Immunology and oxidative stress in multiple sclerosis: Clinical and basic approach

Clinical and Developmental Immunology

Volumn 2013, Issue , 2013, Pages

  Ortiz, Genaro G ^a   Pacheco Moisés, Fermín P ^b   Bitzer Quintero, Oscar K ^a   Ramírez Anguiano, Ana C ^b   Flores Alvarado, Luis J ^b   Ramírez Ramírez, Viridiana ^a   Macias Islas, Miguel A ^a   Torres Sánchez, Erandis D ^a  

^a INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^b UNIVERSITY OF GUADALAJARA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; ARYLDIALKYLPHOSPHATASE; ASCORBIC ACID; AUTOIMMUNE REGULATOR PROTEIN; BETA INTERFERON; CD28 ANTIGEN; CD39 ANTIGEN; CD40 ANTIGEN; CYTOKINE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; IMMUNOGLOBULIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 3; MYELIN; POLYUNSATURATED FATTY ACID; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR NRF2; URIC ACID; ANTIOXIDANT;

AUTOIMMUNE DISEASE; BLOOD BRAIN BARRIER; BRAIN STEM; CENTRAL NERVOUS SYSTEM; CEREBROSPINAL FLUID; DEMYELINATION; GLIOSIS; HUMAN; IMMUNE RESPONSE; IMMUNOLOGY; INFLAMMATION; LIPID PEROXIDATION; LYMPHOCYTE; MACROPHAGE; MICROGLIA; MULTIPLE SCLEROSIS; NERVE FIBER; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN MODIFICATION; REMYELINIZATION; REVIEW; SPINAL CORD; ANIMAL; METABOLISM;

ANIMALS; ANTIOXIDANTS; CYTOKINES; HUMANS; LIPID PEROXIDATION; MULTIPLE SCLEROSIS; NF-KAPPA B; OXIDATIVE STRESS;

EID: 84885601121     PISSN: 17402522     EISSN: 17402530     Source Type: Journal    
DOI: 10.1155/2013/708659     Document Type: Review

References (125)

1. Kakalacheva K., Lünemann J. D., Environmental triggers of multiple sclerosis. FEBS Letters 2011 585 23 3724 3729 2-s2.0-80052250727 10.1016/j.febslet.2011.04.006
2. Chitnis T., Role of puberty in multiple sclerosis risk and course. Clinical Immunology 2013 10.1016/j.clim.2013.03.014
3. Franciotta D., Salvetti M., Lolli F., Serafini B., Aloisi F., B cells and multiple sclerosis. The Lancet Neurology 2008 7 9 852 858 2-s2.0-48849117376 10.1016/S1474-4422(08)70192-3
4. Fletcher J. M., Lalor S. J., Sweeney C. M., Tubridy N., Mills K. H. G., T cells in multiple sclerosis and experimental autoimmune encephalomyelitis. Clinical and Experimental Immunology 2010 162 1 1 11 2-s2.0-77956536780 10.1111/j.1365-2249.2010.04143.x
5. Markovic-Plese S., Pinilla C., Martin R., The initiation of the autoimmune response in multiple sclerosis. Clinical Neurology and Neurosurgery 2004 106 3 218 222 2-s2.0-2642574823 10.1016/j.clineuro.2004.02.018 (Pubitemid 38716149)
6. Minagar A., Alexander J. S., Blood-brain barrier disruption in multiple sclerosis. Multiple Sclerosis 2003 9 6 540 549 2-s2.0-0344961161 10.1191/1352458503ms965oa (Pubitemid 37479401)
7. Zlokovic B. V., The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008 57 2 178 201 2-s2.0-38149090292 10.1016/j.neuron.2008.01.003
8. Miller D. H., Chard D. T., Ciccarelli O., Clinically isolated syndromes. The Lancet Neurology 2012 11 2 157 169 2-s2.0-84856023667 10.1016/S1474-4422(11) 70274-5
9. Poser C. M., The multiple sclerosis trait and the development of multiple sclerosis: genetic vulnerability and environmental effect. Clinical Neurology and Neurosurgery 2006 108 3 227 233 2-s2.0-33644619154 10.1016/j.clineuro.2005. 11.019
10. Alpayci M., Bozan N., Erdem S., Gunes M., Erden M., The possible underlying pathophysiological mechanisms for development of multiple sclerosis in familial Mediterranean fever. Medical Hypotheses 2012 78 6 717 720 2-s2.0-84860364485 10.1016/j.mehy.2012.02.017
11. Kapadia M., Sakic B., Autoimmune and inflammatory mechanisms of CNS damage. Progress in Neurobiology 2011 95 3 301 333 2-s2.0-80054110588 10.1016/j.pneurobio.2011.08.008
