Something in the Air? New Insights into Mammalian Pheromones

Current Biology

Volumn 14, Issue 2, 2004, Pages

  Brennan, Peter A ^a   Keverne, Eric B ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; MAMMALIA; RODENTIA;

EID: 1142302219     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2003.12.052     Document Type: Review

References (76)

1. Karlson P., Lüscher M. Pheromones: a new term for a class of biologically active substances. Nature. 183:1959;55-56.
2. Doty R.L. Mammalian pheromones: fact or fantasy? Doty R.L. Handbook of Olfaction and Gustation. 2003;Marcel Dekker Inc. pp. 34-38.
3. Beauchamp G.K., Yamazaki K. Chemical signalling in mice. Biochem. Soc. Trans. 31:2003;147-151.
4. Stern K., McClintock M.K. Regulation of ovulation by human pheromones. Nature. 392:1998;177-179.
5. Distel H., Hudson R. The contribution of the olfactory and tactile modalities to the performance of nipple-search behaviour in newborn rabbits. J. Comp. Physiol. [A]. 157:1985;599-605.
6. Schaal B., Coureaud G., Langlois D., Giniès C., Sémon E., Perrier G. Chemical and behavioural characterization of the rabbit mammary pheromone. Nature. 424:2003;68-72.
7. Dorries K.M., Adkins R.E., Halpern B.P. Sensitivity and behavioral responses to the pheromone androstenone are not mediated by the vomeronasal organ in domestic pigs. Brain Behav. Evol. 49:1997;53-62.
8. Novotny M.V. Pheromones, binding proteins and receptor responses in rodents. Biochem. Soc. Trans. 31:2003;117-122.
9. Schwende F.J., Wiesler D., Jorgenson J.W., Carmack M., Novotny M.V. Urinary volatile constituents of the house mouse, Mus musculus, and their endocrine dependency. J. Chem. Ecol. 12:1986;277-296.
10. Novotny M.V., Weidong M., Wiesler D., Zidek L. Positive identification of the puberty-accelerating pheromone of the house mouse: the volatile ligands associating with the major urinary protein. Proc. R. Soc. Lond. B. Biol. Sci. 266:1999;2017-2022.
11. Jemiolo B., Harvey S., Novotny M. Promotion of the Whitten effect in female mice by synthetic analogs of male urinary constituents. Proc. Natl. Acad. Sci. USA. 83:1986;4576-4579.
12. Novotny M., Harvey S., Jemiolo B., Alberts J. Synthetic pheromones that promote inter-male aggression in mice. Proc. Natl. Acad. Sci. USA. 82:1985;2059-2061.
13. Flower D.R. The lipocalin protein family: structure and function. Biochem. J. 318:1996;1-14.
14. Loebel D., Scaloni A., Paolini S., Fini C., Ferrara L., Breer H., Pelosi P. Cloning, post-translational modifications, heterologous expression and ligand-binding of boar salivary lipocalin. Biochem. J. 350:2000;369-379.
15. Singer A.G., Macrides F. Aphrodisin: pheromone or transducer? Chem. Senses. 15:1990;199-204.
16. Böcskei Z., Groom C.R., Flower D.R., Wright C.E., Phillips S.E.V., Cavaggioni A., Findlay J.B.C., North A.C.T. Pheromone binding to two rodent urinary proteins revealed by X-ray crystallography. Nature. 360:1992;186-188.
17. Beynon R.J., Hurst J.L. Multiple roles of major urinary proteins in the house mouse, Mus domesticus. Biochem. Soc. Trans. 31:2003;142-146.
18. Hurst J.L. Urine marking in populations of wild house mice Mus domesticus Rutty I. Communication between males . Anim. Behav. 40:1990;209-222.
19. Hurst J.L., Robertson D.H.L., Tolladay U., Beynon R.J. Proteins in urine scent marks of male house mice extend the longevity of olfactory signals. Anim. Behav. 55:1998;1289-1297.
20. Humphries R.E., Robertson D.H.L., Beynon R.J., Hurst J.L. Unravelling the chemical basis of competitive scent marking in house mice. Anim. Behav. 58:1999;1177-1190.
21. Singer A.G., Beauchamp G.K., Yamazaki K. Volatile signals of the major histocompatibility complex in male mouse urine. Proc. Natl. Acad. Sci. USA. 94:1997;2210-2214.
22. Hurst J.L., Payne C.E., Nevison C.M., Marie A.D., Humphries R.E., Robertson D.H.L., Cavaggioni A., Beynon R.J. Individual recognition in mice mediated by major urinary proteins. Nature. 414:2001;631-634.
