Nitric oxide signaling in brain function, dysfunction, and dementia

Neuroscientist

Volumn 16, Issue 4, 2010, Pages 435-452

  Steinert, Joern R ^a   Chernova, Tatyana ^a   Forsythe, Ian D ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Alzheimerg's disease; homeostatic signaling; intrinsic neuronal excitability; K+ channels; neurodegeneration; nitric oxide; oxidative stress; Parkinsong's disease; synaptic transmission

Indexed keywords

CALCIUM; ION CHANNEL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; VOLTAGE GATED POTASSIUM CHANNEL;

ALZHEIMER DISEASE; BRAIN DYSFUNCTION; BRAIN FUNCTION; DEGENERATIVE DISEASE; DEMENTIA; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; EXCITOTOXICITY; HUMAN; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MITOCHONDRION; MULTIPLE SCLEROSIS; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVOUS SYSTEM; NEUROMODULATION; NITRERGIC NERVE; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STROKE;

ANIMALS; BRAIN; DEMENTIA; NEURONAL PLASTICITY; NEURONS; NITRIC OXIDE; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

EID: 77956318603     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858410366481     Document Type: Review

References (174)

1. Abu-Soud HM, Wang J., Rousseau DL, Fukuto JM, Ignarro LJ, Stuehr DJ 1995. Neuronal nitric oxide synthase self-inactivates by forming a ferrous-nitrosyl complex during aerobic catalysis. J Biol Chem 270: 22997-20006.
2. Ahern GP, Hsu SF, Jackson MB 1999. Direct actions of nitric oxide on rat neurohypophysial K+ channels. J Physiol 520 (Pt 1). 165-176.
3. Ahern GP, Klyachko VA, Jackson MB 2002. cGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO. Trends Neurosci 25: 510-517.
4. Alderton WK, Cooper CE, Knowles RG 2001. Nitric oxide synthases: structure, function and inhibition. Biochem J 357: 593-615.
5. Aliev G., Palacios HH, Lipsitt AE, Fischbach K., Lamb BT, Obrenovich ME, and others. 2009. Nitric oxide as an initiator of brain lesions during the development of Alzheimer disease. Neurotox Res 16: 293-305.
6. Artinian L., Tornieri K., Zhong L., Baro D., Rehder V. 2010. Nitric oxide acts as a volume transmitter to modulate electrical properties of spontaneously firing neurons via apaminsensitive potassium channels. J Neurosci 30: 1699-1711.
7. Bartho L., Benko R., Holzer-Petsche U., Holzer P., Undi S., Wolf M. 2008. Role of extrinsic afferent neurons in gastrointestinal motility. Eur Rev Med Pharmacol Sci 12: 21-31.
8. Barthwal MK, Srivastava N., Dikshit M. 2001. Role of nitric oxide in a progressive neurodegeneration model of Parkinsong'ss disease in the rat. Redox Rep 6: 297-302.
9. Bauer PM, Fulton D., Boo YC, Sorescu GP, Kemp BE, Jo H., and others. 2003. Compensatory phosphorylation and protein-protein interactions revealed by loss of function and gain of function mutants of multiple serine phosphorylation sites in endothelial nitric-oxide synthase. J Biol Chem 278: 14841-14849.
10. Beckman JS, Koppenol WH 1996. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 271: C1424-37.
11. Bennett S., Grant MM, Aldred S. 2009. Oxidative stress in vascular dementia and Alzheimerg'ss disease: a common pathology. J Alzheimers Dis 17: 245-257.
12. Biel M., Sautter A., Ludwig A., Hofmann F., Zong X. 1998. Cyclic nucleotide-gated channels-mediators of NO:cGMPregulated processes. Naunyn Schmiedebergs Arch Pharmacol 358: 140-144.
13. Bo L., Dawson TM, Wesselingh S., Mork S., Choi S., Kong PA, and others. 1994. Induction of nitric oxide synthase in demyelinating regions of multiple sclerosis brains. Ann Neurol 36: 778-786.
14. Bogdan C. 2001. Nitric oxide and the immune response. Nat Immunol 2: 907-916.
15. Bossy-Wetzel E., Petrilli A., Knott AB 2008. Mutant huntingtin and mitochondrial dysfunction. Trends Neurosci 31: 609-616.
16. Bossy-Wetzel E., Talantova MV, Lee WD, Scholzke MN, Harrop A., Mathews E., and others. 2004. Crosstalk between nitric oxide and zinc pathways to neuronal cell death involving mitochondrial dysfunction and p38-activated K+ channels. Neuron 41: 351-365.
17. Boxall AR, Garthwaite J. 1996. Long-term depression in rat cerebellum requires both NO synthase and NO-sensitive guanylyl cyclase. Eur J Neurosci 8: 2209-2212.
18. Boyle WA III, Parvathaneni LS, Bourlier V., Sauter C., Laubach VE, Cobb JP 2000. iNOS gene expression modulates microvascular responsiveness in endotoxin-challenged mice. Circ Res 87: E18-24.
