Genotoxicity of intermittent co-exposure to benzene and toluene in male CD-1 mice

Chemico-Biological Interactions

Volumn 173, Issue 3, 2008, Pages 166-178

  Wetmore, Barbara A ^a   Struve, Melanie F ^b   Gao, Pu ^a   Sharma, Sheela ^a   Allison, Neil ^c   Roberts, Kay C ^a   Letinski, Daniel J ^d   Nicolich, Mark J ^d   Bird, Michael G ^d   Dorman, David C ^b  

^a HAMNER INSTITUTES FOR HEALTH SCIENCES   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c EXPERIMENTAL PATHOLOGY LABORATORIES INC   (United States)

^d EXXONMOBIL UPSTREAM RESEARCH COMPANY   (United States)

Author keywords

Benzene; Co exposure; Genotoxicity; Inhalation; Toluene

Indexed keywords

ACETYLCYSTEINE DERIVATIVE; BENZENE; GLUTATHIONE; HYDROQUINONE; MUCONIC ACID; TOLUENE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOLOGICAL MODEL; BONE MARROW DISEASE; CHEMICAL INTERACTION; CONCENTRATION (PARAMETERS); ENZYME ACTIVITY; ERYTHROCYTE; EXPOSURE; GENOTOXICITY; MALE; METABOLISM; MOUSE; NONHUMAN; QUANTITATIVE ANALYSIS;

ANIMALS; ATMOSPHERE EXPOSURE CHAMBERS; BENZENE; BENZENE DERIVATIVES; BODY WEIGHT; BONE MARROW CELLS; DNA; DRUG ADMINISTRATION SCHEDULE; GLUTATHIONE; INHALATION EXPOSURE; LIVER; MALE; MICE; MICRONUCLEI, CHROMOSOME-DEFECTIVE; MOLECULAR STRUCTURE; MUTAGENICITY TESTS; TIME FACTORS; TOLUENE;

ANIMALIA; MUS;

EID: 44649124119     PISSN: 00092797     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbi.2008.03.012     Document Type: Article

References (90)

