Toxic potential of palytoxin

Jiří Patocka , Ramesh C. Gupta , Qing-hua Wu , Kamil Kuca

Current Medical Science ›› 2015, Vol. 35 ›› Issue (5) : 773 -780.

PDF
Current Medical Science ›› 2015, Vol. 35 ›› Issue (5) : 773 -780. DOI: 10.1007/s11596-015-1506-3
Article

Toxic potential of palytoxin

Author information +
History +
PDF

Abstract

This review briefly describes the origin, chemistry, molecular mechanism of action, pharmacology, toxicology, and ecotoxicology of palytoxin and its analogues. Palytoxin and its analogues are produced by marine dinoflagellates. Palytoxin is also produced by Zoanthids (i.e. Palythoa), and Cyanobacteria (Trichodesmium). Palytoxin is a very large, non-proteinaceous molecule with a complex chemical structure having both lipophilic and hydrophilic moieties. Palytoxin is one of the most potent marine toxins with an LD50 of 150 ng/kg body weight in mice exposed intravenously. Pharmacological and electrophysiological studies have demonstrated that palytoxin acts as a hemolysin and alters the function of excitable cells through multiple mechanisms of action. Palytoxin selectively binds to Na+/K+-ATPase with a Kd of 20 pM and transforms the pump into a channel permeable to monovalent cations with a single-channel conductance of 10 pS. This mechanism of action could have multiple effects on cells. Evaluation of palytoxin toxicity using various animal models revealed that palytoxin is an extremely potent neurotoxin following an intravenous, intraperitoneal, intramuscular, subcutaneous or intratracheal route of exposure. Palytoxin also causes non-lethal, yet serious toxic effects following dermal or ocular exposure. Most incidents of palytoxin poisoning have manifested after oral intake of contaminated seafood. Poisonings in humans have also been noted after inhalation, cutaneous/systemic exposures with direct contact of aerosolized seawater during Ostreopsis blooms and/or through maintaining aquaria containing Cnidarian zoanthids. Palytoxin has a strong potential for toxicity in humans and animals, and currently this toxin is of great concern worldwide.

Keywords

phycotoxin / palytoxin / dinoflagellate / toxicity / neurotoxicity

Cite this article

Download citation ▾
Jiří Patocka, Ramesh C. Gupta, Qing-hua Wu, Kamil Kuca. Toxic potential of palytoxin. Current Medical Science, 2015, 35(5): 773-780 DOI:10.1007/s11596-015-1506-3

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

MooreRE, ScheuerPJ. Palytoxin: a new marine toxin from a coelenterate. Science, 1971, 172(3982): 495-498 PMID: 4396320

[2]

DeedsJR, SchwartzMD. Human risk associated with palytoxin exposure. Toxicon, 2010, 56(2): 150-162 PMID: 19505494

[3]

CarballeiraNM, EmilianoA, SostreA, et al. . Fatty acid composition of bacteria associated with the toxic dinoflagellate Ostreopsis lenticularis and with Caribbean Palythoa species. Lipids, 1998, 33(6): 627-632 PMID: 9655379

[4]

TubaroA, SosaS, HungerfordJ. GuptaRC. Toxicology and diversity of marine toxins. Veterinary Toxicology: Basic and Clinical Principles, 2012, Academic Press/Elsevier, Amsterdam, 896-934

[5]

AligizakiK, KatikouP, MilandriA, et al. . Occurrence of palytoxin-group toxins in seafood and future strategies to complement the present state of the art. Toxicon, 2011, 57(3): 390-399 PMID: 21126531

[6]

MundayR. Palytoxin toxicology: Animal studies. Toxicon, 2011, 57(3): 470-477 PMID: 20946911

[7]

EFSA. Scientific opinion on marine biotoxins in shellfish–palytoxin group. EFSA J, 2009,1393(1):1–38

[8]

WuCH. Palytoxin: membrane mechanisms of action. Toxicon, 2009, 54(8): 1183-1189 PMID: 19269304

