Why are there so few resistance-associated mutations in insecticide target genes?

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 353, Issue 1376, 1998, Pages 1685-1693

  Ffrench Constant, Richard H ^a   Pittendrigh, Barry ^a   Vaughan, Ashley ^a   Anthony, Nicola ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Acetylcholinesterase; Insecticide resistance; Para; Rdl; Voltage gated sodium channel; aminobutyric acid receptor

Indexed keywords

EID: 0032578880     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.1998.0319     Document Type: Article

References (61)

1. Anthony, N., Rocheleau, T., Mocelin, G., Lee, H.-J. & ffrench-Constant, R. H. 1995a Cloning, sequencing and functional expression of an acetylcholinesterase gene from the yellow fever mosquito Aedes aegypti. FEBS Lett. 368, 461-465.
2. Anthony, N. M., Brown, J. K., Markham, P. G. & ffrench-Constant, R. H. 1995b Molecular analysis of cyclodiene resistance-associated mutations among populations of the sweetpotato whitefly Bemisia tabaci. Pestic. Biochem. Physiol. 51, 220-228.
3. Aronstein, K. & ffrench-Constant, R. 1995 Immunocytochemistry of a novel GABA receptor subunit Rdl in Drosophila melanogaster. Invert. Neurosci. 1, 25-31.
4. Aronstein, K., Rocheleau, T. & ffrench-Constant, R. H. 1996 Distribution of two GABA receptor-like subunits in the Drosophila CNS. Invert. Neurosci. 2, 115-120.
5. Ayad, H. & Georghiou, G. P. 1975 Resistance to organophosphates and carbamates in Anopheles albimanus based on reduced sensitivity of acetylcholinesterase. J. Econ. Entomol. 68, 295-297.
6. Bourguet, D., Pasteur, N., Bisset, J. & Raymond, M. 1996a Determination of Ace.1 genotypes in single mosquitoes: toward an ecumenical biochemical test. Pestic. Biochem. Physiol. 55, 122-128.
7. Bourguet, D., Raymond, M., Fournier, D., Malcolm, G. A., Toutant, J.-P. & Arpagaus, M. 1996A Existence of two acetylcholinesterases in the mosquito Culex pipiens (Diptera: Culicidae). J. Neurochem. 67, 2115-2123.
8. Cannon, S. C., Brown, R. H. & Corey, D. P. 1991 A sodium channel defect in hyperkalemic periodic paralysis: potassium induced failure of inactivation. Neuron 6, 619-626.
9. Dong, K. 1997 A single amino acid change in the para sodium channel protein is associated with knockdown-resistance (kdr) to pyrethroid insecticides in German cockroaches. Insect Biochem. Molec. Biol. 27, 93-100.
10. Dong, K. & Scott, J. G. 1994 Linkage of kdr-type resistance and the para-homologous sodium channel gene in German cockroaches. Insect Biochem. Molec. Biol. 24, 647-654.
11. Feyereisen, R. 1995 Molecular biology of insecticide resistance. Toxicol. Lett. 82/83, 83-90.
12. ffrench-Constant, R. H. & Bonning, B. C. 1989 Rapid microtitre plate test distinguishes insecticide resistant acetylcholinesterase genotypes in the mosquitoes Anopheles albimanus, An. nigerrimus and Culex pipiens. Med. Vet. Entomol. 3, 9-16.
13. A receptor locus. Proc. Natn. Acad. Sci. USA 88, 7209-7213.
14. ffrench-Constant, R. H., Roush, R. T. & Carino, F. 1992 Drosophila as a tool for investigating the molecular genetics of insecticide resistance. In Molecular approaches to pure and applied entomology (ed. M. J. Whitten & J. G. Oakeshott), p. 137. Berlin: Springer.
15. ffrench-Constant, R. H., Rocheleau, T. A., Steichen, J. C. & Chalmers, A. E. 1993a A point mutation in a Drosophila GABA receptor confers insecticide resistance. Nature 363, 449-451.