1. American Conference of Governmental Industrial Hygienists (ACGIH). 1999 TLVs and BEIs. Threshold Limit Values for Chemical Substances and Physical Agents (1999), Biological Exposure Indices, Cincinnati, OH
2. NCI (National Cancer Institute), Cancer Trends Progress Report. Prevention: Environmental. Benzene in the Air. National Cancer Institute, 2003.
3. Wallace L.A. Major sources of benzene exposure. Environ. Health Perspect. 82 (1989) 165-169
4. Descatha A., Jenabian A., Conso F., and Ameille J. Occupational exposures and haematological malignancies: overview on human recent data. Cancer Causes Control 16 (2005) 939-953
5. Maltoni C., Ciliberti A., Cotti G., Conti B., and Belpoggi F. Benzene, an experimental multipotential carcinogen: results of the long-term bioassays performed at the Bologna Institute of Oncology. Environ. Health Perspect. 82 (1989) 109-124
6. Cronkite E.P., Bullis J., Inoue T., and Drew R.T. Benzene inhalation produces leukemia in mice. Toxicol. Appl. Pharmacol. 75 (1984) 358-361
7. Cronkite E.P., Drew R.T., Inoue T., and Bullis J.E. Benzene hematotoxicity and leukemogenesis. Am. J. Ind. Med. 7 (1985) 447-456
8. Cronkite E.P., Drew R.T., Inoue T., Hirabayashi Y., and Bullis J.E. Hematotoxicity and carcinogenicity of inhaled benzene. Environ. Health Perspect. 82 (1989) 97-108
9. Snyder C.A., Goldstein B.D., Sellakumar A.R., Bromberg I., Laskin S., and Albert R.E. The inhalation toxicology of benzene: incidence of hematopoietic neoplasms and hematotoxicity in ARK/J and C57BL/6J mice. Toxicol. Appl. Pharmacol. 54 (1980) 323-331
10. Snyder C.A., Goldstein B.D., Sellakumar A.R., and Albert R.E. Evidence for hematotoxicity and tumorigenesis in rats exposed to 100 ppm benzene. Am. J. Ind. Med. 5 (1984) 429-434
11. Snyder C.A., Sellakumar A.R., James D.J., and Albert R.E. The carcinogenicity of discontinuous inhaled benzene exposures in CD-1 and C57Bl/6 mice. Arch. Toxicol. 62 (1988) 331-335
12. Farris G.M., Everitt J.I., Irons R.D., and Popp J.A. Carcinogenicity of inhaled benzene in CBA mice. Fundam. Appl. Toxicol. 20 (1993) 503-507
13. Tsutsui T., Hayashi N., Maizumi H., Huff J., and Barrett J.C. Benzene-, catechol-, hydroquinone- and phenol-induced cell transformation, gene mutations, chromosome aberrations, aneuploidy, sister chromatid exchanges and unscheduled DNA synthesis in Syrian hamster embryo cells. Mutat. Res. 373 (1997) 113-123
14. Whysner J., Reddy M.V., Ross P.M., Mohan M., and Lax E.A. Genotoxicity of benzene and its metabolites. Mutat. Res. 566 (2004) 99-130
15. Healy L.N., Pluta L.J., James R.A., Janszen D.B., Torous D., French J.E., and Recio L. Induction and time-dependent accumulation of micronuclei in peripheral blood of transgenic p53+/- mice, Tg.AC (v-Ha-ras) and parental wild-type (C57BL/6 and FVB/N) mice exposed to benzene by inhalation. Mutagenesis 16 (2001) 163-168
16. Yoon B.I., Hirabayashi Y., Kawasaki Y., Kodama Y., Kaneko T., Kim D.Y., and Inoue T. Mechanisms of action of benzene toxicity: cell cycle suppression in hemopoietic progenitor cells (CFU-GM). Exp. Hematol. 29 (2001) 279-285
17. Eastmond D.A., Smith M.T., and Irons R.D. An interaction of benzene metabolites reproduces the myelotoxicity observed with benzene exposure. Toxicol. Appl. Pharmacol. 91 (1987) 85-95
18. Snyder R., Dimitriadis E., Guy R., Hu P., Cooper K., Bauer H., Witz G., and Goldstein B.D. Studies on the mechanism of benzene toxicity. Environ. Health Perspect. 82 (1989) 31-35
