An Adenosine Receptor for Olfaction in Fish

• Published in: Current biology Vol. 27; no. 10; pp. 1437 - 1447.e4
• Main Authors: Wakisaka, Noriko, Miyasaka, Nobuhiko, Koide, Tetsuya, Masuda, Miwa, Hiraki-Kajiyama, Towako, Yoshihara, Yoshihiro
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 22.05.2017
• Subjects: Adenosine - metabolism; adenosine receptor; Adenosine Triphosphatases - metabolism; Adenosine Triphosphate - metabolism; Animals; aquatic vertebrates; ATP; attraction; Behavior, Animal; Calcium - metabolism; ecto-nucleotidase; food searching; Nose - physiology; olfaction; Olfactory Mucosa - cytology; Olfactory Mucosa - physiology; Olfactory Receptor Neurons - cytology; Olfactory Receptor Neurons - physiology; Phylogeny; Receptors, Purinergic P1 - metabolism; Smell - physiology; zebrafish; Zebrafish - physiology; attraction; adenosine receptor; olfaction; zebrafish; ATP; ecto-nucleotidase; food searching; aquatic vertebrates
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2017.04.014

Nucleotides released from food sources into environmental water are supposed to act as feeding cues for many fish species. However, it remains unknown how fish can sensitively detect those nucleotides. Here we discover a novel olfactory mechanism for ATP sensing in zebrafish. Upon entering into the nostril, ATP is efficiently converted into adenosine through enzymatic reactions of two ecto-nucleotidases expressed in the olfactory epithelium. Adenosine subsequently activates a small population of olfactory sensory neurons expressing a novel adenosine receptor A2c that is unique to fishes and amphibians. The information is then transmitted to a single glomerulus in the olfactory bulb and further to four regions in higher olfactory centers. These results provide conclusive evidence for a sophisticated enzyme-linked receptor mechanism underlying detection of ATP as a food-derived attractive odorant linking to foraging behavior that is crucial and common to aquatic lower vertebrates. [Display omitted] •A novel adenosine receptor “A2c” is a chemosensor for olfaction•The A2c gene is specific to and highly conserved in fishes and amphibians•ATP is actively converted to adenosine by two ecto-nucleotidases in zebrafish nose•ATP and adenosine attract zebrafish Wakisaka et al. discover a novel adenosine receptor, A2c, which is specific and common to fish and amphibian species. Upon entering the zebrafish nostril, ATP is efficiently converted to adenosine by two ecto-nucleotidases in the olfactory epithelium. Adenosine then activates A2c-expressing olfactory sensory neurons and evokes attractive responses.