Alternative methods for the detection of emerging marine toxins: Biosensors, biochemical assays and cell-based assays

Marine Drugs

Volumn 12, Issue 12, 2014, Pages 5719-5763

  Reverté, Laia ^a   Soliño, Lucía ^a   Carnicer, Olga ^a   Diogène, Jorge ^a   Campàs, Mònica ^a  

^a IRTA   (Spain)

Author keywords

Biosensors; Cell based assays; Ciguatoxin; Cyclic imines; Hemolytic assays; Immunoassays; Palytoxin; Receptor binding assays; Tetrodotoxin

Indexed keywords

CIGUATOXIN; MARINE TOXIN; PALYTOXIN; TETRODOTOXIN;

BIOCHEMISTRY; BIOSENSOR; CELL ASSAY; COLORIMETRY; ELECTROCHEMICAL ANALYSIS; FLUORESCENCE ANALYSIS; HUMAN; IMMUNOASSAY; MOLECULAR RECOGNITION; NONHUMAN; PRODUCT RECOVERY; PURIFICATION; QUANTITATIVE ANALYSIS; RECEPTOR BINDING ASSAY; REVIEW; SENSITIVITY AND SPECIFICITY; SURFACE PROPERTY; TOXIN ANALYSIS; TOXIN STRUCTURE; ANALYSIS; ANIMAL; BIOASSAY; CHEMISTRY; FOOD CONTAMINATION; GENETIC PROCEDURES; PROCEDURES; SEA FOOD;

ANIMALS; BIOLOGICAL ASSAY; BIOSENSING TECHNIQUES; FOOD CONTAMINATION; HUMANS; MARINE TOXINS; SEAFOOD;

EID: 84919947857     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md12125719     Document Type: Review

References (255)

1. European Food Safety Authority (EFSA). Scientific Opinion on marine biotoxins in shellfish: Cyclic imines (spirolides, gymnodimines, pinnatoxins and pteriatoxins). EFSA J. 2010, 8, doi:10.2903/j.efsa.2010.1628.
2. European Food Safety Authority (EFSA). Scientific Opinion on marine biotoxins in shellfish-Emerging toxins: Ciguatoxin group. EFSA J. 2010, 8, doi:10.2903/j.efsa.2010.1627.
3. European Food Safety Authority (EFSA). Scientific opinion on marine biotoxins in shellfish-palytoxin group. EFSA J. 2009, 7, 1-38.
4. European Comission. Regulation (EC) No 854/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific rules for the organisation of official controls on products of animal origin intended for human consumption. Off. J. Eur. Union 2004, L226, 83-127.
5. European Comission. Regulation (EC) No. 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for food of animal origin. Off. J. Eur. Union 2004, L139, 22-82.
6. European Comission. Regulation (EU) No 15/2011 of 10 January 2011 amending Regulation (EC) No 2074/2005 as regards recognised testing methods for detecting marine biotoxins in live bivalve molluscs. Off. J. Eur. Union 2011, L6, 3-6.
7. Foodstuffs-Determination of domoic acid in shellfish and finfish by RP-HPLC using UV detection. Available online: http://aesan.msssi.gob.es/CRLMB/docs/docs/procedimientos/Foodstuffs.pdf (accessed on 11 November 2014).
8. Lawrence, J.F.; Niedzwiadek, B.; Menard, C. Quantitative determination of paralytic shellfish poisoning toxins in shellfish using prechromatographic oxidation and liquid cromatography with fluorescence detection: Collaborative Study. J. AOAC Int. 2005, 88, 1714-1732.
9. Van de Riet, J.M.; Gibbs, R.S.; Chou, F.W.; Muggah, P.M.; Rourke, W.A.; Burns, G.; Thomas, K.; Quilliam, M.A. Liquid chromatographic post-column oxidation method for analysis of paralytic shellfish toxins in mussels, clams, scallops, and oysters: Single-Laboratory Validation. J. AOAC Int. 2009, 92, 1690-1704.
10. Van de Riet, J.; Gibbs, R.S.; Muggah, P.M.; Rourke, W.A.; MacNeil, J.D.; Quilliam, M.A. Liquid chromatography post-column oxidation (PCOX) method for the determination of paralytic shellfish toxins in mussels, clams, oysters, and scallops: Collaborative study. J. AOAC Int. 2011, 94, 1154-1176.
11. Turner, A.D.; Lewis, A.M.; Rourke, W.A.; Higman, W.A. Inter laboratory comparison of two AOAC liquid chromatographic fluorescence detection methods for paralytic shellfish toxin analysis through characterization of an oyster reference material. J. AOAC Int. 2014, 97, 380-390.
12. Gerssen, A.; Mulder, P.; McElhinney, M.A.; de Boer, J. Liquid chromatography-tandem mass spectrometry method for the detection of marine lipophilic toxins under alkaline conditions. J. Chromatogr. A 2009, 1216, 1421-1430.
13. 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. J. Chromatogr. A 2007, 1157, 273-280.
14. McNabb, P.; Selwood, A.I.; Holland, P.T. Multiresidue method for determination of algal toxins in shellfish: Single-laboratory validation and interlaboratory study. J. AOAC Int. 2005, 88, 761-772.
15. Takada, N.; Umemura, N.; Suenaga, K.; Chou, T.; Nagatsu, A.; Haino, T.; Yamada, K.; Uemura, D. Pinnatoxins B and C, the most toxic components in the pinnatoxin series from the Okinawan bivalve Pinna muricata. Tetrahedron Lett. 2001, 42, 3491-3494.
16. Miles, C.O.; Rundberget, T.; Sandvik, M.; Aasen, J.; Selwood, A.I. The Presence of Pinnatoxins in Norwegian Mussels; National Veterinary Institute: Oslo, Norway, 2010.
17. Lewis, R.J.; Jones, A.; Vernoux, J.-P. HPLC/Tandem Electrospray Mass Spectrometry for the determination of sub-ppb levels of Pacific and Caribbean ciguatoxins in crude extracts of fish. Anal. Chem. 1998, 71, 247-250.
18. Hamilton, B.; Hurbungs, M.; Jones, A.; Lewis, R.J. Multiple ciguatoxins present in Indian Ocean reef fish. Toxicon 2002, 40, 1347-1353.
19. Munday, R. Palytoxin toxicology: Animal studies. Toxicon 2011, 57, 470-477.
20. Moore, R.E.; Scheuer, P.J. Palytoxin: A new marine toxin from a coelenterate. Science 1971, 172, 495-498.
21. Walsh, G.E.B.; Ralph, L. A review of Hawaiian zoanthids with descriptions of three new species. Zool. J. Linn. Soc. 1971, 50, 161-180.
22. Moore, R.E.; Bartolini, G. Structure of palytoxin. J. Am. Chem. Soc. 1981, 103, 2491-2494.
23. Uemura, D.; Ueda, K.; Hirata, Y.; Naoki, H.; Iwashita, T. Further studies on palytoxin. II. Structure of palytoxin. Tetrahedron Lett. 1981, 22, 2781-2784.
24. Ciminiello, P.; Dell'Aversano, C.; Dello Iacovo, E.; Fattorusso, E.; Forino, M.; Grauso, L.; Tartaglione, L.; Florio, C.; Lorenzon, P.; de Bortoli, M. Stereostructure and biological activity of 42-hydroxy-palytoxin: A new palytoxin analogue from Hawaiian Palythoa subspecies. Chem. Res. Toxicol. 2009, 22, 1851-1859.
25. Uemura, D.; Hirata, Y.; Iwashita, T.; Naoki, H. Studies on palytoxins. Tetrahedron 1985, 41, 1007-1017.
26. Inuzuka, T.; Uemura, D.; Arimoto, H. The conformational features of palytoxin in aqueous solution. Tetrahedron 2008, 64, 7718-7723.
27. Mercado, J.A.; Rivera-Rentas, A.L.; Gonzalez, I.; Tosteson, T.R.; Molgó, J.; Escalona de Motta, G. Neuro- and myo-toxicity of extracts from the benthic dinoflagellate Ostreopsis lenticularis is sensitive to μ-conotoxin. Soc. Neurosci. 1994, 20, 718.
28. Ukena, T.; Satake, M.; Usami, M.; Oshima, Y.; Naoki, H.; Fujita, T.; Kan, Y.; Yasumoto, T. Structure elucidation of ostreocin D, a palytoxin analog isolated from the dinoflagellate Ostreopsis siamensis. Biosci. Biotechnol. Biochem. 2001, 65, 2585-2588.
29. Ukena, T.; Satake, M.; Usami, M.; Oshima, Y.; Fujita, T.; Naoki, H.; Yasumoto, T. Structural confirmation of ostreocin-D by application of negative-ion fast-atom bombardment collision-induced dissociation tandem mass spectrometric methods. Rapid Commun. Mass Spectrom. 2002, 16, 2387-2393.
