NADPH diaphorase activity in olfactory receptor neurons and their axons conforms to a rhinotopically-distinct dorsal zone of the hamster nasal cavity and main olfactory bulb

Journal of Chemical Neuroanatomy

Volumn 24, Issue 4, 2002, Pages 269-285

  Schoenfeld, Thomas A ^a   Knott, Thomas K ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

NADPH cytochrome P450 oxidoreductase; NADPH dehydrogenase; Nitric oxide synthase; Odorant receptors; Olfactory mucosa; Topographic brain mapping

Indexed keywords

CYTOCHROME P450 REDUCTASE; NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GLOMERULUS; HAMSTER; HISTOCHEMISTRY; MALE; NERVE ENDING; NERVE FIBER; NONHUMAN; NOSE; NOSE CAVITY; OLFACTORY BULB; OLFACTORY RECEPTOR; PRIORITY JOURNAL; RECEPTOR GENE; TOPOGRAPHY;

ANIMALS; AXONS; CRICETINAE; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MESOCRICETUS; NADPH DEHYDROGENASE; NASAL CAVITY; OLFACTORY BULB; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS;

EID: 0036844257     PISSN: 08910618     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-0618(02)00070-4     Document Type: Article

References (69)

1. Adams D.R., Jones A.M., Plopper C.G., Serabjit-Singh C.J., Philpot R.M. Distribution of cytochrome P-450 monoxygenase enzymes in the nasal mucosa of hamster and rat. Am. J. Anat. 190:1991;291-298.
2. Alonso J.R., Porteros A., Crespo C., Arévalo R., Aijòn J., Weruaga E., Aijòn J. Chemical anatomy of the macaque monkey olfactory bulb: NADPH-diaphorase/nitric oxide synthase activity. J. Comp. Neurol. 402:1998;419-434.
3. Arnhold S., Andressen C., Bloch W., Mai J.K., Addicks K. NO synthase-II is transiently expressed in embryonic mouse olfactory receptor neurons. Neurosci. Lett. 229:1997;165-168.
4. Astic L., Saucier D. Anatomical mapping of the neuroepithelial projection to the olfactory bulb in the rat. Brain Res. Bull. 16:1986;445-454.
5. Briñón J.G., Crespo C., Weruaga E., Alonso J., Sobreviela T., Aijòn J., Alonso J.R. NADPH-diaphorase/nitric oxide synthase-positive elements in the human olfactory bulb. NeuroReport. 9:1998;3141-3146.
6. Clancy A.N., Schoenfeld T.A., Forbes W.B., Macrides F. The spatial organization of the peripheral olfactory system of the hamster. Part II: receptor surfaces and odorant passageways within the nasal cavity. Brain Res. Bull. 34:1994;211-241.
7. Costanzo R.M., Mozell M.M. Electrophysiological evidence for a topographical projection of the nasal mucosa into the olfactory bulb of the frog. J. Gen. Physiol. 68:1976;297-312.
8. Croul-Ottman C.E., Brunjes P.C. NADPH diaphorase staining within the developing olfactory bulbs of normal and unilaterally odor-deprived rats. Brain Res. 460:1988;323-328.
9. Cummings D.M., Emge D.K., Small S.L., Margolis F.L. Pattern of olfactory bulb innervation returns after recovery from reversible peripheral deafferentation. J. Comp. Neurol. 421:2000;362-373.
10. Davis B.J. NADPH-diaphorase activity in the olfactory system of the hamster and rat. J. Comp. Neurol. 314:1991;493-511.
11. Dawson T.M., Bredt D.S., Fotuhi M., Hwang P.M., Snyder S.H. Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc. Natl. Acad. Sci. USA. 88:1991;7797-7801.
12. DellaCorte C., Kalinoski D.L., Huque T., Wysocki L., Restrepo D. NADPH diaphorase staining suggests localization of nitric oxide synthase within mature vertebrate olfactory neurons. Neuroscience. 66:1995;215-225.
