Skip to main content

Nitric Oxide in Experimental Allergic Encephalomyelitis

  • Reference work entry
Handbook of Neurochemistry and Molecular Neurobiology
  • 794 Accesses

Abstract:

Nitric oxide (NO) is a biologically precious molecule responsible for diverse functions in physiology and pathophysiology of many organs including the brain. Accordingly, NO contributes significantly to both neurodegeneration and neuroprotection in experimental allergic encephalomyelitis (EAE), the animal model of multiple sclerosis (MS). The neurodegenerative aspects of NO in EAE are marked by enhanced CNS infiltration, gliosis, and demyelination whereas the neuroprotection is mainly attributed by diminished adhesion and CNS infiltration, inhibition of proinflammatory factors, and immunosuppression. In this chapter, we have made an attempt to illuminate this bidirectional role of NO in EAE and discuss the therapeutic importance of this molecule in EAE and MS.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 249.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

Abbreviations

AOE:

antioxidant enzymes

AP-1:

activator protein-1

APC:

antigen-presenting cell

BBB:

blood-brain barrier

cGMP:

cyclic guanosine-3′, 5′-monophosphate

CNS:

central nervous system

LPS:

lipopolysaccharides

EAE:

experimental allergic encephalomyelitis

ERK:

extracellular signal-regulated kinase

GAPDH:

glyceraldehydes-3-phosphate dehydrogenase

GC:

guanylate cyclase

GPX:

glutathione peroxidase

GSNO:

S-nitroso glutathione

ICAM:

intercellular cell adhesion molecule

iNOS:

nitric oxide synthase

IFN-γ:

interferon-gamma

IL-12R:

interleukin-12 receptor

IL-1β:

interleukin-1beta

LFA1:

lymphocyte function-associated antigen 1

MAPK:

mitogen-activated protein kinase

MBP:

myelin basic protein

MEK:

MAP kinase kinase

MS:

multiple sclerosis

MMP-9:

matrix metalloproteinase-9

NO:

nitric oxide

NF-κB:

nuclear factor-kappaB

NMDA:

N-methyl-d-aspartate NMDA

ONOO− :

peroxynitrite

PKG:

protein kinase G

PARP:

poly (ADP-ribose) polymerase

Raf:

MEK kinase

ROS:

reactive oxygen species

SAPK:

stress-activated protein kinase

SCI:

spinal cord injury

SNAP:

S-nitroso-N-acetylpenicillamine

SNP:

sodium nitroprusside

SOD:

superoxide dismutase

TNF-α:

tumor necrosis factor-alpha

VCAM:

vascular cell adhesion molecule

VLA4:

very-late antigen 4

References

  • Alderton WK, Cooper CE, Knowles RG. 2001. Nitric oxide synthases: Structure, function and inhibition. Biochem J 357: 597.

    Article  Google Scholar 

  • Amici M, Lupidi G, Angeletti M, Fioretti E, Eleuteri AM. 2003. Peroxynitrite-induced oxidation and its effects on isolated proteasomal systems. Free Radic Biol Med 34: 987.

    Article  CAS  PubMed  Google Scholar 

  • Auch CJ, Saha RN, Sheikh FG, Liu X, Jacobs BL, et al. 2004. Role of protein kinase R in double-stranded RNA-induced expression of nitric oxide synthase in human astroglia. FEBS Lett 563: 223.

    Article  CAS  PubMed  Google Scholar 

  • Bagasra O, Michaels FH, Zheng YM, Bobroski LE, Spitsin SV, et al. 1995. Activation of the inducible form of nitric oxide synthase in the brains of patients with multiple sclerosis. Proc Natl Acad Sci USA 92: 12041.

    Article  CAS  PubMed  Google Scholar 

  • Banik NL. 1992. Pathogenesis of myelin breakdown in demyelinating diseases: Role of proteolytic enzymes. Crit Rev Neurobiol 6: 257.

    CAS  PubMed  Google Scholar 

  • Baron JL, Madri JA, Ruddle NH, Hashim G, Janeway CA Jr. 1993. Surface expression of alpha 4 integrin by CD4 T cells is required for their entry into brain parenchyma. J Exp Med 177: 57.

    Article  CAS  PubMed  Google Scholar 

  • Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA. 1990. Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87: 1620.

