Regulatory effect of quercetin on hazardous microcystin-LR-induced apoptosis of Carassius auratus lymphocytes in vitro

Fish and Shellfish Immunology

Volumn 37, Issue 2, 2014, Pages 278-285

  Zhang, Hangjun ^a   Wu, Yingzhu ^a   Fang, Wendi ^a   Wang, Dandan ^a  

^a HANGZHOU NORMAL UNIVERSITY   (China)

Author keywords

Apoptosis; Detoxication effect; Microcystins; Oxidative stress; Quercetin

Indexed keywords

ANTIOXIDANT; MICROCYSTIN; MICROCYSTIN LR; QUERCETIN; REACTIVE OXYGEN METABOLITE; WATER POLLUTANT;

ANIMAL; APOPTOSIS; DRUG EFFECTS; GOLDFISH; LYMPHOCYTE; METABOLISM; OXIDATIVE STRESS; TOXICITY; WATER POLLUTANT;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; GOLDFISH; LYMPHOCYTES; MICROCYSTINS; OXIDATIVE STRESS; QUERCETIN; REACTIVE OXYGEN SPECIES; WATER POLLUTANTS, CHEMICAL;

EID: 84896090306     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2014.02.015     Document Type: Article

References (67)

1. Paerl H.W., Fulton R.S., Moisander P.H., Dyble J. Harmful freshwater algal blooms, with an emphasis on cyanobacteria. ScientificWorldJournal 2001, 1:76-113.
2. Lam A.K.Y., Prepas E.E., Spink D., Hrudey S.E. Chemical control of hepatotoxic phytoplankton blooms: implications for human health. Water Res 1995, 29:1845-1854.
3. Qiu T., Xie P., Kea Z.X., Li L., Guo L.G. In situ studies on physiological and biochemical responses of four fishes with different trophic levels to toxic cyanobacterial blooms in a large Chinese lake. Toxicon 2007, 50:365-376.
4. Duy T.N., Lam P.K.S., Shaw G.R., Connell D.W. Toxicology and risk assessment of fresh water cyanobacterial (Blue-green algae) toxins in water. Rev Environ Contam Toxicol 2000, 163:113-185.
5. Ressom R. Health effects of toxic cyanobacteria (blue-green algae) 1994, National Health and Medical Research Council.
6. Rao P.V.L., Bhattacharaya R., Parida M.M., Jana A.M., Bhaskar A.S. Freshwater cyanobacterium Microcystis aeruginosa (UTEX 2385) induced DNA damage invivo and invitro. Environ Toxicol Pharmacol 1998, 5:1-6.
7. 32P-postlabelling of 8-oxo-7,8-dihydro-2'-deoxyguanosine in DNA as biomarker of microcystin-LR- and nodularin-induced DNA damage invitro in primary cultured rat hepatocytes and invivo in rat liver. Mutat Res - Genet Toxicol Environ Mutagen 2004, 564:9-20.
8. Žegura B., Sedmak B., Filipič M. Microcystin-LR induces oxidative DNA damage in human hepatoma cell line HepG2. Toxicon 2003, 41:41-48.
9. Lankoff A., Krzowski L., Glab J., Banasik A., Lisowska H., Kuszewski T., et al. DNA damage and repair in human peripheral blood lymphocytes following treatment with microcystin-LR. Mutat Res - Genet Toxicol Environ Mutagen 2004, 559:131-142.
10. De Figeiredo D.R., Azeiteiro U.M., Esteves S.M., Gonçalves F.J.M., Pereira M.J. Microcystin-producing blooms - a serious global public health issue. Ecotoxicol Environ Saf 2004, 59:151-163.
11. Jayaraj R., Deb U., Bhaskar A.S.B., Prasad G.B.K.S., Rao P.V.L. Hepatoprotective efficacy of certain flavonoids against microcystin induced toxicity in mice. Environ Toxicol 2007, 22:472-479.
12. Fawell J.K., Mitchell R.E., Everett D.J., Hill R.E. The toxicity of cyanobacterial toxins in the mouse: I microcystin-LR. Hum Exp Toxicol 1999, 18:162-167.
13. Dawson R.M. The toxicology of microcystins. Toxicon 1998, 36:953-962.
14. Bouaïcha N., Maatouk I. Microcystin-LR and nodularin induce intracellular glutathione alteration, reactive oxygen species production and lipid peroxidation in primary cultured rat hepatocytes. Toxicol Lett 2004, 148:53-63.
