Azaspiracid poisoning (AZP) toxins in shellfish: Toxicological and health considerations

Toxicon

Volumn 56, Issue 2, 2010, Pages 173-190

  Furey, Ambrose ^a   O'Doherty, Sinead ^b   O'Callaghan, Keith ^a   Lehane, Mary ^b   James, Kevin J ^a,c  

^a Munster Technological University   (Ireland)

^b Athletic Rehabilitation Therapy Ireland   (Ireland)

^c UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Azaspiracids; AZP; LC MS; Marine toxins; Mytilus edulis

Indexed keywords

AZASPIRACID;

ARTICLE; CARBOXYLATION; CHEMICAL STRUCTURE; CONSUMER; DISEASE SEVERITY; FOOD CONTROL; FOOD INTAKE; GASTROINTESTINAL DISEASE; HUMAN; HYDROXYLATION; INJURY SEVERITY; LIQUID CHROMATOGRAPHY; LUNG TUMOR; METHYLATION; MUSSEL; NONHUMAN; PRIORITY JOURNAL; PUBLIC HEALTH; RISK ASSESSMENT; SENSITIVITY AND SPECIFICITY; SHELLFISH; SHELLFISH POISONING; TANDEM MASS SPECTROMETRY; TISSUE INJURY; TOXIN ANALYSIS;

ANIMALS; CELL LINE, TUMOR; CELL SURVIVAL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; FOODBORNE DISEASES; HUMANS; INTESTINE, SMALL; LUNG NEOPLASMS; MARINE TOXINS; MICE; MICROSCOPY, ELECTRON, SCANNING; MOLECULAR STRUCTURE; MYTILUS EDULIS; NEURONS; SHELLFISH; SHELLFISH POISONING; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPIRO COMPOUNDS; TANDEM MASS SPECTROMETRY; TOXICITY TESTS;

MUS; MYTILUS EDULIS;

EID: 77953286406     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2009.09.009     Document Type: Article

References (138)

1. Aiguade J., Hao J., Forsyth C.J. Biomimetic studies towards the C28-C40 polycyclic domain of the azaspiracids. Tetrahedron Letters 2001, 42:817-820.
2. Aiguade J., Hao J., Forsyth C.J. Synthesis of a 2,9-dioxabicyclo[3.3.1]nonane via double intramolecular hetero-michael addition: to the F-G ring system of the azaspiracids. Organic Letters 2001, 3:979-982.
3. Aiguade J., Hao J.L., Forsyth C.J. Studies toward the total synthesis of azaspiracid 1: synthesis of the C28-C40 polycyclic domain. Abstracts of Papers of the American Chemical Society 2000, 219:766. ORGN.
4. 2+ entry by stored operated channels in human T lymphocytes. Biochemical Pharmacology 2005, 69:1627-1636.
5. Alfonso A., Vieytes M.R., Ofugi K., Satake M., Nicolaou K.C., Frederick M.O., Botana L.M. Azaspiracids modilate intracellular pH levels in human lymphocytes. Biochemical and Biophysical Research Communications 2006, 346:1091-1099.
6. Allingham, J.S., Miles, C.O., and Rayment, E., 2007. A structural basis for regulation of actin polymerisation by pectenotoxins. 371, 959-970.
7. Alvarez G., Uribe E., Avalos P., Marino C., Blanco J. First Identification of azaspiracid and spirolides in Mesodesma donacium and Mulinia edulis from Northern Chile. Toxicon 2010, 55:638-641.
8. Anonymous, 2001. Report of the meeting of the EU Working group on Toxicology of DSP and AZP, May 21st-23rd, Brussels, Belgium.
9. Anonymous, 2005. EU Community Reference Laboratory on Marine Biotoxins Working Group on Toxicology, Cesenatico, October 24-25, 2005.
10. Anonymous Marine biotoxins in shellfish-summary on regulated marine biotoxins. Scientific opinion on contaminants in the food chain. The EFSA Journal 2009, 1-23.
11. Aune T. Risk assessment of marine toxins. Seafood and Freshwater Toxins 2008, 3-20. CRC Press, Taylor and Francis, New York. L.M. Botana (Ed.).
12. Bialojan C., Takai A. Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases. Specificity and kinetics. Journal of Biochemistry 1988, 256:283-290.
13. Blay P.K.S., Brombacher S., Volmer D.A. Studies on azaspiracid biotoxins. III. Instrumental validation for rapid quantification of AZA 1 in complex biological matrices. Rapid Communications in Mass Spectrometry 2003, 17:2153-2159.
