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Role of Mixed-Function Oxidases in Insecticide Resistance

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Book cover Pest Resistance to Pesticides

Abstract

The realization that insects were able to metabolize modern synthetic organic insecticides, and that insect resistance to these insecticides was often associated with an enhanced metabolic detoxi-cation capability, came initially as something of a shock during the late 1940s and early 1950s. It was difficult to comprehend how any organism could possibly attain the complex enzymatic machinery necessary to metabolize such a chemical, which until a few short years earlier had never even seen the light of day and the development of which clearly could not have been foreseen by the insect at which it was directed. Could it really be that the chemical itself was in some way dictating the synthesis of new enzymes, a heretical evolutionary thought, or was it possible that the insects were pre-adaptively equipped to metabolize the insecticide? The latter was obviously a more comfortable concept from a genetic, evolutionary standpoint, although it posed some difficult questions regarding the natural substrates and catalytic functions of the insecticide-metabolizing enzymes.

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References

  • Agosin, M., and Perry, A. S., 1974, Microsomal mixed-function oxidases, in:.”The Physiology of Insecta,” Vol. V., M. Rockstein, ed., pp. 537–596, Academic Press, New York.

    Google Scholar 

  • Agosin, M., Michaeli, D., Miskus, R., Nagasawa, S., and Hoskins, W. M., 1961, A new DDT-metabolizing enzyme in the German cockroach, J. Econ. Entornol., 54:340.

    Google Scholar 

  • Bend, J. R., and Hook, G. E. R., 1977, “Handbook of Physiology,” Section 9, pp. 419–440, American Physiological Society, Washington, D.C.

    Google Scholar 

  • Bend, J. R., and James, M. O., 1978, Xenobiotic metabolism in marine and freshwater species, in: “Tiochemical and Biophysical Perspectives in Marine Biology,” D. C. Malins and J. R. Sargent, eds., Vol. 4., pp. 125–188, Academic Press, New York.

    Google Scholar 

  • Benezet, H. J., Chang, K. M., and Knowles, C. O., 1978, Formamidine pesticides — metabolic aspects, in: “Pesticide and Venom Neurotoxicity,” D. L. Shankland, R. M. Hollingworth and T. Smyth, Jr., eds., pp. 189–206, Plenum Press, New York.

    Chapter  Google Scholar 

  • Benke, G. M., and Wilkinson, C. F., 1971, In vitro mecrosomal epoxi-dase activity and susceptibility to carbaryl and carbaryl-piperonyl butoxide combinations in house crickets of different age and sex, J. Eoon. Entornol., 64:1032.

    CAS  Google Scholar 

  • Bigley, W. S., and Vinson, S. B., 1979, Degradation of (14C)metho-prene in the imported fire ant, Solenopsis invicta, Pestic. Biochem. Physiol., 10:1.

    Article  CAS  Google Scholar 

  • Brattsten, L. B., 1979a, Biochemical defense mechanisms in herbivores against plant allelochemicals, in: “Herbivores: Their Interactions with Secondary Plant Metabolites,” G.A. Rosenthal and D. H. Janzen, eds., pp. 199–270, Academic Press, New York.

    Google Scholar 

  • Brattsten, L. B., 1979b, Ecological significance of mixed-function oxidation, Drug Metab. Revs., 10:35.

    Article  CAS  Google Scholar 

  • Brattsten, L. B., and Metcalf, R. L., 1970, The synergistic ratio of carbaryl and piperonyl butoxide as an indicator of the distribution of multifunction oxidases in the Insects, J. Econ. Entomol., 63:101.

    PubMed  CAS  Google Scholar 

  • Brattsten, L. B., and Wilkinson, C. F., 1973, Induction of microsomal enzymes in the southern armyworm (Prodenia eridanid), Pestic. Biochem. Physiol., 3:393.

    Article  CAS  Google Scholar 

  • Brattsten, L. B., and Wilkinson, C. F., 1977, Insecticide solvents: Interference with insecticidal action, Science, 196:1211.

