Tetrodotoxin binding protein in the marine puffer fish

Yıl 2021, Cilt: 6 Sayı: 1, 39 - 52, 25.01.2021

Bahar Tokur Koray Korkmaz

https://doi.org/10.28978/nesciences.868077

Öz

Marine pufferfish generally involve a potent neurotoxin, tetrodotoxin (TTX), which might be the leading cause for many human intoxications. It blocks nervous impulses’ conduction along nerve fibers and axons during the act, and the LD50 for the mouse is 10 nanograms. Being much larger than the sodium ion, TTX acts as a cork of a bottle, prevents sodium from flowing until it diffuses slowly. The TTX expanse appears to be species-specific in pufferfish bodies. The toxin is thought to bioaccumulate via the marine food based on the observations that marine pufferfishes that are cultured are not toxic, and non-toxic cultured pufferfishes become toxic when they feed on TTX-containing artificial diets. TTX-bearing animals show incredibly high resistance to TTX, and therefore TTX presumably retains or accumulates as a biological defense substance. These animals carrying TTX can accumulate toxins in their bodies despite not killing themselves is an object of interest. Fort his reason, and it is argued that TTX is wrapped in a particular protein and does not bind directly to the target's side-sodium channel, and therefore does not induce intoxication. The pufferfish TTX-binding protein (PSTBP) was first isolated as a potential TTX-carrier protein from the plasma of the marine pufferfish Takifugu niphobles. This protein is discovered to be a dimeric glycoprotein and formed a non-covalent dimer.

