Table of Contents Author Guidelines Submit a Manuscript
Clinical and Developmental Immunology
Volume 2013, Article ID 345092, 11 pages
http://dx.doi.org/10.1155/2013/345092
Research Article

Antigen-Specific Gene Therapy after Immunisation Reduces the Severity of Collagen-Induced Arthritis

1Department of Rheumatology and Inflammatory Research, University of Gothenburg, P.O. Box 480, 405 30 Gothenburg, Sweden
2Medical Inflammation Research, Karolinska Institute, 171 77 Stockholm, Sweden
3Molecular Immunology Unit, Institute of Child Health, UCL, 30 Guilford Street, London WC1N 1EH, UK

Received 1 September 2013; Accepted 25 October 2013

Academic Editor: Nejat Egilmez

Copyright © 2013 Tove Eneljung et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Kukar, O. Petryna, and P. Efthimiou, “Biological targets in the treatment of rheumatoid arthritis: a comprehensive review of current and in-development biological disease modifying anti-rheumatic drugs,” Biologics: Targets & Therapy, vol. 3, pp. 443–457, 2009. View at Google Scholar
  2. J. D. Isaacs, “Therapeutic agents for patients with rheumatoid arthritis and an inadequate response to tumour necrosis factor-α antagonists,” Expert Opinion on Biological Therapy, vol. 9, no. 12, pp. 1463–1475, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. C. Scheinecker, K. Redlich, and J. S. Smolen, “Cytokines as therapeutic targets: advances and limitations,” Immunity, vol. 28, no. 4, pp. 440–444, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. E. F. Rosloniec, K. B. Whittington, D. M. Zaller, and A. H. Kang, “HLA-DR1 (DRB1*0101) and DR4 (DRB1*0401) use the same anchor residues for binding an immunodominant peptide derived from human type II collagen,” Journal of Immunology, vol. 168, no. 1, pp. 253–259, 2002. View at Google Scholar · View at Scopus
  5. E. C. Andersson, B. E. Hansen, H. Jacobsen et al., “Definition of MHC and T cell receptor contacts in the HLA-DR4-restricted immunodominant epitope in type II collagen and characterization of collagen-induced arthritis in HLA-DR4 and human CD4 transgenic mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 13, pp. 7574–7579, 1998. View at Google Scholar · View at Scopus
  6. A. Dessen, C. M. Lawrence, S. Cupo, D. M. Zaller, and D. C. Wiley, “X-ray crystal structure of HLA-DR4 (DRA*0101, DRB1*0401) complexed with a peptide from human collagen II,” Immunity, vol. 7, no. 4, pp. 473–481, 1997. View at Google Scholar · View at Scopus
  7. B.-Y. Diab, N. C. Lambert, F.-E. L'Faqihi, P. Loubet-Lescoulié, C. de Préval, and H. Coppin, “Human collagen II peptide 256-271 preferentially binds to HLA-DR molecules associated with susceptibility to rheumatoid arthritis,” Immunogenetics, vol. 49, no. 1, pp. 36–44, 1999. View at Publisher · View at Google Scholar · View at Scopus
  8. P. Kjellen, U. Brunsberg, J. Broddefalk et al., “The structural basis of MHC control of collagen-induced arthritis, binding of the immunodominant type II collagen 256-270 glycopeptide to H-2Aq and H-2Ap molecules,” European Journal of Immunology, vol. 28, no. 2, pp. 755–767, 1998. View at Google Scholar
  9. E. Michaelsson, M. Andersson, A. Engstrom, and R. Holmdahl, “Identification of an immunodominant type-II collagen peptide recognized by T cells in H-2(q) mice: self tolerance at the level of determinant selection,” European Journal of Immunology, vol. 22, no. 7, pp. 1819–1825, 1992. View at Publisher · View at Google Scholar · View at Scopus
