Nitric oxide (NO·) stabilizes whereas nitrosonium (NO+) enhances filopodial outgrowth by rat retinal ganglion cells in vitro

Brain Research

Volumn 868, Issue 1, 2000, Pages 1-13

  Cheung, Wing S ^a   Bhan, Ishir ^a   Lipton, Stuart A ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b BURNHAM INSTITUTE   (United States)

Author keywords

cGMP; Neuronal outgrowth; No related species; Peroxynitrite; Retina

Indexed keywords

CYCLIC GMP; GROWTH ASSOCIATED PROTEIN; GUANYLATE CYCLASE; NITRIC OXIDE; NITRIC OXIDE DONOR; NITRIC OXIDE SYNTHASE; NITROSONIUM; PEROXYNITRITE; UNCLASSIFIED DRUG; ANTIOXIDANT; CYSTEINE; DRUG DERIVATIVE; NITRITE; NITROGEN OXIDE; NITROSO DERIVATIVE; NITROXYL; S NITROSOCYSTEINE; S NITROSOTHIOL; S-NITROSOCYSTEINE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GROWTH CONE; GROWTH REGULATION; NERVE FIBER GROWTH; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; RAT; RETINA GANGLION CELL; ANIMAL; CELL CULTURE; DRUG EFFECT; IN VITRO STUDY; LONG EVANS RAT; METABOLISM; PSEUDOPODIUM; ULTRASTRUCTURE;

ANIMALS; ANTIOXIDANTS; CELLS, CULTURED; CYCLIC GMP; CYSTEINE; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRITES; NITROGEN OXIDES; NITROSO COMPOUNDS; PSEUDOPODIA; RATS; RATS, LONG-EVANS; RETINAL GANGLION CELLS; S-NITROSOTHIOLS;

EID: 0034674068     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(00)02161-2     Document Type: Article

References (88)