14. Carter R.G., Bourland T.C., Graves D.E. Synthesis of the ABC ring system of azaspiracid. 1. Effect of D ring truncation on bis-spirocyclization. Organic Letters 2002, 4:2177-2179.
15. Carter R.G., Graves D.E., Gronemeyer M.A., Tschumper G.S. Synthesis of the ABC ring system of azaspiracid. 2. A systematic study into the effect of C(16) and C(17) substitution on bis-spirocyclization. Organic Letters 2002, 4:2181-2184.
16. Carter R.G., Bourland T.C., Zhou X.T., Gronemeyer M.A. Controlling influences in bisspiroketal formation: synthesis of the ABC ring system of azaspiracid. Tetrahedron 2003, 59:8963-8974.
17. Carter R.G., Graves D.E. Studies direct toward the total synthesis of azaspiracid. Construction of C1-C9 carbon backbone and synthesis of C10, C13 nonnatural transoidal bisspirocyclic ring system. Tetrahedron Letters 2001, 42:6035-6039.
18. Carter R.G., Weldon D.J. Studies directed toward the total synthesis of azaspiracid: stereoselective construction of C-1-C-12, C-13-C-19, and C-21-C-25 fragments. Organic Letters 2000, 2:3913-3916.
19. Carter, R.G., Weldon, D.J., and Bourland, T.C., 2001. Synthetic studies toward the total synthesis of azaspiracid. Abstracts of Papers of the American Chemical Society 221, 479-ORGN.
20. Cohen P. The structure and regulation of protein phosphatases. Annual Reviews of Biochemistry 1989, 58:453-508.
21. Colman J.R., Twiner M.J., Hess P., McMahon T., Satake M., Yasumoto T., Doucette G.J., Ramsdell J.S. Teratogenic effects of azaspiracid-1 identified by microinjection of Japanese medaka (Oryzias latipes) embryos. Toxicon 2005, 45:881-890.
22. Cooper D.M.F., Mons N., Karpen J.W. Adenylyl cyclases and the interaction between calcium and cAMP signaling. Nature 1995, 374:421-424.
23. De Schrijver K., Maes I., De Man L., Michelet J. An outbreak of diarrhoeic poisoning in Antwerp, Belgium. Eurosurveillance Monthly 2002, 7:138-141.
24. Diaz Sierra M., Furey A., Hamilton B., Lehane M., James K.J. Elucidation of the fragmentation pathways of azaspiracids, using electrospray ionisation, hydrogen/deuterium exchange, and multiple-stage mass spectrometry. Journal of Mass Spectrometry 2003, 38:1178-1186.
25. Diaz Sierra, M., Furey, A., Lehane, M., Magdalena, A.B., James, K.J., 2002. Detection of six new azaspiracids in shellfish using liquid chromatography with multiple tandem mass spectrometry. In: Xth International Conference on Harmful Algae, pp. 204-206.
26. Dounay A.B., Forsyth C.J. Synthetic studies toward the C1-C20 domain of azaspiracid. Abstracts of Papers of the American Chemical Society 2001, 221:475.
27. Draisci R., Palleschi L., Ferretti E., Furey A., James K.J., Satake M., Yasumoto T. Development of a liquid chromatography-tandem mass spectrometry method for the identification of azaspiracid in shellfish. Journal of Chromatography 2000, 871:13-21.
28. FAO/IOC/WHO Report of the Joint FAO/IOC/WHO Ad Hoc Expert Consultation on Biotoxins in Bivalve Molluscs, September 26-30, 2004 2004, Available from:, Oslo, Norway. http://www.fao.org/ag/agn/food/risk_biotoxin_en.stm.
29. Flanagan A.F., Callanan K.R., Donlon J., Palmer R., Forde A., Kane M. A cytotoxicity assay for the detection and differentiation of two families of shellfish toxins. Toxicon 2001, 39:1021-1027.
30. Forsyth C.J., Hao J.L., Aiguade J. Synthesis of the (+)-C26-C40 domain of the azaspiracids by a novel double intramolecular hetero-michael addition strategy. Angewandte Chemie-International Edition 2001, 40:3663.
31. Frederick M.O., Cole K.P., Pertrovic G., Loizidou E., Nicolaou K.C. Structural assignment and total synthesis of azaspiracid-1. Phycotoxins: Chemistry and Biochemistry 2007, 297-309. Blackwell Publishing, Oxford, UK. L.M. Botana (Ed.).
