Nitric oxide synthase, cGMP, and NO-mediated cGMP production in the olfactory bulb of the rat

Journal of Comparative Neurology

Volumn 375, Issue 4, 1996, Pages 641-658

  Hopkins, David A ^a,c   Steinbusch, Harry W M ^b   Markerink Van Ittersum, Marjanne ^b   De Vente, Jan ^b  

^a DALHOUSIE UNIVERSITY   (Canada)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c DALHOUSIE UNIVERSITY   (Canada)

Author keywords

glutamate receptors; intercellular messenger; NO cGMP cascade; soluble guanylyl cyclase

Indexed keywords

CYCLIC GMP; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ANIMAL TISSUE; ARTICLE; ENZYME ASSAY; IMMUNOHISTOCHEMISTRY; MALE; MICROPHOTOGRAPHY; NONHUMAN; OLFACTORY BULB; OLFACTORY NERVE; PRIORITY JOURNAL; RAT; TISSUE SECTION;

ANIMALS; CYCLIC GMP; ENZYME INHIBITORS; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; MALE; NADPH DEHYDROGENASE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITROPRUSSIDE; OLFACTORY BULB; RATS; RATS, INBRED LEW; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION;

EID: 0029859343     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19961125)375:4<641::AID-CNE6>3.0.CO;2-1     Document Type: Article

References (77)

