The male mouse pheromone ESP1 enhances female sexual receptive behaviour through a specific vomeronasal receptor

Nature

Volumn 466, Issue 7302, 2010, Pages 118-122

  Haga, Sachiko ^a   Hattori, Tatsuya ^b   Sato, Toru ^a   Sato, Koji ^a   Matsuda, Soichiro ^a   Kobayakawa, Reiko ^c   Sakano, Hitoshi ^d   Yoshihara, Yoshihiro ^e   Kikusui, Takefumi ^b   Touhara, Kazushige ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b AZABU UNIVERSITY   (Japan)

^c OSAKA BIOSCIENCE INSTITUTE   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EXOCRINE GLAND SECRETING PEPTIDE 1; LIGAND; PHEROMONE; PROTEIN; RECEPTOR; UNCLASSIFIED DRUG; V2RP5 RECEPTOR; VOMERONASAL RECEPTOR;

COPULATION; MOLECULAR ANALYSIS; NEUROLOGY; OLFACTORY CUE; PEPTIDE; RODENT; SEX PHEROMONE; SIGNAL; SOCIAL BEHAVIOR;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COPULATION; FEMALE; HYPOTHALAMUS NUCLEUS; LORDOSIS; MALE; MOUSE; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN DEFICIENCY; SEXUAL BEHAVIOR; VOMERONASAL ORGAN;

ANIMALS; BRAIN; FEMALE; MALE; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; NEURONS; PHEROMONES; PROTEINS; PROTO-ONCOGENE PROTEINS C-FOS; RECEPTORS, ODORANT; RECEPTORS, PHEROMONE; SEXUAL BEHAVIOR, ANIMAL; TRPC CATION CHANNELS; VOMERONASAL ORGAN;

MUS;

EID: 77954231077     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature09142     Document Type: Article

References (35)