[9]

RossiniGP, BigianiA. Palytoxin action on the Na(+),K(+)-ATPase and the disruption of ion equilibria in biological systems. Toxicon, 2011, 57(3): 429-439 PMID: 20932855

[10]

WeidmannS. Effects of palytoxin on the electrical activity of dog and rabbit heart. Experientia, 1977, 33(11): 1487-1489 PMID: 21804

[11]

RossiniGP, BigianiA. Palytoxin action on the Nat,Kt- ATPase and the disruption of ion equilibria in biological systems. Toxicon, 2011, 57(3): 429-439 PMID: 20932855

[12]

FrelinC, Van RenterghemC. Palytoxin. Recent electrophysiological and pharmacological evidence for several mechanisms of action. Gen Pharmacol, 1995, 26(1): 33-37 PMID: 7713364

[13]

ArtigasP, GadsbyDC. Large diameter of palytoxininduced Na/K pump channels and modulation of palytoxin interaction by Na/K pump ligands. J Gen Physiol, 2004, 123(4): 357-376 PMCID: 2217460 PMID: 15024043

[14]

HabermanE. Palytoxin acts through Na+/K-ATPase. Toxicon, 1989, 27(6): 1171-1187

[15]

AresIR, LouzaoMC, VieytesMR, et al. . Actin cytoskeleton of rabbit intestinal cells is a target for potent marine phycotoxins. J Exp Biol, 2005, 208(22): 4345-4354 PMID: 16272256

[16]

ShimizuY. Structural chemistry: Complete structure of palytoxin elucidated. Nature, 1983, 302(1): 112

[17]

MooreRE. Structure of palytoxin. Fortschr Chem Org Naturst, 1985, 48(1): 81-202 PMID: 2868975

[18]

RiobóP, FrancoJM. Palytoxins: Biological and chemical determination. Toxicon, 2011, 57(3): 368-375 PMID: 20933536

[19]

CiminielloP, Dell'AversanoC, Dello IacovoE, et al. . LCMS of palytoxin and its analogues: state of the art and future perspectives. Toxins, 2011, 57(3): 376-389

[20]

MundayR. Palytoxin toxicology: animal studies. Toxicon, 2011, 57(3): 470-477 PMID: 20946911

[21]

KitaM, UemuraD. Marine huge molecules: the longest carbon chains in natural products. Chem Rec, 2010, 10(1): 48-52 PMID: 20143381

[22]

MooreRE, BartoliniG, BarchiJ, et al. . Absolute stereochemistry of palytoxin. J Am Chem Soc, 1982, 104(13): 3776-3779

[23]

RamosV, VasconcelosV. Palytoxin and analogs: biological and ecological effects. Mar Drugs, 2010, 8(7): 2021-2037 PMCID: 2920541 PMID: 20714422

[24]

FernándezDA, LouzaoMC, VilariñoN, et al. . The kinetic, mechanistic and cytomorphological effects of palytoxin in human intestinal cells (Caco-2) explain its lower-thanparenteral oral toxicity. FEBS J, 2013, 280(16): 3906-3919 PMID: 23773601

[25]

CiminielloP, Dell'AversanoC, FattorussoE, et al. . The Genoa 2005 outbreak. Determination of putative palytoxin in Mediterranean Ostreopsis ovata by a new liquid chromatography tandem mass spectrometry method. Anal Chem, 2006, 78(17): 6153-6159 PMID: 16944897

[26]

RiobóP, PazB, FrancoJM. Analysis of palytox-in-like in Ostreopsis cultures by liquid chromatography with precolumn derivatization and fluorescence detection. Anal Chim Acta, 2006, 566(2): 217-223

[27]

MontiM, MinocciM, BeranA, IvenaL. First record of Ostreopsis cfr Ovata on macroalgae in the northern Adriatic. Sea. Mar Pol Bull, 2007, 54(5): 598-601

[28]

