Polyketides from marine dinoflagellates of the genus Prorocentrum, biosynthetic origin and bioactivity of their okadaic acid analogues

Mini-Reviews in Medicinal Chemistry

Volumn 10, Issue 1, 2010, Pages 51-61

  Hu, Weimin ^a   Xu, Jing ^b   Sinkkonen, Jari ^c   Wu, Jun ^a  

^a SOUTH CHINA SEA INSTITUTE OF OCEANOLOGY   (China)

^b OCEAN UNIVERSITY OF CHINA   (China)

^c UNIVERSITY OF TURKU   (Finland)

Author keywords

Biosynthetic origin; Dinoflagellate; Inhibition to PP1 and PP2A; Okadaic acid; Pharmacophore; Polyketide; Prorocentrum

Indexed keywords

2 DEOXYOKADAIC ACID; 4 HYDROXYPROROCENTROLIDE; 9,51 DIHYDROPROROCENTROLIDE; BELIZEANIC ACID; BELIZEANOLIC ACID; BELIZEANOLIDE; CARBON 13; DEUTERIUM; DINOPHYSISTOXIN 1; DINOPHYSISTOXIN 2; DINOPHYSISTOXIN 4; DINOPHYSISTOXIN 5A; DINOPHYSISTOXIN 5B; DINOPHYSISTOXIN 5C; DINOPHYSISTOXIN 6; HOFFMANNIOLIDE; KETONE DERIVATIVE; NOROKADANONE; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 2A; POLYKETIDE; PROROCENTIN; PROROCENTROLIDE; PROROCENTROLIDE 30 SULFATE; PROROCENTROLIDE B; SPIROPROROCENTRIMINE; UNCLASSIFIED DRUG;

BIOSYNTHESIS; CHEMICAL STRUCTURE; DINOFLAGELLATE; ENZYME INHIBITION; NONHUMAN; PHARMACOPHORE; PROROCENTRUM; REVIEW;

ANIMALS; CATALYTIC DOMAIN; DINOFLAGELLIDA; ENZYME INHIBITORS; HUMANS; MACROLIDES; MARINE TOXINS; OKADAIC ACID; PROTEIN BINDING; PROTEIN PHOSPHATASE 1; PROTEIN PHOSPHATASE 2; SPECIES SPECIFICITY;

EID: 77951112385     PISSN: 13895575     EISSN: None     Source Type: Journal    
DOI: 10.2174/138955710791112541     Document Type: Review

References (50)

