The experimental autoimmune encephalomyelitis model for proteomic biomarker studies: From rat to human

Clinica Chimica Acta

Volumn 412, Issue 11-12, 2011, Pages 812-822

  Rosenling, Therese ^a   Attali, Amos ^b   Luider, Theo M ^c   Bischoff, Rainer ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b Chemical Design and Synthesis Unit   (Netherlands)

^c ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Experimental autoimmune encephalomyelitis; Multiple sclerosis; Oxidative stress; Protein biomarkers; Proteomics

Indexed keywords

ALBUMIN; ALPHA 2 MACROGLOBULIN; ALPHA INTERNEXIN; BIOLOGICAL MARKER; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALPHOBINDIN II; CARBONATE DEHYDRATASE II; CATHEPSIN B; CERULOPLASMIN; CYSTATIN C; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; FIBRONECTIN; FILAMIN A; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE DEHYDROGENASE; GLUTATHIONE SYNTHASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCEROPHOSPHOINOSITOL INOSITOLPHOSPHODIESTERASE; HEPATOMA DERIVED GROWTH FACTOR; INITIATION FACTOR 4A; MOESIN; MYELIN BASIC PROTEIN; NUCLEOPHOSMIN; PROTEOME; STRUCTURAL PROTEIN; TRANSFERRIN; TUMOR NECROSIS FACTOR ALPHA; VIMENTIN;

ADAPTIVE IMMUNITY; ALLERGIC ENCEPHALOMYELITIS; BODY FLUID; CEREBROSPINAL FLUID; CEREBROSPINAL FLUID ANALYSIS; DISEASE MODEL; EXCITOTOXICITY; EXTRACELLULAR FLUID; HOMEOSTASIS; HUMAN; INFLAMMATION; MULTIPLE SCLEROSIS; NEUROLOGIC EXAMINATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEOMICS; REVIEW; UNINDEXED SEQUENCE;

ANIMALS; BIOLOGICAL MARKERS; BODY FLUIDS; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; PROTEOMICS; RATS; TRANSLATIONAL MEDICAL RESEARCH;

ANIMALIA; RATTUS;

EID: 79955011675     PISSN: 00098981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cca.2011.02.004     Document Type: Review

References (148)

1. Compston A., Coles A. Multiple sclerosis. Lancet 2008, 372:1502-1517.
2. Ebers G.C. Disease evolution in multiple sclerosis. J Neurol 2006, 253:VI/3-VI/8.
3. Balaguer D.D.G. Un caso de rabia paralítica. Gaceta Médica Catalana 1888, 11:45-57.
4. Hurst E.W. The effects of the injection of normal brain emulsion into rabbits, with special reference to the aetiology of the paralytic accidents of antirabic treatment. J Hyg 1932, 32:33-44.
5. Koritschoner R., Schweinburg F. Klinische und experimentelle Beobachtungen über Lähmungen nach Wutschutzimfung. Ztschr f Immunitätsforsch u Exper Therap 1925, 42:271.
6. Rivers T.M., Sprunt D.H., Berry G.P. Observations on attempts to produce acute disseminated encephalomyelitis in monkeys. J Exp Med 1933, 58:39-53.
7. Rivers T.M., Schwentker F.F. Encephalomyelitis accompanied by myelin destruction experimentally produced in monkeys. J Exp Med 1935, 61:689-702.
8. Baxter A.G. The origin and application of experimental autoimmune encephalomyelitis. Nat Rev Immunol 2007, 7:904-912.
9. Gold R., Linington C., Lassmann H. Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain 2006, 129:1953-1971.
10. Wolf A., Kabat E.A., Bezer A.E. The pathology of acute disseminated encephalomyelitis produced experimentally in the rhesus monkey and its resemblance to human demyelinating disease. J Neuropathol Exp Neurol 1947, 6:333-357.
11. Teitelbaum D., Meshorer A., Arnon R., Sela M. Suppression of experimental allergic encephalomyelitis by a synthetic polypeptide. Eur J Immunol 1971, 1:242-248.
