Cells in the vomeronasal organ express odorant receptors but project to the accessory olfactory bulb

Journal of Comparative Neurology

Volumn 498, Issue 4, 2006, Pages 476-490

  Lévai, Olga ^a,b   Feistel, Torben ^a   Breer, Heinz ^a   Strotmann, Joerg ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b Leica Mikrosysteme Vertrieb GmbH   (Germany)

Author keywords

Accessory olfactory system; Chemoreception; Mouse; Projection

Indexed keywords

COMPLEMENTARY DNA; RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SUBPOPULATION; CELLULAR DISTRIBUTION; CHEMORECEPTOR; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MOLECULAR CLONING; MOUSE; NERVE PROJECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OLFACTORY BULB; OLFACTORY EPITHELIUM; OLFACTORY RECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL; TRANSGENIC MOUSE; VOMERONASAL ORGAN;

ANIMALS; FEMALE; GENE EXPRESSION PROFILING; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS, AFFERENT; OLFACTORY BULB; OLFACTORY MUCOSA; OLFACTORY PATHWAYS; RECEPTORS, ODORANT; TISSUE DISTRIBUTION; VOMERONASAL ORGAN;

EID: 33746593432     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21067     Document Type: Article

References (69)

1. Alenius M, Bohm S. 1997. Identification of a novel neural cell adhesion molecule-related gene with a potential role in selective axonal projection. J Biol Chem 272:26083-26086.
2. Baxi KN, Dorries KM, Eisthen HL. 2005. Is the vomeronasal system really specialized for detecting pheromones? Trends Neurosci 29:1-7.
3. Belluscio L, Koentges G, Axel R, Dulac C. 1999. A map of pheromone receptor activation in the mammalian brain. Cell 97:209-220.
4. Berghard A, Buck LB. 1996. Sensory transduction in vomeronasal neurons: evidence for Gao, Gai2, and adenylyl cyclase II as major components of a pheromone signaling cascade. J Neurosci 16:909-918.
5. Boschat C, Pelofi C, Randin O, Roppolo D, Luscher C, Broillet MC, Rodriguez I. 2002. Pheromone detection mediated by a V1r vomeronasal receptor. Nat Neurosci 5:1261-1262.
6. Breer H, Hoppe R, Kaluza J, Levai O, Strotmann J. 2005. Olfactory subsystems in mammals: specific roles in recognizing chemical signals? Chem Senses 30(Suppl 1):i144-i145.
7. Brennan PA, Keverne EB. 2004. Something in the air? New insights into mammalian pheromones. Curr Biol 14:R81-R89.
8. Buck L, Axel R. 1991. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175-187.
9. Buck LB. 2004. Olfactory receptors and odor coding in mammals. Nutr Rev 62:8184-8188.
10. Chess A, Simon I, Cedar H, Axel R. 1994. Allelic inactivation regulates olfactory receptor gene expression. Cell 78:823-834.
11. Conzelmann S, Malun D, Breer H, Strotmann J. 2001. Brain targeting and glomerulus formation of two olfactory neuron populations expressing related receptor types. Eur J Neurosci 14:1623-1632.
12. Cutforth T, Moring L, Mendelsohn M, Nemes A, Shah NM, Kim MM, Frisen J, Axel R. 2003. Axonal ephrin-as and odorant receptors. Coordinate determination of the olfactory sensory map. Cell 114:311-322.
13. Dorries KM, Adkins-Regan E, Halpern BP. 1997. Sensitivity and behavioral responses to the pheromone androstenone are not mediated by the vomeronasal organ in domestic pigs. Brain Behav Evol 49:53-62.
14. Dulac C, Axel R. 1995. A novel family of genes encoding putative pheromone receptors in mammals. Cell 83:195-206.
15. Dulac C, Torello AT. 2003. Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat Rev Neurosci 4:551-562.
16. Feinstein P, Bozza T, Rodriguez I, Vassalli A, Mombaerts P. 2004. Axon guidance of mouse olfactory sensory neurons by odorant receptors and the beta2 adrenergic receptor. Cell 117:833-846.
17. Feinstein P, Mombaerts P. 2004. A contextual model for axonal sorting into glomeruli in the mouse olfactory system. Cell 117:817-831.
18. Halpern M. 1987. The organization and function of the vomeronasal system. Annu Rev Neurosci 10:325-362.
