The toxic effects of microcystin-LR on rat spermatogonia in vitro

Toxicology Letters

Volumn 212, Issue 1, 2012, Pages 48-56

  Zhou, Yuan ^a   Yuan, Jintao ^a   Wu, Jiang ^a   Han, Xiaodong ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

Cytotoxicity; Microcystin LR; Oatps; Oxidative stress; Spermatogonia; Transport

Indexed keywords

CALCIUM ION; MEMBRANE PROTEIN; MESSENGER RNA; MICROCYSTIN LR; ORGANIC ANION TRANSPORTING POLYPEPTIDE 1A4; ORGANIC ANION TRANSPORTING POLYPEPTIDE 1A5; ORGANIC ANION TRANSPORTING POLYPEPTIDE 2B1; ORGANIC ANION TRANSPORTING POLYPEPTIDE 3A1; ORGANIC ANION TRANSPORTING POLYPEPTIDE 6B1; ORGANIC ANION TRANSPORTING POLYPEPTIDE 6C1; ORGANIC ANION TRANSPORTING POLYPEPTIDE 6D1; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL VIABILITY; CONTROLLED STUDY; CYTOPLASM; FEMALE; IN VITRO STUDY; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPERMATOGONIUM; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; CELL SURVIVAL; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICROCYSTINS; MICROSCOPY, FLUORESCENCE; ORGANIC ANION TRANSPORTERS; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPERMATOGONIA; TESTIS;

CYANOBACTERIA; RATTUS;

EID: 84861467696     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2012.05.001     Document Type: Article

References (48)

