Changes in Tissue Distribution of Tetrodotoxin and Its Analogues in Association with Maturation in the Toxic Flatworm, Planocera multitentaculata

Oyama, Hikaru; Ito, M.; Suo, Rei; Goto‐Inoue, Naoko; Morisasa, Mizuki; Mori, Tsukasa; Sugita, Haruo; Mori, Tetsushi; Nakahigashi, Ryota; Adachi, Masaatsu; Nishikawa, Toshio; Itoi, Shiro

doi:10.1007/s10126-022-10179-z

Cited by 12 publications

(5 citation statements)

References 58 publications

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“…In this study, we also report for the first time the detection of TTX in three species (the cnidaria C. parasitica, an unidentified species, and the bivalve T. donacina) and the presence of the TTX analogues 5,6,11 trideoxy TTX and 5,6,11 trideoxy-epi-TTX in invertebrates from Galicia. TTXs have been found in different species of bivalves, gastropods, other molluscs, echinoderms, crustaceans, and even flatworms from different countries (reviewed in several articles [33,34]) all over the world. In the Atlantic coast of the Iberian Peninsula, the presence of TTX has only been documented in Galicia (Spain) in one sample of cockle (2.3 µg kg −1 ) and one sample of an oyster (below LOQ) (species not reported), without analogues [35], and in Portugal in some species of gastropods [36][37][38][39].…”

Section: Discussionmentioning

confidence: 99%

First Report of Two Gymnodimines and Two Tetrodotoxin Analogues in Invertebrates from the North Atlantic Coast of Spain

Rossignoli¹,

Mariño²,

Martín³

et al. 2023

Marine Drugs

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Gymnodimine D (GYM D), 16-desmethyl gymnodimine D (16-desmethyl GYM D), and two tetrodotoxin analogues have been found in invertebrates obtained from the north Atlantic coast of Spain from May 2021 to October 2022. It is the first report of GYMD and 16-desmethyl GYM D in invertebrates worldwide and of the tetrodotoxin analogues, 5,6,11 trideoxy tetrodotoxin (5,6,11 trideoxy TTX) and its isomer (referred to as 5,6,11 trideoxy-epi-TTX), in the north Atlantic Coast of Spain. In this study, we also report for the first time the detection of tetrodotoxin (TTX) in three species (the cnidaria Calliactis parasitica, an unidentified species, and the bivalve Tellina donacina). The prevalence was medium for GYM D and 16-desmethyl GYM D and low for TTXs overall. The concentrations recorded were variable, with maximum values of GYM D in the bivalve Cerastoderma edule (8.8 μg GYM A equivalents kg−1), of 16-desmethyl GYM D in the bivalve Magellana gigas (10 μg GYM A equivalents kg−1) and of TTX and 5,6,11 trideoxy TTX in the cnidaria C. parasitica (49.7 and 233 μg TTX equivalents kg−1, respectively). There is very scarce information about these compounds. Therefore, the reporting of these new detections will increase the knowledge on the current incidence of marine toxins in Europe that the European Food Safety Authority (EFSA), in particular, and the scientific community, in general, have. This study also highlights the importance of analyzing toxin analogues and metabolites for effective monitoring programs and adequate health protection.

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Section: Discussionmentioning

confidence: 99%

First Report of Two Gymnodimines and Two Tetrodotoxin Analogues in Invertebrates from the North Atlantic Coast of Spain

Rossignoli¹,

Mariño²,

Martín³

et al. 2023

Marine Drugs

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“…Previous studies have suggested that toxic puffers prefer to feed on TTX-bearing organisms (Itoi et al 2015(Itoi et al , 2018(Itoi et al , 2020Okabe et al 2019). These TTXbearing organisms also contain TDT (Ito et al 2023;Oyama et al 2022). Furthermore, the ovaries of toxic puffers contain both TTX and TDT (Ito et al 2023), and it is believed that they are leaking out from the cloaca (Matsumura 1995).…”

Section: Discussionmentioning

confidence: 99%

The odor of a nontoxic tetrodotoxin analog, 5,6,11-trideoxytetrodotoxin, is detected by specific olfactory sensory neurons of the green spotted puffers

