Contrasting Toxin Selectivity between the Marine Pufferfish Takifugu pardalis and the Freshwater Pufferfish Pao suvattii

To clarify the differences in toxin selectivity between marine and freshwater pufferfish, we conducted experiments in artificially reared nontoxic specimens of Takifugu pardalis (marine) and Pao suvattii (freshwater) using tetrodotoxin (TTX) and paralytic shellfish poison (PSP; decarbamoylsaxitoxin (dcSTX) or saxitoxin (STX)). T. pardalis specimens were administered feed homogenate containing TTX or dcSTX (dose of toxin, 55.2 nmol/fish) and P. suvattii specimens were administered feed homogenate containing TTX + STX (dose of each toxin, 19.2 nmol/fish) by oral gavage. The toxin content in the intestine, muscle, skin, liver, and gonads was quantified after 24 and 48 or 72 h. In T. pardalis, TTX administered into the intestine was absorbed into the body and transferred and retained mainly in the skin and liver, while dcSTX was hardly retained in the body, although it partly remained in the intestine. In strong contrast, in P. suvattii, little TTX remained in the body, whereas STX was absorbed into the body and was transferred and retained in the ovary and skin. The findings revealed that TTX/PSP selectivity differs between the marine species T. pardalis and the freshwater species P. suvattii. T. pardalis, which naturally harbors TTX, selectively accumulates TTX, and P. suvattii, which naturally harbors PSP, selectively accumulates PSP.

[1]  M. Yotsu-Yamashita,et al.  Pufferfish Saxitoxin and Tetrodotoxin Binding Protein (PSTBP) Analogues in the Blood Plasma of the Pufferfish Arothron nigropunctatus, A. hispidus, A. manilensis, and Chelonodon patoca , 2018, Marine drugs.

[2]  M. Yotsu-Yamashita,et al.  Spiro Bicyclic Guanidino Compounds from Pufferfish: Possible Biosynthetic Intermediates of Tetrodotoxin in Marine Environments. , 2018, Chemistry.

[3]  O. Arakawa,et al.  Maturation-associated changes in internal distribution and intra-ovarian microdistribution of tetrodotoxin in the pufferfish Takifugu pardalis , 2018, Fisheries Science.

[4]  A. Ohta,et al.  Difference in Uptake of Tetrodotoxin and Saxitoxins into Liver Tissue Slices among Pufferfish, Boxfish and Porcupinefish , 2018, Marine drugs.

[5]  W. Gao,et al.  Profile differences in tetrodotoxin transfer to skin and liver in the pufferfish Takifugu rubripes , 2017, Toxicon : official journal of the International Society on Toxinology.

[6]  M. Yotsu-Yamashita,et al.  Tetrodotoxin and Its Analogues in the Pufferfish Arothron hispidus and A. nigropunctatus from the Solomon Islands: A Comparison of Their Toxin Profiles with the Same Species from Okinawa, Japan , 2015, Toxins.

[7]  J. Finn,et al.  Isolation of 6-deoxytetrodotoxin from the pufferfish, Takifugu pardalis, and a comparison of the effects of the C-6 and C-11 hydroxy groups of tetrodotoxin on its activity. , 2014, Journal of natural products.

[8]  M. Yotsu-Yamashita,et al.  Localization of pufferfish saxitoxin and tetrodotoxin binding protein (PSTBP) in the tissues of the pufferfish, Takifugu pardalis, analyzed by immunohistochemical staining. , 2013, Toxicon : official journal of the International Society on Toxinology.

[9]  V. Paul,et al.  First Identification of 5,11-Dideoxytetrodotoxin in Marine Animals, and Characterization of Major Fragment Ions of Tetrodotoxin and Its Analogs by High Resolution ESI-MS/MS , 2013, Marine drugs.

[10]  O. Arakawa,et al.  Change in the transfer profile of orally administered tetrodotoxin to non-toxic cultured pufferfish Takifugu rubripes depending of its development stage. , 2013, Toxicon : official journal of the International Society on Toxinology.

[11]  Gary S. Sayler,et al.  An Overview on the Marine Neurotoxin, Saxitoxin: Genetics, Molecular Targets, Methods of Detection and Ecological Functions , 2013, Marine drugs.

[12]  O. Arakawa,et al.  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) , 2013, Bioscience, biotechnology, and biochemistry.

[13]  美桜 登田,et al.  わが国における自然毒による食中毒事例の傾向(平成元年~22年) , 2012 .

[14]  Kaoru Morikawa,et al.  [Trends of food poisonings caused by natural toxins in Japan, 1989-2011]. , 2012, Shokuhin eiseigaku zasshi. Journal of the Food Hygienic Society of Japan.

[15]  O. Arakawa,et al.  Transfer profile of orally and intramuscularly administered tetrodotoxin to artificial hybrid specimens of the pufferfish Takifugu rubripes and Takifugu porphyreus. , 2012, Shokuhin eiseigaku zasshi. Journal of the Food Hygienic Society of Japan.

[16]  O. Arakawa,et al.  Transfer profile of intramuscularly administered tetrodotoxin to artificial hybrid specimens of pufferfish, Takifugu rubripes and Takifugu niphobles. , 2011, Toxicon : official journal of the International Society on Toxinology.

[17]  M. Yotsu-Yamashita,et al.  Distribution of homologous proteins to puffer fish saxitoxin and tetrodotoxin binding protein in the plasma of puffer fish and among the tissues of Fugu pardalis examined by Western blot analysis. , 2010, Toxicon : official journal of the International Society on Toxinology.

