CD8+ T cells in human autoimmune arthritis: The unusual suspects

Nature Reviews Rheumatology

Volumn 12, Issue 7, 2016, Pages 421-428

  Petrelli, Alessandra ^a   Van Wijk, Femke ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ABATACEPT; ADALIMUMAB; CORTICOSTEROID; DISEASE MODIFYING ANTIRHEUMATIC DRUG; ETANERCEPT; GAMMA INTERFERON; HLA ANTIGEN CLASS 1; HLA B27 ANTIGEN; INFLIXIMAB; INTERLEUKIN 17; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; METHOTREXATE; NONSTEROID ANTIINFLAMMATORY AGENT; RITUXIMAB; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR INHIBITOR; AUTOANTIBODY; BIOLOGICAL MARKER; HLA B ANTIGEN;

ANKYLOSING SPONDYLITIS; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; ARTHRITIS; AUTOCRINE EFFECT; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHRONIC INFLAMMATION; CROSS PRESENTATION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DAS28; DENDRITIC CELL; DISEASE SEVERITY; GENETIC SUSCEPTIBILITY; HUMAN; JUVENILE RHEUMATOID ARTHRITIS; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE HOMING; MEMORY T LYMPHOCYTE; PRIORITY JOURNAL; PSORIATIC ARTHRITIS; REVIEW; RHEUMATOID ARTHRITIS; T LYMPHOCYTE ACTIVATION; BLOOD; GENE; GENETICS; HOMEOSTASIS; IMMUNOLOGY; PHENOTYPE; REGULATORY T LYMPHOCYTE;

ARTHRITIS, RHEUMATOID; AUTOANTIBODIES; AUTOIMMUNE DISEASES; BIOMARKERS; CD8-POSITIVE T-LYMPHOCYTES; GENES, MHC CLASS I; HLA-B ANTIGENS; HOMEOSTASIS; HUMANS; PHENOTYPE; T-LYMPHOCYTES, REGULATORY;

EID: 84975849745     PISSN: 17594790     EISSN: 17594804     Source Type: Journal    
DOI: 10.1038/nrrheum.2016.74     Document Type: Review

References (105)

1. + T cell lineup. Nat. Immunol. 11, 36-40 (2010).
2. + T cells. J. Autoimmun. 45, 68-79 (2013).
3. Brewerton, D. A. et al. Ankylosing spondylitis and HLA 27. Lancet 1, 904-907 (1973).
4. Brown, M. A., Kenna, T. & Wordsworth, B. P. Genetics of ankylosing spondylitis-insights into pathogenesis. Nat. Rev. Rheumatol. 12, 81-91 (2016).
5. Evans, D. M. et al. Interaction between ERAP1 and HLAB27 in ankylosing spondylitis implicates peptide handling in the mechanism for HLAB27 in disease susceptibility. Nat. Genet. 43, 761-767 (2011).
6. Cortes, A. et al. Major histocompatibility complex associations of ankylosing spondylitis are complex and involve further epistasis with ERAP1. Nat. Commun. 6, 7146 (2015).
7. Bowes, J. et al. Dense genotyping of immune-related susceptibility loci reveals new insights into the genetics of psoriatic arthritis. Nat. Commun. 6, 6046 (2015).
8. Raychaudhuri, S. et al. Five amino acids in three HLA proteins explain most of the association between MHC and seropositive rheumatoid arthritis. Nat. Genet. 44, 291-296 (2012).
9. Hollenbach, J. A. et al. Juvenile idiopathic arthritis and HLA class I and class II interactions and ageatonset effects. Arthritis Rheum. 62, 1781-1791 (2010).
10. Hinks, A. et al. Dense genotyping of immune-related disease regions identifies 14 new susceptibility loci for juvenile idiopathic arthritis. Nat. Genet. 45, 664-669 (2013).
11. Ombrello, M. J. et al. HLADRB1∗11 and variants of the MHC class II locus are strong risk factors for systemic juvenile idiopathic arthritis. Proc. Natl Acad. Sci. USA 115, 15970-15975 (2015).
12. Coulthard, L. R. et al. Differential effects of infliximab on absolute circulating blood leucocyte counts of innate immune cells in early and late rheumatoid arthritis patients. Clin. Exp. Immunol. 170, 36-46 (2012).
