Mechanistic models fit to ED001 data on >40, 000 trout exposed to dibenzo[A, L]pyrene indicate mutations do not drive increased tumor risk

Dose-Response

Volumn 12, Issue 3, 2014, Pages 386-403

  Bogen, Kenneth T ^a  

^a EXPONENT INC   (United States)

Author keywords

Bioassay; Biologically based models; Cancer; Low dose linearity; Mutagen; Tumorigenesis

Indexed keywords

DIBENZO[A,L]PYRENE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOASSAY; CANCER INCIDENCE; CANCER MODEL; CANCER RISK; CELL POPULATION; CHEMICAL CARCINOGENESIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; GENE MUTATION; LIVER CANCER; MATHEMATICAL MODEL; NONHUMAN; NONLINEAR SYSTEM; STOMACH CANCER; TROUT;

EID: 84905671394     PISSN: None     EISSN: 15593258     Source Type: Journal    
DOI: 10.2203/dose-response.13-019.Bogen     Document Type: Article

References (54)

1. Albert R. 1994. Carcinogen risk assessment in the U.S. Environmental Protection Agency. Crit Rev Toxicol 24(1):75-85.
2. Anderson E. L, Albert RE, McGaughy R, Bayard S, Bayliss D, Chen C, Chu M, Gibb H, Haberman B, Hiremath C., Singh D, and Thorslund T. 1983. Quantitative approaches in use to assess cancer risk. Risk Anal 3(4):277-295.
3. Armitage P., and Doll R. 1957. A two-stage theory of carcinogenesis in relation to the age distribution of human cancer. Br J Cancer 11:161-169.
4. Baglivo J., Oliver D, and Pagano M. 1988. Methods for the analysis of contingency tables with large and small cell counts. J Am Statist Assoc 83:1006-1013.
5. Bailey G. S, Reddy AP, Pereira CB, Harttig U, Baird W, Spitsbergen JM, Hendricks JD, Orner GA, Williams D. E, and Swenberg JA. 2009. Non-linear cancer response at ultra-low dose: a 40,800-animal ED001 tumor and biomarker study. Chem Res Toxicol 22:1264-1276.
6. Benninghoff A. D, Orner GA, Buchner CH, Hendricks JD, Duffy AM, and Williams DE. 2012. Promotion of hepatocarcinogenesis by perfluoroalkyl acids in rainbow trout. Toxicol Sci 125(1):69-78.
7. Bogen K.T. 2013. Efficient tumorigenesis by mutation-induced failure to terminate microRNA-mediated adaptive hyperplasia. Med Hypoth 80:83-93.
8. Bolt H. M, Foth H, Hengstler JG, and Degen GH. 2004. Carcinogenicity categorization of chemicalsnew aspects to be considered in a European perspective. Toxicol Lett 151(1):29-41.
9. Busby W. F Jr, Smith H, Crespi CL, and Penman BW. 1995. Mutagenicity of benzo[a]pyrene and dibenzopyrenes in the Salmonella typhimurium TM677 and the MCL-5 human cell forward mutation assays. Mutat Res 342(1-2):9-16.
10. Buters J. T, Mahadevan B, Quintanilla-Martinez L, Gonzalez FJ, Greim H, Baird WM, and Luch A. 2002. Cytochrome P450 1B1 determines susceptibility to dibenzo[a, l]pyrene-induced tumor formation. Chem Res Toxicol 15(9):1127-1135.
11. Chakravarti D., Pelling JC, Cavalieri EL, and Rogan EG. 1995. Relating aromatic hydrocarboninduced DNA adducts and c-H-ras mutations in mouse skin papillomas: The role of apurinic sites. Proc Natl Acad Sci USA 92(22):10422-10426.
12. Chakravarti D., Mailander PC, Cavalieri EL, and Rogan EG. 2000. Evidence that error-prone DNA repair converts dibenzo[a, l]pyrene-induced depurinating lesions into mutations: Formation, clonal proliferation and regression of initiated cells carrying H-ras oncogene mutations in early preneoplasia. Mutat Res 456(1-2):17-32.
