Umbilical cord mesenchymal stem cells inhibit the differentiation of circulating T follicular helper cells in patients with primary Sjögren's syndrome through the secretion of indoleamine 2,3-dioxygenase

Rheumatology (United Kingdom)

Volumn 54, Issue 2, 2015, Pages 332-342

  Liu, Rui ^a   Su, Dinglei ^a   Zhou, Min ^a   Feng, Xuebing ^a   Li, Xia ^b   Sun, Lingyun ^a  

^a THE AFFILIATED DRUM TOWER HOSPITAL OF NANJING UNIVERSITY MEDICAL SCHOOL   (China)

^b DALIAN MEDICAL UNIVERSITY   (China)

Author keywords

3 dioxygenase; Indoleamine 2; Mesenchymal stem cell; Sj gren's syndrome; T follicular helper cell

Indexed keywords

1 METHYL TRYPTOPHAN; CARBOXYFLUORESCEIN DIACETATE SUCCINIMIDYL ESTER; CHEMOKINE RECEPTOR CXCR5; CYCLOOXYGENASE 2; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3 DIOXYGENASE INHIBITOR; INTERLEUKIN 10; INTERLEUKIN 21; LA ANTIBODY; LIPOCORTIN 5; MESSENGER RNA; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN; PROTEIN BCL 6; RETINOID RELATED ORPHAN RECEPTOR ALPHA; RO ANTIBODY; SCATTER FACTOR; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR T BET; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; ANTINUCLEAR ANTIBODY; SS-A ANTIBODIES; SS-B ANTIBODIES;

ADULT; ANTIBODY BLOOD LEVEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL POLARITY; CIRCULATING T FOLLICULAR HELPER CELL; COCULTURE; CORRELATIONAL STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; ENZYME ACTIVITY; ENZYME RELEASE; EUROPEAN LEAGUE AGAINST RHEUMATISM SJOEGREN SYNDROME DISEASE ACTIVITY INDEX; FEMALE; FLOW CYTOMETRY; FLUORESCENCE; HELPER CELL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LUMINEX CYTOKINE ASSAY; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MAJOR CLINICAL STUDY; MALE; MESENCHYMAL STEM CELL; MIDDLE AGED; MRNA EXPRESSION ASSAY; MUSCULOSKELETAL DISEASE ASSESSMENT; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SJOEGREN SYNDROME; STEM CELL CULTURE; SUPERNATANT; T LYMPHOCYTE ACTIVATION; UMBILICAL CORD; UMBILICAL CORD MESENCHYMAL STEM CELL; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; ENZYMOLOGY; IMMUNOLOGY; MESENCHYMAL STROMA CELL; METABOLISM; PHYSIOLOGY; SECRETION (PROCESS);

ANTIBODIES, ANTINUCLEAR; CELL DIFFERENTIATION; CELLS, CULTURED; FEMALE; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; MALE; MESENCHYMAL STROMAL CELLS; MIDDLE AGED; RNA, MESSENGER; SJOGREN'S SYNDROME; T-LYMPHOCYTES, HELPER-INDUCER; UMBILICAL CORD;

EID: 84925582125     PISSN: 14620324     EISSN: 14620332     Source Type: Journal    
DOI: 10.1093/rheumatology/keu316     Document Type: Article

References (48)

