Early biochemical effects of Microcystis aeruginosa extracts on juvenile rainbow trout (Oncorhynchus mykiss)

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 161, Issue 3, 2012, Pages 261-267

  Gélinas, Malorie ^a   Juneau, Philippe ^b   Gagné, François ^a  

^a ENVIRONMENT CANADA   (Canada)

^b UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

Author keywords

Acetylcholinesterase; Metallothionein; Microcystis aeruginosa; Protein phosphatase; Trout

Indexed keywords

ACETYLCHOLINESTERASE; GLUTATHIONE TRANSFERASE; METALLOTHIONEIN; MICROCYSTIN LR; PHOSPHOPROTEIN PHOSPHATASE;

ARTICLE; BACTERIAL STRAIN; BACTERIUM CULTURE; BIOCHEMISTRY; BRAIN; CONCENTRATION (PARAMETERS); ENZYME ACTIVITY; EXPOSURE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIPID PEROXIDATION; LIVER TOXICITY; MICROCYSTIS AERUGINOSA; NONHUMAN; PRIORITY JOURNAL; RAINBOW TROUT; TOXICOLOGY;

CYANOBACTERIA; MICROCYSTIS AERUGINOSA; ONCORHYNCHUS MYKISS; SALMONIDAE;

EID: 84856215642     PISSN: 10964959     EISSN: 18791107     Source Type: Journal    
DOI: 10.1016/j.cbpb.2011.12.002     Document Type: Article

References (66)

