Thymic stromal lymphopoietin as a novel mediator amplifying immunopathology in rheumatic disease

Rheumatology (United Kingdom)

Volumn 54, Issue 10, 2015, Pages 1771-1779

  Hillen, Maarten R ^a   Radstake, Timothy R D J ^a   Hack, Cornelis E ^a   van Roon, Joel A G ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Dendritic cells; Immunopathology; T cells; Thymic stromal lymphopoietin

Indexed keywords

THYMIC STROMAL LYMPHOPOIETIN; CYTOKINE;

ANTIGEN ANTIBODY COMPLEX; ARTICLE; AUTOIMMUNITY; CELL EXPANSION; CYTOKINE PRODUCTION; DENDRITIC CELL; GENE OVEREXPRESSION; HUMAN; IMMUNOPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; RHEUMATIC DISEASE; RHEUMATOID ARTHRITIS; SJOEGREN SYNDROME; SYSTEMIC LUPUS ERYTHEMATOSUS; SYSTEMIC SCLEROSIS; T LYMPHOCYTE ACTIVATION; ANIMAL; DISEASE MODEL; MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; CYTOKINES; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; HUMANS; MICE; RHEUMATIC DISEASES; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84986244035     PISSN: 14620324     EISSN: 14620332     Source Type: Journal    
DOI: 10.1093/rheumatology/kev241     Document Type: Article

References (91)

1. Sims JE, Williams DE, Morrissey PJ, et al. Molecular cloning and biological characterization of a novel murine lymphoid growth factor. J Exp Med 2000;192:671-80.
2. Soumelis V, Reche PA, Kanzler H, et al. Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat Immunol 2002;3:673-80.
3. Kaur D, Doe C, Woodman L, et al. Mast cell-airway smooth muscle crosstalk: the role of thymic stromal lymphopoietin. Chest 2012;142:76-85.
4. Allakhverdi Z, Comeau MR, Jessup HK, et al. Thymic stromal lymphopoietin is released by human epithelial cells in response to microbes, trauma, or inflammation and potently activates mast cells. J Exp Med 2007;204:253-8.
5. Ozawa T, Koyama K, Ando T, et al. Thymic stromal lymphopoietin secretion of synovial fibroblasts is positively and negatively regulated by Toll-like receptors/nuclear factor-kappaB pathway and interferon-gamma/dexamethasone. Mod Rheumatol 2007;17:459-63.
6. Ying S, O'Connor B, RatoffJ, et al. Thymic stromal lymphopoietin expression is increased in asthmatic airways and correlates with expression of Th2-attracting chemokines and disease severity. J Immunol 2005;174:8183-90.
7. Kashyap M, Rochman Y, Spolski R, Samsel L, Leonard WJ. Thymic stromal lymphopoietin is produced by dendritic cells. J Immunol 2011;187:1207-11.
8. Kato A, Favoreto S, Avila PC, Schleimer RP. TLR3-and Th2 cytokine-dependent production of thymic stromal lymphopoietin in human airway epithelial cells. J Immunol 2007;179:1080-7.
9. Lee H-C, Ziegler SF. Inducible expression of the proallergic cytokine thymic stromal lymphopoietin in airway epithelial cells is controlled by NFkappaB. Proc Natl Acad Sci USA 2007;104:914-9.
10. Ma P, Bian F, Wang Z, et al. Human corneal epitheliumderived thymic stromal lymphopoietin links the innate and adaptive immune responses via TLRs and Th2 cytokines. Invest Ophthalmol Vis Sci 2009;50:2702-9.
11. Le TA, Takai T, Vu AT, et al. Glucocorticoids inhibit doublestranded RNA-induced thymic stromal lymphopoietin release from keratinocytes in an atopic cytokine milieu more effectively than tacrolimus. Int Arch Allergy Immunol 2010;153:27-34.
12. Nomura K, Kojima T, Fuchimoto J, et al. Regulation of interleukin-33 and thymic stromal lymphopoietin in human nasal fibroblasts by proinflammatory cytokines. Laryngoscope 2012;122:1185-92.
