Epistatic interactions govern chemically-induced lung tumor susceptibility and Kras mutation site in murine C57BL/6J-ChrA/J chromosome substitution strains

International Journal of Cancer

Volumn 126, Issue 1, 2010, Pages 125-132

  Dwyer Nield, Lori D ^a   McQuillan, Jay ^b   Hill Baskin, Annie ^c   Radcliffe, Richard A ^a   You, Ming ^b   Nadeau, Joseph H ^c   Malkinson, Alvin M ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLCHOLANTHRENE; CARCINOGEN; URETHAN;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER SUSCEPTIBILITY; CHROMOSOME SUBSTITUTION; CODON; CONTROLLED STUDY; GENE CONTROL; GENE MUTATION; GENETIC EPISTASIS; KRAS GENE; LUNG CARCINOGENESIS; LUNG CARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; TUMOR GENE;

ANIMALS; CARCINOGENS; EPISTASIS, GENETIC; FEMALE; GENES, RAS; GENETIC PREDISPOSITION TO DISEASE; LUNG NEOPLASMS; MALE; MICE; MICE, INBRED C57BL; MUTATION;

EID: 73449108812     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.24743     Document Type: Article

References (45)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ. Cancer statistics, 2008. CA Cancer J Clin 2008;58:71-96.
2. Sun S, Schiller JH, Gazdar AF. Lung cancer in never smokers-a different disease. Nat Rev Cancer 2007;7: 778-90.
3. Schwartz AG, Ruckdeschel JC. Familial lung cancer: genetic susceptibility and relationship to chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2006;173:16-22.
4. Bailey-Wilson JE, Amos CI, Pinney SM, Petersen GM, de Andrade M, Wiest JS, Fain P, Schwartz AG, You M, Franklin W, Klein C, Gazdar A, et al. A major lung cancer susceptibility locus maps to chromosome 6q23-25. Am J Hum Genet 2004;75:460-74.
5. Bauer AK, Malkinson AM, Kleeberger SR. Susceptibility to neoplastic and nonneoplastic pulmonary diseases in mice: genetic similarities. Am J Physiol Lung Cell Mol Physiol 2004;287:L685-L703.
6. Malkinson AM. Primary lung tumors in mice as an aid for understanding, preventing, and treating human adenocarcinoma of the lung. Lung Cancer 2001;32:265-79.
7. Fisher GH, Wellen SL, Klimstra D, Lenczowski JM, Tichelaar JW, Lizak MJ, Whitsett JA, Koretsky A, Varmus HE. 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 2001; 15:3249-62.
8. Jackson EL, Willis N, Mercer K, Bronson RT, Crowley D, Montoya R, Jacks T, Tuveson DA. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev 2001;15:3243-8.
9. Floyd HS, Farnsworth CL, Kock ND, Mizesko MC, Little JL, Dance ST, Everitt J, Tichelaar J, Whitsett JA, Miller MS. Conditional expression of the mutant KirasG12C allele results in formation of benign lung adenomas: development of a novel mouse lung tumor model. Carcinogenesis 2005;26:2196-206.
10. Shimkin MB, Stoner GD. Lung tumors in mice: application to carcinogenesis bioassay. Adv Cancer Res 1975;21:1-58.
11. Miller YE, Dwyer-Nield LD, Keith RL, Le M, Franklin WA, Malkinson AM. Induction of a high incidence of lung tumors in C57BL/6 mice with multiple ethyl carbamate injections. Cancer Lett 2003; 198:139-44.
12. Festing MF, Lin L, Devereux TR, Gao F, Yang A, Anna CH, White CM, Malkinson AM, You M. At least four loci and gender are associated with susceptibility to the chemical induction of lung adenomas in A/J x BALB/c mice. Genomics 1998;53: 129-36.
13. Lin L, Festing MF, Devereux TR, Crist KA, Christiansen SC, Wang Y, Yang A, Svenson K, Paigen B, Malkinson AM, You M. Additional evidence that the K-ras protooncogene is a candidate for the major mouse pulmonary adenoma susceptibility (Pas-1) gene. Exp Lung Res 1998;24: 481-97.