1. Wyatt, T. D. Pheromones and Animal Behaviour (Cambridge Univ. Press., 2003).
2. Dulac, C. & Torello, A. T. Molecular detection of pheromone signals in mammals: from genes to behaviour. Nature Rev. Neurosci. 4, 551-562 (2003).
3. Touhara, K. Molecular biology of peptide pheromone production and reception in mice. Adv. Genet. 59, 147-171 (2007).
4. Kimoto, H., Haga, S., Sato, K. & Touhara, K. Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 437, 898-901 (2005).
5. Touhara, K. & Vosshall, L. B. Sensing odorants and pheromones with chemosensory receptors. Annu. Rev. Physiol. 71, 307-332 (2009).
6. Haga, S., Kimoto, H. & Touhara, K. Molecular characterization of vomeronasal sensory neurons responding to a male-specific peptide in tear fluid: Sexual communication in mice. Pure Appl. Chem. 79, 775-784 (2007).
7. Kimoto, H. et al. Sex-and strain-specific expression and vomeronasal activity of mouse ESP family peptides. Curr. Biol. 17, 1879-1884 (2007).
8. He, J., Ma, L., Kim, S., Nakai, J. & Yu, C. R. Encoding gender and individual information in the mouse vomeronasal organ. Science 320, 535-538 (2008).
9. Leypold, B. G. et al. Altered sexual and social behaviors in trp2 mutant mice. Proc. Natl Acad. Sci. USA 99, 6376-6381 (2002).
10. Ishii, T., Hirota, J. & Mombaerts, P. Combinatorial coexpression of neural and immune multigene families in mouse vomeronasal sensory neurons. Curr. Biol. 13, 394-400 (2003).
11. Loconto, J. et al. Functional expression of murine V2R pheromone receptors involves selective association with the M10 and M1 families of MHC class Ib molecules. Cell 112, 607-618 (2003).
12. Del Punta, K., Puche, A., Adams, N. C., Rodriguez, I. & Mombaerts, P. A divergent pattern of sensory axonal projections is rendered convergent by second-order neurons in the accessory olfactory bulb. Neuron 35, 1057-1066 (2002).
13. Ishii, T. & Mombaerts, P. Expression of nonclassical class I major histocompatibility genes defines a tripartite organization of the mouse vomeronasal system. J. Neurosci. 28, 2332-2341 (2008).
14. von Campenhausen, H. & Mori, K. Convergence of segregated pheromonal pathways from the accessory olfactory bulb to the cortex in the mouse. Eur. J. Neurosci. 12, 33-46 (2000).
15. Meredith, M. Vomeronasal, olfactory, hormonal convergence in the brain. Cooperation or coincidence? Ann. NY Acad. Sci. 855, 349-361 (1998).
16. Yoon, H., Enquist, L. W. & Dulac, C. Olfactory inputs to hypothalamic neurons controlling reproduction and fertility. Cell 123, 669-682 (2005).
17. Simerly, R. B. & Swanson, L. W. The organization of neural inputs to the medial preoptic nucleus of the rat. J. Comp. Neurol. 246, 312-342 (1986).
18. Canteras, N. S., Simerly, R. B. & Swanson, L. W. Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J. Comp. Neurol. 360, 213-245 (1995).
19. Pfaff, D. W. & Sakuma, Y. Facilitation of the lordosis reflex of female rats from the ventromedial nucleus of the hypothalamus. J. Physiol. (Lond.) 288, 189-202 (1979). (Pubitemid 9146881)
20. Blaustein, J. D. & Erskine, M. S. in Hormones, Brain and Behavior (eds Pfaff, D. W. et al.) 139-214 (Academic, 2002).
21. Halem, H. A., Cherry, J. A. & Baum, M. J. Vomeronasal neuroepithelium and forebrain Fos responses to male pheromones in male and female mice. J. Neurobiol. 39, 249-263 (1999).
22. Pierman, S., Douhard, Q. & Bakker, J. Evidence for a role of early oestrogens in the central processing of sexually relevant olfactory cues in female mice. Eur. J. Neurosci. 27, 423-431 (2008).
23. Wu, M. V. et al. Estrogen masculinizes neural pathways and sex-specific behaviors. Cell 139, 61-72 (2009).
24. Boschat, C. et al. Pheromone detection mediated by a V1r vomeronasal receptor. Nature Neurosci. 5, 1261-1262 (2002).
25. Mombaerts, P. Genes and ligands for odorant, vomeronasal and taste receptors. Nature Rev. Neurosci. 5, 263-278 (2004). (Pubitemid 38478654)
26. Nakagawa, T., Sakurai, T., Nishioka, T. & Touhara, K. Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307, 1638-1642 (2005).
27. Datta, S. R. et al. The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. Nature 452, 473-477 (2008).
28. Semmelhack, J. L. & Wang, J. W. Select Drosophila glomeruli mediate innate olfactory attraction and aversion. Nature 459, 218-223 (2009).
29. Zijlstra, M. et al. Beta 2-microglobulin deficient mice lack CD4-81 cytolytic T cells. Nature 344, 742-746 (1990).
30. Lalioti, M. & Heath, J. A new method for generating point mutations in bacterial artificial chromosomes by homologous recombination in Escherichia coli. Nucleic Acids Res. 29, E14 (2001).
31. Skene, J. H. & Virag, I. Posttranslational membrane attachment and dynamic fatty acylation of a neuronal growth cone protein, GAP-43. J. Cell Biol. 108, 613-624 (1989).
32. Nagai, T. et al. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nature Biotechnol. 20, 87-90 (2002).
33. Bunting, M., Bernstein, K. E., Greer, J. M., Capecchi, M. R. & Thomas, K. R. Targeting genes for self-excision in the germ line. Genes Dev. 13, 1524-1528 (1999).
34. Taniguchi, M. et al. Disruption of semaphorin III/D gene causes severe abnormality in peripheral nerve projection. Neuron 19, 519-530 (1997).
35. Kudwa, A. E., Bodo, C., Gustafsson, J. A. & Rissman, E. F. A previously uncharacterized role for estrogen receptor beta: defeminization of male brain and behavior. Proc. Natl Acad. Sci. USA 102, 4608-4612 (2005).