Bioaccumulation and clearance of microcystins from salt water mussels, mytilus edulis, and in vivo evidence for covalently bound microcystins in mussel tissues

Toxicon

Volumn 35, Issue 11, 1997, Pages 1617-1625

  Williams, David E ^a   Dawe, Sheila C ^b   Kent, Michael L ^b   Andersen, Raymond J ^a   Craig, Marcia ^c   Holmes, Charles F B ^c  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b PACIFIC BIOLOGICAL STATION   (Canada)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYANOGINOSIN; PHOSPHOPROTEIN PHOSPHATASE; SEA WATER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BIOLOGICAL MONITORING; CONTROLLED STUDY; CYANOBACTERIUM; DRUG CLEARANCE; DRUG DETERMINATION; ENZYME ASSAY; GAS CHROMATOGRAPHY; INTERMETHOD COMPARISON; LIVER TOXICITY; MARINE ENVIRONMENT; MASS SPECTROMETRY; MONITORING; MUSSEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SHELLFISH;

ANIMALS; BIVALVIA; CYANOBACTERIA; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; MICROCYSTINS; PEPTIDES, CYCLIC; PHOSPHOPROTEIN PHOSPHATASE;

ANIMALIA; CYANOBACTERIA; MICROCYSTIS AERUGINOSA; MYTILUS EDULIS;

EID: 0030815213     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0041-0101(97)00039-1     Document Type: Article

References (48)

