Nitric oxide and adult neurogenesis in health and disease

Neuroscientist

Volumn 11, Issue 4, 2005, Pages 294-307

  Estrada, Carmen ^a   Murillo Carretero, Maribel ^a  

^a UNIVERSITY OF CÁDIZ   (Spain)

Author keywords

Angiogenesis; Dentate gyrus; Epidermal growth factor receptor; Nitric oxide synthase; Subventricular zone; Vascular endothelial growth factor

Indexed keywords

7 NITROINDAZOLE; AMINOGUANIDINE; EPIDERMAL GROWTH FACTOR RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; N(G) NITRO DEXTRO ARGININE METHYL ESTER; N(G) NITROARGININE METHYL ESTER; NERVE CELL ADHESION MOLECULE; NESTIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; VASCULOTROPIN; VIMENTIN;

ANGIOGENESIS; BRAIN INJURY; BRAIN ISCHEMIA; CELL TYPE; DENTATE GYRUS; HUMAN; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEIZURE; SURVIVAL TIME; SYNAPTIC TRANSMISSION;

ANIMALS; BRAIN; BRAIN DISEASES; CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; MODELS, NEUROLOGICAL; NITRERGIC NEURONS; NITRIC OXIDE; ORGANOGENESIS; STEM CELLS;

EID: 22844431634     PISSN: 10738584     EISSN: None     Source Type: Journal    
DOI: 10.1177/1073858404273850     Document Type: Review

References (80)

