Altered expression of oligodendrocyte and neuronal marker genes predicts the clinical onset of autoimmune encephalomyelitis and indicates the effectiveness of multiple sclerosis-directed therapeutics

Journal of Immunology

Volumn 192, Issue 9, 2014, Pages 4122-4133

  Evangelidou, Maria ^a   Karamita, Maria ^a   Vamvakas, Sotiris Spyros ^a   Szymkowski, David E ^b   Probert, Lesley ^a  

^a HELLENIC PASTEUR INSTITUTE   (Greece)

^b Xencor Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLATIRAMER; GLYCOPROTEIN GP 35 55; I KAPPA B KINASE BETA; INTERLEUKIN 17; MYELIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; PEPTIDE; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR INHIBITOR; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL LINEAGE; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE COURSE; DISEASE MARKER; DOWN REGULATION; ENZYME DEFICIENCY; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE LOCATION; IL17A GENE; IMMUNOPATHOGENESIS; INNATE IMMUNITY; MARKER GENE; MOUSE; MULTIPLE SCLEROSIS; NERVE CELL; NONHUMAN; OLIGODENDROGLIA; PHARMACOGENETICS; PRIORITY JOURNAL; SPINAL CORD; SYMPTOM; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; BIOLOGICAL MARKERS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIPLE SCLEROSIS; NEURONS; OLIGODENDROGLIA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPINAL CORD; TRANSCRIPTOME;

EID: 84899584253     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300633     Document Type: Article

References (60)