  10. E. F. Rosloniec, K. B. Whittington, D. D. Brand, L. K. Myers, and J. M. Stuart, “Identification of MHC class II and TCR binding residues in the type II collagen immunodominant determinant mediating collagen-induced arthritis,” Cellular Immunology, vol. 172, no. 1, pp. 21–28, 1996. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Mullazehi, M. C. Wick, L. Klareskog, R. van Vollenhoven, and J. Ronnelid, “Anti-type II collagen antibodies are associated with early radiographic destruction in rheumatoid arthritis,” Arthritis Research & Therapy, vol. 14, no. 3, article R100, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. L. K. Myers, Y. Sakurai, B. Tang et al., “Peptide-induced suppression of collagen-induced arthritis in HLA-DR1 transgenic mice,” Arthritis and Rheumatism, vol. 46, no. 12, pp. 3369–3377, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. N. A. Staines, N. Harper, F. J. Ward, V. Malmström, R. Holmdahl, and S. Bansal, “Mucosal tolerance and suppression of collagen-induced arthritis (CIA) induced by nasal inhalation of synthetic peptide 184-198 of bovine type II collagen (CII) expressing a dominant T cell epitope,” Clinical and Experimental Immunology, vol. 103, no. 3, pp. 368–375, 1996. View at Google Scholar · View at Scopus
  14. S. D. Miller, D. M. Turley, and J. R. Podojil, “Antigen-specific tolerance strategies for the prevention and treatment of autoimmune disease,” Nature Reviews Immunology, vol. 7, no. 9, pp. 665–677, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Larché and D. C. Wraith, “Peptide-based therapeutic vaccines for allergic and autoimmune diseases,” Nature Medicine, vol. 11, no. 4, pp. S69–S76, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. C. P. Genain, K. Abel, N. Belmar et al., “Late complications of immune deviation therapy in a nonhuman primate,” Science, vol. 274, no. 5295, pp. 2054–2057, 1996. View at Publisher · View at Google Scholar · View at Scopus
  17. C. E. Smith, T. N. Eagar, J. L. Strominger, and S. D. Miller, “Differential induction of IgE-mediated anaphylaxis after soluble vs. cell-bound tolerogenic peptide therapy of autoimmune encephalomyelitis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 27, pp. 9595–9600, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Honda, A. Ametani, T. Matsumoto et al., “Vaccination with an immunodominant peptide of bovine type II collagen induces an anti-TCR response, and modulates the onset and severity of collage-induced arthritis,” International Immunology, vol. 16, no. 5, pp. 737–745, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. K. Higuchi, M.-N. Kweon, K. Fujihashi, J. R. McGhee, and H. Kiyono, “Comparison of nasal and oral tolerance for the prevention of collagen induced murine arthritis,” Journal of Rheumatology, vol. 27, no. 4, pp. 1038–1044, 2000. View at Google Scholar · View at Scopus
  20. W. Wei, L.-L. Zhang, J.-H. Xu et al., “A multicenter, double-blind, randomized, controlled phase III clinical trial of chicken type II collagen in rheumatoid arthritis,” Arthritis Research and Therapy, vol. 11, no. 6, article R180, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. G. Garcia, Y. Komagata, A. J. Slavin, R. Maron, and H. L. Weiner, “Suppression of collagen-induced arthritis by oral or nasal administration of type II collagen,” Journal of Autoimmunity, vol. 13, no. 3, pp. 315–324, 1999. View at Publisher · View at Google Scholar · View at Scopus
  22. S. D. Khare, C. J. Krco, M. M. Griffiths, H. S. Luthra, and C. S. David, “Oral administration of an immunodominant human collagen peptide modulates collagen-induced arthritis,” Journal of Immunology, vol. 155, no. 7, pp. 3653–3659, 1995. View at Google Scholar · View at Scopus
  23. P. Zhu, X.-Y. Li, H.-K. Wang et al., “Oral administration of type-II collagen peptide 250-270 suppresses specific cellular and humoral immune response in collagen-induced arthritis,” Clinical Immunology, vol. 122, no. 1, pp. 75–84, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Hasselberg, K. Schön, A. Tarkowski, and N. Lycke, “Role of CTA1R7K-COL-DD as a novel therapeutic mucosal tolerance-inducing vector for treatment of collagen-induced arthritis,” Arthritis and Rheumatism, vol. 60, no. 6, pp. 1672–1682, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. X. Song, F. Liang, N. Liu et al., “Construction and characterization of a novel DNA vaccine that is potent antigen-specific tolerizing therapy for experimental arthritis by increasing CD4+CD25+Treg cells and inducing Th1 to Th2 shift in both cells and cytokines,” Vaccine, vol. 27, no. 5, pp. 690–700, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Dzhambazov, K. S. Nandakumar, J. Kihlberg, L. Fugger, R. Holmdahl, and M. Vestberg, “Therapeutic vaccination of active arthritis with a glycosylated collagen type II pepticle in complex with MHC class II molecules,” Journal of Immunology, vol. 176, no. 3, pp. 1525–1533, 2006. View at Google Scholar · View at Scopus