14. Malkinson AM, Radcliffe RA, Bauer AK. Quantitative trait locus mapping of susceptibilities to butylated hydroxytoluene-induced lung tumor promotion and pulmonary inflammation in CXB mice. Carcinogenesis 2002;23:411-7.
15. Wang M, Lemon WJ, Liu G, Wang Y, Iraqi FA, Malkinson AM, You M. Fine mapping and identification of candidate pulmonary adenoma susceptibility 1 genes using advanced intercross lines. Cancer Res 2003;63:3317-24.
16. Festing MF, Yang A, Malkinson AM. At least four genes and sex are associated with susceptibility to urethane-induced pulmonary adenomas in mice. Genet Res 1994;64:99-106.
17. Liu P, Wang Y, Vikis H, Maciag A, Wang D, Lu Y, Liu Y, You M. Candidate lung tumor susceptibility genes identified through whole-genome association analyses in inbred mice. Nat Genet 2006;38:888-95.
18. Manenti G, Galbiati F, Pettinicchio A, Spinola M, Piconese S, Leoni VP, Conti B, Ravagnani F, Incarbone M, Pastorino U, Dragani TA. A V141L polymorphism of the human LRMP gene is associated with survival of lung cancer patients. Carcinogenesis 2006;27:1386-90.
19. Nadeau JH, Singer JB, Matin A, Lander ES. Analysing complex genetic traits with chromosome substitution strains. Nat Genet 2000;24:221-5.
20. Gariboldi M, Manenti G, Canzian F, Falvella FS, Radice MT, Pierotti MA, Della PG, Binelli G, Dragani TA. A major susceptibility locus to murine lung carcinogenesis maps on chromosome 6. Nat Genet 1993;3:132-6.
21. Manenti G, Gariboldi M, Elango R, Fiorino A, De Gregorio L, Falvella FS, Hunter K, Housman D, Pierotti MA, Dragani TA. Genetic mapping of a pulmonary adenoma resistance (Par1) in mouse. Nat Genet 1996;12:455-7.
22. Malkinson AM, Beer DS. Major effect on susceptibility to urethane-induced pulmonary adenoma by a single gene in BALB/cBy mice. J Natl Cancer Inst 1983;70:931-6.
23. Zhang Z, Futamura M, Vikis HG, Wang M, Li J, Wang Y, Guan KL, You M. Positional cloning of the major quantitative trait locus underlying lung tumor susceptibility in mice. Proc Natl Acad Sci USA 2003;100:12642-7.
24. O'Donnell EP, Zerbe LK, Dwyer-Nield LD, Kisley LR, Malkinson AM. Quantitative analysis of early chemically-induced pulmonary lesions in mice of varying susceptibilities to lung tumorigenesis. Cancer Lett 2006;241:197-202.
25. Redente EF, Orlicky DJ, Bouchard RJ, Malkinson AM. Tumor signaling to the bone marrow changes the phenotype of monocytes and pulmonary macrophages during urethane-induced primary lung tumorigenesis in A/J mice. Am J Pathol 2007; 170:693-708.
26. Malkinson AM, Beer DS. Pharmacologic and genetic studies on the modulatory effects of butylated hydroxytoluene on mouse lung adenoma formation. J Natl Cancer Inst 1984;73:925-33.
27. Bauer AK, Dwyer-Nield LD, Keil K, Koski K, Malkinson AM. Butylated hydroxytoluene (BHT) induction of pulmonary inflammation: a role in tumor promotion. Exp Lung Res 2001;27:197-216.
28. Witschi H, Williamson D, Lock S. Enhancement of urethan tumorigenesis in mouse lung by butylated hydroxytoluene. J Natl Cancer Inst 1977;58:301-5.
29. Nuzum EO, Malkinson AM, Beer DG. Specific Ki-ras codon 61 mutations may determine the development of urethaninduced mouse lung adenomas or adenocarcinomas. Mol Carcinog 1990; 3: 287-95.