1. Lucchinetti, C., W. Bruck, J. Parisi, B. Scheithauer, M. Rodriguez, and H. Lassmann. 2000. Heterogeneity of multiple sclerosis lesions: Implications for the pathogenesis of demyelination. Ann. Neurol. 47: 707-717
2. Sawcer, S., G. Hellenthal, M. Pirinen, C. C. Spencer, N. A. Patsopoulos, L. Moutsianas, A. Dilthey, Z. Su, C. Freeman, S. E. Hunt, et al; 2011. International Multiple Sclerosis Genetics Consortium; Wellcome Trust Case Control Consortium Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 476: 214-219
3. Polman, C. H., P. W. O?Connor, E. Havrdova, M. Hutchinson, L. Kappos, D. H. Miller, J. T. Phillips, F. D. Lublin, G. GioVannoni, A. Wajgt, et al; AFFIRM Investigators. 2006. A randomized, placebo-controlled trial of natalizumab for relapsing multiple sclerosis. N. Engl. J. Med. 354: 899-910
4. Hauser, S. L., E.Waubant, D. L. Arnold, T. Vollmer, J. Antel, R. J. Fox, A. Bar-Or, M. Panzara, N. Sarkar, S. Agarwal, et al; HERMES Trial Group. 2008. B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. N. Engl. J. Med. 358: 676-688
5. Trapp, B. D., and K. A. Nave. 2008. Multiple sclerosis: An immune or neurodegenerative disorDer? Annu. Rev. Neurosci. 31: 247-269
6. Gold, R., C. Linington, and H. Lassmann. 2006. UnDerstanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain 129: 1953-1971
7. Flugel, A., T. Berkowicz, T. Ritter, M. Labeur, D. E. Jenne, Z. Li, J. W. Ellwart, M. Willem, H. Lassmann, and H. Wekerle. 2001. Migratory activity and functional changes of green fluorescent effector cells before and during experimental autoimmune encephalomyelitis. Immunity 14: 547-560
8. Bartholomäus, I., N. Kawakami, F. Odoardi, C. Schläger, D. Miljkovic, J. W. Ellwart, W. E. Klinkert, C. Flugel-Koch, T. B. Issekutz, H. Wekerle, and A. Flugel. 2009. Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature 462: 94-98
9. Centonze, D., L. Muzio, S. Rossi, F. Cavasinni, V. De Chiara, A. Bergami, A. Musella, M. D?Amelio, V. Cavallucci, A. Martorana, et al. 2009. Inflammation triggers synaptic alteration and degeneration in experimental autoimmune encephalomyelitis. J. Neurosci. 29: 3442-3452
10. Baranzini, S. E., C. C. Bernard, and J. R. Oksenberg. 2005. Modular transcriptional activity characterizes the initiation and progression of autoimmune encephalomyelitis. J. Immunol. 174: 7412-7422
11. Davalos, D., J. K. Ryu, M. Merlini, K. M. Baeten, N. Le Moan, M. A. Petersen, T. J. Deerinck, D. S. Smirnoff, C. Bedard, H. Hakozaki, et al. 2012. Fibrinogeninduced perivascular microglial clustering is required for the development of axonal damage in neuroinflammation. Nat Commun 3: 1227
12. Park, J. M., F. R. Greten, Z. W. Li, and M. Karin. 2002. Macrophage apoptosis by anthrax lethal factor through p38 MAP kinase inhibition. Science 297: 2048-2051
13. Li, Z. W., S. A. Omori, T. Labuda, M. Karin, and R. C. Rickert. 2003. IKK beta is required for peripheral B cell survival and proliferation. J. Immunol. 170: 4630-4637
14. Boillée, S., K. Yamanaka, C. S. Lobsiger, N. G. Copeland, N. A. Jenkins, G. Kassiotis, G. Kollias, and D. W. Cleveland. 2006. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312: 1389-1392
15. Emmanouil, M., E. Taoufik, V. Tseveleki, S. S. Vamvakas, T. Tselios, M. Karin, H. Lassmann, and L. Probert. 2009. Neuronal I kappa B kinase beta protects mice from autoimmune encephalomyelitis by mediating neuroprotective and immunosuppressive effects in the central nervous system. J. Immunol. 183: 7877-7889
16. Jee, Y., W. H. Piao, R. Liu, X. F. Bai, S. Rhodes, R. Rodebaugh, D. I. Campagnolo, F. D. Shi, and T. L. Vollmer. 2007. CD4(+)CD25(+) regulatory T cells contribute to the therapeutic effects of glatiramer acetate in experimental autoimmune encephalomyelitis. Clin. Immunol. 125: 34-42
17. Steed, P. M., M. G. Tansey, J. Zalevsky, E. A. Zhukovsky, J. R. Desjarlais, D. E. Szymkowski, C. Abbott, D. Carmichael, C. Chan, L. Cherry, et al. 2003. Inactivation of TNF signaling by rationally designed dominant-negative TNF variants. Science 301: 1895-1898
18. Zalevsky, J., T. Secher, S. A. Ezhevsky, L. Janot, P. M. Steed, C. O?Brien, A. Eivazi, J. Kung, D. H. Nguyen, S. K. Doberstein, et al. 2007. Dominantnegative inhibitors of soluble TNF attenuate experimental arthritis without suppressing innate immunity to infection. J. Immunol. 179: 1872-1883
19. Murray, K. M., and S. L. Dahl. 1997. Recombinant human tumor necrosis factor receptor (p75) Fc fusion protein (TNFR:Fc) in rheumatoid arthritis. Ann. Pharmacother. 31: 1335-1338
