Nitric oxide synthase in hypoxic or ischemic brain injury

Reviews in the Neurosciences

Volumn 26, Issue 1, 2015, Pages 105-117

  Liu, Haiting ^a,b   Li, Jiao ^a,b   Zhao, Fengyan ^a,b   Wang, Huiqing ^a,b   Qu, Yi ^a,b   Mu, Dezhi ^a,b,c  

^a SICHUAN UNIVERSITY   (China)

^b SICHUAN UNIVERSITY   (China)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Brain injury; Hypoxia; Ischemia; Nitric oxide synthase

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

APOPTOSIS; ARTICLE; BRAIN BLOOD FLOW; BRAIN FUNCTION; DISEASE COURSE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EXCITOTOXICITY; HUMAN; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IMMUNOREACTIVITY; INFLAMMATION; MITOCHONDRIAL PERMEABILITY; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NITROSYLATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; THROMBOCYTE AGGREGATION; TRANSACTIVATION; ANIMAL; BRAIN HYPOXIA; BRAIN ISCHEMIA; ENZYMOLOGY; METABOLISM; PATHOLOGY;

ANIMALS; BRAIN ISCHEMIA; HUMANS; HYPOXIA, BRAIN; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III;

EID: 84929076288     PISSN: 03341763     EISSN: 21910200     Source Type: Journal    
DOI: 10.1515/revneuro-2014-0041     Document Type: Article

References (97)

1. Alderton, W.K., Cooper, C.E., and Knowles, R.G. (2001) Nitric oxide synthases: Structure, function and inhibition Biochem. J. 357, 593-615.
2. ArunaDevi, R., Ramteke, V.D., Kumar, S., Shukla, M.K., Jaganathan, S., Kumar, D., Sharma, A.K., and Tandan, S.K. (2010). Neuroprotective effect of s-methylisothiourea in transient focal cerebral ischemia in rat. Nitric Oxide 22, 1-10.
3. Atochin, D.N. and Huang, P.L. (2010). Endothelial nitric oxide synthase transgenic models of endothelial dysfunction. Flug. Aach. Eur. J. Phys. 460, 965-974.
4. Atochin, D.N., Wang, A., Liu, V.W., Critchlow, J.D., Dantas, A.P., Looft- Wilson, R., Murata, T., Salomone, S., Shin, H.K., Ayata, C., et al. (2007). The phosphorylation state of eNOS modulates vascular reactivity and outcome of cerebral ischemia in vivo. J. Clin. Invest. 117, 1961-1967.
5. Badamtseren, B., Odkhuu, E., Koide, N., Haque, A., Naiki, Y., Hashimoto, S., Komatsu, T., Yoshida, T., and Yokochi, T. (2011). Thalidomide inhibits interferon-gamma-mediated nitric oxide production in mouse vascular endothelial cells. Cell. Immunol. 270, 19-24.
6. Benavides, G.A., Liang, Q., Dodson, M., Darley-Usmar, V., and Zhang, J. (2013). Inhibition of autophagy and glycolysis by nitric oxide during hypoxia-reoxygenation impairs cellular bioenergetics and promotes cell death in primary neurons. Free Radic. Biol. Med. 65, 1215-1228.
7. Brown, G.C. (2010). Nitric oxide and neuronal death. Nitric Oxide 23, 153-165.
8. Brown, C.M., Dela Cruz, C.D., Yang, E., and Wise, P.M. (2008). Inducible nitric oxide synthase and estradiol exhibit complementary neuroprotective roles after ischemic brain injury. Exp. Neurol. 210, 782-787.
9. Chang, C.C., Wang, Y.H., Chern, C.M., Liou, K.T., Hou, Y.C., Peng, Y.T., and Shen, Y.C. (2011). Prodigiosin inhibits gp91(phox) and iNOS expression to protect mice against the oxidative/nitrosative brain injury induced by hypoxia-ischemia. Toxicol. Appl. Pharmacol. 257, 137-147.
10. Chao, X.D., Ma, Y.H., Luo, P., Cao, L., Lau, W.B., Zhao, B.C., Han, F., Liu, W., Ning, W.D., Su, N., et al. (2013). Up-regulation of heme oxygenase-1 attenuates brain damage after cerebral ischemia via simultaneous inhibition of superoxide production and preservation of NO bioavailability. Exp. Neurol. 239, 163-169.