12. Longbrake E. E., Racke M. K., Why did IL-12/IL-23 antibody therapy fail in multiple sclerosis? Expert Review of Neurotherapeutics 2009 9 3 319 321 2-s2.0-66449113393 10.1586/14737175.9.3.319
13. Vollmer T. L., Wynn D. R., Alam S. M., Valdes J., A phase 2, 24-week, randomized, placebo-controlled, double-blind study examining the efficacy and safety of an anti-interleukin-12 and -23 monoclonal antibody in patients with relapsing-remitting or secondary progressive multiple sclerosis. Multiple Sclerosis 2011 17 2 181 191 2-s2.0-79951524055 10.1177/1352458510384496
14. Piccio L., Naismith R. T., Trinkaus K., Klein R. S., Parks B. J., Lyons J. A., Cross A. H., Changes in B- and T-lymphocyte and chemokine levels with rituximab treatment in multiple sclerosis. Archives of Neurology 2010 67 6 707 714 2-s2.0-77953341196 10.1001/archneurol.2010.99
15. Engel P., Gómez-Puerta J. A., Ramos-Casals M., Lozano F., Bosch X., Therapeutic targeting of B cells for rheumatic autoimmune diseases. Pharmacological Reviews 2011 63 1 127 156 2-s2.0-79952024055 10.1124/pr.109.002006
16. Racke M. K., Immunopathogenesis of multiple sclerosis. Annals of Indian Academy of Neurology 2009 12 4 215 220 2-s2.0-72949116951 10.4103/0972-2327. 58274
17. Brown G. C., Nitric oxide and neuronal death. Nitric Oxide 2010 23 3 153 165 2-s2.0-77956012154 10.1016/j.niox.2010.06.001
18. Herz J., Zipp F., Siffrin V., Neurodegeneration in autoimmune CNS inflammation. Experimental Neurology 2010 225 1 9 17 2-s2.0-77955659717 10.1016/j.expneurol.2009.11.019
19. Hemmer B., Hartung H.-P., Toward the development of rational therapies in multiple sclerosis: what is on the horizon? Annals of Neurology 2007 62 4 314 326 2-s2.0-36148952124 10.1002/ana.21289 (Pubitemid 350105946)
20. Trapp B. D., Nave K.-A., Multiple sclerosis: an immune or neurodegenerative disorder? Annual Review of Neuroscience 2008 31 247 269 2-s2.0-48249139449 10.1146/annurev.neuro.30.051606.094313
21. Dhib-Jalbut S., Arnold D. L., Cleveland D. W., Fisher M., Friedlander R. M., Mouradian M. M., Przedborski S., Trapp B. D., Wyss-Coray T., Wee Yong V., Neurodegeneration and neuroprotection in multiple sclerosis and other neurodegenerative diseases. Journal of Neuroimmunology 2006 176 1-2 198 215 2-s2.0-33746100700 10.1016/j.jneuroim.2006.03.027 (Pubitemid 44080333)
22. Stadelmann C., Wegner C., Brück W., Inflammation, demyelination, and degeneration-Recent insights from MS pathology. Biochimica et Biophysica Acta 2011 1812 2 275 282 2-s2.0-78650172976 10.1016/j.bbadis.2010.07.007
23. Constantinescu C. S., Farooqi N., O'Brien K., Gran B., Experimental autoimmune encephalomyelitis (EAE) as a model for multiple sclerosis (MS). British Journal of Pharmacology 2011 164 4 1079 1106 2-s2.0-80053300497 10.1111/j.1476-5381.2011.01302.x
24. Artemiadis A. K., Anagnostouli M. C., Apoptosis of oligodendrocytes and post-translational modifications of myelin basic protein in multiple sclerosis: possible role for the early stages of multiple sclerosis. European Neurology 2010 63 2 65 72 2-s2.0-73649144250 10.1159/000272940
25. Kostic M. S., Rajkovic J. S., Potic Floranovic M. S., Dimov I. D., Pavlovic D. D., Multiple sclerosis and oxidative stress: a clinical perspective. Neurochemical Journal 2013 7 1 76 86
26. Lipton H. L., Liang Z., Hertzler S., Son K.-N., A specific viral cause of multiple sclerosis: one virus, one disease. Annals of Neurology 2007 61 6 514 523 2-s2.0-34447504060 10.1002/ana.21116 (Pubitemid 47068133)
27. + T cells in multiple sclerosis. Nature Medicine 2008 14 11 1227 1235 2-s2.0-55549104692 10.1038/nm.1881
28. Goverman J., Autoimmune T cell responses in the central nervous system. Nature Reviews Immunology 2009 9 6 393 407 2-s2.0-67349216357 10.1038/nri2550
29. Nylander A., Hafler D. A., Multiple sclerosis. Journal of Clinical Investigation 2012 122 4 1180 1188 2-s2.0-84859724482 10.1172/JCI58649
