Revista de Gestão Costeira Integrada
Volume 13, Número 4, Dezembro 2013, Páginas 525-537

DOI: 10.5894/rgci430
* Submission: 29 July 2013; Evaluation: 26 August 2013; Reception of revised manuscript: 15 November 2013; Accepted: 4 December 2013; Available on-line: 6 December 2013
** Portuguese Title and captions by Ulisses M Azeiteiro on behalf of the Journal Editorial Board.

Cholinesterase activity as biomarker of neurotoxicity: utility in the assessment of aquatic environment contamination *

Actividade da colinesterase como biomarcador de neurotoxicidade: avaliação da contaminação em ambientes aquáticos **

Jamel Jebali ^{@, 1}, Sana Ben Khedher ¹, Marwa Sabbagh ¹, Naouel Kamel ¹, Mohamed Banni ¹, Hamadi Boussetta ¹

---

@ - Corresponding author: : [email protected]; [email protected]
1 - Laboratory of Biochemical and Environmental Toxicology, Higher Institute of Agriculture, Chott-Mariem, 4042-Sousse, Tunisia.

---

ABSTRACT
Cholinesterase can take place in aquatic organisms under a series of environmental adverse conditions. The study of cholinesterases in these organisms can give important information about their physiological status and about environmental health. However, it is very important to know how the environmental factors such as fluctuation of physicochemical parameters associated to the presence of pollutants might affect these cholinesterase activities. We studied the response of cholinesterase activity in the caged cockle Cerastoderma glaucum. In addition, we evaluated the potential uses of cholinesterase activity in the common sole, which inhabit the Tunisian coast, subjected to different stress conditions, such as the exposure to different contaminants. This review summarizes the data obtained in some studies carried out in organisms from the Tunisian aquatic environment.

Keywords: Cholinesterases, Environmental stress, Biomonitoring, Aquatic Environments.

RESUMO
A colinesterase está presente nos organismos aquáticos em condições de stress ambiental. O estudo da colinesterase fornece informações acerca da condição fisiológica e saúde ambiental. Contudo é importante averiguar de que modo os factores ambientais, tais como a flutuação dos parâmetros físico-químicos, associados à presença de poluentes afectam a actividade das colinesterases. Neste trabalho são apresentadas os níveis de actividade da colinesterase em Cerastoderma glaucum. São ainda apresentados os potenciais usos da actividade das colinesterases na solha comum que habita a costa Tunisina. Este trabalho sumariza também os resultados obtidos até agora em outros organismos estudados na Costa Tunisina.

Palavras-chave:Colinesterases, Stress Ambiental, Biomonitorização, Ambientes Aquáticos.

 

Attig, H.; Dagnino, A.; Negri, A.; Jebali, J.; Boussetta, H.; Viarengo, A.; Dondero, F.; Banni, M. (2010) - Uptake and biochemical responses of mussels Mytilus galloprovincialis exposed to sublethal nickel concentrations. Ecotoxicology and Environmental Safety 73(7):1712-1719, doi: 10.1016/j.ecoenv.2010.08.007.

Augustinsson, K.B. (1963) - Cholinesterase and anticholinesterase agents. In: G.B. Koelle, (org),. Handbook of Experimental Pharmacology, pp.89-128, Springer-Verlag, Berlin, Germany. ISBN: 978-3540029885.

Banni, M.; Jebali, J.; Daubeze, M.; Clerandau, C.; Guerbej, H.; Narbonne, J.F.; Boussetta, H. (2005) - Monitoring pollution in Tunisian coasts: application of a classification scale based on biochemical markers. Biomarkers, 10(2-3):105-116. doi: 10.1080/13547500500107497.

Ben-Khedher, S.; Jebali, J.; Kamel, N.; Banni, M.; Rameh, M.; Jrad, A.; Boussetta, H. (2013) - Biochemical effects in crabs (Carcinus maenas) and contamination levels in the Bizerta Lagoon: an integrated approach in biomonitoring of marine complex pollution. Environmental Science and Pollution Research, 20(4):2616-2631. doi: 10.1007/s11356-012-1156-x.

