Species selective resistance of cardiac muscle voltage gated sodium channels: Characterization of brevetoxin and ciguatoxin binding sites in rats and fish

Toxicon

Volumn 48, Issue 6, 2006, Pages 702-712

  Bottein Dechraoui, Marie Yasmine ^a   Wacksman, Jeremy J ^b   Ramsdell, John S ^a  

^a CENTER FOR COASTAL ENVIRONMENTAL HEALTH AND BIOMOLECULAR RESEARCH   (United States)

^b Department of Teacher Education and Department of Sociology and Anthropology   (United States)

Author keywords

Brevetoxin; Ciguatera; Ciguatoxin; Isoform; Mammals; Marine toxins; Teleost fish; Voltage gated sodium channel

Indexed keywords

BREVETOXIN; CIGUATOXIN; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; BRAIN TISSUE; CARDIOSELECTIVITY; CONTROLLED STUDY; HEART; HEART MUSCLE; MAMMAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; RAT; RECEPTOR BINDING; SKELETAL MUSCLE; TELEOST; TOXIN ANALYSIS;

ANIMALS; BASS; BRAIN; CIGUATOXINS; DINOFLAGELLIDA; FISH PROTEINS; MARINE TOXINS; MUSCLE FIBERS; MUSCLE FIBERS, SKELETAL; MYOCYTES, CARDIAC; NEUROTOXINS; OXOCINS; RATS; SODIUM CHANNELS; SPECIES SPECIFICITY;

CENTROPRISTIS STRIATA; CIGUATERA; DINOPHYCEAE; MAMMALIA; TELEOSTEI;

EID: 33749556457     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2006.07.032     Document Type: Article

References (66)