    Article  CAS  PubMed  Google Scholar 

  • Beckman JS, Carson M, Smith CD, Koppenol WH. 1993. ALS, SOD and peroxynitrite. Nature 364: 584.

    Article  CAS  PubMed  Google Scholar 

  • Benveniste, EN. 1997. Role of macrophages/microglia in multiple sclerosis and experimental allergic encephalomyelitis. J Mol Med 75: 165.

    Article  CAS  PubMed  Google Scholar 

  • Bhat NR, Shen Q, Fan F. 2003. TAK1-mediated induction of nitric oxide synthase gene expression in glial cells. J Neurochem 87: 238.

    Article  CAS  PubMed  Google Scholar 

  • Bhat NR, Feinstein DL, Shen Q, Bhat AN. 2002. p38 MAPK-mediated transcriptional activation of inducible nitric-oxide synthase in glial cells. Roles of nuclear factors, nuclear factor kappa B, cAMP response element-binding protein, CCAAT/enhancer- binding protein-beta, and activating transcription factor-2. J Biol Chem 277: 29584.

    Article  CAS  PubMed  Google Scholar 

  • Bhat NR, Zhang P, Lee JC, Hogan EL. 1998. Extracellular signal-regulated kinase and p38 subgroups of mitogen-activated protein kinases regulate inducible nitric oxide synthase and tumor necrosis factor-alpha gene expression in endotoxin-stimulated primary glial cultures. J Neurosci 18: 1633.

    CAS  PubMed  Google Scholar 

  • Bizzozero OA, De Jesus G, Howard TA. 2004. Exposure of rat optic nerves to nitric oxide causes protein S-nitrosation and myelin decompaction. Neurochem Res 29: 1675.

    Article  CAS  PubMed  Google Scholar 

  • Bizzozero OA, De Jesus G, Bixler HA, Pastuszyn A. 2005. Evidence of nitrosative damage in the brain white matter of patients with multiple sclerosis. Neurochem Res 30: 139.

    Article  CAS  PubMed  Google Scholar 

  • Bo L, Dawson TM, Wesselingh S, Mork S, Choi S, et al. 1994. Induction of nitric oxide synthase in demyelinating regions of multiple sclerosis brains. Ann Neurol 36: 778.

    Article  CAS  PubMed  Google Scholar 

  • Bogdan C. 2001. Nitric oxide and the regulation of gene expression. Trends Cell Biol 11: 66.

    Article  CAS  PubMed  Google Scholar 

  • Bossy-Wetzel E, Talantova MV, Lee WD, Scholzke MN, Harrop A, et al. 2004. Crosstalk between nitric oxide and zinc pathways to neuronal cell death involving mitochondrial dysfunction and p38- activated K+ channels. Neuron 41: 351.

    Article  CAS  PubMed  Google Scholar 

  • Boullerne AI, Nedelkoska L, Benjamins JA. 1999. Synergism of nitric oxide and iron in killing the transformed murine oligodendrocyte cell line N20.1. J Neurochem 72: 1050.

    Article  CAS  PubMed  Google Scholar 

  • Boullerne AI, Petry KG, Meynard M, Geffard M. 1995. Indirect evidence for nitric oxide involvement in multiple sclerosis by characterization of circulating antibodies directed against conjugated S-nitrosocysteine. J Neuroimmunol 60: 117.

    Article  CAS  PubMed  Google Scholar 

  • Boullerne AI, Rodriguez JJ, Touil T, Brochet B, Schmidt S, et al. 2002. Anti-S-nitrosocysteine antibodies are a predictive marker for demyelination in experimental autoimmune encephalomyelitis: Implications for multiple sclerosis. J Neurosci 22: 123.

    CAS  PubMed  Google Scholar 

  • Brahmachari S, Fung YK, Pahan K. 2006. Induction of glial fibrillary acidic protein expression in astrocytes by nitric oxide. J Neurosci 26: 4930.

    Article  CAS  PubMed  Google Scholar 

  • Bredt DS. 1999. Endogenous nitric oxide synthesis: Biological functions and pathophysiology. Free Radic Res 31: 577.

    Article  CAS  PubMed  Google Scholar 

  • Carson MJ. 2002. Microglia as liaisons between the immune and central nervous systems: Functional implications for multiple sclerosis. Glia 40: 218.

    Article  PubMed  Google Scholar 

  • Cassina AM, Hodara R, Souza JM, Thomson L, Castro L, et al. 2000. Cytochrome c nitration by peroxynitrite. J Biol Chem 275: 21409.

