Skip to main content

Advertisement

Log in

Tolerogenic dendritic cells and rheumatoid arthritis: current status and perspectives

  • Review
  • Published:
Rheumatology International Aims and scope Submit manuscript

Abstract

Rheumatoid arthritis (RA) is a chronic autoimmune disease characterized by the influxation of synovia and synovial compartments with immune cells including dendritic cells (DCs). DCs that induce autoimmune tolerance are called tolerogenic DCs (tolDCs). As a promising immunotherapeutic strategy for RA, tolDCs have received increasing attention. In this review, we first introduce the significant role of tolDCs in autoimmune regulation and then describe the manipulation strategies to generate tolDCs; next, we summarize recent progress in the experimental application of tolDCs for RA therapy, and finally we discuss the perspectives of tolerogenic vaccination for the treatment for RA in clinic.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Chen M, Wang YH, Wang Y, Huang L, Sandoval H, Liu YJ, Wang J (2006) Dendritic cell apoptosis in the maintenance of immune tolerance. Science 311(5764):1160–1164. doi:10.1126/science.1122545

    Article  PubMed  CAS  Google Scholar 

  2. Imperato AK, Bingham CO III, Abramson SB (2004) Overview of benefit/risk of biological agents. Clin Exp Rheumatol 22(5 Suppl 35):S108–S114

    PubMed  CAS  Google Scholar 

  3. Flores-Borja F, Mauri C, Ehrenstein MR (2008) Restoring the balance: harnessing regulatory T cells for therapy in rheumatoid arthritis. Eur J Immunol 38(4):934–937. doi:10.1002/eji.200738107

    Article  PubMed  CAS  Google Scholar 

  4. Rutella S, Danese S, Leone G (2006) Tolerogenic dendritic cells: cytokine modulation comes of age. Blood 108(5):1435–1440. doi:10.1182/blood-2006-03-006403

    Article  PubMed  CAS  Google Scholar 

  5. Rescigno M (2010) Dendritic cells in tolerance induction for the treatment of autoimmune diseases. Eur J Immunol 40(8):2119–2123. doi:10.1002/eji.201040474

    Article  PubMed  CAS  Google Scholar 

  6. Khan S, Greenberg JD, Bhardwaj N (2009) Dendritic cells as targets for therapy in rheumatoid arthritis. Nat Rev Rheumatol 5(10):566–571. doi:10.1038/nrrheum.2009.185

    Article  PubMed  CAS  Google Scholar 

  7. Piccioli D, Tavarini S, Borgogni E, Steri V, Nuti S, Sammicheli C, Bardelli M, Montagna D, Locatelli F, Wack A (2007) Functional specialization of human circulating CD16 and CD1c myeloid dendritic-cell subsets. Blood 109(12):5371–5379. doi:10.1182/blood-2006-08-038422

    Article  PubMed  CAS  Google Scholar 

  8. Jongbloed SL, Lebre MC, Fraser AR, Gracie JA, Sturrock RD, Tak PP, McInnes IB (2006) Enumeration and phenotypical analysis of distinct dendritic cell subsets in psoriatic arthritis and rheumatoid arthritis. Arthritis Res Ther 8(1):R15. doi:10.1186/ar1864

  9. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K (2010) Development of monocytes, macrophages, and dendritic cells. Science 327(5966):656–661. doi:10.1126/science.1178331

    Article  PubMed  CAS  Google Scholar 

  10. Lebre MC, Tak PP (2009) Dendritic cells in rheumatoid arthritis: which subset should be used as a tool to induce tolerance? Hum Immunol 70(5):321–324. doi:10.1016/j.humimm.2009.02.006

    Article  PubMed  CAS  Google Scholar 

  11. Banchereau J, Steinman RM (1998) Dendritic cells and the control of immunity. Nature 392(6673):245–252. doi:10.1038/32588

    Article  PubMed  CAS  Google Scholar 

  12. Falcon C, Carranza F, Martinez FF, Knubel CP, Masih DT, Motran CC, Cervi L (2010) Excretory-secretory products (ESP) from Fasciola hepatica induce tolerogenic properties in myeloid dendritic cells. Vet Immunol Immunopathol 137(1–2):36–46. doi:10.1016/j.vetimm.2010.04.007