13. Dinerman J.L., Dawson T.M., Schell M.J., Snowman A., Snyder S.H. Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: implications for synaptic plasticity. Proc. Natl. Acad. Sci. USA. 91:1994;4214-4218.
14. Dubois-Dauphin M., Tribollet E., Dreifuss J.J. Relations somatotopiques entre la muqueuse olfactive et la bulbe olfactif chez le triton. Brain Res. 219:1981;269-287.
15. Duncan H.J., Nickell W.T., Shipley M.T., Gesteland R.C. Organization of projections from olfactory epithelium to olfactory bulb in the frog, Rana pipiens. J. Comp. Neurol. 299:1990;299-311.
16. Halpern M., Jia C., Shnayder Shapiro L. Segregated pathways in the vomeronasal system. Micr. Res. Technol. 41:1998;519-529.
17. Hanazawa T., Motosugi H., Konno A., Kaneko T., Tanaka K., Chiba T. Distribution of NADPH-diaphorase positive nerve fibers in the rat nasal mucosa. Neurosci. Lett. 159:1993;71-74.
18. Hope B.T., Michael G.J., Knigge K.M., Vincent S.R. Neuronal NADPH diaphorase is a nitric oxide synthase. Proc. Natl. Acad. Sci. USA. 88:1991;2811-2814.
19. Hopkins D.A., Steinbusch H.W.M., Markerink-van Ittersum M., DeVente J. Nitric oxide synthase, cGMP, and NO-mediated cGMP production in the olfactory bulb of the rat. J. Comp. Neurol. 375:1996;641-658.
20. Ingi T., Ronnett G.V. Direct demonstration of a physiological role for carbon monoxide in olfactory receptor neurons. J. Neurosci. 15:1995;8214-8222.
21. Jang T., Singer A.G., O'Connell R.J. Induction of c-fos in hamster accessory olfactory bulbs by natural and cloned aphrodisin. NeuroReport. 12:2001;449-452.
22. Johnson B.A., Leon M. Odorant molecular length: one aspect of the olfactory code. J. Comp. Neurol. 426:2000;330-338.
23. Kimbell J.S., Godo M.N., Gross E.A., Joyner D.R., Richardson R.B., Morgan K.T. Computer simulation of inspiratory airflow in all regions of the F344 rat nasal passages. Toxicol. Appl. Pharmacol. 145:1997;388-398.
24. Kishimoto J., Keverne E.B., Hardwick J., Emson P.C. Localization of nitric oxide synthase in the mouse olfactory and vomeronasal system: a histochemical, immunological and in situ hybridization study. Eur. J. Neurosci. 5:1993;1684-1694.
25. Kulkarni A.P., Getchell T.V., Getchell M.L. Neuronal nitric oxide synthase is localized in extrinsic nerves regulating perireceptor processes in the chemosensory nasal mucosae of rats and humans. J. Comp. Neurol. 343:1994;1-14.
26. Lema S.C., Nevitt G.A. Re-evaluating NADPH-diaphorase histochemistry as an indicator of nitric oxide synthase: an examination of the olfactory system of coho salmon (Oncorhynchus kisutch). Neurosci. Lett. 313:2001;1-4.
27. Mackay-Sim A., Nathan M.H. The projection from the olfactory epithelium to the olfactory bulb in the salamander, Ambystoma tigrinum. Anat. Embryol. 170:1984;93-97.
28. Macrides F. Dynamic aspects of central olfactory processing. Muller-Schwarze D., Mozell M.M., Chemical Signals in Vertebrates. 1977;499-514 Plenum Press, New York.
29. Maines M.D. The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37:1997;517-554.
30. Matsumoto T., Nakane M., Pollock J.S., Kuk J.E., Förstermann U. A correlation between soluble brain nitric oxide synthase and NADPH-diaphorase activity is only seen after exposure of the tissue to fixative. Neurosci. Lett. 155:1993;61-64.
31. 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.