30. Lenoir, S.; Ten-Hage, L.; Turquet, J.; Quod, J.P.; Bernard, C.; Hennion, M.C., First evidence of palytoxin analogues from an Ostreopsis mascarenensis (Dinophyceae) benthic bloom in Southwestern Indian Ocean. J. Phycol. 2004, 40, 1042-1051.
31. Tubaro, A.; Durando, P.; del Favero, G.; Ansaldi, F.; Icardi, G.; Deeds, J.R.; Sosa, S. Case definitions for human poisonings postulated to palytoxins exposure. Toxicon 2011, 57, 478-495.
32. Milandri, A.; Ceredi, A.; Riccardi, E.; Gasperetti, L.; Susini, F.; Casotti, M.; Faiman, L.; Pigozzi, S. In Impact of Ostreopsis Ovata on Marine Benthic Communities: Accumulation of Palytoxins in Mussels, Sea Urchins and Octopuses from Italy, Proceedings of the ICHA14 Conference, Crete, Greek, 1-5 November 2010; pp. 1-5.
33. Ciminiello, P.; Dell'Aversano, C.; Fattorusso, E.; Forino, M.; Tartaglione, L.; Grillo, C.; Melchiorre, N. Putative palytoxin and its new analogue, Ovatoxin-a, in Ostreopsis ovata collected along the Ligurian Coasts during the 2006 toxic outbreak. J. Am. Soc. Mass Spectrom. 2008, 19, 111-120.
34. Ciminiello, P.; Dell'Aversano, C.; Dello Iacovo, E.; Fattorusso, E.; Forino, M.; Grauso, L.; Tartaglione, L.; Guerrini, F.; Pistocchi, R. Complex palytoxin-like profile of Ostreopsis ovata. Identification of four new ovatoxins by high-resolution liquid chromatography/mass spectrometry. Rapid Commun. Mass Spectrom. 2010, 24, 2735-2744.
35. Ciminiello, P.; Dell'Aversano, C.; Dello Iacovo, E.; Fattorusso, E.; Forino, M.; Tartaglione, L.; Battocchi, C.; Crinelli, R.; Carloni, E.; Magnani, M.; et al. Unique toxin profile of a Mediterranean Ostreopsis cf. ovata Strain: HR LC-MSn characterization of ovatoxin-f, a new palytoxin congener. Chem. Res. Toxicol. 2012, 25, 1243-1252.
36. Munday, R. Occurrence and toxicology of palytoxins. Food Sci. Technol. 2008, 173, 693-713.
37. Aligizaki, K.; Katikou, P.; Milandri, A.; Diogène, J. Occurrence of palytoxin-group toxins in seafood and future strategies to complement the present state of the art. Toxicon 2011, 57, 390-399.
38. Hilgemann, D.W. From a pump to a pore: How palytoxin opens the gates. Proc. Natl. Acad. Sci. USA 2003, 100, 386-388.
39. Artigas, P.; Gadsby, D.C. Na+/K+-pump ligands modulate gating of palytoxin-induced ion channels. Proc. Natl. Acad. Sci. USA 2003, 100, 501-505.
40. Shimahara, T.; Molgó, J. Palytoxin enhances quantal acetylcholine release from motor nerve terminals and increases cytoplasmic calcium levels in a neuronal hybrid cell line. Life Sci. Adv. Pharmacol. 1990, 9, 785-792.
41. Satoh, E.; Ishii, T.; Nishimura, M. Palytoxin-induced increase in cytosolic-free Ca2+ in mouse spleen cells. Eur. J. Pharmacol. 2003, 465, 9-13.
42. Deeds, J.R.; Schwartz, M.D. Human risk associated with palytoxin exposure. Toxicon 2010, 56, 150-162.
43. Onuma, Y.; Satake, M.; Ukena, T.; Roux, J.; Chanteau, S.; Rasolofonirina, N.; Ratsimaloto, M.; Naoki, H.; Yasumoto, T. Identification of putative palytoxin as the cause of clupeotoxism. Toxicon 1999, 37, 55-65.
44. CRLMB (Community Reference Laboratory for Marine Biotoxins). Report on toxicology working group meeting. CRLMB: Cesenatico, Italy, 24-25 October 2005; pp. 24-25.
45. Bignami, G.S.; Raybould, T.J.G.; Sachinvala, N.D.; Grothaus, P.G.; Simpson, S.B.; Lazo, C.B.; Byrnes, J.B.; Moore, R.E.; Vann, D.C. Monoclonal antibody-based enzyme-linked immunoassays for the measurement of palytoxin in biological samples. Toxicon 1992, 30, 687-700.
46. Levine, L.; Fujiki, H.; Gjika, H.B.; Vanvunakis, H. Production of antibodies to palytoxin-neutralization of several biological properties of playtoxin. Toxicon 1987, 25, 1273-1282.
47. Frolova, G.; Kuznetsova, T.; Mikhailov, V.; Elyakov, G. An enzyme linked immunosorbent assay for detecting palytoxin-producing bacteria. Russ. J. Bioorg. Chem. 2000, 26, 285-289.
48. Zamolo, V.A.; Valenti, G.; Venturelli, E.; Chaloin, O.; Marcaccio, M.; Boscolo, S.; Castagnola, V.; Sosa, S.; Berti, F.; Fontanive, G.; et al. Highly sensitive electrochemiluminescent nanobiosensor for the detection of palytoxin. ACS Nano 2012, 6, 7989-7997.
49. Boscolo, S. Sandwich ELISA assay for the quantitation of palytoxin and its analogs in natural samples. Environ. Sci. Technol. 2013, 47, 2034-2042.
50. Garet, E.; Cabado, A.G.; Vieites, J.M.; Gonzalez-Fernandez, A. Rapid isolation of single-chain antibodies by phage display technology directed against one of the most potent marine toxins: Palytoxin. Toxicon 2010, 55, 1519-1526.
51. Yakes, B.; DeGrasse, S.; Poli, M.; Deeds, J. Antibody characterization and immunoassays for palytoxin using an SPR biosensor. Anal. Bioanal. Chem. 2011, 400, 2865-2869.
52. Wattenberg, E.V. Modulation of protein kinase signaling cascades by palytoxin. Toxicon 2011, 57, 440-448.
53. Bellocci, M.; Ronzitti, G.; Milandri, A.; Melchiorre, N.; Grillo, C.; Poletti, R.; Yasumoto, T.; Rossini, G.P. A cytolytic assay for the measurement of palytoxin based on a cultured monolayer cell line. Anal. Biochem. 2008, 374, 48-55.
54. Pawlowiez, R.; Darius, H.T.; Cruchet, P.; Rossi, F.; Caillaud, A.; Laurent, D.; Chinain, M. Evaluation of seafood toxicity in the Australes archipelago (French Polynesia) using the neuroblastoma cell-based assay. Food Add. Contam. A 2013, 30, 567-586.
55. Kerbrat, A.S.; Amzil, Z.; Pawlowiez, R.; Golubic, S.; Sibat, M.; Darius, H.T.; Chinain, M.; Laurent, D. First evidence of palytoxin and 42-hydroxy-palytoxin in the marine cyanobacterium Trichodesmium. Mar. Drugs 2011, 9, 543-560.
56. Ledreux, A.; Krys, S.; Bernard, C. Suitability of the Neuro-2a cell line for the detection of palytoxin and analogues (neurotoxic phycotoxins). Toxicon 2009, 53, 300-308.
57. Cañete, E.; Diogène, J. Comparative study of the use of neuroblastoma cells (Neuro-2a) and neuroblastoma-glioma hybrid cells (NG108-15) for the toxic effect quantification of marine toxins. Toxicon 2008, 52, 541-550.
58. Rossini, G.P.; Bigiani, A. Palytoxin action on the Na +, K+-ATPase and the disruption of ion equilibria in biological systems. Toxicon 2011, 57, 429-439.
59. Bellocci, M.; Sala, G.L.; Prandi, S. The cytolytic and cytotoxic activities of palytoxin. Toxicon 2011, 57, 449-459.
60. Espiña, B.; Cagide, E.; Louzao, M.; Fernandez, M.; Vieytes, M.; Katikou, P.; Villar, A.; Jaen, D.; Maman, L.; Botana, L. Specific and dynamic detection of palytoxins by in vitro microplate assay with human neuroblastoma cells. Biosci. Rep. 2009, 29, 13-23.
61. Penna, A.; Fraga, S.; Battocchi, C.; Casabianca, S.; Giacobbe, M.G.; Riobo, P.; Vernesi, C. A phylogeographical study of the toxic benthic dinoflagellate genus Ostreopsis Schmidt. J. Biogeogr. 2010, 37, 830-841.
62. Pezzolesi, L.; Guerrini, F.; Ciminiello, P.; Dell'Aversano, C.; Iacovo, E.D.; Fattorusso, E.; Forino, M.; Tartaglione, L.; Pistocchi, R. Influence of temperature and salinity on Ostreopsis cf. ovata growth and evaluation of toxin content through HR LC-MS and biological assays. Water Res. 2012, 46, 82-92.
