts with MLH1 but is not required for DNA mismatch repair. J. Biol. Chem. 276 (2001) 30031-30035
29. Pedrazzi G., Perrera C., Blaser H., Kuster P., Marra G., Davies S.L., et al. Direct association of Bloom's syndrome gene product with the human mismatch repair protein MLH1. Nucleic Acids Res. 29 (2001) 4378-4386
30. Yang Q., Zhang R., Wang X.W., Linke S.P., Sengupta S., Hickson I.D., et al. The mismatch DNA repair heterodimer, hMSH2/6, regulates BLM helicase. Oncogene 23 (2004) 3749-3756
31. Meetei A.R., Sechi S., Wallisch M., Yang D., Young M.K., Joenje H., et al. A multiprotein nuclear complex connects Fanconi anemia and Bloom syndrome. Mol. Cell. Biol. 23 (2003) 3417-3426
32. Brosh Jr. R.M., Li J.L., Kenny M.K., Karow J.K., Cooper M.P., Kureekattil R.P., et al. Replication protein A physically interacts with the Bloom's syndrome protein and stimulates its helicase activity. J. Biol. Chem. 275 (2000) 23500-23508
33. von Kobbe C., Karmakar P., Dawut L., Opresko P., Zeng X., Brosh Jr. R.M., et al. Colocalization, physical, and functional interaction between Werner and Bloom syndrome proteins. J. Biol. Chem. 277 (2002) 22035-22044
34. Braybrooke J.P., Li J.L., Wu L., Caple F., Benson F.E., and Hickson I.D. Functional interaction between the Bloom's syndrome helicase and the RAD51 paralog, RAD51L3 (RAD51D). J. Biol. Chem. 278 (2003) 48357-48366
35. Pichierri P., Franchitto A., and Rosselli F. BLM and the FANC proteins collaborate in a common pathway in response to stalled replication forks. Eur. Mol. Biol. Org. J. 23 (2004) 3154-3163
36. Sharma S., Sommers J.A., Wu L., Bohr V.A., Hickson I.D., and Brosh Jr. R.M. Stimulation of flap endonuclease-1 by the Bloom's syndrome protein. J. Biol. Chem. 279 (2004) 9847-9856
37. Warren S.T., Schultz R.A., Chang C.C., Wade M.H., and Trosko J.E. Elevated spontaneous mutation rate in Bloom syndrome fibroblasts. Proc. Natl Acad. Sci. USA 78 (1981) 3133-3137
38. Vijayalaxmi H.J., Evans J.H., and Ray J. German, Bloom's syndrome: evidence for an increased mutation frequency in vivo. Science 221 (1983) 851-853
39. German J. Cytological evidence for crossing-over in vitro in human lymphoid cells. Science 144 (1964) 298-301
40. Kyoizumi S., Nakamura N., Takebe H., Tatsumi K., German J., and Akiyama M. Frequency of variant erythrocytes at the glycophorin-A locus in two Bloom's syndrome patients. Mutat. Res. 214 (1989) 215-222
41. Langlois R.G., Bigbee W.L., Jensen R.H., and German J. Evidenced for increased in vivo mutation and somatic recombination in Bloom's syndrome. Proc. Natl Acad. Sci. USA 86 (1989) 670-674
42. Groden J., Nakamura Y., and German J. Molecular evidence that homologous recombination occurs in proliferating human somatic cells. Proc. Natl Acad. Sci. USA 87 (1990) 4315-4319
43. Hand R., and German J. A retarded rate of DNA chain growth in Bloom's syndrome. Proc. Natl Acad. Sci. USA 72 (1975) 758-762
44. Gianneli F., Benson P.F., Pawsey S.A., and Polani P.E. Ultraviolet light sensitivity and delayed DNA-chain maturation in Bloom's syndrome fibroblasts. Nature 265 (1977) 466-469
45. Lonn U., Lonn S., Nylen U., Winblad G., and German J. An abnormal profile of DNA replication intermediates in Bloom's syndrome. Cancer Res. 50 (1990) 3141-3145
46. Rassool F.V., North P.S., Mufti G.J., and Hickson I.D. Constitutive DNA damage is linked to DNA replication abnormalities in Bloom's syndrome cells. Oncogene 22 (2003) 8749-8757
47. Davalos A.R., and Campisi J. Bloom syndrome cells undergo p53-dependent apoptosis and delayed assembly of BRCA1 and NBS1 repair complexes at stalled replication forks. J. Cell. Biol. 162 (2003) 1197-1209
48. Wu L., Davies S.L., Levitt N.C., and Hickson I.D. Potential role for the BLM helicase in recombinational repair via a conserved interaction with RAD51. J. Biol. Chem. 276 (2001) 19375-19381
49. Schawalder J., Paric E., and Neff N.F. Telomere and ribosomal DNA repeats are chromosomal targets of the bloom syndrome DNA helicase. BioMed Central Cell Biology 4 (2003) 15
50. Nicotera T.M. Molecular and biochemical aspects of Bloom's syndrome. Cancer Genet. Cytogenet. 53 (1991) 1-13
