Folia Biologica
Journal of Cellular and Molecular Biology, Charles University 

Crossref logo

Fol. Biol. 2005, 51, 62-67

https://doi.org/10.14712/fb2005051030062

Cytotoxicity and Apoptotic Effects of Microcystin-LR and Anatoxin-a in Mouse Lymphocytes

I. Teneva1, R. Mladenov1, N. Popov2, Balik M. Dzhambazov2,3

1Department of Botany, University of Plovdiv, Plovdiv, Bulgaria
2Cell Biology Laboratory, Department of Developmental Biology, University of Plovdiv, Plovdiv, Bulgaria
3Department of Experimental Medical Science, Division for Inflammation and Immunology, Lund University, Lund, Sweden

Received April 2005
Accepted April 2005

References

1. Botha, N., Gehringer, M. M., Downing, T. G., van de Venter, M., Shephard, E. G. (2004) The role of microcystin-LR in the induction of apoptosis and oxidative stress in CaCo2 cells. Toxicon 43, 85-92. <https://doi.org/10.1016/j.toxicon.2003.10.025>
2. Carmichael, W. W. (1994) The toxins of cyanobacteria. Sci. Am. 270, 78-86. <https://doi.org/10.1038/scientificamerican0194-78>
3. Carmichael, W. W., Biggs, D. F., Gorham, P. R. (1975) Toxicology and pharmacological action of anabaena flos-aquae toxin. Science 187, 542-544. <https://doi.org/10.1126/science.803708>
4. Chen, W., Wang, H. G., Srinivasula, S. M., Alnemri, E. S., Cooper, N. R. (1999) B cell apoptosis triggered by antigen receptor ligation proceeds via a novel caspase-dependent pathway. J. Immunol. 163, 2483-2491. <https://doi.org/10.4049/jimmunol.163.5.2483>
5. Dawson, R. M. (1998) The toxicology of microcystins. Toxicon 36, 953-962. <https://doi.org/10.1016/S0041-0101(97)00102-5>
6. Ding, W. X., Shen, H. M., Zhu, H. G., Ong, C. N. (1998) Studies on oxidative damage induced by cyanobacteria extract in primary cultured rat hepatocytes. Environ. Res. 78, 12-18. <https://doi.org/10.1006/enrs.1998.3843>
7. Ding, W. X., Shen, H. M., Ong, C. N. (2000) Critical role of reactive oxygen species and mitochondrial permeability transition in microcystin-induced rapid apoptosis in rat hepatocytes. Hepatology 32, 547-555. <https://doi.org/10.1053/jhep.2000.16183>
8. Ding, W. X., Shen, H. M., Ong, C. N. (2001) Critical role of reactive oxygen species formation in microcystin-induced cytoskeleton disruption in primary cultured hepatocytes. J. Toxicol. Environ. Health A 64, 507-519. <https://doi.org/10.1080/152873901753215966>
9. Ding, W. X., Shen, H., Ong, C. N. (2002) Calpain activation after mitochondrial permeability transition in microcystininduced cell death in rat hepatocytes. Biochem. Biophys. Res. Commun. 291, 321-331. <https://doi.org/10.1006/bbrc.2002.6453>
10. Edmondson, J. M., Armstrong, L. S., Martinez, A. O. (1988) A rapid and simple MTT-based spectrophotometric assay for determining drug sensitivity in monolayer cultures. J. Tissue Cult. Meth. 11, 15-17. <https://doi.org/10.1007/BF01404408>
11. Eriksson, J. E., Gronberg, L., Nygard, S. E., Slotte, J. P., Meriluoto, J. A. (1990) Hepatocellular uptake of 3H-dihydromicrocystin-LR, a cyclic peptide toxin. Biochim. Biophys. Acta 1025, 60-66. <https://doi.org/10.1016/0005-2736(90)90190-Y>
12. Eriksson, J. E., Brautigan, D. L., Vallee, R., Olmsted, J., Fujiki, H., Goldman, R. D. (1992) Cytoskeletal integrity in interphase cells requires protein phosphatase activity. Proc. Natl. Acad. Sci. USA 89, 11093-11097. <https://doi.org/10.1073/pnas.89.22.11093>
13. Falconer, I. R., Yeung, D. S. (1992) Cytoskeletal changes in hepatocytes induced by Microcystis toxins and their relation to hyperphosphorylation of cell proteins. Chem. Biol. Interact. 81, 181-196. <https://doi.org/10.1016/0009-2797(92)90033-H>