63. Nascimento, S.M.; Correa, E.V.; Menezes, M.; Varela, D.; Paredes, J.; Morris, S. Growth and toxin profile of Ostreopsis cf. ovata (Dinophyta) from Rio de Janeiro, Brazil. Harmful Algae 2012, 13, 1-9.
64. Vidyarathna, N.K.; Graneli, E. Influence of temperature on growth, toxicity and carbohydrate production of a Japanese Ostreopsis ovata strain, a toxic-bloom-forming dinoflagellate. Aquat. Microb. Ecol. 2011, 65, 261-270.
65. Vidyarathna, N.K.; Graneli, E. Physiological responses of Ostreopsis ovata to changes in N and P availability and temperature increase. Harmful Algae 2013, 21-22, 54-63.
66. Riobo, P.; Paz, B.; Franco, J.M. Analysis of palytoxin-like in Ostreopsis cultures by liquid chromatography with precolumn derivatization and fluorescence detection. Anal. Chim. Acta 2006, 566, 217-223.
67. Habermann, E.; Ahnerthilger, G.; Chhatwal, G.S.; Beress, L. Delayed hemolytic action of palytoxin. General characteristics. Biochim. Biophys. Acta 1981, 649, 481-486.
68. Habermann, E.; Chhatwal, G.S.; Hessler, H.J. Palytoxin raises the nonspecific permeability of erythrocytes in an ouabain-sensitive manner. Naunyn-Schmiedeberg's Arch. Pharmacol. 1981, 317, 374.
69. Habermann, E.; Chhatwal, G.S. Ouabain inhibits the increase due to palytoxin of cation permeability of erythrocytes. Naunyn-Schmiedeberg's Arch. Pharmacol. 1982, 319, 101-107.
70. Bignami, G.S. A rapid and sensitive hemolysis neutralization assay for palytoxin. Toxicon 1993, 31, 817-820.
71. Taniyama, S.; Arakawa, O.; Terada, M.; Nishio, S.; Takatani, T.; Mahmud, Y.; Noguchi, T. Ostreopsis sp., a possible origin of palytoxin (PTX) in parrotfish Scarus ovifrons . Toxicon 2003, 42, 29-33.
72. Riobo, P.; Paz, B.; Franco, J.M.; Vazquez, J.A.; Murado, M.A. Proposal for a simple and sensitive haemolytic assay for palytoxin. Toxicological dynamics, kinetics, ouabain inhibition and thermal stability. Harmful Algae 2008, 7, 415-429.
73. Taniyama, S.; Mahmud, Y.; Terada, M.; Takatani, T.; Arakawa, O.; Noguchi, T. Occurrence of a food poisoning incident by palytoxin from a serranid Epinephelus sp. in Japan. J. Nat. Toxins 2002, 11, 277-282.
74. Rhodes, L.; Adamson, J.; Suzuki, T.; Briggs, L.; Garthwaite, I. Toxic marine epiphytic dinoflagellates, Ostreopsis siamensis and Coolia monotis (Dinophyceae), in New Zealand. N. Z. J. Mar. Freshw. Res. 2000, 34, 371-383.
75. Rhodes, L.; Towers, N.; Briggs, L.; Munday, R.; Adamson, J. Uptake of palytoxin-like compounds by shellfish fed Ostreopsis siamensis (Dinophyceae). N. Z. J. Mar. Freshw. Res. 2002, 36, 631-636.
76. Rhodes, L.L.; Smith, K.F.; Munday, R.; Selwood, A.I.; McNabb, P.S.; Holland, P.T.; Bottein, M.-Y. Toxic dinoflagellates (Dinophyceae) from Rarotonga, Cook Islands. Toxicon 2010, 56, 751-758.
77. Gleibs, S.; Mebs, D.; Werding, B. Studies on the origin and distribution of palytoxin in a Caribbean coral reef. Toxicon 1995, 33, 1531-1537.
78. Gleibs, S.; Mebs, D. Distribution and sequestration of palytoxin in coral reef animals. Toxicon 1999, 37, 1521-1527.
79. Wachi, K.M.; Hokama, Y.; Haga, L.S.; Shiraki, A.; Takenaka, W.E.; Bignami, G.S.; Levine, L. Evidence for palytoxin as one of the sheep erythrocyte lytic in lytic factors in crude extracts of ciguateric and non-ciguateric reef fish tissue. J. Nat. Toxins 2000, 9, 139-146.
80. Wachi, K.M.; Hokama, Y. Diversity of marine biotoxins in the near-shore ocean area: Presence of a palytoxin-like entity at Barber's Point Harbor, Oahu. J. Nat. Toxins 2001, 10, 317-333.
81. Seemann, P.; Gernert, C.; Schmitt, S.; Mebs, D.; Hentschel, U. Detection of hemolytic bacteria from Palythoa caribaeorum (Cnidaria, Zoantharia) using a novel palytoxin-screening assay. Antonie Leeuwenhoek Int. J. Gen. Mol. Microbiol. 2009, 96, 405-411.
82. Huang, K.M.; Liu, S.M.; Huang, Y.W.; Huang, K.L.; Hwang, D.F. Food poisoning caused by Sunfish Masturus lanceolatus in Taiwan. J. Food Drug Anal. 2011, 19, 191-196.
83. Bire, R.; Trotereau, S.; Lemee, R.; Delpont, C.; Chabot, B.; Aumond, Y.; Krys, S. Occurrence of palytoxins in marine organisms from different trophic levels of the French Mediterranean coast harvested in 2009. Harmful Algae 2013, 28, 10-22.
84. Brissard, C.; Herrenknecht, C.; Sechet, V.; Herve, F.; Pisapia, F.; Harcouet, J.; Lemee, R.; Chomerat, N.; Hess, P.; Amzil, Z. Complex toxin profile of French Mediterranean Ostreopsis cf. ovata strains, seafood accumulation and ovatoxins prepurification. Mar. Drugs 2014, 12, 2851-2876.
85. Pagliara, P.; Caroppo, C. Cytotoxic and antimitotic activities in aqueous extracts of eight cyanobacterial strains isolated from the marine sponge Petrosia ficiformis. Toxicon 2011, 57, 889-896.
86. Igarashi, T.; Aritake, S.; Yasumoto, T. Mechanisms underlying the hemolytic and ichthyotoxic activities of maitotoxin. Nat. Toxins 1999, 7, 71-79.
87. Volpe, G.; Cozzi, L.; Migliorelli, D.; Croci, L.; Palleschi, G. Development of a haemolytic-enzymatic assay with mediated amperometric detection for palytoxin analysis: Application to mussels. Anal. Bioanal. Chem. 2014, 406, 2399-2410.
88. Alfonso, A.; Fernandez-Araujo, A.; Alfonso, C.; Carames, B.; Tobio, A.; Louzao, M.C.; Vieytes, M.R.; Botana, L.M. Palytoxin detection and quantification using the fluorescence polarization technique. Anal. Biochem. 2012, 424, 64-70.
89. Vale-Gonzalez, C.; Pazos, M.; Alfonso, A.; Vieytes, M.; Botana, L. Study of the neuronal effects of ouabain and palytoxin and their binding to Na +, K+-ATPases using an optical biosensor. Toxicon 2007, 50, 541-552.
90. Alfonso, A.; Pazos, M.-J.; Fernández-Araujo, A.; Tobio, A.; Alfonso, C.; Vieytes, M.R.; Botana, L.M. Surface plasmon resonance biosensor method for palytoxin detection based on Na+, K+- ATPase affinity. Toxins 2014, 6, 96-107.
91. Scheuer, P.; Takahaski, W.; Tsutsumi, J.; Yoshida, T. Ciguatoxin: Isolation and chemical structure. Science 1967, 155, 1267-1268.
92. Lange, W.R. Ciguatera fish poisoning. Am. Fam. Phys. 1994, 50, 579-584.
93. Yasumoto, T.; Nakajima, I.; Bagnis, R.; Adachi, R. Finding of a dinoflagellate as a likely culprit of ciguatera. Bull. Jpn. Soc. Sci. Fish. 1977, 43, 1021-1026.
94. Bagnis, R.; Hurtel, J.M.; Chanteau, S.; Chungue, E.; Inoue, A.; Yasumoto, T. Dinoflagellate Gambierdiscus-Toxicus Adachi et Fukuyo-Probable cause of ciguatera. Comptes Rendus Hebd. Seances L'Acad. Sci. D 1979, 289, 671-674.
95. Bagnis, R.; Chanteau, S.; Chungue, E.; Hurtel, J.M.; Yasumoto, T.; Inoue, A. Origins of ciguatera fish poisoning-A new Dinoflagellate, Gambierdiscus-Toxicus Adachi and Fukuyo, definitively involved as a causal agent. Toxicon 1980, 18, 199-208.