15. Sicińska P., Bukowska B., Michałowicz J., Duda W. Damage of cell membrane and antioxidative system in human erythrocytes incubated with microcystin-LR invitro. Toxicon 2006, 47:387-397.
16. Ding W.X., Shen H.M., Ong C.N. Critical role of reactive oxygen species and mitochondrial permeability transition in microcystin-LR induced rapid apoptosis in primary rat hepatocytes. Hepatology 2000, 32:547-555.
17. Fu W.Y., Li M.W., Chen J.P., Xu L.H. Detection of apoptosis of renal cells of rat induced by microcystin-LR. Acta Hydrobiol Sin 2004, 28:101-102.
18. Fu W.Y., Chen J.P., Wang X.M., Hu L.H. Altered expression of p53, Bcl-2 and Bax induced by microcystin-LR invivo and invitro. Toxicon 2005, 46:171-177.
19. Qi L.H., Kang L.P., Zhang J.P., Shi N., Zhang M., Wu T.M. Antifibrotic effects of genistein and quercetin invitro. Acta Pharmacol Sin 2001, 36:648-651.
20. Zhang J.Y., Zhang H.J., Chen Y.X. Sensitive apoptosis induced by microcystins in the crucian carp (Carassius auratus) lymphocytes invitro. Toxicol InVitro 2006, 20:560-566.
21. Ding W.X., Shen H.M., Ong C.N. Calpain activation after mitochondrial permeability transition in microcystin-induced cell death in rat hepatocytes. Biochem Biophys Res Commun 2002, 291:321-331.
22. Ding W.X., Shen H.M., Ong C.N. Microcystic cyanobacteria extract induces cytoskeletal disruption and intracellular glutathione alteration in hepatocytes. Environ Health Perspect 2000, 108:605-609.
23. Hermansky S.J., Stohs S.J., Eldeen Z.M., Roche V.F., Mereish K.A. Evaluation of potential chemoprotectants against microcystin-LR hepatotoxicity in mice. JAppl Toxicol 1991, 11:65-73.
24. Xu C., Shu W.Q., Qiu Z.Q., Chen J.A., Zhao Q. Protective effects of green tea polyphenols against subacute hepatotoxicity induced by microcystin-LR in mice. Environ Toxicol Pharmacol 2007, 24:140-148.
25. Singh A., Naidu P.S., Kulkarni S.K. Reversal of aging and chronic ethanol-induced cognitive dysfunction by quercetin a bioflavonoid. Free Radic Res 2003, 37:1245-1252.
26. Liu C.M., Zheng Y.L., Lu J., Zhang Z.F., Fan S.H., Wu D.M., et al. Quercetin protects rat liver against lead-induced oxidative stress and apoptosis. Environ Toxicol Pharmacol 2010, 29:158-166.
27. Ansari M.A., Abdul H.M., Joshi G., Opii W.O., Butterfield D.A. Protective effect of quercetin in primary neurons against Abeta (1-42): relevance to Alzheimer's disease. JNutr Biochem 2009, 20:269-275.
28. Inal M.E., Akgun A., Kahraman A. Radioprotective effects of exogenous glutathione against whole-body gamma-ray irradiation: age- and gender-related changes in malondialdehyde levels, superoxide dismutase and catalase activities in rat liver. Methods Find Exp Clin Pharmacol 2002, 24:209-212.
29. Abdel-Raheem I.T., Abdel-Ghany A.A., Mohamed G.A. Protective effect of quercetin against gentamicin-induced nephrotoxicity in rats. Biol Pharm Bull 2009, 32:61-67.
30. Boots A.W., Haenen G.R., Bast A. Health effects of quercetin: from antioxidant to nutraceutical. Eur J Pharmacol 2008, 585:325-337.
31. Lugli E., Ferraresi R., Roat E., Troiano L., Troiano L., Pinti M., et al. Quercetin inhibits lymphocyte activation and proliferation without inducing apoptosis in peripheral mononuclear cells. Leuk Res 2009, 33:140-150.
32. Mercer L.D., Kelly B.L., Horne M.K., Beart P.M. Dietary polyphenols protect dopamine neurons from oxidative insults and apoptosis: investigations in primary rat mesencephalic cultures. Biochem Pharmacol 2005, 69:339-345.