1. Anderson D.M., and Lobel P.S. The continuing enigma of ciguatera. Biol. Bull. 172 (1987) 92-107
2. Anderson P.A.V., Roberts-Misterly J., and Greenberg R.M. The evolution of voltage-gated sodium channels: were algal toxins involved?. Harlful Algae 4 (2005) 95-107
3. Bagnis R., Kuberski T., and Laugier S. Clinical observations on 3009 cases of ciguatera (fish poisoning) in the South Pacific. Am. J. Trop. Med. Hyg. 28 6 (1979) 1067-1073
4. Benoit, E., Boydron-Le Garec, R., Sauviat, M.P., 2005. Implication de la nociception cutanee dans l'intoxication de type ciguatera. In: Bon, C.G.P.F., Goyffon, M., Sauviat, M.P. (Eds.) Toxines et douleur. Lavoisier.
5. Borison H.L., McCarthy L.E., and Ellis S. Neurological analysis of respiratory, cardiovascular and neuromuscular effects of brevetoxin in cats. Toxicon 23 3 (1985) 517-524
6. Bottein Dechraoui M.Y., and Ramsdell J.S. Type B brevetoxins show tissue selectivity for voltage-gated sodium channels: comparison of brain, skeletal muscle and cardiac sodium channels. Toxicon 41 7 (2003) 919-927
7. Bricelj V.M., Connell L., Konoki K., Macquarrie S.P., Scheuer T., Catterall W.A., and Trainer V.L. Sodium channel mutation leading to saxitoxin resistance in clams increases risk of PSP. Nature 434 7034 (2005) 763-767
8. Cameron J., and Capra M.F. The basis of the paradoxical disturbance of temperature perception in ciguatera poisoning. J. Toxicol. Clin. Toxicol. 31 4 (1993) 571-579
9. Capra M.F., and Cameron J. Ciguatera in Australia. In: M D.M. (Ed). Ciuatera Seafood Toxins (1991), CRC Press, Boca Raton, FL 33-52
10. Catterall W.A. Molecular properties of voltage-sensitive sodium channels. Annu. Rev. Biochem. 55 (1986) 953-985
11. Catterall W.A., Morrow C.S., and Hartshorne R.P. Neurotoxin binding to receptor sites associated with voltage-sensitive sodium channels in intact, lysed, and detergent-solubilized brain membranes. J. Biol. Chem. 254 22 (1979) 11379-11387
12. Chinain M., Faust M.A., and Pauillac S. Morphology and molecular analysis of three toxic species of Gambierdiscus (dinophyceae): G. Pacificus, SP. Nov., G. Australes, SP. Nov., and G. Polynesiensis, SP. Nov. J. Phycol. 35 (1999) 1282-1296
13. Cohen S.A. Immunocytochemical localization of rh1 sodium channel in adult rat heart atria and ventricle-presence in terminal intercalated disks. Circulation 94 12 (1996) 3083-3086
14. Colman J.R., and Ramsdell J.S. The type B brevetoxin (PbTx-3) adversely affects development, cardiovascular function, and survival in Medaka (Oryzias latipes) embryos. Environ. Health Perspect. 111 16 (2003) 1920-1925
15. Colman J.R., Dechraoui M.-Y.B., Dickey R.W., and Ramsdell J.S. Characterization of the developmental toxicity of Caribbean ciguatoxins in finfish embryos. Toxicon 44 1 (2004) 59-66
16. Cruz-Rivera, E., Villareal, T.A., 2005. Macroalgal palatability and the flux of ciguatera toxins through marine food webs. Harmful Algae (in press).
17. Dargent B., and Couraud F. Down-regulation of voltage-dependent sodium channels initiated by sodium influx in developing neurons. Proc. Natl. Acad. Sci. USA 87 15 (1990) 5907-5911
18. Dargent B., Paillart C., Carlier E., Alcaraz G., Martin-Eauclaire M.F., and Couraud F. Sodium channel internalization in developing neurons. Neuron 13 3 (1994) 683-690
19. Dechraoui M.Y., Naar J., Pauillac S., and Legrand A.M. Ciguatoxins and brevetoxins, neurotoxic polyether compounds active on sodium channels. Toxicon 37 1 (1999) 125-143
20. Diss J.K., Fraser S.P., and Djamgoz M.B. Voltage-gated Na+ channels: multiplicity of expression, plasticity, functional implications and pathophysiological aspects. Eur. Biophys. J. 33 3 (2004) 180-193
21. Edmunds J.S., McCarthy R.A., and Ramsdell J.S. Ciguatoxin reduces larval survivability in finfish. Toxicon 37 12 (1999) 1827-1832
22. Edwards R.A., Lutz P.L., and Baden D.G. Relationship between energy expenditure and ion channel density in the turtle and rat brain. Am. J. Physiol. 257 6 Pt 2 (1989) R1354-R1358
23. Eells J.T., Rasmussen J.L., Bandettini P.A., and Propp J.M. Differences in the neuroexcitatory actions of pyrethroid insecticides and sodium channel-specific neurotoxins in rat and trout brain synaptosomes. Toxicol. Appl. Pharmacol. 123 1 (1993) 107-119