12. Yednock T.A., Cannon C., Fritz L.C., Sanchez-Madrid F., Steinmann L., Karin N. Prevention of experimental autoimmune encephalomyelitis by antibodies against a4b1 integrin. Nature 1992, 356:63-66.
13. Ellison G.W., Myers L.W. A review of systemic nonspecific immunosuppressive treatment of multiple sclerosis. Neurology 1978, 28:132-139.
14. Ridge S.C., Sloboda A.E., McReynolds R.A. Suppression of experimental allergic encephalomyelitis by Mitoxantrone. Clin Immunol Immunopathol 1985, 35:35-42.
15. Fox E.J. Mechanism of action of mitoxantrone. Neurology 2004, 63:S15-S18.
16. Sriram S., Steiner I. Experimental Allergic Encephalomyelitis: A misleading model of Multiple Sclerosis. Ann Neurol 2005, 58:939-945.
17. Steinman L., Zamvil S.S. Virtues and pitfalls of EAE for the development of therapies for multiple sclerosis. Trends Immunol 2005, 26:565-571.
18. Joy J.E., Johnston R.B. Multiple Sclerosis-Current Status and Strategies for the future 2001, National Academy Press.
19. Brown A.M., McFarlin D.E. Relapsing experimental allergic encephalomyelitis in the SJL/J mouse. Lab Investig 1981, 45:278-284.
20. Lublin F.D., Maurer P.H., Berry R.G., Tippett D. Delayed, relapsing experimental allergic encephalomyelitis in mice. J Immunol 1981, 126:819-922.
21. Zamvil S., Nelson P., Trotter J., et al. T cell clones specific for myelin basic protein induce chronic relapsing EAE and demyelination. Nature 1985, 317:355-358.
22. Tsunoda I., Kuang L.Q., Theil D.J., Fujinami R.S. Antibody associated with a novel model for primary progressive multiple sclerosis: Induction of relapsing-remitting and progressive forms of EAE in H2(s) mouse strains. Brain Pathol 2000, 10:402-418.
23. Clarke W., Zhang Z., Chan D.W. The application of clinical proteomics to cancer and other diseases. Clin Chem Lab Med 2003, 41:1562-1570.
24. Fields S. Proteomics. Proteomics in genomeland. Science 2001, 291:1221-1224.
25. Giovannoni G. Multiple sclerosis cerebrospinal fluid biomarkers. Dis Markers 2006, 22:187-196.
26. Mischak H., Allmaier G., Apweiler R., et al. Recommendations for biomarker identification and qualification in clinical proteomics. Sci Transl Med 2010, 2. 46ps42.
27. Pierce J.D., Fakhari M., Works K.V., Pierce J.T., Clancy R.L. Understanding proteomics. Nurs Health Sci 2007, 9:54-60.
28. Claverie J.M. Gene number. What if there are only 30, 000 human genes?. Science 2001, 291:1255-1257.
29. Johnson K.P., Arrigo S.C., Nelson B.J., Ginsberg A. Agarose electrophoresis of cerebrospinal fluid in multiple sclerosis. A simplified method for demonstrating cerebrospinal fluid oligoclonal immunoglobulin bands. Neurology 1977, 27:273-277.
30. Poser C.M., Paty D.W., Scheinberg L., et al. New diagnostic criteria for multiple sclerosis: guidelines for research protocols. Ann Neurol 1983, 13:227-231.
31. Johnson K.P., Nelson B.J. Multiple sclerosis: diagnostic usefulness of cerebrospinal fluid. Ann Neurol 1977, 2:425-431.
32. McDonald W.I., Compston A., Edan G., et al. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol 2001, 50:121-127.
33. Kappos L., Achtnichts L., Dahlke F., et al. Genomics and proteomics: role in the management of multiple sclerosis. J Neurol 2005, 252(Suppl 3):iii21-iii27.
34. Ramstrom M., Bergquist J. Miniaturized proteomics and peptidomics using capillary liquid separation and high resolution mass spectrometry. FEBS Lett 2004, 567:92-95.
35. Rosenling T., Slim C.L., Christin C., et al. The effect of preanalytical factors on stability of the proteome and selected metabolites in cerebrospinal fluid (CSF). J Proteome Res 2009, 8:5511-5522.