1. Fox RI. Sjogren's syndrome. Lancet 2005;366:321–31.
2. Amft N, Curnow SJ, Scheel-Toellner D et al. Ectopic expression of the B cell-attracting chemokine BCA-1 (CXCL13) on endothelial cells and within lymphoid follicles contributes to the establishment of germinal center-like structures in Sjogren's syndrome. Arthritis Rheum 2001; 44:2633–41.
3. Hansen A, Lipsky PE, Dorner T. B cells in Sjogren's syndrome: indications for disturbed selection and differentiation in ectopic lymphoid tissue. Arthritis Res Ther 2007;9: 218.
4. Rasheed AU, Rahn HP, Sallusto F, Lipp M, Muller G. Follicular B helper T cell activity is confined to CXCR5(hi)ICOS(hi) CD4 T cells and is independent of CD57 expression. Eur J Immunol 2006;36:1892–903.
5. Haynes NM, Allen CD, Lesley R et al. Role of CXCR5 and CCR7 in follicular Th cell positioning and appearance of a programmed cell death gene-1high germinal centerassociated subpopulation. J Immunol 2007;179: 5099–108.
6. Kroenke MA, Eto D, Locci M et al. Bcl6 and Maf cooperate to instruct human follicular helper CD4 T cell differentiation. J Immunol 2012;188:3734–44.
7. Breitfeld D, Ohl L, Kremmer E et al. Follicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production. J Exp Med 2000;192:1545–52.
8. Simpson N, Gatenby PA, Wilson A et al. Expansion of circulating T cells resembling follicular helper T cells is a fixed phenotype that identifies a subset of severe systemic lupus erythematosus. Arthritis Rheum 2010;62: 234–44.
9. Morita R, Schmitt N, Bentebibel SE et al. Human blood CXCR5(+)CD4(+) T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion. Immunity 2011;34:108–21.
10. Gong YZ, Nititham J, Taylor K et al. Differentiation of follicular helper T cells by salivary gland epithelial cells in primary Sjogren's syndrome. J Autoimmun 2014;51: 57–66.
11. Li XY, Wu ZB, Ding J et al. Role of the frequency of blood CD4(+)CXCR5(+)CCR6(+) T cells in autoimmunity in patients with Sjogren's syndrome. Biochem Biophys Res Commun 2012;422:238–44.
12. Szabo K, Papp G, Barath S et al. Follicular helper T cells may play an important role in the severity of primary Sjogren's syndrome. Clin Immunol 2013;147:95–104.
13. Pittenger MF, Mackay AM, Beck SC et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143–7.
14. Sanchez-Ramos J, Song S, Cardozo-Pelaez F et al. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol 2000;164:247–56.
15. Gu Z, Akiyama K, Ma X et al. Transplantation of umbilical cord mesenchymal stem cells alleviates lupus nephritis in MRL/lpr mice. Lupus 2010;19:1502–14.
16. Zhou K, Zhang H, Jin O et al. Transplantation of human bone marrow mesenchymal stem cell ameliorates the autoimmune pathogenesis in MRL/lpr mice. Cell Mol Immunol 2008;5:417–24.
17. Sun L, Akiyama K, Zhang H et al. Mesenchymal stem cell transplantation reverses multiorgan dysfunction in systemic lupus erythematosus mice and humans. Stem Cells 2009;27:1421–32.
18. Sun L, Wang D, Liang J et al. Umbilical cord mesenchymal stem cell transplantation in severe and refractory systemic lupus erythematosus. Arthritis Rheum 2010;62:2467–75.
19. Augello A, Tasso R, Negrini SM, Cancedda R, Pennesi G. Cell therapy using allogeneic bone marrow mesenchymal stem cells prevents tissue damage in collagen-induced arthritis. Arthritis Rheum 2007;56:1175–86.
20. Gonzalez MA, Gonzalez-Rey E, Rico L, Buscher D, Delgado M. Treatment of experimental arthritis by inducing immune tolerance with human adipose-derived mesenchymal stem cells. Arthritis Rheum 2009;60: 1006–19.
21. Xu J, Wang D, Liu D et al. Allogeneic mesenchymal stem cell treatment alleviates experimental and clinical Sjogren syndrome. Blood 2012;120:3142–51.
22. Vitali C, Bombardieri S, Jonsson R 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: 554–8.
23. Seror R, Ravaud P, Bowman SJ et al. EULAR Sjogren's syndrome disease activity index: development of a consensus systemic disease activity index for primary Sjogren's syndrome. Ann Rheum Dis 2010;69:1103–9.
24. Locht H, Pelck R, Manthorpe R. Clinical manifestations correlated to the prevalence of autoantibodies in a large (n=321) cohort of patients with primary Sjogren's syndrome: a comparison of patients initially diagnosed according to the Copenhagen classification criteria with the American-European consensus criteria. Autoimmun Rev 2005;4:276–81.
