Multi-xenobiotic-resistance a possible explanation for the insensitivity of bivalves towards cyanobacterial toxins

Toxicon

Volumn 52, Issue 8, 2008, Pages 936-943

  Contardo Jara, Valeska ^a   Pflugmacher, Stephan ^a   Wiegand, Claudia ^a,b  

^a LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Cyanobacteria; Molecular biomarkers; MXR; P glycoprotein; Toxin depuration

Indexed keywords

GLUTATHIONE TRANSFERASE; GLYCOPROTEIN P; HEAT SHOCK PROTEIN 70; MICROCYSTIN LR; PHOSPHOPROTEIN PHOSPHATASE 2A; XENOBIOTIC AGENT;

ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; CYANOBACTERIUM; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MUSSEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BACTERIAL TOXINS; CATALASE; CYANOBACTERIA; DREISSENA; DRUG RESISTANCE, MULTIPLE; ENZYME INHIBITORS; GENE EXPRESSION; GLUTATHIONE S-TRANSFERASE PI; MICROCYSTINS; P-GLYCOPROTEIN; PHOSPHOPROTEIN PHOSPHATASES; RHODAMINES; XENOBIOTICS;

BIVALVIA; CYANOBACTERIA; DREISSENA POLYMORPHA;

EID: 57049093260     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2008.09.005     Document Type: Article

References (48)

