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Toxicity of Trumpet Shells Inhabiting the Coastal Waters of Kagoshima Prefecture, Along with Identification of the Responsible Toxin

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Toxicity of Trumpet Shells Inhabiting the Coastal Waters of Kagoshima Prefecture, Along with Identification of the Responsible Toxin Bulletin of the Japanese Society of Scientific Fisheries 51(10), 1727-1731 (1985) Toxicity of Trumpet Shells Inhabiting the Coastal Waters of Kagoshima Prefecture, along with Identification of the Responsible Toxin Tamao NOGUCHI,*1 Joong Kyun JEON,*1 Junichi MARUYAMA,*1 Yukinori SATO,*2 Toshio SAISHO,*2 and Kanehisa HASHIMOTO*1 (Accepted April 12, 1985) A total of 70 specimens of the trumpet shell Charonia sauliae ("boshubora") were collected at eight places in Kagoshima Prefecture in October 1983 through May 1984. Their digestive glands were removed and examined for toxicity by the assay method of tetrodotoxin (TTX). Remarkable regional and individual variations in toxicity were noted. On the whole, the ratio of toxic to total specimens was 43%, the highest and average toxicity scores being 1,670 and 81 MU/g digestive gland, respectively. Trumpet shell toxin was identified as TTX from thin-layer chromatographic and electrophoretic behaviors, along with GC-mass spectrum. Small pieces of a starfish Astropecten scoparius which were found in the digestive canal of some specimens showed a toxicity of 8-30MU/g, suggesting the involvement of this starfish in toxification of the trumpet shell. Two poisoning cases due to ingestion of the Materials and Methods trumpet shell Charonia sauliae ("boshubora") Materials have thus far been recorded: One in Shimizu, A total of 70 specimens of the trumpet shell Shizuoka Prefecture in 1979,1) and the other at Charonia sauliae ("boshubora") were collected at Mihama, Wakayama Prefecture in 1982.2) Sub eight places in Kagoshima Prefecture in October sequent survey disclosed that most of the trumpet 1983 through May 1984 (Fig. 1). The specimens shell specimens collected from both places were were mostly caught by a trawling net, and some more or less toxic in the digestive gland. In by a gill net for lobster or diving. addition, the responsible toxin was rather unex Small pieces of a starfish which was identified pectedly identified as tetrodotoxin (TTX), which as Astropecten scoparius, were collected from the was supposed to have come from a toxic starfish digestive canal contents of two trumpet shell Astropecten polyacanthus by the food chain.3) specimens. Later, we performed a toxicity survey on the Those trumpet shell and starfish specimens trumpet shell specimens collected from Mie*3 and -20℃ thus collected were kept frozen below Miyazaki4) Prefectures whose catches of this shell until used. are high, finding that some of their digestive glands were toxified at a high level. Assay of Toxicity The present study was undertaken to survey Each trumpet shell was partially thawed and the toxicity of trumpet shells inhabiting coastal the digestive gland was removed. A portion of areas of Kagoshima Prefecture. The results it was examined for toxicity by the official assay showed that some specimens of this gastropod method of TTX.5) In the case of starfish, the mollusk were highly toxified, and that the respon whole debris obtained from each of the two trumpet sible toxin was TTX. shell specimens was subjected to toxicity assay similarly. "Toxic" defined here was ≧5MU/g digestive *1 Laboratory of Marine Biochemistry, Faculty of Agriculture, University of Tokyo, Bunkyo, Tokyo 113, Japan (野 口 玉 雄 ・銭 重 均 ・丸 山 純 一 ・佐 藤 之 紀 ・橋 本 周 久:東 京 大 学 農 学 部). *2 Faculty of Fisheries , Kagoshima University, Shimoarata-4, Kagoshima 890, Japan (税所 俊 郎:鹿 児 島大 学水 産 学部) *3 T . NOGUCHI et al.: unpublished data. 1728 NOGUCHI et al. MU/mg) was treated batchwise with 200g of activated charcoal (Wako), and the toxin adsorbed was eluted with 2 volumes of 1% acetic acid in methanol four times. The eluates were combined, condensed and finally freeze-dried (total toxicity: 15,000MU, specific toxicity: 1.3MU/mg). The residue was dissolved in a small amount of 0.1M ammonium acetate (pH 6) and chromatographed on a CM Sephadex C-25 (NH4+) column (2.6×32cm)by means of a linear gradient of 0.1-0.4M ammonium acetate at pH 6. Toxic fractions (total toxicity: 11,400MU, specific toxicity: 47MU/mg) were combined and freeze-dried. The residue was dissolved in a small amount of water and chro matographed on a column (0.8×96cm)of Bio Rex 70 (H+) by a linear gradient of 0-0.1M acetic acid. Toxic fractions were combined and sub mitted to rechromatography in the same manner as above. Toxic fractions were combined and lyophilized. Approximately 3mg of trumpet shell toxin (total toxicity: 7,000MU) thus