Role of nitric oxide during neurogenesis in the olfactory epithelium

Biological Research

Volumn 39, Issue 4, 2006, Pages 589-599

  Sulz, Lorena ^a   Bacigalupo, Juan ^a  

^a UNIVERSITY OF CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE;

CELL PROLIFERATION; DENTATE GYRUS; HUMAN; IN VITRO STUDY; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY EPITHELIUM; REGULATORY MECHANISM; REVIEW; SECOND MESSENGER; SIGNAL TRANSDUCTION; STEM CELL; SUBVENTRICULAR ZONE;

MAMMALIA;

EID: 34547527239     PISSN: 07169760     EISSN: 07176287     Source Type: Journal    
DOI: 10.4067/S0716-97602006000500002     Document Type: Review

References (129)

1. ALTMAN J, DAS GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124: 319-335
2. ASTIC L, SAUCIER D (2001) Neuronal plasticity and regeneration in the olfactory system of mammals: morphological and functional recovery following olfactory bulb deafferentation. Cell Mol Life Sci 58: 538-545
3. BACIGALUPO J, JOHNSON EC, VERGARA C, LISMAN JE (1991) Light-dependent channels from excised patches of Limulus ventral photoreceptors are opened by cGMP. Proc Natl Acad Sci U S A 88: 7938-7942
4. BAKALYAR HA, REED RR (1990) Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science 250: 1403-1406
5. BARBER RD, JAWORSKY DE, YAU KW, RONNETT GV (2000) Isolation and in vitro differentiation of conditionally immortalized murine olfactory receptor neurons. J Neurosci 20: 3695-3704
6. BAUER S, RASIKA S, HAN J, MAUDUIT C, RACCURT M, MOREL G, JOURDAN F, BENAHMED M, MOYSE E, PATTERSON P (2003) Leukemia inhibitory factor is a key signal for injury-induced neurogenesis in the adult mouse olfactory epithelium. J Neurosci 23: 1792-1803
7. BORDERS AS, GETCHELL ML, ETSCHEIDT J, COHEN DA, GETCHELL TV (2006) Macrophage depletion in murine olfactory epithelium leads to decrease neurogenesis. In Association for Chemoreception Sciences, pp. 115, Sarasota, FL, USA
8. BOSS BD, PETERSON GM, COWAN WM (1985) On the number of neurons in the dentate gyrus of the rat. Brain Res 338: 144-150
9. BRANDT I, BRITTEBO EB, FEIL VJ, BAKKE JE (1990) Irreversible binding and toxicity of the herbicide dichlobenil (2,6-dichlorobenzonitrile) in the olfactory mucosa of mice. Toxicol Appl Pharmacol 103: 491-501
10. BREDT DS, SNYDER SH (1994) Transient nitric oxide synthase neurons in embryonic cerebral cortical plate, sensory ganglia, and olfactory epithelium. Neuron 13: 301-313
11. BUCK L, AXEL R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65: 175-187
12. BUCKLAND ME, CUNNINGHAM AM (1998) Alterations in the neurotrophic factors BDNF, GDNF and CNTF in the regenerating olfactory system. Ann N Y Acad Sci 855: 260-265
13. CAGGIANO M, KAUER JS, HUNTER DD (1994) Globose basal cells are neuronal progenitors in the olfactory epithelium: a lineage analysis using a replication-incompetent retrovirus. Neuron 13: 339-352
14. CALOF AL, CHIKARAISHI DM (1989) Analysis of neurogenesis in a mammalian neuroepithelium: proliferation and differentiation of an olfactory neuron precursor in vitro. Neuron 3: 115-127
15. CAMARA CG, HARDING JW (1984) Thymidine incorporation in the olfactory epithelium of mice: early exponential response induced by olfactory neurectomy. Brain Res 308: 63-68
