Regulatory T cell (Treg) subsets return in patients with refractory lupus following stem cell transplantation, and TGF-β-producing CD8+ Treg cells are associated with immunological remission of lupus

Journal of Immunology

Volumn 183, Issue 10, 2009, Pages 6346-6358

  Zhang, Li ^a   Bertucci, Anne M ^a   Ramsey Goldman, Rosalind ^a   Burt, Richard K ^a   Datta, Syamal K ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; AZATHIOPRINE; CD103 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; EPITOPE; HYDROXYCHLOROQUINE; LATENCY ASSOCIATED PEPTIDE; LEFLUNOMIDE; METHOTREXATE; PREDNISONE; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ADOLESCENT; ADULT; APOPTOSIS; ARTICLE; AUTOLOGOUS HEMATOPOIETIC STEM CELL TRANSPLANTATION; CD4+ CD25+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REMISSION; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE ACTIVATION;

ADOLESCENT; ADULT; ANTIGENS, CD; APOPTOSIS REGULATORY PROTEINS; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; INTEGRIN ALPHA CHAINS; INTERFERON-GAMMA; INTERLEUKIN-13; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MIDDLE AGED; NUCLEOSOMES; REMISSION, SPONTANEOUS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA; YOUNG ADULT;

EID: 76349096767     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901773     Document Type: Article

References (71)

