1932

Abstract

The undesired destruction of healthy cells, either endogenous or transplanted, by the immune system results in the loss of tissue function or limits strategies to restore tissue function. Current therapies typically involve nonspecific immunosuppression that may prevent the appropriate response to an antigen, thereby decreasing humoral immunity and increasing the risks of patient susceptibility to opportunistic infections, viral reactivation, and neoplasia. The induction of antigen-specific immunological tolerance to block undesired immune responses to self- or allogeneic antigens, while maintaining the integrity of the remaining immune system, has the potential to transform the current treatment of autoimmune disease and serve as a key enabling technology for therapies based on cell transplantation.

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2016-07-11
2024-12-10
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Literature Cited

  1. Miller SD, Turley DM, Podojil JR. 1.  2007. Antigen-specific tolerance strategies for the prevention and treatment of autoimmune disease. Nat. Rev. Immunol. 7:665–77 [Google Scholar]
  2. Zakrzewski JL, van den Brink MR, Hubbell JA. 2.  2014. Overcoming immunological barriers in regenerative medicine. Nat. Biotechnol. 32:786–94 [Google Scholar]
  3. Tobias LD.3.  2010. A Briefing Report on Autoimmune Diseases and AARDA: Past, Present, and Future Eastpointe, MI: AARDA [Google Scholar]
  4. Fischbach MA, Bluestone JA, Lim WA. 4.  2013. Cell-based therapeutics: the next pillar of medicine. Sci. Transl. Med. 5:179ps7 [Google Scholar]
  5. Shapiro AM, Lakey JR, Ryan EA, Korbutt GS, Toth E. 5.  et al. 2000. Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N. Engl. J. Med. 343:230–38 [Google Scholar]
  6. Ryan EA, Paty BW, Senior PA, Bigam D, Alfadhli E. 6.  et al. 2005. Five-year follow-up after clinical islet transplantation. Diabetes 54:2060–69 [Google Scholar]
  7. Kroon E, Martinson LA, Kadoya K, Bang AG, Kelly OG. 7.  et al. 2008. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat. Biotechnol. 26:443–52 [Google Scholar]
  8. Zhang D, Jiang W, Liu M, Sui X, Yin X. 8.  et al. 2009. Highly efficient differentiation of human ES cells and iPS cells into mature pancreatic insulin-producing cells. Cell Res. 19:429–38 [Google Scholar]
  9. Weiner HL.9.  2009. The challenge of multiple sclerosis: How do we cure a chronic heterogeneous disease?. Ann. Neurol. 65:239–48 [Google Scholar]
  10. Hackstein H, Thomson AW. 10.  2004. Dendritic cells: emerging pharmacological targets of immunosuppressive drugs. Nat. Rev. Immunol. 4:24–34 [Google Scholar]
  11. Kobashigawa JA, Patel JK. 11.  2006. Immunosuppression for heart transplantation: Where are we now?. Nat. Clin. Pract. Cardiovasc. Med. 3:203–12 [Google Scholar]
  12. Van Gelder H, Charles-Schoeman C. 12.  2014. The heart in inflammatory myopathies. Rheum. Dis. Clin. N. Am. 40:1–10 [Google Scholar]
  13. Nikolich-Zugich J, Slifka MK, Messaoudi I. 13.  2004. The many important facets of T-cell repertoire diversity. Nat. Rev. Immunol. 4:123–32 [Google Scholar]
  14. Hafler DA, Slavik JM, Anderson DE, O'Connor KC, De Jager P, Baecher-Allan C. 14.  2005. Multiple sclerosis. Immunol. Rev. 204:208–31 [Google Scholar]
  15. Sulzberger MB.15.  1929. Experiments in prevention and in desensitization. Arch. Dermatol. Syphilol. 20:669–697 [Google Scholar]