Bocquen., G.; Galgani, F.; Walker, C.H. (1997) – Les cholinest.rases, biomarqueurs de neurotoxicit.. In: L. Lagadig, T. Caquet, J.C. Amiard & F. Ramade (eds.), Biomarqueurs en écotoxicologie. Aspect fondamentaux, pp.209-240, Masson, Paris, France.ISBN: 2225830533.

Bonacci, S.; Corsi, I.; Focardi S. (2008) - Cholinesterase activities in the scallop Pecten jacobaeus: Characterization and effects of exposure to aquatic contaminants. Science Of The Total Environment, 392(1):99-109. doi: 10.1016/j.scitotenv.2007.11.029.

Borówka, R.K.; Strobel, W.; Hałas, S. (2012) - Stable isotope composition of subfossil Cerastoderma glaucum shells from the Szczecin Bay brackish deposits and its palaeogeographical implications (South Baltic Coast, Poland). Quaternary Research 77(2):245-250, doi: 10.1016/j.yqres.2012.01.001

Chatonnet, A.; Lockridge, O. (1989) - Comparison of butyrylcholinesterase and acetylcholinesterase. Biochemical, 260(3):625-634. Available at http://www.ncbi.nlm.nih.gov/
pmc/articles/PMC1138724/

Chuiko, G.M. (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. Comparative Biochemistry and Physiology Part C, 127(3):233–242. doi: 10.1016/S0742-8413(00)00150-X.

Çokugras, A.N. (2003) - Butyrylcholinesterase: Structure and Physiological Importance. Turkish Journal of Biochemistry, 28(2):54-61. Available at http://www.turkjbiochem.com/2003/054_061.pdf.

Davoodi, F.; Claireaux, G. (2007) - Effects of exposure to petroleum hydrocarbons upon the metabolism of the common sole Solea solea. Marine Pollution Bulletin, 54(7):928-934. doi: 10.1016/j.marpolbul.2007.03.004

Day, K.E.; Scott, I.M. (1990) - Use of acetylcholinesterase activity to detect sublethal toxicity in stream invertebrates exposed to low concentrations of organophosphate insecticides. Aquatic Toxicology, 18(2-3):201-224. doi: 10.1016/0166-445X(90)90021-G

de la Torre, F.R.; Ferrari, L.; Salibian, A. (2002) - Freshwater pollution biomarker: Response of brain acetylcholinesterase activity in two fish species. Comparative Biochemistry and Physiology Part C 131 (3): 271-280. Available at http://www.sciencedirect.com/science/article/
pii/S1532045602000145.

Dellali, M.; Gnassia-barelli, M.; Romeo, M.; Aissa, P.; (2001) - The use of acetylcholinesterase activity in Ruditapes decussatus and Mitillus galloprovincialis in the biomonitoring of Bizerta lagoon. Comparative Biochemistry and Physiology, 130(2):227-235. doi: 10.1016/S1532-0456(02)00014-5

Elumalai, E.; Antunes, C.; Guilhermino. L. (2007) - Enzymatic biomarkers in the crab Carcinus maenas from the Minho River estuary (NM Portugal) exposed to zinc and mercury. Chemosphere, 66(7):1249-1255. doi: 10.1016/j.chemosphere.2006.07.030

Fathallah, S.; Medhioub, M.N.; Medhioub, A.; Kraiem, M.M. (2011) - Ruditapes decussatus embryo–larval toxicity bioassay for assessment of Tunisian coastal water contamination. Environmental Chemistry and Ecotoxicology, 3(11):277-285. Available at http://academicjournals.org/
article/article1380009080_Fathallah%20et%20al.pdf.

Forget, J.; Bocquené, G. (1999) - Partial purification and enzymatic characterization of acetylcholinesterase from the intertidal marine copepod Tigriopus brevicornis. Comparative Biochemistry and Physiology Part B, 123(4):345–350. doi: 10.1016/S0305-0491(99)00073-5

Galloway, T.S.; Brown, R.J.; Browne, M.A.; Dissanayake, A.; Lowe, D.; Jones, MB.; Depledge, M.H. (2004) - A multibiomarker approach to ecosystem management. Environmental Science and Technology, 38:1723-1731.

Ghedira, J.; Jebali, J.; Banni, M.; Chouba, L.; Boussetta, H.; López-Barea, J.; Alhama, J. (2011) - Use of oxidative stress biomarkers in Carcinus maenas to assess littoral zone contamination in Tunisia. Aquatic Biology, 14:87-98. doi:10.3354/ab00377

Goldberg, E.D.; Broecker, W.S. (1970) - Marine chemistry. In National Academy of Sciences. National Reseach Council 137-146.

