Biochemical characterization of two distinct acetylcholinesterases possessing almost identical catalytic activity in the damselfly Vestalis gracilis

Journal of Asia-Pacific Entomology

Volumn 16, Issue 4, 2013, Pages 465-471

  Kim, Young Ho ^a   Kwon, Deok Ho ^a   Lee, Si Hyeock ^a,b  

^a Seoul National University   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

Acetylcholinesterase; Catalytic activity; Evolution; Neuronal function; Non neuronal function; Vestalis gracilis

Indexed keywords

EID: 84882748688     PISSN: 12268615     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aspen.2013.06.007     Document Type: Article

References (42)

1. Alon M., Alon F., Nauen R., Morin S. Organophosphates resistance in the B-biotype of Bemisia tabaci (Hemiptera: Aleyrodidae) is associated with a point mutation in an ace1-type acetylcholinesterase and overexpression of carboxylesterase. Insect Biochem. Mol. Biol. 2008, 38:940-949.
2. Arpagaus M., Fournier D., Toutant J.P. Analysis of acetylcholinesterase molecular-forms during the development of Drosophila melanogaster - evidence for the existence of an amphiphilic monomer. Insect Biochem. 1988, 18:539-549.
3. Badiou A., Brunet J.L., Belzunces L.P. Existence of two membrane-bound acetylcholinesterases in the honey bee head. Arch. Insect Biochem. Physiol. 2007, 66:122-134.
4. Baek J.H., Kim J.I., Lee D.W., Chung B.K., Miyata T., Lee S.H. Identification and characterization of ace1-type acetylcholine sterase likely associated with organophosphate resistance in Plutella xylostella. Pestic. Biochem. Physiol. 2005, 81:164-175.
5. Fournier D., Cuany A., Bride J.M., Berge J.B. Molecular polymorphism of head acetylcholinesterase from adult houseflies (Musca domestica L.). J. Neurochem. 1987, 49:1455-1461.
6. Fournier D., Berge J.B., Dealmeida M.L.C., Bordier C. Acetylcholinesterases from Musca domestica and Drosophila melanogaster brain are linked to membranes by a glycophospholipid anchor sensitive to an endogenous phospholipase. J. Neurochem. 1988, 50:1158-1163.
7. Fournier D., Bride J.M., Karch F., Berge J.B. Acetylcholinesterase from Drosophila melanogaster - identification of 2 subunits encoded by the same gene. FEBS Lett. 1988, 238:333-337.
8. Gao J.R., Kambhampati S., Zhu K.Y. Molecular cloning and characterization of a greenbug (Schizaphis graminum) cDNA encoding acetylcholinesterase possibly evolved from a duplicate gene lineage. Insect Biochem. Mol. Biol. 2002, 32:765-775.
9. Gnagey A.L., Forte M., Rosenberry T.L. Isolation and characterization of acetylcholinesterase from Drosophila. J. Biol. Chem. 1987, 262:13290-13298.
10. Haas R., Marshall T.L., Rosenberry T.L. Drosophila acetylcholinesterase - demonstration of a glycoinositol phospholipid anchor and an endogenous proteolytic cleavage. Biochemistry 1988, 27:6453-6457.
11. Huchard E., Martinez M., Alout H., Douzery E.J.P., Lutfalla G., Berthomieu A., Berticat C., Raymond M., Weill M. Acetylcholinesterase genes within the Diptera: takeover and loss in true flies. Proc. R. Soc. B 2006, 273:2595-2604.
12. Incardona J.P., Rosenberry T.L. Construction and characterization of secreted and chimeric transmembrane forms of Drosophila acetylcholinesterase: a large truncation of the C-terminal signal peptide does not eliminate glycoinositol phospholipid anchoring. Mol. Biol. Cell 1996, 7:595-611.
13. Jiang X.J., Qu M.J., Denholm I., Fang J.C., Jiang W.H., Han Z.J. Mutation in acetylcholinesterase1 associated with triazophos resistance in rice stem borer, Chilo suppressalis (Lepidoptera: Pyralidae). Biochem. Biophys. Res. Commun. 2009, 378:269-272.
14. Kang J.S., Lee D.W., Koh Y.H., Lee S.H. A soluble acetylcholinesterase provides chemical defense against xenobiotics in the pinewood nematode. PLoS One 2011, 6:e19063.
15. Kim Y.H., Lee S.H. Which acetylcholinesterase functions as the main catalytic enzyme in the Class Insecta?. Insect Biochem. Mol. Biol. 2013, 43:47-53.
16. Kim J.I., Jung C.S., Koh Y.H., Lee S.H. Molecular, biochemical and histochemical characterization of two acetylcholinesterase cDNAs from the German cockroach Blattella germanica. Insect Mol. Biol. 2006, 15:513-522.
17. Kim Y.H., Choi J.Y., Je Y.H., Koh Y.H., Lee S.H. Functional analysis and molecular characterization of two acetylcholinesterases from the German cockroach, Blattella germanica. Insect Mol. Biol. 2010, 19:765-776.
18. Kim Y.H., Cha D.J., Jung J.W., Kwon H.W., Lee S.H. Molecular and kinetic properties of two acetylcholinesterases from the Western honey bee, Apis mellifera. PLoS One 2012, 7:e48838.
19. Lee D.W., Kim S.S., Shin S.W., Kim W.T., Boo K.S. Molecular characterization of two acetylcholinesterase genes from the oriental tobacco budworm, Helicoverpa assulta (Guenee). Biochim. Biophys. Acta 2006, 1760:125-133.
