Studies on the toxic effects of microcystin-LR on the zebrafish (Danio rerio) under different temperatures

Journal of Applied Toxicology

Volumn 31, Issue 6, 2011, Pages 561-567

  Zhang, Xuezhen ^a   Ji, Wei ^b   Zhang, Huan ^a   Zhang, Wei ^a,b   Xie, Ping ^a,b  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF HYDROBIOLOGY   (China)

Author keywords

Glutathione S transferases; LD50; Microcystin LR; Real time PCR; Temperature; Zebrafish

Indexed keywords

GLUTATHIONE TRANSFERASE; MESSENGER RNA; MICROCYSTIN LR;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG DETOXIFICATION; DRUG EXPOSURE; DRUG RESPONSE; DRUG SENSITIVITY; DRUG TOLERANCE; LD 50; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL; TEMPERATURE SENSITIVITY; ZEBRA FISH;

GLUTATHIONE S-TRANSFERASES; LD50; MICROCYSTIN-LR; REAL-TIME PCR; TEMPERATURE; ZEBRAFISH;

ANIMALS; GLUTATHIONE TRANSFERASE; LETHAL DOSE 50; MALE; MICROCYSTINS; OXIDATIVE STRESS; TEMPERATURE; TOXICITY TESTS; ZEBRAFISH;

DANIO RERIO; MAMMALIA;

EID: 80052016545     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.1597     Document Type: Article

References (53)

