Journal of Neuroimmunology
Volume 229, Issue 1 , Pages 146-156 , 15 December 2010

In vitro and in vivo induction and activation of nNOS by LPS in oligodendrocytes

  • S.Y. Yao

      Affiliations

    • Department of Neurology, Multiple Sclerosis Research Center, Nashville, TN 37212, USA
    • ,
  • A. Ljunggren-Rose

      Affiliations

    • Department of Neurology, Multiple Sclerosis Research Center, Nashville, TN 37212, USA
    • ,
  • N. Chandramohan

      Affiliations

    • Department of Neurology, Multiple Sclerosis Research Center, Nashville, TN 37212, USA
    • ,
  • W.O. Whetsell Jr.

      Affiliations

    • Department of Pathology, Vanderbilt University Medical Center, Nashville, TN 37212, USA
    • ,
  • S. Sriram

      Affiliations

    • Department of Neurology, Multiple Sclerosis Research Center, Nashville, TN 37212, USA
    • Corresponding Author InformationCorresponding author. Dept of Neurology, Vanderbilt Medical Center, Nashville, TN 37212, USA. Tel.: +1 615 963 4044; fax: +1 615 321 5247.

Received 19 May 2010 ,Revised 25 July 2010 ,Accepted 27 July 2010.

References 

  1. Akassoglou K, Bauer J, Kassiotis G, Pasparakis M, Lassmann H, Kollias G, et al. Oligodendrocyte apoptosis and primary demyelination induced by local TNF/p55TNF receptor signaling in the central nervous system of transgenic mice: models for multiple sclerosis with primary oligodendrogliopathy. Am. J. Pathol. 1998;153:801–813
  2. Baud O, Li J, Zhang Y, Neve RL, Volpe JJ, Rosenberg PA. Nitric oxide-induced cell death in developing oligodendrocytes is associated with mitochondrial dysfunction and apoptosis-inducing factor translocation. Eur. J. Neurosci. 2004;20:1713–1726
  3. Bhat NR, Zhang P, Bhat AN. Cytokine induction of inducible nitric oxide synthase in an oligodendrocyte cell line: role of p38 mitogen-activated protein kinase activation. J. Neurochem. 1999;72:472–478
  4. Birgbauer E, Rao TS, Webb M. Lysolecithin induces demyelination in vitro in a cerebellar slice culture system. J. Neurosci. Res. 2004;78:157–166
  5. Bitsch A, Schuchardt J, Bunkowski S, Kuhlmann T, Bruck W. Acute axonal injury in multiple sclerosis. Correlation with demyelination and inflammation.. Brain. 2000;123(Pt 6):1174–1183
  6. Boullerne AI, Benjamins JA. Nitric oxide synthase expression and nitric oxide toxicity in oligodendrocytes. Antioxid. Redox Signal. 2006;8:967–980
  7. Boulouard M, Schumann-Bard P, Butt-Gueulle S, Lohou E, Stiebing S, Collot V, et al. 4-substituted indazoles as new inhibitors of neuronal nitric oxide synthase. Bioorg. Med. Chem. Lett. 2007;17:3177–3180
  8. Bradl M, Lassmann H. Oligodendrocytes: biology and pathology. Acta Neuropathol. 2009;119:37–53
  9. Bradl M, Lassmann H. Progressive multiple sclerosis. Semin. Immunopathol. 2009;31:455–465
  10. Brahic M, Bureau JF, Michiels T. The genetics of the persistent infection and demyelinating disease caused by Theiler's virus. Annu. Rev. Microbiol. 2005;59:279–298
  11. Brannan CA, Roberts MR. Resident microglia from adult mice are refractory to nitric oxide-inducing stimuli due to impaired NOS2 gene expression. Glia. 2004;48:120–131
  12. Brown GC, Bal-Price A. Inflammatory neurodegeneration mediated by nitric oxide, glutamate, and mitochondria. Mol. Neurobiol. 2003;27:325–355
  13. Brundin L, Morcos E, Olsson T, Wiklund NP, Andersson M. Increased intrathecal nitric oxide formation in multiple sclerosis; cerebrospinal fluid nitrite as activity marker. Eur. J. Neurol. 1999;6:585–590
  14. Bsibsi M, Ravid R, Gveric D, van Noort JM. Broad expression of Toll-like receptors in the human central nervous system: the toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J. Neuropathol. Exp. Neurol. 2002;61:1013–1021
  15. Calabrese V, Scapagnini G, Ravagna A, Bella R, Foresti R, Bates TE, et al. Nitric oxide synthase is present in the cerebrospinal fluid of patients with active multiple sclerosis and is associated with increases in cerebrospinal fluid protein nitrotyrosine and S-nitrosothiols and with changes in glutathione levels. J. Neurosci. Res. 2002;70:580–587
  16. Campbell IL. Structural and functional impact of the transgenic expression of cytokines in the CNS. Ann. NY Acad. Sci. 1998;840:83–96
