Melanoma cell adhesion molecule-positive CD8 T lymphocytes mediate central nervous system inflammation

Annals of Neurology

Volumn 78, Issue 1, 2015, Pages 39-53

  Larochelle, Catherine ^a,b   Lécuyer, Marc André ^a   Alvarez, Jorge Ivan ^a   Charabati, Marc ^a   Saint Laurent, Olivia ^a   Ghannam, Soufiane ^a   Kebir, Hania ^a   Flanagan, Ken ^c   Yednock, Ted ^c   Duquette, Pierre ^a,b   Arbour, Nathalie ^a,b   Prat, Alexandre ^a,b  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c Prothena Biosciences Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CD146 ANTIGEN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 17; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; TUMOR NECROSIS FACTOR; MCAM PROTEIN, HUMAN; MCAM PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPSY; BLOOD BRAIN BARRIER; CD8+ T LYMPHOCYTE; CENTRAL NERVOUS SYSTEM; CYTOKINE PRODUCTION; DISEASE ACTIVITY; EFFECTOR CELL; ENDOTHELIUM CELL; EX VIVO STUDY; FLOW CYTOMETRY; FROZEN SECTION; HUMAN; HUMAN CELL; IMMUNE SYSTEM; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE MIGRATION; MOUSE; MULTIPLE SCLEROSIS; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; ANIMAL; CASE CONTROL STUDY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; IMMUNOLOGY; INFLAMMATION; METABOLISM; OLIGODENDROGLIA;

ANIMALS; ANTIGENS, CD146; BLOOD-BRAIN BARRIER; CASE-CONTROL STUDIES; CD8-POSITIVE T-LYMPHOCYTES; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; IN VITRO TECHNIQUES; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-17; MICE; MICE, TRANSGENIC; MULTIPLE SCLEROSIS, RELAPSING-REMITTING; OLIGODENDROGLIA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84933180446     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.24415     Document Type: Article

References (58)