19. Barale R., Marrazzini A., Betti C., Vangelisti V., Loprieno N., and Barrai I. Genotoxicity of two metabolites of benzene: phenol and hydroquinone show strong synergistic effects in vivo. Mutat. Res. 244 (1990) 15-20
20. Medinsky M.A., Kenyon E.M., and Schlosser P.M. Benzene: a case study in parent chemical and metabolite interactions. Toxicology 105 (1995) 225-233
21. Smith M.T., Yager J.W., Steinmetz K.L., and Eastmond D.A. Peroxidase-dependent metabolism of benzene's phenolic metabolites and its potential role in benzene toxicity and carcinogenicity. Environ. Health Perspect. 82 (1989) 23-29
22. Smith M.T. The mechanism of benzene-induced leukemia: a hypothesis and speculations on the causes of leukemia. Environ. Health Perspect. 104 Suppl. 6 (1996) 1219-1225
23. Ross D. The role of metabolism and specific metabolites in benzene-induced toxicity: evidence and issues. J. Toxicol. Environ. Health A 61 (2000) 357-372
24. Medinsky M.A., Sabourin P.J., Lucier G., Birnbaum L.S., and Henderson R.F. A physiological model for simulation of benzene metabolism by rats and mice. Toxicol. Appl. Pharmacol. 99 (1989) 193-206
25. Medinsky M.A., Sabourin P.J., Henderson R.F., Lucier G., and Birnbaum L.S. Differences in the pathways for metabolism of benzene in rats and mice simulated by a physiological model. Environ. Health Perspect. 82 (1989) 43-49
26. Medinsky M.A., Sabourin P.J., Lucier G., Birnbaum L.S., and Henderson R.F. A toxicokinetic model for simulation of benzene metabolism. Exp. Pathol. 37 (1989) 150-154
27. Hedli C.C., Hoffmann M.J., Ji S., Thomas P.E., and Snyder R. Benzene metabolism in the isolated perfused mouse liver. Toxicol. Appl. Pharmacol. 146 (1997) 60-68
28. Hoffmann M.J., Ji S., Hedli C.C., and Snyder R. Metabolism of [14C]phenol in the isolated perfused mouse liver. Toxicol. Sci. 49 (1999) 40-47
29. Lan Q., Zhang L., Li G., Vermeulen R., Weinberg R.S., Dosemeci M., Rappaport S.M., Shen M., Alter B.P., Wu Y., Kopp W., Waidyanatha S., Rabkin C., Guo W., Chanock S., Hayes R.B., Linet M., Kim S., Yin S., Rothman N., and Smith M.T. Hematotoxicity in workers exposed to low levels of benzene. Science 306 (2004) 1774-1776
30. Recio L., Bauer A., and Faiola B. Use of genetically modified mouse models to assess pathways of benzene-induced bone marrow cytotoxicity and genotoxicity. Chem. Biol. Interact. 153/154 (2005) 159-164
31. Valentine J.L., Lee S.S., Seaton M.J., Asgharian B., Farris G., Corton J.C., Gonzalez F.J., and Medinsky M.A. Reduction of benzene metabolism and toxicity in mice that lack CYP2E1 expression. Toxicol. Appl. Pharmacol. 141 (1996) 205-213
32. Bauer A.K., Faiola B., Abernethy D.J., Marchan R., Pluta L.J., Wong V.A., Gonzalez F.J., Butterworth B.E., Borghoff S.J., Everitt J.I., and Recio L. Male mice deficient in microsomal epoxide hydrolase are not susceptible to benzene-induced toxicity. Toxicol. Sci. 72 (2003) 201-209
33. Kondrová E., Stopka P., and Soucek P. Cytochrome P450 destruction by benzene metabolites 1,4-benzoquinone and 1,4-hydroquinone and the formation of hydroxyl radicals in minipig liver microsomes. Toxicol. In Vitro 21 (2007) 566-575
34. Rana S.V., and Verma Y. Biochemical toxicity of benzene. J. Environ. Biol. 26 (2005) 157-168
35. Souček P., Ivan G., and Pavel S. Effect of the microsomal system on interconversions between hydroquinone, benzoquinone, oxygen activation, and lipid peroxidation. Chem. Biol. Interact. 126 (2000) 45-61
36. Inayat-Hussain S.H., and Ross D. Intrinsic pathway of hydroquinone induced apoptosis occurs via both caspase-dependent and caspase-independent mechanisms. Chem. Res. Toxicol. 18 (2005) 420-427