    Article  PubMed  CAS  Google Scholar 

  13. Arce F, Breckpot K, Stephenson H, Karwacz K, Ehrenstein MR, Collins M, Escors D (2010) Selective ERK activation suppresses inflammatory arthritis via tolerogenic dendritic cells and antigen-specific regulatory T cells. Arthritis Rheum. doi:10.1002/art.30099

  14. Wei S, Kryczek I, Zou L, Daniel B, Cheng P, Mottram P, Curiel T, Lange A, Zou W (2005) Plasmacytoid dendritic cells induce CD8+ regulatory T cells in human ovarian carcinoma. Cancer Res 65(12):5020–5026. doi:10.1158/0008-5472.CAN-04-4043

    Article  PubMed  CAS  Google Scholar 

  15. Tang Q, Henriksen KJ, Bi M, Finger EB, Szot G, Ye J, Masteller EL, McDevitt H, Bonyhadi M, Bluestone JA (2004) In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J Exp Med 199(11):1455–1465. doi:10.1084/jem.20040139

    Article  PubMed  CAS  Google Scholar 

  16. Kavousanaki M, Makrigiannakis A, Boumpas D, Verginis P (2010) Novel role of plasmacytoid dendritic cells in humans: induction of interleukin-10-producing Treg cells by plasmacytoid dendritic cells in patients with rheumatoid arthritis responding to therapy. Arthritis Rheum 62(1):53–63. doi:10.1002/art.25037

    Article  PubMed  CAS  Google Scholar 

  17. Steinman RM, Banchereau J (2007) Taking dendritic cells into medicine. Nature 449(7161):419–426. doi:10.1038/nature06175

    Article  PubMed  CAS  Google Scholar 

  18. Rossetti M, Gregori S, Roncarolo MG (2010) Granulocyte-colony stimulating factor drives the in vitro differentiation of human dendritic cells that induce anergy in naive T cells. Eur J Immunol 40(11):3097–3106. doi:10.1002/eji.201040659

    Article  PubMed  CAS  Google Scholar 

  19. Harry RA, Anderson AE, Isaacs JD, Hilkens CMU (2010) Generation and characterisation of therapeutic tolerogenic dendritic cells for rheumatoid arthritis. Ann Rheum Dis 69(11):2042–2050. doi:10.1136/ard.2009.126383

    Article  PubMed  CAS  Google Scholar 

  20. Vosters O, Neve J, De Wit D, Willems F, Goldman M, Verhasselt V (2003) Dendritic cells exposed to nacystelyn are refractory to maturation and promote the emergence of alloreactive regulatory t cells. Transplantation 75(3):383–389. doi:10.1097/01.TP.0000043924.09647.61

    Article  PubMed  CAS  Google Scholar 

  21. Healy LJ, Collins HL, Thompson SJ (2008) Systemic administration of tolerogenic dendritic cells ameliorates murine inflammatory arthritis. Open Rheumatol J 2:71–80. doi:10.2174/1874312900802010071

    Article  PubMed  CAS  Google Scholar 

  22. Zheng X, Suzuki M, Ichim TE, Zhang X, Sun H, Zhu F, Shunnar A, Garcia B, Inman RD, Min W (2010) Treatment of autoimmune arthritis using RNA interference-modulated dendritic cells. J Immunol 184(11):6457–6464. doi:10.4049/jimmunol.0901717

    Article  PubMed  CAS  Google Scholar 

  23. Fu BM, He XS, Yu S, Hu AB, Ma Y, Wu LW, Tam NL, Huang JF (2009) Tolerogenic semimature dendritic cells induce effector T-cell hyporesponsiveness by the activation of antigen-specific CD4+ CD25+ T-regulatory cells. Exp Clin Transplant 7(3):149–156

    PubMed  Google Scholar 

  24. Lim DS, Kang MS, Jeong JA, Bae YS (2009) Semi-mature DC are immunogenic and not tolerogenic when inoculated at a high dose in collagen-induced arthritis mice. Eur J Immunol 39(5):1334–1343. doi:10.1002/eji.200838987

    Article  PubMed  CAS  Google Scholar 

  25. Thomson AW, Robbins PD (2008) Tolerogenic dendritic cells for autoimmune disease and transplantation. Ann Rheum Dis 67(Suppl 3):iii90–iii96. doi:10.1136/ard.2008.099176

    Article  PubMed  CAS  Google Scholar 

  26. Zanetti M, Castiglioni P, Schoenberger S, Gerloni M (2003) The role of relB in regulating the adaptive immune response. Ann N Y Acad Sci 987:249–257