13. Hui CCK, Murphy DM, Neighbour H, et al. T cell-mediated induction of thymic stromal lymphopoietin in differentiated human primary bronchial epithelial cells. Clin Exp Allergy 2014;44:953-64.
14. Park LS, Martin U, Garka K, et al. Cloning of the murine thymic stromal lymphopoietin (TSLP) receptor: formation of a functional heteromeric complex requires interleukin 7 receptor. J Exp Med 2000;192:659-70.
15. Pandey A, Ozaki K, Baumann H, et al. Cloning of a receptor subunit required for signaling by thymic stromal lymphopoietin. Nat Immunol 2000;1:59-64.
16. Fry TJ, Mackall CL. Interleukin-7: from bench to clinic. Blood 2002;99:3892-904.
17. Rochman Y, Kashyap M, Robinson GW, et al. Thymic stromal lymphopoietin-mediated STAT5 phosphorylation via kinases JAK1 and JAK2 reveals a key difference from IL-7-induced signaling. Proc Natl Acad Sci USA 2010;107:19455-60.
18. Reche PA, Soumelis V, Gorman DM, et al. Human thymic stromal lymphopoietin preferentially stimulates myeloid cells. J Immunol 2001;167:336-43.
19. Rochman I, Watanabe N, Arima K, Liu Y-J, Leonard WJ. Cutting edge: direct action of thymic stromal lymphopoietin on activated human CD4+ T cells. J Immunol 2007;178:6720-4.
20. Wu WH, Park CO, Oh SH, et al. Thymic stromal lymphopoietin-activated invariant natural killer T cells trigger an innate allergic immune response in atopic dermatitis. J Allergy Clin Immunol 2010;126:290-9-299.e1-4.
21. Perrigoue JG, Saenz SA, Siracusa MC, et al. MHC class II-dependent basophil-CD4+ T cell interactions promote T(H)2 cytokine-dependent immunity. Nat Immunol. 2009;10:697-705.
22. Morshed M, YousefiS, Stöckle C, Simon H-U, Simon D. Thymic stromal lymphopoietin stimulates the formation of eosinophil extracellular traps. Allergy 2012;67:1127-37.
23. Watanabe N, Hanabuchi S, Soumelis V, et al. Human thymic stromal lymphopoietin promotes dendritic cellmediated CD4+ T cell homeostatic expansion. Nat Immunol 2004;5:426-34.
24. Watanabe N, Wang Y-H, Lee HK, et al. Hassall's corpuscles instruct dendritic cells to induce CD4+CD25+ regulatory T cells in human thymus. Nature 2005;436:1181-5.
25. Al-Shami A, Spolski R, Kelly J, et al. A role for thymic stromal lymphopoietin in CD4(+) T cell development. J Exp Med 2004;200:159-68.
26. Peschon JJ, Morrissey PJ, Grabstein KH, et al. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J Exp Med 1994;180:1955-60.
27. Chappaz S, Flueck L, Farr AG, Rolink AG, Finke D. Increased TSLP availability restores T-and B-cell compartments in adult IL-7 deficient mice. Blood 2007;110:3862-70.
28. Puel A, Ziegler SF, Buckley RH, Leonard WJ. Defective IL7R expression in T(-)B(+)NK(+) severe combined immunodeficiency. Nat Genet 1998;20:394-7.
29. Vosshenrich CAJ, Cumano A, Müller W, Di Santo JP, Vieira P. Thymic stromal-derived lymphopoietin distinguishes fetal from adult B cell development. Nat Immunol 2003;4:773-9.
30. Iseki M, Omori-Miyake M, Xu W, et al. Thymic stromal lymphopoietin (TSLP)-induced polyclonal B-cell activation and autoimmunity are mediated by CD4+ T cells and IL-4. Int Immunol 2012;24:183-95.
31. Osborn MJ, Ryan PL, Kirchhof N, et al. Overexpression of murine TSLP impairs lymphopoiesis and myelopoiesis. Blood 2004;103:843-51.
32. Roll JD, Reuther GW. CRLF2 and JAK2 in B-progenitor acute lymphoblastic leukemia: a novel association in oncogenesis. Cancer Res 2010;70:7347-52.