1. Codarri L, Gyulveszi G, Tosevski V, et al., RORgammat drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat Immunol 2011; 12: 560-567.
2. El-Behi M, Ciric B, Dai H, et al., The encephalitogenicity of T(H)17 cells is dependent on IL-1- and IL-23-induced production of the cytokine GM-CSF. Nat Immunol 2011; 12: 568-575.
3. Ghoreschi K, Laurence A, Yang XP, et al., Generation of pathogenic T(H)17 cells in the absence of TGF-beta signalling. Nature 2010; 467: 967-971.
4. Langrish CL, Chen Y, Blumenschein WM, et al., IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 2005; 201: 233-240.
5. Kebir H, Ifergan I, Alvarez JI, et al., Preferential recruitment of interferon-gamma-expressing TH17 cells in multiple sclerosis. Ann Neurol 2009; 66: 390-402.
6. Reboldi A, Coisne C, Baumjohann D, et al., C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat Immunol 2009; 10: 514-523.
7. Brucklacher-Waldert V, Stuerner K, Kolster M, et al., Phenotypical and functional characterization of T helper 17 cells in multiple sclerosis. Brain 2009; 132 (pt 12): 3329-3341.
8. Flanagan K, Fitzgerald K, Baker J, et al., Laminin-411 is a vascular ligand for MCAM and facilitates TH17 cell entry into the CNS. PLoS One 2012; 7: e40443.
9. Larochelle C, Cayrol R, Kebir H, et al., Melanoma cell adhesion molecule identifies encephalitogenic T lymphocytes and promotes their recruitment to the central nervous system. Brain 2012; 135 (pt 10): 2906-2924.
10. Maggi L, Santarlasci V, Capone M, et al., CD161 is a marker of all human IL-17-producing T-cell subsets and is induced by RORC. Eur J Immunol 2010; 40: 2174-2181.
11. Annibali V, Ristori G, Angelini DF, et al., CD161(high)CD8+T cells bear pathogenetic potential in multiple sclerosis. Brain 2011; 134 (pt 2): 542-554.
12. Abrahamsson SV, Angelini DF, Dubinsky AN, et al., Non-myeloablative autologous haematopoietic stem cell transplantation expands regulatory cells and depletes IL-17 producing mucosal-associated invariant T cells in multiple sclerosis. Brain 2013; 136 (pt 9): 2888-2903.
13. Huber M, Heink S, Pagenstecher A, et al., IL-17A secretion by CD8+ T cells supports Th17-mediated autoimmune encephalomyelitis. J Clin Invest 2013; 123: 247-260.
14. Tzartos JS, Friese MA, Craner MJ, et al., Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am J Pathol 2008; 172: 146-155.
15. Ifergan I, Kebir H, Alvarez JI, et al., Central nervous system recruitment of effector memory CD8+ T lymphocytes during neuroinflammation is dependent on alpha4 integrin. Brain 2011; 134 (pt 12): 3560-3577.
16. Denic A, Wootla B, Rodriguez M,. CD8(+) T cells in multiple sclerosis. Expert Opin Ther Targets 2013; 17: 1053-1066.
17. Polman CH, Reingold SC, Banwell B, et al., Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol 2011; 69: 292-302.
18. Ifergan I, Kebir H, Bernard M, et al., The blood-brain barrier induces differentiation of migrating monocytes into Th17-polarizing dendritic cells. Brain 2008; 131 (pt 3): 785-799.
19. Pollinger B, Krishnamoorthy G, Berer K, et al., Spontaneous relapsing-remitting EAE in the SJL/J mouse: MOG-reactive transgenic T cells recruit endogenous MOG-specific B cells. J Exp Med 2009; 206: 1303-1316.
20. Alvarez JI, Teale JM,. Multiple expression of matrix metalloproteinases in murine neurocysticercosis: implications for leukocyte migration through multiple central nervous system barriers. Brain Res 2008; 1214: 145-158.
21. Ifergan I, Wosik K, Cayrol R, et al., Statins reduce human blood-brain barrier permeability and restrict leukocyte migration: relevance to multiple sclerosis. Ann Neurol 2006; 60: 45-55.
22. Pittet CL, Newcombe J, Antel JP, Arbour N,. The majority of infiltrating CD8 T lymphocytes in multiple sclerosis lesions is insensitive to enhanced PD-L1 levels on CNS cells. Glia 2011; 59: 841-856.
23. Cayrol R, Wosik K, Berard JL, et al., Activated leukocyte cell adhesion molecule promotes leukocyte trafficking into the central nervous system. Nat Immunol 2008; 9: 137-145.
24. 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.
25. Saikali P, Antel JP, Pittet CL, et al., Contribution of astrocyte-derived IL-15 to CD8 T cell effector functions in multiple sclerosis. J Immunol 2010; 185: 5693-5703.
26. Zaguia F, Saikali P, Ludwin S, et al., Cytotoxic NKG2C+ CD4 T cells target oligodendrocytes in multiple sclerosis. J Immunol 2013; 190: 2510-2518.
27. D'Souza S, Alinauskas K, McCrea E, et al., Differential susceptibility of human CNS-derived cell populations to TNF-dependent and independent immune-mediated injury. J Neurosci 1995; 15: 7293-7300.
28. D'Souza SD, Bonetti B, Balasingam V, et al., Multiple sclerosis: Fas signaling in oligodendrocyte cell death. J Exp Med 1996; 184: 2361-2370.
29. Wosik K, Ruffini F, Almazan G, et al., Resistance of human adult oligodendrocytes to AMPA/kainate receptor-mediated glutamate injury. Brain 2004; 127 (pt 12): 2636-2648.
30. McLaurin J, Trudel GC, Shaw IT, et al., A human glial hybrid cell line differentially expressing genes subserving oligodendrocyte and astrocyte phenotype. J Neurobiol 1995; 26: 283-293.
