Mlh1-dependent suppression of specific mutations induced in vivo by the food-borne carcinogen 2-amino-1-methyl-6-phenylimidazo [4,5-b] pyridine (PhIP)

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 594, Issue 1-2, 2006, Pages 101-112

  Smith Roe, Stephanie L ^a   Hegan, Denise Campisi ^b   Glazer, Peter M ^b   Buermeyer, Andrew B ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Colon; Mismatch repair; Mlh1; Mutagenesis; PhIP

Indexed keywords

2 AMINO 1 METHYL 6 PHENYLIMIDAZO[4,5 B]PYRIDINE; CARCINOGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; COLON; FOOD; GENE MUTATION; LYMPHOMA; MISMATCH REPAIR; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; THYMUS;

ANIMALS; CARCINOGENS; CARRIER PROTEINS; COLON; DNA REPAIR; GENES, REPORTER; HETEROZYGOTE DETECTION; IMIDAZOLES; INTESTINE, SMALL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MUTAGENS; MUTATION; NUCLEAR PROTEINS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS; VIRAL PROTEINS;

ANIMALIA;

EID: 31644442038     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2005.08.011     Document Type: Article

References (68)

1. M.J. Schofield, and P. Hsieh DNA mismatch repair: molecular mechanisms and biological function Annu. Rev. Microbiol. 57 2003 579 608
2. T.A. Kunkel, and D.A. Erie DNA mismatch repair Annu. Rev. Biochem. 74 2005 681 710
3. L. Stojic, R. Brun, and J. Jiricny Mismatch repair and DNA damage signalling DNA Repair (Amst.) 3 2004 1091 1101
4. G.M. Li The role of mismatch repair in DNA damage-induced apoptosis Oncol. Res. 11 1999 393 400
5. P. Peltomaki Role of DNA mismatch repair defects in the pathogenesis of human cancer J. Clin. Oncol. 21 2003 1174 1179
6. F.S. Leach, N.C. Nicolaides, N. Papadopoulos, B. Liu, J. Jen, R. Parsons, P. Peltomaki, P. Sistonen, L.A. Aaltonen, and M. Nystrom-Lahti Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer Cell 75 1993 1215 1225
7. C.E. Bronner, S.M. Baker, P.T. Morrison, G. Warren, L.G. Smith, M.K. Lescoe, M. Kane, C. Earabino, J. Lipford, and A. Lindblom Mutation in the DNA mismatch repair gene homologue hMLH1 is associated with hereditary non-polyposis colon cancer Nature 368 1994 258 261
8. Q. Wang, C. Lasset, F. Desseigne, D. Frappaz, C. Bergeron, C. Navarro, E. Ruano, and A. Puisieux Neurofibromatosis and early onset of cancers in hMLH1-deficient children Cancer Res. 59 1999 294 297
9. M.D. Ricciardone, T. Ozcelik, B. Cevher, H. Ozdag, M. Tuncer, A. Gurgey, O. Uzunalimoglu, H. Cetinkaya, A. Tanyeli, E. Erken, and M. Ozturk Human MLH1 deficiency predisposes to hematological malignancy and neurofibromatosis type 1 Cancer Res. 59 1999 290 293
10. D. Whiteside, R. McLeod, G. Graham, J.L. Steckley, K. Booth, M.J. Somerville, and S.E. Andrew A homozygous germ-line mutation in the human MSH2 gene predisposes to hematological malignancy and multiple cafe-au-lait spots Cancer Res. 62 2002 359 362
11. J.G. Herman, A. Umar, K. Polyak, J.R. Graff, N. Ahuja, J.P. Issa, S. Markowitz, J.K. Willson, S.R. Hamilton, K.W. Kinzler, M.F. Kane, R.D. Kolodner, B. Vogelstein, T.A. Kunkel, and S.B. Baylin Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma Proc. Natl. Acad. Sci. U.S.A. 95 1998 6870 6875
12. A. Duval, and R. Hamelin Genetic instability in human mismatch repair deficient cancers Ann. Genet. 45 2002 71 75