19. Bredt DS, Ferris CD, Snyder SH 1992. Nitric oxide synthase regulatory sites: phosphorylation by cyclic AMP-dependent protein kinase, protein kinase C, and calcium/calmodulin protein kinase; identification of flavin and calmodulin binding sites. J Biol Chem 267: 10976-10981.
20. Brenman JE, Chao DS, Gee SH, McGee AW, Craven SE, Santillano DR, and others. 1996. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains. Cell 84: 757-767.
21. Burger S., Noack M., Kirazov LP, Kirazov EP, Naydenov CL, Kouznetsova E., and others. 2009. Vascular endothelial growth factor (VEGF) affects processing of amyloid precursor protein and beta-amyloidogenesis in brain slice cultures derived from transgenic Tg2576 mouse brain. Int J Dev Neurosci 27: 517-523.
22. Burnett AL, Lowenstein CJ, Bredt DS, Chang TS, Snyder SH 1992. Nitric oxide: a physiologic mediator of penile erection. Science 257: 401-403.
23. Chang YW, Jakobi R., McGinty A., Foschi M., Dunn MJ, Sorokin A. 2000. Cyclooxygenase 2 promotes cell survival by stimulation of dynein light chain expression and inhibition of neuronal nitric oxide synthase activity. Mol Cell Biol 20: 8571-8579.
24. Chaudhury A., He XD, Goyal RK Aug 2009. Role of PSD95 in membrane association and catalytic activity of nNOS{alpha} in nitrergic varicosities in mice gut. Am J Physiol Gastrointest Liver Physiol 297: G806 - G813.
25. Cheret C., Gervais A., Lelli A., Colin C., Amar L., Ravassard P., and others. 2008. Neurotoxic activation of microglia is promoted by a nox1-dependent NADPH oxidase. J Neurosci 28: 12039-12051.
26. Cho DH, Nakamura T., Fang J., Cieplak P., Godzik A., Gu Z., and others. 2009. S-nitrosylation of Drp1 mediates beta-amyloid-related mitochondrial fission and neuronal injury. Science 324: 102-105.
27. Chung CY, Koprich JB, Endo S., Isacson O. 2007. An endogenous serine/threonine protein phosphatase inhibitor, G-substrate, reduces vulnerability in models of Parkinsong'ss disease. J Neurosci 27: 8314-8323.
28. Chung KK, Thomas B., Li X., Pletnikova O., Troncoso JC, Marsh L., and others. 2004. S-nitrosylation of parkin regulates ubiquitination and compromises parking'ss protective function. Science 304: 1328-1331.
29. Closs EI 2002. Expression, regulation and function of carrier proteins for cationic amino acids. Curr Opin Nephrol Hyper-tens 11: 99-107.
30. Contestabile A. 2008. Regulation of transcription factors by nitric oxide in neurons and in neural-derived tumor cells. Prog Neurobiol 84: 317-328.
31. Danielson SR, Andersen JK 2008. Oxidative and nitrative protein modifications in Parkinsong'ss disease. Free Radic Biol Med 44: 1787-1794.
32. de la Torre JC 2009. Cerebrovascular and cardiovascular pathology in Alzheimerg'ss disease. Int Rev Neurobiol 84: 35-48.
33. Dimmeler S., Assmus B., Hermann C., Haendeler J., Zeiher AM 1998. Fluid shear stress stimulates phosphorylation of Akt in human endothelial cells: involvement in suppression of apoptosis. Circ Res 83: 334-341.
34. Dinerman JL, Steiner JP, Dawson TM, Dawson V., Snyder SH 1994. Cyclic nucleotide dependent phosphorylation of neuronal nitric oxide synthase inhibits catalytic activity. Neuropharmacology 33: 1245-1251.
35. Dudzinski DM, Igarashi J., Greif D., Michel T. 2006. The regulation and pharmacology of endothelial nitric oxide synthase. Annu Rev Pharmacol Toxicol 46: 235-276.
36. Eliasson MJ, Blackshaw S., Schell MJ, Snyder SH 1997. Neuronal nitric oxide synthase alternatively spliced forms: prominent functional localizations in the brain. Proc Natl Acad Sci USA 94: 3396-3401.
37. Endo S., Nairn AC, Greengard P., Ito M. 2003. Thr123 of rat G-substrate contributes to its action as a protein phosphatase inhibitor. Neurosci Res 45: 79-89.
38. Endo S., Shutoh F., Dinh TL, Okamoto T., Ikeda T., Suzuki M., and others. 2009. Dual involvement of G-substrate in motor learning revealed by gene deletion. Proc Natl Acad Sci USA 106: 3525-3530.
39. Erusalimsky JD, Moncada S. 2007. Nitric oxide and mitochondrial signaling: from physiology to pathophysiology. Arterioscler Thromb Vasc Biol 27: 2524-2531.
40. Erwin PA, Lin AJ, Golan DE, Michel T. 2005. Receptor-regulated dynamic S-nitrosylation of endothelial nitric-oxide synthase in vascular endothelial cells. J Biol Chem 280: 19888-19894.