32. FSAI Risk Assessment of Azaspiracids (AZAs) in Shellfish 2001, Food Safety Authority of Ireland.
33. FSAI, 2006. Risk assessment of azaspiracids in shellfish. A report of the Scientific Comittee of the food safety authority of Ireland.
34. Furey A., Braña-Magdalena A., Lehane M., Moroney C., James K.J., Satake M., Yasumoto T. Determination of azaspiracids in shellfish using liquid chromatography-tandem electrospray mass spectrometry. Rapid Communications in Mass Spectrometry 2002, 16:238-242.
35. Furey A., Moroney C., Magdalena A.B., Saez M.J.F., Lehane M., James K.J. Geographical, temporal, and species variation of the polyether toxins, azaspiracids, in shellfish. Environmental Science and Technology 2003, 37:3078-3084.
36. Fux E., McMillan D., Bire R., Hess P. Development of an ultra-performance liquid chromatography-mass spectrometry method for the detection of lipophilic marine toxins. Journal of Chromatography A 2007, 1157:273-280.
37. Gent J., Braakman I. Low-density lipoprotein receptor structure and folding. Cellular and Molecular Life Sciences 2004, 61:2461-2470.
38. Graziano F., Humar B., Guilford P. The role of the E-cadherin gene (CDH1) in diffuse gastric cancer susceptibility: from the laboratory to clinical practise. Annals of Oncology 2003, 14:1705-1713.
39. Green D., Reed J. Mitochondria and apoptosis. Science 1998, 281:1309-1312.
40. Hamilton B., Sierra M.D., Lehane M., Furey A., James K.J. The fragmentation pathways of azaspiracids elucidated using positive nanospray hybrid quadrupole time-of-flight (QqTOF) mass spectrometry. Spectroscopy-an International Journal 2004, 18:355-362.
41. Hao J., Aiguade J., Forsyth C.J. Remarkably chemoselective indium-mediated coupling en route to the C21-C40 acyclic portion of the azaspiracids. Tetrahedron Letters 2001, 42:821-824.
42. Hao J.L., Aiguade J., Forsyth C.J. Studies toward the total synthesis of azaspiracid 2: synthesis of C21-C27 and C21-C40 fragments. Abstracts of Papers of the American Chemical Society 2000, 219:767. ORGN.
43. Hess P., Butter T., Petersen A., Silke J., McMohan T. Performance of the EU-harmonised mouse bioassay for lipophilic toxins for the detection of azaspiracids in naturally contaminated mussel (Mytilus edulis) hepatopancreas tissue homogenates characterised by liquid chromatography coupled to tandem mass spectrometry. Toxicon 2009, 53:713-722.
44. Hess P., McCarron P., Rehmann N., Kilcoyne J., McMahan T., Ryan G., Ryan P.M., Twiner M.J., Doucette G.J., Ito E., Yasumoto T. Isolation and Purification of Azaspiracids from Naturally Contaminated Materials, and Evaluation of Their Toxicological Effects Final Project Report. Marine Environment and Health Series 28 2007, Marine Institute, p. 129.
45. Hess P., Nguyen L., Aason J., Keogh M., Kilcoyne J., McCarron P., Aune T. Tissue distribution, effects of cooking and parameters affecting the extraction of azaspiracids from mussels, Mytilus edulis, prior to analysis by liquid chromatography coupled to mass spectrometry. Toxicon 2005, 46:62-71.
46. Hu T.M., Curtis J.M., Oshima Y., Quilliam M.A., Watson-Wright W.M., Wright J.L.C. Spirolides B and D, two novel macrocycles isolated from the digestive glands of shellfish. Journal of the Chemical Society, Chemical Communications 1995, 2159-2161.
47. Huss H. Control of indigenous pathogenic bacteria in seafood. Food Control 1997, 18:91-98.
48. Ito E. Toxicology of Azaspiracid-1: acute and chronic poisoning, tumourigenicity and chemical structure relationship to toxicity in a mouse bioassay. Seafood and Freshwater Toxins: Pharmacology, Physiology and Detection 2008, 775-784. CRC Press, Taylor and Francis, New York. L.M. Botana (Ed.).
49. Ito E., Frederick M.O., Koftis T.V., Tang W., Petrovic G., Ling T., Nicolaou K.C. Structure toxicity relationships of synthetic azaspiracid-1 and analogs in mice. Harmful Algae 2006, 5:486-591.
