Gaseous neuromodulator-related genes expressed in the brain of honeybee Apis mellifera

Takayuki Watanabe, Mika Kikuchi, Dai Hatakeyama, Takumi Shiga, Takehiro Yamamoto, Hitoshi Aonuma, Masakazu Takahata, Norio Suzuki, Etsuro Ito

Research output: Contribution to journalArticlepeer-review

22 Citations (Scopus)


Nitric oxide (NO), hydrogen sulfide (H2S), and carbon monoxide (CO) are thought to act as gaseous neuromodulators in the brain across species. For example, in the brain of honeybee Apis mellifera, NO plays important roles in olfactory learning and discrimination, but the existence of H2S- and CO-mediated signaling pathways remains unknown. In the present study, we identified the genes of nitric oxide synthase (NOS), soluble guanylyl cyclase (sGC), cystathionine β-synthase (CBS), and heme oxygenase (HO) from the honeybee brain. The honeybee brain contains at least one gene for each of NOS, CBS, and HO. The deduced proteins for NOS, CBS, and HO are thought to contain domains to generate NO, H2S, and CO, respectively, and to contain putative Ca2+/calmodulin-binding domains. On the other hand, the honeybee brain contains three subunits of sGC: sGCα1, sGCβ1, and sGCβ3. Phylogenetic analysis of sGC revealed that Apis sGCα1 and sGCβ1 are closely related to NO- and CO-sensitive sGC subunits, whereas Apis sGCβ3 is closely related to insect O2-sensitive sGC subunits. In addition, we performed in situ hybridization for Apis NOS mRNA and NADPH-diaphorase histochemistry in the honeybee brain. The NOS gene was strongly expressed in the optic lobes and in the Kenyon cells of the mushroom bodies. NOS activity was detected in the optic lobes, the mushroom bodies, the central body complex, the lateral protocerebral lobes, and the antennal lobes. These findings suggest that NO is involved in various brain functions and that H 2S and CO can be endogenously produced in the honeybee brain.

Original languageEnglish
Pages (from-to)456-473
Number of pages18
JournalDevelopmental Neurobiology
Issue number4
Publication statusPublished - 2007 Mar
Externally publishedYes


  • Apis
  • Cystathionine β-synthase
  • Heme oxygenase
  • Nitric oxide synthase
  • Soluble guanylyl cyclase

ASJC Scopus subject areas

  • Developmental Neuroscience
  • Cellular and Molecular Neuroscience


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