González-Wangüemert, M.; Cánovas, F.; Marcos, C.; Pérez-Ruzafa, A. (2009) - Phosphoglucose isomerase variability of Cerastoderma glaucum as a model for testing the influence of environmental conditions and dispersal patterns through quantitative ecology approaches. Biochemical Systematics and Ecology, 37(4):325–333. doi: 10.1016/j.bse.2009.05.013

Harel, M.; Sussman, J.L.; Krejci, E.; Bon, S.; Chanal, P.; Massouli., J.; Silman, I. (1992) - Conversion of acetylcholinesterase to butyrylcholinesterase: Modeling and mutagenesis. Proceedings of the National Academy of Sciences of the United States of America, 89(22):10827-10831. Available at http://www.pnas.org/content/89/22/
10827.full.pdf

Helmut, S.; Braunbeck, T. (1998) - Cellular response profile to chemical stress. In: Gerrit Schüürmann &Bernd Markert (eds.), Ecotoxicology: Ecological Fundamentals, Chemical Exposure, and Biological Effects, pp.521-569, Wiley, New York, U.S.A. ISBN: 0471176443

Jebali, J.; Banni, M.; Guerbej, H.; Almeida, E.A.; Bannaoui, A.; Boussetta, H. (2006) - Effects of malathion and cadmium on acetylcholinesterase activity and metallothionein levels in the fish Seriola dumerilli. Fish Physiology Biochemistry, 32(1):93-98. doi: 10.1007/s10695-006-0041-2.

Jebali, J.; Banni, M.; DeAlmeida, E.A.; Boussetta, H. (2007) - Oxidative DNA damage levels and catalase activity in the clam Ruditapes decussatus as pollution biomarkers of Tunisian marine environment. Environmental Monitoring Assessment, 124:195-200. doi: 10.1007/s10661-006-9217-6.

Jebali, J.; Ben-Khedher, S.; Kamel, N.; Ghedira, J.; Bouraoui, Z.; Boussetta, H. (2011) - Characterization and evaluation of cholinesterase activity in the cockle Cerastoderma glaucum. Aquatic Biology, 13:243–250. doi:10.3354/ab00365

Jebali, J.; Sabbagh, M.; Banni, M.; Kamel, N.; Ben-Khedher, S.; M’hamdi, N.; Boussetta, H. (2013c) - Multiple biomarkers of pollution effects in Solea solea fish on the Tunisia coastline. Environmental Science and Pollution Research, 20(6):3812-3821. doi: 10.1007/s11356-012-1321-2.

Jebali, J.; Chicano-Gálvez, E.; Banni, M.; Guerbej, H.; Boussetta, H.; López-Barea, J.; Alhama, J. (2013a) – Biochemical responses in sea bream (Sparus aurata) caged in-field or exposed to benzo (a) pyrene and paraquat. Characterization of glutathione S-transferases. Ecotoxicology and Environmental Safety, 88:169–177. doi: 10.1016/j.ecoenv.2012.11.013.

Jebali, J.; Banni, M.; Ben-Khedher, S.; Guerbej, H.; Boussetta, H. (2013b) - Biochemical Response of Sea bass Dichentrarchus labrax Experimentally Exposed to Nickel and Chlorpyriphos. Biomarkers in Drug Development, 2(1): online doi: 10.4172/jbdd.1000101.

Johnson, G.; Moore, S.W. (2000) - Cholinesterases modulate cell adhesion in human neuroblastoma cells in vitro. International Journal of Developmental Neuroscience, 18(8):781–790. doi: 10.1016/S0736-5748(00)00049-6

Kamel, N.; Jebali, J.; Banni, M.; Ben-Khedher, S.; Chouba, L.; Boussetta, H. (2012) -Biochemical Responses and metals levels in Ruditapes decussatus after exposure to treated municipal effluents. Ecotoxicology and Environmental Safety, 82:40-46. doi: 10.1016/j.ecoenv.2012.05.008.

