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The Journal of Neuroscience, August 19, 2009, 29(33):10184-10190; doi:10.1523/JNEUROSCI.2443-09.2009

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Development/Plasticity/Repair
Evidence for Developmentally Regulated Local Translation of Odorant Receptor mRNAs in the Axons of Olfactory Sensory Neurons

Caroline Dubacq,^1,2 Sophie Jamet,^1,2 and Alain Trembleau^1,2

¹Avenir/Inserm and Fondation pour la Recherche Médicale Team "Development and Plasticity of Neural Networks," Université Pierre et Marie Curie (UPMC), Unité Mixte de Recherche (UMR) 7102, and ²Centre National de la Recherche Scientifique, UMR 7102, F-75005 Paris, France

Correspondence should be addressed to Alain Trembleau, Avenir/Inserm Team, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7102, Université Pierre et Marie Curie, Boîte 12, 9 quai Saint Bernard, 75252 Paris Cedex 05, France. Email: alain.trembleau{at}upmc.fr

Odorant receptor mRNAs are transported within axons of olfactory sensory neurons that project into the olfactory bulb. Odorant receptor proteins have been identified along the distal part of these axons, which raises the possibility of their local synthesis in axons. We took advantage of the anatomical separation between the olfactory mucosa (which contains the sensory neuron cell bodies) and the bulb (which contains sensory axons but no sensory neuron cell bodies) to address this issue using a quantitative biochemical approach. Combining a method that separates polysome-associated mRNAs from untranslated mRNAs with a reverse transcription–quantitative PCR approach, we demonstrate that significant amounts of odorant receptor mRNAs are associated with polysomes in the sensory axons of the adult mouse bulb. We thus provide the first evidence for local synthesis of odorant receptor proteins in these axons. Interestingly, the rate of odorant receptor mRNA translation in axons is significantly greater during periods when the proportion of immature axons is higher (i.e., at postnatal day 4 or on regeneration after chemical lesion in adults). In contrast, the olfactory marker protein mRNA, which is restricted to mature axons, is translated at a low and constant level. Overall, we demonstrate that translation levels of odorant receptor mRNAs in axons are developmentally regulated, and positively correlated to the stage of axonal growth into the bulb. Given the established function of odorant receptors in the axonal wiring of sensory projections, we propose that this regulated axonal translation may play a role in the development and maintenance of the glomerular array.

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Received May 21, 2009; revised July 7, 2009; accepted July 10, 2009.

Correspondence should be addressed to Alain Trembleau, Avenir/Inserm Team, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7102, Université Pierre et Marie Curie, Boîte 12, 9 quai Saint Bernard, 75252 Paris Cedex 05, France. Email: alain.trembleau{at}upmc.fr

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