37. Martinez-Velazquez M., Maldonado V., Ortega A., Melendez-Zajgla J., and Albores A. Benzene metabolites induce apoptosis in lymphocytes. Exp. Toxicol. Pathol. 58 (2006) 65-70
38. Vaughan A.T., Betti C.J., Villalobos M.J., Premkumar K., Cline E., Jiang Q., and Diaz M.O. Surviving apoptosis: a possible mechanism of benzene-induced leukemia. Chem. Biol. Interact. 153/154 (2005) 179-185
39. Henderson R.F., Sabourin P.J., Bechtold W.E., Griffith W.C., Medinaky M.A., Birnbaum L.S., and Lucier G.W. The effect of dose, rate, route of administration, and species on tissue and blood levels of benzene metabolites. Environ. Health Perspect. 82 (1989) 9-17
40. Medinsky M.A., Kenyon E.M., Seaton M.J., and Schlosser P.M. Mechanistic considerations in benzene physiological model development. Environ. Health Perspect. 104 Suppl. 6 (1996) 1399-1404
41. Souček P. Cytochrome P450 destruction by quinones: comparison of effects in rat and human liver microsomes. Chem. Biol. Interact. 121 (1999) 223-236
42. Sato A., and Nakajima T. Dose-dependent metabolic interaction between benzene and toluene in vivo and in vitro. Toxicol. Appl. Pharmacol. 48 (1979) 249-256
43. Andrews L.S., Lee E.W., Witmer C.M., Kocsis J.J., and Snyder R. Effects of toluene on the metabolism, disposition and hemopoietic toxicity of [3H]benzene. Biochem. Pharmacol. 26 (1977) 293-300
44. Gad-El-Karim M.M., Harper B.L., and Legator M.S. Modifications in the myeloclastogenic effect of benzene in mice with toluene, phenobarbital, 3-methylcholanthrene, Aroclor 1254, SKF- 525A. Mutat. Res. 135 (1984) 225-243
45. Plappert U., Barthel E., and Seidel H.J. Reduction of benzene toxicity by toluene. Environ. Mol. Mutagen. 24 (1994) 283-292
46. Toft L., Olofsson T., and Tunek T. Toxic effects on mouse bone marrow caused by inhalation of benzene. Arch. Toxicol. 51 (1982) 295-302
47. Luke C.A., Tice R.R., and Drew R.T. The effect of exposure regimen and duration on benzene-induced bone marrow damage in mice. II. Strain comparisons involving B6C3F1, C57Bl/6 and DBA/2 male mice. Mutat. Res. 203 (1988) 273-295
48. Cox L.A. Biological basis of chemical carcinogenesis: insights from benzene. Risk Anal. 11 (1991) 453-464
49. Waidyanatha S., Rothman N., Li G., Smith M.T., Yin S., and Rappaport S.M. Rapid determination of six urinary benzene metabolites in occupationally exposed and unexposed subjects. Anal. Biochem. 327 (2004) 184-199
50. Balansky R.M., and Blagoeva P.M. Tobacco smoke-induced clastogenicity in mouse fetuses and in newborn mice. Mutat. Res. 223 (1989) 1-6
51. Brusick D. Genetic toxicology. In: Hayes A.W. (Ed). Principles and Methods in Toxicology. third edition (1994), Raven Press Ltd., New York 545-577
52. OECD, Test Guidance 474, Mammalian Erythrocyte Micronucleus Test, in: OECD Guidance for Testing of Chemicals, Organization for Economic Cooperation & Development, Paris, 1997.
53. Wetmore B.A., Mitchell A.D., Meyer S.A., and Genter M.B. Evidence for site-specific bioactivation of alachlor in the olfactory mucosa of the Long-Evans rat. Toxicol. Sci. 49 (1999) 202-212
54. Koop D.R. Hydroxylation of p-nitrophenol by rabbit ethanol-inducible cytochrome P-450 isozyme 3a. Mol. Pharmacol. 29 (1986) 399-404
55. Reinke L.A., and Moyer M.J. p-Nitrophenol hydroxylation. A microsomal oxidation which is highly inducible by ethanol. Drug Metab. Dispos. 13 (1985) 548-552
56. Tierney D.J., Haas A.L., and Koop D.R. Degradation of cytochrome P450 2E1: selective loss after labilization of the enzyme. Arch. Biochem. Biophys. 293 (1992) 9-16
