Correlation of in vivo versus in vitro Benchmark doses (BMDs) derived from micronucleus test data: A proof of concept study

Toxicological Sciences

Volumn 148, Issue 2, 2015, Pages 355-367

  Soeteman Hernández, Lya G ^a   Fellows, Mick D ^b   Johnson, George E ^c   Slob, Wout ^a  

^a NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^b ASTRAZENECA   (United Kingdom)

^c SWANSEA UNIVERSITY   (United Kingdom)

Author keywords

Genotoxic potenc; In vitro micronucleus; TK6 cells, benchmark dose approach

Indexed keywords

1,2 DIBROMOETHANE; 1,2 DIMETHYLHYDRAZINE; 1,2 PHENYLENEDIAMINE; 4 CHLORO 2 PHENYLENEDIAMINE; 4 CHLOROANILINE; 4,4 DICHLORODIPHENYLSULFONE; BENZO[A]PYRENE; CARCINOGEN; CHLORAL HYDRATE; CHLORAMBUCIL; CHLOROFORM; CLASTOGEN; CYCLOPHOSPHAMIDE; DECALIN; DIAMINE DERIVATIVE; DIMETHYL SULFOXIDE; ETHER; GLYCERYL TRINITRATE; GLYCIDOL; HEXYLRESORCINOL; METHYLNITROSOUREA; MUTAGENIC AGENT; N (2 FLUORENYL)ACETAMIDE; PHENOLPHTHALEIN; PROPYLENE GLYCOL MONO TERT BUTYL ETHER; SULFONE DERIVATIVE; TETRACHLOROETHANE; TRICHLOROETHYLENE; UNCLASSIFIED DRUG; URETHAN;

ARTICLE; CARCINOGENICITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENOTOXICITY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LYMPHOBLASTOID CELL LINE; MALIGNANT NEOPLASTIC DISEASE; METABOLIC ACTIVATION; MICRONUCLEUS TEST; MUTAGENICITY; ANIMAL; ANIMAL TESTING ALTERNATIVE; BENCHMARKING; BIOLOGICAL MODEL; CELL LINE; CHEMICALLY INDUCED; COMPARATIVE STUDY; DOSE RESPONSE; DRUG EFFECTS; LYMPHOCYTE; MICRONUCLEUS; PATHOLOGY; REPRODUCIBILITY; RISK ASSESSMENT; STANDARDS;

ANIMAL TESTING ALTERNATIVES; ANIMALS; BENCHMARKING; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; LYMPHOCYTES; MICRONUCLEI, CHROMOSOME-DEFECTIVE; MICRONUCLEUS TESTS; MODELS, BIOLOGICAL; REPRODUCIBILITY OF RESULTS; RISK ASSESSMENT;

EID: 84952897103     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfv189     Document Type: Article

References (67)

