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Review Articles

Procedural application of mode-of-action and human relevance analysis: styrene-induced lung tumors in mice

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Pages 134-151 | Received 20 Jun 2023, Accepted 18 Jan 2024, Published online: 05 Mar 2024

References

  • Andersen ME, Cruzan G, Black MB, Pendse SN, Dodd D, Bus JS, Sarang SS, Banton MI, Waites R, McMullen PD. 2017. Assessing molecular initiating events (MIEs), key events (KEs) and modulating factors (MFs) for styrene responses in mouse lungs using whole genome gene expression profiling following 1-day and multi-week exposures. Toxicol Appl Pharmacol. 335:28–40. doi: 10.1016/j.taap.2017.09.015.
  • Andersen ME, Cruzan G, Black MB, Pendse SN, Dodd DE, Bus JS, Sarang SS, Banton MI, Waites R, Layko DB, et al. 2018. Strain-related differences in mouse lung gene expression over a two-year period of inhalation exposure to styrene: relevance to human risk assessment. Regul Toxicol Pharmacol. 96:153–166. doi: 10.1016/j.yrtph.2018.05.011.
  • Beliles RP, Butala JH, Stack CR, Makris S. 1985. Chronic toxicity and three-generation reproduction study of styrene monomer in the drinking water of rats. Fundam Appl Toxicol. 5(5):855–868. doi: 10.1016/0272-0590(85)90168-x.
  • Bertke SJ, Keil AP, Daniels RD. 2021. Lung cancer mortality and styrene exposure in the reinforced-plastics boatbuilding industry: evaluation of healthy worker survivor bias. Am J Epidemiol. 190(9):1784–1792. doi: 10.1093/aje/kwab108.
  • Bertke SJ, Yiin JH, Daniels RD. 2018. Cancer mortality update with an exposure response analysis among styrene-exposed workers in the reinforced plastics boatbuilding industry. Am J Ind Med. 61(7):566–571. doi: 10.1002/ajim.22853.
  • Boobis AR, Cohen SM, Dellarco V, McGregor D, Meek ME, Vickers C, Willcocks D, Farland W. 2006. IPCS framework for analyzing the relevance of a cancer mode of action for humans. Crit Rev Toxicol. 36(10):781–792. doi: 10.1080/10408440600977677.
  • Boogaard PJ, de Kloe KP, Wong BA, Sumner SC, Watson WP, van Sittert NJ. 2000. Quantification of DNA adducts formed in liver, lungs, and isolated lung cells of rats and mice exposed to (14)C-styrene by nose-only inhalation. Toxicol Sci. 57(2):203–216. doi: 10.1093/toxsci/57.2.203.
  • Born SL, Fix AS, Caudill D, Lehman-McKeeman LD. 1998. Selective Clara cell injury in mouse lung following acute administration of coumarin. Toxicol Appl Pharmacol. 151(1):45–56. doi: 10.1006/taap.1998.8442.
  • Carlson GP. 1997. Effects of inducers and inhibitors on the microsomal metabolism of styrene to styrene oxide in mice. J Toxicol Environ Health. 51(5):477–488. doi: 10.1080/00984109708984038.
  • Carlson GP. 2002. Effect of the inhibition of the metabolism of 4-vinylphenol on its hepatotoxicity and pneumotoxicity in rats and mice. Toxicology. 179(1-2):129–136. doi: 10.1016/S0300-483X(02)00340-2.
  • Carlson GP. 2008. Critical appraisal of the expression of cytochrome P450 enzymes in human lung and evaluation of the possibility that such expression provides evidence of potential styrene tumorigenicity in humans. Toxicology. 254(1–2):1–10. doi: 10.1016/j.tox.2008.09.017.
  • Chan PC, Hasemani JK, Mahleri J, Aranyi C. 1998. Tumor induction in F344/N rats and B6C3F1 mice following inhalation exposure to ethylbenzene. Toxicol Lett. 99(1):23–32. doi: 10.1016/S0378-4274(98)00133-7.
  • Cohen SM, Zhongyu Y, Bus JS. 2020. Relevance of mouse lung tumors to human risk assessment. J Toxicol Environ Health B Crit Rev. 23(5):214–241. doi: 10.1080/10937404.2020.1763879.
