Elimination of the cyanobacterial hepatotoxin microcystin from the freshwater pulmonate snail lymnaea stagnalis jugularis (say)

Journal of Toxicology and Environmental Health - Part A

Volumn 69, Issue 4, 2006, Pages 303-318

  Zurawell, Ronald W ^a,c   Holmes, Charles F B ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b LAKEHEAD UNIVERSITY   (Canada)

^c ALBERTA ENVIRONMENT AND PARKS   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; CYANOGINOSIN; FRESH WATER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVIAN STOMACH; CECUM; CYANOBACTERIUM; ENVIRONMENT; ENVIRONMENTAL TEMPERATURE; EXOCRINE GLAND; FECES; LYMNAEA; NONHUMAN; PHYTOPLANKTON; PRIORITY JOURNAL; SNAIL; STATISTICAL SIGNIFICANCE;

ANIMALS; BACTERIAL TOXINS; CYANOBACTERIA; EUTROPHICATION; FRESH WATER; GASTROINTESTINAL TRACT; LYMNAEA; MICROCYSTINS; PEPTIDES, CYCLIC; TEMPERATURE;

ANIMALIA; AVES; BACTERIA (MICROORGANISMS); CYANOBACTERIA; GASTROPODA; LYMNAEA; LYMNAEA STAGNALIS; LYMNAEA STAGNALIS JUGULARIS;

EID: 30944469424     PISSN: 15287394     EISSN: 10872620     Source Type: Journal    
DOI: 10.1080/15287390500227498     Document Type: Article

References (45)