1. Tachibana, K.; Scheuer, P. J.; Tsukitani, Y.; Kikuchi, H.; Van Engen, D.; Clardy, J.; Gopichand, Y.; Schmitz, F. J. Okadaic acid, a cytotoxic polyether from two marine sponges of the genus Halichondria. J. Am. Chem. Soc., 1981, 103, 2469-2471
2. Schmitz, F. J.; Prasad, R. S.; Gopichand, Y.; Hossain, M. B.; Van der Helm, D.; Schmidt, P. Acanthifolicin, a new episulfide-containing polyether carboxylic acid from extracts of the marine sponge Pandaros acanthifolium. J. Am. Chem. Soc., 1981, 103, 2467-2469
3. Murakami, Y.; Oshima, Y.; Yasumoto, T. Identification of okadaic acid as a toxic component of a marine dinoflagellate Prorocentrum lima. Bull. Jpn. Soc. Sci. Fish., 1982, 48, 69-72.
4. Hu, T. M.; Marr, J.; Defreitas, A. S. W.; Quilliam, M. A.; Walter, J. A.; Wright, J. L. C.; Pleasance, S. New diol esters isolated from cultures of the dinoflagellates Prorocentrum lima and Prorocentrum concavum. J. Nat. Prod., 1992, 55, 1631-1637
5. Morton, S. L. Morphology and toxicology of Prorocentrum faustiae sp. nov., a toxic species of non-planktonic dinoflagellate from Heron Island, Australia. Bot. Mar., 1998, 41, 565-569
6. Ten-Hage, L.; Delaunay, N.; Pichon, V.; Coute, A.; Puiseux-Dao, S.; Turquet, J. Okadaic acid production from the marine benthic dinoflagellate Prorocentrum arenarium Faust (Dinophyceae) isolated from Europa Island coral reef ecosystem (SW Indian Ocean). Toxicon, 2000, 38, 1043-1054
7. Cruz, P. G.; Daranas, A. H.; Fernandez, J. J.; Souto, M. L.; Norte, M. DTX5c, a new OA sulphate ester derivative from cultures of Prorocentrum belizeanum. Toxicon, 2006, 47, 920-924
8. Dickey, R. W.; Bobzin, S. C.; Faulkner, D. J.; Bencsath, F. A.; Andrzejewski, D. Identification of okadaic acid from a Caribbean dinoflagellate, Prorocentrum concavum. Toxicon, 1990, 28, 371-377
9. Cruz, P. G.; Daranas, A. H.; Fernandez, J. J.; Norte, M. 19-epiokadaic acid, a novel protein phosphatase inhibitor with enhanced selectivity. Org. Lett., 2007, 9, 3045-3048
10. Marr, J. C.; Jackson, A. E.; Mclachlan, J. L. Occurrence of Prorocentrum lima, a DSP toxin-producing species from the Atlantic coast of Canada. J. Appl. Phycol., 1992, 4, 17-24.
11. Bravo, I.; Fernandez, M. L.; Ramilo, I.; Martinez, A. Toxin composition of the toxic dinoflagellate Prorocentrum lima isolated from different locations along the Galician coast (NW Spain). Toxicon, 2001, 39, 1537-1545
12. Hu, T. M.; Curtis, J. M.; Walter, J. A.; Wright, J. L. C. Identification of DTX-4, a new water-soluble phosphatase inhibitor from the toxic dinoflagellate Prorocentrum lima. J. Chem. Soc. Chem.Commun., 1995, 597-599
13. Nascimento, S. M.; Purdie, D. A.; Morris, S. Morphology, toxin composition and pigment content of Prorocentrum lima strains isolated from a coastal lagoon in southern UK. Toxicon, 2005, 45, 633-649
14. Hu, T.; Curtis, J. M.; Walter, J. A.; McLachlan, J. L.; Wright, J. L. C. Two New Water-soluble DSP toxin derivatives from the dinoflagellate Prorocentrum maculosum: possible storage and excretion products. Tetrahedron Lett., 1995, 36, 9273-9276
15. Suarez-Gomez, B.; Souto, M. L.; Norte, M.; Fernandez, J. J. Isolation and structural determination of DTX-6, a new okadaic acid derivative. J. Nat. Prod., 2001, 64, 1363-1364