33. Chapiro E, Russell L, Lainey E, et al. Activating mutation in the TSLPR gene in B-cell precursor lymphoblastic leukemia. Leukemia 2010;24:642-5.
34. Brocker T. Survival of mature CD4 T lymphocytes is dependent on major histocompatibility complex class II-expressing dendritic cells. J Exp Med 1997;186:1223-32.
35. Metzger TC, Anderson MS. Control of central and peripheral tolerance by Aire. Immunol Rev 2011;241:89-103.
36. Al-Shami A, Spolski R, Kelly J, Keane-Myers A, Leonard WJ. A role for TSLP in the development of inflammation in an asthma model. J Exp Med 2005;202:829-39.
37. Watanabe N, Hanabuchi S, Marloie-Provost M-A, et al. Human TSLP promotes CD40 ligand-induced IL-12 production by myeloid dendritic cells but maintains their Th2 priming potential. Blood 2005;105:4749-51.
38. Yokoi T, Amakawa R, Tanijiri T, et al. Mycobacterium bovis Bacillus Calmette-Gué rin suppresses inflammatory Th2 responses by inducing functional alteration of TSLP-activated dendritic cells. Int Immunol 2008;20:1321-9.
39. Tanaka J, Watanabe N, Kido M, et al. Human TSLP and TLR3 ligands promote differentiation of Th17 cells with a central memory phenotype under Th2-polarizing conditions. Clin Exp Allergy 2009;39:89-100.
40. Zhou B, Comeau MR, Smedt TD, et al. Thymic stromal lymphopoietin as a key initiator of allergic airway inflammation in mice. Nat Immunol 2005;6:1047-53.
41. Leipe J, Grunke M, Dechant C, et al. Role of Th17 cells in human autoimmune arthritis. Arthritis Rheum 2010;62:2876-85.
42. Duhen T, Geiger R, Jarrossay D, Lanzavecchia A, Sallusto F. Production of interleukin 22 but not interleukin 17 by a subset of human skin-homing memory T cells. Nat Immunol 2009;10:857-63.
43. Iellem A, Mariani M, Lang R, et al. Unique chemotactic response profile and specific expression of chemokine receptors CCR4 and CCR8 by CD4(+)CD25(+) regulatory T cells. J Exp Med 2001;194:847-53.
44. Scott DL, Wolfe F, Huizinga TW. Rheumatoid arthritis. Lancet 2010;376:1094-108.
45. Yudoh K, Matsuno H, Nakazawa F, Yonezawa T, Kimura T. Reduced expression of the regulatory CD4+ T cell subset is related to Th1/Th2 balance and disease severity in rheumatoid arthritis. Arthritis Rheum 2000;43:617-27.
46. Kremer JM, Westhovens R, Leon M, et al. Treatment of rheumatoid arthritis by selective inhibition of T-cell activation with fusion protein CTLA4Ig. N Engl J Med 2003;349:1907-15.
47. Edwards JCW, Szczepanski L, Szechinski J, et al. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med 2004;350:2572-81.
48. Moret FM, Hack CE, van der Wurff-Jacobs KMG, et al. Thymic stromal lymphopoietin (TSLP): a novel proinflammatory mediator in rheumatoid arthritis that potently activates CD1c(+) myeloid dendritic cells to attract and stimulate T cells. Arthritis Rheum 2014;66:1176-84.
49. Koyama K, Ozawa T, Hatsushika K, et al. A possible role for TSLP in inflammatory arthritis. Biochem Biophys Res Commun 2007;357:99-104.
50. Brentano F, Schorr O, Gay RE, Gay S, Kyburz D. RNA released from necrotic synovial fluid cells activates rheumatoid arthritis synovial fibroblasts via Toll-like receptor 3. Arthritis Rheum 2005;52:2656-65.
51. Jeong H-J, Nam S-Y, Oh H-A, et al. Interleukin-32-induced thymic stromal lymphopoietin plays a critical role in macrophage differentiation through the activation of caspase-1 in vitro. Arthritis Res Ther 2012;14:R259.