    Article  CAS  PubMed  Google Scholar 

  • Chen CC, Wang JK, Chen WC, Lin SB. 1998. Protein kinase C eta mediates lipopolysaccharide-induced nitric-oxide synthase expression in primary astrocytes. J Biol Chem 273: 19424.

    Article  CAS  PubMed  Google Scholar 

  • Cho HJ, Xie QW, Calaycay J, Mumford RA, Swiderek KM, et al. 1992. Calmodulin is a subunit of nitric oxide synthase from macrophages. J Exp Med 176: 599.

    Article  CAS  PubMed  Google Scholar 

  • Chung KK, Thomas B, Li X, Pletnikova O, Troncoso JC, et al. 2004. S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science 304: 1328.

    Article  CAS  PubMed  Google Scholar 

  • Cudd A, Fridovich I. 1982. Electrostatic interactions in the reaction mechanism of bovine erythrocyte superoxide dismutase. J Biol Chem 257: 11443.

    CAS  PubMed  Google Scholar 

  • Cvetkovic I, Miljkovic D, Vuckovic O, Harhaji L, Nikolic Z, et al. 2004. Taxol activates inducible nitric oxide synthase in rat astrocytes: The role of MAP kinases and NF-kappaB. Cell Mol Life Sci 61: 1167.

    Article  CAS  PubMed  Google Scholar 

  • Dasgupta S, Jana M, Liu X, Pahan K. 2002. Myelin basic protein-primed T cells induce nitric oxide synthase in microglial cells. Implications for multiple sclerosis. J Biol Chem 277: 39327.

    Article  CAS  PubMed  Google Scholar 

  • Dasgupta S, Zhou Y, Jana M, Banik NL, Pahan K. 2003. Sodium phenylacetate inhibits adoptive transfer of experimental allergic encephalomyelitis in SJL/J mice at multiple steps. J Immunol 170: 3874.

    CAS  PubMed  Google Scholar 

  • Dauer W, Przedborski S. 2003. Parkinson's disease: Mechanisms and models. Neuron 39: 889.

    Article  CAS  PubMed  Google Scholar 

  • Dell'Albani P, Santangelo R, Torrisi L, Nicoletti VG, de Vellis J, et al. 2001. JAK/STAT signaling pathway mediates cytokine-induced iNOS expression in primary astroglial cell cultures. J Neurosci Res 65: 417.

    Article  PubMed  Google Scholar 

  • Dela Torre A, Schroeder RA, Bartlett ST, Kuo PC. 1998. Differential effects of nitric oxide-mediated S-nitrosylation on p50 and c-jun DNA binding. Surgery 124: 137.

    CAS  Google Scholar 

  • Dela Torre A, Schroeder RA, Punzalan C, Kuo PC. 1999. Endotoxin-mediated S-nitrosylation of p50 alters NF-kappa B-dependent gene transcription in ANA-1 murine macrophages. J Immunol 162: 4101.

    CAS  Google Scholar 

  • Ding M, Zhang M, Wong JL, Rogers NE, Ignarro LJ, et al. 1998. Antisense knockdown of inducible nitric oxide synthase inhibits induction of experimental autoimmune encephalomyelitis in SJL/J mice. J Immunol 160: 2560.

    CAS  PubMed  Google Scholar 

  • Dobashi K, Pahan K, Chahal A, Singh I. 1997. Modulation of endogenous antioxidant enzymes by nitric oxide in rat C6 glial cells. J Neurochem 68: 1896.

    Article  CAS  PubMed  Google Scholar 

  • Eng LF, Ghirnikar RS. 1994. GFAP and astrogliosis. Brain Pathol 4: 229.

    Article  CAS  PubMed  Google Scholar 

  • Eng LF, Yu AC, Lee YL. 1992. Astrocytic response to injury. Prog Brain Res 94: 353.

    Article  CAS  PubMed  Google Scholar 

  • Engelhardt B, Ransohoff RM. 2005. The ins and outs of T-lymphocyte trafficking to the CNS: Anatomical sites and molecular mechanisms. Trends Immunol 26: 485.

    Article  CAS  PubMed  Google Scholar 

  • Engelhardt B, Laschinger M, Schulz M, Samulowitz U, Vestweber D, et al. 1998. The development of experimental autoimmune encephalomyelitis in the mouse requires alpha4-integrin but not alpha4beta7-integrin. J Clin Invest 102: 296.

