Advertisement

The Use of Cholinesterases in Ecotoxicology

  • Bruno Nunes
Chapter
Part of the Reviews of Environmental Contamination and Toxicology book series (RECT, volume 212)

Abstract

The need for reproducible and accurate biomarkers in Environmental Toxicology has led researchers to implement methods to evaluate the physiological effects caused by contaminants. Such methods are of particular biological importance and ecological interest if they allow the measurement of direct impairment of key endpoints in the test organisms or nontarget species. Neurotransmission impairment via cholinesterase ChE inhibition is the target of two important classes of modern ­pesticides, the ­organophosphates (OPs), and the carbamates (CBs). Because of their extensive use in modern agriculture, these two classes of compounds are widely employed. Metcalfe et al. (2002) estimated for the California Department of Food and Agriculture that the ban from current agricultural use of such compounds would cause the loss of 209,000 jobs and would result in a national economic loss of $17 billion. Therefore, it is not difficult to conclude that these chemical agents will continue to be used, despite the fact that humans and many nontarget organisms are exposed to them (spray drift from crop application, run off from agricultural fields that contaminate adjacent water bodies, residues in food, etc.) (Vermeire et al. 2001).

Keywords

AChE Activity AChE Inhibition Cholinesterasic Activity Exposed Organism Nontarget Species 
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.

Notes

Acknowledgments

The present work was funded by projects “BiOtoMetal” (PTDC/AMB/70431/2006). We would like to acknowledge the contribution of Sérgio Barreira, for his most appreciated scientific comments and chemical expertise.

References

  1. Aamodt S, Konestabo HS, Sverdrup LE, Gudbrandsen M, Reinecke SA, Reinecke AJ, Stenersen J (2007) Recovery of cholinesterase activity in the earthworm Eisenia fetida Savigny following exposure to chlorpyrifos. Environ Toxicol Chem 26(9): 1963–7.Google Scholar
  2. Andersen RA, Aune T, Barstad JAB (1978) Characteristics of cholinesterase of the earthworm Eisenia foetida. Compar Biochem Physiol Part C: Compar Pharmacol 61(1): 81–87.Google Scholar
  3. Arufe MI, Arellano JM, García L, Albendín G, Sarasquete C (2007) Cholinesterase activity in gilthead seabream (Sparus aurata) larvae: characterization and sensitivity to the organophosphate azinphosmethyl. Aquat Toxicol 84: 328–336.Google Scholar
  4. Bain D, Buttemer WA, Astheimer L, Fildes K, Hooper MJ (2004) Effects of sublethal fenitrothion ingestion on cholinesterase inhibition, standard metabolism, thermal preference, and ­prey-capture ability in the Australian central bearded dragon (Pogona vitticeps, Agamidae) Environ Toxicol Chem 23(1): 109–16.Google Scholar
  5. Barata C, Solayan A, Porte C (2004) Role of B-esterases in assessing toxicity of organophosphorus (chlorpyrifos, malathion) and carbamate (carbofuran) pesticides to Daphnia magna. Aquat Toxicol 66: 125–139.Google Scholar
  6. Bonacci S, Corsi I, Focardi S (2009) Cholinesterases in the Antarctic scallop Adamussium colbecki: Characterization and sensitivity to pollutants. Ecotoxicol Environ Saf 72: 1481–1488.Google Scholar
  7. Boschetti N, Brodbeck U (1996) The membrane anchor of mammalian brain acetylcholinesterase consists of a single glycosylated protein of 22 kDa. FEBS Letters 380: 133–136.Google Scholar
