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Intrabody Tetrodotoxin Distribution and Possible Hypothesis for Its Migration in Ribbon Worms Cephalothrix Cf

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Intrabody Tetrodotoxin Distribution and Possible Hypothesis for Its Migration in Ribbon Worms Cephalothrix Cf marine drugs Article Intrabody Tetrodotoxin Distribution and Possible Hypothesis for Its Migration in Ribbon Worms Cephalothrix cf. simula (Palaeonemertea, Nemertea) Grigorii V. Malykin, Alexei V. Chernyshev and Timur Yu. Magarlamov * A.V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, 690041 Vladivostok, Russia; [email protected] (G.V.M.); [email protected] (A.V.C.) * Correspondence: [email protected]; Tel.: +7-914-661-7949 Abstract: Tetrodotoxin (TTX) is a potent neurotoxin found in many marine and terrestrial animals, but only a few species, such as the ribbon worms of the genus Cephalothrix, accumulate it in extremely high concentrations. The intrabody distribution of TTX in highly toxic organisms is of great interest because it helps researchers to understand the pathways by which the toxin migrates, accumulates, and functions in tissues. Using immunohistochemistry with anti-TTX antibodies, the authors of this study investigated the toxin’s distribution inside the organs, tissues, and cells of Cephalothrix cf. simula. The cell types of TTX-positive tissues were identified by light microscopy. The main sites of TTX accumulation occurred in the secretory cells of the integuments, the microvilli of the epidermal ciliary cells, cephalic glands, the glandular epithelia of the proboscises, the enterocytes of the digestive systems, and nephridia. Obtained data suggest the toxin migrates from the digestive Citation: Malykin, G.V.; system through blood vessels to target organs. TTX is excreted from the body through the nephridia Chernyshev, A.V.; Magarlamov, T.Y. and mucus of epidermal cells. Intrabody Tetrodotoxin Distribution and Possible Hypothesis for Its Keywords: tetrodotoxin; TTX; TTX distribution; CLSM; LC–MC/MC; ribbon worm; Nemertea; Migration in Ribbon Worms Cephalothrix Cephalothrix cf. simula ; toxin migration (Palaeonemertea, Nemertea). Mar. Drugs 2021, 19, 494. https:// doi.org/10.3390/md19090494 1. Introduction Academic Editors: Andrew Turner Nemertea (ribbon worms) comprise a phylum of invertebrates, mainly marine an- and Tim Harwood imals, that are currently divided into three classes: Palaeonemertea, Pilidiophora, and Hoplonemertea [1]. Most nemerteans are active predators but also feed on carrion [2–4]. Received: 26 July 2021 Small crustaceans, polychaetes, and mollusks are high on the list of food priorities. Even Accepted: 26 August 2021 though all the members of the phylum are soft-bodied (i.e., have no external mechanically Published: 29 August 2021 protective structures), they do not usually have natural predators. For hunting and protec- tion, nemerteans secrete a poison containing a wide range of toxins [5,6]. The only toxin Publisher’s Note: MDPI stays neutral found in representatives of all three classes is tetrodotoxin (TTX), which was discovered with regard to jurisdictional claims in more than 30 years ago [7]. In subsequent years, the presence of TTX and its analogues published maps and institutional affil- (TTXs) in nemerteans was reported by various scientific groups [8–11], but the genus iations. Cephalothrix was found to have a toxin concentration comparable to that of the pufferfish and blue-ringed octopuses [8,10–15], making it the only nemertean species to be classified as “extremely toxic” (toxicity higher than 1000 MU/g (178 µg/g)), according to the toxicity classification established by Japan’s Ministry of Health, Labor and Social Security [10]. Copyright: © 2021 by the authors. In 2004, Tanu et al. [16] were the first to investigate the intrabody distribution of TTX Licensee MDPI, Basel, Switzerland. in an unidentified species of the genus Cephalothrix, but they only studied the intrabody This article is an open access article distribution in the foregut region and only described TTX-positive cells, not all the cell types distributed under the terms and in TTX-positive tissues and organs. In the current work, four regions of toxic Cephalothrix cf. conditions of the Creative Commons simula were studied: the precerebral, the foregut, and the anterior and posterior regions of Attribution (CC BY) license (https:// the intestine. At the light-optical level, all the cell types of TTX-positive tissues (the cephalic creativecommons.org/licenses/by/ 4.0/). gland, the integument, the epithelium of digestive system, the glandular epithelium of Mar. Drugs 2021, 19, 494. https://doi.org/10.3390/md19090494 https://www.mdpi.com/journal/marinedrugs Mar. Drugs 2021, 19, 494 2 of 18 Mar. Drugs 2021, 19, 494 2 of 17 (the cephalic gland, the integument, the epithelium of digestive system, the glandular ep- ithelium of the