Carboxyl/cholinesterases: A case study of the evolution of a successful multigene family

BioEssays

Volumn 21, Issue 12, 1999, Pages 1031-1042

  Oakeshott, J G ^a   Claudianos, C ^a   Russell, R J ^a   Robin, G C ^a  

^a CSIRO   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0033486287     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1521-1878(199912)22:1<1031::AID-BIES7>3.0.CO;2-J     Document Type: Review

References (76)

1. Chothia C. Protein families in the metazoan genome. In: Akam M, Holland P, Ingram P, Wray G, editors. Development supplement: The evolution of developmental mechanisms. Cambridge: The Company of Biologists Limited; 1994. p 27-33.
2. Orengo CA Michie AD, Jones S, Jones DT, Swindells MB, Thornton JM. CATH - a hierarchic classification of protein domain structures. Structure 1997;5:1093-1108.
3. Zschunke F, Salmassi A, Kreipe H, Buck F, Parwaresch MR, Radzun HJ. cDNA cloning and characterization of human monocyte/macrophage serine esterase-1. Blood 1991;78:506-512.
4. Cygler M, Schrag JD, Ergan F. Advances in structural understanding of lipases. Biotech Genet Eng Rev 1992;10:143-184
5. Benning MM, Kuo JM, Raushel FM, Holden HM. Three dimensional structure of the binuclear metal center of phosphotriesterase. Biochemistry 1995;34:7973-7978.
6. Ollis DL, Cheah E, Cygler M, Dijkstra B, Frolow F, Franken SM, Harel M, Remington SJ, Silman I, Schrag J, Sussman JL, Verschueren KHG, Goldman A. The α/β hydrolase fold. Protein Eng 1992;5:197-211.
7. Oakeshott JG, van Papenrecht EA, Boyce TM, Healy MJ, Russell RJ. Evolutionary genetics of Drosophila esterases. Genetica 1993;90:239-268.
8. Hermila H, Koivula TT, Palva I. Hormone-sensitive lipase is closely related to several bacterial proteins, and distantly related to acetylcholinesterase and lipoprotem lipase: identification of a superfamily of esterases and lipases. Biochem Biophys Acta 1994;1210 249-253.
9. Cygler M, Schrag JD, Sussman JC, Harel M, Silman I, Gentry MK, Doctor BP. Relationship between sequence conservation and three dimensional structure in a large family of esterases, lipases and related proteins. Protein Sci 1993;2:366-382.
10. Sussman JL, Harel M, Frolow F, Oefner C, Goldman A, Toker L, Silman I. Atomic structure of acetylcholinesterase from Torpedo californica: A prototypic acetylcholine-binding protein. Science 1991;253:872-879.
11. Grochulski P, Li Y, Schrag JD, Bouthillier F, Smith R, Harrison D, Rubin B, Cygler M. Insights into interfacial activation from an open structure of Candida rugosa lipase. J Biol Chem 1993;268 12843-12847.
12. Taylor P, Radic Z. The cholinesterases: from genes to proteins. Annu Rev Pharmacol Toxicol 1994;34:281-320.
13. Maxwell DM, Brecht K, Saxena A, Feaster S, Doctor BP. Comparisons of cholinesterases and carboxylesterase as bioscavengers for organophosphorus compounds. In: Doctor BP, Taylor P, Quinn DM, Rotundo RL, Gentry MK, editors. Structure and function of cholinesterases and related proteins. New York Plenum Press: 1998. p 387-392.
14. Hortsch M, Patel NH, Bieber AJ, Traquina ZR, Goodman CS. Drosophila neurotactin, a surface glycoprotein with homology to serine esterases, is dynamically expressed during embryogenesis. Development 1990;110: 1327-1340.
15. Auld VJ, Fetter RD, Broadie K, Goodman CS. Gliotactin, a novel transmembrane protein on peripheral glia, is required to form the blood-nerve barrier in Drosophila Cell 1995;81:757-767.
16. Ichtchenko K, Hata Y, Nguyen T, Ullrich B, Missler M, Moomaw C, Sudhof TC. Neuroligin 1: a splice site specific ligand for β-reurexins Cell 1995;81:435-443.
17. Oakeshott JG, Boyce TM, Russell RJ, Healy MJ. Molecular insights into the evolution of an enzyme: esterase 6 in Drosophila. Trends Ecol Evol 1995;1C:103-110.
