The localization of neuronal nitric oxide synthase may influence its role in neuronal precursor proliferation and synaptic maintenance

Developmental Biology

Volumn 269, Issue 1, 2004, Pages 165-182

  Chen, Jijun ^a   Tu, Yajun ^a   Moon, Cheil ^a   Matarazzo, Valéry ^a   Palmer, Amy M ^a   Ronnett, Gabriele V ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

BrdU; Development; Neurogenesis; Neuron specific tubulin type III; Neuronal nitric oxide synthase; Nitric oxide; Nitric oxide synthase; NO; NOS; NST; Olfactory glomerulus; Olfactory marker protein; Olfactory neurons; Olfactory receptor neuron; OMP; ORN; Synapse

Indexed keywords

CYCLIC GMP; NEURONAL NITRIC OXIDE SYNTHASE;

ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; ENZYME LOCALIZATION; GENE DELETION; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; OLFACTORY BULB; OLFACTORY EPITHELIUM; OLFACTORY SYSTEM; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; STEM CELL; SYNAPSE;

GLOMERULUS;

EID: 1842665660     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2004.01.024     Document Type: Article

References (113)

1. Alderton W.K., Cooper C.E., Knowles R.G. Nitric oxide synthases: structure, function and inhibition. Biochem. J. 357:2001;593-615.
2. Arancio O., Kiebler M., Lee C.J., Lev-Ram V., Tsien R.Y., Kandel E.R., Hawkins R.D. Nitric oxide acts directly in the presynaptic neuron to produce long- term potentiation in cultured hippocampal neurons. Cell. 87:1996;1025-1035.
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. Baker H., Kawano T., Margolis F.L., Joh T.H. Transneuronal regulation of tyrosine hydroxylase expression in olfactory bulb of mouse and rat. J. Neurosci. 3:1983;69-78.
5. Baker H.M.K., Stone D.M., Maruniak J.A. Adult naris closure profoundly reduced tyrosine hydroxylase expression in mouse olfactory bulb. Brain Res. 614:1993;109-116.
6. Baranano D.E., Ferris C.D., Snyder S.H. Atypical neural messengers. Trends Neurosci. 24:2001;99-106.
7. Beckman J.S., Beckman T.W., Chen J., Marshall P.A., Freeman B.A. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. U. S. A. 87:1990;1620-1624.
8. Benowitz L.I., Routtenberg A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 20:1997;84-91.
9. Bergmann M., Schuster T., Grabs D., Marqueze-Pouey B., Betz H., Traurig H., Mayerhofer A., Gratzl M. Synaptophysin and synaptoporin expression in the developing rat olfactory system. Brain Res. Dev. Brain Res. 74:1993;235-244.
10. Borras D., Pumarola M., Ferrer I. Neuronal nuclear DNA fragmentation in the aged canine brain: apoptosis or nuclear DNA fragility? Acta Neuropathol. (Berl.). 99:2000;402-408.
11. Bredt D.S., Snyder S.H. Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc. Natl. Acad. Sci. U. S. A. 86:1989;9030-9033.
12. Bredt D.S., Snyder S.H. Transient nitric oxide synthase neurons in embryonic cerebral cortical plate, sensory ganglia, and olfactory epithelium. Neuron. 13:1994;301-313.
13. Bredt D.S., Hwang P.M., Snyder S.H. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature. 347:1990;768-770.
14. Bredt D.S., Glatt C.E., Hwang P.M., Fotuhi M., Dawson T.M., Snyder S.H. Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron. 7:1991;615-624.
15. Brenman J.E., Bredt D.S. Synaptic signaling by nitric oxide. Curr. Opin. Neurobiol. 7:1997;374-378.
16. Broillet M.C., Firestein S. Direct activation of the olfactory cyclic nucleotide-gated channel through modification of sulfhydryl groups by NO compounds. Neuron. 16:1996;377-385.