Anahtar Kelimeler

pufferfish, tetrodotoxin (TTX), TTX-binding protein

Kaynakça

• Akbora, H. D., Kunter, İ., Erçeti̇n, T., Elagöz, A. M., & Çi̇çek, B. A. (2020). Determination of tetrodotoxin (TTX) levels in various tissues of the silver cheeked puffer fish (Lagocephalus sceleratus (Gmelin, 1789)) in Northern Cyprus Sea (Eastern Mediterranean). Toxicon, 175, 1-6.
• Arakawa, K. (2001). Resistibility against TTX and PSP. In: Studies on the Toxicity of a Japanese Newt Cynops pyrrhogaster, Doctoral thesis, Nagasaki University, Nagasaki, pp. 50– 53.
• Arakawa, O., Nishio, S., Noguchi, T., Shida, Y., Onoue, Y. (1995). A new saxitoxin analogue from a xanthid crab Atergatis floridus. Toxicon 33, 1577–1584.
• Bane, V., M. Lehane, M. Dikshit, A. O'Riordan, and A. Furey. (2014). Tetrodotoxin: Chemistry, toxicity, source, distribution and detection. Toxins, 6: 693-755.
• Chau, R.; Kalaitzis, J.A.; Neilan, B.A. On the origins and biosynthesis of tetrodotoxin. Aquatic Toxicology, 2011, 104, 61–72.
• Fournier, T., Medjoubi-N, N., & Porquet, D. (2000). Alpha-1-acid glycoprotein. Biochimica et Biophysica Acta (BBA)-Protein Structure and Molecular Enzymology, 1482(1-2), 157-171.
• Fuchi, Y., Tsubone, N., Morisaki, S., Mizokoshi, T., Shuto, M., Fujii, M., Yamada, K., Hayashi, K. (1986). A survey on toxicity of pufferfishes, Fugu rubripes rubripes (torafugu) and Fugu rubripes chinensis (karasu). Journal of the Food Hygienic Society of Japan, 27, 569–572.
• Gao, W., Kanahara, Y., Tatsuno, R., Soyano, K., Nishihara, G.N., Urata, C., Takatani, T., Arakawa, O. (2018). Maturation-associated changes in internal distribution and intra-ovarian microdistribution of tetrodotoxin in the pufferfish Takifugu pardalis. Fisheries Science, 84, 723–732.
• Gao, W., Kanahara, Y., Yamada, M., Tatsuno, R., Yoshikawa, H., Doi, H., Takatani, T., Arakawa, O. (2019). Contrasting toxin selectivity between the marine pufferfish Takifugu pardalis and the freshwater pufferfish Pao suvattii. Toxins, 11, 470.
• Gao, W., Yamada, M., Ohki, R., Nagashima, Y., Tatsuno, R., Ikeda, K., ... & Arakawa, O. (2020). Evaluation of the tetrodotoxin uptake ability of pufferfish Takifugu rubripes tissues according to age using an in vitro tissue slice incubation method. Toxicon, 174, 8-12.
• Geffeney, S. L., E. Fujimoto, E. D. III Brodie, E. D. Jr. Brodie, and P.C. Ruben. (2005). Evolutionary diversification of TTX-resistant sodium channels in a predator-prey interaction. Nature, 434: 759–763.
• Halstead, B.W., (1988). Poisonous and Venomous Marine Animals of the World, second ed. The Darwin Press Inc., Princeton, pp. 525–644.
• Hashiguchi Y., J. M. Lee, M. Shitaishi, S. Komatsui, S. Miki, Y. Shimasaki, N. Mochioka, T. Kusakabe, and Y. Oshima. (2015). Characterization and evolutionary analysis of tributyltin-binding protein and pufferfish saxitoxin and tetrodotoxin-binding protein genes in toxic and nontoxic pufferfishes. Evolutionary Biology, 28: 1103-1118.
• Hwang, D.-F., Kao, C.-Y., Yang, H.-C., Jeng, S.-S., Noguchi, T., Hashimoto, K. (1992). Toxicity of puffer in Taiwan. Nippon Suisan Gakkaishi, 58, 1541– 1547.
• Hwang P. A., Y. H. Tsai, H. P. Lin, and D. F. Hwang. (2007). Tetrodotoxin-binding proteins isolated from five species of toxic gastropods. Food Chemistry, 103: 1153-1158.
• Ikeda, K. (2009). Studies on the Transfer/Accumulation Profile of Tetrodotoxin in Pufferfish. Ph.D. Thesis. Nagasaki University, Nagasaki, Japan.