96. Sperr, A.E.; Doucette, G.J. Variation in growth rate and ciguatera toxin production among geographically distinct isolates of Gambierdiscus toxicus. In Harmful and Toxic Algal Blooms; Yasumoto, T., Oshima, Y., Fukuyo, Y., Eds.; IOC of UNESCO: Paris, France, 1996; pp. 309-312.
97. Litaker, R.W.; Vandersea, M.W.; Faust, M.A.; Kibler, S.R.; Nau, A.W.; Holland, W.C.; Chinain, M.; Holmes, M.J.; Tester, P.A. Global distribution of ciguatera causing dinoflagellates in the genus Gambierdiscus. Toxicon 2010, 56, 711-730.
98. Chinain, M.; Darius, H.T.; Ung, A.; Cruchet, P.; Wang, Z.; Ponton, D.; Laurent, D.; Pauillac, S. Growth and toxin production in the ciguatera-causing dinoflagellate Gambierdiscus polynesiensis (Dinophyceae) in culture. Toxicon 2010, 56, 739-750.
99. Mills, A.R. Poisonous fish in the South Pacific. J. Trop. Med. Hyg. 1956, 59, 99-103.
100. Vernoux, J.P.; Lahlou, N.; Elandaloussi, S.A.; Riyeche, N.; Magras, L.P. A study of the distribution of ciguatoxin in indiviual Caribbean fish. Acta Trop. 1985, 42, 225-233.
101. Murata, M.; Legrand, A.M.; Ishibashi, Y.; Yasumoto, T. Structures of ciguatoxin and its congener. J. Am. Chem. Soc. 1989, 111, 8929-8931.
102. Murata, M.; Legrand, A.N.; Ishibashi, Y.; Fukui, M.; Yasumoto, T. Conformations of ciguatoxin and related polyethers. Abstr. Pap. Am. Chem. Soc. 1990, 200, 54-AGFD.
103. Lewis, R.J.; Sellin, M.; Poli, M.A.; Norton, R.S.; MacLeod, J.K.; Sheil, M.M. Purification and characterization of ciguatoxins from moray eel (Lycodontis javanicus, Muraenidae). Toxicon 1991, 29, 1115-1127.
104. Satake, M.; Ishimaru, T.; Legrand, A.M.; Yasumoto, T. Isolation of a ciguatoxin analog from cultures of Gambierdiscus toxicus . In Toxic Pyhtoplankton Blooms in the Sea; Samyda, T.J., Shimizu, Y., Eds.; Elsevier: New York, NY, USA, 1993; Volume 3, pp. 575-579.
105. Satake, M.; Murata, M.; Yasumoto, T. The structure of CTX3C, a ciguatoxin congener isolated from cultured Gambierdiscus toxicus. Tetrahedron Lett. 1993, 34, 1975-1978.
106. Satake, M.; Morohashi, A.; Oguri, H.; Oishi, T.; Hirama, M.; Harada, N.; Yasumoto, T. The absolute configuration of ciguatoxin. J. Am. Chem. Soc. 1997, 119, 11325-11326.
107. Satake, M.; Fukui, M.; Legrand, A.M.; Cruchet, P.; Yasumoto, T. Isolation and structures of new ciguatoxin analogs, 2,3-dihydroxyCTX3C and 51-hydroxyCTX3C, accumulated in tropical reef fish. Tetrahedron Lett. 1998, 39, 1197-1198.
108. Lehane, L.; Lewis, R.J. Ciguatera: Recent advances but the risk remains. Int. J. Food Microbiol. 2000, 61, 91-125.
109. Lewis, R.J.; Vernoux, J.P.; Brereton, I.M. Structure of Caribbean ciguatoxin isolated from Caranx latus. J. Am. Chem. Soc. 1998, 120, 5914-5920.
110. Hamilton, B.; Hurbungs, M.; Vernoux, J.P.; Jones, A.; Lewis, R.J. Isolation and characterisation of Indian Ocean ciguatoxin. Toxicon 2002, 40, 685-693.
111. Bidard, J.N.; Vijverberg, H.P.M.; Frelin, C.; Chungue, E.; Legrand, A.M.; Bagnis, R.; Lazdunski, M. Ciguatoxin is a novel type of Na+ channel toxin. J. Biol. Chem. 1984, 259, 8353-8357.
112. Molgo, J.; Comella, J.X.; Legrand, A.M. Ciguatoxin enhances quantal transmitter release from frog motor-nerve terminals. Br. J. Pharmacol. 1990, 99, 695-700.
113. Molgo, J.; Gaudrytalarmain, Y.M.; Legrand, A.M.; Moulian, N. Ciguatoxin extracted from poisonous moray eels gymnothorax-javanicus triggers acetylcholine-release from torpedo cholinergic synaptosomes via reversed Na+/Ca2+ exchange. Neurosci. Lett. 1993, 160, 65-68.
114. Benoit, E.; Juzans, P.; Legrand, A.M.; Molgo, J. Nodal swelling produced by ciguatoxin-induced selective activation of sodium channels in myelinated nerve fibers. Neuroscience 1996, 71, 1121-1131.
115. Mattei, C.; Dechraoui, M.Y.; Molgo, J.; Meunier, F.A.; Legrand, A.M.; Benoit, E. Neurotoxins targetting receptor site 5 of voltage-dependent sodium channels increase the nodal volume of myelinated axons. J. Neurosci. Res. 1999, 55, 666-673.
116. Lewis, R.J. Ion channel toxins and therapeutics: From cone snail venoms to ciguatera. Ther. Drug Monit. 2000, 22, 61-64.
117. Caillaud, A.; de la Iglesia, P.; Darius, H.T.; Pauillac, S.; Aligizaki, K.; Fraga, S.; Chinain, M.; Diogene, J. Update on methodologies available for ciguatoxin determination: Perspectives to confront the onset of ciguatera fish poisoning in Europe. Mar. Drugs 2010, 8, 1838-1907.
118. Perez-Arellano, J.L.; Luzardo, O.P.; Brito, A.P.; Cabrera, M.H.; Zumbado, M.; Carranza, C.; Angel-Moreno, A.; Dickey, R.W.; Boada, L.D. Ciguatera fish poisoning, Canary Islands. Emerg. Infect. Dis. 2005, 11, 1981-1982.
119. Gouveia, N.; Delgado, J.; Vale, P. Primeiro registo da ocorrência de episódios do tipo ciguatérico no arquipélago da Madeira. In Abstract Book of X Reuniao Oberica, Fitoplancton Toxico e Biotoxinas; IPIMAR: Lisbon, Portugal, 2009.
120. th European Phycological Congress; Elsevier Science: Oviedo, Spain, 2007; p. 41.
121. Stebbing, A.R.D.; Turk, S.M.T.; Wheeler, A.; Clarke, K.R. Immigration of southern fish species to south-west England linked to warming of the North Atlantic (1960-2001). J. Mar. Biol. Assoc. UK 2002, 82, 177-180.
122. CDC (Centers for Disease Control and Prevention). Cluster of Ciguatera Fish Poisoning, 2007. Morbidity and Mortality Weekly Report (MMWR); CDC: North Carolina, NC, USA, 2009; pp. 283-285.
123. Hokama, Y.; Banner, A.H.; Boylan, D.B. A radioimmunoassay for the detection of ciguatoxin. Toxicon 1977, 15, 317-325.
124. Hokama, Y.; Abad, M.A.; Kimura, L.H. A rapid enzyme-immunoassay for the detection of ciguatoxin in contaminated fish-tissues. Toxicon 1983, 21, 817-824.
125. Hokama, Y. A rapid, simplified enzyme-immunoassay stick test for the detecction of ciguatoxin and related polyethers from fish-tissues. Toxicon 1985, 23, 939-946.
126. Hokama, Y.; Shirai, L.K.; Iwamoto, L.M.; Kobayashi, M.N.; Goto, C.S.; Nakagawa, L.K. Assessment of a rapid enzyme-immunoassay stick test for the detection of ciguatoxin and related polyether toxins in fish-tissues. Biol. Bull. 1987, 172, 144-153.
127. Park, D.L. Detection of ciguatera and diarrheic shellfish toxins in finfish and shellfish with ciguatect kit. J. AOAC Int. 1995, 78, 533-537.
128. Bienfang, P.; DeFelice, S.; Dowling, A. Quantitative evaluation of commercially available test kit for ciguatera in fish. Food Nutr. Sci. 2011, 2, 594-598.
129. Ebesu, J.S.; Campora, C.E. Comment on "Quantitative evaluation of commercially available test kit for ciguatera in fish". Food Nutr. Sci. 2012, 3, 1233-1237.