  17. Colello RJ, Sato-Bigbee C. Purification of oligodendrocytes and their progenitors using immunomagnetic separation and Percoll gradient centrifugation. Curr. Protoc. Neurosci. 2001;3–12Chapter 3, Unit
  18. Compston A, Coles A. Multiple sclerosis. Lancet. 2008;372:1502–1517
  19. Cordelier P, Esteve JP, Najib S, Moroder L, Vaysse N, Pradayrol L, et al. Regulation of neuronal nitric-oxide synthase activity by somatostatin analogs following SST5 somatostatin receptor activation. J. Biol. Chem. 2006;281:19156–19171
  20. Cua DJ, Groux H, Hinton DR, Stohlman SA, Coffman RL. Transgenic interleukin 10 prevents induction of experimental autoimmune encephalomyelitis. J. Exp. Med. 1999;189:1005–1010
  21. Dalton DK, Wittmer S. Nitric-oxide-dependent and independent mechanisms of protection from CNS inflammation during Th1-mediated autoimmunity: evidence from EAE in iNOS KO mice. J. Neuroimmunol. 2005;160:110–121
  22. Ding M, St Pierre BA, Parkinson JF, Medberry P, Wong JL, Rogers NE, et al. Inducible nitric-oxide synthase and nitric oxide production in human fetal astrocytes and microglia. A kinetic analysis.. J. Biol. Chem. 1997;272:11327–11335
  23. Felts PA, Woolston A-M, Fernando HB, Asquith S, Gregson NA, Mizzi OJ, et al. Inflammation and primary demyelination induced by the intraspinal injection of lipopolysaccharide. Brain. 2005;128:1649–1666
  24. Fenyk-Melody JE, Garrison AE, Brunnert SR, Weidner JR, Shen F, Shelton BA, et al. Experimental autoimmune encephalomyelitis is exacerbated in mice lacking the NOS2 gene. J. Immunol. 1998;160:2940–2946
  25. Ghafourifar P, Cadenas E. Mitochondrial nitric oxide synthase. Trends Pharmacol. Sci. 2005;26:190–195
  26. Ghafourifar P, Sen CK. Mitochondrial nitric oxide synthase. Front. Biosci. 2007;12:1072–1078
  27. Giovannoni G. Cerebrospinal fluid and serum nitric oxide metabolites in patients with multiple sclerosis. Mult. Scler. 1998;4:27–30
  28. Giulivi C. Characterization and function of mitochondrial nitric-oxide synthase. Free Radic. Biol. Med. 2003;34:397–408
  29. Haynes V, Elfering S, Traaseth N, Giulivi C. Mitochondrial nitric-oxide synthase: enzyme expression, characterization, and regulation. J. Bioenerg. Biomembr. 2004;36:341–346
  30. Hewett JA, Hewett SJ, Winkler S, Pfeiffer SE. Inducible nitric oxide synthase expression in cultures enriched for mature oligodendrocytes is due to microglia. J. Neurosci. Res. 1999;56:189–198
  31. Horwitz MS, Evans CF, McGavern DB, Rodriguez M, Oldstone MB. Primary demyelination in transgenic mice expressing interferon-gamma. Nat. Med. 1997;3:1037–1041
  32. Jack C, Antel J, Bruck W, Kuhlmann T. Contrasting potential of nitric oxide and peroxynitrite to mediate oligodendrocyte injury in multiple sclerosis. Glia. 2007;55:926–934
  33. Jack C, Ruffini F, Bar-Or A, Antel JP. Microglia and multiple sclerosis. J. Neurosci. Res. 2005;81:363–373
  34. Kanai AJ, Pearce LL, Clemens PR, Birder LA, VanBibber MM, Choi SY, et al. Identification of a neuronal nitric oxide synthase in isolated cardiac mitochondria using electrochemical detection. Proc. Natl Acad. Sci. USA. 2001;98:14126–14131
  35. Kugler P, Drenckhahn D. Astrocytes and Bergmann glia as an important site of nitric oxide synthase I. Glia. 1996;16:165–173
  36. Li J, Baud O, Vartanian T, Volpe JJ, Rosenberg PA. Peroxynitrite generated by inducible nitric oxide synthase and NADPH oxidase mediates microglial toxicity to oligodendrocytes. Proc. Natl Acad. Sci. USA. 2005;102:9936–9941
  37. Linares D, Taconis M, Mana P, Correcha M, Fordham S, Staykova M, et al. Neuronal nitric oxide synthase plays a key role in CNS demyelination. J. Neurosci. 2006;26:12672–12681
  38. Lipton SA, Gu Z, Nakamura T. Inflammatory mediators leading to protein misfolding and uncompetitive/fast off-rate drug therapy for neurodegenerative disorders. Int. Rev. Neurobiol. 2007;82:1–27
  39. Marik C, Felts PA, Bauer J, Lassmann H, Smith KJ. Lesion genesis in a subset of patients with multiple sclerosis: a role for innate immunity?. Brain. 2007;130:2800–2815
  40. Matsushima GK, Morell P. The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol. 2001;11:107–116