AligizakiK, PanagiotaK, NikolaidisG, et al. . First episode of shellfish contamination by palytoxin-like compounds from Ostreopsis species (Aegean Sea, Greece). Toxicon, 2008, 51(3): 418-427 PMID: 18067938

[29]

RhodesL. World-wide occurrence of the toxic dinoflagellate genus oxytropsis Schmidt. Toxicon, 2011, 57(3): 400-407 PMID: 20510260

[30]

KatikouP. BotanaLM. Palytoxin and analogues: etiology and origin, chemistry, metabolism, and chemical analysis. Seafood and Freshwater Toxins: Pharmacology, Physiology and Detection, 2008, CRC Press, Boca Raton, 631-663

[31]

CiminielloP, Dell'AversanoC, DelloI, et al. . 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(18): 2735-2744 PMID: 20814980

[32]

TichadouL, GlaizalM, ArmengaudA, et al. . Health impact of unicellular algae of the Ostreopsis genus blooms in the Mediterranean Sea: experience of the French Mediterranean coast surveillance network from 2006 to 2009. Clin Toxicol, 2010, 48(8): 839-844

[33]

SansoniG, BorghiniB, CamiciG, et al. . Fioriture algali di Ostreopsis Ovata (Gonyaulacales: Dinophyceae): Unproblema emergente. Biol Ambientale, 2003, 17(1): 17-23

[34]

GallitelliM, UngaroN, AddanteLM, et al. . Respiratory illness as a reaction to tropical algal bloom occurring in a temperate climate. J Am Med Assoc, 2005, 293(21): 2599-2600

[35]

LouzaoMC, AresIR, VieytesMR, et al. . The cytoskeleton, a structure that is susceptible to the toxic mechanism activated by palytoxins in human excitable cells. FEBS J, 2007, 274(8): 1991-2004 PMID: 17371505

[36]

GleibsS, MebsD. Distribution and sequestration of palytoxin in coral reef animals. Toxicon, 1999, 37(11): 1521-1527 PMID: 10482387

[37]

HarmelN, ApellHJ. Palytoxin-induced effects on partial reactions of the Na,K-ATPase. J Gen Physiol, 2006, 128(1): 103-118 PMCID: 2151552 PMID: 16801384

[38]

RodriguesAM, InfantosiAF, de AlmeidaAC. Palytoxin and the sodium/potassium pump—phosphorylation and potassium interaction. Phys Biol, 2009, 6(3): 036010 PMID: 19461129

[39]

VedovatoN, GadsbyDC. The two C-terminal tyrosines stabilize occluded Na/K pump conformations containing Na or K ions. J Gen Physiol, 2010, 136(1): 63-82 PMCID: 2894553 PMID: 20548052

[40]

RedondoJ, FiedlerB, Scheiner-BobisG. Palytoxininduced Na+ influx into yeast cells expressing the mammalian sodium pump is due to the formation of a channel within the enzyme. Mol Pharmacol, 1996, 49(1): 49-57 PMID: 8569711

[41]

LouzaoMC, AresIR, CagideE. Marine toxins and the cytoskeleton: a new view of palytoxin toxicity. FEBS J, 2008, 275(24): 6067-6074 PMID: 19016862

[42]

Toxicol Lett, 2012, 21(1

[43]

TatsumiM, TakahashiM, OhizumiY. Mechanism of palytoxin-induced [3H]norepinephrine release from a rat pheochromocytoma cell line. Mol Pharmacol, 1984, 253): 379-383 PMID: 6145092

[44]

YoshizumiY, NakanishiA, HouchiH, et al. . Characterization of palytoxin-induced catecholamine secretion from cultured bovine adrenal chromaffin cells. Effects of Na+- and Ca2+-channel blockers. Biochem Pharmacol, 1991, 42(1): 17-23 PMID: 1676886

[45]

SatohE, NakazatoY. Mode of action of palytoxin on the release of acetylcholine from rat cerebrocrtical synaptosomes. J Neurochem, 1991, 57(4): 1276-1280 PMID: 1680161