36. Minagar A., Adamashvili I., Kelley R.E., Gonzalez-Toledo E., McLarty J., Smith S.J. Saliva soluble HLA as a potential marker of response to interferon-beta 1a in multiple sclerosis: a preliminary study. J Neuroinflammation 2007, 4:16.
37. Calais G., Forzy G., Crinquette C., et al. Tear analysis in clinically isolated syndrome as new multiple sclerosis criterion. Mult Scler 2010, 16:87-92.
38. Minagar A., Alexander J.S. Blood-brain barrier disruption in multiple sclerosis. Mult Scler 2003, 9:540-549.
39. Wolburg-Buchholz K., Mack A.F., Steiner E., Pfeiffer F., Engelhardt B., Wolburg H. Loss of astrocyte polarity marks blood-brain barrier impairment during experimental autoimmune encephalomyelitis. Acta Neuropathol 2009, 118:219-233.
40. El Behi M., Zephir H., Lefranc D., et al. Changes in self-reactive IgG antibody repertoire after treatment of experimental autoimmune encephalomyelitis with anti-allergic drugs. J Neuroimmunol 2007, 182:80-88.
41. Kidd B.A., Ho P.P., Sharpe O., et al. Epitope spreading to citrullinated antigens in mouse models of autoimmune arthritis and demyelination. Arthritis Res Ther 2008, 10:R119.
42. Villarroya H., Violleau K., Ben Younes-Chennoufi A., Baumann N. Myelin-induced experimental allergic encephalomyelitis in Lewis rats: tumor necrosis factor alpha levels in serum and cerebrospinal fluid immunohistochemical expression in glial cells and macrophages of optic nerve and spinal cord. J Neuroimmunol 1996, 64:55-61.
43. Consiglio A.R., Lucion A.B. Technique for collecting cerebrospinal fluid in the cisterna magna of non-anesthetized rats. Brain Res Brain Res Protoc 2000, 5:109-114.
44. Nirogi R., Kandikere V., Mudigonda K., et al. A simple and rapid method to collect the cerebrospinal fluid of rats and its application for the assessment of drug penetration into the central nervous system. J Neurosci Meth 2009, 178:116-119.
45. Lai Y.L., Smith P.M., Lamm W.J., Hildebrandt J. Sampling and analysis of cerebrospinal fluid for chronic studies in awake rats. J Appl Physiol 1983, 54:1754-1757.
46. Liu L, Duff K. A technique for serial collection of cerebrospinal fluid from the cisterna magna in mouse. J Vis Exp 2008;21. pii: 960. doi:10.3791/960.
47. van den Berg M.P., Romeijn S.G., Verhoef J.C., Merkus F.W. Serial cerebrospinal fluid sampling in a rat model to study drug uptake from the nasal cavity. J Neurosci Meth 2002, 116:99-107.
48. Boshi G., Launay N., Rips R., Scherrmann J.-M. Brain microdialysis in the mouse. J Pharmacol Toxicol Meth 1995, 33:29-33.
49. Afinowi R., Tisdall M., Keir G., Smith M., Kitchen N., Petzold A. Improving the recovery of S100B protein in cerebral microdialysis: implications for multimodal monitoring in neurocritical care. J Neurosci Meth 2009, 181:95-99.
50. Mazzeo A.T., Bullock R. Effect of bacterial meningitis complicating severe head trauma upon brain microdialysis and cerebral perfusion. Neurocrit Care 2005, 2:282-287.
51. Tisdall M.M., Smith M. Cerebral microdialysis: research technique or clinical tool. Br J Anaesth 2006, 97:18-25.
52. Maurer M.H. Proteomics of brain extracellular fluid (ECF) and cerebrospinal fluid (CSF). Mass Spectrom Rev 2010, 29:17-28.
53. Linker R.A., Lee D.H. Models of autoimmune demyelination in the central nervous system: on the way to translational medicine. Exp Transl Stroke Med 2009, 1:5.
54. James P. Protein identification in the post-genome era: the rapid rise of proteomics. Q Rev Biophys 1997, 30:279-331.