1. An, J. S., and Carmichael, W. W. 1994. Use of a colorimetric protein phosphatase inhibition assay and enzyme linked immunosorbent assay for the study of microcystins and nodularins. Toxicon 32:1495-1507.
2. Beasley, V. R., Lovell, R. A., Holmes, K. R., Walcott, H. E., Schaeffer, D. J., Hoffmann, W. E., and Carmichael, W.W. 2000. Microcystin-LR decreases hepatic and renal perfusion, and causes circulatory shock, severe hypoglycemia, and terminal hyperkalemia in intravascularly dosed swine. J. Toxicol. Environ. Health A. 61:281-303.
3. Boer, H. H., and Kits, K. S. 1990. Histochemical and ultrastructural study of the alimentary tract of the freshwater snail Lymnaea stagnalis. J. Morphol. 205:97-111.
4. Botes, D. P., Wessels, P. L., Kruger, H., Runnegar, M. T. C., Santikarn, S., Smith, R. J., Barna, J. C. J., and Williams, D. H. 1985. Structural studies on cyanoginosins-LR, -YR, -YA, and -YM, peptide toxins from Microcystis aeruginosa. J. Chem. Soc. Perkin Trans. 1:2747-2748.
5. Calow, P. 1975a. The feeding strategies of two freshwater gastropods, Ancylus fluviatilis Müll. and Planorbis con-tortus Linn. (Pulmonata), in terms of ingestion rates and absorption efficiencies. Oecologia 20:33-49.
6. Calow, P. 1975b. Defaecation strategies of two freshwater gastropods, Ancylus fluviatilis Müll. and Planorbis contortus Linn. (Pulmonata) with a comparison of field and laboratory estimates of food absorption rate. Oecologia 20:51-63.
7. Carmichael, W. W. 1994. The toxins of cyanobacteria. Sci. Am. 270:78-86.
8. Carriker, M. R. 1946. Observations on the functioning of the alimentary system of the snail Lymnaea stagnalis appressa Say. Biol. Bull. 91:88-111.
9. Chorus, I. 2001. Cyanotoxin occurrence in freshwaters—A summary of survey results from different countries. In Cyanotoxins—Occurrence, causes, consequences, pp. 75-78. Berlin: Springer-Verlag.
10. Chorus, I., Falconer, I. R., Salas, H. J., and Bartram, J. 2000. Health risks caused by freshwater cyanobacteria in recreational waters. J. Toxicol. Environ. Health B 3:323-347.
11. Clarke, A. H. 1981. The freshwater molluscs of Canada. Ottawa: National Museums of Canada.
12. Clifford, H. 1993. Aquatic invertebrates of Alberta. Edmonton: University of Alberta Press.
13. Codd, G. A., Bell, S. G., Kaya, K., Ward, C. J., Beattie, K. A., and Metcalf, J. S. 1999. Cyanobacterial toxins, exposure routes and human health. Eur. J. Phycol. 34:405-415.
14. Dabholkar, A. S., and Carmichael, W. W. 1987. Ultrastructural changes in the mouse liver induced by hepatotoxin from the freshwater cyanobacterium Microcystis aeruginosa strain 7820. Toxicon 25:285-292.
15. de Silva, E. D., Williams, D. E., Andersen, R. J., Klix, H., Holmes, C. F. B., and Allen, T. M. 1992. Motu-porin, a potent protein phosphatase inhibitor isolated from the Papua New Guinea sponge Theonella swinhoei Gray. Tetrahedron Lett. 33:1561-1564.
16. Elder, J. F., and Collins, J. J. 1991. Freshwater molluscs as indicators of bioavailability and toxicity of metals in surface-water systems. Rev. Environ. Contam. Toxicol. 122:37-79.
17. Eriksson, J. E., Meriluoto, J. A. O., and Lindholm, T. 1989. Accumulation of a peptide toxin from the cyanobacterium Oscillatoria agardhii in the freshwater mussel Anodonta cygnea. Hydrobiologia 183:211-216.
18. Falconer, I. R. 1991. Tumor promotion and liver injury caused by oral consumption of cyanobacteria. Environ. Toxicol. Water Qual. 6:177-184.
19. Harada, K.- I., Tsuji, K., Watanabe, M. F., and Kondo, F. 1996. Stability of microcystins from cyanobacteria—III. Effect of pH and temperature. Phycologia 35:83-88.
20. Hooser, S. B., Beasley, V. R., Basgall, E. J., Carmichael, W. W., and Haschek, W.M. 1990. Microcystin-LR-induced ultrastructural changes in rats. Vet. Pathol. 27:9-15.
21. Humpage, A. R., Hardy, S. J., Moore, E. J., Froscio, S. M., and 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.
22. Jochimsen, E. M., Carmichael, W. W., An, J. S., Cardo, D. M., Cookson, S. T., Holmes, C. E. M., Antunes, M. B., De Melo, Filho D. A., Lyra, T. M., Barreto, V. S. T., Azevedo, S. M., and Jarvis, W.R. 1998. Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. N. Engl. J. Med. 338:873-878.
23. Jones, G. J., Blackburn, S. I., and Parker, N. S. 1994. A toxic bloom of Nodularia spumigena Mertens in Ori-elton Lagoon, Tasmania. Aust. J. Mar. Freshwater Res. 45:787-800.