1. Amorim A., and Vasconcelos V. Dynamics of microcystins in the mussel Mytilus galloprovincialis. Toxicon 37 (1999) 1041-1052
2. Bard S.M. Multixenobiotic resistance as a cellular defense mechanism in aquatic organisms. Aquatic Toxicology 48 (2000) 357-389
3. Bolhuis H., vanVeen H.W., Poolman B., Driessen A.J.M., and Konings W.N. Mechanisms of multidrug transporters. FEMS Microbiology Reviews 21 (1997) 55-84
4. Bykova O., Laursen A., Bostan V., Bautista J., and McCarthy L. Do zebra mussels (Dreissena polymorpha) alter lake water chemistry in a way that favours Microcystis growth?. Science of the Total Environment 371 (2006) 362-372
5. Carmichael W.W., Beasley V., Bunner D.L., Eloff J.N., Falconer I., Gorham P., Harada K.I., Krishnamurthy T., Yu M.J., Moore R.E., Rinehart K., Runnegar M., Skulberg O.M., and Watanabe M. Naming of cyclic heptapeptide toxins of cyanobacteria (blue-green-algae). Toxicon 26 (1988) 971-973
6. Carmichael W.W., and Li R.H. Cyanobacteria toxins in the Salton Sea. Saline Systems 2 5 (2006) 1-13. http://www.salinesystems.org/content/2/1/5 Available from:
7. Cazenave J., Bistoni M.D.L.A., Zwirnmann E., Wunderlin D.A., and Wiegand C. Attenuating effects of natural organic matter on microcystin toxicity in zebra fish (Danio rerio) embryos - benefits and costs of microcystin detoxication. Environmental Toxicology 21 (2006) 22-32
8. de Souza Votto A.P., Renon V.P., Yunes J.S., Rumjanek V.M., Capella M.A., Neto V.M., de Freitas M.S., Geracitano L.A., Monserrat J.M., and Trindade G.S. Sensitivity to microcystins: a comparative study in human cell lines with and without multidrug resistance phenotype. Cell Biology International 31 (2007) 1359-1366
9. Doyen, P., Vasseur, P., Rodius, F., 2006. DQ459993. Available from: http://www.ncbi.nlm.nih.gov/.
10. Eufemia N.A., and Epel D. Induction of the multixenobiotic defence mechanism (MXR), P-glycoprotein, in the mussel Mytilus californianus as a general cellular response to environmental stresses. Aquatic Toxicology 49 (2000) 89-100
11. Fernald S.H., Caraco N.F., and Cole J.J. Changes in cyanobacterial dominance following the invasion of the zebra mussel Dreissena polymorpha: long-term results from the Hudson River Estuary. Estuaries and Coasts 30 (2007) 163-170
12. Funari E., and Testai E. Human health risk assessment related to cyanotoxins exposure. Critical Reviews in Toxicology 38 (2008) 97-125
13. Harada K., and Tsuji K. Persistence and decomposition of hepatotoxic microcystins produced by cyanobacteria in natural environment. Journal of Toxicology - Toxin Reviews 17 (1998) 385-403
14. Ibelings B.W., Bruning K., de Jonge J., Wolfstein K., Pires L.M.D., Postma J., and Burger T. Distribution of microcystins in a lake foodweb: no evidence for biomagnification. Microbial Ecology 49 (2005) 487-500
15. Juhel G., Davenport J., O'Halloran J., Culloty S., Ramsay R., James K., Furey A., and Allis O. Pseudodiarrhoea in zebra mussels Dreissena polymorpha (Pallas) exposed to microcystins. Journal of Experimental Biology 209 (2006) 810-816
16. Kankaanpaa H., Leinio S., Olin M., Sjovall O., Meriluoto J., and Lehtonen K.K. Accumulation and depuration of cyanobacterial toxin nodularin and biomarker responses in the mussel Mytilus edulis. Chemosphere 68 (2007) 1210-1217
17. Lamers, A.E., Heiney, J.P., Ram, J.L., 2002. AF508223. Available from: http://www.ncbi.nlm.nih.gov/.
18. Lindholm T., Eriksson J.E., and Meriluoto J.A.O. Toxic cyanobacteria and water-quality problems - examples from a eutropic lake on Aland, South West Finland. Water Research 23 (1989) 481-486
19. Metcalf J.S., Lindsay J., Beattie K.A., Birmingham S., Saker M.L., Torokne A.K., and Codd G.A. Toxicity of cylindrospermopsin to the brine shrimp Artemia salina: comparisons with protein synthesis inhibitors and microcystins. Toxicon 40 (2002) 1115-1120
20. Minier C., Abarnou A., Jaouen-Madoulet A., and Le Guellec A.M. A pollution-monitoring pilot study involving contaminant and biomarker measurements in the Seine Estuary, France, using zebra mussels (Dreissena polymorpha). Environmental Toxicology and Chemistry 25 (2006) 112-119
21. Pain S., Devin S., and Parant M. Biomarker versus environmental factors: seasonal variations and modelling multixenobiotic defence (MXD) transport activity in transplanted zebra mussels. Science of the Total Environment 373 (2007) 103-112
22. Peuthert, A., Wiegand, C., 2004. Glutathione involvement in detoxication and oxidative stress caused by cyanobacteria. In: Sixth International Conference on Toxic Cyanobacteria, Bergen, Norway, Abstract book, p. 54.
23. Peuthert, A., 2007a. EF681763. Available from: http://www.ncbi.nlm.nih.gov/.
24. Peuthert, A., 2007b. EF526096. Available from: http://www.ncbi.nlm.nih.gov/.
25. Pflugmacher S., Wiegand C., Oberemm A., Beattie K.A., Krause E., Codd G.A., and Steinberg C.E.W. Identification of an enzymatically formed glutathione conjugate of the cyanobacterial hepatotoxin microcystin-LR: the first step of detoxication. Biochimica et Biophysica Acta - General Subjects 1425 (1998) 527-533