16. ffrench-Constant, R. H.; Steichen, J., Rocheleau, T. A., Aronstein, K. & Roush, R. T. 1993b A single amino-acid substitution in a γ-aminobutyric acid subtype A receptor locus associated with cyclodiene insecticide resistance in Drosophila populations. Proc. Natn. Acad. Sci. USA 90, 1957-1961.
17. ffrench-Constant, R. H., Steichen, J. C. & Ode, P. 1993c Cyclodiene insecticide resistance in Drosophila melanogaster (Meigen) is associated with a temperature sensitive phenotype. Pestic. Biochem. Physiol. 46, 73-77.
18. ffrench-Constant, R. H., Steichen, J. C. & Brun, L. O. 1994 A molecular diagnostic for endosulfan insecticide resistance in the coffee berry borer Hypothenemus hampei (Coleoptera: Scolytidae). Bull. Entomol. Res. 84, 11-16.
19. ffrench-Constant, R. H., Zhang, H.-G. & Jackson, M. B. 1995 Biophysical analysis of a single amino acid replacement in the resistance to dieldrin γ-aminobutyric acid receptor: novel dual mechanism for cyclodiene insecticide resistance. In Molecular action of insecticides on ion channels (ed. J. M. Clarke), pp. 192-204. San Diego, CA: American Chemical Society.
20. Field, L. M., Anderson, A. P., Denholm, I., Foster, S. P., Harling, Z. K., Javed, N., Martinez-Torres, D., Moores, G. D., Williamson, M. S. & Devonshire, A. L. 1997 Use of biochemical and DNA diagnostics for characterising multiple mechanisms of insecticide resistance in the peach-potato aphid, Myzus persicae (Sulzer). Pestic. Sci. 51, 283-289.
21. Fournier, D., Berrada, S. & Bongibault, V. 1996 Molecular genetics of acetylcholinesterase in insecticide-resistant Drosophila melanogaster. In Molecular genetics and evolution of pesticide resistance (ed. T. M. Brown), pp. 17-27. Washington: American Chemical Society.
22. Guerrero, F. D., Jamroz, R. C., Kammlah, D. & Kunz, S. E. 1997 Toxicological and molecular characterization of pyrethroid-resistant horn flies, Haematobia irritans: identification of kdr and super-kdr point mutations. Insect Biochem. Molec. Biol. 27, 745-755.
23. Haas, R., Marshall, T. L. & Rosenberry, T. L. 1988 Drosophila acetylcholinesterase: demonstration of a glycoinositol phospholipid anchor and an endogenous proteolytic cleavage. Biochemistry 27, 6453-6457.
24. Hall, L. M. & Malcolm, C. A. 1991 The acetylcholinesterase gene of Anopheles stephensi. Cell. Molec. Neurobiol. 11, 131-141.
25. Hall, L. M. & Spierer, P. 1986 The Ace locus of Drosophila melanogaster: structural gene for acetylcholinesterase with an unusual 5′ leader. EMBO J. 5, 2949-2954.
26. Hemingway, J. & Georghiou, G. P. 1983 Studies on the acetylcholinesterase of Anopheles albimanus resistant and susceptible to organophosphorus and carbamate insecticides. Pestic. Biochem. Physiol. 19, 167-171.
27. Hemingway, J., Malcolm, C., Kissoon, K., Boddington, R., Curtis, C. & Hill, N. 1985 The biochemistry of insecticide resistance in Anopheles sacharovi: comparative studies with a range of insecticide susceptible and resistant Anopheles and Culex species. Pestic. Biochem. Physiol. 24, 68-76.
28. Hosie, A. M., Aronstein, K., Sattelle, D. B. & ffrench-Constant, R. 1997 Molecular biology of insect neuronal GABA receptors. Trends Neurosci. 20, 578-583.
29. + channel. Nature 353, 86-90.
30. Knipple, D. C., Doyle, K. E., Marsella-Herrick, P. A. & Soderlund, D. M. 1994 Tight genetic linkage between the kdr insecticide resistance trait and a voltage-sensitive sodium channel gene in the house fly. Proc. Natn. Acad. Sci. USA 91, 2483-2487.