16. CAMERON HA, MCKAY R (1998) Stem cells and neurogenesis in the adult brain. Curr Opin Neurobiol 8: 677-680
17. CANCALON P (1982) Degeneration and regeneration of olfactory cells induced by ZnS04 and other chemicals. Tissue Cell 14: 717-733
18. CARR VM, FARBMAN AI (1992) Ablation of the olfactory bulb up-regulates the rate of neurogenesis and induces precocious cell death in olfactory epithelium. Exp Neurol 115: 55-59
19. CARTER LA, MACDONALD JL, ROSKAMS AJ (2004) Olfactory horizontal basal cells demonstrate a conserved multipotent progenitor phenotype. J Neurosci 24: 5670-5683
20. CHEN J, LI Y, ZHANG R, KATAKOWSKI M, GAUTAM SC, XU Y, LU M, ZHANG Z, CHOPP M (2004a) Combination therapy of stroke in rats with a nitric oxide donor and human bone marrow stromal cells enhances angiogenesis and neurogenesis. Brain Res 1005: 21-28
21. CHEN J, TU Y, MOON C, MATARAZZO V, PALMER AM, RONNETT GV (2004b) The localization of neuronal nitric oxide synthase may influence its role in neuronal precursor proliferation and synaptic maintenance. Dev Biol 269: 165-182
22. CHEN J, ZHANG ZG, LI Y, WANG Y, WANG L, JIANG H, ZHANG C, LU M, KATAKOWSKI M, FELDKAMP CS, CHOPP M (2003) Statins induce angiogenesis, neurogenesis, and synaptogenesis after stroke. Ann Neurol 53: 743-751
23. CUNNINGHAM AM, MANIS PB, REED RR, RONNETT GV (1999) Olfactory receptor neurons exist as distinct subclasses of immature and mature cells in primary culture. Neuroscience 93: 1301-1312
24. DAWSON TM, BREDT DS, FOTUHI M, HWANG PM, SNYDER SH (1991) Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc Natl Acad Sci U S A 88: 7797-7801
25. DAWSON TM, DAWSON VL, SNYDER SH (1993) Nitric oxide as a mediator of neurotoxicity. NIDA Res Monogr 136: 258-271; discussion 271-253
26. DAWSON TM, DAWSON VL, SNYDER SH (1994) Molecular mechanisms of nitric oxide actions in the brain. Ann N Y Acad Sci 738: 76-85
27. DELALEU JC, SICARD G (1995) Physiological and histological recovery of the olfactory mucosa of the frog after a dichlobenil injection. Chem Senses 20: 433-440
28. EDELMAN GM, GALLY JA (1992) Nitric oxide: linking space and time in the brain. Proc Natl Acad Sci U S A 89: 11651-11652
29. ERIKSSON PS, PERFILIEVA E, BJORK-ERIKSSON T, ALBORN AM, NORDBORG C, PETERSON DA, GAGE FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4: 1313-1317
30. FARBMAN AI (1990) Olfactory neurogenesis: genetic or environmental controls? Trends Neurosci 13: 362-365
31. FARBMAN AI, BUCHHOLZ JA (1996) Transforming growth factor-alpha and other growth factors stimulate cell division in olfactory epithelium in vitro. J Neurobiol 30: 267-280
32. FERON F, MACKAY-SIM A, ANDRIEU JL, MATTHAEI KI, HOLLEY A, SICARD G (1999a) Stress induces neurogenesis in non-neuronal cell cultures of adult olfactory epithelium. Neuroscience 88: 571-583
33. FERON F, VINCENT A, MACKAY-SIM A (1999b) Dopamine promotes differentiation of olfactory neuron in vitro. Brain Res 845: 252-259
34. FIRESTEIN BL, BREDT DS (1998) Regulation of sensory neuron precursor proliferation by cyclic GMP-dependent protein kinase. J Neurochem 71: 1846-1853