130. Dickey, R.W.; Granade, H.R.; McClure, F.D. Evaluation of the Ciguatect Solid-Phase Immunobead Assay for the Detection of Ciguatera-Related Biotoxins in Caribbean Finfish. In Proceedings of the International Workshop on Ciguatera Management, Brisbane, Australia, 13-16 April 1994; Memoirs of the Queensland Museum: Brisbane, Australia, 1994; pp. 481-488.
131. Hokama, Y.; Honda, S.A.A.; Kobayashi, M.N.; Nakagawa, L.K.; Asahina, A.Y.; Miyahara, J.T. Monoclonal-antibody (MAb) in detection of ciguatoxin (CTX) and related polyethers by the stick-enzyme immunoassay (S-EIA) in fish-tissues associated with ciguatera poisoning. In Mycotoxins and Phycotoxins; Natori, S., Hashimoto, K., Ueno, Y., Eds.; Elsevier: Amsterdam, The Netherlands, 1989; Volume 10, pp. 303-310.
132. Campora, C.E.; Hokama, Y.; Ebesu, J.S.M. Comparative analysis of purified pacific and Caribbean ciguatoxin congeners and related marine toxins using a modified ELISA technique. J. Clin. Lab. Anal. 2006, 20, 121-125.
133. Pauillac, S.; Sasaki, M.; Inoue, M.; Naar, J.; Branaa, P.; Chinain, M.; Tachibana, K.; Legrand, A.M. Characterization of mice antisera elicited with a ciguatoxin tetracyclic synthetic ring fragment (JKLM) conjugated to carrier proteins. Toxicon 2000, 38, 669-685.
134. Campora, C.E.; Dierking, J.; Tamaru, C.S.; Hokama, Y.; Vincent, D. Detection of ciguatoxin in fish tissue using sandwich ELISA and neuroblastoma cell bioassay. J. Clin. Lab. Anal. 2008, 22, 246-253.
135. Campora, C.E.; Hokama, Y.; Yabusaki, K.; Isobe, M. Development of an enzyme-linked immunosorbent assay for the detection of ciguatoxin in fish tissue using chicken immunoglobulin Y. J. Clin. Lab. Anal. 2008, 22, 239-245.
136. Oguri, H.; Hirama, M.; Tsumuraya, T.; Fujii, I.; Maruyama, M.; Uehara, H.; Nagumo, Y. Synthesis-based approach toward direct sandwich immunoassay for ciguatoxin CTX3C. J. Am. Chem. Soc. 2003, 125, 7608-7612.
137. Tsumuraya, T.; Fujii, I.; Inoue, M.; Tatami, A.; Miyazaki, K.; Hirama, M. Production of monoclonal antibodies for sandwich immunoassay detection of ciguatoxin 51-hydroxyCTX3C. Toxicon 2006, 48, 287-294.
138. Tsumuraya, T.; Fujii, I.; Hirama, M. Production of monoclonal antibodies for sandwich immunoassay detection of Pacific ciguatoxins. Toxicon 2010, 56, 797-803.
139. Tsumuraya, T.; Takeuchi, K.; Yamashita, S.; Fujii, I.; Hirama, M. Development of a monoclonal antibody against the left wing of ciguatoxin CTX1B: Thiol strategy and detection using a sandwich ELISA. Toxicon 2012, 60, 348-357.
140. Tsumuraya, T.; Fujii, I.; Hirama, M. Preparation of anti-ciguatoxin monoclonal antibodies using synthetic haptens: Sandwich ELISA detection of ciguatoxins. J. AOAC Int. 2014, 97, 373-379.
141. Manger, R.L.; Leja, L.S.; Lee, S.Y.; Hungerford, J.M.; Wekell, M.M. Tetrazolium-based cell bioassay for neurotoxins active on voltage-sensitive sodium channels: Semiautomated assay for saxitoxins, brevetoxins, and ciguatoxins. Anaytical Biochem. 1993, 214, 190-194.
142. Cañete, E.; Diogène, J. Improvements in the use of neuroblastomaxglioma hybrid cells (NG108-15) for the toxic effect quantification of marine toxins. Toxicon 2010, 55, 381-389.
143. Fairey, E.R.; Edmunds, J.; Deamer-Melia, N.J.; Glasgow, H., Jr.; Johnson, F.M.; Moeller, P.R.; Burkholder, J.; Ramsdell, J.S. Reporter gene assay for fish-killing activity produced by Pfiesteria piscicida. Environ. Health Perspect. 1999, 107, 711-714.
144. Landsberg, J.; Flewelling, L.; Naar, J. Karenia brevis red tides, brevetoxins in the food web, and impacts on natural resources: Decadal advancements. Harmful Algae 2009, 8, 598-607.
145. McFarren, E.; Tanabe, H.; Silva, F.; Wilson, W.; Campbell, J.; Lewis, K. The occurrence of a ciguatera-like poison in oysters, clams, and Gymnodinium breve cultures. Toxicon 1965, 3, 111-123.
146. Watkins, S.M.; Reich, A.; Fleming, L.E.; Hammond, R. Neurotoxic shellfish poisoning. Mar. Drugs 2008, 6, 431-455.
147. Woofter, R.T.; Brendtro, K.; Ramsdell, J.S. Uptake and elimination of brevetoxin in blood of striped mullet (Mugil cephalus) after aqueous exposure to Karenia brevis. Environ. Health Perspect. 2005, 113, 11-16.
148. Dechraoui, M.; Bottein, Y.; Tiedeken, J.A.; Persad, R.; Wang, Z.; Granade, H.; Dickey, R.W.; Ramsdell, J.S. Use of two detection methods to discriminate ciguatoxins from brevetoxins: Application to great barracuda from Florida Keys. Toxicon 2005, 46, 261-270.
149. Bottein Dechraoui, M.-Y.; Wacksman, J.J.; Ramsdell, J.S. Species selective resistance of cardiac muscle voltage gated sodium channels: Characterization of brevetoxin and ciguatoxin binding sites in rats and fish. Toxicon 2006, 48, 702-712.
150. Manger, R.; Woodle, D.; Berger, A.; Dickey, R.W.; Jester, E.; Yasumoto, T.; Lewis, R.; Hawryluk, T.; Hungerford, J. Flow cytometric-membrane potential detection of sodium channel active marine toxins: Application to ciguatoxins in fish muscle and feasibility of automating saxitoxin detection. J. AOAC Int. 2014, 97, 299-306.
151. Lewis, R.J. Detection of toxins associated with ciguatera fish poisoning. In Manual on Harmful Marine Microalgae; Hallegraeff, G.M., Anderson, D.M., Cembella, A.D., Eds.; UNESCO: Paris, France, 2003; p. 267.
152. Yasumoto, T.; Fukui, M.; Sasaki, K.; Sugiyama, K. Determinations of marine toxins in foods. J. AOAC Int. 1995, 78, 574-582.
153. Campora, C.E.; Hokama, Y.; Tamaru, C.S.; Anderson, B.; Vincent, D. Evaluating the risk of ciguatera fish poisoning from reef fish grown at marine aquaculture facilities in Hawaii. J. World Aquac. Soc. 2010, 41, 61-70.
154. Dickey, R.W.; Granade, H.R.; Jester, E.L.E.; Abraham, A.; El Said, K.R.; Plakas, S.M. A tiered method for determination of Caribbean and Pacific ciguatoxins in fish and formulation of regulatory advisory levels. In Proceedings of the Ciguatera and Related Biotoxins Workshop, Noumea, New Caledonia, 27-31 October 2008.
155. Darius, H.T.; Ponton, D.; Revel, T.; Cruchet, P.; Ung, A.; Fouc, M.T.; Chinain, M. Ciguatera risk assessment in two toxic sites of French Polynesia using the receptor-binding assay. Toxicon 2007, 50, 612-626.
156. Wu, J.J.; Mak, Y.L.; Murphy, M.B.; Lam, J.C.W.; Chan, W.H.; Wang, M.; Chan, L.L.; Lam, P.K.S. Validation of an accelerated solvent extraction liquid chromatography-tandem mass spectrometry method for Pacific ciguatoxin-1 in fish flesh and comparison with the mouse neuroblastoma assay. Anal. Bioanal. Chem. 2011, 400, 3165-3175.
157. Bottein Dechraoui, M.Y.; Wang, Z.; Turquet, J.; Chinain, M.; Darius, T.; Cruchet, P.; Radwan, F.F.; Dickey, R.W.; Ramsdell, J.S. Biomonitoring of ciguatoxin exposure in mice using blood collection cards. Toxicon 2005, 46, 243-251.
158. Bottein Dechraoui, M.Y.; Wang, Z.; Ramsdell, J.S. Optimization of ciguatoxin extraction method from blood for Pacific ciguatoxin (P-CTX-1). Toxicon 2007, 49, 100-105.
159. Ledreux, A.; Ramsdell, J.S. Bioavailability and intravenous toxicokinetic parameters for Pacific ciguatoxin P-CTX-1 in rats. Toxicon 2013, 64, 81-86.
