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Journal of Immunology Research
Volume 2015, Article ID 129682, 14 pages
http://dx.doi.org/10.1155/2015/129682
Research Article

Infusion of Sulfosuccinimidyl-4-[N-maleimidomethyl]cyclohexane-1-carboxylate-Conjugated MOG35–55-Coupled Spleen Cells Effectively Prevents and Reverses Experimental Autoimmune Encephalomyelitis in Mice

1Department of Hematology, Xuanwu Hospital, Capital Medical University, Beijing 100053, China
2Department of Pathology, Immunology and Laboratory Medicine, University of Florida College of Medicine, Gainesville, FL 32610, USA

Received 27 April 2015; Revised 12 June 2015; Accepted 16 June 2015

Academic Editor: Ethan M. Shevach

Copyright © 2015 Lanfang Zhang 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. Rangachari and V. K. Kuchroo, “Using EAE to better understand principles of immune function and autoimmune pathology,” Journal of Autoimmunity, vol. 45, pp. 31–39, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. C. S. Constantinescu, N. Farooqi, K. O'Brien, and B. Gran, “Experimental autoimmune encephalomyelitis (EAE) as a model for multiple sclerosis (MS),” British Journal of Pharmacology, vol. 164, no. 4, pp. 1079–1106, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. A. P. Robinson, C. T. Harp, A. Noronha, and S. D. Miller, “The experimental autoimmune encephalomyelitis (EAE) model of MS. utility for understanding disease pathophysiology and treatment,” Handbook of Clinical Neurology, vol. 122, pp. 179–189, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. Y. Komiyama, S. Nakae, T. Matsuki et al., “IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis,” The Journal of Immunology, vol. 177, no. 1, pp. 566–573, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. G. Chen and M. Frances Shannon, “Transcription factors and Th17 cell development in experimental autoimmune encephalomyelitis,” Critical Reviews in Immunology, vol. 33, no. 2, pp. 165–182, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. M. El-Behi, A. Rostami, and B. Ciric, “Current views on the roles of Th1 and Th17 cells in experimental autoimmune encephalomyelitis,” Journal of Neuroimmune Pharmacology, vol. 5, no. 2, pp. 189–197, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. C. S. Garris, L. Wu, S. Acharya et al., “Defective sphingosine 1-phosphate receptor 1 (S1P1) phosphorylation exacerbates TH17-mediated autoimmune neuroinflammation,” Nature Immunology, vol. 14, no. 11, pp. 1166–1172, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. A. S. Farias, R. L. Talaisys, Y. C. Blanco et al., “Regulatory T cell induction during Plasmodium chabaudi infection modifies the clinical course of experimental autoimmune encephalomyelitis,” PLoS ONE, vol. 6, no. 3, Article ID e17849, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. T. Schneider-Hohendorf, M.-P. Stenner, C. Weidenfeller et al., “Regulatory T cells exhibit enhanced migratory characteristics, a feature impaired in patients with multiple sclerosis,” European Journal of Immunology, vol. 40, no. 12, pp. 3581–3590, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. L. Steinman and Y. Shoenfeld, “From defining antigens to new therapies in multiple sclerosis: honoring the contributions of Ruth Arnon and Michael Sela,” Journal of Autoimmunity, vol. 54, pp. 1–7, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. B. Yuan, L. Zhao, F. Fu et al., “A novel nanoparticle containing MOG peptide with BTLA induces T cell tolerance and prevents multiple sclerosis,” Molecular Immunology, vol. 57, no. 2, pp. 93–99, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. J. N. H. Stern, D. B. Keskin, Z. Kato et al., “Promoting tolerance to proteolipid protein-induced experimental autoimmune encephalomyelitis through targeting dendritic cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 40, pp. 17280–17285, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. F. Puentes, K. Dickhaut, M. Hofstätter, K. Falk, and O. Rötzschke, “Active suppression induced by repetitive self-epitopes protects against EAE development,” PLoS ONE, vol. 8, no. 5, Article ID e64888, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. D. M. Turley and S. D. Miller, “Peripheral tolerance induction using ethylenecarbodiimide-fixed APCs uses both direct and indirect mechanisms of antigen presentation for prevention of experimental autoimmune encephalomyelitis,” The Journal of Immunology, vol. 178, no. 4, pp. 2212–2220, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. C. E. Smith and S. D. Miller, “Multi-peptide coupled-cell tolerance ameliorates ongoing relapsing EAE associated with multiple pathogenic autoreactivities,” Journal of Autoimmunity, vol. 27, no. 4, pp. 218–231, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. T. Kheradmand, S. Wang, R. F. Gibly et al., “Permanent protection of PLG scaffold transplanted allogeneic islet grafts in diabetic mice treated with ECDI-fixed donor splenocyte infusions,” Biomaterials, vol. 32, no. 20, pp. 4517–4524, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. B. T. Fife, I. Guleria, M. G. Bupp et al., “Insulin-induced remission in new-onset NOD mice is maintained by the PD-1-PD-L1 pathway,” Journal of Experimental Medicine, vol. 203, no. 12, pp. 2737–2747, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. T. Kheradmand, S. Wang, J. Bryant et al., “Ethylenecarbodiimide-fixed donor splenocyte infusions differentially target direct and indirect pathways of allorecognition for induction of transplant tolerance,” The Journal of Immunology, vol. 189, no. 2, pp. 804–812, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Lutterotti, S. Yousef, A. Sputtek et al., “Antigen-specific tolerance by autologous myelin peptide-coupled cells: a phase 1 trial in multiple sclerosis,” Science Translational Medicine, vol. 5, no. 188, Article ID 188ra75, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. D. M. Turley and S. D. Miller, “Prospects for antigen-specific tolerance based therapies for the treatment of multiple sclerosis,” Results and Problems in Cell Differentiation, vol. 51, pp. 217–235, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. C.