Acute effects of pure cylindrospermopsin on the activity and transcription of antioxidant enzymes in tilapia (Oreochromis niloticus) exposed by gavage

Ecotoxicology

Volumn 20, Issue 8, 2011, Pages 1852-1860

  Puerto, María ^a   Jos, Angeles ^a   Pichardo, Silvia ^a   Gutiérrez Praena, Daniel ^a   Cameán, Ana M ^a  

^a Faculty of Pharmacy   (Spain)

Author keywords

Cyanotoxin; Cylindrospermopsin; Glutathione peroxidase; Glutathione S transferase

Indexed keywords

ANTIOXIDANT; BIOLOGICAL MARKER; CYLINDROSPERMOPSIN; GLUTATHIONE TRANSFERASE; MESSENGER RNA;

BIOMARKER; ENZYME ACTIVITY; GENE EXPRESSION; PATHOGENICITY; PERCIFORM; POLLUTION EFFECT; TOXICITY; TOXIN;

ACUTE TOXICITY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FEEDING; GENE; GENE ACTIVITY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GLUTATHIONE PEROXIDASE GENE; KIDNEY PARENCHYMA; LIPID PEROXIDATION; LIVER PARENCHYMA; NONHUMAN; NUCLEOTIDE SEQUENCE; OREOCHROMIS NILOTICUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SOLUBLE GLUTATHIONE S TRANSFERASE GENE; TOXICITY TESTING; TRANSCRIPTION INITIATION; WESTERN BLOTTING;

ANIMALS; ANTIOXIDANTS; CICHLIDS; ENZYMES; FRESH WATER; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; KIDNEY; LIPID PEROXIDATION; LIVER; REAL-TIME POLYMERASE CHAIN REACTION; TOXICITY TESTS, ACUTE; URACIL;

CYANOBACTERIA; OREOCHROMIS NILOTICUS; TILAPIA;

EID: 80054904581     PISSN: 09639292     EISSN: 15733017     Source Type: Journal    
DOI: 10.1007/s10646-011-0723-0     Document Type: Article

References (61)