1. Acou A., Robinet T., Lance E., Gerard C., Mounaix B., Brient L., Le Rouzic B., Feunteun E. Evidence of silver eels contamination by microcystin-LR at the onset of their seaward migration: what consequences for breeding potential?. J. Fish Biol. 2008, 72:753-762.
2. Al-Kahtani M.A.A., Fathi A.A. Physiological studies on tilapia fish (Oreochromis niloticus) as influenced by the cyanobacterial toxins microcystin. J. Biol. Sci. 2008, 8:1226-1230.
3. Amado L.L., Monserrat J.M. Oxidative stress generation by microcystins in aquatic animals: why and how. Environ. Int. 2010, 36:226-235.
4. Amado L.L., Garcia M.L., Ramos P.B., Yunes J.S., Monserrat J.M. Influence of a toxic Microcystis aeruginosa strain on glutathione synthesis and glutathione-S-transferase activity in common carp Cyprinus carpio (Teleostei: cyprinidae). Arch. Environ. Contam. Toxicol. 2011, 60:319-326.
5. Aras M.A., Hara H., Hartnett K.A., Kandler K., Aizenman E. Protein kinase C regulation of neuronal zinc signalling mediates survival during preconditioning. J. Neurochem. 2009, 110:106-117.
6. Atencio L., Moreno I., Jos A., Pichardo S., Moyano R., Blanco A., Camean A.M. Dose-dependent antioxidant responses and pathological changes in tenca (Tinca tinca) after acute oral exposure to Microcystis under laboratory condition. Toxicon 2008, 52:1-12.
7. Atif F., Kaur M., Yousuf S., Raisuddin S. In vitro free radical scavenging activity of hepatic metallothionein induced in an Indian freshwater fish, Channa punctata. Bloch. Chem. Biol. Interact. 2006, 162:172-180.
8. Barford D. Molecular mechanisms of the protein serine/threosine phosphatases. TIBS 1996, 21:407-412.
9. Best J.H., Pflugmacher S., Wiegand C., Eddy F.B., Metcalf J.S., Codd G.A. Effects of enteric bacterial and cyanobacterial lipopolysaccharides, and of microcystin-LR, on glutathione S-transferase activitiesin zebra fish (Danio rerio). Aquat. Toxicol. 2002, 60:223-231.
10. Bonacci S., Brown M.A., Dissanayake A., Hagger J.A., Corsi I., Focardi S., Galloway T.S. Esterase activities in the bivalve mollusk Adamussium colbecki as a biomarker for pollution monitoring in the Antarctic marine environment. Mar. Pollut. Bull. 2004, 49:445-455.
11. Bouaïcha N., Maatouk I., Vincent G., Levi Y. A colorimetric and fluorometric microplate assay for the detection of microcystin-LR in drinking water without preconcentration. Food Chem. Toxicol. 2002, 40:1677-1683.
12. Bradford M.M. A sensitive method for total protein determination using the principle of protein-dye binding. Anal. Biochem. 1976, 72:249-251.
13. Carmichael W.W. The toxins of cyanobacteria. Sci. Am. 1994, 270:78-86.
14. Cazenave J., Nores M.L., Miceli M., Diaz M.P., Wunderlin D.A., Bistoni M.A. Changes in swimming activity and the glutathione-S-transferase activity of Jenynsia multidentata fed with microcystin-RR. Water Res. 2008, 42:1299-1307.
15. Cazenava J., de los Angeles Bistoni M., Fabiana Pesce S., Wunderlin D.A. Differential detoxification and antioxidant response in diverse organs of Corydoras paleatus experimentally exposed to microcystin-RR. Aquat. Toxicol. 2006, 76:1-12.
16. Chen J., Xie P., Zhang D., Ke Z., Yang H. In situ studies on the bioaccumulation of microcystins in the phytoplanktivorous silver carp (Hypophthalmichthys molitrix) stocked in Lake Taihu with dense toxic Microcystis blooms. Aquaculture 2006, 261:1026-1038.
17. Chen J., Zhang D., Xie P., Wand Q., Ma Z. Simultaneous determination of microcystin contaminations in various vertebrates (fish, turtle, duck and water bird) from a large eutrophic Chinese lake, Lake Thahu, with toxic Microcystis blooms. Sci Total Environ. 2009, 407:3317-3322.
18. Chen J., Xie P., Xu J. First identification of the hepatotoxic microcystins in the serum of a chronically exposed human population together with indication of hepatocellular damage. Toxicol. Sci. 2009, 108:81-89.
19. Codd G.A., Bell S.G., Brooks W.P. Cyanobacterial toxins in water. Water Sci. Technol. 1989, 21:1-13.
20. Deblois C.P., Juneau P. Effect of light on microcystin production and photosynthetic activity of a toxic Microcystis aeruginosa strain. Harmful Algae 2010, 9:18-24.
21. Deblois C.P., Aranda-Rodriguez R., Giani A., Bird D.F. Microcystin accumulation in liver and muscle of tilapia in two large Brazilian hydroelectric reservoirs. Toxicon 2008, 51:435-448.
22. Dietrich D.R., Hoeger S. Guidance values for microcystins in water and cyanobacterial products (blue-green algal supplements): a reasonable or misguided approach?. Toxicol. Appl. Pharmacol. 2005, 203:273-289.
23. Fischer W.J., Dietrich D.R. Toxicity of the cyanobacterial cyclic heptapeptide toxins microcystin-LR and -RR in early life-stages of the African clawed frog (Xenopus laevis). Aquat. Toxicol. 2000, 49:189-198.