11. Chen, J., Li, C., Pei, D.S., Han, D., Liu, X.M., Jiang, H.X., Wang, X.T., Guan, Q.H., Wen, X.R., Hou, X.Y., et al. (2009a). GluR6-containing KA receptor mediates the activation of p38 MAP kinase in rat hippocampal CA1 region during brain ischemia injury. Hippocampus 19, 79-89.
12. Chen, M., Sun, H.Y., Li, S.J., Das, M., Kong, J.M., and Gao, T.M. (2009b). Nitric oxide as an upstream signal of p38 mediates hypoxia/reoxygenation-induced neuronal death. Neuro-Signals 17, 162-168.
13. Chern, C.M., Liou, K.T., Wang, Y.H., Liao, J.F., Yen, J.C., and Shen, Y.C. (2011). Andrographolide inhibits PI3K/AKTdependent NOX2 and iNOS expression protecting mice against hypoxia/ischemia-induced oxidative brain injury. Planta Med. 77, 1669-1679.
14. Cheyuo, C., Wu, R., Zhou, M., Jacob, A., Coppa, G., and Wang, P. (2011). Ghrelin suppresses inflammation and neuronal nitric oxide synthase in focal cerebral ischemia via the vagus nerve. Shock 35, 258-265.
15. Corsani, L., Bizzoco, E., Pedata, F., Gianfriddo, M., Faussone- Pellegrini, M.S., and Vannucchi, M.G. (2008). Inducible nitric oxide synthase appears and is co-expressed with the neuronal isoform in interneurons of the rat hippocampus after transient ischemia induced by middle cerebral artery occlusion. Exp. Neurol. 211, 433-440.
16. Criollo, A., Senovilla, L., Authier, H., Maiuri, M.C., Morselli, E., Vitale, I., Kepp, O., Tasdemir, E., Galluzzi, L., Shen, S., et al. (2010). The IKK complex contributes to the induction of autophagy. EMBO J. 29, 619-631.
17. Danton, G.H. and Dietrich, W.D. (2003). Inflammatory mechanisms after ischemia and stroke. J. Neuropathol. Exp. Neurol. 62, 127-136.
18. Di, J.H., Li, C., Yu, H.M., Zheng, J.N., and Zhang, G.Y. (2012). nNOS downregulation attenuates neuronal apoptosis by inhibiting nNOS-GluR6 interaction and GluR6 nitrosylation in cerebral ischemic reperfusion. Biochem. Biophys. Res. Commun. 420, 594-599.
19. Doyle, K.P., Simon, R.P., and Stenzel-Poore, M.P. (2008). Mechanisms of ischemic brain damage. Neuropharmacology 55, 310-318.
20. Endres, M., Laufs, U., Liao, J.K., and Moskowitz, M.A. (2004). Targeting eNOS for stroke protection. Trends Neurosci. 27, 283-289.
21. Fang Li, Q., Xu, H., Sun, Y., Hu, R., and Jiang, H. (2012). Induction of inducible nitric oxide synthase by isoflurane post-conditioning via hypoxia inducible factor-1alpha during tolerance against ischemic neuronal injury. Brain Res. 1451, 1-9.
22. Forstermann, U. and Sessa, W.C. (2012). Nitric oxide synthases: Regulation and function. Eur. Heart J. 33, 829-837, 837a-837d.
23. Francis, S.H., Busch, J.L., Corbin, J.D., and Sibley, D. (2010). cGMPdependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action. Pharmacol. Rev. 62, 525-563.
24. Fujioka, H., Shintaku, H., Nakanishi, H., Kim, T.J., Kusuda, S., and Yamano, T. (2008). Biopterin in the acute phase of hypoxiaischemia in a neonatal pig model. Brain Dev. 30, 1-6.
25. Gardoni, F. and Di Luca, M. (2006). New targets for pharmacological intervention in the glutamatergic synapse. Eur. J. Pharmacol. 545, 2-10.
26. Gu, Z., Nakamura, T., and Lipton, S.A. (2010). Redox reactions induced by nitrosative stress mediate protein misfolding and mitochondrial dysfunction in neurodegenerative diseases. Mol. Neurobiol. 41, 55-72.
