Single-cell analysis of glandular T cell receptors in Sjögren’s syndrome

Journal of Clinical Investigation

Volumn 1, Issue 8, 2016, Pages

  Joachims, Michelle L ^a   Leehan, Kerry M ^a,b   Lawrence, Christina ^a   Pelikan, Richard C ^a   Moore, Jacen S ^a   Pan, Zijian ^a   Rasmussen, Astrid ^a   Radfar, Lida ^c   Lewis, David M ^c   Grundahl, Kiely M ^a   Kelly, Jennifer A ^a   Wiley, Graham B ^a   Shugay, Mikhail ^d,e,f   Chudakov, Dmitriy M ^d,e,f   Lessard, Christopher J ^a,b   Stone, Donald U ^b   Scofield, R Hal ^a,b,c   Montgomery, Courtney G ^a   Sivils, Kathy L ^a,b   Thompson, Linda F ^a   Farris, A Darise ^a,b   more..

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^d SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^e PIROGOV RUSSIAN NATIONAL RESEARCH MEDICAL UNIVERSITY   (Russian Federation)

^f MASARYK UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85030484213     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/jci.insight.85609     Document Type: Article

References (70)

1. Jonsson R, Vogelsang P, Volchenkov R, Espinosa A, Wahren-Herlenius M, Appel S. The complexity of Sjogren’s syndrome: novel aspects on pathogenesis. Immunol Lett. 2011;141(1):1–9.
2. Mavragani CP, Moutsopoulos HM. Sjogren’s syndrome. Annu Rev Pathol. 2014;9:273–285.
3. Vitali C, et al. Classification criteria for Sjogren’s syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis. 2002;61(6):554–558.
4. Daniels TE. Labial salivary gland biopsy in Sjogren’s syndrome. Assessment as a diagnostic criterion in 362 suspected cases. Arthritis Rheum. 1984;27(2):147–156.
5. Fox RI, Carstens SA, Fong S, Robinson CA, Howell F, Vaughan JH. Use of monoclonal antibodies to analyze peripheral blood and salivary gland lymphocyte subsets in Sjogren’s syndrome. Arthritis Rheum. 1982;25(4):419–426.
6. Adamson TC 3rd, Fox RI, Frisman DM, Howell FV. Immunohistologic analysis of lymphoid infiltrates in primary Sjogren’s syndrome using monoclonal antibodies. J Immunol. 1983;130(1):203–208.
7. Talal N, Sylvester RA, Daniels TE, Greenspan JS, Williams RC Jr. T and B lymphocytes in peripheral blood and tissue lesions in Sjogren’s syndrome. J Clin Invest. 1974;53(1):180–189.
8. Moutsopoulos HM, Hooks JJ, Chan CC, Dalavanga YA, Skopouli FN, Detrick B. HLA-DR expression by labial minor salivary gland tissues in Sjogren’s syndrome. Ann Rheum Dis. 1986;45(8):677–683.
9. Zumla A, Mathur M, Stewart J, Wilkinson L, Isenberg D. T cell receptor expression in Sjogren’s syndrome. Ann Rheum Dis. 1991;50(10):691–693.
10. Ohyama Y, et al. T-cell receptor Vα and Vβ gene use by infiltrating T cells in labial glands of patients with Sjogren’s syndrome. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1995;79(6):730–737.
11. Matthews JB, et al. Primed and naive helper T cells in labial glands from patients with Sjogren’s syndrome. Virchows Arch A Pathol Anat Histopathol. 1991;419(3):191–197.
12. Christodoulou MI, Kapsogeorgou EK, Moutsopoulos HM. Characteristics of the minor salivary gland infiltrates in Sjogren’s syndrome. J Autoimmun. 2010;34(4):400–407.
13. Petrie HT, Livak F, Schatz DG, Strasser A, Crispe IN, Shortman K. Multiple rearrangements in T cell receptor alpha chain genes maximize the production of useful thymocytes. J Exp Med. 1993;178(2):615–622.
14. Padovan E, Casorati G, Dellabona P, Meyer S, Brockhaus M, Lanzavecchia A. Expression of two T cell receptor alpha chains: dual receptor T cells. Science. 1993;262(5132):422–424.
15. Smith MD, et al. Selective expression of V beta families by T cells in the blood and salivary gland infiltrate of patients with primary Sjogren’s syndrome. J Rheumatol. 1994;21(10):1832–1837.
16. Kay RA, et al. An abnormal T cell repertoire in hypergammaglobulinaemic primary Sjogren’s syndrome. Clin Exp Immunol. 1991;85(2):262–264.
17. Matsumoto I, et al. Common T cell receptor clonotype in lacrimal glands and labial salivary glands from patients with Sjogren’s syndrome. J Clin Invest. 1996;97(8):1969–1977.
18. Sasaki M, et al. Accumulation of common T cell clonotypes in the salivary glands of patients with human T lymphotropic virus type I-associated and idiopathic Sjogren’s syndrome. J Immunol. 2000;164(5):2823–2831.
19. Sumida T, et al. T cell receptor repertoire of infiltrating T cells in lips of Sjogren’s syndrome patients. J Clin Invest. 1992;89(2):681–685.