50. Ito E., Satake M. Azaspiracid, a new marine toxin isolated from mussels: chemistry and histopathology. Seafood Safety and Human Health 2002, vol. 7:31-39. Science Publishers, Enfield, New Hampshire. M. Fingerman, R. Nagabhushanam (Eds.).
51. Ito, E., Satake, M., Ofugi, K., McMahon, T., Silke, J., James, K.J., Yasumoto, T., 2000a. Small intestine injuries in mice caused by a new toxin, azaspiracid, isolated from Irish mussels. In: Ninth International Conference on Harmful Algal Blooms, pp. 395-398.
52. Ito E., Satake M., Ofuji K., Higashi M., Harigaya K., McMahon T., Yasumoto T. Chronic effects in mice caused by oral administration of sublethal doses of azaspiracid, a new marine toxin isolated from mussels. Toxicon 2002, 40:193-203.
53. Ito E., Satake M., Ofuji K., Kurita N., James K.J., McMahon T., Yasumoto T. Multiple organ damage caused by a new toxin azaspiracid, isolated from mussels produced in Ireland. Toxicon 2000, 38:917-930.
54. Ito E., Terao K. Injury and recovery process of intestine caused by okadaic acid and related compounds. Natural Toxins 1994, 2:371-377.
55. Ito E., Terao K., McMahon T., Silke J., Yasumoto T. Acute pathological changes in mice caused by crude extracts of novel toxins isolated from Irish mussels. Harmful Algae 1997, 588-589.
56. James K.J., Fidalgo Sáez M.J., Furey A., Lehane M. Azaspiracid poisoning, the food-borne illness associated with shellfish consumption: a review. Food Additives and Contaminants 2004, 21:879-892.
57. James, K.J., Furey, A., Lehane, M., Moroney, C., Satake, M., Yasumoto, T., 2001. LC-MS methods for the investigation of a new shellfish toxic syndrome-Azaspiracid Poisoning (AZP). Mycotoxins and Phycotoxins in Perspective at the Turn of the Century, pp. 401-408.
58. James K.J., Furey A., Lehane M., Ramstad H., Aune T., Hovgaard P., Msorris S., Higman W., Satake M., Yasumoto T. First evidence of an extensive northern European distribution of azaspiracid poisoning (AZP) toxins in shellfish. Toxicon 2002, 40:909-915.
59. James, K.J., Furey, A., Satake, M., Yasumoto, T., 2000. Azaspiracid poisoning (AZP): A new shellfish toxic syndrome in Europe. In: Ninth International Conference on Harmful Algal Blooms, pp. 250-253.
60. James K.J., Lehane M., Moroney C., Fernandez-Puente P., Satake M., Yasumoto T., Furey A. Azaspiracid shellfish poisoning: unusual toxin dynamics in shellfish and the increased risk of acute human intoxications. Food Additives and Contaminants 2002, 19:555-561.
61. James K.J., Moroney C., Roden C., Satake M., Yasumoto T., Lehane M., Furey A. Ubiquitous 'benign' alga emerges as the cause of shellfish contamination responsible for the human toxic syndrome, azaspiracid poisoning. Toxicon 2003, 41:145-151.
62. James K.J., O'Driscoll D., Fernandez J.G., Furey A. Azaspiracids: chemistry, bioconversion and determination. Seafood and Freshwater Toxins: Pharmacology, Physiology and Detection 2008, 763-773. CRC Press, Taylor and Francis, New York. L.M. Botana (Ed.).
63. James K.J., Sierra M.D., Lehane M., Magdalena A.B., Furey A. Detection of five new hydroxyl analogues of azaspiracids in shellfish using multiple tandem mass spectrometry. Toxicon 2003, 41:277-283.
64. Kellmann R., Schaffer C.A.M., Gronset T.A., Satake M., Ziegler M., Fladmark K.E. Proteomic response of human neuroblastoma cells to azaspiracid-1. Journal of Proteomics 2009, 72:695-707.
65. Korsnes M.S., Hetland D.L., Espenes A., Aune T. Induction of apoptosis by YTX in myoblast cell lines via mitochondrial signalling transduction pathway. Toxicology in Vitro 2006, 20:1419-1426.
66. Krock B., Tillmann U., John U., Cembella A.D. Characterization of azaspiracids in plankton size-fractions and isolation of an azaspiracid-producing dinoflagellate from the North Sea. Harmful Algae 2008, 8:254-263.
