Inactivation of an invertebrate acetylcholinesterase by sulfhydryl reagents: The roles of two cysteines in the catalytic gorge of the enzyme

Invertebrate Neuroscience

Volumn 6, Issue 2, 2006, Pages 47-55

  Pezzementi, Leo ^a   Rowland, Melissa ^a   Wolfe, Matthew ^a   Tsigelny, Igor ^b  

^a BIRMINGHAM SOUTHERN COLLEGE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acetylcholinesterase; Amphioxus; Aphids; Cysteine; Sulfhydryl reagents

Indexed keywords

5,5' DITHIOBIS(2 NITROBENZOIC ACID); ACETYLCHOLINESTERASE; CYSTEINE; LIGAND; N ETHYLMALEIMIDE; PROPIDIUM IODIDE; THIOL DERIVATIVE;

ALLOSTERISM; APHID; ARTICLE; CATALYSIS; ENZYME INACTIVATION; MUTANT; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS;

AMPHIBIAN PROTEINS; ANIMALS; CATALYTIC DOMAIN; CERCOPITHECUS AETHIOPS; CHOLINESTERASE INHIBITORS; CHOLINESTERASES; COS CELLS; CYSTEINE; DITHIONITROBENZOIC ACID; ENZYME ACTIVATION; ETHYLMALEIMIDE; INHIBITORY CONCENTRATION 50; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; SEQUENCE ALIGNMENT; SULFHYDRYL REAGENTS; TIME FACTORS; TRANSFECTION;

EID: 33745033541     PISSN: 13542516     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10158-006-0017-z     Document Type: Article

References (37)