55. Grant J.E., Hu J., Liu T., Jain M.R., Elkabes S., Li H. Post-translational modifications in the rat lumbar spinal cord in experimental autoimmune encephalomyelitis. J Proteome Res 2007, 6:2786-2791.
56. Morgan L., Shah B., Rivers L.E., et al. Inflammation and dephosphorylation of the tight junction protein occludin in an experimental model of multiple sclerosis. Neuroscience 2007, 147:664-673.
57. Ohgoh M., Hanada T., Smith T., et al. Altered expression of glutamate transporters in experimental autoimmune encephalomyelitis. J Neuroimmunol 2002, 125:170-178.
58. Qi X., Lewin A.S., Sun L., Hauswirth W.W., Guy J. Mitochondrial protein nitration primes neurodegeneration in experimental autoimmune encephalomyelitis. Biol Chem 2006, 281:31950-31962.
59. Stegbauer J., Lee D.H., Seubert S., et al. Role of the renin-angiotensin system in autoimmune inflammation of the central nervous system. Proc Natl Acad Sci U S A 2009, 106:14942-14947.
60. Jain M.R., Bian S., Liu T., Hu J., Elkabes S., Li H. Altered proteolytic events in experimental autoimmune encephalomyelitis discovered by iTRAQ shotgun proteomics analysis of spinal cord. Proteome Sci 2009, 7:25.
61. Linker R.A., Brechlin P., Jesse S., et al. Proteome profiling in murine models of multiple sclerosis: identification of stage specific markers and culprits for tissue damage. PLoS ONE 2009, 4:e7624.
62. Liu T., Donahue K.C., Hu J., et al. Identification of differentially expressed proteins in experimental autoimmune encephalomyelitis (EAE) by proteomic analysis of the spinal cord. J Proteome Res 2007, 6:2565-2575.
63. Mikkat S., Lorenz P., Scharf C., Yu X., Glocker M.O., Ibrahim S.M. MS characterization of qualitative protein polymorphisms in the spinal cords of inbred mouse strains. Proteomics 2010, 10:1050-1062.
64. Alt C., Duvefelt K., Franzen B., Yang Y., Engelhardt B. Gene and protein expression profiling of the microvascular compartment in experimental autoimmune encephalomyelitis in C57Bl/6 and SJL mice. Brain Pathol 2005, 15:1-16.
65. Barnett M.H., Parratt J.D., Cho E.S., Prineas J.W. Immunoglobulins and complement in postmortem multiple sclerosis tissue. Ann Neurol 2009, 65:32-46.
66. Carlin C., Murray L., Graham D., Doyle D., Nicoll J. Involvement of apolipoprotein E in multiple sclerosis: absence of remyelination associated with possession of the APOE epsilon2 allele. J Neuropathol Exp Neurol 2000, 59:361-367.
67. Chiasserini D., Di F.M., Candeliere A., et al. CSF proteome analysis in multiple sclerosis patients by two-dimensional electrophoresis. Eur J Neurol 2008, 15:998-1001.
68. Elderfield A.J., Newcombe J., Bolton C., Flower R.J. Lipocortins (annexins) 1, 2, 4 and 5 are increased in the central nervous system in multiple sclerosis. J Neuroimmunol 1992, 39:91-100.
69. Fazekas F., Strasser-Fuchs S., Kollegger H., et al. Apolipoprotein E epsilon 4 is associated with rapid progression of multiple sclerosis. Neurology 2001, 57:853-857.
70. Gay F.W. Early cellular events in multiple sclerosis. Intimations of an extrinsic myelinolytic antigen. Clin Neurol Neurosurg 2006, 108:234-240.
71. Hammack B.N., Fung K.Y., Hunsucker S.W., et al. Proteomic analysis of multiple sclerosis cerebrospinal fluid. Mult Scler 2004, 10:245-260.
72. Hedegaard C.J., Chen N., Sellebjerg F., et al. Autoantibodies to myelin basic protein (MBP) in healthy individuals and in patients with multiple sclerosis: a role in regulating cytokine responses to MBP. Immunology 2009, 128:e451-e461.