17. Broillet M.C., Firestein S. Gaseous second messengers in vertebrate olfaction. J. Neurobiol. 30:1996;49-57.
18. Calof A.L., Chikaraishi D.M. Analysis of neurogenesis in a mammalian neuroepithelium: proliferation and differentiation of an olfactory neuron precursor in vitro. Neuron. 3:1989;115-127.
19. Calof A.L., Hagiwara N., Holcomb J.D., Mumm J.S., Shou J. Neurogenesis and cell death in olfactory epithelium. J. Neurobiol. 30:1996;67-81.
20. Calof A.L., Holcomb J.D., Mumm J.S., Haglwara N., Tran P., Smith K.M., Shelton D. Factors affecting neuronal birth and death in the mammalian olfactory epithelium. Ciba Found. Symp. 196:1996;188-205. (discussion 205-10).
21. Calof A.L., Rim P.C., Askins K.J., Mumm J.S., Gordon M.K., Iannuzzelli P., Shou J. Factors regulating neurogenesis and programmed cell death in mouse olfactory epithelium. Ann. N.Y. Acad. Sci. 855:1998;226-229.
22. Chen J., Tu Y., Moon C., Nagata E., Ronnett G.V. Heme oxygenase-1 and heme oxygenase-2 have distinct roles in the proliferation and survival of olfactory receptor neurons mediated by cGMP and bilirubin, respectively. J. Neurochem. 85:2003;1247-1261.
23. Cheng A., Wang S., Cai J., Rao M.S., Mattson M.P. Nitric oxide acts in a positive feedback loop with BDNF to regulate neural progenitor cell proliferation and differentiation in the mammalian brain. Dev. Biol. 258:2003;319-333.
24. Cho J.Y., Min N., Franzen L., Baker H. Rapid down-regulation of tyrosine hydroxylase expression in the olfactory bulb of naris-occluded adult rats. J. Comp. Neurol. 369:1996;264-276.
25. Contestabile A. Roles of NMDA receptor activity and nitric oxide production in brain development. Brain Res. Brain Res. Rev. 32:2000;476-509.
26. Cramer K.S., Angelucci A., Hahm J.O., Bogdanov M.B., Sur M. A role for nitric oxide in the development of the ferret retinogeniculate projection. J. Neurosci. 16:1996;7995-8004.
27. Crespo C., Gracia-Llanes F.J., Blasco-Ibanez J.M., Gutierrez-Mecinas M., Marques-Mari A.I., Martinez-Guijarro F.J. Nitric oxide synthase containing periglomerular cells are GABAergic in the rat olfactory bulb. Neurosci. Lett. 349:2003;151-154.
28. Davis J.A., Reed R.R. Role of Olf-1 and Pax-6 transcription factors in neurodevelopment. J. Neurosci. 16:1996;5082-5094.
29. Dawson V.L., Dawson T.M. Nitric oxide in neurodegeneration. Prog. Brain Res. 118:1998;215-229.
30. de Vente J., Bol J.G., Steinbusch H.W. Localization of cGMP in the cerebellum of the adult rat: an immunohistochemical study. Brain Res. 504:1989;332-337.
31. De Vente J., Hopkins D.A., Markerink-Van Ittersum M., Emson P.C., Schmidt H.H., Steinbusch H.W. Distribution of nitric oxide synthase and nitric oxide-receptive, cyclic GMP-producing structures in the rat brain. Neuroscience. 87:1998;207-241.
32. 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. U. S. A. 91:1994;4214-4218.
33. Farbman A.I. Olfactory neurogenesis: genetic or environmental controls? Trends Neurosci. 13:1990;362-365.
34. Farbman A.I., Margolis F.L. Olfactory marker protein during ontogeny: immunohistochemical localization. Develop. Biol. 74:1980;205-215.
35. G-methylarginine requires NADPH-dependent hydroxylation. J. Med. Chem. 36(4):1993;491-496.
36. Firestein B.L., Bredt D.S. Regulation of sensory neuron precursor proliferation by cyclic GMP-dependent protein kinase. J. Neurochem. 71:1998;1846-1853.
