Inducible nitric oxide synthase is an endogenous neuroprotectant after traumatic brain injury in rats and mice

Journal of Clinical Investigation

Volumn 104, Issue 5, 1999, Pages 647-656

  Sinz, Elizabeth H ^a,b   Kochanek, Patrick M ^a,b   Dixon, C Edward ^a,b   Clark, Robert S B ^a,b   Carcillo, Joseph A ^a   Schiding, Joanne K ^a,b   Chen, Minzhi ^a   Wisniewski, Stephen R ^c   Carlos, Timothy M ^a   Williams, Debra ^d   DeKosky, Steven T ^a   Watkins, Simon C ^a   Marion, Donald W ^a,b   Billiar, Timothy R ^d  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOGUANIDINE; N IMINOETHYLLYSINE; NEUROPROTECTIVE AGENT; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; ENZYME INDUCTION; HISTOPATHOLOGY; HYPOXEMIA; KNOCKOUT MOUSE; MAZE TEST; MOTOR PERFORMANCE; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0032728075     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI6670     Document Type: Article

References (74)

1. Lassmann, H. 1997. Basic mechanisms of brain inflammation. J. Neural Transm. Suppl. 50:183-190.
2. McGeer, P.L., and McGeer, E.G. 1995. The inflammatory response system of brain: implications for therapy of Alzheimer and other neurodegenerative diseases. Brain Res. Brain Res. Rev. 21:195-218.
3. Pfister, H.W., and Scheld, W. 1997. Brain injury in bacterial meningitis: therapeutic implications. Curr. Opin. Neurol. 10:254-259.
4. Feuerstein, G.Z., Wang, X., and Barone, F.C. 1997. Inflammatory gene expression in cerebral ischemia and trauma. Potential new therapeutic targets. Ann. NY Acad. Sci. 825:179-193.
5. Hallenbeck, J.M. 1996. Significance of the inflammatory response in brain ischemia. Acta Neurochir. Suppl. 66:27-31.
6. Mattson, M.P., and Scheff, S.W. 1994. Endogenous neuroprotection factors and traumatic brain injury: mechanisms of action and implications for therapy. J. Neurotrauma. 11:3-33.
7. Bruce, A.J., et al. 1996. Altered neuronal and microglial responses to excitotoxic and ischemic brain injury in mice lacking TNF receptors. Nat. Med. 2:788-794.
8. Cheng, B., Christakos, S., and Mattson, M.P. 1994. Tumor necrosis factors protect neurons against metabolic-excitotoxic insults and promote maintenance of calcium homeostasis. Neuron. 12:139-153.
9. DeKosky, S.T., et al. 1996. Interleukin-1 receptor antagonist suppresses neurotrophin response in injured rat brain. Ann. Neurol. 39:123-127.
10. Mattson, M.P., Goodman, Y., Luo, H., Fu, W., and Furukawa, K. 1997. Activation of NF-kappaB protects hippocampal neurons against oxidative stress-induced apoptosis: evidence for induction of manganese superoxide dismutase and suppression of peroxynitrite production and protein tyrosine nitration. J. Neurosci. Res. 49:681-697.
11. Brown, G.C. 1997. Nitric oxide inhibition of cytochrome oxidase and mitochondrial respiration: implications for inflammatory, neurodegenerative and ischaemic pathologies. Mol Cell. Biochem. 174:189-192.
12. Holscher, C. 1997. Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity. Trends Neurosci. 20:298-303.
13. Bredt, D.S., Hwang, P.M., and Snyder, S.H. 1990. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature. 347:768-770.
14. Iadecola, C., Zhang, F., Xu, S., Casey, R., and Ross, M.E. 1995. Inducible nitric oxide synthase gene expression in brain following cerebral ischemia. J. Cereb. Blood Flow Metab. 15:378-384.
15. Iadecola, C., Zhang, F., Casey, R., Nagayama, M., and Ross, M.E. 1997. Delayed reduction of ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene. J. Neurosci. 17:9157-9164.
