NNOS mediated mitochondrial injury in LPS stimulated oligodendrocytes

Mitochondrion

Volumn 12, Issue 2, 2012, Pages 336-344

  Yao, S Y ^a   Natarajan, C ^a   Sriram, S ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Demyelination; INOS; LPS; Mitochondria; NNOS; Oligodendrocyte

Indexed keywords

7 NITROINDAZOLE; APOPTOSIS INDUCING FACTOR; CYTOCHROME C; CYTOCHROME C OXIDASE; INDUCIBLE NITRIC OXIDE SYNTHASE; NEURONAL NITRIC OXIDE SYNTHASE; PROTEIN KINASE B; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; CYTOSOL; DEMYELINATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; INNATE IMMUNITY; MITOCHONDRIAL MEMBRANE POTENTIAL; NERVE CELL LESION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN TRANSPORT; RAT; RESPIRATORY CHAIN;

ANIMALS; APOPTOSIS; CELL SURVIVAL; CELLS, CULTURED; CYTOCHROMES C; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX IV; LIPOPOLYSACCHARIDES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NITRIC OXIDE SYNTHASE; OLIGODENDROGLIA; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84858009125     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2012.01.002     Document Type: Article

References (63)

1. Akassoglou K., Bauer J., Kassiotis G., Pasparakis M., Lassmann H., Kollias G., Probert L. 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. Aravalli R.N., Peterson P.K., Lokensgard J.R. Toll-like receptors in defense and damage of the central nervous system. J. Neuroimmune Pharmacol. 2007, 2:297-312.
3. Basu S., Pathak S.K., Banerjee A., Pathak S., Bhattacharyya A., Yang Z., Talarico S., Kundu M., Basu J. Execution of macrophage apoptosis by PE_PGRS33 of Mycobacterium tuberculosis is mediated by Toll-like receptor 2-dependent release of tumor necrosis factor-alpha. J. Biol. Chem. 2007, 282:1039-1050.
4. Baud O., Li J., Zhang Y., Neve R.L., Volpe J.J., Rosenberg P.A. 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.
5. Bhat N.R., Zhang P., Bhat A.N. 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.
6. Boullerne A.I., Benjamins J.A. 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., Rault S. 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. Brannan C.A., Roberts M.R. Resident microglia from adult mice are refractory to nitric oxide-inducing stimuli due to impaired NOS2 gene expression. Glia 2004, 48:120-131.
11. Brundin L., Morcos E., Olsson T., Wiklund N.P., Andersson M. Increased intrathecal nitric oxide formation in multiple sclerosis; cerebrospinal fluid nitrite as activity marker. Eur. J. Neurol. 1999, 6:585-590.
12. Bsibsi M., Ravid R., Gveric D., van Noort J.M. 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.
13. Buntinx M., Stinissen P., Steels P., Ameloot M., Raus J. Immune-mediated oligodendrocyte injury in multiple sclerosis: molecular mechanisms and therapeutic interventions. Crit. Rev. Immunol. 2002, 22:391-424.
14. Calabrese V., Scapagnini G., Ravagna A., Bella R., Foresti R., Bates T.E., Giuffrida Stella A.M., Pennisi G. 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.
15. Campbell I.L. Structural and functional impact of the transgenic expression of cytokines in the CNS. Ann. N. Y. Acad. Sci. 1998, 840:83-96.
16. Chaurasia B., Mauer J., Koch L., Goldau J., Kock A.S., Bruning J.C. Phosphoinositide-dependent kinase 1 provides negative feedback inhibition to Toll-like receptor-mediated NF-kappaB activation in macrophages. Mol. Cell. Biol. 2010, 30:4354-4366.
17. Colello R.J., Sato-Bigbee C. Purification of oligodendrocytes and their progenitors using immunomagnetic separation and Percoll gradient centrifugation. Curr. Protoc. Neurosci. 2001, 3:1-14. (Chapter 12).
18. Compston A., Coles A. Multiple sclerosis. Lancet 2008, 372:1502-1517.
