A juvenile mouse pheromone inhibits sexual behaviour through the vomeronasal system

Nature

Volumn 502, Issue 7471, 2013, Pages 368-371

  Ferrero, David M ^a   Moeller, Lisa M ^b   Osakada, Takuya ^c   Horio, Nao ^c   Li, Qian ^a   Roy, Dheeraj S ^a   Cichy, Annika ^b   Spehr, Marc ^b   Touhara, Kazushige ^c   Liberles, Stephen D ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EXOCRINE GLAND SECRETING PEPTIDE 22; PEPTIDE; PHEROMONE; UNCLASSIFIED DRUG;

ADULT; AGE; BEHAVIORAL RESPONSE; JUVENILE; MATING BEHAVIOR; PEPTIDE; PHEROMONE; SENSORY SYSTEM; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; LACRIMAL FLUID; LACRIMAL GLAND; MALE; MATING; MEDIAL AMYGDALA; MOUSE; NONHUMAN; OLFACTORY SYSTEM; PRIORITY JOURNAL; PUBERTY; SENSORY NERVE CELL; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; VOMERONASAL ORGAN;

AGING; AMYGDALA; ANIMALS; FEMALE; LACRIMAL APPARATUS; MALE; MICE; MICE, INBRED C57BL; PHEROMONES; SENSORY RECEPTOR CELLS; SEXUAL BEHAVIOR, ANIMAL; SEXUAL MATURATION; TEARS; TRPC CATION CHANNELS; VOMERONASAL ORGAN;

ANIMALIA; MUS;

EID: 84885844429     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12579     Document Type: Article

References (32)

1. Tirindelli, R., Dibattista, M., Pifferi, S. & Menini, A. From pheromones to behavior. Physiol. Rev. 89, 921-956 (2009).
2. Leypold, B. G. et al. Altered sexual and social behaviors in trp2 mutant mice. Proc. Natl Acad. Sci. USA 99, 6376-6381 (2002).
3. Stowers, L., Holy, T. E., Meister, M., Dulac, C. & Koentges, G. Loss of sex discrimination andmale-male aggression in mice deficient for TRP2. Science 295, 1493-1500 (2002).
4. Ferrero, D. M. & Liberles, S. D. The secret codes of mammalian scents. Wiley Interdiscip. Rev. Syst. Biol. Med. 2, 23-33 (2010).
5. Nodari, F. et al. Sulfated steroids as natural ligands of mouse pheromone-sensing neurons. J. Neurosci. 28, 6407-6418 (2008).
6. Novotny, M. V. Pheromones, binding proteins and receptor responses in rodents. Biochem. Soc. Trans. 31, 117-122 (2003).
7. Touhara, K. Sexual communication via peptide and protein pheromones. Curr. Opin. Pharmacol. 8, 759-764 (2008).
8. Karn, R. C. & Laukaitis, C. M. The roles of gene duplication, gene conversion and positive selection in rodent esp and mup pheromone gene families with comparison to the abp family. PLoS ONE 7, e47697 (2012).
9. Kimoto, H.,Haga,S.,Sato,K. & Touhara,K.Sex-specificpeptides fromexocrineglands stimulate mouse vomeronasal sensory neurons. Nature 437, 898-901 (2005).
10. Logan, D. W.,Marton, T. F. & Stowers, L.Species specificity inmajor urinary proteins by parallel evolution. PLoS ONE 3, e3280 (2008).
11. Chamero, P. et al. G protein Gao is essential for vomeronasal function and aggressive behavior in mice. Proc. Natl Acad. Sci. USA 108, 12898-12903 (2011).
12. Papes, F., Logan, D. W. & Stowers, L. The vomeronasal organmediates interspecies defensive behaviors through detection of protein pheromone homologs. Cell 141, 692-703 (2010).
13. Haga, S. et al. The male mouse pheromone ESP1 enhances female sexual receptive behaviour through a specific vomeronasal receptor. Nature 466, 118-122 (2010).
14. Kimoto, H. et al. Sex- and strain-specific expression and vomeronasal activity of mouse ESP family peptides. Curr. Biol. 17, 1879-1884 (2007).
15. Li, Q. et al. Synchronous evolution of an odor biosynthesis pathway and behavioral response. Curr. Biol. 23, 11-20 (2013).
16. Mandiyan, V. S., Coats, J. K. & Shah, N. M. Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nature Neurosci. 8, 1660-1662 (2005).
17. Wang, Z. et al. Pheromone detection in male mice depends on signaling through the type 3 adenylyl cyclase in the main olfactory epithelium. J. Neurosci. 26, 7375-7379 (2006).
18. He, J. et al. Distinct signals conveyed by pheromone concentrations to the mouse vomeronasal organ. J. Neurosci. 30, 7473-7483 (2010).
19. Dulac, C. & Wagner, S. Genetic analysis of brain circuits underlying pheromone signaling. Annu. Rev. Genet. 40, 449-467 (2006).
20. Choi, G. B. et al. Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron 46, 647-660 (2005).
21. Yang, C. F. et al. Sexually dimorphic neurons in the ventromedial hypothalamus govern mating in both sexes and aggression in males. Cell 153, 896-909 (2013).
22. Chamero, P. et al. Identification of protein pheromones that promote aggressive behaviour. Nature 450, 899-902 (2007).
23. Novotny, M., Harvey, S., Jemiolo, B. & Alberts, J. Synthetic pheromones that promote inter-male aggression in mice. Proc. Natl Acad. Sci. USA 82, 2059-2061 (1985).
24. Liberles, S. D. & Buck, L. B. A second class of chemosensory receptors in the olfactory epithelium. Nature 442, 645-650 (2006).
25. Montmayeur, J. P., Liberles, S. D., Matsunami, H. & Buck, L. B. A candidate taste receptor gene near a sweet taste locus. Nature Neurosci. 4, 492-498 (2001).
26. Liberles, S. D. et al. Formyl peptide receptors are candidatechemosensory receptors in the vomeronasal organ. Proc. Natl Acad. Sci. USA 106, 9842-9847 (2009).
27. Shevchenko, A., Wilm, M.,Vorm, O. & Mann, M.Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858 (1996).
28. Peng, J. & Gygi, S. P. Proteomics: the move to mixtures. J. Mass Spectrom. 36, 1083-1091 (2001).
29. Eng, J. K., Mccormack, A. L. & Yates, J. R. An approach to correlate tandem massspectral data of peptides with amino-acid-sequences in a protein database. J. Am. Soc. Mass Spectrom. 5, 976-989 (1994).
30. Hagendorf, S., Fluegge, D., Engelhardt, C. & Spehr, M. Homeostatic control of sensory output in basal vomeronasal neurons: activity-dependent expression of ether-a-go-go-related gene potassium channels. J. Neurosci. 29, 206-221 (2009).
31. Spehr, J. et al. Ca21-calmodulin feedback mediates sensory adaptation and inhibits pheromone-sensitive ion channels in the vomeronasal organ. J.Neurosci. 29, 2125-2135 (2009).
32. Franklin, K. & Paxinos, G. The Mouse Brain in Stereotaxic Coordinates Fig. 44 (Academic, 2008).