Suzuki,

Nakahigashi,

Adachi

et al. 2023

Preprint

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Toxic puffers accumulate tetrodotoxin (TTX), a well-known neurotoxin, by feeding on TTX-bearing organisms and using it to defend themselves from predators. Our previous studies have demonstrated that toxic puffers are attracted to 5,6,11-trideoxytetrodotoxin (TDT), a nontoxic TTX analog that is simultaneously accumulated with TTX in toxic puffers and their prey. In addition, activity labeling using immunohistochemistry targeting neuronal activity marker suggests that TDT activates crypt olfactory sensory neurons (OSN) of the green spotted puffer. However, it remains to be determined whether individual crypt OSNs can physiologically respond to TDT and whether TDT is processed differently from other odors in the brain. By employing electroporation to express GCaMP6s in OSNs, we successfully identified a distinct group of oval OSNs that exhibited a specific calcium response when exposed to TDT in green spotted puffers. These oval OSNs showed no response to amino acids (AAs), which serve as food odor cues for teleosts. Furthermore, immunohistochemistry targeting neural activity markers revealed that TDT and AAs odors activate extensively overlapping areas in the dorsomedial olfactory bulb. These results suggest that while different types of OSNs detect TDT and AAs in the olfactory epithelium, these substances are processed as similar odors in the olfactory bulb. The TDT odor may act as a chemoattractant for finding conspecific toxic puffers and for feeding TTX-bearing organisms for effective toxification.

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“…Recently, it has been reported that P. multitentaculata possess a variety of TTX analogs, including dideoxyTTXs, deoxyTTXs, and 11-norTTX-( S )-ol, in addition to large amounts of TTX and 5,6,11-trideoxyTTX (Suo et al 2022 ). Although the internal localization of these TTX analogs in the flatworm changes during growth (Oyama et al 2022 ), there is no difference in the composition of TTX analogs between samples collected in different sites (Suo et al 2024 ), indicating that the flatworm might possess biosynthetic processes of TTX in the body. On the other hand, there is no information on TTX analogs in planocerid flatworms, with the exception of the planocerid in Guam (Ritson-Williams et al 2006 ) and P. multitentaculata as mentioned (Suo et al 2022 , 2024 ).…”

Section: Introductionmentioning

confidence: 99%

Japanese Planocerid Flatworms: Difference in Composition of Tetrodotoxin and Its Analogs and the Effects of Ingestion by Toxin-Bearing Fishes in the Ryukyu Islands, Japan

Ueda,

Ito,

Yonezawa

et al. 2024

Mar Biotechnol

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Tetrodotoxin (TTX), known as pufferfish toxin, is a potent neurotoxin blocking sodium channels in muscle and nerve tissues. TTX has been detected in various taxa other than pufferfish, including marine polyclad flatworms, suggesting that pufferfish toxin accumulates in fish bodies via food webs. The composition of TTX and its analogs in the flatworm Planocera multitentaculata was identical to those in wild grass puffer Takifugu alboplumbeus. Previously, Planocera sp. from Okinawa Island, Japan, were reported to possess high level of TTX, but no information was available on TTX analogs in this species. Here we identified TTX and analogs in the planocerid flatworm using high-resolution liquid chromatography–mass spectrometry, and compared the composition of TTX and analogs with those of another toxic and non-toxic planocerid species. We show that the composition of TTX and several analogs, such as 5,6,11-trideoxyTTX, dideoxyTTXs, deoxyTTXs, and 11-norTTX-6(S)-ol, of Planocera sp. was identical to those of toxic species, but not to its non-toxic counterpart. The difference in the toxin composition was reflected in the phylogenetic relationship based on the mitochondrial genome sequence. A toxification experiment using predatory fish and egg plates of P. multitentaculata demonstrated that the composition of TTX and analogs in wild T. alboplumbeus juveniles was reproduced in artificially toxified pufferfish. Additionally, feeding on the flatworm egg plates enhanced the signal intensities of all TTX compounds in Chelonodon patoca and that of deoxyTTXs in Yongeichthys criniger.

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Changes in Tissue Distribution of Tetrodotoxin and Its Analogues in Association with Maturation in the Toxic Flatworm, Planocera multitentaculata

Cited by 12 publications

References 58 publications

First Report of Two Gymnodimines and Two Tetrodotoxin Analogues in Invertebrates from the North Atlantic Coast of Spain

First Report of Two Gymnodimines and Two Tetrodotoxin Analogues in Invertebrates from the North Atlantic Coast of Spain

The odor of a nontoxic tetrodotoxin analog, 5,6,11-trideoxytetrodotoxin, is detected by specific olfactory sensory neurons of the green spotted puffers

Japanese Planocerid Flatworms: Difference in Composition of Tetrodotoxin and Its Analogs and the Effects of Ingestion by Toxin-Bearing Fishes in the Ryukyu Islands, Japan

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