30. Mahad D., Lassmann H., Turnbull D., Review: mitochondria and disease progression in multiple sclerosis. Neuropathology and Applied Neurobiology 2008 34 6 577 589 2-s2.0-56549086013 10.1111/j.1365-2990.2008.00987.x
31. Stolp H. B., Dziegielewska K. M., Review: role of developmental inflammation and blood-brain barrier dysfunction in neurodevelopmental and neurodegenerative diseases. Neuropathology and Applied Neurobiology 2009 35 2 132 146 2-s2.0-61849149792 10.1111/j.1365-2990.2008.01005.x
32. Weiner H. L., The challenge of multiple sclerosis: how do we cure a chronic heterogeneous disease? Annals of Neurology 2009 65 3 239 248 2-s2.0-65249142200 10.1002/ana.21640
33. Liu Y.-J., A unified theory of central tolerance in the thymus. Trends in Immunology 2006 27 5 215 221 2-s2.0-33646162855 10.1016/j.it.2006.03.004
34. Gardner J. M., Fletcher A. L., Anderson M. S., Turley S. J., AIRE in the thymus and beyond. Current Opinion in Immunology 2009 21 6 582 589 2-s2.0-70449492717 10.1016/j.coi.2009.08.007
35. Haegert D. G., Hackenbroch J. D., Duszczyszyn D., Fitz-Gerald L., Zastepa E., Mason H., Lapierre Y., Antel J., Bar-Or A., Reduced thymic output and peripheral naïve CD4 T-cell alterations in primary progressive multiple sclerosis (PPMS). Journal of Neuroimmunology 2011 233 1-2 233 239 2-s2.0-79953324122 10.1016/j.jneuroim.2010.12.007
36. Urdinguio R. G., Sanchez-Mut J. V., Esteller M., Epigenetic mechanisms in neurological diseases: genes, syndromes, and therapies. The Lancet Neurology 2009 8 11 1056 1072 2-s2.0-70449725209 10.1016/S1474-4422(09)70262-5
37. Meffre E., Wardemann H., B-cell tolerance checkpoints in health and autoimmunity. Current Opinion in Immunology 2008 20 6 632 638 2-s2.0-56349161598 10.1016/j.coi.2008.09.001
38. Hug A., Korporal M., Schröder I., Haas J., Glatz K., Storch-Hagenlocher B., Wildemann B., Thymic export function and T cell homeostasis in patients with relapsing remitting multiple sclerosis. Journal of Immunology 2003 171 1 432 437 2-s2.0-0037530472 (Pubitemid 36745317)
39. + regulatory T cells in human autoimmune diseases. Nature Reviews Immunology 2010 10 12 849 859 2-s2.0-78649526238 10.1038/nri2889
40. Wucherpfennig K. W., Call M. J., Deng L., Mariuzza R., Structural alterations in peptide-MHC recognition by self-reactive T cell receptors. Current Opinion in Immunology 2009 21 6 590 595 2-s2.0-70449470318 10.1016/j.coi.2009.07.008
41. Huang H., Patel D. D., Manton K. G., The immune system in aging: roles of cytokines, T cells and NK cells. Frontiers in Bioscience 2005 10 192 215 2-s2.0-23044439649
42. Josefowicz S. Z., Lu L.-F., Rudensky A. Y., Regulatory T cells: mechanisms of differentiation and function. Annual Review of Immunology 2012 30 531 564 2-s2.0-84859416933 10.1146/annurev.immunol.25.022106.141623
43. Xing Y., Hogquist K. A., T-cell tolerance: central and peripheral. Cold Spring Harbor Perspectives in Biology 2012 4 6, article a006957
44. Miller A., Glass-Marmor L., Abraham M., Grossman I., Shapiro S., Galboiz Y., Bio-markers of disease activity and response to therapy in multiple sclerosis. Clinical Neurology and Neurosurgery 2004 106 3 249 254 2-s2.0-2642514600 10.1016/j.clineuro.2004.02.008 (Pubitemid 38716156)
45. Shilling R. A., Bandukwala H. S., Sperling A. I., Regulation of T:B cell interactions by the Inducible Costimulator molecule: does ICOS "induce" disease? Clinical Immunology 2006 121 1 13 18 2-s2.0-33748627960 10.1016/j.clim.2006.04.574 (Pubitemid 44380409)
46. Kwon B., CD137-CD137 Ligand Interactions in Inflammation. Immune Network 2009 9 84 89