20. Ajjan RA, et al. Analysis of the T-cell receptor Valpha repertoire and cytokine gene expression in Sjogren’s syndrome. Br J Rheumatol. 1998;37(2):179–185.
21. Sumida T, et al. TCR in Fas-sensitive T cells from labial salivary glands of patients with Sjogren’s syndrome. J Immunol. 1997;158(2):1020–1025.
22. Matsumoto I, et al. Single cell analysis of T cells infiltrating labial salivary glands from patients with Sjogren’s syndrome. Int J Mol Med. 1999;4(5):519–527.
23. Sumida T, Kita Y, Yonaha F, Maeda T, Iwamoto I, Yoshida S. T cell receptor Vα repertoire of infiltrating T cells in labial salivary glands from patients with Sjogren’s syndrome. J Rheumatol. 1994;21(9):1655–1661.
24. Krischer JP, et al. Screening strategies for the identification of multiple antibody-positive relatives of individuals with type 1 diabetes. J Clin Endocrinol Metab. 2003;88(1):103–108.
25. Weiner ES, et al. Prognostic significance of anticentromere antibodies and anti-topoisomerase I antibodies in Raynaud’s disease. A prospective study. Arthritis Rheum. 1991;34(1):68–77.
26. van Venrooij WJ, van Beers JJ, Pruijn GJ. Anti-CCP antibodies: the past, the present and the future. Nat Rev Rheumatol. 2011;7(7):391–398.
27. Michels AW, von Herrath M. 2011 Update: antigen-specific therapy in type 1 diabetes. Curr Opin Endocrinol Diabetes Obes. 2011;18(4):235–240.
28. Steinman L. Inverse vaccination, the opposite of Jenner’s concept, for therapy of autoimmunity. J Intern Med. 2010;267(5):441–451.
29. Walczak A, Siger M, Ciach A, Szczepanik M, Selmaj K. Transdermal application of myelin peptides in multiple sclerosis treatment. JAMA Neurol. 2013;70(9):1105–1109.
30. Turner SJ, Doherty PC, McCluskey J, Rossjohn J. Structural determinants of T-cell receptor bias in immunity. Nat Rev. 2006;6(12):883–894.
31. Lessard CJ, et al. Variants at multiple loci implicated in both innate and adaptive immune responses are associated with Sjogren’s syndrome. Nat Genet. 2013;45(11):1284–1292.
32. Zal T, Weiss S, Mellor A, Stockinger B. Expression of a second receptor rescues self-specific T cells from thymic deletion and allows activation of autoreactive effector function. Proc Natl Acad Sci U S A. 1996;93(17):9102–9107.
33. Sarukhan A, Garcia C, Lanoue A, von Boehmer H. Allelic inclusion of T cell receptor alpha genes poses an autoimmune hazard due to low-level expression of autospecific receptors. Immunity. 1998;8(5):563–570.
34. Ni PP, Solomon B, Hsieh CS, Allen PM, Morris GP. The ability to rearrange dual TCRs enhances positive selection, leading to increased Allo- and Autoreactive T cell repertoires. J Immunol. 2014;193(4):1778–1786.
35. Morris GP, Uy GL, Donermeyer D, Dipersio JF, Allen PM. Dual receptor T cells mediate pathologic alloreactivity in patients with acute graft-versus-host disease. Sci Transl Med. 2013;5(188):188ra74.
36. Robins HS, et al. Comprehensive assessment of T-cell receptor beta-chain diversity in alphabeta T cells. Blood. 2009;114(19):4099–4107.
37. Venturi V, Kedzierska K, Turner SJ, Doherty PC, Davenport MP. Methods for comparing the diversity of samples of the T cell receptor repertoire. J Immunol Methods. 2007;321(1-2):182–195.
38. Spreafico R, et al. A circulating reservoir of pathogenic-like CD4+ T cells shares a genetic phenotypic signature with the inflamed synovial micro-environment. Ann Rheum Dis. 2016;75(2):459–465.
39. Venturi V, et al. Sharing of T cell receptors in antigen-specific responses is driven by convergent recombination. Proc Natl Acad Sci U S A. 2006;103(49):18691–18696.
40. Britanova OV, et al. Age-related decrease in TCR repertoire diversity measured with deep and normalized sequence profiling. J Immunol. 2014;192(6):2689–2698.
41. Egorov ES, et al. Quantitative profiling of immune repertoires for minor lymphocyte counts using unique molecular identifiers. J Immunol. 2015;194(12):6155–6163.
42. Shugay M, et al. VDJtools: unifying post-analysis of T cell receptor repertoires. PLoS Comput Biol. 2015;11(11):e1004503.
43. Leehan KM, et al. Precisely quantified fibrosis in labial salivary glands predicts Sjögren’s syndrome classification in a multiple regression model. Arthritis Rheumatol. 2014;66:S1280.
44. Ji Q, Perchellet A, Goverman JM. Viral infection triggers central nervous system autoimmunity via activation of CD8+ T cells expressing dual TCRs. Nat Immunol. 2010;11(7):628–634.