    Article  PubMed  CAS  Google Scholar 

  • Brattsten, L. B., Wilkinson, C. F., and Eisner, T., 1977, Herbivore plant interactions: Mixed-function oxidases and secondary plant substances, Science, 196:1349.

    Article  PubMed  CAS  Google Scholar 

  • Brooks, G. T., 1972, Pathways of enzymatic degradation of pesticides, in; “Environmental Quality and Safety,” F. Coulston and F. Korte, eds., pp. 106–164, Academic Press, New York.

    Google Scholar 

  • Brooks, G. T., 1974, “Chlorinated Insecticides,” Vol. II, CRC Press, Cleveland.

    Google Scholar 

  • Brown, H. D., and Rogers, E. F., 1950, The insecticidal activity of 1,1-dianisyl neopentane, J. Am. Chem. Soc., 72:1864.

    Article  CAS  Google Scholar 

  • Burt, M. E., Kuhr, R. J., and Bowers, W. S., 1978, Metabolism of precocene II in the cabbage looper and European corn borer, Pestic. Biochem. Physiol., 9:300.

    Article  CAS  Google Scholar 

  • Casida, J. E., 1969, Insect microsomes and insecticide chemical oxidations, in: “Microsomes and Drug Oxidations,” J. R. Gillette et al., eds., pp. 517–531, Academic Press, New York.

    Google Scholar 

  • Casida, J. E., 1970, Mixed function oxidase involvement in the biochemistry of insecticide synergists, J. Agr. Food Chem., 18:753.

    Article  CAS  Google Scholar 

  • Conney, A. H., 1967, Pharmacolgical implications of microsomal enzyme induction, Pharmacol. Rev., 19:317.

    PubMed  CAS  Google Scholar 

  • Coon, M. J., Vermillion, J. L., Vatsis, K. P., French, J. S., Dean, W. L., and Haugen, D. A., 1977, Biochemical studies on drug metabolism: Isolation of multiple forms of liver microsomal cytochrome P-450, in: “Drug Metabolism Concepts,” D. M. Jerina, ed., pp. 46–71, A.C.S. Symposium Series No. 44, Washington, D.C.

    Chapter  Google Scholar 

  • Eldefrawi, M. E., Miskus, R., and Sutcher, V., 1960, Methylenedioxy-phenyl derivatives as synergists for carbamate insecticides on susceptible, DDT- and parathion-resistant house flies, J. Econ. Entomol., 53:231.

    CAS  Google Scholar 

  • Elliott, M., Janes, N. F., Kimmel, E. C., and Casida, J. E., 1972, Metabolic fate of Pyrethrin I, pyrethrin II and allethrin administered orally to rats, J. Agr. Food Chem., 20:300.

    Article  CAS  Google Scholar 

  • Estabrook, R. W., Wrringloer, J., and Peterson, J. A., 1979, The use of animal subcellular fractions to study type I metabolism of xenobiotics, in: “Xenobiotic Metabolism: In Vitro Methods,” G. D. Paulson, D. S. Frear and E. P. Marks, eds., pp. 149–179, A.C.S. Symposium Series No. 97, Washington, D.C.

    Chapter  Google Scholar 

  • Farnham, A. W., 1973, Genetics of resistance of pyrethroid-selected houseflies, Musca domestica L., Pestic. Sci., 4:513.

    Article  CAS  Google Scholar 

  • Fukami, J., Shishido, T., Fukunaga, K., and Casida, J. E., 1969, Oxidative metabolism of rotenone in mammals, fish and insects and its relation to selective toxicity, J. Agr. Food Chem., 17:1217.

    Article  CAS  Google Scholar 

  • Georghiou, G. P., 1962, Carbamate insecticides: The cross-resistance spectra of four carbamate-resistant strains of the house fly after protracted selection pressure, J. Econ. Entomol., 55:494.

    CAS  Google Scholar 

  • Georghiou, G. P., and Metcalf, R. L., 1961, The absorption and metabolism of 3-isopropylphenyl N-methylcarbamate by susceptible and carbamate-selected strains of houseflies, J. Econ. Entomol., 54:231.