• Ikeda, K., Emoto, Y., Tatsuno, R., Wang, J.J., Ngy, L., Taniyama, S., Takatani, T., Arakawa, O. (2010). Maturation-associated changes in toxicity of the pufferfish Takifugu poecilonotus. Toxicon, 55, 289–297.
• Isbister, G.K., Kiernan, M.C. (2005). Neurotoxic marine poisoning. Lancet Neurol., 4(4):219–228.
• Itoi, S., Ishizuka, K., Mitsuoka, R., Takimoto, N., Yokoyama, N., Detake, A., Takayanagi, C., Yoshikawa, S., Sugita, H. (2016). Seasonal changes in the tetrodotoxin content of the pufferfish Takifugu niphobles. Toxicon, 114, 53–58.
• Jang, J., Yotsu-Yamashita, M. (2006). Distribution of tetrodotoxin, saxitoxin, and their analogs among tissues of the puffer fish Fugu pardalis. Toxicon, 48, 980–987.
• Jang, J.H., Lee, J.S., Yotsu-Yamashita, M. (2010). LC/MS analysis of tetrodotoxin and its deoxy analogs in the marine puffer fish Fugu niphobles from the southern coast of Korea, and in the brackishwater puffer fishes Tetraodon nigroviridis and Tetraodon biocellatus from Southeast Asia. Marine Drugs, 8, 1049–1058.
• Kanoh, S., Noguchi, T., Otsuka, M., Hashimoto, K. (1984). Comparison of toxicity of two pufferfish, Fugu rubripes chinensis (“karasu”) and Fugu rubripes rubripes (“torafugu”). Journal of the Food Hygienic Society of Japan, 25, 436–439.
• Kanoh, S. (1988). Distribution of tetrodotoxin in vertebrates. In: Hshimoto, K. (Ed.), Recent Advances in Tetrodotoxin Research. Koseisha- Koseikaku, Tokyo, pp. 32– 44. Kono, M., Matsui, T., Furukawa, K., Yotsu-Yamashita, M., Yamamori, K. (2008). Accumulation of tetrodotoxin and 4,9-anhydrotetrodotoxin in cultured juvenile kusafugu Fugu niphobles by dietary administration of natural toxic komonfugu Fugu poecilonotus liver. Toxicon 51, 1269–1273.
• Kosker, A. R., Özogul, F., Durmus, M., Ucar, Y., Ayas, D., Regenstein, J. M., & Özogul, Y. (2016). Tetrodotoxin levels in pufferfish (Lagocephalus sceleratus) caught in the Northeastern Mediterranean Sea. Food Chemistry, 210, 332-337.
• Kosker, A. R., Özogul, F., Durmus, M., Ucar, Y., Ayas, D., Šimat, V., & Özogul, Y. (2018). First report on TTX levels of the yellow spotted pufferfish (Torquigener flavimaculosus) in the Mediterranean Sea. Toxicon, 148, 101-106.
• Koyama, K., Noguchi, T., Uzu, A., Hashimoto, K. (1983). Resistibility of toxic and nontoxic crabs against paralytic shellfish poison and tetrodotoxin. Nippon Suisan Gakkaishi, 49, 485–489.
• Lee, C.H., Ruben, P.C. (2008). Interaction between voltage-gated sodium channels and the neurotoxin, tetrodotoxin. Channels (Austin), 2, 407–412.
• Lin, S.J., Chai, T.J., Jeng, S.S., Hwang, D.F. (1998). Toxicity of the puffer Takifugu rubripes cultured in northern Taiwan. Fisheries Science, 64, 766–770.
• Lipkind, G.M., Fozzard, H.A. (2005). Molecular modeling of local anesthetic drug binding by voltage-gated sodium channels. Molecular Pharmacology, 68, 1611–1622.
• Magarlamov, T.Y., Melnikova, D.I., Chernyshev, A.V. (2017). Tetrodotoxin-producing bacteria: detection, distribution and migration of the toxin in aquatic systems. Toxins, 9, 166.
• Matsui, T., Hamada, S., Konosu, S. (1981). Difference in accumulation of puffer fish toxin and crystalline tetrodotoxin in the puffer fish, Fugu rubripes rubripes. Nippon Suisan Gakkaishi, 47, 535–537.
• Matsui, T., Sato, H., Hamada, S., Shimizu, C. (1982). Comparison of toxicity of the cultured and wild puffer fish Fugu niphobles. Nippon Suisan Gakkaishi, 48, 253.
• Matsui T. K. Yamamori, K. Furukawa, and M. Kono. (2000). Purification and some properties of a tetrodotoxin binding protein from the blood plasma of kusafugu, Takifugu niphobles. Toxicon, 38: 463-468.