37. Gibbs S.M. Regulation of neuronal proliferation and differentiation by nitric oxide. Mol. Neurobiol. 27:2003;107-120.
38. Gibbs S.M., Truman J.W. Nitric oxide and cyclic GMP regulate retinal patterning in the optic lobe of Drosophila. Neuron. 20:1998;83-93.
39. Gibson N.J., Rossler W., Nighorn A.J., Oland L.A., Hildebrand J.G., Tolbert L.P. Neuron-glia communication via nitric oxide is essential in establishing antennal-lobe structure in Manduca sexta. Dev. Biol. 240:2001;326-339.
40. Goheen B.L., Kott J.N., Westrum L.E. Tyrosine hydroxylase expression in rat olfactory bulb transplant: an electron microscope study. Synapse. 23:1996;132-141.
41. Graziadei P.P.C., Monti-Graziadei M. The olfactory system: a model for the study of neurogenesis and axon regeneration in mammals. Cotmm C.W. Neuronal Plasticity. 1978;131-153 Raven, New York.
42. Gudi T., Hong G.K., Vaandrager A.B., Lohmann S.M., Pilz R.B. Nitric oxide and cGMP regulate gene expression in neuronal and glial cells by activating type II cGMP-dependent protein kinase. FASEB J. 13:1999;2143-2152.
43. Hawkins R.D., Zhuo M., Arancio O. Nitric oxide and carbon monoxide as possible retrograde messengers in hippocampal long-term potentiation. J. Neurobiol. 25:1994;652-665.
44. Hess D.T., Patterson S.I., Smith D.S., Skene J.H. Neuronal growth cone collapse and inhibition of protein fatty acylation by nitric oxide. Nature. 366:1993;562-565.
45. Hindley S., Juurlink B.H., Gysbers J.W., Middlemiss P.J., Herman M.A., Rathbone M.P. Nitric oxide donors enhance neurotrophin-induced neurite outgrowth through a cGMP-dependent mechanism. J. Neurosci. Res. 47:1997;427-439.
46. Holscher C. Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity. Trends Neurosci. 20:1997;298-303.
47. Huard J.M., Schwob J.E. Cell cycle of globose basal cells in rat olfactory epithelium. Dev. Dyn. 203:1995;17-26.
48. Jastreboff P.J., Pedersen P.E., Greer C.A., Stewart W.B., Kauer J.S., Benson T.E., Shepherd G.M. Specific olfactory receptor populations projecting to identified glomeruli in the rat olfactory bulb. Proc. Natl. Acad. Sci. U. S. A. 81:1984;5250-5254.
49. Johnson B.A., Woo C.C., Ninomiya-Tsuboi K., Leon M. Synaptophysin-like immunoreactivity in the rat olfactory bulb during postnatal development and after restricted early olfactory. Dev. Brain Res. 91:1996;24-30.
50. Kafitz K.W., Leinders-Zufall T., Zufall F., Greer C.A. Cyclic GMP evoked calcium transients in olfactory receptor cell growth cones. NeuroReport. 11:2000;677-681.
51. Kalb R.G., Agostini J. Molecular evidence for nitric oxide-mediated motor neuron development. Neuroscience. 57:1993;1-8.
52. Kasowski H.J., Kim H., Greer C.A. Compartmental organization of the olfactory bulb glomerulus. J. Comp. Neurol. 407:1999;261-274.
53. Kawano T.M.F. Tranassynaptic regulation of olfactory bulb catecholamines in mice and rats. J. Neurochem. 39:1982;342-348.
54. 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.
55. Koppenol W.H., Moreno J.J., Pryor W.A., Ischiropoulos H., Beckman J.S. Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide. Chem. Res. Toxicol. 5:1992;834-842.
56. Kosaka K., Toida K., Aika Y., Kosaka T. How simple is the organization of the olfactory glomerulus?: the heterogeneity of so-called periglomerular cells. Neurosci. Res. 30:1998;101-110.
57. Kream R.M., Margolis F.L. Olfactory marker protein: turnover and transport in normal and regenerating neurons. J. Neurosci. 4:1984;868-879.
