Aquaporin 4-specific T cells in neuromyelitis optica exhibit a Th17 bias and recognize Clostridium ABC transporter

Annals of Neurology

Volumn 72, Issue 1, 2012, Pages 53-64

  Varrin Doyer, Michel ^a   Spencer, Collin M ^a   Schulze Topphoff, Ulf ^a   Nelson, Patricia A ^a   Stroud, Robert M ^a   C Cree, Bruce A ^a   Zamvil, Scott S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; AQUAPORIN 4; CYTOKINE; LEUKOCYTE ANTIGEN; PROTEIN P21; PROTEIN P30; PROTEIN P40; PROTEIN P80; RITUXIMAB; V SET DOMAIN CONTAINING T CELL ACTIVATION INHIBITOR 1;

ADULT; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CELL PROLIFERATION; CLINICAL ARTICLE; CLOSTRIDIUM PERFRINGENS; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; MALE; MONOCYTE; MYELOOPTIC NEUROPATHY; PRIORITY JOURNAL; T LYMPHOCYTE; TH17 CELL;

ADULT; AQUAPORIN 4; ATP-BINDING CASSETTE TRANSPORTERS; CELL PROLIFERATION; CLOSTRIDIUM; EPITOPES, T-LYMPHOCYTE; FEMALE; HUMANS; MALE; MIDDLE AGED; NEUROMYELITIS OPTICA; T-LYMPHOCYTES;

EID: 84864431745     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.23651     Document Type: Article

References (50)

