Sensory coding of pheromone signals in mammals

Current Opinion in Neurobiology

Volumn 10, Issue 4, 2000, Pages 511-518

  Dulac, Catherine ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHEROMONE;

MOLECULAR BIOLOGY; NONHUMAN; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; VOMERONASAL ORGAN;

EID: 0033866349     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(00)00121-5     Document Type: Review

References (60)

1. Halpern M. The organization and function of the vomeronasal system. Annu Rev Neurosci. 10:1987;325-362.
2. Wysocki, C.J. Vomeronasal chemoreception: its role in reproductive fitness and physiology. In Neural Control of Reproductive Function. New York, Alan R Liss Inc; 1989:545-566.
3. 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.
4. 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.
5. •].
6. •], the authors have undertaken structural and biochemical identification of small organic compounds involved in various pheromone-induced neuroendocrine changes. These pheromonal ligands are carried by the major urinary protein.
7. Buck L., Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 65:1991;175-187.
8. Dulac C., Axel R. A novel family of genes encoding putative pheromone receptors in mammals. Cell. 83:1995;195-206.
9. 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.
10. Matsunami H., Buck L.B. A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell. 90:1997;775-784.
11. Ryba N.J., Tirindelli R. A new multigene family of putative pheromone receptors. Neuron. 19:1997;371-379.
12. Ichikawa M., Takami S., Osada T., Graziadei P. Differential development of binding sites of two lectins in the vomeronasal axons of the rat accessory olfactory bulb. Dev Brain Res. 78:1994;1-9.
13. Imamura K., Mori K., Fujita S., Obata K. Immunocytochemical identification of subgroups of vomeronasal nerve fibers and their segregated terminations in the accessory olfactory bulb. Brain Res. 326:1985;362-366.
14. Halpern M., Shapiro L., Jia C. Differential localization of G proteins in the opossum vomeronasal system. Brain Res. 677:1995;157-161.
15. Jia C., Halpern M. Subclasses of vomeronasal receptor neurons: differential expression of G proteins (Gi alpha 2 and G(o alpha)) and segregated projections to the accessory olfactory bulb. Brain Res. 719:1996;117-128.
16. 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.
17. Sugai T., Sugitani M., Onoda N. Novel subdivisions of the rat accessory olfactory bulb revealed by the combined method with lectin histochemistry, electrophysiological and optical recordings. Neuroscience. 95:2000;23-32. The authors present molecular and physiological evidence for the partition of the accessory olfactory bulb into two or more distinct units.
18. Brennan P.A., Schellinck H.M., Keverne E.B. Patterns of expression of the immediate-early gene egr-1 in the accessory olfactory bulb of female mice exposed to pheromonal constituents of male urine. Neuroscience. 90:1999;1463-1470.
19. Dudley C.A., Moss R.L. Activation of an anatomically distinct subpopulation of accessory olfactory bulb neurons by chemosensory stimulation. Neuroscience. 91:1999;1549-1556.
20. Matsuoka M., Yokosuka M., Mori Y., Ichikawa M. Specific expression pattern of Fos in the accessory olfactory bulb of male mice after exposure to soiled bedding of females. Neurosci Res. 35:1999;189-195.
21. Tsujikawa K., Kashiwayanagi M. Protease-sensitive urinary pheromones induce region-specific Fos-expression in rat accessory olfactory bulb. Biochem Biophys Res Commun. 260:1999;222-224.
22. •].
23. •].
24. •].
25. +-sensing receptor in Fugu. Proc Natl Acad Sci USA. 95:1998;5178-5181.
26. Cao Y., Oh B.C., Stryer L. Cloning and localization of two multigene receptor families in goldfish olfactory epithelium. Proc Natl Acad Sci USA. 95:1998;11987-11992.
27. Sorensen P.W., Christensen T.A., Stacey N.E. Discrimination of pheromonal cues in fish: emerging parallels with insects. Curr Opin Neurobiol. 8:1998;458-467.
28. Speca D.J., Lin D.M., Sorensen P.W., Isacoff E.Y., Ngai J., Dittman A.H. Functional identification of a goldfish odorant receptor. Neuron. 23:1999;487-498. An expression cloning strategy led to the identification of a receptor within the olfactory epithelium that is specifically activated by basic amino acids. In contrast to other known chemosensory receptors, this receptor gene is widely expressed by a large population of neurons in the olfactory epithelium as well as in other structures.
29. •].
30. Troemel E.R., Chou J.H., Dwyer N.D., Colbert H.A., Bargmann C.I. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell. 83:1995;207-218.
31. Sengupta P., Chou J.H., Bargmann C.I. odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell. 84:1996;899-909.
32. •].
33. •].