20. Nicolussi, E. M., S. Huck, H. Lassmann, and M. Bradl. 2009. The cholinergic anti-inflammatory system limits T cell infiltration into the neurodegenerative CNS, but cannot counteract complex CNS inflammation. Neurobiol. Dis. 35: 24-31
21. Tseveleki, V., R. Rubio, S. S. Vamvakas, J. White, E. Taoufik, E. Petit, J. Quackenbush, and L. Probert. 2010. Comparative gene expression analysis in mouse models for multiple sclerosis, Alzheimer?s disease and stroke for identifying commonly regulated and disease-specific gene changes. Genomics 96: 82-91
22. Ibrahim, S. M., E. Mix, T. Böttcher, D. Koczan, R. Gold, A. Rolfs, and H. J. Thiesen. 2001. Gene expression profiling of the nervous system in murine experimental autoimmune encephalomyelitis. Brain 124: 1927-1938
23. Jelinsky, S. A., J. S. Miyashiro, K. A. Saraf, C. Tunkey, P. Reddy, J. Newcombe, J. L. Oestreicher, E. Brown, W. L. Trepicchio, J. P. Leonard, and S. Marusic. 2005. Exploiting genotypic differences to identify genes important for EAE development. J. Neurol. Sci. 239: 81-93
24. Whitney, L. W., S. K. Ludwin, H. F. McFarland, and W. E. Biddison. 2001. Microarray analysis of gene expression in multiple sclerosis and EAE identifies 5-lipoxygenase as a component of inflammatory lesions. J. Neuroimmunol. 121: 40-48
25. Lock, C., G. Hermans, R. Pedotti, A. Brendolan, E. Schadt, H. Garren, A. Langer-Gould, S. Strober, B. Cannella, J. Allard, et al. 2002. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat. Med. 8: 500-508
26. Tajouri, L., A. S. Mellick, K. J. Ashton, A. E. Tannenberg, R. M. Nagra, W. W. Tourtellotte, and L. R. Griffiths. 2003. Quantitative and qualitative changes in gene expression patterns characterize the activity of plaques in multiple sclerosis. Brain Res. Mol. Brain Res. 119: 170-183
27. Graumann, U., R. Reynolds, A. J. Steck, and N. Schaeren-Wiemers. 2003. Molecular changes in normal appearing white matter in multiple sclerosis are characteristic of neuroprotective mechanisms against hypoxic insult. Brain Pathol. 13: 554-573
28. Lindberg, R. L., C. J. De Groot, U. Certa, R. Ravid, F. Hoffmann, L. Kappos, and D. Leppert. 2004. Multiple sclerosis as a generalized CNS disease-comparative microarray analysis of normal appearing white matter and lesions in secondary progressive MS. J. Neuroimmunol. 152: 154-167
29. Mycko, M. P., R. Papoian, U. Boschert, C. S. Raine, and K. W. Selmaj. 2004. Microarray gene expression profiling of chronic active and inactive lesions in multiple sclerosis. Clin. Neurol. Neurosurg. 106: 223-229
30. Carmody, R. J., B. Hilliard, K. Maguschak, L. A. Chodosh, and Y. H. Chen. 2002. Genomic scale profiling of autoimmune inflammation in the central nervous system: The nervous response to inflammation. J. Neuroimmunol. 133: 95-107
31. Li, H., and W. D. Richardson. 2008. The evolution of Olig genes and their roles in myelination. Neuron Glia Biol. 4: 129-135
32. Aharoni, R., A. Herschkovitz, R. Eilam, M. Blumberg-Hazan, M. Sela, W. Bruck, and R. Arnon. 2008. Demyelination arrest and remyelination induced by glatiramer acetate treatment of experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA 105: 11358-11363
33. Johnson, K. P., B. R. Brooks, J. A. Cohen, C. C. Ford, J. Goldstein, R. P. Lisak, L. W. Myers, H. S. Panitch, J. W. Rose, and R. B. Schiffer. 1995. Copolymer 1 reduces relapse rate and improves disability in relapsing-remitting multiple sclerosis: Results of a phase III multicenter, double-blind placebo-controlled trial. The Copolymer 1 Multiple Sclerosis Study Group. Neurology 45: 1268-1276
34. Heppner, F. L., M. Greter, D. Marino, J. Falsig, G. Raivich, N. Hövelmeyer, A. Waisman, T. Rulicke, M. Prinz, J. Priller, et al. 2005. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat. Med. 11: 146-152
35. Ellrichmann, G., J. Thöne, D. H. Lee, R. A. Rupec, R. Gold, and R. A. Linker. 2012. Constitutive activity of NF-kappa B in myeloid cells drives pathogenicity of monocytes and macrophages during autoimmune neuroinflammation. J. Neuroinflammation 9: 15
36. Cho, I. H., J. Hong, E. C. Suh, J. H. Kim, H. Lee, J. E. Lee, S. Lee, C. H. Kim, D. W. Kim, E. K. Jo, et al. 2008. Role of microglial IKKbeta in kainic acidinduced hippocampal neuronal cell death. Brain 131: 3019-3033
37. Taoufik, E., V. Tseveleki, S. Y. Chu, T. Tselios, M. Karin, H. Lassmann, D. E. Szymkowski, and L. Probert. 2011. Transmembrane tumour necrosis factor is neuroprotective and regulates experimental autoimmune encephalomyelitis via neuronal nuclear factor-kappaB. Brain 134: 2722-2735
38. Wu, F., W. Cao, Y. Yang, and A. Liu. 2010. Extensive infiltration of neutrophils in the acute phase of experimental autoimmune encephalomyelitis in C57BL/6 mice. Histochem. Cell Biol. 133: 313-322
