The FISH VENOM TOXINS: NATURAL SOURCE OF PHARMACEUTICALS AND THERAPEUTIC AGENTS “PHARMACEUTICAL AND THERAPEUTIC USES OF FISH VENOM TOXINS
DOI:
https://doi.org/10.22159/ijpps.2020v12i11.38215Keywords:
Fish toxin, Envenomation, Pharmaceutical activity, Bio-pesticides, Anti-venom therapyAbstract
The present review article explains fish toxins from different species with their pharmaceutical and therapeutic uses. Fish stinging is a major problem in coastal areas as it exerts severe toxic effects mainly in fishermen, locals, and tourists. Fish toxins cause severe pain that radiates up in the limbs and regional lymphatics. These also impose venular stasis, hemorrhage and make changes in the arteriolar wall diameter. Fish toxins target ion-channels, ligand-gated channels and G-protein coupled receptors present in body cells and obstructs their physiological and metabolic functions. They affect molecules that participate in signaling pathways, and cause hemolytic, cardiovascular, and make obstruction in nerve function and smooth muscle contraction. For quick neutralization, fish venom-induced effects in victim’s toxin-specific antibodies are used. These quickly provide relief from pain, minimize the symptoms, and stop the immediate inflammatory reaction. Fish venom toxins are of wider biomedical applications and can be used for the preparation of immune diagnostics, bio-pesticides, anticancer agents, and analgesics by using its biological information.
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References
Church JE, Hodgson WC. The pharmacological activity of fish venoms. Toxicon 2002;40:1083-93.
Halstead BW. Poisonous and venomous marine animals of the world. Vol 3. Washington, DC: U. S. Government Printing Office; 1970.
Halstead BW. Poisonous and venomous marine animals of the world. 2nd ed. Princeton NJ: The Darwin Press; 1988.
Hardman M. The phylogenetic relationships among extant catfishes, with special reference to Ictaluridae (Otophysi: Siluriformes) (Ph. D. dissertation). Urbana-Champaign, IL: University of Illinois; 2002. p. 1–206.
Nelson G. Phylogeny of major fish groups, in the hierarchy of life: molecules and morphology in phylogenetic analysis (Fernholm B, Bremer K, Jornvall. eds) Amsterdam, the Netherlands: Excerpta Medica; 1989. p. 325–36.
Nelson JS. Fishes of the World. 3rd Ed. New York: John Wiley and Sons; 1994.
Smith WL, Wheeler WC. Polyphyly of the mail-cheeked fishes (Teleostei: Scorpaeniformes): evidence from mitochondrial and nuclear sequence data. Mol Phylogenet Evol 2004;32:627-46.
Smith Vaniz WF, Satapoomin U, Allen GR. Meiacanthus urostigma, a new fang blenny from the northeastern Indian Ocean, with discussion and examples of mimicry in species of Meiacanthus (Teleostei: Blenniidae: Nemophini). Aqua J Ichthyol Aquat Biol 2001;5:25-3.
Smith WL, Wheeler WC. Venom evolution widespread in fishes: a phylogenetic road map for the bioprospecting of piscine venoms. J Hered 2006;97:206-17.
Haddad V, Jr Martins IA. Frequency and gravity of human envenomations caused by marine catfish (suborder siluroidei): a clinical and epidemiological study. Toxicon 2006;47:838-43.
Haddad V, Martins IA, Makyama HM. Injuries caused by scorpionfishes (Scorpaena plumieri Bloch, 1789 and Scorpaena brasiliensis Cuvier, 1829) in the Southwestern Atlantic Ocean (Brazilian coast): Epidemiologic, clinic, and therapeutic aspects of 23 stings in humans. Toxicon 2003;42:79-3.
O’Connor JM, Hahn ST. An epidemiological study of bullrout (Notesthes robusta) envenomation on the north coast of NSW. Aust Emerg Nurs J 2001;4:16-8.
Muirhead D. Applying pain theory in fish spine envenomation. SPUMS; 2002.
Zhang H, Gao S, Lercher MJ, Hu S, Chen WH. Evol view, an online tool for visualizing, annotating, and managing phylogenetic trees. Nucleic Acids Res 2012;40:569-72.
Hardman M. The phylogenetic relationships among extant catfishes, with special reference to Ictaluridae (Otophysi: Siluriformes) (Ph. D. dissertation). Urbana-Champaign, IL: University of Illinois; 2002.
Halstead BW, Chitwood MJ, Modglin FR. The anatomy of the venom apparatus of the zebrafish, Pterois volitans (Linnaeus). Anat Rec 1955;122:317-33.
Chitwood BW, Modglin MJ, Modglin FR. Stonefish stings, and the venom apparatus of Synanceja horrida (Linnaeus). Trans Am Microsc Soc 1956;75:381-97.
Halstead BW, Chitwood MJ, Modglin FR. The venom apparatus of the California scorpionfish, Scorpaena guttata Girard. Trans Am Microsc Soc 1955;74:145-58.
Fishelson L. Histology and ultrastructure of the recently found buccal toxic gland in the fish Meiacanthus nigrolineatus (Blenniidae). Copeia 1974;2:386-92.