  16. Chiller JM, Weigle WO. 16.  1971. Cellular events during induction of immunologic unresponsiveness in adult mice. J. Immunol. 106:1647–53 [Google Scholar]
  17. Burstein HJ, Shea CM, Abbas AK. 17.  1992. Aqueous antigens induce in vivo tolerance selectively in IL-2- and IFN-γ-producing (Th1) cells. J. Immunol. 148:3687–91 [Google Scholar]
  18. Critchfield JM, Racke MK, Zúñiga-Pflücker JC, Cannella B, Raine CS. 18.  et al. 1994. T cell deletion in high antigen dose therapy of autoimmune encephalomyelitis. Science 263:1139–43 [Google Scholar]
  19. Gaur A, Wiers B, Liu A, Rothbard J, Fathman CG. 19.  1992. Amelioration of autoimmune encephalomyelitis by myelin basic protein synthetic peptide–induced anergy. Science 258:1491–94 [Google Scholar]
  20. Racke MK, Critchfield JM, Quigley L, Cannella B, Raine CS. 20.  et al. 1996. Intravenous antigen administration as a therapy for autoimmune demyelinating disease. Ann. Neurol. 39:46–56 [Google Scholar]
  21. Smith CE, Eagar TN, Strominger JL, Miller SD. 21.  2005. Differential induction of IgE-mediated anaphylaxis after soluble versus cell-bound tolerogenic peptide therapy of autoimmune encephalomyelitis. PNAS 102:9595–600 [Google Scholar]
  22. Genain CP, Abel K, Belmar N, Villinger F, Rosenberg DP. 22.  et al. 1996. Late complications of immune deviation therapy in a nonhuman primate. Science 274:2054–57 [Google Scholar]
  23. Kontos S, Kourtis IC, Dane KY, Hubbell JA. 23.  2013. Engineering antigens for in situ erythrocyte binding induces T-cell deletion. PNAS 110:e60–68 [Google Scholar]
  24. Griffith TS, Ferguson TA. 24.  2011. Cell death in the maintenance and abrogation of tolerance: the five Ws of dying cells. Immunity 35:456–66 [Google Scholar]
  25. Nagata S, Hanayama R, Kawane K. 25.  2010. Autoimmunity and the clearance of dead cells. Cell 140:619–30 [Google Scholar]
  26. Getts DR, McCarthy DP, Miller SD. 26.  2013. Exploiting apoptosis for therapeutic tolerance induction. J. Immunol. 191:5341–46 [Google Scholar]
  27. Ferguson TA, Choi J, Green DR. 27.  2011. Armed response: how dying cells influence T-cell functions. Immunol. Rev. 241:77–88 [Google Scholar]
  28. Yamazaki S, Dudziak D, Heidkamp GF, Fiorese C, Bonito AJ. 28.  et al. 2008. CD8+ CD205+ splenic dendritic cells are specialized to induce Foxp3+ regulatory T cells. J. Immunol. 181:6923–33 [Google Scholar]
  29. Crispe IN.29.  2011. Liver antigen-presenting cells. J. Hepatol. 54:357–65 [Google Scholar]
  30. Dunham RM, Thapa M, Velazquez VM, Elrod EJ, Denning TL. 30.  et al. 2013. Hepatic stellate cells preferentially induce Foxp3+ regulatory T cells by production of retinoic acid. J. Immunol. 190:2009–16 [Google Scholar]
  31. Burghardt S, Erhardt A, Claass B, Huber S, Adler G. 31.  et al. 2013. Hepatocytes contribute to immune regulation in the liver by activation of the Notch signaling pathway in T cells. J. Immunol. 191:5574–82 [Google Scholar]
  32. Ichikawa S, Mucida D, Tyznik AJ, Kronenberg M, Cheroutre H. 32.  2011. Hepatic stellate cells function as regulatory bystanders. J. Immunol. 186:5549–55 [Google Scholar]
  33. Kasagi S, Zhang P, Che L, Abbatiello B, Maruyama T. 33.  et al. 2014. In vivo–generated antigen-specific regulatory T cells treat autoimmunity without compromising antibacterial immune response. Sci. Transl. Med. 6:241ra78 [Google Scholar]
