K-Ras mutant fraction in A/J mouse lung increases as a function of benzo[a]pyrene dose

Environmental and Molecular Mutagenesis

Volumn 51, Issue 2, 2010, Pages 146-155

  Meng, Fanxue ^a   Knapp, Geremy W ^b   Green, Terry ^b   Ross, Jeffrey A ^b   Parsons, Barbara L ^a  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^b U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

A J mouse; Allele specific competitive blocker PCR; B a P DNA adduct; Carcinogenesis; K Ras, mutant fraction; Lung; Lung cancer; Mutation; Risk assessment

Indexed keywords

BENZO[A]PYRENE; DNA; K RAS PROTEIN;

ACCURACY; ALLELE; ALLELE SPECIFIC COMPETITIVE BLOCKER POLYMERASE CHAIN REACTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CODON; CONTROLLED STUDY; DNA ADDUCT; GENE MUTATION; LUNG; LUNG ALVEOLUS CELL; MALE; MOUSE; MUTATION RATE; NONHUMAN; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; WILD TYPE;

ANIMALS; BENZO(A)PYRENE; DNA ADDUCTS; DOSE-RESPONSE RELATIONSHIP, DRUG; GENES, RAS; HUMANS; LUNG; LUNG NEOPLASMS; MALE; MICE; MICE, INBRED STRAINS; MUTAGENICITY TESTS; POINT MUTATION; POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY;

MUS;

EID: 77249134225     PISSN: 08936692     EISSN: 10982280     Source Type: Journal    
DOI: 10.1002/em.20513     Document Type: Article

References (40)