Kanazawajun, J. (1975) - Uptake and Excretion of Organophosphorus and Carbamate Insecticides by Fresh Water Fish, Motsugo, Pseudorasbora parva. Bulletin of Environmental Contamination & Toxicology, 14(3):346-352. Available at http://www.ncbi.nlm.nih.gov/pubmed/1174751.

Kessabi, K.; Annabi, A.; Ibn Hadj Hassin, A.; Bazin, I.; Mnif, W.; Said, K.; Messaoudi, I. (2013) - Possible chemical causes of skeletal deformities in natural populations of Aphanius fasciatus collected from the Tunisian coast. Chemosphere, 90(11):2683–2689. doi: 10.1016/j.chemosphere.2012.11.047.

Kirby, M.F.; Morris, S.; Hurst, M.; Kirby, S.J.; Neall, P.; Tylor, T. (2000) - The use of cholinesterase activity in flounder (Platichthys flesus) muscle tissue as a biomarker of neurotoxic contamination in UK estuaries. Marine Pollution Bulletin, 40(9):780–791. doi: 10.1016/S0025-326X(00)00069-2

Koenig, S.; Guillén, K.; Solé, M. (2013) - Comparative xenobiotic metabolism capacities and pesticide sensitivity in adults of Solea solea and Solea senegalensis. Comparative Biochemistry and Physiology Part C, 157(4):329–336. doi: 10.1016/j.cbpc.2013.03.002.

Kovarik, Z.; Bosak, A.; Sinko, G.; Latas, T. (2003) - Exploring the Active Sites of Cholinesterases by Inhibition with Bambuterol and Haloxon. Croatica Chemica Acta, 76(1):63-67. Available at http://cat.inist.fr/?aModele=afficheN&cpsidt=14767748.

Lavado, R.; Ureña, R.; Martin-Skilton. R.; Torreblanca, A.; Del Ramo, J.. Raldúa, D.; Porte, C. (2006) - The combined use of chemical and biochemical markers to assess water quality along the Ebro River. Environmental Pollution, 139(2):330–339. Available at http://www.ncbi.nlm.nih.gov/pubmed/16040174.

Livingstone, D.R. (1998) - The fate of organic xenobiotics in aquatic ecosystems: quantitative and qualitative differences in biotransformation by invertebrates and fish. Comparative Biochemistry and Physiology Part A, 120(1):43-49. Available at http://www.ncbi.nlm.nih.gov/pubmed/9773498.

Lopez-Carillo, L.; Lopez-Cervantes, M. (1993) - Effect of exposure to organophosphate pesticides on serum cholinesterase levels. Archives of environmental health, 48(5):359-363. Available at http://www.ncbi.nlm.nih.gov/pubmed/8215602.

Machreki-Ajmi, M.; Ketata, I.; Ladhar-Chaabouni, R.; Hamza-Chaffai, A. (2008) - The effect of in situ cadmium contamination on some biomarkers in Cerastoderma glaucum. Ecotoxicology, 17(1):1-11. Available at http://www.ncbi.nlm.nih.gov/pubmed/18060580.

Massoulié, J.; Pezzementi, L.; Bon, S.; Krejci, E.; Vallette, F.M.; (1993) - Molecular and cell biology of cholinesterases. Progress in Neurobiology, 41(1):31-91. Available at http://www.ncbi.nlm.nih.gov/pubmed/8321908.

Mastrantonio, G.; Mack, H.G.; Della Védova, C.O. (2008) - Interpretation of the mechanism of acetylcholinesterase inhibition ability by organophosphorus compounds through a new conformational descriptor. An experimental and theoretical study. Molecular Model, 14(9):813-821. doi: 10.1007/s00894-008-0321-0.

Matozzo, V.; Marin, M.G. (2007) - First evidence of altered vitellogenin-like protein levels in clam Tapes philippinarum and in cockle Cerastoderma glaucum from the Lagoon of Venice. Marine Pollution Bulletin, 55(10-12): 494-504. Available at http://www.ncbi.nlm.nih.gov/pubmed/17936854.

Monserrat, J.M.; Bianchini, A.; Bainy, A.C.D. (2002) - Kinetic and toxicological characteristics of acetylcholinesterase from the gills of oysters (Crassostrea rhizophorae) and other aquatic species. Marine Environmental Reseach, 54(3-5): 781–785. Available at http://www.ncbi.nlm.nih.gov/pubmed/12408650.