13. Carvalheiro, H., Duarte, C., Silva-Cardoso, S., da Silva, J. A. & Souto-Carneiro, M. M. CD8+ T cell profiles in patients with rheumatoid arthritis and their relationship to disease activity. Arthritis Rheumatol. 67, 363-371 (2015).
14. Li, S. et al. Expression of programmed death1 (PD1) on CD4+ and CD8+ T cells in rheumatoid arthritis. Inflammation 37, 116-121 (2014).
15. Liu, Y. et al. Increased Tim3 expression on peripheral lymphocytes from patients with rheumatoid arthritis negatively correlates with disease activity. Clin. Immunol. 137, 288-295 (2010).
16. Costello, P., Bresnihan, B., O'Farrelly, C. & FitzGerald, O. Predominance of CD8+ T lymphocytes in psoriatic arthritis. J. Rheumatol. 26, 1117-1124 (1999).
17. Hunter, P. J. et al. Biologic predictors of extension of oligoarticular juvenile idiopathic arthritis as determined from synovial fluid cellular composition and gene expression. Arthritis Rheum. 62, 896-907 (2010).
18. + T cells in the synovial fluid of rheumatoid arthritis. J. Clin. Immunol. 32, 709-720 (2012).
19. Romio, M. et al. Extracellular purine metabolism and signaling of CD73derived adenosine in murine Treg and Teff cells. Am. J. Physiol. Cell Physiol. 301, C530-C539 (2011).
20. Botta Gordon-Smith, S., Ursu, S., Eaton, S., Moncrieffe, H. & Wedderburn, L. R. Correlation of low CD73 expression on synovial lymphocytes with reduced adenosine generation and higher disease severity in juvenile idiopathic arthritis. Arthritis Rheumatol. 67, 545-554 (2015).
21. + T cells: conditions for cloning T cells from psoriatic plaques. Exp. Dermatol. 13, 607-612 (2004).
22. Menon, B. et al. Interleukin17+CD8+ T cells are enriched in the joints of patients with psoriatic arthritis and correlate with disease activity and joint damage progression. Arthritis Rheumatol. 66, 1272-1281 (2014).
23. Sallusto, F., Lenig, D., Forster, R., Lipp, M. & Lanzavecchia, A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401, 708-712 (1999).
24. + T cell differentiation. Nat. Rev. Immunol. 12, 749-761 (2012).
25. Borgato, L. et al. The T cell receptor repertoire in psoriatic synovitis is restricted and T lymphocytes expressing the same TCR are present in joint and skin lesions. J. Rheumatol. 29, 1914-1919 (2002).
26. Mueller, S. N. & Mackay, L. K. Tissue-resident memory T cells: local specialists in immune defence. Nat. Rev. Immunol. 16, 79-89 (2016).
27. Vukmanovic-Stejic, M., Vyas, B., Gorak-Stolinska, P., Noble, A. & Kemeny, D. M. Human Tc1 and Tc2/Tc0 CD8 Tcell clones display distinct cell surface and functional phenotypes. Blood 95, 231-240 (2000).
28. Yen, H. R. et al. Tc17 CD8 T cells: functional plasticity and subset diversity. J. Immunol. 183, 7161-7168 (2009).
29. Liu, Y. et al. Interleukin21 induces the differentiation of human Tc22 cells via phosphorylation of signal transducers and activators of transcription. Immunology 132, 540-548 (2011).
30. Luan, L., Ding, Y., Han, S., Zhang, Z. & Liu, X. An increased proportion of circulating Th22 and Tc22 cells in psoriasis. Cell. Immunol. 290, 196-200 (2014).
31. + T lymphocytes from psoriasis skin plaques are cytotoxic effector cells that secrete Th17related cytokines. J. Leukoc. Biol. 86, 435-443 (2009).
32. Kirkham, B. W., Kavanaugh, A. & Reich, K. Interleukin17A: a unique pathway in immune-mediated diseases: psoriasis, psoriatic arthritis and rheumatoid arthritis. Immunology 141, 133-142 (2014).
33. Prezzemolo, T. et al. Functional signatures of human CD4 and CD8 T cell responses to Mycobacterium tuberculosis. Front. Immunol. 5, 180 (2014).