1. JA Almeida YS Diniz SFG Marques LA Faine BO Ribas RC Burneiko ELB Novelli 2002 The use of oxidative stress responses as biomarkers in Nile tilapia (Oreochromis niloticus) exposed to in vivo cadmium contamination Environ Int 27 673 679 10.1016/S0160-4120(01)00127-1 1:CAS:528:DC%2BD38XislCrs70%3D (Pubitemid 34257504)
2. L Atencio J Moreno A Jos S Pichardo R Moyano A Blanco AM Cameán 2008 Dose-dependent antioxidant responses and pathological changes in tenca (Tinca tinca) after acute oral exposure to Microcystis under laboratory conditions Toxicon 52 1 12 10.1016/j.toxicon.2008.05.009 1:CAS:528: DC%2BD1cXpt1alt74%3D
3. R Banker S Carmeli O Hadas B Teltsch R Porat A Sukenik 1997 Identification of cylindrospermopsin in Aphanizomenon ovalisporum isolated from Lake Kinneret, Israel J Phycol 33 613 616 10.1111/j.0022-3646.1997.00613.x 1:CAS:528:DyaK2sXlvV2qtro%3D (Pubitemid 27383385)
4. R Banker S Carmeli B Teltsch A Sukenik 2000 7-epicylindrospermopsin, a toxic minor metabolite of the cyanobacterium Aphanizomenon ovalisporum from Lake Kinneret, Israel J Nat Prod 63 387 389 10.1021/np990498m 1:CAS:528: DC%2BD3cXhtlKjtLs%3D (Pubitemid 30173701)
5. JP Berry PDL Gibbs MC Schmale ML Saker 2009 Toxicity of cylindrospermopsin, and other apparent metabolites from Cylindrospermopsis raciborskii and Aphanizomenon ovalisporum, to the zebrafish (Danio rerio) embryo Toxicon 53 289 299 10.1016/j.toxicon.2008.11.016 1:CAS:528: DC%2BD1MXmvVOntA%3D%3D
6. M Birringer S Pilawa L Flohè 2002 Trends in selenium biochemistry Nat Pro. Re. 19 693 718 10.1039/b205802m 1:CAS:528:DC%2BD3sXos1ajtA%3D%3D (Pubitemid 36029227)
7. M Bradford 1976 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal Biochem 72 248 254 10.1016/0003-2697(76)90527-3 1:CAS:528: DyaE28XksVehtrY%3D
8. L Brient M Lengronne M Bormans J Fastner 2009 First occurrence of cylindrospermopsin in freshwater in France Environ Toxicol 24 415 420 10.1002/tox.20439 1:CAS:528:DC%2BD1MXotFCiurY%3D
9. J Cazenave MA Bistoni SF Pesce DA Wunderlin 2006 Differential detoxification and antioxidant response in diverse organs of Corydoras paleatus experimentally exposed to microcystin-RR Aquat Toxicol 76 1 12 10.1016/j.aquatox.2005.08.011 1:CAS:528:DC%2BD2MXht12ktb%2FJ (Pubitemid 41758443)
10. MWK Chong BSF Wong PKS Lam GR Shaw AA Seawright 2002 Toxicity and uptake mechanism of cylindrospermopsin and lophyrotomin in primary rat hepatocytes Toxicon 40 205 211 10.1016/S0041-0101(01)00228-8 1:CAS:528:DC%2BD3MXnvVyhsrk%3D (Pubitemid 33016550)
11. H Esterbauer KH Cheeseman 1990 Determination of aldehydic lipid peroxidation products: Malonaldehyde and 4-hydroxynonetal Methods Enzymol 186 407 421 10.1016/0076-6879(90)86134-H 1:CAS:528:DyaK3MXks1Olt7w%3D (Pubitemid 20279982)
12. IR Falconer 2007 Cyanobacterial toxins present in Microcystis aeruginosa extracts-more than microcystin! Toxicon 50 585 588 10.1016/j.toxicon.2007.03.023 1:CAS:528:DC%2BD2sXhtVSku7nL (Pubitemid 47368580)
13. IR Falconer SJ Hardy AR Humpage SM Froscio GJ Tozer PR Hawkins 1999 Hepatic and renal toxicity of the blue-green alga (cyanobacterium) Cylindrospermopsis raciborskii in male Swiss albino mice Environ Toxicol 14 143 150 10.1002/(SICI)1522-7278(199902)14:1<143::AID-TOX18>3.0.CO;2-H 1:CAS:528:DyaK1MXntl2jsg%3D%3D (Pubitemid 29151391)
14. A Fathaili ABR Jenhani C Moreira M Saker M Romdhane V Vasconcelos 2010 First observation of the potentially toxic and invasive cyanobacterium species Cylindrospermopsis raciborskii (Woloszynska) in Tunisian freshwaters: toxicity assessment and molecular characterization Fresen Environ Bull 19 1074 1083
15. V Fessard C Bernard 2003 Cell Alterations but no DNA strand breaks induced in vitro by cylindrospermopsin in CHO K1 cells Environ Toxicol 18 353 359 10.1002/tox.10136 1:CAS:528:DC%2BD3sXnvFOltb8%3D (Pubitemid 37258748)