[18]  M. Yotsu-Yamashita,et al.  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 , 2010, Marine drugs.

[19]  S. Taniyama,et al.  Transfer profile of intramuscularly administered tetrodotoxin to non-toxic cultured specimens of the pufferfish Takifugu rubripes. , 2009, Toxicon : official journal of the International Society on Toxinology.

[20]  T. Noguchi,et al.  Tetrodotoxin – Distribution and Accumulation in Aquatic Organisms, and Cases of Human Intoxication , 2008, Marine drugs.

[21]  Chun-fai Yu,et al.  Occurrence of paralytic shellfish toxins in Cambodian Mekong pufferfish Tetraodon turgidus: selective toxin accumulation in the skin. , 2008, Toxicon : official journal of the International Society on Toxinology.

[22]  M. Yotsu-Yamashita,et al.  6,11-Dideoxytetrodotoxin from the puffer fish, Fugu pardalis. , 2007, Toxicon : official journal of the International Society on Toxinology.

[23]  M. Yotsu-Yamashita,et al.  Distribution of tetrodotoxin, saxitoxin, and their analogs among tissues of the puffer fish Fugu pardalis. , 2006, Toxicon : official journal of the International Society on Toxinology.

[24]  T. Noguchi,et al.  Accumulation and depuration profiles of PSP toxins in the short-necked clam Tapes japonica fed with the toxic dinoflagellate Alexandrium catenella. , 2006, Toxicon : official journal of the International Society on Toxinology.

[25]  K. Steidinger,et al.  Saxitoxin Puffer Fish Poisoning in the United States, with the First Report of Pyrodinium bahamense as the Putative Toxin Source , 2006, Environmental health perspectives.

[26]  T. Noguchi,et al.  Toxicity of pufferfish Takifugu rubripes cultured in netcages at sea or aquaria on land. , 2006, Comparative biochemistry and physiology. Part D, Genomics & proteomics.

[27]  K. Takayama,et al.  Difference Between Tetrodotoxin and Saxitoxins in Accumulation in Puffer Fish Takifugu rubripes Liver Tissue Slices , 2006, Fish Physiology and Biochemistry.

[28]  玉雄 野口,et al.  テトロドトキシン添加飼料投与による養殖トラフグ Takifugu rubripes の毒化 , 2005 .

[29]  S. Taniyama,et al.  Occurrence of saxitoxins as a major toxin in the ovary of a marine puffer Arothron firmamentum. , 2004, Toxicon : official journal of the International Society on Toxinology.

[30]  Y. Nagashima,et al.  In vitro accumulation of tetrodotoxin in pufferfish liver tissue slices. , 2003, Toxicon : official journal of the International Society on Toxinology.

[31]  T. Yasumoto,et al.  Purification, characterization, and cDNA cloning of a novel soluble saxitoxin and tetrodotoxin binding protein from plasma of the puffer fish, Fugu pardalis. , 2001, European journal of biochemistry.

[32]  M. Yotsu-Yamashita CHEMISTRY OF PUFFER FISH TOXIN , 2001 .

[33]  S. Sato,et al.  Frequent occurrence of paralytic shellfish poisoning toxins as dominant toxins in marine puffer from tropical water. , 2000, Toxicon : official journal of the International Society on Toxinology.

[34]  T. Noguchi,et al.  Transformation of Gonyautoxins in the Xanthid Crab Atergatis floridus , 1998 .

[35]  O. Arakawa,et al.  Occurrence of paralytic shellfish poisons in Thai freshwater puffers. , 1997, Toxicon : official journal of the International Society on Toxinology.

[36]  O. Arakawa,et al.  Occurrence of paralytic shellfish poison in Bangladeshi freshwater puffers. , 1997, Toxicon : official journal of the International Society on Toxinology.

[37]  S. Sato,et al.  Saxitoxin as a toxic principle of a freshwater puffer, Tetraodon fangi, in Thailand. , 1997, Toxicon : official journal of the International Society on Toxinology.

[38]  T. Noguchi,et al.  Occurrence of 11-Oxotetrodotoxin and 11-Nortetrodotoxin-6 (R)-ol in a Xanthid Crab Atergatis loridus Collected at Kojima, Ishigaki Island , 1994 .

[39]  T. Noguchi,et al.  Occurrence of carbamoyl-N-hydroxy derivatives of saxitoxin and neosaxitoxin in a xanthid crab Zosimus aeneus. , 1994, Toxicon : official journal of the International Society on Toxinology.

[40]  T. Noguchi,et al.  Resistibility of toxic and nontoxic pufferfish against tetrodotoxin , 1985 .

[41]  T. Yasumoto,et al.  Tetrodotoxin derivatives in puffer fish. , 1985, Toxicon : official journal of the International Society on Toxinology.

[42]  J. Jeon,et al.  Toxicity of the cultured pufferfish Fugu rubripes rubripes along with their resistibility against tetrodotoxin , 1984 .

[43]  T. Yasumoto,et al.  Occurrence of saxitoxin in puffer fish. , 1984, Toxicon : official journal of the International Society on Toxinology.

[44]  M. Kodama,et al.  Occurrence of saxitoxin and other toxins in the liver of the pufferfish Takifugu pardalis. , 1983, Toxicon : official journal of the International Society on Toxinology.

[45]  Y. Shimizu,et al.  Transformation of paralytic shellfish toxins as demonstrated in scallop homogenates. , 1981, Science.