67. Kulagina N.V., Mikulski C.M., Gray S.A., Ma W., Doucette G.J., Ramsdell J.S., Pancrazio J.J. Neuronal networks on microelctrode arrays for the detection of marine toxins, brevetoxin and saxitoxin. Environmental Science and Technology 2006, 40:578-583.
68. Kulagina N.V., O'Shaughnessy T.J., Wu Ma, Ramsdell J.S., Pancrazio J.J. Pharmacological effect of marine toxins, brevetoxin-2 and saxitoxin, on murine frontal cortex neuronal networks. Toxicon 2004, 44:669-676.
69. Kulagina N.V., Twiner M.J., Hess P., McMahon T., Satake M., Yasumoto T., Ramsdell J.S., Doucette G.J., Ma W., O'Shaughnessy T.J. Azaspiraicd-1 inhibits bioelectrical activity of spinal cord neuronal networks. Toxicon 2006, 47:766-773.
70. Lehane M., Brana-Magdalena A., Moroney C., Furey A., James K.J. Liquid chromatography with electrospray ion trap mass spectrometry for the determination of five azaspiracids in shellfish. Journal of Chromatography A 2002, 950:139-147.
71. Lehane M., Saez M.J.F., Magdalena A.B., Canas I.R., Sierra M.D., Hamilton B., Furey A., James K.J. Liquid chromatography-multiple tandem mass spectrometry for the determination of ten azaspiracids, including hydroxyl analogues in shellfish. Journal of Chromatography A 2004, 1024:63-70.
72. Leira F., Alvarez C., Cabado A.G., Vieites J.M., Vieytes M.R., Botana L.M. Development of a F-actin-based live-cell fluorimetric microplate assay for diarrhetic shellfish toxins. Biochemical Pharmacology 2002, 63:1979-1988.
73. Leira F., Alvarez C., Vieites J.M., Vieytes M.R., Botana L.M. Study of cytosketal changes induced by okadaic acid in BE(2)-M17 cells by means of a quantitative fluorimetric assay. Toxicology in Vitro. 2001, 277-282.
74. Leising A., Horner R., Pierson J.J., Postel J., Halsband-Lenk C. The balance between microzooplankton grazing and phytoplankton growth in a highly productive estuarine fjord. Progress in Oceanography 2005, 67:366-383.
75. López-Rivera, A., O. C.K., Moriarty, M., O'Driscoll, D., Hamilton, B., Lehane, M., James, K.J., Furey, A. First evidence of azaspiracids (AZAs): a family of lipophilic polyether marine toxins in scallops (Argopecten purpuratus) and mussels (Mytilus chilensis) collected in two regions of Chile. Toxicon, in press. doi:10.1016/j.tocixon.2009.10.020.
76. Magdalena A.B., Lehane M., Krys S., Fernandez M.L., Furey A., James K.J. The first identification of azaspiracids in shellfish from France and Spain. Toxicon 2003, 42:105-108.
77. Magdalena A.B., Lehane M., Moroney C., Furey A., James K.J. Food safety implications of the distribution of azaspiracids in the tissue compartments of scallops (Pecten maximus). Food Additives and Contaminants 2003, 20:154-160.
78. McCarron P., Kilcoyne J., Miles C.O., Hess P. Formation of azaspiracids -3, -4, -6 and -9 via decarboxylation of carboxyazaspiracid metabolites from shellfish. Journal of Agricultural and Food Chemistry 2009, 57:160-169.
79. McElhatton P.R. Principles of teratogenicity. Current Obstetrics and Gynaecology 1999, 9:163-169.
80. McMahon T., Silke J. West coast of Ireland; winter toxicity of unknown aetiology in mussels. Harmful Algae News 1996, 14:2.
81. McMahon T., Silke J. Re-occurrence of winter toxicity. Harmful Algae News 1998, 17:12.
82. Moroney C., Lehane M., Brana-Magdalena A., Furey A., James K.J. Comparison of solid-phase extraction methods for the determination of azaspiracids in shellfish by liquid chromatography-electrospray mass spectrometry. Journal of Chromatography A 2002, 963:353-361.
83. Nath D. Cytoskeleton. Nature 2003, 442:741-745.
84. Nicolaou K.C., Chen D.Y.K., Li Y.W., Qian W.Y., Ling T.T., Vyskocil S., Koftis T.V., Govindasamy M., Uesaka N. Total synthesis of the proposed azaspiracid-1 structure, part 2: coupling of the C1-C20, C21-C27, and C28-C40 fragments and completion and synthesis. Angewandte Chemie-International Edition 2003, 42:3649-3653.