    Article  Google Scholar 

  • Faruqi TR, Erzurum SC, Kaneko FT, Di Corleto PE. 1997. Role of nitric oxide in poly(I- C)-induced endothelial cell expression of leukocyte adhesion molecules. Am J Physiol 273: H2490.

    CAS  PubMed  Google Scholar 

  • Fenyk-Melody JE, Garrison AE, Brunnert SR, Weidner JR, Shen F, et al. 1998. Experimental autoimmune encephalomyelitis is exacerbated in mice lacking the NOS2 gene. J Immunol 160: 2940.

    CAS  PubMed  Google Scholar 

  • Furchgott RF, Zawadzki JV. 1980. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288: 373.

    Article  CAS  PubMed  Google Scholar 

  • Go YM, Patel RP, Maland MC, Park H, Beckman JS, et al. 1999. Evidence for peroxynitrite as a signaling molecule in flow-dependent activation of c- Jun NH(2)-terminal kinase. Am J Physiol 277: H1647.

    CAS  PubMed  Google Scholar 

  • Gonzalez-Scarano F, Baltuch G. 1999. Microglia as mediators of inflammatory and degenerative diseases. Annu Rev Neurosci 22: 219.

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Scarano F, Martin-Garcia J. 2005. The neuropathogenesis of AIDS. Nat Rev Immunol 5: 69.

    Article  CAS  PubMed  Google Scholar 

  • Gu Z, Kaul M, Yan B, Kridel SJ, Cui J, et al. 2002. S-nitrosylation of matrix metalloproteinases: Signaling pathway to neuronal cell death. Science 297: 1186.

    Article  CAS  PubMed  Google Scholar 

  • Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS. 2005. Protein S-nitrosylation: Purview and parameters. Nat Rev Mol Cell Biol 6: 150.

    Article  CAS  PubMed  Google Scholar 

  • Hooper DC, Bagasra O, Marini JC, Zborek A, Ohnishi ST, et al. 1994. Proc Natl Acad Sci USA 94: 2528.

    Article  Google Scholar 

  • Hua LL, Zhao ML, Cosenza M, Kim MO, Huang H, et al. 2002. Role of mitogen-activated protein kinases in inducible nitric oxide synthase and TNFalpha expression in human fetal astrocytes. J Neuroimmunol 126: 180.

    Article  CAS  PubMed  Google Scholar 

  • Huie RE, Padmaja S. 1993. The reaction of NO with superoxide. Free Radic Res Commun 18: 195.

    Article  CAS  PubMed  Google Scholar 

  • Hurst RD, Clark JB. 1997. Nitric oxide-induced blood-brain barrier dysfunction is not mediated by inhibition of mitochondrial respiratory chain activity and/or energy depletion. Nitric Oxide 1: 121.

    Article  CAS  PubMed  Google Scholar 

  • Hurst RD, Azam S, Hurst A, Clark JB. 2001. Nitric-oxide-induced inhibition of glyceraldehyde-3-phosphate dehydrogenase may mediate reduced endothelial cell monolayer integrity in an in vitro model blood-brain barrier. Brain Res 894: 181.

    Article  CAS  PubMed  Google Scholar 

  • Ignarro LJ. 1999. Nitric oxide: A unique endogenous signaling molecule in vascular biology. Biosci Rep 19: 51.

    Article  CAS  PubMed  Google Scholar 

  • Isaksson J, Farooque M, Olsson Y. 2005. Improved functional outcome after spinal cord injury in iNOS-deficient mice. Spinal Cord 43: 167.

    Article  CAS  PubMed  Google Scholar 

  • Jana M, Anderson JA, Saha RN, Liu X, Pahan K. 2005. Regulation of inducible nitric oxide synthase in proinflammatory cytokine-stimulated human primary astrocytes. Free Radic Biol Med 38: 655.

    Article  CAS  PubMed  Google Scholar 

  • Jana M, Liu X, Koka S, Ghosh S, Petro TM, et al. 2001. Ligation of CD40 stimulates the induction of nitric-oxide synthase in microglial cells. J Biol Chem 276: 44527.