24. Fischer W.J., Altheimer S., Cattori V., Meier P.J., Dietrich D.R., Hagenbuch B. Organic anion transporting polypeptides expressed in liver and brain mediate uptake of microcystin. Toxicol. Appl. Pharmacol. 2005, 203:257-263.
25. Fu J., Xie P. The acute effects of microcystin LR on the transcription of nine glutathione S transferase genes in common carp Cyprinus carpio. Aquat. Toxicol. 2005, 80:261-266.
26. Gagné F., Blaise C., Pellerin J., Pelletier E., Douville M., Gauthier-Clerc S., Viglino L. Sex alteration in solf-shell clams (Mya aernaria) in an interdidal zone of the St. Lawrence River (Québec, Canada). Comp. Biochem. Physiol. C 2003, 134:189-198.
27. Gagné F., André C., Blaise C. The dual nature of metallothioneins in the metabolism of heavy metals and reactive oxygen species in aquatic organisms: implications of use as a biomarker of heavy-metal effects in field investigations. Biochem Insights 2008, 1:31-41.
28. Gagné F., Gélinas M., Gagnon C., André C., Blaise C. Change in metallothionein phosphorylation state in Mya arenaria clams: implication in metal metabolism and oxidative stress. Invertebr. Surv. J. 2010, 7:22-31.
29. Ghazali I.E., Saqrane S., Carvalho A.P., Ouahid Y., Del Campos F.F., Vasconcelos V., Oudra B. Effects of the microcystin profile of a cyanobacterial bloom on growth and toxin accumulation in common carp Cyprinus carpio larvae. J. Fish Biol. 2010, 76:1415-1430.
30. Gowland B.T., McIntosh A.D., Davies I.M., Moffat C.F., Webster L. Implications from a field study regarding the relationship between polycyclic aromatic hydrocarbons and glutathione S-transferase activity in mussels. Mar. Environ. Res. 2002, 54:231-235.
31. Hagenbuch B., Meier P.J. The superfamily of organic anion transporting polypeptides. Biochim. Biophys. Acta 2003, 1609:1-18.
32. Jiang J., Gu X., Song R., Zhang Q., Geng J., Wand X., Yang L. Time-dependent oxidative stress and histopathological changes in Cyprinus carpio L. exposed to microcystin-LR. Ecotoxicology 2011, 20:1000-1009.
33. Kim H.G., Hwang Y.P., Han E.H., Choi C.Y., Yeo C.Y., Kim J.Y., Lee K.Y., Jeong H.G. Metallothionein-III provides neuronal protection through activation of Nuclear Factor-{kappa}B via theTrkA/Phosphatidylinositol-3 kinase Akt signaling pathway. Toxicol. Sci. 2009, 112:435-449.
34. Li X., Lui Y., Song L., Liu J. Responses of antioxidant systems in the hepatocytes of common carp (Cyprinus crapio L.) to the toxicity of microcystin-LR. Toxicon 2003, 42:85-89.
35. Li L., Xie P., Chen J. Biochemical and ultrastructural changes of the liver and kidney of the phytoplanktivorous silver carp feeding naturally on toxic Microcystis blooms in Thaihu lake China. Toxicon 2007, 49:1042-1053.
36. Li G., Xie P., Fu J., Hao L., Xiong Q., Li H. Microcystin-induces variations in transcription of GSTs in an omnivorous freshwater fish, goldfish. Aquat. Toxicol. 2008, 88:75-80.
37. Li L., Xie P., Guo L. Antioxidant response in liver of the phytoplanktovorous bighead carp (Aristichthys nobilis) intraperitoneally-injected with extracted microcystins. Fish Physiol. Biochem. 2010, 36:165-172.
38. Liu Y., Song L., Li X., Liu T. The toxic effects of MC-LR on embryo-larval and juvenile development of loach, Misguruns mizolepis Gunthe. Toxicon 2002, 40:395-399.
39. Malbrouck C., Kestemont P. Effects of microcystins on fish. Environ. Toxicol. Chem. 2006, 25:72-86.
40. Malbrouck C., Trausch G., Devois P., Kestemon P. Hepatic accumulation and effects of microcystin-LR on juvenile goldfish Carassius auratus. Comp. Biochem. Physiol. C 2003, 135:39-48.
41. Martins J.C., Vasconcelos V.M. Microcystin dynamics in aquatic organisms. J. Toxicol. Environ. Health B 2009, 12:65-82.
42. Mezhoud K., Praseuth D., Puiseaux-Dao S., François J.-C., Bernard C., Edery M. Global quantitative analysis of protein expression and phosphorylation status in the liver of the medaka fish (Orizias latipes) exposed to microcystin-LR: I. Balneation study. Aquat. Toxicol. 2008, 86:166-175.
43. Mohamed Z.A., Carmichael W.W., Hussein A.A. Estimation of microcystins in the freshwater fish Oreochromis niloticus in an Egyptian fish farm containing a Microcystis bloom. Environ. Toxicol. 2003, 18:137-141.
44. Oberemm A., Becker J., Codd G.A., Steinberg C. Effects of microcystin-LR and cyanobacteria crude extracts on embryo-larval development of zebrafish (Danio rerio). Wat Res. 1997, 31:2918-2921.
45. Perceval O., Couillard Y., Pinel-Alloul B., Giguère A., Campbell P.G.C. Metal-induced stress in bivalves living along a gradient of Cd contamination: relating sub-cellular metal distribution to population-level responses. Aquat. Toxicol. 2004, 69:327-345.
