A unique transcriptome at the brain-environment interface: local translation in the rat olfactory epithelium

All olfactory epithelium cells, including rapidly self-renewing olfactory sensory neurons (OSN), are continuously subjected to external airborne aggressions. We hypothesized that the apical part of rat olfactory epithelia (AOE) could be the site of a local translation to be able to respond rapidly to external stimuli. We purified significant amounts of mRNAs from AOE. Sequencing of the cDNA library identified 348 mRNA species. Of these, the 220 AOE transcripts encoding proteins with known biological functions were classified in functional groups. The main functional class (40%) coded for defense, detoxification, anti-oxidant stress and innate immunity. Other classes comprised mRNAs encoding functions for neuronal metabolism and life (19%), nuclear transcription control (15%), cell survival and proliferation (13%), RNA processing and translation (12%). They did not contain any known members of the olfactory transduction pathway. The expression of a sub-set of AOE transcripts was investigated in sub-cellular AOE fractions highly enriched in ciliated dendrites and in AOE fractions after forced hemilateral OSN-specific degeneration. All the mRNAs tested were found to be: i) present in enriched ciliated dendrite preparations ii) down-regulated after OSN degeneration iii) co-purified with polysomal fractions, suggesting their commitment to local translation. We provide strong evidence that the extreme apical side of the olfactory epithelium expresses a unique transcriptome, whose function is not related to olfaction but mainly to defense and survival. The possible local translation of this transcriptome is demonstrated, in supporting cells as well as in olfactory neuron ciliated dendrites.