    Article  CAS  PubMed  Google Scholar 

  • Kapahi P, Takahashi T, Natoli G, Adams SR, Chen Y, et al. 2000. Inhibition of NF-kappa B activation by arsenite through reaction with a critical cysteine in the activation loop of Ikappa B kinase. J Biol Chem 275: 36062.

    Article  CAS  PubMed  Google Scholar 

  • Koprowski H, Spitsin SV, Hooper DC. 2001. Prospects for the treatment of multiple sclerosis by raising serum levels of uric acid, a scavenger of peroxynitrite. Ann Neurol 49: 139.

    Article  CAS  PubMed  Google Scholar 

  • Kuhlmann CR, Lessmann V, Luhmann HJ. 2006. Fluvastatin stabilizes the blood-brain barrier in vitro by nitric oxide-dependent dephosphorylation of myosin light chains. Neuropharmacology 51: 907.

    Article  CAS  PubMed  Google Scholar 

  • Lander HM, Jacovina AT, Davis RJ, Tauras JM. 1996. Differential activation of mitogen- activated protein kinases by nitric oxide-related species. J Biol Chem 271: 19705.

    Article  CAS  PubMed  Google Scholar 

  • Lassmann H. 2003. Hypoxia-like tissue injury as a component of multiple sclerosis lesions. J Neurol Sci 206: 187.

    Article  CAS  PubMed  Google Scholar 

  • Lawson LJ, Perry VH, Dri P, Gordon S. 1990. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 39: 151.

    Article  CAS  PubMed  Google Scholar 

  • Liedtke W, Edelmann W, Bieri PL, Chiu FC, Cowan NJ, et al. 1996. GFAP is necessary for the integrity of CNS white matter architecture and long-term maintenance of myelination. Neuron 17: 607.

    Article  CAS  PubMed  Google Scholar 

  • Ling EA, Wong WC. 1993. The origin and nature of ramified and amoeboid microglia: A historical review and current concepts. Glia 7: 9.

    Article  CAS  PubMed  Google Scholar 

  • Liu JS, Zhao ML, Brosnan CF, Lee SC. 2001. Expression of inducible nitric oxide synthase and nitrotyrosine in multiple sclerosis lesions. Am J Pathol 158: 2057.

    CAS  PubMed  Google Scholar 

  • Luth HJ, Holzer M, Gartner U, Staufenbiel M, Arendt T. 2001. Expression of endothelial and inducible NOS-isoforms is increased in Alzheimer's disease, in APP23 transgenic mice and after experimental brain lesion in rat: Evidence for an induction by amyloid pathology. Brain Res 13: 57.

    Article  Google Scholar 

  • Mander P, Borutaite V, Moncada S, Brown GC. 2005. Nitric oxide from inflammatory-activated glia synergizes with hypoxia to induce neuronal death. J Neurosci Res 79: 208.

    Article  CAS  PubMed  Google Scholar 

  • Marchetti B, Morale MC, Brouwer J, Tirolo C, Testa N, et al. 2002. Exposure to a dysfunctional glucocorticoid receptor from early embryonic life programs the resistance to experimental autoimmune encephalomyelitis via nitric oxide-induced immunosuppression. J Immunol 168: 5848.

    CAS  PubMed  Google Scholar 

  • Martin R, McFarland HF, McFarlin DE. 1992. Immunological aspects of demyelinating diseases. Annu Rev Immunol 10: 153.

    Article  CAS  PubMed  Google Scholar 

  • Mayhan WG. 1996. Role of nitric oxide in histamine-induced increases in permeability of the blood-brain barrier. Brain Res 743: 70.

    Article  CAS  PubMed  Google Scholar 

  • McDonald JW, Althomsons SP, Hyrc KL, Choi DW, Goldberg MP. 1998. Oligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxicity. Nat Med 4: 291.

    Article  CAS  PubMed  Google Scholar 

  • Merrill JE, Ignarro LJ, Sherman MP, Melinek J, Lane TE. 1993. Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J Immunol 151: 2132.

    CAS  PubMed  Google Scholar 

  • Michel T, Feron O. 1997. Nitric oxide synthases: Which, where, how, and why? J Clin Invest 100: 2146.

    Article  CAS  PubMed  Google Scholar 

  • Newman DK, Hoffman S, Kotamraju S, Zhao T, Wakim B, et al. 2002. Nitration of PECAM-1 ITIM tyrosines abrogates phosphorylation and SHP-2 binding. Biochem Biophys Res Commun 296: 1171.