1. Abele D, Burlando B, Viarengo A, Pörtner H-O. 1998. Exposure to elevated temperatures and hydrogen peroxide elicits oxidative stress and antioxidant response in the Antarctic intertidal limpet Nacella concinna. Comp. Biochem. Physiol. B 120: 425-435.
2. Andersen RJ, Luu HA, Chen DZX, Holmes CFB, Kent ML, Le Blanc M, Taylor FJR, Williams DE. 1993. Chemical and biological evidence links microcystins to salmon netpen liver disease. Toxicon 31: 1315-1323.
3. Baldia SF, Pagador GE, Kawai K, Nishijima T, Harada K. 2002. Effects of miceocystin-LR, a cyclic heptapetide toxin from the cyanobacterium Microcystis aeruginosa, on the freshwater ornamental fish Carassius auratus. 5th International Symposium on Sediment Quality Assessment, 16-18 October 2002, Chicago, IL, USA.
4. Best JH, Pflugmacher S, Wiegand C, Eddy FB, Metcalf JS, Codd GA. 2002. Effects of enteric bacterial and cyanobacterial lipopolysaccharides, and of microcystin-LR, on glutathione-S- transferase activities in zebra fish (Danio rerio). Aquat. Toxicol. 60: 223-231.
5. Blanchette B, Feng X, Singh BR. 2007. Marine glutathione S-transferases. Mar. Biotechnol. 23: 513-542.
6. Buetler TM, Gallagher EP, Wang C, Stahl DL, Hayes JD, Eaton DL. 1995. Induction of phase I and phase II drug-metabolizing enzyme mRNA, protein, and activity by BHA, ethoxyquin and oltipraz. Toxicol. Appl. Pharmacol. 135: 45-57.
7. Chen J, Xie P, Li L, Xu J. 2009. First identification of the hepatotoxic microcystins in the serum of a chronically exposed human population together with indication of hepatocellular damage. Toxicol. Sci. 108: 81-89.
8. Doi AM, Pham RT, Hughes EM, Barber DS, Gallagher EP. 2004. Molecular cloning and characterization of a glutathione S-transferase from largemouth bass (Micropterus salmoides) liver that is involved in the detoxification of 4- hydroxynonenal. Biochem. Pharmacol. 67: 2129-2139.
9. Falconer IR, Yeung DSK. 1992. Cytoskeletal changes in hepatocytes induced by Microcystis toxins and their relation to hyperphosphorylation of cell proteins. Chem. Biol. Interact. 81: 181-196.
10. Fastner J, Codd GA, Metcalf JS, Woitke P, Wiedner C, Utkilen H. 2002. An international intercomparison exercise for the determination of purified microcystin-LR and microcystins in cyanobacterial field material. Anal. Biochem. Chem. 374: 437-444.
11. Fischer WJ, Dietrich DR. 2000. Pathological and biochemical characterization of microcystins- induced hepatopancreas and kidney damage in carp (Cyprinus carpio). Toxicol. Appl. Pharmacol. 164: 73-81.
12. Frova C. 2006. Glutathione transferases in the genomics era: new insights and perspectives. Biomol. Eng. 23: 149-169.
13. Fu J, Xie P. 2006. The acute effects of microcystin LR on the transcription of nine glutathione S-transferase genes incommoncarp Cyprinus carpio L. Aquat. Toxicol. 80: 261-266.
14. Gehringer MM, Shephard EG, Downing TG, Wiegand C, Neilan BA. 2004. An investigation into the detoxification of microcystin-LR by the glutathione pathway in BALB/C mice. Int. J. Biochem. Cell Biol. 36: 931-941.
15. Gordon CJ. 2005. Temperature and Toxicology: An Integrative, Comparative and Environmental Approach. Taylor and Francis: Boca Raton, FL.
16. Hao L, Xie P, Fu J, Li G, Xiong Q, Li H. 2008. The effect of cyanobacterial crude extract on the transcription of GST mu, GST kappa and GST rho in different organs of goldfish (Carassius auratus). Aquat. Toxicol. 90: 1-7.
17. Hayes JD, Flanangan JU, Jowsey IR. 2005. Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 45: 51-88.
18. He J, He Z, Guo Q. 1997. The toxicity of Microcystis aeruginosa to fishes and daphnia. J. Lake Sci. 9: 49-56.
19. Ibelings BW, Bruning K, Jonge J de, Wolfstein K, Pires LMD, Postma J, Burger T. 2005. Distribution of microcystins in a lake foodweb: no evidence for biomagnification. Microb. Ecol. 49: 487-500.
20. Ito E, Takai A, Kondo F, Masui H, Imanishi S, Harada K. 2002. Comparison of protein phosphatase inhibitory activity and apparent toxicity of microcystins and related compounds. Toxicon 40: 1017-1025.
21. Kim M, Ahn IY, Cheon J, Park H. 2009. Molecular cloning and thermal stress-induced expression of a pi-class glutathione S-transferase (GST) in the Antarctic bivalve Laternula elliptica. Comp. Biochem. Physiol. A 152: 207-213.
22. Kleinow KM, Johnston BD, Holmes EP, McCarrol ME. 2006. Rhodamine 123 permeability through the catfish intestinal wall: relationship to thermal acclimation and acute temperature change. Comp. Biochem. Physiol. C 144: 205-215.
23. Konishi T, Kato K, Araki T, Shiraki K, Takagi M, Tamaru Y. 2005. Molecular cloning and characterization of a-class glutathione S-transferase genes from the hepatopancreas of red sea bream, Pagrus major. Comp. Biochem. Physiol. C 140: 309-320.
24. Kotak BJ, Semalulu S, Friytz DL, Prepas EE, Hrudey SE, Coppock RW. 1996. Hepatic and renal pathology of intraperitoneally administered microcystin-LR in rainbow trout (Oncorhynchus mykiss). Toxicon 34: 517-525.
25. Lawrence C. 2007. The husbandry of zebrafish (Danio rerio): a review. Aquaculture 269: 1-20.
26. Lee YM, Seo JS, Jung SO, Kim IC, Lee JS. 2006. Molecular cloning and characterization of theta-class glutathione S-transferase (GST-T) from the hermaphroditic fish Rivulus marmoratus and biochemical comparisons with alpha-class glutathione S-transferase (GST-A). Biochem. Biophys. Res. Commun. 346: 1053-1061.