73. Jongen P.J., Nijeholt G., Lamers K.J., et al. Cerebrospinal fluid IgM index correlates with cranial MRI lesion load in patients with multiple sclerosis. Eur Neurol 2007, 58:90-95.
74. KABAT E.A., FREEDMAN D.A. A study of the crystalline albumin, gamma globulin and total protein in the cerebrospinal fluid of 100 cases of multiple sclerosis and in other diseases. Am J Med Sci 1950, 219:55-64.
75. MacPherson C.F., Cosgrove J.B. An unusual IgG globulin. Frequency of occurrence in cerebrospinal fluid in multiple sclerosis. Arch Neurol 1968, 19:503-509.
76. Padilla-Docal B., Dorta-Contreras A.J., Fundora-Hernandez H., et al. C3c intrathecal synthesis evaluation in patients with multiple sclerosis. Arq Neuropsiquiatr 2007, 65:800-802.
77. Philippe J., Debruyne J., Leroux-Roels G., Willems A., Dereuck J. In vitro TNF-alpha, IL-2 and IFN-gamma production as markers of relapses in multiple sclerosis. Clin Neurol Neurosurg 1996, 98:286-290.
78. Sobel R.A., Mitchell M.E. Fibronectin in multiple sclerosis lesions. Am J Pathol 1989, 135:161-168.
79. Spuler S., Yousry T., Scheller A., et al. Multiple sclerosis: prospective analysis of TNF-alpha and 55kDa TNF receptor in CSF and serum in correlation with clinical and MRI activity. J Neuroimmunol 1996, 66:57-64.
80. Stoop M.P., Dekker L.J., Titulaer M.K., et al. Quantitative matrix-assisted laser desorption ionization-fourier transform ion cyclotron resonance (MALDI-FT-ICR) peptide profiling and identification of multiple-sclerosis-related proteins. J Proteome Res 2009, 8:1404-1414.
81. Tourtellotte W.W., Parker J.A. Multiple sclerosis: brain immunoglobulin-G and albumin. Nature 1967, 214:683-686.
82. van Horssen J., Bo L., Vos C.M., Virtanen I., De Vries H.E. Basement membrane proteins in multiple sclerosis-associated inflammatory cuffs: potential role in influx and transport of leukocytes. J Neuropathol Exp Neurol 2005, 64:722-729.
83. Zhang B., Jiang Y., Yang Y., Peng F., Hu X. Correlation between serum thyroxine and complements in patients with multiple sclerosis and neuromyelitis optica. Neuro Endocrinol Lett 2008, 29:256-260.
84. Kawajiri M., Mogi M., Osoegawa M., et al. Reduction of angiotensin II in the cerebrospinal fluid of patients with multiple sclerosis. Mult Scler 2008, 14:557-560.
85. Ottervald J., Franzen B., Nilsson K., et al. Multiple sclerosis: Identification and clinical evaluation of novel CSF biomarkers. J Proteomics 2010.
86. Wosik K., Cayrol R., Dodelet-Devillers A., et al. Angiotensin II controls occludin function and is required for blood brain barrier maintenance: relevance to multiple sclerosis. J Neurosci 2007, 27:9032-9042.
87. Szczucinski A., Losy J. Chemokines and chemokine receptors in multiple sclerosis. Potential targets for new therapies. Acta Neurol Scand 2007, 115:137-146.
88. Berger T., Rubner P., Schautzer F., et al. Antimyelin antibodies as a predictor of clinically definite multiple sclerosis after a first demyelinating event. N Engl J Med 2003, 349:139-145.
89. Egg R., Reindl M., Deisenhammer F., Linington C., Berger T. Anti-MOG and anti-MBP antibody subclasses in multiple sclerosis. Mult Scler 2001, 7:285-289.
90. Vojdani A., Vojdani E., Cooper E. Antibodies to myelin basic protein, myelin oligodendrocytes peptides, alpha-beta-crystallin, lymphocyte activation and cytokine production in patients with multiple sclerosis. J Intern Med 2003, 254:363-374.
91. Gunnarsson M., Sundstrom P., Stigbrand T., Jensen P.E. Native and transformed alpha2-macroglobulin in plasma from patients with multiple sclerosis. Acta Neurol Scand 2003, 108:16-21.
