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The Journal of Neuroscience, September 1, 1999, 19(17):7468-7475

Cloning and Expression of a Queen Pheromone-Binding Protein in the Honeybee: an Olfactory-Specific, Developmentally Regulated Protein

Emmanuelle Danty¹, Loïc Briand², Christine Michard-Vanhée³, Valérie Perez², Gérard Arnold¹, Odile Gaudemer², Dominique Huet³, Jean-Claude Huet², Christian Ouali², Claudine Masson¹, and Jean-Claude Pernollet²

¹ Centre Européen des Sciences du Goût, Centre National de la Recherche Scientifique (CNRS), Unité "Olfaction, Gustation, Nutrition," 21000 Dijon, France, ² Unité de Recherches de Biochimie et Structure des Protéines, Institut National de la Recherche Agronomique Unité Recherche 477, 78352 Jouy-en-Josas Cedex, France, and ³ Neurobiologie Expérimentale et Théorie des Systèmes Complexes, CNRS Unité Propre de Recherche 9081, 75231 Paris Cedex 05, France

Odorant-binding proteins (OBPs) are small abundant extracellular proteins thought to participate in perireceptor events of odor-pheromone detection by carrying, deactivating, and/or selecting odor stimuli. The honeybee queen pheromone is known to play a crucial role in colony organization, in addition to drone sex attraction. We identified, for the first time in a social insect, a binding protein called antennal-specific protein 1 (ASP1), which binds at least one of the major queen pheromone components. ASP1 was characterized by cDNA cloning, expression in Pichia pastoris, and pheromone binding. In situ hybridization showed that it is specifically expressed in the auxiliary cell layer of the antennal olfactory sensilla. The ASP1 sequence revealed it as a divergent member of the insect OBP family. The recombinant protein presented the exact characteristics of the native protein, as shown by mass spectrometry, and N-terminal sequencing and exclusion-diffusion chromatography showed that recombinant ASP1 is dimeric. ASP1 interacts with queen pheromone major components, opposite to another putative honeybee OBP, called ASP2. ASP1 biosynthetic accumulation, followed by nondenaturing electrophoresis during development, starts at day 1 before emergence, in concomitance with the functional maturation of olfactory neurons. The isobar ASP1b isoform appears simultaneously to ASP1a in workers, but only at ~2 weeks after emergence in drones. Comparison of in vivo and heterologous expressions suggests that the difference between ASP1 isoforms might be because of dimerization, which might play a physiological role in relation with mate attraction.

Key words: queen pheromone; binding protein; olfaction; antenna; sensilla; honeybee; Pichia pastoris expression

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Copyright © 1999 Society for Neuroscience  0270-6474/99/19177468-08$05.00/0

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