46. Pflugmacher S., Wiegand C., Oberemm A., Beattie K.A., Krause E., Cod G.A., Steinberg C.E.W. Identification of an enzymatically formed glutathione conjugate of the cyanobacterial hepatotoxin microcystin-LR: The first step of detoxification. Biochim. Biophys. Acta 1998, 1425:527-533.
47. Prieto A.I., Jos A., Pichardo S., Moreno I.M., Caméan A.M. Differential oxidative stress responses to microcystins LR and RR in intraperitoneally exposed tilapia fish (Oreochromis sp.). Aquat. Toxicol. 2006, 77:314-321. 10.1016/j.aquatox.2005.12.012.
48. Prieto A.I., Pichardo S., Jos A., Moreno I.M., Caméan A.M. Time dependent oxidative stress responses after acute exposure to toxic cyanobacterial cells containing microcystins in tilapia fish (Oreochromis niloticus) under laboratory conditions. Aquat. Toxicol. 2007, 84:337-345. 10.1016/j.aquatox.2007.06.012.
49. Puerto M., Prieto A., Pichardo S., Moreno I., Jos A., Moyano R., Caméan A.M. Effects of dietary acetylcysteine on the oxidative stress induced in tilapia (Oreochromis niloticus) exposed to a microcystin-producing cyanobacterial water bloom. Environ. Toxicol. Chem. 2009, 28:1679-1686.
50. Quinn B., Gagné F., Blaise C. Oxidative metabolism activity in Hydra attenuata exposed to carbamazepine. Fresenius Environ. Bull. 2004, 13:783-788.
51. Rolland A., Bird D., Giani A. Seasonal changes in composition of the cyanobacterial community and the occurrence of hepatotoxic blooms in the eastern townships, Québec, Canada. J. Plankton Res. 2005, 27:683-694.
52. Runnegar M., Berndt N., Kaplowitz N. Microcystin uptake and inhibition of protein phosphatases: effects of chemoprotectants and self-inhibition in relation to known hepatic transporters. Toxicol. Appl. Pharmacol. 1995, 134:264-272.
53. Sherman A.D. Isolation of metabolically distinct synaptosomes on Percoll gradients. Neurochem. Res. 1989, 14:97-101.
54. Stanton M.G. Colorimetric determination of inorganic phosphate in the presence of biological material and adenosine triphosphate. Anal. Biochem. 1968, 22:27-34.
55. Thomas P.E., Ryan D., Levin W. Improved staining procedure for the detection of the peroxidase activity of cytochrome P450 on sodium dodecyl sulfate polyacrylamide gels. Anal. Biochem. 1976, 75:168-176.
56. Viarengo A., Ponzanon E., Dondero F., Fabbri R. A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antarctic molluscs. Mar. Environ. Res. 1997, 44:69-84.
57. Vinagre T.M., Aciati J.C., Yunes J.S., Richards J., Bianchini A., Monserrat J.M. Effects of extracts from the cyanobacterium Microcystis aeruginosa on ion regulation and gill Na+, K+-ATPase and K+ dependent phosphatase activities of the estuarine crab Chasmagnathus granulata (Decapoda, Grapsidae). Physiol. Biochem. Zool. 2002, 75:600-608.
58. Vinagre T.M., Alciati J.C., Regoli F., Bocchetti R., Yunes J.S., Bianchini A., Monserrat J.M. Effect of microcystin on ion regulation and antioxidant system in gills of the estuarine crab Chasmagnathus granulatus (Decapoda, Grapsidae). Comp. Biochem. Physiol. C 2003, 135:67-75.
59. Wiegand C., Pflugmacher S. Ecotoxicological effects of selected cyanobacterial secondary metabolites a short review. Toxicol. Appl. Pharmacol. 2005, 203:201-208.
60. Wills E.D. Evaluation of lipid peroxidation in lipids and biological membranes. Biochemical Toxicology: A Practical Approach 1987, 127-150. IRL Press, Washington D.C. K. Snell, B. Mullock (Eds.).
61. Xie L., Xie P., Guo L., Li L., Miyabara Y., Park H.-D. Organ distribution and bioaccumulation of microcystins in freshwater fish at different trophic levels from the eutrophic Lake Chaohu, China. Environ. Toxicol. 2005, 20:293-300.
62. Zhang X., Xie P., Wang W., Li D., Li L., Tang R., Lei H., Shi Z. Dose-dependent effects of extracted microcystins on embryonic development, larval growth and histopathological changes of southern catfish (Silurus meridionalis). Toxicon 2008, 51:449-456.
63. Zhang D., Xie P., Chen J., Dai M., Qiu T., Liu Y., Liang G. Determination of microcystin-LR and its metabolites in snail (Bellamya aeruginosa, shrimps, (Macrobrachium nipponensis) and silver carp (Hypophthalmichthys molitrix) from Lake Taihu, China. Chemosphere 2009, 76:974-981.
64. Zhang X., Xie P., Li D., Tang R., Lei H., Zhao Y. Time-dependent oxidative stress responses of crucian carp (Carassius auratus) to intraperitoneal injection of extracted microcystins. Bull. Environ. Contam. Toxicol. 2009, 82:574-578.
65. Zhang X., Ji W., Zhang H., Zhang W., Xie P. Studies on the toxix effects of microcystin-LR on the zebrafish (Danio rerio) under different temperatures. J. Appl. Toxicol. 2011, 10.1002/jat.1597.
66. Zhao M., Xie S., Zhu Z., Yang Y., Gan N., Song L. Effect of dietary cyanobacteria on growth and accumulation of microcystins in Nile tilapia (Oreochromis niloticus). Aquaculture 2006, 261:960-966.