    Article  PubMed  CAS  Google Scholar 

  27. Tracey D, Klareskog L, Sasso EH, Salfeld JG, Tak PP (2008) Tumor necrosis factor antagonist mechanisms of action: a comprehensive review. Pharmacol Ther 117(2):244–279. doi:10.1016/j.pharmthera.2007.10.001

    Article  PubMed  CAS  Google Scholar 

  28. Wang L, Pino-Lagos K, de Vries VC, Guleria I, Sayegh MH, Noelle RJ (2008) Programmed death 1 ligand signaling regulates the generation of adaptive Foxp3+ CD4+ regulatory T cells. Proc Natl Acad Sci USA 105(27):9331–9336. doi:10.1073/pnas.0710441105

    Article  PubMed  CAS  Google Scholar 

  29. Kabalak G, Dobberstein SB, Matthias T, Reuter S, The YH, Dörner T, Schmidt RE, Witte T (2009) Association of immunoglobulin-like transcript 6 deficiency with Sjögren’s syndrome. Arthritis Rheum 60(10):2923–2925. doi:10.1002/art.24804

    Article  PubMed  CAS  Google Scholar 

  30. Criado G, Simelyte E, Inglis JJ, Essex D, Williams RO (2009) Indoleamine 2,3dioxygenase-mediated tryptophan catabolism regulates accumulation of Th1/Th17 cells in the joint in collagen-induced arthritis. Arthritis Rheum 60(5):1342–1351. doi:10.1002/art.24446

    Article  PubMed  Google Scholar 

  31. Tuettenberg A, Huter E, Hubo M, Horn J, Knop J, Grimbacher B, Kroczek RA, Stoll S, Jonuleit H (2009) The role of ICOS in directing T cell responses: ICOS-dependent induction of T cell anergy by tolerogenic dendritic cells. J Immunol 182(6):3349–3356. doi:10.4049/jimmunol.0802733

    Article  PubMed  CAS  Google Scholar 

  32. Ip WK, Lau YL (2004) Distinct maturation of, but not migration between, human monocyte-derived dendritic cells upon ingestion of apoptotic cells of early or late phases. J Immunol 173(1):189–196

    PubMed  CAS  Google Scholar 

  33. Skoberne M, Beignon AS, Larsson M, Bhardwaj N (2005) Apoptotic cells at the crossroads of tolerance and immunity. Curr Top Microbiol 289:259–292

    Article  CAS  Google Scholar 

  34. Kushwah R, Wu J, Oliver JR, Jiang G, Zhang JY, Siminovitch KA, Hu J (2010) Uptake of apoptotic DC converts immature DC into tolerogenic DC that induce differentiation of Foxp3(+) Treg. Eur J Immunol 40(4):1022–1035. doi:10.1002/eji.200939782

    Article  PubMed  CAS  Google Scholar 

  35. Kushwah R, Oliver JR, Zhang JY, Siminovitch KA, Hu J (2009) Apoptotic dendritic cells induce tolerance in mice through suppression of dendritic cell maturation and induction of antigen-specific regulatory T cells. J Immunol 183(11):7104–7118. doi:10.4049/jimmunol.0900824

    Article  PubMed  CAS  Google Scholar 

  36. Perone MJ, Larregina AT, Shufesky WJ, Papworth GD, Sullivan ML, Zahorchak AF, Stolz DB, Baum LG, Watkins SC, Thomson AW, Morelli AE (2006) Transgenic galectin-1 induces maturation of dendritic cells that elicit contrasting responses in naive and activated T cells. J Immunol 176(12):7207–7220

    PubMed  CAS  Google Scholar 

  37. Zheng X, Suzuki M, Zhang X, Ichim TE, Zhu F, Ling H, Shunnar A, Wang MH, Garcia B, Inman RD, Min WP (2010) RNAi-mediated CD40-CD154 interruption promotes tolerance in autoimmune arthritis. Arthritis Res Ther 12(1):R13. doi:10.1186/ar2914

    Article  PubMed  Google Scholar 

  38. Morelli AE, Thomson AW (2007) Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol 7(8):610–621. doi:10.1038/nri2132

    Article  PubMed  CAS  Google Scholar 

  39. Korn T, Bettelli E, Oukka M, Kuchroo VK (2009) IL-17 and Th17 cells. Annu Rev Immunol 27:485–517. doi:10.1146/annurev.immunol.021908.132710

