Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.


Logo for

Science 307 (5715): 1638-1642

Copyright © 2005 by the American Association for the Advancement of Science

Insect Sex-Pheromone Signals Mediated by Specific Combinations of Olfactory Receptors

Takao Nakagawa,1 Takeshi Sakurai,2,4 Takaaki Nishioka,3,4* Kazushige Touhara1*

Abstract: We describe two male-specific olfactory receptors (ORs) in the silk moth, Bombyx mori, that are mutually exclusively expressed in a pair of adjacent pheromone-sensitive neurons of male antennae: One is specifically tuned to bombykol, the sex pheromone, and the other to bombykal, its oxidized form. Both pheromone ORs are coexpressed with an OR from the highly conserved insect OR subfamily. This coexpression promotes the functional expression of pheromone receptors and confers ligand-stimulated nonselective cation channel activity. The same effects were also observed for general ORs. Both odorant and pheromone signaling pathways are mediated by means of a common mechanism in insects.

1 Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Chiba 277-8562, Japan.
2 Division of Applied Biosciences Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan.
3 Division of Applied Life Sciences, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan.
4 Core Research for Evolution Science and Technology of Japan Science and Technology Agency, Kawaguchi, 332–0012 Japan.

* To whom correspondence should be addressed. E-mail: touhara{at} (K.T.); nishioka{at} (T.N.)