27. Guix, F.X., Uribesalgo, I., Coma, M., and Munoz, F.J. (2005). The physiology and pathophysiology of nitric oxide in the brain. Prog. Neurobiol. 76, 126-152.
28. Guner, Y.S., Ochoa, C.J., Wang, J., Zhang, X., Steinhauser, S., Stephenson, L., Grishin, A., and Upperman, J.S. (2009). Peroxynitrite- induced p38 MAPK pro-apoptotic signaling in enterocytes. Biochem. Biophys. Res. Commun. 384, 221-225.
29. Gunther, M., Al Nimer, F., Gahm, C., Piehl, F., and Mathiesen, T. (2012). iNOS-mediated secondary inflammatory response differs between rat strains following experimental brain contusion. Acta Neurochir. (Wien) 154, 689-697.
30. Hayashi, S., Osuka, K., Watanabe, Y., Yasuda, M., Takayasu, M., and Wakabayashi, T. (2011). Hypothermia enhances the colocalization of calmodulin kinase IIalpha with neuronal nitric oxide synthase in the hippocampus following cerebral ischemia. Neurosci. Lett. 505, 228-232.
31. Haynes, R.L., Folkerth, R.D., Trachtenberg, F.L., Volpe, J.J., and Kinney, H.C. (2009). Nitrosative stress and inducible nitric oxide synthase expression in periventricular leukomalacia. Acta Neuropathol. 118, 391-399.
32. Hu, Z., Bian, X., Liu, X., Zhu, Y., Zhang, X., Chen, S., Wang, K., and Wang, Y. (2013). Honokiol protects brain against ischemiareperfusion injury in rats through disrupting PSD95-nNOS interaction. Brain Res. 1491, 204-212.
33. Hua, Q., Zhu, X., Li, P., Tang, H., Cai, D., Xu, Y., Jia, X., Chen, J., and Shen, Y. (2008). Refined Qing Kai Ling, traditional Chinese medicinal preparation, reduces ischemic stroke-induced infarct size and neurological deficits and increases expression of endothelial nitric oxide synthase. Biol. Pharm. Bull. 31, 633-637.
34. Ignarro, L.J., Buga, G.M., Wood, K.S., Byrns, R.E., and Chaudhuri, G. (1987). Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. USA 84, 9265-9269.
35. Ito, Y., Ohkubo, T., Asano, Y., Hattori, K., Shimazu, T., Yamazato, M., Nagoya, H., Kato, Y., and Araki, N. (2010). Nitric oxide production during cerebral ischemia and reperfusion in eNOS- and nNOS-knockout mice. Curr. Neurovasc. Res. 7, 23-31.
36. Jekabsone, A., Neher, J.J., Borutaite, V., and Brown, G.C. (2007). Nitric oxide from neuronal nitric oxide synthase sensitises neurons to hypoxia-induced death via competitive inhibition of cytochrome oxidase. J. Neurochem. 103, 346-356.
37. Ji, H., Tan, S., Igarashi, J., Li, H., Derrick, M., Martasek, P., Roman, L.J., Vasquez-Vivar, J., Poulos, T.L., and Silverman, R.B. (2009). Selective neuronal nitric oxide synthase inhibitors and the prevention of cerebral palsy. Ann. Neurol. 65, 209-217.
38. Jung, J., Na, C., and Huh, Y. (2012). Alterations in nitric oxide synthase in the aged CNS. Oxid. Med. Cell. Longev. 2012, 718976.
39. Kim, S.F., Huri, D.A., and Snyder, S.H. (2005). Inducible nitric oxide synthase binds, S-nitrosylates, and activates cyclooxygenase- 2. Science 310, 1966-1970.
40. Kleinert, H., Pautz, A., Linker, K., and Schwarz, P.M. (2004). Regulation of the expression of inducible nitric oxide synthase. Eur. J. Pharmacol. 500, 255-266.
41. Koh, P.O. (2008). Melatonin regulates nitric oxide synthase expression in ischemic brain injury. J. Vet. Med. Sci. 70, 747-750.
