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BMC Biol. 2012; 10: 56.
Published online Jun 21, 2012. doi:  10.1186/1741-7007-10-56
PMCID: PMC3414785
A carboxylesterase, Esterase-6, modulates sensory physiological and behavioral response dynamics to pheromone in Drosophila
Thomas Chertemps,1 Adrien François,1,2 Nicolas Durand,1 Gloria Rosell,3 Teun Dekker,4 Philippe Lucas,2 and Martine Maïbèche-Coisnecorresponding author1
1Université Pierre et Marie Curie, UMR 1272, Physiologie de l'Insecte, Signalisation et Communication, F-75252, Paris, France
2INRA, UMR 1272, Physiologie de l'Insecte, Signalisation et Communication, F-78026, Versailles, France
3University of Barcelona, Faculty of Pharmacy, Unit of Medicinal Chemistry, 08028, Barcelona, Spain
4Swedish University of Agricultural Sciences, Department of Plant Protection Biology, 23053, Alnarp, Sweden
corresponding authorCorresponding author.
Thomas Chertemps: thomas.chertemps/at/snv.jussieu.fr; Adrien François: adrien.francois/at/versailles.inra.fr; Nicolas Durand: nfdurand/at/gmail.com; Gloria Rosell: grpqob/at/iiqab.csic.es; Teun Dekker: teun.dekker/at/slu.fr; Philippe Lucas: philippe.lucas/at/versailles.inra.fr; Martine Maïbèche-Coisne: martine.maibeche/at/snv.jussieu.fr
Received February 27, 2012; Accepted June 21, 2012.
Abstract
Background
Insects respond to the spatial and temporal dynamics of a pheromone plume, which implies not only a strong response to 'odor on', but also to 'odor off'. This requires mechanisms geared toward a fast signal termination. Several mechanisms may contribute to signal termination, among which odorant-degrading enzymes. These enzymes putatively play a role in signal dynamics by a rapid inactivation of odorants in the vicinity of the sensory receptors, although direct in vivo experimental evidences are lacking. Here we verified the role of an extracellular carboxylesterase, esterase-6 (Est-6), in the sensory physiological and behavioral dynamics of Drosophila melanogaster response to its pheromone, cis-vaccenyl acetate (cVA). Est-6 was previously linked to post-mating effects in the reproductive system of females. As Est-6 is also known to hydrolyze cVA in vitro and is expressed in the main olfactory organ, the antenna, we tested here its role in olfaction as a putative odorant-degrading enzyme.
Results
We first confirm that Est-6 is highly expressed in olfactory sensilla, including cVA-sensitive sensilla, and we show that expression is likely associated with non-neuronal cells. Our electrophysiological approaches show that the dynamics of olfactory receptor neuron (ORN) responses is strongly influenced by Est-6, as in Est-6° null mutants (lacking the Est-6 gene) cVA-sensitive ORN showed increased firing rate and prolonged activity in response to cVA. Est-6° mutant males had a lower threshold of behavioral response to cVA, as revealed by the analysis of two cVA-induced behaviors. In particular, mutant males exhibited a strong decrease of male-male courtship, in association with a delay in courtship initiation.
Conclusions
Our study presents evidence that Est-6 plays a role in the physiological and behavioral dynamics of sex pheromone response in Drosophila males and supports a role of Est-6 as an odorant-degrading enzyme (ODE) in male antennae. Our results also expand the role of Est-6 in Drosophila biology, from reproduction to olfaction, and highlight the role of ODEs in insect olfaction.
Keywords: carboxylesterase, esterase 6, olfaction, pheromone, signal termination
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