51. Ababou M., Dutertre S., Lécluse Y., Onclercq R., Chatton B., and Amor-Guéret M. ATM-dependent phosphorylation and accumulation of endogenous BLM protein in response to ionizing radiation. Oncogene 19 (2000) 5955-5963
52. Ababou M., Dumaire V., Lécluse Y., and Amor-Guéret M. Bloom's syndrome protein response to ultraviolet C radiation and hydroxyurea mediated DNA synthesis inhibition. Oncogene 21 (2002) 2079-2088
53. Wang X.W., Tseng A., Ellis N.A., Spillare E.A., Linke S.P., Robles A.I., et al. Functional interaction of p53 and BLM DNA helicase in apoptosis. J. Biol. Chem. 276 (2001) 32948-32955
54. Seker H., Rubbi C., Linke S.P., Bowman E.D., Garfield S., Hansen L., et al. UV-C-induced DNA damage leads to p53-dependent nuclear trafficking of PML. Oncogene 22 (2003) 1620-1628
55. Aurias A., Antoine J.L., Assathiany R., Odievre M., and Dutrillaux B. Radiation sensitivity of Bloom's syndrome lymphocytes during S and G2 phases. Cancer Genet. Cytogenet. 16 (1985) 131-136
56. Franchitto A., and Pichierri P. Bloom's syndrome protein is required for correct relocalization of RAD50/MRE11/NBS1 complex after replication fork arrest. J. Cell. Biol. 157 (2002) 19-30
57. Sengupta S., Robles A.I., Linke S.P., Sinogeeva N.I., Zhang R., Pedeux R., et al. Functional interaction between BLM helicase and 53BP1 in a Chk1-mediated pathway during S-phase arrest. J. Cell. Biol. 166 (2004) 801-813
58. Yang Q., Zhang R., Wang X.W., Spillare E.A., Linke S.P., Subramanian D., et al. The processing of Holliday junctions by BLM and WRN helicases is regulated by p53. J. Biol. Chem. 277 (2002) 31980-31987
59. Sengupta S., Linke S.P., Pedeux R., Yang Q., Farnsworth J., Garfield S.H., et al. BLM helicase-dependent transport of p53 to sites of stalled DNA replication forks modulates homologous recombination. Eur. Mol. Biol. Org. J. 22 (2003) 1-13
60. Zhang R., Sengupta S., Yang Q., Linke S.P., Yanaihara N., Bradsher J., et al. BLM helicase facilitates Mus81 endonuclease activity in human cells. Cancer Res. 65 (2005) 2526-2531
61. Foucault F., Buard J., Praz F., Jaulin C., Stoppa-Lyonnet D., Vergnaud G., et al. Stability of microsatellites and minisatellites in Bloom syndrome, a human syndrome of genetic instability. Mutat. Res. 362 (1996) 227-236
62. Valerie K., and Povirk L.F. Regulation and mechanisms of mammalian double-strand break repair. Oncogene 22 (2003) 5792-5812
63. Rünger T.M., and Kraemer K.H. Joining of linear plasmid DNA is reduced and error prone in Bloom's syndrome cells. Eur. Mol. Biol. Org. J. 8 (1989) 1419-1425
64. Langland G., Elliott J., Li Y., Creaney J., Dixon K., and Groden J. The BLM helicase is necessary for normal DNA double-strand break repair. Cancer Res. 62 (2002) 2766-2770
65. Gaymes T.J., North P.S., Brady N., Hickson I.D., Mufti G.J., and Rassool F.V. Increased error-prone non homologous DNA end-joining-a proposed mechanism of chromosomal instability in Bloom's syndrome. Oncogene 21 (2002) 2525-2533
66. Onclercq-Delic R., Calsou P., Delteil C., Salles B., Papadopoulo D., and Amor-Guéret M. Possible anti-recombinogenic role of Bloom's syndrome helicase in double-strand break processing. Nucleic Acids Res. 31 (2003) 6272-6282
67. So S., Adachi N., Lieber M.R., and Koyama H. Genetic interactions between BLM and DNA ligase IV in human cells. J. Biol. Chem. 279 (2004) 55433-55442
68. Bischof O., Galande S., Farzaneh F., Kohwi-Shigematsu T., and Campisi J. Selective cleavage of BLM, the Bloom syndrome protein, during apoptotic cell death. J. Biol. Chem. 276 (2001) 12068-12075
69. Freire R., d'Adda Di Fagagna F., Wu L., Pedrazzi G., Stagljar I., Hickson I.D., et al. Cleavage of the Bloom's syndrome gene product during apoptosis by caspase-3 results in an impaired interaction with topoisomerase III alpha. Nucleic Acids Res. 29 (2001) 3172-3180
70. Ababou M., Dumaire V., Lécluse Y., and Amor-Guéret M. Cleavage of BLM protein and sensitivity of Bloom's syndrome cells to hydroxyurea and UVC radiation. Cell Cycle 4 (2002) 262-266
71. Frei C., and Gasser S.M. RecQ-like helicases: the DNA replication checkpoint connection. J. Cell. Sci. 113 (2000) 2641-2646