1. Ahmad, I., T. Leinders-Zufall, J.D. Kocsis, G.M. Shepherd, F. Zufall, and C.J. Barnstable (1994) Retinal ganglion cells express a cGMP-gated cation conductance activatable by nitric oxide donors. Neuron 12: 155-165.
2. Bailey, M.S., and M.T. Shipley (1993) Astrocyte subtypes in the rat olfactory bulb: Morphological heterogeneity and differential laminar distribution. J. Comp. Neurol. 328:501-526.
3. Boekhoff, I., and H. Breer (1992) Termination of second messenger signaling in olfaction. Proc. Natl. Acad. Sci. USA 89:471-474.
4. Boulton, C.L., A.J. Irving, E. Southam, B. Potier, J. Garthwaite, and J.L. Collingridge (1994) The nitric oxide-cyclic GMP pathway and synaptic depression in rat hippocampal slices. Eur. J. Neurosci. 6:1528-1535.
5. Bredt, D.S., and S.H. Snyder (1989) Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc. Natl. Acad. Sci. USA 86:9030-9033.
6. Bredt, D.S., P.M. Hwang, and S.H. Snyder (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347:768-770.
7. Breer, H., and G.M. Shepherd (1993) Implications of the NO/cGMP system for olfaction. Trends Neurosci. 16:5-9.
8. Breer, H., I. Boekhoff, and E. Tareilus (1990) Rapid kinetics of second messenger formation in olfactory transduction. Nature 345:65-68.
9. Breer, H., T. Klemm, and I. Boekhoff (1992) Nitric oxide mediated formation of cyclic GMP in the olfactory system. NeuroReport 3:1030-1032.
10. Brooker, G., J.F. Harper, W.L. Terasaki, and R.D. Moylan (1979) Radioimmunoassay of cyclic AMP and cyclic GMP. Adv. Cycl. Nucl. Res. 10:1-33.
11. Brüne, B., and V. Ullrich (1987) Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase. Mol. Pharmacol. 32:497-504.
12. Burgunder, J.-M., and P.T. Cheung (1994) Expression of soluble guanylyl cyclase gene in adult rat brain. Eur. J. Neurosci. 6:211-217.
13. 2+-calmodulin of cyclic nucleotide-activated channel of rat olfactory receptor neurons. Nature 368:545-548.
14. Crespo, C., R. Arévalo, J.G. Briñón, A. Porteros, J. Aijón, and J.R. Alonso (1995) Colocalization of NADPH-diaphorase and acetylcholinesterase in the rat olfactory bulb. J. Chem. Neuroanat. 9:207-216.
15. Davis, B.J. (1991) NADPH-diaphorase activity in the olfactory system of the hamster and rat. J. Comp. Neurol. 314:493-511.
16. Dawson, T.M., D.S. Bredt, M. Fotuhi, P.M. Hwang, and S.H. Snyder (1991) Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc. Natl. Acad. Sci. USA 88:7797-7801.
17. Dellacorte, C., D.L. Kalinoski, T. Huque, L. Wysocki, and D. Restrepo (1995) NADPH diaphorase staining suggests localization of nitric oxide synthase within mature vertebrate olfactory neurons. Neuroscience 66:215-225.
18. De Vente, J., and H.W.M. Steinbusch (1992) On the stimulation of soluble and particulate guanylate cyclase in the rat brain and the involvement of nitric oxide as studied by cGMP immunocytochemistry. Acta Histochem. 92:13-38.
19. De Vente, J., H.W.M. Steinbusch, and J. Schipper (1987) A new approach to immunocytochemistry of 3′,5′-cyclic guanosine monophosphate: Preparation, specificity, and initial application of a new antiserum against formaldehyde-fixed 3′,5′-cyclic guanosine monophosphate. Neuroscience 22:361-373.
20. De Vente, J., J.G.J.M. Bol, and H.W.M. Steinbusch (1989) cGMP-producing, atrial natriuretic factor-responding cells in the rat brain. An immunocytochemical study. Eur. J. Neurosci. 1:436-460.
21. Egebjerg, J., B. Bettler, I. Hermans-Borgmeyer, and S. Heinemann (1991) Cloning of a cDNA for a glutamate receptor subunit activated by kainate but not by AMPA. Nature 351:745-748.
22. Ewing, J.F., and M.D. Maines (1992) In situ hybridization and immunohistochemical localization of heme oxygenase-2 mRNA and protein in normal rat brain: Differential distribution of isozyme 1 and 2. Mol. Cell. Neurosci. 3:559-570.
23. Frings, S., J.W. Lynch, and B. Lindemann (1992) Properties of cyclic nucleotide-gated channels mediating olfactory transduction. J. Gen. Physiol. 100:45-67.
24. Furuyama, T., S. Inagaki, and H. Takagi (1993) Localizations of α1 and β1 subunits of soluble guanylate cyclase in the rat brain. Mol. Brain Res. 20:335-344.
25. Furuyama, T., Y. Iwahashi, Y. Tano, H. Takagi, and S. Inagaki (1994) Localization of 63-kDa calmodulin-stimulated phosphodiesterase mRNA in the rat brain by in situ hybridization histochemistry. Mol. Brain Res. 26:331-336.
26. Garbers, D.L., and D.G. Lowe (1994) Guanylyl cyclase receptors. J. Biol. Chem. 269:30741-30744.
27. Garthwaite, J. (1991) Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci. 14:60-67.