1. Asano, N., and Hagiwara, T. (1992). The mouse peripheral blood micronucleus test with 2-acetylaminofluorene using the acridine orange supravital staining method. Mutat. Res. 278, 153-157.
2. Ashby, J., and Mirkova, E. (1987). Re-evaluation of 1, 2-dimethylhydrazine in the mouse bone marrow micronucleus assay: observation of a positive response. Environ. Mutagen. 9, 177-181.
3. Barlow, S., Renwick, A. G., Kleiner, J., Bridges, J. W., Busk, L., Dybing, E., Edler, L., Eisenbrand, G., Fink-Gremmels, J., Knaap, A., et al. (2006). Risk assessment of substances that are both genotoxic and carcinogenic report of an International Conference organized by EFSA and WHO with support of ILSI Europe. Food Chem. Toxicol. 44, 1636-1650.
4. Bemis, J. C., Wills, J. W., Bryce, S. M., Torous, D. K., Dertinger, S. D., and Slob, W. (2015). Comparison of in vitro and in vivo clastogenic potency based on benchmark dose analysis of flow cytometric micronucleus data. Mutagenesis. DOI: 10.1093/mutage/gev041.
5. Benford, D., Dinovi, M., and Setzer, R. W. (2010). Application of the margin-of-exposure (MoE) approach to substances in food that are genotoxic and carcinogenic e.g.: Benzo[a]pyrene and polycyclic aromatic hydrocarbons. Food Chem. Toxicol. 48 (Suppl 1), S42-S48.
6. Blaauboer, B. J. (2010). Biokinetic modeling and in vitro-in vivo extrapolations. J. Toxicol. Environ. Health. B Crit. Rev. 13, 242-252.
7. Bolognesi, C., and Creus, A., Ostrosky-Wegman, P., and Marcos, R. (2011). Micronuclei and pesticide exposure. Mutagenesis 26, 19-26.
8. Bonassi, S., El-Zein, R., Bolognesi, C., and Fenech, M. (2011). Micronuclei frequency in peripheral blood lymphocytes and cancer risk: Evidence from human studies. Mutagenesis 26, 93-100.
9. Burke, D. A., Wedd, D. J., Herriott, D., Bayliss, M. K., Spalding, D. J., and Wilcox, P. (1994). Evaluation of pyrazole and ethanol induced S9 fraction in bacterial mutagenicity testing. Mutagenesis 9, 23-29.
10. Butterworth, B. E., Templin, M. V., Constan, A. A., Sprankle, C. S., Wong, B. A., Pluta, L. J., Everitt, J. I., and Recio, L. (1998). Longterm mutagenicity studies with chloroform and dimethylnitrosamine in female lacI transgenic B6C3F1 mice. Environ. Mol. Mutagen. 31, 248-256.
11. Colacci, A., Bartoli, S., Bonora, B., Buttazzi, C., Lattanzi, G., Mazzullo, M., Niero, A., Turina, M. P., and Grilli, S. (1989). Covalent binding of 1, 1, 1, 2-tetrachloroethane to nucleic acids as evidence of genotoxic activity. J. Toxicol. Environ. Health 26, 485-495.
12. Doak, S. H., Jenkins, G. J., Johnson, G. E., Quick, E., Parry, E. M., and Parry, J. M. (2007). Mechanistic influences for mutation induction curves after exposure to DNA-reactive carcinogens. Cancer Res. 67, 3904-3911.
13. Eastmond, D. A., Hartwig, A., Anderson, D., Anwar, W. A., Cimino, M. C., Dobrev, I., Douglas, G. R., Nohmi, T., Phillips, D. H., and Vickers, C. (2009). Mutagenicity testing for chemical risk assessment: Update of the WHO/IPCS Harmonized Scheme. Mutagenesis 24, 341-349.
14. EFSA. (2009a). Risk Assessment Methodologies and Approaches for Genotoxic and Carcinogenic Substances. Available at: http://ec.europa.eu/health/ph_risk/committees/04_scher/docs/scher_o_113.pdf. Accessed July 10, 2014.
15. EFSA. (2009b). European Food Safety Authority. Guidance of the scientific committee on use of the benchmark dose approach in risk assessment. EFSA J. 1150, 1-72.
16. Fellows, M. D., Doherty, A. T., Priestley, C. C., Howarth, V., and O'Donovan, M. R. (2011). The ability of the mouse lymphoma TK assay to detect aneugens. Mutagenesis 26, 771-781.
17. Gollapudi, B. B., Johnson, G. E., Hernandez, L. G., Pottenger, L. H., Dearfield, K. L., Jeffrey, A. M., Julien, E., Kim, J. H., Lovell, D. P., Macgregor, J. T., et al. (2013). Quantitative approaches for assessing dose-response relationships in genetic toxicology studies. Environ. Mol. Mutagen. 54, 8-18.
18. Gorelick, N. J., Andrews, J. L., deBoer, J. G., Young, R., Gibson, D. P., and Walker, V. E. (1999). Tissue-specific mutant frequencies and mutational spectra in cyclophosphamide-treated lacI transgenic mice. Environ. Mol. Mutagen. 34, 154-166.