proboscis, and the blood vascular and excretory systems) were character- izedthe proboscis,. Using confocal and the laser blood-scanning vascular microscopy and excretory (CLSM) systems) with anti were-TTX characterized. antibodies and Using cry- osections,confocal laser-scanning the types of cell microscopy accumulating (CLSM) the toxins with anti-TTX were identified antibodies, thereby and cryosections, providing new the datatypes on of toxin cell accumulating localization. I thessues toxins regarding were identified, toxin intake thereby and migration providing with newin data the on nemer- toxin teanlocalization.’s body, as Issues well regardingas TTX functions, toxin intake are discussed. and migration within the nemertean’s body, as well as TTX functions, are discussed. 2. Results 2. Results 2.1. TTX Measurement by LC–MS/MS 2.1. TTX Measurement by LC–MS/MS High-performance liquid chromatography–tandem mass spectrometry (HPLC– MS/MSHigh-performance) analysis revealed liquid TTX chromatography–tandem in whole-body extracts mass of two spectrometry specimens (HPLC–MS/MS) of Cephalothrix analysis revealed TTX in whole-body extracts of two specimens of Cephalothrix cf. simula: cf. simula: in Worm 1, the TTX concentration was 13,478.26 ng/g of body weight, and in in Worm 1, the TTX concentration was 13,478.26 ng/g of body weight, and in Worm 2, it Worm 2, it was 9685 ng/g of body weight (Figure 1). was 9685 ng/g of body weight (Figure1). FigureFigure 1. 1. HighHigh-performance-performance liquid liquid chromatography chromatography–tandem–tandem mass mass spectrometry spectrometry (HPLC (HPLC–MS/MS)–MS/MS) chromatogramschromatograms of of standard standard tetrodotoxin tetrodotoxin (TTX) (TTX) and and TTX TTX obtained obtained from from whole whole-body-body extracts extracts of of twotwo worms worms of of CephalothrixCephalothrix cf.cf. simulasimula.. 2.2.2.2. TTX TTX D Distributionistribution by by CLSM CLSM CLSMCLSM with with the the anti anti-TTX-TTX antibodies antibodies revealed revealed the the toxin toxin in inall all four four regions regions (the (the prece- pre- rebralcerebral region region,, the the foregut, foregut, and and the theanterior anterior and andposterior posterior regions regions of the of intestine) the intestine) of two of wormstwo worms (Figure (Figure 2). An2 ).intense An intense label was label found was in found the glandular in the glandular epithelium epithelium of the proboscis, of the nephridia,proboscis, epidermis, nephridia, foregut epidermis,, and foregut, intestinal and epitheli intestinala (Table epithelia 1 and (TableFigure1 3).and A Figuremedium3).- intensityA medium-intensity label was detected label was in detectedthe cephalic in the gland, cephalic lateral gland, nerve laterals, and nerves, oocytes and (T oocytesable 1). Weak(Table TTX1). Weak-like immunoreactivity TTX-like immunoreactivity was observed was observedin the musculature in the musculature of the body of thewall body and proboscis,wall and proboscis, as well asas in wellthe endothelium as in the endothelium of blood vessels of blood (Table vessels 1). (Table1). Mar. Drugs 2021, 19, 494 3 of 17 Mar. Drugs 2021, 19, 494 3 of 18 Mar. Drugs 2021, 19, 494 3 of 18 FigureFigure 2.2. TetrodotoxinTetrodotoxin (TTX)-like(TTX)-like immunoreactivityimmunoreactivity in different body regions of Cephalothrix cf. simula.. The The c confocal onfocal laser laser scanning micrographs show substacks of transverse sections. Red, TTX-like immunoreactivity; green, -acetylated tubulin scanningFigure 2. micrographs Tetrodotoxin show (TTX) substacks-like immunoreactivity of transverse sections.in different Red, body TTX-like regions immunoreactivity; of Cephalothrix cf. simula green,. Theα-acetylated confocal laser tubulin immunoreactivity; blue, nuclei, (4′,6-diamidino-2-phenylindole (DAPI) stain; yellow, musculature, phalloidin-positive. (А) immunoreactivity;scanning micrographs blue, show nuclei, substacks (40,6-diamidino-2-phenylindole of transverse sections. Red, (DAPI)TTX-like stain; immunoreactivity; yellow, musculature, green, - phalloidin-positive.acetylated tubulin Precerebral region. (В) Foregut region. (C) Anterior intestine region. (D) Posterior intestine region. bv, blood vessel; cg, ce- (Aimmunoreactivity;) Precerebral region. blue (B, nuclei,) Foregut (4′,6 region.-diamidino (C)- Anterior2-phenylindole intestine (DAPI region.) stain (D; yellow) Posterior, musculature, intestine phalloidin region. bv,-positive. blood vessel; (А) phalic gland; ds, dorsal side; ep, epidermis; fg, foregut; in, intestine; ln, lateral nerve; mw, musculature of body wall; pr, pro- cg,Precerebral cephalic gland; region. ds, (В dorsal) Foregut side; region. ep, epidermis; (C) Anterior fg, intestine foregut; region in, intestine;. (D) Posterior ln, lateral intestine nerve; region mw, musculature. bv, blood vessel; of body cg, ce- wall; boscis;phalic rc,
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