16. J Fu P Xie 2006 The acute effects of microcystin LR on the transcription of nine glutathione S-transferase genes in common carp Cyprinus carpio L Aquat Toxicol 80 261 266 10.1016/j.aquatox.2006.09.003 1:CAS:528:DC%2BD28Xht1ersrzE (Pubitemid 44739060)
17. Gutiérrez-Praena D, Pichardo S, Jos A, Cameán AM (2011) Toxicity and glutathione implication in the effects observed by exposure of the liver fish cell line PLHC-1 to pure cylindrospermopsin. Ecotox Environ Safe. doi: 10.1016/j.ecoenv.2011.04.030
18. WH Habig MJ Pabst WB Jakoby 1974 Glutathione S-transferases: the first enzymatic step in mercapturic acid formation Biol Chem 249 7130 7139 1:CAS:528:DyaE2MXltlahtg%3D%3D
19. L Hao P Xie J Fu G Li Q Xiong H Li 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 10.1016/j.aquatox.2008.07.006 1:CAS:528:DC%2BD1cXht1ShsrrF
20. KI Harada I Ohtani K Iwamoto M Suzuki MF Watanabe M Watanabe K Terao 1994 Isolation of cylindrospermopsin from a cyanobacterium Umezekia natans and its screening method Toxicon 32 73 84 10.1016/0041-0101(94)90023-X 1:CAS:528:DyaK2cXht1Ogurw%3D (Pubitemid 24047963)
21. AR Humpage IR Falconer 2003 Oral toxicity of the cyanobacterial toxin cylindrospermopsin in male swiss albino mice: determination of no observed adverse effect level for deriving a drinking water guideline value Environ Toxicol 18 94 103 10.1002/tox.10104 1:CAS:528:DC%2BD3sXivVeksrg%3D (Pubitemid 44783326)
22. AR Humpage M Fenech P Thomas IR Falconer 2000 Micronucleus induction and chromosome loss in transformed human white cells indicate clastogenic and aneugenic action of the cyanobacterial toxin, cylindrospermopsin Mutat Res 472 155 161 1:CAS:528:DC%2BD3cXoslGntL4%3D
23. AR Humpage F Fontaine S Froscio P Burcham IR Falconer 2005 Cylindrospermopsin genotoxicity and cytotoxicity: role of cytochrome P-450 and oxidative stress J Toxicol Environ Health Part A 68 739 753 10.1080/ 15287390590925465 1:CAS:528:DC%2BD2MXks1Kiu7k%3D (Pubitemid 40734187)
24. P Jaiswal PK Singh R Prasanna 2008 Cyanobacterial bioactive molecules: an overview on their toxic properties Can J Microbiol 54 701 717 10.1139/W08-034 1:CAS:528:DC%2BD1cXhtVOmsrnM
25. S Kinnear 2010 Cylindrospermopsin: a decade of progress on bioaccumulation research Mar Drugs 8 542 564 10.3390/md8030542 1:CAS:528:DC%2BC3cXjsVeqs7k%3D
26. S Kinnear LD Fabbro LJ Duivenvoorden EMA Hibberd 2007 Multiple-organ yoxicity resulting from cylindrospermopsin exposure in tadpoles of the cane toad (Bufo marinus) Environ Toxicol 22 550 558 10.1002/tox.20299 1:CAS:528:DC%2BD2sXhtlems7jP (Pubitemid 350105965)
27. Kuiper-Goodman T, Falconer I, Fitzgerald J (1999) Human health aspects. In: Chorus I, Bartram MJ (eds) Toxic cyanobacteria in water. A guide to their public health consequences, monitoring and management. E & FN Spon, New York, pp 113-153
28. UK Laemmli 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 680 685 10.1038/227680a0 1:CAS:528:DC%2BD3MXlsFags7s%3D
29. A Lawrence RF Burk 1976 Glutathione peroxidase activity in selenium deficient rat liver Biochem Biophys Res Comm 71 952 958 10.1016/0006-291X(76) 90747-6 1:CAS:528:DyaE28XlsVWls7s%3D
30. MJ Leaver SG George 1998 A piscine glutathione S-transferase which efficiently conjugates the end-products of lipid peroxidation Mar Environ Res 46 71 74 10.1016/S0141-1136(97)00071-8 1:CAS:528:DyaK1cXmtVOjtr8%3D (Pubitemid 28434802)
31. R Li WW Carmichael S Brittain GK Eaglesham GR Shaw Y Liu MM Watanabe 2001 First report of the cyanotoxins cylindrospermopsin and deoxycylindrospermopsin from Raphidiopsis curvata J Phycol 37 1121 1126 10.1046/j.1529-8817.2001.01075.x 1:CAS:528:DC%2BD38XnsVygsw%3D%3D (Pubitemid 34067670)
32. G Li P Xie J Fu L Hao Q Xiong H Li 2008 Microcystin-induced variations in transcription of GSTs in an omnivorous freshwater fish, goldfish Aquat Toxicol 88 75 80 10.1016/j.aquatox.2008.03.007 1:CAS:528:DC%2BD1cXlslagsL8%3D