    Article  CAS  PubMed  Google Scholar 

  • Niedbala W, Wei XQ, Campbell C, Thomson D, Komai-Koma M, et al. 2002. Nitric oxide preferentially induces type 1 T cell differentiation by selectively up-regulating IL-12 receptor beta 2 expression via cGMP. Proc Natl Acad Sci USA 99: 16186.

    Article  CAS  PubMed  Google Scholar 

  • Oldendorf WH, Cornford ME, Brown WJ. 1977. The large apparent work capability of the blood-brain barrier: A study of the mitochondrial content of capillary endothelial cells in brain and other tissues of the rat. Ann Neurol 1: 409.

    Article  CAS  PubMed  Google Scholar 

  • Padgett CM, Whorton AR. 1997. Glutathione redox cycle regulates nitric oxide-mediated glyceraldehyde-3-phosphate dehydrogenase inhibition. Am J Physiol 272: C99.

    CAS  PubMed  Google Scholar 

  • Pahan K, Raymond JR, Singh I. 1999. Inhibition of phosphatidylinositol 3-kinase induces nitric-oxide synthase in lipopolysaccharide- or cytokine-stimulated C6 glial cells. J Biol Chem 274: 7528.

    Article  CAS  PubMed  Google Scholar 

  • Pahan K, Liu X, Wood C, Raymond JR. 2000. Expression of a constitutively active form of phosphatidylinositol 3-kinase inhibits the induction of nitric oxide synthase in human astrocytes. FEBS Lett 472: 203.

    Article  CAS  PubMed  Google Scholar 

  • Pahan K, Sheikh FG, Namboodiri AM, Singh I. 1997. Lovastatin and phenylacetate inhibit the induction of nitric oxide synthase and cytokines in rat primary astrocytes, microglia, and macrophages. J Clin Invest 100: 2671.

    Article  CAS  PubMed  Google Scholar 

  • Pahan K, Sheikh FG, Namboodiri AM, Singh I. 1998b. Inhibitors of protein phosphatase 1 and 2A differentially regulate the expression of inducible nitric-oxide synthase in rat astrocytes and macrophages. J Biol Chem 273: 12219.

    Article  CAS  Google Scholar 

  • Pahan K, Namboodiri AM, Sheikh FG, Smith BT, Singh I. 1997a. Increasing cAMP attenuates induction of inducible nitric-oxide synthase in rat primary astrocytes. J Biol Chem 272: 7786.

    Article  CAS  Google Scholar 

  • Pahan K, Sheikh FG, Khan M, Namboodiri AM, Singh I. 1998. Sphingomyelinase and ceramide stimulate the expression of inducible nitric-oxide synthase in rat primary astrocytes. J Biol Chem 273: 2591.

    Article  CAS  PubMed  Google Scholar 

  • Pahan K, Liu X, McKinney MJ, Wood C, Sheikh FG, et al. 2000. Expression of a dominant-negative mutant of p21(ras) inhibits induction of nitric oxide synthase and activation of nuclear factor-kappaB in primary astrocytes. J Neurochem 74: 2288.

    Article  CAS  PubMed  Google Scholar 

  • Pahan K, Sheikh FG, Liu X, Hilger S, McKinney M, et al. 2001. Induction of nitric-oxide synthase and activation of NF-kappaB by interleukin-12 p40 in microglial cells. J Biol Chem 276: 7899.

    Article  CAS  PubMed  Google Scholar 

  • Pannu R, Won JS, Khan M, Singh AK, Singh I. 2004. A novel role of lactosylceramide in the regulation of lipopolysaccharide/interferon-gamma-mediated inducible nitric oxide synthase gene expression: Implications for neuroinflammatory diseases. J Neurosci 24: 5942.

    Article  CAS  PubMed  Google Scholar 

  • Park HS, Huh SH, Kim MS, Lee SH, Choi EJ. 2000. Nitric oxide negatively regulates c- Jun N-terminal kinase/stress-activated protein kinase by means of S-nitrosylation. Proc Natl Acad Sci USA 97: 14382.

    Article  CAS  PubMed  Google Scholar 

  • Parkinson JF, Mitrovic B, Merrill JE. 1997. The role of nitric oxide in multiple sclerosis. J Mol Med 75: 174.

