Toxicity of aflatoxin B1 to Helicoverpa zea and bioactivation by cytochrome P450 monooxygenases

Journal of Chemical Ecology

Volumn 32, Issue 7, 2006, Pages 1459-1471

  Zeng, Ren Sen L ^a,b   Niu, Guodong ^a   Wen, Zhimou ^c   Schuler, Mary A ^c   Berenbaum, May R ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Aflatoxin B1; Bioactivation; Cytochrome P450 monooxygenase; Helicoverpa zea; Mycotoxin; Piperonyl butoxide

Indexed keywords

CYTOCHROME; DOSE-RESPONSE RELATIONSHIP; ENZYME ACTIVITY; FUNGUS; HOST-PATHOGEN INTERACTION; INHIBITOR; MAIZE; MOTH; PUPATION; TOXICITY TEST; TOXIN;

ASPERGILLUS; FUNGI; HELICOVERPA ZEA; HEXAPODA; INVERTEBRATA; VERTEBRATA; ZEA MAYS;

AFLATOXIN B1; CYTOCHROME P450; ENZYME INHIBITOR; PESTICIDE; PHENOBARBITAL; PIPERONYL BUTOXIDE;

ANIMAL; ARTICLE; DRUG ANTAGONISM; DRUG DETOXIFICATION; DRUG EFFECT; ENZYME ACTIVATION; INSECTICIDE RESISTANCE; LARVA; LEPIDOPTERA; METABOLISM; PHYSIOLOGY; TOXICITY TESTING;

AFLATOXIN B1; ANIMALS; CYTOCHROME P-450 ENZYME SYSTEM; ENZYME ACTIVATION; ENZYME INHIBITORS; INSECTICIDE RESISTANCE; LARVA; LEPIDOPTERA; METABOLIC DETOXICATION, DRUG; PESTICIDE SYNERGISTS; PHENOBARBITAL; PIPERONYL BUTOXIDE; TOXICITY TESTS;

EID: 33846940732     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-006-9062-7     Document Type: Article

References (47)