33. MA Maire E Bazin V Fessard C Rast AR Humpage P Vasseur 2010 Morphological cell transformation of Syrian hamster embryo (SHE) cells by the cyanotoxin, cylindrospermopsin Toxicon 55 1317 1322 10.1016/j.toxicon.2010.01.025 1:CAS:528:DC%2BC3cXkvVahtbg%3D
34. A Mate A Barfull AM Hermosa L Gomez-Amores CM Vazquez JM Planas 2006 Regulation of sodium-glucose cotransporter SGLT1 in the intestine of hypertensive rats Am J Physiol Regul Integr Comp Physiol 291 760 767 10.1152/ajpregu.00524.2005 (Pubitemid 44352360)
35. V Messineo S Melchiorre A Di Corcia P Gallo M Bruno 2010 Seasonal succession of Cylindrospermopsis raciborskii and Aphanizomenon ovalisporum blooms with cylindrospermopsin occurrence in the volcanic Lake Albano, Central Italy Environ Toxicol 25 18 27 1:CAS:528:DC%2BC3cXhslWrsLk%3D
36. RLG Norris GK Eaglesham G Pierens GR Shaw MJ Smith RK Chiswell AA Seawright MR Moore 1999 Deoxycylindropermopsin, an analog of cylindropermopsin from Cylindrospermopsis raciborskii Environ Toxicol 14 163 165 10.1002/(SICI)1522-7278(199902)14:1<163::AID-TOX21>3.0.CO;2-V 1:CAS:528:DyaK1MXntl2jsQ%3D%3D (Pubitemid 29151394)
37. RLG Norris AA Seawright GR Shaw P Senogles GK Eaglesham MJ Smith RK Chiswell MR Moore 2002 Hepatic xenobiotic metabolism of cylindrospermopsin in vivo in the mouse Toxicon 40 471 476 10.1016/S0041-0101(01)00243-4 1:CAS:528:DC%2BD3MXoslGgtrY%3D (Pubitemid 34014819)
38. I Ohtani RE Moore MTC Runnegar 1992 Cylindrospermopsin, a potent hepatotoxin from the blue-green alga Cylindrospermopsis raciborski J Am Chem Soc 144 7941 7942 10.1021/ja00046a067
39. HW Paerl J Huisman 2008 Blooms like it hot Science 4 57 58 10.1126/science.1155398 (Pubitemid 351492505)
40. AI Prieto A Jos S Pichardo I Moreno AM Cameán 2006 Differential oxidative stress responses to microcystins LR and RR in intraperitoneally exposed tilapia fish (Oreochromis sp.) Aquat Toxicol 77 314 321 10.1016/j.aquatox.2005.12.012 1:CAS:528:DC%2BD28XjvVWrtLg%3D
41. AI Prieto S Pichardo A Jos I Moreno AM Cameán 2007 Time dependent oxidative stress responses after acute exposure to toxic cyanobacterial cells containing microcystins in tilapia fish (Oreochromis niloticus) under laboratory conditions Aquat Toxicol 84 337 345 10.1016/j.aquatox.2007.06.012 1:CAS:528:DC%2BD2sXpt1Cmt78%3D (Pubitemid 47259537)
42. M Puerto AI Prieto S Pichardo I Moreno A Jos R Moyano AM Cameán 2009 Effects of dietary N-acetylcysteine (NAC) on the oxidative stress induced in tilapia (Oreochromis niloticus) exposed to a microcystin-producing cyanobacterial water bloom Environ Toxicol Chem 28 1679 1686 10.1897/08-520.1 1:CAS:528:DC%2BD1MXovFertrs%3D
43. M Puerto D Gutiérrez-Praena AI Prieto S Pichardo A Jos JL Miguel-Carrasco CM Vázquez A Cameán 2011 Subchronic effects of cyanobacterial cells on the transcription of antioxidant enzyme genes in tilapia (Oreochromis sp.) Ecotoxicology 20 479 490 10.1007/s10646-011-0600-x 1:CAS:528:DC%2BC3MXhvVWqtbc%3D
44. Puerto M, Jos A, Pichardo S, Moyano R, Blanco A, Cameán A (2011b) Effects on oxidative stress biomarkers and pathological changes in Tilapia (Oreochromis niloticus) exposed to acute doses of pure Cylindrospermopsin by gavage. Toxicol Pathol (in press)
45. A Quesada E Moreno D Carrasco T Paniagua L Wormer C De Hoyos A Sukenik 2006 Toxicity of Aphanizomenon ovalisporum (Cyanobacteria) in a Spanish water reservoir Eur J Phycol 41 39 45 10.1080/09670260500480926 1:CAS:528: DC%2BD28XisVaqtLk%3D (Pubitemid 43379203)
46. J Rücker A Stüken B Nixdorf J Fastner I Chorus C Wiedner 2007 Concentrations of particulate and dissolved cylindrospermopsin in 21 Aphanizomenon-dominated temperate lakes Toxicon 50 800 809 10.1016/j.toxicon. 2007.06.019 (Pubitemid 47454637)
47. MT Runnegar SM Kong YZ Zhong JL Ge SC Lu 1994 The role of glutathione in the toxicity of a novel cyanobacterial alkaloid cylindrospermopsin in cultured rat hepatocytes Biochem Biophys Res Commun 201 235 241 10.1006/bbrc.1994.1694 1:CAS:528:DyaK2cXktVaqurY%3D (Pubitemid 24213719)