• Matsumoto T., Y. Nagashima, H. Jusuhara, Y. Sugiyama, S. Ishizaki, K. Shimakura, and K. Shiomi. (2007). Involvement of carrier-mediated transport system in uptake of tetrodotoxin into liver tissue slices of puffer fish Takifugu rubripes. Toxicon, 50: 173-179.
• Matsumoto, T., Tanuma, D., Tsutsumi, K., Jeon, J. K., Ishizaki, S., & Nagashima, Y. (2010). Plasma protein binding of tetrodotoxin in the marine puffer fish Takifugu rubripes. Toxicon, 55(2-3), 415-420.
• Miller J. A., W. S. Agnew, and S. R. Levinson. (1983). Principal Glycopeptide of the Tetrodotoxin/ Saxitoxin Binding protein form Electophorus electricus: isolation and partial chemical and physical characterization. Biochemistry, 22: 462-470.
• Nagashima Y., K. Yamamoto, K. Shimakura, and K. Shiomi. (2002). A tetrodotoxin-binding protein in the hemolymph of shore crab Hemigraspsus sanguineus: Purification and properties. Toxicon, 40: 753-760.
• Narahashi, T., Anderson, N. C., & Moore, J. W. (1967). Comparison of tetrodotoxin and procaine in internally perfused squid giant axons. The Journal of General Physiology, 50 (5), 1413-1428.
• Narahashi, T. (2001). Pharmacology of tetrodotoxin. Journal of Toxicology: Toxin Reviews, 20, 67–84.
• Ngy, L., Yu, C., Taniyama, S., Takatani, T., Arakawa, O. (2009). Co-occurrence of tetrodotoxin and saxitoxin in Cambodian marine pufferfish Takifugu oblongus. African Journal of Marine Science, 31.
• Noguchi, T., Arakawa, O., Takatani, T. (2006). TTX accumulation in pufferfish. Comparative Biochemistry & Physiology,. Part D 1, 145–152.
• Noguchi, T., and O. Arakawa. (2008). Tetrodotoxin-Distribution and accumulation in aquatic organisms, and cases of human intoxication. Marine Drugs, 6: 220-242.
• Noguchi, T., Onuki, K., & Arakawa, O. (2011). Tetrodotoxin poisoning due to pufferfish and gastropods, and their intoxication mechanism. ISRN toxicology.
• Oba, Y., Y. Shimasaki, Y. Oshima, H. Satone, T. Kitano, M. Nakao, S. Kawabata, and T. Honjo. (2007). Purification and characterization of tributyltin-binding protein type 2 from plasma of Japanese flounder, Paralichthys olivaceus. Journal of Biochemistry, 142: 229–238.
• Pinto, E. P., Rodrigues, S. M., Gouveia, N., Timóteo, V., & Costa, P. R. (2019). Tetrodotoxin and saxitoxin in two native species of puffer fish, Sphoeroides marmoratus and Lagocephalus lagocephalus, from NE Atlantic Ocean (Madeira Island, Portugal). Marine Environmental Research, 151, 104780.
• Saito, T., Noguchi, T., Harada, T., Murata, O., Abe, T., Hashimoto, K. (1985). Resistibility of toxic and nontoxic pufferfish against tetrodotoxin. Bulletin of the Japanese Society of Scientific Fisheries, 51, 1371.
• Shimasaki, Y., Kitano, T., Oshima, Y., Inoue, S., Imada, N., & Honjo, T. (2003). Tributyltin causes masculinization in fish. Environmental Toxicology and Chemistry: An International Journal, 22(1), 141-144.
• Soong, T. W., & Venkatesh, B. (2006). Adaptive evolution of tetrodotoxin resistance in animals. TRENDS in Genetics, 22(11), 621-626.
• Tani, T. (1945). Nihonsan Fugu no Chudokugakuteki Kenkyu (Toxicological Studies on Japanese Puffer), Teikoku Tosho, Tokyo.
• Tatsuno, R. (2012). Studies on the Growth/Maturation-Associated Changes in Internal Tetrodotoxin (TTX) Distribution and Expression of TTX-Binding Proteins. Ph.D. Thesis. Nagasaki University, Nagasaki, Japan.