    CAS  Google Scholar 

  • Georghiou, G. P., Metcalf, R. L., and March, R. B., 1961, The development and characterization of resistance to carbamate insecticides in the housefly, Musca domestica, J. Econ. Entomol., 54:132.

    CAS  Google Scholar 

  • Georghiou, G. P., and C. E. Taylor, 1976, Pesticide resistance as an evolutionary phenomenon, Proc. XV Int. Congr. Entomol., pp. 759–785.

    Google Scholar 

  • Gordon, H. T., 1961, Nutritional factors in insect resistance to insecticides, Ann. Rev. Entomol., 6:27.

    Article  CAS  Google Scholar 

  • Gunsalus, I. C., 1972, Early reactions in the degradation of camphor: P-450 hydroxylase, in: “Degradation of Synthetic Organic Molecules in the Biosphere,” pp. 137–145, National Academy of Sciences, Washington, D.C.

    Google Scholar 

  • Hammock, B. D., Mumby, S. M., and Lee, P. W., 1977, Mechanisms of resistance to the juvenoid methoprene in the housefly, Musca domestica L., Pestic. Biochem. Physiol., 7:261.

    Article  CAS  Google Scholar 

  • Hodgson, E., 1976, Cytochrome P-450 interactions, in: “Insecticide Biochemistry and Physiology,” C. F. Wilkinson, ed., pp. 115–148, Plenum Press, New York.

    Google Scholar 

  • Hodgson, E., 1980, This volume.

    Google Scholar 

  • Hodgson, E., and Casida, J. E., 1960, Biological oxidation of N, N-dialkyl carbamates, Biochem. Biophys. Acta., 43:184.

    Article  Google Scholar 

  • Hodgson, E., and Philpot, R. M., 1974, Interaction of methylenedioxy-phenyl (1,3-benzodioxole) compounds with enzymes and their effect, in vivo, on animals, Drug Metdb. Revs., 3:323.

    Google Scholar 

  • Hodgson, E., and Plapp F. W., Jr., 1970, Biochemical Characteristics of insect microsomes, J. Agr. Food Chem., 18:1048.

    Article  CAS  Google Scholar 

  • Kawalek, J. C., and Lu, A. Y. H., 1975, Reconstituted liver microsomal enzyme system that hydroxylates drugs, other foreign compounds and endogenous substrates, Mot. Pharmacol., 11:201.

    CAS  Google Scholar 

  • Khan, M. A. Q., and Bederka, J. P., Jr., (eds.), 1974, “Survival in Toxic Environments,” Academic Press, New York, 553 pp.

    Google Scholar 

  • Krieger, R. I., and Wilkinson, C. F., 1969, Microsomal mixed-function oxidases in insects. I. Localization and properties of an enzyme system effecting aldrin epoxidation in larvae of the southern armyworm (Prodenia eridania), Biochem. Pharmacol., 18:1403.

    Article  PubMed  CAS  Google Scholar 

  • Krieger, R. I., Feeny, P. P., and Wilkinson, C. F., 1971, Detoxica-tion in the guts of caterpillars: An evolutionary answer to plant defenses? Science, 172:579.

    Article  PubMed  CAS  Google Scholar 

  • Kuhr, R. J., 1971, Comparative metabolism of carbaryl by resistant and susceptible strains of the cabbage looper, J. Econ. Entomol., 64:1373.

    PubMed  CAS  Google Scholar 

  • Lamoureux, G. L., and Frear, D. S., 1979, Pesticide metabolism in higher plants: In vitro enzyme studies, in: “Xenobiotic Metabolism: In Vitro Methods,” G. D. Paulson, D. S. Frear and E. P. Marks, eds., pp. 77–128, A.C.S. Sy-posium Series No. 97, Washington, D.C.

    Chapter  Google Scholar 

  • Lu, A. Y. H., and Levin, W., 1974, The resolution and reconstitution of the liver microsomal hydroxylation system, Biochim., Biophys. Acta, 344:205.

