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Journal of Neuroscience, Vol 13, 2651-2661, Copyright © 1993 by Society for Neuroscience

ARTICLE

Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures

VL Dawson, TM Dawson, DA Bartley, GR Uhl and SH Snyder
National Institute on Drug Abuse, Addiction Research Center, Laboratory of Molecular Neurobiology, Baltimore, Maryland 21224.

In addition to mediating several physiological functions, nitric oxide (NO) has been implicated in the cytotoxicities observed following activation of macrophages or excess stimulation of neurons by glutamate. We extend our previous observations of glutamate-stimulated, NO-mediated neurotoxicity in primary cultures of rat fetal cortical, striatal, and hippocampal neurons. Neurotoxicity elicited by either NMDA or sodium nitroprusside (SNP) exhibits a similar concentration- effect relationship and time course. The concentration-effect curve of NMDA-induced neurotoxicity is shifted to the right in the presence of nitro-L-arginine and farther to the right in arginine-free media. The rank order of potency of several NO synthase (NOS) inhibitors in preventing neurotoxicity is the same as the rank order of these compounds in inhibiting NOS, and this inhibition is stereospecific. NMDA neurotoxicity is also prevented by flavoprotein inhibitors and calmodulin inhibitors, fitting with the roles of flavoproteins and calmodulin as NOS regulators. 8-Bromo-cGMP and guanylyl cyclase inhibitors do not affect neurotoxicity, while superoxide dismutase attenuates neurotoxicity. NOS neurons appear to be the source of neurotoxic NO in culture, as lesions of these neurons with 20 microM quisqualate diminish subsequent NMDA neurotoxicity. Moreover, NMDA neurotoxicity develops over time in culture coincident with the expression of NOS. Immunohistochemical localization of NOS in cultures and intact brain demonstrates widespread distribution of the cell processes suggesting that NOS neurons contact the majority of cortical neurons and so could mediate widespread neurotoxicity.


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Measurement of Nitric Oxide and Peroxynitrite Generation in the Postischemic Heart. EVIDENCE FOR PEROXYNITRITE-MEDIATED REPERFUSION INJURY
J. Biol. Chem., November 15, 1996; 271(46): 29223 - 29230.
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M. V. Brock, M. E. Blue, C. J. Lowenstein, F. A. Northington, M. S. Lange, M. V. Johnston, and W. A. Baumgartner
Induction of Neuronal Nitric Oxide After Hypothermic Circulatory Arrest
Ann. Thorac. Surg., November 1, 1996; 62(5): 1313 - 1320.
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R. J. White and I. J. Reynolds
Mitochondrial Depolarization in Glutamate-Stimulated Neurons: An Early Signal Specific to Excitotoxin Exposure
J. Neurosci., September 15, 1996; 16(18): 5688 - 5697.
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T. Hiramatsu, R. A. Jonas, T. Miura, A. duPlessis, M. Tanji, J. M. Forbess, and D. Holtzman
CEREBRAL METABOLIC RECOVERY FROM DEEP HYPOTHERMIC CIRCULATORY ARREST AFTER TREATMENT WITH ARGININE AND NITRO-ARGININE METHYL ESTER
J. Thorac. Cardiovasc. Surg., September 1, 1996; 112(3): 698 - 707.
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J. Aronowski, R. Strong, J.C. Grotta, and H. A. Kontos
Combined Neuroprotection and Reperfusion Therapy for Stroke: Effect of Lubeluzole and Diaspirin Cross-Linked Hemoglobin in Experimental Focal Ischemia
Stroke, September 1, 1996; 27(9): 1571 - 1577.
[Abstract] [Full Text]

