Predicting the carcinogenicity of chemicals with alternative approaches: Recent advances

Expert Opinion on Drug Metabolism and Toxicology

Volumn 10, Issue 9, 2014, Pages 1199-1208

  Benigni, Romualdo ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Alternative; Carcinogen; Cell transformation; Genotox; Nongenotox; Predictive toxicology; Quantitative structure activity relationships; Read across; ToxCast

Indexed keywords

CARCINOGEN; CHEMICAL COMPOUND; DNA; DISINFECTANT AGENT;

CARCINOGENICITY; CELL TRANSFORMATION; CHEMICAL CARCINOGENESIS; DNA ADDUCT; DNA DAMAGE; FALSE NEGATIVE RESULT; FALSE POSITIVE RESULT; GENOTOXICITY; HIGH THROUGHPUT SCREENING; HUMAN; IN VITRO STUDY; NONHUMAN; QUANTITATIVE STRUCTURE ACTIVITY RELATION; REVIEW; SALMONELLA; TECHNOLOGY; TISSUE GROWTH; TISSUE INJURY; TOXICITY TESTING; ANIMAL; ANIMAL TESTING ALTERNATIVE; BIOASSAY; CARCINOGEN TESTING; CHEMISTRY; LABORATORY DIAGNOSIS; MUTAGEN TESTING; PROCEDURES; TOXICITY;

ANIMAL TESTING ALTERNATIVES; ANIMALS; BIOLOGICAL ASSAY; CARCINOGENICITY TESTS; CARCINOGENS; DISINFECTANTS; FALSE NEGATIVE REACTIONS; FALSE POSITIVE REACTIONS; HUMANS; MUTAGENICITY TESTS; QUANTITATIVE STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84906060242     PISSN: 17425255     EISSN: 17447607     Source Type: Journal    
DOI: 10.1517/17425255.2014.934670     Document Type: Review

References (50)