85. Nicolaou K.C., Li Y., Uesaka N., Koftis T.V., Vyskocil S., Ling T., Govindasamy M., Qian W., Bernal F., Chen D.Y. Total synthesis of the proposed azaspiracid-1 structure, part 1: construction of the enantiomerically pure C1-C20, C21-C27, and C28-C40 fragments. Angewandte Chemie-International Edition 2003, 42:3643-3648.
86. Nicolaou K.C., Frederick M.O., Pertrovic G., Cole K.P., Loizidou E. Total synthesis and confirmation of the revised strucutres of azaspiracid-2 and azaspiracid-3. Angewandte Chemie-International Edition 2006, 45:2609-2615.
87. Nicolaou K.C., Koftis T.V., Vyskocil S., Petrovic G., Ling T.T., Yamada Y.M.A., Tang W.J., Frederick M.O. Structural revision and total synthesis of azaspiracid-1, part 2: definition of the ABCD domain and total synthesis. Angewandte Chemie-International Edition 2004, 43:4318-4324.
88. Nicolaou K.C., Vyskocil S., Koftis T.V., Yamada Y.M.A., Ling T.T., Chen D.Y.K., Tang W.J., Petrovic G., Frederick M.O., Li Y.W., Satake M. Structural revision and total synthesis of azaspiracid-1, part 1: intelligence gathering and tentative proposal. Angewandte Chemie-International Edition 2004, 43:4312-4318.
89. Nicolaou K.C., Pihko P.M., Diedrichs N., Zou N., Bernal F. Synthesis of the FGHI ring system of azaspiracid. Angewandte Chemie-International Edition 2001, 40. 1573-1573.
90. Nicolaou K.C., Qian W., Bernal F., Uesaka N., Pihko P.M., Hinrichs J. Synthesis of the ABCD ring system of azaspiracid. Angewandte Chemie-International Edition (England) 2001, 40:4068-4071.
91. Nishiwaki S., Fujiki H., Suganuma M., Furuya-Suguri H., Matsushima R., Iida Y., Ojika M., Yamada K., Uemura D., Yasmuoto T., Schmitz F.J., Sugimura T. Structure-activity relationship within a series of okadaic acid derivatives. Carcinogenesis 1990, 11:1837-1841.
92. Nzoughet J.K., Hamilton J.T.G., Botting C.H., Douglas A., Devine L., Nelson J., Elliot C.T. Proteomics identification of azaspiracid toxin biomarkers in Blue Mussels, Mytilus edulis. Molecular and Cellular Proteomics 2009, 8:1811-1822.
93. Nzoughet K.J., Hamilton J.T.G., Floyd S.D., Douglas A., Nelson J., Devine L., Elliott C.T. Azaspiracid: first evidence of protein binding in shellfish. Toxicon 2008, 51:1255-1263.
94. Ofuji K., Satake M., McMahon T., James K.J., Naoki H., Oshima Y., Yasumoto T. Structures of azaspiracid analogs, azaspiracid-4 and azaspiracid-5, causative toxins of azaspiracid poisoning in Europe. Bioscience Biotechnology and Biochemistry 2001, 65:740-742.
95. Ofuji K., Satake M., McMahon T., Silke J., James K.J., Naoki H., Oshima Y., Yasumoto T. Two analogs of azaspiracid isolated from mussels, Mytilus edulis, involved in human intoxication in Ireland. Natural Toxins 1999, 7:99-102.
96. Ofuji K., Satake M., Oshima Y., McMahon T., James K.J., Yasumoto T. A sensitive and specific determination method for azaspiracids by liquid chromatography mass spectrometry. Natural Toxins 1999, 7:247-250.
97. Pierotti S., Malaguti C., Milandri A., Poletti R., Rossini G.P. Functional assay to measure yessotoxins in contaminated mussel samples. Analytical Biochemistry 2003, 2:208-216.
98. Pollard T.D. The cytoskeleton, cellular motility and the reductionist agenda. Nature 2003, 422:731-745.
99. Quilliam, M.A., Hess, P., Dell'Aversano, C., 2001. Recent developments in the analysis of phycotoxins by liquid chromatography-mass spectrometry. Mycotoxins and Phycotoxins in Perspective at the Turn of the Century, pp. 383-391.