  8. Brown M, Davies IM, Moffat CF, Redshaw J, Craft JA (2004) Characterisation of choline esterases and their tissue and subcellular distribution in mussel (Mytilus edulis) Mar Environ Res 57: 155–169.Google Scholar
  9. Caselli F, Gastaldi L, Gambi N, Fabbri E (2006) In vitro characterization of cholinesterases in the earthworm Eisenia andrei. Comp Biochem Physiol, Part C 143: 416–421.Google Scholar
  10. Chebbi SG, David M (2009) Neurobehavioral responses of the freshwater teleost, Cyprinus carpio (Linnaeus.) under quinalphos intoxication. Biotechnol Animal Husband 25(3-4): 241–249.Google Scholar
  11. Choi RCY, Yama SCY, Hui B, Wan DCC, Tsim KWK (1998) Over-expression of acetylcholinesterase stimulates the expression of agrin in NG108–15 cells. Neurosci Lett 248: 17–20.Google Scholar
  12. Chuiko GM (2000) Comparative study of acetylcholinesterase and butyrylcholinesterase in brain and serum of several freshwater fish: specific activities and in vitro inhibition by DDVP, an organophosphorus pesticide. Compar Biochem Physiol, part C Toxicol Pharmacol 127(3): 233–42.Google Scholar
  13. Corsi I, Bonacci S, Santovito G, Chiantore M, Castagnolo L, Focardi S (2004) Cholinesterase activities in the Antartic scallop Adamussium colbecki: tissue expression and effect of ZnCl2 exposure. Mar Environ Res 58: 401–406.Google Scholar
  14. Cunha I, Mangas-Ramirez E, Guilhermino L (2007) Effects of copper and cadmium on cholinesterase and glutathione S-transferase activities of two marine gastropods (Monodonta lineata and Nucella lapillus). Compar Biochem Physiol, Part C 145: 648–657.Google Scholar
  15. Dahm KCS, Rückert C, Tonial EM, Bonan CD (2006) In vitro exposure of heavy metals on nucleotidase and cholinesterase activities from the digestive gland of Helix aspersa. Compar Biochem Physiol, Part C 143: 316–320.Google Scholar
  16. Dauberschmidt C, Dietrich DR, Christian Schlatter C (1997) Esterases in the zebra mussel Dreissena polymorpha: activities, inhibition, and binding to organophosphates. Aquat Toxicol 37(4): 295–305.Google Scholar
  17. Denoyelle R, Rault M, Mazzia C, Mascle O, Capowiez Y (2007) Cholinesterase activity as a biomarker of pesticide exposure in Allolobophora chlorotica earthworms living in apple orchards under different management strategies. Environ Toxicol Chem 26(12): 2644–9.Google Scholar
  18. Deschênes-Furry J, Bélanger G, Perrone-Bizzozero N, Jasmin BJ (2003) Post-transcriptional Regulation of Acetylcholinesterase mRNAs in Nerve Growth Factor-treated PC12 Cells by the RNA-binding Protein HuD. J Biolog Chem 278(8): 5710–5717.Google Scholar
  19. Duquesne S (2006) Effects of an organophosphate on Daphnia magna at suborganismal and organismal levels: Implications for population dynamics. Ecotoxicol Environ Saf 65: 145–150.Google Scholar
  20. Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7: 88–95.Google Scholar
  21. Escartín E, Porte C (1996) Acetylcholinesterase Inhibition in the Crayfish Procambarus clarkii Exposed to Fenitrothion. Ecotoxicolo Environ Saf 34: 160–164.Google Scholar
  22. Eto M (1984) Organophosphorus Pesticides: Organic and Biological Chemistry. Ohio: CRC Press, Inc. 1974.Google Scholar
  23. Falugi C, Amaroli A, Evangelisti V, Viarengo A, Delmonte Corrado MU (2002) Cholinesterase activity and effects of its inhibition by neurotoxic drugs in Dictyostelium discoideum. Chemosphere 48: 407–414.Google Scholar