92. Jensen P.E., Humle J.S., Datta P., Sorensen P.S. Significantly increased fractions of transformed to total alpha2-macroglobulin concentrations in plasma from patients with multiple sclerosis. Biochim Biophys Acta 2004, 1690:203-207.
93. Newcombe J., Uddin A., Dove R., et al. Glutamate receptor expression in multiple sclerosis lesions. Brain Pathol 2008, 18:52-61.
94. Vallejo-Illarramendi A., Domercq M., Perez-Cerda F., Ravid R., Matute C. Increased expression and function of glutamate transporters in multiple sclerosis. Neurobiol Dis 2006, 21:154-164.
95. Werner P., Pitt D., Raine C.S. Multiple sclerosis: altered glutamate homeostasis in lesions correlates with oligodendrocyte and axonal damage. Ann Neurol 2001, 50:169-180.
96. Lisman J., Schulman H., Cline H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 2002, 3:175-190.
97. Poggi A., Zocchi M.R., Carosio R., et al. Transendothelial migratory pathways of V delta 1+TCR gamma delta+and V delta 2+TCR gamma delta+T lymphocytes from healthy donors and multiple sclerosis patients: involvement of phosphatidylinositol 3 kinase and calcium calmodulin-dependent kinase II. J Immunol 2002, 168:6071-6077.
98. Gonsette R.E. Neurodegeneration in multiple sclerosis: the role of oxidative stress and excitotoxicity. J Neurol Sci 2008, 274:48-53.
99. LeVine S.M., Lynch S.G., Ou C.N., Wulser M.J., Tam E., Boo N. Ferritin, transferrin and iron concentrations in the cerebrospinal fluid of multiple sclerosis patients. Brain Res 1999, 821:511-515.
100. LeVine S.M., Chakrabarty A. The role of iron in the pathogenesis of experimental allergic encephalomyelitis and multiple sclerosis. Ann NY Acad Sci 2004, 1012:252-266.
101. Rathore K.I., Kerr B.J., Redensek A., et al. Ceruloplasmin protects injured spinal cord from iron-mediated oxidative damage. J Neurosci 2008, 28:12736-12747.
102. Tapryal N., Mukhopadhyay C., Das D., Fox P.L., Mukhopadhyay C.K. Reactive oxygen species regulate ceruloplasmin by a novel mRNA decay mechanism involving its 3'-untranslated region: implications in neurodegenerative diseases. J Biol Chem 2009, 284:1873-1883.
103. Hunter M.I., Nlemadim B.C., Davidson D.L. Lipid peroxidation products and antioxidant proteins in plasma and cerebrospinal fluid from multiple sclerosis patients. Neurochem Res 1985, 10:1645-1652.
104. Lok C.N., Loh T.T. Regulation of transferrin function and expression: review and update. Biol Signals Recept 1998, 7:157-178.
105. Stout D.L. The role of transferrin in heme transport. Biochem Biophys Res Commun 1992, 189:765-770.
106. Weller M., List U., Schabet M., Melms A., Dichgans J. Elevated CSF lactoferrin in superficial siderosis of the central nervous system. J Neurol 1999, 246:943-945.
107. Abo-Krysha N., Rashed L. The role of iron dysregulation in the pathogenesis of multiple sclerosis: an Egyptian study. Mult Scler 2008, 14:602-608.
108. Tajouri L., Mellick A.S., Ashton K.J., et al. Quantitative and qualitative changes in gene expression patterns characterize the activity of plaques in multiple sclerosis. Brain Res Mol Brain Res 2003, 119:170-183.
109. Tumani H., Lehmensiek V., Rau D., et al. CSF proteome analysis in clinically isolated syndrome (CIS): candidate markers for conversion to definite multiple sclerosis. Neurosci Lett 2009, 452:214-217.
110. Zeman D., Adam P., Kalistova H., et al. Transferrin in patients with multiple sclerosis: a comparison among various subgroups of multiple sclerosis patients. Acta Neurol Scand 2000, 101:89-94.