  • Cruzan G, Bus JS, Andersen ME, Carlson GP, Banton MI, Sarang SS, Waites R. 2018. Based on an analysis of mode of action, styrene-induced mouse lung tumors are not a human cancer concern. Regul Toxicol Pharmacol. 95(January):17–28. doi: 10.1016/j.yrtph.2018.02.010.
  • Cruzan G, Bus JS, Banton MI, Sarang SS, Waites R, Layko DB, Raymond J, Dodd D, Andersen ME. 2017. Complete attenuation of mouse lung cell proliferation and tumorigenicity in CYP2F2 knockout and CYP2F1 humanized mice exposed to inhaled styrene for up to 2 years supports a lack of human relevance. Toxicol Sci. 159(2):413–421. doi: 10.1093/toxsci/kfx141.
  • Cruzan G, Bus J, Hotchkiss J, Harkema J, Banton M, Sarang S. 2012. CYP2F2-generated metabolites, not styrene oxide, are a key event mediating the mode of action of styrene-induced mouse lung tumors. Regul Toxicol Pharmacol. 62(1):214–220. doi: 10.1016/j.yrtph.2011.10.007.
  • Cruzan G, Bus J, Hotchkiss J, Sura R, Moore C, Yost G, Banton M, Sarang S. 2013. Studies of styrene, styrene oxide and 4-hydroxystyrene toxicity in CYP2F2 knockout and CYP2F1 humanized mice support lack of human relevance for mouse lung tumors. Regul Toxicol Pharmacol. 66(1):24–29. doi: 10.1016/j.yrtph.2013.02.008.
  • Cruzan G, Carlson GP, Johnson KA, Andrews LS, Banton MI, Bevan C, Cushman JR. 2002. Styrene respiratory tract toxicity and mouse lung tumors are mediated by CYP2F-generated metabolites. Regul Toxicol Pharmacol. 35(3):308–319. doi: 10.1006/rtph.2002.1545.
  • Cruzan G, Cushman JR, Andrews LS, Granville GC, Johnson KA, Bevan C, Hardy CJ, Coombs DW, Mullins PA, Brown WR. 2001. Chronic toxicity/oncogenicity study of styrene in CD-1 mice by inhalation exposure for 104 weeks. J Appl Toxicol. 21(3):185–198. doi: 10.1002/jat.737.
  • Cruzan G, Cushman JR, Andrews LS, Granville GC, Johnson KA, Hardy CJ, Coombs DW, Mullins PA, Brown WR. 1998. Chronic toxicity/oncogenicity study of styrene in cd rats by inhalation exposure for 104 weeks. Toxicol Sci. 46(2):266–281. doi: 10.1093/toxsci/46.2.266.
  • Cruzan G, Cushman JR, Andrews LS, Granville GC, Miller RR, Hardy CJ, Coombs DW, Mullins PA. 1997. Subchronic inhalation studies of styrene in CD rats and CD-1 mice. Fundam Appl Toxicol. 35(2):152–165. doi: 10.1006/faat.1996.2273.
  • Csanády GA, Kessler W, Hoffmann HD, Filser JG. 2003. A toxicokinetic model for styrene and its metabolite styrene-7,8-oxide in mouse, rat and human with special emphasis on the lung. Toxicol Lett. 138(1-2):75–102. doi: 10.1016/S0378-4274(02)00409-5.
  • Daniels RD, Bertke SJ. 2020. Exposure-response assessment of cancer mortality in styrene-exposed boatbuilders. Occup Environ Med. 77(10):706–712. doi: 10.1136/oemed-2020-106445.
  • Dixon D, Herbert RA, Kissling GE, Brix AE, Miller RA, Maronpot RR. 2008. Summary of Chemically Induced Pulmonary Lesions in the National Toxicology Program (NTP) Toxicology and Carcinogenesis Studies. Toxicol Pathol. 36(3):428–439. doi: 10.1177/0192623308315360.