    CAS  Google Scholar 

  • Lu, A. Y. H., Ryan, D., Kawalek, J., Thomas, P., West, S. B., Huang, M. T., and Levin, W., 1976, Multiplicity of liver microsomal cytochrome P-450: Separation, purification and characterization, Biochem. Soc. (London) Trans., 4:169.

    CAS  Google Scholar 

  • Machinist, J. M., Dehner, E. W., and Ziegler, D. M., 1968, Microsomal oxidases. III. Comparison of species and organ distribution of dialkylarylamine N-oxide dealkylase and dialkylamine N-oxidase, Arch. Biochem. Biophys., 125:854.

    Article  Google Scholar 

  • Mannering, G. J., 1971, Microsomal enzyme systems which catalyze drug metabolism, in: “Fundamentals of Drug Metabolism and Drug Disposition,” B. N. LaDu, H. G. Mandel and E. L. Way, eds., pp. 206–252, Williams and Wilkins, Baltimore.

    Google Scholar 

  • Metcalf, R. L., 1976, Organochlorine insecticides, survey and prospects, in: “Insecticides for the Future: Needs and Prospects,” R. L. Metcalf and J. J. McKelvey, Jr., eds., pp. 223–285, John Wiley and Sons, New York.

    Google Scholar 

  • Metcalf, R. L., and Fukuto, T. R., 1965, Carbamate insecticides: Effect of chemical structure on intoxication and detoxication of phenyl N-methyl-carbamates in insects, J. Agr. Food Chem., 13:220.

    Article  CAS  Google Scholar 

  • Metcalf, R. L., Kapoor, I. P., and Hirwe, A. S., 1971, Biodegradable analogues of DDT, Bull. WHO, 44:363.

    PubMed  CAS  Google Scholar 

  • Moorefield, H. H., 1960, Resistance of carbamate insecticides, Misc. Publ. Entomol. Soc. Am., 2:151.

    Google Scholar 

  • Nakatsugawa, T., and Morelli, M. A., 1976, Microsomal oxidation and insecticide metabolism, in: “Insecticide Biochemistry and Physiology,” C. F. Wilkinson, ed., pp. 61–114, Plenum Press, New York.

    Google Scholar 

  • Nelson, P. A., Stewart, R. R., Morelli, M. A., and Nakatsugawa, T., 1976, Aldrin spoxidation in the earthworm, Lumbricus terrestris L., Pestic. Biochem. Physiol., 6:243.

    Article  CAS  Google Scholar 

  • Neuhauser, E., and Hartenstein, R., 1976, On the presence of O-demethylase activity in invertebrates, Comp. Biochem. Physiol., 53C:37.

    Google Scholar 

  • Oppenoorth, F. J., 1965, DDT-resistance in the housefly dependent on different mechanisms and the action of synergists, Mededeel, Landbouwhogeschool Opzoekingsstat. Gent., 30:1390.

    CAS  Google Scholar 

  • Oppenoorth, F. J., 1971, Resistance in insects: The role of metabolism and the possible use of synergists, Bull. WHO, 44:195.

    PubMed  CAS  Google Scholar 

  • Oppenoorth, F. J., 1976, Development of resista-ce to insecticides, in: “Insecticides for the Future: Needs and Prospects,” R. L. Metcalf and J. J. McKelvey, Jr., eds., pp. 41–59, John Wiley and Sons, New York.

    Google Scholar 

  • Oppenoorth, F. J., and Houx, N. W. H., 1968, DDT resistance in the house fly caused by microsomal degradation, Entorno!. Exp. Appl., 11:81.

    Article  CAS  Google Scholar 

  • Oppenoorth, F. J., and Welling, W., 1976, Biochemistry and Physiology of resistance, in: “Insecticide Biochemistry and Physiology,” C. F. Wilkinson, ed., pp. 507–551, Plenum Press, New York.

    Google Scholar 

  • Pan, H. P., Hook, G. E. R., and Fouts, J. R., 1975, The liver parenchyma and foreign compound metabolism in red-winged blackbird compared with rat, Xenobiotica, 5:17.