  41. Merrill JE, Matsushima K. Production of and response to interleukin 1 by cloned human oligodendroglioma cell lines. J. Biol. Regul. Homeost. Agents. 1988;2:77–86
  42. Merrill JE, Murphy SP, Mitrovic B, Mackenzie-Graham A, Dopp JC, Ding M, et al. Inducible nitric oxide synthase and nitric oxide production by oligodendrocytes. J. Neurosci. Res. 1997;48:372–384
  43. Molina-Holgado E, Vela JM, Arevalo-Martin A, Guaza C. LPS/IFN-gamma cytotoxicity in oligodendroglial cells: role of nitric oxide and protection by the anti-inflammatory cytokine IL-10. Eur. J. Neurosci. 2001;13:493–502
  44. Owens T. Toll-like receptors in neurodegeneration. Curr. Top. Microbiol. Immunol. 2009;336:105–120
  45. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 2007;87:315–424
  46. Pacher P, Szabo C. Role of the peroxynitrite-poly(ADP-ribose) polymerase pathway in human disease. Am. J. Pathol. 2008;173:2–13
  47. Pearce LL, Kanai AJ, Birder LA, Pitt BR, Peterson J. The catabolic fate of nitric oxide: the nitric oxide oxidase and peroxynitrite reductase activities of cytochrome oxidase. J. Biol. Chem. 2002;277:13556–13562
  48. Perez-Rodriguez R, Roncero C, Olivan AM, Gonzalez MP, Oset-Gasque MJ. Signaling mechanisms of interferon gamma induced apoptosis in chromaffin cells: involvement of nNOS, iNOS, and NFkappaB. J. Neurochem. 2009;108:1083–1096
  49. Radi R, Cassina A, Hodara R, Quijano C, Castro L. Peroxynitrite reactions and formation in mitochondria. Free Radic. Biol. Med. 2002;33:1451–1464
  50. Rejdak K, Eikelenboom MJ, Petzold A, Thompson EJ, Stelmasiak Z, Lazeron RH, et al. CSF nitric oxide metabolites are associated with activity and progression of multiple sclerosis. Neurology. 2004;63:1439–1445
  51. Rejdak K, Petzold A, Sharpe MA, Kay AD, Kerr M, Keir G, et al. Cerebrospinal fluid nitrite/nitrate correlated with oxyhemoglobin and outcome in patients with subarachnoid hemorrhage. J. Neurol. Sci. 2004;219:71–76
  52. Rejdak K, Petzold A, Stelmasiak Z, Giovannoni G. Cerebrospinal fluid brain specific proteins in relation to nitric oxide metabolites during relapse of multiple sclerosis. Mult. Scler. 2008;14:59–66
  53. Smith KJ, Kapoor R, Hall SM, Davies M. Electrically active axons degenerate when exposed to nitric oxide. Ann. Neurol. 2001;49:470–476
  54. Smith KJ, Lassmann H. The role of nitric oxide in multiple sclerosis. Lancet Neurol. 2002;1:232–241
  55. Tolias CM, McNeil CJ, Kazlauskaite J, Hillhouse EW. Superoxide generation from constitutive nitric oxide synthase in astrocytes in vitro regulates extracellular nitric oxide availability. Free Radic. Biol. Med. 1999;26:99–106
  56. van Noort JM, Bsibsi M. Toll-like receptors in the CNS: implications for neurodegeneration and repair. Prog. Brain Res. 2009;175:139–148
  57. Wizemann TM, Gardner CR, Laskin JD, Quinones S, Durham SK, Goller NL, et al. Production of nitric oxide and peroxynitrite in the lung during acute endotoxemia. J. Leukoc. Biol. 1994;56:759–768
  58. Yao S, Pandey P, Rose A, Sriram S. LPS mediated injury to oligodendrocytes is mediated by the activation of nNOS: relevance to human demyelinating disease. Nitric Oxide. 2009;22:197–204
  59. Yuan Z, Liu B, Yuan L, Zhang Y, Dong X, Lu J. Evidence of nuclear localization of neuronal nitric oxide synthase in cultured astrocytes of rats. Life Sci. 2004;74:3199–3209
  60. Yuan ZR, Liu B, Zhang Y, Yuan L, Muteliefu G, Lu J. Upregulated expression of neuronal nitric oxide synthase by insulin in both neurons and astrocytes. Brain Res. 2004;1008:1–10
  61. Zeis T, Graumann U, Reynolds R, Schaeren-Wiemers N. Normal-appearing white matter in multiple sclerosis is in a subtle balance between inflammation and neuroprotection. Brain. 2008;131:288–303
  62. Zeis T, Probst A, Steck AJ, Stadelmann C, Bruck W, Schaeren-Wiemers N. Molecular changes in white matter adjacent to an active demyelinating lesion in early multiple sclerosis. Brain Pathol. 2009;19:459–466

PII: S0165-5728(10)00336-X

doi: 10.1016/j.jneuroim.2010.07.023

Journal of Neuroimmunology
Volume 229, Issue 1 , Pages 146-156 , 15 December 2010

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