58. Kuzin B., Roberts I., Peunova N., Enikolopov G. Nitric oxide regulates cell proliferation during Drosophila development. Cell. 87:1996;639-649.
59. Lee V.M., Pixley S.K. Age and differentiation-related differences in neuron-specific tubulin immunostaining of olfactory sensory neurons. Brain Res. Dev. Brain Res. 83:1994;209-215.
60. Lee M.K., Tuttle J.B., Rebhun L.I., Cleveland D.W., Frankfurter A. The expression and posttranslational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell Motil. Cytoskelet. 17:1990;118-132.
61. Leo J.M., Devine A.H., Brunjes P.C. Focal denervation alters cellular phenotypes and survival in the developing rat olfactory bulb. J. Comp. Neurol. 417:2000;325-336.
62. Lev-Ram V., Jiang T., Wood J., Lawrence D.S., Tsien R.Y. Synergies and coincidence requirements between NO, cGMP, and Ca2+ in the induction of cerebellar long-term depression. Neuron. 18:1997;1025-1038.
63. Linden D.J., Dawson T.M., Dawson V.L. An evaluation of the nitric oxide/cGMP/cGMP-dependent protein kinase cascade in the induction of cerebellar long-term depression in culture. J. Neurosci. 15:1995;5098-5105.
64. Liu P.K., Robertson C.S., Valadka A. The association between neuronal nitric oxide synthase and neuronal sensitivity in the brain after brain injury. Ann. N.Y. Acad. Sci. 962:2002;226-241.
65. Lu D., Mahmood A., Zhang R., Copp M. Upregulation of neurogenesis and reduction in functional deficits following administration of DEtA/NONOate, a nitric oxide donor, after traumatic brain injury in rats. J. Neurosurg. 99:2003;351-361.
66. Mackay-Sim A., Chuah M.I. Neurotrophic factors in the primary olfactory pathway. Prog. Neurobiol. 62:2000;527-559.
67. Margolis F.L. A marker protein for the olfactory chemoreceptor neuron. Bradshaw R.A., Schneider D.M. Proteins of the Nervous System. second ed. 1980;59-84 Raven, New York.
68. Margolis F.L., Verhaagen J., Biffo S., Huang F.L., Grillo M. Regulation of gene expression in the olfactory neuroepithelium: a neurogenetic matrix. Prog. Brain Res. 89:1991;97-122.
69. Markerink-Van Ittersum M., Steinbusch H.W., De Vente J. Region-specific developmental patterns of atrial natriuretic factor- and nitric oxide-activated guanylyl cyclases in the postnatal frontal rat brain. Neuroscience. 78:1997;571-587.
70. Mize R.R., Lo F. Nitric oxide, impulse activity, and neurotrophins in visual system development(1). Brain Res. 886:2000;15-32.
71. Moon C., Jaberi P., Otto-Bruc A., Baehr W., Palczewski K., Ronnett G. Calcium-sensitive particulate guanylyl cyclase as a modulator of cAMP in olfactory neurons. J. Neurosci. 18:1998;3195-3205.
72. Mori K., Nagao H., Yoshihara Y. The olfactory bulb: coding and processing of odor molecule information. Science. 286:1999;711-715.
73. Morys J., Berdel B., Kowianski P., Dziewiatkowski J. The pattern of synaptophysin changes during the maturation of the amygdaloid body and hippocampal hilus in the rat. Folia Neuropathol. 36:1998;15-23.
74. Murphy G.J., Isaacson J.S. Presynaptic cyclic nucleotide-gated ion channels modulate neurotransmission in the mammalian olfactory bulb. Neuron. 37:2003;639-647.
75. Nadi N.S., Head R., Grillo M., Hempstead J., Granno-Reisfeid N., Margolis F.L. Chemical deafferentation of the olfactory bulb, plasticity of the levels of tyrosine hydroxylase, dopamine and norepinephrine. Brain Res. 213:1981;365-377.
76. O'Dell T.J., Huang P.L., Dawson T.M., Dinerman J.L., Snyder S.H., Kandel E.R., Fishman M.C. Blockade of long-term potentiation by inhibitors of nitric oxide synthase in mice lacking the neuronal isoform suggests a role for the endothelial isoform. Science. 1994.