31. Schneider R, Mohebiany AN, Ifergan I, et al., B cell-derived IL-15 enhances CD8 T cell cytotoxicity and is increased in multiple sclerosis patients. J Immunol 2011; 187: 4119-4128.
32. Dagur PK, Biancotto A, Wei L, et al., MCAM-expressing CD4(+) T cells in peripheral blood secrete IL-17A and are significantly elevated in inflammatory autoimmune diseases. J Autoimmun 2011; 37: 319-327.
33. Dagur PK, Tatlici G, Gourley M, et al., CD146+ T lymphocytes are increased in both the peripheral circulation and in the synovial effusions of patients with various musculoskeletal diseases and display pro-inflammatory gene profiles. Cytometry B Clin Cytom 2010; 78: 88-95.
34. Kamiyama T, Watanabe H, Iijima M, et al., Coexpression of CCR6 and CD146 (MCAM) is a marker of effector memory T-helper 17 cells. J Dermatol 2012; 39: 838-842.
35. Duan H, Xing S, Luo Y, et al., Targeting endothelial CD146 attenuates neuroinflammation by limiting lymphocyte extravasation to the CNS. Sci Rep 2013; 3: 1687.
36. Staquicini FI, Tandle A, Libutti SK, et al., A subset of host B lymphocytes controls melanoma metastasis through a melanoma cell adhesion molecule/MUC18-dependent interaction: evidence from mice and humans. Cancer Res 2008; 68: 8419-8428.
37. Rothhammer V, Muschaweckh A, Gasteiger G, et al., alpha4-integrins control viral meningoencephalitis through differential recruitment of T helper cell subsets. Acta Neuropathol Commun 2014; 2: 27.
38. Schneider-Hohendorf T, Rossaint J, Mohan H, et al., VLA-4 blockade promotes differential routes into human CNS involving PSGL-1 rolling of T cells and MCAM-adhesion of TH17 cells. J Exp Med 2014; 211: 1833-1846.
39. International Multiple Sclerosis Genetics Consortium; Wellcome Trust Case Control Consortium 2, Sawcer S, Hellenthal G, Pirinen M, et al., Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 2011; 476: 214-219.
40. Lucchinetti CF, Popescu BF, Bunyan RF, et al., Inflammatory cortical demyelination in early multiple sclerosis. N Engl J Med 2011; 365: 2188-2197.
41. Skulina C, Schmidt S, Dornmair K, et al., Multiple sclerosis: brain-infiltrating CD8+ T cells persist as clonal expansions in the cerebrospinal fluid and blood. Proc Natl Acad Sci U S A 2004; 101: 2428-2433.
42. Babbe H, Roers A, Waisman A, et al., Clonal expansions of CD8(+) T cells dominate the T cell infiltrate in active multiple sclerosis lesions as shown by micromanipulation and single cell polymerase chain reaction. J Exp Med 2000; 192: 393-404.
43. Hauser SL, Bhan AK, Gilles F, et al., Immunohistochemical analysis of the cellular infiltrate in multiple sclerosis lesions. Ann Neurol 1986; 19: 578-587.
44. Monteiro J, Hingorani R, Pergolizzi R, et al., Clonal dominance of CD8+ T-cell in multiple sclerosis. Ann N Y Acad Sci 1995; 756: 310-312.
45. Gravano DM, Hoyer KK,. Promotion and prevention of autoimmune disease by CD8+ T cells. J Autoimmun 2013; 45: 68-79.
46. Ciric B, El-behi M, Cabrera R, et al., IL-23 drives pathogenic IL-17-producing CD8+ T cells. J Immunol 2009; 182: 5296-5305.
47. Najafian N, Chitnis T, Salama AD, et al., Regulatory functions of CD8+CD28- T cells in an autoimmune disease model. J Clin Invest 2003; 112: 1037-1048.
48. Gilliet M, Liu YJ,. Generation of human CD8 T regulatory cells by CD40 ligand-activated plasmacytoid dendritic cells. J Exp Med 2002; 195: 695-704.
49. Correale J, Villa A,. Role of CD8+ CD25+ Foxp3+ regulatory T cells in multiple sclerosis. Ann Neurol 2010; 67: 625-638.
50. Hadjinicolaou AV, Wu L, Fang B, et al., Relationship of CD146 expression to activation of circulating T cells: exploratory studies in healthy donors and patients with connective tissue diseases. Clin Exp Immunol 2013; 174: 73-88.
51. Dagur PK, Biancotto A, Stansky E, et al., Secretion of interleukin-17 by CD8+ T cells expressing CD146 (MCAM). Clin Immunol 2014; 152: 36-47.
52. Mehta NN, Dagur PK, Rose SM, et al., IL-17A production in human psoriatic blood and lesions by CD146+ T cells. J Invest Dermatol 2015; 135: 311-314.
53. Agrawal SM, Yong VW,. The many faces of EMMPRIN-roles in neuroinflammation. Biochim Biophys Acta 2011; 1812: 213-219.
54. Agrawal SM, Silva C, Tourtellotte WW, Yong VW,. EMMPRIN: a novel regulator of leukocyte transmigration into the CNS in multiple sclerosis and experimental autoimmune encephalomyelitis. J Neurosci 2011; 31: 669-677.
55. Biegler BW, Yan SX, Ortega SB, et al., Glatiramer acetate (GA) therapy induces a focused, oligoclonal CD8+ T-cell repertoire in multiple sclerosis. J Neuroimmunol 2006; 180: 159-171.
56. Satoh T, Tajima M, Wakita D, et al., The development of IL-17/IFN-gamma-double producing CTLs from Tc17 cells is driven by epigenetic suppression of Socs3 gene promoter. Eur J Immunol 2012; 42: 2329-2342.
57. Tajima M, Wakita D, Satoh T, et al., IL-17/IFN-gamma double producing CD8+ T (Tc17/IFN-gamma) cells: a novel cytotoxic T-cell subset converted from Tc17 cells by IL-12. Int Immunol 2011; 23: 751-759.
58. Sarin R, Wu X, Abraham C,. Inflammatory disease protective R381Q IL23 receptor polymorphism results in decreased primary CD4+ and CD8+ human T-cell functional responses. Proc Natl Acad Sci U S A 2011; 108: 9560-9565.