1. Andersen, R. J., Luu, H. A., Chen, D. Z. X., Holmes, C. F. B., Kent, M. L., Leblanc, M., 'Max' Taylor, F. J. R. and Williams, D. E. (1993) Chemical and biological evidence links microcystins to salmon 'netpen liver disease'. Toxicon 31, 1315-1323.
2. Bagu, J. R., Sönnichsen, F. D., Williams, D. E., Andersen, R. J., Sykes, B. D. and Holmes, C. F. B. (1995) Comparison of the solution structures of microcystin-LR and motuporin. Nature - Structural Biology 2, 114-116.
3. Carmichael, W. W. (1988) Freshwater cyanobacteria (blue - green algal) toxins. In Natural Toxins: Characterization, Pharmacology and Therapeutics, ed. C. L. Ownby and G. V. Odell, pp. 3-16. Pergamon Press, London.
4. Carmichael, W. W. (1992) Cyanobacteria secondary metabolites - the cyanotoxins. Journal of Applied Bacteriology 72, 445-459.
5. Carmichael, W. W. (1994) The toxins of Cyanobacteria. Scientific American 270, Jan, 78-86.
6. Chen, D. Z. X., Boland, M. P., Smillie, M. A., Klix, H., Ptak, C., Andersen, R. J. and Holmes, C. F. B. (1993) Identification of protein phosphatase inhibitors of the microcystin class in the marine environment. Toxicon 31, 1407-1414.
7. Cohen, P. and Cohen, P. T. W. (1989) Protein phosphatases come of age. Journal of Biological Chemistry 264, 21435-21438.
8. Craig, M., McCready, T. L., Luu, H. A., Smillie, M. A., Dubord, P. and Holmes, C. F. B. (1993) Identification and characterization of Hydrophobic microcystins in Canadian freshwater Cyanobacteria. Toxicon 31, 1541-1549.
9. Craig, M., Luu, H. A., McCready, T., Williams, D. E., Andersen, R. J. and Holmes, C. F. B. (1996) Molecular mechanisms underlying the interaction of motuporin and microcystins with type-1 and 2A protein phosphatases. Biochemistry and Cell Biology 74, 569-578.
10. Dunn, J. (1996) Algae kill dialysis patients in Brazil. British Medical Journal 312, 1183-1184.
11. Eriksson, J. F., Meriluoto, J. A. O. and Lindholm, T. (1989) Accumulation of a peptide toxin from the cyanobacterium Oscillatoria agardhii in the freshwater mussel Anadonta cygnea. Hydrobiologia 183, 211-216.
12. Falconer, I. R. and Choice, A. (1992) Toxicity of edible mussels (Mytilus edulis) growing naturally in an estuary during a water bloom of the blue - green alga Nodularia spumigena. Environmental Toxicology and Water Quality 7, 119-123.
13. Falconer, I. R., Beresford, A. M. and Runnegar, M. T. C. (1983) Evidence of liver damage by toxin from a bloom of the blue - green alga, Microcysiis aeruginosa. Medical Journal of Australia 1, 511-514.
14. Fujiki, H. and Suganuma, M. (1993) Tumour promotion by inhibitors of protein phosphatases 1 and 2A: the okadaic acid class of compounds. Advances in Cancer Research 61, 143-194.
15. Goldberg, J., Huang, H., Kwon, Y., Greengard, P., Nairn, A. C. and Kuriyan, J. (1995) Three-dimensional structure of the catalytic subunit of protein serine/threonine phosphatase-1. Nature 376, 745-753.
16. Harada, K., Murata, H., Qiang, Z., Suzuki, M. and Kondo, F. (1996) Mass spectrometric screening method for microcystins in cyanobacteria. Toxicon 34, 701-710.
17. Hashimoto, Y. (1979) Venerupin or short necked clam toxin. In Marine Toxins and Other Bioactive Marine Metabolites, pp. 53-55. Japan Scientific Societies Press, Tokyo.
18. Holmes, C. F. B. (1991) Liquid chromatography-linked protein phophatase bioassay; a highly sensitive marine bioscreen for okadaic acid and related diarrhetic shellfish toxins. Toxicon 29, 469-477.
19. Honkanen, R. E., Zwiller, J., Moore, R. E., Daily, S. L., Khatra, B. S., Dukelow, M. and Boynton, A. L. (1990) Characterization of microcystin-LR, a potent inhibitor of type 1 and type 2A protein phosphatases. Journal of Biological Chemistry 265, 19401-19404.
20. Kalbe, L. (1984) Animal experiments on the oral toxicity of blue - green algae water blooms. Limnologica (Berlin) 15, 559-562.-
21. Lemieux, R. U. and Rudloff, E. Von. (1955a) Periodate-permanganate oxidations: i. Oxidation of olefins. Canadian Journal of Chemistry 33, 1701-1709.
22. Lemieux, R. U. and Rudloff, E. Von. (1955b) Periodate-permanganate oxidations: ii. Determination of terminal methylene groups. Canadian Journal of Chemistry 33, 1710-1713.
23. Luu, H. A., Chen, D. Z. X., Magoon, J., Worms, J., Smith, J. and Holmes, C. F. B. (1993) Quantification of diarrhetic shellfish toxins and identification of novel protein phosphatase inhibitors in marine phytoplankton and mussels. Toxicon 31, 75-83.
24. MacKintosh, C., Beattie, K. A., Klumpp, S., Cohen, P. and Codd, G. A. (1990) Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphalases 1 and 2A from both mammals and higher plants. FEBS Letters 264, 187-192.
25. MacKintosh, R. W., Dalby, K. N., Campbell, D. G., Cohen, P. T. W., Cohen, P. and MacKintosh, C. (1995) The cyanobacterial toxin microcystin binds covalently to cysteine-273 on protein phosphatase 1. FEBS Letters 371, 236-240.