    Article  PubMed  CAS  Google Scholar 

  • Papadopoulos, N. M., and Kintzios, J. A., 1963, Formation of metabolites from nicotine by a rabbit liver preparation, J. Pharmacol. Exp. Ther., 140:269.

    PubMed  CAS  Google Scholar 

  • Perry, A. S., and Agosin, M., 1974, The physiology of insecticide resistance by insects, in: “The Physiology of Insecta,” Vol. VI, M. Rockstein, ed., pp. 3–124, Academic Press, New York.

    Google Scholar 

  • Pimprikar, G. D., and Georghiou, G. P., 1979, Mechanisms of resistance to diflubenzuron in the house fly, Musca domestica (L.), Pestic. Biochem. Physiol., 12:10.

    Article  CAS  Google Scholar 

  • Plapp, F. W., Jr., and Casida, J. E., 1969, Genetic control of house fly NADPH-dependent oxidases: Relation to insecticide chemical metabolism and resistance, J. Econ. Entomol., 62:1174.

    PubMed  CAS  Google Scholar 

  • Ranasingh, L. E., and Georghiou, G. P., 1980, Comparative modifications of insecticide-resistance spectrum of Culex pipiens fati-gans Wied. by selection with temephos and temephos/synergist combinations, Pestic. Sci., submitted.

    Google Scholar 

  • Sacher, R. M., Metcalf, R. L., and Fukuto, R. R., 1968, Propynyl naphthyl ethers as selective cambamate synergists, J. Agr. Food Chem., 16:779.

    Article  CAS  Google Scholar 

  • Sawicki, R. M., 1973, Recent advances in the study of the genetics of resistance in the housefly, Musca domestica, Pestic. Sci., 4:501.

    Article  CAS  Google Scholar 

  • Schonbrod, R. D., Philleo, W. W., and Terriere, L. C., 1965, Hydroxy-lation as a factor in resistance in houseflies and blow flies, J. Econ. Entomol., 58:74.

    PubMed  CAS  Google Scholar 

  • Schonbrod, R. D., Khan, M. A. Q., Terriere, L. C., and Plapp, F. W., Jr., 1968, Microsomal oxidases in the housefly: A survey of fourteen strains, Life Sci., 7:681.

    Article  CAS  Google Scholar 

  • Shono, T., Unai, T., and Casida, J. E., 1978, Metabolism of permeth-rin isomers in American cockroach adults, housefly adults and cabbage looper larvae, Pestic. Biochem. Physiol., 9:96.

    Article  CAS  Google Scholar 

  • Shrivastava, S. P., Tsukamoto, M., and Casida, J. E., 1969, Oxidative metabolism of C14-labeled Baygon by living houseflies and by housefly enzyme preparations, J. Econ. Entomol., 62:483.

    CAS  Google Scholar 

  • Shrivastava, S. P., Georghiou, G. P., Metcalf, R. L., and Fukuto, T. R., 1970, Carbamate resistance in mosquitoes: The metabolism of propoxur by susceptible and resistant larvae of Culex pipiens fatigans, Bull. WHO, 42:931.

    CAS  Google Scholar 

  • Slade, M., and Zibitt, C. H., 1972, Metabolism of Cecropia juvenile hormone in insects and in mammals, in: “Insect Juvenile Hormones: Chemistry and Action,” J. J. Menn and M. Beroza, eds., pp. 155–176, Academic Press, New York.

    Google Scholar 

  • Stanton, R. H., Plapp F. W., Jr., White, R. A., and Agosin, M., 1978, Induction of multiple cytochrime P-450 species in house fly microsomes — SDS gel electrophoresis studies, Comp. Biochem. Physiol., 61B:297.

    CAS  Google Scholar 

  • Sun, Y. P., and Johnson, E. R., 1960, Synergistic and antagonistic actions of insecticide-synergist combinations and their mode of action, J. Agr. Food Chem., 8:261.