1. 14C in house flies. J. Econ. Entomol. 65:375-378.
2. BATARD, Y., LERET, M., SCHALK, M., ROBINEAU, T., DURST, F., and WERCK-REICHHART, D. 1998. Molecular cloning and functional expression in yeast of CYP76B1, a xenobiotic-inducible 7-ethoxycoumarin O-deethylase from Helianthus tuberosus. Plant J. 14:111-120.
3. BROWN, D., ZHANG, L., WEN, Z., and SCOTT, J. G. 2003. Induction of P450 monooxygenases in the German cockroach Blattella germanica. Arch. Insect Biochem. Physiol. 53:119-124.
4. BRUN, A., CUANY, A., LE MOUEL, T., BERGE, J., and AMICHOT, M. 1996. Inducibility of the Drosophila melanogaster cytochrome P450 gene, CYP6A2, by phenobarbital in insecticide susceptible or resistant strains. Insect Biochem. Mol. Biol. 26:697-703.
5. CHINNICI, J. P. and BETTINGER, D. A. 1984. Effects of aflatoxin B1 and caffeine on viability in natural strains of Drosophila melanogaster. J. Invertebr. Pathol. 44:263-266.
6. CHINNICI, J. P. and MELONE, P. D. 1985. Genetic aspects of aflatoxin B1 resistance in Drosophila melanogaster. J. Heredity 76:85-88.
7. CRESPI, C. L., PENMAN, B. W., LEAKEY, J. A., ARLOTTO, M. P., STARK, A., PARKINSON, A., TURNER, T., STEIMEL, D. T., RUDO, K., and DAVIES, R. L. 1990. Human cytochrome P450IIA3: cDNA sequence, role of the enzyme in the metabolic activation of promutagens, comparison to nitrosamine activation by human cytochrome P450IIE1. Carcinogenesis 11:1293-1300.
8. DOWD, P. F. 1998. The involvement of arthropods in the establishment of mycotoxigenic fungi under field conditions, pp 307-350, in K. K. Sinha and D. Bhatnagar (eds.). Mycotoxins in Agriculture and Food Safety. Marcel Dekker, New York.
9. DOWD, P. F. 2001. Biotic and abiotic factors limiting efficacy of Bt corn in indirectly reducing mycotoxin levels in commercial fields. J. Econ. Entomol. 94:1067-1074.
10. DOWD, P. F. and WHITE, D. G. 2002. Corn earworm, Helicoverpa zea (Lepidoptera: Noctuidae) and other insect associated resistance in the maize inbred Tex6. J. Econ. Entomol. 95:628-634.
11. DOWD, P. F., DUVICK, J. P., and ROOD, T. 1997. Comparative toxicity of allelochemicals and their enzymatic oxidation products to maize fungal pathogens, emphasizing Fusarium graminearum. Nat. Toxins 5:180-185.
12. DUNKOV, B. C., GUZOV, V. M., MOCELIN, G., SHOTKOSKI, F., BRUN, A., AMICHOT, M., FFRENCH-CONSTANT, R. H., and FEYEREISEN, R. 1997. The Drosophila cytochrome P450 gene Cyp6a2: structure, localization, heterologous expression, and induction by phenobarbital. DNA Cell Biol. 16:1345-1356.
13. EATON, D. L., MONROE, D. H., BELLAMY, G., and KALMAN, D. A. 1988. Identification of a novel dihydroxy metabolite of aflatoxin B1 produced in vitro and in vivo in rats and mice. Chem. Res. Toxicol. 1:108-114.
14. EATON, D. L., RAMSDELL, H. S., and NEAL, G. E. 1994. Biotransformation of aflatoxins, pp. 45-72, in D. L. Eaton and J. D. Groopman (eds.). The Toxicology of Aflatoxins. Human Health, Veterinary and Agricultural Significance. Academic Press, London.
15. FOERSTER, R. E. and WURGLER, F. E. 1984. In vitro studies on the metabolism of aflatoxin B1 and aldrin in testes of genetically different strains of Drosophila melanogaster. Arch Toxicol. 56:12-17.
16. GUENGERICH, F. P., JOHNSON, W. W., SHIMADA, T., UENG, Y. F., YAMAZAKI, H., and LANGOUET, S. 1998. Activation and detoxication of aflatoxin B1. Mutat. Res. 402:121-128.
17. HATCHER, P. E. 1995. Three-way interactions between plant pathogenic fungi, herbivorous insects and their host plants. Biol. Rev. 70:639-694.
18. IYER, R. S., VOEHLER, M. W., and HARRIS, T. M. 1994. Adenine adduct of aflatoxin B1 epoxide. J. Am. Chem. Soc. 116:8863-8869.
19. 1, on larval viability and gross morphology in Drosophila melanogaster. Dev. Ind. Microbiol. 17:443-449.
20. 1 by larvae of navel orangeworm, Amyelois transitella (Walker) (Insecta, Lepidoptera, Pyralidae) and codling moth, Cydia pomonella (L.) (Insecta, Lepidoptera, Tortricidae). Arch. Insect Biochem. Physiol. 45:166-174.
21. LI, X., BERENBAUM, M. R, and SCHULER, M. A. 2000. Molecular cloning and expression of. CYP6B8: A xanthotoxin- inducible cytochrome P450 cDNA from Helicoverpa zea. Insect Biochem. Mol. Biol. 30:75-84.
22. LI, X., BERENBAUM, M. R., and SCHULER, M. A. 2002a. Plant allelochemicals differentially regulate Helicoverpa zea cytochrome P450 genes. Insect Mol. Biol. 11:343-351.
23. LI, X., SCHULER, M. A., and BERENBAUM, M. R. 2002b. Jasmonate and salicylate induce expression of herbivore cytochrome P450 genes. Nature 419:712-715.
24. LI, X., BAUDRY, J., BERENBAUM, M. R., and SCHULER, M. A. 2004. Structural and functional divergence of insect CYP6B proteins: From specialist to generalist cytochrome P450. Proc. Natl. Acad. Sci. USA 101:2939-2944.