16. Fernandez, J. J.; Suarez-Gomez, B.; Souto, M. L.; Norte, M. Identification of new okadaic acid derivatives from laboratory cultures of Prorocentrum lima. J. Nat. Prod., 2003, 66 (9), 1294-1296
17. Suarez-Gomez, B.; Souto, M. L.; Cruz, P. G.; Fernandez, J. J.; Norte, M. New targets in diarrhetic shellfish poisoning control. J. Nat. Prod., 2005, 68, 596-599
18. Yasumoto, T.; Murata, M.; Lee, J.; Torigoe, K. In Mycotoxins and Phycotoxins '88, Natori, S.; Hashimoto, K.; Ueno, Y., Ed.; Elsevier Science Publishers: Amsterdam, 1989, pp. 375-382
19. Yasumoto, T.; Seino, N.; Murakami, Y.; Murata, M. Toxins produced by benthic dinoflagellates. Biol. Bull., 1987, 172, 128-131
20. Nagai, H.; Satake, M.; Yasumoto, T. Antimicrobial activities of polyether compounds of dinoflagellate origins. J. Appl. Phycol., 1990, 2, 305-308
21. Norte, M.; Padilla, A.; J. Fernandez, J.; L. Souto, M. Structural determination and biosynthetic origin of two ester derivatives of okadaic acid isolated from Prorocentrum lima. Tetrahedron, 1994, 50, 9175-9180
22. Schmitz, F. J.; Yasumoto, T. The 1990 United States-Japan seminar on bioorganic marine chemistry, meeting report. J. Nat. Prod., 1991, 54, 1469-1490
23. Holmes, M. J.; Lee, F. C.; Khoo, H. W.; Teo, S. L. M. Production of 7-deoxy-okadaic acid by a new caledonian strain of Prorocentrum lima (Dinophyceae). J. Phycol., 2001, 37, 280-288
24. Cruz, P. G.; Fernandez, J. J.; Norte, M.; Daranasa, A. H., Belizeanic acid: A potent protein phosphatase 1 inhibitor belonging to the okadaic acid class, with an unusual skeleton. Chem. Eur. J., 2008, 14, 6948-6956
25. Terao, K.; Ito, E.; Yanagi, T.; Yasumoto, T. Histopathological studies on experimental marine toxin poisoning. Ultrastructuralchanges in the small-intestine and liver of suckling mice induced by dinophysistoxin-1 and pectenotoxin-11. Toxicon, 1986, 24, 1141-1151
26. Yasumoto, T.; Murata, M. Polyether toxins involved in seafood poisoning. In Marine Toxins: Origin, structure and molecular pharmacology, Hall, S. and Strichartz, G., Ed.; American Chemical Society, 1990; pp. 120-132
27. Aune, T.; Larsen, S.; Aasen, J. A. B.; Rehmann, N.; Satake, M.; Hess, P. Relative toxicity of dinophysistoxin-2 (DTX-2) compared with okadaic acid, based on acute intraperitoneal toxicity in mice. Toxicon, 2007, 49, 1-7.
28. Torigoe, K.; Murata, M.; Yasumoto, T.; Iwashita, T. Prorocentrolide, a toxic nitrogenous macrocycle from a marine dinoflagellate, Prorocentrum lima. J. Am. Chem. Soc., 1988, 110, 7876-7877
29. Torigoe, K. Structure and biosynthesis of bioactive substances produced by the dinoflagellate Prorocentrum lima. Tohoku University: Sendai, 1990.
30. Lu, C.-K.; Lee, G.-H.; Huang, R.; Chou, H.-N. Spiroprorocentrimine, a novel macrocyclic lactone from a benthic Prorocentrum sp. of Taiwan. Tetrahedron Lett., 2001, 42, 1713-1716
31. Hu, T.; deFreitas, A. S. W.; Curtis, J. M.; Oshima, Y.; Walter, J. A.; Wright, J. L. C. Isolation and structure of prorocentrolide b, a fast-acting toxin from Prorocentrum maculosum. J. Nat. Prod., 1996, 59, 1010-1014
32. Hu, T.; Curtis, J. M.; Walter, J. A.; Wright, J. L. C. Hoffmanniolide: a novel macrolide from Prorocentrum hoffmannianum. Tetrahedron Lett., 1999, 40, 3977-3980
33. Lu, C. K.; Chou, H. N.; Lee, C. K.; Lee, T. H. Prorocentin, a new polyketide from the marine dinoflagellate Prorocentrum lima. Org. Lett., 2005, 7 (18), 3893-3896