23. Dulac C., Torello A.T. Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat. Rev. Neurosci. 4:2003;551-562.
24. Døving K.B., Trotier D. Structure and function of the vomeronasal organ. J. Exp. Biol. 21:1998;2913-2925.
25. Meredith M., O'Connell R.J. Efferent control of stimulus access to the hamster vomeronasal organ. J. Physiol. 286:1979;301-316.
26. Meredith M. Chronic recording of vomeronasal pump activation in awake behaving hamsters. Physiol. Behav. 56:1994;345-354.
27. Luo M.M., Fee M.S., Katz L.C. Encoding pheromonal signals in the accessory olfactory bulb of behaving mice. Science. 299:2003;1196-1201.
28. Trinh K., Storm D.R. Vomeronasal organ detects odorants in absence of signaling through main olfactory epithelium. Nat. Neurosci. 6:2003;519-525.
29. Leinders-Zufall T., Lane A.P., Puche A.C., Ma W., Novotny M.V., Shipley M.T., Zufall F. Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature. 405:2000;792-796.
30. Sam M., Vora S., Malnic B., Ma W., Novotny M.V., Buck L.B. Odorants may arouse instinctive behaviours. Nature. 412:2001;142.
31. Millar A.R., Gutzke W.H.N. The role of the vomeronasal organ of crotalines (Reptilia: Serpentes: Viperidae) in predator detection. Anim. Behav. 58:1999;53-57.
32. Rodriguez I., Del Punta K., Rothman A., Ishii T., Mombaerts P. Multiple new and isolated families within the mouse superfamily of V1r vomeronasal receptors. Nat. Neurosci. 5:2002;134-140.
33. Zhang X., Firestein S. The olfactory receptor gene superfamily of the mouse. Nat. Neurosci. 5:2002;124-133.
34. Malnic B., Hirono J., Sato T., Buck L.B. Combinatorial receptor codes for odors. Cell. 96:1999;713-723.
35. Herrada G., Dulac C. A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell. 90:1997;763-773.
36. Matsunami H., Buck L.B. A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell. 90:1997;775-784.
37. Ryba N.J.P., Tirindelli R. A new multigene family of putative pheromone receptors. Neuron. 19:1997;371-379.
38. Adler E., Hoon M.A., Mueller K.L., Chandrashekar J., Ryba N.J.P., Zucker C.S. A novel family of mammalian taste receptors. Cell. 100:2000;693-702.
39. Dulac C., Axel R. A novel family of genes encoding putative pheromone receptors in mammals. Cell. 83:1995;195-206.
40. Boschat C., Pélofi C., Randin O., Roppolo D., Lüscher C., Broillet M., Rodriguez I. Pheromone detection mediated by a V1r vomeronasal receptor. Nat. Neurosci. 5:2002;1261-1262.
41. Matsunami H., Amrein H. Taste and pheromone perception in mammals and flies. Genome Biol. 4:2003;220.
42. Martini S., Silvotti L., Shirazi A., Ryba J.P., Tirindelli R. Co-expression of putative pheromone receptors in the sensory neurons of the vomeronasal organ. J. Neurosci. 21:2001;843-848.
43. Loconto J., Papes F., Chang E., Stowers L., Jones E.P., Takada T., Kumanovics A., Fischer-Lindahl K., Dulac C. Functional expression of murine V2R pheromone receptors involves selective association with the M10 and M1 families of MHC class 1b molecules. Cell. 112:2003;607-618.
44. Ishii T., Hirota J., Mombaerts P. Combinational coexpression of neural and immune multigene families in mouse vomeronasal sensory systems. Curr. Biol. 13:2003;394-400.
45. Kelliher K., Ziesmann J., Munger S.D., Reed R.R., Zufall F. Importance of the CNGA4 channel gene for odor discrimination and adaptation in behaving mice. Proc. Natl. Acad. Sci. USA. 100:2003;4299-4304.
46. Holy T.E., Dulac C., Meister M. Responses of vomeronasal neurons to natural stimuli. Science. 289:2000;1569-1572.
47. Rosser A.E., Remfry C.J., Keverne E.B. Restricted exposure of mice to primer pheromones coincident with prolactin surges blocks pregnancy by changing hypothalamic dopamine release. J. Reprod. Fertil. 87:1989;553-559.
48. Liman E.R., Corey D.P., Dulac C. TRP2: A candidate transduction channel for mammalian pheromone sensory signaling. Proc. Natl. Acad. Sci. USA. 96:1999;5791-5796.
