Advertisement

Role of Mixed-Function Oxidases in Insecticide Resistance

  • C. F. Wilkinson

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.

Keywords

Insect Resistance Organophosphorus Compound MUsca Domestica Carbamate Insecticide Cabbage Looper 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 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
  2. 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
  3. 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
  4. 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
  5. 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.CrossRefGoogle Scholar
  6. 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.Google Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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
  9. Brattsten, L. B., 1979b, Ecological significance of mixed-function oxidation, Drug Metab. Revs., 10:35.CrossRefGoogle Scholar
  10. 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.PubMedGoogle Scholar
  11. Brattsten, L. B., and Wilkinson, C. F., 1973, Induction of microsomal enzymes in the southern armyworm (Prodenia eridanid), Pestic. Biochem. Physiol., 3:393.CrossRefGoogle Scholar
  12. Brattsten, L. B., and Wilkinson, C. F., 1977, Insecticide solvents: Interference with insecticidal action, Science, 196:1211.PubMedCrossRefGoogle Scholar
  13. Brattsten, L. B., Wilkinson, C. F., and Eisner, T., 1977, Herbivore plant interactions: Mixed-function oxidases and secondary plant substances, Science, 196:1349.PubMedCrossRefGoogle Scholar
  14. 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
  15. Brooks, G. T., 1974, “Chlorinated Insecticides,” Vol. II, CRC Press, Cleveland.Google Scholar
  16. Brown, H. D., and Rogers, E. F., 1950, The insecticidal activity of 1,1-dianisyl neopentane, J. Am. Chem. Soc., 72:1864.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 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
  19. Casida, J. E., 1970, Mixed function oxidase involvement in the biochemistry of insecticide synergists, J. Agr. Food Chem., 18:753.CrossRefGoogle Scholar
  20. Conney, A. H., 1967, Pharmacolgical implications of microsomal enzyme induction, Pharmacol. Rev., 19:317.PubMedGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. 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.Google Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. Farnham, A. W., 1973, Genetics of resistance of pyrethroid-selected houseflies, Musca domestica L., Pestic. Sci., 4:513.CrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.Google Scholar
  28. 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.Google Scholar
  29. 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.Google Scholar
  30. Georghiou, G. P., and C. E. Taylor, 1976, Pesticide resistance as an evolutionary phenomenon, Proc. XV Int. Congr. Entomol., pp. 759–785.Google Scholar
  31. Gordon, H. T., 1961, Nutritional factors in insect resistance to insecticides, Ann. Rev. Entomol., 6:27.CrossRefGoogle Scholar
  32. 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
  33. 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.CrossRefGoogle Scholar
  34. 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
  35. Hodgson, E., 1980, This volume.Google Scholar
  36. Hodgson, E., and Casida, J. E., 1960, Biological oxidation of N, N-dialkyl carbamates, Biochem. Biophys. Acta., 43:184.CrossRefGoogle Scholar
  37. 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
  38. Hodgson, E., and Plapp F. W., Jr., 1970, Biochemical Characteristics of insect microsomes, J. Agr. Food Chem., 18:1048.CrossRefGoogle Scholar
  39. 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.Google Scholar
  40. Khan, M. A. Q., and Bederka, J. P., Jr., (eds.), 1974, “Survival in Toxic Environments,” Academic Press, New York, 553 pp.Google Scholar
  41. 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.PubMedCrossRefGoogle Scholar
  42. 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.PubMedCrossRefGoogle Scholar
  43. Kuhr, R. J., 1971, Comparative metabolism of carbaryl by resistant and susceptible strains of the cabbage looper, J. Econ. Entomol., 64:1373.PubMedGoogle Scholar
  44. 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.CrossRefGoogle Scholar
  45. Lu, A. Y. H., and Levin, W., 1974, The resolution and reconstitution of the liver microsomal hydroxylation system, Biochim., Biophys. Acta, 344:205.Google Scholar
  46. 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.Google Scholar
  47. 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.CrossRefGoogle Scholar
  48. 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
  49. 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
  50. 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.CrossRefGoogle Scholar