111. Tolosano E., Altruda F. Hemopexin: structure, function, and regulation. DNA Cell Biol 2002, 21:297-306.
112. Rithidech K.N., Honikel L., Milazzo M., Madigan D., Troxell R., Krupp L.B. Protein expression profiles in pediatric multiple sclerosis: potential biomarkers. Mult Scler 2009, 15:455-464.
113. Gabay C., Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med 1999, 340:448-454.
114. Fuchs E., Weber K. Intermediate filaments: structure, dynamics, function, and disease. Annu Rev Biochem 1994, 63:345-382.
115. van der Flier A., Sonnenberg A. Structural and functional aspects of filamins. Biochim Biophys Acta 2001, 1538:99-117.
116. Lock C., Hermans G., Pedotti R., et al. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat Med 2002, 8:500-508.
117. Amieva M.R., Furthmayr H. Subcellular localization of moesin in dynamic filopodia, retraction fibers, and other structures involved in substrate exploration, attachment, and cell-cell contacts. Exp Cell Res 1995, 219:180-196.
118. Holley J.E., Gveric D., Newcombe J., Cuzner M.L., Gutowski N.J. Astrocyte characterization in the multiple sclerosis glial scar. Neuropathol Appl Neurobiol 2003, 29:434-444.
119. Malmestrom C., Haghighi S., Rosengren L., Andersen O., Lycke J. Neurofilament light protein and glial fibrillary acidic protein as biological markers in MS. Neurology 2003, 61:1720-1725.
120. Norgren N., Sundstrom P., Svenningsson A., Rosengren L., Stigbrand T., Gunnarsson M. Neurofilament and glial fibrillary acidic protein in multiple sclerosis. Neurology 2004, 63:1586-1590.
121. Rosengren L.E., Lycke J., Andersen O. Glial fibrillary acidic protein in CSF of multiple sclerosis patients: relation to neurological deficit. J Neurol Sci 1995, 133:61-65.
122. Selmaj K., Pawlowska Z., Walczak A., Koziolkiewicz W., Raine C.S., Cierniewski C.S. Corpora amylacea from multiple sclerosis brain tissue consists of aggregated neuronal cells. Acta Biochim Pol 2008, 55:43-49.
123. Petzold A., Gveric D., Groves M., et al. Phosphorylation and compactness of neurofilaments in multiple sclerosis: indicators of axonal pathology. Exp Neurol 2008, 213:326-335.
124. Kolln J., Ren H.M., Da R.R., et al. Triosephosphate isomerase- and glyceraldehyde-3-phosphate dehydrogenase-reactive autoantibodies in the cerebrospinal fluid of patients with multiple sclerosis. J Immunol 2006, 177:5652-5658.
125. Bever C.T., Panitch H.S., Johnson K.P. Increased cathepsin B activity in peripheral blood mononuclear cells of multiple sclerosis patients. Neurology 1994, 44:745-748.
126. Bever C.T., Garver D.W. Increased cathepsin B activity in multiple sclerosis brain. J Neurol Sci 1995, 131:71-73.
127. Sueoka E., Yukitake M., Iwanaga K., Sueoka N., Aihara T., Kuroda Y. Autoantibodies against heterogeneous nuclear ribonucleoprotein B1 in CSF of MS patients. Ann Neurol 2004, 56:778-786.
128. Yukitake M., Sueoka E., Sueoka-Aragane N., et al. Significantly increased antibody response to heterogeneous nuclear ribonucleoproteins in cerebrospinal fluid of multiple sclerosis patients but not in patients with human T-lymphotropic virus type I-associated myelopathy/tropical spastic paraparesis. J Neurovirol 2008, 14:130-135.
129. Schonbrunner E.R., Schmid F.X. Peptidyl-prolyl cis-trans isomerase improves the efficiency of protein disulfide isomerase as a catalyst of protein folding. Proc Natl Acad Sci USA 1992, 89:4510-4513.
130. Ramanathan M., Weinstock-Guttman B., Nguyen L.T., et al. In vivo gene expression revealed by cDNA arrays: the pattern in relapsing-remitting multiple sclerosis patients compared with normal subjects. J Neuroimmunol 2001, 116:213-219.