1. Amirchaghmaghi M., Sedighi G.M. Isolation, purification and cryopreservation of type A spermatogonia from prepubertal rat testis. European Urology Supplements 2008, 7. 91-91.
2. Bellve A.R., Cavicchia J.C., Millette C.F., O'Brien D.A., Bhatnagar Y.M., Dym M. Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. Journal of Cell Biology 1977, 74:68-85.
3. Benzie I.F., Strain J.J. The ferric reducing ability of plasma (FRAP) as a measure of antioxidant power: the FRAP assay. Analytical Biochemistry 1996, 239:70-76.
4. 2 cells. Toxicon 2004, 43:85-92.
5. Campos A., Vasconcelos V. Molecular mechanisms of microcystin toxicity in animal cells. International Journal of Molecular Sciences 2010, 11:268-287.
6. Carey C.C., Haney J.F., Cottingham K.L. First report of microcystin-LR in the cyanobacterium Gloeotrichia echinulata. Environmental Toxicology 2007, 22:337-339.
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., Li L., Xu J. First identification of the hepatotoxic microcystins in the serum of a chronically exposed human population together with indication of hepatocellular damage. Toxicological Sciences 2009, 108:81-89.
9. Chen Y., Xu J., Li Y., Han X. Decline of sperm quality and testicular function in male mice during chronic low-dose exposure to microcystin-LR. Reproductive Toxicology 2011.
10. Craig M., Luu H.A., McCready T.L., Williams D., Andersen R.J., Holmes C.F. Molecular mechanisms underlying he interaction of motuporin and microcystins with type-1 and type-2A protein phosphatases. Biochemistry and Cell Biology-Biochimie et Biologie Cellulaire 1996, 74:569-578.
11. Dai M., Xie P., Liang G., Chen J., Lei H. Simultaneous determination of microcystin-LR and its glutathione conjugate in fish tissues by liquid chromatography-tandem mass spectrometry. Journal of Chromatography. B, Analytical Technologies in the Biomedical and Life Sciences 2008, 862:43-50.
12. Dietrich D., Hoeger S. Guidance values for microcystins in water and cyanobacterial supplement products (blue-green algal supplements): a reasonable or misguided approach?. Toxicology and Applied Pharmacology 2005, 203:273-289.
13. Ding W.X., Shen H.M., Ong C.N. Pivotal role of mitochondrial Ca(2+) in microcystin-induced mitochondrial permeability transition in rat hepatocytes. Biochemical and Biophysical Research Communications 2001, 285:1155-1161.
14. Dym M., Jia M.C., Dirami G., Price J.M., Rabin S.J., Mocchetti I., Ravindranath N. Expression of c-kit receptor and its autophosphorylation in immature rat type A spermatogonia. Biology of Reproduction 1995, 52:8-19.
15. Eriksson J.E., Gronberg L., Nygard S., Slotte J.P., Meriluoto J.A. Hepatocellular uptake of 3H-dihydromicrocystin-LR, a cyclic peptide toxin. Biochimica et Biophysica Acta 1990, 1025:60-66.
16. Feurstein D., Holst K., Fischer A., Dietrich D.R. Oatp-associated uptake and toxicity of microcystins in primary murine whole brain cells. Toxicology and Applied Pharmacology 2009, 234:247-255.
17. 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. Toxicology and Applied Pharmacology 2005, 203:257-263.
18. Gehringer M.M. Microcystin-LR and okadaic acid-induced cellular effects: a dualistic response. FEBS Letters 2004, 557:1-8.
19. Gkelis S., Harjunpaa V., Lanaras T., Sivonen K. Diversity of hepatotoxic microcystins and bioactive anabaenopeptins in cyanobacterial blooms from Greek freshwaters. Environmental Toxicology 2005, 20:249-256.
20. Guzman R.E., Solter P.F. Hepatic oxidative stress following prolonged sublethal microcystin LR exposure. Toxicologic Pathology 1999, 27:582-588.
21. Harada K. Recent advances of toxic cyanobacteria researches. Journal of Health Science 1999, 45:150-165.
22. Hong Y., Liu T., Zhao H., Xu H., Wang W., Liu R., Chen T., Deng J., Gui J. Establishment of a normal medakafish spermatogonial cell line capable of sperm production in vitro. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:8011-8016.
23. Izadyar F., Spierenberg G.T., Creemers L.B., den Ouden K., de Rooij D.G. Isolation and purification of type A spermatogonia from the bovine testis. Reproduction 2002, 124:85-94.
24. Javitt N.B. Hep G2 cells as a resource for metabolic studies: lipoprotein, cholesterol, and bile acids. FASEB Journal 1990, 4:161-168.
25. Klaassen C.D., Aleksunes L.M. Xenobiotic, bile acid, and cholesterol transporters: function and regulation. Pharmacological Reviews 2010, 62:1-96.
26. Komatsu M., Furukawa T., Ikeda R., Takumi S., Nong Q., Aoyama K., Akiyama S., Keppler D., Takeuchi T. Involvement of mitogen-activated protein kinase signaling pathways in microcystin-LR-induced apoptosis after its selective uptake mediated by OATP1B1 and OATP1B3. Toxicological Sciences 2007, 97:407-416.