16. Lipton, S.A., et al. 1993. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature. 364:626-632.
17. Ding, M., Wong, J.L., Rogers, N.E., Ignarro, L.J., and Voskuhl, R.R. 1997. Gender differences of inducible nitric oxide production in SJL/J mice with experimental autoimmune encephalomyelitis. J. Neuroimmunol. 77:99-106.
18. Campbell, I.L. 1996. Exacerbation of lymphocytic choriomeningitis in mice treated with the inducible nitric oxide synthase inhibitor aminoguanidine. J. Neuroimmunol. 71:31-36.
19. DeWitt, D.S., et al. 1997. L-arginine and superoxide dismutase prevent or reverse cerebral hypoperfusion after fluid-percussion traumatic brain injury. J. Neurotrauma. 14:223-233.
20. Huang, Z., et al. 1996. Enlarged infarcts in endothelial nitric oxide synthase knockout mice are attenuated by nitro-L-arginine. J. Cereb. Blood Flow Metab. 16:981-998.
21. Huang, Z., et al. 1994. Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science. 265:1883-1885.
22. Schulz, J.B., et al. 1995. Blockade of neuronal nitric oxide synthase protects against excitotoxicity in vivo. J. Neurosci. 15:8419-8429.
23. Yoshida, T., Limmroth, V., Irikura, K., and Moskowitz, M.A. 1994. The NOS inhibitor, 7-nitroindazole, decreases focal infarct volume but not the response to topical acetylcholine in pial vessels. J. Cereb. Blood Flow Metab. 14:924-929.
24. Billiar, T.R. 1995. Nitric oxide. Novel biology with clinical relevance. Ann. Surg. 221:339-349.
25. Taylor, B.S., et al. 1998. Multiple NF-kappaB enhancer elements regulate cytokine induction of the human inducible nitric oxide synthase gene. J. Biol. Chem. 273:15148-15156.
26. Clark, R.S., et al. 1996. Inducible nitric oxide synthase expression in cerebrovascular smooth muscle and neucrophils after traumatic brain injury in immature rats. Pediatr. Res. 39:784-790.
27. D'Ambrosio, R., Maris, D.O., Grady, M.S., Winn, H.R., and Janigro, D. 1998. Selective loss of hippocampal long-term potentiation, but not depression, following fluid percussion injury. Brain Res. 786:64-79.
28. Iadecola, C., Zhang, F., and Xu, X. 1995. Inhibition of nitric oxide synthase ameliorates cerebral ischemic damage. Am. J. Physiol. 268:R286-R292.
29. Cockroft, K.M., et al. 1996. Cerebroprotective effects of aminoguanidine in a rodent model of stroke. Stroke. 27:1393-1398.
30. Zhang, F., Casey, R.M., Ross, M.E., and Iadecola, C. 1996. Aminoguanidine ameliorates and L-arginine worsens brain damage from intraluminal middle cerebral artery occlusion. Stroke. 27:317-323.
31. Fenyk-Melody, J.E., et al. 1998. Experimental autoimmune encephalomyelitis is exacerbated in mice lacking the nitric oxide synthase 2 gene. J. Immunol. 160:2940-2946.
32. Sahrbacher, U.C., et al. 1998. Mice with an inactivation of the inducible nitric oxide synthase gene are susceptible to experimental autoimmune encephalomyelitis. Eur. J. Immunol. 28:1332-1338.
33. Clark, R.S.B., et al. 1997. Early neuropathologic effects of mild or moderate hypoxemia after controlled cortical impact injury in rats. J. Neurotrauma. 14:179-189.
34. Dixon, C.E., Clifton, G.L., Lighthall, J.W., Yaghamai, A.A., and Hayes, R.L. 1991. A controlled cortical impact model of traumatic brain injury in the rat. J. Neurosci. Methods. 39:253-262.
35. Kochanek, P.M., et al. 1995. Severe controlled cortical impact in rats: assessment of cerebral edema, blood flow, and contusion volume. J. Neurotrauma. 12:1015-1025.
36. Clark, R.S.B., et al. 1997. Apoptosis-suppressor gene bcl-2 expression after traumatic brain injury in rats. J. Neurosci. 17:9172-9182.
