Nitric oxide donors enhance neurotrophin-induced neurite outgrowth through a cGMP-dependent mechanism

Journal of Neuroscience Research

Volumn 47, Issue 4, 1997, Pages 427-439

  Hindley, Shaun ^a   Juurlink, Bernhard H J ^b   Gysbers, John W ^a   Middlemiss, Pamela J ^a   Herman, Mary A R ^a   Rathbone, Michel P ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

hippocampal neurons; neurite outgrowth; NGF; PC12 cells; plasticity

Indexed keywords

6 ANILINO 5,8 QUINOLINEQUINONE; 8 BROMO CYCLIC GMP; CYCLIC GMP; NEUROTROPHIN; NITRIC OXIDE;

ANIMAL CELL; ARTICLE; ENZYME ACTIVATION; ENZYME ACTIVITY; GROWTH REGULATION; GROWTH STIMULATION; HIPPOCAMPUS; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NEUROTROPISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; RAT;

ANIMALS; ASTROCYTES; CELLS, CULTURED; CEREBRAL CORTEX; CYCLIC GMP; HIPPOCAMPUS; MICE; NERVE GROWTH FACTORS; NEURITES; NEUROTROPHIN 3; NITRIC OXIDE; NITROPRUSSIDE; PC12 CELLS; RATS; SODIUM NITRITE;

EID: 0031035005     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19970215)47:4<427::AID-JNR8>3.0.CO;2-G     Document Type: Article

References (83)