1. Kotzin, B. L. 1996. Systemic lupus erythematosus. Cell 85: 303-306.
2. Rahman, A., and D. A. Isenberg. 2008. Systemic lupus erythematosus. N. Engl. J. Med. 358: 929-939.
3. Datta, S. K. 2003. Major peptide autoepitopes for nucleosome-centered T and B cell interaction in human and murine lupus. Ann. NY Acad. Sci. 987: 79-90.
4. Krishnan, S., D. L. Farber, and G. C. Tsokos. 2003. T cell rewiring in differentiation and disease. J. Immunol. 171: 3325-3331.
5. Datta. S. K., L. Zhang, and L. Xu. 2005. T-helper cell intrinsic defects in lupus that break peripheral tolerance to nuclear autoantigens. J. Mol. Med. 83: 267-278.
6. Mohan, C., S. Adams, V. Stanik, and S. K. Datta. 1993. Nucleosome: a major immunogen for the pathogenic autoantibody-inducing T cells of lupus. J. Exp. Med. 177: 1367-1381. (Pubitemid 23117127)
7. Kaliyaperumal, A., C. Mohan, W. Wu, and S. K. Datta. 1996. Nucleosomal peptide epitopes for nephritis-inducing T helper cells of murine lupus. J. Exp. Med. 183: 2459-2469.
8. Kaliyaperumal, A., M. A. Michaels, and S. K. Datta. 2002. Naturally processed chromatin peptides reveal a major autoepitope that primes pathogenic T and B cells of lupus. J. Immunol. 168: 2530-2537. (Pubitemid 34171860)
9. Lu, L., A. Kaliyaperumal, D. T. Boumpas, and S. K. Datta. 1999. Major peptide autoepitopes for nucleosome-specific T cells of human lupus. J. Clin. Invest. 104: 345-355.
10. Kaliyaperumal, A., M. A. Michaels, and S. K. Datta. 1999. Antigen-specific therapy of murine lupus nephritis using nucleosomal peptides: tolerance spreading impair pathogenic function of autoimmune T and B cells. J. Immunol. 162: 5775-5783. (Pubitemid 29314928)
11. Kang, H.-K., M. A. Michaels, B. R. Berner, and S. K. Datta. 2005. Very low-dose tolerance with nucleosomal peptides controls lupus and induces potent regulatory T cell subsets. J. Immunol. 174: 3247-3255.
12. Sakaguchi, S. 2000. Regulatory T cells: key controllers of immunologic selftolerance. Cell 101: 455-458.
13. Shevach, E. M. 2000. Regulatory T cells in autoimmunity. Annu. Rev. Immunol. 18: 423-449.
14. + T cell subset inhibits antigen-specific T cell responses and prevents colitis. Nature 389: 737-742.
15. Chen, Y., V. K. Kuchroo, J. Inobe, D. A. Hafler, and H. L. Weiner. 1994. Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science 265: 1237-1240. (Pubitemid 24291983)
16. Hori, S., T. Nomura, and S. Sakaguchi. 2003. Control of regulatory T cell development by the transcription factor Foxp3. Science 299: 1057-1061.
17. + regulatory T cells. Nat. Immunol. 4: 330-336.
18. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198: 1875-1886.
19. + regulatory T cells generated ex vivo with IL-2 and TGF-beta suppress a stimulatory graft-versus-host disease with a lupuslike syndrome. J. Immunol. 172: 1531-1539.
20. Gershon, R. K., and K. Kondo. 1971. Infectious immunological tolerance. Immunology 21: 903-914.
21. + T suppressor cells are back to the game: are they players in autoimmunity? Autoimmunity Rev. 1: 279-283.
22. + T cells is mediated by interferon-γ and is defective in chronic progressive multiple sclerosis. J. Clin. Invest. 95: 2711-2719.
23. Gilliet, M., and Y. J. Liu. 2002. Generation of human CD8 T regulatory cells by CD40 ligand-activated plasmacytoid dendritic cells. J. Exp. Med. 195: 695-704.
24. + T cells in EAE mice. Proc. Natl. Acad. Sci. USA 98: 6301-6306.
25. Kosiewicz, M. M., P. Alard, S. Liang, and S. L. Clark. 2004. Mechanisms of tolerance induced by transforming growth factor-β-treated antigen-presenting cells: CD8 regulatory T cells inhibit the effector phase of the immune response in primed mice through a mechanism involving Fas ligand. Int. Immunol. 16: 697-706.
26. Mellor-Pita, S., M. J. Citores, R. Castejon, P. Tutor-Ureta, M. Yebra-Bango, J. L. Andreu, and J. A. Vargas. 2006. Decrease of regulatory T cells in patients with systemic lupus erythematosus. Ann. Rheum. Dis. 65: 553-554.