  24. Ferrari A, Venturino A, Pechén de D’Angelo AM (2007) Muscular and brain cholinesterase sensitivities to azinphos methyl and carbaryl in the juvenile rainbow trout Oncorhynchus mykiss. Compar Biochem Physiol, Part C 146: 308–313.Google Scholar
  25. Forget J, Livet S, Leboulenger F (2002) Partial purification and characterization of ­acetylcholinesterase (AChE) from the estuarine copepod Eurytemora affinis (Poppe). Compar Biochem Physiol Part C 132: 85–92.Google Scholar
  26. Forget J, Bocquené G (1999) Partial purification and enzymatic characterization of acetylcholinesterase from the intertidal marine copepod Tigriopus brevicornis. Compar Biochem Physiol Part B 123: 345–350.Google Scholar
  27. Fournier D, Bride JM, Karch F, Bergé JB (1988) Acetylcholinesterase from Drosophila melanogaster – Identification of two subunits encoded by the same gene. FEBS Letters 238(2): 333–337.Google Scholar
  28. Frasco MF, Fournier D, Carvalho F, Guilhermino L (2006) Cholinesterase from the common prawn (Palaemon serratus) eyes: Catalytic properties and sensitivity to organophosphate and carbamate compounds. Aquat Toxicol 77: 412–421.Google Scholar
  29. Frasco MF, Fournier D, Carvalho F, Guilhermino L (2005) Do metals inhibit acetylcholinesterase (AChE)? Implementation of assay conditions for the use of AChE activity as a biomarker of metal toxicity. Biomarkers 10(5): 360–375.Google Scholar
  30. Fulton MH, Key PB (2001) Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ Toxicol Chem 20: 37–45.Google Scholar
  31. Gambi N, Pasteris A, Fabbri E (2007) Acetylcholinesterase activity in the earthworm Eisenia andrei at different conditions of carbaryl exposure. Compar Biochem Physiol, Part C 145: 678–685.Google Scholar
  32. Gao JR, Zhu KY (2002) Increased expression of an acetylcholinesterase gene may confer organophosphate resistance in the greenbug, Schizaphis graminum (Homoptera: Aphididae). Pesticide Biochem Physiol 73: 164–173.Google Scholar
  33. Garcia LM, Castro B, Ribeiro R, Guilhermino L (2000) Characterization of cholinesterase from guppy (Poecilia reticulata) muscle and its in vitro inhibition by environmental contaminants. Biomarkers 5(4): 274–284.Google Scholar
  34. Giacobini E (2004) Cholinesterase inhibitors: new roles and therapeutic alternatives. Pharmacological Res 50: 433–440.Google Scholar
  35. Gonçalves A, Padrão J, Gonçalves F, Nunes B (2010) In vivo acute effects of several pharmaceutical drugs (diazepam, clofibrate, clofibric acid) and detergents (sodium dodecyl-sulphate and benzalkonium chloride) on cholinesterases from Gambusia holbrooki. Fresenius Environ Bull 19(4): 628–634.Google Scholar
  36. Greene LA, Rukenstein A (1981) Regulation of Acetylcholinesterase Activity by Nerve Growth Factor. J Biolog Chem 256(12): 6363–6367.Google Scholar
  37. Guilhermino L, Lacerda MN, Nogueira AJA, Soares AMVM (2000) In vitro and in vivo inhibition of Daphnia magna acetylcholinesterase by surfactant agents: possible implications for contamination biomonitoring. Sci Tot Env 247: 137–141.Google Scholar
  38. Hai DQ, Ilona Varga Sz, Matkovics B (1997) Organophosphate effects on antioxidant system of carp (Cyprinus carpio) and catfish (Ictalarus nebulosus). Compar Bioch Physiol 117C(1): 83–88.Google Scholar
  39. Iko WM, Archuleta AS, Knopf FL (2003) Plasma cholinesterase levels of mountain plovers (Charadrius montanus) wintering in central California, USA. Environ Toxicol Chem 22(1): 119–25.Google Scholar