  34. Wetzig R, Hanson DG, Miller SD, Claman HN. 34.  1979. Binding of ovalbumin to mouse spleen cells with and without carbodiimide. J. Immunol. Methods 28:361–68 [Google Scholar]
  35. Podojil JR, Miller SD. 35.  2009. Molecular mechanisms of T-cell receptor and costimulatory molecule ligation/blockade in autoimmune disease therapy. Immunol. Rev. 229:337–55 [Google Scholar]
  36. Prasad S, Xu D, Miller SD. 36.  2012. Tolerance strategies employing antigen-coupled apoptotic cells and carboxylated PLG nanoparticles for the treatment of type 1 diabetes. Rev. Diabet. Stud. 9:319–27 [Google Scholar]
  37. Turley DM, Miller SD. 37.  2007. Peripheral tolerance induction using ethylenecarbodiimide-fixed APCs uses both direct and indirect mechanisms of antigen presentation for prevention of experimental autoimmune encephalomyelitis. J. Immunol. 178:2212–20 [Google Scholar]
  38. Karpus WJ, Peterson JD, Miller SD. 38.  1994. Anergy in vivo: down-regulation of antigen-specific CD4+ Th1 but not Th2 cytokine responses. Int. Immunol. 6:721–30 [Google Scholar]
  39. Getts DR, Turley DM, Smith CE, Harp CT, McCarthy D. 39.  et al. 2011. Tolerance induced by apoptotic antigen-coupled leukocytes is induced by PD-L1+ and IL-10-producing splenic macrophages and maintained by T regulatory cells. J. Immunol. 187:2405–17 [Google Scholar]
  40. Vandenbark AA, Barnes D, Finn T, Bourdette DN, Whitham R. 40.  et al. 2000. Differential susceptibility of human Th1 versus Th2 cells to induction of anergy and apoptosis by ECDI/antigen-coupled antigen-presenting cells. Int. Immunol. 12:57–66 [Google Scholar]
  41. Vandenbark AA, Celnik B, Vainiene M, Miller SD, Offner H. 41.  1995. Myelin antigen-coupled splenocytes suppress experimental autoimmune encephalomyelitis in Lewis rats through a partially reversible anergy mechanism. J. Immunol. 155:5861–67 [Google Scholar]
  42. Lutterotti A, Yusef S, Sputtek A, Sturner K, Stellmann J-P. 42.  et al. 2013. Antigen-specific tolerance by autologous myelin peptide-coupled cells: a phase 1 trial in multiple sclerosis. Sci. Transl. Med. 5:188ra75 [Google Scholar]
  43. Getts DR, Martin AJ, McCarthy DP, Terry RL, Hunter ZH. 43.  et al. 2012. Microparticles bearing encephalitogenic peptides induce T-cell tolerance and ameliorate experimental autoimmune encephalomyelitis. Nat. Biotechnol. 30:1217–24 [Google Scholar]
  44. Jing J, Yang IV, Hui L, Patel JA, Evans CM. 44.  et al. 2013. Role of macrophage receptor with collagenous structure in innate immune tolerance. J. Immunol. 190:6360–67 [Google Scholar]
  45. Canton J, Neculai D, Grinstein S. 45.  2013. Scavenger receptors in homeostasis and immunity. Nat. Rev. Immunol. 13:621–34 [Google Scholar]
  46. Kanno S, Furuyama A, Hirano S. 46.  2007. A murine scavenger receptor MARCO recognizes polystyrene nanoparticles. Toxicol. Sci. 97:398–406 [Google Scholar]
  47. Hunter Z, McCarthy DP, Yap WT, Harp CT, Getts DR. 47.  et al. 2014. A biodegradable nanoparticle platform for the induction of antigen-specific immune tolerance for treatment of autoimmune disease. ACS Nano 8:2148–60 [Google Scholar]
  48. Getts DR, Terry RL, Getts MT, Deffrasnes C, Müller M. 48.  et al. 2014. Therapeutic inflammatory monocyte modulation using immune-modifying microparticles. Sci. Transl. Med. 6:219ra7 [Google Scholar]