• Tatsuno, R., Shikina, M., Shirai, Y., Wang, J., Soyano, K., Nishihara, G.N., Takatani, T., Arakawa, O. (2013a). Change in the transfer profile of orally administered tetrodotoxin to non-toxic cultured pufferfish Takifugu rubripes depending of its development stage. Toxicon, 65, 76–80.
• Tatsuno, R., Yamaguchi, K., Takatani, T., & Arakawa, O. (2013). RT-PCR-and MALDI-TOF mass spectrometry-based identification and discrimination of isoforms homologous to pufferfish saxitoxin-and tetrodotoxin-binding protein in the plasma of non-toxic cultured pufferfish (Takifugu rubripes). Bioscience, Biotechnology, and Biochemistry, 77(1), 208-212.
• Venkatesh, B., S. Q. Lu, N. Dandona, S. L. See, S. Brenner, and T. W. Soong. (2005). Genetic basis of tetrodotoxin resistance in pufferfishes. Current Biology, 15: 2069-72.
• Walker, J. R., Novick, P. A., Parsons, W. H., McGregor, M., Zablocki, J., Pande, V. S., & Du Bois, J. (2012). Marked difference in saxitoxin and tetrodotoxin affinity for the human nociceptive voltage-gated sodium channel (Nav1. 7). Proceedings of the National Academy of Sciences, 109(44), 18102-18107.
• Wang, J., Araki, T., Tatsuno, R., Nina, S., Ikeda, K., Hamasaki, M., Sakakura, Y., Takatani, T., Arakawa, O. (2011). Transfer profile of intramuscularly administered tetrodotoxin to artificial hybrid specimens of pufferfish, Takifugu rubripes and Takifugu niphobles. Toxicon, 58, 565–569.
• Yamamori, K., Kono, M., Furukawa, K., Matsui, T. (2004). The toxification of juvenile cultured kusafugu Takifugu niphobles by oral administration of crystalline tetrodotoxin. Journal of the Food Hygienic Society of Japan , 45, 73–75.
• Yotsu-Yamashita M., A. Sugimoto, T. Terakawa, Y. Shoji, T. Miyazawa, and T. Yasumoto. (2001). Purification, characterization, and cDNA cloning of a novel soluble saxitoxin and tetrodotoxin binding protein from plasma of the puffer fish, Fugu pardalis. The FEBS Journal, 268: 5937-46.
• Yotsu-Yamashita, M., Shoji, Y., Terakawa, T., Yamada, S., Mıyazawa, T., & Yasumoto, T. (2002). Mutual binding inhibition of tetrodotoxin and saxitoxin to their binding protein from the plasma of the puffer fish, Fugu pardalis. Bioscience, Biotechnology, and Biochemistry, 66(11): 2520-2524.
• Yotsu-Yamashita, M.; Yamaki, H.; Okoshi, N.; Araki, N. (2010). Distribution of homologous proteins to pufferfish saxitoxin and tetrodotoxin binding protein in the plasma of pufferfish and among the tissues of Fugu pardalis examined byWestern blot analysis. Toxicon, 55, 1119–1124
• Yotsu-Yamashita, M.; Okoshi, N.; Watanabe, K.; Araki, N.; Yamaki, H.; Shoji, Y.; Terakawa, T. (2013). Localization of pufferfish saxitoxin and tetrodotoxin binding protein (PSTBP) in the tissues of the pufferfish, Takifugu pardalis, analyzed by immunohistochemical staining. Toxicon, 72, 23–28.
• Yotsu-Yamashita, M., Nagaoka, Y., Muramoto, K., Cho, Y., & Konoki, K. (2018). Pufferfish saxitoxin and tetrodotoxin binding protein (PSTBP) analogues in the blood plasma of the pufferfish Arothron nigropunctatus, A. hispidus, A. manilensis, and Chelonodon patoca. Marine Drugs, 16(7), 224.
• Yu, C., P. Yu, P. Chan, Q. Yan, and P. Wong. (2004). Two novel species of tetrodotoxin-producing bacteria isolated from toxic marine puffer fishes. Toxicon, 44: 641–647.
• Zhang, X., Han, C., Chen, S., Li, L., Zong, J., Zeng, J., & Mei, G. (2018). Response Surface Methodology for the Optimization of Ultrasound-Assisted Extraction of Tetrodotoxin from the Liver of Takifugu pseudommus. Toxins, 10(12), 529.