31. Kohrman, D. C., Smith, M. R., Goldin, A. L., Harris, J. & Meisler, M. H. 1996 A missense mutation in the sodium channel Scn8a is responsible for cerebellar ataxia in the mouse mutant jolting. J. Neurosci. 16, 5993-5999.
32. Lee, H.-J., Rocheleau, T., Zhang, H.-G., Jackson, M. B. & ffrench-Constant, R. H. 1993 Expression of a Drosophila GABA receptor in a baculovirus insect cell system: functional expression of insecticide susceptible and resistant GABA receptors from the cyclodiene resistance gene Rdl. FEBS Lett. 335, 315-318.
33. Leonard, R. J., Labarca, C. G., Charnet, P., Davidson, N. & Lester, H. A. 1988 Evidence that the M2 membrane-spanning region lines the ion channel pore of the nicotinic receptor. Science 242, 1578-1581.
34. Loughney, K., Kreber, R. & Ganetzky, B. 1989 Molecular analysis of the para locus, a sodium channel gene in Drosophila. Cell 58, 1143-1154.
35. McClatchey, A. I., McKenna-Yasek, D., Cros, D., Worthen, H. G., Kuncl, R. W., DeSilva, S. M., Cornblath, D. R., Gusella, J. F. & Brown, R. H. 1992 Novel mutations in families with unusual and variable disorders of the skeletal muscle sodium channel. Nat. Genet. 2, 148-152.
36. Martinez-Torres, D., Chandre, F., Williamson, M. S., Darriet, F., Berge, J. B., Devonshire, A. L., Guillet, P., Pasteur, N. & Pauron, D. 1998 Molecular characterization of pyrethroid resistance in the major knockdown resistance (kdr) malaria vector Anopheles gambiae ss. Insect Molec. Biol. 7, 179-184.
37. Miyazaki, M., Ohyama, K., Dunlap, D. Y. & Matsumura, F. 1996 Cloning and sequencing of the para-type sodium channel gene from susceptible and kdr-resistanct German cockroaches (Blattella germanica) and the housefly (Musca domestica). Molec. Gen. Genet. 252, 61-68.
38. Mutero, A., Pralavorio, M., Bride, J.-M. & Fournier, D. 1994 Resistance-associated point mutations in insecticide-insensitive acetylcholinesterase. Proc. Natn. Acad. Sci. USA 91, 5922-5926.
39. Newland, C. F. & Cull-Candy, S. G. 1992 On the mechanism of action of picrotoxin on GABA receptor channels in dissociated sympathetic neurones of the rat. J. Physiol. 447, 191-213.
40. Park, Y. & Taylor, M. F. J. 1997 A novel mutation L1029H in sodium channel gene hscp associated with pyrethroid resistance for Heliothis virescens (Lepidoptera: Noctuidae). Insect Biochem. Molec. Biol. 27, 9-13.
41. Pittendrigh, B., Reenan, R., ffrench-Constant, R. H. & Ganetzky, B. 1997 Point mutations in the Drosophila sodium channel gene para associated with resistance to DDT and pyrethroid insecticides. Molec. Gen. Genet. 256, 602-610.
42. Ptacek, L. J., George, A. L., Griggs, R. C., Tawil, R., Kallen, R. G., Barchi, R. L., Robertson, M. & Leppert, M. F. 1991 Identification of a mutation in the gene causing hyperkalemic periodic paralysis. Cell 67, 1021-1027.
43. Raymond, M., Fournier, D., Bride, J.-M., Cuany, A., Berge, J., Magnin, M. & Pasteur, N. 1986 Identification of resistance mechanisms in Culex pipiens (Diptera: Culicidae) from southern France: insensitive acetylcholinesterase and detoxifying oxidases. J. Econ. Entomol. 79, 1452-1458.
44. + channel alpha-subunit in hyperkalemic periodic paralysis. Nature 354, 387-389.
45. Severson, D. W., Anthony, N. M., Andreen, O. & ffrench-Constant, R. H. 1997 Molecular mapping of insecticide resistance genes in the yellow fever mosquito (Aedes aegypti). J. Hered. 88, 520-524.