27. + T cells in peripheral blood of patients with systemic lupus erythematosus. Scand. J. Immunol. 59: 198-202.
28. high T regulatory cell function in patients with active systemic lupus erythematosus. J. Immunol. 178: 2579-2588.
29. + T cells permits the development of spontaneous lupus-like disease in mice, and can be reversed by induction of mucosal tolerance to histone peptide autoantigen. Lupus 13: 192-200.
30. Kang, H.-K., M. Liu, and S. K. Datta. 2007. Low-dose peptide tolerance therapy of lupus generates plasmacytoid dendritic cells that cause expansion of autoantigen-specific Treg cells and contraction of inflammatory TH17 cells (cover page figure). J. Immunol. 178: 7849-7858.
31. 1 mice suppress in vitro production of antibodies to DNA. J. Immunol. 173: 3542-3548.
32. + cells and TGF-β. Proc. Natl. Acad. Sci. USA 103: 8810-8815.
33. Hahn, B. H., M. Anderson, E. Le, and A. La Cava. 2008. Anti-DNA Ig peptides promote Treg cell activity in systemic lupus erythematosus patients. Arthritis Rheum. 58: 2488-2497.
34. + regulatory T cells in vitro: a novel defect of T cell regulation in systemic lupus erythematosus. Arthritis Rheum. 52: 1180-1184.
35. -/low regulatory T cells in patients with active systemic lupus erythematosus. Arthritis Rheum. 58: 2120-2130.
36. + regulatory T cells to TGF-β in Cbl-b-/- mice. J. Immunol. 173: 1059-1065.
37. Yi, Y., M. McNerney, and S. K. Datta. 2000. Regulatory defects in Cbl and mitogen-activated protein kinase (extracellular signal-related kinase) pathways cause persistent hyperexpression of CD40 ligand in human lupus T cells. J. Immunol. 165: 6627-6634.
38. Jury, E. C., P. S. Kabouridis, F. Flores-Borja, R. A. Mageed, and D. A. Isenberg,. 2004. Altered lipid raft-associated signaling and ganglioside expression in T lymphocytes from patients with systemic lupus erythematosus. J. Clin. Invest. 113: 1176-1187.
39. Xu, L., L. Zhang, Y. Yi, H.-K. Kang, and S. K. Datta. 2004. Human lupus T cells resist inactivation and escape death by upregulating COX-2. Nat. Med. 10: 411-415.
40. + cells to support autoantibody synthesis. Arthritis Rheum. 33: 1216-1225.
41. Desai-Mehta, A., L. Lu, R. Ramsey-Goldman, and S. K. Datta. 1996. Hyperexpression of CD40 ligand by B and T cells in human lupus and its role in pathogenic autoantibody production. J. Clin. Invest. 97: 2063-2073. (Pubitemid 26143961)
42. Stohl, W., J. E. Elliott, L. Li, E. R. Podack, D. H. Lynch, and C. O. Jacob. 1997. Impaired nonrestricted cytolytic activity in systemic lupus erythematosus: involvement of a pathway independent of Fas, tumor necrosis factor, and extracellular ATP that is associated with little detectable perforin. Arthritis Rheum. 40: 1130-1137.
43. + T suppressor cell function in patients with active systemic lupus erythematosus. J. Immunol. 166: 6452-6457.
44. Crispín, J. C., M. Oukka, G. Bayliss, R. A. Cohen, C. A. Van Beek, I. E. Stillman, V. C. Kyttaris, V. T. Juang, and G. C. Tsokos. 2008. Expanded double negative T cells in patients with systemic lupus erythematosus produce IL-17 and infiltrate the kidneys. J. Immunol. 181: 8761-8766.
45. Hsu, H. C., P. Yang, J. Wang, Q. Wu, R. Myers, J. Chen, J. Yi, T. Guentert, A. Tousson, A. L. Stanus, et al. 2008. Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice. Nat. Immunol. 9: 166-175.
46. Bauquet, A. T., H. Jin, A. M. Paterson, M. I. Mitsdeorffer, I. C. Ho, A. H. Sharpe, and V. K. Kuchroo. 2009. The costimulatory molecule ICOS regulates the expression of c-Maf and IL-21 in the development of follicular T helper cells and Th-17 cells. Nat. Immunol. 10: 167-175.
47. + follicular helper T cells. J. Immunol. 181: 6038-6050.
48. Malissen, B. 2009. Revisiting the follicular helper T cell paradigm. Nat. Immunol. 10: 371-372.
49. Mohan, C., Y. Shi, J. D. Laman, and S. K. Datta. 1995. Interaction between CD40 and its ligand gp39 in the development of murine lupus nephritis. J. Immunol. 154: 1470-1480.