19. Hatanaka, Y., Kitagawa, Y., Toyoda, Y., Kawata, T., Ando, N., Kawabata, Y., Iwai, M., and Arimura, H. (1992). Micronucleus test with cyclophosphamide using mouse peripheral blood reticulocytes. Mutat. Res. 278, 99-101.
20. Heflich, R. H., and Neft, R. E. (1994). Genetic toxicity of 2-acetylaminofluorene, 2-aminofluorene and some of their metabolites and model metabolites. Mutat. Res. 318, 73-114.
21. Hernandez, L. G., and Forkert, P. G. (2007). In vivo mutagenicity of vinyl carbamate and ethyl carbamate in lung and small intestine of F1 (Big Blue x A/J) transgenic mice. Int. J. Cancer 120, 1426-1433.
22. Hernandez, L. G., Slob, W., van Steeg, H., and van Benthem, J. (2011). Can carcinogenic potency be predicted from in vivo genotoxicity data? a meta-analysis of historical data. Environ. Mol. Mutagen. 52, 518-528.
23. Hernandez, L. G., van Benthem, J., and Johnson, G. E. (2013). A mode-of-action approach for the identification of genotoxic carcinogens. PLoS One 8, e64532.
24. Hernandez, L. G., van Benthem, J., and Slob, W. (2012). Estimating the carcinogenic potency of chemicals from the in vivo micronucleus test. RIVM Report 340700007/2012. Available at: http://www.rivm.nl/dsresource?objectid=rivmp:204525&type=org&disposition=inline. Accessed January 20, 2014.
25. Iarmarcovai, G., Ceppi, M., Botta, A., Orsiere, T., and Bonassi, S. (2008). Micronuclei frequency in peripheral blood lymphocytes of cancer patients: A meta-analysis. Mutat. Res. 659, 274-283.
26. ICCVAM. (2006). Interagency Coordinating Committee on the Validation of Alternative Methods (ICCVAM) Test Method Evaluation: in vitro Cytotoxicity Test Methods for Estimating Starting Doses for Acute Oral Systemic Toxicity Tests. Available at: http://ntp.niehs.nih.gov/iccvam/docs/acutetox_docs/brd_tmer/at-tmer-complete.pdf. Accessed July 8, 2015.
27. Ikeda, N., Fujii, K., Sarada, M., Saito, H., Kawabata, M., Naruse, K., Yuki, K., Nakagiri, H., Honda, H., Tamaki, Y., et al. (2012). Genotoxicity studies of glycidol fatty acid ester (glycidol linoleate) and glycidol. Food Chem. Toxicol. 50, 3927-3933.
28. Jacobson-Kram, D., Sistare, F. D., and Jacobs, A. C. (2004). Use of transgenic mice in carcinogenicity hazard assessment. Toxicol. Pathol. 32 (Suppl 1), 49-52.
29. Johnson, G. E., Doak, S. H., Griffiths, S. M., Quick, E. L., Skibinski, D. O., Zair, Z. M., and Jenkins, G. J. (2009). Non-linear doseresponse of DNA-reactive genotoxins: Recommendations for data analysis. Mutat. Res. 678, 95-100.
30. Johnson, G. E., Slob, W., Doak, S. H., Fellows, M., G., B., Heflich, R. H., Soeteman-Hernandez, L. G., Verma, J., Willis, J., Jenkins, G., and White, P. A. (2014a). New approaches to advance the use of genetic toxicology analyses for human health risk assessment and regulatory decision-making. Toxicol. Res. 4, 667-676.
31. Johnson, G. E., Soeteman-Hernández, L. G., Gollapudi, B. B., Bodger, O. G., Dearfield, K. L., Heflich, R. H., Hixon, J. H., Lovell, D. P., MacGRegor, J. T., Pottenger, L. H., et al. (2014b). Derivation of points of departure (PoD) estimates in genetic toxicology studies and their potential application in risk assessment. Environ. Mol. Mutagen. 55, 609-623.
32. Kirkland, D., Zeiger, E., Madia, F., Gooderham, N., Kasper, P., Lynch, A., Morita, T., Ouedraogo, G., Parra Morte, J. M., Pfuhler, S., et al. (2014). Can in vitro mammalian cell genotoxicity test results be used to complement positive results in the Ames test and help predict carcinogenic or in vivo genotoxic activity? I. Reports of individual databases presented at an EURL ECVAM Workshop. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 775-776, 55-68.
33. Levy, J. A., Virolainen, M., and Defendi, V. (1968). Human lymphoblastoid lines from lymph node and spleen. Cancer. 22, 517-524.
34. Liu, L., Watanabe, K., Fang, Q., Williams, K. M., Guengerich, F. P., and Pegg, A. E. (2007). Effect of alterations of key active site residues in O6-alkylguanine-DNA Alkyltransferase on its ability to modulate the genotoxicity of 1, 2-dibromoethane. Chem. Res. Toxicol. 20, 155-163.