100. RASFF Rapid Alert System for Food and Feed: France. 2008.0426. Azaspiracid Shellfish Poisoning (AZP), 15th April 2008 2008, Available from:. http://ec.europa.eu/food/food/rapidalert/reports/week16-2008_en.pdf.
101. Rehmann N., Hess P., Quilliam M.A. Discovery of new analogs of the marine biotoxin azaspiracid in blue mussels Mytilus edulis by ultra-performance liquid chromatography/tandem mass spectrometry. Rapid Communications in Mass Spectrometry 2008, 22:549-558.
102. Roman Y., Alfonso A., Louzao M.C., de la Rosa L.A., Leira F., Vieites J.M., Vieytes M.R., Ofuji K., Satake M., Yasumoto T., Botana L.M. Azaspiracid-1, a potent, nonapoptotic new phycotoxin with several cell targets. Cellular Signalling 2002, 14:703-716.
103. 2+], and pH. Chemical Research in Toxicology 2004, 17:1338-1349.
104. Ronzitti G., Hess P., Rehmann N., Rossini G.P. Azaspiracid-1 alters the E-cadherin pool in epithelial cells. Toxicological Sciences 2007, 95:427-435.
105. Rossini G.P. Functional assays in marine biotoxin detection. Toxicology 2005, 3:451-462.
106. Rossini G.P., Sgarbi N., Malaguti C. The toxic responses induced by okadaic acid involve processing of multiple caspase isoforms. Toxicon 2001, 39:763-770.
107. Ryan, G.E., Hess, P., Ryan, M.P., 2004. Development of a functional in vitro bioassay for azaspiracids (AZA) using human colonic epithelial cells. In: Proceedings of the 5th International Conference on Molluscan Shellfish Safety, Galway, Ireland.
108. Sasaki M., Iwamuro Y., Nemoto J., Oikawa M. Studies toward the total synthesis of azaspiracids: synthesis of the FGHI ring domain. Tetrahedron Letters 2003, 44:6199-6201.
109. Satake M., Ofugi K., James K.J., Furey A., Yasumoto T. New toxic event caused by Irish mussels. Harmful Algae 1997, 468-469.
110. Satake M., Ofuji K., Naoki H., James K.J., Furey A., McMahon T., Silke J., Yasumoto T. Azaspiracid, a new marine toxin having unique spiro ring assemblies, isolated from Irish mussels, Mytilus edulis. Journal of the American Chemical Society 1998, 120:9967-9968.
111. Scheuer P.J. Marine toxin research - an historical overview. Journal of Natural Toxins 1996, 5:181-189.
112. Seki T., Satake M., Mackenzie L., Kaspar H.F., Yasumoto T. Gymnodimine, a new marine toxin of unprecedented structure isolated from New Zealand oysters and the dinoflagellate, Gymnodinium sp. Tetrahedron Letters 1995, 36:7093-7096.
113. Shimizu Y. Microalgal metabolites: a new perspective. Annual Review of Microbiology 1996, 50:431-465.
114. Smythe E., Ayscough K.R. Regulation of actin in endocytosis. Journal of Cell Science 2006, 119:4589-4598.
115. Takeichi M. Cadherins: a molecular family important in selective cell-cell adhesion. Annual Reviews of Biochemistry 1990, 59:237-252.
116. Taleb H., Vale P., Amanhir R., Benhadouch A., Sagou R., Chafik A. First detection of azaspiraicds in mussels in north west Africa. Journal of Shellfish Research 2006, 25:1067-1070.
117. Thorburn A. Death receptor-induced cell killing. Cellular Signalling 2004, 16:139-144.
118. Tillman U., Elbrachter M., Krock B., John U., Cembella A. Azadinium Spinosum gen. et sp. nov. (Dinophycae) identified as primary producer of azaspiracid toxins. European Journal of Phycology 2009, 44:63-79.
119. Torgersen T., Bremnes N.B., Rundberget T., Aune T. Structural confirmation and occurrence of azaspiracids in Scandinavian brown crabs (Cancer pagurus). Toxicon 2008, 51:93-101.
120. Torigoe K., Murata M., Yasumoto T., Iwashita T. Prorocentrolide, a toxic nitrogenous macrocycle from a marine dinoflagellate, Prorocentrum lima. Journal of the American Chemical Society 1988, 110:7876-7877.
121. Twiner M.J., Hess P., Bottein Dechraoui M.Y., McMahon T., Samons M.S., Satake M., Yasumoto T., Ramsdell J.S., Doucette G.J. Cytotoxic and cytoskeletal effects of azaspiracid-1 on mammalian cell lines. Toxicon 2005, 45:891-900.