Farnesol-Detecting Olfactory Neurons in Drosophila.
D. S. Ronderos, C.-C. Lin, C. J. Potter, and D. P. Smith (2014)
J. Neurosci. 34, 3959-3968
   Abstract »    Full Text »    PDF »
Anatomical and functional analysis of domestication effects on the olfactory system of the silkmoth Bombyx mori.
S. Bisch-Knaden, T. Daimon, T. Shimada, B. S. Hansson, and S. Sachse (2013)
Proc R Soc B 281, 20132582
   Abstract »    Full Text »    PDF »
Pheromone discrimination by a pH-tuned polymorphism of the Bombyx mori pheromone-binding protein.
F. F. Damberger, E. Michel, Y. Ishida, W. S. Leal, and K. Wuthrich (2013)
PNAS 110, 18680-18685
   Abstract »    Full Text »    PDF »
Sense of achievement.
M. Knaden and B. S. Hansson (2013)
eLife Sci 2, e01605
   Abstract »    Full Text »    PDF »
The joy of sex pheromones.
C. Gomez-Diaz and R. Benton (2013)
EMBO Rep. 14, 874-883
   Abstract »    Full Text »    PDF »
Pheromone responsiveness threshold depends on temporal integration by antennal lobe projection neurons.
M. Tabuchi, T. Sakurai, H. Mitsuno, S. Namiki, R. Minegishi, T. Shiotsuki, K. Uchino, H. Sezutsu, T. Tamura, S. S. Haupt, et al. (2013)
PNAS 110, 15455-15460
   Abstract »    Full Text »    PDF »
Blockade of Insect Odorant Receptor Currents by Amiloride Derivatives.
G. M. Pask, Y. V. Bobkov, E. A. Corey, B. W. Ache, and L. J. Zwiebel (2013)
Chem Senses 38, 221-229
   Abstract »    Full Text »    PDF »
Amiloride Derivatives Are Effective Blockers of Insect Odorant Receptors.
K. Rollecke, M. Werner, P. M. Ziemba, E. M. Neuhaus, H. Hatt, and G. Gisselmann (2013)
Chem Senses 38, 231-236
   Abstract »    Full Text »    PDF »
Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species.
G. P. Leary, J. E. Allen, P. L. Bunger, J. B. Luginbill, C. E. Linn Jr., I. E. Macallister, M. P. Kavanaugh, and K. W. Wanner (2012)
PNAS 109, 14081-14086
   Abstract »    Full Text »    PDF »
Subunit Contributions to Insect Olfactory Receptor Function: Channel Block and Odorant Recognition.
A. S. Nichols, S. Chen, and C. W. Luetje (2011)
Chem Senses 36, 781-790
   Abstract »    Full Text »    PDF »
Sex-linked transcription factor involved in a shift of sex-pheromone preference in the silkmoth Bombyx mori.
T. Fujii, T. Fujii, S. Namiki, H. Abe, T. Sakurai, A. Ohnuma, R. Kanzaki, S. Katsuma, Y. Ishikawa, and T. Shimada (2011)
PNAS 108, 18038-18043
   Abstract »    Full Text »    PDF »
Insect olfaction from model systems to disease control.
A. F. Carey and J. R. Carlson (2011)
PNAS 108, 12987-12995
   Abstract »    Full Text »    PDF »
Sugar-regulated cation channel formed by an insect gustatory receptor.
K. Sato, K. Tanaka, and K. Touhara (2011)
PNAS 108, 11680-11685
   Abstract »    Full Text »    PDF »
A Unified Nomenclature System for the Insect Olfactory Coreceptor.
L. B. Vosshall and B. S. Hansson (2011)
Chem Senses 36, 497-498
   Full Text »    PDF »
Antennal transcriptome of Manduca sexta.
E. Grosse-Wilde, L. S. Kuebler, S. Bucks, H. Vogel, D. Wicher, and B. S. Hansson (2011)
PNAS 108, 7449-7454
   Abstract »    Full Text »    PDF »
Diversity in Copy Number and Structure of a Silkworm Morphogenetic Gene as a Result of Domestication.
T. Sakudoh, T. Nakashima, Y. Kuroki, A. Fujiyama, Y. Kohara, N. Honda, H. Fujimoto, T. Shimada, M. Nakagaki, Y. Banno, et al. (2011)
Genetics 187, 965-976
   Abstract »    Full Text »    PDF »
Conservation of Indole Responsive Odorant Receptors in Mosquitoes Reveals an Ancient Olfactory Trait.
J. D. Bohbot, P. L. Jones, G. Wang, R. J. Pitts, G. M. Pask, and L. J. Zwiebel (2011)
Chem Senses 36, 149-160
   Abstract »    Full Text »    PDF »
Highly sensitive and selective odorant sensor using living cells expressing insect olfactory receptors.
N. Misawa, H. Mitsuno, R. Kanzaki, and S. Takeuchi (2010)
PNAS 107, 15340-15344
   Abstract »    Full Text »    PDF »
Topographic Mapping--The Olfactory System.
T. Imai, H. Sakano, and L. B. Vosshall (2010)
Cold Spring Harb Perspect Biol 2, a001776
   Abstract »    Full Text »    PDF »
Smells like a new species: Gene duplication at the periphery.
D. G. Heckel (2010)
PNAS 107, 9481-9482
   Full Text »    PDF »
Transmembrane Segment 3 of Drosophila melanogaster Odorant Receptor Subunit 85b Contributes to Ligand-Receptor Interactions.
A. S. Nichols and C. W. Luetje (2010)
J. Biol. Chem. 285, 11854-11862
   Abstract »    Full Text »    PDF »
