Engineered regulatory T cells coexpressing MHC class II: Peptide complexes are efficient inhibitors of autoimmune T cell function and prevent the development of autoimmune arthritis

Journal of Immunology

Volumn 190, Issue 11, 2013, Pages 5382-5391

  Qian, Zhaohui ^a   Latham, Kary A ^a   Whittington, Karen B ^b   Miller, David C ^a   Brand, David D ^a,b   Rosloniec, Edward F ^a,b  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; COLLAGEN; GAMMA INTERFERON; HLA DR1 ANTIGEN; INTERLEUKIN 17; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TRANSCRIPTION FACTOR FOXP3;

ADOPTIVE IMMUNOTHERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTHRITIS; ARTICLE; AUTOIMMUNE ARTHRITIS; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CELL COUNT; CONTROLLED STUDY; DNA PROTEIN COMPLEX; IN VIVO STUDY; LYMPHOCYTE SUBPOPULATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; TH1 CELL; TH17 CELL;

ANIMALS; ARTHRITIS; ARTHRITIS, EXPERIMENTAL; AUTOIMMUNE DISEASES; AUTOIMMUNITY; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; CELL SURVIVAL; COLLAGEN TYPE II; CYTOKINES; GENE EXPRESSION; GENE ORDER; GENETIC VECTORS; HLA-DR1 ANTIGEN; HUMANS; MICE; MICE, TRANSGENIC; PEPTIDES; PHENOTYPE; RETROVIRIDAE; T-LYMPHOCYTES, REGULATORY; TRANSDUCTION, GENETIC;

EID: 84878081603     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300024     Document Type: Article

References (42)