    Article  CAS  Google Scholar 

  • Swingle, M. C., 1939, The effect of previous diet on the toxic action of lead arsenate to a leaf-feeding insect, J. Econ. Entomol., 32:884.

    CAS  Google Scholar 

  • Tanaka, K., Kurihara, N., and Nakajima, M., 1979, Oxidative metabolism of lindane and its isomers with microsomes from rat liver and housefly abdomen, Pestic. Bioohem. Physiol., 10:96.

    Article  CAS  Google Scholar 

  • Terriere, L. C., 1980, This volume.

    Google Scholar 

  • Terriere, L. C., Yu, S. J., and Hoyer, R. F., 1971, Induction of microsomal oxidase in F1 hybrids of a high and a low oxidase housefly strain, Science, 171:581.

    Article  PubMed  CAS  Google Scholar 

  • Testa, B., and Jenner, P., 1976, “Drub Metabolism: Chemical and Biochemical Aspects,” Dekker, New York, 500 pp.

    Google Scholar 

  • Tsukamoto, M., and Casida, J. E., 1967, Metabolism of methylcarbamate insecticides by the NADPH2-requiring enzyme system from house-flies, Nature, 213:49.

    Article  CAS  Google Scholar 

  • Wickramasinghe, R. H., and Villee, C. A., 1975, Early role during chemical evolution for cytochrome P-450 in oxygen detoxification, Nature, 256:509.

    Article  CAS  Google Scholar 

  • Wilkinson, C. F., 1968, The role of insecticide synergists in resistance problems, Wrld. Rev. Pest Control, 7:155.

    CAS  Google Scholar 

  • Wilkinson, C. F., 1971, Effects of synergists on the metabolism and toxicity of anticholinesterases, Bull. WHO, 44:171.

    PubMed  CAS  Google Scholar 

  • Wilkinson, C. F., 1976, Insecticide synergism, in: “Insecticides for the Future: Needs and Prospects,” R. L. Metcalf and J. J. McKelvey, Jr., eds., pp. 195–218, John Wiley and Sons, New York.

    Google Scholar 

  • Wilkinson, C. F., 1979, The use of insect subcellular components for studying the metabolism of Xenobiotics, in: “Xenobiotic Metabolism: In Vitro Methods,” G. D. Paulson, D. S. Frear and E. P. Marks, eds., pp. 249–284, A.C.S. Symposium Series No. 97, American Chemical Society, Washington, D.C.

    Chapter  Google Scholar 

  • Wilkinson, C. F., 1980, The metabolism of xenobiotics: A study in biochemical evolution, in: “The Scientific Basis of Toxicity Assessment,” H. R. Witschi, ed., pp. 251–268, Elsevier, North Holland.

    Google Scholar 

  • Wilkinson, C. F., and Brattsten, L. B., 1972, Microsomal drug metabolizing enzymes in insects, Drug Metab. Revs., 1:153.

    Article  CAS  Google Scholar 

  • Williamson, R. L., and Schecter, M. S., 1970, Microsomal epoxidation of aldrin in lepidopterous larvae, Biochem. Pharmacol., 19:1719.

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto, I., Kimmel, E. C., and Casida, J. E., 1969, Oxidative metabolism of pyrethroids in houseflies, J. Agr. Food Chem., 17:1227.

    Article  CAS  Google Scholar 

  • Yu, S. J., and Terriere, L. C., 1971, Induction of microsomal oxidases in the housefly and the action of inhibitors and stress factors, Pestic. Biochem. Physiol., 1:173.

    Article  CAS  Google Scholar 

  • Yu, S. J., and Terriere, L. C., 1972, Enzyme induction in the housefly: The specificity of the cyclodiene insecticides, Pestic. Biochem. Physiol., 2:184.

    Article  CAS  Google Scholar 

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Wilkinson, C.F. (1983). Role of Mixed-Function Oxidases in Insecticide Resistance. In: Georghiou, G.P., Saito, T. (eds) Pest Resistance to Pesticides. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-4466-7_7

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