Toxic effects of microcystin-LR on the reproductive system of male Rana nigromaculata in vitro

Aquatic Toxicology

Volumn 126, Issue , 2013, Pages 283-290

  Zhang, Hangjun ^a   Cai, Chenchen ^a   Wu, Yingzhu ^a   Ye, Binhui ^a   Han, Li ^a   Shou, Xiaolu ^a   Wang, Mengdi ^a   Wang, Jia ^a   Jia, Xiuying ^a  

^a HANGZHOU NORMAL UNIVERSITY   (China)

Author keywords

Frog; MCLR; Reproductive toxicity; Testis

Indexed keywords

AROMATASE; CATALASE; CELL PROTEIN; GLUTATHIONE; GLUTATHIONE TRANSFERASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MALONALDEHYDE; MICROCYSTIN LR; REACTIVE OXYGEN METABOLITE; STEROID HORMONE SYNTHESIS FACTOR 1; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ANTIOXIDANT; ENZYME; FROG; MITOCHONDRION; REPRODUCTIVE BIOLOGY; SPERM; TOXICITY;

ANIMAL CELL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; GLUTATHIONE METABOLISM; GOLGI COMPLEX; IN VITRO STUDY; MALE; MALE GENITAL SYSTEM; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RANA; RANA NIGROMACULATA; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCTIVE TOXICITY; SEMEN ABNORMALITY; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; ULTRASTRUCTURE;

ANIMALS; ENZYME ACTIVATION; ENZYMES; GENE EXPRESSION REGULATION; GENITALIA, MALE; MALE; MALONDIALDEHYDE; MICROCYSTINS; MICROSCOPY, ELECTRON, TRANSMISSION; RANIDAE; REACTIVE OXYGEN SPECIES; SERTOLI CELLS; SPERMATOZOA; WATER POLLUTANTS, CHEMICAL;

AMPHIBIA; ANURA; RANA NIGROMACULATA;

EID: 84871777035     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2012.09.017     Document Type: Article

References (52)

