A role for Mus81 in the repair of chromium-induced DNA damage

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 660, Issue 1-2, 2009, Pages 57-65

  Tamblyn, Laura ^a   Li, Erica ^a   Sarras, Haya ^a   Srikanth, Prarthana ^b   Hande, M Prakash ^b   McPherson, J Peter ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

H2AX; Chromium VI ; Chromosomal instability; Eme1; Mus81; Rad51

Indexed keywords

CHROMIUM; DNA; ENDONUCLEASE; PROTEIN EME1; PROTEIN MUS81; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARCINOGEN DNA INTERACTION; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA REPLICATION FORK; DRUG DNA BINDING; DRUG PROTEIN BINDING; GENOTOXICITY; HOMOLOGOUS RECOMBINATION; MALIGNANT TRANSFORMATION; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELLS, CULTURED; CHROMIUM; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; ENDONUCLEASES; FLOW CYTOMETRY; KARYOTYPING; MICE;

EID: 58149474831     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2008.10.013     Document Type: Article

References (78)

1. Gochfeld M. Setting the research agenda for chromium risk assessment. Environ. Health Perspect. 92 (1991) 3-5
2. Fishbein L. Sources, transport and alterations of metal compounds: an overview. I. Arsenic, beryllium, cadmium, chromium, and nickel. Environ. Health Perspect. 40 (1981) 43-64
3. Zhitkovich A. Importance of chromium-DNA adducts in mutagenicity and toxicity of chromium(VI). Chem. Res. Toxicol. 18 (2005) 3-11
4. Salnikow K., and Zhitkovich A. Genetic and epigenetic mechanisms in metal carcinogenesis and cocarcinogenesis: nickel, arsenic, and chromium. Chem. Res. Toxicol. 21 (2008) 28-44
5. Cancer I.A.F.R.O. Chromium, Nickel and Welding (1990), World Health Organization, Lyons, France
6. Langard S. One hundred years of chromium and cancer: a review of epidemiological evidence and selected case reports. Am. J. Ind. Med. 17 (1990) 189-215
7. Gibb H.J., Lees P.S., Pinsky P.F., and Rooneym B.C. Lung cancer among workers in chromium chemical production. Am. J. Ind. Med. 38 (2000) 115-126
8. Leonard A., and Lauwerys R.R. Carcinogenicity and mutagenicity of chromium. Mutat. Res. 76 (1980) 227-239
9. Cohen M.D., Kargacin B., Klein C.B., and Costa M. Mechanisms of chromium carcinogenicity and toxicity. Crit. Rev. Toxicol. 23 (1993) 255-281
10. De Flora S., Bagnasco M., Serra D., and Zanacchi P. Genotoxicity of chromium compounds. A review. Mutat. Res. 238 (1990) 99-172
11. Arslan P., Beltrame M., and Tomasi A. Intracellular chromium reduction. Biochim. Biophys. Acta 931 (1987) 10-15
12. Alcedo J.A., and Wetterhahn K.E. Chromium toxicity and carcinogenesis. Int. Rev. Exp. Pathol. 31 (1989) 85-108
13. Manning F.C.R., Xu J., and Patierno S.R. Transcriptional inhibition by carcinogenic chromate: relationship to DNA damage. Mol. Carcinog. 6 (1992) 270-279
14. Tsapakos M.J., Hampton T.H., and Wetterhahn K.E. Chromium(VI)-induced DNA lesions and chromium distribution in rat kidney, liver and lung. Cancer Res. 43 (1983) 5662-5667
15. Hamilton J.W., and Wetterhahn K.E. Chromium(VI)-induced DNA damage in chick embryo liver and blood cells in vivo. Carcinogenesis 7 (1986) 2085-2088