33. Zhang H.J., Zhang J.Y., Zhu Y.M. Invitro investigations for the QSAR mechanism of lymphocytes apoptosis induced by substituted aromatic toxicants. Fish Shellfish Immunol 2008, 25:710-717.
34. Ferrari M., Fornasiero M.C., Isetta A.M. MTT colorimetric assay for testing macrophage cytotoxic activity invitro. JImmunol Methods 1990, 131:165-172.
35. Cathcart R., Schwiers E., Ames B.N. Detection of picomole levels of hydroperoxides using a fl{ligature}uorescent dichlorfl{ligature}uorescein assay. Anal Biochem 1983, 134:111-116.
36. Del Bino G., Lassota P., Darzynkiewicz Z. The S-phase cytotoxicity of camptothecin. Exp Cell Res 1991, 193:27-35.
37. Tavakkol-Afshari J., Brook A., Mousavi S.H. Study of cytotoxic and apoptogenic properties of saffron extract in human cancer cell lines. Food Chem Toxicol 2008, 46:3443-3447.
38. Das B.K., Ellis A.E., Collet B. Induction and persistence of Mx protein in tissues, blood and plasma of Atlantic salmon parr, Salmo salar, injected with poly I: C. Fish Shellfish Immunol 2009, 26:40-48.
39. R Core Team R: a language and environment for statistical computing 2012, R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
40. Hothorn T., Bretz F., Westfallm P. Simultaneous inference parametric models. Biom J 2008, 50:346-363.
41. Schaarschmidt F., Gerhard D., Sill M. MCPAN. Multiple comparisons using normal approximation, R package version 1.1-14 2012, http://cran.r-project.org/package=MCPAN.
42. Ding W.X., Ong C.N. Role of oxidative stress and mitochondrial changes in cyanobacteria-induced apoptosis and hepatotoxicity. FEMS Microbiol Lett 2003, 220:1-7.
43. Prieto A.I., Jos Á., Pichardo S., Moreno I., Cameán A.M. Protective role of vitamin E on the microcystin-induced oxidative stress in tilapia fish (Oreochromis niloticus). Environ Toxicol Chem 2008, 27:1152-1159.
44. Zhang H.J., Shao D.D., Wu Y.Z., Dai B.R., Cai C.C., Fang W.D., et al. Regulation of nodularin-induced apoptosis by epigallocatechin-3-gallate on fish lymphocytes invitro. Fish Shellfish Immunol 2013, 34:1085-1093.
45. Ding W.X., Shen H.M., Zhu H.G., Ong C.N. Studies on oxidative damage induced by cyanobacteria extract in primary cultured rat hepatocytes. Environ Res 1998, 78:12-18.
46. Patten D.A., Germain M., Kelly M.A., Slack R.S. Reactive oxygen species: stuck in the middle of neurodegeneration. JAlzheimers Dis 2010, 20:357-367.
47. Monteiro D.A., Rantin F.T., Kalinin A.L. The effects of selenium on oxidative stress biomarkers in the freshwater characid fish matrinxã (Brycon cephalus) (Günther, 1869) exposed to organophosphate insecticide Folisuper 600 BR (methyl parathion). Comp Biochem Physiol C Toxicol Pharmacol 2009, 149:40-49.
48. Li X., Liu Y., Song L., Liu J. Responses of antioxidant systems in the hepatocytes of common carp (Cyprinus carpio L) to the toxicity of microcystin-LR. Toxicon 2003, 42:85-89.
49. Rymuszka A., Skowronski T., Bownik A. Invitro effects of pure microcystin-LR on the lymphocyte proliferation in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 2007, 22:289-292.
50. Cazenave J., Bistoni M.A., Pesce S.F., 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.
51. Moreno I., Pichardo S., Gómez-Amores L., Mate A., Vazquez C.M., Cameán A.M. Antioxidant enzyme activity and lipid peroxidation in liver and kidney of rats exposed to microcystin-LR administered intraperitoneally. Toxicon 2005, 45:395-402.