    Article  PubMed  CAS  Google Scholar 

  40. Dong C (2008) TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat Rev Immunol 8(5):337–348. doi:10.1038/nri2295

    Article  PubMed  CAS  Google Scholar 

  41. Holoshitz J, De Almeida DE, Ling S (2010) A role for calreticulin in the pathogenesis of rheumatoid arthritis. Ann N Y Acad Sci 1209:91–98. doi:10.1111/j.1749-6632.2010.05745.x

    Article  PubMed  CAS  Google Scholar 

  42. Miossec P (2007) Interleukin-17 in fashion, at last: ten years after its description, its cellular source has been identified. Arthritis Rheum 56(7):2111–2115. doi:10.1002/art.22733

    Article  PubMed  CAS  Google Scholar 

  43. Lubberts E (2008) IL-17/Th17 targeting: on the road to prevent chronic destructive arthritis? Cytokine 41(2):84–91. doi:10.1016/j.cyto.2007.09.014

    Article  PubMed  CAS  Google Scholar 

  44. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, Weaver CT (2005) Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 6(11):1123–1132. doi:10.1038/ni1254

    Article  PubMed  CAS  Google Scholar 

  45. Sato K, Kawamura T, Abo T (2010) “Senobi” stretch ameliorates asthma symptoms by restoring autonomic nervous system balance. J Investig Med 58(8):968–970. doi:10.231/JIM.0b013e3181f9167b

    PubMed  Google Scholar 

  46. Takayanagi H (2005) Inflammatory bone destruction and osteoimmunology. J Periodontal Res 40(4):287–293. doi:10.1111/j.1600-0765.2005.00814.x

    Article  PubMed  CAS  Google Scholar 

  47. Paradowska-Gorycka A, Grzybowska-Kowalczyk A, Wojtecka-Lukasik E, Maslinski S (2010) IL-23 in the pathogenesis of rheumatoid arthritis. Scand J Immunol 71(3):134–145. doi:10.1111/j.1365-3083.2009.02361.x

    Article  PubMed  CAS  Google Scholar 

  48. Torres-Aguilar H, Aguilar-Ruiz SR, Gonzalez-Perez G, Munguia R, Bajana S, Meraz-Rios MA, Sanchez-Torres C (2010) Tolerogenic dendritic cells generated with different immunosuppressive cytokines induce antigen-specific anergy and regulatory properties in memory CD4+ T cells. J Immunol 184(4):1765–1775. doi:10.4049/jimmunol.0902133

    Article  PubMed  CAS  Google Scholar 

  49. Stoop JN, Harry RA, von Delwig A, Isaacs JD, Robinson JH, Hilkens CM (2010) Therapeutic effect of tolerogenic dendritic cells in established collagen-induced arthritis is associated with a reduction in Th17 responses. Arthritis Rheum 62(12):3656–3665. doi:10.1002/art.27756

    Article  PubMed  Google Scholar 

  50. Turnquist HR, Raimondi G, Zahorchak AF, Fischer RT, Wang Z, Thomson AW (2007) Rapamycin-conditioned dendritic cells are poor stimulators of allogeneic CD4+ T cells, but enrich for antigen-specific Foxp3+ T regulatory cells and promote organ transplant tolerance. J Immunol 178(11):7018–7031

    PubMed  CAS  Google Scholar 

  51. Fischer R, Turnquist HR, Taner T, Thomson AW (2009) Use of rapamycin in the induction of tolerogenic dendritic cells. Handb Exp Pharmacol 188(III):215–232. doi:10.1007/978-3-540-71029-5_10

    Google Scholar 

  52. Miller RH, Fyffe-Maricich SL (2010) Restoring the balance between disease and repair in multiple sclerosis: insights from mouse models. Dis Model Mech 3(9–10):535–539. doi:10.1242/dmm.001958

    Article  PubMed  Google Scholar 

  53. Birch NW, Zeleznik-Le NJ (2010) Glycogen synthase kinase-3 and leukemia: restoring the balance. Cancer Cell 17(6):529–531. doi:10.1016/j.ccr.2010.05.017

    Article  PubMed  CAS  Google Scholar 

  54. Xu X, Guo Z, Jiang X, Yao Y, Gao Q, Ding Y, Cao X (2011) Regulatory dendritic cells program generation of interleukin-4-producing alternative memory CD4 T cells with suppressive activity. Blood 117(4):1218–1227. doi:10.1182/blood-2010-05-285494