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S. J. Hewett, J. K. Muir, D. Lobner, A. Symons, D. W. Choi, M. A. Moskowitz, and C. Ayata
Potentiation of Oxygen-Glucose Deprivation–Induced Neuronal Death After Induction of iNOS
Stroke, September 1, 1996; 27(9): 1586 - 1591.
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P. J. L. M. Strijbos, M. J. Leach, and J. Garthwaite
Vicious Cycle Involving Na+ Channels, Glutamate Release, and NMDA Receptors Mediates Delayed Neurodegeneration through Nitric Oxide Formation
J. Neurosci., August 15, 1996; 16(16): 5004 - 5013.
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K. M. Cockroft, M. Meistrell III, G. A. Zimmerman, D. Risucci, O. Bloom, A. Cerami, K. J. Tracey, and G. Feuerstein
Cerebroprotective Effects of Aminoguanidine in a Rodent Model of Stroke
Stroke, August 1, 1996; 27(8): 1393 - 1398.
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P. H. Chan
Role of Oxidants in Ischemic Brain Damage
Stroke, June 1, 1996; 27(6): 1124 - 1129.
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D. Trotti, D. Rossi, O. Gjesdal, L. M. Levy, G. Racagni, N. C. Danbolt, and A. Volterra
Peroxynitrite Inhibits Glutamate Transporter Subtypes
J. Biol. Chem., March 15, 1996; 271(11): 5976 - 5979.
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J. I. Simpson, T. R. Eide, G. A. Schiff, S. B. Newman, J. F. Clagnaz, I. Hossain, S. B. Schulman, and J. E. Gropper
Effect of Nitroglycerin on Spinal Cord Ischemia After Thoracic Aortic Cross-Clamping
Ann. Thorac. Surg., January 1, 1996; 61(1): 113 - 117.
[Abstract] [Full Text]

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K.-W. Yoon, H. L. Mitchell, L. D. Broder, R. W. Brooker, and R. K. Delisle
Trauma-Induced Neurotoxicity in Rat Hippocampal Neurons
Stroke, January 1, 1996; 27(1): 122 - 126.
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M. Colasanti, T. Persichini, M. Menegazzi, S. Mariotto, E. Giordano, C. M. Caldarera, V. Sogos, G. M. Lauro, and H. Suzuki
Induction of Nitric Oxide Synthase mRNA Expression
J. Biol. Chem., November 10, 1995; 270(45): 26731 - 26733.
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A. Bhardwaj, F. J. Northington, R. C. Koehler, T. Stiefel, D. F. Hanley, and R. J. Traystman
Adenosine Modulates N-Methyl-D-Aspartate–Stimulated Hippocampal Nitric Oxide Production In Vivo
Stroke, September 1, 1995; 26(9): 1627 - 1633.
[Abstract] [Full Text]

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H. Wakita, H. Tomimoto, I. Akiguchi, and J. Kimura
Protective Effect of Cyclosporin A on White Matter Changes in the Rat Brain After Chronic Cerebral Hypoperfusion
Stroke, August 1, 1995; 26(8): 1415 - 1422.
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K. Abe, M. Aoki, J. Kawagoe, T. Yoshida, A. Hattori, K. Kogure, and Y. Itoyama
Ischemic Delayed Neuronal Death : A Mitochondrial Hypothesis
Stroke, August 1, 1995; 26(8): 1478 - 1489.
[Abstract] [Full Text]

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 NeuroscientistHome page
T. M. Dawson and V. L. Dawson
REVIEW {blacksquare} : Nitric Oxide: Actions and Pathological Roles
Neuroscientist, January 1, 1995; 1(1): 7 - 18.
[Abstract] [PDF]

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 ScienceHome page
Z Huang, P. Huang, N Panahian, T Dalkara, M. Fishman, and M. Moskowitz
Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase
Science, September 23, 1994; 265(5180): 1883 - 1885.
[Abstract] [PDF]

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 ScienceHome page
P. Montague, C. Gancayco, M. Winn, R. Marchase, and M. Friedlander
Role of NO production in NMDA receptor-mediated neurotransmitter release in cerebral cortex
Science, February 18, 1994; 263(5149): 973 - 977.
[Abstract] [PDF]

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 ScienceHome page
J Zhang, V. Dawson, T. Dawson, and S. Snyder
Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity
Science, February 4, 1994; 263(5147): 687 - 689.
[Abstract] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
T. Kume, N. Asai, H. Nishikawa, N. Mano, T. Terauchi, R. Taguchi, H. Shirakawa, F. Osakada, H. Mori, N. Asakawa, et al.
Isolation of a diterpenoid substance with potent neuroprotective activity from fetal calf serum
PNAS, March 5, 2002; 99(5): 3288 - 3293.
[Abstract] [Full Text] [PDF]


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