16. Bridgewater L.C., Manning F.C., and Patierno S.R. Base-specific arrest of in vitro DNA replication by carcinogenic chromium: relationship to DNA interstrand crosslinking. Carcinogenesis 15 (1994) 2421-2427
17. Xu J., Bubley G.J., Detrick B., Blankenship L.J., and Patierno S.R. Chromium(VI) treatment of normal human lung cells results in guanine-specific DNA polymerase arrest, DNA-DNA cross-links and S-phase blockade of cell cycle. Carcinogenesis 17 (1996) 1511-1517
18. Miller III C.A., and Costa M. Characterization of DNA-protein complexes induced in intact cells by the carcinogen chromate. Mol. Carcinog. 1 (1988) 125-133
19. Fornace Jr. A.J., Seres D.S., Lechner J.F., and Harris C.C. DNA-protein cross-linking by chromium salts. Chem. Biol. Interact. 36 (1981) 345-354
20. Miller III C.A., Cohen M.D., and Costa M. Complexing of actin and other nuclear proteins to DNA by cis-diamminedichloroplatinum(II) and chromium compounds. Carcinogenesis 12 (1991) 269-276
21. Wedrychowski A., Ward W.S., Schmidt W.N., and Hnilica L.S. Chromium-induced cross-linking of nuclear proteins and DNA. J. Biol. Chem. 260 (1985) 7150-7155
22. Zhitkovich A., Voitkun V., and Costa M. Glutathione and free amino acids form stable complexes with DNA following exposure of intact mammalian cells to chromate. Carcinogenesis 16 (1995) 907-913
23. Quievyrn G., Messer J., and Zhitkovich A. Carcinogenic chromium(VI) induces cross-linking of vitamin C to DNA in vitro and in human lung A549 cells. Biochemistry 41 (2002) 3156-3167
24. Ha L., Ceryak S., and Patierno S.R. Generation of S phase-dependent DNA double-strand breaks by Cr(VI) exposure: involvement of ATM in Cr(VI) induction of gamma-H2AX. Carcinogenesis 25 (2004) 2265-2274
25. Bryant H.E., Ying S., and Helleday T. Homologous recombination is involved in repair of chromium-induced DNA damage in mammalian cells. Mutat. Res. 599 (2006) 116-123
26. Ueno S., Kashimoto T., Susa N., Furukawa Y., Ishii M., Yokoi K., Yasuno M., Sasaki Y.F., Ueda J., Nishimura Y., and Sugiyama M. Detection of dichromate(VI)-induced DNA strand breaks and formation of paramagnetic chromium in multiple mouse organs. Toxicol. Appl. Pharmacol. 170 (2001) 56-62
27. Werfel U., Langen V., Eickhoff I., Schoonbrood J., Vahrenholz C., Brauksiepe A., Popp W., and Norpoth K. Elevated DNA single-strand breakage frequencies in lymphocytes of welders exposed to chromium and nickel. Carcinogenesis 19 (1998) 413-418
28. Reynolds M., Peterson E., Quievryn G., and Zhitkovich A. Human nucleotide excision repair efficiently removes chromium-DNA phosphate adducts and protects cells against chromate toxicity. J. Biol. Chem. 279 (2004) 30419-30424
29. O'Brien T.J., Brooks B.R., and Patierno S.R. Nucleotide excision repair functions in the removal of chromium-induced DNA damage in mammalian cells. Mol. Cell. Biochem. 279 (2005) 85-95
30. Voitkun V., Zhitkovich A., and Costa M. Cr(III)-mediated crosslinks of glutathione or amino acids to the DNA phosphate backbone are mutagenic in human cells. Nucl. Acids Res. 26 (1998) 2024-2030
31. Zhitkovich A., Song Y., Quievryn G., and Voitkun V. Non-oxidative mechanisms are responsible for the induction of mutagenesis by reduction of Cr(VI) with cysteine: role of ternary DNA adducts in Cr(III)-dependent mutagenesis. Biochemistry 40 (2001) 549-560