42. Kunz, A., Abe, T., Hochrainer, K., Shimamura, M., Anrather, J., Racchumi, G., Zhou, P., and Iadecola, C. (2008). Nuclear factor-kappaB activation and postischemic inflammation are suppressed in CD36-null mice after middle cerebral artery occlusion. J. Neurosci. 28, 1649-1658.
43. Lee, J.J., Cho, Y.W., Huh, Y., Cha, C.I., and Yeo, S.G. (2008). Effect of nitric oxide on auditory cortical neurons of aged rats. Neurosci. Lett. 447, 37-41.
44. Leppanen, T., Korhonen, R., Laavola, M., Nieminen, R., Tuominen, R.K., and Moilanen, E. (2013). Down-regulation of protein kinase Cdelta inhibits inducible nitric oxide synthase expression through IRF1. PloS One 8, e52741.
45. Li, L., Qu, Y., Mao, M., Xiong, Y., and Mu, D. (2008a). The involvement of phosphoinositid 3-kinase/Akt pathway in the activation of hypoxia-inducible factor-1alpha in the developing rat brain after hypoxia-ischemia. Brain Res. 1197, 152-158.
46. Li, L., Xiong, Y., Qu, Y., Mao, M., Mu, W., Wang, H., and Mu, D. (2008b). The requirement of extracellular signal-related protein kinase pathway in the activation of hypoxia inducible factor 1 alpha in the developing rat brain after hypoxia-ischemia. Acta Neuropathol. 115, 297-303.
47. Li, Q.F., Zhu, Y.S., and Jiang, H. (2008c). Isoflurane preconditioning activates HIF-1alpha, iNOS and Erk1/2 and protects against oxygen-glucose deprivation neuronal injury. Brain Res. 1245, 26-35.
48. Li, S., Wang, W., Wang, C., and Tang, Y.Y. (2010). Possible involvement of NO/NOS signaling in hippocampal amyloid-beta production induced by transient focal cerebral ischemia in aged rats. Neurosci. Lett. 470, 106-110.
49. Li, H., Liu, B., Huang, J., Chen, H., Guo, X., and Yuan, Z. (2013a). Insulin inhibits lipopolysaccharide-induced nitric oxide synthase expression in rat primary astrocytes. Brain Res. 1506, 1-11.
50. Li, L.L., Ginet, V., Liu, X., Vergun, O., Tuittila, M., Mathieu, M., Bonny, C., Puyal, J., Truttmann, A.C., and Courtney, M.J. (2013b). The nNOS-p38MAPK pathway is mediated by NOS1AP during neuronal death. J. Neurosci. 33, 8185-8201.
51. Lin, H.Y., Wu, C.L., and Huang, C.C. (2010). The Akt-endothelial nitric oxide synthase pathway in lipopolysaccharide preconditioning- induced hypoxic-ischemic tolerance in the neonatal rat brain. Stroke 41, 1543-1551.
52. Liu, Y., Zou, L.P., and Du, J.B. (2011). Nitric oxide-mediated neuronal functional recovery in hypoxic-ischemic brain damaged rats subjected to electrical stimulation. Brain Res. 1383, 324-328.
53. Liu, H., Liu, X., Wei, X., Chen, L., Xiang, Y., Yi, F., and Zhang, X. (2012). Losartan, an angiotensin II type 1 receptor blocker, ameliorates cerebral ischemia-reperfusion injury via PI3K/Aktmediated eNOS phosphorylation. Brain Res. Bull. 89, 65-70.
54. Liu, D.H., Yuan, F.G., Hu, S.Q., Diao, F., Wu, Y.P., Zong, Y.Y., Song, T., Li, C., and Zhang, G.Y. (2013). Endogenous nitric oxide induces activation of apoptosis signal-regulating kinase 1 via S-nitrosylation in rat hippocampus during cerebral ischemia-reperfusion. Neuroscience 229, 36-48.
55. Llansola, M. and Felipo, V. (2010). Metabotropic glutamate receptor 5, but not 1, modulates NMDA receptor-mediated activation of neuronal nitric oxide synthase. Neurochem. Int. 56, 535-545.
56. Lopez-Arenas, E., Mackay-Sim, A., Bacigalupo, J., and Sulz, L. (2012). Leukaemia inhibitory factor stimulates proliferation of olfactory neuronal progenitors via inducible nitric oxide synthase. PloS One 7, e45018.