25. Linterman MA, Pierson W, Lee SK et al. Foxp3+ follicular regulatory T cells control the germinal center response. Nat Med 2011;17:975–82.
26. Kawakami A, Nakashima K, Tamai M et al. Toll-like receptor in salivary glands from patients with Sjogren's syndrome: functional analysis by human salivary gland cell line. J Rheumatol 2007;34:1019–26.
27. Lovgren T, Eloranta ML, Kastner B et al. Induction of interferon-alpha by immune complexes or liposomes containing systemic lupus erythematosus autoantigenand Sjogren's syndrome autoantigen-associated RNA. Arthritis Rheum 2006;54:1917–27.
28. Liu Y, Mu R, Wang S et al. Therapeutic potential of human umbilical cord mesenchymal stem cells in the treatment of rheumatoid arthritis. Arthritis Res Ther 2010; 12:R210.
29. Wollenberg I, Agua-Doce A, Hernandez A et al. Regulation of the germinal center reaction by Foxp3+ follicular regulatory T cells. J Immunol 2011;187:4553–60.
30. Sage PT, Francisco LM, Carman CV, Sharpe AH. The receptor PD-1 controls follicular regulatory T cells in the lymph nodes and blood. Nat Immunol 2013;14: 152–61.
31. Crotty S. Follicular helper CD4 T cells (TFH). Annu Rev Immunol 2011;29:621–63.
32. Spaggiari GM, Capobianco A, Abdelrazik H et al. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood 2008;111:1327–33.
33. Nemeth K, Leelahavanichkul A, Yuen PS et al. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med 2009;15: 42–9.
34. Neuss S, Becher E, Woltje M, Tietze L, Jahnen-Dechent W. Functional expression of HGF and HGF receptor/c-met in adult human mesenchymal stem cells suggests a role in cell mobilization, tissue repair, and wound healing. Stem Cells 2004;22: 405–14.
35. Jui HY, Lin CH, Hsu WT et al. Autologous mesenchymal stem cells prevent transplant arteriosclerosis by enhancing local expression of interleukin-10, interferon-g, and indoleamine 2,3-dioxygenase. Cell Transplant 2012;21: 971–84.
36. Patel SA, Meyer JR, Greco SJ et al. Mesenchymal stem cells protect breast cancer cells through regulatory T cells: role of mesenchymal stem cell-derived TGF-β. J Immunol 2010;184:5885–94.
37. Meisel R, Zibert A, Laryea M et al. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood 2004;103:4619–21.
38. Grohmann U, Fallarino F, Puccetti P. Tolerance, DCs and tryptophan: much ado about IDO. Trends Immunol 2003; 24:242–8.
39. Ren G, Su J, Zhang L et al. Species variation in the mechanisms of mesenchymal stem cell-mediated immunosuppression. Stem Cells 2009;27:1954–62.
40. Ryan JM, Barry F, Murphy JM, Mahon BP. Interferon-g does not break, but promotes the immunosuppressive capacity of adult human mesenchymal stem cells. Clin Exp Immunol 2007;149:353–63.
41. Mellor AL, Munn DH. Tryptophan catabolism and T-cell tolerance: immunosuppression by starvation? Immunol Today 1999;20:469–73.
42. Frumento G, Rotondo R, Tonetti M et al. Tryptophanderived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. J Exp Med 2002;196:459–68.
43. Terness P, Bauer TM, Rose L et al. Inhibition of allogeneic T cell proliferation by indoleamine 2,3-dioxy-genase-expressing dendritic cells: mediation of suppression by tryptophan metabolites. J Exp Med 2002;196: 447–57.
44. Von Bubnoff D, Scheler M, Wilms H, Fimmers R, Bieber T. Identification of IDO-positive and IDO-negative human dendritic cells after activation by various proinflammatory stimuli. J Immunol 2011;186:6701–9.
45. Harden JL, Egilmez NK. Indoleamine 2,3-dioxygenase and dendritic cell tolerogenicity. Immunol Invest 2012;41: 738–64.
46. Chen W, Liang X, Peterson AJ, Munn DH, Blazar BR. The indoleamine 2,3-dioxygenase pathway is essential for human plasmacytoid dendritic cell-induced adaptive T regulatory cell generation. J Immunol 2008;181:5396–404.
47. Chung DJ, Rossi M, Romano E et al. Indoleamine 2,3-dioxygenase-expressing mature human monocyte-derived dendritic cells expand potent autologous regulatory T cells. Blood 2009;114:555–63.
48. Francois M, Romieu-Mourez R, Li M, Galipeau J. Human MSC suppression correlates with cytokine induction of indoleamine 2,3-dioxygenase and bystander M2 macrophage differentiation. Mol Ther 2012;20:187–95.