13. X. Qin, L. Liu, and S.L. Gerson Mice defective in the DNA mismatch gene PMS2 are hypersensitive to MNU induced thymic lymphoma and are partially protected by transgenic expression of human MGMT Oncogene 18 1999 4394 4400
14. N. Claij, A. van der Wal, M. Dekker, L. Jansen, and H. te Riele DNA mismatch repair deficiency stimulates N-ethyl-N-nitrosourea-induced mutagenesis and lymphomagenesis Cancer Res. 63 2003 2062 2066
15. C. Colussi, S. Fiumicino, A. Giuliani, S. Rosini, P. Musiani, C. Macri, C.S. Potten, M. Crescenzi, and M. Bignami 1,2-Dimethylhydrazine-induced colon carcinoma and lymphoma in msh2(-/-) mice J. Natl. Cancer Inst. 93 2001 1534 1540
16. H. Kawate, R. Itoh, K. Sakumi, Y. Nakabeppu, T. Tsuzuki, F. Ide, T. Ishikawa, T. Noda, H. Nawata, and M. Sekiguchi A defect in a single allele of the Mlh1 gene causes dissociation of the killing and tumorigenic actions of an alkylating carcinogen in methyltransferase-deficient mice Carcinogenesis 21 2000 301 305
17. N.J. Gooderham, H. Zhu, S. Lauber, A. Boyce, and S. Creton Molecular and genetic toxicology of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) Mutat. Res. 506-507 2002 91 99
18. R.H. Dashwood Use of transgenic and mutant animal models in the study of heterocyclic amine-induced mutagenesis and carcinogenesis J. Biochem. Mol. Biol. 36 2003 35 42
19. S. Shibutani, A. Fernandes, N. Suzuki, L. Zhou, F. Johnson, and A.P. Grollman Mutagenesis of the N-(deoxyguanosin-8-yl)-2-amino-1-methyl-6- phenylimidazo[4,5-b]pyridine DNA adduct in mammalian cells. Sequence context effects J. Biol. Chem. 274 1999 27433 27438
20. A.J. Cross, and R. Sinha Meat-related mutagens/carcinogens in the etiology of colorectal cancer Environ. Mol. Mutagen. 44 2004 44 55
21. D.W. Layton, K.T. Bogen, M.G. Knize, F.T. Hatch, V.M. Johnson, and J.S. Felton Cancer risk of heterocyclic amines in cooked foods: an analysis and implications for research Carcinogenesis 16 1995 39 52
22. Report on Carcinogens, 11th ed., P.H.S.U.S., Department of Health, Human Services (Ed.), National Toxicology Program, 2004.
23. W.E. Glaab, and T.R. Skopek Cytotoxic and mutagenic response of mismatch repair-defective human cancer cells exposed to a food-associated heterocyclic amine Carcinogenesis 20 1999 391 394
24. P.M. Leong-Morgenthaler, R. Duc, and S. Morgenthaler Comparison of the mutagenic responses of mismatch repair-proficient (TK6) and mismatch repair-deficient (MT1) human lymphoblast cells to the food-borne carcinogen PhIP Environ. Mol. Mutagen. 38 2001 323 328
25. R. Duc, and P.M. Leong-Morgenthaler Heterocyclic amine induced apoptotic response in the human lymphoblastoid cell line TK6 is linked to mismatch repair status Mutat. Res. 486 2001 155 164
26. S. Zhang, R. Lloyd, G. Bowden, B.W. Glickman, and J.G. de Boer Msh2 DNA mismatch repair gene deficiency and the food-borne mutagen 2-amino-1-methy1-6- phenolimidazo [4,5-b] pyridine (PhIP) synergistically affect mutagenesis in mouse colon Oncogene 20 2001 6066 6072
27. N. Sugawara, F. Paques, M. Colaiacovo, and J.E. Haber Role of Saccharomyces cerevisiae Msh2 and Msh3 repair proteins in double-strand break-induced recombination Proc. Natl. Acad. Sci. U.S.A. 94 1997 9214 9219