  40. Jbilo O, Toutant JP, Vatsis KP, Chatonnet A, Lockridge O (1994) Promoter and Transcription Start Site of Human and Rabbit Butyrylcholinesterase Genes. J Biolog Chem 269(33): 20829–20837.Google Scholar
  41. Jokanovic M (2001) Biotransformation of organophosphorus compounds. Toxicology 166: 139–160.Google Scholar
  42. Jung JH, Addison RF, Shim WJ (2007) Characterization of cholinesterases in marbled sole, Limanda yokohamae, and their inhibition in vitro by the fungicide iprobenfos. Mar Environl Res 63: 471–478Google Scholar
  43. Key PB, Fulton MH (2002) Characterization of cholinesterase activity in tissues of the grass shrimp (Palaemonetes pugio). Pesticide Biochem Physiol 72: 186–192.Google Scholar
  44. Kitz RJ, Braswell LM, Ginsburg S (1970) On the question: is acetylcholinesterase an allosteric protein? Molecular Pharmacol 6: 108–121.Google Scholar
  45. Klumpp D, Humphrey C, King SC (2007) Biomarker responses in coral trout (Plectropomus leopardus) as an indicator of exposure to contaminants in a coral reef environment. Austral J Ecotoxicol 13: 9–17.Google Scholar
  46. Kopecka J, Rybakowas A, Barsiené J, Pempkowiak J (2004) AChE levels in mussels and fish collected off Lithuania and Poland (southern Baltic). Oceanologia 46(3): 405–418.Google Scholar
  47. Kozlovskaya VI, Mayer FL, Menzikova OV, Chuyko GM (1993) Cholinesterases of aquatic animals. Rev Environ Contam Toxicol 132: 117–142.Google Scholar
  48. Kristoff G, Guerrero NR, Cochón AC (2010) Inhibition of cholinesterases and carboxylesterases of two invertebrate species, Biomphalaria glabrata and Lumbriculus variegatus, by the carbamate pesticide carbaryl. Aquat Toxicol 96(2): 115–23.Google Scholar
  49. Laguerre C, Sanchez-Hernandez JC, Köhler HR, Triebskorn R, Capowiez Y, Rault M, Mazzia C (2009) B-type esterases in the snail Xeropicta derbentina: An enzymological analysis to evaluate their use as biomarkers of pesticide exposure. Environ Pollut 157: 199–207.Google Scholar
  50. Leticia AG, Gerardo GB (2008) Determination of esterase activity and characterization of cholinesterases in the reef fish Haemulon plumieri. Ecotoxicol Environm Saf 71: 787–797.Google Scholar
  51. Li M-H (2008) Effects of nonionic and ionic surfactants on survival, oxidative stress, and cholinesterase activity of planarian. Chemosphere 70: 1796–1803Google Scholar
  52. MacGregor JA, Plunkett LM, Youngren SH, Manley A, Plunkett JB, Starr TB (2005) Humans appear no more sensitive than laboratory animals to the inhibition of red blood cell cholinesterase by dichlorvos. Regulatory Toxicol Pharmacol 43: 150–167.Google Scholar
  53. Magnotti RA, Zaino JP, McConnell RS (1994) Pesticide-sensitive fish muscle cholinesterases. Compar Biochem Physiol Part C: Pharmaco, Toxicol Endocrinol 108(2): 187–194.Google Scholar
  54. Mack A, Robitzki A (2000) The key role of butyrylcholinesterase during neurogenesis and neural disorders: an antisense-5′butyrylcholinesterase-DNA study. Progress in Neurobiol 60: 607–628.Google Scholar
  55. Malany S, Baker N, Verweyst N, Medhekar R, Quinn DM, Velan B, Kronman C, Shafferman A (1999) Theoretical and experimental investigations of electrostatic effects on acetylcholinesterase catalysis and inhibition. Chemico-Biolog Interact 119–120: 99–110.Google Scholar
  56. Massoulié J, Perrier N, Noureddine H, Liang D, Bon S (2008) Old and new questions about cholinesterases. Chemico-Biolog Interact 175: 30–44Google Scholar