46. Smith, T. J., Lee, S. H., Ingles, P. J., Knipple, D. C. & Soderlund, D. M. 1997 The L1014F point mutation in the housefly Vssc1 sodium channel confers knockdown resistance to pyrethroids. Insect Biochem. Molec. Biol. 27, 807-812.
47. Soderlund, D. M. & Bloomquist, J. R. 1989 Neurotoxic actions of pyrethroid insecticides. A. Rev. Entomol. 34, 77-96.
48. Sussman, J. L., Harel, M., Frolow, F., Oefner, C., Goldman, A., Toker, L. & Silman, I. 1991 Atomic structure of acetylcholin-esterase from Torpedo californica: a prototypic acetylcholine-binding protein. Science 253, 872-879.
49. Tang, Z. H. & Cammak, S. L. 1990 Acetylcholinesterase activity in organophosphorus and carbamate resistant and susceptible strains of the Culex pipiens complex. Pestic. Biochem. Physiol. 37, 192-199.
50. Thompson, M., Steichen, J. C. & ffrench-Constant, R. H. 1993 Conservation of cyclodiene insecticide resistance associated mutations in insects. Insect Molec. Biol. 2, 149-154.
51. Vais, H., Williamson, M. S., Hick, C. A., Eldursi, N., Devonshire, A. L. & Usherwood, P. N. R. 1997 Functional analysis of a rat sodium channel carrying a mutation for insect knock-down resistance (kdr) to pyrethroids. FEBS Lett. 413, 327-332.
52. Vaughan, A., Rocheleau, T. & ffrench-Constant, R. 1997 Site-directed mutagenesis of an acetylcholinesterase gene from the yellow fever mosquito Aedes aegypti confers insecticide insensitivity. Expl Parasitol. 87, 237-244.
53. Vaughan, A., Chadee, D. D. & ffrench-Constant, R. 1998 Biochemical monitoring of organophosphorous and carbamate insecticide resistance in Aedes aegypti mosquitoes from Trinidad. Med. Vet. Entomol. 12, 318-321.
54. Wang, Q., Shen, J., Li, Z., Timothy, K., Vincent, G. M., Priori, S. G., Schwartz, P. J. & Keating, M. T. 1995 Cardiac sodium channel mutations in patients with long QT syndrome, an inherited cardiac arrhythmia. Hum. Molec. Genet. 4, 1603-1607.
55. Williamson, M. S., Denholm, I., Bell, C. A. & Devonshire, A. L. 1993 Knockdown resistance (kdr) to DDT and pyrethroid insecticides maps to a sodium channel gene locus in the housefly (Musca domestica). Molec. Gen. Genet. 240, 17-22.
56. Williamson, M. S., Martinez-Torres, D., Hick, C. A. & Devonshire, A. L. 1996 Identification of mutations in the housefly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Molec. Gen. Genet. 252, 51-60.
57. Wilson, T. G. 1988 Drosophila melanogaster (Diptera: Drosophilidae): a model insect for insecticide resistance studies. J. Econ. Entomol. 81, 22-27.
58. Yang, N., Ji, J., Zhou, M., Ptacek, L. J., Barchi, R. L., Horn, R. & George, A. L. 1994 Sodium channel mutations in paramyotonia congenita exhibit similar biophysical phenotypes in vitro. Proc. Natn. Acad. Sci. USA 91, 12785-12789.
59. Zhang, H.-G., ffrench-Constant, R. H. & Jackson, M. B. 1994 A unique amino acid of the Drosophila GABA receptor with influence on drug sensitivity by two mechanisms. J. Physiol. 479, 65-75.
60. Zhang, H.-G., Lee, H.-J., Rocheleau, T., ffrench-Constant, R. H. & Jackson, M. B. 1995 Subunit composition determines picrotoxin and bicuculline sensitivity of Drosophila GABA receptors. Molec. Pharmacol. 48, 835-840.
61. Zhu, K. Y. & Clark, J. M. 1997 Validation of a point mutation of acetylcholinesterase in Colorado potato beetle by polymerase chain reaction coupled to enzyme inhibition assay. Pestic. Biochem. Physiol. 57, 28-35.