72. Franchitto A., and Pichierri P. Protecting genomic integrity during DNA replication: correlation between Werner's and Bloom's syndrome gene products and the MRE11 complex. Hum. Mol. Genet. 11 (2002) 2447-2453
73. Hickson I.D. RecQ helicases: caretakers of the genome. Nat. Rev. Cancer 3 (2003) 169-178
74. Nakayama H. RecQ family helicases: roles as tumor suppressor proteins. Oncogene 21 (2002) 9008-9021
75. Bachrati C.Z., and Hickson I.D. RecQ helicases: suppressors of tumorigenesis and premature aging. Biochem. J. 374 (2003) 577-606
76. Chester N., Kuo F., Kozak C., O'Hara C.D., and Leder P. Stage-specific apoptosis, developmental delay, and embryonic lethality in mice homozygous for a targeted disruption in the murine Bloom's syndrome gene. Genes Dev. 12 (1998) 3382-3393
77. German J. Bloom's syndrome. I. Genetical and clinical observations in the first twenty-seven patients. Am. J. Hum. Genet. 2 (1969) 196-227
78. Radman M. Phenomenology of an inducible mutagenic DNA repair: SOS repair hypothesis. In: Prakasch L., Sherman F., Miller M., Lawrence C., and Tabor H.W. (Eds). Molecular and Environmental Aspects of Mutagenesis (1974), Thomas, Springfield, IL 128-142
79. Witkin E.M. Ultraviolet mutagenesis and inducible DNA repair in Escherichia coli. Bacteriol. Rev. 40 (1976) 869-907
80. Cox M.M. The bacterial RecA protein as a motor protein. Annu. Rev. Microbiol. 57 (2003) 551-577
81. Radman M., Taddei F., and Matic I. Evolution-driving genes. Res. Microbiol. 151 (2000) 91-95
82. Defais M., and Devoret R. SOS Response, Encyclopedia of Life Sciences (2001), Nature Publishing Group pp. 1-9
83. Michel B., Flores M.J., Viguera E., Grompone G., Seigneur M., and Bidnenko V. Rescue of arrested replication forks by homologous recombination. Proc. Natl Acad. Sci. USA 98 (2001) 8181-8188
84. Kogoma T. Stable DNA replication: interplay between DNA replication, homologous recombination, and transcription. Microbiol. Mol. Biol. Rev. 61 (1997) 212-238
85. Kreuzer K.N. Interplay Between DNA Replication and Recombination in Prokaryotes. Annu. Rev. Microbiol. (2005) (Epub ahead of print)
86. Liberi G., Maffioletti G., Lucca C., Chiolo I., Baryshnikova A., Cotta-Ramusino C., et al. Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev. 19 (2005) 339-350
87. Cox M.M., Goodman M.F., Kreuzer K.N., Sherratt D.J., Sandler S.J., and Marians K.J. The importance of repairing stalled replication forks. Nature 404 (2000) 37-41
88. Foster P.L., Trimarchi J.M., and Maurer R.A. Two enzymes, both of which process recombination intermediates, have opposite effects on adaptive mutation in Escherichia coli. Genetics 142 (1996) 25-37
89. McGlynn P., Mahdi A.A., and Lloyd R.G. Characterisation of the catalytically active form of RecG helicase. Nucleic Acids Res. 28 (2000) 2324-2332
90. Asai T., and Kogoma T. Roles of ruvA, ruvC and recG gene functions in normal and DNA damage-inducible replication of the Escherichia coli chromosome. Genetics 137 (1994) 895-902
91. O'Reilly E.K., and Kreuzer K.N. Isolation of SOS constitutive mutants of Escherichia coli. J. Bacteriol. 186 (2004) 7149-7160
92. Michel B. Replication fork arrest and DNA recombination. Trends Biochem. Sci. 25 (2000) 173-178
93. Hishida T., Han Y.W., Shibata T., Kubota Y., Ishino Y., Iwasaki H., et al. Role of the Escherichia coli RecQ DNA helicase in SOS signaling and genome stabilization at stalled replication forks. Genes Dev. 18 (2004) 1886-1897
94. Heyer W.D. Damage signaling: RecQ sends an SOS to you. Curr. Biol. 14 (2004) R895-R897
95. Ames B.N. Carcinogens are mutagens: their detection and classification. Environ. Health Perspect. 6 (1973) 115-118
96. Norppa H. Cytogenetic biomarkers and genetic polymorphisms. Toxicol. Lett. 149 (2004) 309-334
97. Bishop A.J., and Schiestl R.H. Role of homologous recombination in carcinogenesis. Exp. Mol. Pathol. 74 (2003) 94-105
98. Thacker J. The RAD51 gene family, genetic instability and cancer. Cancer Lett. 219 (2005) 125-135
99. German J. Bloom's syndrome. XX. The first 100 cancers. Cancer Genet. Cytogenet. 93 (1997) 100-106
100. Vineis P. Cancer as an evolutionary process at the cell level: an epidemiological perspective. Carcinogenesis 24 (2003) 1-6