18. Pohlenz HD, Boidol W, Schuttke I, Streber WR. Purification and properties of an Arthrobacter oxydans P52 carbamate hydrolase specific for the herbicide phenmedipham and nucleotide sequence of the corresponding gene. J Bacteriol 1992;174:6600-6607.
19. Moore JC, Arnold FH. Directed evolution of a para-nitrobenzyl esterase for aqueous-organic solvents. Nature Biotech 1996;14:458-467
20. Talusov RL, Koonin EV, Lipman DJ. A genomic perspective on protein families Science 1997;278:631-637.
21. Klenk HP, Clayton RA, Tomb J, White O, Nelson KE, Ketchum KA, Dodson RJ, Gwinn M, Hickey EK Peterson JD, Richardson DL, Kerlavage AR, Graharr DE, Kyrpides NC, Fleischmann RD, Quackenbush J, Lee NH, Suttor GG, Gill S, Kirkness EF, Dougherty BA, McKenney K Adams MD, Loftus B, Peterson S Reich CI, McNeil NK, Badger JH, Glodek A, Zhou L, Overbeek R, Gocayne JD, Weidman JF, McDonald L, Utterback T, Cotton MD, Spriggs T, Artiach P, Kaine BP, Sykes SM, Sadow PW, D'Andrea KP, Bowman C, Fujii C, Garland SA, Mason TM, Olsen GJ, Fraser CM, Smith HO, Woese CR, Venler JC. The complete genome sequence of the hyperthermophilic sulphate-reducing archaeon Archaeoglobus fulgidus. Nature (London) 1997;390:364-370.
22. Goffeau A, Barrel BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnson M, Louis EJ, Mewes HW, Murakami Y, Philippsen P, Tettelin H, Oliver SG. Life with 6000 genes. Science 1996;274:563-567.
23. Lotti M, Grandon R, Fusetti F, Longhi S, Brocca S, Tramonlano A, Alberghina L. Cloning and analysis of Candida cylandracea lipase sequences. Gene 1993;124:45-55.
24. Bomblies L, Biegelmann E, Doring V, Gerisch G, Krafft-Czepa H, Noegel AA, Schliecher M, Humbel BM. Membrane-enclosed crystals in Dictyostelium discoideum cells consisting of developmentally regulated proteins with sequence similarities to known esterases. J Cell Biol 1990;110:669-679.
25. Baudouin E, Charpenteau M, Roby D, Marco Y, Ranjeva R, Ranty B. Functional expression of a tobacco gene related to the serine hydrolase family esterase activity towards short-chain dinitrophenyl acyesters. Eur J Biochem 1997;248:700-706.
26. Arpagaus M, Combes D, Culetto E, Grauso M, Fedon Y, Romani R, Toutant JP Four acetylcholinesterase genes in the nematode Caenorhabditis elegans. J Physiol Paris 1998;92:363-367.
27. Waterston R, Sulston J. The genome of Caenorhabditis elegans. Proc Nat Acad Sci USA 1995;92:10836-10840.
28. Oakeshott JG, Claudianos C, Campbell PM, Robin GC, Newcomo RA, Odgers WA, Harcourt RL, Russell RJ. Molecular basis of esterase-mediated OP resistance in two higher Diptera. In: Doctor BP, Taylor P, Quinn DM, Rotundo RL, Gentry MK. editors. Structure and function of cholinesterases and related proteins. New York: Plenum Press; 1998. p 497-502.
29. Satoh T, Hosokawa M. The mammalian carboxylesterases: from molecules to functions. Annu Rev Pharmacol Toxicol 1998;38:257-288.
30. Doolittle RF, Feng D-F, Tsang S, Cho G, Little E Determining divergence times of the major kingdoms of living organisms with a protein clock Science 1996;271:470-477.
31. Devonshire AL, Field LM. Gene amplification and insecticide resistance. Annu Rev Entomol 1991;36:1-23.
32. Brady JP, Richmond RC An evolutionary model for the duplication and divergence of esterase genes in Drosophila. J Molec Evo: 1992;34:506-521.
33. Robin GC. The evolution of the alpha-esterase gene cluster of Drosophila. Ph.D. thesis, The Australian National University. 1998.
34. Claudianos C. The evolution of alpha-esterase mediated organophosphate resistance in Musca domestics. Ph.D. thesis, The Australian National University, 1999.
35. Russell RJ, Robin GC, Kostakos P, Newcomb RD, Boyce TM, Medveczky KM, Oakeshott JG. Molecular cloning of an alpha-esterase gene cluster on chromosome 3R of Drosophila melanogaster. Insect Biochem Molec Biol 1996;26:235-247.