1. Aruffo C, Ferszt R, Hildebrandt AG, Cervos-Navarro J (1987): Low doses of L-monosodium glutamate promote neuronal growth and differentiation in vitro. Dev Neurosci 9:228-239.
2. Balazs R, Hack N, Jorgensen OS (1988a): Stimulation of the N-methyl-D-aspartate receptor has a trophic effect on differentiating cerebellar granule cells. Neurosci Lett 87:80-86.
3. Balazs R, Jorgensen OS, Hack N (1988b): N-methyl-D-aspartate promotes the survival of cerebellar granule cells in culture. Neurosci 27:437-451.
4. Barde Y-A (1991): The nerve growth factor family. Prog Growth Factor Res 2:237-248.
5. Bohme E, Grossman O, Herz J, Muisch A, Spies C, Schultz G (1984): Regulation of cyclic GMP formation by soluble guanylate cyclase: Stimulation by NO-containing compounds. Adv Cyclic Nucleotide Prot Phosphorylation Res 17:259-266.
6. Bothwell M (1991): Keeping track of neurotrophic receptors. Cell 65:915-918.
7. Bredt DS, Snyder SH (1992): Nitric oxide, a novel neuronal messenger. Neuron 8:3-11.
8. Brewer GJ, Cotman CW (1989): NMDA receptor regulation of neuronal morphology in cultured hippocampal neurons. Neurosci Lett 99:268-273.
9. Bruhwyler J, Chleide E, Liegeois JF, Carreer F (1993): Nitric oxide: A new messenger in the brain. Neurosci Biobehav Rev 17: 373-384.
10. Brune B, Mohr S, Messmer UK (1995): Protein thiol modification and apoptotic cell death as cGMP-independent nitric oxide (NO) signaling pathways. Rev Physiol Biochem Pharmacol 127:1-30.
11. Bulloch AGM (1989): Sprouting by intact helisoma neurons: Role for glutamate. J Neurosci Res 23:384-395.
12. Bulloch AGM, Hauser GC (1990): Sprouting by isolated helisoma neurons: enhancement by glutamate. Int J Dev Neurosci 8:391-398.
13. 2+ release in neurosecretory PC-12 cells: Inhibition of phospholipase C activity via cyclic GMP-dependent protein kinase 1. Mol Pharmacol 47:517-524.
14. Cornwell TL, Arnold E, Boerth NJ, Lincoln TM (1994): Inhibition of smooth muscle cell growth by nitric oxide and activation of cAMP-dependent protein kinase by cGMP. Am J Physiol 36: C1405-C1413.
15. Dawson VL, Dawson TM, Bartley DA, Uhl GR, Snyder SH (1993): Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures. J Neurosci 13:2651-2661.
16. De Koninck P, Carbonetto S, Cooper E (1993): NGF induces neonatal rat sensory neurons to extend dendrites in culture after removal of satellite cells. J Neurosci 13:577-585.
17. Desole MS, Kim W-K. Rabin RA, Laychock SG (1994): Nitric oxide reduces depolarization-induced calcium influx in PC12 cells by a cyclic GMP-mediated mechanism. Neuropharmacology 33: 193-198.
18. Farinelli SE, Park DS, Greene LA (1996): Nitric oxide delays the death of trophic factor-deprived PC12 cells and sympathetic neurons by a cGMP-medialed mechanism. J Neurosci 16: 2325-2334.
19. Fujita K, Lazarovici P, Guroff G (1989): Regulation of the differentiation of PC12 pheochromocytoma cells. Environ Health Perspect 80:127-142.
20. Gage FH, Buzsaki G, Armstrong DM (1990): NGF-dependent sprouting and regeneration in the hippocampus. Prog Brain Res 83: 357-370.
21. Gally JA, Montague PR, Reeke J, Edelman GM (1990): The NO hypothesis: Possible effects of a short-lived, rapidly diffusible signal in the development and function of the nervous system. Proc NY Acad Sci 87:3547-3551.
22. Garthwaite J (1991): Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci 14:60-67.
23. Greene LA, Tischler AS (1982): PC12 pheochromocytoma cultures in neurobiological research. Adv Cell Neurosci 3:373-414.
24. Gunning PW, Landreth GE, Bothwell MA, Shooter EM (1981a): Differential and synergistic actions of nerve growth factor and cyclic AMP in PC12 cells. J Cell Biol 89:240-245.
25. Gunning PW, Hetourneau PC, Handreth GE, Shooter IM (1981b): The action of nerve growth factor and dibutyryl adenosine cyclic 3′5′ monophosphate on rat pheochromocytoma reveals distinct stages in the mechanisms underlying neurite outgrowth. J Neurosci 1:1085-1095.
26. Gysbers JW, Rathbone MP (1992): Guanosine enhances NGF-stimulated neurite outgrowth in PC12 cells. NeuroReport 3:997-1000.
27. Halegoua S, Armstrong RC, Kremer NE (1991): Dissecting the mode of action of a neuronal growth factor. Curr Top Microbiol Immunol 165:119-170.
28. Herman MAR, Schultz CA, Claude P (1994): Responses to cAMP depend on state of neuronal differentiation of NGF-treated adrenal chromaffin cells. Dev Biol 161:477-489.
29. Hertz L, Juurlink BHJ, Hertz E, Fosmark H, Schousboe A (1989): Preparation of primary cultures of mouse (rat) astrocytes. In Shahar A, de Vellis J, Vernadakis A, Haber B (eds): "A Dissection and Tissue Culture Manual of the Nervous System." New York: Alan R. Liss, Inc., pp 105-108.