1. Allen R.D., Allen N.S., Travis J.L. Video-enhanced contrast, differential interference contrast (AVEC-DIC) microscopy: a new method capable of analyzing microtubule-related motility in the reticulopodial network of Allogromia laticollaris. Cell. Motil. 1:1981;291-302.
2. Arancio O., Kandel E.R., Hawkins R.D. Activity-dependent long-term enhancement of transmitter release by presynaptic 3′,5′-cyclic GMP in cultured hippocampal neurons. Nature. 376:1995;74-80.
3. Atkinson J., Panni M.K. Optic target regulation of NADPH-diaphorase by larval retinal axons in Drosophila. Neurosci. Lett. 262:1999;21-24.
4. Baader S.L., Bucher S., Schilling K. The development expression of neuronal nitric oxide synthase in cerebellar granule cells is sensitive to GABA and neurotrophins. Dev. Neurosci. 19:1997;283-290.
5. Becker K., Savvides S.N., Keese M., Schirmer F.H., Karplus P.A. Enzyme inactivation through sulfhydryl oxidation by physiologic NO-carriers. Nature Struct. Biol. 5:1998;267-271.
6. Beckman J.S. The physiological and pathological chemistry of nitric oxide. Lancaster J. The Biological Chemistry of Nitric Oxide. 1994;Academic Press, San Diego, CA.
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. Böhme G.A., Bon C., Stutzmann J.M., Doble A., Blanchard J.C. Possible involvement of nitric oxide in long-term potentiation. Eur. J. Pharmacol. 199:1991;379-381.
9. Bon C., Böhme G.A., Doble A., Stutzmann J.M., Blanchard J.C. A role for nitric oxide in long-term potentiation. Eur. J. Neurosci. 4:1992;420-424.
10. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., Lipton S.A. Apoptosis and necrosis: two distinct events induced respectively by mild and intense insults with NMDA or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. U.S.A. 92:1995;7162-7166.
11. Boulton C.L., Irving A.J., Southam E., Potier B., Garthwaite J., Collingridge G.L. The nitric oxide-cyclic GMP pathway and synaptic depression in rat hippocampal slices. Eur. J. Neurosci. 6:1994;1528-1535.
12. 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.
13. Bredt D.S., Snyder S.H. Nitric oxide, a novel neuronal messenger. Neuron. 8:1992;3-11.
14. Brenman J.E., Chao D.S., Gee S.H., McGee A.W., Craven S.E., Santilliano D.R., Wu Z., Huang F., Xia H., Peters M.F., Froehner S.C., Bredt D.S. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and α1-syntrophin mediated by PDZ domains. Cell. 84:1996;757-767.
15. Brüne B., von Knethen A., Sandau K.B. Nitric oxide and its role in apoptosis. Eur. J. Pharmacol. 351:1998;261-272.
16. 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.
17. Dawson T.M., Dawson V.L., Snyder S.H. A novel neuronal messenger molecule in brain: the free radical, nitric oxide. Ann. Neurol. 32:1992;297-311.
18. Dawson V.L., Dawson T.M., Bartley D.A., Uhl G.R., Snyder S.H. Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures. J. Neurosci. 13:1993;2651-2661.
19. Dawson V.L., Dawson T.M., London E.D., Bredt D.S., Snyder S.H. Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl. Acad. Sci. U.S.A. 88:1991;6368-6371.
20. Djamgoz M.B.A., Aguilo R., Greenstreet E.H., Reynolds R., Wilkin G.P. Histochemistry of NADPH-diaphorase - a marker for neuronal nitric oxide synthase - in the carp retina. Neurochem. Int. 28:1996;283-291.
21. East S.J., Garthwaite J. NMDA receptor activation in rat hippocampus induces cyclic GMP formation through the L-arginine-nitric oxide pathway. Neurosci. Lett. 123:1991;17-19.
22. Ernst A., Gallo G., Letourneau P., McLoon S. BDNF protects against nitric oxide induced retinal growth cone collapse. Soc. Neurosci. Abstr. 24:1998;1518.
23. Gally J.A., Montague P.R., Reeke G.N.J., Edelman G.M. The nitric oxide hypothesis: possible effects of a short-lived, rapidly diffusible signal in development and function of the nervous system. Proc. Natl. Acad. Sci. U.S.A. 87:1990;3547-3551.
24. Garthwaite J. Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci. 14:1991;60-67.
25. Garthwaite J., Charles S.L., Chess W.R. Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature. 336:1988;385-388.
26. Garthwaite J., Southam E., Boulton C.L., Nielsen E.B., Schmidt K., Mayer B. Potent and selective inhibition of nitric oxide-sensitive guanylate cyclase by 1H-[1,2,4-oxadiazolo[4,3-a]quinoxalin-1-one. Mol. Pharmacol. 48:1995;184-188.
27. 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.
28. Gow A.J., Stamler J.S. Reactions between nitric oxide and haemoglobin under physiological conditions. Nature. 391:1998;169-173.
29. Goy M. cGMP: the wayward child of the cyclic nucleotide family. Trends Neurosci. 14:1991;293-299.
30. Gribkoff V.K., Lum-Ragan J.T. Evidence for nitric oxide synthase inhibitor-sensitive and insensitive hippocampal synaptic potentiation. J. Neurophysiol. 68:1992;639-642.