1. Alford R.A., Richards S.J. Global amphibian declines: a problem in applied ecology. Annual Review of Ecology and Systematics 1999, 30:133-165.
2. Battaglin W.A., Rice K.C., Focazio M.J. The occurrence of glyphosate, atrazine, and other pesticides in vernal pools and adjacent streams in Washington, DC, Maryland, Iowa, and Wyoming, 2005-2006. Environmental Monitoring and Assessment 2009, 155:281-307.
3. Boekelheide K., Fleming S.L., Johnson K.J.J., Sutchin R.P., Heidi A.S. Role of sertoli cells in injury associated testicular germ cell apoptosis. Proceedings of the Society for Experimental Biology and Medicine 2000, 225:105-115.
4. Boone M.D., Stacy M.J. Interactions of an insecticide, herbicide, and natural stressors in amphibian community mesocosms. Ecological Applications 2003, 13:829-841.
5. Brunberg A.K., Blomqvist P. Recruitment of microcystis (Cyanophyceae) from lake sediments: the importance of littoral inocula. Journal of Phycology 2003, 39:58-63.
6. Campos A., Vasconcelos V. Molecular mechanisms of microcystin toxicity in animal cells. International Journal of Molecular Sciences 2010, 11:268-287.
7. Chen J., Xie P. Tissue distributions and seasonal dynamics of the hepatotoxic microcystins-LR and -RR in two freshwater shrimps, Palaemon modestus and Macrobrachium nipponensis, from a large shallow, eutrophic lake of the subtropical China. Toxicon 2005, 45:615-625.
8. Chen J., Xie P., Guo L.G., Zheng L., Ni L.Y. Tissue distributions and seasonal dynamics of the hepatotoxic microcystins-LR and -RR in a freshwater snail (Bellamya aeruginosa) from a large shallow, eutrophic lake of the subtropical China. Environmental Pollution 2005, 134:423-430.
9. Chorus I., Bartram J. Toxic cyanobacteria in water, a guide to their public health consequences, monitoring and management, published by WHO 1999, Spon Press, London.
10. Cortizo A.M., Bruzzone L., Molinuevo S., Etcheverry S.B. A possible role of oxidative stress in the vanadium-induced cytotoxicity in the MC3T3E1 osteoblast and UMR 106 osteosaroma cell lines. Toxicology 2000, 147:89-99.
11. Curtin J.F., Donovan M., Cotter T.F. Regulation and measurement of oxidative stress in apoptosis. Journal of Immunological Methods 2002, 265:49-72.
12. de Figueiredo D.R., Azeiteiro U.M., Esteves S.M., Goncalves F.J., Pereira M.J. Microcystin-producing blooms-a serious global public health issue. Ecotoxicology and Environment Safety 2004, 59:151-163.
13. Ding X.S., Li X.Y., Duan H.Y., Chuan I.K., Lee J.A. Toxic effects of microcystis cell extracts on the reproductive system of male mice. Toxicon 2006, 48:973-979.
14. d'Istria M., Pmiero C., Serino I., Izzo G., Minucci S. Inhibition of the basal and oestradiol-stimulated mitotic activity of primary spermatogonia by melatonin in the testis of the frog, Rana esculenta, in vivo and in vitro. Reproduction 2003, 126:83-90.
15. Dong L., Zhang H.Z., Duan L.J., Cheng X.M., Cui L.X. Genotoxicity of testicle cell of mice induced by microcystin-LR. Life Science Journal 2008, 5:43-45.
16. Ernst B., Dietz L., Hoeger S.J., Dietrich D.R. Recovery of MC-LR in fish liver tissue. Environmental Toxicology 2005, 20:449-458.
17. Fan W.Q., Yanase T., Morinaga H., Gondo S., Okabe T., Nomura M., Hayes T.B., Tkayanagi R., Nawata H. Herbicide atrazine activates SF-1 by direct affinity and concomitant co-activators recruitments to induce aromatase expression via promoter II. Biochemical and Biophysical Research Communications 2007, 355:1012-1018.
18. 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). Aquatic Toxicology 2000, 49:189-198.
19. Gehringer M.M., Shephard E.G., Downing T.G., Wiegand C., Neilan B.A. An investigation into the detoxification of microcystin-LR by the glutathione pathway in Balb/c mice. International Journal of Biochemistry and Cell Biology 2004, 36:931-941.
20. Gerald A., Ellen M., Ralph S. Overview of a workshop on screening methods for detecting potential (anti-) estrogenic/androgenic chemicals in wildlife. Environmental Toxicology and Chemistry 1998, 17:68-87.
21. Gunderson M.P., Veldhoen N., Skirrow R.C., Macnab M.K., Ding W., van Aggelen G., Helbing C.C. Effect of low dose exposure to the herbicide atrazine and its metabolite on cytochrome P450 aromatase and steroidogenic factor-1 mRNA levels in the brain of premetamorphic bullfrog tadpoles (Rana catesbeiana). Aquatic Toxicology 2011, 102:31-38.
22. Hayes T.B., Falso P., Gallipeau S., Stice M. The cause of global amphibian declines: a developmental endocrinologist's perspective. Journal of Experimental Biology 2010, 213:921-933.
23. Hayes T.B., Khourya V., Narayana A. Atrazine induces complete feminization and chemical castration in male african clawed frogs (Xenopus laevis). Ecology 2010, 107:4612-4617.
24. Hyenstrand P., Rohrlack T., Beattie K.A., Metcalf J.S., Codd G.A., Christoffersen K. Laboratory studies of dissolved radiolabelled microcystin-LR in lake water. Water Research 2003, 37:3299-3306.
25. Jia X.Y., Wang M.Z., Shi C.L., Liu X.X. Effects of lead exposure on sperm toxicity and levels of sexual hormone in sera of male Rana nigromaculata. Acta Scientiae Circumstantiae 2009, 5:1072-1076.
