Marine Toxins. Origin, Structure, and Molecular Pharmacology

Special Issue on Marine Toxins
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Key words: Heteractis magnifica , marine toxin, hemolysin, cytolysin. The cnidarians comprise species of mostly marine aquatic invertebrates that constitute the phylum Cnidaria represented by sea anemones, corals, sea fans, sea pens, jellyfish and zooanthids, which are known to secrete a variety of cytolytic toxins mainly for defensive purposes Four major groups of these cytolysins are found in cnidarians 5, 6. Among them, the kDa pore-forming cytolysins are the most predominant However, Hmg III is the most potent and active cytolysin, whose molecular mass has been determined as 19 kDa The N-terminal amino acid sequences of Hmg III also exhibited homology with other sea anemone hemolysins such as equinatoxins from Actinia equina , tenebrosin-C from Actinia tenebrosa and cytolysin III from Stichodactyla helianthus Besides being known as a pore-forming cytolysin, Hmg III has not been further investigated on its physiological characteristics regarding the cytolytic activity.

Hence, the present study has been undertaken on the isolation, physiological characterization and purification of the cytolysin Hmg III from the sea anemone Heteractis magnifica employing a human erythrocyte model. Furthermore, the sequence verification has also been performed on this Indian sea anemone species and compared with a Singaporean species of which the sequence has been already known. The sequence comparison among cytolysins of other cnidarians - such as Stichodactyla helianthus , Heteractis crispa , Actinia equina and Oulactis orientalis - has also been performed by a phylogenetic analysis for establishing a genetic relationship.

Collection of the Sea Anemone Heteractis magnifica. The sea anemone Heteractis magnifica - identified by Fautin and Allen 22 - was collected from Andaman Islands, India, at a depth of 5 m by scuba diving. Preparation of the Toxin. In the laboratory, the live animal was induced through osmotic thermal stress to eject the epithelial mucus that contains the toxins 8. The cnidarian toxins are stored in the cnida, a capsule within specialized cells that contains a barbed, threadlike tube that delivers a paralyzing sting when propelled into attackers and prey.

After 15 minutes, the anemone was removed and the solution was filtered. The filtrate was stored in mL aliquots in liquid nitrogen for transportation. When required, the aliquots were thawed, concentrated by lyophilization and reconstituted in phosphate buffered saline at pH 7. Protein concentration was determined by the Lowry et al.

The protein concentration during purification studies was measured from the absorbance at nm. Human blood agar plate was prepared by adding 5 mL of human blood to 95 mL of sterile nutrient agar and pouring the mixture immediately on petri plates. After solidification, wells were cut on the agar plate using a corkscrew borer 8 mm diameter. The plates were observed for hemolysis after overnight incubation at room temperature.

Hemolytic activity of the toxin was measured quantitatively in terms of attenuance on human red blood cells at room temperature using a microplate reader. Freshly collected human blood with heparin was centrifuged to remove the buffy coat. Afterward, the obtained erythrocytes RBC were washed three times in 0. Characterization of the Hemolytic Extract. The crude hemolytic extract was characterized with respect to thermal and pH stability, freeze-thaw stability and treatment with human serum.


Effect of temperature and freeze-thaw process. The freeze-thaw procedure was repeated three times and the hemolytic activity was assessed. The buffer pH of the extract was 9 and was adjusted to 3, 4, 5, 6, 7 and 8 with hydrochloric acid HCl , then, incubated for one hour at room temperature and assayed. Effect of human serum. The mixtures were assessed for hemolytic activity against human RBC, with serum-free extract as control.

Ammonium Sulfate Precipitation. The precipitates were resuspended in 10 mM sodium phosphate buffer pH 7. The dialyzed fractions were purified by ion-exchange chromatography. The column-stabilizing buffer was 10 mM sodium phosphate buffer, pH 7. Elution of the bound proteins was performed using a linear gradient of sodium chloride 0. The dialyzed fractions were subjected to cation-exchange chromatography using CM-cellulose column and a similar method previously described in this study. Total RNA was isolated from the tentacles of the sea anemone H. The quality of the RNA preparation was determined by electrophoresis in agarose gel 1.

One microgram of H. Primer sequences were obtained according to Wang et. The PCR product was electrophoresed on 1. The PCR band was excised from the agarose gel and eluted and purified using a gel elution kit Eppendorf, Germany according to the manufacturer's protocol. The purified PCR product was sequenced. The hemolytic activity of the crude extract is shown in the Figure 1. A 6-mm diameter clear zone of lysis was observed around the wells in human blood agar plates when 50 mg of crude extract was added after incubation Figure 1. The hemolysis induced by hemolysins in red blood cells suspension was concentration-dependent Figure 2.