31. Haby C., Lisovoski F., Aunis D., Zwiller J. Stimulation of the cyclic GMP pathway by NO induces expression of the immediate early genes c-fos and junB in PC12 cells. J. Neurochem. 62:1994;496-501.
32. Haley J.E., Wilcox G.L., Chapman P.F. The role of nitric oxide in hippocampal long-term potentiation. Neuron. 8:1992;211-216.
33. Hess D.T., Patterson S.I., Smith D.S., Skene J.H.P. Neuronal growth cone collapse and inhibition of protein fatty acylation by nitric oxide. Nature. 366:1993;562-565.
34. Johnson J.E., Barde Y.A., Schwab M., Thoenen H. Brain-derived neurotrophic factor supports the survival of cultured rat retinal ganglion cells. J. Neurosci. 6:1986;3031-3038.
35. Johnston H.M., Morris B.J. Selective regulation of dendritic MAP-2 mRNA levels in hippocampal granule cells by nitric oxide. Neurosci. Lett. 117:1994;5-10.
36. Kashii S., Mandai M., Kikuchi M., Honda T., Tamurea T., Kaneda K., Akaike A. Dual actions of nitric oxide in N-methyl-D-aspartate receptor-mediated neurotoxicity in cultured retinal neurons. Brain Res. 711:1996;93-101.
37. -. Neuron. 24:1999;461-469.
38. Kim W.-K., Rayudu P.V., Mullins M.E., Stamler J.S., Lipton S.A. Down regulation of NMDA receptor activity in cortical neurons by peroxynitrite. Moncada S., Stamler J.S., Gross S., Higgs E.A. The Biology of Nitric Oxide. Part 5:1996;126 Portland Press, London.
39. Kluge I., Gutteck-Amsler U., Zollinger M., Do K.Q. S-nitrosoglutathione in rat cerebellum: identification and quantification by liquid chromatography-mass spectrometry. J. Neurochem. 69:1997;2599-2607.
40. Lau K.S., So K.F., Tay D., Leung M.C. NADPH-diaphorase neurons in the retina of the hamster. J. Comp. Neurol. 350:1994;550-558.
41. Lei S.Z., Pan Z.-H., Aggarwal S.K., Chen H.-S.V., Hartman J., Sucher N.J., Lipton S.A. Effect of nitric oxide production on the redox modulatory site of the NMDA receptor-channel complex. Neuron. 8:1992;1087-1099.
42. Leifer D., Lipton S.A., Barnstable C.J., Masland R.H. Monoclonal antibody to Thy-1 enhances regeneration of processes by rat retinal ganglion cells in culture. Science. 224:1984;303-306.
43. Liepe B.A., Stone C., Koistinaho J., Copenhagen D.R. Nitric oxide synthase in Müller cells and neurons of salamander and fish retina. J. Neurosci. 14:1994;7641-7654.
44. Lingren C.A., Laird M.V. Nitroprusside inhibits neurotransmitter release at the frog neuromuscular junction. NeuroReport. 5:1994;2205-2208.
45. Lipton S.A., Choi Y.-B., Pan Z.-H., Lei S.Z., Chen H.-S.V., Sucher N.J., Loscalzo J., Singel D.J., Stamler J.S. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature. 364:1993;626-632.
46. Lipton S.A., Stamler J.S. Actions of redox-related congeners of nitric oxide at the NMDA receptor. Neuropharmacology. 33:1994;1229-1233.
47. Lipton S.A., Tauck D.L. Voltage-dependent conductances of solitary ganglion cells dissociated from the rat retina. J. Physiol. (London). 385:1987;361-391.
48. Manzoni O., Prezeau L., Marin P., Deshager S., Bockaert J., Fagni L. Nitric oxide-induced blockade of NMDA receptors. Neuron. 8:1992;653-662.
49. ·NO with nucleophiles as agents for the controlled biological release of nitric oxide. Vasorelaxant effects. J. Med. Chem. 34:1991;3242-3247.
50. Marla S.S., Lee J., Groves J.T. Peroxynitrite rapidly permeates phospholipid membranes. Proc. Natl. Acad. Sci. U.S.A. 94:1997;14243-14248.
51. Meffert M.K., Calakos N.C., Scheller R.H., Schulman H. Nitric oxide modulates synaptic vesicle docking/fusion reactions. Neuron. 16:1996;1229-1236.
52. 2+-independent synaptic vesicle release. Neuron. 12:1994;1235-1244.
53. Meyer-Franke A., Kaplan M.R., Pfieger F.W., Barres B.A. Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron. 15:1995;805-819.
54. Moncada S., Higgs A. The L-arginine-nitric oxide pathway. N. Engl. J. Med. 329:1993;2002-2012.
55. Montague P.R., Gancayco C.D., Winn M.J., Marchase R.B., Friedlander M.J. Role of NO production in NMDA receptor-mediated neurotransmitter release in cerebral cortex. Science. 263:1994;973-977.
56. Murphy K.P.S.J., Williams J.H., Bettache N., Bliss T.V.P. Photolytic release of nitric oxide modulates NMDA receptor-mediated transmission but does not induce long-term potentiation at hippocampal synapses. Neuropharmacology. 33:1994;1375-1385.
57. O'Dell T.J., Hawkins R.D., Kandel E.R., Arancio O. Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger. Proc. Natl. Acad. Sci. U.S.A. 88:1991;11285-11289.
58. Osborne N.N., Barnett N.L., Herrera A.J. NADPH diaphorase localization and nitric oxide synthetase activity in the retina and anterior uvea of the rabbit eye. Brain Res. 610:1993;194-198.