13. Crump K. S, Subramaniam RP, and Van Landingham CB. 2005. A numerical solution to the nonhomogeneous two-stage MVK model of cancer. Risk Anal 25(4):921-926.
14. Dashwood, R, Negishi T, Hayatsu H, Breinholt V, Hendricks J, and Bailey G. 1999. Chemopreventive properties of chlorophylls towards aflatoxin B1: a review of the antimutagenicity and anticarcinogenicity data in rainbow trout. Carcinogenesis 20(10):1919-1926.
15. DeMarini D. M, Hanley NM, Warren SH, Adams LD, and King LC. 2011. Association between mutation spectra and stable and unstable DNA adduct profiles in Salmonella for benzo[a]pyrene and dibenzo[a, l]pyrene. Mutat Res 714(1-2):17-25.
16. FAO. 2011. Small-scale rainbow trout farming. FAO Fisheries and Aquaculture Technical Paper 561, by Woynarovich A, Hoitsy G, and Moth-Poulsen T. United Nations Food and Agriculture Program (FAO), Rome, Italy, p. 11.
17. Guttenplan J. B, Kosinska W, Zhao ZL, Chen KM, Aliaga C, DelTondo J, Cooper T, Sun YW, Zhang SM, Jiang K., Bruggeman R, Sharma AK, Amin S, Ahn K, and El-Bayoumy K. 2012. Mutagenesis and carcinogenesis induced by dibenzo[a, l]pyrene in the mouse oral cavity: a potential new model for oral cancer. Int J Cancer 130(12):2783-2790.
18. Higginbotham S., RamaKrishna NV, Johansson SL, Rogan EG, and Cavalieri EL. 1993. Tumor-initiating activity and carcinogenicity of dibenzo[a, l]pyrene versus 7,12-dimethylbenz [a]anthracene and benzo[a]pyrene at low doses in mouse skin. Carcinogenesis 14:875-878.
19. Kushman M. E, Kabler SL, Ahmad S, Doehmer J, Morrow CS, and Townsend AJ. 2007. Cytotoxicity and mutagenicity of dibenzo[a, l]pyrene and (+/-)-dibenzo[a, l]pyrene-11,12-dihydrodiol in V79MZ cells co-expressing either hCYP1A1 or hCYP1B1 together with human glutathione-S-transferase A1. Mutat Res 624(1-2):80-87.
20. Lagerqvist A., Håkansson D, Prochazka G, Lundin C, Dreij K, Segerbäck D, Jernström B, Törnqvist M, Seidel A., Erixon K, and Jenssen D. 2008. Both replication bypass fidelity and repair efficiency influence the yield of mutations per target dose in intact mammalian cells induced by benzo[a]pyrene-diol-epoxide and dibenzo[a, l]pyrene-diol-epoxide. DNA Repair (Amst) 7(8):1202-1212.
21. Lemieux C. L, Douglas GR, Gingerich J, Phonethepswath S, Torous DK, Dertinger SD, Phillips DH, Arlt V. M, and White PA. 2011. Simultaneous measurement of benzo[a]pyrene-induced Pig-a and lacZ mutations, micronuclei and DNA adducts in Muta™ Mouse. Environ Molec Mutagen 52(9):756-765.
22. Leubeck E. G, Heidenreich WF, Hazelton WD, Paretzke HG, and Moolgavkar SH. 1999. Biologically based analysis of the data for the Colorado uranium miners cohort: Age, dose and dose-rate effects. Radiat Res 152:339-351.
23. Mahadevan B., Luch A, Bravo CF, Atkin J, Steppan LB, Pereira C, Kerkvliet NI, and Baird WM. 2005. Dibenzo[a, l]pyrene induced DNA adduct formation in lung tissue in vivo. Cancer Lett 227(1):25-32.
24. Meschini R., Berni A, Marotta E, Filippi S, Fiore M, Mancinelli P, Natarajan AT, and Palitti F. 2010. DNA repair mechanisms involved in the removal of DBPDE-induced lesions leading to chromosomal alterations in CHO cells. Cytogenet Genome Res 128(1-3):124-130.