Physiological Properties. The pI of this toxin ranges from 9. Therefore, its activity in in vitro conditions has also been assumed to occur at this high pH level. Hence, hemolysis was favored in an alkaline pH Figure 3 - B whereas activity was reduced in acidic medium. Precipitation of Hemolytic Toxin. Table 1 shows the relative distribution of the hemolytic activity of H.

All the fractions obtained during salting out process showed hemolytic activity, which indicates that the toxin was precipitated in all fractions Table 1. SDS-PAGE analysis of ammonium sulfate precipitated fractions possessing cytolytic activity revealed the presence of a protein band with a molecular weight of 19 kDa Figure 4. Toxin Purification by Ion-Exchange Chromatography. The fractionation of the ammonium sulfate precipitated crude extract of H. Peak A fractions were found to exhibit hemolytic activity. Dialyzed fractions were lyophilized and purified by carboxymethyl-cellulose CM cation-exchange chromatography.

The result reveals the presence of the 19 kDa pore-forming cytolysin in the purified fractions. One hundred micrograms of RNA were extracted from mg of tissue. The purified PCR product was sequenced accession n. The present study demonstrated the hemolytic activity of a cytolysin isolated from the sea anemone H. Additionally, this study included cDNA amplification which enabled comparison of the conserved region of this cytolysin with others. The nucleotide sequence of H. The intoxication is usually not fatal. Onset is rapid and symptoms subside within a few hours or days at most.

There is no antidote. The symptoms appear to be due to two brevetoxins produced by G. They may be analyzed chemically, but this is not done routinely. Identification of a dangerous condition is readily made by observation of red tide conditions, including characteristic fish kills, and of the organisms themselves in the water. Local authorities then routinely close shellfish harvesting to industries and the public. Diarrhetic shellfish poisoning is caused by ingestion of mussels, scallops, or clams that have been feeding on Dinophysis fortii or D.

There have been no confirmed outbreaks in the United States, but the disease is common in Japan and has become a problem in Europe. One confirmed DSP episode occurred in Canada in Symptoms include diarrhea, nausea, vomiting, and abdominal pain. Onset occurs from 30 minutes to a few hours after eating toxic shellfish, and the duration is usually short with a maximum of a few days in severe cases. The disease is not life threatening Yasumoto et al. At least five toxins have been isolated from dinoflagellates and shellfish. Okadaic acid is most commonly encountered in Europe where D.

There is a mouse bioassay for the toxins. For the U. Shellfish should be imported only from countries with whom the United States has a memorandum of understanding MOU. Testing for shellfish toxins should be part of the general practice under the MOU. Nevertheless, because Dinophysis does occur in U. Puffer fish poisoning results from ingestion of the flesh of certain species of fish belonging to the Tetraodontidae Halstead, The toxin involved is called tetrodotoxin and was originally believed to be a true ichthyosarcotoxin produced by the fish itself.

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Accessed March 12, Login or Register to save! The histamine is produced in the fish flesh by decarboxylation of free histidine, which is naturally present at high levels in species of fish implicated in scombroid fish poisoning Lukton and Olcott, Expert Opin Pharmacother ; More statistics for editors and authors Login to your personal dashboard for more detailed statistics on your publications. Hemolytic activity of the toxin was measured quantitatively in terms of attenuance on human red blood cells at room temperature using a microplate reader. Murakami, T.

The toxicity of poisonous puffers fluctuates greatly Halstead, Recent observations that cultured puffer fish are atoxic has supported a food chain origin for the toxin, but this has not yet been confirmed Mosher and Fuhrman, It has recently been shown, however, that certain common marine vibrios can produce a form of the toxin Narita et al. Puffer fish poisoning has not been reported in mainland United States in recent years, but incidents were reported in the past.

Seven cases were reported in Florida between and , including three fatalities Benson, ; Hemmert, They appear to have been caused by the consumption of locally caught species of Sphoeroides. The common puffer fish, Arothron hispidus , has been implicated in at least seven fatalities in Hawaii HDH, There are deaths from fugu poisoning in Japan each year, where various species of puffer fish are eaten as a delicacy; this occurs despite very stringent controls imposed by Japanese authorities on the marketing and restaurant preparation of the dish Ogura, The symptoms of puffer fish poisoning are similar to those described for paralytic shellfish poisoning, including initial tingling and numbness of lips, tongue, and fingers leading to paralysis of the extremities; ataxia; difficulty in speaking; and finally, death by asphyxiation due to respiratory paralysis.