47. Perona-Wright G., Jenkins S. J., O'Connor R. A., Zienkiewicz D., McSorley H. J., Maizels R. M., Anderton S. M., MacDonald A. S., A pivotal role for CD40-mediated IL-6 production by dendritic cells during IL-17 induction in vivo. Journal of Immunology 2009 182 5 2808 2815 2-s2.0-64849093183 10.4049/jimmunol.0803553
48. De Jagera P. L., Baecher-Allana C., Maiera L. M., The role of the CD58 locus in multiple sclerosis. Proceedings of National Academy of Science 2009 106 13 5264 5269
49. Campbell D. J., Koch M. A., Phenotypical and functional specialization of FOXP3+ regulatory T cells. Nature Reviews Immunology 2011 11 2 119 130 2-s2.0-79251500661 10.1038/nri2916
50. Fontenot J. D., Rudensky A. Y., A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nature Immunology 2005 6 4 331 337 2-s2.0-16844363097 10.1038/ni1179 (Pubitemid 41716769)
51. Rojas J. I., González S. J., Patrucco L., Cristiano E., Rol de las células T regulatorias en Esclerosis Múltiple. Medicina (Buenos Aires) 2010 70 79 86
52. Magliozzi R., Howell O. W., Reeves C., Roncaroli F., Nicholas R., Serafini B., Aloisi F., Reynolds R., A Gradient of neuronal loss and meningeal inflammation in multiple sclerosis. Annals of Neurology 2010 68 4 477 493 2-s2.0-78249280011 10.1002/ana.22230
53. Romme-Christensen J., Bornsen L., Hesse D., Cellular sources of dysregulated cytokines in relapsing-remitting multiple sclerosis. Journal of Neuroinflammation 2012 9 215
54. Opdenakker G., Van Damme J., Probing cytokines, chemokines and matrix metalloproteinases towards better immunotherapies of multiple sclerosis. Cytokine and Growth Factor Reviews 2011 22 5-6 359 365 2-s2.0-82955203465 10.1016/j.cytogfr.2011.11.005
55. Beck J., Rondot P., Catinot L., Falcoff E., Kirchner H., Wietzerbin J., Increased production of interferon gamma and tumor necrosis factor precedes clinical manifestation in multiple sclerosis: do cytokines trigger off exacerbations? Acta Neurologica Scandinavica 1988 78 4 318 323 2-s2.0-0023794099 (Pubitemid 18266650)
56. Maimone D., Gregory S., Arnason B. G. W., Reder A. T., Cytokine levels in the cerebrospinal fluid and serum of patients with multiple sclerosis. Journal of Neuroimmunology 1991 32 1 67 74 2-s2.0-0026066932 10.1016/0165-5728(91)90073- G
57. Navikas V., Link H., Review: cytokines and the pathogenesis of multiple sclerosis. Journal of Neuroscience Research 1996 45 4 322 333 (Pubitemid 26299587)
58. Amedei A., Prisco D., D'Elios M. M., Multiple sclerosis: the role of cytokines in pathogenesis and in therapies. International Journal of Molecular Sciences 2012 13 10 13438 13460
59. Cua D. J., Sherlock J., Chen Y., Murphy C. A., Joyce B., Seymour B., Lucian L., To W., Kwan S., Churakova T., Zurawski S., Wiekowski M., Lira S. A., Gorman D., Kastelein R. A., Sedgwick J. D., Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003 421 6924 744 748 2-s2.0-0037434789 10.1038/nature01355 (Pubitemid 36227625)
60. Aggarwal S., Ghilardi N., Xie M.-H., De Sauvage F. J., Gurney A. L., Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. Journal of Biological Chemistry 2003 278 3 1910 1914 2-s2.0-0037449737 10.1074/jbc.M207577200 (Pubitemid 36801431)
61. Mangan P. R., Harrington L. E., O'Quinn D. B., Helms W. S., Bullard D. C., Elson C. O., Hatton R. D., Wahl S. M., Schoeb T. R., Weaver C. T., Transforming growth factor- β induces development of the T H17 lineage. Nature 2006 441 7090 231 234 2-s2.0-33646560950 10.1038/nature04754
62. Christophi G. P., Gruber R. C., Panos M., Christophi R. L., Jubelt B., Massa P. T., Interleukin-33 upregulation in peripheral leukocytes and CNS of multiple sclerosis patients. Clinical Immunology 2012 142 3 308 319 2-s2.0-84857370530 10.1016/j.clim.2011.11.007
63. Esendagli G., Kurne A. T., Sayat G., Kilic A. K., Guc D., Karabudak R., Evaluation of Th17- related cytokines and receptors in multiple sclerosis patients under interferon beta-1 therapy. Journal of Neuroimmunology 2013 255 1-2 81 84