25. Moolgavkar S. H, and Knudson AG Jr. 1981. Mutation and cancer: A model for human carcinogenesis. J Natl Cancer Inst; 66:1037-1052.
26. Moolgavkar S.H. 1983. Model for human carcinogenesis: Action of environmental agents. Environ Health Perspect 50:285-291.
27. Moolgavkar S.H. 1988. Biologically motivated two-stage model for cancer risk assessment. Toxicol Lett 43:139-150.
28. Moolgavkar S., and Luebeck G. 1990. Two-event model for carcinogenesis: Biological, mathematical, and statistical considerations. Risk Anal 10:323-341.
29. Moolgavkar S. H, and Venzon DJ. 1979. Two-event models for carcinogenesis: Incidence curves for childhood and adult tumors. Math Biosci 47:55-77.
30. Moolgavkar S. H, Dewanji A, and Venzon DJ. 1988. A stochastic two-stage model for cancer risk assessment. 1. The hazard function and the probability of tumor. Risk Anal 8:383-392.
31. Moolgavkar S. H, Dewanji A, and Luebeck G. 1989. Cigarette smoking and lung cancer: A reanalysis of the British doctors' data. JNCI 81:415-420.
32. Mourón S. A, Grillo CA, Dulout FN, and Golijow CD. 2006. Genotoxic effects of benzo[a]pyrene and dibenzo[a, l]pyrene in a human lung cell line. Int J Toxicol 25(1):49-55.
33. Nesnow S., Davis C, Nelson G, Ross JA, Allison J, Adams L, and King LC. 1997. Comparison of the morphological transforming activities of dibenzo[a, l]pyrene and benzo[a]pyrene in C3H10T1/2CL8 cells and characterization of the dibenzo[a, l]pyrene-DNA adducts. Carcinogenesis 18(10):1973-1978.
34. Nesnow S., Davis C, Padgett WT, Adams L, Yacopucci M, and King LC. 2000. 8,9-dihydroxy-8,9-dihydrodibenzo[a, l]pyrene is a potent morphological cell-transforming agent in C3H10T(1)/(2)Cl8 mouse embryo fibroblasts in the absence of detectable stable covalent DNA adducts. Carcinogenesis 21(6):1253-1257.
35. NRC. 1994. Science and judgment in risk assessment. National Research Council (NRC). National Academies Press, Washington, DC.
36. O'Brien J, Renwick AG, Constable A, Dybing E, Müller DJ, Schlatter J, Slob W, Tueting W, van Benthem J., Williams GM, and Wolfreys A. 2006. Approaches to the risk assessment of genotoxic carcinogens in food: a critical appraisal. Food Chem Toxicol 44(10):1613-1635.
37. Plísková M., Vondrácek J, Vojtesek B, Kozubík A, and Machala M. 2005. Deregulation of cell proliferation by polycyclic aromatic hydrocarbons in human breast carcinoma MCF-7 cells reflects both genotoxic and nongenotoxic events. Toxicol Sci 83(2):246-256.
38. Prahalad A. K, Ross JA, Nelson GB, Roop BC, King LC, Nesnow S, and Mass MJ. 1997. Dibenzo[a, l]pyrene-induced DNA adduction, tumorigenicity, and Ki-ras oncogene mutations in strain A/J mouse lung. Carcinogenesis 18(10):1955-1563.
39. Press W. H, Teukolsky SA, Vetterling WT, and Flannery BP. 1986. Numerical Recipes. Cambridge University Press, New York, NY, p. 521-528.
40. Reddy A. P, Harttig U, Barth MC, Baird WM, Schimerlik M, Hendricks JD, and Bailey GS. 1999a. Inhibition of dibenzo[a, l]pyrene-induced multi-organ carcinogenesis by dietary chlorophyllin in rainbow trout. Carcinogenesis 20(10):1919-1926.