1. Ahrendt SA, Decker PA, Alawi EA, Zhu YR, Sanchez-Cespedes M, Yang SC, Haasler GB, Kajdacsy-Balla A, Demeure MJ, Sidransky D. 2001. Cigarette smoking is strongly associated with mutation of the K-ras gene in patients with primary adenocarcinoma of the lung. Cancer 92:1525-1530.
2. Alexandrov K, Rojas M, Geneste O, Castegnaro M, Camus AM, Petruzzelli S, Giuntini C, Bartsch H. 1992. An improved fluorometric assay for dosimetry of benzo(a)pyrene diol-epoxide-DNA adducts in smokers' lung: Comparisons with total bulky adducts and aryl hydrocarbon hydroxylase activity. Cancer Res 52:6248-6253.
3. Andreassen A, Kure EH, Nielsen PS, Autrup H, Haugen A. 1996. Comparative synchronous fluorescence spectrophotometry and 32 P-postlabeling analysis of PAH-DNA adducts in human lung and the relationship to TP53 mutations. Mutat Res 368:275-282.
4. Baird WM, Hooven LA, Mahadevan B. 2005. Carcinogenic polycyclic aromatic hydrocarbon-DNA adducts and mechanism of action. Environ Mol Mutagen 45:106-114.
5. Banasiewicz M, Nelson G, Swank A, Grubor N, Ross J, Nesnow S, Kofeler H, Small GJ, Jankowiak R. 2004. Identification and quantitation of benzo[a]pyrene-derived DNA adducts formed at low adduction level in mice lung tissue. Anal Biochem 334:390-400.
6. Boysen G, Hecht SS. 2003. Analysis of DNA, protein adducts of benzo[a]pyrene in human tissues using structure-specific methods. Mutat Res 543:17-30.
7. Burdick AD, Ivnitski-Steele ID, Lauer FT, Burchiel SW. 2006. PYK2 mediates anti-apoptotic AKT signaling in response to benzo[a]pyrene diol epoxide in mammary epithelial cells. Carcinogenesis 27:2331-2340.
8. DeMarini DM, Landi S, Tian D, Hanley NM, Li X, Hu F, Roop BC, Mass MJ, Keohavong P, Gao W, Olivier M, Hainaut P, Mumford JL. 2001. Lung tumor KRAS and TP53 mutations in nonsmokers reflect exposure to PAH-rich coal combustion emissions. Cancer Res 61:6679-6681.
9. Dimashki M, Lim LH, Harrison RM, Harrad S. 2001. Temporal trends, temperature dependence, and relative reactivity of atmospheric polycyclic aromatic hydrocarbons. Environ Sci Technol 35:2264-2267.
10. Ding L, Getz G, Wheeler DA, Mardis ER, McLellan MD, Cibulskis K, Sougnez C, Greulich H, Muzny DM, Morgan MB, Fulton L, Fulton RS, Zhang Q, Wendl MC, Lawrence MS, Larson DE, Chen K, Dooling DJ, Sabo A, Hawes AC, Shen H, Jhangiani SN, Lewis LR, Hall O, Zhu Y, Mathew T, Ren Y, Yao J, Scherer SE, Clerc K, Metcalf GA, Ng B, Milosavljevic A, Gonzalez-Garay ML, Osborne JR, Meyer R, Shi X, Tang Y, Koboldt DC, Lin L, Abbott R, Miner TL, Pohl C, Fewell G, Haipek C, Schmidt H, Dunford-Shore BH, Kraja A, Crosby SD, Sawyer CS, Vickery T, Sander S, Robinson J, Winckler W, Baldwin J, Chirieac LR, Dutt A, Fennell T, Hanna M, Johnson BE, Onofrio RC, Thomas RK, Tonon G, Weir BA, Zhao X, Ziaugra L, Zody MC, Giordano T, Orringer MB, Roth JA, Spitz MR, Wistuba II, Ozenberger B, Good PJ, Chang AC, Beer DG, Watson MA, Ladanyi M, Broderick S, Yoshizawa A, Travis WD, Pao W, Province MA, Weinstock GM, Varmus HE, Gabriel SB, Lander ES, Gibbs RA, Meyerson M, Wilson RK. 2008. Somatic mutations affect key pathways in lung adenocarcinoma. Nature 455:1069-1075.
11. Fisher GH, Wellen SL, Klimstra D, Lenczowski JM, Tichelaar JW, Lizak MJ, Whitsett JA, Koretsky A, Varmus HE. 2001. Induction and apoptotic regression of lung adenocarcinomas by regulation of a K-Ras transgene in the presence and absence of tumor suppressor genes. Genes Dev 15:3249-3262.
12. Hakura A, Tsutsui Y, Sonoda J, Mikami T, Tsukidate K, Sagami F, Kerns WD. 1999. Multiple organ mutation in the lacZ transgenic mouse (Muta mouse) 6 months after oral treatment (5 days) with benzo[a]pyrene. Mutat Res 426:71-77.
13. Jiao S, Liu B, Gao A, Ye M, Jia X, Zhang F, Liu H, Shi X, Huang C. 2008. Benzo(a)pyrene-caused increased G1-S transition requires the activation of c-Jun through p53-dependent PI-3K/Akt/ERK pathway in human embryo lung fibroblasts. Toxicol Lett 178:167-175.
14. Kohler SW, Provost GS, Fieck A, Kretz PL, Bullock WO, Sorge JA, Putman DL, Short JM. 1991. Spectra of spontaneous and mutagen-induced mutations in the lacI gene in transgenic mice. Proc Natl Acad Sci USA 88:7958-7962.
15. Mackay W, Benasutti M, Drouin E, Loechler EL. 1992. Mutagen by (+)-anti-B[a]P-N2-Gua, the major adduct of activated benzo[a]pyrene, when studied in an Escherichia coli plasmid using sitedirected methods. Carcinogenesis 13:1415-1425.
16. Mass MJ, Jeffers AJ, Ross JA, Nelson G, Galati AJ, Stoner GD, Nesnow S. 1993. Ki-ras oncogene mutations in tumors and DNA adducts formed by benz[j]aceanthrylene and benzo[a]pyrene in the lungs of strain A/J mice. Mol Carcinog 8:186-192.
17. McKinzie PB, Delongchamp RR, Heflich RH, Parsons BL. 2001. Prospects for applying genotypic selection of somatic oncomutation to chemical risk assessment. Mutat Res 489:47-78.