24. Ellis, S., Spikes, J.J., Johnson, G.L., 1979. Respiratory and cardiovascular effects of G. breve toxin in dogs. In: Second International Conference on Toxic Dinoflagellate Blooms, p. 431.
25. Flewelling l., Naar J., Abbott J., Baden D.G., Barros N.B., Bottein Dechraoui M.-Y., Hammond D., Haubold E., Heil C., Henry M., Jacocks H., Leighfield T., Pierce R., Pitchford T., Rommel S., Rowles T., Scott P., Steidinger K.A., Truby E., Van Dolah F., and Landsberg J. Red tide and marine mammal mortalities. Nature 435 (2005) 755-756
26. Fraser S.P., Diss J.K., Chioni A.M., Mycielska M.E., Pan H., Yamaci R.F., Pani F., Siwy Z., Krasowska M., Grzywna Z., Brackenbury W.J., Theodorou D., Koyuturk M., Kaya H., Battaloglu E., De Bella M.T., Slade M.J., Tolhurst R., Palmieri C., Jiang J., Latchman D.S., Coombes R.C., and Djamgoz M.B. Voltage-gated sodium channel expression and potentiation of human breast cancer metastasis. Clin. Cancer Res. 11 15 (2005) 5381-5389
27. Fraser S.P., Salvador V., Manning E.A., Mizal J., Altun S., Raza M., Berridge R.J., and Djamgoz M.B. Contribution of functional voltage-gated Na+ channel expression to cell behaviors involved in the metastatic cascade in rat prostate cancer: I. Lateral motility. J. Cell. Physiol. 195 3 (2003) 479-487
28. Gillespie N.C., Lewis R.J., Pearn J.H., Bourke A.T., Holmes M.J., Bourke J.B., and Shields W.J. Ciguatera in Australia. Occurrence, clinical features, pathophysiology and management. Med. J. Austr. 145 11&12 (1986) 584-590
29. Giraud P., Alcaraz G., Jullien F., Sampo B., Jover E., Couraud F., and Dargent B. Multiple pathways regulate the expression of genes encoding sodium channel subunits in developing neurons. Brain Res. Mol. Brain Res. 56 1&2 (1998) 238-255
30. Goldin A.L., Barchi R.L., Caldwell J.H., Hofmann F., Howe J.R., Hunter J.C., Kallen R.G., Mandel G., Meisler M.H., Netter Y.B., Noda M., Tamkun M.M., Waxman S.G., Wood J.N., and Catterall W.A. Nomenclature of voltage-gated sodium channels. Neuron 28 2 (2000) 365-368
31. Hahn S.T., Capra M.F., and Walsh T.P. Ciguatoxin-protein association in skeletal muscle of Spanish mackerel (Scomberomorus commersoni). Toxicon 30 8 (1992) 843-852
32. Hoffman B.F., and Cranefield P.F. Electrophysiology of the Heart (1960), McGraw-Hill Book Co Inc, New York, NY
33. Huang J.M., Wu C.H., and Baden D.G. Depolarizing action of a red-tide dinoflagellate brevetoxin on axonal membranes. J. Pharmacol. Exp. Therapeut. 229 2 (1984) 615-621
34. Johnson G.L., Spikes J.J., and Ellis S. Cardiovascular effects of brevetoxins in dogs. Toxicon 23 3 (1985) 505-515
35. Kimm-Brinson K.L., and Ramsdell J.S. The red tide toxin, brevetoxin, induces embryo toxicity and developmental abnormalities. Environ. Health Perspect. 109 4 (2001) 377-381
36. Kirkpatrick B., Fleming L.E., Squicciarini D., Backer L.C., Clark R., Abraham W., Benson J., Cheng Y.S., Johnson D., and Pierce R. Literature review of Florida red tide: implications for human health effects. Harmful Algae 3 2 (2004) 99-115
37. Landsberg J.H. The effects of harmful algal blooms on aquatic organisms. Rev. Fish. Sci. 10 2 (2002) 113-390
38. Lehane L., and Lewis R.J. Ciguatera: recent advances but the risk remains. Int. J. Food Microbiol. 61 2&3 (2000) 91-125
39. Lewis R.J. Ciguatoxins are potent ichthyotoxins. Toxicon 30 2 (1992) 207-211
40. Lombet A., Bidard J.N., and Lazdunski M. Ciguatoxin and brevetoxins share a common receptor site on the neuronal voltage-dependent Na+ channel. FEBS Lett. 219 2 (1987) 355-359
41. Lopreato G.F., Lu Y., Southwell A., Atkinson N.S., Hillis D.M., Wilcox T.P., and Zakon H.H. Evolution and divergence of sodium channel genes in vertebrates. Proc. Natl. Acad. Sci. USA 98 13 (2001) 7588-7592
42. McFarren E., Silva F., Tanabe H., Wilson W., Campbell J., and Lewis K. The occurrence of a ciguatera-like poison in oysters, clams, and Gymnodinium breve cultures. Toxicon 3 2 (1965) 111-123
43. Music S.I., Howell J.T., and Brumback C.L. Red tide. Its public health implications. JFMA 60 11 (1973) 27-29
44. Naar, J., Flewelling, L., Lenzi, A., Landsberg, J.H., Jacocks, H., Musser, S., Bourdelais, A., Steidinger, K., Baden, D. G., 2003. Experimental bioaccumulation of ichthyotoxic brevetoxins in health fish. In: Second Symposium on Harmful Marine Algae in the US