160. Bottein Dechraoui, M.Y.; Wang, Z.; Ramsdell, J.S. Toxicokinetics of the ciguatoxin P-CTX-1 in rats after intraperitoneal or oral administration. Toxicology 2011, 284, 1-6.
161. O'Toole, A.C.; Dechraoui Bottein, M.-Y.; Danylchuk, A.J.; Ramsdell, J.S.; Cooke, S.J. Linking ciguatera poisoning to spatial ecology of fish: A novel approach to examining the distribution of biotoxin levels in the great barracuda by combining non-lethal blood sampling and biotelemetry. Sci. Total Environ. 2012, 427, 98-105.
162. Fraga, S.; Rodríguez, F.; Caillaud, A.; Diogène, J.; Raho, N.; Zapata, M. Gambierdiscus excentricus sp. nov. (Dinophyceae), a benthic toxic dinoflagellate from the Canary Islands (NE Atlantic Ocean). Harmful Algae 2011, 11, 10-22.
163. Caillaud, A.; de la Iglesia, P.; Barber, E.; Eixarch, H.; Mohammad-Noor, N.; Yasumoto, T.; Diogene, J. Monitoring of dissolved ciguatoxin and maitotoxin using solid-phase adsorption toxin tracking devices: Application to Gambierdiscus pacificus in culture. Harmful Algae 2011, 10, 433-446.
164. Shimojo, R.Y.; Iwaoka, W.T. A rapid hemolysis assay for the detection of sodium channel-specific marine toxins. Toxicology 2000, 154, 1-7.
165. Holland, W.C.; Litaker, R.W.; Tomas, C.R.; Kibler, S.R.; Place, A.R.; Davenport, E.D.; Tester, P.A. Differences in the toxicity of six Gambierdiscus (Dinophyceae) species measured using an in vitro human erythrocyte lysis assay. Toxicon 2013, 65, 15-33.
166. Poli, M.A.; Lewis, R.J.; Dickey, R.W.; Musser, S.M.; Buckner, C.A.; Carpenter, L.G. Identification of Caribbean ciguatoxins as the cause of an outbreak of fish poisoning among US soldiers in Haiti. Toxicon 1997, 35, 733-741.
167. Yasumoto, T. Search for ciguatoxin producing clones of Gambierdiscus toxicus on Okinawa coastal reefs. In Abstract book of the Ciguatera and related biotoxins workshop; Institut de recherche pour le développement (IRD): Noumea, New Caledonia, 27-31 October 2008.
168. McCall, J.R.; Jacocks, H.M.; Niven, S.C.; Poli, M.A.; Baden, D.G.; Bourdelais, A.J. Development and utilization of a fluorescence-based receptor-binding assay for the site 5 voltage-sensitive sodium channel ligands brevetoxin and ciguatoxin. J. AOAC Int. 2014, 97, 307-315.
169. Caillaud, A.; Eixarch, H.; de la Iglesia, P.; Rodriguez, M.; Dominguez, L.; Andree, K.; Diogene, J. Towards the standardisation of the neuroblastoma (neuro-2a) cell-based assay for ciguatoxin-like toxicity detection in fish: Application to fish caught in the Canary Islands. Food Add. Contam. A 2012, 29, 1000-1001.
170. Robertson, A.; Garcia, A.C.; Quintana, H.A.F.; Smith, T.B.; Castillo, B.F.; Reale-Munroe, K.; Gulli, J.A.; Olsen, D.A.; Hooe-Rollman, J.I.; Jester, E.L.E.; et al . Invasive lionfish (Pterois volitans): A potential human health threat for ciguatera fish poisoning in tropical waters. Mar. Drugs 2014, 12, 88-97.
171. Kerbrat, A.-S.; Darius, H.T.; Pauillac, S.; Chinain, M.; Laurent, D. Detection of ciguatoxin-like and paralysing toxins in Trichodesmium spp. from New Caledonia lagoon. Mar. Pollut. Bull. 2010, 61, 360-366.
172. Otero, A.; Chapela, M.-J.; Atanassova, M.; Vieites, J.M.; Cabado, A.G. Cyclic Imines: Chemistry and mechanism of action: A review. Chem. Res. Toxicol. 2011, 24, 1817-1829.
173. Chatzianastasiou, M.; Katikou, P.; Zacharaki, T.; Papazachariou, A.; McKevitt, A. Cyclic imines, as emerging marine toxins: Chemical properties, distribution, toxicological aspects and detection methods. J. Hell. Vet. Med. Soc. 2011, 62, 240-248.
174. Cembella, A.; Lewis, N.; Quilliam, M. The marine dinoflagellate Alexandrium ostenfeldii (Dinophyceae) as the causative organism of spirolide shellfish toxins. Phycologia 2000, 39, 67-74.
175. Touzet, N.; Franco, J.M.; Raine, R. Morphogenetic diversity and biotoxin composition of Alexandrium (Dinophyceae) in Irish coastal waters. Harmful Algae 2008, 7, 782-797.
176. Seki, T.; Satake, M.; Mackenzie, L.; Kaspar, H.F.; Yasumoto, T. Gymnodimine, a new marine toxin of unprecedented structure isolated from New-Zeland oysters and the dinofalgellate Gymnnodinium sp. Tetrahedron Lett. 1995, 36, 7093-7096.
177. Rhodes, L.; Smith, K.; Selwood, A.; McNabb, P.; van Ginkel, R.; Holland, P.; Munday, R. Production of pinnatoxins by a peridinoid dinoflagellate isolated from Northland, New Zealand. Harmful Algae 2010, 9, 384-389.
178. Nezan, E.; Chomerat, N. Vulcanodinium rugosum gen. nov., sp. nov. (Dinophyceae): A new marine dinoflagellate from the French Mediterranean coast. Cryptogam. Algol. 2011, 32, 3-18.
179. 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.
180. Lu, C.K.; Lee, G.H.; Huang, R.; Chou, H.N. Spiro-prorocentrimine, a novel macrocyclic lactone from a benthic Prorocentrum sp. of Taiwan. Tetrahedron Lett. 2001, 42, 1713-1716.
181. Miles, C.O.; Wilkins, A.L.; Stirling, D.J.; MacKenzie, A.L. Gymnodimine C, an isomer of gymnodimine B, from Karenia selliformis. J. Agric. Food Chem. 2003, 51, 4838-4840.
182. Van Wagoner, R.M.; Misner, I.; Tomas, C.R.; Wright, J.L. Occurrence of 12-methylgymnodimine in a spirolide-producing dinoflagellate Alexandrium peruvianum and the biogenetic implications. Tetrahedron Lett. 2011, 52, 4243-4246.
183. Gueret, S.M.; Brimble, M.A. Spiroimine shellfish poisoning (SSP) and the spirolide family of shellfish toxins: Isolation, structure, biological activity and synthesis. Nat. Prod. Rep. 2010, 27, 1350-1366.
184. Selwood, A.I.; Miles, C.O.; Wilkins, A.L.; van Ginkel, R.; Munday, R.; Rise, F.; McNabb, P. Isolation, structural determination and acute toxicity of pinnatoxins E, F and G. J. Agric. Food Chem. 2010, 58, 6532-6542.
185. Molgó, J.; Girard, E.; Benoit, E. 18 Cyclic Imines: An insight into this emerging group of bioactive marine toxins. In Phycotoxins: Chemistry and Biochemistry; Botana, L.M., Ed.; Wiley-Blackwell: Ames, IA, USA, 2008; pp. 319-335.
186. Aasen, J.A.; Hardstaff, W.; Aune, T.; Quilliam, M.A. Discovery of fatty acid ester metabolites of spirolide toxins in mussels from Norway using liquid chromatography/tandem mass spectrometry. Rapid Commun. Mass Spectrom. 2006, 20, 1531-1537.
187. McCarron, P.; Rourke, W.A.; Hardstaff, W.; Pooley, B.; Quilliam, M.A. Identification of pinnatoxins and discovery of their fatty acid ester metabolites in mussels (Mytilus edulis) from Eastern Canada. J. Agric. Food Chem. 2012, 60, 1437-1446.
188. Hu, T.; deFreitas, A.S.; Curtis, J.M.; Oshima, Y.; Walter, J.A.; Wright, J.L. Isolation and structure of prorocentrolide B, a fast-acting toxin from Prorocentrum maculosum . J. Nat. Prod. 1996, 59, 1010-1014.
189. MacKenzie, L.A.; Haywood, A.J.; Adamson, J.; Truman, P.; Till, D.; Seki, T.; Satake, M.; Yasumoto, T. Gymnodimine contamination in shellfish in New Zealand. In Harmful and Toxic Algal Blooms; Yasumoto, T., Oshima, Y., Fukuyo, Y., Eds.; The Intergovernmental Oceanographic Commission of UNESCO: Paris, France, 1996; pp. 97-100.