28. O.J. Sansom, S.M. Bishop, H. Court, S. Dudley, R.M. Liskay, and A.R. Clarke Apoptosis and mutation in the murine small intestine: loss of Mlh1- and Pms2-dependent apoptosis leads to increased mutation in vivo DNA Repair (Amst.) 2 2003 1029 1039
29. A. Duval, and R. Hamelin Mutations at coding repeat sequences in mismatch repair-deficient human cancers: toward a new concept of target genes for instability Cancer Res. 62 2002 2447 2454
30. S.M. Baker, A.W. Plug, T.A. Prolla, C.E. Bronner, A.C. Harris, X. Yao, D.M. Christie, C. Monell, N. Arnheim, A. Bradley, T. Ashley, and R.M. Liskay Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over Nat. Genet. 13 1996 336 342
31. L. Narayanan, J.A. Fritzell, S.M. Baker, R.M. Liskay, and P.M. Glazer Elevated levels of mutation in multiple tissues of mice deficient in the DNA mismatch repair gene Pms2 Proc. Natl. Acad. Sci. U.S.A. 94 1997 3122 3127
32. E.G. Leach, E.J. Gunther, T.M. Yeasky, L.H. Gibson, T.L. Yang-Feng, and P.M. Glazer Frequent spontaneous deletions at a shuttle vector locus in transgenic mice Mutagenesis 11 1996 49 56
33. J.L. Jakubczak, G. Merlino, J.E. French, W.J. Muller, B. Paul, S. Adhya, and S. Garges Analysis of genetic instability during mammary tumor progression using a novel selection-based assay for in vivo mutations in a bacteriophage lambda transgene target Proc. Natl. Acad. Sci. U.S.A. 93 1996 9073 9078
34. A.M. Lynch, N.J. Gooderham, and A.R. Boobis Organ distinctive mutagenicity in MutaMouse after short-term exposure to PhIP Mutagenesis 11 1996 505 509
35. T. Itoh, T. Kuwahara, T. Suzuki, M. Hayashi, and Y. Ohnishi Regional mutagenicity of heterocyclic amines in the intestine: mutation analysis of the cII gene in lambda/lacZ transgenic mice Mutat. Res. 539 2003 99 108
36. H. Esumi, H. Ohgaki, E. Kohzen, S. Takayama, and T. Sugimura Induction of lymphoma in CDF1 mice by the food mutagen, 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine Jpn. J. Cancer Res. 80 1989 1176 1178
37. I.K. Sorensen, E. Kristiansen, A. Mortensen, C. van Kreijl, R.H. Adamson, and S.S. Thorgeirsson Lymphoma induction by heterocyclic amines in E mu-pim-1 transgenic mice Arch. Toxicol. Suppl. 19 1997 377 386
38. M. Ochiai, H. Imai, T. Sugimura, M. Nagao, and H. Nakagama Induction of intestinal tumors and lymphomas in C57BL/6N mice by a food-borne carcinogen, 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine Jpn. J. Cancer Res. 93 2002 478 483
39. X.B. Zhang, J.S. Felton, J.D. Tucker, C. Urlando, and J.A. Heddle Intestinal mutagenicity of two carcinogenic food mutagens in transgenic mice: 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine and amino(alpha)carboline Carcinogenesis 17 1996 2259 2265
40. S.E. Andrew, X.S. Xu, A. Baross-Francis, L. Narayanan, K. Milhausen, R.M. Liskay, F.R. Jirik, and P.M. Glazer Mutagenesis in PMS2- and MSH2-deficient mice indicates differential protection from transversions and frameshifts Carcinogenesis 21 2000 1291 1295
41. S.E. Andrew, A.H. Reitmair, J. Fox, L. Hsiao, A. Francis, M. McKinnon, T.W. Mak, and F.R. Jirik Base transitions dominate the mutational spectrum of a transgenic reporter gene in MSH2 deficient mice Oncogene 15 1997 123 129