Harris RJ, Jenner RA. Evolutionary ecology of fish venom: adaptations and consequences of evolving a venom system. Toxins (Basel) 2019;11:60.
Ortiz E, Gurrola GB, Schwartz EF, Possani LD. Scorpion venom components as potential candidates for drug development. Toxicon 2015;93:125-35.
Wright JJ. Diversity, phylogenetic distribution, and origins of venomous catfishes. BMC Evol Biol 2009;9:282.
Church JE, Hodgson WC. The pharmacological activity of fish venoms. Toxicon 2002;40:1083-93.
King G. Venoms to drugs: venom as a source for the development of human therapeutics; Royal Society of Chemistry: London, UK; 2015.
Garnier P, Goudey Perriere F, Breton P, Dewulf C, Petek F, Perriere C. Enzymatic properties of the stonefish (Synanceia verrucosa Bloch and Schneider, 1801) venom and purification of a lethal, hypotensive and cytolytic factor. Toxicon 1995;33:143-55.
Garnier P, Sauviat MP, Goudey Perriere F, Perriere C. Cardiotoxicity of verrucotoxin, a protein isolated from the venom of Synanceia verrucosa. Toxicon 1997;35:47-5.
Yazawa K, Wang JW, Hao LY, Onoue Y, Kameyama M. Verrucotoxin, a stonefish venom, modulates calcium channel activity in guinea-pig ventricular myocytes. Br J Pharmacol 2007;151:1198-203.
Garnier P, Ducancel F, Ogawa T, Boulain JC, Goudey Perriere F, Perriere C, et al. Complete amino-acid sequence of the α-subunit of VTX from venom of the stonefish (Synanceia verrucosa) as identified from cDNA cloning experiments. Biochim Biophys Acta 1997;1337:1-5.
Poh C, Yuen R, Khoo H, Chung M, Gwee M, Gopalakrishnakone P. Purification and partial characterization of stonustoxin (lethal factor) from Synanceja horrida venom. Comp Biochem Physiol B: 19 Comp Biochem 1991;99:793-8.
Ghadessy FJ, Chen D, Kini RM, Chung MC, Jeyaseelan K, Khoo HE, et al. Stonustoxin is a novel lethal factor from stonefish (Synanceja horrida) venom cDNA cloning and characterization. J Biol Chem 1996;271:25575-81.
Ueda A, Suzuki M, Honma T, Nagai H, Nagashima Y, Shiomi K. Purification, properties and cDNA cloning of neoverrucotoxin (neoVTX), a hemolytic lethal factor from the stonefish Synanceia verrucosa venom. BBA-Gen Subj 2006;1760:1713-22.
Khoo H, Hon W, Lee S, Yuen R. Effects of stonustoxin (lethal factor from Synanceja horrida venom) on platelet aggregation. Toxicon 1995;33:1033-41.
Khoo H, Chen D, Yuen R. Role of free thiol groups in the biological activities of stonustoxin, a lethal factor from stonefish (Synanceja horrida) venom. Toxicon 1998;36:469-76.
Chen D, Kini R, Yuen R, Khoo H. Haemolytic activity of stonustoxin from stonefish (Synanceja horrida) venom: pore formation and the role of cationic amino acid residues. Biochem J 1997;325:685-91.
Garnier P, Grosclaude JM, Goudey Perriere F, Gervat V, Gayral P, Jacquot C, et al. Presence of norepinephrine and other biogenic amines in stonefish venom. J Chromotogr B: Biomed 1996;685:364–9.
Khoo H, Chen D, Yuen R. The role of cationic amino acid residues in the lethal activity of stonustoxin from stonefish (Synanceja horrida) venom. IUBMB Life 1998;44:643-6.
Yuen R, Cai B, Khoo H. Production and characterization of monoclonal antibodies against stonustoxin from Synanceja horrida. Toxicon 1995;33:1557-64.
Low KS, Gwee ME, Yuen R, Gopalakrishnakone, Khoo H. Stonustoxin: a highly potent endothelium-dependent vasorelaxant in the rat. Toxicon 1993;31:1471-8.
Liew H, Khoo H, Moore P, Bhatia Lu, J Moochhala S. Synergism between hydrogen sulfide (H2S) and nitric oxide (NO) in vasorelaxation induced by stonustoxin (SNTX), a lethal and hypotensive protein factor isolated from stonefish Synanceja horrida venom. Life Sci 2007;80:1664-8.
Colasante C, Meunier FA, Kreger A, Molgo J. Selective depletion of clear synaptic vesicles and enhanced quantal transmitter release at frog motor nerve endings produced by trachynilysin, a protein toxin isolated from stonefish (Synanceia trachynis) venom. Eur J Neurosci 1996;8:2149-56.
Sauviat MP, Meunier FA, Kreger A, Molgo J. Effects of trachynilysin, a protein isolated from stonefish (Synanceia trachynis) venom, on frog atrial heart muscle. Toxicon 2000;38:945-59.