57. Martinez-Ruiz, A., Cadenas, S., and Lamas, S. (2011). Nitric oxide signaling: Classical, less classical, and nonclassical mechanisms. Free Radic. Biol. Med. 51, 17-29.
58. Mishra, O.P., Randis, T., Ashraf, Q.M., and Delivoria-Papadopoulos, M. (2006). Hypoxia-induced Bax and Bcl-2 protein expression, caspase-9 activation, DNA fragmentation, and lipid peroxidation in mitochondria of the cerebral cortex of newborn piglets: The role of nitric oxide. Neuroscience 141, 1339-1349.
59. Mungrue, I.N. and Bredt, D.S. (2004). nNOS at a glance: Implications for brain and brawn. J. Cell. Sci. 117, 2627-2629.
60. Nishimura, M., Izumiya, Y., Higuchi, A., Shibata, R., Qiu, J., Kudo, C., Shin, H.K., Moskowitz, M.A., and Ouchi, N. (2008). Adiponectin prevents cerebral ischemic injury through endothelial nitric oxide synthase dependent mechanisms. Circulation 117, 216-223.
61. Oh, Y.T., Lee, J.Y., Lee, J., Lee, J.H., Kim, J.E., Ha, J., and Kang, I. (2010). Oleamide suppresses lipopolysaccharide-induced expression of iNOS and COX-2 through inhibition of NF-kappaB activation in BV2 murine microglial cells. Neurosci. Lett. 474, 148-153.
62. Park, E.M., Cho, S., Frys, K.A., Glickstein, S.B., Zhou, P., Anrather, J., Ross, M.E., and Iadecola, C. (2006). Inducible nitric oxide synthase contributes to gender differences in ischemic brain injury. J. Cereb. Blood Flow Metab. 26, 392-401.
63. Pautz, A., Art, J., Hahn, S., Nowag, S., Voss, C., and Kleinert, H. (2010). Regulation of the expression of inducible nitric oxide synthase. Nitric Oxide 23, 75-93.
64. Pei, D.S., Song, Y.J., Yu, H.M., Hu, W.W., Du, Y., and Zhang, G.Y. (2008). Exogenous nitric oxide negatively regulates c-Jun N-terminal kinase activation via inhibiting endogenous NO-induced S-nitrosylation during cerebral ischemia and reperfusion in rat hippocampus. J. Neurochem. 106, 1952-1963.
65. Qi, S.H., Hao, L.Y., Yue, J., Zong, Y.Y., and Zhang, G.Y. (2013). Exogenous nitric oxide negatively regulates the S-nitrosylation p38 mitogen-activated protein kinase activation during cerebral ischaemia and reperfusion. Neuropathol. Appl. Neurobiol. 39, 284-297.
66. Rameau, G.A., Tukey, D.S., Garcin-Hosfield, E.D., Titcombe, R.F., Misra, C., Khatri, L., Getzoff, E.D., and Ziff, E.B. (2007). Biphasic coupling of neuronal nitric oxide synthase phosphorylation to the NMDA receptor regulates AMPA receptor trafficking and neuronal cell death. J. Neurosci. 27, 3445-3455.
67. Rao, K.M. (2000). Molecular mechanisms regulating iNOS expression in various cell types. J. Toxicol. Environ. Health B Crit. Rev. 3, 27-58.
68. Ridder, D.A. and Schwaninger, M. (2009). NF-kappaB signaling in cerebral ischemia. Neuroscience 158, 995-1006.
69. Sarkar, S., Korolchuk, V.I., Renna, M., Imarisio, S., Fleming, A., Williams, A., Garcia-Arencibia, M., Rose, C., Luo, S., Underwood, B.R., et al. (2011). Complex inhibitory effects of nitric oxide on autophagy. Mol. Cell. 43, 19-32.
70. Sen, N., Hara, M.R., Kornberg, M.D., Cascio, M.B., Bae, B.I., Shahani, N., Thomas, B., Dawson, T.M., Dawson, V.L., Snyder, S.H., et al. (2008). Nitric oxide-induced nuclear GAPDH activates p300/CBP and mediates apoptosis. Nat. Cell Biol. 10, 866-873.