37. Smith, D.H., et al. 1995. A model of parasagittal controlled cortical impact in the mouse: cognitive and histopathologic effects. J. Neurotrauma. 12:169-178.
38. Whalen, M.J., et al. 1999. Effect of traumatic brain injury in mice deficient in intercellular adhesion molecule-1: assessment of histopathologic and functional outcome. J. Neurotrauma. 16:299-309.
39. 32P-labeled PCR/Southern blotting technique in quantitative analysis of human and rat mRNA. PCR Methods Appl. 3:292-297.
40. Dixon, C.E., et al. 1987. A fluid percussion model of experimental brain injury in the rat. J. Neurosurg. 67:110-119.
41. Feeney, D.M., Gonzalez, A., and Law, W.A. 1982. Amphetamine, haloperiodol, and experience interact to affect rate of recovery after motor cortex injury. Science. 217:855-857.
42. Hall, E.D., Yonkers, P.A., McCall, J.M., and Braughler, J.M. 1988. Effects of the 21-aminosteroid U74006F on experimental head injury in mice. J. Neurosurg. 68:456-461.
43. Southan, G.J., and Szabo, C. 1996. Selective pharmacological inhibition of distinct nitric oxide synthase isoforms. Biochem. Pharmacol. 51:383-394.
44. Moore, W.M., et al. 1994. L-N6-(1-iminoethyl) lysine: a selective inhibitor of inducible nitric oxide synthase. J. Med. Chem. 37:3886-3888.
45. Wray, G.M., Millar, C.G., Hinds, C.J., and Thiemermann, C. 1998. Selective inhibition of the activity of inducible nitric oxide synthase prevents the circulatory failure, but not the organ injury/dysfunction, caused by endotoxin. Shock. 9:329-335.
46. Dinerman, J.L., Dawson, T.M., Schell, M.J., Snowman, A., and Snyder, S.H. 1994. Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: implications for synaptic plasticity. Proc. Natl. Acad. Sci. USA. 91:4214-4218.
47. Kantor, D.B., et al. 1996. A role for endothelial NO synthase in LTP revealed by adenovirus-mediated inhibition and rescue. Science. 274:1744-1748.
48. O'Dell, T.J., et al. 1994. Endothelial NOS and the blockade of LTP by NOS inhibitors in mice lacking neuronal NOS. Science. 265:542-546.
49. Banbury Conference on Genetic Background in Mice. 1997. Mutant mice and neuroscience: recommendation concerning genetic background. Neuron. 19:755-759.
50. Iadecola, C., Zhang, F., Casey, R., Clark, H.B., and Ross, M.E. 1996. Inducible nitric oxide synthase gene expression in vascular cells after transient focal cerebral ischemia. Stroke. 27:1373-1380.
51. Bryk, R., and Wolff, D.J. 1998. Mechanism of inducible nitric oxide synthase inactivation by aminoguanidine and L-N6-(1-iminoethyl) lysine. Biochemistry. 37:4844-4852.
52. Okuda, Y., Sakoda, S., Fujimura, H., and Yanagihara, T. 1998. Aminoguanidine, a selective inhibitor of the inducible nitric oxide synthase, has different effects of experimental allergic encephalomyelitis in the induction and progression phase. J. Neuroimmunol. 81:201-210.
53. Shohami, E., Bass, R., Wallach, D., Yamin, A., and Gallily, R. 1996. Inhibition of tumor necrosis factor alpha (TNF alpha) activity in rat brain is associated with cerebroprotection after closed head injury. J. Cereb. Blood Flow Metab. 16:378-384.
54. Scherbel, U., Raghupathi, R., Nakamura, M., Saatman, K., and McIntosh, T.K. 1997. Evaluation of neurobehavioral deficits in brain-injured tumor necrosis factor-deficient (TNF-/-) mice after experimental brain injury. J. Neurotrauma. 14:781.
55. Wada, K., Chatzipanteli, K., Kraydieh, S., Busto, R., and Dietrich, W.D. 1998. Inducible nitric oxide synthase expression after traumatic brain injury and neuroprotection with aminoguanidine treatment in rats. Neurosurgery. 43:1427-1436.