1. Huff JE, Haseman JK, Rall DP. Scientific concepts, value, and significance of chemical carcinogenesis studies. Ann Rev Pharmacol Toxicol 1991;31:621-5
2. Huff J. Value, validity, and historical development of carcinogenesis studies for predicting and confirming carcinogenic risks to humans. In: Kitchin KT, editor. Carcinogenicity. Testing, predicting, and interpreting chemical effects. Marcel Dekker, Inc, New York; 1999. p. 21-123
3. Huff J. Long-term chemical carcinogenesis bioassays predict human cancer hazards. Issues, controversies, and uncertainties. Ann NY Acad Sci 1999;895:56-79
4. Judson R, Richard AM, Dix D, et al. ACToR - Aggregated Computational Toxicology Resource. Toxicol Appl Pharmacol 2008;233:7-13
5. Kubinyi H. Drug research: myths, hype and reality. Nat Rev Drug Discov 2003;2:665-8
6. Durham SK, Pearl GM. Computational methods to predict drug safety liability. Curr Opin Drug Discov Devel 2001;4:110-15
7. Greene N, Naven R. Early toxicity screening strategies. Curr Opin Drug Discov Devel 2009;12:90-7
8. Sankar U. The delicate toxicity balance in drug discovery. Scientist 2005;19:32
9. Zeiger E. Identification of rodent carcinogens and noncarcinogens using genetic toxicity tests: premises, promises, and performance. Regul Toxicol Pharmacol 1998;28:85-95
10. Benigni R. Alternatives to the carcinogenicity bioassay for toxicity prediction: are we there yet? Expert Opin Drug Metab Toxicol 2012;8:1-11
11. Kirkland D, Pfuhler S, Tweats D, et al. How to reduce false positive results when undertaking in vitro genotoxicity testing and thus avoid unnecessary follow-up animal tests: report of an ECVAM Workshop. Mutat Res 2007;628:31-55
12. Kirkland D, Speit G. Evaluation of the ability of a battery of three in vitro genotoxicity tests to discriminate rodent carcinogens and non-carcinogens III. Appropriate follow-up testing in vivo. Mutat Res 2008;654:114-32
13. Hernandez LG, van Steeg H, Luijten M, van Benthem J. Mechanisms of nongenotoxic carcinogens and importance of a weight of evidence approach. Mutat Res 2009;682:94-109
14. Schmidt C. Testing for carcinogens: shift from animals to automation gathers steam - slowly. J Natl Cancer Inst 2009;101:910-12
15. EFSA. Existing approaches incorporating replacement, reduction and refinement of animal testing: applicability in food and feed risk assessment. EFSA J 2009;1052:1-57
16. Bishop P, Manuppello JR, Willett JB, Sandler JT. Animal use and lessons learned in the US High Production Volume chamicals challenge program. Environ Health Perspect 2013;120:1631-9
17. Basketter DA, Clewell HJ, Kimber I, et al. A roadmap for the development of alternative (non-animal) methods for systemic toxicity testing. ALTEX 2012;29:3-91
18. Abbott A. Animal testing: more than a cosmetic change. Nature 2005;438:144-6
19. Benigni R, Bossa C, Tcheremenskaia O. In vitro cell transformation assays for an integrated, alternative assessment of carcinogenicity: a data-based analysis. Mutagenesis 2013;28:107-16
20. Yamasaki H. Non-genotoxic mechanisms of carcinogenesis: studies of cell transformation and gap junctional intercellular communication. Toxicol Lett 1995;77:55-61
21. Benigni R, Bossa C. Alternative strategies for carcinogenicity assessment: an efficient and simplified approach based on in vitro mutagenicity and cell transformation assays. Mutagenesis 2011;26:455-60
22. International Agency for Research on Cancer, World Health Organisation. Available from: http://monographs.iarc.fr/ENG/Classification/index.php [Accessed 11 June 2014]
23. Benigni R, Bossa C, Battistelli CL, Tcheremenskaia O. IARC. Class 1 and 2 carcinogens are successfully identified by an alternative strategy that detects DNA-reactivity and cell transformation ability of chemicals. Mutat Res 2013;578:56-61
24. Woo YT. Mechanisms of action of chemical carcinogens, and their role in Structure-Activity Relationships (SAR) analysis and risk assessment. In: Benigni R, editor. Quantitative Structure-Activity Relationship (QSAR) models of mutagens and carcinogens. CRC Press, Boca Raton; 2003. p. 41-80
25. Benigni R, Bossa C. Mechanisms of chemical carcinogenicity and mutagenicity: a review with implications for predictive toxicology. Chem Rev 2011;111:2507-36
26. Creton S, Aardema MJ, Carmichael P, et al. Cell transformation assays for prediction of carcinogenic potential: state of the science and future research needs. Mutagenesis 2012;62:93-101
27. Mauthe RJ, Gibson DP, Bunch RT, Custer L. The Syrian Hamster Embryo (SHE) cell transformation assay: review of the methods and results. Toxicol Pathol 2001;29:138-46
28. Haga K, Ohno S, Yugawa T, et al. Efficient immortalization of primary human cells by p.16INK4a-specific short hairpin RNA or Bmi-1, combined with introduction of hTERT. Cancer Sci 2007;98:147-54
29. Stuard SB, Kerckaert GA, Lehman-McKeeman LD. Characterisation of the metabolic capacity of Syrian hamster embryo (SHE) cells. Toxicol Sci 1999;48:366
30. Nguyen-Ba G, Vasseur P. Epigenetic events during the process of cell transformation induced by carcinogens (review). Oncol Rep 1999;6:925-32
31. OECD. Detailed review paper on cell transformation assays for detection of chemical carcinogens. OECD, Paris; 2007
32. Corvi R, Aardema MJ, Gribaldo L, et al. ECVAM prevalidation study on in vitro cell transformation assays: general outline and conclusions of the study. Mutat Res 2011;744:12-19
33. Benigni R, Bossa C, Tcheremenskaia O. Nongenotoxic carcinogenicity of chemicals: mechanisms of action, and early recognition through a new set of structural alerts. Chem Rev 2013;113:2940-57
34. Lai DY, Woo YT. Reducing carcinogenicity and mutagenicity through mechanism-based molecular design of chemicals. In: Boethling RS, Voutchkova AM, editors. Green processes. Volume 9 Designing safer chemicals Wiley-VCH, Heidelberg; 2012
35. Dix DJ, Houck KA, Martin MT, et al. The TOXCast program for prioritizing toxicity testing of environmental chemicals. Toxicol Sci 2007;95:5-12
36. Kavlock RJ, Austin CP, Tice RR. Toxicity testing in the 21st century: implications for human health risk assessment. Risk Anal 2009;29:485-7
37. Kleinstreuer NC, Dix D, Houck K, et al. In vitro perturbations of targets in cancer hallmark processes predict rodent chemical carcinogenesis. Toxicol Sci 2013;131:40-55
38. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70
39. Benigni R. Evaluation of the toxicity forecasting capability of EPA's ToxCast Phase I data: can ToxCast in vitro assays predict carcinogenicity? J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 2013;31:201-12
40. Thomas RS, Black MB, Li L, et al. A comprehensive statistical analysis of predicting in vivo hazard using highthroughput in vitro screening. Toxicol Sci 2012;128:398-417
41. Kavlock RJ, Tice RR, Austin CP. A 2012 US Tox21 Progress Report. In: Seidle T, Spielmann H, editors. Alternative testing strategies, and AXLR8-3 workshop report on a "Roadmap to next generation safety testing under Horizon 2000". Organization for the Economic Cooperation and Development (OECD), Berlin; 2012. p. 180-5
42. Carcino GENOMICS, a project of the European Union. Available from: http://www.carcinogenomics.eu/index.php?id=100 [Last accessed 11 June 2014]
43. Woo YT, Lai DY. Oncologic: a mechanism based expert system for predicting the carcinogenic potential of chemicals. In: Helma C, editor. Predictive toxicology. Taylor and Francis, Boca Raton; 2005. p. 385-413
44. Woo YT, Lai DY. Mechanism-based structure-activity relationship analysis of chemical carcinogens. In: Hsu G, Stedeford T, editors. Cancer risk assessment: chemical carcinogenesis, hazard evaluation, and risk quantification. Wiley, New York; 2010. p. 517-56
45. Van Leeuwen K, Schultz TW, Henry T, et al. Using chemical categories to fill data gaps in hazard assessment. SAR QSAR Environ Res 2009;20:207-20
46. OECD, Better policies for better lives. Available from: http://www.oecd.org/env/ehs/risk-assessment/groupingofchemical schemicalcategoriesandread-across.htm [Last accessed 11 June 2014]
47. OECD, Better policies for better lives. Available from: http://www.oecd.org/chemicalsafety/theoecdqsartoolbox.htm [Last accessed 11 June 2014]
48. OECD, Better policies for better lives. Available from: http://www.oecd.org/chemicalsafety/testing/adverse-outcomepathways-molecular- screening-andtoxicogenomics.htm [Last accessed 11 June 2014]
49. Benigni R, Bossa C, Tcheremenskaia O, et al. The new ISSMIC database on in vivo micronucleus, and its role in assessing genotoxicity testing strategies. Mutagenesis 2012;27:87-92
50. Veith GD, Benigni R, Manuppello JR, et al. Recommendations for sstakeholder discussion on reducing animal testing in cancer assessment. International QSAR Foundation; Duluth, MN; 2012