Next-Generation Sequencing Reveals Restriction and Clonotypic Expansion of Treg Cells in Juvenile Idiopathic Arthritis

Arthritis and Rheumatology

Volumn 68, Issue 7, 2016, Pages 1758-1768

  Henderson, Lauren A ^a   Volpi, Stefano ^a   Frugoni, Francesco ^a   Janssen, Erin ^a   Kim, Susan ^a   Sundel, Robert P ^a   Dedeoglu, Fatma ^a   Lo, Mindy S ^a   Hazen, Melissa M ^a   Beth Son, Mary ^a   Mathieu, Ronald ^a   Zurakowski, David ^a   Yu, Neng ^b   Lebedeva, Tatiana ^b   Fuhlbrigge, Robert C ^c   Walter, Jolan E ^a   Nee Lee, Yu ^a   Nigrovic, Peter A ^c   Notarangelo, Luigi D ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b AMERICAN RED CROSS BLOOD SERVICES   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

T LYMPHOCYTE RECEPTOR BETA CHAIN;

ADOLESCENT; AMPLICON; ARTICLE; AUTOIMMUNITY; BLOOD; CD4+ CD25+ T LYMPHOCYTE; CELL CLONING; CELL EXPANSION; CHILD; CLINICAL ARTICLE; CLONAL VARIATION; COMPARATIVE STUDY; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; FEMALE; GENE; HLA TYPING; HUMAN; HUMAN CELL; HYDROPHOBICITY; IMMUNE DEFICIENCY; JUVENILE RHEUMATOID ARTHRITIS; LYME DISEASE; LYMPHOCYTE FUNCTION; LYMPHOCYTE SUBPOPULATION; MALE; MULTIPLEX POLYMERASE CHAIN REACTION; NEXT GENERATION SEQUENCING; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SYNOVIAL FLUID;

EID: 84976568322     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.39606     Document Type: Article

References (50)