Monserrat, J.M.; Martínez, P.E.; Geracitano, L.; Amado, L.L.; Gaspar Martins, C.M.; Leães Pinho, G.L.; Chaves, I.S.; Ferreira-Cravo, M.; Ventura-Lima, J.; Bianchini, A.; (2007) - Pollution biomarkers in estuarine animals: critical review and new perspectives. Comparative Biochemistry and Physiology Part C, 146(1-2):221-234. Available at http://www.ncbi.nlm.nih.gov/pubmed/17045848.

Nicolet, Y.; Lockridge, O.; Masson, P.; Fontecilla-Camps, J.C.; Nachon, F. (2003) - Crystal Structure of Human Butyrylcholinesterase and of Its Complexes with Substrate and Products. Biological Chemistry, 278(42): 41141-41147. Available at http://www.ncbi.nlm.nih.gov/pubmed/
12869558.

O’Brien, R.D. (1976) - Acetylcholinesterase and its inhibition. In: C.F. Wilkinson (ed.), Insecticide Biochemistry and Physiology, pp.271-296, Springer Science + Business Media, New York, NY, U.S.A. ISBN: 978-1489922144.

Ozmen, M.; Ayas, Z.; Gungurdu, A.; Ekmekci, G. F.; Yerli, S. (2007) - Ecotoxicological assessment of water pollution in Sariyar Dam Lake, Turkey. Ecotoxicology and Environmental Safety, 70(1):163–173. Available at http://www.ncbi.nlm.nih.gov/pubmed/17582495.

Palermo, FA.; Cocci, P.; Nabissi, M.; Polzonetti-Magni, A.; Mosconi, G. (2012) - Cortisol response to waterborne 4-nonylphenol exposure leads to increased brain POMC and HSP70 mRNA expressions and reduced total antioxidant capacity in juvenile sole (Solea solea). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 156(3-4):135-139. doi: 10.1016/j.cbpc.2012.08.002.

Penã-Llopis, S.; Dolores Ferrando, M.; Penã, J.B. (2003) - Fish tolerance to organoohosphate- induced oxidative stress is dependent on the glutathione metabolism and enhanced by N-acetylcycteine. Aquatic Toxicology, 65(4):337-360. Available at http://www.ncbi.nlm.nih.gov/pubmed/14568351.

Pezzementi, L.; Chatonnet, A. (2010) - Evolution of cholinesterases in the animal kingdom. Chemico-Biological Interactions, 187(1-3):27–33. doi:10.1016/j.cbi.2010.03.043.

Pezzementi, L.; Nickson, H.C.; Dunn, R.C.; Bradley, R.G. (1989) - Molecular forms of acetylcholinesterase from the skeletal muscle of the ammocoete of the lamprey Petromyzon marinus. Comparative Biochemistry and Physiology Part B, 92(2):385–387. Available at http://www.ncbi.nlm.nih.gov/pubmed/2924545.

Quinn, D.M. (1987) - Acetylcholinesterase: enzyme structure, reaction dynamics, and virtual transition states. Chemical Reviews, 87(5):955-979. doi: 10.1021/cr00081a005.

Rezgui, A. (2007) - Contribution of geographic information systems for the determination of the impact of heavy metals on the surface sediments of coastal Monastir-Sayada. Diplôma of master. TUNIS II University, Tunisia.

Ribecco, C.; Hardiman, G.; Sášik, R.; Vittori, S.; Carnevali, O. (2012) - Teleost fish (Solea solea): a novel model for ecotoxicological assay of contaminated sediments. Aquatic Toxicology, 109:133–142. doi: 10.1016/j.aquatox.2011.12.002.

Romani, R.; Corsi, I.; Bonacci, S.; Focardi, S.; De Medio, G.E.; De Santis, A.; Incarnato, F.; Giovannini, E.; Rosi, G.; (2006) - Organophosphate-resistant forms of acetylcholinesterases in two scallops-the Antarctic Adamussium colbecki and the Mediterranean Pecten jacobaeus. Comparative Biochemistry and Physiology Part B, 145(2):188–196. Available at http://www.ncbi.nlm.nih.gov/pubmed/16931084.