[46]

CrinelliR, CarloniE, GiaconiniE, et al. . Palytoxin and an Ostreopsis toxin extract increase the levels of mRNAs encoding inflammation-related proteins in human macrophages via p38 MAPK and NF-κB. PloS One, 2012, 7(6): e38139 PMCID: 3365899 PMID: 22675515

[47]

ItoK, UrakawaN, KoikeH. Cardiovascular toxicity of palytoxin in anesthetized dogs. Arch Intl de Pharmacod et de Ther, 1982, 258(1): 146-154

[48]

SosaS, Del FaveroG, De BortoliM, et al. . Palytoxin toxicity after acute oral administration in mice. Toxicol Lett, 2009, 191(2–3): 253-259 PMID: 19766704

[49]

ItoE, OhkusuM, YasumotoT. Intestinal injuries caused by experimental palytoxicosis in mice. Toxicon, 1996, 34(6): 643-652 PMID: 8817810

[50]

ItoE, YasumotoT. Toxicological studies on palytoxin and ostreocin-D administered to mice by three different routes. Toxicon, 2009, 54(3): 244-251 PMID: 19376151

[51]

RamosV, VasconcelosV. Palytoxin and analogs: biological and ecological effects. Mar Drugs, 2010, 8(7): 2021-2037 PMCID: 2920541 PMID: 20714422

[52]

FujikiH, SuganumaM, NakayasuM, et al. . Palytoxin is a non 12-O-tetradecanoylphorbol-13-acetate type tumor promotor in two-stage skin carcinogenesis. Carcinogenesis, 1986, 7(5): 707-710 PMID: 2870823

[53]

TeraoK, ItoE, YasumotoT. Light and electron microscopic observation of experimental palytoxin poisoning in mice. Bull Soc Pathol Exot, 1992, 85(5): 494-496 PMID: 1364106

[54]

Del FaveroG, BeltramoD, SciancaleporeM, et al. . Toxicity of palytoxin after repeated oral exposure in mice and in vitro effects on cardiomyocytes. Toxicon, 2013, 75(1): 3-15 PMID: 23770425

[55]

PelinM, SosaS, PacorS, et al. . The marine toxin palytoxin induces necrotic death in HaCaT cells through a rapid mitochondrial damage. Toxicol Lett, 2014, 229(3): 440-450 PMID: 25066017

[56]

TubaroA D, FaveroG, BeltramoD, et al. . Acute oral toxicity in mice of a new oalytoxin analog: 42-hydroxypalytoxin. Toxicon, 2011, 57(5): 755-763 PMID: 21333670

[57]

TubaroA, DurandoP D, FaveroG, et al. . Case definitions for human poisonings postulated to palytoxins exposure. Toxicon, 2011, 57(3): 478-495 PMID: 21255599

[58]

ForinoM, CiminielloP, FattorussoE, et al. . Palytoxins: a still haunting Hawaiian curse. Pytochem Rev, 2010, 9(4): 491-500

[59]

WattenbergEV, FujikiH, RosnerMR. Heterologous regulation of the epidermal growth factor receptor by palytoxin, anon-12-O-tetradecanoylphorbol-13-acetatetype tumor promoter. Cancer Res, 1987, 47(17): 4618-4622 PMID: 2887282

[60]

RumoreMM, HoustBM. Palytoxin poisoning via inhalation in pediatric siblings. Int J Case Rep Images, 2014, 5(7): 501-504

[61]

TubaroA, DurandoP, Del FaveroG, et al. . Case definitions for human poisonings postulated to palytoxins exposure. Toxicon, 2011, 57(3): 478-495 PMID: 21255599

[62]

HoffmannK, Hermanns-ClausenM, BuhlC, et al. . A case of palytoxin poisoning due to contact with zoanthid corals through skin injury. Toxicon, 2008, 51(8): 1535-1537 PMID: 18433818