41. Fleming I., Fisslthaler B., Dimmeler S., Kemp BE, Busse R. 2001. Phosphorylation of Thr(495) regulates Ca(2+)/calmodulin-dependent endothelial nitric oxide synthase activity. Circ Res 88: E68-75.
42. Fleming I., Schulz C., Fichtlscherer B., Kemp BE, Fisslthaler B., Busse R. 2003. AMP-activated protein kinase (AMPK) regulates the insulin-induced activation of the nitric oxide synthase in human platelets. Thromb Haemost 90: 863-871.
43. Flodstrom M., Horwitz MS, Maday A., Balakrishna D., Rodriguez E., Sarvetnick N. 2001. A critical role for inducible nitric oxide synthase in host survival following coxsackievirus B4 infection. Virology 281: 205-215.
44. Foxton RH, Land JM, Heales SJ 2007. Tetrahydrobiopterin availability in Parkinsong'ss and Alzheimerg'ss disease; potential pathogenic mechanisms. Neurochem Res 32: 751-756.
45. Friebe A., Koesling D. 2009. The function of NO-sensitive guanylyl cyclase: what we can learn from genetic mouse models. Nitric Oxide 21: 149-156.
46. Fulton D., Ruan L., Sood SG, Li C., Zhang Q., Venema RC 2008. Agonist-stimulated endothelial nitric oxide synthase activation and vascular relaxation: role of eNOS phosphorylation at Tyr83. Circ Res 102: 497-504.
47. Furchgott RF, Zawadzki JV 1980. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288: 373-376.
48. Gally JA, Montague PR, Reeke GN Jr, 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 Natl Acad Sci USA 87: 3547-3551.
49. Garthwaite G., Bartus K., Malcolm D., Goodwin D., Kollb-Sielecka M., Dooldeniya C., and others. 2006. Signaling from blood vessels to CNS axons through nitric oxide. J Neurosci 26: 7730-7740.
50. Garthwaite J. 2008. Concepts of neural nitric oxide-mediated transmission. Eur J Neurosci 27: 2783-2802.
51. Gatto EM, Riobo NA, Carreras MC, Chernavsky A., Rubio A., Satz ML, and others. 2000. Overexpression of neutrophil neuronal nitric oxide synthase in Parkinsong'ss disease. Nitric Oxide 4: 534-539.
52. Gillardon F., Krep H., Brinker G., Lenz C., Bottiger B., Hossmann KA 1998. Induction of protein inhibitor of neuronal nitric oxide synthase/cytoplasmic dynein light chain following cerebral ischemia. Neuroscience 84: 81-88.
53. Gingerich S., Krukoff TL 2008. Activation of ERbeta increases levels of phosphorylated nNOS and NO production through a Src/PI3K/Akt-dependent pathway in hypothalamic neurons. Neuropharmacology 55: 878-885.
54. Gomez R., Nunez L., Vaquero M., Amoros I., Barana A., de Prada T., and others. 2008. Nitric oxide inhibits Kv4.3 and human cardiac transient outward potassium current (Ito1). Cardiovasc Res 80: 375-384.
55. Gonzalez-Forero D., Portillo F., Gomez L., Montero F., Kasparov S., Moreno-Lopez B. 2007. Inhibition of resting potassium conductances by long-term activation of the NO/cGMP/protein kinase G pathway: a new mechanism regulating neuronal excitability. J Neurosci 27: 6302-6312.
56. Gyurko R., Leupen S., Huang PL 2002. Deletion of exon 6 of the neuronal nitric oxide synthase gene in mice results in hypogonadism and infertility. Endocrinology 143: 2767-2774.
57. Hamel E., Nicolakakis N., Aboulkassim T., Ongali B., Tong XK 2008. Oxidative stress and cerebrovascular dysfunction in mouse models of Alzheimerg'ss disease. Exp Physiol 93: 116-120.
58. Hantraye P., Brouillet E., Ferrante R., Palfi S., Dolan R., Matthews RT, and others. 1996. Inhibition of neuronal nitric oxide synthase prevents MPTP-induced parkinsonism in baboons. Nat Med 2: 1017-1021.
59. Hardingham N., Fox K. 2006. The role of nitric oxide and GluR1 in presynaptic and postsynaptic components of neocortical potentiation. J Neurosci 26: 7395-7404.
60. Hardingham N., Glazewski S., Pakhotin P., Mizuno K., Chapman PF, Giese KP, and others. 2003. Neocortical long-term potentiation and experience-dependent synaptic plasticity require alpha-calcium/calmodulin- dependent protein kinase II auto-phosphorylation. J Neurosci 23: 4428-4436.
61. Hartell NA 1994. cGMP acts within cerebellar Purkinje cells to produce long term depression via mechanisms involving PKC and PKG. Neuroreport 5: 833-836.
62. Hayashi Y., Nishio M., Naito Y., Yokokura H., Nimura Y., Hidaka H., and others. 1999. Regulation of neuronal nitric-oxide synthase by calmodulin kinases. J Biol Chem 274: 20597-20602.
63. Heales SJ, Bolanos JP, Stewart VC, Brookes PS, Land JM, Clark JB 1999. Nitric oxide, mitochondria and neurological disease. Biochim Biophys Acta 1410: 215-228.