Roméo, M.; Hoarau, P.; Garello, G.; Gnassia-Barelli, M.; Girard, J.P. (2003) - Mussel transplantation and biomarkers as useful tools for assessing water quality in the NW Mediterranean. Environmental Pollution, 122(3):369–378. doi: 10.1016/S0269-7491(02)00303-2

Rosenberry, T.L. (1975) - Catalysis by acetylcholinesterase: Evidence that the rate-limiting step for acylation with certain substrates precedes general acid-base catalysis Proceedings of the National Academy of Sciences of the United States of America, 72(10):3834-3838. Available at http://www.pnas.org/content/72/10/3834.full.pdf.

Sabbagh, M. (2011) - Study of biochemical biomarkers and biometrics in Solea solea: Validation of the use of some sites Tunisian coast. 60p., diplôma of master, Monastir University, Tunisia. Unpublished.

Sahnoun, O. (2000) - Geochemistry studies of heavy metals (Cu, Zn, Cd, Mn, Cr, Ni, Pb and Fe) in the sediments of Monastir bay. 132p., diplôma of master, Tunis II University,Tunisia. Unpublished.

Sanders, M.; Mathews, B.; Sutherland, D.; Soong, W.; Giles, H.; Pezzementi, L. (1996) -Biochemical and molecular characterization of acetylcholinesterase from the hagfish Myxine glutinosa. Comparative Biochemistry and Physiology Part B, 115(1):97-109. Available at http://www.ncbi.nlm.nih.gov/pubmed/8896335.

Scheil, V.; Köhler, H.R. (2009) - Influence of Nickel Chloride, Chlorpyrifos, and Imidacloprid in Combination with Different Temperatures on the Embryogenesis of the Zebrafish Danio rerio. Arch Environmental Contamination Toxicology, 56(2):238-243. doi: 10.1007/s00244-008-9192-8.

Silman, I.; Sussman, J.L. (2005) - Acetylcholinesterase: ‘classical’ and ‘non-classical’ functions and pharmacology. Current Opinion in Pharmacology, 5(3):293–302. Available at http://www.ncbi.nlm.nih.gov/pubmed/15907917.

Solé, M.; Porte, C.; Barcelo, D.; Albaiges, J. (2000) - Bivalves Residue Analysis for the Assessment of Coastal Pollution in the Ebro Delta (NW Mediterranean). Marine Pollution Bulletin, 40(9):746-753. doi: 10.1016/S0025-326X(00)00011-4

Solé, M.; Vega, S.; Varó, I. (2012) - Characterization of type “B” esterases and hepatic CYP450 isoenzymes in Senegalese sole for their further application in monitoring studies. Ecotoxicology Environmental Safety, 78:72-79. doi: 10.1016/j.ecoenv.2011.11.013.

Soreq, H.; Zakut, H. (eds.) (1990) - Cholinesterase Genes Multileveled Regulation. 108p., S Karger Pub, Basel, Switzerland. ISBN 13: 9783805551373

Sturm, A.; Wogram, J.; Segner, H.; Liess, M. (2000) - Different sensitivity to organophosphates of acetylcholinesterase and butyrylcholinesterase from three-spined stickleback (Gasterosteus aculeatus): application in biomonitoring. Environmental and Toxicology Chemosphere, 19:1607–15. Available at http://www.ufz.de/index.php?en=14784.

Sussman, J.L.; 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(5022): 872-879. doi: 10.1126/science.1678899

Talesa, V.; Grauso, M.; Arpagaus, M.; Giovannini, E.; Romani, R.; Rosi, G. (1999) - Molecular cloning and expression of a full-length cDNA encoding acetylcholinesterase in optic lobes of Loligo opalescens: a new member of the cholinesterase family resistant to diisopropyl fluorophosphate. Neurochemical, 72(3):1250–1258. Available at http://www.ncbi.nlm.nih.gov/pubmed/10037498.

Talesa, V.; Principato, G.B.; Giovannini, E.; Grauso, M.; Rosi, G. (1993) - Evidence for a molecular polymorphism of Cholinesterase in Sepia officinalis (Cephalopoda: Decapoda). Comparative Biochemistry and Physiology Part B,106(3):557-562. doi: 10.1016/0305-0491(93)90132-O

Talesa, V.; Principato, G.B.; Giovannini, E.; Norton, S.J.; Rosi, G. (1994) - Presence of a solubile tetrameric (blood) and membrane-bound dimeric forms of cholinesterase in the mollusk Murex brandaris (Gastropoda: Neogastropoda). Experimental Zoology, 270:233–244. doi: 10.1002/jez.1402700302.