19. Cordelier P., Esteve J.P., Najib S., Moroder L., Vaysse N., Pradayrol L., Susini C., Buscail L. Regulation of neuronal nitric-oxide synthase activity by somatostatin analogs following SST5 somatostatin receptor activation. J. Biol. Chem. 2006, 281:19156-19171.
20. Cregan S.P., Dawson V.L., Slack R.S. Role of AIF in caspase-dependent and caspase-independent cell death. Oncogene 2004, 23:2785-2796.
21. Cua D.J., Groux H., Hinton D.R., Stohlman S.A., Coffman R.L. Transgenic interleukin 10 prevents induction of experimental autoimmune encephalomyelitis. J. Exp. Med. 1999, 189:1005-1010.
22. Cudrici C., Niculescu T., Niculescu F., Shin M.L., Rus H. Oligodendrocyte cell death in pathogenesis of multiple sclerosis: protection of oligodendrocytes from apoptosis by complement. J. Rehabil. Res. Dev. 2006, 43:123-132.
23. Denis M. Human monocytes/macrophages: NO or no NO?. J. Leukoc. Biol. 1994, 55:682-684.
24. Domercq M., Etxebarria E., Perez-Samartin A., Matute C. Excitotoxic oligodendrocyte death and axonal damage induced by glutamate transporter inhibition. Glia 2005, 52:36-46.
25. Duncan A.J., Heales S.J. Nitric oxide and neurological disorders. Mol. Aspects Med. 2005, 26:67-96.
26. Follett P.L., Deng W., Dai W., Talos D.M., Massillon L.J., Rosenberg P.A., Volpe J.J., Jensen F.E. Glutamate receptor-mediated oligodendrocyte toxicity in periventricular leukomalacia: a protective role for topiramate. J. Neurosci. 2004, 24:4412-4420.
27. Ghafourifar P., Cadenas E. Mitochondrial nitric oxide synthase. Trends Pharmacol. Sci. 2005, 26:190-195.
28. Giovannoni G. Cerebrospinal fluid and serum nitric oxide metabolites in patients with multiple sclerosis. Mult. Scler. 1998, 4:27-30.
29. Giovannoni G., Heales S.J., Land J.M., Thompson E.J. The potential role of nitric oxide in multiple sclerosis. Mult. Scler. 1998, 4:212-216.
30. Giulivi C. Characterization and function of mitochondrial nitric-oxide synthase. Free Radic. Biol. Med. 2003, 34:397-408.
31. Giulivi C., Kato K., Cooper C.E. Nitric oxide regulation of mitochondrial oxygen consumption I: cellular physiology. Am. J. Physiol. Cell Physiol. 2006, 291:C1225-C1231.
32. Hewett J.A., Hewett S.J., Winkler S., Pfeiffer S.E. Inducible nitric oxide synthase expression in cultures enriched for mature oligodendrocytes is due to microglia. J. Neurosci. Res. 1999, 56:189-198.
33. Hill K.E., Zollinger L.V., Watt H.E., Carlson N.G., Rose J.W. Inducible nitric oxide synthase in chronic active multiple sclerosis plaques: distribution, cellular expression and association with myelin damage. J. Neuroimmunol. 2004, 151:171-179.
34. Horwitz M.S., Evans C.F., McGavern D.B., Rodriguez M., Oldstone M.B. Primary demyelination in transgenic mice expressing interferon-gamma. Nat. Med. 1997, 3:1037-1041.
35. Ignarro L.J., Cirino G., Casini A., Napoli C. Nitric oxide as a signaling molecule in the vascular system: an overview. J. Cardiovasc. Pharmacol. 1999, 34:879-886.
36. Ishii K.J., Takeshita F., Gursel I., Gursel M., Conover J., Nussenzweig A., Klinman D.M. Potential role of phosphatidylinositol 3 kinase, rather than DNA-dependent protein kinase, in CpG DNA-induced immune activation. J. Exp. Med. 2002, 196:269-274.
37. 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.
38. Jack C., Ruffini F., Bar-Or A., Antel J.P. Microglia and multiple sclerosis. J. Neurosci. Res. 2005, 81:363-373.
39. Kieseier B.C., Hemmer B., Hartung H.P. Multiple sclerosis-novel insights and new therapeutic strategies. Curr. Opin. Neurol. 2005, 18:211-220.
40. Lai Y., Thomas G.D., Yue Y., Yang H.T., Li D., Long C., Judge L., Bostick B., Chamberlain J.S., Terjung R.L., Duan D. Dystrophins carrying spectrin-like repeats 16 and 17 anchor nNOS to the sarcolemma and enhance exercise performance in a mouse model of muscular dystrophy. J. Clin. Invest. 2009, 119:624-635.