64. Hensley K., Maidt ML, Yu Z., Sang H., Markesbery WR, Floyd RA 1998. Electrochemical analysis of protein nitro-tyrosine and dityrosine in the Alzheimer brain indicates region-specific accumulation. J Neurosci 18: 8126-8132.
65. Higashi Y., Noma K., Yoshizumi M., Kihara Y. 2009. Endothelial function and oxidative stress in cardiovascular diseases. Circ J 73: 411-418.
66. Hodara R., Norris EH, Giasson BI, Mishizen-Eberz AJ, Lynch DR, Lee VM, and others. 2004. Functional consequences of alpha-synuclein tyrosine nitration: diminished binding to lipid vesicles and increased fibril formation. J Biol Chem 279: 47746-47753.
67. Hollenberg SM, Broussard M., Osman J., Parrillo JE 2000. Increased microvascular reactivity and improved mortality in septic mice lacking inducible nitric oxide synthase. Circ Res 86: 774-778.
68. Huang PL, Dawson TM, Bredt DS, Snyder SH, Fishman MC 1993. Targeted disruption of the neuronal nitric oxide synthase gene. Cell 75: 1273-1286.
69. Huang Y., Man HY, Sekine-Aizawa Y., Han Y., Juluri K., Luo H., and others. 2005. S-nitrosylation of N-ethylmaleimide sensitive factor mediates surface expression of AMPA receptors. Neuron 46: 533-540.
70. Huang Z., Huang PL, Ma J., Meng W., Ayata C., Fishman MC, and others. 1996. Enlarged infarcts in endothelial nitric oxide synthase knockout mice are attenuated by nitro-L-arginine. J Cereb Blood Flow Metab 16: 981-987.
71. Hunot S., Boissiere F., Faucheux B., Brugg B., Mouatt-Prigent A., Agid Y., and others. 1996. Nitric oxide synthase and neuronal vulnerability in Parkinsong'ss disease. Neuroscience 72: 355-363.
72. Hurt KJ, Musicki B., Palese MA, Crone JK, Becker RE, Moriarity JL, and others. 2002. Akt-dependent phosphorylation of endothelial nitric-oxide synthase mediates penile erection. Proc Natl Acad Sci USA 99: 4061-4066.
73. Ihara H., Kuwamura M., Atsuta M., Nihonmatsu I., Okada T., Mukamoto M., and others. 2006. Expression of neuronal nitric oxide synthase variant, nNOS-mu, in rat brain. Nitric Oxide 15: 13-19.
74. Jacoby S., Sims RE, Hartell NA 2001. Nitric oxide is required for the induction and heterosynaptic spread of long-term potentiation in rat cerebellar slices. J Physiol 535: 825-839.
75. Jaffrey SR, Snowman AM, Eliasson MJ, Cohen NA, Snyder SH 1998. CAPON: a protein associated with neuronal nitric oxide synthase that regulates its interactions with PSD95. Neuron 20: 115-124.
76. Jaffrey SR, Snyder SH 1996. PIN: an associated protein inhibitor of neuronal nitric oxide synthase. Science 274: 774-777.
77. Jeong Y., Won J., Yim J. 1998. Cloning and structure of a rabbit protein inhibitor of neuronal nitric oxide synthase (PIN) gene and its pseudogene. Gene 214: 67-75.
78. Joy S., Siow RC, Rowlands DJ, Becker M., Wyatt AW, Aaronson PI, and others. 2006. The isoflavone Equol mediates rapid vascular relaxation: Ca2+-independent activation of endothelial nitric-oxide synthase/Hsp90 involving ERK1/2 and Akt phosphorylation in human endothelial cells. J Biol Chem 281: 27335-27345.
79. Kang Y., Dempo Y., Ohashi A., Saito M., Toyoda H., Sato H., and others. 2007. Nitric oxide activates leak K+ currents in the presumed cholinergic neuron of basal forebrain. J Neurophysiol 98: 3397-3410.
80. Kawano T., Zoga V., Kimura M., Liang MY, Wu HE, Gemes G., and others. 2009. Nitric oxide activates ATP-sensitive potassium channels in mammalian sensory neurons: action by direct S-nitrosylation. Mol Pain 5: 12.
81. Keilhoff G., Fansa H., Wolf G. 2004. Neuronal NOS deficiency promotes apoptotic cell death of spinal cord neurons after peripheral nerve transection. Nitric Oxide 10: 101-111.
82. Kerchner GA, Nicoll RA 2008. Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci 9: 813-825.
83. Keynes RG, Griffiths CH, Hall C., Garthwaite J. 2005. Nitric oxide consumption through lipid peroxidation in brain cell suspensions and homogenates. Biochem J 387: 685-694.
84. Kleppisch T. 2009. Phosphodiesterases in the central nervous system. Handb Exp Pharmacol 191: 71-92.
85. Knoch ME, Hartnett KA, Hara H., Kandler K., Aizenman E. 2008. Microglia induce neurotoxicity via intraneuronal Zn2+ release and a K+ current surge. Glia 56: 89-96.