[63]

AlcalaAC, AlcalaLC, GarthJS, et al. . Human fatality due to ingestion of the crab Demania reynaudii that contained a palytoxin-like toxin. Toxicon, 1988, 26(1): 105-107 PMID: 2894726

[64]

GranéliE, FerreiraCEL, YasumotoT, et al. . Sea urchins poisoning by the benthic dinoflagellate Ostreopsis ovata on the Brazilian coast. Book of Abstracts of Xth International Conference on Harmful Algae, 2002, Florida, St. Petersburg

[65]

FukuiM, MurataM, InoueA, et al. . Occurrence of palytoxin in the trigger fish Melichtys vidua. Toxicon, 1987, 25(10): 1121-1124 PMID: 2892288

[66]

OkanoH, MasuokaH, KameiS, et al. . Rhabdomyolysis and myocardial damage induced by palytoxin, a toxin of blue humphead parrotfish. Int Med, 1998, 37(3): 330-333

[67]

OnumaY, SatakeM, UkenaT, et al. . Identification of putative palytoxin as the cause of clupeotoxism. Toxicon, 1999, 37(1): 55-65 PMID: 9920480

[68]

BéressL, ZwickJ, KolkenbrockHJ, et al. . A method for the isolation of the caribbean palytoxin (C-PTX) from the coelenterate (zooanthid) Palythoa caribaeorum. Toxicon, 1983, 21(2): 285-290 PMID: 6134356

[69]

NordtSP, WuJ, ZahllerS, et al. . Palytoxin poisoning after dermal contact with Zoanthid coral. J Emerg Med, 2009, 40(4): 397-399 PMID: 19545971

[70]

VasconcelosV, RamosV. Palytoxin and analogs: Biological and ecological effects. Mar Drugs, 2010, 8(7): 2021-2037 PMCID: 2920541 PMID: 20714422

[71]

YoshimineK, OritaS, OkadaS, et al. . Two cases of parrotfish poisoning with rhabdomyolysis. Nippon Naika Gakkai Zasshi, 2001, 90(7): 1339-1341 PMID: 11519116

[72]

EFSA (European Food Safety Authority). Scientific opinion on marine biotoxins in shellfish-palytoxin group. EFSA J, 2009,1393:1–38

[73]

RhodesL, MundayR, BriggsL. Moestrup. Ostreopsis siamensis and palytoxin-related compounds in New Zealand: a risk to human health. Proceedings of the 12th International Conference on Harmful Algae, 2008, ISSHA and Intergovernmental Oceanographic Commision of UNESCO, Copenhagen, 326-329

[74]

MajlesiN, SuMK, ChanGM, et al. . A case of inhalation exposure to palytoxin. Clin Toxicol, 2008, 46(1): 673

[75]

WilesJ, VickJ, ChristensenM. Toxicological evaluation of palytoxin in several animal species. Toxicon, 1974, 12(4): 427-433 PMID: 4155146

[76]

MebsD. Occurrence and sequestration of toxins in food chains. Toxicon, 1998, 36(11): 1519-1522 PMID: 9792167

[77]

KaulPN, DaftariP. Marine pharmacology: bioactive molecules from the sea. Annu Rev Pharmacol Toxicol, 1986, 26(1): 117-142 PMID: 3521453

[78]

MahnirVM, KozlovskayaEP, KalinovskyAI. Sea anemone Radianthus macrodactylus—a new source of palytoxin. Toxicon, 1992, 30(11): 1449-1456 PMID: 1362473

[79]

WebberHH, RuggieriGD. Food-Drugs from the Sea. Proceedings of the Conference, 4th, Mayaguez, 1974, 1974, Marine Technology Soc, Washington, DC, 311

[80]

VickJA, WilesJS. The mechanism of action and treatment of palytoxin poisoning. Toxicol Appl Pharmacol, 1975, 34(2): 214-223 PMID: 1871

AI Summary AI Mindmap
PDF

139

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/