41. Reddy A. P, Spitsbergen JM, Mathews C, Hendricks JD, and Bailey GS. 1999b. Experimental hepatic tumorigenicity by environmental hydrocarbon dibenzo[a, l]pyrene. J Environ Pathol Toxicol Oncol 18(4):261-269.
42. Schober W., Luch A, Soballa VJ, Raab G, Stegeman JJ, Doehmer J, Jacob J, and Seidel A. 2006. On the species-specific biotransformation of dibenzo[a, l]pyrene. Chem Biol Interact 161(1):37-48.
43. Topinka J., Marvanová S, Vondrácek J, Sevastyanova O, Nováková Z, Krcmár P, Pencíková K, and Machala M. 2008. DNA adducts formation and induction of apoptosis in rat liver epithelial 'stem-like' cells exposed to carcinogenic polycyclic aromatic hydrocarbons. Mutat Res 638(12):122-132.
44. U.S. EPA. 1976. Health Risk and Economic Impact Assessments of Suspected Carcinogens: Interim Procedures & Guidelines. Federal Register 47(102, May 25):21402-21405. U.S. Environmental Protection Agency (EPA), National Center for Environmental Assessment, Washington, DC.
45. U.S. EPA. 1986. Guidelines for Carcinogen Risk Assessment. EPA/630/R-00/004, September 1986. Federal Register 51(185, September 24):33992-34003. U.S. Environmental Protection Agency (EPA), Risk Assessment Forum, Washington, DC.
46. U.S. EPA. 2005. Guidelines for carcinogen risk assessment. EPA/630/P-03/001F, March 2005. U.S. Environmental Protection Agency (EPA), Risk Assessment Forum, Washington, DC.
47. U.S. EPA. 2007. Framework for Determining a Mutagenic Mode of Action for Carcinogenicity: Using EPA's 2005 Cancer Guidelines and Supplemental Guidance for Assessing Susceptibility from Early-Life Exposure to Carcinogens. EPA 120/R-07/002-A, September 2007.
48. U.S. Environmental Protection Agency (EPA), Risk Assessment Forum Technical Panel on Mutagenic Mode of Action, Washington, DC.
49. Williams D.E. 2012. The rainbow trout liver cancer model: response to environmental chemicals and studies on promotion and chemoprevention. Comp Biochem Physiol C Toxicol Pharmacol 155(1):121-127.
50. Williams D. E, Bailey GS, Reddy A, Hendricks JD, Oganesian A, Orner GA, Pereira CB, and Swenberg JA. 2003. The rainbow trout (Oncorhynchus mykiss) tumor model: recent applications in lowdose exposures to tumor initiators and promoters. Toxicol Pathol 31 Suppl:58-61.
51. Williams D. E, Orner G, Willard KD, Tilton S, Hendricks JD, Pereira C, Benninghoff AD, and Bailey GS. 2009. Rainbow trout (Oncorhynchus mykiss) and ultra-low dose cancer studies. Comp Biochem Physiol C. Toxicol Pharmacol 149(2):175-181.
52. Wolfram Research. 2013. Wolfram Mathematica9 Documentation Center. Wolfram Research, Inc., Champaign, IL. http://reference.wolfram.com/mathematica/guide/Mathematica.html (www.wolfram.com).
53. Yoon J. H, Besaratinia A, Feng Z, Tang MS, Amin S, Luch A, and Pfeifer GP. 2004. DNA damage, repair, and mutation induction by (+)-Syn and (-)-anti-dibenzo[a, l]pyrene-11,12-diol-13,14-epoxides in mouse cells. Cancer Res 64(20):7321-7328.
54. Zipperman M. 1999. Detecting apoptosis in carcinogen exposed trout livers. Bioresource Research Thesis. Oregon State University, Corvallis, OR. http://ir.library.oregonstate.edu/xmlui/bitstream/handle/1957/7407/Zipperma.pdf?sequence=1