86. Knott AB, Bossy-Wetzel E. 2008. Impairing the mitochondrial fission and fusion balance: a new mechanism of neurodegeneration. Ann N Y Acad Sci 1147: 283-292.
87. Knott AB, Bossy-Wetzel E. 2009. Nitric oxide in health and disease of the nervous system. Antioxid Redox Signal 11: 541-554.
88. Knott AB, Perkins G., Schwarzenbacher R., Bossy-Wetzel E. 2008. Mitochondrial fragmentation in neurodegeneration. Nat Rev Neurosci 9: 505-518.
89. Komeima K., Hayashi Y., Naito Y., Watanabe Y. 2000. Inhibition of neuronal nitric-oxide synthase by calcium/calmodulin-dependent protein kinase IIalpha through Ser847 phosphorylation in NG108-15 neuronal cells. J Biol Chem 275: 28139-28143.
90. Korneev SA, Straub V., Kemenes I., Korneeva EI, Ott SR, Benjamin PR, and others. 2005. Timed and targeted differential regulation of nitric oxide synthase (NOS) and anti-NOS genes by reward conditioning leading to long-term memory formation. J Neurosci 25: 1188-1192.
91. Kroncke KD, Fehsel K., Schmidt T., Zenke FT, Dasting I., Wesener JR, and others. 1994. Nitric oxide destroys zinc-sulfur clusters inducing zinc release from metallothionein and inhibition of the zinc finger-type yeast transcription activator LAC9. Biochem Biophys Res Commun 200: 1105-1110.
92. Kuiper MA, Visser JJ, Bergmans PL, Scheltens P., Wolters EC 1994. Decreased cerebrospinal fluid nitrate levels in Parkinsong'ss disease, Alzheimerg'ss disease and multiple system atrophy patients. J Neurol Sci 121: 46-49.
93. Kurauchi Y., Hisatsune A., Isohama Y., Katsuki H. 2009. Nitric oxide-cyclic GMP signaling pathway limits inflammatory degeneration of midbrain dopaminergic neurons: cell type-specific regulation of heme oxygenase-1 expression. Neuroscience 158: 856-866.
94. Langnaese K., Richter K., Smalla KH, Krauss M., Thomas U., Wolf G., and others. 2007. Splice-isoform specific immunolocalization of neuronal nitric oxide synthase in mouse and rat brain reveals that the PDZ-complex-building nNOSalpha beta-finger is largely exposed to antibodies. Dev Neurobiol 67: 422-437.
95. Lee MY, Griendling KK 2008. Redox signaling, vascular function, and hypertension. Antioxid Redox Signal 10: 1045-1059.
96. Lei S., Jackson MF, Jia Z., Roder J., Bai D., Orser BA, and others. 2000. Cyclic GMP-dependent feedback inhibition of AMPA receptors is independent of PKG. Nat Neurosci 3: 559-565.
97. Lipton SA, Choi YB, Takahashi H., Zhang D., Li W., Godzik A., and others. 2002. Cysteine regulation of protein function- as exemplified by NMDA-receptor modulation. Trends Neurosci 25: 474-480.
98. Liu J., Garcia-Cardena G., Sessa WC 1995. Biosynthesis and palmitoylation of endothelial nitric oxide synthase: mutagenesis of palmitoylation sites, cysteines-15 and/or -26, argues against depalmitoylation-induced translocation of the enzyme. Biochemistry 34: 12333-12340.
99. Malenka RC, Bear MF 2004. LTP and LTD: an embarrassment of riches. Neuron 44: 5-21.
100. Malinow R., Malenka RC 2002. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25: 103-126.
101. Manczak M., Anekonda TS, Henson E., Park BS, Quinn J., Reddy PH 2006. Mitochondria are a direct site of A beta accumulation in Alzheimerg'ss disease neurons: implications for free radical generation and oxidative damage in disease progression. Hum Mol Genet 15: 1437-1449.
102. Mann GE, Yudilevich DL, Sobrevia L. 2003. Regulation of amino acid and glucose transporters in endothelial and smooth muscle cells. Physiol Rev 83: 183-252.
103. Marlatt MW, Lucassen PJ, Perry G., Smith MA, Zhu X. 2008. Alzheimerg'ss disease: cerebrovascular dysfunction, oxidative stress, and advanced clinical therapies. J Alzheimers Dis 15: 199-210.
104. Michel JB, Feron O., Sase K., Prabhakar P., Michel T. 1997. Caveolin versus calmodulin: counterbalancing allosteric modulators of endothelial nitric oxide synthase. J Biol Chem 272: 25907-25912.
105. Michel T. 1999. Targeting and translocation of endothelial nitric oxide synthase. Braz J Med Biol Res 32: 1361-1366.
106. Michell BJ, Harris MB, Chen ZP, Ju H., Venema VJ, Blackstone MA, and others. 2002. Identification of regulatory sites of phosphorylation of the bovine endothelial nitric-oxide synthase at serine 617 and serine 635. J Biol Chem 277: 42344-42351.
107. Miller RL, James-Kracke M., Sun GY, Sun AY 2009. Oxidative and inflammatory pathways in Parkinsong'ss disease. Neurochem Res 34: 55-65.