34. •] illustrate the extensive variety in chemosensory receptor structures identified so far in vertebrates, C. elegans and Drosophila.
35. Berghard A., Buck L.B. Sensory transduction in vomeronasal neurons: evidence for Gαo, Gα12, and adenylyl cyclase II as major components of a pheromone signaling cascade. J Neurosci. 16:1996;909-918.
36. Berghard A., Buck L.A., Liman E.R. Evidence for distinct signaling mechanisms in two mammalian olfactory sense organs. Proc Natl Acad Sci USA. 93:1996;2365-2369.
37. Liman E., Corey D. Electrophysiological characterization of chemosensory neurons from the mouse vomeronasal organ. J Neurosci. 16:1996;4625-4637.
38. Scott K., Zuker C.S. TRP, TRPL and trouble in photoreceptor cells. Curr Opin Neurobiol. 8:1998;383-388.
39. Colbert H.A., Smith T.L., Bargmann C.I. OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J Neurosci. 17:1997;8259-8269.
40. Liman E., Corey D., Dulac C. TRP2: a candidate transduction channel for mammalian pheromone sensory signaling. Proc Natl Acad Sci USA. 96:1999;5791-5796. The identification of a member of the TRP family of ion channels that is very highly and specifically expressed in microvilli of VNO sensory neurons, together with previous work showing that pheromone-evoked signaling is unlikely to involve cyclic nucleotides, has led to the proposal that mammalian pheromone signaling involves a VNO tranduction cascade that shares similarities with the Drosophila phototransduction cascade.
41. Luo Y., Lu S., Chen P., Wang D., Halpern M. Identification of chemoattractant receptors and G-proteins in the vomeronasal system of garter snakes. J Biol Chem. 269:1994;16867-16877.
42. Kroner C., Breer H., Singer A.G., O'Connell R.J. Pheromone-induced second messenger signaling in the hamster vomeronasal organ. Neuroreport. 7:1996;2989-2992.
43. Wekesa K.S., Anholt R.R. Pheromone regulated production of inositol-(1, 4, 5)-trisphosphate in the mammalian vomeronasal organ. Endocrinology. 138:1997;3497-3504.
44. Krieger J., Schmitt A., Lobel D., Gudermann T., Schultz G., Breer H., Boekhoff I. Selective activation of G protein subtypes in the vomeronasal organ upon stimulation with urine-derived compounds. J Biol Chem. 274:1999;4655-4662.
45. ••].
46. ••], the authors describe how modification of V1R receptor loci by gene targeting allows the direct visualization of axonal projection patterns generated by neurons expressing a given pheromone receptor. Results indicate that the organization of the vomeronasal sensory afferents is dramatically different from that of the main olfactory system. These differences have important implications for the logic of coding of pheromone signals.
47. Vassar R., Chao S.K., Sitcheran R., Nunez J.M., Vosshall L.B., Axel R. Topographic organization of sensory projections to the olfactory bulb. Cell. 79:1994;981-991.
48. Ressler K.J., Sullivan S.L., Buck L.B. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell. 79:1994;1245-1255.
49. 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.
50. Cajal, R. Textura del lobulo olfactivo accesorio. In Trabajos Laboratorio de Investigaciones Biologicas, vol 1. Madrid; 1901:141-150.
51. Takami S., Graziadei P.P.C. Morphological complexity of the glomerulus in the rat accessory olfactory bulb - a Golgi study. Brain Res. 510:1990;339-342.
52. Takami S., Graziadei P.P.C. Light microscopic Golgi study of mitral/tufted cells in the accessory olfactory bulb of the adult rat. J Comp Neurol. 311:1991;65-83.
53. Jia C., Chen W.R., Shepherd G.M. Synaptic organization and neurotransmitters in the rat accessory olfactory bulb. J Neurophysiol. 81:1999;345-355.
54. Christensen T.A., Hildebrand J.G. Coincident stimulation with pheromone components improves temporal pattern resolution in central olfactory neurons. J Neurophysiol. 77:1997;775-781.
55. Tanaka M., Treloar H., Kalb R.G., Greer C.A., Strittmatter S.M. G(o) protein-dependent survival of primary accessory olfactory neurons. Proc Natl Acad Sci USA. 96:1999;14106-14111.
56. Wang F., Nemes A., Mendelsohn M., Axel R. Odorant receptors govern the formation of a precise topographic map. Cell. 93:1998;47-60.
57. ••].
58. ••], the authors have performed stereotaxic injections in the glomerular and mitral cell layers of the anterior and/or posterior AOB of the mouse and the opossum in order to trace further projections to the amygdala. Data from the two studies suggest that the sensory pathways originating from the apical and basal zones of the VNO neuroepithelium and that are kept segregated in the anterior and posterior AOBs may at least partially converge in higher brain centers.
59. ••].
60. ••] provide the first systematic analysis of the response of large populations of VNO neurons to pheromonal stimuli. The characteristics of the VNO sensory response appear remarkably different from that of the MOE.