45. Perez-Arellano J.L., Luzardo O.P., Perez Brito A., Hernandez Cabrera M., Zumbado M., Carranza C., Angel-Moreno A., Dickey R.W., and Boada L.D. Ciguatera fish poisoning, Canary Islands. Emerg. Infect. Dis. 11 12 (2005) 1981-1982
46. Poli M.A., Mende T.J., and Baden D.G. Brevetoxins, unique activators of voltage-sensitive sodium channels, bind to specific sites in rat brain synaptosomes. Mol. Pharmacol. 30 2 (1986) 129-135
47. Poli M.A., Templeton C.B., Thompson W.L., and Hewetson J.F. Distribution and elimination of brevetoxin PbTx-3 in rats. Toxicon 28 8 (1990) 903-910
48. Pottier I., Vernoux J.P., Jones A., and Lewis R.J. Characterisation of multiple Caribbean ciguatoxins and congeners in individual specimens of horse-eye jack (Caranx latus) by high-performance liquid chromatography/mass spectrometry. Toxicon 40 7 (2002) 929-939
49. Rodgers R.L., Chou H.N., Temma K., Akera T., and Shimizu Y. Positive inotropic and toxic effects of brevetoxin-B on rat and guinea pig heart. Toxicol. Appl. Pharmacol. 76 2 (1984) 296-305
50. Sauviat M.P., Marquais M., and Vernoux J.P. Muscarinic effects of the Caribbean ciguatoxin C-CTX-1 on frog atrial heart muscle. Toxicon 40 8 (2002) 1155-1163
51. Schreibmayer W., and Jeglitsch G. The sodium channel activator Brevetoxin-3 uncovers a multiplicity of different open states of the cardiac sodium channel. Biochim. Biophys. Acta 1104 2 (1992) 233-242
52. Snow P.J., Plenderleith M.B., and Wright L.L. Quantitative study of primary sensory neurone populations of three species of elasmobranch fish. J. Comp. Neurol. 334 1 (1993) 97-103
53. Strachan L.C., Lewis R.J., and Nicholson G.M. Differential actions of pacific ciguatoxin-1 on sodium channel subtypes in mammalian sensory neurons. J. Pharmacol. Exp. Therapeut. 288 1 (1999) 379-388
54. Stuart A.M., and Baden D.G. Florida red tide brevetoxins and binding in fish brain synaptosomes. Aquat. Toxicol. 13 (1988) 271-280
55. Toledo-Aral J.J., Moss B.L., He Z.J., Koszowski A.G., Whisenand T., Levinson S.R., Wolf J.J., Silos-Santiago I., Halegoua S., and Mandel G. Identification of PN1, a predominant voltage-dependent sodium channel expressed principally in peripheral neurons. Proc. Natl. Acad. Sci. USA 94 4 (1997) 1527-1532
56. Templeton C.B., Poli M.A., and LeClaire R.D. Cardiorespiratory effects of brevetoxin (PbTx-2) in conscious, tethered rats. Toxicon 27 9 (1989) 1043-1049
57. Tester P.A., Turner J., and Shea D. Vectorial transport of toxins from the dinoflagellate Gymnodinium breve through copepods to fish. J. Plankton Res. 22 (2000) 47-61
58. Trainer V.L., and Baden D.G. High affinity binding of red tide neurotoxins to marine mammal brain. Aquat. Toxicol. 46 2 (1999) 139-148
59. Trainer V.L., Baden D.G., and Catterall W.A. Identification of peptide components of the brevetoxin receptor site of rat brain sodium channels. J. Biol. Chem. 269 31 (1994) 19904-19909
60. Trainer V.L., Baden D.G., and Catterall W.A. Detection of marine toxins using reconstituted sodium channels. J. AOAC Int. 78 2 (1995) 570-573
61. Van Dolah F.M., Finley E.L., Haynes B.L., Doucette G.J., Moeller P.D., and Ramsdell J.S. Development of rapid and sensitive high throughput pharmacologic assays for marine phycotoxins. Nat. Toxins 2 4 (1994) 189-196
62. Waxman S.G. Acquired channelopathies in nerve injury and MS. Neurology 56 12 (2001) 1621-1627
63. Woofter R., Brendtro K., and Ramsdell J. Uptake and elimination of brevetoxin in blood of striped mullet (Mugil Cephalus) after aqueous exposure to Karenia brevis. Environ. Health Perspect. 113 1 (2005) 11-16
64. Wu C.H., Huang J.M., Vogel S.M., Luke V.S., Atchison W.D., and Narahashi T. Actions of Ptychodiscus brevis toxins on nerve and muscle membranes. Toxicon 23 3 (1985) 481-487
65. Yasumoto T., Igarashi T., Legrand A.M., Cruchet P., Chinain M., Fujita T., and Naoki H. Structural elucidation of ciguatoxin congeners by fast-atom bombardment tandem mass spectroscopy. J. Am. Chem. Soc. 122 20 (2000) 4988-4989
66. Yotsu-Yamashita M., Nishimori K., Nitanai Y., Isemura M., Sugimoto A., and Yasumoto T. Binding properties of (3)H-PbTx-3 and (3)H-saxitoxin to brain membranes and to skeletal muscle membranes of puffer fish Fugu pardalis and the primary structure of a voltage-gated Na(+) channel alpha-subunit (fMNa1) from skeletal muscle of F. pardalis. Biochem. Biophys. Res. Commun. 267 1 (2000) 403-412