52. Messer L, Alsaleh G, Freyssinet J-M, et al. Microparticleinduced release of B-lymphocyte regulators by rheumatoid synoviocytes. Arthritis Res Ther 2009;11:R40.
53. Moret FM, Hack CE, van der Wurff-Jacobs KMG, et al. Intra-articular CD1c-expressing 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 2013;15:R155.
54. Menten P, Wuyts A, Van Damme J. Macrophage inflammatory protein-1. Cytokine Growth Factor Rev 2002;13:455-81.
55. Loetscher P, Uguccioni M, Bordoli L, et al. CCR5 is characteristic of Th1 lymphocytes. Nature 1998 22;391:344-5.
56. Imai T, Nagira M, Takagi S, et al. Selective recruitment of CCR4-bearing Th2 cells toward antigen-presenting cells by the CC chemokines thymus and activation-regulated chemokine and macrophage-derived chemokine. Int Immunol 1999;11:81-8.
57. Acosta-Rodriguez EV, Rivino L, Geginat J, et al. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat Immunol 2007;8:639-46.
58. Semmling V, Lukacs-Kornek V, Thaiss CA, et al. Alternative cross-priming through CCL17-CCR4-mediated attraction of CTLs toward NKT cell-licensed DCs. Nat Immunol 2010;11:313-20.
59. Kato T, Saeki H, Tsunemi Y, et al. Thymus and activationregulated chemokine (TARC)/CC chemokine ligand (CCL) 17 accelerates wound healing by enhancing fibroblast migration. Exp Dermatol 2011;20:669-74.
60. Chabaud M, Lubberts E, Joosten L, van Den Berg W, Miossec P. IL-17 derived from juxta-articular bone and synovium contributes to joint degradation in rheumatoid arthritis. Arthritis Res 2001;3:168-77.
61. Zhang L, Li J-M, Liu X-G, et al. Elevated Th22 cells correlated with Th17 cells in patients with rheumatoid arthritis. J Clin Immunol 2011;31:606-14.
62. Hillen MR, Moret FM, Lafeber FPJG, et al. Targeting CD1cexpressing MDCs to inhibit T cell activation and thymus and activation regulated chemokine (TARC)-dependent chemotaxis in RA. [abstract]. Arthritis Rheum 2013;65 (Suppl 10):949.
63. Bugatti S, Vitolo B, Caporali R, Montecucco C, Manzo A. B cells in rheumatoid arthritis: from pathogenic players to disease biomarkers. Biomed Res Int 2014;2014:681678.
64. Xu W, He B, Chiu A, et al. Epithelial cells trigger frontline immunoglobulin class switching through a pathway regulated by the inhibitor SLPI. Nat Immunol 2007;8:294-303.
65. Hartgring SAY, Willis CR, Dean CE Jr, et al. Critical proinflammatory role of thymic stromal lymphopoietin and its receptor in experimental autoimmune arthritis. Arthritis Rheum 2011;63:1878-87.
66. Gabrielli A, Avvedimento EV, Krieg T. Scleroderma. N Engl J Med 2009;360:1989-2003.
67. Christmann RB, Mathes A, Affandi AJ, et al. Thymic stromal lymphopoietin is up-regulated in the skin of patients with systemic sclerosis and induces profibrotic genes and intracellular signaling that overlap with those induced by interleukin-13 and transforming growth factor β. Arthritis Rheum 2013;65:1335-46.
68. Usategui A, Criado G, Izquierdo E, et al. A profibrotic role for thymic stromal lymphopoietin in systemic sclerosis. Ann Rheum Dis 2013;72:2018-23.
69. Taneda S, Segerer S, Hudkins KL, et al. Cryoglobulinemic glomerulonephritis in thymic stromal lymphopoietin transgenic mice. Am J Pathol 2001;159:2355-69.
70. Mühlfeld AS, Segerer S, Hudkins K, et al. Deletion of the Fcg receptor IIb in thymic stromal lymphopoietin transgenic mice aggravates membranoproliferative glomerulonephritis. Am J Pathol 2003;163:1127-36.
