Synthesis and organotropism of 3H-dihydro derivatives of the cyanobacterial peptide hepatotoxin nodularin

Toxicon

Volumn 41, Issue 2, 2003, Pages 153-162

  Spoof, Lisa ^a   Klimova, Svetlana ^b   Mikhailov, Andrey ^c   Eriksson, John E ^c,d   Meriluoto, Jussi ^a  

^a ÅBO AKADEMI UNIVERSITY   (Finland)

^b NAGOYA UNIVERSITY HOSPITAL   (Japan)

^c TURKU CENTRE FOR BIOTECHNOLOGY   (Finland)

^d UNIVERSITY OF TURKU   (Finland)

Author keywords

Cyanobacteria; Nodularin; Organotropism; Radiolabelling; Toxin

Indexed keywords

DIHYDRONODULARIN; METHANOL; NODULARIN; SODIUM BOROHYDRIDE; SODIUM SULFATE; UNCLASSIFIED DRUG; CYCLOPEPTIDE; MARINE TOXIN; TRITIUM;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CYANOBACTERIUM; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ISOTOPE LABELING; MOUSE; NONHUMAN; PRIORITY JOURNAL; REACTION OPTIMIZATION; REDUCTION; STEREOISOMERISM; SYNTHESIS; TOXIN ANALYSIS; ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; DRUG EFFECT; LIVER; METABOLISM; TOXIC HEPATITIS;

CYANOBACTERIA;

ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYANOBACTERIA; FEMALE; HEPATITIS, TOXIC; ISOTOPE LABELING; LIVER; MARINE TOXINS; MICE; MICE, INBRED BALB C; PEPTIDES, CYCLIC; STEREOISOMERISM; TRITIUM;

EID: 0037304493     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0041-0101(02)00245-3     Document Type: Article

References (48)