1. Prakken B, Albani S, Martini A. Juvenile idiopathic arthritis. Lancet 2011;377:2138–49.
2. Macaubas C, Nguyen K, Milojevic D, Park JL, Mellins ED. Oligoarticular and polyarticular JIA: epidemiology and pathogenesis. Nat Rev Rheumatol 2009;5:616–26.
3. Hinks A, Cobb J, Marion MC, Prahalad S, Sudman M, Bowes J, et al. Dense genotyping of immune-related disease regions identifies 14 new susceptibility loci for juvenile idiopathic arthritis. Nat Genet 2013;45:664–9.
4. Prahalad S, Thompson SD, Conneely KN, Jiang Y, Leong T, Prozonic J, et al. Hierarchy of risk of childhood-onset rheumatoid arthritis conferred by HLA–DRB1 alleles encoding the shared epitope. Arthritis Rheum 2012;64:925–30.
5. Kruithof E, Van den Bossche V, De Rycke L, Vandooren B, Joos R, Canete JD, et al. Distinct synovial immunopathologic characteristics of juvenile-onset spondylarthritis and other forms of juvenile idiopathic arthritis. Arthritis Rheum 2006;54:2594–604.
6. Ruperto N, Lovell DJ, Quartier P, Paz E, Rubio-Perez N, Silva CA, et al, for the Paediatric Rheumatology International Trials Organization and the Pediatric Rheumatology Collaborative Study Group. Long-term safety and efficacy of abatacept in children with juvenile idiopathic arthritis. Arthritis Rheum 2010;62:1792–802.
7. Amariglio N, Klein A, Dagan L, Lev A, Padeh S, Rechavi G, et al. T-cell compartment in synovial fluid of pediatric patients with JIA correlates with disease phenotype. J Clin Immunol 2011;31:1021–8.
8. Chini L, Bardare M, Cancrini C, Angelini F, Mancia L, Cortis E, et al. Evidence of clonotypic pattern of T-cell repertoire in synovial fluid of children with juvenile rheumatoid arthritis at the onset of the disease. Scand J Immunol 2002;56:512–7.
9. Wedderburn LR, Patel A, Varsani H, Woo P. Divergence in the degree of clonal expansions in inflammatory T cell subpopulations mirrors HLA-associated risk alleles in genetically and clinically distinct subtypes of childhood arthritis. Int Immunol 2001;13:1541–50.
10. Morgan ME, Flierman R, van Duivenvoorde LM, Witteveen HJ, van Ewijk W, van Laar JM, et al. Effective treatment of collagen-induced arthritis by adoptive transfer of CD25+ regulatory T cells. Arthritis Rheum 2005;52:2212–21.
11. bright regulatory T cells actively regulate inflammation in the joints of patients with the remitting form of juvenile idiopathic arthritis. J Immunol 2004;172:6435–43.
12. Nistala K, Moncrieffe H, Newton KR, Varsani H, Hunter P, Wedderburn LR. Interleukin-17–producing T cells are enriched in the joints of children with arthritis, but have a reciprocal relationship to regulatory T cell numbers. Arthritis Rheum 2008;58:875–87.
13. Haufe S, Haug M, Schepp C, Kuemmerle-Deschner J, Hansmann S, Rieber N, et al. Impaired suppression of synovial fluid CD4+CD25– T cells from patients with juvenile idiopathic arthritis by CD4+CD25+ Treg cells. Arthritis Rheum 2011;63:3153–62.
14. Wehrens EJ, Mijnheer G, Duurland CL, Klein M, Meerding J, van Loosdregt J, et al. Functional human regulatory T cells fail to control autoimmune inflammation due to PKB/c-akt hyperactivation in effector cells. Blood 2011;118:3538–48.
15. Wehrens EJ, Vastert SJ, Mijnheer G, Meerding J, Klein M, Wulffraat NM, et al. Anti–tumor necrosis factor α targets protein kinase B/c-Akt–induced resistance of effector cells to suppression in juvenile idiopathic arthritis. Arthritis Rheum 2013;65:3279–84.
16. Nie H, Zheng Y, Li R, Guo TB, He D, Fang L, et al. Phosphorylation of FOXP3 controls regulatory T cell function and is inhibited by TNF-α in rheumatoid arthritis. Nat Med 2013;19:322–8.
17. Ferreira C, Singh Y, Furmanski AL, Wong FS, Garden OA, Dyson J. Non-obese diabetic mice select a low-diversity repertoire of natural regulatory T cells. Proc Natl Acad Sci U S A 2009;106:8320–5.
18. Tanaka S, Maeda S, Hashimoto M, Fujimori C, Ito Y, Teradaira S, et al. Graded attenuation of TCR signaling elicits distinct autoimmune diseases by altering thymic T cell selection and regulatory T cell function. J Immunol 2010;185:2295–305.
19. Le Campion A, Gagnerault MC, Auffray C, Becourt C, Poitrasson-Riviere M, Lallemand E, et al. Lymphopenia-induced spontaneous T-cell proliferation as a cofactor for autoimmune disease development. Blood 2009;114:1784–93.
20. Oh S, Aitken M, Simons DM, Basehoar A, Garcia V, Kropf E, et al. Requirement for diverse TCR specificities determines regulatory T cell activity in a mouse model of autoimmune arthritis. J Immunol 2012;188:4171–80.
21. Petty RE, Southwood TR, Manners P, Baum J, Glass DN, Goldenberg J, et al. International League of Associations for Rheumatology classification of juvenile idiopathic arthritis: second revision, Edmonton, 2001. J Rheumatol 2004;31:390–2.
22. Robins HS, Campregher PV, Srivastava SK, Wacher A, Turtle CJ, Kahsai O, et al. Comprehensive assessment of T-cell receptor β-chain diversity in αβ T cells. Blood 2009;114:4099–107.