19. Halpern M, Martinez-Marcos A. 2003. Structure and function of the vomeronasal system: an update. Prog Neurobiol 70:245-318.
20. Halpern M, Shnayder Shapiro L, Jia Ch. 1995. Differential localization of G proteins in the opossum vomeronasal system. Brain Res 677:157-161.
21. Henion TR, Raitcheva D, Grosholz R, Biellmann F, Skarnes WC, Hennet T, Schwarting GA. 2005. {beta}1,3-N-Acetylglucosaminyltransferase 1 glycosylation is required for axon pathfinding by olfactory sensory neurons. J Neurosci 25:1894-1903.
22. Herrada G, Dulac C. 1997. A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90:763-773.
23. Jia C, Halpern M. 1996. 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 719:117-128.
24. Jones DT, Reed RR. 1989. Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science 244:790-795.
25. Kaluza JF, Gussing F, Bohm S, Breer H, Strotmann J. 2004. Olfactory receptors in the mouse septal organ. J Neurosci Res 76:442-452.
26. Leinders-Zufall T, Lane AP, Puche AC, Ma W, Novotny MV, Shipley MT, Zufall F. 2000. Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405:792-796.
27. Levai O, Breer H, Strotmann J. 2003. Subzonal organization of olfactory sensory neurons projecting to distinct glomeruli within the mouse olfactory bulb. J Comp Neurol 458:209-220.
28. Levai O, Strotmann J. 2003. Projection pattern of nerve fibers from the septal organ: DiI-tracing studies with transgenic OMP mice. Histchem Cell Biol 120:483-492.
29. Liman ER, Corey DP, Dulac C. 1999. TRP2: a candidate transduction channel for mammalian pheromone sensory signaling. Proc Natl Acad Sci U S A 96:5791-5796.
30. Lin dY, Zhang SZ, Block E, Katz LC. 2005. Encoding social signals in the mouse main olfactory bulb. Nature 434:470-477.
31. Lipscomb BW, Treloar HB, Greer CA. 2002. Cell surface carbohydrates reveal heterogeneity in olfactory receptor cell axons in the mouse. Cell Tissue Res 308:7-17.
32. Lipscomb BW, Treloar HB, Henoff J, Greer CA. 2003. Cell surface carbohydrates and glomerular targeting of olfactory sensory neuron axons in the mouse. J Comp Neurol 467:22-31.
33. Luo M, Fee MS, Katz LC. 2003. Encoding pheromonal signals in the accessory olfactory bulb of behaving mice. Science 299:1196-1201.
34. Ma M, Grosmaitre X, Iwema CL, Baker H, Greer CA, Shepherd GM. 2003. Olfactory signal transduction in the mouse septal organ. J Neurosci 23:317-324.
35. Malnic B, Hirono J, Sato T, Buck LB. 1999. Combinatorial receptor codes for odors. Cell 96:713-723.
36. Matsunami H, Buck LB. 1997. A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90:775-784.
37. Mendoza AS. 1993. Morphological studies on the rodent main and accessory olfactory systems: the regio olfactoria and vomeronasal organ. Ann Anat 175:425-446.
38. Miyamichi K, Serizawa S, Kimura HM, Sakano H. 2005. Continuous and overlapping expression domains of odorant receptor genes in the olfactory epithelium determine the dorsal/ventral positioning of glomeruli in the olfactory bulb. J Neurosci 25:3586-3592.
39. Mombaerts P. 2004. Genes and ligands for odorant, vomeronasal and taste receptors. Nat Rev Neurosci 5:263-278.
40. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R. 1996. Visualizing an olfactory sensory map. Cell 87:675-686.
41. Potter SM, Zheng C, Koos DS, Feinstein P, Fraser SE, Mombaerts P. 2001. Structure and emergence of specific olfactory glomeruli in the mouse. J Neurosci 21:9713-9723.
42. Raming K, Krieger J, Strotmann J, Boekhoff I, Kubick S, Baumstark C, Breer H. 1993. Cloning and expression of odorant receptors. Nature 361:353-356.
43. Ressler KJ, Sullivan SL, Buck LB. 1993. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73:597-609.
44. Rodriguez I. 2004. Pheromone receptors in mammals. Horm Behav 46:219-230.
45. Rodriguez I, Feinstein P, Mombaerts P. 1999. Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell 97:199-208.