1. Aicher A, Heeschen C, Dimmeler S. 2004. The role of NOS3 in stem cell mobilization. Trends Mol Med 10:421-5.
2. Alderton WK, Cooper CB, Knowles RG. 2001. Nitric oxide synthases: structure, function and inhibition. Biochem J 357:593-615.
3. Alvarez-Buylla A, García-Verdugo JM. 2002. Neurogenesis in adult subventricular zone. J Neurosci 22:629-34.
4. Alvarez-Buylla A, Lim DA. 2004. For the long run: maintaining germinal niches in the adult brain. Neuron 41:683-6.
5. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. 2002. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8:963-70.
6. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, and others. 1999. Bone marrow origin of endothelial progenitor cells responsible for postnatal vaseulogenesis in physiological and pathological neovascularization. Circ Res 85:221-8.
7. Bouloumie A, Schini-Kerth VB, Busse R. 1999. Vascular endothelial growth factor up-regulated nitric oxide synthase expression in endothelial cells. Cardiovasc Res 41:773-80.
8. Bredt DS, Hawing PH, Snyder SH. 1990. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347:768-70.
9. Bredt DS, Snyder SH. 1994. Transient nitric oxide synthase neurons in embryonic cerebral cortical plate, sensory ganglia and olfactory epithelium. Neuron 13:301-13.
10. Carleton A, Petreanu LT, Lansford R, Alvarez-Buylla A, Lledo PM. 2003. Becoming a new neuron in the adult olfactory bulb. Nat Neurosci 6:507-18.
11. Chen J, Li Y, Zhang R, Katakowski M, Gautam SC, Xu Y, and others. 2004. Combination therapy of stroke in rats with a nitric oxide donor and human bone marrow stromal cells enhances angiogenesis and neurogenesis. Brain Res 1005:21-8.
12. Chcn J, Zhang ZG, Li Y, Wang Y, Wang L, Jiang H, and others. 2003. Statins induce angiogenesis, neurogenesis, and synaptogenesis after stroke. Ann Neurol 53:743-51.
13. Cheng A, Wang S, Cai J, Rao MS, Mattson MP. 2003. Nitric oxide acts in a positive feedback loop with BDNF to regulate neural progenitor cell proliferation and differentiation in the mammalian brain. Dev Biol 258:319-33.
14. Ciani E, Severi S, Contestabile A, Bartesaghi R, Contestabile A. 2004. Nitric oxide negatively regulates proliferation and promotes neuronal differentiation through N-Myc downregulation. J Cell Sci 117:4727-37.
15. Cooke JP. 2003. NO and angiogenesis. Atheroscler Suppl 4:53-60.
16. Craig CG, Tropepe V, Morshead CM, Reynolds BA, Weiss S, van der Kooy D. 1996. In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci 16:2649-58.
17. Doetsch F, Caille I, Lim DA, García-Verdugo JM, Alvarez-Buylla A. 1999. SVZ astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-16.
18. Doetsch F, García-Verdugo JM, Alvarez-Buylla A. 1997. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17:5046-61.
19. Doetsch F, Petreanu L, Caille I, García-Verdugo JM, Alvarez-Buylla A. 2002. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36:1021-34.
20. Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn A-M, Nordborg C, Peterson DA, Gage FH. 1998. Neurogenesis in the adult human hippocampus. Nat Med 4:1313-7.
21. Estrada C, Gomez C, Martin-Nieto J, De Frutos T, Jimenez A, Villalobo A. 1997. Nitric oxide reversibly inhibits the epidermal growth factor receptor tyrosine kinase. Biochem J 326:369-76.
22. Gage FH. 2000. Mammalian neural stem cells. Science 287:1433-8.
23. Garg UC, Hassid A. 1989. Nitric oxide-generating vasodilators and 8-bromo-cyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J Clin Invest 83:1774-7.
24. Garg UC, Hassid A. 1990. Nitric oxide-generating vasodilators inhibit mitogenesis and proliferation of BALB/c 3T3 fibroblasts by a cyclic GMP-independent mechanism. Biochem Biophys Res Commun 171:474-9.
25. Gibbs SM. 2003. Regulation of neuronal proliferation and differentiation by nitric oxide. Mol Neurobiol 27:107-20.
26. Gritti A, Frölichsthal-Schoeller P, Galli R, Parati EA, Cova L, Pagano SF, and others. 1999. Epidermal and fibroblast growth factors behave as mitogenic regulators for a single multipotent stem cell-like population from the subventricular region of the adult mouse forebrain. J Neurosci 19:3287-97.
27. Jiang W, Xiao L, Wang JC, Huang YG, Zhang X. 2004. Effects of nitric oxide on dentate gyrus cell proliferation after seizures induced by pentylenetrazol in the adult rat brain. Neurosci Lett 367:344-8.
28. Jin K, Mao XO, Sun Y, Xie L, Jin L, Nishi E, and others. 2002. Heparin-binding epidermal growth factor-like growth factor: hypoxia-inducible expression in vitro and stimulation of neurogenesis in vitro and in vivo. J Neurosci 22:5365-73.
29. Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP, Greenberg DA. 2001. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci U S A 98:4710-5.
30. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, Greenberg DA. 2002. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci U S A 99:11946-50.
31. Kawahara N, Mishima K, Higashiyama S, Taniguchi N, Tamura A, Kirino T. 1999. The gene for heparin-binding epidermal growth factor-like growth factor is stress-inducible: its role in cerebral ischemia. J Cereb Blood Flow Metab 19:307-20.
32. Keynes RG, Garthwaite J. 2004. Nitric oxide and its role in ischaemic brain injury. Cur Mol Med 4:175-87.
33. Knowles RG, Moncada S. 1994. Nitric oxide synthases in mammals. Biochem J 298:249-58.
34. 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 17:5820-9.
35. Kuzin B, Roberts I, Peunova N, Enikolopov G. 1996. Nitric oxide regulates cell proliferation during Drosophila development. Cell 87:639-49.
36. Liu J, Solway K, Messing RO, Sharp FR. 1998. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci 18:7768-78.
37. Lo EH, Hara H, Rogowska J, Trocha M, Pierce AR, Huang PL, and others. 1996. Temporal correlation mapping analysis of the hemodynamic penumbra in mutant mice deficient in endothelial nitric oxide synthase gene expression. Stroke 27:1381-5.
38. Lois C, Alvarez-Buylla A. 1993. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci U S A 90:2074-7.
39. Lois C, Alvarez-Buylla A. 1994. Long-distance neuronal migration in the adult mammalian brain. Science 264:1145-8.
40. López-Figueroa MO, Itoi K, Watson SJ. 1998. Regulation of nitric oxide synthase messenger RNA expression in the rat hippocampus by glucocorticoids. Neuroscience 87:439-46.