1. Graber DJ, Levy M, Kerr D, Wade WF,. Neuromyelitis optica pathogenesis and aquaporin 4. J Neuroinflammation 2008; 5: 22.
2. Lennon VA, Kryzer TJ, Pittock SJ, et al. IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel. J Exp Med 2005; 202: 473-477. (Pubitemid 41186945)
3. Nurieva RI, Chung Y,. Understanding the development and function of T follicular helper cells. Cell Mol Immunol 2010; 7: 190-197.
4. Bennett JL, Lam C, Kalluri SR, et al. Intrathecal pathogenic anti-aquaporin-4 antibodies in early neuromyelitis optica. Ann Neurol 2009; 66: 617-629.
5. Bradl M, Misu T, Takahashi T, et al. Neuromyelitis optica: pathogenicity of patient immunoglobulin in vivo. Ann Neurol 2009; 66: 630-643.
6. Lucchinetti CF, Mandler RN, McGavern D, et al. A role for humoral mechanisms in the pathogenesis of Devic's neuromyelitis optica. Brain 2002; 125 (pt 7): 1450-1461. (Pubitemid 34755161)
7. Uzawa A, Mori M, Arai K, et al. Cytokine and chemokine profiles in neuromyelitis optica: significance of interleukin-6. Mult Scler 2010; 16: 1443-1452.
8. Wingerchuk DM, Lennon VA, Pittock SJ, et al. Revised diagnostic criteria for neuromyelitis optica. Neurology 2006; 66: 1485-1489. (Pubitemid 43958540)
9. Jacob A, Weinshenker BG, Violich I, et al. Treatment of neuromyelitis optica with rituximab: retrospective analysis of 25 patients. Arch Neurol 2008; 65: 1443-1448.
10. Ho JD, Yeh R, Sandstrom A, et al. Crystal structure of human aquaporin 4 at 1.8 A and its mechanism of conductance. Proc Natl Acad Sci U S A 2009; 106: 7437-7442.
11. Nielsen M, Lundegaard C, Lund O,. Prediction of MHC class II binding affinity using SMM-align, a novel stabilization matrix alignment method. BMC Bioinformatics 2007; 8: 238.
12. Nielsen M, Lund O,. NN-align. An artificial neural network-based alignment algorithm for MHC class II peptide binding prediction. BMC Bioinformatics 2009; 10: 296.
13. Zamvil SS, Mitchell DJ, Moore AC, et al. T-cell epitope of the autoantigen myelin basic protein that induces encephalomyelitis. Nature 1986; 324: 258-260. (Pubitemid 17180453)
14. Owens G, Ritchie A, Lam C, Bennett J,. Mutagenesis of aquaporin-4 extracellular domains defines binding patterns of neuromyelitis optica intrathecal IgG. Mult Scler 2011; 17 (10 suppl): S291-S292.
15. Mannering SI, Morris JS, Jensen KP, et al. A sensitive method for detecting proliferation of rare autoantigen-specific human T cells. J Immunol Methods 2003; 283: 173-183. (Pubitemid 37501068)
16. Nelson PA, Khodadoust M, Prodhomme T, et al. Immunodominant T cell determinants of aquaporin-4, the autoantigen associated with neuromyelitis optica. PLoS One 2010; 5: e15050.
17. Kalluri SR, Rothhammer V, Staszewski O, et al. Functional characterization of aquaporin-4 specific T cells: towards a model for neuromyelitis optica. PLoS One 2011; 6: e16083.
18. Slavin AJ, Soos JM, Stuve O, et al. Requirement for endocytic antigen processing and influence of invariant chain and H-2M deficiencies in CNS autoimmunity. J Clin Invest 2001; 108: 1133-1139. (Pubitemid 32995371)
19. Soos JM, Morrow J, Ashley TA, et al. Astrocytes express elements of the class II endocytic pathway and process central nervous system autoantigen for presentation to encephalitogenic T cells. J Immunol 1998; 161: 5959-5966. (Pubitemid 28535964)
20. Zamvil S, Nelson P, Trotter J, et al. T-cell clones specific for myelin basic protein induce chronic relapsing paralysis and demyelination. Nature 1985; 317: 355-358. (Pubitemid 15232523)
21. Vyas JM, Van der Veen AG, Ploegh HL,. The known unknowns of antigen processing and presentation. Nat Rev Immunol 2008; 8: 607-618.
22. Matsushita T, Matsuoka T, Isobe N, et al. Association of the HLA-DPB1*0501 allele with anti-aquaporin-4 antibody positivity in Japanese patients with idiopathic central nervous system demyelinating disorders. Tissue Antigens 2009; 73: 171-176.
23. Brum DG, Barreira AA, dos Santos AC, et al. HLA-DRB association in neuromyelitis optica is different from that observed in multiple sclerosis. Mult Scler 2010; 16: 21-29.
24. Deschamps R, Paturel L, Jeannin S, et al. Different HLA class II (DRB1 and DQB1) alleles determine either susceptibility or resistance to NMO and multiple sclerosis among the French Afro-Caribbean population. Mult Scler 2011; 17: 24-31.
25. Fujinami RS, Oldstone MB,. Amino acid homology between the encephalitogenic site of myelin basic protein and virus: mechanism for autoimmunity. Science 1985; 230: 1043-1045. (Pubitemid 16192692)
