An almost nontoxic tetrodotoxin analog, 5,6,11-trideoxytetrodotoxin, as an odorant for the grass puffer

Abstract Toxic puffers contain the potent neurotoxin, tetrodotoxin (TTX). Although TTX is considered to serve as a defense substance, previous behavioral studies have demonstrated that TTX acts as an attractive pheromone for some toxic puffers. To elucidate the physiological mechanism of putative ph...

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Main Authors: Yoshihisa Noguchi, Takehisa Suzuki, Keigo Matsutani, Ryo Sakakibara, Ryota Nakahigashi, Masaatsu Adachi, Toshio Nishikawa, Hideki Abe
Format: Article
Language:English
Published: Nature Portfolio 2022-09-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-022-19355-6
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author Yoshihisa Noguchi
Takehisa Suzuki
Keigo Matsutani
Ryo Sakakibara
Ryota Nakahigashi
Masaatsu Adachi
Toshio Nishikawa
Hideki Abe
author_facet Yoshihisa Noguchi
Takehisa Suzuki
Keigo Matsutani
Ryo Sakakibara
Ryota Nakahigashi
Masaatsu Adachi
Toshio Nishikawa
Hideki Abe
author_sort Yoshihisa Noguchi
collection DOAJ
description Abstract Toxic puffers contain the potent neurotoxin, tetrodotoxin (TTX). Although TTX is considered to serve as a defense substance, previous behavioral studies have demonstrated that TTX acts as an attractive pheromone for some toxic puffers. To elucidate the physiological mechanism of putative pheromonal action of TTX, we examined whether grass puffers Takifugu alboplumbeus can detect TTX. Electroolfactogram (EOG) results suggest that the olfactory epithelium (OE) of grass puffers responded to a type of TTX analog (5,6,11-trideoxyTTX), although it did not respond to TTX. We also examined the attractive action of 5,6,11-trideoxyTTX on grass puffers by recording their swimming behavior under dark conditions. Grass puffers preferred to stay on the side of the aquarium where 5,6,11-trideoxyTTX was administered, and their swimming speed decreased. Additionally, odorant-induced labeling of olfactory sensory neurons by immunohistochemistry against neural activity marker (phosphorylated extracellular signal regulated kinase; pERK) revealed that labeled olfactory sensory neurons were localized in the region surrounding “islets” where there was considered as nonsensory epithelium. 5,6,11-trideoxyTTX has been known to accumulate in grass puffers, but its toxicity is much lower (almost nontoxic) than TTX. Our results suggest that toxic puffers may positively use this TTX analog, which has been present in their body with TTX but whose function was unknown, as an odorant for chemical communication or effective TTX accumulation.
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spelling doaj.art-294104921c1b4b438fb675c2d050dd6a2022-12-22T01:44:44ZengNature PortfolioScientific Reports2045-23222022-09-0112111010.1038/s41598-022-19355-6An almost nontoxic tetrodotoxin analog, 5,6,11-trideoxytetrodotoxin, as an odorant for the grass pufferYoshihisa Noguchi0Takehisa Suzuki1Keigo Matsutani2Ryo Sakakibara3Ryota Nakahigashi4Masaatsu Adachi5Toshio Nishikawa6Hideki Abe7Laboratory of Fish Biology, Graduate School of Bioagricultural Sciences, Nagoya UniversityLaboratory of Fish Biology, Graduate School of Bioagricultural Sciences, Nagoya UniversityLaboratory of Fish Biology, Graduate School of Bioagricultural Sciences, Nagoya UniversityLaboratory of Organic Chemistry, Graduate School of Bioagricultural Sciences, Nagoya UniversityLaboratory of Organic Chemistry, Graduate School of Bioagricultural Sciences, Nagoya UniversityLaboratory of Organic Chemistry, Graduate School of Bioagricultural Sciences, Nagoya UniversityLaboratory of Organic Chemistry, Graduate School of Bioagricultural Sciences, Nagoya UniversityLaboratory of Fish Biology, Graduate School of Bioagricultural Sciences, Nagoya UniversityAbstract Toxic puffers contain the potent neurotoxin, tetrodotoxin (TTX). Although TTX is considered to serve as a defense substance, previous behavioral studies have demonstrated that TTX acts as an attractive pheromone for some toxic puffers. To elucidate the physiological mechanism of putative pheromonal action of TTX, we examined whether grass puffers Takifugu alboplumbeus can detect TTX. Electroolfactogram (EOG) results suggest that the olfactory epithelium (OE) of grass puffers responded to a type of TTX analog (5,6,11-trideoxyTTX), although it did not respond to TTX. We also examined the attractive action of 5,6,11-trideoxyTTX on grass puffers by recording their swimming behavior under dark conditions. Grass puffers preferred to stay on the side of the aquarium where 5,6,11-trideoxyTTX was administered, and their swimming speed decreased. Additionally, odorant-induced labeling of olfactory sensory neurons by immunohistochemistry against neural activity marker (phosphorylated extracellular signal regulated kinase; pERK) revealed that labeled olfactory sensory neurons were localized in the region surrounding “islets” where there was considered as nonsensory epithelium. 5,6,11-trideoxyTTX has been known to accumulate in grass puffers, but its toxicity is much lower (almost nontoxic) than TTX. Our results suggest that toxic puffers may positively use this TTX analog, which has been present in their body with TTX but whose function was unknown, as an odorant for chemical communication or effective TTX accumulation.https://doi.org/10.1038/s41598-022-19355-6
spellingShingle Yoshihisa Noguchi
Takehisa Suzuki
Keigo Matsutani
Ryo Sakakibara
Ryota Nakahigashi
Masaatsu Adachi
Toshio Nishikawa
Hideki Abe
An almost nontoxic tetrodotoxin analog, 5,6,11-trideoxytetrodotoxin, as an odorant for the grass puffer
Scientific Reports
title An almost nontoxic tetrodotoxin analog, 5,6,11-trideoxytetrodotoxin, as an odorant for the grass puffer
title_full An almost nontoxic tetrodotoxin analog, 5,6,11-trideoxytetrodotoxin, as an odorant for the grass puffer
title_fullStr An almost nontoxic tetrodotoxin analog, 5,6,11-trideoxytetrodotoxin, as an odorant for the grass puffer
title_full_unstemmed An almost nontoxic tetrodotoxin analog, 5,6,11-trideoxytetrodotoxin, as an odorant for the grass puffer
title_short An almost nontoxic tetrodotoxin analog, 5,6,11-trideoxytetrodotoxin, as an odorant for the grass puffer
title_sort almost nontoxic tetrodotoxin analog 5 6 11 trideoxytetrodotoxin as an odorant for the grass puffer
url https://doi.org/10.1038/s41598-022-19355-6
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