64. Paty D. W., Li D. K. B., Interferon beta-1b is effective in relapsing-remitting multiple sclerosis. II. MRI analysis results of a multicenter, randomized, double-blind, placebo- controlled trial. Neurology 1993 43 4 662 667 2-s2.0-0027521002 (Pubitemid 23121952)
65. Bongioanni P., Lombardo F., Moscato G., Mosti S., Meucci G., T-cell interleukin-6 receptor binding in interferon- β -1b-treated multiple sclerosis patients. European Journal of Neurology 2000 7 6 647 653 2-s2.0-0034480122 10.1046/j.1468-1331.2000.00139.x (Pubitemid 32154395)
66. Langemann H., Kabiersch A., Newcombe J., Measurement of low-molecular-weight antioxidants, uric acid, tyrosine and tryptophan in plaques and white matter from patients with multiple sclerosis. European Neurology 1992 32 5 248 252 2-s2.0-0026647212
67. Ortiz G. G., Macías-Islas M. A., Pacheco-Moisés F. P., Oxidative stress is increased in serum from Mexican patients with relapsing-remitting multiple sclerosis. Disease Markers 2009 26 1 35 39
68. van Muiswinkel F. L., Kuiperij H. B., The Nrf2-ARE signalling pathway: promising drug target to combat oxidative stress in neurodegenerative disorders. Current Drug Targets 2005 4 3 267 281 2-s2.0-19944384264 10.2174/ 1568007054038238 (Pubitemid 40754162)
69. Jaiswal A. K., Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radical Biology and Medicine 2004 36 10 1199 1207 2-s2.0-1942520367 10.1016/j.freeradbiomed.2004.02.074 (Pubitemid 38526313)
70. Iuvone T., D'Acquisto F., Van Osselaer N., Di Rosa M., Carnuccio R., Herman A. G., Evidence that inducible nitric oxide synthase is involved in LPS-induced plasma leakage in rat skin through the activation of nuclear factor- B. British Journal of Pharmacology 1998 123 7 1325 1330 2-s2.0-0031889021 10.1038/sj.bjp.0701730 (Pubitemid 28143131)
71. Jiménez- Jiménez F. J., de Bustos F., Molina J. A., Cerebrospinal fluid levels of alphatocopherol in patients with multiple sclerosis. Neuroscience Letters 1998 249 65 67 (Pubitemid 28308235)
72. Kretz-Remy C., Mehlen P., Mirault M.-E., Arrigo A.-P., Inhibition of I B- α phosphorylation and degradation and subsequent NF- B activation by glutathione peroxidase overexpression. Journal of Cell Biology 1996 133 5 1083 1093 2-s2.0-0029999693
73. Leto T. L., Geiszt M., Role of Nox family NADPH oxidases in host defense. Antioxidants and Redox Signaling 2006 8 9-10 1549 1561 2-s2.0-33750926794 10.1089/ars.2006.8.1549 (Pubitemid 44726330)
74. Lewén A., Matz P., Chan P. H., Free radical pathways in CNS injury. Journal of Neurotrauma 2000 17 10 871 890 2-s2.0-0033789565
75. Halliwell B., Reactive oxygen species and the central nervous system. Journal of Neurochemistry 1992 59 5 1609 1623 2-s2.0-0026754574 10.1111/j.1471-4159.1992.tb10990.x
76. Smith W. L., DeWitt D. L., Garavito R. M., N-glycosylation of prostaglandin endoperoxide synthase-1 and-2 and their ori- entations in the endoplasmic. Annual Review of Biochemistry 2000 69 145 182
77. Dringen R., Pawlowski P. G., Hirrlinger J., Peroxide detoxification by brain cells. Journal of Neuroscience Research 2005 79 1-2 157 165 2-s2.0-12244291916 10.1002/jnr.20280 (Pubitemid 40116430)
78. McCord J. M., Edeas M. A., SOD, oxidative stress and human pathologies: a brief history and a future vision. Biomedicine and Pharmacotherapy 2005 59 4 139 142 2-s2.0-18044363639 10.1016/j.biopha.2005.03.005 (Pubitemid 40603324)
79. Arthur J. R., The glutathione peroxidases. Cellular and Molecular Life Sciences 2000 57 13-14 1825 1835 2-s2.0-0034489653 (Pubitemid 32102578)
80. Jaiswal A. K., Regulation of genes encoding NAD(P)H:quinone oxidoreductases. Free Radical Biology and Medicine 2000 29 3-4 254 262 2-s2.0-0033800922 10.1016/S0891-5849(00)00306-3