35. FIRESTEIN S, ZUFALL F, SHEPHERD GM (1991) Single odor-sensitive channels in olfactory receptor neurons are also gated by cyclic nucleotides. J Neurosci 11: 3565-3572
36. GAGE FH (2000) Mammalian neural stem cells. Science 287: 1433-1438
37. GARTHWAITE J (1991) Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci 14: 60-67
38. GARTHWAITE J, BOULTON CL (1995) Nitric oxide signaling in the central nervous system. Annu Rev Physiol 57: 683-706
39. GENTER MB, DEAMER NJ, CAO Y, LEVI PE (1994) Effects of P450 inhibition and induction on the olfactory toxicity of beta,beta'-iminodipropionitrile (IDPN) in the rat. J Biochem Toxicol 9: 31-39
40. GETCHELL TV, SHAH DS, PARTIN JV, SUBHEDAR NK, GETCHELL ML (2002) Leukemia inhibitory factor mRNA expression is upregulated in macrophages and olfactory receptor neurons after target ablation. J Neurosci Res 67: 246-254
41. GIUILI G, LUZI A, POYARD M, GUELLAEN G (1994) Expression of mouse brain soluble guanylyl cyclase and NO synthase during ontogeny. Brain Res Dev Brain Res 81: 269-283
42. GORDON MK, MUMM JS, DAVIS RA, HOLCOMB JD, CALOF AL (1995) Dynamics of MASH1 expression in vitro and in vivo suggest a non-stem cell site of MASH1 action in the olfactory receptor neuron lineage. Mol Cell Neurosci 6: 363-379
43. GOULD E, MCEWEN BS, TANAPAT P, GALEA LA, FUCHS E (1997) Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 17: 2492-2498
44. GOULD E, TANAPAT P (1999) Stress and hippocampal neurogenesis. Biol Psychiatry 46: 1472-1479
45. GOULDING EH, NGAI J, KRAMER RH, COLICOS S, AXEL R, SIEGELBAUM SA, CHESS A (1992) Molecular cloning and single-channel properties of the cyclic nucleotide-gated channel from catfish olfactory neurons. Neuron 8: 45-58
46. GRAZIADEI PP (1973) Cell dynamics in the olfactory mucosa. Tissue Cell 5: 113-131
47. GRAZIADEI PP, MONTI GRAZIADEI AG (1983) Regeneration in the olfactory system of vertebrates. Am J Otolaryngol 4: 228-233
48. GRAZIADEI PP, 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
49. GRAZIADEI PP, MONTI GRAZIADEI GA (1980) Neurogenesis and neuron regeneration in the olfactory system of mammals. III. Deafferentation and reinnervation of the olfactory bulb following section of the fila olfactoria in rat. J Neurocytol 9: 145-162
50. GUDI T, HONG GK, VAANDRAGER AB, LOHMANN SM, PILZ RB (1999) Nitric oxide and cGMP regulate gene expression in neuronal and glial cells by activating type II cGMP-dependent protein kinase. Faseb J 13: 2143-2152
51. HARDING J, GRAZIADEI PP, MONTI GRAZIADEI GA, MARGOLIS FL (1977) Denervation in the primary olfactory pathway of mice. IV. Biochemical and morphological evidence for neuronal replacement following nerve section. Brain Res 132: 11-28
52. HAYNES LW, KAY AR, YAU KW (1986) Single cyclic GMP-activated channel activity in excised patches of rod outer segment membrane. Nature 321: 66-70
53. HEMPSTEAD JL, MORGAN JI (1983) Monoclonal antibodies to the rat olfactory sustentacular cell. Brain Res 288: 289-295
54. HESS SD, DOROSHENKO PA, AUGUSTINE GJ (1993) A functional role for GTP-binding proteins in synaptic vesicle cycling. Science 259: 1169-1172
55. HINDS JW, HINDS PL, MCNELLY NA (1984) An autoradiographic study of the mouse olfactory epithelium: evidence for long-lived receptors. Anat Rec 210: 375-383