36. Robin C, Russell RJ, Medveczky KM, Oakeshott JG. Duplication and divergence of the genes of the alpha-esterase cluster of Drosophila melanogaster. J Molec Evol 1996;43:241-252.
37. Spackman ME, Oakeshott JG, Smyth K-A, Medveczky KM, Russell RJ. A cluster of esterase genes on chromosome 3R of Orosophila melanogaster includes homologues of esterase genes conferring insecticide resistance in Lucilia cuprina Biochem Genet 1994;32:39-62.
38. Batterham P, Davies AG, Game AY, McKenzie JA. Assymetry - where evolutionary and developmental genetics meet. BioEssays 1996;18:841-845.
39. Healy MJ, Dumancic MM, Oakeshott JG. Biochemical and physiological studies of soluble esterases from Drosophila melanogaster. Biochem Genet 1991;29:365-388.
40. Newcomb RD, East PD, Russell RJ, Oakeshott JG. Isolation of α-cluster esterases associated with organophosphate resistance in Lucilia cuprina. Insect Molec Biol 1996;5:211-216.
41. Powell JR, De Salle R. Drosophila molecular phylogenies and their uses In: Hecht MK, MacIntyre RJ, Clegg MT, editors. Evolutionary biology, Vol 28. New York: Plenum Press: 1995. p 87-138.
42. Petrov DA, Lozovskaya ER, Hartl DL. High instrinsic rate of DNA loss in Drosophila. Nature (London) 1996;384:346-349.
43. Petrov DA, Hartl DL. High rate of DNA loss in Drosophila melanogaster and Drosophila virilis species groups. Molec Biol Evol 1998;15:293-302.
44. Collet C, Nielsen KM, Russell RJ, Karl M, Oakeshott JG, Richmond RC. Molecular analysis of duplicated esterase genes in Drosophila melanogaster. Molec Biol Evol 1990;7:9-28.
45. Dumancic MM, Oakeshott JG, Russell RJ, Healy MJ. Characterisation of the ESTP protein in Drosophila melanogaster and its conservation in Drosophilids. Biochem Genet 1997;35:251-271.
46. Ludwig MZ, Tamarina NA, Richmond RC. Localization of sequences controlling the spatal, temporal, and sex-specific expression of the esterase 6 locus in Drosophila melanogaster adults. Proc Natl Acad Sci USA 1993;90:6233-6237.
47. Korochkin L, Ludwig M, Tamarina N, Uspensky I, Yenikolopov G, Khechumijan R, Kopantseva M, Evgeniev M, Kuzin B, Bakayeva T, Mudjoian L, Malevantschuk O, Tsatyian V, Ivanov A, Lukianov S. Molecular genetic mechanisms of tissue-specific esterase isozymes and protein expression in Drosophila. In: Markert C, Scandalios J, editors. Isozymes: structure, function and use in biology and medicine. New York: Wiley-Liss: 1990. p 399-440.
48. East PD, Graham A, Whitington G. Molecular isolation and preliminary characterisation of a duplicated esterase locus in Drosophila buzzatii. In: Barker JSF, Starmer WT, MacIntyre R, editors. Ecological and evolutionary genetics of Drosophila. New York: Plenum Press; 1990. p 389-406.
49. van Papenrecht EA, Nucleotide and functional divergence in esterase 6 amongst sibling species of Drosophila. Ph.D. thesis. The Australian National University, 1995.
50. Myers MA, Healy MJ, Oakeshott JG. Mutational analysis of N-linked glycosylation of esterase 6 in Drosophila melanogaster. Biochem Genet 1996;34:201-218.
51. Qiao C-L, Raymond M. The same esterase B1 haplotype is amplified in insecticide-resistant mosquitoes of the Culex pipiens complex from the Americas and China. Heredity 1995;74:339-345.
52. Field LM, Devonshire AL. Evidence that the E4 and FE4 esterase genes responsible for insecticide resistance in the aphid Myzus persicae (Sulzer) are part of a gene family. Biochem J 1998;330:169-173.
53. Vaughan A, Rocheleau T, ffrench-Constant R. Site-directed mutagenesis of an acetylcholinesterase gene from the yellow fever mosquito Aedes aegypti confers insecticide insensitivity. Exp Parasitol 1997;87:237-244.
54. Devonshire AL, Byrne FJ, Moores GD, Williamson MS. Biochemical and molecular characterisation of insecticide insensitive acetylcholinesterase in resistant insects. In: Doctor BP, Quinn DM, Rotundo RL, Taylor P, editors. Structure and function of cholinesterases and related proteins New York: Plenum Press; 1998. p 489-494.