  51. Metcalf, R. L., Kapoor, I. P., and Hirwe, A. S., 1971, Biodegradable analogues of DDT, Bull. WHO, 44:363.PubMedGoogle Scholar
  52. Moorefield, H. H., 1960, Resistance of carbamate insecticides, Misc. Publ. Entomol. Soc. Am., 2:151.Google Scholar
  53. 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
  54. 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.CrossRefGoogle Scholar
  55. Neuhauser, E., and Hartenstein, R., 1976, On the presence of O-demethylase activity in invertebrates, Comp. Biochem. Physiol., 53C:37.Google Scholar
  56. Oppenoorth, F. J., 1965, DDT-resistance in the housefly dependent on different mechanisms and the action of synergists, Mededeel, Landbouwhogeschool Opzoekingsstat. Gent., 30:1390.Google Scholar
  57. Oppenoorth, F. J., 1971, Resistance in insects: The role of metabolism and the possible use of synergists, Bull. WHO, 44:195.PubMedGoogle Scholar
  58. 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
  59. Oppenoorth, F. J., and Houx, N. W. H., 1968, DDT resistance in the house fly caused by microsomal degradation, Entorno!. Exp. Appl., 11:81.CrossRefGoogle Scholar
  60. 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
  61. 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.PubMedCrossRefGoogle Scholar
  62. Papadopoulos, N. M., and Kintzios, J. A., 1963, Formation of metabolites from nicotine by a rabbit liver preparation, J. Pharmacol. Exp. Ther., 140:269.PubMedGoogle Scholar
  63. 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
  64. 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.CrossRefGoogle Scholar
  65. 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.PubMedGoogle Scholar
  66. 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
  67. Sacher, R. M., Metcalf, R. L., and Fukuto, R. R., 1968, Propynyl naphthyl ethers as selective cambamate synergists, J. Agr. Food Chem., 16:779.CrossRefGoogle Scholar
  68. Sawicki, R. M., 1973, Recent advances in the study of the genetics of resistance in the housefly, Musca domestica, Pestic. Sci., 4:501.CrossRefGoogle Scholar
  69. 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.PubMedGoogle Scholar
  70. 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.CrossRefGoogle Scholar
  71. 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.CrossRefGoogle Scholar
  72. 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.Google Scholar
  73. 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.Google Scholar
  74. 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
  75. 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.Google Scholar
  76. 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.CrossRefGoogle Scholar
  77. 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.Google Scholar
  78. 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.CrossRefGoogle Scholar
  79. Terriere, L. C., 1980, This volume.Google Scholar
  80. 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.PubMedCrossRefGoogle Scholar
  81. Testa, B., and Jenner, P., 1976, “Drub Metabolism: Chemical and Biochemical Aspects,” Dekker, New York, 500 pp.Google Scholar
  82. Tsukamoto, M., and Casida, J. E., 1967, Metabolism of methylcarbamate insecticides by the NADPH2-requiring enzyme system from house-flies, Nature, 213:49.CrossRefGoogle Scholar
  83. Wickramasinghe, R. H., and Villee, C. A., 1975, Early role during chemical evolution for cytochrome P-450 in oxygen detoxification, Nature, 256:509.CrossRefGoogle Scholar
  84. Wilkinson, C. F., 1968, The role of insecticide synergists in resistance problems, Wrld. Rev. Pest Control, 7:155.Google Scholar
  85. Wilkinson, C. F., 1971, Effects of synergists on the metabolism and toxicity of anticholinesterases, Bull. WHO, 44:171.PubMedGoogle Scholar
  86. 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
  87. 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.CrossRefGoogle Scholar
  88. 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
  89. Wilkinson, C. F., and Brattsten, L. B., 1972, Microsomal drug metabolizing enzymes in insects, Drug Metab. Revs., 1:153.CrossRefGoogle Scholar
  90. Williamson, R. L., and Schecter, M. S., 1970, Microsomal epoxidation of aldrin in lepidopterous larvae, Biochem. Pharmacol., 19:1719.PubMedCrossRefGoogle Scholar
  91. Yamamoto, I., Kimmel, E. C., and Casida, J. E., 1969, Oxidative metabolism of pyrethroids in houseflies, J. Agr. Food Chem., 17:1227.CrossRefGoogle Scholar
  92. 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.CrossRefGoogle Scholar
  93. Yu, S. J., and Terriere, L. C., 1972, Enzyme induction in the housefly: The specificity of the cyclodiene insecticides, Pestic. Biochem. Physiol., 2:184.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1983

Authors and Affiliations

  • C. F. Wilkinson
    • 1
  1. 1.Department of EntomologyCornell UniversityIthacaUSA

Personalised recommendations