50. + T cell-mediated suppression of autoimmunity in a murine lupus model of peptideinduced immune tolerance depends on Foxp3 expression. J. Immunol. 178: 7649-7657.
51. + immune regulatory network. Blood 107: 1696-1702.
52. Burt, R. K., A. Traynor, and R. Ramsey-Goldman. 1997. Hematopoietic stem-cell transplantation for systemic lupus erythematosus. N. Engl. J. Med. 337: 1777-1778.
53. Traynor, A. E., J. Schroeder, R. M. Rosa, D. Cheng, J. Stefka, S. Mujais, S. Baker, and R. K. Burt. 2000. Treatment of severe systemic lupus erythematosus with high-dose chemotherapy and haemopoietic stem-cell transplantation: a phase I study. Lancet 356: 701-707.
54. Burt, R. K., A. Traynor, L. Statkute, W. G. Barr, R. Rosa, J. Schroeder, L. Verda, and N. Krosnjar. 2006. Nonmyeloablative hematopoietic stem cell transplantation for systemic lupus erythematosus. JAMA 295: 527-535.
55. Burt, R. K., A. Marmont, Y. Oyama, S. Slavin, R. Arnold, F. Hiepe, A. Fassas, and J. Snowden. 2006. Randomized controlled trials of autologous hematopoietic stem cell transplantation for autoimmune diseases: the evolution from myeloablative to lymphoablative transplant regimens. Arthritis Rheum. 54: 3750-3760.
56. Muraro, P. A., D. C. Douek, A. Packer, K. Chung, F. J. Guenaga, R. Cassiani-Ingoni. C. Campbell, S. Memon, J. W. Nagle, F. T. Hakim, et al. 2005. Thymic output generates a new and diverse TCR repertoire after autologous stem cell transplantation in multiple sclerosis patients. J. Exp. Med. 201: 805-816.
57. Tan, E. M., A. S. Cohen, J. F. Fries, A. T. Masi, D. J. McShane, N. F. Rothfield, J. G. Schaller, N. Talal, and R. J. Winchester. 1982. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 25: 1271-1277.
58. Bombardier, C., D. D. Gladman, M. B. Urowitz, D. Caron, and C. H. Chang. 1992. Derivation of the SLEDAI. A disease activity index for lupus patients: the Committee on Prognosis Studies in SLE. Arthritis Rheum. 35: 630-640.
59. high regulatory T cells. In Current Protocols in Immunology. J. E. Coligan, B. E. Bierer, D. H. Margulies, E. M. Shevach, and W. Strober, eds. John Wiley & Sons, New York, 7.4B. 1-7.4B.2.
60. +CD28- T suppressor cells and the induction of antigen-specific, antigen-presenting cellmediated suppression of Th reactivity. Immunol. Rev. 182: 201-206.
61. + T regulatory cells use a novel genetic program that includes CD103 to suppress Th1 immunity in eye-derived tolerance. Invest. Ophthalmol. Vis. Sci. 47: 1533-1542.
62. Okazaki, T., Y. Iwai, and T. Honjo. 2002. New regulatory co-receptors: inducible co-stimulator and PD-1. Curr. Opin. Immunol. 14: 779-782.
63. + regulatory T cell function. Science 322: 271-275.
64. Ma, A., R. Koka, and P. Burkett. 2006. Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu. Rev. Immunol. 24: 657-679.
65. Gaffen, A. L., and K. D. Lie. 2004. Overview of interleukin-2 function, production and clinical applications. Cytokine 28: 109-123.
66. Burt, R. K., and A. E. Traynor. 2003. SLE: hematopoietic stem cell transplantation for systemic lupus erythematosus. Arthritis Res. Ther. 5: 207-209. (Pubitemid 37139034)
67. Pavletic, S. Z., and G. G. Illei. 2005. The role of immune ablation and stem cell transplantation in severe SLE. Best Pract. Res. Clin. Rheumatol. 19: 839-858.
68. + regulatory T cells in untreated active systemic lupus erythematosus secondary to interferon-α-producing antigen-presenting cells. Arthritis Rheum. 58: 801-812.
69. + regulatory T cells: Interruption of the NKG2A-Qa-1 interaction allows robust suppressive activity and resolution of autoimmune disease. Proc. Natl. Acad. Sci. USA 105: 19420-19425.
70. Barthlott, T., G. Kassiotis, and B. Stockinger. 2003. T cell regulation as a side effect of homeostasis and competition. J. Exp. Med. 197: 451-460.
71. Shustov, A., I. Luzina, P. Nguyen, J. C. Papadimitriou, B. Handwerger, K. B. Elkon, and C. S. Via. 2000. Role of perforin in controlling B-cell hyperactivity and humoral autoimmunity. J. Clin. Invest. 106: R39-R47.