27. Kubota H., Brinster R.L. Technology Insight: in vitro culture of spermatogonial stem cells and their potential therapeutic uses. Nature Clinical Practice Endocrinology 2006, 2:99-108.
28. Li Y., Sheng J., Sha J., Han X. The toxic effects of microcystin-LR on the reproductive system of male rats in vivo and in vitro. Reproductive Toxicology 2008, 26:239-245.
29. Meier-Abt F., Hammann-Hanni A., Stieger B., Ballatori N., Boyer J.L. The organic anion transport polypeptide 1d1 (Oatp1d1) mediates hepatocellular uptake of phalloidin and microcystin into skate liver. Toxicology and Applied Pharmacology 2007, 218:274-279.
30. Monks N.R., Liu S., Xu Y., Yu H., Bendelow A.S., Moscow J.A. Potent cytotoxicity of the phosphatase inhibitor microcystin LR and microcystin analogues in OATP1B1- and OATP1B3-expressing HeLa cells. Molecular Cancer Therapeutics 2007, 6:587-598.
31. Morena A.R., Boitani C., Pesce M., De Felici M., Stefanini M. Isolation of highly purified type A spermatogonia from prepubertal rat testis. Journal of Andrology 1996, 17:708-717.
32. Nong Q., Komatsu M., Izumo K., Indo H.P., Xu B., Aoyama K., Majima H.J., Horiuchi M., Morimoto K., Takeuchi T. Involvement of reactive oxygen species in microcystin-LR-induced cytogenotoxicity. Free Radical Research 2007, 41:1326-1337.
33. Pichardo S., Jos A., Zurita J.L., Salguero M., Camean A.M., Repetto G. Acute and subacute toxic effects produced by microcystin-YR on the fish cell lines RTG-2 and PLHC-1. Toxicology In Vitro 2007, 21:1460-1467.
34. Schrans-Stassen B.H., van de Kant H.J., de Rooij D.G., van Pelt A.M. Differential expression of c-kit in mouse undifferentiated and differentiating type A spermatogonia. Endocrinology 1999, 140:5894-5900.
35. Sicinska P., Bukowska B., Michalowicz J., Duda W. Damage of cell membrane and antioxidative system in human erythrocytes incubated with microcystin-LR in vitro. Toxicon 2006, 47:387-397.
36. Soares R.M., Cagido V.R., Ferraro R.B., Meyer-Fernandes J.R., Rocco P.R., Zin W.A., Azevedo S.M. Effects of microcystin-LR on mouse lungs. Toxicon 2007, 50:330-338.
37. Sohoni P., Tyler C.R., Hurd K., Caunter J., Hetheridge M., Williams T., Woods C., Evans M., Toy R., Gargas M., Sumpter J.P. Reproductive effects of long-term exposure to Bisphenol A in the fathead minnow (Pimephales promelas). Environmental Science and Technology 2001, 35:2917-2925.
38. Song L., Chen W., Peng L., Wan N., Gan N., Zhang X. Distribution and bioaccumulation of microcystins in water columns: a systematic investigation into the environmental fate and the risks associated with microcystins in Meiliang Bay, Lake Taihu. Water Research 2007, 41:2853-2864.
39. Sorrentino V., Giorgi M., Geremia R., Besmer P., Rossi P. Expression of the c-kit protooncogene in the murine male germ-cells. Oncogene 1991, 6:149-151.
40. Svircev Z., Baltic V., Gantar M., Jukovic M., Stojanovic D., Baltic M. Molecular aspects of microcystin-induced hepatotoxicity and hepatocarcinogenesis. Journal of Environmental Science and Health. Part C, Environmental Carcinogenesis & Ecotoxicology Reviews 2010, 28:39-59.
41. Swan S.H., Elkin E.P. Declining semen quality: can the past inform the present?. Bioessays 1999, 21:614-621.
42. Ueno Y., Nagata S., Tsutsumi T., Hasegawa A., Watanabe M.F., Park H.D., Chen G.C., Chen G., Yu S.Z. Detection of microcystins, a blue-green algal hepatotoxin, in drinking water sampled in Haimen and Fusui, endemic areas of primary liver cancer in China, by highly sensitive immunoassay. Carcinogenesis 1996, 17:1317-1321.
43. Vasconcelos V.M., Sivonen K., Evans W.R., Carmichael W.W., Namikoshi M. Hepatotoxic microcystin diversity in cyanobacterial blooms collected in portuguese freshwaters. Water Research 1996, 30:2377-2384.
44. Wang M., Wang D., Lin L., Hong H. Protein profiles in zebrafish (Danio rerio) brains exposed to chronic microcystin-LR. Chemosphere 2010, 81:716-724.
45. Watanabe M.F., Oishi S., Harda K., Matsuura K., Kawai H., Suzuki M. Toxins contained in Microcystis species of cyanobacteria (blue-green algae). Toxicon 1988, 26:1017-1025.
46. Watanabe M.F., Park H.D., Kondo F., Harada K., Hayashi H., Okino T. Identification and estimation of microcystins in freshwater mussels. Natural Toxins 1997, 5:31-35.
47. Weng D., Lu Y., Wei Y., Liu Y., Shen P. The role of ROS in microcystin-LR-induced hepatocyte apoptosis and liver injury in mice. Toxicology 2007, 232:15-23.
48. Yan C., Huang D., Zhang Y. The involvement of ROS overproduction and mitochondrial dysfunction in PBDE-47-induced apoptosis on Jurkat cells. Experimental and Toxicologic Pathology 2010.