  57. Massoulié J, Bon S (1982) The molecular forms of cholinesterase and acetylcholinesterase in vertebrates. Ann Rev Neurosci 5: 57–106.Google Scholar
  58. Maul JD, Farris JL (2005) Monitoring exposure of northern cardinals, Cardinalis cardinalis, to cholinesterase-inhibiting pesticides: enzyme activity, reactivations, and indicators of environmental stress. Environ Toxicol Chem 24(7): 1721–30.Google Scholar
  59. McInnes PF, Andersen DE, Hoff DJ, Hooper MJ, Kinkell LL (1996) Monitoring exposure of nestling songbirds to agricultural application of an organophosphorus insecticide using cholinesterase activity. Environ Toxicol Chem 15(4): 544–552.Google Scholar
  60. Melo JB, Agostinho P, Oliveira CR (2003) Involvement of oxidative stress in the enhancement of acetylcholinesterase activity induced by amyloid beta-peptide. Neurosci Res 45: 117–127.Google Scholar
  61. Metcalfe M, McWilliams B, Hueth B, Van Steenwyk R, Sunding D, Swoboda A, Zilberman D (2002) Report: The Economic Importance of Organophosphates in California Agriculture. California Department of Food and Agriculture.Google Scholar
  62. Monteiro M, Quintaneiro C, Morgado F, Soares AMVM, Guilhermino L (2005) Characterization of the cholinesterases present in head tissues of the estuarine fish Pomatoschistus microps: Application to biomonitoring. Ecotoxicol Environ Saf 62: 341–347Google Scholar
  63. Mora P, Fournier D, Narbonne JF (1999) Cholinesterases from the marine mussels Mytilus galloprovincialis Lmk. and M. edulis L. and from the freshwater bivalve Corbicula fluminea Müller. Compar Biochem Physiol Part C 122: 353–361.Google Scholar
  64. Nunes B, Carvalho F, Guilhermino L (2005) Characterization and use of the total head soluble cholinesterases from mosquitofish (Gambusia holbrooki) for screening of anticholinesterase activity. J Enzym Inhibit Medic Chem 20(4): 369–376.Google Scholar
  65. Padilla S (1995) Regulatory and research issues related to cholinesterase inhibition. Toxicology 102: 215–220.Google Scholar
  66. Panda S, Sahu SK (2004) Recovery of acetylcholine esterase activity of Drawida willsi (Oligochaeta) following application of three pesticides to soil. Chemosphere 55: 283–290.Google Scholar
  67. Parsons KC, Matz AC, Hooper MJ, Pokras MA (1999) Monitoring wading bird exposure to agricultural chemicals using serum cholinesterase activity. Environ Toxicol Chem 19(5): 1317–1323.Google Scholar
  68. Pham TPT, Cho CW, Yun YS (2010) Environmental fate and toxicity of ionic liquids: A review. Water Res 44: 352–372.Google Scholar
  69. Principato GB, Contenti S, Talesa V, Mangiabene C, Pascolini R, Rosi G (1989) Propionylcholinesterase from Allolobophora caliginosa. Compar Biochem Physiol Part C: Compar Pharmacol 94(1): 23–27.Google Scholar
  70. Principato GB, Ambrosini MV, Menghini A, Giovannini E, Dell’Agata M (1978) Multiple forms of acetylcholinesterase in Allolobophora caliginosa: Purification and partial characterization. Compar Biochem Physiol Part C: Compar Pharmacol 61(1): 147–151.Google Scholar
  71. Rahman MF, Siddiqui MKJ, Jamil K (2000) Inhibition of Acetylcholinesterase and Different ATPases by a Novel Phosphorothionate (RPR-II) in Rat Brain. Ecotoxicol Environ Saf 47: 125–129.Google Scholar
  72. Rault M, Mazzia C, Capowiez Y (2007) Tissue distribution and characterization of cholinesterase activity in six earthworm species. Compar Biochem Physiol, Part B 147: 340–346.Google Scholar