56. HOLBROOK EH, SZUMOWSKI KE, SCHWOB JE (1995) An immunochemical, ultrastructural, and developmental characterization of the horizontal basal cells of rat olfactory epithelium. J Comp Neurol 363: 129-146
57. HOLMQVIST B, ELLINGSEN B, FORSELL J, ZHDANOVA I, ALM P (2004) The early ontogeny of neuronal nitric oxide synthase systems in the zebrafish. J Exp Biol 207: 923-935
58. HURTT ME, THOMAS DA, WORKING PK, MONTICELLO TM, MORGAN KT (1988) Degeneration and regeneration of the olfactory epithelium following inhalation exposure to methyl bromide: pathology, cell kinetics, and olfactory function. Toxicol Appl Pharmacol 94: 311-328
59. ILLING N, BOOLAY S, SIWOSKI JS, CASPER D, LUCERO MT, ROSKAMS AJ (2002) Conditionally immortalized clonal cell lines from the mouse olfactory placode differentiate into olfactory receptor neurons. Mol Cell Neurosci 20: 225-243
60. JONES DT, REED RR (1989) Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science 244: 790-795
61. KEILHOFF G, SEIDEL B, NOACK H, TISCHMEYER W, STANEK D, WOLF G (1996) Patterns of nitric oxide synthase at the messenger RNA and protein levels during early rat brain development. Neuroscience 75: 1193-1201
62. KEYNES RG, GARTHWAITE J (2004) Nitric oxide and its role in ischaemic brain injury. Curr Mol Med 4: 179-191
63. KIM EJ, SIMPSON PJ, PARK DJ, LIU BQ, RONNETT GV, MOON C (2005) Leukemia inhibitory factor is a proliferative factor for olfactory sensory neurons. Neuroreport 16: 25-28
64. KLEINERT H, SCHWARZ PM, FORSTERMANN U (2003) Regulation of the expression of inducible nitric oxide synthase. Biol Chem 384: 1343-1364
65. KUHN HG, WINKLER J, KEMPERMANN G, THAL LJ, GAGE FH (1997) Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci 17: 5820-5829
66. KUZIN B, REGULSKI M, STASIV Y, SCHEINKER V, TULLY T, ENIKOLOPOV G (2000) Nitric oxide interacts with the retinoblastoma pathway to control eye development in Drosophila. Curr Biol 10: 459-462
67. KUZIN B, ROBERTS I, PEUNOVA N, ENIKOLOPOV G (1996) Nitric oxide regulates cell proliferation during Drosophila development. Cell 87: 639-649
68. LEUNG CT, REED RR (2006) Horizontal basal cells are multipotent neuronal progenitos in olfactory epithelium. In Association for Chemoreception Sciences, pp. 115, Sarasota, FL, USA
69. LU D, MAHMOOD A, ZHANG R, COPP M (2003) 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: 351-361
70. MACKAY-SIM A, KITTEL P (1991) Cell dynamics in the adult mouse olfactory epithelium: a quantitative autoradiographic study. J Neurosci 11: 979-984
71. MAHALIK TJ (1996) Apparent apoptotic cell death in the olfactory epithelium of adult rodents: death occurs at different developmental stages. J Comp Neurol 372: 457-464
72. MAHANTHAPPA NK, SCHWARTING GA (1993) Peptide growth factor control of olfactory neurogenesis and neuron survival in vitro: roles of EGF and TGF-beta s. Neuron 10: 293-305
73. MATARREDONA ER, MURILLO-CARRETERO M, MORENO-LOPEZ B, ESTRADA C (2004) Nitric oxide synthesis inhibition increases proliferation of neural precursors isolated from the postnatal mouse subventricular zone. Brain Res 995: 274-284