35. MacGregor, J. T., Frötschl, R., White, P. A., Crump, K. S., Eastmond, D. A., Fukushima, S., Guérard, M., Hayashi, M., Soeteman-Hernandez, L., Johnson, G. E., et al. (2014a). IWGT report on quantitative approaches to genotoxicity risk assessment II. Use of point-of-departure (PoD) metrics in defining acceptable exposure limits and assessing human risk. Mutat. Res. Genet. Toxicol. Environ. Mutagen 783, 66-78.
36. MacGregor, J. T., Frötschl, R., White, P. A., Crump, K. S., Eastmond, D. A., Fukushima, S., Guérard, M., Hayashi, M., Soeteman-Hernández, L. G., Kasamatsu, T., et al. (2014b). IWGT report on quantitative approaches to genotoxicity risk assessment I. Methods and metrics for defining exposure-response relationships and points of departure (PoDs). Mutat. Res. Genet. Toxicol. Environ. Mutagen. 783, 55-65.
37. McGregor, D. B., Brown, A., Cattanach, P., Edwards, I., McBride, D., Riach, C., and Caspary, W. J. (1988). Responses of the L5178Y tk+/tk-mouse lymphoma cell forward mutation assay: III. 72 coded chemicals. Environ. Mol. Mutagen. 12, 85-154.
38. Meli, C., and Seeberg, A. H. (1990). Activity of 1, 2-dimethylhydrazine in the mouse bone marrow micronucleus assay using a triple-and a single-dosing protocol. Mutat. Res. 234, 155-159.
39. Mohamed, D., Mowaka, S., Thomale, J., and Linscheid, M. W. (2009). Chlorambucil-adducts in DNA analyzed at the oligonucleotide level using HPLC-ESI MS. Chem. Res. Toxicol. 22, 1435-1446.
40. Molloy, J., Doherty, A. T., Chocian, K., Hayes, J., and O'Donovan, M. (2010). Karyotypic analysis and stability with time in culture of TK6 and L5178Y cell lines. Mutagenesis 25, 645.
41. Morita, T., Asano, N., Awogi, T., Sasaki, Y. F., Sato, S., Shimada, H., Sutou, S., Suzuki, T., Wakata, A., Sofuni, T., et al. (1997). Evaluation of the rodent micronucleus assay in the screening of IARC carcinogens (groups 1, 2A and 2B) the summary report of the 6th collaborative study by CSGMT/JEMS MMS. Collaborative Study of the Micronucleus Group Test. Mammalian Mutagenicity Study Group. Mutat. Res. 389, 3-122.
42. Newell, L. E., and Heddle, J. A. (2004). The potent colon carcinogen, 1, 2-dimethylhydrazine induces mutations primarily in the colon. Mutat. Res. 564, 1-7.
43. NRC. (2007). National Research Council (NRC) of The Academies. Toxicity Testing in the 21st Century: A Vision and a Strategy. The National Academies Press. The National Academy of Sciences. Washington, D.C.
44. NTP. (1988). NTP Toxicology and Carcinogenesis Studies of 4-Hexylresorcinol (CAS No. 136-77-6) in F344/N Rats and B6C3F1 Mice (Gavage Studies). Natl. Toxicol. Program Tech. Rep. Ser. 330, 1-166.
45. NTP. (1989). NTP Toxicology and Carcinogenesis Studies of para-Chloroaniline Hydrochloride (CAS No. 20265-96-7) in F344/N Rats and B6C3F1 Mice (Gavage Studies). Natl. Toxicol. Program Tech. Rep. Ser. 351, 1-256.
46. NTP. (1996). NTP Toxicology and Carcinogenesis Studies of Phenolphthalein (CAS No. 77-09-8) in F344/N Rats and B6C3F1 Mice (Feed Studies). Natl. Toxicol. Program Tech. Rep. Ser. 465, 1-354.
47. NTP. (2001). Toxicology and carcinogenesis studies of p, p'-dichlorophenyl sulfone (CAS No. 80-07-9) in F344/N rats and B6C3F1 mice (feed studies). Natl. Toxicol. Program Tech. Rep. Ser. 7-262.
48. NTP. (2004). NTP technical report on the toxicology and carcinogenesis studies of propylene glycol mono-t-butyl ether (CAS No. 57018-52-7) in F344/N rats and B6C3F1 mice and a toxicology study of propylene glycol mono-t-butyl ether in male NBR rats (inhalation studies). Natl. Toxicol. Program Tech. Rep. Ser. 1-306.
49. NTP. (2005). NTP toxicology and carcinogenesis studies of decalin (CAS No. 91-17-8) in F344/N rats and B6C3F(1) mice and a toxicology study of decalin in male NBR rats (inhalation studies). Natl. Toxicol. Program Tech. Rep. Ser. 1-316.
50. OECD. (2008). Draft OECD Guideline for the Testing of Chemicals, Test Guideline 451: Carcinogenicity Studies. Available at: http://www.oecd.org/dataoecd/30/46/41753121.pdf. Accessed January 31, 2014.