77. Ogilvie P., Schilling K., Billingsley M.L., Schmidt H.H. Induction and variants of neuronal nitric oxide synthase type I during synaptogenesis. FASEB J. 9:1995;799-806.
78. Ovtscharoff W., Bergmann M., Marqueze-Pouey B., Knaus P., Betz H., Grabs D., Reisert I., Gratzl M. Ontogeny of synaptophysin and synaptoporin in the central nervous system: differential expression in striatal neurons and their afferents during development. Brain Res. Dev. Brain Res. 72:1993;219-225.
79. Paakkari I., Lindsberg P. Nitric oxide in the central nervous system. Ann. Med. 27:1995;369-377.
80. Packer M.A., Stasiv Y., Benraiss A., Chmielnicki E., Grinberg A., Westphal H., Goldman S.A., Enikolopov G. Nitric oxide negatively regulates mammalian adult neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 100:2003;9566-9571.
81. Park C., Kang M., Kwon Y.K., Chung J.H., Ahn H., Huh Y. Inhibition of neuronal nitric oxide synthase enhances cell proliferation in the dentate gyrus of the adrenalectomized rat. Neurosci. Lett. 309:2001;9-12.
82. Peunova N., Enikolopovc G. Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature. 375:1995;68-73.
83. Peunova N., Scheinker V., Cline H., Enikolopov G. Nitric oxide is an essential negative regulator of cell proliferation in Xenopus brain. J. Neurosci. 21:2001;8809-8818.
84. Philpot B.D., Lim J.H., Brunjes P.C. Activity-dependent regulation of calcium-binding proteins in the developing rat olfactory bulb. J. Comp. Neurol. 387:1997;12-26.
85. Phung Y.T., Bekker J.M., Hallmark O.G., Black S.M. Both neuronal NO synthase and nitric oxide are required for PC12 cell differentiation: a cGMP independent pathway. Brain Res. Mol. Brain Res. 64:1999;165-178.
86. Pinching A.J., Powell T.P. The neuron types of the glomerular layer of the olfactory bulb. J. Cell. Sci. 9:1971;305-345.
87. Pineda J., Kogan J.H., Aghajanian G.K. Nitric oxide and carbon monoxide activate locus coeruleus neurons through a cGMP-dependent protein kinase: involvement of a nonselective cationic channel. J. Neurosci. 16:1996;1389-1399.
88. Poluha W., Schonhoff C.M., Harrington K.S., Lachyankar M.B., Crosbie N.E., Bulseco D.A., Ross A.H. A novel, nerve growth factor-activated pathway involving nitric oxide, p53, and p21WAF1 regulates neuronal differentiation of PC12 cells. J. Biol. Chem. 272:1997;24002-24007.
89. Radi R., Beckman J.S., Bush K.M., Freeman B.A. Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch. Biochem. Biophys. 288:1991;481-487.
90. Renteria R.C., Constantine-Paton M. Exogenous nitric oxide causes collapse of retinal ganglion cell axonal growth cones in vitro. J. Neurobiol. 29:1996;415-428.
91. Rialas C.M., Nomizu M., Patterson M., Kleinman H.K., Weston C.A., Weeks B.S. Nitric oxide mediates laminin-induced neurite outgrowth in PC12 cells. Exp. Cell Res. 260:2000;268-276.
92. 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.
93. Roskams A.J., Cai X., Ronnett G.V. Expression of neuron-specific beta-III tubulin during olfactory neurogenesis in the embryonic and adult rat. Neuroscience. 83:1998;191-200.
94. Samama B., Boehm N. Ontogeness of NADPH-diaphorase activity in the olfactory bulb of the rat. Brain Res. Dev. Brain Res. 96:1996;192-203.
95. Satoh M., Yoshida T. Promotion of neurogenesis in mouse olfactory neuronal progenitor cells by leukemia inhibitory factor in vitro. Neurosci. Lett. 225:1997;165-168.