26. Wucherpfennig KW, Strominger JL,. Molecular mimicry in T cell-mediated autoimmunity: viral peptides activate human T cell clones specific for myelin basic protein. Cell 1995; 80: 695-705.
27. Warabi Y, Yagi K, Hayashi H, Matsumoto Y,. Characterization of the T cell receptor repertoire in the Japanese neuromyelitis optica: T cell activity is up-regulated compared to multiple sclerosis. J Neurol Sci 2006; 249: 145-152. (Pubitemid 44665918)
28. Acosta-Rodriguez EV, Napolitani G, Lanzavecchia A, Sallusto F,. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol 2007; 8: 942-949. (Pubitemid 47300008)
29. Katzman SD, Gallo E, Hoyer KK, Abbas AK,. Differential requirements for Th1 and Th17 responses to a systemic self-antigen. J Immunol 2011; 186: 4668-4673.
30. Kuchroo VK, Das MP, Brown JA, et al. B7-1 and B7-2 costimulatory molecules activate differentially the Th1/Th2 developmental pathways: application to autoimmune disease therapy. Cell 1995; 80: 707-718.
31. Benjamin DC, Berzofsky JA, East IJ, et al. The antigenic structure of proteins: a reappraisal. Annu Rev Immunol 1984; 2: 67-101.
32. Weber MS, Prod'homme T, Patarroyo JC, et al. B-cell activation influences T-cell polarization and outcome of anti-CD20 B-cell depletion in central nervous system autoimmunity. Ann Neurol 2010; 68: 369-383.
33. Kaushansky N, Zhong MC, Kerlero de Rosbo N, et al. Epitope specificity of autoreactive T and B cells associated with experimental autoimmune encephalomyelitis and optic neuritis induced by oligodendrocyte-specific protein in SJL/J mice. J Immunol 2006; 177: 7364-7376. (Pubitemid 44715107)
34. Morita R, Schmitt N, Bentebibel SE, et al. Human blood CXCR5(+)CD4(+) T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion. Immunity 2011; 34: 108-121.
35. Popescu BF, Lennon VA, Parisi JE, et al. Neuromyelitis optica unique area postrema lesions: nausea, vomiting, and pathogenic implications. Neurology 2011; 76: 1229-1237.
36. Kebir H, Kreymborg K, Ifergan I, et al. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat Med 2007; 13: 1173-1175. (Pubitemid 47530640)
37. Huppert J, Closhen D, Croxford A, et al. Cellular mechanisms of IL-17-induced blood-brain barrier disruption. FASEB J 2010; 24: 1023-1034.
38. Roussel L, Houle F, Chan C, et al. IL-17 promotes p38 MAPK-dependent endothelial activation enhancing neutrophil recruitment to sites of inflammation. J Immunol 2010; 184: 4531-4537.
39. Berer K, Mues M, Koutrolos M, et al. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 2011; 479: 538-541.
40. Ochoa-Reparaz J, Mielcarz DW, Begum-Haque S, Kasper LH,. Gut, bugs, and brain: role of commensal bacteria in the control of central nervous system disease. Ann Neurol 2011; 69: 240-247.
41. Nielsen M, Justesen S, Lund O, et al. NetMHCIIpan-2.0 - improved pan-specific HLA-DR predictions using a novel concurrent alignment and weight optimization training procedure. Immunome Res 2010; 6: 9.
42. Lindstrom M, Heikinheimo A, Lahti P, Korkeala H,. Novel insights into the epidemiology of Clostridium perfringens type A food poisoning. Food Microbiol 2011; 28: 192-198.
43. Ivanov, II, Atarashi K, Manel N, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009; 139: 485-498.
44. Atarashi K, Tanoue T, Shima T, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011; 331: 337-341.
45. Lindsey JW, Meulmester KM, Brod SA, et al. Variable results after rituximab in neuromyelitis optica. J Neurol Sci 2012; 317: 103-105.
46. Axtell RC, Raman C, Steinman L,. Interferon-beta exacerbates Th17-mediated inflammatory disease. Trends Immunol 2011; 32: 272-277.
47. Warabi Y, Matsumoto Y, Hayashi H,. Interferon beta-1b exacerbates multiple sclerosis with severe optic nerve and spinal cord demyelination. J Neurol Sci 2007; 252: 57-61. (Pubitemid 44909191)
48. Shimizu J, Hatanaka Y, Hasegawa M, et al. IFNbeta-1b may severely exacerbate Japanese optic-spinal MS in neuromyelitis optica spectrum. Neurology 2010; 75: 1423-1427.
49. Palace J, Leite MI, Nairne A, Vincent A,. Interferon Beta treatment in neuromyelitis optica: increase in relapses and aquaporin 4 antibody titers. Arch Neurol 2010; 67: 1016-1017.
50. Crane JM, Tajima M, Verkman AS,. Live-cell imaging of aquaporin-4 diffusion and interactions in orthogonal arrays of particles. Neuroscience 2010; 168: 892-902.