Meunier FA, Mattei C, Chameau P, Lawrence G, Colasante C, Kreger A, et al. Trachynilysin mediates SNARE-dependent release of catecholamines from chromaffin cells via external and stored Ca2+. J Cell Sci 2000;113:1119-25.
Ouanounou G, Malo M, Stinnakre J, Kreger A, Molgo J. Trachynilysin, a neurosecretory protein isolated from stonefish (Synanceia trachynis) venom, forms nonselective pores in the membrane of NG108–15 cells. J Biol Chem 2002;277:39119-27.
Andrich F, Carnielli J, Castle J, Lautner R, Santos R, Pimenta A, et al. A potent vasoactive cytolysin isolated from Scorpaena plumieri scorpionfish venom. Toxicon 2010;56:487-96.
Gomes HL, Andrich F, Fortes Dias CL, Perales J, Teixeira Ferreira A, Vassallo DV, et al. Molecular and biochemical characterization of a cytolysin from the Scorpaena plumieri (scorpionfish) venom: evidence of pore formation on the erythrocyte cell membrane. Toxicon 2013:74:92-100.
Nagasaka K, Nakagawa H, Satoh F, Hosotani T, Yokoigawa K, Sakai H, et al. A novel cytotoxic protein, Karatoxin, from the dorsal spines of the redfin velvetfish, Hypodytes rubripinnis. Toxin Rev 2009;28:260–5.
Rebekah Ziegman, Paul Alewood. bioactive components in fish venoms. Toxins (Basel) 2015;7:1497-31.
Shinohara M, Nagasaka K, Nakagawa H, Edo K, Sakai H, Kato K, et al. A novel chemoattractant lectin, karatoxin, from the dorsal spines of the small scorpionfish Hypodytes rubripinnis. J Pharmacol Sci 2010;113:414-7.
Fabiana V Campos, Thiago N Menezes, Pedro F Malacarne, Fabio LS Costa, Gustavo B Naumann, Helena L Gomes, et al. A review on the Scorpaena plumieri fish venom and its bioactive compounds. J Venom Anim Toxins Incl Trop Dis 2016;22:35.
Abe T, Sumatora M, Hashimoto Y, Yoshihara J, Shimamura Y, Fukami J. Purification and properties of a cardioactive toxin, cardioleputin, from stonefish, Synanceja verrucosa. J Venom Anim Toxins 1996;2:135-49.
De Santana, Evangelista K, Andrich F, de Rezende FF, Niland S, Cordeiro MN, Horlacher T, Castelli R, Schmidt Hederich A, Seeberger PH, Sanchez EF. Plumieribetin, a fish lectin homologous to mannose-binding B-type lectins, inhibits the collagen-binding α1β1 integrin. J Biol Chem 2009;284:34747-59.
Chhatwal I, Dreyer F. Isolation and characterization of dracotoxin from the venom of the greater weever fish Trachinus draco. Toxicon 1992;30:87-93.
Perriere C, Goudey Perriere F, Petek F. Purification of a lethal fraction from the venom of the weever fish, Trachinus vipera CV. Toxicon 1988;26:1222–7.
Chhatwal I, Dreyer F. Biological properties of a crude venom extract from the greater weever fish Trachinus draco. Toxicon 1992;30:77-85.
Karmakar S, Muhuri D, Dasgupta S, Nagchaudhuri A, Gomes A. Isolation of a hemorrhagic protein toxin (SA-HT) from the Indian venomous butterfish (Scatophagus argus) sting extract. Indian J Exp Biol 2004;42:452-60.
Karla de Santana Evangelista, Filipe Andrich, Flavia Figueiredo de Rezende, Stephan Niland, Marta N Cordeiro, Tim Horlacher, et al. Plumieribetin, a fish lectin homologous to mannose-binding b-type lectins, inhibits the collagen-binding α1β1. Integrin J Biol Chem 2009;284:34747-59.
Andrich F, Richardson M, Naumann G, Cordeiro M, Santos A, Santos D, et al. Identification of C-type isolectins in the venom of the scorpionfish Scorpaena plumieri. Toxicon 2015;95:67-71.
Sosa Rosales JI, Piran Soares AA, Farsky SH, Takehara HA, Lima C, Lopes-Ferreira M. Important biological activities induced by Thalassophryne maculosa fish venom. Toxicon 2005;45:155-61.
Lopes Ferreira M, Magalhaes GS, Fernandez JH, Junqueira de Azevedo, IDLM, le Ho P, et al. Structural and biological characterization of Nattectin, a new C-type lectin from the venomous fish Thalassophryne nattereri. Biochimie 2011;93:971-80.
Komegae EN, Ramos A, D Oliveira AK, de Toledo Serrano SM, Lopes Ferreira M, Lima C. Insights into the local pathogenesis induced by fish toxins: Role of natterins and nattectin in the disruption of cell-cell and cell-extracellular matrix interactions and modulation of cell migration. Toxicon 2011;58:509-17.
Ramos AD, Conceicao K, Silva PI Jr, Richardson M, Lima C, Lopes Ferreira M. Specialization of the sting venom and skin mucus of Cathorops spixii reveals functional diversification of the toxins. Toxicon 2012;59:651–65.