1. Bagu J.R., Sykes B.D., Craig M.M., Holmes C.F.B. A molecular basis for different interactions of marine toxins with protein phosphatase-1. J. Biol. Chem. 272:1997;5087-5097.
2. Botes D.P., Viljoen C.C., Kruger H., Wessels P.L., Williams D.H. Configuration assignments of the amino acid residues and the presence of N-methyldehydroalanine in toxins from the blue-green alga, Microcystis aeruginosa. Toxicon. 20:1982;1037-1042.
3. Botes D.P., Tuinman A.A., Wessels P.L., Viljoen C.C., Kruger H., Williams D.H., Santikarn S., Smith R.J., Hammond S.J. The structure of cyanoginosin-LA, a cyclic heptapeptide toxin from the cyanobacterium Microcystis aeruginosa. J. Chem. Soc. Perkin Trans. 1:1984;2311-2318.
4. Brooks W.P., Codd G.A. Distribution of Microcystis aeruginosa peptide toxin and interactions with hepatic microsomes in mice. Pharmacol. Toxicol. 60:1987;187-191.
5. 3H-microcystin-LR, a cyanobacterial toxin, in rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 42:1998;139-148.
6. Carmichael W.W., Azevedo S.M.F.O., An J.S., Molica R.J.R., Jochimsen E.M., Lau S., Rinehart K.L., Shaw G.R., Eaglesham G.K. Human fatalities from cyanobacteria: chemical and biological evidence for cyanotoxins. Environ. Health Perspect. 109:2001;663-668.
7. Craig M., Luu H.A., McCready T.L., Williams D., Andersen R.J., Holmes C.F.B. Molecular mechanisms underlying the interaction of motuporin and microcystins with type-1 and type-2A protein phosphatases. Biochem. Cell Biol. 74:1996;569-578.
8. Dahlem, A.M., 1989. Structure/toxicity relationships and fate of low molecular weight peptide toxins from cyanobacteria. PhD thesis, University of Illinois, Urbana-Champaign.
9. Eriksson J.E., Meriluoto J.A.O., Kujari H.P., Österlund K., Fagerlund K., Hällbom L. Preliminary characterization of a toxin isolated from the cyanobacterium Nodularia spumigena. Toxicon. 26:1988;161-166.
10. Eriksson J.E., Toivola D., Meriluoto J.A.O., Karaki H., Han Y.-G., Hartshorne D. Hepatocyte deformation induced by cyanobacterial toxins reflects inhibition of protein phosphatases. Biochem. Biophys. Res. Commun. 173:1990;1347-1353.
11. Falconer I.R., Buckley T.H. Tumour promotion by Microcystis sp., a blue-green alga occurring in water supplies. Med. J. Aust. 150:1989;351.
12. Falconer I.R., Humpage A.R. Tumour promotion by cyanobacterial toxins. Phycologia. 35:(Suppl. 6):1996;74-79.
13. 125I-labelled toxic peptide from the blue-green alga Microcystis aeruginosa. Aust. J. Biol. Sci. 39:1986;17-21.
14. Fischer W.J., Dietrich D.R. Pathological and biochemical characterization of microcystin-induced hepatopancreas and kidney damage in carp (Cyprinus carpio). Toxicol. Appl. Pharmacol. 164:2000;73-81.
15. Fischer W.J., Hitzfeld B.C., Tencalla F., Eriksson J.E., Mikhailov A., Dietrich D.R. Microcystin-LR toxicodynamics, induced pathology, and immunohistochemical localization in livers of blue-green algae exposed rainbow trout (Oncorhyncus mykiss). Toxicol. Sci. 54:2000;365-373.
16. Freitas de Magalhaes V., Moraes Soares R., Azevedo S.M.F.O. Microcystin contamination in fish from the Jacarepaguá Lagoon (Rio de Janeiro, Brazil): ecological implication and human health risk. Toxicon. 39:2001;1077-1085.
17. Hooser S.B., Kuhlenschmidt M.S., Dahlem A.M., Beasley V.R., Carmichael W.W., Haschek W.M. Uptake and subcellular localization of tritiated dihydro-microcystin-LR in rat liver. Toxicon. 29:1991;589-601.
18. Hormazábal V., Østensvik O., Underdal B., Skulberg O.M. Simultaneous determination of the cyanotoxins anatoxin a, microcystin desmethyl-3, LR, RR, and YR in fish muscle using liquid chromatography-mass spectrometry. J. Liquid Chromatogr. Rel. Technol. 23:2000;185-196.
19. Jochimsen E.M., Carmichael W.W., An J., Cardo D.M., Cookson S.T., Holmes C.E.M., de C. Antunes M.B., de Melo Filho D.A., Lyra T.M., Barreto V.S.T., Azevedo S.M.F.O., Jarvis W.R. Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. N. Engl. J. Med. 338:1998;873-878.
20. Kondo F., Ikai Y., Oka H., Okumura M., Ishikawa N., Harada K.-, Matsuura K., Murata H., Suzuki M. Formation, characterization, and toxicity of the glutathione and cysteine conjugates of toxic heptapeptide microcystins. Chem. Res. Toxicol. 5:1992;591-596.
21. Kondo F., Matsumoto H., Yamada S., Ishikawa N., Ito E., Nagata S., Ueno Y., Suzuki M., Harada K.-. Detection and identification of metabolites of microcystins formed in vivo in mouse and rat livers. Chem. Res. Toxicol. 9:1996;1355-1359.
22. Liesch J.M., Millington D.S., Pandey R.C., Rinehart K.L. Jr. Berninamycin. 2. Products of acidic hydrolysis, methanolysis, and acetolysis of berninamycin A. J. Am. Chem. Soc. 98:1976;8237-8249.
23. MacKintosh C., Beattie K.A., Klumpp S., Cohen P., Codd G.A. Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants. FEBS Lett. 264:1990;187-192.
24. MacKintosh R.W., Dalby K.N., Campbell D.G., Cohen P.T.W., Cohen P., MacKintosh C. The cyanobacterial toxin microcystin binds covalently to cysteine-273 on protein phosphatase 1. FEBS Lett. 371:1995;236-240.