30. You M, Candrian U, Maronpot RR, Stoner GD, Anderson MW. Activation of the Kiras protooncogene in spontaneously occurring and chemically induced lung tumors of the strain A mouse. Proc Natl Acad Sci USA 1989;86:3070-4.
31. Fijneman RJ, de Vries SS, Jansen RC, Demant P. Complex interactions of new quantitative trait loci, Sluc1, Sluc2, Sluc3, and Sluc4, that influence the susceptibility to lung cancer in the mouse. Nat Genet 1996;14:465-7.
32. Svenson KL, Von SR, Magnani PA, Suetin HR, Paigen B, Naggert JK, Li R, Churchill GA, Peters LL. Multiple trait measurements in 43 inbred mouse strains capture the phenotypic diversity characteristic of human populations. J Appl Physiol 2007;102:2369-78.
33. Jackson Laboratories. Mouse Phenome Database. Mouse Genome Informatics 2008. Available at: www.informatics.jax.org. Accessed on October 2008.
34. Radiloff DR, Rinella ES, Threadgill DW. Modeling cancer patient populations in mice: Complex genetic and environmental factors. Drug Discovery Today: Disease Models 2007;4:83-8.
35. Pinto LH, Eaton E, Chen B, Fleisher J, Shuster D, McCauley J, Kedainis D, Siepka SM, Shimomura K, Song EJ, Husain A, Lakser OJ, et al. Gene-environment interactions in a mutant mouse kindred with native airway constrictor hyperresponsiveness. Mamm Genome 2008; 19:2-14.
36. Heston WE. Genetic analysis of susceptibility to induced pulmonary tumors in mice. J Natl Cancer Inst 1942;3:69-78.
37. Chen B, Johanson L, Wiest JS, Anderson MW, You M. The second intron of the Kras gene contains regulatory elements associated with mouse lung tumor susceptibility. Proc Natl Acad Sci USA 1994;91:1589-93.
38. Cooper CA, Carby FA, Bubb VJ, Lamb D, Kerr KM, Wyllie AH. The pattern of K-ras mutation in pulmonary adenocarcinoma defines a new pathway of tumour development in the human lung. J Pathol 1997;181:401-4.
39. Suzuki M, Shigematsu H, Iizasa T, Hiroshima K, Nakatani Y, Minna JD, Gazdar AF, Fujisawa T. Exclusive mutation in epidermal growth factor receptor gene, HER-2, and KRAS, and synchronous methylation of nonsmall cell lung cancer. Cancer 2006;106:2200-7.
40. Riely GJ, Kris MG, Rosenbaum D, Marks J, Li A, Chitale DA, Nafa K, Riedel ER, Hsu M, Pao W, Miller VA, Ladanyi M. Frequency and distinctive spectrum of KRAS mutations in never smokers with lung adenocarcinoma. Clin Cancer Res 2008;14:5731-4.
41. Siegfried JM, Gillespie AT, Mera R, Casey TJ, Keohavong P, Testa JR, Hunt JD. Prognostic value of specific KRAS mutations in lung adenocarcinomas. Cancer Epidemiol Biomarkers Prev 1997;6: 841-7.
42. Hunt JD, Strimas A, Martin JE, Eyer M, Haddican M, Luckett BG, Ruiz B, Axelrad TW, Backes WL, Fontham ET. Differences in KRAS mutation spectrum in lung cancer cases between African Americans and Caucasians after occupational or environmental exposure to known carcinogens. Cancer Epidemiol Biomarkers Prev 2002;11:1405-12.
43. Smit VT, Boot AJ, Smits AM, Fleuren GJ, Cornelisse CJ, Bos JL. KRAS codon 12 mutations occur very frequently in pancreatic adenocarcinomas. Nucleic Acids Res 1988;16:7773-82.
44. Fearon ER, Kohn DB, Winkelstein JA, Vogelstein B, Blaese RM. Carrier detection in the Wiskott Aldrich syndrome. Blood 1988;72:1735-9.
45. Slebos RJ, Kibbelaar RE, Dalesio O, Kooistra A, Stam J, Meijer CJ, Wagenaar SS, Vanderschueren RG, van Zandwijk N, Mooi WJ. K-ras oncogene activation as a prognostic marker in adenocarcinoma of the lung. N Engl J Med 1990;323:561-5.