32. Mori K., von Campenhause H., Yoshihara Y. Zonal organization of the mammalian main and accessory olfactory systems. Philos. Trans. R. Soc. London B Biol. Sci. 355:2000;1801-1812.
33. Mozell M.M., Jagodowicz M. Chromatographic separation of odorants by the nose: retention times measured across in vivo olfactory mucosa. Science. 181:1973;1247-1249.
34. Nagao H., Yoshihara Y., Mitsui S., Fujisawa H., Mori K. Two mirror-image sensory maps with domain organization in the mouse main olfactory bulb. NeuroReport. 11:2000;3023-3027.
35. Norris P.J., Hardwick J.P., Emson P.C. Localization of NADPH cytochrome P450 oxidoreductase in rat brain by immunohistochemistry and in situ hybridization and a comparison with the distribution of neuronal NADPH-diaphorase staining. Neuroscience. 61:1994;331-350.
36. Porteros A., Arévalo R., Crespo C., Briñón J.G., Weruaga E., Aijòn J., Alonso J.R. Nitric oxide synthase activity in the olfactory bulb of anuran and urodele amphibians. Brain Res. 724:1996;67-72.
37. Radtke-Schuller S., Kunzle H. Olfactory bulb and retrobulbar regions in the hedgehog tenrec: organization and interconnections. J. Comp. Neurol. 423:2000;687-705.
38. Ressler K.J., Sullivan S.L., Buck L.B. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell. 73:1993;597-609.
39. 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.
40. Roskams A.J., Bredt D.S., Dawson T.M., Ronnett G.V. Nitric oxide mediates the formation of synaptic connections in developing and regenerating olfactory receptor neurons. Neuron. 13:1994;289-299.
41. Sanchez-Islas E., Leon-Olea M. Histochemical and immunohistochemical localization of neuronal nitric oxide synthase in the olfactory epithelium of the axolotl, Ambystoma mexicanum. Nitric Oxide. 5:2001;302-316.
42. Schaefer M.L., Finger T.E., Restrepo D. Variability of position of the P2 glomerulus within a map of the mouse olfactory bulb. J. Comp. Neurol. 436:2001;351-362.
43. Schaefer M.L., Young D.A., Restrepo D. Olfactory fingerprints for major histocompatibility complex-determined body odors. J. Neurosci. 21:2001;2481-2487.
44. Schmachtenberg O., Bicker G., Bacigalupo J. NADPH diaphorase is developmentally regulated in rat olfactory epithelium. NeuroReport. 12:2001;1039-1043.
45. Schoenfeld T.A., Macrides F. Topographic organization of connections between the main olfactory bulb and pars externa of the anterior olfactory nucleus in the hamster. J. Comp. Neurol. 227:1984;121-135.
46. Schoenfeld T.A., Marchand J.E., Macrides F. Topographic organization of tufted cell axonal projections in the hamster main olfactory bulb: an intrabulbar associational system. J. Comp. Neurol. 235:1985;503-518.
47. Schoenfeld T.A., Clancy A.N., Forbes W.B., Macrides F. The spatial organization of the peripheral olfactory system of the hamster. Part I: receptor neuron projections to the main olfactory bulb. Brain Res. Bull. 34:1994;183-210.
48. Schwarting G.A., Crandall J.E. Subsets of olfactory and vomeronasal sensory epithelial cells and axons revealed by monoclonal antibodies to carbohydrate antigens. Brain Res. 547:1991;239-248.
49. Schwob J.E., Gottlieb D.I. Purification and characterization of an antigen that is spatially segregated in the primary olfactory projection. J. Neurosci. 8:1988;3470-3480.
50. Scott J.W., McDonald J.K., Pemberton J.L. Short axon cells of the rat olfactory bulb display NADPH-diaphorase activity, neuropeptide Y-like immunoreactivity, and somatostatin-like immunoreactivity. J. Comp. Neurol. 260:1987;378-391.