48. MT Runnegar SM Kong YZ Zhong SC Lu 1995 Inhibition of reduced glutathione synthesis by cyanobacterial alkaloid cylindrospermopsin in cultured rat hepatocytes Biochem Pharmacol 49 219 225 10.1016/S0006-2952(94)00466-8 1:CAS:528:DyaK2MXjsVKhsLw%3D
49. ML Saker ICG Nogueira VM Vasconcelos 2004 Distribution and toxicity of Cylindrospermopsis raciborskii (Cyanobacteria) in Portuguese freshwaters Limnetica 23 145 152 (Pubitemid 40875777)
50. AA Seawright CC Nolan GR Shaw RK Chiswell RL Norris MR Moore MJ Smith 1999 The oral toxicity for mice of the tropical cyanobacterium Cylindrospermopsis raciborskii (Woloszynska) Environ Toxicol 14 135 142 10.1002/(SICI)1522-7278(199902)14:1<135::AID-TOX17>3.0.CO;2-L 1:CAS:528:DyaK1MXntlyquw%3D%3D (Pubitemid 29151390)
51. M Seifert G McGregor G Eaglesham W Wickramasinghe G Shaw 2007 First evidence for the production of cylindrospermopsin and deoxy-cylindrospermopsin by the freshwater benthic cyanobacterium, Lyngbya wollei Harmful Algae 6 73 80 10.1016/j.hal.2006.07.001 1:CAS:528:DC%2BD2sXitVehurw%3D (Pubitemid 46038239)
52. GR Shaw AA Seawright MA Moore PKS Lam 2000 Cylindrospermopsin, a cyanobacterial alkaloid: evaluation of its toxicological activity Ther Drug Monit 22 89 92 10.1097/00007691-200002000-00019 1:CAS:528:DC%2BD3cXhtlajt7k%3D (Pubitemid 30083105)
53. Silva RC, Neto F, Oliveira CA, Azevedo SMFO, Magalhaes VF (2010) Cylindrospermopsin effects on primary cultured hepatocytes of the neotropical fish Hoplias malabaricus. The 8th International Conference on Toxic Cyanobacteria. Aug 29th-Sep 4th, Istanbul, p 188
54. Y Sun R Tang D Li X Zhang J Fu P Xie 2008 Acute effects of Microcystins on the transcription of antioxidant enzyme genes in crucian carp Carassius auratus Environ Toxicol 23 145 152 10.1002/tox.20317 1:CAS:528: DC%2BD1cXkt1CmsLo%3D (Pubitemid 351458203)
55. K Terao S Ohmori K Igarashi I Ohtani MF Watanabe KI Harada E Ito M Watanabe 1994 Electron microscopic studies on experimental poisoning in mice induced by cylindrospermopsin isolated from blue-green alga Umezakia natans Toxicon 32 833 843 10.1016/0041-0101(94)90008-6 1:CAS:528:DyaK2cXksFajtrw%3D (Pubitemid 24193482)
56. ME van Apeldoorn HP van Egmond GJA Speijers GJI Bakker 2007 Toxins of cyanobacteria Mol Nutr Food Res 51 7 60 10.1002/mnfr.200600185 (Pubitemid 46144763)
57. P Vernet E Rock A Mazur Y Rayssiguier JP Dufaure JR Drevet 1999 Selenium-independent epididymis-restricted glutathione peroxidase 5 protein (GPX5) can back up failing Se-dependent GPXs in mice subjected to selenium deficiency Mol Reprod Dev 54 362 370 10.1002/(SICI)1098-2795(199912)54:4<362: :AID-MRD6>3.0.CO;2-# 1:CAS:528:DyaK1MXntFCltLs%3D (Pubitemid 29519865)
58. L Wang XF Liang WQ Liao LM Lei BP Han 2006 Structural and functional characterization of microcystin detoxification-related liver genes in a phytoplanktivorous fish, Nile tilapia (Oreochromis niloticus) Comp Biochem Physiol Part C 144 216 227 (Pubitemid 44834350)
59. SH White LJ Duivenvoorden LD Fabbro GK Eaglesham 2007 Mortality and toxin bioaccumulation in Bufo marinus following exposure to Cylindrospermopsis raciborskii cell extracts and live cultures Environ Pollut 147 158 167 10.1016/j.envpol.2006.08.010 1:CAS:528:DC%2BD2sXisVWntbk%3D
60. C Wiegand S Pflugmacher A Oberemm C Steinberg 2000 Activity development of selected detoxification enzymes during the ontogenesis of the zebrafish (Danio rerio) Int Rev Hydrobiol 85 413 422 10.1002/1522-2632(200008)85:4<413: :AID-IROH413>3.0.CO;2-3 1:CAS:528:DC%2BD3cXmtl2qsb8%3D
61. F Yan WK Yang XY Li TT Lin YN Lun F Lin SW Lv GL Yan JQ Liu JC Shen Y Mu GM Luo 2008 A trifunctional enzyme with glutathione S-transferase, glutathione peroxidase and superoxide dismutase activity Biochim Biophys Acta 1780 869 872 1:CAS:528:DC%2BD1cXmtVSjurk%3D