81. Wagener F. A. D. T. G., Volk H.-D., Willis D., Abraham N. G., Soares M. P., Adema G. J., Figdor C. G., Different faces of the heme-heme oxygenase system in inflammation. Pharmacological Reviews 2003 55 3 551 571 2-s2.0-0041967387 10.1124/pr.55.3.5 (Pubitemid 37013215)
82. Floyd R. A., 'Copper in the brain and Alzheimer's Disease', 12. Floyd, R. A. Proceedings of the Society for Experimental Biology and Medicine 1999 222 236 245
83. Van der Goes A., Wouters D., Van Der Pol S. M., Huizinga R., Ronken E., Adamson P., Greenwood J., Dijkstra C. D., De Vries H. E., Reactive oxygen species enhance the migration of monocytes across the blood-brain barrier in vitro. The FASEB Journal 2001 15 10 1852 1854 2-s2.0-0035430445
84. Schreibelt G., Musters R. J. P., Reijerkerk A., De Groot L. R., Van Der Pol S. M. A., Hendrikx E. M. L., Döpp E. D., Dijkstra C. D., Drukarch B., De Vries H. E., Lipoic acid affects cellular migration into the central nervous system and stabilizes blood-brain barrier integrity. Journal of Immunology 2006 177 4 2630 2637 2-s2.0-33746924887 (Pubitemid 44201022)
85. Van Der Goes A., Brouwer J., Hoekstra K., Roos D., Van Den Berg T. K., Dijkstra C. D., Reactive oxygen species are required for the phagocytosis of myelin by macrophages. Journal of Neuroimmunology 1998 92 1-2 67 75 2-s2.0-0032414199 10.1016/S0165-5728(98)00175-1 (Pubitemid 29015991)
86. Van Meeteren M. E., Hendriks J. J. A., Dijkstra C. D., Van Tol E. A. F., Dietary compounds prevent oxidative damage and nitric oxide production by cells involved in demyelinating disease. Biochemical Pharmacology 2004 67 5 967 975 2-s2.0-1042287039 10.1016/j.bcp.2003.10.018 (Pubitemid 38201642)
87. Hendriks J. J. A., Teunissen C. E., De Vries H. E., Dijkstra C. D., Macrophages and neurodegeneration. Brain Research Reviews 2005 48 2 185 195 2-s2.0-17844381010 10.1016/j.brainresrev.2004.12.008 (Pubitemid 40585749)
88. Giovannoni G., Heales S. J. R., Land J. M., Thompson E. J., The potential role of nitric oxide in multiple sclerosis. Multiple Sclerosis 1998 4 3 212 216 2-s2.0-0031679809 (Pubitemid 28410053)
89. Hartung H.-P., Jung S., Stoll G., Zielasek J., Schmidt B., Archelos J. J., Toyka K. V., Inflammatory mediators in demyelinating disorders of the CNS and PNS. Journal of Neuroimmunology 1992 40 2-3 197 210 2-s2.0-0026746211 10.1016/0165-5728(92)90134-7
90. Smith K. J., Kapoor R., Felts P. A., Demyelination: the role of reactive oxygen and nitrogen species. Brain Pathology 1999 9 1 69 92 2-s2.0-0032950964 (Pubitemid 29056521)
91. Bagasra O., Michaels F. H., Zheng Y. M., Bobroski L. E., Spitsin S. V., Fu Z. F., Tawadros R., Koprowski H., Activation of the inducible form of nitric oxide synthase in the brains of patients with multiple sclerosis. Proceedings of the National Academy of Sciences of the United States of America 1995 92 26 12041 12045 2-s2.0-0029592005 10.1073/pnas.92.26.12041 (Pubitemid 26014007)
92. Calabrese V., Scapagnini G., Ravagna A., Bella R., Foresti R., Bates T. E., Stella A.-M. G., 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. Journal of Neuroscience Research 2002 70 4 580 587 2-s2.0-0037110706 10.1002/jnr.10408 (Pubitemid 35253528)
93. Esterbauer H., Schaur R. J., Zollner H., Chemistry and Biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radical Biology and Medicine 1991 11 1 81 128 2-s2.0-0025814980 10.1016/0891-5849(91)90192-6 (Pubitemid 121003917)
94. Schneider C., Porter N. A., Brash A. R., Routes to 4-hydroxynonenal: fundamental issues in the mechanisms of lipid peroxidation. Journal of Biological Chemistry 2008 283 23 15539 15543 2-s2.0-47049095632 10.1074/jbc.R800001200