23. ® tools for the nucleotide analysis of immunoglobulin (IG) and T cell receptor (TR) V-(D)-J repertoires, polymorphisms, and IG mutations: IMGT/V-QUEST and IMGT/HighV-QUEST for NGS. Methods Mol Biol 2012;882:569–604.
24. Carlson CS, Emerson RO, Sherwood AM, Desmarais C, Chung MW, Parsons JM, et al. Using synthetic templates to design an unbiased multiplex PCR assay. Nat Commun 2013;4:2680.
25. Rogosch T, Kerzel S, Hoi KH, Zhang Z, Maier RF, Ippolito GC, et al. Immunoglobulin analysis tool: a novel tool for the analysis of human and mouse heavy and light chain transcripts. Front Immunol 2012;3:176.
26. Stewart JJ, Lee CY, Ibrahim S, Watts P, Shlomchik M, Weigert M, et al. A Shannon entropy analysis of immunoglobulin and T cell receptor. Mol Immunol 1997;34:1067–82.
27. Pielou EC. The measurement of diversity in different types of biological collections. J Theor Biol 1966;13:131–44.
28. Hammer O, Harper DA, Ryan PD. PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 2001;4:1–9.
29. Wang C, Sanders CM, Yang Q, Schroeder HW Jr, Wang E, Babrzadeh F, et al. High throughput sequencing reveals a complex pattern of dynamic interrelationships among human T cell subsets. Proc Natl Acad Sci U S A 2010;107:1518–23.
30. – T cells. J Immunol 2007;179:3412–6.
31. − counterparts. J Immunol 2004;172:6123–8.
32. Hollenbach JA, Thompson SD, Bugawan TL, Ryan M, Sudman M, Marion M, et al. Juvenile idiopathic arthritis and HLA class I and class II interactions and age-at-onset effects. Arthritis Rheum 2010;62:1781–91.
33. Thomson W, Barrett JH, Donn R, Pepper L, Kennedy LJ, Ollier WE, et al. Juvenile idiopathic arthritis classified by the ILAR criteria: HLA associations in UK patients. Rheumatology (Oxford) 2002;41:1183–9.
34. Begovich AB, Bugawan TL, Nepom BS, Klitz W, Nepom GT, Erlich HA. A specific HLA-DPβ allele is associated with pauciarticular juvenile rheumatoid arthritis but not adult rheumatoid arthritis. Proc Natl Acad Sci U S A 1989;86:9489–93.
35. Venturi V, Price DA, Douek DC, Davenport MP. The molecular basis for public T-cell responses? Nat Rev Immunol 2008;8:231–8.
36. Schroeder HW Jr, Ippolito GC, Shiokawa S. Regulation of the antibody repertoire through control of HCDR3 diversity. Vaccine 1998;16:1383–90.
37. Souto-Carneiro MM, Longo NS, Russ DE, Sun HW, Lipsky PE. Characterization of the human Ig heavy chain antigen binding complementarity determining region 3 using a newly developed software algorithm, JOINSOLVER. J Immunol 2004;172:6790–802.
38. Verhagen J, Genolet R, Britton GJ, Stevenson BJ, Sabatos-Peyton CA, Dyson J, et al. CTLA-4 controls the thymic development of both conventional and regulatory T cells through modulation of the TCR repertoire. Proc Natl Acad Sci U S A 2013;110:E221–30.
39. Godebu E, Summers-Torres D, Lin MM, Baaten BJ, Bradley LM. Polyclonal adaptive regulatory CD4 cells that can reverse type I diabetes become oligoclonal long-term protective memory cells. J Immunol 2008;181:1798–805.
40. Codina-Busqueta E, Scholz E, Munoz-Torres PM, Roura-Mir C, Costa M, Xufre C, et al. TCR bias of in vivo expanded T cells in pancreatic islets and spleen at the onset in human type 1 diabetes. J Immunol 2011;186:3787–97.
41. 2-glycoprotein I in patients with antiphospholipid syndrome. Blood 2002;99:2499–504.
42. Duhen T, Duhen R, Lanzavecchia A, Sallusto F, Campbell DJ. Functionally distinct subsets of human FOXP3+ Treg cells that phenotypically mirror effector Th cells. Blood 2012;119:4430–40.
43. Koch MA, Tucker-Heard G, Perdue NR, Killebrew JR, Urdahl KB, Campbell DJ. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat Immunol 2009;10:595–602.
44. Zhou X, Bailey-Bucktrout SL, Jeker LT, Penaranda C, Martinez-Llordella M, Ashby M, et al. Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo. Nat Immunol 2009;10:1000–7.
45. Komatsu N, Okamoto K, Sawa S, Nakashima T, Oh-hora M, Kodama T, et al. Pathogenic conversion of Foxp3+ T cells into TH17 cells in autoimmune arthritis. Nat Med 2014;20:62–8.
46. Bailey-Bucktrout SL, Martinez-Llordella M, Zhou X, Anthony B, Rosenthal W, Luche H, et al. Self-antigen-driven activation induces instability of regulatory T cells during an inflammatory autoimmune response. Immunity 2013;39:949–62.
47. Bending D, Pesenacker AM, Ursu S, Wu Q, Lom H, Thirugnanabalan B, et al. Hypomethylation at the regulatory T cell-specific demethylated region in CD25hi T cells is decoupled from FOXP3 expression at the inflamed site in childhood arthritis. J Immunol 2014;193:2699–708.
48. high T cells in the synovial fluid of patients with antibiotic-refractory Lyme arthritis. Arthritis Rheum 2013;65:1643–53.
49. DeKosky BJ, Ippolito GC, Deschner RP, Lavinder JJ, Wine Y, Rawlings BM, et al. High-throughput sequencing of the paired human immunoglobulin heavy and light chain repertoire. Nat Biotechnol 2013;31:166–9.
50. Burzyn D, Kuswanto W, Kolodin D, Shadrach JL, Cerletti M, Jang Y, et al. A special population of regulatory T cells potentiates muscle repair. Cell 2013;155:1282–95.