96. Shepherd G.M. Synaptic organization of the mammalian olfactory bulb. Physiol. Rev. 52:1972;864-917.
97. Shepherd G., Greer C. The olfactory bulb. Shepherd G. The Synaptic Organization of the Brain. 1990;133-169 Oxford Univ. Press, New York.
98. Simpson P.J., Miller I.L., Moon C., Hanlon A.L., Liebl D.J., Ronnett G.V. Atrial natriuretic peptide type C (CNP) induces a cell cycle switch from proliferation to differentiation in BDNF- or NGF-primed olfactory receptor neurons. J. Neurosci. 22:2002;5536-5551.
99. Simpson P.J., Wang E., Moon C., Matarazzo V., Cohen D.R., Liebl D.J., Ronnett G. Neurotrophin-3 signaling maintains maturatonal homestasis between neuronal populations in the olfactory epithelium. Mol. Cell. Neurosci. 24:2003;858-874.
100. Smith R.L., Baker H., Kolstad K., Spencer D.D., Greer C.A. Localization of tyrosine hydroxylase and olfactory marker protein immunoreactivities in the human and macaque olfactory bulb. Brain Res. 548:1991;140-148.
101. Stamler J.S. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell. 78:1994;931-936.
102. 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. U. S. A. 96:1999;14106-14111.
103. Truman J.W., De Vente J., Ball E.E. Nitric oxide-sensitive guanylate cyclase activity is associated with the maturational phase of neuronal development in insects. Development. 122:1996;3949-3958.
104. Van Wagenen S., Rehder V. Regulation of neuronal growth cone filopodia by nitric oxide. J. Neurobiol. 39:1999;168-185.
105. Van Wagenen S., Rehder V. Regulation of neuronal growth cone filopodia by nitric oxide depends on soluble guanylyl cyclase. J. Neurobiol. 46:2001;206-219.
106. Verhaagen J., Oestreicher A.B., Gispen W.H., Margolis F.L. The expression of the growth associated protein B50/GAP43 in the olfactory system of neonatal and adult rats. J. Neurosci. 9:1989;683-691.
107. Verhaagen J., Greer C., Margolis F.L. B-50/GAP43 gene expression in the rat olfactory system during postnatal development and aging. Eur. J. Neurosci. 2:1990;397-407.
108. Verhaagen J., Oestreicher A.B., Grillo M., Khew-Goodall Y., Gispen W.H., Margolis F.L. Neuroplasticity in the olfactory system: differential effects of central and peripheral lesions of the primary olfactory pathway on the expression of B-50/GAP43 and the olfactory marker protein. J. Neurosci. Res. 26:1990;31-44.
109. Wang S.S., Tsai R.Y.L., Reed R.R. The characterization of the Olf-1/EBF-like HLH transcription factor family: implications in olfactory gene regulation and neuronal development. J. Neurosci. 17:1997;4149-4158.
110. Weruaga E., Brinon J.G., Porteros A., Arevalo R., Aijon J., Alonso J.R. Expression of neuronal nitric oxide synthase/NADPH-diaphorase during olfactory deafferentation and regeneration. Eur. J. Neurosci. 12:2000;1177-1193.
111. Williams J.H., Li Y.-G., Navak A., Errington M.L., Murphy K.P.S.J., Bliss T.V.P. The suppression of long-term potentiation in rat hippocampus by inhibitors of nitric oxide synthase is temperature and age dependent. Neuron. 11:1993;877-884.
112. Wu H.H., Williams C.V., McLoon S.C. Involvement of nitric oxide in the elimination of a transient retinotectal projection in development. Science. 265:1994;1593-1596.
113. Zhang R., Zhang L., Zhang Z., Wang Y., Lu M., Lapointe M., Chopp M. A nitric oxide donor induces neurogenesis and reduces functional deficits after stroke in rats. Ann. Neurol. 50:2001;602-611.