71. Shao, L., Guo, Z., and Geller, D.A. (2007). Transcriptional suppression of cytokine-induced iNOS gene expression by IL-13 through IRF-1/ISRE signaling. Biochem. Biophys. Res. Commun. 362, 582-586.
72. Shi, Z.Q., Sunico, C.R., McKercher, S.R., Cui, J., Feng, G.S., Nakamura, T., and Lipton, S.A. (2013). S-nitrosylated SHP-2 contributes to NMDA receptor-mediated excitotoxicity in acute ischemic stroke. Proc. Natl. Acad. Sci. USA 110, 3137-3142.
73. Sun, M., Zhao, Y., Gu, Y., and Xu, C. (2009). Inhibition of nNOS reduces ischemic cell death through down-regulating calpain and caspase-3 after experimental stroke. Neurochem. Int. 54, 339-346.
74. Takagi, N., Logan, R., Teves, L., Wallace, M.C., and Gurd, J.W. (2000). Altered interaction between PSD-95 and the NMDA receptor following transient global ischemia. J. Neurochem. 74, 169-178.
75. Tang, L.J., Li, C., Hu, S.Q., Wu, Y.P., Zong, Y.Y., Sun, C.C., Zhang, F., and Zhang, G.Y. (2012). S-nitrosylation of c-Src via NMDARnNOS module promotes c-Src activation and NR2A phosphorylation in cerebral ischemia/reperfusion. Mol. Cell. Biochem. 365, 363-377.
76. Tripathi, A. and Sodhi, A. (2009). Growth hormone-induced production of cytokines in murine peritoneal macrophages in vitro: Role of JAK/STAT, PI3K, PKC and MAP kinases. Immunobiology 214, 430-440.
77. Tuna, M., Yilmaz, D.M., Erman, T., Arslan, A., Ozgur, H. and Polat, S. (2009). Effect of neutralization of rat interleukin 6 bioactivity on inducible nitric oxide synthase up-regulation and cerebral ischemic damage. Neurol Res 31, 714-720.
78. Udayabanu, M., Kumaran, D., Nair, R.U., Srinivas, P., Bhagat, N., Aneja, R., and Katyal, A. (2008). Nitric oxide associated with iNOS expression inhibits acetylcholinesterase activity and induces memory impairment during acute hypobaric hypoxia. Brain Res. 1230, 138-149.
79. Vaibhav, K., Shrivastava, P., Javed, H., Khan, A., Ahmed, M.E., Tabassum, R., Khan, M.M., Khuwaja, G., Islam, F., Siddiqui, M.S., et al. (2012). Piperine suppresses cerebral ischemiareperfusion- induced inflammation through the repression of COX-2, NOS-2, and NF-kappaB in middle cerebral artery occlusion rat model. Mol. Cell. Biochem. 367, 73-84.
80. Wang, W.W., Hu, S.Q., Li, C., Zhou, C., Qi, S.H., and Zhang, G.Y. (2010). Transduced PDZ1 domain of PSD-95 decreases Src phosphorylation and increases nNOS (Ser847) phosphorylation contributing to neuroprotection after cerebral ischemia. Brain Res. 1328, 162-170.
81. Wei, Y., Pattingre, S., Sinha, S., Bassik, M., and Levine, B. (2008). JNK1-mediated phosphorylation of Bcl-2 regulates starvationinduced autophagy. Mol. Cell. 30, 678-688.
82. Yagita, Y., Kitagawa, K., Oyama, N., Yukami, T., Watanabe, A., Sasaki, T., and Mochizuki, H. (2013). Functional deterioration of endothelial nitric oxide synthase after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 33, 1532-1539.
83. Yang, M.Z., Mun, C.H., Choi, Y.J., Baik, J.H., Park, K.A., Lee, W.T., and Lee, J.E. (2007). Agmatine inhibits matrix metalloproteinase-9 via endothelial nitric oxide synthase in cerebral endothelial cells. Neurol. Res. 29, 749-754.
84. Yang, Z.J., Carter, E.L., Torbey, M.T., Martin, L.J., and Koehler, R.C. (2010). Sigma receptor ligand 4-phenyl-1-(4-phenylbutyl)- piperidine modulates neuronal nitric oxide synthase/postsynaptic density-95 coupling mechanisms and protects against neonatal ischemic degeneration of striatal neurons. Exp. Neurol. 221, 166-174.