Auddy B, Muhuri DC, Alam MI, Gomes A. A lethal protein toxin (toxin-PC) from the Indian catfish (Plotosus canius, Hamilton) venom. Nat Toxins 1995;3:363-8.
Tamura S, Yamakawa M, Shiomi K. Purification, characterization and cDNA cloning of two natterin-like toxins from the skin secretion of oriental catfish Plotosus lineatus. Toxicon 2011;58:430-8.
Primor N, Tu AT. Conformation of pardaxin, the toxin of the flatfish Pardachirus marmoratus. Biochim Biophys Acta 1980;626:299-6.
Primor N, Lazarovici P. Pardachirus marmoratus (Red Sea flatfish) secretion and its isolated toxic fraction pardaxin: the relationship between hemolysis and ATPase inhibition. Toxicon 1981;19:573-8.
Primor N. Pardaxin produces postjunctional muscle contraction in guinea-pig intestinal smooth muscle. Br J Pharmacol 1984;82:43 9.
Shai Y, Fox J, Caratsch C, Shih YL, Edwards C, Lazarovici P. Sequencing and synthesis of pardaxin, a polypeptide from the red sea moses sole with ionophore activity. FEBS Lett 1988;242:161-6.
Shiomi K, Takamiya M, Yamanaka H, Kikuchi T, Suzuki Y. Toxins in the skin secretion of the oriental catfish (Plotosus lineatus): immunological properties and immunocytochemical identification of producing cells. Toxicon 1988;26:353-61.
Katia Conceicao, Katsuhiro Konno, Robson L Melo, Elineide Marques, Clelia A Hiruma Lima, Carla Lima Orpotrin. A novel vasoconstrictor peptide from the venom of the brazilian stingray potamotrygon gr. Orbignyi Peptides 2007;27:3039-46.
Conceicao K, Santos JM, Bruni FM, Klitzke CF, Marques EE, Borges MH, et al. Characterization of a new bioactive peptide from Potamotrygon grorbignyi freshwater stingray venom. Peptides 2009;30:2191-9.
Sri Balasubashini M, Karthigayan S, Somasundaram S, Balasubramanian T, Viswanathan V, et al. Fish venom (Pterios volitans) peptide reduces tumor 55 burden and ameliorates oxidative stress in Ehrlich’s ascites carcinoma xenografted mice. Bioorg Med Chem Lett 2006;16:6219–25.
Carlisle D. On the venom of the lesser weeverfish, Trachinus vipera. J Mar Biol Assoc UK 1962;42:155-62.
Hopkins BJ, Hodgson WC, Sutherland SK. An in vitro pharmacological examination of venom from the soldierfish Gymnapistes marmoratus. Toxicon 1997;35:1101-11.
Kaji T, Sugiyama N, Ishizaki S, Nagashima Y, Shiomi K. Molecular cloning of grammistins, peptide toxins from the soapfish Pogonoperca punctata, by hemolytic screening of a cDNA library. Peptides 2006;27:3069-76.
Sugiyama N, Araki M, Ishida M, Nagashima Y, Shiomi K. Further isolation and characterization of grammistins from the skin secretion of the soapfish Grammistes sexlineatus. Toxicon 2005;45:595-1.
Garnier P, Grosclaude JM, Goudey Perriere F, Gervat V, Gayral P, Jacquot C, et al. Presence of norepinephrine and other biogenic amines in stonefish venom. J Chromotogr B Biomed 1996;685:364-9.
Hopkins BJ, Hodgson WC, Sutherland SK. Pharmacological studies of stonefish (Synanceja trachynis) venom. Toxicon 1994;32:1197-10.
Kaji T, Sugiyama N, Ishizaki S, Nagashima Y, Shiomi K. Molecular cloning of grammistins, peptide toxins from the soapfish Pogonoperca punctata, by hemolytic screening of a cDNA library. Peptides 2006;27:3069-76.
Sugiyama N, Araki M, Ishida M, Nagashima Y, Shiomi K. Further isolation and characterization of grammistins from the skin secretion of the soapfish Grammistes sexlineatus. Toxicon 2005;45:595-1.
Shiomi K, Igarashi T, Yokota H, Nagashima Y, Ishida M. Isolation and structures of grammistins, peptide toxins from the skin secretion of the soapfish Grammistes sexlineatus. Toxicon 2000;38:91-3.
Lopes Ferreira M, Emim JADS, Oliveira V, Puzer L, Cezari MH, Araujo MDS, et al. Kininogenase activity of Thalassophryne nattereri fish venom. Biochem Pharmacol 2004;68:2151-7.
Conceicao K, Konno K, Melo RL, Marques EE, Hiruma Lima CA, Lima C, et al. Orpotrin: a novel vasoconstrictor peptide from the venom of the Brazilian stingray Potamotrygon gr. orbignyi. Peptides 2006;27:3039-46.
Conceicao K, Santos JM, Bruni FM, Klitzke CF, Marques EE, Borges MH, et al. Characterization of a new bioactive peptide from Potamotrygon gr. orbignyi freshwater stingray venom. Peptides 2009;30:2191-9.