1. Ariel N, Ordentlich A, Barak D, Bino T, Velan B, Shafferman A (1998) The 'aromatic patch' of three proximal residues in the human acetylcholinesterase active centre allows for versatile interaction modes with inhibitors. Biochem J 335:95-102
2. Bourne Y, Taylor P, Bougis PE, Marchot P (1999) Crystal structure of mouse acetylcholinesterase. J Biol Chem 274:2963-2970
3. Brestkin AP, Maizel EB, Moralev SN, Novozhilov KV, Sazonova IN (1985) Isolation, partial purification and some properties of cholinesterases from spring grain aphid Schizaphis gramina (Rond.). Insect Biochem 15:309-314
4. Changeux J-P (1966) Responses of acetylcholinesterase from Torpedo marmorata to salts and curarizing drugs. Mol Pharmacol 2:369-392
5. Doctor BP, Toker L, Roth E, Silman I (1987) Microtiter assay for acetylcholinesterase. Anal Biochem 166:399-403
6. Dolginova EA, Roth E, Silman I, Weiner LM (1992) Chemical modification of Torpedo acetylcholinesterase by disulfides: appearance of a "molten globule" state. Biochemistry 31:12248-12254
7. Ellman GL, Courtney DK, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88-95
8. Gibney G, Taylor P (1990) Biosynthesis of Torpedo acetylcholinesterase in mammalian cells: functional expression and mutagenesis of the glycophospholipid-anchored form. J Biol Chem 265:12576-12583
9. Gao JR, Kambhampati S, Zhu KY (2002) Molecular cloning and characterization of a greenbug (Schizaphis graminum) cDNA encoding acetylcholinesterase possibly evolved from a dupliate gene lineage. Insect Biochem Mol Biol 32:765-775
10. Harel M, Sussman JL, Krejci E, Bon S, Chanal P, Massoulié J, Silman I (1992) Conversion of acetylcholinesterase to butyrylcholinesterase: modeling and mutagenesis. Proc Natl Acad Sci USA 89:10827-10831
11. Harel M, Kryger G, Rosenberry TL, Mallender WD, Lewis T, Fletcher RJ, Guss JM, Silman I, Sussman JL (2000) Three-dimensional structures of Drosophila melanogaster acetylcholinesterase and of its complexes with two potent inhibitors. Protein Sci 9:1063-1072
12. Kaplan D, Ordentlich A, Barak D, Ariel N, Kronman C, Velan D, Shafferman A (2001) Does "butyrylization" of acetylcholinesterase through substitution of the six divergent aromatic amino acids in the active center gorge generate an enzyme mimic of butyrylcholinesterase? Biochemistry 40:7433-7445
13. Kryger G, Harel M, Giles K, Toker L, Velan G, Lazar A, Kronman C, Barak D, Ariel N, Shafferman A, Silman I, Sussman JL (2000) Structures of recombinant native and E303Q mutant human acetylcholinesterase complexed with the snake-venom toxin fasciculin-II. Acta Crystallogr D Biol Crystallogr 56:1385-1394
14. Li F, Han ZJ (2002) Two different genes encoding acetylcholinesterase existing in cotton aphid (Aphis gossypii). Genome 45:1134-1141
15. Manulis S, Ishaaya I, Perry AS (1981) Acetylcholinesterase of Aphis citricola: properties and significance in determining toxicity of systemic organophosphorus and carbamate compounds. Pest Biochem Physio 15:267-274
16. Massoulié J, Pezzementi L, Bon S, Krejci E, Vallette F-M (1993) Molecular and cellular biology of cholinesterases. Prog Neurobiol 41:31-91
17. McClellan JS, Coblentz WB, Sapp M, Rulewicz G, Gaines DI, Hawkins A, Ozment C, Bearden A, Merritt S, Cunningham J, Palmer E, Contractor A, Pezzementi L (1998) cDNA cloning, in vitro expression, and biochemical characterization of cholinesterase 1 and cholinesterase 2 from amphioxus: comparison with cholinesterase 1 and cholinesterase 2 produced in vivo. Eur J Biochem 258:419-429
18. Moralev SN, Rozengart E (2006) Comparative enzymology of cholinesterases. Intern Univ Line, La Jolla (in press)
19. Morel N, Bon S, Greenblatt M, van Belle D, Wodak SJ, Sussman JL, Massoulié J, Silman I (1999) Effect of mutations within the peripheral anionic site on the stability of acetylcholinesterase. Molec Pharmacol 55:982-992
20. Nabeshima T, Toshinori K, Takashi T, Kono Y (2003) An amino acid substitution on the second acetylcholinesterase in the primicarb-resistant strains of the peach potato aphid, Myzus persicae. Biochem Biophys Res Commun 307:15-22
21. Novoshilov KV, Brestkin AP, Khovanskikh AE, Maizel EB, Moralev SN, Nikanorova EV, Sazonova IN (1989) Cholinesterases of aphids - III. Sensitivity of acetylcholinesterases to several inhibitors as a possible phylogenetic character. Insect Biochem 19:15-18
22. Pezzementi L, Sutherland D, Sanders M, Soong W, Milner D, McClellan JS, Sapp M, Coblentz WB, Rulewicz G, Merritt S (1998) Structure and function of cholinesterases from agnathans and cephalochordates: implications for the evolution of cholinesterases. In: Doctor BP, Taylor P, Quinn DM, Rotundo RL, Gentry MK (eds) Structure and function of cholinesterases and related proteins. Plenum, London, pp 105-110
23. Pezzementi L, Johnson K, Tsigelny I, Cotney J, Manning E, Barker A, Merritt S (2003) Amino acids defining the acyl pocket of an invertebrate cholinesterase. Comp Biochem Physiol B 136:813-832
24. Ordentlich A, Barak D, Kronman C, Flashner Y, Leitner M, Segall Y, Ariel N, Cohen S, Velan B, Shafferman A (1993) Dissection of the human acetylcholinesterase active center: identification of residues constituting the anionic site, the hydrophobic site, and the acyl pocket. J Biol Chem 268:17083-17095
25. Ordentlich A, Barak D, Kronman C, Ariel N, Segal Y, Velan B, Shafferman A (1995) Contribution of aromatic moieties of tyrosine 133 and of the anionic subsite tryptophan 86 to catalytic efficiency and allosteric modulation of acetylcholinesterase. J Biol Chem 270:2082-2091
26. Radić Z, Pickering NA, Vellom DC, Camp S, Taylor P (1993) Three distinct domains in the cholinesterase molecule confer selectivity for acetyl- and butyrylcholinesterase inhibitors. Biochemistry 32:12074-12084
27. Satoh G, Wang Y, Zhang P, Satoh N (2001) Early development of amphioxus nervous system with special reference to segmental cell organization and putative sensory cell precursors: a study based on the expression of pan-neuronal marker gene Hu/elav. J Exptl Zool 291:354-364
28. Shapira M, Thompson CK, Soreq H, Robinson GE (2001) Changes in neuronal acetylcholinesterase gene expression and division of labor in honey bee colonies. J Mol Neurosci 17:1-12
29. Smissart HR (1976) Reactivity of a critical sufhydryl group of the acetylcholinesterase from aphids (Myzus persicae). Pest Biochem Physiol 6:215-222
30. Steinberg N, Roth E, Silman I (1990) Torpedo acetylcholinesterase is inactivated by thiol reagents. Biochem Int 21:1043-1050
31. Sussman JL, Harel M, Frolow F, Oefner C, Goldman A, Toker L, Silman I (1991) Atomic structure of acetylcholinesterase from Torpedo californica: a prototypic acetylcholine-binding protein. Science 253:872-878
32. Sutherland D, McClellan JS, Milner D, Soong W, Axon N, Sanders M, Hester A, Kao YH, Poczatek T, Routt S, Pezzementi L (1997) Two cholinesterase activities and genes are present in amphioxus. J Exp Zool 277:213-229
33. Taylor P, Radić Z (1994) The cholinesterases: from genes to proteins. Annu Rev Pharmacol Toxicol 34:281-320
34. Vellom DC, Radić Z, Li Y, Pickering NA, Camp S, Taylor P (1993) Amino acid residues controlling acetylcholinesterase and butyrylcholinesterase specificity. Biochemistry 32:12-17
35. Weill M, Fort P, Berthomieu A, Dubois MP, Pasteur N, Raymond M (2002) A novel acetylcholinesterase gene in mosquitoes codes for the insecticide target and is nonhomologous to the ace gene in Drosophila. Proc R Soc Lond B Biol Sci 269:2007-2116
36. Wilson EJ, Massoulié J, Bon S, Rosenberry TL (1996) The rate of thermal inactivation of Torpedo acetylcholinesterase is not reduced in the C231S mutant. FEBS Lett 379:161-164
37. Zahavi M, Tahori AS, Klimer F (1972) An acetylcholinesterase sensitive to sulfhydryl inhibitors. Biochim Biophys Acta 276:577-583