26. Moorhead, G., MacKintosh, R. W., Morrice, N., Gallagher, T. and MacKintosh, C. (1994) Purification of type 1 protein (serine/threonine) phosphatases by microcystin-sepharose affinity chromatography. FEBS Letters 356, 46-50.
27. Namikoshi, M., Sun, F., Choi, B. W., Rinehart, K. L., Carmichael, W. W., Evans, W. R. and Beasley, V. R. (1995) Seven more microcystins from Homer Lake cells: application of the general method for structure assignment of peptides containing α,β-dehydoamino acid unit(s). Journal of Organic Chemistry 60, 3671-3679.
28. Nishiwaki-Matsushima, R., Nishiwaki, S., Ohta, T., Yoshizawa, S., Suganuma, M., Harada, K.-I., Watanabe, M. F. and Fujiki, H. (1991) Structure - function relationships of microcystin liver tumour promoters interaction with protein phosphatase. Japanese Journal of Cancer Research 82, 993-996.
29. Nishiwaki-Matsushima, R., Ohta, T., Nishiwaki, S., Suganuma, M., Kohyama, K., Ishiwaka, T., Carmichael, W. W. and Fujiki, H. (1992) Liver tumour promotion by the cyanobacterial cyclic peptide toxin microcystin-LR. Journal of Cancer Research and Clinical Oncology 118, 420-424.
30. Phillips, M. J., Roberts, R. J. and Stewart, J. A. (1985) The toxicity of the cyanobacterium Microcystis aeruginosa to rainbow trout, Salmo gairdneri Richardson. Journal of Fish Diseases 8, 339-344.
31. Rinehart, K. L., Namikoshi, M. and Choi, B. W. (1994) Structure and biosynthesis of toxins from blue - green algae (cyanobacteria). Journal of Applied Phycology 6, 159-176.
32. Robinson, N. A., Matson, C. F. and Pace, J. G. (1991a) Association of microcystin-LR and its biotransformation product with a hepatic - cytosolic protein. Journal of Biochemical Toxicology 6, 171-180.
33. Robinson, N. A., Pace, J. G., Matson, C. E., Miura, G. A. and Lawrence, W. B. (1991b) Tissue distribution, excretion and hepatic biotransformation of microcystin-LR in mice. Journal of Pharmacology and Experimental Therapeutics 256, 176-182.
34. Rodger, H. D., Turnbull, T., Edwards, C. and Codd, G. A. (1994) Cyanobacterial (blue - green algal) bloom associated pathology in brown trout, Salmo trutta L., in Loch Leven, Scotland. Journal of Fish Diseases 17, 177-181.
35. Rudloff, E. Von. (1955) Periodate-permanganate oxidations: iii. Determination of isopropylidene groups. Canadian Journal of Chemistry 33, 1714-1719.
36. Rudloff, E. Von. (1956) Periodate-permanganate oxidations: v. Oxidation of lipids in media containing organic solvents. Canadian Journal of Chemistry 34, 1413-1418.
37. Rudloff, E. Von. (1965) Permanganate-periodate oxidations: vi. The oxidation of various aliphatic compounds. Canadian Journal of Chemistry 43, 1784-1791.
38. Runnegar, M., Berndt, N., Kong, S.-M., Lee, E. Y. C. and Zhang, L. (1995) In vivo and in vitro binding of microcystin to protein phosphatases 1 and 2A. Biochemical and Biophysical Research Communications 216, 162-169.
39. Sano, T., Nohara, K., Shiraishi, F. and Kaya, K. (1992) A method for micro-determination of total microcystin content in waterblooms of cyanobacteria (blue - green algae). International Journal of Environmental and Analytical Chemistry 49, 163-170.
40. Sargunar, H. and Sargunar, A. (1990) In Proceedings of the 4th International IUPAC Symposium on Mycotoxins and Phycotoxins, Abstract no. 610. Lausane, Switzerland.
41. Tanaka, Y., Takenaka, S., Matsuo, H., Kitamori, S. and Tokiwa, H. (1993) Levels of microcystins in Japanese lakes. Toxicology and Environmental Chemistry 39, 21-27.
42. Toivola, D. M., Eriksson, J. E. and Brautigan, D. L. (1994) Identification of protein phosphatase 2A as the primary target for microcystin-LR in rat homogenates. FEBS Letters 344, 175-180.
43. Williams, D. E., Kent, M. L., Andersen, R. J., Klix, H. and Holmes, C. F. B. (1995) Tissue distribution and clearance of tritium-labelled dihydromicrocystin-LR epimers administered to Atlantic salmon via interperitoneal injection. Toxicon 33, 125-131.
44. Williams, D. E., Andersen, R. J., Craig, M. and Holmes, C. F. B. (1996) Ferintoic acids A and B, novel cyclic hexapeptides isolated from a natural bloom of the freshwater cyanobacteria Microcystis aeruginosa. Journal of Natural Products 59, 570-575.
45. Williams, D. E., Craig, M., Dawe, S. C., Kent, M. L., Andersen, R. J. and Holmes, C. F. B. (1997a) Evidence for a covalently bound form of microcystin-LR in salmon liver and dungeness crab larvae. Chemical Research Toxicology 10, 463-469.
46. 14C-Labelled microcystin-LR administered to Atlantic salmon via intraperitoneal injection provides in vivo evidence for covalent binding of microcystin-LR in salmon livers. Toxicon in press.
47. Yoshizawa, S., Matsushima, R., Watanabe, M. R., Harada, K. A., Ichihara, A., Carmichael, W. W. and Fujiki, H. (1990) Inhibition of protein phosphatases by microcystin and nodularin associated with hepatotoxicity. Journal of Cancer Research and Clinical Oncology 116, 609-614.
48. Yu, S.-Z. (1989) Drinking water and primary liver cancer. In Primary Liver Cancer, ed. Z. Y. Tang, M. C. Wu and S. S. Xia, pp. 30-37. China Academic, Beijing/Springer, Berlin.