25. Meriluoto J. Toxins of freshwater cyanobacteria (blue-green algae). Bogusz M.J. Forensic Science. 2000;359-390 Elsevier, Amsterdam.
26. Meriluoto J.A.O., Nygård S.E., Dahlem A.M., Eriksson J.E. Synthesis, organotropism and hepatocellular uptake of two tritium-labeled epimers of dihydromicrocystin-LR, a cyanobacterial peptide toxin analog. Toxicon. 28:1990;1439-1446.
27. Moorhead G., MacKintosh R.W., Morrice N., Gallagher T., MacKintosh C. Purification of type 1 protein (serine/threonine) phosphatases by microcystin-Sepharose affinity chromatography. FEBS Lett. 356:1994;46-50.
28. Namikoshi M., Choi B.W., Sun F., Rinehart K.L., Evans W.R., Carmichael W.W. Chemical characterization and toxicity of dihydro derivatives of nodularin and microcystin-LR, potent cyanobacterial cyclic peptide hepatotoxins. Chem. Res. Toxicol. 6:1993;151-158.
29. Nishiwaki R., Ohta T., Sueoka E., Suganuma M., Harada K.-, Watanabe M.F., Fujiki H. Two significant aspects of microcystin-LR: specific binding and liver specificity. Cancer Lett. 83:1994;283-289.
30. Nishiwaki-Matsushima R., Ohta T., Nishiwaki S., Suganuma M., Kohyama K., Ishikawa T., Carmichael W.W., Fujiki H. Liver tumor promotion by the cyanobacterial cyclic peptide toxin microcystin-LR. J. Cancer Res. Clin. Oncol. 118:1992;420-424.
31. Ohta T., Sueoka E., Iida N., Komori A., Suganuma M., Nishiwaki R., Tatematsu M., Kim S.-J., Carmichael W.W., Fujiki H. Nodularin, a potent inhibitor of protein phosphatases 1 and 2A, is a new environmental carcinogen in male F344 rat liver. Cancer Res. 54:1994;6402-6406.
32. Pflugmacher S., Wiegand C., Beattie K.A., Codd G.A., Steinberg C.E.W. Uptake of the cyanobacterial hepatotoxin microcystin-LR by aquatic macrophytes. J. Appl. Bot. 72:1998;228-232.
33. Pouria S., de Andrade A., Barbosa J., Cavalcanti R.L., Barreto V.T.S., Ward C.J., Preiser W., Poon G.K., Neild G.H., Codd G.A. Fatal microcystin intoxication in haemodialysis unit in Caruaru, Brazil. Lancet. 352:1998;21-26.
34. Rinehart K.L., Namikoshi M., Choi B.W. Structure and biosynthesis of toxins from blue-green algae (cyanobacteria). J. Appl. Phycol. 6:1994;159-176.
35. Robinson N.A., Miura G.A., Matson C.F., Dinterman R.E., Pace J.G. Characterization of chemically tritiated microcystin-LR and its distribution in mice. Toxicon. 27:1989;1035-1042.
36. 125I-labelled toxic peptides from the blue-green alga Microcystis aeruginosa. Toxicon. 24:1986;506-509.
37. Runnegar M., Berndt N., Kong S.-M., Lee E.Y.C., Zhang L. In vivo and in vitro binding of microcystin to protein phosphatases 1 and 2A. Biochem. Biophys. Res. Commun. 216:1995;162-169.
38. Sano T., Nohara K., Shiraishi F., Kaya K. A method for micro-determination of total microcystin content in waterblooms of cyanobacteria (blue-green algae). Int. J. Environ. Anal. Chem. 49:1992;163-170.
39. Sipiä V., Kankaanpää H., Lahti K., Carmichael W.W., Meriluoto J. Detection of nodularin in flounders and cod from the Baltic Sea. Environ. Toxicol. 16:2001;121-126.
40. Sivonen K., Jones G. Cyanobacterial toxins. Chorus I., Bartram J. Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring, and Management. 1999;41-111 E & FN Spon, London.
41. Sivonen K., Niemelä S.I., Niemi R.M., Lepistö L., Luoma T.H., Räsänen L.A. Toxic cyanobacteria (blue-green algae) in Finnish fresh and coastal waters. Hydrobiologia. 190:1990;267-275.
42. Stotts R.R., Twardock A.R., Haschek W.M., Choi B.W., Rinehart K.L., Beasley V.R. Distribution of tritiated dihydromicrocystin in swine. Toxicon. 35:1997;937-953.
43. Stotts R.R., Twardock A.R., Koritz G.D., Haschek W.M., Manuel R.K., Hollis W.B., Beasley V.R. Toxicokinetics of tritiated dihydromicrocystin-LR in swine. Toxicon. 35:1997;455-465.
44. Watanabe M.F., Park H.-D., Kondo F., Harada K.-, Hayashi H., Okino T. Identification and estimation of microcystins in freshwater mussels. Nat. Toxins. 5:1997;31-35.
45. Williams D.E., Kent M.L., Andersen R.J., Klix H., Holmes C.F.B. Tissue distribution and clearance of tritium-labeled dihydromicrocystin-LR epimers administered to Atlantic salmon via intraperitoneal injection. Toxicon. 33:1995;125-131.
46. Williams D.E., Craig M., Dawe S.C., Kent M.L., Holmes C.F.B., Andersen R.J. Evidence for a covalently bound form of microcystin-LR in salmon liver and dungeness crab larvae. Chem. Res. Toxicol. 10:1997;463-469.
47. Yoshida T., Makita Y., Tsutsumi T., Nagata S., Tashiro F., Yoshida F., Sekijima M., Tamura S.-I., Harada T., Maita K., Ueno Y. Immunohistochemical localization of microcystin-LR in the liver of mice: a study on the pathogenesis of microcystin-LR-induced hepatotoxicity. Toxicol. Pathol. 26:1998;411-418.
48. Yoshizawa S., Matsushima R., Watanabe M.F., Harada K.-, Ichihara A., Carmichael W.W., Fujiki H. Inhibition of protein phosphatases by microcystins and nodularin associated with hepatotoxicity. J. Cancer Res. Clin. Oncol. 116:1990;609-614.