51. Scott J.W., Brierley T., Schmidt F.H. Chemical determinants of the rat electro-olfactogram. J. Neurosci. 20:2000;4721-4731.
52. Spessert R., Claassen M. Histochemical differentiation between nitric oxide synthase-related and unrelated diaphorase activity in the rat olfactory bulb. Histochem. J. 30:1998;41-50.
53. Spessert R., Wohlgemuth C., Reuss S., Layes E. 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. 42:1994;569-575.
54. Stewart W.B., Pedersen P.E. The spatial organization of olfactory nerve projections. Brain Res. 411:1985;248-258.
55. Stoward P.J., Meijer A.E.F.H., Seidler E., Wohlrab F. Dehydrogenases. Stoward P.J., Pearse A.G.E., Histochemistry: Theoretical and Applied. 1991;27-71 Churchill Livingstone, New York.
56. Strotmann J., Krieger J., Beck A., Wanner I., Helfrich T., Breer H. Zonal topography of odorant receptor expression in the rat olfactory epithelium. Adv. Biosci. 93:1994;53-58.
57. Strotmann J., Conzelmann S., Beck A., Feinstein P., Breer H., Mombaerts P. Local permutations in the glomerular array of the mouse olfactory bulb. J. Neurosci. 20:2000;6927-6938.
58. Thomas E., Pearse A.G.E. The solitary active cells: histochemical demonstration of damage-resistant nerve cells with a TPN-diaphorase reaction. Acta Neuropathol. 3:1964;238-249.
59. Tracey W.R., Nakane M., Pollock J.S., Forstermann U. Nitric oxide synthases in neuronal cells, macrophages and endothelium are NADPH diaphorases, but represent only a fraction of total cellular NADPH diaphorase activity. Biochem. Biophys. Res. Commun. 195:1993;1035-1040.
60. Van Essen D.C., Newsome W.T., Maunsell J.H. The visual field representation in striate cortex of the macaque monkey: asymmetries, anisotropies, and individual variability. Vision Res. 24:1984;429-448.
61. Vassar R., Ngai J., Axel R. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell. 74:1993;309-318.
62. Vassar R., Chao S.K., Sitcheran R., Nuñez J.M., Vosshall L.B., Axel R. Topographic organization of sensory projections to the olfactory bulb. Cell. 79:1994;981-991.
63. Verma A., Hirsch D.J., Glatt C.E., Ronnett G.V., Snyder S.H. Carbon monoxide: a putative neural messenger. Science. 259:1993;381-384.
64. Voigt J.M., Guengerich F.P., Baron J. Localization of a cytochrome P-450 isozyme (cytochrome P-450 PB-B) and NADPH-cytochrome P-450 reductase in rat nasal mucosa. Cancer Lett. 27:1985;241-247.
65. Wang F., Nemes A., Mendelsohn M., Axel R. Odorant receptors govern the formation of a precise topographic map. Cell. 93:1998;47-60.
66. Wenisch S., Andressen C., Derouiche A., Arnhold S., Addicks K., Leiser R. Heme oxygenase-2 and nitric oxide synthase immunoreactivity of bovine olfactory receptor neurons and a comparison with the distribution of NADPH-diaphorase staining. Histochem. J. 32:2000;381-388.
67. Xu F., Greer C.A., Shepherd G.M. Odor maps in the olfactory bulb. J. Comp. Neurol. 422:2000;489-495.
68. Yoshihara Y., Kawasaki M., Tamada A., Fujita H., Hayashi H., Kagamiyama H., Mori K. OCAM: a new member of the neural cell adhesion molecule family related to zone-to-zone projection of olfactory and vomeronasal axons. J. Neurosci. 17:1997;5830-5842.
69. Zhao H., Firestein S., Greer C.A. NADPH-diaphorase localization in the olfactory system. NeuroReport. 6:1994;149-152.