Translocator protein mediates olfactory repulsion.

Translocator protein (TSPO, 18kDa), which was previously known as a peripheral-type benzodiazepine receptor, is associated with psychiatric disorders and acts as a neuroimaging biomarker. However, its function and mechanism in modulating behaviors are less well-known. Herein, we found that TSPO in migratory locusts shows conserved protein traits and is expressed at high levels in the brains. The expression levels of tspo mRNA and protein were higher in brains of solitary locusts than those in gregarious locusts, whereas the mRNA and protein expression levels remained stable during crowding and isolation, suggesting that the expression level of TSPO is potentially associated with behavioral phenotype of solitary locusts. Moreover, tspo RNAi knockdown in the brains of solitary locusts decreased their olfactory repulsion. After RNAi knockdown of tyramine receptor (TyR) in the brains of solitary locusts, RNA-seq analysis identified that a functional class of receptors, which included tspo, was downregulated significantly. Moreover, tspo mRNA and protein expression levels were downregulated and upregulated after TyR RNAi knockdown and activation, respectively. tspo RNAi knockdown in the brains of solitary locusts induced the attractive response and inhibited the function of tyramine (TA)-TyR in inducing olfactory repulsion. In gregarious locusts, tspo RNAi knockdown inhibited the function of TA-TyR inducing olfactory repulsion. This study confirms that TSPO acts as a crucial effector protein in TA-TyR signaling to modulate olfactory repulsion. Furthermore, this study provides a novel mechanism by which TSPO functionally connects a G-protein-coupled receptor and a mitochondria membrane protein in modulating olfactory repulsion.