    Article  PubMed  CAS  Google Scholar 

  55. Boissier MC, Assier E, Falgarone G, Bessis N (2008) Shifting the imbalance from Th1/Th2 to Th17/treg: the changing rheumatoid arthritis paradigm. Joint Bone Spine 75(4):373–375. doi:10.1016/j.jbspin.2008.04.005

    Article  PubMed  CAS  Google Scholar 

  56. Zhai Y, Ghobrial RM, Busuttil RW, Kupiec-Weglinski JW (1999) Th1 and Th2 cytokines in organ transplantation: paradigm lost? Crit Rev Immunol 19(2):155–172

    PubMed  CAS  Google Scholar 

  57. Chabaud M, Aarvak T, Garnero P, Natvig JB, Miossec P (2001) Potential contribution of IL-17-producing Th(1)cells to defective repair activity in joint inflammation: partial correction with Th(2)-promoting conditions. Cytokine 13(2):113–118. doi:10.1006/cyto.2000.0811

    Article  PubMed  CAS  Google Scholar 

  58. van Duivenvoorde LM, Han WG, Bakker AM, Louis-Plence P, Charbonnier LM, Apparailly F, van der Voort EI, Jorgensen C, Huizinga TW, Toes RE (2007) Immunomodulatory dendritic cells inhibit Th1 responses and arthritis via different mechanisms. J Immunol 179(3):1506–1515

    PubMed  Google Scholar 

  59. Nadkarni S, Mauri C, Ehrenstein MR (2007) Anti-TNF-alpha therapy induces a distinct regulatory T cell population in patients with rheumatoid arthritis via TGF-beta. J Exp Med 204(1):33–39. doi:10.1084/jem.20061531

    Article  PubMed  CAS  Google Scholar 

  60. Notley CA, Ehrenstein MR (2010) The yin and yang of regulatory T cells and inflammation in RA. Nat Rev Rheumatol 6(10):572–577. doi:10.1038/nrrheum.2010.143

    Article  PubMed  CAS  Google Scholar 

  61. Chen W, Liang X, Peterson AJ, Munn DH, Blazar BR (2008) The indoleamine 2,3-dioxygenase pathway is essential for human plasmacytoid dendritic cell-induced adaptive T regulatory cell generation. J Immunol 181(8):5396–5404

    PubMed  CAS  Google Scholar 

  62. Bianco NR, Kim SH, Ruffner MA, Robbins PD (2009) Therapeutic effect of exosomes from indoleamine 2, 3-dioxygenase-positive dendritic cells in collagen-induced arthritis and delayed-type hypersensitivity disease models. Arthritis Rheum 60(2):380–389. doi:10.1002/Art.24229

    Article  PubMed  CAS  Google Scholar 

  63. Matsui JI, Ryals BM (2005) Hair cell regeneration: an exciting phenomenon…but will restoring hearing and balance be possible? J Rehabil Res Dev 42(4 Suppl 2):187–198

    Article  PubMed  Google Scholar 

  64. Sharma MD, Baban B, Chandler P, Hou DY, Singh N, Yagita H, Azuma M, Blazar BR, Mellor AL, Munn DH (2007) Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2, 3-dioxygenase. J Clin Invest 117(9):2570–2582. doi:10.1172/JCI31911

    Article  PubMed  CAS  Google Scholar 

  65. Tisch R (2010) Immunogenic versus tolerogenic dendritic cells: a matter of maturation. Int Rev Immunol 29(2):111–118. doi:10.3109/08830181003602515

    Article  PubMed  CAS  Google Scholar 

  66. Chorny A, Gonzalez-Rey E, Fernandez-Martin A, Pozo D, Ganea D, Delgado M (2005) Vasoactive intestinal peptide induces regulatory dendritic cells with therapeutic effects on autoimmune disorders. Proc Natl Acad Sci USA 102(38):13562–13567. doi:10.1073/pnas.0504484102

    Article  PubMed  CAS  Google Scholar 

  67. Kim SH, Kim S, Evans CH, Ghivizzani SC, Oligino T, Robbins PD (2001) Effective treatment of established murine collagen-induced arthritis by systemic administration of dendritic cells genetically modified to express IL-4. J Immunol 166(5):3499–3505

    PubMed  CAS  Google Scholar 

  68. Kim SH, Kim S, Oligino TJ, Robbins PD (2002) Effective treatment of established mouse collagen-induced arthritis by systemic administration of dendritic cells genetically modified to express FasL. Mol Ther 6(5):584–590