108. Mitchell DA, Erwin PA, Michel T., Marletta MA 2005. Snitrosation and regulation of inducible nitric oxide synthase. Biochemistry 44: 4636-4647.
109. Moncada S., Bolanos JP 2006. Nitric oxide, cell bioenergetics and neurodegeneration. J Neurochem 97: 1676-1689.
110. Moreno H., Vega-Saenz de Miera E., Nadal MS, Amarillo Y., Rudy B. 2001. Modulation of Kv3 potassium channels expressed in CHO cells by a nitric oxide-activated phosphatase. J Physiol 530: 345-358.
111. Mount PF, Fraser SA, Watanabe Y., Lane N., Katsis F., Chen ZP, and others. 2006. Phosphorylation of neuronal and endothelial nitric oxide synthase in the kidney with high and low salt diets. Nephron Physiol 102 :p 36-50.
112. Mount PF, Kemp BE, Power DA 2007. Regulation of endothelial and myocardial NO synthesis by multi-site eNOS phosphorylation. J Mol Cell Cardiol 42: 271-279.
113. Mustafa AK, Gadalla MM, Snyder SH 2009. Signaling by gasotransmitters. Sci Signal 2: re2.
114. Nakagomi S., Barsoum MJ, Bossy-Wetzel E., Sutterlin C., Malhotra V., Lipton SA 2008. A Golgi fragmentation pathway in neurodegeneration. Neurobiol Dis 29: 221-231.
115. Nakane M., Mitchell J., Forstermann U., Murad F. 1991. Phosphorylation by calcium calmodulin-dependent protein kinase II and protein kinase C modulates the activity of nitric oxide synthase. Biochem Biophys Res Commun 180: 1396-1402.
116. Nanhoe-Mahabier W., de Laat KF, Visser JE, Zijlmans J., de Leeuw FE, Bloem BR 2009. Parkinson disease and comorbid cerebrovascular disease. Nat Rev Neurol 5: 533-541.
117. Niwa K., Porter VA, Kazama K., Cornfield D., Carlson GA, Iadecola C. 2001. A beta-peptides enhance vasoconstriction in cerebral circulation. Am J Physiol Heart Circ Physiol 281: H2417-24.
118. Nunez L., Vaquero M., Gomez R., Caballero R., Mateos-Caceres P., Macaya C., and others. 2006. Nitric oxide blocks hKv1.5 channels by S-nitrosylation and by a cyclic GMP-dependent mechanism. Cardiovasc Res 72: 80-89.
119. Og'sDell TJ, Huang PL, Dawson TM, Dinerman JL, Snyder SH, Kandel ER, and others. 1994. Endothelial NOS and the blockade of LTP by NOS inhibitors in mice lacking neuronal NOS. Science 265: 542-546.
120. Ogasawara H., Doi T., Doya K., Kawato M. 2007. Nitric oxide regulates input specificity of long-term depression and context dependence of cerebellar learning. PLoS Comput Biol 3: e179.
121. Ortiz PA, Garvin JL 2003. Cardiovascular and renal control in NOS-deficient mouse models. Am J Physiol Regul Integr Comp Physiol 284: R628-38.
122. Pan J., Burgher KL, Szczepanik AM, Ringheim GE 1996. Tyrosine phosphorylation of inducible nitric oxide synthase: implications for potential post-translational regulation. Biochem J 314: 889-894.
123. Phillips KG, Hardingham NR, Fox K. 2008. Postsynaptic action potentials are required for nitric-oxide-dependent long-term potentiation in CA1 neurons of adult GluR1 knock-out and wild-type mice. J Neurosci 28: 14031-14041.
124. Qiu DL, Knopfel T. 2007. An NMDA receptor/nitric oxide cascade in presynaptic parallel fiber-Purkinje neuron long-term potentiation. J Neurosci 27: 3408-3415.
125. Queen LR, Ji Y., Xu B., Young L., Yao K., Wyatt AW, and others. 2006. Mechanisms underlying beta2-adrenoceptor-mediated nitric oxide generation by human umbilical vein endothelial cells. J Physiol 576: 585-594.
126. Rameau GA, Chiu LY, Ziff EB 2004. Bidirectional regulation of neuronal nitric-oxide synthase phosphorylation at serine 847 by the N-methyl-D-aspartate receptor. J Biol Chem 279: 14307-14314.
127. Rameau GA, Tukey DS, Garcin-Hosfield ED, Titcombe RF, Misra C., Khatri L., and others. 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.
128. Regehr WG, Carey MR, Best AR 2009. Activity-dependent regulation of synapses by retrograde messengers. Neuron 63: 154-170.
129. Reynolds MR, Berry RW, Binder LI 2005. Site-specific nitration and oxidative dityrosine bridging of the tau protein by peroxynitrite: implications for Alzheimerg'ss disease. Biochemistry 44: 1690-1700.
130. Ribeiro M., Straub VA, Schofield M., Picot J., Benjamin PR, Og'sShea M., and others. 2008. Characterization of NO-sensitive guanylyl cyclase: expression in an identified interneuron involved in NO-cGMP-dependent memory formation. Eur J Neurosci 28: 1157-1165.
