Interaction among activated lymphocytes and mesenchymal cells through podoplanin is critical for a high IL-17 secretion

Arthritis Research and Therapy

Volumn 18, Issue 1, 2016, Pages

  Noack, Mélissa ^a   Ndongo Thiam, Ndiémé ^a   Miossec, Pierre ^a  

^a University of Lyon   (France)

Author keywords

Cell interactions; IL 17; Podoplanin; Rheumatoid arthritis; Synoviocytes

Indexed keywords

CD3 ANTIGEN; CD4 ANTIGEN; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6; PHYTOHEMAGGLUTININ; PODOPLANIN; IL17A PROTEIN, HUMAN; MEMBRANE PROTEIN; PDPN PROTEIN, HUMAN;

ARTICLE; CELL ACTIVATION; CELL CONTACT; CELL INTERACTION; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LYMPHOCYTE; LYMPHOCYTE DIFFERENTIATION; MESENCHYME CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; RHEUMATOID ARTHRITIS; STAINING; SYNOVIOCYTE; T LYMPHOCYTE ACTIVATION; TH17 CELL; CELL DIFFERENTIATION; GENE SILENCING; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MONONUCLEAR CELL; REAL TIME POLYMERASE CHAIN REACTION; SECRETION (PROCESS);

ARTHRITIS, RHEUMATOID; CELL DIFFERENTIATION; COCULTURE TECHNIQUES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE KNOCKDOWN TECHNIQUES; HUMANS; INTERLEUKIN-17; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE ACTIVATION; MEMBRANE GLYCOPROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; SYNOVIOCYTES; TH17 CELLS;

EID: 84978033552     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/s13075-016-1046-6     Document Type: Article

References (50)