  • Gamer AO, Leibold E, Deckardt K, Kittel B, Kaufmann W, Tennekes HA, Van Ravenzwaay B. 2004. The effects of styrene on lung cells in female mice and rats. Food Chem Toxicol. 42(10):1655–1667. doi: 10.1016/j.fct.2004.06.002.
  • Green T, Lee R, Toghill A, Meadowcroft S, Lund V, Foster J. 2001. The toxicity of styrene to the nasal epithelium of mice and rats: studies on the mode of action and relevance to humans. Chem Biol Interact. 137(2):185–202. doi: 10.1016/S0009-2797(01)00236-8.
  • Green T, Toghill A, Foster JR. 2001. The role of cytochromes P-450 in styrene induced pulmonary toxicity and carcinogenicity. Toxicology. 169(2):107–117. doi: 10.1016/S0300-483X(01)00488-7.
  • Greenberg AK, Yee H, Rom WN. 2002. Preneoplastic lesions of the lung. Respir Res. 3(1):20. doi: 10.1186/rr170.
  • Hahn FF, Gigliotti A, Hutt JA. 2007. Comparative oncology of lung tumors. Toxicol Pathol. 35(1):130–135. doi: 10.1080/01926230601132063.
  • Hill T, Conolly RB. 2019. Development of a novel AOP for Cyp2F2-mediated lung cancer in mice. Toxicol Sci. 172(1):1–10. doi: 10.1093/toxsci/kfz185.
  • Johanson G, Ernstgard L, Gullstrand E, Lof A, Johanson G, Ernstgard L, Osterman-Golkar S, Williams CC, Sumner SCJ. 2000. Styrene oxide in blood, hemoglobin adducts, and urinary metabolites in human volunteers exposed to 13C8-styrene vapors. Toxicol Appl Pharmacol. 168(1):36–49. doi: 10.1006/taap.2000.9007.
  • Kogevinas M, Gwinn WM, Kriebel D, Phillips DH, Sim M, Bertke SJ, Calaf GM, Colosio C, Fritz JM, Fukushima S, et al. 2018. Carcinogenicity of quinoline, styrene, and styrene-7,8-oxide. Lancet Oncol. 19(6):728–729. doi: 10.1016/S1470-2045(18)30316-4.
  • Manenti G, Dragani TA. 2005. Pas1 haplotype-dependent genetic predisposition to lung tumorigenesis in rodents: a meta-analysis. Carcinogenesis. 26(5):875–882. doi: 10.1093/carcin/bgh299.
  • Meek ME, Boobis A, Cote I, Dellarco V, Fotakis G, Munn S, Seed J, Vickers C. 2014. New developments in the evolution and application of the WHO/IPCS framework on mode of action/species concordance analysis. J Appl Toxicol. 34(1):1–18. doi: 10.1002/jat.2949.
  • Meek ME, Bucher JR, Cohen SM, Dellarco V, Hill RN, Lehman-McKeeman LD, Longfellow DG, Pastoor T, Seed J, Patton DE. 2003. A framework for human relevance analysis of information on carcinogenic modes of action. Crit Rev Toxicol. 33(6):591–653. doi: 10.1080/713608373.
  • Meek ME, Palermo CM, Bachman AN, North CM, Lewis RJ. 2014. Mode of action human relevance (species concordance) framework: evolution of the Bradford Hill considerations and comparative analysis of weight of evidence. J Appl Toxicol. 34(6):595–606. doi: 10.1002/jat.2984.
  • Mori M, Rao SK, Popper HH, Cagle PT, Fraire AE. 2001. Atypical adenomatous hyperplasia of the lung: a probable forerunner in the development of adenocarcinoma of the lung. Mod Pathol. 14(2):72–84. doi: 10.1038/modpathol.3880259.
  • Nakajima T, Elovaara E, Gonzalez FJ, Gelboin HV, Raunio H, Pelkonen O, Vainio H, Aoyama T. 1994. Styrene metabolism by cDNA-expressed human hepatic and pulmonary cytochromes P450. Chem Res Toxicol. 7(6):891–896. doi: 10.1021/tx00042a026.