34. Li, S. et al. Expression of TIM3 on CD4+ and CD8+ T cells in the peripheral blood and synovial fluid of rheumatoid arthritis. APMIS 122, 899-904 (2014).
35. Kang, Y. M. et al. CD8 T cells are required for the formation of ectopic germinal centers in rheumatoid synovitis. J. Exp. Med. 195, 1325-1336 (2002).
36. Harada, S. et al. Production of interleukin7 and interleukin15 by fibroblast-like synoviocytes from patients with rheumatoid arthritis. Arthritis Rheum. 42, 1508-1516 (1999).
37. McInnes, I. B. et al. The role of interleukin15 in T cell migration and activation in rheumatoid arthritis. Nat. Med. 2, 175-182 (1996).
38. Fitzgerald, J. E. et al. Analysis of clonal CD8+ T cell expansions in normal individuals and patients with rheumatoid arthritis. J. Immunol. 154, 3538-3547 (1995).
39. Hingorani, R. et al. Oligoclonality of V beta 3 TC R chains in the CD8+ T cell population of rheumatoid arthritis patients. J. Immunol. 156, 852-858 (1996).
40. Hall, F. C., Thomson, K., Procter, J., McMichael, A. J. & Wordsworth, B. P. TCRb spectratyping in RA: evidence of clonal expansions in peripheral blood lymphocytes. Ann. Rheum. Dis. 57, 319-322 (1998).
41. Fazou, C., Yang, H., McMichael, A. J. & Callan, M. F. Epitope specificity of clonally expanded populations of CD8+ T cells found within the joints of patients with inflammatory arthritis. Arthritis Rheum. 44, 2038-2045 (2001).
42. Klarenbeek, P. L. et al. Inflamed target tissue provides a specific niche for highly expanded Tcell clones in early human autoimmune disease. Ann. Rheum. Dis. 71, 1088-1093 (2012).
43. Sathaliyawala, T. et al. Distribution and compartmentalization of human circulating and tissue-resident memory T cell subsets. Immunity 38, 187-197 (2013).
44. Iijima, N. & Iwasaki, A. Tissue instruction for migration and retention of TRM cells. Trends Immunol. 36, 556-564 (2015).
45. Thome, J. J. et al. Spatial map of human T cell compartmentalization and maintenance over decades of life. Cell 159, 814-828 (2014).
46. Farber, D. L., Yudanin, N. A. & Restifo, N. P. Human memory T cells: generation, compartmentalization and homeostasis. Nat. Rev. Immunol. 14, 24-35 (2014).
47. + tissue-resident memory T cells of skin. Nat. Immunol. 14, 1294-1301 (2013).
48. Clark, R. A. Resident memory T cells in human health and disease. Sci. Transl. Med. 7, 269rv261 (2015).
49. Cheuk, S. et al. Epidermal Th22 and Tc17 cells form a localized disease memory in clinically healed psoriasis. J. Immunol. 192, 3111-3120 (2014).
50. Henderson, L. A. et al. Novel 3dimensional explant method facilitates the study of lymphocyte populations in the synovium and reveals a large population of resident memory T cells in rheumatoid arthritis. Arthritis Rheum. 66, S209-S209 (2014).
51. Keir, M. E., Butte, M. J., Freeman, G. J. & Sharpe, A. H. PD1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 26, 677-704 (2008).
52. Okazaki, T., Chikuma, S., Iwai, Y., Fagarasan, S. & Honjo, T. A rheostat for immune responses: the unique properties of PD1 and their advantages for clinical application. Nat. Immunol. 14, 1212-1218 (2013).
53. Butte, M. J., Keir, M. E., Phamduy, T. B., Sharpe, A. H. & Freeman, G. J. Programmed death1 ligand 1 interacts specifically with the B71 costimulatory molecule to inhibit T cell responses. Immunity 27, 111-122 (2007).
54. Schneider, H. et al. Reversal of the TCR stop signal by CTLA4. Science 313, 1972-1975 (2006).
55. Francisco, L. M. et al. PDL1 regulates the development, maintenance, and function of induced regulatory T cells. J. Exp. Med. 206, 3015-3029 (2009).
56. + regulatory Tcell-mediated suppression. Immunology 118, 240-249 (2006).
57. Sehrawat, S. et al. Galectin9/TIM3 interaction regulates virus-specific primary and memory CD8 T cell response. PLoS Pathog. 6, e1000882 (2010).