45. He X, et al. Dual receptor T cells extend the immune repertoire for foreign antigens. Nat Immunol. 2002;3(2):127–134.
46. Sumida T, Matsumoto I, Maeda T, Nishioka K. T-cell receptor in Sjogren’s syndrome. Br J Rheumatol. 1997;36(6):622–629.
47. Ishigaki K, et al. Quantitative and qualitative characterization of expanded CD4+ T cell clones in rheumatoid arthritis patients. Sci Rep. 2015;5:12937.
48. Jonsson MV, Skarstein K, Jonsson R, Brun JG. Serological implications of germinal center-like structures in primary Sjogren’s syndrome. J Rheumatol. 2007;34(10):2044–2049.
49. Maier-Moore JS, et al. Antibody-secreting cell specificity in labial salivary glands reflects the clinical presentation and serology in patients with Sjogren’s syndrome. Arthritis Rheumatol. 2014;66(12):3445–3456.
50. Tengner P, Halse AK, Haga HJ, Jonsson R, Wahren-Herlenius M. Detection of anti-Ro/SSA and anti-La/SSB autoantibody-producing cells in salivary glands from patients with Sjogren’s syndrome. Arthritis Rheum. 1998;41(12):2238–2248.
51. Theander E, et al. Lymphoid organisation in labial salivary gland biopsies is a possible predictor for the development of malignant lymphoma in primary Sjogren’s syndrome. Ann Rheum Dis. 2011;70(8):1363–1368.
52. Vissink A, Bootsma H, Spijkervet FK, Hu S, Wong DT, Kallenberg CG. Current and future challenges in primary Sjogren’s syndrome. Curr Pharm Biotechnol. 2012;13(10):2026–2045.
53. Daniels TE, et al. Associations between salivary gland histopathologic diagnoses and phenotypic features of Sjogren’s syndrome among 1,726 registry participants. Arthritis Rheum. 2011;63(7):2021–2030.
54. Malladi AS, et al. Primary Sjogren’s syndrome as a systemic disease: a study of participants enrolled in an international Sjogren’s syndrome registry. Arthritis Care Res (Hoboken). 2012;64(6):911–918.
55. Jensen SB, Vissink A. Salivary gland dysfunction and xerostomia in Sjogren’s syndrome. Oral Maxillofac Surg Clin North Am. 2014;26(1):35–53.
56. Bookman AA, et al. Whole stimulated salivary flow: correlation with the pathology of inflammation and damage in minor salivary gland biopsy specimens from patients with primary Sjogren’s syndrome but not patients with sicca. Arthritis Rheum. 2011;63(7):2014–2020.
57. Blank U, Boitel B, Mege D, Ermonval M, Acuto O. Analysis of tetanus toxin peptide/DR recognition by human T cell receptors reconstituted into a murine T cell hybridoma. Eur J Immunol. 1993;23(12):3057–3065.
58. Delong T, et al. Pathogenic CD4 T cells in type 1 diabetes recognize epitopes formed by peptide fusion. Science. 2016;351(6274):711–714.
59. Shiboski SC, et al. American College of Rheumatology classification criteria for Sjogren’s syndrome: a data-driven, expert consensus approach in the Sjogren’s International Collaborative Clinical Alliance cohort. Arthritis Care Res (Hoboken). 2012;64(4):475–487.
60. Rasmussen A, et al. Comparison of the American-European Consensus Group Sjogren’s syndrome classification criteria to newly proposed American College of Rheumatology criteria in a large, carefully characterised sicca cohort. Ann Rheum Dis. 2014;73(1):31–38.
61. Bunce M, et al. Phototyping: comprehensive DNA typing for HLA-A, B, C, DRB1, DRB3, DRB4, DRB5 & DQB1 by PCR with 144 primer mixes utilizing sequence-specific primers (PCR-SSP). Tissue Antigens. 1995;46(5):355–367.
62. Zheng X, et al. HIBAG-HLA genotype imputation with attribute bagging. Pharmacogenomics J. 2014;14(2):192–200.
63. Wang GC, Dash P, McCullers JA, Doherty PC, Thomas PG. T cell receptor αβ diversity inversely correlates with pathogen-specific antibody levels in human cytomegalovirus infection. Sci Transl Med. 2012;4(128):128ra42.
64. Lefranc MP, et al. IMGT, the international ImMunoGeneTics information system. Nucleic Acids Res. 2009;37(Database issue):D1006–D1012.
65. Brochet X, Lefranc MP, Giudicelli V. IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucleic Acids Res. 2008;36(Web Server issue):W503–W508.
66. Caporaso JG, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–336.
67. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26(19):2460–2461.
68. Camacho C, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10:421.
69. Stothard P. The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques. 2000;28(6):1102.
70. Kivioja T, et al. Counting absolute numbers of molecules using unique molecular identifiers. Nat Methods. 2012;9(1):72–74.