41. 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 995:274-84.
42. Moreno-López B, Noval JA, González-Bonet L, Estrada C. 2000. Morphological bases for a role of nitric oxide in adult neurogenesis. Brain Res 869:244-50.
43. 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.
44. Murillo-Carretero M, Ruano MJ, Matarredona ER, Villalobo A, Estrada C. 2002. Antiproliferative effect of nitric oxide on epidermal growth factor-responsive human neuroblastoma cells. J Neurochem 83:119-31.
45. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, Kawahara N, and others. 2002. Regeneration of hippocampal pyramidal neurons after ischemic brain injury, by recruitment of endogenous neural progenitors. Cell 110:429-41.
46. Nelson RJ, Demas GE, Huang PL, Fishman MC, Dawson WL, Dawson TM, Snyder SH. 1995. Behavioural abnormalities in male mice lacking neuronal nitric oxide synthase. Nature 378:383-6.
47. Obregón E, Punzón MC, González-Nicolás J, Fernandez-Cruz E, Fresno M, Muñoz-Fernández MA. 1997. Induction of adhesion/differentiation of human neuroblastoma cells by tumor necrosis factor-alpha requires the expression of an inducible nitric oxide synthase. Eur J Neurosci 9:1184-93.
48. Ogura T, Nakayama K, Fujisawa H, Esumi H. 1996. Neuronal nitric oxide expression in neuronal cell differentiation. Neurosci Lett 204:89-92.
49. Packer MA, Stasiv Y, Benraiss A, Chmielnicki E, Grinberg A, Westphal H, and others. 2003. Nitric oxide negatively regulates mammalian adult neurogenesis. Proc Natl Acad Sci U S A 100:9566-71.
50. Palmer TD, Markakis EA, Willhoite AR, Safar F, Gage FH. 1999. Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci 19:8487-97.
51. Palmer TD, Willhoite AR, Gage FH. 2000. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425:479-94.
52. Papapetropoulos A, Garcia-Cardena G, Madri JA, Sessa WC. 1997. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J Clin Invest 100:3131-9.
53. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH. 1997. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17:3727-38.
54. Park C, Kang M, Kwon YK, Chung JH, Ahn H, Huh Y. 2001. Inhibition of neuronal nitric oxide synthase enhances cell proliferation in the dentate gyrus of the adrenalectomized rat. Neurosci Lett 309:9-12.
55. Park C, Sohn Y, Shin KS, Kim J, Ahn H, Huh Y. 2003. The chronic inhibition of nitric oxide synthase enhances cell proliferation in the adult rat hippocampus. Neurosci Lett 339:9-12.
56. Pencea V, Bingaman KD, Wiegand SJ, Luskin MB. 2001. Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J Neurosci 21:6706-17.
57. Peterson DA. 2004. Umbilical cord blood cells and brain stroke injury: bringing in fresh blood to address an old problem. J Clin Invest 114:312-4.
58. Peunova N, Enikolopov G. 1995. Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature 375:68-73.
59. Peunova N, Scheinker V, Cline H, Enikolopov G. 2001. Nitric oxide is an essential regulator of cell proliferation in Xenopus brain. J Neurosci 21:8809-18.
60. Rafii S, Lyden D. 2003. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 9:702-12.
61. Reif A, Schmitt A, Fritzen S, Chourbaji S, Bartsch C, Urani A, and others. 2004. Differential effect of endothelial nitric oxide synthase (NOS-III) on the regulation of adult neurogenesis and behaviour. Eur J Neurosci 20:885-95.
62. Reynolds BA, Weiss S. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-10.
63. Rochefort C, Gheusi G, Vincent J-D, Lledo P-M. 2002. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci 22:2679-89.
64. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbara NM, Gupta N, Kunwar S, and others. 2004. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427:740-4.
65. Santacana M, Uttenthal LO, Bentura ML, Fernández AP, Serrano J, Martinez de Velasco J, and others. 1998. Expression of neuronal nitric oxide synthase during embryonic development of the rat cerebral cortex. Brain Res Dev Brain Res 111:205-22.
66. Schanzer A, Wachs FP, Wilhelm D, Acker T, Cooper-Kuhn C, Beck H, and others. 2004. Direct stimulation of adult neural stem cells in vitro and neurogenesis in vivo by vascular endothelial growth factor. Brain Pathol 14:237-48.
67. Seri B, Garcia-Verdugo JM, Collado-Morente L, Cewen BS, Alvarez-Buylla A. 2004. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 478:359-78.
68. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A. 2001. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153-60.
69. Shizukuda Y, Tang S, Yokota R, Ware JA. 1999. Vascular endothelial growth factor-induced endothelial cell migration and proliferation depend on a nitric oxide-mediated decrease in protein kinase Cdelta activity. Circ Res 85:247-56.
70. Stamler JS, Lamas S, Fang FC. 2001. Nitrosylation, the prototypic redox-based signaling mechanism. Cell 106:675-83.
71. Taguchi A, Soma T, Tanaka H, Kanda T, Nishimura H, Yoshikawa H, and others. 2004. Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J Clin Invest 114:330-8.
72. Teramoto T, Qiu J, Plumier JC, Moskowitz MA. 2003. EGF amplifies the replacement of parvalbumin-expressing striatal interneurons after ischemia. J Clin Invest 111:1125-32.
73. Tropepe V, Craig CG, Morshead CM, van der Kooy D. 1997. Transforming growth factor-alpha null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. J Neurosci 17:7850-9.
74. Tropepe V, Sibilia M, Ciruna BG, Rossant J, Wagner EF, van der Kooy D. 1999. Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev Biol 208:166-88.
75. Wang L, Zhang Z, Wang Y, Zhang R, Chopp M. 2004. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 35:1732-7.
76. Zhang H, Vutskits L, Pepper MS, Kiss JZ. 2003. VEGF is a chemoattractant for FGF-2-stimulated neural progenitors. J Cell Biol 163:1375-84.
77. Zhang R, Wang L, Zhang L, Cheng J, Zhu Z, Zhang Z, Chopp M. 2003. Nitric oxide enhances angiogenesis via the synthesis of vascular endothelial growth factor and cGMP after stroke in the rat. Circ Res 92:308-13.
78. 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 50:602-11.
79. Zhang ZG, Zhang L, Jiang Q, Zhang R, Davies K, Powers C, and others. 2000. VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J Clin Invest 106:829-38.
80. 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 23:223-9.