  73. Rocío Marcos M, Sánchez-Yague J, Hernéndez-Hernández A, Llanillo M (1998) Amphiphilic and hydrophilic forms of acetylcholinesterase from sheep platelets. Biochimica et Biophysica Acta 1415: 163–173.Google Scholar
  74. Rodríguez-Castellano L, Sanchez-Hernandez JC (2007a) Earthworm biomarkers of pesticide contamination: Current status and perspectives. J Pesticide Sci 32: 360–371.Google Scholar
  75. Rodríguez-Castellanos L, Sanchez-Hernandez JC (2007b) Chemical Reactivation and Aging Kinetics of Organophosphorus-Inhibited Cholinesterases from Two Earthworms Species. Environ Toxicol Chem 26(9): 1992–2000.Google Scholar
  76. Rodríguez-Fuentes G, Armstrong J, Schlenk D (2008) Characterization of muscle cholinesterases from two demersal flatfish collected near a municipal wastewater outfall in Southern California. Ecotoxicol Environ Saf 69: 466–471.Google Scholar
  77. Rodríguez-Fuentes G, Gold-Bouchot G (2004) Characterization of cholinesterase activity from different tissues of Nile tilapia (Oreochromus niloticus). Mar Environ Res 58: 505–509.Google Scholar
  78. Romani R, Antognelli C, Baldracchini F, De Santis A, Isani G, Giovannini E, Rosi G (2003) Increased acetylcholinesterase activities in specimens of Sparus auratus exposed to sublethal copper concentrations. Chemico-Biological Interact 145: 321–329.Google Scholar
  79. Sanchez JC, Fossi MC, Focardi S (1997) Serum “B” Esterases as a Nondestructive Biomarker for Monitoring the Exposure of Reptiles to Organophosphorus Insecticides. Ecotoxicol Environ Saf 37: 45–52.Google Scholar
  80. Sánchez-Fortún S, Barahona V (2001) The use of carbamates, atropine, and 2-pyridine aldoxime methoiodide in the protection of Artemia salina against poisoning by carbophenothion. Environ Toxicol Chem 20(9): 2008–2013.Google Scholar
  81. Sánchez-Hernandez JC (2007) Ecotoxicological perspectives of B-esterases in the assessment of pesticide contamination. In: Plattenberg RH (ed.) Environmental Pollution: New Research. Nova Science Publishers, New York, USA, pp. 1–45.Google Scholar
  82. Sánchez-Hernández JC, Carbonell R, Henríquez Pérez A, Montealegre M, Gómez L (2004) Inhibition of plasma butyrylcholinesterase activity in the lizard Gallotia galloti palmae by pesticides: a field study. Environ Pollut 132: 479–488.Google Scholar
  83. Sanchez-Hernandez JC (2003) Evaluating reptile exposure to cholinesterase-inhibiting agrochemicals by serum butyrylcholinesterase activity. Environ Toxicol Chem 22(2): 296–301.Google Scholar
  84. Sanchez-Hernandez JC, Sanchez BM (2002) Lizard cholinesterases as biomarkers of pesticide exposure: enzymological characterization. Environ Toxicol Chem 21(11): 2319–25.Google Scholar
  85. Sánchez-Hernandez JC (2001) Wildlife exposure to organophosphorus insecticides. Rev Environ Contam Toxicol 172: 21–63.Google Scholar
  86. Sánchez-Hernandez JC, Walker CH (2000) In vitro and in vivo cholinesterase inhibition in Lacertides by phosphonate- and phosphorothioate-type organophosphates. Pesticide Biochem Physiol 67: 1–12.Google Scholar
  87. Sancho E, Fernandez-Vega C, Sanchez M, Ferrando MD, Andreu-Moliner E (2000) Alterations on AChE Activity of the Fish Anguilla anguilla as Response to Herbicide-Contaminated Water. Ecotoxicol Environ Saf 46: 57–63.Google Scholar
  88. Sancho E, Ferrando MD, Andreu E (1998) In vivo inhibition of AChE activity in the European eel Anguilla anguilla exposed to technical grade fenitrothion. Comparat Biochem Physiol Part C 120: 389–395.Google Scholar