42. S. Zhang, R. Lloyd, G. Bowden, B.W. Glickman, and J.G. de Boer Msh2 deficiency increases the mutation frequency in all parts of the mouse colon Environ. Mol. Mutagen. 40 2002 243 250
43. A. Baross-Francis, N. Makhani, R.M. Liskay, and F.R. Jirik Elevated mutant frequencies and increased C:G→T:A transitions in Mlh1-/- versus Pms2-/- murine small intestinal epithelial cells Oncogene 20 2001 619 625
44. S.C. Mark, L.E. Sandercock, H.A. Luchman, A. Baross, W. Edelmann, and F.R. Jirik Elevated mutant frequencies and predominance of G:C to A:T transition mutations in Msh6(-/-) small intestinal epithelium Oncogene 21 2002 7126 7130
45. X.S. Xu, L. Narayanan, B. Dunklee, R.M. Liskay, and P.M. Glazer Hypermutability to ionizing radiation in mismatch repair-deficient, Pms2 knockout mice Cancer Res. 61 2001 3775 3780
46. S.E. Andrew, M. McKinnon, B.S. Cheng, A. Francis, J. Penney, A.H. Reitmair, T.W. Mak, and F.R. Jirik Tissues of MSH2-deficient mice demonstrate hypermutability on exposure to a DNA methylating agent Proc. Natl. Acad. Sci. U.S.A. 95 1998 1126 1130
47. X. Yao, A.B. Buermeyer, L. Narayanan, D. Tran, S.M. Baker, T.A. Prolla, P.M. Glazer, R.M. Liskay, and N. Arnheim Different mutator phenotypes in Mlh1- versus Pms2-deficient mice Proc. Natl. Acad. Sci. U.S.A. 96 1999 6850 6855
48. A.B. Buermeyer, S.M. Deschenes, S.M. Baker, and R.M. Liskay Mammalian DNA mismatch repair Annu. Rev. Genet. 33 1999 533 564
49. I.K. Sorensen, E. Kristiansen, A. Mortensen, H. van Kranen, C. van Kreijl, R. Fodde, and S.S. Thorgeirsson Short-term carcinogenicity testing of a potent murine intestinal mutagen, 2-amino-1-methyl-6-phenylimidazo (4,5-b)pyridine (PhIP), in Apc1638N transgenic mice Carcinogenesis 18 1997 777 781
50. I.K. Sorensen, A. Mortensen, E. Kristiansen, C. van Kreijl, R.H. Adamson, and S.S. Thorgeirsson Short-term carcinogenicity testing of 2-amino-1-methyl-6-phenylimidazo [4,5-b]pyridine (PhIP) and 2-amino-3- methylimidazo [4,5-f]quinoline (IQ) in E(mu)-pim-1 transgenic mice Carcinogenesis 17 1996 2221 2227
51. K. Masumura, K. Matsui, M. Yamada, M. Horiguchi, K. Ishida, M. Watanabe, O. Ueda, H. Suzuki, Y. Kanke, K.R. Tindall, K. Wakabayashi, T. Sofuni, and T. Nohmi Mutagenicity of 2-amino-1-methyl-6-phenylimidazo [4,5-b]pyridine (PhIP) in the new gpt delta transgenic mouse Cancer Lett. 143 1999 241 244
52. K.W. Turteltaub, J.S. Vogel, C.E. Frantz, and N. Shen Fate and distribution of 2-amino-1-methyl-6-phenylimidazo [4,5-b] pyridine in mice at a human dietary equivalent dose Cancer Res. 52 1992 4682 4687
53. S.N. Lauber, S. Ali, and N.J. Gooderham The cooked food derived carcinogen 2-amino-1-methyl-6-phenylimidazo [4,5-b] pyridine is a potent oestrogen: a mechanistic basis for its tissue-specific carcinogenicity Carcinogenesis 25 2004 2509 2517
54. N.J. Toft, D.J. Winton, J. Kelly, L.A. Howard, M. Dekker, H. te Riele, M.J. Arends, A.H. Wyllie, G.P. Margison, and A.R. Clarke Msh2 status modulates both apoptosis and mutation frequency in the murine small intestine Proc. Natl. Acad. Sci. U.S.A. 96 1999 3911 3915
55. Y. Takagi, M. Takahashi, M. Sanada, R. Ito, M. Yamaizumi, and M. Sekiguchi Roles of MGMT and MLH1 proteins in alkylation-induced apoptosis and mutagenesis DNA Repair (Amst.) 2 2003 1135 1146