39. Schmied, M., H. Breitschopf, R. Gold, H. Zischler, G. Rothe, H. Wekerle, and H. Lassmann. 1993. Apoptosis of T lymphocytes in experimental autoimmune encephalomyelitis. Evidence for programmed cell death as a mechanism to control inflammation in the brain. Am. J. Pathol. 143: 446-452
40. Korn, T., E. Bettelli, M. Oukka, and V. K. Kuchroo. 2009. IL-17 and Th17 Cells. Annu. Rev. Immunol. 27: 485-517
41. Lee, M. A., A. M. Blamire, S. Pendlebury, K. H. Ho, K. R. Mills, P. Styles, J. Palace, and P. M. Matthews. 2000. Axonal injury or loss in the internal capsule and motor impairment in multiple sclerosis. Arch. Neurol. 57: 65-70
42. Rodriguez, M., N. Prayoonwiwat, C. Howe, and K. Sanborn. 1994. Proteolipid protein gene expression in demyelination and remyelination of the central nervous system: A model for multiple sclerosis. J. Neuropathol. Exp. Neurol. 53: 136-143
43. Woodward, K. J. 2008. The molecular and cellular defects unDerlying Pelizaeus-Merzbacher disease. Expert Rev. Mol. Med. 10: E14
44. Nave, K. A. 2010. Myelination and support of axonal integrity by glia. Nature 468: 244-252
45. Kassmann, C. M., C. Lappe-Siefke, M. Baes, B. Brugger, A. Mildner, H. B. Werner, O. Natt, T. Michaelis, M. Prinz, J. Frahm, and K. A. Nave. 2007. Axonal loss and neuroinflammation caused by peroxisome-deficient oligodendrocytes. Nat. Genet. 39: 969-976
46. Cajigas, I. J., G. Tushev, T. J. Will, S. tom Dieck, N. Fuerst, and E. M. Schuman. 2012. The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. Neuron 74: 453-466
47. Rizo, J., and T. C. Sudhof. 2012. The membrane fusion enigma: SNAREs, Sec1/ Munc18 proteins, and their accomplices-guilty as charged? Annu. Rev. Cell Dev. Biol. 28: 279-308
48. Stefansson, H., E. Sigurdsson, V. Steinthorsdottir, S. Bjornsdottir, T. Sigmundsson, S. Ghosh, J. Brynjolfsson, S. Gunnarsdottir, O. Ivarsson, T. T. Chou, et al. 2002. Neuregulin 1 and susceptibility to schizophrenia. Am. J. Hum. Genet. 71: 877-892
49. Smith, T., A. Groom, B. Zhu, and L. Turski. 2000. Autoimmune encephalomyelitis ameliorated by AMPA antagonists. Nat. Med. 6: 62-66
50. Yang, G., C. N. Parkhurst, S. Hayes, and W. B. Gan. 2013. Peripheral elevation of TNF-a leads to early synaptic abnormalities in the mouse somatosensory cortex in experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA 110: 10306-10311
51. Marik, C., P. A. Felts, J. Bauer, H. Lassmann, and K. J. Smith. 2007. Lesion genesis in a subset of patients with multiple sclerosis: A role for innate immunity? Brain 130: 2800-2815
52. Ghosh, S., and M. Karin. 2002. Missing pieces in the NF-kappaB puzzle. Cell 109(Suppl.): S81-S96
53. Brambilla, R., J. J. Ashbaugh, R. Magliozzi, A. Dellarole, S. Karmally, D. E. Szymkowski, and J. R. Bethea. 2011. Inhibition of soluble tumour necrosis factor is therapeutic in experimental autoimmune encephalomyelitis and promotes axon preservation and remyelination. Brain 134: 2736-2754
54. Begum-Haque, S., A. Sharma, I. R. Kasper, D. M. Foureau, D. W. Mielcarz, A. Haque, and L. H. Kasper. 2008. Downregulation of IL-17 and IL-6 in the central nervous system by glatiramer acetate in experimental autoimmune encephalomyelitis. J. Neuroimmunol. 204: 58-65
55. Skihar, V., C. Silva, A. Chojnacki, A. Döring, W. B. Stallcup, S. Weiss, and V. W. Yong. 2009. Promoting oligodendrogenesis and myelin repair using the multiple sclerosis medication glatiramer acetate. Proc. Natl. Acad. Sci. USA 106: 17992-17997
56. Gilgun-Sherki, Y., H. Panet, V. Holdengreber, R. Mosberg-Galili, and D. Offen. 2003. Axonal damage is reduced following glatiramer acetate treatment in C57/ bl mice with chronic-induced experimental autoimmune encephalomyelitis. Neurosci. Res. 47: 201-207
57. Aharoni, R., R. Arnon, and R. Eilam. 2005. Neurogenesis and neuroprotection induced by peripheral immunomodulatory treatment of experimental autoimmune encephalomyelitis. J. Neurosci. 25: 8217-8228
58. Aharoni, R., R. Eilam, H. Domev, G. Labunskay, M. Sela, and R. Arnon. 2005. The immunomodulator glatiramer acetate augments the expression of neurotrophic factors in brains of experimental autoimmune encephalomyelitis mice. Proc. Natl. Acad. Sci. USA 102: 19045-19050
59. Hong, J., Y. C. Zang, G. Hutton, V. M. Rivera, and J. Z. Zhang. 2004. Gene expression profiling of releVant biomarkers for treatment evaluation in multiple sclerosis. J. Neuroimmunol. 152: 126-139
60. Carpintero, R., K. J. Brandt, L. Gruaz, N. Molnarfi, P. H. Lalive, and D. Burger. 2010. Glatiramer acetate triggers PI3Kd/Akt and MEK/ERK pathways to induce IL-1 receptor antagonist in human monocytes. Proc. Natl. Acad. Sci. USA 107: 17692-17697