    Article  CAS  PubMed  Google Scholar 

  • Peng HB, Libby P, Liao JK. 1995. Induction and stabilization of I kappa B alpha by nitric oxide mediates inhibition of NF-kappa B. J Biol Chem 270: 14214.

    Article  CAS  PubMed  Google Scholar 

  • Piccio L, Rossi B, Scarpini E, Laudanna C, Giagulli C, et al. 2002. Molecular mechanisms involved in lymphocyte recruitment in inflamed brain microvessels: Critical roles for P-selectin glycoprotein ligand-1 and heterotrimeric G(i)-linked receptors. J Immunol 168: 1940.

    CAS  PubMed  Google Scholar 

  • Pitt D, Werner P, Raine CS. 2000. Glutamate excitotoxicity in a model of multiple sclerosis. Nat Med 6: 67.

    Article  CAS  PubMed  Google Scholar 

  • Pitt D, Nagelmeier IE, Wilson HC, Raine CS. 2003. Glutamate uptake by oligodendrocytes: Implications for excitotoxicity in multiple sclerosis. Neurology 61: 1113.

    CAS  PubMed  Google Scholar 

  • Popp R, Fleming I, Busse R. 1998. Pulsatile stretch in coronary arteries elicits release of endothelium-derived hyperpolarizing factor: A modulator of arterial compliance. Circ Res 82: 696.

    CAS  PubMed  Google Scholar 

  • Radi R, Beckman JS, Bush KM, Freeman BA. 1991. Peroxynitrite-induced membrane lipid peroxidation: The cytotoxic potential of superoxide and nitric oxide. Arch Biochem Biophys 288: 481.

    Article  CAS  PubMed  Google Scholar 

  • Ravi K, Brennan LA, Levic S, Ross PA, Black SM. 2004. S-nitrosylation of endothelial nitric oxide synthase is associated with monomerization and decreased enzyme activity. Proc Natl Acad Sci USA 101: 2619.

    Article  CAS  PubMed  Google Scholar 

  • Reynaert NL, Ckless K, Korn SH, Vos N, Guala AS, et al. 2004. Nitric oxide represses inhibitory kappaB kinase through S-nitrosylation. Proc Natl Acad Sci USA 101: 8945.

    Article  CAS  PubMed  Google Scholar 

  • Rock RB, Gekker G, Hu S, Sheng WS, Cheeran M, et al. 2004. Role of microglia in central nervous system infections. Clin Microbiol Rev 17: 942.

    Article  CAS  PubMed  Google Scholar 

  • Rosin C, Bates TE, Skaper SD. 2004. Excitatory amino acid induced oligodendrocyte cell death in vitro: Receptor-dependent and -independent mechanisms. J Neurochem 90: 1173.

    Article  CAS  PubMed  Google Scholar 

  • Roy A, Fung YK, Liu X, Pahan K. 2006. Up-regulation of microglial CD11b expression by nitric oxide. J Biol Chem 281: 14971.

    Article  CAS  PubMed  Google Scholar 

  • Saha RN, Pahan K. 2006. Regulation of inducible nitric oxide synthase gene in glial cells. Antioxid Redox Signal 8: 929.

    Article  CAS  PubMed  Google Scholar 

  • Saha RN, Pahan K. 2006a. Signals for the induction of nitric oxide synthase in astrocytes. Neurochem Int 49: 154.

    Article  CAS  Google Scholar 

  • Scott GS, Virag L, Szabo C, Hooper DC. 2003. Peroxynitrite-induced oligodendrocyte toxicity is not dependent on poly(ADP-ribose) polymerase activation. Glia 41: 105.

    Article  PubMed  Google Scholar 

  • Scott GS, Spitsin SV, Kean RB, Mikheeva T, Koprowski H, et al. 2002. Therapeutic intervention in experimental allergic encephalomyelitis by administration of uric acid precursors. Proc Natl Acad Sci USA 99: 16303.

    Article  CAS  PubMed  Google Scholar 

  • Shigemori Y, Katayama Y, Mori T, Maeda T, Kawamata T. 2006. Matrix metalloproteinase-9 is associated with blood-brain barrier opening and brain edema formation after cortical contusion in rats. Acta Neurochir Suppl 96: 130.

    Article  CAS  PubMed  Google Scholar 

  • Simmons ML, Murphy S. 1992. Induction of nitric oxide synthase in glial cells. J Neurochem 59: 897.