26. Jiang J.P., Song R., Ren J.H., Wang X.R., Yang L.Y. Advances in pollution of cyanobacterial blooms-producing microcystins and their ecotoxicological effects on aquatic organisms. Progress in Inorganic Chemistry 2011, 23:247-253.
27. Joseph M., Kiesecker Andrew R., Blaustein Lisa, Belden K. Complex causes of amphibian population declines. Nature 2001, 401:681-683.
28. Kato T., Matsui K., Takase M., Kobayashi M., Nakamura M. Expression of P450 aromatase protein in developing and in sex-reversed gonads of the XX/XY type of the frog Rana rugosa. General and Comparative Endocrinology 2004, 137. pp 237-236.
29. Kaur P., Kaur G., Bansal M.P. Tertiary-butyl hydroperoxide induced oxidative stress and male reproductive activity in mice: role of transcription factor NF-kB and testicular antioxidant enzymes. Reproductive Toxicology 2006, 22:479-484.
30. Khan S.A., Wickstrom M.L., Haschek-Hock W.M., Schaeffer D.J., Ghosh S., Beasley B.R. Microcystin-LR-induced alterations in the cytoskeleton of cultured hepatocytes, kidney cells, and fibroblasts. Natural Toxins 1996, 4:217-220.
31. Li K.Y., Song L.R., Wan N. Studies on recruitment and growth characteristic of microcystis in sediment. Acta Hydrobiologica Sinica 2004, 28:113-117.
32. Li L., Xie P., Chen J. In vivo studies on toxin accumulation in liver and ultrastructural changes of hepatocytes of the phytoplanktivorous bighead carp i.p.-injected with extracted microcystins. Toxicon 2005, 46:533-545.
33. Li T., Huang P., Liang J., Fu W.Y., Guo Z.J. Microcystin-LR (MCLR) induces a compensation of PP2A activity mediated by α4 protein in HEK293 cells. International Journal of Biological Sciences 2011, 7:740-752.
34. Li X.Y., Liu Y.D., Song L.R. Cytological alterations in isolated hepatocytes from common carp (Cyprinus carpio L.) exposed to microcystin-LR. Environmental Toxicology 2001, 16:517-522.
35. Li X.Y., Liu Y.D., Song L.R., Liu J.T. Responses of antioxidant systems in the hepatocytes of common carp (Cyprinus carpio L.) to the toxicity of microcystin-LR. Toxicon 2003, 42:85-89.
36. Li Y., Sheng J., Sha J.H., Han X.D. The toxic effects of microcystin-LR on the reproductive system of male rats in vivo and in vitro. Reproductive Toxicology 2008, 26:239-245.
37. Liu Y., Xie P., Qiu T., Li H.Y., Li G.Y., Hao L., Xiong Q. Microcystin extracts induce ultrastructural damage and biochemical disturbance in male rabbit testis. Environmental Toxicology 2010, 25:9-17.
38. Loretta P.M., Stefanie L.O., Cheryl A.D., Catherine R.P. Sexually dimorphic expression of steroidogenic factor 1 (SF-1) in developing gonads of the American bullfrog, Rana catesbeiana. General and Comparative Endocrinology 2002, 127:40-47.
39. Luana Q., Ennio M., Oretta M., Massimo B. Effects of paraquat and glyphosate on steroidogenesis in gonads of the frog Rana esculenta in vitro. Pesticide Biochemistry and Physiology 2009, 93:91-95.
40. Milutinovic A., Sedmak B., Horvat-Znidarsic I., Suput D. Renal injuries induced by chronic intoxication with microcystins. Cellular and Molecular Biology Letters 2002, 7:139-141.
41. Oziol L., Bouaïcha N. First evidence of estrogenic potential of the cyanobacterial heptotoxins the nodularin-R and the microcystin-LR in cultured mammalian cells. Journal of Hazardous Materials 2010, 174:610-615.
42. Palen W.J., Schindlerb D.E. Water clarity, maternal behavior, and physiology combine to eliminate UV radiation risk to amphibians in a montane landscape. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:9701-9706.
43. Saradha B., Vaithinathan S., Mathur P.P. Lindane induces testicular apoptosis in adult Wistar rats through the involvement of Fas-FasL and mitochondria-dependent pathways. Toxicology 2009, 255:131-139.
44. Sieroslawska A., Rymuszka A., Bownik A., Skowroiiski T. The influence of microcystin-LR on fish phagocytic cells. Human and Experimental Toxicology 2007, 26:603-607.
45. Stuart S.N., Chanson J.S., Cox N.A., Young B.E., Rodrigues A.S.L., Fischman D.L., Waller R.W. Status and trends of amphibian declines and extinctions worldwide. Science 2004, 306:1783-1786.
46. van Apeldoorn M.E., Van Egmond H.P., Speijers G.J., Bakker G.J. Toxins of cyanobacteria. Molecular Nutrition and Food Research 2007, 51:7-60.
47. Wake D.B. Declining amphibian populations. Science 1991, 253:860.
48. Wickstrom M.L., Khan S.A., Haschek W.M., Wyman J.F., Eriksson J.E., Schaefer D.J., Beasley V.R. Alterations in microtubules, intermediate filaments, and microfilaments induced by microcystin-LR in cultured cells. Toxicologic Pathology 1995, 23:325-337.
49. Wu Z.J., Li Y.M. Causes and conservation strategies of amphibian population declination. Chinese Journal of Ecology 2004, 23:140-146.
50. Žegura B., Lah T.T., Filipič M. Alteration of intracellular GSH levels and its role in microcystin-LR-induced DNA damage in human hepatoma HepG2 cells. Mutation Research: Genetic Toxicology 2006, 611:25-33.
51. Zhang J.Y., Zhang H.Y., Chen Y.X. Sensitive apoptosis induced by microcystins in the crucian carp (Carassius auratus) lymphocytes in vitro. Toxicology in Vitro 2006, 20:560-566.
52. Zhou Z., Xie F., Jiang J., Zheng Z.H. Research advances of amphibian declines. Chinese Journal of Applied and Environmental Biology 2004, 10:128-132.