52. Lima P.L., Benassi J.C., Pedrosa R.C., Dal Magro J., Oliveira T.B., Wilhelm Filho D. Time course variations of DNA damage and biomarkers of oxidative stress in tilapia (Orechromis niloticus) exposed to effluents from a swine industry. Arch Environ Contam Toxicol 2006, 50:23-30.
53. Sk U.H., Bhattacharya S. Prevention of cadmium induced lipid peroxidation, depletion of some antioxidative enzymes and glutathione by a series of novel organoselenocyanates. Environ Toxicol Pharmacol 2006, 22:298-308.
54. Xu L., Zhou B., Lam P.K.S., Chen J., Zhang Y., Harada K.I. Invivo protein phosphatase 2A inhibition and glutathione reduction by MC-LR in grass carp (Ctenopharyngodon idellus). Proceedings, ninth international conference on harmful algal blooms 2000, 7-11. Hobart, Australia.
55. Cazenave J., Nores M., Miceli M., Díaz M.P., Wunderlin D.A., Bistoni M.A. Changes in the swimming activity and the glutathione S-transferase activity of Jenynsia multidentata fed with microcystin-RR. Water Res 2008, 42:1299-1307.
56. Amado L.L., Garcia M.L., Pereira T.C.B., Yunes J.S., Bogoc M.R., Monserrat J.M. Chemoprotection of lipoic acid against microcystin-induced toxicosis in common carp (Cyprinus carpio, Cyprinidae). Comp Biochem Physiol C Toxicol Pharmacol 2011, 154:146-153.
57. Sarada S.K.S., Sairam M., Dipti P., Anju B., Pauline T., Kain A.K., et al. Role of selenium in reducing hypoxia-induced oxidative stress: an invivo study. Biomed Pharmacother 2002, 56:173-178.
58. Mcdermott C.M., Nho C.W., Howard W., Holton B. The cyanobacterial toxin, microcystin-LR can induce apoptosis in a variety of cell types. Toxicon 1998, 36:1981-1996.
59. Fladmark K.E., Brustugun O.T., Hovland R., Boe R., Gjertsen B.T., Zhivo-tovsky B., et al. Ultrarapid caspase-3 dependent apoptosis induction by serine/threonine phosphatase inhibitors. Cell Death Differ 1999, 6:1099-1108.
60. Hockenbery D., Nuñez G., Milliman C., Schreiber R.D., Korsmeyer S.J. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 1990, 348:334-336.
61. Cao X.G., Li X.X., Bao Y.Z., Xing N.Z., Chen Y. Responses of human lens epithelial cells to quercetin and DMSO. Invest Ophthalmol Vis Sci 2007, 48:3714-3718.
62. Chen Y., Li X.X., Xing N.Z., Cao X.G. Quercetin inhibits choroidal and retinal angiogenesis invitro. Graefes Arch Clin Exp Ophthalmol 2008, 246:373-378.
63. Kook D., Wolf A.H., Yu A.L., Neubauer A.S., Priglinger S.G., Kampik A., et al. The protective effect of quercetin against oxidative stress in the human RPE invitro. Invest Ophthalmol Vis Sci 2008, 49:1712-1720.
64. Selvakumar K., Bavithra S., Suganthi M., Benson C.S., Elumalai P., Arunkumar R., et al. Protective role of quercetin on PCBs-induced oxidative stress and apoptosis in hippocampus of adult rats. Neurochem Res 2012, 37:708-721.
65. Suematsu N., Hosoda M., Fujimori K. Protective effects of quercetin against hydrogen peroxide-induced apoptosis inhuman neuronal SH-SY5Y cells. Neurosci Lett 2011, 504:223-227.
66. De David C., Rodrigues G., Silvia Bona S., Meurer L., González-Gallego J., Tuñón M.J., et al. Role of quercetin in preventing thioacetamide-induced liver injury in rats. Toxicol Pathol 2011, 39:949-957.
67. Bournival J., Francoeur M.A., Renaud J., Martinoli M.G. Quercetin and sesamin protect neuronal pc12 cells from high-glucose-induced oxidation, nitrosative stress, and apoptosis. Rejuvenation Res 2012, 15:322-333.