    Article  CAS  PubMed  Google Scholar 

  • Staddon JM, Herrenknecht K, Smales C, Rubin LL. 1995. Evidence that tyrosine phosphorylation may increase tight junction permeability. J Cell Sci 108: 609.

    CAS  PubMed  Google Scholar 

  • Stojkovic T, Colin C, Le Saux F, Jacque C. 1998. Specific pattern of nitric oxide synthase expression in glial cells after hippocampal injury. Glia 22: 329.

    Article  CAS  PubMed  Google Scholar 

  • Takao T, Flint N, Lee L, Ying X, Merrill J, et al. 2004. 17beta-estradiol protects oligodendrocytes from cytotoxicity induced cell death. J Neurochem 89: 660.

    Article  CAS  PubMed  Google Scholar 

  • Touil T, Deloire-Grassin MS, Vital C, Petry KG, Brochet B. 2001. In vivo damage of CNS myelin and axons induced by peroxynitrite. Neuroreport 12: 3637.

    Article  CAS  PubMed  Google Scholar 

  • Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mork S, et al. 1998. Axonal transection in the lesions of multiple sclerosis. N Engl J Med 338: 278.

    Article  CAS  PubMed  Google Scholar 

  • Tuohy, VK, Sobel, RA, Less MB. 1988. Myelin proteolipid protein-induced experimental allergic encephalomyelitis. J Immunol 140: 1868.

    CAS  PubMed  Google Scholar 

  • Whiteman M, Ketsawatsakul U, Halliwell B. 2002. A reassessment of the peroxynitrite scavenging activity of uric acid. Ann N Y Acad Sci 962: 242.

    Article  CAS  PubMed  Google Scholar 

  • Won JS, Im YB, Singh AK, Singh I. 2004. Dual role of cAMP in iNOS expression in glial cells and macrophages is mediated by differential regulation of p38-MAPK/ATF-2 activation and iNOS stability. Free Radic Biol Med 37: 1834.

    Article  CAS  PubMed  Google Scholar 

  • Won JS, Im YB, Key L, Singh I, Singh AK. 2003. The involvement of glucose metabolism in the regulation of inducible nitric oxide synthase gene expression in glial cells: Possible role of glucose-6-phosphate dehydrogenase and CCAAT/enhancing binding protein. J Neurosci 23: 7470.

    CAS  PubMed  Google Scholar 

  • Wong D, Prameya R, Dorovini-Zis K, Vincent SR. 2004. Nitric oxide regulates interactions of PMN with human brain microvessel endothelial cells. Biochem Biophys Res Commun 233: 142.

    Article  CAS  Google Scholar 

  • Wong D, Prameya R, Wu V, Dorovini-Zis K, Vincent SR. 2005. Nitric oxide reduces T lymphocyte adhesion to human brain microvessel endothelial cells via a cGMP-dependent pathway. Eur J Pharmacol 514: 91.

    Article  CAS  PubMed  Google Scholar 

  • Yednock TA, Cannon C, Fritz LC, Sanchez-Madrid F, Steinman L, et al. 1992. Prevention of experimental autoimmune encephalomyelitis by antibodies against alpha 4 beta 1 integrin. Nature 356: 63.

    Article  CAS  PubMed  Google Scholar 

  • Yuceyar N, Taskiran D, Sagduyu A. 2001. Serum and cerebrospinal fluid nitrite and nitrate levels in relapsing-remitting and secondary progressive multiple sclerosis patients. Clin Neurol Neurosurg 103: 206.

    Article  CAS  PubMed  Google Scholar 

  • Zhao W, Tilton RG, Corbett JA, McDaniel ML, Misko TP, et al. 1996. Experimental allergic encephalomyelitis in the rat is inhibited by aminoguanidine, an inhibitor of nitric oxide synthase. J Neuroimmunol 64: 123.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by grants from NIH (NS39940 and NS48923), National Multiple Sclerosis Society (RG3422A1/1), and Michael J. Fox Foundation for Parkinson Research.

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science+Business Media, LLC

About this entry

Cite this entry

Brahmachari, S., Pahan, K. (2009). Nitric Oxide in Experimental Allergic Encephalomyelitis. In: Lajtha, A., Banik, N., Ray, S.K. (eds) Handbook of Neurochemistry and Molecular Neurobiology. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-30375-8_13

Download citation

Publish with us

Policies and ethics