34. Napolitano, J. G.; Norte, M.; Padron, J. M.; Fernandez, J. J.; Daranas, A. H. Belizeanolide, a cytotoxic macrolide from the dinoflagellate Prorocentrum belizeanum. Angew. Chem. Int. Ed., 2009, 48, 796-799
35. Norte, M.; Padilla, A.; Fernandez, J. J. Studies on the biosynthesis of the polyether marine toxin di nophysistoxin-1 (DTX-1). Tetrahedron Lett., 1994, 35, 1441-1444
36. Needham, J.; Mclachlan, J. L.; Walter, J. A.; Wright, J. L. C. Biosynthetic origin of C-37 and C-38 in the polyether toxins okadaic acid and dinophysistoxin-1. J. Chem. Soc. Chem. Commun., 1994, 2599-2600
37. Daranas, A. H.; Fernández, J. J.; Norte, M.; Gavín, J. A.; Suaŕez-Gómez, B.; Souto, M. L. Biosynthetic studies of the DSP toxin skeleton. Chem. Rec., 2004, 4, 1-9.
38. 2]acetate elucidated by collision-induced dissociation tandem mass spectrometry. J. Am. Chem. Soc., 1998, 120, 147-151
39. 18o in dinoflagellate Prorocentrum Lima elucidated by tandem mass spectrometry. Eur. J. Biochem., 2000, 267, 5179-5183
40. Wright, J. L. C.; Hu, T.; McLachlan, J. L.; Needham, J.; Walter, J. A. Biosynthesis of DTX-4: confirmation of a polyketide pathway, proof of a Baeyer-Villiger oxidation step, and evidence for an unusual carbon deletion process. J. Am. Chem. Soc., 1996, 118, 8757-8758
41. Macpherson, G. R.; Burton, I. W.; LeBlanc, P.; Walter, J. A.; Wright, J. L. Studies of the biosynthesis of DTX-5a and DTX-5b by the dinoflagellate Prorocentrum maculosum: regiospecificity of the putative Baeyer-Villigerase and insertion of a single amino acid in a polyketide chain. J. Org. Chem., 2003, 68, 1659-1664
42. Bialojan, C.; Takai, A. Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases: specificity and kinetics. Biochem. J., 1988, 256, 283-290
43. Haystead, T. A. J.; Sim, A. T. R.; Carling, D.; Honnor, R. C.; Tsukitani, Y.; Cohen, P.; Hardie, D. G. Effects of the tumour promoter okadaic acid on intracellular protein phosphorylation and metabolism. Nature, 1989, 337, 78-81.
44. Cohen, P.; Klumpp, S.; Schelling, D. L. An Improved procedure for identifying and quantitating protein phosphatases in mammalian-tissues. FEBS Lett., 1989, 250, 596-600.
45. Villafranca, J. E.; Kissinger, C. R.; Parge, H. E. Protein serine/threonine phosphatases. Curr. Opin. Biotechnol., 1996, 7, 397-402.
46. Maynes, J. T.; Bateman, K. S.; Cherney, M. M.; Das, A. K.; Luu, H. A.; Holmes, C. F. B.; James, M. N. G. Crystal structure of the tumor-promoter okadaic acid bound to protein phosphatase-1. J. Biol. Chem., 2001, 276, 44078-44082
47. Xing, Y.; Xu, Y.; Chen, Y.; Jeffrey, P. D.; Chao, Y.; Lin, Z.; Li, Z.; Strack, S.; Stock, J. B.; Shi, Y. Structure of protein phosphatase 2A core enzyme bound to tumor-inducing toxins. Cell, 2006, 127, 341-353
48. Colby, D. A.; Chamberlin, A. R. Pharmacophore identification: The case of the Ser/Thr protein phosphatase inhibitors. Mini-Rev. Med. Chem. 2006, 6, 657-665
49. Fernandez, J. J.; Candenas, M. L.; Souto, M. L.; Trujillo, M. M.; Norte, M. Okadaic acid, useful tool for studying cellular processes. Curr. Med. Chem., 2002, 9, 229-262
50. Vilarino, N.; Ares, I. R.; Cagide, E.; Louzao, M. C.; Vieytes, M. R.; Yasumoto, T.; Botana, L. M. Induction of actin cytoskeleton rearrangement by methyl okadaate-comparison with okadaic acid. FEBS J., 2008, 275, 926-934