131. Rogers NE, Ignarro LJ 1992. Constitutive nitric oxide synthase from cerebellum is reversibly inhibited by nitric oxide formed from L-arginine. Biochem Biophys Res Commun 189: 242-249.
132. Rotmann A., Simon A., Martine U., Habermeier A., Closs EI 2007. Activation of classical protein kinase C decreases transport via systems y+ and y+L. Am J Physiol Cell Physiol 292: C2259-68.
133. Roy B., Garthwaite J. 2006. Nitric oxide activation of guanylyl cyclase in cells revisited. Proc Natl Acad Sci USA 103: 12185-12190.
134. Ryu JK, Cho T., Choi HB, Wang YT, McLarnon JG 2009. Microglial VEGF receptor response is an integral chemotactic component in Alzheimerg'ss disease pathology. J Neurosci 29: 3-13.
135. Sanders KM, Koh SD 2006. Two-pore-domain potassium channels in smooth muscles: new components of myogenic regulation. J Physiol 570: 37-43.
136. Schapira AH, Cooper JM, Dexter D., Jenner P., Clark JB, Marsden CD 1989. Mitochondrial complex I deficiency in Parkinsong'ss disease. Lancet 1: 1269.
137. Selvakumar B., Huganir RL, Snyder SH 2009. S-nitrosylation of stargazin regulates surface expression of AMPAglutamate neurotransmitter receptors. Proc Natl Acad Sci USA 106: 16440-16445.
138. Serulle Y., Arancio O., Ziff EB 2008. A role for cGMP-dependent protein kinase II in AMPA receptor trafficking and synaptic plasticity. Channels 2: 230-232.
139. Sessa WC 2004. eNOS at a glance. J Cell Sci 117: 2427-2429.
140. Shaul PW, Smart EJ, Robinson LJ, German Z., Yuhanna IS, Ying Y., and others. 1996. Acylation targets emdothelial nitric-oxide synthase to plasmalemmal caveolae. J Biol Chem 271: 6518-6522.
141. Shibuki K., Okada D. 1991. Endogenous nitric oxide release required for long-term synaptic depression in the cerebellum. Nature 349: 326-328.
142. Shin JH, Linden DJ 2005. An NMDA receptor/nitric oxide cascade is involved in cerebellar LTD but is not localized to the parallel fiber terminal. J Neurophysiol 94: 4281-4289.
143. Sims NR, Nilsson M., Muyderman H. 2004. Mitochondrial glutathione: a modulator of brain cell death. J Bioenerg Biomembr 36: 329-333.
144. Singh S., Das T., Ravindran A., Chaturvedi RK, Shukla Y., Agarwal AK, and others. 2005. Involvement of nitric oxide in neurodegeneration: a study on the experimental models of Parkinsong'ss disease. Redox Rep 10: 103-109.
145. Son H., Hawkins RD, Martin K., Kiebler M., Huang PL, Fishman MC, and others. 1996. Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell 87: 1015-1023.
146. Song I., Huganir RL 2002. Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci 25: 578-588.
147. Song T., Hatano N., Horii M., Tokumitsu H., Yamaguchi F., Tokuda M., and others. 2004. Calcium/calmodulin-dependent protein kinase I inhibits neuronal nitric-oxide synthase activity through serine 741 phosphorylation. FEBS Lett 570: 133-137.
148. Song T., Hatano N., Kume K., Sugimoto K., Yamaguchi F., Tokuda M., and others. 2005. Inhibition of neuronal nitric-oxide synthase by phosphorylation at Threonine1296 in NG108-15 neuronal cells. FEBS Lett 579: 5658-5662.
149. Stamler JS, Lamas S., Fang FC 2001. Nitrosylation: the prototypic redox-based signaling mechanism. Cell 106: 675-683.
150. Steinert JR, Kopp-Scheinpflug C., Baker C., Challiss RA, Mistry R., Haustein MD, and others. 2008. Nitric oxide is a volume transmitter regulating postsynaptic excitability at a glutamatergic synapse. Neuron 60: 642-656.
151. Steinert JR, Wyatt AW, Jacob R., Mann GE 2009. Redox modulation of Ca2+ signaling in human endothelial and smooth muscle cells in pre-eclampsia. Antioxid Redox Signal 11: 1149-1163.
152. Sultana R., Perluigi M., Butterfield DA 2009. Oxidatively modified proteins in Alzheimerg'ss disease (AD), mild cognitive impairment and animal models of AD: role of Abeta in pathogenesis. Acta Neuropathol 118: 131-150.
153. Sultana R., Perluigi M., Newman SF, Pierce WM, Cini C., Coccia R., and others. 2010. Redox proteomic analysis of carbonylated brain proteins in mild cognitive impairment and early Alzheimerg'ss disease. Antioxid Redox Signal 12: 327-336.
154. Sultana R., Poon HF, Cai J., Pierce WM, Merchant M., Klein JB, and others. 2006. Identification of nitrated proteins in Alzheimerg'ss disease brain using a redox proteomics approach. Neurobiol Dis 22: 76-87.