32. Quievyrn G., Peterson E., Messer J., and Zhitkovich A. Genotoxicity and mutagenicity of chromium (VI)/ascorbate-generated DNA adducts in human and bacterial cells. Biochemistry 42 (2003) 1062-1070
33. Brooks B., O'Brien T.J., Ceryak S., Wise Sr. J.P., Wise S.S., Wise Jr. J.P., DeFabo E., and Patierno S.R. Excision repair is required for genotoxin-induced mutagenesis in mammalian cells. Carcinogenesis 29 (2008) 1064-1069
34. Grlickova-Duzevik E., Wise S.S., Munroe R.C., Thompson W.D., and Wise Sr. J.P. XRCC1 protects against particulate chromate-induced chromosome damage and cytotoxicity in chinese hamster ovary cells. Toxicol. Sci. 92 (2006) 96-102
35. Grlickova-Duzevik E., Wise S.S., Munroe R.C., Thompson W.D., and Wise Sr. J.P. XRCC1 protects cells from chromate-induced chromosome damage, but does not affect cytotoxicity. Mutat. Res. 610 (2006) 31-37
36. Levis A.G., Buttignol M., Bianchi V., and Sponza G. Effects of potassium dichromate on nucleic acid and protein syntheses and on precursor uptake in BHK fibroblasts. Cancer Res. 38 (1978) 110-116
37. Levis A.G., Bianchi V., Tamino G., and Pegoraro B. Cytotoxic effects of hexavalent and trivalent chromium on mammalian cells in vitro. Br. J. Cancer 37 (1978) 386-396
38. Bianchi V., Dal Toso R., Debetto P., Levis A.G., Luciani S., Majone F., and Tamino G. Mechanisms of chromium toxicity in mammalian cell cultures. Toxicology 17 (1980) 219-224
39. Nishio A., and Uyeki E.M. Inhibition of DNA synthesis by chromium compounds. J. Toxicol. Environ. Health 15 (1985) 237-244
40. Bridgewater L.C., Manning F.C., Woo E.S., and Patierno S.R. DNA polymerase arrest by adducted trivalent chromium. Mol. Carcinog. 9 (1994) 122-133
41. Peterson-Roth E., Reynolds M., Quievryn G., and Zhitkovich A. Mismatch repair proteins are activators of toxic responses to chromium-DNA damage. Mol. Cell. Biol. 25 (2005) 3596-3607
42. Reynolds M., Stoddard L., Bespalov I., and Zhitkovich A. Ascorbate acts as a highly potent inducer of chromate mutagenesis and clastogenesis: linkage to DNA breaks in G2 phase by mismatch repair. Nucl. Acids Res. 35 (2007) 465-476
43. Arnaudeau C., Lundin C., and Helleday T. DNA double-strand breaks associated with replication forks are predominantly repaired by homologous recombination involving an exchange mechanism in mammalian cells. J. Mol. Biol. 307 (2001) 1235-1245
44. Lundin C., Erixon K., Arnaudeau C., Schultz N., Jenssen D., Meuth M., and Helleday T. Different roles for nonhomologous end joining and homologous recombination following replication arrest in mammalian cells. Mol. Cell. Biol. 22 (2002) 5869-5878
45. Rothkamm K., Kruger I., Thompson L.H., and Lobrich M. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol. 23 (2003) 5706-5715
46. Saleh-Gohari N., and Helleday T. Conservative homologous recombination preferentially repairs DNA double-strand breaks in the S phase of the cell cycle in human cells. Nucl. Acids Res. 32 (2004) 3683-3688
47. Stackpole M.M., Wise S.S., Goodale B.C., Grlickova Duzevik E., Munroe R.C., Douglas Thompson W., Thacker J., Thompson L.H., Hinz J.M., and Wise Sr. J.P. Homologous recombination repair protects against particulate chromate-induced chromosome instability in chinese hamster cells. Mutat. Res. 625 (2007) 145-154