95. Jana A., Pahan K., Oxidative stress kills human primary oligodendrocytes via neutral sphingomyelinase: implications for multiple sclerosis. Journal of Neuroimmune Pharmacology 2007 2 2 184 193 2-s2.0-34247477204 10.1007/s11481-007-9066-2
96. Karlhuber G. M., Bauer H. C., Eckl P. M., Cytotoxic and genotoxic effects of 4-hydroxynonenal in cerebral endothelial cells. Mutation Research 1997 381 2 209 216 2-s2.0-0031589737 10.1016/S0027-5107(97)00170-X (Pubitemid 28015416)
97. Usatyuk P. V., Parinandi N. L., Natarajan V., Redox regulation of 4-hydroxy-2-nonenal-mediated endothelial barrier dysfunction by focal adhesion, adherens, and tight junction proteins. Journal of Biological Chemistry 2006 281 46 35554 35566 2-s2.0-33845629703 10.1074/jbc.M607305200 (Pubitemid 46036589)
98. van Horssen J., Schreibelt G., Drexhage J., Hazes T., Dijkstra C. D., van der Valk P., de Vries H. E., Severe oxidative damage in multiple sclerosis lesions coincides with enhanced antioxidant enzyme expression. Free Radical Biology and Medicine 2008 45 12 1729 1737 2-s2.0-56349160121 10.1016/j.freeradbiomed.2008.09.023
99. Leitinger N., Cholesteryl ester oxidation products in atherosclerosis. Molecular Aspects of Medicine 2003 24 4-5 239 250 2-s2.0-0042170261 10.1016/S0098-2997(03)00019-0 (Pubitemid 36945024)
100. Ferretti G., Bacchetti T., Principi F., Di Ludovico F., Viti B., Angeleri V. A., Danni M., Provinciali L., Increased levels of lipid hydroperoxides in plasma of patients with multiple sclerosis: a relationship with paraoxonase activity. Multiple Sclerosis 2005 11 6 677 682 2-s2.0-28044438183 10.1191/1352458505ms1240oa (Pubitemid 41685138)
101. Newcombe J., Li H., Cuzner M. L., Low density lipoprotein uptake by macrophages in multiple sclerosis plaques: implications for pathogenesis. Neuropathology and Applied Neurobiology 1994 20 2 152 162 2-s2.0-0028210146 (Pubitemid 24123546)
102. Bizzozero O. A., DeJesus G., Callahan K., Pastuszyn A., Elevated protein carbonylation in the brain white matter and gray matter of patients with multiple sclerosis. Journal of Neuroscience Research 2005 81 5 687 695 2-s2.0-27244450879 10.1002/jnr.20587 (Pubitemid 41532164)
103. van Horssen J., Schreibelt G., Bö L., Montagne L., Drukarch B., van Muiswinkel F. L., de Vries H. E., NAD(P)H:quinone oxidoreductase 1 expression in multiple sclerosis lesions. Free Radical Biology and Medicine 2006 41 2 311 317 2-s2.0-33745227281 10.1016/j.freeradbiomed.2006.04.013 (Pubitemid 43928505)
104. Toshniwal P. K., Zarling E. J., Evidence for increased lipid peroxidation in multiple sclerosis. Neurochemical Research 1992 17 2 205 207 2-s2.0-0026500136
105. Mattsson N., Haghighi S., Andersen O., Yao Y., Rosengren L., Blennow K., Praticò D., Zetterberg H., Elevated cerebrospinal fluid F2-isoprostane levels indicating oxidative stress in healthy siblings of multiple sclerosis patients. Neuroscience Letters 2007 414 3 233 236 2-s2.0-33847185147 10.1016/j.neulet.2006.12.044
106. Jack C., Antel J., Brück W., Kuhlmann T., Contrasting potential of nitric oxide and peroxynitrite to mediate oligodendrocyte injury in multiple sclerosis. Glia 2007 55 9 926 934 2-s2.0-34250186821 10.1002/glia.20514 (Pubitemid 46903993)
107. Besler H. T., Comoǧlu S., Okçu Z., Serum levels of antioxidant vitamins and lipid peroxidation in multiple sclerosis. Nutriology Neuroscience 2002 5 3 215 220 (Pubitemid 34568217)
108. Kalousová M., Havrdová E., Mrázová K., Advanced glycoxidation end products in patients with multiple sclerosis. Prague Medical Report 2005 106 167 174
109. Mazzella G. L., Sinforiani E., Savoldi F., Blood cells glutathione peroxidase activity and selenium in multiple sclerosis. European Neurology 1983 22 6 442 446 2-s2.0-0021012422 (Pubitemid 14208474)
110. Zachara B., Gromadzinska J., Czernicki J., Red blood cell glutathione peroxidase activity in multiple sclerosis. Klinische Wochenschrift 1984 62 4 179 182 2-s2.0-0021325817 (Pubitemid 14190839)