1. Miossec P, Kolls JK. Targeting IL-17 and TH17 cells in chronic inflammation. Nat Rev Drug Discov. 2012;11(10):763-76.
2. Miossec P, Korn T, Kuchroo VK. Interleukin-17 and type 17 helper T cells. N Engl J Med. 2009;361(9):888-98.
3. Page G, Sattler A, Kersten S, Thiel A, Radbruch A, Miossec P. Plasma cell-like morphology of Th1-cytokine-producing cells associated with the loss of CD3 expression. Am J Pathol. 2004;164(2):409-17.
4. Nestle FO, Kaplan DH, Barker J. Psoriasis. N Engl J Med. 2009;361(5):496-509.
5. Firestein GS. Evolving concepts of rheumatoid arthritis. Nature. 2003;423(6937):356-61.
6. Olin JT, Wechsler ME. Asthma: pathogenesis and novel drugs for treatment. BMJ. 2014;349:g5517.
7. Eljaafari A, Tartelin ML, Aissaoui H, Chevrel G, Osta B, Lavocat F, et al. Bone marrow-derived and synovium-derived mesenchymal cells promote Th17 cell expansion and activation through caspase 1 activation: contribution to the chronicity of rheumatoid arthritis. Arthritis Rheum. 2012;64(7):2147-57.
8. Del Rey MJ, Izquierdo E, Fare R, Usategui A, Miranda V, Criado G, et al. Podoplanin-mediated interaction of rheumatoid arthritis synovial fibroblasts with platelets modulates IL-8 expression. Arthritis Rheum. 2012;64(Ssuppl 10):1183.
9. Miyamoto Y, Uga H, Tanaka S, Kadowaki M, Ikeda M, Saegusa J, et al. Podoplanin is an inflammatory protein upregulated in Th17 cells in SKG arthritic joints. Mol Immunol. 2013;54(2):199-207.
10. Peters A, Pitcher LA, Sullivan JM, Mitsdoerffer M, Acton SE, Franz B, et al. Th17 cells induce ectopic lymphoid follicles in central nervous system tissue inflammation. Immunity. 2011;35(6):986-96.
11. Ekwall AK, Eisler T, Anderberg C, Jin C, Karlsson N, Brisslert M, et al. The tumour-associated glycoprotein podoplanin is expressed in fibroblast-like synoviocytes of the hyperplastic synovial lining layer in rheumatoid arthritis. Arthritis Res Ther. 2011;13(2):R40.
12. Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT. Bingham 3rd CO, et al. 2010 Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum. 2010;62(9):2569-81.
13. Bartok B, Firestein GS. Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunol Rev. 2010;233(1):233-55.
14. Annunziato F, Cosmi L, Santarlasci V, Maggi L, Liotta F, Mazzinghi B, et al. Phenotypic and functional features of human Th17 cells. J Exp Med. 2007;204(8):1849-61.
15. Cosmi L, De Palma R, Santarlasci V, Maggi L, Capone M, Frosali F, et al. Human interleukin 17-producing cells originate from a CD161 + CD4+ T cell precursor. J Exp Med. 2008;205(8):1903-16.
16. 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(9):942-9.
17. Wilson NJ, Boniface K, Chan JR, McKenzie BS, Blumenschein WM, Mattson JD, et al. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol. 2007;8(9):950-7.
18. Yang L, Anderson DE, Baecher-Allan C, Hastings WD, Bettelli E, Oukka M, et al. IL-21 and TGF-beta are required for differentiation of human T(H)17 cells. Nature. 2008;454(7202):350-2.
19. Harrington LE, Mangan PR, Weaver CT. Expanding the effector CD4 T-cell repertoire: the Th17 lineage. Curr Opin Immunol. 2006;18(3):349-56.
20. Tran CN, Lundy SK, White PT, Endres JL, Motyl CD, Gupta R, et al. Molecular interactions between T cells and fibroblast-like synoviocytes: role of membrane tumor necrosis factor-alpha on cytokine-activated T cells. Am J Pathol. 2007;171(5):1588-98.
21. Cho ML, Yoon CH, Hwang SY, Park MK, Min SY, Lee SH, et al. Effector function of type II collagen-stimulated T cells from rheumatoid arthritis patients: cross-talk between T cells and synovial fibroblasts. Arthritis Rheum. 2004;50(3):776-84.
22. Miranda-Carus ME, Balsa A, Benito-Miguel M, Perez de Ayala C, Martin-Mola E. IL-15 and the initiation of cell contact-dependent synovial fibroblast-T lymphocyte cross-talk in rheumatoid arthritis: effect of methotrexate. J Immunol. 2004;173(2):1463-76.
23. Sivalingam SP, Thumboo J, Vasoo S, Thio ST, Tse C, Fong KY. In vivo pro- and anti-inflammatory cytokines in normal and patients with rheumatoid arthritis. Ann Acad Med Singapore. 2007;36(2):96-9.
24. Hot A, Zrioual S, Lenief V, Miossec P. IL-17 and tumour necrosis factor alpha combination induces a HIF-1alpha-dependent invasive phenotype in synoviocytes. Ann Rheum Dis. 2012;71(8):1393-401.
25. Toh ML, Gonzales G, Koenders MI, Tournadre A, Boyle D, Lubberts E, et al. Role of interleukin 17 in arthritis chronicity through survival of synoviocytes via regulation of synoviolin expression. PLoS One. 2010;5(10):e13416.
26. Hot A, Miossec P. Effects of interleukin (IL)-17A and IL-17 F in human rheumatoid arthritis synoviocytes. Ann Rheum Dis. 2011;70(5):727-32.
27. Tak PP, Bresnihan B. The pathogenesis and prevention of joint damage in rheumatoid arthritis: advances from synovial biopsy and tissue analysis. Arthritis Rheum. 2000;43(12):2619-33.
28. Choy EH, Panayi GS. Cytokine pathways and joint inflammation in rheumatoid arthritis. N Engl J Med. 2001;344(12):907-16.