48. Osman F., and Whitby M.C. Exploring the roles of Mus81-Eme1/MMS4 at perturbed replication forks. DNA Repair 6 (2007) 1004-1017
49. Ciccia A., McDonald N., and West S.C. Structural and functional relationships of the XPF/Mus81 family of proteins. Annu. Rev. Biochem. 77 (2008) 259-287
50. McPherson J.P., Lemmers B., Chahwan R., Pamidi A., Migon E., Matysiak-Zablocki E., Moynahan M.E., Essers J., Hanada K., Poonepalli A., Sanchez-Sweatman O., Khohka R., Kanaar R., Jasin M., Hande M.P., and Hakem R. Involvement of mammalian Mus81 in genome integrity and tumour suppression. Science 304 (2004) 1822-1826
51. Dendouga N., Gao H., Moechars D., Janicot M., Vialard J., and McGowan C.H. Disruption of murine Mus81 increases genomic instability and DNA damage sensitivity but does not promote tumorigenesis. Mol. Cell. Biol. 25 (2005) 7569-7579
52. McPherson J.P., Hande M.P., Poonepalli A., Lemmers B., Zablocki E., Migon E., Shehabeldin A., Porras A., Karaskova J., Vukovic B., Squire J., and Hakem R. A role for Brca1 in chromosome end maintenance. Hum. Mol. Genet. 15 (2006) 1-8
53. Bryan T.M., and Reddel R.R. SV40-induced immortalization of human cells. Crit. Rev. Oncog. 5 (1994) 331-357
54. Hiyama T., Katsura M., Yoshihara T., Ishida M., Kinomura A., Tonda T., Asahara T., and Miyagawa K. Haploinsufficiency of the Mus81-Eme1 endonuclease activates the intra-S-phase and G2/M checkpoints and promotes rereplication in human cells. Nucl. Acids Res. 34 (2006) 880-892
55. Hanada K., Budzowska M., Modesti M., Maas A., Wyman C., Essers J., and Kanaar R. The structure-specific endonuclease Mus81-Eme1 promotes conversion of interstrand DNA crosslinks into double-strand breaks. EMBO J. 25 (2006) 4921-4932
56. Pritchard D.E., Ceryak S., Ha L., Fornsaglio J.L., Hartman S.K., O'Brien T.J., and Patierno S.R. Mechanism of apoptosis and determination of cellular fate in chromium(VI)-exposed populations of telomerase-immortalized human fibroblasts. Cell Growth Differ. 12 (2001) 487-496
57. Carlisle D.L., Pritchard D.E., Singh J., and Patierno S.R. Chromium(VI) induces p53-dependent apoptosis in diploid human lung and mouse dermal fibroblasts. Mol. Carcinog. 28 (2000) 111-118
58. Carlisle D.L., Pritchard D.E., Singh J., Owens B.M., Blankenship L.J., Orenstein J.M., and Patierno S.R. Apoptosis and P53 induction in human lung fibroblasts exposed to chromium(VI): effect of ascorbate and tocopherol. Toxicol. Sci. 55 (2000) 60-68
59. Hanada K., Budzowska M., Davies S.L., van Drunen E., Onizawa H., Beverloo H.B., Maas A., Essers J., Hickson I.D., and Kanaar R. The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat. Struct. Mol. Biol. 14 (2007) 1096-1104
60. Abraham J., Lemmers B., Hande M.P., Moynahan M.E., Chahwan C., Ciccia A., Essers J., Hanada K., Chahwan R., Khaw A.K., McPherson P., Shehabeldin A., Laister R., Arrowsmith C., Kanaar R., West S.C., Jasin M., and Hakem R. Eme1 is involved in DNA damage processing and maintenance of genomic stability in mammalian cells. EMBO J. 22 (2003) 6137-6147
61. Shimura T., Torres M.J., Martin M.M., Rao V.A., Pommier Y., Katsura M., Miyagawa K., and Aladjem M.I. Bloom's syndrome helicase and mus81 are required to induce transient double-strand DNA breaks in reponse to DNA replication stress. J. Mol. Biol. 375 (2007) 1152-1164