Nausea and vomiting are common early symptoms. The similarity in symptoms is not surprising because tetrodotoxin, although chemically different from the saxitoxins, also blocks sodium channels. The toxicity of tetrodotoxin is similar to that of saxitoxin, and mg constitutes a lethal dose for humans. There is disagreement concerning the toxicity of U. Atlantic puffer fish.

However, Hemmert shows a table indicating that the viscera, skin, and some flesh of S. Larson et al. The species Arothron hispidus has been implicated in at least seven fatalities in Hawaii. The wholesaling, preparation, and selling of puffers as food in Japan, even under the most rigid public health conditions by trained and certified puffer cooks, has not eliminated the danger of eating these fish.

The fugu puffer still remains a major cause of fatal food intoxications in Japan. In brief, eating poisonous puffers is at best a game of Russian roulette. All of the U. There are too many variables in the puffer business, and sale of these should be prohibited in the United States. This subject has been documented and discussed at great length by Halstead , In view of these reports, it would seem prudent to exclude puffer fish, whether domestic or imported, from U. Even though very strict requirements have been imposed in an attempt to ensure that the fish are nontoxic, the continuing Japanese experience should raise questions concerning the safety of this process for the U.

Amnesic shellfish poisoning has been proposed by Todd as a name for the syndrome caused by domoic acid. This severe disease has been identified only in a series of outbreaks in Canada in November and December involving people. The toxin is present in some varieties of the diatom Nitzschia pungens and accumulated in mussels and clams in Atlantic Canada during a period of blooms of the diatom. Symptoms included vomiting, abdominal cramps, diarrhea, disorientation, and memory loss Perl et al.

Short-term memory loss was the most persistent symptom and lasted over a year in several cases. Autopsies on three fatalities showed necrosis of the hippocampus. The disease is particularly severe among older people, some of whom died in the Canadian outbreak. Clearly, this is a toxin to be considered in U. Nitzschia pungens and N. States in the northeastern United States are now testing mussels for domoic acid.

There are sporadic reports of other intoxications from seafoods from time to time Halstead, ; Wekell and Liston, , but these have not been investigated sufficiently to identify the toxic agent. As noted earlier, the somewhat variable symptoms defined as ciguatera and the reported association of polyether substances and palytoxin Hokama et al. One well-defined syndrome reported to occur in Hawaii is "hallucinogenic fish poisoning.

Hallucinations, insomnia, intense dreaming, weakness, and burning of the throat are common soon after eating the fish Halstead and Schantz, Terrifying nightmares have been reported and constrictive chest pains occur. The condition is short-lived and self-resolving Halstead, ; HDH, There does not seem to be any analytical test for this toxin. Diseases caused by natural fish poisoning are listed in Table Three of these are of direct significance to the U. Of these three, PSP, which has potentially the most severe health consequences, is well controlled by state surveillance and harvest closure practices.

Ciguatera, for which the largest number of cases is reported, has a major public health impact in Hawaii, Guam, and Caribbean island communities and a small effect in Florida. Prevention of ciguatera can be ensured only by interdiction of the supply of potentially toxic tropical reef fish to the U. This is theoretically possible through banning imports to the U. Such action would probably be unacceptable in the island states and possessions, where local fishing provides essential employment and is closely tied to the tourist industry.

Furthermore, blanket rejection of such species as groupers, which are mostly nontoxic, would greatly reduce consumer choice and adversely affect the income of fishermen and others in areas remote from the toxin problem. Fortunately, current research at the University of Hawaii provides good promise of early development of a simple reliable test for ciguatoxic fish. Such a test is urgently needed to enable selective rejection of toxic fish by testing either on board the fishing vessel or at dockside.

On a longer-term basis, research should be directed toward the prediction of developing toxic conditions so that closure of fishing areas can be applied before human intoxications occur. Scombroid fish poisoning is unquestionably a consequence of improper handling or processing of certain types of fish. Control of this hazard at the commercial level can be ensured, to a reasonable degree, by proper application of temperature control in handling and processing fish with known high content of free histidine. Where uncertainty exists concerning the quality of primary handling, as for some imported fish, reliable analytical tests may be used to determine whether fish or fish products exceed the limit for histamine content used by FDA.