29. Mor A, Abramson SB, Pillinger MH. The fibroblast-like synovial cell in rheumatoid arthritis: a key player in inflammation and joint destruction. Clin Immunol. 2005;115(2):118-28.
30. Brennan FM, McInnes IB. Evidence that cytokines play a role in rheumatoid arthritis. J Clin Invest. 2008;118(11):3537-45.
31. Chabaud M, Durand JM, Buchs N, Fossiez F, Page G, Frappart L, et al. Human interleukin-17: A T cell-derived proinflammatory cytokine produced by the rheumatoid synovium. Arthritis Rheum. 1999;42(5):963-70.
32. Moran EM, Heydrich R, Ng CT, Saber TP, McCormick J, Sieper J, et al. IL-17A expression is localised to both mononuclear and polymorphonuclear synovial cell infiltrates. PLoS One. 2011;6(8):e24048.
33. Genovese MC, Greenwald M, Cho CS, Berman A, Jin L, Cameron GS, et al. A phase II randomized study of subcutaneous ixekizumab, an anti-interleukin-17 monoclonal antibody, in rheumatoid arthritis patients who were naive to biologic agents or had an inadequate response to tumor necrosis factor inhibitors. Arthritis Rheumatol. 2014;66(7):1693-704.
34. Hueber W, Patel DD, Dryja T, Wright AM, Koroleva I, Bruin G, et al. Effects of AIN457, a fully human antibody to interleukin-17A, on psoriasis, rheumatoid arthritis, and uveitis. Sci Transl Med. 2010;2(52):52ra72.
35. Leipe J, Schramm MA, Prots I, Schulze-Koops H, Skapenko A. Increased Th17 cell frequency and poor clinical outcome in rheumatoid arthritis are associated with a genetic variant in the IL4R gene, rs1805010. Arthritis Rheumatol. 2014;66(5):1165-75.
36. Wallis SK, Cooney LA, Endres JL, Lee MJ, Ryu J, Somers EC, et al. A polymorphism in the interleukin-4 receptor affects the ability of interleukin-4 to regulate Th17 cells: a possible immunoregulatory mechanism for genetic control of the severity of rheumatoid arthritis. Arthritis Res Ther. 2011;13(1):R15.
37. Hazlett J, Stamp LK, Merriman T, Highton J, Hessian PA. IL-23R rs11209026 polymorphism modulates IL-17A expression in patients with rheumatoid arthritis. Genes Immun. 2012;13(3):282-7.
38. Takakubo Y, Oki H, Naganuma Y, Saski K, Sasaki A, Tamaki Y, et al. Distribution of podoplanin in synovial tissues in rheumatoid arthritis patients using biologic or conventional disease-modifying anti-rheumatic drugs. Curr Rheumatol Rev. 2016;12(3): Epub ahead of print.
39. Jones GW, Bombardieri M, Greenhill CJ, McLeod L, Nerviani A, Rocher-Ros V, et al. Interleukin-27 inhibits ectopic lymphoid-like structure development in early inflammatory arthritis. J Exp Med. 2015;212(11):1793-802.
40. Del Rey MJ, Fare R, Izquierdo E, Usategui A, Rodriguez-Fernandez JL, Suarez-Fueyo A, et al. Clinicopathological correlations of podoplanin (gp38) expression in rheumatoid synovium and its potential contribution to fibroblast platelet crosstalk. PLoS One. 2014;9(6):e99607.
41. Acton SE, Astarita JL, Malhotra D, Lukacs-Kornek V, Franz B, Hess PR, et al. Podoplanin-rich stromal networks induce dendritic cell motility via activation of the C-type lectin receptor CLEC-2. Immunity. 2012;37(2):276-89.
42. Acton SE, Farrugia AJ, Astarita JL, Mourao-Sa D, Jenkins RP, Nye E, et al. Dendritic cells control fibroblastic reticular network tension and lymph node expansion. Nature. 2014;514(7523):498-502.
43. Lowe KL, Navarro-Nunez L, Benezech C, Nayar S, Kingston BL, Nieswandt B, et al. The expression of mouse CLEC-2 on leucocyte subsets varies according to their anatomical location and inflammatory state. Eur J Immunol. 2015;45(9):2484-93.
44. Astarita JL, Cremasco V, Fu J, Darnell MC, Peck JR, Nieves-Bonilla JM, et al. The CLEC-2-podoplanin axis controls the contractility of fibroblastic reticular cells and lymph node microarchitecture. Nat Immunol. 2015;16(1):75-84.
45. Peters A, Burkett PR, Sobel RA, Buckley CD, Watson SP, Bettelli E, et al. Podoplanin negatively regulates CD4+ effector T cell responses. J Clin Invest. 2015;125(1):129-40.
46. Darlington PJ, Boivin MN, Renoux C, Francois M, Galipeau J, Freedman MS, et al. Reciprocal Th1 and Th17 regulation by mesenchymal stem cells: implication for multiple sclerosis. Ann Neurol. 2010;68(4):540-5.
47. Luz-Crawford P, Noel D, Fernandez X, Khoury M, Figueroa F, Carrion F, et al. Mesenchymal stem cells repress Th17 molecular program through the PD-1 pathway. PLoS One. 2012;7(9):e45272.
48. Liu C, Jiang J, Gao L, Wang X, Hu X, Wu M, et al. Soluble PD-1 aggravates progression of collagen-induced arthritis through Th1 and Th17 pathways. Arthritis Res Ther. 2015;17(1):340.
49. Huang YH, Tsai K, Ma C, Vallance BA, Priatel JJ, Tan R. SLAM-SAP signaling promotes differentiation of IL-17-producing T cells and progression of experimental autoimmune encephalomyelitis. J Immunol. 2014;193(12):5841-53.
50. Paulos CM, Carpenito C, Plesa G, Suhoski MM, Varela-Rohena A, Golovina TN, et al. The inducible costimulator (ICOS) is critical for the development of human T(H)17 cells. Sci Transl Med. 2010;2(55):55ra78.