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An essential role for a CD36-related receptor in pheromone detection in Drosophila

Nature volume 450, pages 289–293 (2007)Cite this article

Abstract

The CD36 family of transmembrane receptors is present across metazoans and has been implicated biochemically in lipid binding and transport1. Several CD36 proteins function in the immune system as scavenger receptors for bacterial pathogens and seem to act as cofactors for Toll-like receptors by facilitating recognition of bacterially derived lipids2,3,4. Here we show that a Drosophila melanogaster CD36 homologue, Sensory neuron membrane protein (SNMP), is expressed in a population of olfactory sensory neurons (OSNs) implicated in pheromone detection. SNMP is essential for the electrophysiological responses of OSNs expressing the receptor OR67d to (Z)-11-octadecenyl acetate (cis-vaccenyl acetate, cVA), a volatile male-specific fatty-acid-derived pheromone that regulates sexual and social aggregation behaviours5,6,7,8. SNMP is also required for the activation of the moth pheromone receptor HR13 by its lipid-derived pheromone ligand (Z)-11-hexadecenal9, but is dispensable for the responses of the conventional odorant receptor OR22a to its short hydrocarbon fruit ester ligands. Finally, we show that SNMP is required for responses of OR67d to cVA when ectopically expressed in OSNs not normally activated by pheromones. Because mammalian CD36 binds fatty acids10, we suggest that SNMP acts in concert with odorant receptors to capture pheromone molecules on the surface of olfactory dendrites. Our work identifies an unanticipated cofactor for odorant receptors that is likely to have a widespread role in insect pheromone detection. Moreover, these results define a unifying model for CD36 function, coupling recognition of lipid-based extracellular ligands to signalling receptors in both pheromonal communication and pathogen recognition through the innate immune system.

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Figure 1: A comparative genomics screen for olfactory molecules identifies Drosophila SNMP, a CD36-related receptor.
Figure 2: SNMP localizes to sensory cilia of pheromone-sensitive OSNs.
Figure 3: Genetic analysis of Snmp.
Figure 4: SNMP mediates electrophysiological responses to cVA.
Figure 5: SNMP is specifically required, and sufficient, for pheromone detection.

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Acknowledgements

We thank R. Fenster and S. Katz for expert technical assistance; W. Jones for training in electrophysiology; M. Ditzen for providing spike analysis software; P. Morozov of the Columbia Genome Centre and AMDeC Bioinformatics Core Facility for programing to permit batch retrieval of insect-specific orthologues and expressed sequence tags; E. Zdobnov for providing a D. melanogaster/A. gambiae orthologue data set; P. Howell and M. Q. Benedict of the CDC and MR4 for mosquitoes; D. Smith for reagents; B. Dickson for sharing unpublished fly reagents; S. Piccinotti for graphic design; R. Vogt for discussions; and M. Heiman, K. Lee, S. Martin, K. Scott and members of the Vosshall laboratory for comments on the manuscript. R.B. was supported by an EMBO Long-Term Fellowship and the Helen Hay Whitney Foundation. This work was supported by grants to L.B.V. from the NIH and the McKnight Endowment Fund for Neuroscience.

Author Contributions R.B. and K.S.V. performed the screen for olfactory genes. R.B. carried out all other experiments and analysed the data. R.B. and L.B.V. together designed the experiments, interpreted the results, produced the figures and wrote the paper.

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Author notes

  1. Richard Benton & Kirsten S. Vannice

    Present address: Present addresses: Center for Integrative Genomics, Genopode Building, University of Lausanne, CH-1015 Lausanne, Switzerland (R.B.); Johns Hopkins Bloomberg School of Public Health, 615 North Wolfe Street, Baltimore, Maryland 21205, USA (K.S.V.).,

Authors and Affiliations

  1. Laboratory of Neurogenetics and Behaviour, The Rockefeller University, 1230 York Avenue, Box 63, New York, New York 10065, USA ,

    Richard Benton, Kirsten S. Vannice & Leslie B. Vosshall

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Correspondence to Leslie B. Vosshall.

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Supplementary information

Supplementary Information

The file contains Supplementary Figures S1-S2 with Legends and Supplementary Table S1 which lists genes identified in the comparative genomics screen. (PDF 16268 kb)

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Benton, R., Vannice, K. & Vosshall, L. An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450, 289–293 (2007). https://doi.org/10.1038/nature06328

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