85. Yu, H.M., Xu, J., Li, C., Zhou, C., Zhang, F., Han, D., and Zhang, G.Y. (2008). Coupling between neuronal nitric oxide synthase and glutamate receptor 6-mediated c-Jun N-terminal kinase signaling pathway via S-nitrosylation contributes to ischemia neuronal death. Neuroscience 155, 1120-1132.
86. Zeng, X.W., Li, M.W., Pan, J., Ji, T.L., Yang, B., Zhang, B., and Wang, X.Q. (2011). Activation of c-Jun N-terminal kinase 1/2 regulated by nitric oxide is associated with neuronal survival in hippocampal neurons in a rat model of ischemia. Chin. Med. J. (Engl.) 124, 3367-3372.
87. Zhang, F., Li, C., Wang, R., Han, D., Zhang, Q.G., Zhou, C., Yu, H.M., and Zhang, G.Y. (2007a). Activation of GABA receptors attenuates neuronal apoptosis through inhibiting the tyrosine phosphorylation of NR2A by Src after cerebral ischemia and reperfusion. Neuroscience 150, 938-949.
88. Zhang, P., Liu, Y., Li, J., Kang, Q., Tian, Y., Chen, X., Zhao, J., Shi, Q., and Song, T. (2007b). Decreased neuronal nitric oxide synthase expression and cell migration in the peri-infarction after focal cerebral ischemia in rats. Neuropathology 27, 347-354.
89. Zhang, Y., Lu, J., Shi, J., Lin, X., Dong, J., Zhang, S., Liu, Y., and Tong, Q. (2008). Central administration of angiotensin-(1-7) stimulates nitric oxide release and upregulates the endothelial nitric oxide synthase expression following focal cerebral ischemia/reperfusion in rats. Neuropeptides 42, 593-600.
90. Zhang, L., Dong, L.Y., Li, Y.J., Hong, Z., and Wei, W.S. (2012a). The microRNA miR-181c controls microglia-mediated neuronal apoptosis by suppressing tumor necrosis factor. J. Neuroinflamm. 9, 211.
91. Zhang, Y., Chen, J., Li, F., Li, D., Xiong, Q., Lin, Y., Zhang, D., Wang, X.F., Yang, P., and Rui, Y.C. (2012b). A pentapeptide monocyte locomotion inhibitory factor protects brain ischemia injury by targeting the eEF1A1/endothelial nitric oxide synthase pathway. Stroke 43, 2764-2773.
92. Zhang, L., Liu, Q., Yuan, X., Wang, T., Luo, S., Lei, H., and Xia, Y. (2013). Requirement of heat shock protein 70 for inducible nitric oxide synthase induction. Cell. Signal. 25, 1310-1317.
93. Zhou, L. and Zhu, D.Y. (2009). Neuronal nitric oxide synthase: Structure, subcellular localization, regulation, and clinical implications. Nitric Oxide 20, 223-230.
94. Zhou, C., Li, C., Yu, H.M., Zhang, F., Han, D., and Zhang, G.Y. (2008). Neuroprotection of gamma-aminobutyric acid receptor agonists via enhancing neuronal nitric oxide synthase (Ser847) phosphorylation through increased neuronal nitric oxide synthase and PSD95 interaction and inhibited protein phosphatase activity in cerebral ischemia. J. Neurosci. Res. 86, 2973-2983.
95. Zhou, L., Li, F., Xu, H.B., Luo, C.X., Wu, H.Y., Zhu, M.M., Lu, W., Ji, X., Zhou, Q.G., and Zhu, D.Y. (2010). Treatment of cerebral ischemia by disrupting ischemia-induced interaction of nNOS with PSD-95. Nat. Med. 16, 1439-1443.
96. Zhou M., Wang, C.M., Yang, W.L., and Wang, P. (2013). Microglial CD14 activated by iNOS contributes to neuroinflammation in cerebral ischemia. Brain Res. 1506, 105-114.
97. Zhu, H., Vishwamitra, D., Curry, C.V., Manshouri, R., Diao, L., Khan, A., and Amin, H.M. (2013). NPM-ALK up-regulates iNOS expression through a STAT3/microRNA-26a-dependent mechanism. J. Pathol. 230, 82-94.