Neuroligin-associated microRNA-932 targets actin and regulates memory

Increasing evidence suggests microRNAs (miRNAs) control levels of mRNA expression during development of the nervous system and during sensory elicited remodelling of the brain. We used an associative olfactory learning paradigm (proboscis extension response) in the honeybee Apis mellifera to detect gene expression changes in the brain. Transcriptome analysis of bees trained to associate an odor with a reward and control bees exposed to air without reward, helped us abstract mRNA-miRNA interactions for empirical testing. Functional studies, feeding cholesterol-conjugated antisense RNA to bees resulted in the inhibition of miR-210 and of miR-932 that is embedded within the neuroligin 2 (Nlg2) gene involved in synapse development. Loss of miR-932 prevents long-term memory formation but not learning. We validated 3’UTR target site interactions of miR-932 and show miR-932 dysregulates actin, a key cytoskeletal molecule involved in neuronal development and activity-dependent plasticity of the brain. The analysis used Air group (no odor learning) as control sample for comparison to two groups of odor-conditioned bees: linalool and floral mix.