  • [NCI] National Cancer Institute (US). 1979. Bioassay of Styrene for Possible Carcinogenicity (CAS No.100-42-5). Natl Toxicol Program Tech Rep Ser. 185:1–107. https://ntp.niehs.nih.gov/ntp/htdocs/lt_rpts/tr185.pdf.
  • Nicholson AG, Tsao MS, Beasley MB, Borczuk AC, Brambilla E, Cooper WA, Dacic S, Jain D, Kerr KM, Lantuejoul S, et al. 2022. The 2021 WHO Classification of Lung Tumors: impact of Advances Since 2015. J Thorac Oncol. 17(3):362–387. doi: 10.1016/j.jtho.2021.11.003.
  • Nikitin AY, Alcaraz A, Anver MR, Bronson RT, Cardiff RD, Dixon D, Fraire AE, Gabrielson EW, Gunning WT, Haines DC, et al. 2004. Classification of proliferative pulmonary lesions of the mouse. Cancer Res. 64(7):2307–2316. doi: 10.1158/0008-5472.CAN-03-3376.
  • [NRC] National Research Council (US). 2014. Review of the Styrene Assessment in the National Toxicology Program 12th Report on Carcinogens [Internet]. Washington, D.C.: National Academies Press. doi: 10.17226/18725.
  • [NTP] National Toxicology Program (US). 1989. NTP Toxicology and Carcinogenesis Studies of Benzofuran (CAS No. 271-89-6) in F344/N Rats and B6C3F1 Mice (Gavage Studies). [place unknown]. doi: 10.1016/0300-483X(86)90137-X.
  • [NTP] National Toxicology Program (US). 1993. NTP Toxicology and Carcinogenesis Studies of Coumarin (CAS No. 91-64-5) in F344/N Rats and B6C3F1 Mice (Gavage Studies). Natl Toxicol Program Tech Rep Ser. 422:1–340. http://www.ncbi.nlm.nih.gov/pubmed/12616289.
  • [NTP] National Toxicology Program (US). 2000. Toxicology and carcinogenesis studies of naphthalene (cas no. 91-20-3) in F344/N rats (inhalation studies). Natl Toxicol Program Tech Rep Ser. (500):1–173. http://www.ncbi.nlm.nih.gov/pubmed/11725561.
  • [NTP] National Toxicology Program (US). 2007. Toxicology and carcinogenesis studies of alpha-methylstyrene (Cas No. 98-83-9) in F344/N rats and B6C3F1 mice (inhalation studies). Natl Toxicol Program Tech Rep Ser. (543):1–210. http://www.ncbi.nlm.nih.gov/pubmed/18685715.
  • [NTP] National Toxicology Program (US). 2009. Toxicology and carcinogenesis studies of cumene (CAS No. 98-82-8) in F344/N rats and B6C3F1 mice (inhalation studies). Natl Toxicol Program Tech Rep Ser. (542):1–200. http://www.ncbi.nlm.nih.gov/pubmed/19340095.
  • Oesch F, Fabian E, Landsiedel R. 2019. Xenobiotica-metabolizing enzymes in the lung of experimental animals, man and in human lung models. In Archives of Toxicology (Vol. 93, Issue 12). Springer: Berlin Heidelberg. doi: 10.1007/s00204-019-02602-7.
  • Otteneder M, Lutz U, Lutz WK. 2002. DNA adducts of styrene-7,8-oxide in target and non-target organs for tumor induction in rat and mouse after repeated inhalation exposure to styrene. Mutat Res. 500(1-2):111–116. doi: 10.1016/S0027-5107(02)00008-8.
  • Pandiri A. 2015. Comparative pathobiology of environmentally induced lung cancers in humans and rodents. Toxicol Pathol. 43(1):107–114. doi: 10.1177/0192623314556516.
  • Pandiri AR, Sills RC, Ziglioli V, Ton TVT, Hong HHL, Lahousse SA, Gerrish KE, Auerbach SS, Shockley KR, Bushel PR, et al. 2012. Differential transcriptomic analysis of spontaneous lung tumors in B6C3F1 mice: comparison to human non-small cell lung cancer. Toxicol Pathol. 40(8):1141–1159. doi: 10.1177/0192623312447543.