28. Hirata, M., and F. Murad (1994) Interrelationships of cyclic GMP, inositol phosphates, and calcium. Adv. Pharmacol. 26:195-216.
29. Hope, B.T., G.J. Michael, K.M. Knigge, and S.R. Vincent (1991) Neuronal NADPH-diaphorase is a nitric oxide synthase. Proc. Natl. Acad. Sci. USA 88:2811-2814.
30. Ignarro, L.J. (1994) Regulation of cytosolic guanylyl cyclase by porphyrins and metalloporphyrins. Adv. Pharmacol. 26:36-65.
31. Ingi, T., and G.V. Ronnett (1995) Direct demonstration of a physiological role for carbon monoxide in olfactory receptor neurons. J. Neurosci. 15:8214-8222.
32. Jaworsky, D.E., O. Matsuzaki, F.F. Borisy, and G.V. Ronnett (1995) Calcium modulates the rapid kinetics of the odorant-induced cyclic AMP signal in rat olfactory cilia. J. Neurosci. 15:310-318.
33. Kishimoto, J., E.B. Keverne, J. Hardwick, and P.C. Emson (1993) Localization of nitric oxide synthase in the mouse olfactory and vomeronasal system: A histochemical, immunological and in situ hybridization study. Eur. J. Neurosci. 5:1684-1694.
34. Knowles, R.G., M. Palacios, R.M.J. Parker, and S. Moncada (1989) Formation of nitric oxide from L-arginine in the central nervous system: A transduction mechanism for stimulation of the soluble guanylate cyclase. Proc. Natl. Acad. Sci. USA 86:5159-5162.
35. 2+ regulates the sensitivity of cyclic nucleotide-gated channels in olfactory receptor neurons. Neuron 9:897-906.
36. Kutsuwada, T., N. Kashiwabuchi, H. Mori, K. Sakimura, E. Kushiya, K. Araki, H. Meguro, H. Masaki, T. Kumanishi, M. Arakawa, and M. Mishina (1992) Molecular diversity of the NMDA receptor channel. Nature 358:36-41.
37. Laurie, D.J., and P.H. Seeburg (1994) Regional and developmental heterogeneity in splicing of the rat brain NMDAR1 mRNA. J. Neurosci. 14:3180-3194.
38. Leinders-Zufall, T., G.M. Shepherd, and F. Zufall (1995) Regulation of cyclic nucleotide-gated channels and membrane excitability in olfactory receptor cells by carbon monoxide. J. Neurophysiol. 74:1498-1507.
39. Lowry, O.H., N.J. Rosebrough, A.L. Farr, and F.J. Randall (1951) Protein measurement with the Folin reagent. J. Biol. Chem. 193:265-275.
40. Luo, D., and S.R. Vincent (1994) Metalloporphyrins inhibit nitric oxide-dependent cGMP formation in vivo. Eur. J. Pharmacol. 267:263-267.
41. Martin, L.J., C.D. Blackstone, A.I. Levey, R.L. Huganir, and D.L. Price (1993) AMPA glutamate receptor subunits are differentially distributed in rat brain. Neuroscience 53:327-358.
42. Matsuoka, I., G. Giuili, M. Poyard, D. Stengel, J. Parma, G. Guellaen, and J. Hanoune (1992) Localization of adenylyl and guanylyl cyclase in rat brain by in situ hybridization: Comparison with calmodulin mRNA distribution. J. Neurosci. 12:3350-3360.
43. McLean, J.H., M.T. Shipley, W.T. Nickell, G. Aston-Jones, and C.K.H. Reyher (1989) Chemoanatomical organization of the noradrenergic input from locus coeruleus to the olfactory bulb of the adult rat. J. Comp. Neurol. 285:339-349.
44. Molnár, E., A. Baude, S.A. Richmond, P.B. Patel, P. Somogyi, and R.A.J. McIlhinney (1993) Biochemical and immunocytochemical characterization of antipeptide antibodies to a cloned GluR1 glutamate receptor subunit: Cellular and subcellular distribution in the rat forebrain. Neuroscience 53:307-326.
45. Monyer, H., R. Sprengel, R. Schoepfer, A. Herb, M. Higuchi, H. Lomeli, N. Burnashev, B. Sakmann, and P.H. Seeburg (1992) Heteromeric NMDA receptors: Molecular and functional distinction of subtypes. Science 256:1217-1221.
46. Mori, H., and M. Mishina (1995) Structure and function of the NMDA receptor channel. Neuropharmacology 34:1219-1237.
47. Moriyoshi, K., M. Masu, T. Ishii, R. Shigemoto, N. Mizuno, and S. Nakanishi (1991) Molecular cloning and characterization of the rat NMDA receptor. Nature 354:31-37.
48. Murad, F. (1994) Regulation of cytosolic guanylyl cyclase by nitric oxide: The NO-cyclic GMP signal transduction system. Adv. Pharmacol. 26:19-33.
49. Murad, F., C.K. Mittal, W.P. Arnold, S. Katsuki, and H. Kimura (1978) Guanylate cyclase: Activation by azide, nitro compounds, nitric oxide, and hydroxyl radical and inhibition by hemoglobin and myoglobin. Adv. Cyc. Nucleotide Res. 9:145-158.
50. Nakamura, T., and G.H. Gold (1987) A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature 325:442-444.
51. Petralia, R.S., and R.J. Wenthold (1992) Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J. Comp. Neurol. 318:329-354.