Magalhaes G, Lopes Ferreira M, Junqueira-de-Azevedo, I Spencer P, Araujo M, Portaro F, et al. Natterins, a new class of proteins with kininogenase activity characterized from Thalassophryne nattereri fish venom. Biochimie 2005;87:687-9.
Komegae EN, Ramos AD, Oliveira K, de Toledo Serrano SM, Lopes Ferreira M, Lima C. Insights into the local pathogenesis induced by fish toxins: role of natterins and nattectin in the disruption of cell-cell and cell-extracellular matrix interactions and modulation of cell migration. Toxicon 2011;58:509-7.
Magalhaes G, Junqueira-de-Azevedo I, Lopes Ferreira M, Lorenzini D, Ho P, Moura-da-Silva A. Transcriptome analysis of expressed sequence tags from the venom glands of the fish Thalassophryne nattereri. Biochimie 2006;88:693-9.
Ferreira MJ, Lima C, Lopes Ferreira M. Anti-inflammatory effect of natterins, the major toxins from the Thalassophryne nattereri fish venom is dependent on TLR4/MyD88/PI3K signaling pathway. Toxicon 2014;87:54-7.
Poh C, Yuen R, Chung M, Khoo H. Purification and partial characterization of hyaluronidase from stonefish (Synanceja horrida) venom. Comp Biochem Physiol 1992;101:159-3.
Ng HC, Ranganathan S, Chua KL, Khoo H. Cloning and molecular characterization of the first aquatic hyaluronidase, SFHYA1, from the venom of stonefish (Synanceja horrida). Gene 2005;346:71-1.
Sugahara K, Yamada S, Sugiura M, Takeda K, Yuen R, Khoo H, et al. Identification of the reaction products of the purified hyaluronidase from stonefish (Synanceja horrida) venom. Biochem J 1992;283:99-4.
Madokoro M, Ueda A, Kiriake A, Shiomi K. Properties and cDNA cloning of a hyaluronidase from the stonefish Synanceia verrucosa venom. Toxicon 2011;58:285-92.
Magalhaes MR. A hyaluronidase from Potamotrygon motoro (freshwater stingrays) venom: isolation and characterization. Toxicon 2008;51:1060-7.
Kiriake A, Madokoro M, Shiomi K. Enzymatic properties and primary structures of hyaluronidases from two species of lionfish (Pterois antennata and Pterois volitans). Fish Physiol Biochem 2014;40:1043–3.
Cohen AS, Olek AJ. An extract of lionfish (Pterois volitans) spine tissue contains acetylcholine and a toxin that affects neuromuscular transmission. Toxicon 1989;27:1367-6.
Carlisle D. On the venom of the lesser weeverfish, Trachinus vipera. J Mar Biol Assoc UK 1962;42:155–2.
Garnier P, Grosclaude JM, Goudey Perriere F, Gervat V, Gayral P, Jacquot C, et al. Presence of norepinephrine and other biogenic amines in stonefish venom. J Chromotogr B Biomed 1996;685:364–9.
Hopkins BJ, Hodgson WC, Sutherland SK. Pharmacological studies of stonefish (Synanceja trachynis) venom. Toxicon 1994;32:1197-10.
Nair M, Cheung P, Leong I, Ruggieri GD. A non-proteinaceous toxin from the venomous spines of the lionfish Pterois volitans (Linnaeus). Toxicon 1985;23:525-7.
Cohen AS, Olek AJ. An extract of lionfish (Pterois volitans) spine tissue contains acetylcholine and a toxin that affects neuromuscular transmission. Toxicon 1989;27:1367-6.
Nagasaka K, Nakagawa H, Satoh F, Hosotani T, Yokoigawa K, Sakai H, et al. A novel cytotoxic protein, Karatoxin, from the dorsal spines of the redfin velvetfish, Hypodytes rubripinnis. Toxin Rev 2009;28:260-5.
Shinohara M, Nagasaka K, Nakagawa H, Edo K, Sakai H, Kato K, et al. A novel chemoattractant lectin, karatoxin, from the dorsal spines of the small scorpionfish Hypodytes rubripinnis. J Pharmacol Sci 2010;113:414-7.
Huang TC, Lee JF, Chen JY. Pardaxin, an antimicrobial peptide, triggers caspase-dependent and ROS-mediated apoptosis in HT-1080 cells. Mar Drugs 2011;9:1995-9.
Fitzgerald GJ. Analysis of 24 cases of bullrout envenomation. Emerg Med 1993;5:199-200.
Kizer KW, McKinney HE, Auerbach PS. Scorpaenidae envenomation: a five-year poison center experience. JAMA 1985;253:807-10.
Lee J, Teoh L, Leo S. Stonefish envenomations of the hand-a local marine hazard: a series of 8 cases and review of the literature. Ann Acad Med Singap 2004;33:515–20.
Nistor A, Gie O, Biegger P, Fusetti C, Lucchina S. Surgical vacuum-assisted closure for treatment of the dramatic case of stonefish envenomation. Chin J Traumatol 2010;13:250-2.