190. Uemura, 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. J. Am. Chem. Soc. 1995, 117, 1155-1156.
191. Bourne, Y.; Radic, Z.; Aráoz, R.; Talley, T.T.; Benoit, E.; Servent, D.; Taylor, P.; Molgó, J.; Marchot, P. Structural determinants in phycotoxins and AChBP conferring high affinity binding and nicotinic AChR antagonism. Proc. Natl. Acad. Sci. USA 2010, 107, 6076-6081.
192. Stivala, C.E.; Benoit, E.; Araoz, R.; Servent, D.; Novikov, A.; Molgo, J.; Zakarian, A. Synthesis and biology of cyclic imine toxins, an emerging class of potent, globally distributed marine toxins. Nat. Prod. Rep. 2014, doi:10.1039/C4NP00089G.
193. th ICHA, 4-8 September 2006; ISSHA and IOC of UNESCO: Copenhagen, Denmark, 2008; pp. 319-322.
194. Kharrat, R.; Servent, D.; Girard, E.; Ouanounou, G.; Amar, M.; Marrouchi, R.; Benoit, E.; Molgo, J. The marine phycotoxin gymnodimine targets muscular and neuronal nicotinic acetylcholine receptor subtypes with high affinity. J. Neurochem. 2008, 107, 952-963.
195. Dragunow, M.; Trzoss, M.; Brimble, M.A.; Cameron, R.; Beuzenberg, V.; Holland, P.; Mountfort, D. Investigations into the cellular actions of the shellfish toxin gymnodimine and analogues. Environ. Toxicol. Pharmacol. 2005, 20, 305-312.
196. Geiger, M.; Desanglois, G.; Hogeveen, K.; Fessard, V.; Lepretre, T.; Mondeguer, F.; Guitton, Y.; Herve, F.; Sechet, V.; Grovel, O.; et al. Cytotoxicity, fractionation and dereplication of extracts of the Dinoflagellate Vulcanodinium rugosum, a producer of pinnatoxin G. Mar. Drugs 2013, 11, 3350-3371.
197. Hellyer, S.D.; Selwood, A.I.; van Ginkel, R.; Munday, R.; Sheard, P.; Miles, C.O.; Rhodes, L.; Kerr, D.S. In vitro labelling of muscle type nicotinic receptors using a fluorophore-conjugated pinnatoxin F derivative. Toxicon 2014, 87, 17-25.
198. Tatters, A.O.; Muhlstein, H.I.; Tomas, C.R. The hemolytic activity of Karenia selliformis and two clones of Karenia brevis throughout a growth cycle. J. Appl. Phycol. 2010, 22, 435-442.
199. Eschbach, E.; Scharsack, J.P.; John, U.; Medlin, L.K. Improved erythrocyte lysis assay in microtitre plates for sensitive detection and efficient measurement of haemolytic compounds from ichthyotoxic algae. J. Appl. Toxicol. 2001, 21, 513-519.
200. Vilariño, N.; Fonfria, E.S.; Molgo, J.; Araoz, R.; Botana, L.M. Detection of gymnodimine-A and 13-desmethyl C spirolide phycotoxins by fluorescence polarization. Anal. Chem. 2009, 81, 2708-2714.
201. Fonfria, E.S.; Vilarino, N.; Molgo, J.; Araoz, R.; Otero, P.; Espina, B.; Carmen Louzao, M.; Alvarez, M.; Botana, L.M. Detection of 13,19-didesmethyl C spirolide by fluorescence polarization using Torpedo electrocyte membranes. Anal. Biochem. 2010, 403, 102-107.
202. Fonfria, E.S.; Vilarino, N.; Espina, B.; Carmen Louzao, M.; Alvarez, M.; Molgo, J.; Araoz, R.; Botana, L.M. Feasibility of gymnodimine and 13-desmethyl C spirolide detection by fluorescence polarization using a receptor-based assay in shellfish matrixes. Anal. Chim. Acta 2010, 657, 75-82.
203. Otero, P.; Alfonso, A.; Alfonso, C.; Araoz, R.; Molgo, J.; Vieytes, M.R.; Botana, L.M. First direct fluorescence polarization assay for the detection and quantification of spirolides in mussel samples. Anal. Chim. Acta 2011, 701, 200-208.
204. Rodriguez, L.P.; Vilarino, N.; Molgo, J.; Araoz, R.; Antelo, A.; Vieytes, M.R.; Botana, L.M. Solid-phase receptor-based assay for the detection of cyclic imines by chemiluminescence, fluorescence, or colorimetry. Anal. Chem. 2011, 83, 5857-5863.
205. Rodriguez, L.P.; Vilarino, N.; Molgo, J.; Araoz, R.; Botana, L.M. High-throughput receptor-based assay for the detection of spirolides by chemiluminescence. Toxicon 2013, 75, 35-43.
206. Araoz, R.; Ramos, S.; Pelissier, F.; Guerineau, V.; Benoit, E.; Vilarino, N.; Botana, L.M.; Zakarian, A.; Molgo, J. Coupling the Torpedo microplate-receptor binding assay with mass spectrometry to detect cyclic imine neurotoxins. Anal. Chem. 2012, 84, 10445-10453.
207. Rodriguez, L.P.; Vilarino, N.; Molgo, J.; Araoz, R.; Carmen Louzao, M.; Taylor, P.; Talley, T.; Botana, L.M. Development of a solid-phase receptor-based assay for the detection of cyclic imines using a microsphere-flow cytometry system. Anal. Chem. 2013, 85, 2340-2347.
208. Yotsu-Yamashita, M.; Sugimoto, A.; Takai, A.; Yasumoto, T. Effects of specific modifications of several hydroxyls of tetrodotoxin on its affinity to rat brain membrane. J. Pharmacol. Exp. Ther. 1999, 289, 1688-1696.
209. Bane, V.; Lehane, M.; Dikshit, M.; O'Riordan, A.; Furey, A. Tetrodotoxin: Chemistry, toxicity, source, distribution and detection. Toxins 2014, 6, 693-755.
210. Tahara, Y.; Hirata, Y. Studies on the puffer fish toxin. J. Pharm. Soc. Jpn. 1909, 29, 587-625.
211. Yokoo, A. Chemical studies on pufferfish toxin (3)-separation of spheroidine. J. Chem. Soc. Jpn. 1950, 71, 590-592.
212. Tsuda, K.; Tachikawa, R.; Sakai, K.; Tamura, C.; Amakasu, O.; Kawamura, M.; Ikuma, S. On the structure of tetrodotoxin. Chem. Pharm. Bull. 1964, 12, 642-645.
213. Woodward, R.; Gougoutas, J.Z. The structure of tetrodotoxin. Pure Appl. Chem. 1964, 9, 49-74.
214. Goto, T.; Kishi, Y.; Takahashi, S.; Hirata, Y. Tetrodotoxin. Tetrahedron 1965, 21, 2059-2088.
215. Noguchi, T.; Arakawa, O.; Takatani, T. TTX accumulation in pufferfish. Comp. Biochem. Physiol. D 2006, 1, 145-152.
216. Chau, R.; Kalaitzis, J.A.; Neilan, B.A. On the origins and biosynthesis of tetrodotoxin. Aquat. Toxicol. 2011, 104, 61-72.
217. Pratheepa, V.; Vasconcelos, V. Microbial diversity associated with tetrodotoxin production in marine organisms. Environ. Toxicol. Pharmacol. 2013, 36, 1046-1054.
218. Rodriguez, P.; Alfonso, A.; Vale, C.; Alfonso, C.; Vale, P.; Tellez, A.; Botana, L.M. First toxicity report of tetrodotoxin and 5,6,11-trideoxyTTX in the trumpet shell Charonia lampas lampas in Europe. Anal. Chem. 2008, 80, 5622-5629.
219. Bentur, Y.; Ashkar, J.; Lurie, Y.; Levy, Y.; Azzam, Z.S.; Litmanovich, M.; Golik, M.; Gurevych, B.; Golani, D.; Eisenman, A. Lessepsian migration and tetrodotoxin poisoning due to Lagocephalus sceleratus in the eastern Mediterranean. Toxicon 2008, 52, 964-968.
220. Silva, M.; Azevedo, J.; Rodriguez, P.; Alfonso, A.; Botana, L.M.; Vasconcelos, V. New gastropod vectors and tetrodotoxin potential expansion in temperate waters of the Atlantic Ocean. Mar. Drugs 2012, 10, 712-726.
221. Kawatsu, K.; Hamano, Y.; Yoda, T.; Terano, Y.; Shibata, T. Rapid and highly sensitive enzyme immunoassay for quantitative determination of tetrodotoxin. Jpn. J. Med. Sci. Biol. 1997, 50, 133-150.
222. Zhou, Y.; Li, Y.; Pan, F.; Liu, Z.; Wang, Z. Identification of tetrodotoxin antigens and a monoclonal antibody. Food Chem. 2009, 112, 582-586.