Talesa, V.; Romani, R.; Antognelli, C.; Giovannini, E.; Rosi, G.; (2002) - Different expressions of organophosphate resistant acetylcholinesterases in the bivalve mollusk Scapharca inaequivalvis living in three different habitats. Environmental Toxicology Chemistry, 21(1):102–108. Available at http://www.ncbi.nlm.nih.gov/pubmed/
11804042.

Talesa, V.; Romani, R.; Rosi, G.; Giovannini, E. (1996) - Biochemical Characterization and Histochemical Localization in the Nervous System. European Journal of Biochemistry, 238(2):538-548. doi: 10.1111/j.1432-1033.1996.0538z.x

Taylor, P. (1991) - The cholinesterases. Biology Chemistry 266: 4025-4028. Available at http://www.jbc.org/content/266/7/4025.full.pdf+html.

Tlili, S.; Jebali, J.; Banni, M.; Haouas, Z.; Mlayah, A.; Helal, A.N.; Boussetta, H. (2010a) - Multimarker approach analysis in common carp Cyprinus carpio sampled from three freshwater sites. Environmental Monitoring and Assessment, 168:285-298. doi: 10.1007/s10661-009-1112-5.

Tlili, S.; Métais, I.; Boussetta, H.; Mouneyrac, C. (2010b) - Linking changes at sub-individual and population levels in Donax trunculus: Assessment of marine stress. Chemosphere, 81(6):692–700. doi: 10.1016/j.chemosphere.2010.07.064.

Tõugu, V.; (2001) - Acetylcholinesterase: mechanism of catalysis and inhibition. Current Medicinal Chemistry - Central Nervous System Agents, 1:155-170. doi:10.2174/1568015013358536.

Trisciani, A.; Corsi, I.; Della Torre, C.; Perra, G.; Focardi, S.; (2011) - Hepatic biotransformation genes and enzymes and PAH metabolites in bile of common sole (Solea solea, Linnaeus, 1758) from an oil contaminated site in the Mediterranean Sea: a field study. Marine Pollution Bulletin, 62(4):806–814. doi: 10.1016/j.marpolbul.2011.01.001.

Van der Oost, R.; Lopes, S.C.C.; Komen, H.; Satumalay, K. (1998) - Assessment of environmental quality and inland water pollution using biomarker responses in caged carp (Cyprinus carpio): Use of a bioactivation: Detoxication ratio as a Biotransformation Index (BTI). Marine Environmental Research, 46(1–5):315–319. doi: 10.1016/S0141-1136(97)00096-2

Vioque-Fernández, A.; Alves de Almeida, E.; Ballesteros, J.; García-Barrera, T.; Gómez-Ariza, J.L.; López-Barea, J. (2007) - Dõnana National Park survey using crayfish (Procambarus clarkii) as bioindicator: esterase inhibition and pollutant levels. Toxicology Letters, 168(3):260–268. Available at http://www.ncbi.nlm.nih.gov/pubmed/
17157454.

Wang, M.H.; Wang, G.Z. (2009) - Biochemical response of the copepod Tigriopus japonicus mori experimentally exposed to cadmium. Arch Environmental Contamination Toxicology, 57(4):707–717. doi: 10.1007/s00244-009-9319-6.

Whittaker, M. (1980) - Plasma cholinesterase variants and the anaesthetist Anaesthesia 35 (2): 174-97. Available at http://www.ncbi.nlm.nih.gov/pubmed/6992635.

Whittaker, M. (1986) - Cholinesterase. 134p., S Karger Pub, Basel, Switzerland. ISBN: 9783805542579

Zrafi, I.; Bakhrouf, A.; Rouabhia, M.; Saidane-Mosbahi, D. (2013) - Aliphatic and aromatic biomarkers for petroleum hydrocarbon monitoring in Khniss Tunisian-Coast, (Mediterranean Sea) Procedia Environmental Sciences, 18: 211–220. doi: 10.1016/j.proenv.2013.04.027. al., 2011

 

em construção