  27. T. Sakuma, M. A. Barry, and Y. Ikeda, “Lentiviral vectors: basic to translational,” The Biochemical Journal, vol. 443, no. 3, pp. 603–618, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Charrier, D. Stockholm, K. Seye et al., “A lentiviral vector encoding the human Wiskott-Aldrich syndrome protein corrects immune and cytoskeletal defects in WASP knockout mice,” Gene Therapy, vol. 12, no. 7, pp. 597–606, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. C.-C. Chen, A. Rivera, N. Ron, J. P. Dougherty, and Y. Ron, “A gene therapy approach for treating T-cell-mediated autoimmune diseases,” Blood, vol. 97, no. 4, pp. 886–894, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. I. Gjertsson, K. L. Laurie, J. Devitt et al., “Tolerance induction using lentiviral gene delivery delays onset and severity of collagen II arthritis,” Molecular Therapy, vol. 17, no. 4, pp. 632–640, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. N. Srinivasakumar, “HIV-1 vector systems,” Somatic Cell and Molecular Genetics, vol. 26, no. 1–6, pp. 51–81, 2001. View at Publisher · View at Google Scholar · View at Scopus
  32. C. Demaison, K. Parsley, G. Brouns et al., “High-level transduction and gene expression in hematopoietic repopulating cells using a human imunodeficiency virus type 1-based lentiviral vector containing an internal spleen focus forming virus promoter,” Human Gene Therapy, vol. 13, no. 7, pp. 803–813, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. S. P. Perfetto, P. K. Chattopadhyay, and M. Roederer, “Seventeen-colour flow cytometry: unravelling the immune system,” Nature Reviews Immunology, vol. 4, no. 8, pp. 648–655, 2004. View at Google Scholar · View at Scopus
  34. A. M. Thornton, P. E. Korty, D. Q. Tran et al., “Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells,” Journal of Immunology, vol. 184, no. 7, pp. 3433–3441, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. T. Batsalova, B. Dzhambazov, D. Klaczkowska, and R. Holmdahl, “Mice producing less reactive oxygen species are relatively resistant to collagen glycopeptide vaccination against arthritis,” Journal of Immunology, vol. 185, no. 5, pp. 2701–2709, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Behrens, M. Smart, D. Luckey, H. Luthra, and V. Taneja, “To B or not to B: role of B cells in pathogenesis of arthritis in HLA transgenic mice,” Journal of Autoimmunity, vol. 37, no. 2, pp. 95–103, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. E. Schurgers, A. Billiau, and P. Matthys, “Collagen-induced arthritis as an animal model for rheumatoid arthritis: focus on interferon-γ,” Journal of Interferon and Cytokine Research, vol. 31, no. 12, pp. 917–926, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Svensson, J. Jirholt, R. Holmdahl, and L. Jansson, “B cell-deficient mice do not develop type II collagen-induced arthritis (CIA),” Clinical and Experimental Immunology, vol. 111, no. 3, pp. 521–526, 1998. View at Publisher · View at Google Scholar · View at Scopus