Haddad V, Jr Martins IA. Frequency and gravity of human envenomations caused by marine catfish (suborder siluroidei): a clinical and epidemiological study. Toxicon 2006;47:838-3.
Chhatwal I, Dreyer F. Isolation and characterization of dracotoxin from the venom of the greater weever fish Trachinus draco. Toxicon 1992;30:87-3.
Khoo H, Hon W, Lee S, Yuen R. Effects of stonustoxin (lethal factor from Synanceja horrida venom) on platelet aggregation. Toxicon 1995;33:1033-41.
Shiomi K, Hosaka M, Fujita S, Yamanaka H, Kikuchi T. Venoms from six species of marine fish: Lethal and hemolytic activities and their neutralization by commercial stonefish antivenom. Mar Biol 1989;103:285-9.
Kiriake A, Suzuki Y, Nagashima Y, Shiomi K. Proteinaceous toxins from three species of scorpaeniform fish (lionfish Pterois lunulata, devil stinger Inimicus japonicus and wasp fish Hypodytes rubripinnis): close similarity in properties and primary structures to stonefish toxins. Toxicon 2013;70:184-3.
Grotendorst GR, Hessinger DA. Purification and partial characterization of the phospholipase a 2 and co-lytic factor from sea anemone (Aiptasia pallida) nematocyst venom. Toxicon 1999;37:1779-6.
Valdez Cruz NA, Batista CV, Possani LD. Phaiodactylipin, a glycosylated heterodimeric phospholipase A2 from the venom of the scorpion Anuroctonus phaiodactylus. Eur J Biochem 2004;27:1453-4.
Gul S, Smith AD. Hemolysis of intact human erythrocytes by purified cobra venom phospholipase A 2 in the presence of albumin and Ca 2+. BBA-Biomembr 1974;367:271-1.
Sivan G, Venketesvaran K, Radhakrishnan C. Biological and biochemical properties of Scatophagus argus venom. Toxicon 2007;50:563-1.
Lopes Ferreira M, Moura-da-Silva AM, Piran Soares AA, Angulo Y, Lomonte B, Gutierrez JMA, et al. Hemostatic effects induced by Thalassophryne nattereri fish venom: a model of endothelium-mediated blood flow impairment. Toxicon 2002;40:1141-7.
Han Han, Kate Baumann, Nicholas R Casewell, Syed A Ali, James Dobson, Ivan Koludarov, et al. The cardiovascular and neurotoxic effects of the venoms of six bony and cartilaginous fish species. Toxins (Basel) 2017;9:67.
Auddy B, Alam MI, Gomes A. Pharmacological actions of the venom of the Indian catfish (Plotosus canius Hamilton). Indian J Med Res 1994;99:47-1.
Sarmiento BE, Rangel M, Gonçalves JC, Pereira L, Rego S, Campos LA, et al. First report of the characterization of the pathophysiological mechanisms caused by the freshwater catfish Pimelodus maculatus (order: siluriformes). Toxicon 2015;101:55-2.
Bartho L, Sandor Z, Bencsik T. Effects of the venom of the brown bullhead catfish (Ameiurus nebulosus) on isolated smooth muscles. Acta Biol Hung 2018;69:135-3.
Khoo H, Yuen R, Poh C, Tan C. Biological activities of Synanceja horrida (stonefish) venom. Nat Toxins 1992;1:54-60.
Ramos AD, Conceicao K, Silva PI Jr, Richardson M, Lima C, Lopes Ferreira M. Specialization of the sting venom and skin mucus of Cathorops spixii reveals functional diversification of the toxins. Toxicon 2012;59:651-5.
Junqueira MEP, Grund LZ, Orii NM, Saraiva TC, de Magalhaes Lopes CA, Lima C, et al. Analysis of the inflammatory reaction induced by the catfish (Cathorops spixii) venoms. Toxicon 2007;49:909-9.
Bo J, Yang Y, Zheng R, Fang C, Jiang, Liu J, et al. Antimicrobial activity and mechanisms of multiple antimicrobial peptides isolated from rockfish Sebastiscus marmoratus. Fish Shellfish Immunol 2019;93:1007-7.
Kim CH, Kim EJ, Nam YK. Subfunctionalization and evolution of liver-expressed antimicrobial peptide 2 (LEAP2) isoform genes in Siberian sturgeon (Acipenser baerii), a primitive chondroitin fish species. Fish Shellfish Immunol 2019;93:161-3.
Pal R, Barenholz Y, Wagner RR. Transcription of vesicular stomatitis virus activated by pardaxin, a fish toxin that permeabilizes the virion membrane. J Virol 1981;39:641-5.
Carrijo LC, Andrich F, de Lima ME, Cordeiro MN, Richardson M, Figueiredo SG. Biological properties of the venom from the scorpionfish Scorpaena plumieri and purification of a gelatinolytic protease. Toxicon 2005;45:843–50.
Garnier P, Goudey Perriere F, Breton P, Dewulf C, Petek F, Perriere C. Enzymatic properties of the stonefish (Synanceia verrucosa) bloch and schneider, 1801) venom and purification of a lethal, hypotensive and cytolytic factor. Toxicon 1995;33:143-55.
