Sensory transduction in vomeronasal neurons: Evidence for Gαo, Gαi2, and adenylyl cyclase II as major components of a pheromone signaling cascade

Journal of Neuroscience

Volumn 16, Issue 3, 1996, Pages 909-918

  Berghard, Anna ^a   Buck, Linda B ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

adenylyl cyclase; chemosensory; G protein; Jacobson's organ; olfactory; pheromone; signal transduction; vomeronasal

Indexed keywords

ADENYLATE CYCLASE; COMPLEMENTARY DNA; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANYLATE CYCLASE; MESSENGER RNA; PHEROMONE; POLYADENYLATED RNA;

ANIMAL CELL; ARTICLE; ENZYME ACTIVITY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NEUROEPITHELIUM; NONHUMAN; OLFACTORY NERVOUS SYSTEM; PRIORITY JOURNAL; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; VOMERONASAL ORGAN;

EID: 0029914569     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-03-00909.1996     Document Type: Article

References (59)

1. Ache BW (1994) Towards a common strategy for transducing olfactory information. Semin Cell Biol 5:55-63.
2. Bakalyar HA, Reed RR (1990) Identification of a specialized adenylate cyclase that may mediate odorant detection. Science 250:1403-1406.
3. Barber PC, Raisman G (1978) Cell division in the vomeronasal organ of the adult mouse. Brain Res 141:57-66.
4. Berghard A, Buck LB, Liman ER (1996) Evidence for distinct signalling mechanisms in two mammalian olfactory sense organs. Proc Natl Acad Sci USA, in press.
5. Boekhoff I, Tareilus E, Strotmann J, Breer H (1990) Rapid activation of alternative second messenger pathways in olfactory cilia from rats by different odorants. EMBO J 9:2453-2458.
6. Bray P, Carter A, Simons C, Guo V, Puckett C, Kamholz J, Spiegel A, Nirenberg M (1986) Human cDNA clones for four species of Gα signal transduction protein. Proc Natl Acad Sci USA 83:8893-8897.
7. Breer H, Raming K, Krieger J (1994) Signal recognition and transduction in olfactory neurons. Biochim Biophys Acta 1224:277-287.
8. Buck LB (1996) Information coding in the vertebrate olfactory system. Ann Rev Neurosci, in press.
9. Buck LB, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175-187.
10. Caggiano M, Kauer JS, Hunter DD (1994) Globose basal cells are neuronal progenitors in the olfactory epithelium: a linage analysis using a replication-incompetent retrovirus. Neuron 13:339-352.
11. Cathala G, Savouret J-F, Mendez B, West BL, Karin M, Martial JA, Baxter JD (1983) A method for isolation of intact translationally active ribonucleic acid. DNA 2:329-335.
12. Chen J, Iyengar R (1993) Inhibition of cloned adenylyl cyclases by mutant-activated Gi-α and specific suppression of type 2 adenylyl cyclase inhibition by phorbol ester treatment. J Biol Chem 268:12253-12256.
13. Cunningham AM, Ryugo DK, Sharp AH, Reed RR, Snyder SH, Ronnett GV (1993) Neuronal inositol 1,4,5-triphosphate receptor localized to the plasma membrane of olfactory cilia. Neuroscience 57:339-352.
14. Cuschieri A, Bannister LH (1975) The development of the olfactory mucosa in the mouse: light microscopy. J Anat 119:277-286.
15. Danciger E, Mettling C, Vidal M, Morris R, Margolis F (1989) Olfactory marker protein gene: its structure and olfactory neuron-specific expression in transgenic mice. Proc Natl Acad Sci USA 86:8565-8569.
16. Farbman AI, Margolis FL (1980) Olfactory marker protein during ontogeny: immunohistochemical localization. Dev Biol 74:205-215.
17. 2+/calmodulin-insensilive adenylyl cyclase from rat brain. Proc Natl Acad Sci USA 88:10173-10177.
18. Garrosa M, Coca S (1991) Postnatal development of the vomeronasal epithelium in the rat: an ultrastructural study. J Morphol 208:257-269.
19. Graziadei PPC, Monti-Graziadei GA (1979) Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J Neurocytol 8:1-18.
20. Halpern M (1987) The organization and function of the vomeronasal system. Annu Rev Neurosci 10:325-362.
21. Halpern M, Shapiro LS, Jia CP (1995) Differential localization of G proteins in the opossum vomeronasal system. Brain Res 677:157-161.
22. Hille B (1994) Modulation of ion-channel function by G-protein-coupled receptors. Trends Neurosci 17:531-535.
23. Keverne EB (1983) Pheromonal influences on the endocrine regulation of reproduction Trends Neurosci 6:381-384.
24. Kleuss C, Scherubl H, Hescheler J, Schultz G, Wittig B (1993) Selectivity in signal transduction determined by γ subunits of heterotrimeric G proteins. Science 259:832-834.
25. Koshimoto H, Katoh K, Yoshihara Y, Mori K (1992) Distribution of putative odour receptor proteins in olfactory epithelium. NeuroReport 3:521-523.
26. Krieger J, Schleicher S, Strotmann J, Wanner I, Boekhoff I, Raming K, De Geus P, Breer H (1994) Probing olfactory receptors with sequence-specific antibodies. Eur J Biochem 219:829-835.