14. Falconer, I., Humpage, A. R. (1996) Tumour promotion by cyanobacterial toxins. Phycologia 35, 74-79. <https://doi.org/10.2216/i0031-8884-35-6S-74.1>
15. Fladmark, K. E., Brustugun, O. T., Hovland, R., Boe, R., Gjertsen, B. T., Zhivotovsky, B., Doskeland, S. O. (1999) Ultrarapid caspase 3 dependent apoptosis induction by serine/threonine phosphatase inhibitors. Cell Death Diff. 6, 1099-1108. <https://doi.org/10.1038/sj.cdd.4400590>
16. Fladmark, K. E., Brustugun, O. T., Mellgren, G., Krakstad, C., Boe, R., Vintermyr, O. K., Schulman, H., Doskeland, S. O. (2002) Ca2+/calmodulin-dependent protein kinase II is required for microcystin-induced apoptosis. J. Biol. Chem. 277, 2804-2811. <https://doi.org/10.1074/jbc.M109049200>
17. Graves, J. D., Draves, K. E., Craxton, A., Krebs, E. G., Clark, E. A. (1998) A comparison of signaling requirements for apoptosis of human B lymphocytes induced by the B cell receptor and CD95/Fas. J. Immunol. 161, 168-174. <https://doi.org/10.4049/jimmunol.161.1.168>
18. Hitzfeld, B. C., Hoger, S. J., Dietrich, D. R. (2000) Cyanobacterial toxins: removal during drinking water treatment, and human risk assessment. Environ. Health Perspect. 108 Suppl 1, 113-122.
19. Humpage, A. R., Hardy, S. J., Moore, E. J., Froscio, S. M., Falconer, I. R. (2000) Microcystins (cyanobacterial toxins) in drinking water enhance the growth of aberrant crypt foci in the mouse colon. J. Toxicol. Environ. Health A 61, 155-165.
20. Kerr, J. F. R., Wyllie, A. H., Currie, A. R. (1972) Apoptosis: a basic biological phenomenon with wide ranging implications in tissue kinetics. Br. J. Cancer 26, 239-257. <https://doi.org/10.1038/bjc.1972.33>
21. Lakshmana Rao, P. V., Bhattacharya, R., Gupta, N., Parida, M. M., Bhaskar, A. S., Dubey, R. (2002a) Involvement of caspase and reactive oxygen species in cyanobacterial toxin anatoxin-a-induced cytotoxicity and apoptosis in rat thymocytes and Vero cells. Arch. Toxicol. 76, 227-235. <https://doi.org/10.1007/s00204-002-0330-1>
22. Lakshmana Rao, P. V., Gupta, N., Bhaskar, A. S., Jayaraj, R. (2002b) Toxins and bioactive compounds from cyanobacteria and their implications on human health. J. Environ. Biol. 23, 215-224.
23. Lankoff, A., Carmichael, W. W., Grasman, K. A., Yuan, M. (2004a) The uptake kinetics and immunotoxic effects of microcystin-LR in human and chicken peripheral blood lymphocytes in vitro. Toxicology 204, 23-40. <https://doi.org/10.1016/j.tox.2004.05.016>
24. Lankoff, A., Krzowski, L., Glab, J., Banasik, A., Lisowska, H., Kuszewski, T., Gozdz, S., Wojcik, A. (2004b) DNA damage and repair in human peripheral blood lymphocytes following treatment with microcystin-LR. Mutat. Res. 559, 131-142. <https://doi.org/10.1016/j.mrgentox.2004.01.004>
25. Li, H., Zhu, H., Xu, C. J., Yuan, J. (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94, 491-501. <https://doi.org/10.1016/S0092-8674(00)81590-1>
26. Luo, X., Budihardjo, I., Zou, H., Slaughter, C., Wang, X. (1998) Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94, 481-490. <https://doi.org/10.1016/S0092-8674(00)81589-5>
27. MacKintosh, C., Beattie, K. A., Klumpp, S., Cohen, P., Codd, G. A. (1990) Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants. FEBS Lett. 264, 187-192. <https://doi.org/10.1016/0014-5793(90)80245-E>