1. Bennett, C. L., J. Christie, F. Ramsdell, M. E. Brunkow, P. J. Ferguson, L. Whitesell, T. E. Kelly, F. T. Saulsbury, P. F. Chance, and H. D. Ochs. 2001. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat. Genet. 27: 20-21. (Pubitemid 32044513)
2. Wildin, R. S., F. Ramsdell, J. Peake, F. Faravelli, J. L. Casanova, N. Buist, E. Levy-Lahad, M. Mazzella, O. Goulet, L. Perroni, et al. 2001. X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy. Nat. Genet. 27: 18-20. (Pubitemid 32044512)
3. Fontenot, J. D., M. A. Gavin, and A. Y. Rudensky. 2003. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4: 330-336. (Pubitemid 36432314)
4. Torgerson, T. R., and H. D. Ochs. 2002. Immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome: a model of immune dysregulation. Curr. Opin. Allergy Clin. Immunol. 2: 481-487. (Pubitemid 36105810)
5. Lyon, M. F., J. Peters, P. H. Glenister, S. Ball, and E. Wright. 1990. The scurfy mouse mutant has previously unrecognized hematological abnormalities and resembles Wiskott-Aldrich syndrome. Proc. Natl. Acad. Sci. USA 87: 2433-2437.
6. + regulatory T cells rescue scurfy mice. Eur. J. Immunol. 38: 1814-1821.
7. Hori, S., T. Takahashi, and S. Sakaguchi. 2003. Control of autoimmunity by naturally arising regulatory CD4+ T cells. Adv. Immunol. 81: 331-371. (Pubitemid 38009046)
8. + regulatory T cells. Int. Immunol. 16: 249-256.
9. + regulatory cells mediate genetic resistance to experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA 101: 15434-15439.
10. + regulatory T cells suppress antigen-specific autoreactive immune responses and central nervous system inflammation during active experimental autoimmune encephalomyelitis. J. Immunol. 169: 4712-4716.
11. Morgan, M. E., R. Flierman, L. M. van Duivenvoorde, H. J. Witteveen, W. van Ewijk, J. M. van Laar, R. R. de Vries, and R. E. Toes. 2005. Effective treatment of collagen-induced arthritis by adoptive transfer of CD25+ regulatory T cells. Arthritis Rheum. 52: 2212-2221. (Pubitemid 40994344)
12. + T cells. Arthritis Res. Ther. 7: R291-R301.
13. Haque, R., F. Lei, X. Xiong, Y. Bian, B. Zhao, Y. Wu, and J. Song. 2012. Programming of regulatory T cells from pluripotent stem cells and prevention of autoimmunity. J. Immunol. 189: 1228-1236.
14. Tang, Q., K. J. Henriksen, M. Bi, E. B. Finger, G. Szot, J. Ye, E. L. Masteller, H. McDevitt, M. Bonyhadi, and J. A. Bluestone. 2004. In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J. Exp. Med. 199: 1455-1465. (Pubitemid 38780401)
15. Jaeckel, E., H. von Boehmer, and M. P. Manns. 2005. Antigen-specific FoxP3-transduced T-cells can control established type 1 diabetes. Diabetes 54: 306-310.
16. Scalapino, K. J., Q. Tang, J. A. Bluestone, M. L. Bonyhadi, and D. I. Daikh. 2006. Suppression of disease in New Zealand Black/New Zealand White lupusprone mice by adoptive transfer of ex vivo expanded regulatory T cells. J. Immunol. 177: 1451-1459. (Pubitemid 44092478)
17. + T cells during cure of colitis. J. Immunol. 177: 5852-5860.
18. van Herwijnen, M. J., L. Wieten, R. van der Zee, P. J. van Kooten, J. P. Wagenaar-Hilbers, A. Hoek, I. den Braber, S. M. Anderton, M. Singh, H. D. Meiring, et al. 2012. Regulatory T cells that recognize a ubiquitous stress-inducible self-antigen are long-lived suppressors of autoimmune arthritis. Proc. Natl. Acad. Sci. USA 109: 14134-14139.
19. Wright, G. P., C. A. Notley, S. A. Xue, G. M. Bendle, A. Holler, T. N. Schumacher, M. R. Ehrenstein, and H. J. Stauss. 2009. Adoptive therapy with redirected primary regulatory T cells results in antigen-specific suppression of arthritis. Proc. Natl. Acad. Sci. USA 106: 19078-19083.
20. + regulatory T cells prevent autoimmunity by inhibiting dendritic cells from activating autoreactive T cells. J. Immunol. 179: 4685-4693.
21. Benoist, C., and D. Mathis. 1990. Regulation of major histocompatibility complex class-II genes: X, Y and other letters of the alphabet. Annu. Rev. Immunol. 8: 681-715. (Pubitemid 20135643)
22. Baecher-Allan, C., E. Wolf, and D. A. Hafler. 2006. MHC class II expression identifies functionally distinct human regulatory T cells. J. Immunol. 176: 4622-4631.