59. Pan Z.-H., Segal M.M., Lipton S.A. Nitric oxide-related species inhibit evoked neurotransmission but enhance spontaneous miniature synaptic currents in central neuronal cultures. Proc. Natl. Acad. Sci. U.S.A. 93:1996;15234-15428.
60. Peunova N., Enikolopov G. Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature. 375:1995;68-73.
61. Radi R., Beckman J.S., Bush K.M., Freeman B.A. Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J. Biol. Chem. 266:1991;4244-4250.
62. 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.
63. Samdani A.F., Newcamp C., Resink A., Facchinetti F., Hoffman B.E., Dawson V.L., Dawson T.M. Differential susceptibility to neurotoxicity mediated by neurotrophins and neuronal nitric oxide synthase. J. Neurosci. 17:1997;4633-4641.
64. ·NO from NO synthase. Proc. Natl. Acad. Sci. U.S.A. 93:1996;14492-14497.
65. Schuman E.M., Madison D.V. A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science. 254:1991;1503-1506.
66. Schuman E.M., Madison D.V. Locally distributed synaptic potentiation in the hippocampus. Science. 263:1994;532-536.
67. Shen S., Wiemelt A.P., McMorris F.A., Barres B.A. Retinal ganglion cells lose trophic responsiveness after axotomy. Neuron. 23:1999;285-295.
68. Son H., Hawkins R.D., Martin K., Kiebler M., Huang P.L., Fishman M.C., Kandel E.R. Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell. 87:1996;1015-1023.
69. Song H.-J., Ming G.-L., He Z., Lehmann M., McKerracher L., Tessier-Lavigne M., Poo M.-M. Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science. 281:1998;1515-1518.
70. Stamler J.S. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell. 78:1994;931-936.
71. Stamler J.S., Hausladen A. Oxidative modifications in nitrosative stress. Nature Struc. Biol. 5:1998;247-249.
72. Stamler J.S., Jia L., Eu J.P., McMahon T.J., Demchenko I.T., Bonaventura J., Gernert K., Piantadosi C.A. Blood flow regulation by S-nitroso-hemoglobin in the physiological oxygen gradient. Science. 276:1997;2034-2037.
73. Stamler J.S., Simon D.I., Osborne J.A., Mullins M.E., Jaraki O., Michel T., Singel D.J., Loscalzo J. S-nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compounds. Proc. Natl. Acad. Sci. U.S.A. 89:1992;444-448.
74. Stamler J.S., Singel D.J., Loscalzo J. Biochemistry of nitric oxide and its redox activated forms. Science. 258:1992;1898-1902.
75. Stamler J.S., Toone E.J., Lipton S.A., Sucher N.J. (S)NO signals: Translocation, regulation, and a consensus motif. Neuron. 18:1997;691-696.
76. Tenneti L., D'Emilia D.M., Lipton S.A. Suppression of neuronal apoptosis by S-nitrosylation of caspases. Neurosci. Lett. 236:1997;139-142.
77. Vaccaro T.M., Cobcroft M.D., Provis J.M., Mitrofanis J. NADPH-diaphorase reactivity in adult and developing cat retinae. Cell. Tissue Res. 265:1991;371-379.
78. Van Wagenen S., Rehder V. Regulation of neuronal growth cone filopodia by nitric oxide. J. Neurobiol. 39:1999;168-185.
79. Wang T., Xie Z., Lu B. Nitric oxide mediates activity-dependent synaptic depression at developing neuromuscular synapses. Nature. 374:1995;262-266.
80. Wang X., Robinson P.J. Cyclic GMP-dependent protein kinase and cellular signaling in the nervous system. J. Neurochem. 68:1997;443-456.
81. Wässle H., Chun M.H., Müller F. Amacrine cells in the ganglion cell layer in the cat retina. J. Comp. Neurol. 265:1987;391-408.
82. Wayne D.B., Bonaventura J., Sheetz M.P. Nitric oxide (NO) regulation of neuronal growth cone motility. Soc. Neurosci. Abstr. 19:1993;620.
83. Wu H.H., Williams C.V., McLoon S.L. Involvement of nitric oxide in the elimination of a transient retinotectal projection in development. Science. 265:1994;1593-1596.
84. Xia Y., Dawson V.L., Dawson T.M., Snyder S.H., Zweier J.L. Nitric oxide synthase generates superoxide and nitric oxide in arginine-depleted cells leading to peroxynitrite-mediated cellular injury. Proc. Natl. Acad. Sci. U.S.A. 93:1996;6770-6774.
85. Xia Y., Zweier J.L. Superoxide and peroxynitrite generation from inducible nitric oxide synthase in macrophages. Proc. Natl. Acad. Sci. U.S.A. 94:1997;6954-6958.
86. Xiong H., Yamada K., Han D., Nabeshima T., Enikolopov G., Carnahan J., Nawa H. Mutual regulation between the intercellular messengers nitric oxide and brain-derived neurotrophic factor in rodent neocortical neurons. Eur. J. Neurosci. 11:1999;1567-1576.
87. Yamamoto R., Bredt D.S., Snyder S.H., Stone R.A. The localization of nitric oxide synthase in the rat eye and related cranial ganglia. Neuroscience. 54:1993;189-200.
88. Zhuo M., Kandel E.R., Hawkins R.D. Nitric oxide and cGMP produce either synaptic depression or potentiation depending on the frequency of presynaptic stimulation in the hippocampus. NeuroReport. 5:1994;1033-1036.