52. Petralia, R.S., Y.-X. Wang, and R.J. Wenthold (1994) Histological and ultrastructural localization of the kainate receptor subunits, KA2 and GluR6/7, in the rat nervous system using selective antipeptide antibodies. J. Comp. Neurol. 349:85-110.
53. Pinching, A.J., and T.P.S. Powell (1971) The neuron types of the glomerular layer of the olfactory bulb. J. Cell Sci. 9:305-345.
54. Porteros, A., J.R. Alonso, R. Arévalo, E. García-Ojeda, C. Crespo, and J. Aijón (1994) Histochemical localization of NADPH-diaphorase in the rat accessory olfactory bulb. Chem. Senses 19:413-424.
55. Price, J.L., and T.P.S. Powell (1970a) The morphology of the granule cells of the olfactory bulb. J. Cell Sci. 7:91-123.
56. Price, J.L., and T.P.S. Powell (1970b) The synaptology of the granule cells of the olfactory bulb. J. Cell Sci. 7:125-155.
57. Rodrigo, J., D.R. Springall, O. Uttenthal, M.L. Bentura, F. Abadia-Molina, V. Riveros-Moreno, R. Martinez-Murillo, J.M. Polak, and S. Moncada (1994) Localization of nitric oxide synthase in the adult rat brain. Philos. Trans. R. Soc. Lond. [Biol] 345:175-221.
58. Roskams, A., D.S. Bredt, T.M., and G.V. Ronnett (1994) Nitric oxide mediates the formation of synaptic connections in developing and regenerating olfactory receptor neurons. Neuron 13:289-299.
59. Sato, K., G. Mick, H. Kiyama, and M. Tohyama (1995) Expression patterns of a glutamate-binding protein in the rat central nervous system: Comparison with N-methyl-D-aspartate receptor subunit 1 in rat. Neuroscience 64:459-475.
60. Scherer-Singler, U., S.R. Vincent, H. Kimura, and E.G. McGeer (1983) Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry. J. Neurosci. Methods 9:229-234.
61. Schmidt, H.H.H.W., G.D. Gagne, M. Nakane, J.S. Pollock, M.F. Miller, and F. Murad (1992) Mapping of neural nitric oxide synthase in the rat suggests frequent colocalization with NADPH diaphorase but not with soluble guanylyl cyclase, and novel paraneural functions for nitrinergic signal transduction. J. Histochem. Cytochem. 40:1439-1456.
62. Scott, J.W., J.K. McDonald, and J.L. Pemberton (1987) Short axon cells of the rat olfactory bulb display NADPH-diaphorase activity, neuropeptide Y-like immunoreactivity, and somatostatin-like immunoreactivity. J. Comp. Neurol. 260:378-391.
63. Shepherd, G.M., and C.A. Greer (1990) Olfactory bulb. In G.M. Shepherd (ed): The Synaptic Organization of the Brain. New York: Oxford University Press, pp. 133-169.
64. Shipley, M.T., J.H. McLean, and M. Ennis (1995) Olfactory system. In G. Paxinos (ed): The Rat Nervous System. San Diego: Academic Press, pp. 899-926.
65. Shuttleworth, C.W., C. Xue, S.M. Ward, J. de Vente, and K.M. Sanders (1993) Immunohistochemical localization of 3′,5′-cyclic guanosine monophosphate in the canine proximal colon: Responses to nitric oxide and electrical stimulation of enteric inhibitory neurons. Neuroscience 56:513-522.
66. Sonnenburg, W.K., and J.A. Beavo (1994) Cyclic GMP and regulation of cyclic nucleotide hydrolysis. Adv. Pharmacol. 26:87-114.
67. Southam, E., and J. Garthwaite (1993) The nitric oxide-cyclic GMP signalling pathway in rat brain. Neuropharmacology 32:1267-1277.
68. Spessert, R., C. Wohlgemuth, S. Reuss, and E. Layes (1994) NADPH-diaphorase activity of nitric oxide synthase in the olfactory bulb: Co-factor specificity and characterization regarding the interrelation to NO formation. J. Histochem. Cytochem. 42:569-575.
69. Struble, R.G., and C.P. Walters (1982) Light microscopic differentiation of two populations of rat olfactory bulb granule cells. Brain Res. 236:237-251.
70. Traylor, T.G., and V.S. Sharma (1992) Why NO? Biochemistry 31:263-267.
71. Verma, A., O.J. Hirsch, C.E. Glatt, G.V. Ronnett, and S.H. Snyder (1993) Carbon monoxide: a putative neural messenger. Science 259:381-384.
72. Vincent, S.R. (1994) Nitric oxide: A radical neurotransmitter in the central nervous system. Prog. Neurobiol. 42:129-160.
73. Vincent, S.R., and H. Kimura (1992) Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46:755-784.
74. Waldman, S.A., and F. Murad (1987) Cyclic GMP synthesis and function. Pharmacol. Rev. 39:163-196.
75. Young, H.M., K. McConalogue, J.B. Furness, and J. de Vente (1993) Nitric oxide targets in the guinea-pig intestine identified by induction of cyclic GMP immunoreactivity. Neuroscience 55:583-596.
76. Zhao, H., S. Firestein, and C.A. Greer (1994) NADPH-diaphorase localization in the olfactory system. NeuroReport 6:149-152.
77. Zufall, F., S. Firestein, and G.M. Shepherd (1991) Analysis of single cyclic nucleotide-gated channels in olfactory receptor cells. J. Neurosci. 11:3573-3580.