58. Kim, P. S. & Ahmed, R. Features of responding T cells in cancer and chronic infection. Curr. Opin. Immunol. 22, 223-230 (2010).
59. Speiser, D. E. et al. T cell differentiation in chronic infection and cancer: functional adaptation or exhaustion? Nat. Rev. Immunol. 14, 768-774 (2014).
60. Wakim, L. M. et al. The molecular signature of tissue resident memory CD8 T cells isolated from the brain. J. Immunol. 189, 3462-3471 (2012).
61. Raptopoulou, A. P. et al. The programmed death 1/programmed death ligand 1 inhibitory pathway is upregulated in rheumatoid synovium and regulates peripheral T cell responses in human and murine arthritis. Arthritis Rheum. 62, 1870-1880 (2010).
62. + regulatory T cells. J. Immunol. 181, 7350-7355 (2008).
63. regs involves IL6mediated signaling. Sci. Transl. Med. 5, 170ra115 (2013).
64. /low regulatory T cells in patients with active systemic lupus erythematosus. Arthritis Rheum. 58, 2120-2130 (2008).
65. - T cells by regulatory T cells in patients with rheumatoid arthritis. J. Clin. Immunol. 6, 1112-1119 (2011).
66. Wehrens, E. J. et al. Functional human regulatory T cells fail to control autoimmune inflammation due to PKB/cakt hyperactivation in effector cells. Blood 118, 3538-3548 (2011).
67. Haufe, S. et al. Impaired suppression of synovial fluid CD4+CD25-T cells from patients with juvenile idiopathic arthritis by CD4+CD25+ Treg cells. Arthritis Rheum. 63, 3153-3162 (2011).
68. Petrelli, A. et al. Self-sustained resistance to suppression of CD8+ Teff cells at the site of autoimmune inflammation can be reversed by tumor necrosis factor and interferon-y blockade. Arthritis Rheumatol. 68, 229-236 (2016).
69. Wehrens, E. J. et al. Anti-tumor necrosis factor a targets protein kinase B/cAkt-induced resistance of effector cells to suppression in juvenile idiopathic arthritis. Arthritis Rheum. 65, 3279-3284 (2013).
70. + regulatory T cells in the maintenance of T cell homeostasis. J. Exp. Med. 200, 1123-1134 (2004).
71. Moore, J. S. & Calkins, C. E. In vitro regulation of the pathogenic autoantibody response of New Zealand black mice. I. Loss with age of suppressive activity in T cell populations. J. Immunol. 134, 3838-3844 (1985).
72. Notley, C. A., McCann, F. E., Inglis, J. J. & Williams, R. O. ANTICD3 therapy expands the numbers of CD4+ and CD8+ Treg cells and induces sustained amelioration of collagen-induced arthritis. Arthritis Rheum. 62, 171-178 (2010).
73. + regulatory T cells under inflammatory or non-inflammatory conditions. Seminars Immunol. 23, 424-430 (2011).
74. + Tcell subset as a memory-like Treg family. Cell. Mol. Immunol. 11, 326-331 (2014).
75. + regulatory thymocytes. Blood 102, 4107-4114 (2003).
76. +CD28-regulatory T cell suppressor function in rheumatoid arthritis is restored by tumour necrosis factor inhibitor therapy. Clin. Exp. Immunol. 174, 18-26 (2013).
77. Ellis, S. D. et al. Induced CD8+FoxP3+ Treg cells in rheumatoid arthritis are modulated by p38 phosphorylation and monocytes expressing membrane tumor necrosis factor a and CD86. Arthritis Rheumatol. 66, 2694-2705 (2014).
78. Guilliams, M. et al. Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat. Rev. Immunol. 14, 571-578 (2014).
79. Boltjes, A. & van Wijk, F Human dendritic cell functional specialization in steady-state and inflammation. Front. Immunol. 5, 131 (2014).
80. Ziegler-Heitbrock, L. The CD14+ CD16+ blood monocytes: their role in infection and inflammation. J. Leukoc. Biol. 81, 584-592 (2007).
81. Thomas, R. & Quinn, C. Functional differentiation of dendritic cells in rheumatoid arthritis: role of CD86 in the synovium. J. Immunol. 156, 3074-3086 (1996).