223. Raybould, T.J.G.; Bignami, G.S.; Inouye, L.K.; Simpson, S.B.; Byrnes, J.B.; Grothaus, P.G.; Vann, D.C. A monoclonal antibody-based immunoassay for detecting tetrodotoxin in biological samples. J. Clin. Lab. Anal. 1992, 6, 65-72.
224. Neagu, D.; Micheli, L.; Palleschi, G. Study of a toxin-alkaline phosphatase conjugate for the development of an immunosensor for tetrodotoxin determination. Anal. Bioanal. Chem. 2006, 385, 1068-1074.
225. Tao, J.; Wei, W.; Nan, L.; Lei, L.; Hui, H.; Fen, G.; Jun, L.; Jing, Z.; Rong, J. Development of competitive indirect ELISA for the detection of tetrodotoxin and a survey of the distribution of tetrodotoxin in the tissues of wild puffer fish in the waters of south-east China. Food Add. Contam. 2010, 27, 1589-1597.
226. Stokes, A.N.; Williams, B.L.; French, S.S. An improved competitive inhibition enzymatic immunoassay method for tetrodotoxin quantification. Biol. Proced. Online 2012, 14, 1-5.
227. Wang, R.; Huang, A.; Liu, L.; Xiang, S.; Li, X.; Ling, S.; Wang, L.; Lu, T.; Wang, S. Construction of a single chain variable fragment antibody (scFv) against tetrodotoxin (TTX) and its interaction with TTX. Toxicon 2014, 83, 22-34.
228. Kreuzer, M.P.; Pravda, M.; O'Sullivan, C.K.; Guilbault, G.G. Novel electrochemical immunosensors for seafood toxin analysis. Toxicon 2002, 40, 1267-1274.
229. Yu, C.-H.; Yu, C.-F.; Tam, S.; Hoi-Fu Yu, P. Rapid screening of tetrodotoxin in urine and plasma of patients with puffer fish poisoning by HPLC with creatinine correction. Food Add. Contam. 2010, 27, 89-96.
230. Zhou, Y.; Li, Y.; Lu, S.; Ren, H.; Li, Z.; Zhang, Y.; Pan, F.; Liu, W.; Zhang, J.; Liu, Z. Gold nanoparticle probe-based immunoassay as a new tool for tetrodotoxin detection in puffer fish tissues. Sens. Actuators B 2010, 146, 368-372.
231. Thattiyaphong, A.; Unahalekhaka, J.; Mekha, N.; Nispa, W.; Kluengklangdon, P.; Rojanapantip, L. Efficiency of a rapid test for detection of tetrodotoxin in puffer fish. J. Immunoass. Immunochem. 2013, 35, 111-119.
232. Yakes, B.J.; Deeds, J.; White, K.; DeGrasse, S.L. Evaluation of surface plasmon resonance biosensors for detection of tetrodotoxin in food matrices and comparison to analytical methods. J. Agric. Food Chem. 2011, 59, 839-846.
233. Taylor, A.D.; Ladd, J.; Etheridge, S.; Deeds, J.; Hall, S.; Jiang, S. Quantitative detection of tetrodotoxin (TTX) by a surface plasmon resonance (SPR) sensor. Sens. Actuators B 2008, 130, 120-128.
234. Taylor, A.D.; Vaisocherová, H.; Deeds, J.; DeGrasse, S.; Jiang, S. Tetrodotoxin detection by a surface plasmon resonance sensor in pufferfish matrices and urine. J. Sens. 2011, doi:10.1155/2011/601704.
235. Vaisocherova, H.; Taylor, A.D.; Jiang, S.; Hegnerova, K.; Vala, M.; Homola, J.; Yakes, B.J.; Deeds, J.; DeGrasse, S. Surface plasmon resonance biosensor for determination of tetrodotoxin: Prevalidation study. J. AOAC Int. 2011, 94, 596-604.
236. Campbell, K.; Barnes, P.; Haughey, S.; Higgins, C.; Kawatsu, K.; Vasconcelos, V.; Elliott, C. Development and single laboratory validation of an optical biosensor assay for tetrodotoxin detection as a tool to combat emerging risks in European seafood. Anal. Bioanal. Chem. 2013, 405, 7753-7763.
237. Yakes, B.J.; Kanyuck, K.M.; DeGrasse, S.L. First report of a direct surface plasmon resonance immunosensor for a small molecule seafood toxin. Anal. Chem. 2014, 86, 9251-9255.
238. Yakes, B.J.; Etheridge, S.M.; Mulvaney, S.P.; Tamanaha, C.R. Fluidic force discrimination assays: A new technology for tetrodotoxin detection. Mar. Drugs 2010, 8, 565-576.
239. Kogure, K.; Tamplin, M.L.; Simidu, U.; Colwell, R.R. A tissue culture assay for tetrodotoxin, saxitoxin and related toxins. Toxicon 1988, 26, 191-197.
240. Narahashi, T.; Moore, J.W.; Scott, W.R. Tetrodotoxin blockage of sodium conductance increase in lobster giant axons. J. Gen. Physiol. 1964, 47, 965-974.
241. Catterall, W.A.; Nirenberg, M. Sodium uptake associated with activation of action potential ionophores of cultured neuroblastoma and muscle cells. Proc. Natl. Acad. Sci. USA 1973, 70, 3759-3763.
242. Do, H.; Hamasaki, K.; Ohwada, K.; Simidu, U.; Noguchi, T.; Shida, Y.; Kogure, K. Presence of tetrodotoxin and tetrodotoxin-producing bacteria in freshwater sediments. Appl. Environ. Microbiol. 1993, 59, 3934-3937.
243. Wu, Z.; Xie, L.; Xia, G.; Zhang, J.; Nie, Y.; Hu, J.; Wang, S.; Zhang, R. A new tetrodotoxin-producing actinomycete, Nocardiopsis dassonvillei, isolated from the ovaries of puffer fish Fugu rubripes. Toxicon 2005, 45, 851-859.
244. Gallacher, S.; Birkbeck, T. A tissue culture assay for direct detection of sodium channel blocking toxins in bacterial culture supernates. FEMS Microbiol. Lett. 1992, 92, 101-107.
245. Hamasaki, K.; Kogure, K.; Ohwada, K. A biological method for the quantitative measurement of tetrodotoxin (TTX): Tissue culture bioassay in combination with a water-soluble tetrazolium salt. Toxicon 1996, 34, 490-495.
246. Hamasaki, K.; Kogure, K.; Ohwada, K. An improved method of tissue culture bioassay for tetrodotoxin. Fish. Sci. 1996b, 62, 825-829.
247. Kodama, M.; Ogata, T.; Noguchi, T.; Maruyama, J.; Hashimoto, K. Occurrence of saxitoxin and other toxins in the liver of the pufferfish Takifugu pardalis. Toxicon 1983, 21, 897-900.
248. Jang, J.; Yotsu-Yamashita, M. Distribution of tetrodotoxin, saxitoxin, and their analogs among tissues of the puffer fish Fugu pardalis. Toxicon 2006, 48, 980-987.
249. Jen, H.-C.; Lin, S.-J.; Lin, S.-Y.; Huang, Y.-W.; Liao, I.; Arakawa, O.; Hwang, D.-F. Occurrence of tetrodotoxin and paralytic shellfish poisons in a gastropod implicated in food poisoning in southern Taiwan. Food Add. Contam. 2007, 24, 902-909.
250. Yotsu-Yamashita, M.; Mebs, D. Occurrence of 11-oxotetrodotoxin in the red-spotted newt, Notophthalmus viridescens, and further studies on the levels of tetrodotoxin and its analogues in the newt's efts. Toxicon 2003, 41, 893-897.
251. Cheun, B.; Endo, H.; Hayashi, T.; Nagashima, Y.; Watanabe, E. Development of an ultra high sensitive tissue biosensor for determination of swellfish poisoning, tetrodotoxin. Biosens. Bioelectron. 1996, 11, 1185-1191.
252. Pancrazio, J.J.; Gray, S.A.; Shubin, Y.S.; Kulagina, N.; Cuttino, D.S.; Shaffer, K.M.; Eisemann, K.; Curran, A.; Zim, B.; Gross, G.W. A portable microelectrode array recording system incorporating cultured neuronal networks for neurotoxin detection. Biosens. Bioelectron. 2003, 18, 1339-1347.
253. Charkhkar, H.; Knaack, G.L.; Gnade, B.E.; Keefer, E.W.; Pancrazio, J.J. Development and demonstration of a disposable low-cost microelectrode array for cultured neuronal network recording. Sens. Actuators B 2012, 161, 655-660.
254. Mohan, D.K.; Molnar, P.; Hickman, J.J. Toxin detection based on action potential shape analysis using a realistic mathematical model of differentiated NG108-15 cells. Biosens. Bioelectron. 2006, 21, 1804-1811.
255. Weiser, T. A novel toxicity-based assay for the identification of modulators of voltage-gated Na+ channels. J. Neurosci. Methods 2004, 137, 79-85.