23. Hori, S., T. Nomura, and S. Sakaguchi. 2003. Control of regulatory T cell development by the transcription factor Foxp3. Science 299: 1057-1061. (Pubitemid 36222930)
24. Rosloniec, E. F., D. D. Brand, L. K. Myers, K. B. Whittington, M. Gumanovskaya, D. M. Zaller, A. Woods, D. M. Altmann, J. M. Stuart, and A. H. Kang. 1997. An HLA-DR1 transgene confers susceptibility to collagen-induced arthritis elicited with human type II collagen. J. Exp. Med. 185: 1113-1122. (Pubitemid 27136803)
25. Woods, A., H. Y. Chen, M. E. Trumbauer, A. Sirotina, R. Cummings, and D. M. Zaller. 1994. Human major histocompatibility complex class II-restricted T cell responses in transgenic mice. J. Exp. Med. 180: 173-181. (Pubitemid 24181066)
26. Rosloniec, E. F., M. Cremer, A. Kang, and L. K. Myers. 2001. Collagen-induced arthritis. Curr. Protoc. Immunol. Chapter 15: Unit 15.
27. Persons, D. A., J. A. Allay, E. R. Allay, R. J. Smeyne, R. A. Ashmun, B. P. Sorrentino, and A. W. Nienhuis. 1997. Retroviral-mediated transfer of the green fluorescent protein gene into murine hematopoietic cells facilitates scoring and selection of transduced progenitors in vitro and identification of genetically modified cells in vivo. Blood 90: 1777-1786. (Pubitemid 27377287)
28. Donnelly, M. L., L. E. Hughes, G. Luke, H. Mendoza, E. ten Dam, D. Gani, and M. D. Ryan. 2001. The 'cleavage' activities of foot-and-mouth disease virus 2A site-directed mutants and naturally occurring '2A-like' sequences. J. Gen. Virol. 82: 1027-1041. (Pubitemid 32454603)
29. Donnelly, M. L., G. Luke, A. Mehrotra, X. Li, L. E. Hughes, D. Gani, and M. D. Ryan. 2001. Analysis of the aphthovirus 2A/2B polyprotein 'cleavage' mechanism indicates not a proteolytic reaction, but a novel translational effect: a putative ribosomal 'skip'. J. Gen. Virol. 82: 1013-1025. (Pubitemid 32454602)
30. Latham, K. A., K. B. Whittington, R. Zhou, Z. Qian, and E. F. Rosloniec. 2005. Ex vivo characterization of the autoimmune T cell response in the HLA-DR1 mouse model of collagen-induced arthritis reveals long-term activation of type II collagen-specific cells and their presence in arthritic joints. J. Immunol. 174: 3978-3985. (Pubitemid 40395972)
31. Denizot, F., and R. Lang. 1986. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J. Immunol. Methods 89: 271-277. (Pubitemid 16080782)
32. Mosmann, T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65: 55-63. (Pubitemid 14203433)
33. Kappler, J. W., B. Skidmore, J. White, and P. Marrack. 1981. Antigen-inducible, H-2?restricted, interleukin-2 ?producing T cell hybridomas: lack of independent antigen and H-2 recognition. J. Exp. Med. 153: 1198-1214. (Pubitemid 11107588)
34. Qian, Z., K. A. Latham, K. B. Whittington, D. C. Miller, D. D. Brand, and E. F. Rosloniec. 2010. An autoantigen-specific, highly restricted T cell repertoire infiltrates the arthritic joints of mice in an HLA-DR1 humanized mouse model of autoimmune arthritis. J. Immunol. 185: 110-118.
35. Kozono, H., J. White, J. Clements, P. Marrack, and J. Kappler. 1994. Production of soluble MHC class II proteins with covalently bound single peptides. Nature 369: 151-154. (Pubitemid 24153438)
36. Fransson, M., E. Piras, J. Burman, B. Nilsson, M. Essand, B. Lu, R. A. Harris, P. U. Magnusson, E. Brittebo, and A. S. Loskog. 2012. CAR/FoxP3-engineered T regulatory cells target the CNS and suppress EAE upon intranasal delivery. J. Neuroinflammation 9: 112.
37. Holling, T. M., E. Schooten, and P. J. van Den Elsen. 2004. Function and regulation of MHC class II molecules in T-lymphocytes: of mice and men. Hum. Immunol. 65: 282-290. (Pubitemid 38543063)
38. + T regulatory cell-mediated suppression. Immunity 30: 636-645.
39. + T cells involving acquired MHC class II:peptide complexes: another mechanism to limit clonal expansion? Blood 101: 2704-2710.
40. + Treg. Eur. J. Immunol. 39: 1108-1117.
41. + T reg cells impinge on autoimmune diabetes. J. Exp. Med. 202: 1387-1397.
42. LeGuern, C., Y. Akiyama, S. Germana, K. Tanaka, L. Fernandez, Y. Iwamoto, S. Houser, and G. Benichou. 2010. Intracellular MHC class II controls regulatory tolerance to allogeneic transplants. J. Immunol. 184: 2394-2400.