62. Interthal H., and Heyer W.-D. Mus81 encodes a novel helix-hairpin-helix protein involved in the response to UV- and methylation-induced DNA damage in Saccharomyces cerevisiae. Mol. Gen. Genet. 263 (2000) 812-827
63. Boddy M.N., Lopez-Girona A., Shanahan P., Interthal H., Heyer W.-D., and Russell P. Damage tolerance protein Mus81 associates with the FHA1 domain of checkpoint kinase Cds1. Mol. Cell. Biol. 20 (2000) 8758-8766
64. Boddy M.N., Gaillard P.-H.L., McDonald W.H., Shanahan P., Yates III J.R., and Russell P. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107 (2001) 537-548
65. Doe C.L., Ahn J.S., Dixon J., and Whitby M.C. Mus81-Eme1 and Rqh1 involvement in processing stalled and collapsed replication forks. J. Biol. Chem. 36 (2002) 32753-32759
66. Fabre F., Ahn J.S., Dixon J., and Whitby M.C. Alternate pathways involving Sgs1/Top3, Mus81/Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 16887-16892
67. Haaf T., Golub E.I., Reddy G., Radding C.M., and Ward D.C. Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 2298-2302
68. Sung P., Krejci L., Van Komen S., and Sehorn M.G. Rad51 recombinase and recombination mediators. J. Biol. Chem. 278 (2003) 42729-42732
69. Lord C.J., and Ashworth A. RAD51, BRCA2 and DNA repair: a partial resolution. Nat. Struct. Mol. Biol. 14 (2007) 461-462
70. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., and Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273 (1998) 5858-5868
71. Ward I.M., and Chen J. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276 (2001) 47759-47762
72. Celeste A., Fernandez-Capetillo O., Kruhlak M.J., Pilch D.R., Staudt D.W., Lee A., Bonner R.F., Bonner W.M., and Nussenzweig A. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 5 (2003) 675-679
73. van Attikum H., and Gasser S.M. The histone code at DNA breaks: a guide to repair?. Nat. Rev. Mol. Cell. Biol. 6 (2005) 757-765
74. Niedernhofer L.J., Odijk H., Budzowska M., van Drunen E., Maas A., Theil A.F., de Wit J., Jaspers N.G.J., Beverloo H.B., Hoeijmakers J.H.J., and Kanaar R. The structure-specific endonuclease Ercc1-Xpf is required to resolve DNA interstrand cross-link-induced double-strand breaks. Mol. Cell. Biol. 24 (2004) 5776-5787
75. Vilcheck S.K., O'Brien T.J., Pritchard D.E., Ha L., Ceryak S., Fornsaglio J.L., and Patierno S.R. Fanconi anemia complementation group A cells are hypersensitive to chromium(VI)-induced toxicity. Environ. Health Perspect. 110 Suppl 5 (2002) 773-777
76. Vilcheck S.K., Ceryak S., O'Brien T.J., and Patierno S.R. FANCD2 monoubiquitination and activation by hexavalent chromium [Cr(VI)] exposure: activation is not required for repair of Cr(VI)-induced DSBs. Mutat. Res. 610 (2006) 21-30
77. Savery L.C., Grlickova-Duzevik E., Wise S.S., Thompson W.D., Hinz J.M., Thompson L.H., and Wise J.P. Role of the Fancg gene in protecting cells from particulate chromate-induced chromosome instability. Mutat. Res. 626 (2007) 120-127
78. Wu F.Y., Tsais F.J., Kuo H.W., Tsai C.H., Wu W.Y., Wang R.Y., and Lai J.S. Cytogenetic study of workers exposed to chromium compounds. Mutat. Res. 464 (2000) 289-296