30. Hess DT, Patterson SI, Smith DS, Pate Skene JH (1993): Neuronal growth cone collapse and inhibition of protein fatty acylation by nitric oxide. Nature 366:562-565.
31. Hindley S, Rathbone MP (1994): Nitric oxide and carbon monoxide enhance neurite outgrowth from PC12 cells by activating soluble guanylate cyclase. Nitric oxide in the Nervous System-Neuropharmacology II 1:5.10. (Abstr)
32. Hirsch DB, Steiner JP, Dawson TM, Mammen A, Hayek E, Snyder SH (1993): Neurotransmitter release regulated by nitric oxide in PC-12 cells and brain synaptosomes. Curr Biol 3:749-754.
33. Holtzman DM, Kilbridge J, Bredt DS, Black SM, Li Y, Clary DO, Reichardt LF, Mobley WC (1994): NOS induction by NGF in basal forebrain cholinergic neurones: Evidence for regulation of brain NOS by a neurotrophin. Neurobiol Disease 1:51-60.
34. Huffacker T, Corcoran T, Wagner JA (1984): Adenosine inhibits cell division and promotes neurite extension in PC12 cells. J Cell Physiol 120:188-196.
35. Ip NY, Li Y, van de Stadt I, Panayatatos N, Alderson RF, Lindsay RM (1991): Ciliary neurotrophic factor enhances neuronal survival in embryonic rat hippocampal cultures. J Neurosci 11: 3124-3134.
36. Ip NY, Li Y, Yancopoulos GD, Lindsay RM (1993): Cultured hippocampal neurons show responses to BDNF, NT-3, and NT-4, but not NGF. J Neurosci 13:3394-3405.
37. Kaupp UB (1991): The cyclic nucleotide-gated channels of vertebrate photoreceptors and olfactory epithelium. Trends Neurosci 14: 150-157.
38. Laasberg T, Pihlak A, Neuman T, Paves H, Saarma M (1988): Nerve growth factor increases the cyclic GMP level and activates the cyclic GMP phosphodiesterase in PC12 cells. FEBS Lett 239: 367-370.
39. Laustiola KE, Vuorinen P, Porsti I, Metsa-Ketela T, Manninen V (1991): Exogenous GTP enhances the effects of sodium nitrite on cyclic GMP accumulation, vascular smooth muscle relaxation and platelet aggregation. Pharmacol Toxicol 68:60-63.
40. Light DB, Corbin JD, Stanton BA (1990): Dual ion-channel regulation by cyclic GMP and cyclic GMP-dependent protein kinase. Nature 344:336-339.
41. Lincoln TM, Corbin JD (1983): Characterization and biological role of the cGMP-dependent protein kinase. Ad Cyclic Nucleo Res 15:139-192.
42. Lincoln TM, Cornwell TL (1993): Intracellular cyclic GMP receptor proteins. FASEB J 7:328-338.
43. Lipton SA, Choi Y-B, Pan Z-H, Lei SZ, Chen H-SV, Sucher NJ, Loscalzo J, Singel DJ, Stamler JS (1993): A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364: 626-632.
44. MacFarland RT, Stroop SD, Beavo JA (1990): Structural and functional characteristics of cyclic GMP-stimulated phosphodiesterases and their role in intracallular signal transduction. In Jacobson KA, Daly JW, Manganiello V (eds): "Purines in Cellular Signaling Targets for New Drugs." New York: Springer-Verlag, pp 281-296.
45. Maness LM, Kastin AJ, Weber JT, Banks WA, Beckman BS, Zadina JE (1994): The neurotrophins and their receptors: Structure, function, and neuropathology. Neurosci Biobehav Rev 18: 143-159.
46. Martin W, Villani GM, Jothianandan D, Furchgott RFJ (1985): Selective blockade of endothelium-dependent and glyceryl trinitrate-induced relaxation by hemoglobin and by methylene blue in the rabbit aorta. J Pharmacol Exp Ther 232:708-716.
47. Maurice DH, Haslam RJ (1990): Molecular basis of the synergistic inhibition of platelet function by nitrovasodilators and activators of adenylate cyclase: Inhibition of cyclic AMP breakdown by cyclic GMP. Mol Pharmacol 37:671-681.
48. Mayer B, Brunner F, Schmidt K (1993): Inhibition of nitric oxide synthesis by methylene blue. Biochem Pharmacol 45:367-374.
49. Meakin SO, Shooter EM (1992): The nerve growth factor family of receptors. Trends Neurosci 15:323-331.
50. 2+ current is regulated by cyclic GMP-dependent protein kinase in mammalian cardiac myocytes. Proc Natl Acad Sci 88:1197-1201.
51. Miller JP, Uno H, Christensen LF, Robins RK, Meyer RB (1981): Effect of modification of 1-, 2-, and 6-positions of 9-β-D-ribofuranosylpurine cyclic 3′,5′-phosphate on the cyclic nucleotide specificity of adenosine cyclic 3′,5′-phosphate- and guanosine cyclic 3′,5′-phosphate-dependent protein kinases. Biochem Pharmacol 30:509-515.
52. Moriguchi M, Manning LR, Manning JM (1992): Nitric oxide can modify amino acid residues in proteins. Biochem Biophys Res Commun 183:598-604.
53. Munoz-Fernandez MA, Cano E, O'Donnell CA, Doyle J, Liew FY, Fresno M (1994): Tumor necrosis factor-α (TNF-α), interferon-γ, and interleukin-6 but not TNF-β induce differentiation of neuroblastoma cells: The role of nitric oxide. J Neurochem 62:1330-1336.