  39. B. Tang, D. L. Cullins, J. Zhou et al., “Modulation of collagen-induced arthritis by adenovirus-mediated intra-articular expression of modified collagen type II,” Arthritis Research and Therapy, vol. 12, no. 4, article R136, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. I. Kochetkova, T. Thornburg, G. Callis, and D. W. Pascual, “Segregated regulatory CD39+CD4+ T cell function: TGF-β-producing Foxp3- and IL-10-producing Foxp3+ cells are interdependent for protection against collagen-induced arthritis,” Journal of Immunology, vol. 187, no. 9, pp. 4654–4666, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. M. E. Morgan, R. P. M. Sutmuller, H. J. Witteveen et al., “CD25+ cell depletion hastens the onset of severe disease in collagen-induced arthritis,” Arthritis and Rheumatism, vol. 48, no. 5, pp. 1452–1460, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. K.-M. Chavele and M. R. Ehrenstein, “Regulatory T-cells in systemic lupus erythematosus and rheumatoid arthritis,” FEBS Letters, vol. 585, no. 23, pp. 3603–3610, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. G. P. Wright, H. J. Stauss, and M. R. Ehrenstein, “Therapeutic potential of Tregs to treat rheumatoid arthritis,” Seminars in Immunology, vol. 23, no. 3, pp. 195–201, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. J. Abe, S. Ueha, J. Suzuki, Y. Tokano, K. Matsushima, and S. Ishikawa, “Increased Foxp3+ CD4+ regulatory T cells with intact suppressive activity but altered cellular localization in murine lupus,” American Journal of Pathology, vol. 173, no. 6, pp. 1682–1692, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. J. H. Buckner, “Mechanisms of impaired regulation by CD4+ CD25+ FOXP3+ regulatory T cells in human autoimmune diseases,” Nature Reviews Immunology, vol. 10, no. 12, pp. 849–859, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Sakaguchi, M. Miyara, C. M. Costantino, and D. A. Hafler, “FOXP3+ regulatory T cells in the human immune system,” Nature Reviews Immunology, vol. 10, no. 7, pp. 490–500, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Bettini and D. A. Vignali, “Regulatory T cells and inhibitory cytokines in autoimmunity,” Current Opinion in Immunology, vol. 21, no. 6, pp. 612–618, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Oh, A. L. Rankin, and A. J. Caton, “CD4+CD25+ regulatory T cells in autoimmune arthritis,” Immunological Reviews, vol. 233, no. 1, pp. 97–111, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. M. E. Morgan, R. Flierman, L. M. van Duivenvoorde et al., “Effective treatment of collagen-induced arthritis by adoptive transfer of CD25+ regulatory T cells,” Arthritis and Rheumatism, vol. 52, no. 7, pp. 2212–2221, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. M. R. Ehrenstein, J. G. Evans, A. Singh et al., “Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFα therapy,” The Journal of Experimental Medicine, vol. 200, no. 3, pp. 277–285, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. T. Akimova, U. H. Beier, L. Wang, M. H. Levine, and W. W. Hancock, “Helios expression is a marker of T cell activation and proliferation,” PLoS ONE, vol. 6, no. 8, Article ID e24226, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Rantapää-Dahlqvist, B. A. W. de Jong, E. Berglin et al., “Antibodies against cyclic citrullinated peptide and IgA rheumatoid factor predict the development of rheumatoid arthritis,” Arthritis and Rheumatism, vol. 48, no. 10, pp. 2741–2749, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. K. S. Nandakumar, “Pathogenic antibody recognition of cartilage,” Cell and Tissue Research, vol. 339, no. 1, pp. 213–220, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. M. J. Rowley, K. S. Nandakumar, and R. Holmdahl, “The role of collagen antibodies in mediating arthritis,” Modern Rheumatology, vol. 18, no. 5, pp. 429–441, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. K. S. Nandakumar, E. Bajtner, L. Hill et al., “Arthritogenic antibodies specific for a major type II collagen triple-helical epitope bind and destabilize cartilage independent of inflammation,” Arthritis and Rheumatism, vol. 58, no. 1, pp. 184–196, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. R. Holmdahl, M. Andersson, T. J. Goldschmidt, K. Gustafsson, L. Jansson, and J. A. Mo, “Type II collagen autoimmunity in animals and provocations leading to arthritis,” Immunological Reviews, vol. 118, no. 1, pp. 193–232, 1990. View at Google Scholar · View at Scopus