24. Kotak, B. G., Lam, A. K. - Y., Prepas, E. E., Kenefick, S. L., and Hrudey, S. E. 1995. Variability of the hepatotoxin microcystin-LR in hypereutrophic drinking water lakes. J. Phycol. 31:248-263.
25. Kotak, B. G., Zurawell, R. W., Prepas, E. E., and Holmes, C. F. B. 1996. Microcystin-LR concentration in aquatic food web compartments from lakes of varying trophic status. Can. J. Fish. Aquat. Sci. 53:1974-1985.
26. Krishnamuthy, T., Carmichael, W. W., and Sarver, E. W. 1986. Toxic peptides from freshwater cyanobacteria (blue-green algae). I. Isolation, purification and characterization of peptides from Microcystis aeruginosa and Anabaena flos-aquae. Toxicon 24:865-873.
27. Loonen, H., Muir, D. C. G., Parsons, J. R., and Govers, H. A. J. 1997. Effects of sediment on the bioaccumulation of polychlorinated dibenzo-p-dioxins by oligochaetes. Environ. Toxicol. Chem. 16:1518-1525.
28. MacKintosh, C., and Klumpp, S. 1990. Tautomycin from the bacterium Streptomyces verticillatus. FEBS Lett 277:137-140.
29. 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 phosphatases 1 and 2A from both mammals and higher plants. FEBSLett. 264:187-192.
30. Meriluoto, J. A. O., Sandstrom, A., Eriksson, J. E., Remaud, G., Craig, A. G., and Chattopadhyaya, J. 1989. Structure and toxicity of a peptide hepatotoxin from the cyanobacterium Oscillatoria agardhii. Toxicon 27:1021-1034.
31. Namikoshi, M., Rinehart, K., Sakai, R., Sivonen, K., and Carmichael, W. W. 1990. Structures of three new cyclic heptapeptide hepatotoxins produced by the cyanobacterium (blue-green algae) Nostoc sp. strain 152. J. Org. Chem. 55:6135-6139.
32. Nishiwaki-Matsushima, R., Ohta, T., Nishiwaki, S., Suganuma, M., Kohyama, K., Ishikawa, T., Carmichael, W. W., and Fujiki, H. 1992. Liver tumor promotion by the cyanobacterial cyclic peptide toxin micro-cystin-LR. J. Cancer Res. Clin. Oncol. 118:420-424.
33. Pastershank, G. M., Muir, D. C. G., and Fairchild, W. L. 1999. Accumulation and depuration of 2,3,7,8-tet-rachlorodibenzofuran and octachlorodibenzo-p-dioxin by caddisfly larvae (Hydropsyche bidens (Ross)) in miniature laboratory streams. Environ. Toxicol. Chem. 18:2352-2360.
34. Peters, R. H. 1983. The ecological implications of body size. New York: Cambridge University Press.
35. Prepas, E. E., Kotak, B. G., Campbell, L. M., Evans, J. C., Hrudey, S. E., and Holmes, C. F. B. 1997. Accumulation and elimination of cyanobacterial hepatotoxins by the freshwater clam Anodonta grandis sim-psoniana. Can. J. Fish. Aquat. Sci. 54:41-46.
36. Scheerboom, J. E. M., Hemminga, M. A., and Doderer, A. 1978. The effects of a change of diet on consumption and assimilation and on the haemolymph-glucose concentration of the pond snail Lymnaea stagnalis (L.). Proc. Konin. Neth. Akad. van Wet. Ser. C. 81:335-346.
37. Stein, R. A., Goodman, C. G., and Marschall, E.A. 1984. Using time and energetic measures of cost in estimating prey value for fish predators. Ecology 65:702-715.
38. Theiss, W. C., Carmichael, W. W., Wyman, J., and Bruner, R. 1988. Blood pressure and hepatocellular effects of the cyclic heptapeptide toxin produced by the freshwater cyanobacterium (blue-green alga) Microcystis aeruginosa strain PCC-7820. Toxicon 26:603-613.
39. Veldhuijzen, J. P. 1974. Sorting and retention times of particles in the digestive system of Lymnaea stagnalis (L.). Neth. J. Zool. 24:10-21.
40. Watanabe, M. F., Park, H.-D., Kondo, F., Harada, K. -I., Hayashi, H., and Okino, T. 1997. Identification and estimation of microcystins in freshwater mussels. Natural Toxins 5:31-35.
41. Yasumoto, T., Murata, M., Oshima, Y., Sano, M., Matsumoto, G. K., and Clardy, J. 1985. Diarrhetic shellfish toxins. Tetrahedron 41:1019-1025.
42. Zar, J. H. 1984. Biostatistical analysis, (2nd ed). Englewood Cliffs, NJ: Prentice Hall.
43. Zhou, L., Yu, H., and Chen, K. 2002. Relationship between microcystin in drinking water and colorectal cancer. Biomed. Environ Sci. 15:166-171.
44. Zurawell, R. W., Kotak, B. G., and Prepas, E. E. 1999. Influence of lake trophic status on the occurrence of microcystin-LR in the tissue of pulmonate snails. Freshwater Biol 42:707-718.
45. Zurawell, R. W., Chen, H., Burke, J. M., and Prepas, E. E. 2005. Hepatotoxic cyanobacteria: A review of the biological importance of microcystins in freshwater environments. J. Toxicol. Environ. Health B 8:1-37.