57. Bornheim L.M., and Correia M.A. Selective inactivation of mouse liver cytochrome P-450IIIA by cannabidiol. Mol. Pharmacol. 38 (1990) 319-326
58. Lee C., Hutson J.R., Tzau V.K., and Riddick D.S. Regulation of constitutive mouse hepatic cytochromes P450 and growth hormone signaling components by 3-methylcholanthrene. Drug Metab. Dispos. 34 (2006) 1530-1538
59. Usmani K.A., Rose R.L., and Hodgson E. Inhibition and activation of the human liver microsomal and human cytochrome P450 3A4 metabolism of testosterone by deployment-related chemicals. Drug Metab. Dispos. 31 (2003) 384-391
60. Doderer K., and Schmid R.D. Fluorometric assay for determining epoxide hydrolase activity. Biotechnol. Lett. 26 (2004) 835-839
61. Habig W.H., Pabst M.J., and Jakoby W.B. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249 (1974) 7130-7139
62. Sharma S., Nemecz S.K., Zhu S., and Steele V.E. Identification of chemopreventive agents by screening for induction of glutathione S-transferase as a biomarker. Methods Cell Sci. 19 (1991) 49-52
63. Prochaska H.J., and Santamaria A.B. Direct measurement of NAD(P)H:quinone reductase from cells cultured in microtiter wells: a screening assay for anticarcinogenic enzyme inducers. Anal. Biochem. 169 (1988) 328-336
64. Sharma S., Pennington L.P., and Steele V.E. Induction of NADPH-quinone reductase as a screening assay for potential chemopreventive agents. Methods Cell Sci. 19 (1997) 63-66
65. Griffith O.W. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 106 (1980) 207-212
66. Schmid W. The micronucleus test. Mutat. Res. 31 (1975) 9-15
67. Farris G.M., Wong V.A., Wong B.A., Janszen D.B., and Shah R.S. Benzene-induced micronuclei in erythrocytes: an inhalation concentration-response study in B6C3F1 mice. Mutagenesis 11 (1996) 455-462
68. Luke C.A., Tice R.R., and Drew R.T. The effect of exposure regimen and duration on benzene-induced bone-marrow damage in mice. I. Sex comparison in DBA/2 mice. Mutat. Res. 203 (1988) 251-271
69. Faiola B., Bauer A.K., Fuller E.S., Wong V.A., Pluta L.J., Abernethy D.J., Mangum J.B., Everitt J.I., and Recio L. Variations in Prkdc and susceptibility to benzene-induced toxicity in mice. Toxicol. Sci. 75 (2003) 321-332
70. Bauer A.K., Faiola B., Abernethy D.J., Marchan R., Pluta L.J., Wong V.A., Roberts K., Jaiswal A.K., Gonzalez F.J., Butterworth B.E., Borghoff S., Parkinson H., Everitt J., and Recio L. Genetic susceptibility to benzene-induced toxicity: role of NADPH: quinone oxidoreductase-1. Cancer Res. 63 (2003) 929-935
71. Tice R.R., Luke C.A., and Drew R.T. Effect of exposure route, regimen, and duration on benzene-induced genotoxic and cytotoxic bone marrow damage in mice. Environ. Health Perspect. 82 (1989) 65-74
72. Mortazavi S.B., Safari A., Khavanin A., Kazemnejad A., Mozazzeni A.M., and Rezaee A. Induction of micronuclei in mice lymphocytes exposed to microwave and toluene. Am. J. Appl. Sci. 2 (2005) 1321-1324
73. Mohtashamipur E., Strater H., Triebel R., and Norpoth K. Effects of pretreatment of male NMRI mice with enzyme inducers or inhibitors on clastogenicity of toluene. Arch. Toxicol. 60 (1987) 460-463
74. McGregor D. The genetic toxicology of toluene. Mutat. Res. 317 (1994) 213-228
75. Sabourin P.J., Bechtold W.E., Griffith W.C., Birnbaum L.S., Lucier G., and Henderson R.F. Effect of exposure concentration, exposure rate, and route of administration on metabolism of benzene by F344 rats and B6C3F1 mice. Toxicol. Appl. Pharmacol. 99 (1989) 421-444