There seems to be no easy solution to the problem of recreationally caught fish mostly tuna and bluefish because it is unlikely that a mandatory inspection and testing program could be imposed. Education on proper fish handling to avoid the hazard and warnings issued by states to their recreational anglers and to businesses supporting such activity charter boats, gear suppliers, etc. The other intoxications discussed in this chapter are rare and apparently under control in the United States e.

Nevertheless, agencies responsible for ensuring the safety of the U. Appropriate tests should be sought and laboratories prepared for their use. Importers should be required to ensure that seafood products from countries where such intoxications have occurred are not toxic. This is best done by controlling imports through an MOU that would include provisions for toxicity testing. Organoleptic inspection systems have little value in protecting the consumer from seafood intoxications.

Toxic fish and shellfish usually look and smell perfectly normal. Protection of the consumer requires a multifaceted approach involving industry practices and regulations, control of harvest and distribution, and as a last resort, testing, seizure, and detention. This requires action by states and local authorities from different departments e. In the final analysis the most effective measure is likely to be education of the fish-eating public about which fish and shellfish may be naturally toxic.

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Except for scombroid poisoning, toxicity is a function of the normal feeding habits of wild animals and cannot be controlled. Thus, potentially toxic fish may enter the food supply. Fortunately, the serious life-threatening intoxications are controllable so that most incidents of fish poisoning are of short duration and are self-resolving. Nevertheless, research aimed at the detection and elimination of toxic fish from the food supply and at methods of treatment for intoxications such as ciguatera that can have long-lasting and even disabling effects should be encouraged.

There is a need for educational materials to be made available to the fishing industry, public health workers, divers, and sports fishers. A number of popular handbooks have been published dealing with the potential health hazards caused by marine organisms Halstead, , ; Halstead et al. However, much of this information does not reach regulatory, clinical public health, and poison control centers Freudenthal, In dealing with this subject matter, it is essential that the educational materials be fully illustrated, preferably in color.

More charts and informational pamphlets are required. Toxic dinoflagellates: Gonyaulax catenella Pacific ; G. Numbness, paralysis after eating; death hours; prognosis good after 24 hours. Abdominal pain, nausea, vomiting, severe diarrhea within 4 hours after eating; rarely fatal. Feeling of nausea from red tide spray, symptoms like ciguatera from eating bivalves.

Itching, redness, allergic symptoms, headache, dizziness, diarrhea, peppery taste. Vomiting, cramps, diarrhea, memory loss and disorientation; memory loss has lasted a year.

Remarks: In most cases toxic shellfish are not detectable by organoleptic means. It is therefore important that practical chemical or biological tests, specific for the detection of the toxins, be developed. Although not all the listed diseases are problems in the United States, seafood inspectors and processors should always be aware that toxigenic dinoflagellates, or other microorganisms producing toxins that get into fish and shellfish, may become established in areas where fish and shellfish are harvested for U.

An example: diarrhetic shellfish poisoning is not a problem in the United States, but the dinoflagellate that produces the toxin may become established in shellfish areas that supply U. Fish of species reported by health authorities to have caused ciguatera, which are to be imported to the United States from regions of high ciguatera incidence, should carry certification of nontoxicity. States and territories in which ciguatera is a problem should license marine sports fishers and, at the point of issuance of the license, issue clear and specific warnings regarding the dangers of ciguateric fish.

Pamphlets on poisonous fish should be generally available to the public in areas where ciguatera is endemic. When feasible, reef fishing should be closed in areas where ciguatoxic fish are present. This closure should apply to sports fishers as well as to commercial vessels. Research should be accelerated on the development of simple, rapid tests for toxicity such as the Hokama stick test.

Research should also be directed toward analysis of the events leading to the appearance of toxic fish in particular reef environments, with the objective of developing predictive indices that can be used to close areas to fishing before human intoxications occur. This should be controlled by routine lot testing. Similar temperature records should be maintained for such species during processing and shipment on land. Advisory leaflets describing the causes of scombroid poisoning and providing advice on how to handle fish to minimize risk of the disease should be made widely available to sports fishers who target potentially scombrotoxic species.

Research to develop a rapid field test for PSP toxicity in shellfish should be strongly encouraged and supported. Such a test could be applied directly by commercial growers and recreational shellfish gatherers. Nevertheless, state agencies should continue to monitor the PSP condition of local shellfish. The consumption of puffer fish should be strongly discouraged, and their importation to the United States should be banned.

Regulatory agencies should maintain awareness of potential toxin problems, such as diarrhetic shellfish poisoning and amnesic shellfish poisoning, and their technical personnel should be trained and equipped to run definitive analyses on these and other toxins. Shellfish should be imported only under an MOU that includes a provision for toxicity testing.