51. OECD. (2010). OECD Series on Testing and Assessment No. 129: Guidance Document on Dusing Cytotoxicity Tests to Estimate Starting Doses for Acute Oral Systemic Toxicity Tests. Available at: http://www.oecd.org/officialdocuments/publicdisplaydocumentpdf/?cote=env/jm/mono(2010)20&doclanguage=en. Accessed May 30, 2015.
52. OECD. (2014). Test No. 487: In Vitro Mammalian Cell Micronucleus Test, OECD Guidelines for the Testing of Chemicals, Section 4, OECD Publishing. Available at: http://www.oecd-ilibrary.org/docserver/download/9714561e.pdf?expires=1441917467&id=id&accname=guest&checksum=92451B952EF8DD10F3007D2EB865A2B9. Accessed May 30, 2015.
53. Piersma, A. H., Janer, G., Wolterink, G., Bessems, J. G., Hakkert, B. C., and Slob, W. (2008). Quantitative extrapolation of in vitro whole embryo culture embryotoxicity data to developmental toxicity in vivo using the benchmark dose approach. Toxicol. Sci. 101, 91-100.
54. Rosin, M. P. (1992). The use of the micronucleus test on exfoliated cells to identify anti-clastogenic action in humans: A biological marker for the efficacy of chemopreventive agents. Mutat. Res. 267, 265-276.
55. Shimada, H., Suzuki, H., Itoh, S., Hattori, C., Matsuura, Y., Tada, S., and Watanabe, C. (1992). The micronucleus test of benzo[a]pyrene with mouse and rat peripheral blood reticulocytes. Mutat. Res. 278, 165-168.
56. Slob, W. (2002). Dose-response modeling of continuous endpoints. Toxicol. Sci. 66, 298-312.
57. Slob, W., and Setzer, R. W. (2014). Shape and steepness of toxicological dose-response relationships of continuous endpoints. Crit. Rev. Toxicol. 44, 270-297.
58. Sobol, Z., Homiski, M. L., Dickinson, D. A., Spellman, R. A., Li, D., Scott, A., Cheung, J. R., Coffing, S. L., Munzner, J. B., Sanok, K. E., et al. (2012). Development and validation of an in vitro micronucleus assay platform in TK6 cells. Mutat. Res. 746, 29-34.
59. Soeteman-Hernandez, L. G., Johnson, G. E., and Slob, W. (2015). Estimating the carcinogenic potency of chemicals from the in vivo micronucleus test. Mutagenesis. gev043.
60. Spielmann, H., Genschow, E., Liebsch, M., and Halle, W. (1999). Determination of the starting dose for acute oral toxicity (LD50) testing in the up and down procedure (UDP) from cytotoxicity data. Altern. Lab. Anim. 27, 957-966.
61. Staedtler, F., Crespo-Perez, J., Sagelsdorff, P., Steiner, S., and Suter, W. (1999). 4-chloro-o-phenylenediamine induces a dose-related increase in G:C > T:A transversions and one major DNA adduct in the liver of Big Blue mice after 26 weeks in feed treatment. Mutat. Res. 430, 121-130.
62. Tabrez, S., and Ahmad, M. (2009). Toxicity, biomarkers, genotoxicity, and carcinogenicity of trichloroethylene and its metabolites: A review. J. Environ. Sci. Health Part C Environ. Carcinogen. Ecotoxicol. Rev. 27, 178-196.
63. Vrzoc, M., and Petras, M. L. (1997). Comparison of alkaline single cell gel (Comet) and peripheral blood micronucleus assays in detecting DNA damage caused by direct and indirect acting mutagens. Mutat. Res. 381, 31-40.
64. Walum, E., Hedander, J., and Garberg, P. (2005). Research perspectives for pre-screening alternatives to animal experimentation: On the relevance of cytotoxicity measurements, barrier passage determinations and high throughput screening in vitro to select potentially hazardous compounds in large sets of chemicals. Toxicol. Appl. Pharmacol. 207(2 Suppl), 393-397.
65. Wang, Y., Yang, H., Li, L., Wang, H., Xia, X., and Zhang, C. (2012). Biomarkers of chromosomal damage in peripheral blood lymphocytes induced by polycyclic aromatic hydrocarbons: A meta-analysis. Int. Arch. Occup. Environ. Health 85, 13-25.
66. Wilmer, J. W., Spencer, P. J., Ball, N., and Bus, J. S. (2014). Assessment of the genotoxicity of trichloroethylene in the in vivo micronucleus assay by inhalation exposure. Mutagenesis 29, 209-214.
67. Yoon, M., Efremenko, A., Blaauboer, B. J., and Clewell, H. J. (2014). Evaluation of simple in vitro to in vivo extrapolation approaches for environmental compounds. Toxicol. In Vitro 28, 164-170.