71. Hanrotel-Saliou C, Segalen I, Le Meur Y, Youinou P, Renaudineau Y. Glomerular antibodies in lupus nephritis. Clin Rev Allerg Immunol 2011;40:151-8.
72. Ellison CA, Lissitsyn YV, Gheorghiu I, Gartner JG. Immunomodulatory effects of palifermin (recombinant human keratinocyte growth factor) in an SLE-like model of chronic graft-versus-host disease. Scand J Immunol 2012;75:69-76.
73. Hillen MR, Bikker A, Kruize AA, et al. Decreased expression of TSLP in labial salivary glands of patients with primary Sjögren's syndrome is associated with local and systemic disease parameters. J Transl Med 2012;10(Suppl 3):P36.
74. Hu W, Pasare C. Location, location, location: tissuespecific regulation of immune responses. J Leukoc Biol 2013;94:409-21.
75. Noble CL, Abbas AR, Lees CW, et al. Characterization of intestinal gene expression profiles in Crohn's disease by genome-wide microarray analysis. Inflamm Bowel Dis 2010;16:1717-28.
76. Taylor BC, Zaph C, Troy AE, et al. TSLP regulates intestinal immunity and inflammation in mouse models of helminth infection and colitis. J Exp Med 2009;206:655-67.
77. Biton M, Levin A, Slyper M, et al. Epithelial microRNAs regulate gut mucosal immunity via epithelium-T cell crosstalk. Nat Immunol 2011;12:239-46.
78. Rimoldi M, Chieppa M, Salucci V, et al. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat Immunol 2005;6:507-14.
79. Bjerkan L, Schreurs O, Engen SA, et al. The short form of TSLP is constitutively translated in human keratinocytes and has characteristics of an antimicrobial peptide. Mucosal Immunol 2015;8:49-56.
80. Besin G, Gaudreau S, Mé nard M, et al. Thymic stromal lymphopoietin and thymic stromal lymphopoietinconditioned dendritic cells induce regulatory T-cell differentiation and protection of NOD mice against diabetes. Diabetes 2008;57:2107-17.
81. Zhang Z, Hener P, Frossard N, et al. Thymic stromal lymphopoietin overproduced by keratinocytes in mouse skin aggravates experimental asthma. Proc Natl Acad Sci USA 2009;106:1536-41.
82. Han H, Xu W, Headley MB, et al. Thymic stromal lymphopoietin (TSLP)-mediated dermal inflammation aggravates experimental asthma. Mucosal Immunol 2012;5:342-51.
83. Valencia X, Stephens G, Goldbach-Mansky R, et al. TNF downmodulates the function of human CD4+CD25hi Tregulatory cells. Blood 2006;108:253-61.
84. Flores-Borja F, Jury EC, Mauri C, Ehrenstein MR. Defects in CTLA-4 are associated with abnormal regulatory T cell function in rheumatoid arthritis. Proc Natl Acad Sci USA 2008;105:19396-401.
85. high T cells in type 1 diabetes may be partially mediated by IL-2 deprivation. PLoS One 2009;4:e6527.
86. + regulatory T cells. J Immunol 2008;181:7350-5.
87. + regulatory T cells in patients with type 1 diabetes from effects mediated by TNF. Cytokine 2011;55:353-61.
88. van Amelsfort JM, van Roon JA, Noordergraaf M, et al. Proinflammatory mediator-induced reversal of CD4+, CD25+ regulatory T cell-mediated suppression in rheumatoid arthritis. Arthritis Rheum 2007; 56:732-42.
89. Ito T, Wang Y-H, Duramad O, et al. TSLP-activated dendritic cells induce an inflammatory T helper type 2 cell response through OX40 ligand. J Exp Med 2005;202:1213-23.
90. Ziegler SF, Artis D. Sensing the outside world: TSLP regulates barrier immunity. Nat Immunol 2010;11:289-93.
91. Gauvreau GM, O'Byrne PM, Boulet L-P, et al. Effects of an anti-TSLP antibody on allergen-induced asthmatic responses. N Engl J Med 2014;370:2102-10.