54. Murphy S, Simmons ML, Agullo L, Garcia A, Feinstein DL, Galea E, Reis DJ, Minc-Golomb D, Schwartz JP (1993): Synthesis of nitric oxide in CNS glial cells. Trends Neurosci 16:323-328.
55. Nakamura T, Gold GH (1987): A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature 325:442-444.
56. Nathan C (1992): Nitric oxide as a secretory product of mammalian cells. FASEB J 6:3051-3064.
57. Nobles M, Diener M, Rummel W (1991): Segment-specific effects of the heat stable enterotoxin E. coli on electrolyte transport in the rat colon. Eur J Pharmacol 202:201-211.
58. - cotransport in vascular smooth muscle cells. J Biol Chem 261:15461-15466.
59. Ogreid D, Ekanger R, Suva RH, Miller JP, Doskeland SO (1989): Comparison of the two classes of binding sites (A and B) of type I and type II cyclic - AMP - dependent protein kinases by using cyclic nucleotide analogs. Eur J Biochem 181:19-31.
60. Ouedraogo S, Tschopl M, Stoclet J-C, Bucher B (1994): Effects of cyclic GMP and analogues on neurogenic transmission in the rat tail artery. Br J Pharmacol 112:867-872.
61. Patel AJ, Hunt A, Sanfeliu C (1990): Cell-type specific effects of N-methyl-D-asparate on biochemical differentiation of subcortical neurons in culture. Int J Dev Neurosci 8:379-389.
62. 2+ current increase in snail neurons. Nature 323:812-814.
63. Pearce IA, Cambray-Deakin MA, Burgoyne RD (1987): Glutamate acting on NMDA receptors stimulates neurite outgrowth from cerebellar granule cells. FEBS Lett 223:143-147.
64. Peunova N, Enikolopov G (1995): Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature 374:68-73.
65. Rauschecker JP, Egert U, Kossel A (1993): Effects of NMDA antagonists on developmental plasticity in kitten visual cortex. Int J Dev Neurosci 8:425-435.
66. Reeklies A, Rathbone MP, Hall RH (1974): Stimulation of nerve fiber growth from cultured sympathetic explants. Can J Physiol Pharmacol 52:840-851.
67. Ritcher-Landsberg C, Jastorff B (1986): The role of cAMP in nerve growth factor-promoted neurite outgrowth in PC12 cells. J Cell Biol 102:821-829.
68. Rudge JS (1993): Astrocyte-derived Neurotrophic Factors. In Murphy S (ed): "Astrocytes: Pharmacology and Function." San Diego: Academic Press, Inc., pp 267-305.
69. Schmidt HHHW, Lohmann SM, Ulrich W (1993): The nitric oxide and cGMP signal transduction system: Regulation and mechanism of action. Biochim Biophys Acta 1178:153-175.
70. Schuman EM, Madison DV (1991): A requirement for intercellular messenger nitric oxide in long-term potentiation. Science 254: 1503-1506.
71. Schulick A, Gusovsky F, Yasumoto T, Daly JW (1990): Effects of maitotoxin on atrial natriuretic factor-mediated accumulation of cyclic GMP in PC12 cells. Life Sciences 46:671-678.
72. Sonnenburg WK, Beavo JA (1994): Cyclic GMP and regulation of cyclic nucleotide hydrolysis. Adv Pharmacol 26:87-114.
73. Thoenen H (1991): The changing scene of neurotrophic factors. Trends Neurosci 14:165-170.
74. Van Der Zee CEEM, Fawcett J, Diamond J (1992): Antibody to NGF inhibits collateral sprouting of septohippocampal fibers following entorhinal cortex lesion in adult rats. J Comp Neurol 326: 91-100.
75. Varon S, Conner JM (1994): Nerve growth factor in CNS repair. J Neurotrauma 11:473-486.
76. Verge VMK, Xu Z, Xu X-J, Weisenfeld-Hallin Z, Hokfelt T (1992): Proc Natl Acad Sci U S A 89:11617-11621.
77. Vidal-Sanz M, Bray GM, Villegas-Perez MP, Thanos S, Aguayo AJ (1987): Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in adult rat. J Neurosci 7:2894-2909.
78. Walicke P, Cowan WM, Ueno N, Baird A, Guillemin R (1986): Fibroblast growth factor promotes survival of dissociated hippocampal neurons and enhances neurite extension. Proc Natl Acad Sci 83:3012-3016.
79. Whalin ME, Scammell JG, Strada SJ, Thompson WJ (1991): Phosphodiesterase II, the cGMP-activable cyclic nucleotide phosphodiesterase, regulates cyclic AMP metabolism in PC12 cells. Mol Pharmacol 39:711-717.
80. Wink DA, Kasprzak KS, Maragos CM, Elespuru RK, Misra M, Dunams TM, Cebula TA, Koch WH, Andrews AW, Allen JS, Keefer LK (1991): DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science 254:1001-1003.
81. Zhuo M, Small SA. Kandel ER, Hawkins RD (1993): Nitric oxide and carbon monoxide produce activity-dependent long term synaptic enhancement in hippocampus. Science 260:1946-1950.
82. Zurn AD (1991): Catecholaminergic traits in chick sympathetic neurons may be differentially regulated by a cGMP-dependent pathway. Brain Res Dev Brain Res 58:105-110.
83. Zwiller J, Goridis C, Ciesielski-Tresda J, Mandel P (1977): Cyclic GMP in a neuroblastoma clone: possible involvement in morphological differentiation induced by dibutyryl cyclic AMP. J Neurochem 29:273-278.