Barbaro KC, Lira MS, Malta MB, Soares SL, Garrone Neto D, Cardoso JL, et al. Comparative study on extracts from the tissue covering the stingers of freshwater (Potamotrygon falkneri) and marine (Dasyatis guttata) stingrays. Toxicon 2007;50:676–7.
Monteiro-dos-Santos J, Conceicao K, Seibert CS, Marques EE, Silva PI Jr, Soares AB, et al. Studies on pharmacological properties of mucus and sting venom of Potamotrygon cf. henlei. Int Immunopharmacol 2011;11:1368–7.
Lopes Ferreira M, Barbaro K, Cardoso D, Moura-da-Silva A, Mota I. Thalassophryne nattereri fish venom: biological and biochemical characterization and serum neutralization of its toxic activities. Toxicon 1998;36:405–10.
Sosa Rosales JI, Piran Soares AA, Farsky SH, Takehara HA, Lima C, Lopes Ferreira M. Important biological activities induced by Thalassophryne maculosa fish venom. Toxicon 2005;45:155–1.
Balasubashini MS, Karthigayan S, Somasundaram S, Balasubramanian T, Viswanathan P, Menon VP. In vivo and in vitro characterization of the biochemical and pathological changes induced by lionfish (Pterios volitans) venom in mice. Toxicol Mech Method 2006;16:525–31.
Sivan G, Venketasvaran K, Radhakrishnan C. Characterization of biological activity of Scatophagus argus venom. Toxicon 2010;56:914–5.
Cameron AM, Surridge J, Stablum W, Lewis RJ. A conotoxin from the skin tubercle glands of a stonefish (Synanceia trachynis). Toxicon 1981;19:159–70.
Hopkins BJ, Hodgson WC. Enzyme and biochemical studies of stonefish (Synanceja trachynis) and soldierfish (Gymnapistes marmoratus) venoms. Toxicon 1998;36:791–3.
De Araujo Tenorio H, da Costa Marques, ME Machado SS, Pereira HJV. Angiotensin processing activities in the venom of Talassophryne nattereri. Toxicon. 2015;98:49-53.
Ghafari SM, Jamili S, Bagheri KP, Ardakani EM, Fatemi MR, Shahbazzadeh F, et al. The first report on some toxic effects of green scat, Scatophagus argus an Iranian persian Gulf venomous fish. Toxicon 2013;66:82–7.
Kiriake A, Madokoro M, Shiomi K. Enzymatic properties and primary structures of hyaluronidases from two species of lionfish (Pterois antennata and Pterois volitans). Fish Physiol Biochem 2014;40:1043-53.
Lopes Ferreira M, Gomes EM, Bruni FM, Ferreira MJ, Charvet P, Lima C. First report of interruption of mast cell degranulation and endothelial cells activation by anti-inflammatory drugs controlling the acute response provoked by Pseudoplatystoma fasciatum fish venom. Toxicon 2014;90:237–48.
Kimura LF, Prezotto Neto JP, Antoniazzi MM, Jared SG, Santoro M, Barbaro KC. Characterization of the inflammatory response induced by Potamotrygon motoro stingray venom in mice. Exp Biol Med 2014;239:601–9.
Lima C, Clissa PCB, Piran Soares AA, Tanjong I, Moura-da-Silva AM, Lopes-Ferreira M. Characterisation of the local inflammatory response induced by Thalassophryne nattereri fish venom in a mouse model of tissue injury. Toxicon 2003;42:499–7.
Ishizuka EK, Ferreira MJ, Grund LZ, Coutinho EMM, Komegae EN, Cassado AA, et al. Role of the interplay between IL-4 and IFN-γ in the in regulating M1 macrophage polarization induced by Nattectin. Int Immunopharmacol 2012;14:513-22.
Monica Lopes Ferreira, Lidiane Zito Grund, Carla Lima. Thalassophryne nattereri fish venom: from the envenoming to the understanding of the immune system. J Venom Anim Toxins Incl Trop Dis 2014;20:35.
Saraiva TC, Grund LZ, Komegae EN, Ramos AD, Conceicao K, Orii NM, et al. Nattectin a fish C-type lectin drives Th1 responses in vivo: licenses macrophages to differentiate into cells exhibiting typical DC function. Int Immunopharmacol 2011;11:1546–6.
Grund LZ, Souza VMO, Faquim Mauro EL, Lima C, Lopes Ferreira M. Experimental immunization with Thalassophryne nattereri fish venom: striking IL-5 production and impaired of B220+cells. Toxicon 2006;48:499–8.
Komegae EN, Grund LZ, Lopes Ferreira M, Lima C. The longevity of Th2 humoral response induced by proteases natterins requires the participation of long-lasting innate-like B cells and plasma cells in the spleen. PLoS One 2013;8:e67135.
Grund LZ, Komegae EN, Lopes Ferreira M, Lima C. IL-5, and IL-17A are critical for the chronic IgE response and differentiation of long-lived antibody-secreting cells in inflamed tissues. Cytokine 2012;59:335–51.