-Q. Xia and K.-J. Kao, “Induction of immune tolerance across major histocompatibility complex barrier by transfusion of ultraviolet B-irradiated immature dendritic cells,” Transfusion, vol. 45, no. 2, pp. 181–188, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. I. K. H. Poon, C. D. Lucas, A. G. Rossi, and K. S. Ravichandran, “Apoptotic cell clearance: basic biology and therapeutic potential,” Nature Reviews Immunology, vol. 14, no. 3, pp. 166–180, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Q. Xia, R. Peng, Y. Qiu, M. Annamalai, D. Gordon, and M. J. Clare-Salzler, “Transfusion of apoptotic β-cells induces immune tolerance to β-cell antigens and prevents type 1 diabetes in NOD mice,” Diabetes, vol. 56, no. 8, pp. 2116–2123, 2007. View at Publisher · View at Google Scholar
  24. M. Oukka, “Interplay between pathogenic Th17 and regulatory T cells,” Annals of the Rheumatic Diseases, vol. 66, no. 3, pp. iii87–iii90, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. T. Aranami and T. Yamamura, “Th17 cells and autoimmune encephalomyelitis (EAE/MS),” Allergology International, vol. 57, no. 2, pp. 115–120, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. U. Kalinke and M. Prinz, “Endogenous, or therapeutically induced, type i interferon responses differentially modulate Th1/Th17-mediated autoimmunity in the CNS,” Immunology and Cell Biology, vol. 90, no. 5, pp. 505–509, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. H. Batoulis, K. Addicks, and S. Kuerten, “Emerging concepts in autoimmune encephalomyelitis beyond the CD4/T(H)1 paradigm,” Annals of Anatomy, vol. 192, no. 4, pp. 179–193, 2010. View at Google Scholar
  28. J. E. Christiaansen, D. Gallardo, S. S. Burnside, A. A. Nelson, and D. W. Sears, “Rapid covalent coupling of proteins to cell surfaces: immunological characterization of viable protein-cell conjugates,” Journal of Immunological Methods, vol. 74, no. 2, pp. 229–239, 1984. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. X. Guo, L. Zhang, S. Wan et al., “Tolerance induction between two different strains of parental mice prevents graft-versus-host disease in haploidentical hematopoietic stem cell transplantation to F1 mice,” Biochemical and Biophysical Research Communications, vol. 446, no. 4, pp. 1035–1041, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. C.-Q. Xia, Y. Qiu, R.-H. Peng, J. Lo-Dauer, and M. J. Clare-Salzler, “Infusion of UVB-treated splenic stromal cells induces suppression of β cell antigen-specific T cell responses in NOD mice,” Journal of Autoimmunity, vol. 30, no. 4, pp. 283–292, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. A. A. Vandenbark, B. Celnik, M. Vainiene, S. D. Miller, and H. Offner, “Myelin antigen-coupled splenocytes suppress experimental autoimmune encephalomyelitis in Lewis rats through a partially reversible anergy mechanism,” Journal of Immunology, vol. 155, no. 12, pp. 5861–5867, 1995. View at Google Scholar · View at Scopus
  32. E. J. McMahon, S. L. Bailey, C. V. Castenada, H. Waldner, and S. D. Miller, “Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis,” Nature Medicine, vol. 11, no. 3, pp. 335–339, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. J. L. Croxford, J. K. Olson, and S. D. Miller, “Epitope spreading and molecular mimicry as triggers of autoimmunity in the Theiler's virus-induced demyelinating disease model of multiple sclerosis,” Autoimmunity Reviews, vol. 1, no. 5, pp. 251–260, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. C. L. Vanderlugt and S. D. Miller, “Epitope spreading in immune-mediated diseases: implications for immunotherapy,” Nature Reviews Immunology, vol. 2, no. 2, pp. 85–95, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. M. T. Stephan, J. J. Moon, S. H. Um, A. Bersthteyn, and D. J. Irvine, “Therapeutic cell engineering with surface-conjugated synthetic nanoparticles,” Nature Medicine, vol. 16, no. 9, pp. 1035–1041, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. V. Kuchroo, “Interplay between pathogenic effector Th17 and regulatory T cells in autoimmunity and tissue inflammation,” Clinical and Experimental Rheumatology, vol. 26, no. 4, p. 714, 2008. View at Google Scholar
  37. S. Sakaguchi, N. Sakaguchi, M. Asano, M. Itoh, and M. Toda, “Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases,” Journal of Immunology, vol. 155, no. 3, pp. 1151–1164, 1995. View at Google Scholar · View at Scopus
  38. J. G. Henderson, A. Opejin, A. Jones, C. Gross, and D. Hawiger, “CD5 instructs extrathymic regulatory T cell development in response to self and tolerizing antigens,” Immunity, vol. 42, no. 3, pp. 471–483, 2015. View at Publisher · View at Google Scholar
  39. C. Olofsson, T. Ahl, T. Johansson et al., “A multicenter clinical study of the safety and activity of maleimide-polyethylene glycol-modified hemoglobin (Hemospan) in patients undergoing major orthopedic surgery,” Anesthesiology, vol. 105, no. 6, pp. 1153–1163, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. T. Gilewski, G. Ragupathi, S. Bhuta et al., “Immunization of metastatic breast cancer patients with a fully synthetic globo H conjugate: a phase I trial,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 6, pp. 3270–3275, 2001. View at Publisher · View at Google Scholar · View at Scopus