122. Twiner M.J., Rehmann N., Hess P., Doucette G.J. Azaspiracid shellfish poisoning: a review on the chemistry, ecology and toxicology with an emphasis on human health impact. Marine Drugs 2008, 6:39-72.
123. Twiner M.J., Ryan J.C., Morey J.S., Smith K.J., Hammad S.M., Van Dolah F.M., Hess P., McMahon T., Satake M., Yasumoto T., Doucette G.J. Transcriptional profiling and inhibition of cholesterol biosynthesis in human lymphocyte T cells by the marine toxin azaspiracid. Genomics 2008, 91:289-300.
124. Uemera D., Chou T., Haino T., Nagatsu A., Fukuzawa S., Zheng S.-Z., Chen H.-S. Pinnatoxin A: a toxic amphoteric macrocycle from the Okinawan bivalve, Pinna muricata. Journal of the American Chemical Society 1995, 17:1155-1156.
125. Ueoka R., Ito A., Izumikawa M., Maeda S., Takagi M., Shin-ya K., Yoshida M., van Soest R.W.M., Matsunaga S. Isolation of azaspiracid-2 from marine sponge Echinoclathria sp. as a potent cytotoxin. Toxicon 2009, 53:680-684.
126. Vale C., Gomez-Limia B., Nicolaou K.C., Frederick M.O., Vieytes M.R., Botana L.M. The c-Jun-N-terminal kinase is involved in the neurotoxic effect of azaspiracid-1. Cellular Physiology and Biochemistry 2007, 20:957-966.
127. Vale C., Nicolaou K.C., Frederick M.O., Gomez-Limia B., Alfonso A., Vieytes M.R., Botana L.M. Effects of azaspiracid-1, a potent cytotoxic agent, on primary neuronal cultures. A structure-activity relationship study. Journal of Medical Chemistry 2007, 50:356-363.
128. Vale C., Wandscheer C., Nicolaou K.C., Frederick M.O., Alfonso C., Vieytes M.R., Botana L.M. Cytotoxic effect of azaspiracid-2 and azaspiracid-2-methyl ester in cultured neurons: Involvement of the c-Jun N-terminal kinase. Journal of Neuroscience Research 2008, 86:2952-2962.
129. Vale P. Is there a risk of human poisoning by azaspiracids from shellfish harvested at the Portuguese coast?. Toxicon 2004, 44:943-947.
130. Vale P.J., Botelho M.J., Rodrifues S.M., Gomes S.S., Sampayo M.A.de M. Two decades of marine biotoxin monitoring in bivalves from Portugal (1986-2006): a review of exposure assessment. Harmful Algae 2008, 7:11-25.
131. Vilariño N., Nicolaou K.C., Frederick M.O., Cagide E., Ares I.R., Louzao M.C., Vieytes M.R., Botana L.M. Cell growth inhibition and actin cytoskeleton disorganization induced by azaspiracid-1 structure-activity studies. Chemical Research in Toxicology 2006, 19:1459-1466.
132. Vilariño N., Nicolaou K.C., Frederick M.O., Vieytes M.R., Botana L.M. Irreversible cytoskeletal disarrangement is independent of caspase activation during in vitro azaspiracid toxicity in human neuroblastoma cells. Biochemical Pharmacology 2007, 74:327-335.
133. Volmer D.A., Brombacher S., Whitehead B. Studies on azaspiracid biotoxins. I. Ultrafast high-resolution liquid chromatography/mass spectrometry separations using monolithic columns. Rapid Communications in Mass Spectrometry 2002, 16:2298-2305.
134. Whitmarsh A.J., Davis R.J. Structural organisation of MAP-kinase signalling modules by scaffold proteins in yeast and mammals. Trends in Biochemical Science 1998, 12:481-485.
135. Willoughby D., Cooper D.M.F. Use of single-cell imaging techniques to assess the regulation of cAMP dynamics. Biochemical Society Transactions 2006, 34:468-471.
136. Wright J.L.C. Dealing with seafood toxins: present approaches and future options. Food Research International 1995, 28:347-358.
137. Yasumoto T. The chemistry and biological function of natural marine toxins. Chemical Record 2001, 1:228-242.
138. Yasumoto T., Murata M., Oshima Y., Matsumoto G.K., Clardy J. Diarrhetic shellfish poisoning. Seafood Toxins 1984, American Chemical Society, Washington, DC.