25. LILLEHOJ, E. B. 1992. Aflatoxin genetic mobilization agent, pp. 1-22, in D. Bhatnagar, E. B. Lillehoj, and D. K. ARORA (eds.). Mycotoxins in Ecological Systems, Handbook of Applied Mycology, Vol. 5. Marcel Dekker, New York.
26. 1 among several strains of Drosophila melanogaster (Diptera). J. Invertebr. Pathol. 31:37-40.
27. MAITRA, S., DOMBROWSKI, S. M., WATERS, L. C., and GANGULY, R. 1996. Three second chromosome-linked clustered Cyp6 genes show differential constitutive and barbital-induced expression in DDT-resistant and susceptible strains of Drosophila melanogaster. Gene 180:165-171.
28. MURRAY, R. D. H., MENDEZ, J., and BROWN, S. A. 1982. The Natural Coumarins: Occurrence, Chemistry and Biochemistry. John Wiley and Sons, Chichester, UK, pp 702.
29. NEWBERNE, P. M. and BUTLER, W. H. 1969. Acute and chronic effects of aflatoxin on the liver of domestic and laboratory animals: a review. Cancer Res. 29:236-250.
30. OBRECHT-PFLUMIO, S., CHASSAT T., DIRHEIMER, G., and MARZIN, D. 1999. Genotoxicity of ochratoxin A by Salmonella mutagenicity test after bioactivation by mouse kidney microsomes. Mutat. Res. 446:95-102.
31. PELKONEN, P., LANG, M. A., WILD, C. P., NEGISHI, M., and JUVONEN, R. O. 1994. Activation of aflatoxin B1 by mouse CYP2A enzymes and cytotoxicity in recombinant yeast cells. Eur. J. Pharmacol. 292:67-73.
32. PERSANS, M. W., WANG, J., and SCHULER, M. A. 2001. Characterization of maize cytochrome P450 monooxygenases induced in response to safeners and bacterial pathogens. Plant Physiol. 125:1126-1138.
33. RAMSDELL, H. S. and EATON, D. L. 1990. Species susceptibility to aflatoxin B1 carcinogenesis: comparative kinetics of microsomal transformation. Cancer Res. 50:615-620.
34. SADEK, M. M., CRAILSHEIM, K., and AZAB, S. G. 1996. The chemosterilizing activity of some mycotoxins and their influence on the development and survival of Spodoptera littoralis (Boisd.) (Lep., Noctuidae). J. Appl. Entomol. 120:53-61.
35. SANER, C., WEIBEL, B., WURGLER, F. E., and SENGSTAG, C. 1996. Metabolism of promutagens catalyzed by Drosophila melanogaster CYP6A2 enzyme in Saccharomyces cerevisiae. Environ. Mol. Mutagen. 27:46-58.
36. SASABE, M., WEN, Z., BERENBAUM, M. R., and SCHULER, M. A. 2004. Molecular analysis of CYP321A1, a novel cytochrome P450 involved in metabolism of plant allelochemicals (furanocoumarins) and insecticides (cypermethrin) in Helicoverpa zea. Gene 338:163-175.
37. STEVENS, J. L., SNYDER, M. J., KOENER, J. F., and FEYEREISEN, R. 2000. Inducible P450s of the CYP9 family from larval Manduca sexta midgut. Insect Biochem. Mol. Biol. 30:559-568.
38. STONE, T. B. and SIMS, S. R. 1993. Geographic susceptibility of Heliothis virescens and Helicoverpa zea (Lepidoptera: Noctuidae) to Bacillus thuringiensis. J. Econ. Entomol. 86:989-994.
39. U.S. Department of Agriculture (USDA). 1998. Grain Inspection, Packers and Stockyards Administration (GIPSA). "GIPSA Backgrounder: Aflatoxin." http://www.gipsa.usda.gov/reference-library/handbooks/ aflatoxin/aflatoxin-ch04.pdf. Accessed Nov. 2005.
40. U.S. Department of Agriculture (USDA), Agricultural Res. Service. 1999. Food Safety National Program. USDA-ARS, Beltsville, MD.
41. UENG, Y. F., SHIMADA, T., YAMAZAKI, H., and GUENGERICH, F. P. 1995. Oxidation of aflatoxin B1 by bacterial recombinant human cytochrome P450 enzymes. Chem. Res. Toxicol. 8:218-225.
42. WALDBAUER, G. P., COHEN, R. W., and RRIEDMAN, S. 1984. An improved procedure for laboratory rearing of the corn earworm, Heliothis zea (Lepidoptera: Noctuidae). Great Lakes Entomol. 17:113-118.
43. WAXMAN, D. J. 1999. P450 gene induction by structurally diverse xenochemicals: central role of nuclear receptors CAR, PXR, and PPAR. Arch. Biochem. Biophys. 369:11-23.
44. WINDHAM, G. L., WILLIAMS, W. P., and DAVIS, F. M. 1999. Effects of the southwestern corn borer on Aspergillus flavus kernel infection and aflatoxin accumulation in maize hybrids. Plant Dis. 83:535-540.
45. WISEMAN, B. R. 1999. Corn earworm, pp. 59-61, in K. L. Steffey, M. E. Rice, J. All, D. A. Andow, M. E. Gray, and J. W. Van Duyn (eds.). Handbook of Corn Insects. Entomological Society of America, Lanham, MD.
46. WRIGHT, V. F., VESONDER, R. F., and CIEGLER, A. 1982. Mycotoxins and other fungal metabolites as insecticides, pp. 559-583, in E. Kurstak (ed.). Microbial and Viral Pesticides, Chap. 17. Marcel Dekker, New York.
47. YUN, C. H., SHIMADA, T., and GUENGERICH, F. P. 1991. Purification and characterization of human liver microsomal cytochrome P-450 2A6. Mol. Pharmacol. 40:679-685.