46. Royal SJ, Key B. 1999. Development of P2 olfactory glomeruli in P2-internal ribosome entry site-tau-LacZ transgenic mice. J Neurosci 19:9856-9864.
47. Ryba NJP, Tirindelli R. 1997. A new multigene family of putative pheromone receptors. Neuron 19:371-379.
48. Sam M, Vora S, Malnic B, Ma W, Novotny MV, Buck LB. 2001. Neuropharmacology. Odorants may arouse instinctive behaviours. Nature 412:142.
49. Schaal B, Coureaud G, Langlois D, Ginies C, Semon E, Perrier G. 2003. Chemical and behavioural characterization of the rabbit mammary pheromone. Nature 424:68-72.
50. Schwarting GA, Kostek C, Ahmad N, Dibble C, Pays L, Puschel AW. 2000. Semaphorin 3A is required for guidance of olfactory axons in mice. J Neurosci 20:7691-7697.
51. St. John JA, Clarris HJ, Key B. 2002. Multiple axon guidance cues establish the olfactory topographic map: how do these cues interact? Int J Dev Biol 46:639-647.
52. Storan MJ, Magnaldo T, Biol-N'Garagba MC, Zick Y, Key B. 2004. Expression and putative role of lactoseries carbohydrates present on NCAM in the rat primary olfactory pathway. J Comp Neurol 475:289-302.
53. Stowers L, Marton TF. 2005. What is a pheromone? Mammalian pheromones reconsidered. Neuron 46:699-702.
54. Strotmann J, Wanner I, Helfrich T, Beck A, Meinken C, Kubick S, Breer H. 1994. Olfactory neurones expressing distinct odorant receptor subtypes are spatially segregated in the nasal neuroepithelium. Cell Tissue Res 276:429-438.
55. Swann J, Rahaman F, Bijak T, Fiber J. 2001. The main olfactory system mediates pheromone-induced fos expression in the extended amygdala and preoptic area of the male Syrian hamster. Neuroscience 105:695-706.
56. Taniguchi M, Nagao H, Takahashi YK, Yamaguchi M, Mitsui S, Yagi T, Mori K, Shimizu T. 2003. Distorted odor maps in the olfactory bulb of semaphorin 3A-deficient mice. J Neurosci 23:1390-1397.
57. Tian H, Ma M. 2004. Molecular organization of the olfactory septal organ. J Neurosci 24:8383-8390.
58. Trinh K, Storm DR. 2003. Vomeronasal organ detects odorants in absence of signaling through main olfactory epithelium. Nat Neurosci. 6:519-525.
59. Trinh K, Storm DR. 2004. Detection of odorants through the main olfactory epithelium and vomeronasal organ of mice. Nutr Rev 62:8189-8192.
60. Vassalli A, Rothman A, Feinstein P, Zapotocky M, Mombaerts P. 2002. Minigenes impart odorant receptor-specific axon guidance in the olfactory bulb. Neuron 35:681.
61. Vassar R, Ngai J, Axel R. 1993. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74:309-318.
62. Wang F, Nemes A, Mendelsohn M, Axel R. 1998. Odorant receptors govern the formation of a precise topographic map. Cell 93:47-60.
63. Wong ST, Trinh K, Hacker B, Chan GC, Lowe G, Gaggar A, Xia Z, Gold GH, Storm DR. 2000. Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron 27:487-497.
64. Wysocki CJ, Meredith M. 1987. The vomeronasal system. In: Finger TE, Silver WL, editors. Neurobiology of taste and smell. New York: John Wiley & Sons, p 125-150.
65. Xu F, Schaefer M, Kida I, Schafer J, Liu N, Rothman DL, Hyder F, Restrepo D, Shepherd GM. 2005. Simultaneous activation of mouse main and accessory olfactory bulbs by odors or pheromones. J Comp Neurol 489:491-500.
66. Yoshihara Y, Kawasaki M, Tamada A, Fujita H, Hayashi H, Kagamiyama H, Mori K. 1997. OCAM: a new member of the neural cell adhesion molecule family related to zone-to-zone projection of olfactory and vomeronasal axons. J Neurosci 17:5830-5842.
67. Young JM, Shykind BM, Lane RP, Tonnes-Priddy L, Ross JA, Walker M, Williams EM, Trask BJ. 2003. Odorant receptor expressed sequence tags demonstrate olfactory expression of over 400 genes, extensive alternate splicing and unequal expression levels. Genome Biol 4:R71.
68. Zhang X, Firestein S. 2002. The olfactory receptor gene superfamily of the mouse. Nat Neurosci 5:124-133.
69. Zou Z, Horowitz LF, Montmayeur JP, Snapper S, Buck LB. 2001. Genetic tracing reveals a stereotyped sensory map in the olfactory cortex. Nature 414:173-179.