56. H. Frandsen, S. Grivas, R. Andersson, L. Dragsted, and J.C. Larsen Reaction of the N-2-acetoxy derivative of 2-amino-1-methyl-6-phenylimidazo[4,5- b]pyridine (PhIP) with 2′-deoxyguanosine and DNA. Synthesis and identification of N-2-(2′-deoxyguanosin-8-yl)-PhIP Carcinogenesis 13 1992 629 635
57. D. Lin, K.R. Kaderlik, R.J. Turesky, D.W. Miller, J.O. Lay Jr., and F.F. Kadlubar Identification of N-(deoxyguanosin-8-yl)-2-amino-1-methyl-6- phenylimidazo [4,5-b]pyridine as the major adduct formed by the food-borne carcinogen, 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine, with DNA Chem. Res. Toxicol. 5 1992 691 697
58. E.D. Larson, K. Iams, and J.T. Drummond Strand-specific processing of 8-oxoguanine by the human mismatch repair pathway: inefficient removal of 8-oxoguanine paired with adenine or cytosine DNA Repair (Amst.) 2 2003 1199 1210
59. A.M. Carothers, W. Yuan, B.E. Hingerty, S. Broyde, D. Grunberger, and E.G. Snyderwine Mutation and repair induced by the carcinogen 2-(hydroxyamino)-1-methyl-6-phenylimidazo[4,5-b]pyridine (N-OH-PhIP) in the dihydrofolate reductase gene of Chinese hamster ovary cells and conformational modeling of the dG-C8-PhIP adduct in DNA Chem. Res. Toxicol. 7 1994 209 218
60. S. Shibutani, N. Suzuki, and A.P. Grollman Mutagenic specificity of (acetylamino)fluorene-derived DNA adducts in mammalian cells Biochemistry 37 1998 12034 12041
61. C. Masutani, R. Kusumoto, S. Iwai, and F. Hanaoka Mechanisms of accurate translesion synthesis by human DNA polymerase eta EMBO J. 19 2000 3100 3109
62. S. Shibutani, N. Suzuki, and A.P. Grollman Mechanism of frameshift (deletion) generated by acetylaminofluorene-derived DNA adducts in vitro Biochemistry 43 2004 15929 15935
63. D.C. Thomas, X. Veaute, R.P. Fuchs, and T.A. Kunkel Frequency and fidelity of translesion synthesis of site-specific N-2-acetylaminofluorene adducts during DNA replication in a human cell extract J. Biol. Chem. 270 1995 21226 21233
64. M. Yasui, H. Dong, R.R. Bonala, N. Suzuki, H. Ohmori, F. Hanaoka, F. Johnson, A.P. Grollman, and S. Shibutani Mutagenic properties of 3-(deoxyguanosin-N2-yl)-2-acetylaminofluorene, a persistent acetylaminofluorene- derived DNA adduct in mammalian cells Biochemistry 43 2004 15005 15013
65. J.C. Klein, R.B. Beems, P.E. Zwart, M. Hamzink, G. Zomer, H. van Steeg, and C.F. van Kreijl Intestinal toxicity and carcinogenic potential of the food mutagen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in DNA repair deficient XPA-/- mice Carcinogenesis 22 2001 619 626
66. K. Imaida, K. Ogawa, S. Takahashi, T. Ito, T. Yamaguchi, Y. Totsuka, K. Wakabayashi, K. Tanaka, N. Ito, and T. Shirai Delay of DNA-adduct repair and severe toxicity in xeroderma pigmentosum group A gene (XPA) deficient mice treated with 2-amino-1-methyl-6-phenyl-imidazo [4,5-b] pyridine (PhIP) Cancer Lett. 150 2000 63 69
67. C.L. Chang, G. Marra, D.P. Chauhan, H.T. Ha, D.K. Chang, L. Ricciardiello, A. Randolph, J.M. Carethers, and C.R. Boland Oxidative stress inactivates the human DNA mismatch repair system Am. J. Physiol. Cell. Physiol. 283 2002 C148 C154
68. V.T. Mihaylova, R.S. Bindra, J. Yuan, D. Campisi, L. Narayanan, R. Jensen, F. Giordano, R.S. Johnson, S. Rockwell, and P.M. Glazer Decreased expression of the DNA mismatch repair gene Mlh1 under hypoxic stress in mammalian cells Mol. Cell. Biol. 23 2003 3265 3273