74. MENCO BP, CUNNINGHAM AM, QASBA P, LEVY N, REED RR (1997) Putative odour receptors localize in cilia of olfactory receptor cells in rat and mouse: a freeze-substitution ultrastructural study. J Neurocytol 26: 691-706
75. MIN YG, RHEE CS, CHOO MJ, SONG HK, HONG SC (1994) Histopathologic changes in the olfactory epithelium in mice after exposure to sulfur dioxide. Acta Otolaryngol 114: 447-452
76. MIZE RR, LO F (2000) Nitric oxide, impulse activity, and neurotrophins in visual system development(1). Brain Res 886: 15-32
77. MONCADA S, PALMER RM, HIGGS EA (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43: 109-142
78. MOON C, YOO JY, MATARAZZO V, SUNG YK, KIM EJ, RONNETT GV (2002) Leukemia inhibitory factor inhibits neuronal terminal differentiation through STAT3 activation. Proc Natl Acad Sci U S A 99: 9015-9020
79. MORALES B, BACIGALUPO J (1996) Chemical reception in vertebrate olfaction: evidence for multiple transduction pathways. Biol Res 29: 333-341
80. MORALES B, MADRID R, BACIGALUPO J (1997) Calcium mediates the activation of the inhibitory current induced by odorants in toad olfactory receptor neurons. FEBS Lett 402: 259-264
81. MORALES B, UGARTE G, LABARCA P, BACIGALUPO J (1994) Inhibitory K+ current activated by odorants in toad olfactory neurons. Proc Biol Sci 257: 235-242
82. MORENO-LÓPEZ B, ROMERO-GRIMALDI C, NOVAL JA, MURILLO-CARRETERO M, MATARREDONA ER, ESTRADA C (2004) Nitric oxide is a physiological inhibitor of neurogenesis in the adult mouse subventricular zone and olfactory bulb. J Neurosci 24: 85-95
83. MORO MA, CÁRDENAS A, HURTADO 0, LEZA JC, LIZASOAIN I (2004) Role of nitric oxide after brain ischaemia. Cell Calcium 36: 265-275
84. MOULTON DG (1974) Dynamics of cell populations in the olfactory epithelium. Ann N Y Acad Sci 237: 52-61
85. NAN B, GETCHELL ML, PARTIN JV, GETCHELL TV (2001) Leukemia inhibitory factor, interleukin-6, and their receptors are expressed transiently in the olfactory mucosa after target ablation. J Comp Neurol 435: 60-77
86. NATHAN C (1992) Nitric oxide as a secretory product of mammalian cells. Faseb J 6: 3051-3064
87. NEWMAN MP, FERON F, MACKAY-SIM A (2000) Growth factor regulation of neurogenesis in adult olfactory epithelium. Neuroscience 99: 343-350
88. OBREGON E, PUNZON MC, GONZÁLEZ-NICOLAS J, FERNÁNDEZ-CRUZ E, FRESNO M, MUÑOZ-FERNÁNDEZ MA (1997) Induction of adhesion/differentiation of human neuroblastoma cells by tumour necrosis factor-alpha requires the expression of an inducible nitric oxide synthase. Eur J Neurosci 9: 1184-1193
89. OKANO HJ, PFAFF DW, GIBBS RB (1996) Expression of EGFR-, p75NGFR-, and PSTAIR (cdc2)-like immunoreactivity by proliferating cells in the adult rat hippocampal formation and forebrain. Dev Neurosci 18: 199-209
90. PACKER MA, STASIV Y, BENRAISS A, CHMIELNICKI E, GRINBERG A, WESTPHAL H, GOLDMAN SA, ENIKOLOPOV G (2003) Nitric oxide negatively regulates mammalian adult neurogenesis. Proc Natl Acad Sci U S A 100: 9566-9571
91. PAYS L, SCHWARTING G (2000) Gal-NCAM is a differentially expressed marker for mature sensory neurons in the rat olfactory system. J Neurobiol 43: 173-185
92. PEUNOVA N, ENIKOLOPOV G (1993) Amplification of calcium-induced gene transcription by nitric oxide in neuronal cells. Nature 364: 450-453