82. Moret, F M. et al. Intra-articular CD1cexpressing myeloid dendritic cells from rheumatoid arthritis patients express a unique set of T cell-attracting chemokines and spontaneously induce Th1, Th17 and Th2 cell activity. Arthritis Res. Ther. 15, R155 (2013).
83. Jongbloed, S. L. et al. Enumeration and phenotypical analysis of distinct dendritic cell subsets in psoriatic arthritis and rheumatoid arthritis. Arthritis Res. Ther 8, R15 (2006).
84. Kawanaka, N. et al. CD14+, CD16+ blood monocytes and joint inflammation in rheumatoid arthritis. Arthritis Rheum. 46, 2578-2586 (2002).
85. Yoon, B. R. et al. Functional phenotype of synovial monocytes modulating inflammatory Tcell responses in rheumatoid arthritis (RA). PLoS ONE 9, e109775 (2014).
86. +dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J. Exp. Med. 207, 1247-1260 (2010).
87. Kassianos, A. J., Jongbloed, S. L., Hart, D. N. & Radford, K. J. Isolation of human blood DC subtypes. Methods Mol. Biol. 595, 45-54 (2010).
88. Kurts, C. et al. Constitutive class Irestricted exogenous presentation of self antigens in vivo. J. Exp. Med. 184, 923-930 (1996).
89. + myeloid dendritic cells. Blood 119, 2284-2292 (2012).
90. + nonlymphoid dendritic cells. Immunity 37, 60-73 (2012).
91. Smolewska, E. et al. Distribution and clinical significance of blood dendritic cells in children with juvenile idiopathic arthritis. Ann. Rheum. Dis. 67, 762-768 (2008).
92. Prakken, B., Albani, S. & Martini, A. Juvenile idiopathic arthritis. Lancet 377, 2138-2149 (2011).
93. Sakkas, L. I., Bogdanos, D. P., Katsiari, C. & Platsoucas, C. D. Anti-citrullinated peptides as autoantigens in rheumatoid arthritis-relevance to treatment. Autoimmun. Rev. 13, 1114-1120 (2014).
94. Bulatovic Calasan, M. et al. Methotrexate treatment affects effector but not regulatory T cells in juvenile idiopathic arthritis. Rheumatology 54, 1724-1734 (2015).
95. Aravena, O. et al. Anti-TNF therapy in patients with rheumatoid arthritis decreases Th1 and Th17 cell populations and expands IFN-γ-producing NK cell and regulatory T cell subsets. Immunobiology 216, 1256-1263 (2011).
96. Scarsi, M. et al. Reduction of peripheral blood T cells producing IFN-γ and IL17 after therapy with abatacept for rheumatoid arthritis. Clin. Exp. Rheumatol. 32, 204-210 (2014).
97. Melet, J. et al. Rituximab-induced T cell depletion in patients with rheumatoid arthritis: association with clinical response. Arthritis Rheum. 65, 2783-2790 (2013).
98. Nejentsev, S. et al. Localization of type 1 diabetes susceptibility to the MHC class I genes HLAB and HLAA. Nature 450, 887-892 (2007).
99. Sawcer, S. et al. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 476, 214-219 (2011).
100. Coppieters, K. T. et al. Demonstration of islet-autoreactive CD8 T cells in insulitic lesions from recent onset and long-term type 1 diabetes patients. J. Exp. Med. 209, 51-60 (2012).
101. Unger, W. W. et al. Islet-specific CTL cloned from a type 1 diabetes patient cause beta-cell destruction after engraftment into HLAA2 transgenic NOD/scid/IL2RG null mice. PLoS ONE 7, e49213 (2012).
102. + T cells persist as clonal expansions in the cerebrospinal fluid and blood. Proc. Natl Acad. Sci. USA 101, 2428-2433 (2004).
103. + T cells in multiple sclerosis revealed by novel flow cytometric assay. Blood 103, 4222-4231 (2004).
104. + T cell transcription signature predicts prognosis in autoimmune disease. Nat. Med. 16, 586-591 (2010).
105. McKinney, E. F., Lee, J. C., Jayne, D. R., Lyons, P. A. & Smith, K. G. Tcell exhaustion, costimulation and clinical outcome in autoimmunity and infection. Nature 523, 612-616 (2015).