76. Brondeau M.T., Ducos P., Gaudin R., Morel G., Bonnet P., and de Ceaurriz J. Evaluation of the interaction of benzene and toluene on the urinary excretion of t,t-muconic acid in rats. Toxicol. Lett. 61 (1992) 311-316
77. Farris G.M., Robinson S.N., Gaido K.W., Wong B.A., Wong V.A., Hahn W.P., and Shah R.S. Benzene-induced hematotoxicity and bone marrow compensation in B6C3F1 mice. Fundam. Appl. Toxicol. 36 (1997) 119-129
78. Torous D.K., Hall N.E., Murante F.G., Gleason S.E., Tometsko C.R., and Dertinger S.D. Comparative scoring of micronucleated reticulocytes in rat peripheral blood by flow cytometry and microscopy. Toxicol. Sci. 74 (2003) 309-314
79. Weisel C., Yu R., Roy A., and Georgopoulos P. Biomarkers of environmental benzene exposure. Environ. Health Perspect. 104 Suppl. 6 (1996) 1141-1146
80. Wiwanitkit V., Suwansaksri J., and Nasuan P. Feasibility of urinary trans,trans-muconic acid determination using high performance liquid chromatography for biological monitoring of benzene exposure. J. Med. Assoc. Thai 84 Suppl. 1 (2001) S263-S268
81. Inoue O., Seiji K., Watanabe T., Kasahara M., Nakatsuka H., Yin S.N., Li G.L., Cai S.X., Jin C., and Ikeda M. Mutual metabolic suppression between benzene and toluene in man. Int. Arch. Occup. Environ. Health 60 (1988) 15-20
82. Qu Q., Shore R., Li G., Jin X., Chen L.C., Cohen B., Melikian A.A., Eastmond D., Rappaport S., Li H., Rupa D., Waidyanatha S., Yin S., Yan H., Meng M., Winnik W., Kwok E.S., Li Y., Mu R., Xu B., Zhang X., and Li K. Validation and evaluation of biomarkers in workers exposed to benzene in China. Res. Rep. Health Eff. Inst. 115 (2003) 1-87
83. Kivisto H., Pekari K., Peltonen K., Svinhufvud J., Veidebaum T., Sorsa M., and Aitio A. Biological monitoring of exposure to benzene in the production of benzene and in a cokery. Sci. Total Environ. 199 (1997) 49-63
84. Kivisto H., Scherer G., Renner T., and Meger M. Analysis and evaluation of trans,trans-muconic acid as a biomarker for benzene exposure. J. Chromatogr. B 717 (1998) 179-199
85. Ghittori S., Maestri L., Fiorentino M.L., and Imbrianai M. Evaluation of occupational exposure to benzene by urinalysis. Int. Arch. Occup. Environ. Health 67 (1995) 195-200
86. Barbieri A., Accorsi A., Raffi G.B., Nicoli L., and Violante F.S. Lack of sensitivity of urinary trans,trans-muconic acid in determining low-level (ppb) benzene exposure in children. Arch. Environ. Health 57 (2002) 224-228
87. Fustinoni S., Buratti M., Campo L., Colombi A., Consonni D., Pesatori A.C., Bonzini M., Farmer P., Garte S., Valerio F., Merlo D.F., and Bertazzi P.A. Urinary t,t-muconic acid, S-phenylmercapturic acid and benzene as biomarkers of low benzene exposure. Chem. Biol. Interact. 153/154 (2005) 253-256
88. Sanguinetti G., Accorsi A., Barbieri A., Raffi G.B., and Violante F.S. Failure of urinary trans,trans-muconic acid as a biomarker for indoor environmental benzene exposure at PPB levels. J. Toxicol. Environ. Health A 63 (2001) 599-604
89. Violante F.S., Sanguinetti G., Barbieri A., Accorsi A., Mattioli S., Cesari R., Fimognari C., and Hrelia P. Lack of correlation between environmental or biological indicators of benzene exposure at parts per billion levels and micronuclei induction. Environ. Res. 91 (2003) 135-142
90. Medinsky M.A., Schlosser P.M., and Bond J.A. Critical issues in benzene toxicity and metabolism: the effect of interactions with other organic chemicals on risk assessment. Environ. Health Perspect. 102 Suppl. 9 (1994) 119-124