27. Lamb TD, Pugh Jr EN (1992) G-protein cascades: gain and kinetics. Trends Neurosci 15:291-298.
28. Luo Y, Lu S, Chen P, Wang D, Halpern M (1994) Identification of chemoattractant receptors and G-proteins in the vomeronasal system of Garter snakes. J Biol Chem 269:16867-16877.
29. Menco BPM, Bruch RC, Dau B, Danho W (1992) Ultrastructural localization of olfactory transduction components: the G protein subunit Golfα and type III adenylate cyclase. Neuron 8:441-453.
30. Menco BPM, Tekula FD, Farbman AI, Danho W (1994) Developmental expression of G-proteins and adenylyl cyclase in peripheral olfactory systems: light microscopic and freeze-substitution electron microscopic immunohistochemistry. J Neurocytol 23:708-727.
31. 2+-insensitive adenylyl cyclases in the rat brain. Synapse 14:51-59.
32. Monti-Graziadei GA, Stanley RS, Graziadei PPC (1980) The olfactory marker protein in the olfactory system of the mouse during development. Neuroscience 5:1239-1252.
33. Murtagh Jr JJ, Moss J, Vaughan M (1994) Alternative splicing of the guanine nucleotide binding regulatory protein Goα generates four distinct mRNAs. Nucleic Acids Res 22:842-849.
34. Nakamura T, Gold G (1987) A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature 325:442-444.
35. Neer EJ (1995) Heterotrimeric G proteins: organizers of transmembrane signals. Cell 80:249-257.
36. Neubig RR (1994) Membrane organization in G-protein mechanisms. FASEB J 8:939-936.
37. Pedersen PE, Stewart WB, Greer CA, Shepherd GM (1983) Evidence for olfactory function in utero. Science 221:478-480.
38. Pieroni JP, Jacobowitz O, Chen J, Iyengar R (1993) Signal recognition and integration by Gs-stimulated adenylyl cyclases. Curr Opin Neurobiol 3:345-351.
39. Reed RR (1992) Signaling pathways in odorant detection. Neuron 8:205-209.
40. Ressler KJ, Sullivan SL, Buck LB (1993) A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73:597-609.
41. Ronnett GV, Snyder SH (1992) Molecular messengers of olfaction. Trends Neurosci 15:508-513.
42. Ronnett GV, Cho H, Hester LD, Wood SF, Snyder SH (1993) Odorants differentially enhance phosphoinositide turnover and adenylyl cyclase in olfactory receptor neurons. J Neurosci 13:1751-1758.
43. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd Ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
44. Sassoon DA, Garner I, Buckingham M (1988) Transcripts of α-cardiac and α-skeletal actins are early markers for myogenesis in the mouse embryo. Development 104:155-164.
45. Segovia S, Guillamon A (1993) Sexual dimorphism in the vomeronasal pathway and sex differences in reproductive behaviors. Brain Res Rev 18:51-74.
46. Senogles SE, Spiegel AM, Padrell E, Iyengar R, Caron MG (1990) Specificity of receptor-G protein interactions. J Biol Chem 265:4507-4514.
47. Shepherd GM (1988) Neurobiology. New York: Oxford UP.
48. Shinohara H, Asano T, Kato K (1992a) Differential localization of G-proteins Gi and Go in the accessory olfactory bulb of the rat. J Neurosci 12:1275-1279.
49. Shinohara H, Kato K, Asano T (1992b) Differential localization of G proteins, Gi and Go, in the olfactory epithelium and the main olfactory bulb of the rat. Acta Anat 144:167-171.
50. Sternweis PC (1994) The active role of βγ in signal transduction. Curr Opin Cell Biol 6:198-203.
51. Strittmatter SM, Fishman MC, Zhu X-P (1994) Activated mutants of the subunit of Go promote an increased number of neurites per cell. J Neurosci 14:2327-2338.
52. Strittmatter SM, Valenzuela D, Kennedy TE, Neer EJ, Fishman MC (1990) Go is a major growth cone protein subject to regulation by GAP-43. Nature 344:836-841.
53. Sullivan SL, Bohm S, Ressler KJ, Horowitz LF, Buck LB (1995) Target-independent pattern specification in the olfactory epithelium. Neuron 15:779-789.
54. Tang W-J, Gilman AG (1991) Type-specific regulation of adenylyl cyclase by G protein βγ subunits. Science 254:1500-1503.
55. Taniguchi M, Kashiwayanagi M, Kurihara K (1995) Intracellular injection of inositol 1,4,5-trisphosphate increases a conductance in membranes of turtle vomeronasal receptor neurons in the slice preparation. Neurosci Lett 188:5-8.
56. Taussig R, Gilman AG (1995) Mammalian membrane-bound adenylyl cyclases. J Biol Chem 270:1-4.
57. Wysocki CJ, Meredith M (1987) The vomeronasal system. In: The neurobiology of taste and smell (Finger TE, Silver WL, eds), pp 125-150. New York: Wiley.
58. Yoshimura M, Cooper DMF (1993) Type-specific stimulation of adenylyl cyclase by protein kinase C. J Biol Chem 268:4604-4607.
59. Zufall F, Firestein S, Shepherd GM (1994) Cyclic nucleotide-gated ion channels and sensory transduction in olfactory receptor cells. Annu Rev Biophys Struct 23:577-607.