In view of the complexity of seafood intoxications, the federal government should establish or support two to three centers of research into such toxins to enlarge understanding of the phenomena, provide possible remedies, and develop particular tests. Because of the highly localized impact, primary responsibility for control of seafood toxins should reside at the state level, with funding, quality control, and specialist assistance from a federal seafood safety agency.

The toxigenic strains have also been designated Protogonyaulax , and more recently, the genus name Alexandrium has been proposed. Anderson, B. Sims, N. Wiebenga, and M. The epidemiology of ciguatera fish poisoning in Hawaii Arnold, S. Price, and W. Histamine formation by bacteria isolated from skipjack tuna, Katsuwonas pelamis. Fish Williams, ed. Baden, D. Mende, M. Poli, and R. Toxins from Florida's red tide dinoflagellate Ptychodiscus brevis.

Ragelis, ed. Seafood Toxins. American Chemical Society, Washington, D. Bagnis, R. Kuberski, and S. Clinical observations on cases of ciguatera fish poisoning in the South Pacific. Chanteau, E. Chungue, J. Hurtel, T. Yasumoto, and A. Origins of ciguatera fish poisoning: A new dinoflagellate Gambierdiscus toxicus Adachi and Fukuyo, definitely involved as a causal agent.

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Marine Toxins: Origin, Structure, and Molecular Pharmacology. Anal. Chem., , 62 (13), pp A–A. DOI: /aca Origin, Structure, and Molecular Pharmacology. M. Joan Comstock, Series Editor. pp i-iv. DOI: /bkfw First Page.

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Review Articles

Kodama, A. Hokama, T. Yasumoto, M. Fukui, S. Manea, and N. Clinical and laboratory findings implicating palytoxin as cause of ciguatera poisoning due to Decapterus macrosoma mackerel. Lalone, R. DeVillez, and E. An assay of the toxicity of the Atlantic puffer fish Sphoeroides maculatus. Lange, W. Kreider, M. Hattwick, and J. Potential benefit of tocainide in the treatment of ciguatera: Report of three cases.

Larson, E. Rivas, R. Lalone, and S. The Pharmacologists Abstract. Lalone, and L. Comparative toxicity of the Atlantic pufferfishes of the genera Sphoeroides, Lactophrys, Lagocelhalus and Chilomycterus. Lawrence, D. Enriquez, R. Lumish, and A. Ciguatera fish poisoning in Miami. Legrand, A. Mode of action of ciguatera toxins. Lukton, A. Content of free imidazole compounds in the muscle tissue of aquatic animals. Food Res. Miller, M. Ciguatera Seafood Toxins. Morris, J. Lewin, N.

Hargrett, C. Smith, P. Blake, and R. Clinical features of ciguatera fish poisoning: A study of the disease in the U. Lewin, C. Ciguatera fish poisoning: Epidemiology of the disease on St. Thomas, U. Mosher, H. Occurrence and origin of tetrodotoxin. Murata, M. Legrand, Y. Ishibashi, M. Fukui, and T. Structures and configurations of ciguatoxin from the moray eel Gymnothorax javanicus and its likely precursor from the dinoflagellate Gambierdiscus toxicus.

Narita, H. Matsubara, N. Miwa, S. Akahane, M. Murakami, T. Goto, M. Nara, T. Noguchi, T. Shida, and K. Vibrio alginolyticus a TTX-producing bacterium isolated from the starfish Astropecten polyacanthus. Nippon Suisan Gakk. Nishitani, L. Ogura, Y. Fugu puffer fish poisoning and the pharmacology of crystalline tetrodotoxin in poisoning. Simpson, ed. Neuropoisons, Vol.

Plenum Press, New York. Palafox, N. Jain, A. Pinano, T. Gulick, R. Williams, and I. Perl, T. Kosatsky, J. Hockin, E. Todd, and R. An outbreak of toxic encephalopathy caused by eating mussels contaminated with domoic acid. Ragelis, E. Ciguatera seafood poisoning: An overview. Randall, J. A survey of ciguatera at Eniwetok and Bikini Marshall Islands, with notes on the systematics and food habits of ciguatoxic fish. Fish Bull. Ruff, T. Ciguatera in the Pacific: A link with military activities.

Lancet Schantz, E. Seafood toxicants.

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National Academy Press, Washington, D. Chemistry and biology of saxitoxins and related toxins.