ob tained was analyzed as described below, with an authentic specimen of TTX which was prepared from pufferfish ovary as reported before.6) Thin-Layer Chromatography Thin-layer chromatography (TLC) was per formed on 10×10cm Whatman LHP-K plates with a solvent system of pyridine-ethyl acetate acetic acid-water (15: 5: 3: 4). Toxins were visualized as a yellow or blue fluorescent spot under UV light (365nm) by spraying 1% H2O2 Fig. 1. Map showing eight sampling places of and 10% KOH, followed by heating at 110℃ trumpet shell specimens in Kagoshima Prefec for 10min. ture. Electrophoresis Electrophoresis was performed on 5×18㎝ gland of trumpet shell and starfish. cellulose acetate strips (Chemetron) using 0.08M Tris-HC1 buffer (pH 8.7) under a constant current Isolation of Trumpet Shell Toxin of 0.8mA/cm width for 30min. Toxins were Remaining portions of the digestive glands visualized as in TLC. (750g) were combined and used to isolate toxin by combination of our previous methods for Gas Chromatography-Mass Spectrometry (GC-MS) TTX.1-3) To the combined material was added 3 The trimethylsilyl (TMS) derivative of 2-amino volumes of 1% acetic acid in methanol, and homo 6-hydroxymethyl-8-hydroxyquinazoline (C9-base) genized with an Ultra-Turrax homogenizer. The was prepared from trumpet shell toxin and the homogenate was centrifuged at 6,000×g for 10 authentic TTX, by the procedure reported pre min. The above procedure was repeated two viously.1-3) Both TMS derivatives thus provided more times for the residue, and the supernatants were analyzed with a GC-mass spectrometer obtained were combined, condensed under re JEOL JMS DX-300. on a column (O.3×200cm) duced pressure, and defatted with dichloro packed with 2% OV-1. Column temperature was methane. raised from 190℃ to 220℃ at a rate of 4℃/min. A portion (30,000MU) of the aqueous layer The flow rate of inlet helium gas was kept at (total toxicity: 59,000 MU, specific toxicity: 0.7 20ml/min. Ionizing voltage was 70eV. Toxicity of Trumpet Shells in Kagoshima Prefecture 1729 Table 1. A summary of toxicity scores of 70 trumpet shell specimens collected at eight places in Kagoshima Prefecture, along with those in other prefectures Highest toxicity No. of toxic*1 Average loxicity Place of Year of specimens/No. of ±S. E. MU/g collection collection specimens (MU/g digestive -MU per digestive assayed giand) individual gland Kagoshima Prefecture: Akune 1983-'84 6/13 (46)*2 187±131 1,670 20,000 Koshikijima Islands 1984 6/12 (50) 170±115 1,400 53,000 Bonotsu 1984 1/7 (14) 34±34 240 5,000 Yamagawa 1983-'84 4/21 (19) 21±19 400 12,000 Onejiine 1983-'84 1/5 (20) 4±4 21 670 Uchinoura 1984 3/5 (60) 54±37 200 6,600 Shibushi 1983-'84 1/2 (50) 15±15 30 420 Sata 1984 1/5 (20) 38±38 190 5,700 Total 30/70 (43) 81±33 Other Prefectures: Shizuoka1) 1979-'80 40/42 (95) 235±54*3 1.950 54,600*3 Wakayama2) 1982-'83 50/74 (68) 45士7*3 480 36,960 Mie*3 1982-'83 102/155 (66) 85 460 12,000 Miyazaki4) 1983-'84 72/375(19) 4*3 106 5,300 *1 "Toxic" defined here is ≧5MU/g digestive gland. *2 The number in parenthesis represents the frequency of toxic specimens (%). *3 T . Nonucin et al.: unpublished data. Results and Discussion Toxicityof Trumpet Shell Specimens Out of the 70 trumpet shell specimens assayed, 30 were found to be toxic (Table 1). The fre quency of toxic specimens was calculated to be 43% on an average. However, the frequency varied from 14 to 60%, depending upon the place of collection. The average toxicity of all the specimens was calculated to be 81MU/g digestive gland, assum Fig. 2. TLC of trumpet shell toxin and an authentic ing for convenience that the toxic scores of all TTX. nontoxic specimens were zero. The highest toxicity recorded was 1,670MU/g digestive gland of an Akune specimen. The total toxicity of this one was calculated to be 20,000MU. The highest total toxicity was 53,000MU in a Koshikijima specimen,the value which was equivalent to more than five times the minimum lethal dose in human. Regionality of Toxicity Fig. 3. Electrophoresis of trumpet shell toxin and The regionality in toxicity was clearly recogniz an authentic TTX. ed, as shown in Table 1. The trumpet shell speci mens from Akune and Koshikijima Islands front from Bonotsu which also faces the East China Sea ing on the East China Sea were notable: The fre were, however, rather low in these three parame quency of the toxic specimens was 46 and 50%, ters. The specimens collected from Yamagawa, respectively. In both the average and highest Onejime, and Sata which are situated at the mouth toxicity, Akune specimens (187MU/g, 1,670 of Kagoshima Bay showed low scores in the MU/g) were highest, followed by Koshikijima frequency of toxic specimens (19-20%) and average specimens (170MU/g, 1,400MU/g).
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