28. Mankiewicz, J., Walter, Z., Tarczynska, M., Zalewski, M., Fladmark, K. E., Doskeland, S. O. (2000) Apoptotic effect of cyanobacterial blooms collected from Polish water reservoirs. Int. J. Occup. Med. Environ. Health 13, 335-344.
29. Mankiewicz, J., Tarczynska, M., Fladmark, K. E., Doskeland, S. O., Walter, Z., Zalewski, M. (2001) Apoptotic effect of cyanobacterial extract on rat hepatocytes and human lymphocytes. Environ. Toxicol. 16, 225-233. <https://doi.org/10.1002/tox.1028>
30. McDermott, C. M., Nho, C. W., Howard, W., Holton, B. (1998) The cyanobacterial toxin, microcystin-LR, can induce apoptosis in a variety of cell types. Toxicon 36, 1981-1996. <https://doi.org/10.1016/S0041-0101(98)00128-7>
31. Nakano, M., Nakano, Y., Saito-Taki, T., Mori, N., Kojima, M., Ohtake, A., Shirai, M. (1989) Toxicity of Microcystis aeruginosa K-139 strain. Microbiol. Immunol. 33, 787-792. <https://doi.org/10.1111/j.1348-0421.1989.tb00964.x>
32. Nicholson, D. W., Thornberry, N. A. (1997) Caspases: killer proteases. Trends Biochem. Sci. 22, 299-306. <https://doi.org/10.1016/S0968-0004(97)01085-2>
33. Nishiwaki-Matsushima, R., Ohta, T., Nishiwaki, S., Suganuma, M., Kohyama, K., Ishikawa, T., Carmichael, W. W., Fujiki, H. (1992) Liver tumor promotion by the cyanobacterial cyclic peptide toxin microcystin-LR. J. Cancer Res. Clin. Oncol. 118, 420-424. <https://doi.org/10.1007/BF01629424>
34. Ruiz-Vela, A., Gonzales, D. B., Martinez, A. (1999) Implication of calpain in caspase activation during B cell clonal deletion. Embo J. 18, 4988-4998. <https://doi.org/10.1093/emboj/18.18.4988>
35. Runnegar, M. T., Gerdes, R. G., Falconer, I. R. (1991) The uptake of the cyanobacterial hepatotoxin microcystin by isolated rat hepatocytes. Toxicon 29, 43-51. <https://doi.org/10.1016/0041-0101(91)90038-S>
36. Sivonen, K. (1996) Cyanobacterial toxins and toxin production. Phycologia 35, 12-24. <https://doi.org/10.2216/i0031-8884-35-6S-12.1>
37. Spivak, C. E., Witkop, B., Albuquerque, E. X. (1980) Anatoxin-a: a novel, potent agonist at the nicotinic receptor. Mol. Pharmacol. 18, 384-394. <https://doi.org/10.1016/S0026-895X(25)14518-5>
38. Vander Heiden, M. G., Thompson, C. B. (1999) Bcl-2 proteins: regulators of apoptosis or of mitochondrial homeostasis? Nat. Cell Biol. 1, E209-216. <https://doi.org/10.1038/70237>
39. Wyllie, A. H., Kerr, J. F. R., Currie, A. R. (1980) Cell death: the significance of apoptosis. Int. Rev. Cytol. 68, 251-306. <https://doi.org/10.1016/S0074-7696(08)62312-8>
40. Yea, S. S., Kim, H. M., Oh, H. M., Paik, K. H., Yang, K. H. (2001) Microcystin-induced down-regulation of lymphocyte functions through IL-2 mRNA stability. Toxicol. Lett. 122, 21-31. <https://doi.org/10.1016/S0378-4274(01)00339-3>
41. Yoshida, T., Makita, Y., Nagata, S., Tsutsumi, T., Yoshida, F., Sekijima, M., Tamura, S., Ueno, Y. (1997) Acute oral toxicity of microcystin-LR, a cyanobacterial hepatotoxin, in mice. Nat. Toxins 5, 91-95. <https://doi.org/10.1002/nt.1>
42. Yoshizawa, S., Matsushima, R., Watanabe, M. F., Harada, K., Ichihara, A., Carmichael, W. W., Fujiki, H. (1990) Inhibition of protein phosphatases by microcystins and nodularin associated with hepatotoxicity. J. Cancer Res. Clin. Oncol. 116, 609-614. <https://doi.org/10.1007/BF01637082>
43. Zamzami, N., Marchetti, P., Castedo, M., Zanin, C., Vayssiere, J. L., Petit, P. X., Kroemer, G. (1995) Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J. Exp. Med. 181, 1661-1672. <https://doi.org/10.1084/jem.181.5.1661>
front cover

ISSN 0015-5500 (Print) ISSN 2533-7602 (Online)

Open access journal

Submissions

Archive