The immunoglobulin superfamily (IgSF) has been indicated as functioning in the development and maintenance of nervous systems through cell-cell recognition and communication in several model invertebrates, Drosophila melanogaster and Caenorhabditis elegans. To further explore the functions of the IgSF in the brain of an invertebrate with more complex behavior, we identified and characterized a novel brain-specific Dscam family member, AbsCAM, from honey bee (Apis mellifera). The level of the AbsCAM protein was high in newly hatched bees and was dramatically reduced with age. The AbsCAM protein level was constant among worker bees of the same age performing different tasks, suggesting that it was primarily determined by age and not task in adult brains. Two different AbsCAM transcripts (AbsCAM-Ig7A and B) were generated by the alternative splicing of exon 11 encoding immunoglobulin domain 7 in an age-dependent manner. AbsCAM was expressed in the major brain neuropils where the synaptic density was high. AbsCAM can mediate the isoform-specific homophilic cell adhesion in vitro, and affected the axonal projections in Drosophila embryonic central nervous system and adult mushroom body by ectopic expression. Furthermore, AbsCAM promoted the neurite outgrowth of cultured neurons isolated from honey bee pupal brains. These results thus suggest that AbsCAM is the first honey bee IgSF implicated as functioning in neuronal wiring during honey bee brain development.
Honeybees have been shown to exhibit cognitive performances that were thought to be specific to some vertebrates. However, the molecular and cellular mechanisms of such cognitive abilities of the bees have not been understood. We have identified a novel gene, Mahya, expressed in the brain of the honeybee, Apis mellifera, and other Hymenoptera. Mahya orthologues are present in Deuterostomes but are absent or highly diverged in nematodes and, intriguingly, in two dipteran insects (fruit fly and mosquito) and Lepidoptera (silk moth). Mahya genes encode novel secretory proteins with a follistatin-like domain (Kazal-type serine/threonine protease inhibitor domain and EF-hand calcium-binding domain), two immunoglobulin domains, and a C-terminal novel domain. Honeybee Mahya is expressed in the mushroom bodies and antennal lobes of the brain. Zebra fish Mahya orthologues are expressed in the olfactory bulb, telencephalon, habenula, optic tectum, and cerebellum of the brain. Mouse Mahya orthologues are expressed in the olfactory bulb, hippocampus, and cerebellum of the brain. These results suggest that Mahya may be involved in learning and memory and in processing of sensory information in Hymenoptera and vertebrates. Furthermore, the limited existence of Mahya in the genomes of Hymenoptera and Deuterostomes supports the hypothesis that the genes typically represented by Mahya were lost or highly diverged during the evolution of the central nervous system of specific Bilaterian branches under the specific selection and subsequent adaptation associated with different ecologies and life histories.
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