131. Witte M.E., Bo L., Rodenburg R.J., et al. Enhanced number and activity of mitochondria in multiple sclerosis lesions. J Pathol 2009, 219:193-204.
132. Myllykoski M., Kursula P. Expression, purification, and initial characterization of different domains of recombinant mouse 2', 3'-cyclic nucleotide 3'-phosphodiesterase, an enigmatic enzyme from the myelin sheath. BMC Res Notes 2010, 3:12.
133. Lovato L., Cianti R., Gini B., et al. Transketolase and 2', 3'-cyclic-nucleotide 3'-phosphodiesterase type I isoforms are specifically recognized by IgG autoantibodies in multiple sclerosis patients. Mol Cell Proteomics 2008, 7:2337-2349.
134. Walsh M.J., Murray J.M. Dual implication of 2', 3'-cyclic nucleotide 3' phosphodiesterase as major autoantigen and C3 complement-binding protein in the pathogenesis of multiple sclerosis. J Clin Invest 1998, 101:1923-1931.
135. Irani D.N., Anderson C., Gundry R., et al. Cleavage of cystatin C in the cerebrospinal fluid of patients with multiple sclerosis. Ann Neurol 2006, 59:237-247.
136. Nakashima I., Fujinoki M., Fujihara K., et al. Alteration of cystatin C in the cerebrospinal fluid of multiple sclerosis. Ann Neurol 2007, 62:197-200.
137. Artru A.A. Spinal cerebrospinal fluid chemistry and physiology. Spinal drug and delivery 1999, 177-238. Elsevier Sciences B.V., Seattle, WA, USA.
138. Reindl M., Knipping G., Wicher I., et al. Increased intrathecal production of apolipoprotein D in multiple sclerosis. J Neuroimmunol 2001, 119:327-332.
139. Pitt D., Nagelmeier I.E., Wilson H.C., Raine C.S. Glutamate uptake by oligodendrocytes: Implications for excitotoxicity in multiple sclerosis. Neurology 2003, 61:1113-1120.
140. Moscarello M.A., Mastronardi F.G., Wood D.D. The role of citrullinated proteins suggests a novel mechanism in the pathogenesis of multiple sclerosis. Neurochem Res 2007, 32:251-256.
141. De Seze J., Dubucquoi S., Lefranc D., et al. IgG reactivity against citrullinated myelin basic protein in multiple sclerosis. J Neuroimmunol 2001, 117:149-155.
142. Kim J.K., Mastronardi F.G., Wood D.D., Lubman D.M., Zand R., Moscarello M.A. Multiple sclerosis: an important role for post-translational modifications of myelin basic protein in pathogenesis. Mol Cell Proteomics 2003, 2:453-462.
143. Tranquill L.R., Cao L., Ling N.C., Kalbacher H., Martin R.M., Whitaker J.N. Enhanced T cell responsiveness to citrulline-containing myelin basic protein in multiple sclerosis patients. Mult Scler 2000, 6:220-225.
144. Oguz K.K., Kurne A., Aksu A.O., et al. Assessment of citrullinated myelin by 1H-MR spectroscopy in early-onset multiple sclerosis. AJNR Am J Neuroradiol 2009, 30:716-721.
145. Gresle M.M., Shaw G., Jarrott B., et al. Validation of a novel biomarker for acute axonal injury in experimental autoimmune encephalomyelitis. J Neurosci Res 2008, 86:3548-3555.
146. Proia P., Schiera G., Salemi G., Ragonese P., Savettieri G., Di L.I. Neuronal and BBB damage induced by sera from patients with secondary progressive multiple sclerosis. Int J Mol Med 2009, 24:743-747.
147. Blecharz K.G., Haghikia A., Stasiolek M., et al. Glucocorticoid effects on endothelial barrier function in the murine brain endothelial cell line cEND incubated with sera from patients with multiple sclerosis. Mult Scler 2010, 16:293-302.
148. Minagar A., Ostanin D., Long A.C., et al. Serum from patients with multiple sclerosis downregulates occludin and VE-cadherin expression in cultured endothelial cells. Mult Scler 2003, 9:235-238.