93. PEUNOVA N, ENIKOLOPOV G (1995) Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature 375: 68-73
94. PEUNOVA N, SCHEINKER V, CLINE H, ENIKOLOPOV G (2001) Nitric oxide is an essential negative regulator of cell proliferation in Xenopus brain. J Neurosci 21: 8809-8818
95. PINEDA J, KOGAN JH, AGHAJANIAN GK (1996) Nitric oxide and carbon monoxide activate locus coeruleus neurons through a cGMP-dependent protein kinase: involvement of a nonselective cationic channel. J Neurosci 16: 1389-1399
96. PIXLEY SK, DANGORIA NS, ODOMS KK, HASTINGS L (1998) Effects of insulin-like growth factor 1 on olfactory neurogenesis in vivo and in vitro. Ann N Y Acad Sci 855: 244-247
97. PLENDL J, STIERSTORFER B, SINOWATZ F (1999) Growth factors and their receptors in the olfactory system. Anat Histol Embryol 28: 73-79
98. REIF A, SCHMITT A, FRITZEN S, CHOURBAJI S, BARTSCH C, URANI A, WYCISLO M, MOSSNER R, SOMMER C, GASS P, LESCH KP (2004) Differential effect of endothelial nitric oxide synthase (NOS-III) on the regulation of adult neurogenesis and behaviour. Eur J Neurosci 20: 885-895
99. RHEIN LD, CAGAN RH (1980) Biochemical studies of olfaction: isolation, characterization, and odorant binding activity of cilia from rainbow trout olfactory rosettes. Proc Natl Acad Sci U S A 77: 4412-4416
100. ROSKAMS AJ, BREDT DS, DAWSON TM, RONNETT GV (1994) Nitric oxide mediates the formation of synaptic connections in developing and regenerating olfactory receptor neurons. Neuron 13: 289-299
101. SANTACANA M, UTTENTHAL LO, BENTURA ML, FERNÁNDEZ AP, SERRANO J, MARTÍNEZ DE VELASCO J, ALONSO D, MARTÍNEZ-MURILLO R, RODRIGO J (1998) Expression of neuronal nitric oxide synthase during embryonic development of the rat cerebral cortex. Brain Res Dev Brain Res 111: 205-222
102. SATOH M, YOSHIDA T (1997) Promotion of neurogenesis in mouse olfactory neuronal progenitor cells by leukemia inhibitory factor in vitro. Neurosci Lett 225: 165-168
103. SATOH M, YOSHIDA T (2000) Expression of neural properties in olfactory cytokeratin-positive basal cell line. Brain Res Dev Brain Res 121: 219-222
104. SAUCIER D, ASTIC L (1995) Morpho-functional alterations in the olfactory system of rainbow trout (Oncorhynchus mykiss) and possible acclimation in response to long-lasting exposure to low copper levels. Comp. Biochem. Physiol. 112A: 273-284
105. SCHILD D, RESTREPO D (1998) Transduction mechanisms in vertebrate olfactory receptor cells. Physiol Rev 78: 429-466
106. SCHMACHTENBERG O, BICKER G, BACIGALUPO J (2001) NADPH diaphorase is developmentally regulated in rat olfactory epithelium. Neuroreport 12: 1039-1043
107. SCHULTZ EW (1960) Repair of the olfactory mucosa with special reference to regeneration of olfactory cells (sensory neurons). Am J Pathol 37: 1-19
108. SCHWARTZ LEVEY M, CHIKARAISHI DM, KAUER JS (1991) Characterization of potential precursor populations in the mouse olfactory epithelium using immunocytochemistry and autoradiography. J Neurosci 11: 3556-3564
109. SCHWOB JE, SZUMOWSKI KE, STASKY AA (1992) Olfactory sensory neurons are trophically dependent on the olfactory bulb for their prolonged survival. J Neurosci 12: 3896-3919