  89. Sandahl JF, Baldwin DH, Jenkins JJ, Scholz NL (2005) Comparative thresholds for acetylcholinesterase inhibition and behavioral impairment in Coho salmon exposed to chlorpyrifos. Environ Toxicol Chem 24(1): 136–145.Google Scholar
  90. Schmidt SR (2003) Reptile Cholinesterase Characterization and Use in Monitoring Anti-cholinesterases. Thesis in Environmental Toxicology. Texas Tech University.Google Scholar
  91. Schmidt GH, Ibrahim NMM (1994) Heavy metal content (Hg2+, Cd2+, Pb2+) in various body parts: Its impact on cholinesterase activity and binding glycoproteins in the grasshopper Aiolopus thalassinus adults. Ecotoxicol Environ Saf 29(2): 148–164.Google Scholar
  92. Scott-Fordsmand JJ, Weeks JM (2000) Biomarkers in earthworms. Rev Environ Contam Toxicol 165:117–59.Google Scholar
  93. Schweitzer ES (1993) Regulated and constitutive secretion of distinct molecular forms of acetylcholinesterase from PC12 cells. J Cell Sci 106: 731–740.Google Scholar
  94. Small DH, Michaelson S, Sberna G (1996) Non-classical actions of cholinesterases: role in cellular differentiation, tumorigenesis and Alzheimer’s disease. Neurochem Internat 5/6: 453–483.Google Scholar
  95. Solé M, Lobera G, Lima D, Reis-Henriques MA, Santos MM (2008) Esterases activities and lipid peroxidation levels in muscle tissue of the shanny Lipophrys pholis along several sites from the Portuguese Coast. Mar Pollut Bull 56: 999–1007.Google Scholar
  96. Somnuek C, Cheevaporn V, Saengkul C and Beamish FWH (2007) Variability in Acetylcholinesterase upon Exposure to Chlorpyrifos and Carbaryl in Hybrid Catfish. ScienceAsia 33: 301–305.Google Scholar
  97. Stefano B, Ilaria C, Silvano F (2008) Cholinesterase activities in the scallop Pecten jacobaeus: Characterization and effects of exposure to aquatic contaminants. Sci Tot Env 392: 99–109.Google Scholar
  98. Stenersen J, Brekke E, Engelstad F (1992) Earthworms for toxicity testing; species differences in response towards cholinesterase inhibiting insecticides. Soil Biol Biochem 24(12): 1761–1764.Google Scholar
  99. Stenersen J (1980) Esterases of earthworms. Part I: Characterisation of the cholinesterases in Eisenia foetida (Savigny) by substrates and inhibitors. Compar Biochem Physiol Part C: Compar Pharmacol 66(1): 37–44.Google Scholar
  100. Sturm A, Silva de Assis HC, Hansen PD (1999a) Cholinesterases of marine teleost fish: enzymological characterization and potential use in the monitoring of neurotoxic contamination. Mar Environ Res 47: 389–398.Google Scholar
  101. Sturm A, Wogram J, Hansen PD, Liess M (1999b) Potential use of cholinesterase in monitoring low levels of organophosphates in small streams: natural variability in three-spined stickleback (Gasterosteus aculeatus) and relation to pollution. Environ Toxicol Chem 18(2): 194–200.Google Scholar
  102. Talesa V, Romani R, Antognelli C, Giovannini E, Rosi G (2001) Soluble and membrane-bound acetylcholinesterases in Mytilus galloprovincialis (Pelecypoda: Filibranchia) from the northern Adriatic sea. Chemico-Biological Interact 134: 151–166.Google Scholar
  103. Talesa V, Romani R, Rosi G, Giovannini E (1997) Acetylcholinesterase in Spirographis spallanzanii (Polychaeta: Sedentaria): Presence of two dimeric membrane-bound forms. Biochimie 79: 397–405.Google Scholar