27. Lei H, Xie P, Chen J, Liang G, Dai M, Zhang X. 2008. Distribution of toxins in various tissues of crucian carp intraperitoneally injected with hepatotoxic microcystins. Environ. Toxicol. Chem. 27: 1167-1174.
28. Li G, Xie P, Fu J, Hao L, Xiong Q, Li H. 2008. Microcystin-induced variations in transcription of GSTs in an omnivorous freshwater fish, goldfish. Aquat. Toxicol. 88: 75-80.
29. Liang XF, Li GG, He S, Huang Y. 2007. Transcriptional responses of alpha- and rho-class glutathione S-transferase genes in the liver of three freshwater fishes intraperitoneally injectedwith microcystin-LR: relationship of inducible expression and tolerance. J. Biochem. Mol. Toxicol. 21: 289-298.
30. Linthicum DS, Carey FG. 1972. Regulation of brain and eye temperatures by the bluefin tuna. Comp. Biochem. Physiol. A 43: 425-433.
31. Malbrouck C, Kestemont P. 2006. Effects of microcystins on fish. Environ. Toxicol. Chem. 25: 72-86.
32. Malbrouck C, Trausch G, Devos P, Kestemont P. 2003. Hepatic accumulation and effects of microcystin-LR on juvenile goldfish Carassius auratus L. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 135: 39-48.
33. Malek RL, Sajadia H, Abraham J, Grundy MA, Gerhard GS. 2004. The effects of temperature reduction on gene expression and oxidative stress in skeletal muscle from adult zebrafish. Comp. Biochem. Physiol. C 138: 363-373.
34. Matthews M, Trevarrow B, Matthews J. 2002. Avirtual tour of the guide for zebrafish users. Lab. Anim. 31: 34-40.
35. Paerl HW, Fulton RS, Moisander PH, Dyble J. 2001. Harmful freshwater algal blooms, with an emphasis on cyanobacteria. Sci. World J. 1: 76-113.
36. Pflugmacher S, Wiegand C, Oberemm A, Beattie KA, Krause E, Codd GA, Steinberg C. 1998. Identification of an enzymatically-formed glutathione conjugate of the cyanobacterial hepatotoxin microcystin-LR: the first step of detoxification. Biochem. Biophys. Acta 1425: 527-533.
37. Pouria S, Andrade A de, Barbosa J, Cavalcanti RL, Barreto VTS, Ward CJ, Preiser W, Poon GK, Neild GH, Codd GA. 1998. Fatal microcystin intoxication in haemodialysis unit in Caruaru, Brazil. The Lancet 352: 21-26.
38. Prieto AI, Jos A, Pichardo S, Moreno IM, Caméan AM. 2006. Differential oxidative stress responses to microcystins LR and RR in intraperitoneally exposed tilapia fish (Oreochromis sp.). Aquat. Toxicol. 77: 314-321.
39. Råbergh CMI, Bylund G, Eriksson JE. 1991. Histopathological effects of microcystin-LR, a cyclic peptide toxin from the cyanobacterium (blue-green alga) Microcystis aeruginosa on common carp (Cyprinus carpio L.). Aquat. Toxicol. 20: 131-146.
40. Runnegar M, Gerdes R, Falconer I. 1991. The uptake of the cyanobacterial hepatotoxin microcystin by isolated rat hepatocytes. Toxicon 29: 43-51.
41. Schaefer J, Ryan A. 2006. Developmental plasticity in the thermal tolerance of zebrafish Danio rerio. J. Fish Biol. 69: 722-734.
42. Šetlíková I, Wiegand C. 2009. Hepatic and branchial glutathione S-transferases of two fish species: Substrate specificity and biotransformation of microcystin-LR. Comp. Biochem. Physiol C 149: 515-523.
43. Sheehan D, Meade G, Foley VM, Dowd CA. 2001. Structure, function and evolution of glutathione transferases: implications for classification of nonmammalian members of an ancient enzyme superfamily. Biochem. J. 360: 1-16.
44. Sokolova IM, Lannig G. 2008. Interactive effects ofmetal pollution and temperature on metabolism in aquatic ectotherms: implications of global climate change. Climate Res. 37: 181-201.
45. Tencalla FG, Dietrich DR, Schattler C. 1994. Toxicity of Microcystis aeruginosa peptide toxin to yearling rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 30: 215-224.
46. Trute M, Gallis B, Doneanu C, Shaffer S, Goodlett D, Gallagher E. 2007. Characterization of hepatic glutathione S-transferases in coho salmon (Oncorhynchus kisutch). Aquat. Toxicol. 81: 126-136.
47. Vajcová V, Navrati S, Palikova M. 1998. The effect of intraperitoneally applied pure microcystin-LR on haematological, biochemical and morphological indices of silver carp (Hypophthalmichthys molitrix Val.). Acta Vet. Brno 67: 281-287.
48. Wang L, Liang XF, Liao WQ, Lei LM, Han BP. 2006. Structural and functional characterization of microcystin detoxification-related liver genes in a phytoplanktivorous fish, Nile tilapia (Oreochromis niloticus). Comp. Biochem. Physiol. C 144: 216-227.
49. Williams DE, Kent ML, Andersen RJ, Klix H, Holmes CFB. 1995. Tissue distribution and clearance of tritium-labeled dihydromicrocystin-LR epimers administered to Atlantic salmon via intraperitoneal injection. Toxicon 33: 125-131.
50. Xie P. 2006. Microcystins in Aquatic Animals with Potential Risk to Human Health. Science Press: Bejing.
51. Zhang X, Xie P, Li D, Shi Z. 2007. Haematological and plasma biochemical responses of crucian carp (Carassius auratus) to intraperitoneal injection of extracted microcystins with the possible mechanisms of anemia. Toxicon 49: 1150-1157.
52. Zhang X, Xie P, Wang W, Li D, Li L, Tang R, Lei H, Shi Z. 2008. Dose dependent effects of extracted microcystins on embryonic development, larval growth and histopathological changes of southern catfish Silurus meridionalis. Toxicon 51: 449-456.
53. Zurawell RW, Chen H, Burke JM, Prepas EE. 2005. Hepatotoxic cyanobacteria: a review of the biological importance of microcystins in freshwater environments. J. Toxicol. Environ. Health B 8: 1-37.