111. Szeinberg A., Golan R., Ben-Ezzer J., Glutathione peroxidase activity in various types of blood cells in multiple sclerosis. Acta Neurologica Scandinavica 1981 63 1 67 75 2-s2.0-0019351540 (Pubitemid 11172561)
112. Wong E. K. Jr., Enomoto H., Leopold I. H., Williams J. L., Kladde L., Hollander D. H., Intestinal absorption of dietary fat in patients with multiple sclerosis. Metabolic, Pediatric and Systemic Ophthalmology 1993 16 3-4 39 41 2-s2.0-0027859091 (Pubitemid 24191482)
113. de Bustos F., Jimenez-Jimenez F. J., Molina J. A., Serum levels of coenzyme Q10 in patients with multiple sclerosis. Acta Neurology Scandinave 2000 101 209 211 (Pubitemid 30112303)
114. Kastenbauer S., Kieseier B. C., Becker B. F., No evidence of increased oxidative degradation of urate to allantoin in the CSF and serum of patients with multiple sclerosis. Journal of Neurology 2005 252 5 611 612 2-s2.0-20044390760 10.1007/s00415-005-0697-z (Pubitemid 40768182)
115. Amorini A. M., Petzold A., Tavazzi B., Eikelenboom J., Keir G., Belli A., Giovannoni G., Di Pietro V., Polman C., D'Urso S., Vagnozzi R., Uitdehaag B., Lazzarino G., Increase of uric acid and purine compounds in biological fluids of multiple sclerosis patients. Clinical Biochemistry 2009 42 10-11 1001 1006 2-s2.0-67349252457 10.1016/j.clinbiochem.2009.03.020
116. Peng F., Zhang B., Zhong X., Li J., Xu G., Hu X., Qiu W., Pei Z., Serum uric acid levels of patients with multiple sclerosis and other neurological diseases. Multiple Sclerosis 2008 14 2 188 196 2-s2.0-43149117933 10.1177/1352458507082143 (Pubitemid 351639627)
117. 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. Journal of Neuroimmunology 2004 151 1-2 171 179 2-s2.0-2442497293 10.1016/j.jneuroim.2004. 02.005 (Pubitemid 38624411)
118. Gonsette R. E., Oxidative stress and excitotoxicity: a therapeutic issue in multiple sclerosis? Multiple Sclerosis 2008 14 1 22 34 2-s2.0-42149088270 10.1177/1352458507080111 (Pubitemid 351541394)
119. Noseworthy J. H., Lucchinetti C., Rodriguez M., Weinshenker B. G., Multiple sclerosis. The New England Journal of Medicine 2000 343 13 938 952 2-s2.0-0034727066 10.1056/NEJM200009283431307
120. Schreibelt G., van Horssen J., van Rossum S., Dijkstra C. D., Drukarch B., de Vries H. E., Therapeutic potential and biological role of endogenous antioxidant enzymes in multiple sclerosis pathology. Brain Research Reviews 2007 56 2 322 330 2-s2.0-36448981390 10.1016/j.brainresrev.2007.07.005 (Pubitemid 350166526)
121. Manna S. K., Kuo M. T., Aggarwal B. B., Overexpression of γ -glutamylcysteine synthetase suppresses tumor necrosis factor-induced apoptosis and activation of nuclear transcription factor-kappa B and activator protein-1. Oncogene 1999 18 30 4371 4382 2-s2.0-0033615032 10.1038/sj.onc.1202811 (Pubitemid 29392378)
122. Baeuerle P. A., Henkel T., Function and activation of NF- B in the immune system. Annual Review of Immunology 1994 12 141 179 2-s2.0-0028174061
123. Marnett L. J., Rowlinson S. W., Goodwin D. C., Kalgutkar A. S., Lanzo C. A., Arachidonic acid oxygenation by COX-1 and COX-2. Mechanisms of catalysis and inhibition. Journal of Biological Chemistry 1999 274 33 22903 22906 2-s2.0-0033551847 10.1074/jbc.274.33.22903 (Pubitemid 29388029)
124. Barañano D. E., Ferris C. D., Snyder S. H., Atypical neural messengers. Trends in Neurosciences 2001 24 2 99 106 2-s2.0-0035254766 10.1016/S0166-2236(00)01716-1 (Pubitemid 32115440)
125. Xia Y., Roman L. J., Masters B. S. S., Zweier J. L., Inducible nitric-oxide synthase generates superoxide from the reductase domain. Journal of Biological Chemistry 1998 273 35 22635 22639 2-s2.0-0032575598 10.1074/jbc.273.35.22635 (Pubitemid 28399833)