18. McKinzie PB, Delongchamp RR, Chen T, Parsons BL. 2006. ACB-PCR measurement of K-ras codon 12 mutant fractions in livers of big blue rats treated with N-hydroxy-2-acetylamino.uorene. Mutagen 21:391-397.
19. Menzie CA, Potocki BB, Santodonato J. 1992. Exposure to carcinogenic PAHs in the environment. Environ Sci Technol 26:1278-1284.
20. Mukherjee JJ, Sikka HC. 2006. Attenuation of BPDE-induced p53 accumulation by TPA is associated with a decrease in stability and phosphorylation of p53 and downregulation of NFκB activation: Role of p 38 MAP kinase. Carcinogenesis 27:631-638.
21. Naumova YY, Eisenreich SJ, Turpin BJ, Weisel CP, Morandi MT, Colome SD, Totten LA, Stock TH, Winer AM, Alimokhtari S, et al. 2002. Polycyclic aromatic hydrocarbons in the indoor and outdoor air of three cities in the US. Environ Sci Technol 36:2552-2559.
22. Nesnow S, Ross JA, Stoner GD, Mass MJ. 1995. Mechanistic linkage between DNA adducts, mutations in oncogenes and tumorigenesis of carcinogenic environmental polycyclic aromatic hydrocarbons in strain A/J mice. Toxicology 105:403-413.
23. Parsons BL, Beland FA, Von Tungeln LS, Delongchamp RR, Fu PP, Heflich RH. 2005. Levels of 4-aminobiphenyl-induced somatic H-ras mutation in mouse liver DNA correlate with potential for liver tumor development. Mol Carcinog 42:193-201.
24. Reynolds SH, Anderson MW. 1991. Activation of proto-oncogenes in human and mouse lung tumors. Environ Health Perspect 93:145-148.
25. Rodenhuis S, Slebos RJ, Boot AJ, Evers SG, Mooi WJ, Wagenaar SS, van Bodegom PC, Bos JL. 1988. Incidence and possible clinical significance of K-ras oncogene activation in adenocarcinoma of the human lung. Cancer Res 48:5738-5741.
26. Rojas M, Alexandrov K, Cascorbi I, Brockmoller J, Likhachev A, Pozharisski K, Bouvier G, Auburtin G, Mayer L, Kopp-Schneider A, et al. 1998. High benzo[a]pyrene diol-epoxide DNA adduct levels in lung and blood cells from individuals with combined CYP1A1 MspI/Msp-GSTM1*0/*0 genotypes. Pharmacogenetics 8:109-118.
27. Ross JA, Nesnow S. 1999. Polycyclic aromatic hydrocarbons: Correlations between DNA adducts and ras oncogene mutations. Mutat Res 424:155-166.
28. Ross JA, Nelson GB, Wilson KH, Rabinowitz JR, Galati A, Stoner GD, Nesnow S, Mass MJ. 1995. Adenomas induced by polycyclic aromatic hydrocarbons in strain A/J mouse lung correlate with time-integrated DNA adduct levels. Cancer Res 55:1039-1044.
29. Shimmyo T, Okada A, Hashimoto T, Kobayashi Y, Miyagi Y, Ishikawa Y, Nakagawa K, Osada H, Tsuchiya E. 2008. Etiologic value of p53 mutation spectra and differences with histology in lung cancers. Cancer Sci 99:287-295.
30. Straif K, Baan R, Grosse Y, Secretan B, El Ghissassi F, Cogliano V. 2005. Carcinogenicity of polycyclic aromatic hydrocarbons. Lancet Oncol 6:931-932.
31. Tannheimer SL, Ethier SP, Caldwell KK, Burchiel SW. 1998. Benzo[a]pyrene-and TCDD-induced alterations in tyrosine phosphorylation and insulin-like growth factor signaling pathways in the MCF-10A human mammary epithelial cell line. Carcinogenesis 19:1291-1297.
32. Tretyakova N, Matter B, Jones R, Shallop A. 2002. Formation of benzo[a]pyrene diol epoxide-DNA adducts at specific guanines within K-ras and p53 gene sequences: Stable isotope-labeling mass spectrometry approach. Biochemistry 41:9535-9544.
33. Tuveson DA, Jacks T. 1999. Modeling human lung cancer in mice: Similarities and shortcomings. Oncogene 18:5318-5324.
34. Verkler TL, Delongchamp RR, Couch LH, Miller BJ, Warbritton A, Mellick PW, Howard PC, Parsons BL. 2008a. Populations of p53 codon 270 CGT to TGT mutant cells in SKH-1 mouse skin tumors induced by simulated solar light. Mol Carcinog 47:822-834.
35. Verkler TL, Delongchamp RR, Miller BJ, Webb PJ, Howard PC, Parsons BL. 2008b. Simulated solar light-induced p53 mutagenesis in SKH-1 mouse skin: A dose-response assessment. Mol Carcinog 47:599-607.
36. World Health Organization Regional Office for Europe. 1987. Air quality guidelines for Europe. WHO Regional Publications, European Series, No. 23. Copenhagen. pp 105-117.
37. Yan Y, Wang Y, Tan Q, Lubet RA, You M. 2005. Efficacy of deguelin and silibinin on benzo(a)pyrene-induced lung tumorigenesis in A/J mice. Neoplasia 7:1053-1057.
38. Yan Y, Wang Y, Tan Q, Hara Y, Yun TK, Lubet RA, You M. 2006. Efficacy of polyphenon E, red ginseng, and rapamycin on benzo. (a) pyrene-induced lung tumorigenesis in A/J mice. Neoplasia 8:52-58.
39. You M, Candrian U, Maronpot RR, Stoner GD, Anderson MW. 1989. Activation of the Ki-ras protooncogene in spontaneously occurring and chemically induced lung tumors of the strain A mouse. Proc Natl Acad Sci USA 86:3070-3074.
40. You M, Wang Y, Stoner G, You L, Maronpot R, Reynolds SH, Anderson M. 1992. Parental bias of Ki-ras oncogenes detected in lung tumors from mouse hybrids. Proc Natl Acad Sci USA 89:5804-5808.