56. Stoffel, M., Rinecker, M., Plesnila, N., Eriskat, J., and Baethmann, A. 1999. Attenuation of secondary lesion growth of the brain after trauma by selective inhibition of the inducible no-synthase. Proceedings of the Eleventh International Symposium of Brain Oedema and Mechanisms of Cellular Injury. 62. (Abstr.)
57. McIntosh, T.K. 1993. Novel pharmacologice therapies in the treatment of experimental traumatic brain injury: a review. J. Neurotrauma. 10:215-261.
58. Kim, Y.M., Talanian, R.V., and Billiar, T.R. 1997. Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J. Biol. Chem. 272:31138-31148.
59. Tzeng, E., et al. 1997. Adenoviral transfer of the inducible nitric oxide synthase gene blocks endothelial cell apoptosis. Surgery. 122:255-263.
60. Estévez, A.G., et al. 1998. Nitric oxide-dependent production of cGMP supports the survival of rat embryonic motor neurons cultured with brain-derived neurotrophic factor. J. Neurosci. 18:3708-3714.
61. Farinelli, S.E., Park, D.S., and Greene, L.A. 1996. Nitric oxide delays the death of trophic factor-deprived PC12 cells and sympathetic neurons by a cGMP-mediated mechanism. J. Neurosci. 16:2325-2334.
62. Yakovlev, A.G., et al. 1997. Activation of CPP32-like caspases contributes to neuronal apoptosis and neurological dysfunction after traumatic brain injury. J. Neurosci. 17:7415-7424.
63. MacLean, A., et al. 1998. Mice lacking inducible nitric-oxide synthase are more susceptible to herpes simples virus infection despite enhanced Th1 cell responses. J. Gen. Virol. 79:825-830.
64. Wei, X.-Q., et al. 1995. Altered immune responses in mice lacking inducible nitric oxide synthase. Nature. 375:408-411.
65. Hickey, M.J., et al. 1997. Inducible nitric oxide synthase-deficient mice have enhanced leukocyte-endothelium interactions in endotoxemia. FASEB J. 11:955-964.
66. Clark, R.S.B., Schiding, J.K., Kaczorowski, S.L., Marion, D.W., and Kochanek, P.M. 1994. Neutrophil accumulation after traumatic brain injury in rats: comparison of weight-drop and controlled cortical impact models. J. Neurotrauma. 11:499-506.
67. Hierholzer, C., et al. 1998. Essential role of induced nitric oxide in the initiation of the inflammatory response after hemorrhagic shock. J. Exp. Med. 187:917-928.
68. Brodie, C. 1996. Differential effects of Th1 and Th2 derived cytokines on NGF synthesis by mouse astrocytes. FEBS Lett. 394:117-120.
69. Brodie, C., Goldreich, N., Haiman, T., and Kazimirsky, G. 1998. Functional IL-4 receptors on mouse astrocytes: IL-4 inhibits astrocyte activation and induced NGF secretion. J. Neuroimmunol. 81:20-30.
70. Awatsuji, H., et al. 1993. Interleukin-4 and -5 as modulators of nerve growth factor synthesis/secretion in astrocytes. J. Neurosci. 34:539-545.
71. Forbes, M.L., et al. 1997. Assessment of cerebral blood flow and CO2 reactivity after controlled cortical impact by perfusion magnetic resonance imaging using arterial spin labeling in rats. J. Cereb. Blood Flow Metab. 17:865-874.
72. Yamakami, I., and McIntosh, T.K. 1991. Alterations in regional cerebral blood flow following brain injury in the rat. J. Cereb. Blood Flow Metab. 11:655-660.
73. von Stuck, S.L., Lee, S.M., Hovda, D.A., and Becker, D.P. 1996. L-arginine increases cerebral blood flow following cortical contusion injury: implications regarding vulnerability. J. Neurotrauma. 13:618.
74. Whalen, M.J., Carlos, T.M., Kochanek, P.M., and Heineman, S. 1998. Blood-brain barrier permeability, neutrophil accumulation and vascular adhesion molecule expression after controlled cortical impact in rats: a preliminary study. Acta Neurochir. Suppl. 71:212-214.