  104. Talesa V, Grauso M, Giovannini E, Rosi G, Toutant JP (1995a) Acetylcholinesterase in tentacles in Octopus vulgaris (cephalopoda). Histochemical localization and characterization of a specific high salt-soluble and heparin-soluble fraction of globular forms. Neurochem Internat 27(2): 201–211.Google Scholar
  105. Talesa V, Grauso M, Giovannini E, Rosi G, Toutant JP (1995b) Solubilization, molecular forms, purification and substrate specificity of two acetylcholinesterases in the medicinal leech (Hirudo medicinalis). Biochem J 306: 687–692.Google Scholar
  106. Tsim KWK (1998) The signaling pathway of calcitonin gene-related peptide-induced ­acetylcholinesterase expression in muscle is mediated by cyclic AMP. Abstract book of the Xth International Symposium on Cholinergic Mechanisms, Arcachon, France September 1–5, 1998: 109.Google Scholar
  107. Valbonesi P, Sartor G, Fabbri E (2003) Characterization of cholinesterase activity in three bivalves inhabiting the North Adriatic sea and their possible use as sentinel organisms for biosurveillance programmes. Sci To Environ 312: 79–88.Google Scholar
  108. Varó I, Navarro JC, Amat F, Guilhermino L (2003) Effect of dichlorvos on cholinesterase activity of the European sea bass (Dicentrarchus labrax). Pesticide Biochem Physiol 75: 61–72.Google Scholar
  109. Varó I, Navarro JC, Amat F, Guilhermino L(2002) Characterisation of cholinesterases and evaluation of the inhibitory potential of chlorpyrifos and dichlorvos to Artemia salina and Artemia parthenogenetica. Chemosphere 48: 563–569.Google Scholar
  110. Vermeire T, McPhail R, Waters M (2001) D. Organophosphorous pesticides in the environment. World Health Organization. IV. Meeting Report of the International Workshop on Approaches to Integrated Risk Assessment: 1–18.Google Scholar
  111. Wan DCC, Choi RCY, Siow NL, Tsim KWK (2000) The promoter of human acetylcholinesterase is activated by a cyclic adenosine 3′, 5′-monophosphate-dependent pathway in cultured NG108-15 neuroblastoma cells. Neurosc Lett 288: 81–85.Google Scholar
  112. Wang J, Grisle S, Schlenk D (2001) Effects of Salinity on Aldicarb Toxicity in Juvenile Rainbow Trout (Oncorhynchus mykiss) and Striped Bass (Morone saxatilis  ×  chrysops) Toxicolog Sci 64: 200–207.Google Scholar
  113. Wogram J, Sturm A, Segner H, Liesse M (2001) Effects of parathion on acetylcholinesterase, butyrilcholinesterase, and carboxylesterase in three-spined stickleback (Gasterosteus aculeatues) following short-term exposure. Environ Toxicol Chem 20(7): 1528–1531.Google Scholar
  114. Xuereb B, Noury P, Felten V, Garric J, Geffard O (2007) Cholinesterase activity in Gammarus pulex (Crustacea Amphipoda): characterization and effects of chlorpyrifos. Toxicology 236: 178–189.Google Scholar
  115. Yang L, He HY, Zhang XJ (2002) Increased expression of intranuclear AChE involved in apoptosis of SK-N-SH cells. Neurosci Res 42: 261–268.Google Scholar
  116. Zinkl JG, Lochkart WL, Kenny SA, Ward FJ (1991) The effects of cholinesterase inhibiting insecticides on fish. In: Cholinesterase-Inhibiting Insecticides. Their Impact on wildlife and the Environment. Mineau P (ed), pp. 234–243. Elsevier, New York.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.CIAGEB, FCS-UFP: Global Change, Energy Environment and Bioengineering Unit, Faculdade de Ciências da Saúde daUniversidade Fernando PessoaPortoPortugal
  2. 2.CESAM-LA, Centro de Estudos do Ambiente e do Mar, Laboratório Associado, Departamento de BiologiaUniversidade de AveiroAveiroPortugal

Personalised recommendations