155. Takahashi H. 2002. Pathology of neurodegenerative diseases: with special reference to Parkinsong'ss disease and amyotrophic lateral sclerosis. Rinsho Shinkeigaku 42: 1085-1087.
156. Takahashi H., Shin Y., Cho SJ, Zago WM, Nakamura T., Gu Z., and others. 2007. Hypoxia enhances S-nitrosylation-mediated NMDA receptor inhibition via a thiol oxygen sensor motif. Neuron 53: 53-64.
157. Tansey EP, Chow A., Rudy B., McBain CJ 2002. Developmental expression of potassium-channel subunit Kv3.2 within subpopulations of mouse hippocampal inhibitory interneurons. Hippocampus 12: 137-148.
158. Taqatqeh F., Mergia E., Neitz A., Eysel UT, Koesling D., Mittmann T. 2009. More than a retrograde messenger: nitric oxide needs two cGMP pathways to induce hippocampal long-term potentiation. J Neurosci 29: 9344-9350.
159. Tarkowski E., Issa R., Sjogren M., Wallin A., Blennow K., Tarkowski A., and others. 2002. Increased intrathecal levels of the angiogenic factors VEGF and TGF-beta in Alzheimerg'ss disease and vascular dementia. Neurobiol Aging 23: 237-243.
160. Toda N., Herman AG 2005. Gastrointestinal function regulation by nitrergic efferent nerves. Pharmacol Rev 57: 315-338.
161. Townsend KP, Obregon D., Quadros A., Patel N., Volmar C., Paris D., and others. 2002. Proinflammatory and vasoactive effects of Abeta in the cerebrovasculature. Ann N Y Acad Sci 977: 65-76.
162. Tran MH, Yamada K., Nakajima A., Mizuno M., He J., Kamei H., and others. 2003. Tyrosine nitration of a synaptic protein synaptophysin contributes to amyloid beta-peptide-induced cholinergic dysfunction. Mol Psychiatry 8: 407-412.
163. Tsutsui M., Shimokawa H., Morishita T., Nakashima Y., Yanagihara N. 2006. Development of genetically engineered mice lacking all three nitric oxide synthases. J Pharmacol Sci 102: 147-154.
164. Wallace MN, Geddes JG, Farquhar DA, Masson MR 1997. Nitric oxide synthase in reactive astrocytes adjacent to beta-amyloid plaques. Exp Neurol 144: 266-272.
165. Wang X., Zhao Q., Matta R., Meng X., Liu X., Liu CG, and others. 2009. Inducible nitric-oxide synthase expression is regulated by mitogen-activated protein kinase phosphatase-1. J Biol Chem 284: 27123-27134.
166. Wood J., Garthwaite J. 1994. Models of the diffusional spread of nitric oxide: implications for neural nitric oxide signalling and its pharmacological properties. Neuropharmacology 33: 1235-1244.
167. Xia Y., Dawson VL, Dawson TM, Snyder SH, Zweier JL 1996. Nitric oxide synthase generates superoxide and nitric oxide in arginine-depleted cells leading to peroxynitrite-mediated cellular injury. Proc Natl Acad Sci USA 93: 6770-6774.
168. Yang Q., Chen SR, Li DP, Pan HL 2007. Kv1.1/1.2 channels are downstream effectors of nitric oxide on synaptic GABA release to preautonomic neurons in the paraventricular nucleus. Neuroscience 149: 315-327.
169. Yang SP, Bae DG, Kang HJ, Gwag BJ, Gho YS, Chae CB 2004. Co-accumulation of vascular endothelial growth factor with beta-amyloid in the brain of patients with Alzheimerg'ss disease. Neurobiol Aging 25: 283-290.
170. Yao D., Gu Z., Nakamura T., Shi ZQ, Ma Y., Gaston B., and others. 2004. Nitrosative stress linked to sporadic Parkinsong'ss disease: S-nitrosylation of parkin regulates its E3 ubiquitin ligase activity. Proc Natl Acad Sci USA 101: 10810-10814.
171. Yokoyama H., Yano R., Aoki E., Kato H., Araki T. 2008. Comparative pharmacological study of free radical scavenger, nitric oxide synthase inhibitor, nitric oxide synthase activator and cyclooxygenase inhibitor against MPTP neurotoxicity in mice. Metab Brain Dis 23: 335-349.
172. Yuan H., Gerencser AA, Liot G., Lipton SA, Ellisman M., Perkins GA, and others. 2007. Mitochondrial fission is an upstream and required event for bax foci formation in response to nitric oxide in cortical neurons. Cell Death Differ 14: 462-471.
173. Zhang Z., Klyachko V., Jackson MB 2007. Blockade of phosphodiesterase type 5 enhances rat neurohypophysial excitability and electrically evoked oxytocin release. J Physiol 584: 137-147.
174. Zuliani G., Cavalieri M., Galvani M., Passaro A., Munari MR, Bosi C., and others. 2008. Markers of endothelial dysfunction in older subjects with late onset Alzheimerg'ss disease or vascular dementia. J Neurol Sci 272: 164-170.