20. Lee S.W., Kasai S., Komagata O., Kobayashi M., Agui N., Kono Y., Tomita T. Molecular characterization of two acetylcholinesterase cDNAs in Pediculus human lice. J. Med. Entomol. 2007, 44:72-79.
21. Lewis P.R., Shute C.C.D. The distribution of cholinesterase in cholinergic neurons demonstrated with electron microscope. J. Cell Sci. 1966, 1:381-390.
22. Li F., Han Z.J. Purification and characterization of acetylcholinesterase from cotton aphid (Aphis gossypii Glover). Arch. Insect Biochem. 2002, 51:37-45.
23. Lu Y.H., Pang Y.P., Park Y., Gao X.W., Yao J.X., Zhang X., Zhu K.Y. Genome organization, phylogenies, expression patterns, and three-dimensional protein models of two acetylcholinesterase genes from the red flour beetle. PLoS One 2012, 7:e32288.
24. Lu Y.H., Park Y., Gao X.W., Zhang X., Yao J.X., Pang Y.P., Jiang H.B., Zhu K.Y. Cholinergic and non-cholinergic functions of two acetylcholinesterase genes revealed by gene-silencing in Tribolium castaneum. Sci. Rep. 2012, 2. 10.1038/srep00288.
25. Malcolm C.A., Bourguet D., Ascolillo A., Rooker S.J., Garvey C.F., Hall L.M., Pasteur N., Raymond M. A sex-linked Ace gene, not linked to insensitive acetylcholinesterase-mediated insecticide resistance in Culex pipiens. Insect Mol. Biol. 1998, 7:107-120.
26. Massoulie J., Bon S. The molecular forms of cholinesterase and acetylcholinesterase in vertebrates. Annu. Rev. Neurosci. 1982, 5:57-106.
27. Massoulie J., Pezzementi L., Bon S., Krejci E., Vallette F.M. Molecular and cellular biology of cholinesterases. Prog. Neurobiol. 1993, 41:31-91.
28. Mori A., Tomita T., Hidoh O., Kono Y., Severson D.W. Comparative linkage map development and identification of an autosomal locus for insensitive acetylcholinesterase-mediated insecticide resistance in Culex tritaeniorhynchus. Insect Mol. Biol. 2001, 10:197-203.
29. Mutero A., Fournier D. Post-translational modifications of Drosophila acetylcholinesterase. In vitro mutagenesis and expression in Xenopus oocytes. J. Biol. Chem. 1992, 267:1695-1700.
30. Nabeshima T., Kozaki T., Tomita T., Kono Y. An amino acid substitution on the second acetylcholinesterase in the pirimicarb-resistant strains of the peach potato aphid, Myzus persicae. Biochem. Biophys. Res. Commun. 2003, 307:15-22.
31. Nabeshima T., Mori A., Kozaki T., Iwata Y., Hidoh O., Harada S., Kasai S., Severson D.W., Kono Y., Tomita T. An amino acid substitution attributable to insecticide-insensitivity of acetylcholinesterase in a Japanese encephalitis vector mosquito, Culex tritaeniorhynchus. Biochem. Biophys. Res. Commun. 2004, 313:794-801.
32. Oh S.H., Kozaki T., Mizuno H., Tomita T., Kono Y. Expression of Ace-paralogous acetylcholinesterase of Culex tritaeniorhynchus with an amino acid substitution conferring insecticide insensitivity in baculovirus-insect cell system. Pestic. Biochem. Physiol. 2006, 85:46-51.
33. Perrier A., Cousin X., Boschetti N., Haas R., Chatel J.M., Bon S., Roberts W.L., Pickett S.R., Massoulie J., Rosenberry T.L., Krejci E. Two distinct proteins are associated with tetrameric acetylcholinesterase on the cell surface. J. Biol. Chem. 2000, 275:34260-34265.
34. Pezzementi L., Chatonnet A. Evolution of cholinesterases in the animal kingdom. Chem. Biol. Interact. 2010, 187:27-33.
35. Russell R.J., Claudianos C., Campbell P.M., Horne I., Sutherland T.D., Oakeshott J.G. Two major classes of target site insensitivity mutations confer resistance to organophosphate and carbamate insecticides. Pestic. Biochem. Physiol. 2004, 79:84-93.
36. Seong K.M., Kim Y.H., Kwon D.H., Lee S.H. Identification and characterization of three cholinesterases from the common bed bug, Cimex lectularius. Insect Mol. Biol. 2012, 21:149-159.
37. Shang J.Y., Shao Y.M., Lang G.J., Yuan G., Tang Z.H., Zhang C.X. Expression of two types of acetylcholinesterase gene from the silkworm, Bombyx mori, in insect cells. Insect Sci. 2007, 14:443-449.
38. Toutant J.P. Insect acetylcholinesterase - catalytic properties, tissue distribution and molecular-forms. Prog. Neurobiol. 1989, 32:423-446.
39. Toutant J.P., Arpagaus M., Fournier D. Native molecular forms of head acetylcholinesterase from adult Drosophila melanogaster: quaternary structure and hydrophobic character. J. Neurochem. 1988, 50:209-218.
40. Weill M., Fort P., Berthomieu A., Dubois M.P., Pasteur N., Raymond M. A novel acetylcholinesterase gene in mosquitoes codes for the insecticide target and is non-homologous to the ace gene in Drosophila. Proc. Biol. Sci. 2002, 269:2007-2016.
41. Weill M., Lutfalla G., Mogensen K., Chandre F., Berthomieu A., Berticat C., Pasteur N., Philips A., Fort P., Raymond M. Insecticide resistance in mosquito vectors. Nature 2003, 423:136-137.
42. Zador E. Tissue specific expression of the acetylcholinesterase gene in Drosophila melanogaster. Mol. Gen. Genet. 1989, 218:487-490.