41. Lehnardt S., Lachance C., Patrizi S., Lefebvre S., Follett P.L., Jensen F.E., Rosenberg P.A., Volpe J.J., Vartanian T. The toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J. Neurosci. 2002, 22:2478-2486.
42. Makela S.M., Osterlund P., Julkunen I. TLR ligands induce synergistic interferon-beta and interferon-lambda1 gene expression in human monocyte-derived dendritic cells. Mol. Immunol. 2011, 48:505-515.
43. Matute C., Alberdi E., Domercq M., Perez-Cerda F., Perez-Samartin A., Sanchez-Gomez M.V. The link between excitotoxic oligodendroglial death and demyelinating diseases. Trends Neurosci. 2001, 24:224-230.
44. Molina-Holgado E., Vela J.M., 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.
45. Munshi N., Fernandis A.Z., Cherla R.P., Park I.W., Ganju R.K. Lipopolysaccharide-induced apoptosis of endothelial cells and its inhibition by vascular endothelial growth factor. J. Immunol. 2002, 168:5860-5866.
46. Pacher P., Beckman J.S., Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 2007, 87:315-424.
47. Peltier D.C., Simms A., Farmer J.R., Miller D.J. Human neuronal cells possess functional cytoplasmic and TLR-mediated innate immune pathways influenced by phosphatidylinositol-3 kinase signaling. J. Immunol. 2010, 184:7010-7021.
48. Perez-Rodriguez R., Roncero C., Olivan A.M., Gonzalez M.P., Oset-Gasque M.J. Signaling mechanisms of interferon gamma induced apoptosis in chromaffin cells: involvement of nNOS, iNOS, and NFkappaB. J. Neurochem. 2009, 108:1083-1096.
49. 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.
50. Rodriguez M., Scheithauer B.W., Forbes G., Kelly P.J. Oligodendrocyte injury is an early event in lesions of multiple sclerosis. Mayo Clin. Proc. 1993, 68:627-636.
51. Salaun B., Romero P., Lebecque S. Toll-like receptors' two-edged sword: when immunity meets apoptosis. Eur. J. Immunol. 2007, 37:3311-3318.
52. Schneemann M., Schoeden G. Macrophage biology and immunology: man is not a mouse. J. Leukoc. Biol. 2007, 81:579. discussion 580.
53. Schneemann M., Schoedon G., Linscheid P., Walter R., Blau N., Schaffner A. Nitrite generation in interleukin-4-treated human macrophage cultures does not involve the nitric oxide synthase pathway. J. Infect. Dis. 1997, 175:130-135.
54. Sloane J.A., Batt C., Ma Y., Harris Z.M., Trapp B., Vartanian T. Hyaluronan blocks oligodendrocyte progenitor maturation and remyelination through TLR2. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:11555-11560.
55. Taylor D.L., Pirianov G., Holland S., McGinnity C.J., Norman A.L., Reali C., Diemel L.T., Gveric D., Yeung D., Mehmet H. Attenuation of proliferation in oligodendrocyte precursor cells by activated microglia. J. Neurosci. Res. 2010, 88:1632-1644.
56. Tolias C.M., McNeil C.J., Kazlauskaite J., Hillhouse E.W. Superoxide generation from constitutive nitric oxide synthase in astrocytes in vitro regulates extracellular nitric oxide availability. Free Radic. Biol. Med. 1999, 26:99-106.
57. Watts C., West M.A., Zaru R. TLR signalling regulated antigen presentation in dendritic cells. Curr. Opin. Immunol. 2010, 22:124-130.
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 2010, 22(3):109-204.
59. Yao S.Y., Rose A., Chandramohan N., Whetsell W., Sriram S. In vitro and in vivo induction and activation of nNOS by LPS in oligodendrocytes. J. Neuroimmunol. 2010, 229:145-156.
60. 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.
61. Yuan Z.R., 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.
62. 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.
63. Zeis T., Probst A., Steck A.J., 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.