110. SCHWOB JE, YOUNGENTOB SL, MEZZA RC (1995) Reconstitution of the rat olfactory epithelium after methyl bromide-induced lesion. J Comp Neurol 359: 15-37
111. SCOTT SP, HARRISON RW, WEBER IT, TANAKA JC (1996) Predicted ligand interactions of 3'5′-cyclic nucleotide-gated channel binding sites: comparison of retina and olfactory binding site models. Protein Eng 9: 333-344
112. SEROOGY KB, GALL CM, LEE DC, KORNBLUM HI (1995) Proliferative zones of postnatal rat brain express epidermal growth factor receptor mRNA. Brain Res 670: 157-164
113. SIMPSON PJ, WANG E, MOON C, MATARAZZO V, COHEN DR, LIEBL DJ, RONNETT GV (2003) Neurotrophin-3 signaling maintains maturational homeostasis between neuronal populations in the olfactory epithelium. Mol Cell Neurosci 24: 858-874
114. SMITH CG (1951) Regeneration of sensory olfactory epithelium and nerves in adult frogs. Anat Rec 109: 661-671
115. SNYDER SH (1992) Nitric oxide and neurons. Curr Opin Neurobiol 2: 323-327
116. STAMLER JS (1994) Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 78: 931-936
117. STAMLER JS, JIA L, EU JP, MCMAHON TJ, DEMCHENKO IT, BONAVENTURA J, GERNERT K, PIANTADOSI CA (1997a) Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science 276: 2034-2037
118. STAMLER JS, TOONE EJ, LIPTON SA, SUCHER NJ (1997b) (S)NO signals: translocation, regulation, and a consensus motif. Neuron 18: 691-696
119. TAO Y, BLACK IB, DICICCO-BLOOM E (1996) Neurogenesis in neonatal rat brain is regulated by peripheral injection of basic fibroblast growth factor (bFGF) J Comp, Neurol 376: 653-663
120. VAN WAGENEN S, REHDER V (2001) Regulation of neuronal growth cone filopodia by nitric oxide depends on soluble guanylyl cyclase. J Neurobiol 46: 206-219
121. VERGE VM, XU Z, XU XJ, WIESENFELD-HALLIN Z, HOKFELT T (1992) Marked increase in nitric oxide synthase mRNA in rat dorsal root ganglia after peripheral axotomy: in situ hybridization and functional studies. Proc Natl Acad Sci U S A 89: 11617-11621
122. VERHAAGEN J, OESTREICHER AB, GRILLO M, KHEW-GOODALL YS, GISPEN WH, MARGOLIS FL (1990) 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: 31-44
123. WANG T, FITZGERALD TJ, HAREGEWOIN A (1999) Differential expression of nitric oxide synthases in EGF-responsive mouse neural precursor cells. Cell Tissue Res 296: 489-497
124. WEISS S, VAN DER KOOY D (1998) CNS stem cells: where's the biology (a.k.a. beef)? J Neurobiol 36: 307-314
125. WELLER JL, KLEIN DC (1992) The pineal adrenergic--cyclic GMP response develops two weeks after the adrenergic--cyclic AMP response. Brain Res Dev Brain Res 68: 144-147
126. WESTERMAN RA, VON BAUMGARTEN R (1964) Regeneration of olfactory paths in carp (Cyprinus carpio L.) Experientia 20: 519-520
127. ZHANG R, ZHANG L, ZHANG Z, WANG Y, LU M, LAPOINTE M, CHOPP M (2001) A nitric oxide donor induces neurogenesis and reduces functional deficits after stroke in rats. Ann Neurol 50: 602-611
128. ZHU DY, LIU SH, SUN HS, LU YM (2003) Expression of inducible nitric oxide synthase after focal cerebral ischemia stimulates neurogenesis in the adult rodent dentate gyrus. J Neurosci 23: 223-229
129. ZORUMSKI CF, IZUMI Y (1993) Nitric oxide and hippocampal synaptic plasticity. Biochem Pharmacol 46: 777-785