55. Mutero A, Pralavoria M, Bride J-M, Fournier D. Resistance-associated point mutations in insecticide-insensitive acetylcholinesterase. Proc Natl Acad Sci USA 1994;91:5922-5926.
56. Newcomb RD, Campbell PM, Ollis DL, Cheah E, Russell RJ, Oakeshott JG. A single amino acid substitution converts a carboxylesterase to an organophosphorus hydrolase and confers insecticide resistance on a blowfly. Proc Natl Acad Sci USA 1997;94:7464-7468.
57. Campbell PM, Newcomb RD, Russell RJ, Oakeshott JG. Two different amino acid substitutions in the ali-esterase, E3, confer alternative types of organophosphorus insecticide resistance in the sheep blowfly, Lucilia cuprina. Insect Biochem Molec Biol 1998;28:139-150.
58. Moore JC, Jin HM, Kirchner O, Arnold FH. Strategies for the in vitro evolution of protein function: enzyme evolution by random recombination of improved sequences. J Mo ec Biol 1997;272:336-347.
59. Cooke PH, Oakeshott JG. Amino acid polymorphisms for esterase 6 in Drosophila melanogaster. Proc Natl Acad Sci USA 1989;86:1426-1430.
60. Odgers WA, Healy MJ, Oakeshott JG. Nucleotide polymorphism in the 5′ promoter region of esterase 6 in Drosophila melanogaster and its relationship to enzyme activity variation. Genetics 1995;141:215-222.
61. Odgers WA. Molecular bases of esterase 6 regulatory variation in Drosophila melanogaster. Ph.D. thesis, The Australian National University, 1995.
62. Dickinson WJ. On the architecture of regulatory systems: Evolutionary insights and implications. BioEssays 1988;8:204-208.
63. Balakirev ES, Ayala FJ. Is esterase-P encoded by a cryptic pseudogene in Drosophila melanogaster? Genetics 1996;144:1511-1518.
64. Hammock BD. Regulation of juvenile hormone litre: degradation. In: Kerkut GA, Gilbert LI, editors. Comprehensive insect physiology, biochemistry and pharmacology. New York: Liss. 1985: p 315-328.
65. Vogt RG, Riddiford LM, Prestwich GD. Kinetic properties of a sex pheromone-degrading enzyme: the sensiliar esterase of Antheraea polyphemus. Proc Natl Acad Sci USA 1985;82:8827-8831.
66. Gould SJ. Tempo and mode in the macroevolutionary reconstruction of Darwinism. Proc Natl Acad Sci USA 1994;91:6764-6771.
67. Fitch WM, Ayala FJ. The superoxide dismutase molecular clock revisited. Proc Natl Acad Sci USA 1994;91:6802-6807.
68. Miyamoto MM, Fitch WM. Testing the covarion hypothesis of molecular evolution. Molec Biol Evol 1995;12:503-513.
69. Hugnes AL. The evolution of functionally novel proteins after gene duplication. Proc Roy Soc London (Biol) 1994;256:119-124.
70. Sonnhammer EL, Eddy SR, Birney E, Bateman A, Durbin R. Pfam: multiple sequence alignments and HMM-profiles of protein domains. Nucleic Acids Res 1998;26:320-322.
71. Devereux J, Haeberli P, Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 1994;12:387-95.
72. Swofford DL, PAUP: phylogenetic analysis using parsimony. Version 4.0D64. Illinois Natural History Survey, Champaign, IL, 1998.
73. Shimada Y, Sugihara A, Iizumi T, Tominaga Y, cDNA cloning and characterisation of Geotrichum candidum lipase II. J Biochem 1990;107: 703-707.
74. Zorio DA, Cheng NN, Blumenthal T, Spieth J. Operons as a common form of chromosomal organization in C. elegans. Nature (London) 1994;372: 270-272.
75. Kennedy BP, Aamodt EJ, Allen FL, Chung MA, Heschl MFP, McGhee JD. The gul esterase gene (ges-1) from the nematodes Caenorhabditis elegans and Caenorhabditis briggsae. J Molec Biol 1993;229:890-908.
76. Fedon Y, Cousin X, Toutant JP, Thierry-Mieg D, Arpagaus M. cDNA sequence, gene structure, and cholmesterase-like domains of an esterase from Caenorhabditis elegans mapped to chromosome V. DNA Seq 1993;3:347-356.