Role of G-Proteins in Odor-Sensing and CO2-Sensing Neurons in Drosophila.
C. A. Yao and J. R. Carlson (2010)
J. Neurosci. 30, 4562-4572
   Abstract »    Full Text »    PDF »
Molecular basis of odor coding in the malaria vector mosquito Anopheles gambiae.
G. Wang, A. F. Carey, J. R. Carlson, and L. J. Zwiebel (2010)
PNAS 107, 4418-4423
   Abstract »    Full Text »    PDF »
Smelling the difference: controversial ideas in insect olfaction.
M. Pellegrino and T. Nakagawa (2009)
J. Exp. Biol. 212, 1973-1979
   Abstract »    Full Text »    PDF »
HR11 and HR13 Receptor-Expressing Neurons Are Housed Together in Pheromone-Responsive Sensilla Trichodea of Male Heliothis virescens.
J. Krieger, I. Gondesen, M. Forstner, T. Gohl, Y. Dewer, and H. Breer (2009)
Chem Senses 34, 469-477
   Abstract »    Full Text »    PDF »
Odorant Receptors from the Light brown Apple Moth (Epiphyas postvittana) Recognize Important Volatile Compounds Produced by Plants.
M. D. Jordan, A. Anderson, D. Begum, C. Carraher, A. Authier, S. D.G. Marshall, A. Kiely, L. N. Gatehouse, D. R. Greenwood, D. L. Christie, et al. (2009)
Chem Senses 34, 383-394
   Abstract »    Full Text »    PDF »
A Candidate Pheromone Receptor and Two Odorant Receptors of the Hawkmoth Manduca sexta.
H. M. Patch, R. A. Velarde, K. K.O. Walden, and H. M. Robertson (2009)
Chem Senses 34, 305-316
   Abstract »    Full Text »    PDF »
Reduced Odor Responses from Antennal Neurons of Gq{alpha}, Phospholipase C{beta}, and rdgA Mutants in Drosophila Support a Role for a Phospholipid Intermediate in Insect Olfactory Transduction.
P. Kain, T. S. Chakraborty, S. Sundaram, O. Siddiqi, V. Rodrigues, and G. Hasan (2008)
J. Neurosci. 28, 4745-4755
   Abstract »    Full Text »    PDF »
The molecular and cellular basis of olfactory-driven behavior in Anopheles gambiae larvae.
Y. Xia, G. Wang, D. Buscariollo, R. J. Pitts, H. Wenger, and L. J. Zwiebel (2008)
PNAS 105, 6433-6438
   Abstract »    Full Text »    PDF »
Insect Odorant Receptors Are Molecular Targets of the Insect Repellent DEET.
M. Ditzen, M. Pellegrino, and L. B. Vosshall (2008)
Science 319, 1838-1842
   Abstract »    Full Text »    PDF »
On the hierarchical classification of G protein-coupled receptors.
M. N. Davies, A. Secker, A. A. Freitas, M. Mendao, J. Timmis, and D. R. Flower (2007)
Bioinformatics 23, 3113-3118
   Abstract »    Full Text »    PDF »
A honey bee odorant receptor for the queen substance 9-oxo-2-decenoic acid.
K. W. Wanner, A. S. Nichols, K. K. O. Walden, A. Brockmann, C. W. Luetje, and H. M. Robertson (2007)
PNAS 104, 14383-14388
   Abstract »    Full Text »    PDF »
Smell and taste on a high: Symposium on Chemical Senses: From Genes to Perception.
K. Asahina and R. Benton (2007)
EMBO Rep. 8, 634-638
   Full Text »    PDF »
The chemoreceptor superfamily in the honey bee, Apis mellifera: Expansion of the odorant, but not gustatory, receptor family.
H. M. Robertson and K. W. Wanner (2006)
Genome Res. 16, 1395-1403
   Abstract »    Full Text »    PDF »
Pheromone reception in fruit flies expressing a moth's odorant receptor.
Z. Syed, Y. Ishida, K. Taylor, D. A. Kimbrell, and W. S. Leal (2006)
PNAS 103, 16538-16543
   Abstract »    Full Text »    PDF »
Olfactory responses in a gustatory organ of the malaria vector mosquito Anopheles gambiae.
H.-W. Kwon, T. Lu, M. Rutzler, and L. J. Zwiebel (2006)
PNAS 103, 13526-13531
   Abstract »    Full Text »    PDF »
A Pheromone Receptor Mediates 11-cis-Vaccenyl Acetate-Induced Responses in Drosophila..
T. S. Ha and D. P. Smith (2006)
J. Neurosci. 26, 8727-8733
   Abstract »    Full Text »    PDF »
A Pheromone-Binding Protein Mediates the Bombykol-Induced Activation of a Pheromone Receptor In Vitro.
E. Grosse-Wilde, A. Svatos, and J. Krieger (2006)
Chem Senses 31, 547-555
   Abstract »    Full Text »    PDF »
EPPENDORF 2005 WINNER: A Drosophila OBP Required for Pheromone Signaling.
P. Xu (2005)
Science 310, 798-799
   Abstract »    Full Text »    PDF »
From The Cover: Rapid inactivation of a moth pheromone.
Y. Ishida and W. S. Leal (2005)
PNAS 102, 14075-14079
   Abstract »    Full Text »    PDF »
One Neuron-Multiple Receptors: Increased Complexity in Olfactory Coding?.
M. Spehr and T. Leinders-Zufall (2005)
Sci. STKE 2005, pe25
   Abstract »    Full Text »    PDF »

To Advertise     Find Products

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882