  • Phimister AJ, Lee MG, Morin D, Buckpitt AR, Plopper CG. 2004. Glutathione depletion is a major determinant of inhaled naphthalene respiratory toxicity and naphthalene metabolism in mice. Toxicol Sci. 82(1):268–278. doi: 10.1093/toxsci/kfh258.
  • Plopper CG, Hyde DM. 2015. Epithelial cells of the bronchiole. In: Comparative biology of the normal lung. 2nd ed. Waltham (MA): Academic Press; 83–92. doi: 10.1016/B978-0-12-404577-4.00007-2.
  • Ponomarkov V, Tomatis L. 1978. Effects of long-term oral administration of styrene to mice and rats. Scand J Work Environ Health. 4(2):127–135. doi: 10.5271/sjweh.2754.
  • Raz DJ, He B, Rosell R, Jablons DM. 2006. Bronchioloalveolar carcinoma: a review. Clin Lung Cancer. 7(5):313–322. doi: 10.3816/CLC.2006.n.012.
  • Renne R, Brix A, Harkema J, Herbert R, Kittel B, Lewis D, March T, Nagano K, Pino M, Rittinghausen S, et al. 2009. Proliferative and nonproliferative lesions of the rat and mouse respiratory tract. Toxicol Pathol. 37(7 Suppl):5S–73S. doi: 10.1177/0192623309353423.
  • Sarangapani R, Teeguarden JG, Cruzan G, Clewell HJ, Andersen ME. 2002. Physiologically based pharmacokinetic modeling of styrene and styrene oxide respiratory-tract dosimetry in rodents and humans. Inhal Toxicol. 14(8):789–834. doi: 10.1080/08958370290084647.
  • Shultz MA, Choudary PV, Buckpitt AR. 1999. Role of murine cytochrome P-450 2F2 in metabolic activation of naphthalene and metabolism of other xenobiotics. J Pharmacol Exp Ther. 290(1):281–288.
  • Stott WT, Johnson KA, Bahnemann R, Day SJ, McGuirk RJ. 2003. Evaluation of potential modes of action of inhaled ethylbenzene in rats and mice. Toxicol Sci. 71(1):53–66. doi: 10.1093/toxsci/71.1.53.
  • Tikk K, Sookthai D, Fortner RT, Johnson T, Rinaldi S, Romieu I, Tjønneland A, Olsen A, Overvad K, Clavel-Chapelon F, et al. 2015. Circulating prolactin and in situ breast cancer risk in the European EPIC cohort: a case-control study. Breast Cancer Res. 17(1):49. doi: 10.1186/s13058-015-0563-6.
  • Travis WD, Brambilla E, Noguchi M, Nicholson AG, Geisinger KR, Yatabe Y, Beer DG, Powell CA, Riely GJ, Van Schil PE, et al. 2011. International association for the study of lung cancer/American Thoracic Society/European Respiratory Society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol. 6(2):244–285. doi: 10.1097/JTO.0b013e318206a221.
  • Vodicka P, Koskinen M, Vodicková L, Stetina R, Smerák P, Bárta I, Hemminki K. 2001. DNA adducts, strand breaks and micronuclei in mice exposed to styrene by inhalation. Chem Biol Interact. 137(3):213–227. doi: 10.1016/S0009-2797(01)00253-8.
  • Vodicka P, Koskinen M, Naccarati A, Oesch-Bartlomowicz B, Vodickova L, Hemminki K, Oesch F. 2006. Styrene metabolism, genotoxicity, and potential carcinogenicity. Drug Metab Rev. 38(4):805–853. doi: 10.1080/03602530600952222.
  • West JAA, Pakehham G, Morin D, Fleschner CA, Buckpitt AR, Plopper CG. 2001. Inhaled naphthalene causes dose dependent Clara cell cytotoxicity in mice but not in rats. Toxicol Appl Pharmacol. 173(2):114–119. doi: 10.1006/taap.2001.9151.
  • Xu L, Tavora F, Burke A. 2012. ‘Bronchioloalveolar carcinoma’: is the term really dead? A critical review of a new classification system for pulmonary adenocarcinomas. Pathology. 44(6):497–505. doi: 10.1097/PAT.0b013e3283579fda.