Grund LZ, Lopes Ferreira M, Lima C. The hierarchical process of differentiation of long-lived antibody-secreting cells is dependent on integrated signals derived from antigen and IL-17A. PLoS One 2013;8:e74566.
Komegae EN, Grund LZ, Lopes Ferreira M, Lima C. TLR2, TLR4, and the MyD88 signaling are crucial for the in vivo generation and the longevity of long-lived antibody-secreting cells. PLoS One 2013;8:e71185.
Adi L, Ephraim Y, Philip L. the molecular basis of toxins’ interactions with intracellular signaling via discrete portals. Toxins (Basel) 2017;9:107.
Austin L, Gillis R, Youatt G. Stonefish venom: some biochemical and chemical observations. Aust J Exp Biol Med Sci 1965;43:79-90.
Gisha S. Fish venom: pharmacological features and biological significance. Fish Fisheries 2009;10:159-2.
Church JE. Hodgson the pharmacological activity of fish venoms. Toxicon 2002;40:1083-93.
Waring MJ, Arrowsmith J, Leach AR, Leeson PD, Mandrell S, Owen RM, et al. An analysis of drug candidates from four major pharmaceutical companies. Nat Rev Drug Discovery 2015;14:475-86.
Cornet C, Calzolari S, Minana Prieto R, Dyballa S, van Doornmalen E, Rutjes H, et al. An innovative approach to address organ drug toxicity using zebrafish. Int J Mol Sci 2017;18:864.
John H Tibbetts. Turning toxins into treatments: researchers use new tools to identify therapeutic ingredients in animal venom. BioScience 2015;65:957–62.
Fry BG, Koludarov I, Jackson TNW, Holford M, Terrat Y, Casewell NR, et al. Seeing the Woods for the trees: understanding venom evolution as a guide for biodiscovery. In: Venoms to drugs: venom as a source for the development of human therapeutics; King GF. Ed. Royal society of chemistry: London UK; 2015. p. 1–36.
Glenn F King. Venom as a source for the development of human therapeutics. Royal Soc Chem 2015. p. 1-36. DOI:10.1039/9781849737876–00001
Olivera BM. Conus venom peptides, receptor and ion channel targets, and drug design: 50 million years of neuropharmacology. Mol Biol Cell 1997;8:2101-9.
Siddall M, Gavin M. Venom: sinister species with deadly consequences. American Museum of Natural History. Publisher: Sterling; 2014. Available from: https://www.amazon.in/Poison-Sinister-Species-Consequences-American/dp/1454907649 [Last accessed on 03 Jun 2014]
Quentin Kaas, David J. Craik, bioinformatics-aided venomics. Toxins (Basel) 2015;7:2159–7.
Zhao XM, Chu XH, Liu Y, Liu QN, Jiang SH, Zhang DZ, et al. A myeloid differentiation factor 88 gene from yellow catfish Pelteobagrus fulvidraco and its molecular characterization in response to polyriboinosinic-polyribocytidylic acid and lipopolysaccharide challenge. Int J Biol Macromol 2018; 120: 1080-6.
Bartho L, Sandor Z, Bencsik T. Effects of the venom of the brown bullhead catfish (Ameiurus nebulosus) on isolated smooth muscles. Acta Biol Hung 2018;69:135-3.
Lahiani A, Yavin E, Lazarovici P. The molecular basis of toxins' interactions with intracellular signaling via discrete portals. Toxins (Basel) 2017;9:107.
Memar B, Jamili S, Shahbazzadeh D, Bagheri KP. The first report on coagulation and phospholipase A2 activities of persian gulf lionfish, Pterois russelli, an Iranian venomous fish. Toxicon 2016;113:25-31.
Komegae EN, Souza TA, Grund LZ, Lima C, Lopes Ferreira M. Multiple functional therapeutic effects of TnP: a small stable synthetic peptide derived from fish venom in a mouse model of multiple sclerosis. PLoS One 2017;12:e0171796.
Dhanda SK, Usmani SS, Agrawal P, Nagpal G, Gautam A, Raghava GP. Novel in silico tools for designing peptide-based subunit vaccines and immunotherapeutic. Brief Bioinform 2017;18:467-78.
Adessi C, Soto C. Converting a peptide into a drug: strategies to improve stability and bioavailability. Curr Med Chem 2002;9:963-78.
Shen GS, Layer RT, Mc Cabe RT. Conopeptides: from deadly venoms to novel therapeutics. Drug Discovery Today 2000;5:98-6.
Leader B, Baca QJ, Golan DE. Protein therapeutics: a summary and pharmacological classification. Nat Rev Drug Discovery 2008;7:21-39.
Lopes Ferreira M, Moura-da-Silva A, Mota I, Takehara H. Neutralization of Thalassophryne nattereri (niquim) fish venom by an experimental antivenom. Toxicon 2000;38:1149-56.
Piran Soares AA, Souza VMO, Fonseca LA, Lima C, Lopes Ferreira M. Neutralizing antibodies obtained in a persistent immune response are effective against deleterious effects induced by the Thalassophryne nattereri fish venom. Toxicon 2007;49:920–30.
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