49. Stowers L., Holy T.E., Meister M., Dulac C., Koentges G. Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science. 295:2002;1493-1500.
50. Leypold B.G., Yu C.R., Leinders-Zufall T., Kim M.M., Zufall F., Axel R. Altered sexual and social behaviours in trp2 mutant mice. Proc. Natl. Acad. Sci. USA. 99:2002;6376-6381.
51. Maruniak J.A., Wysocki C.J., Taylor J.A. Mediation of male mouse urine marking and aggression by the vomeronasal organ. Physiol. Behav. 37:1986;655-657.
52. Clancy A.N., Coquelin A., Macrides F., Gorski R.A., Nobles E.P. Sexual behavior and aggression in male mice: Involvement of the vomeronasal organ. J. Neurosci. 4:1984;2222-2229.
53. Wysocki C.J., Lepri J.L. Consequences of removing the vomeronasal organ. J. Steroid Biochem. Mol. Biol. 39:1991;661-669.
54. Del Punta K., Leinders-Zufall T., Rodriguez I., Jukam D., Wysocki C.J., Ogawa S., Zufall F., Mombaerts P. Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes. Nature. 419:2002;70-74.
55. Norlin E.M., Gussing F., Berghard A. Vomeronasal phenotype and behavioral alterations in Gαi2 mutant mice. Curr. Biol. 13:2003;1214-1219.
56. Li C.S., Kaba H., Saito H., Seto K. Neural mechanisms underlying the action of primer pheromones in mice. Neuroscience. 36:1990;773-778.
57. Swanson L.W., Petrovich G.D. What is the amygdala? Trends Neurosci. 21:1998;323-331.
58. Halpern M., Jia C.P., Shapiro L.S. Segregated pathways in the vomeronasal system. Microsc. Res. Tech. 41:1998;519-529.
59. Sugai T., Sugitani M., Onoda N. Subdivisions of the guinea pig accessory olfactory bulb revealed by the combined method with immunohistochemistry, electrophysiological, and optical recordings. Neuroscience. 79:1997;871-885.
60. von Campenhausen H., Mori K. Convergence of segregated pheromonal pathways from the accessory olfactory bulb to the cortex in the mouse. Eur. J. Neurosci. 12:2000;33-46.
61. Mombaerts P., Wang F., Dulac C., Chao S.K., Nemes A., Mendelsohn M., Edmondson J., Axel R. Visualizing an olfactory sensory map. Cell. 87:1996;675-686.
62. Rodriguez I., Feinstein P., Mombaerts P. Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell. 97:1999;199-208.
63. Belluscio L., Koentges G., Axel R., Dulac C. A map of pheromone receptor activation in the mammalian brain. Cell. 97:1999;209-220.
64. Mori K. Membrane and synaptic properties of identified neurons in the olfactory bulb. Prog. Neurobiol. 29:1987;275-320.
65. 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. 35:2002;1057-1066.
66. Brennan P., Kaba H., Keverne E.B. Olfactory Recognition: a simple memory system. Science. 250:1990;1223-1226.
67. Kaba H., Nakanishi S. Synaptic mechanisms of olfactory recognition memory. Rev. Neurosci. 6:1995;125-141.
68. Hudson R., Distel H. Pheromonal release of suckling in rabbits does not depend on the vomeronasal organ. Physiol. Behav. 37:1986;123-129.
69. Weiler E., Farbman A.I. The septal organ of the rat during postnatal development. Chem. Senses. 28:2003;581-593.
70. Meredith M. Vomeronasal organ removal before sexual experience impairs male hamster mating behavior. Physiol. Behav. 36:1986;737-743.
71. Meredith M. Vomeronasal, olfactory, hormonal convergence in the brain. Ann. N.Y. Acad. Sci. 855:1998;349-361.
72. Kindermann U., Hudson R., Distel H. Learning of suckling odors by newborn rabbits declines with age and suckling experience. Dev. Psychobiol. 27:1994;111-122.
73. Meredith M. Human vomeronasal organ function: a critical review of best and worst cases. Chem. Senses. 26:2001;433-445.
74. Liman E.R., Innan H. Relaxed selective pressure on an essential component of pheromone transduction in primate evolution. Proc. Natl. Acad. Sci. USA. 100:2003;3328-3332.
75. Rodriguez I., Mombaerts P. Novel human vomeronasal receptor-like genes reveal species-specific families. Curr. Biol. 12:2002;R409-R411.
76. Rodriguez I., Greer C.A., Mok M.Y., Mombaerts P. A putative pheromone receptor gene expressed in human olfactory mucosa. Nat. Genet. 26:2000;18-19.