26. Pflugmacher S., Wiegand C., Beattie K.A., Krause E., Steinberg C.E.W., and Codd G.A. Uptake, effects, and metabolism of cyanobacterial toxins in the emergent reed plant Phragmites australis (Cav.) Trin. ex Steud. Environmental Toxicology and Chemistry 20 (2001) 846-852
27. Pires L.M.D., Kusserow R., and Van Donk E. Influence of toxic and non-toxic phytoplankton on feeding and survival of Dreissena polymorpha (Pallas) larvae. Hydrobiologia 491 (2003) 193-200
28. Pires L.M.D., Karlsson K.M., Meriluoto J.A.O., Kardinaal E., Visser P.M., Siewertsen K., Van Donk E., and Ibelings B.W. Assimilation and depuration of microcystin-LR by the zebra mussel, Dreissena polymorpha. Aquatic Toxicology 69 (2004) 385-396
29. Pires L.M.D., Bontes B.M., Samchyshyna L., Jong J., Van Donk E., and Ibelings B.W. Grazing on microcystin-producing and microcystin-free phytoplankters by different filter-feeders: implications for lake restoration. Aquatic Sciences 69 (2007) 534-543
30. Rajagopal S., van der Velde G., van der Gaag M., and Jenner H.A. Byssal detachment underestimates tolerance of mussels to toxic compounds. Marine Pollution Bulletin 50 (2005) 20-29
31. Rivas M., Garcia C., Liberona J.L., and Lagos N. Biochemical characterization and inhibitory effects of dinophysistoxin-1, okadaic acid and microcystine l-r on protein phosphatase 2a purified from the mussel Mytilus chilensis. Biological Research 33 (2000) 197-206
32. Runnegar M.T.C., Gerdes R.G., and Falconer I.R. The uptake of the cyanobacterial hepatotoxin microcystin by isolated rat hepatocytes. Toxicon 29 (1991) 43-51
33. Saker M.L., and Griffiths D.J. The effect of temperature on growth and cylindrospermopsin content of seven isolates of Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) from water bodies in northern Australia. Phycologia 39 (2000) 349-354
34. Sipia V.O., Kankaanpaa H.T., Flinkman J., Lahti K., and Meriluoto J.A.O. Time-dependent accumulation of cyanobacterial hepatotoxins in flounders (Platichthys flesus) and mussels (Mytilus edulis) from the northern Baltic Sea. Environmental Toxicology 16 (2001) 330-336
35. Smital T., Sauerborn R., Pivcevic B., Krca S., and Kurelec B. Interspecies differences in P-glycoprotein mediated activity of multixenobiotic resistance mechanism in several marine and freshwater invertebrates. Comparative Biochemistry and Physiology C-Toxicology & Pharmacology 126 (2000) 175-186
36. Svensson S., Sarngren A., and Forlin L. Mussel blood cells, resistant to the cytotoxic effects of okadaic acid, do not express cell membrane p-glycoprotein activity (multixenobiotic resistance). Aquatic Toxicology 65 (2003) 27-37
37. Toivola D.M., Eriksson J.E., and Brautigan D.L. Identification of protein phosphatase 2A as the primary target for microcystin-1R in rat-liver homogenates. FEBS Letters 344 (1994) 175-180
38. Tutundjian, R., 1999. AJ250733. Available from: http://www.ncbi.nlm.nih.gov/.
39. Tutundjian, R., Leboulenger, F., Minier, C., 2002. AJ506742. Available from: http://www.ncbi.nlm.nih.gov/.
40. Vanderploeg H.A., Liebig J.R., Carmichael W.W., Agy M.A., Johengen T.H., Fahnenstiel G.L., and Nalepa T.F. Zebra mussel (Dreissena polymorpha) selective filtration promoted toxic Microcystis blooms in Saginaw Bay (Lake Huron) and Lake Erie. Canadian Journal of Fisheries and Aquatic Sciences 58 (2001) 1208-1221
41. Vasconcelos V.M. Uptake and depuration of the heptapeptide toxin microcystin-LR in Mytilus galloprovincialis. Aquatic Toxicology 32 (1995) 227-237
42. Vasconcelos V.M., Wiegand C., and Pflugmacher S. Dynamics of glutathione-S-transferases in Mytilus galloprovincialis exposed to toxic Microcystis aeruginosa cells, extracts and pure toxins. Toxicon 50 (2007) 740-745
43. Wera S., and Hemmings B.A. Serine threonine protein phosphatases. Biochemical Journal 311 (1995) 17-29
44. Wiegand C., Pflugmacher S., Oberemm A., Meems N., Beattie K.A., Steinberg C.E.W., and Codd G.A. Uptake and effects of microcystin-LR on detoxication enzymes of early life stages of the zebra fish (Danio rerio). Environmental Toxicology 14 (1999) 89-95
45. Wiegand C., and Pflugmacher S. Ecotoxicological effects of selected cyanobacterial secondary metabolites a short review. Toxicology and Applied Pharmacology 203 (2005) 201-218
46. Zegura B., Lah T.T., and Filipic M. The role of reactive oxygen species in microcystin-LR-induced DNA damage. Toxicology 200 (2004) 59-68
47. Zehnder A., and Gorham P.R. Factors influencing the growth of Microcystis aeruginosa Kutz Emend Elenkin. Canadian Journal of Microbiology 6 (1960) 645-660
48. Zurawell R.W., Chen H.R., Burke J.M., and Prepas E.E. Hepatotoxic cyanobacteria: a review of the biological importance of microcystins in freshwater environments. Journal of Toxicology and Environmental Health-Part B-Critical Reviews 8 (2005) 1-37