    Article  PubMed  CAS  Google Scholar 

  69. Martin E, Capini C, Duggan E, Lutzky VP, Stumbles P, Pettit AR, O’Sullivan B, Thomas R (2007) Antigen-specific suppression of established arthritis in mice by dendritic cells deficient in NF-kappaB. Arthritis Rheum 56(7):2255–2266. doi:10.1002/art.22655

    Article  PubMed  CAS  Google Scholar 

  70. Balanescu A, Nat R, Regalia T, Radu E, Bojinca V, Ionescu R, Predescu V, Popescu E, Predeteanu D (2003) Correlation between the immunophenotypical presentation of dendritic cells and the clinical response to anti-rheumatic treatment in rheumatoid arthritis. Rom J Intern Med 41(3):255–267

    PubMed  Google Scholar 

  71. Hilkens CM, Isaacs JD, Thomson AW (2010) Development of dendritic cell-based immunotherapy for autoimmunity. Int Rev Immunol 29(2):156–183. doi:10.3109/08830180903281193

    Article  PubMed  CAS  Google Scholar 

  72. Sidhu M, Griffiths MM, Bradley DS (2009) Vaccination with collagen-pulsed dendritic cells prevents the onset and reduces the disease severity in the mouse model of spontaneous polychondritis. Clin Exp Immunol 157(3):350–358. doi:10.1111/j.1365-2249.2009.03968.x

    Article  PubMed  CAS  Google Scholar 

  73. Pouniotis DS, Proudfoot O, Bogdanoska V, Apostolopoulos V, Fifis T, Plebanski M (2004) Dendritic cells induce immunity and long-lasting protection against blood-stage malaria despite an in vitro parasite-induced maturation defect. Infect Immun 72(9):5331–5339. doi:10.1128/IAI.72.9.5331-5339.2004

    Article  PubMed  CAS  Google Scholar 

  74. Pandha HS, John RJ, Hutchinson J, James N, Whelan M, Corbishley C, Dalgleish AG (2004) Dendritic cell immunotherapy for urological cancers using cryopreserved allogeneic tumour lysate-pulsed cells: a phase I/II study. BJU Int 94(3):412–418. doi:10.1111/j.1464-410X.2004.04922.x

    Article  PubMed  CAS  Google Scholar 

  75. Akbar SM, Furukawa S, Hasebe A, Horiike N, Michitaka K, Onji M (2004) Production and efficacy of a dendritic cell-based therapeutic vaccine for murine chronic hepatitis B virus carrier. Int J Mol Med 14(2):295–299

    PubMed  CAS  Google Scholar 

  76. Aguillon JC, Cruzat A, Contreras-Levicoy J, Dotte A, Pesce B, Aravena O, Salazar L, Catalan D, Abello P, Aguirre A, Llanos C, Cuchacovich M (2005) Emergent therapies for rheumatoid arthritis. Rev Med Chil 133(8):969–976

    PubMed  Google Scholar 

  77. Popov I, Li M, Zheng X, San H, Zhang X, Ichim TE, Suzuki M, Feng B, Vladau C, Zhong R, Garcia B, Strejan G, Inman RD, Min WP (2006) Preventing autoimmune arthritis using antigen-specific immature dendritic cells: a novel tolerogenic vaccine. Arthritis Res Ther 8(5):R141. doi:10.1186/ar2031

    Article  PubMed  Google Scholar 

  78. Figdor CG, de Vries IJ, Lesterhuis WJ, Melief CJ (2004) Dendritic cell immunotherapy: mapping the way. Nat Med 10(5):475–480. doi:10.1038/nm1039

    Article  PubMed  CAS  Google Scholar 

  79. Nestle FO, Banchereau J, Hart D (2001) Dendritic cells: on the move from bench to bedside. Nat Med 7(7):761–765. doi:10.1038/89863

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Dr. Fu Jinqiu, Tian Zhoubin and Zhao Kai for their review of the manuscript. This work was supported by grant from the National Natural Science Foundation of China (No. 30801258 M.H.) and The Star of Jinan Youth Science and Technology Project (No. 20100114).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bin Ning.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhao, Y., Zhang, A., Du, H. et al. Tolerogenic dendritic cells and rheumatoid arthritis: current status and perspectives. Rheumatol Int 32, 837–844 (2012). https://doi.org/10.1007/s00296-011-2133-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00296-011-2133-2

Keywords

Navigation