  49. Maldonado RA, LaMothe RA, Ferrari JD, Zhang AH, Rossi RJ. 49.  et al. 2015. Polymeric synthetic nanoparticles for the induction of antigen-specific immunological tolerance. PNAS 112:e156–65 [Google Scholar]
  50. Yeste A, Nadeau M, Burns EJ, Weiner HL, Quintana FJ. 50.  2012. Nanoparticle-mediated codelivery of myelin antigen and a tolerogenic small molecule suppresses experimental autoimmune encephalomyelitis. PNAS 109:11270–75 [Google Scholar]
  51. Carambia A, Freund B, Schwinge D, Bruns OT, Salmen SC. 51.  et al. 2015. Nanoparticle-based autoantigen delivery to Treg-inducing liver sinusoidal endothelial cells enables control of autoimmunity in mice. J. Hepatol. 62:1349–56 [Google Scholar]
  52. Carambia A, Freund B, Schwinge D, Heine M, Laschtowitz A. 52.  et al. 2014. TGF-β-dependent induction of CD4+CD25+Foxp3+ Tregs by liver sinusoidal endothelial cells. J. Hepatol. 61:594–99 [Google Scholar]
  53. McHugh MD, Park J, Uhrich R, Gao W, Horwitz DA, Fahmy TM. 53.  2015. Paracrine co-delivery of TGF-β and IL-2 using CD4-targeted nanoparticles for induction and maintenance of regulatory T cells. Biomaterials 59:172–81 [Google Scholar]
  54. Jhunjhunwala S, Chen LC, Nichols EE, Thomson AW, Raimondi G, Little SR. 54.  2013. All-trans retinoic acid and rapamycin synergize with transforming growth factor β1 to induce regulatory T cells but confer different migratory capacities. J. Leukoc. Biol. 94:981–89 [Google Scholar]
  55. Pabst O, Mowat AM. 55.  2012. Oral tolerance to food protein. Mucosal Immunol. 5:232–39 [Google Scholar]
  56. Wells HG, Osborne TB. 56.  1911. The biological reactions of the vegetable proteins. I. Anaphylaxis. J. Infect. Dis. 8:66–124 [Google Scholar]
  57. Faria AMC, Weiner HL. 57.  2005. Oral tolerance. Immunol. Rev. 206:232–59 [Google Scholar]
  58. Mizrahi M, Ilan Y. 58.  2009. The gut mucosa as a site for induction of regulatory T cells. Curr. Pharm. Des. 15:1191–202 [Google Scholar]
  59. Brandtzaeg P, Kiyono H, Pabst R, Russell MW. 59.  2008. Terminology: nomenclature of mucosa-associated lymphoid tissue. Mucosal Immunol. 1:31–37 [Google Scholar]
  60. Bitar DM, Whitacre CC. 60.  1988. Suppression of experimental autoimmune encephalomyelitis by the oral administration of myelin basic protein. Cell Immunol. 112:364–70 [Google Scholar]
  61. Whitacre CC, Gienapp IE, Orosz CG, Bitar DM. 61.  1991. Oral tolerance in experimental autoimmune encephalomyelitis. III. Evidence for clonal anergy. J. Immunol. 147:2155–63 [Google Scholar]
  62. Khoury SJ, Hancock WW, Weiner HL. 62.  1992. Oral tolerance to myelin basic protein and natural recovery from experimental autoimmune encephalomyelitis are associated with downregulation of inflammatory cytokines and differential upregulation of transforming growth factor β, interleukin 4, and prostaglandin E expression in the brain. J. Exp. Med. 176:1355–64 [Google Scholar]
  63. Chen Y, Kuchroo VK, Inobe J, Hafler DA, Weiner HL. 63.  1994. Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science 265:1237–40 [Google Scholar]
  64. Miller A, Lider O, Roberts AB, Sporn MB, Weiner HL. 64.  1992. Suppressor T cells generated by oral tolerization to myelin basic protein suppress both in vitro and in vivo immune responses by the release of transforming growth factor β after antigen-specific triggering. PNAS 89:421–25 [Google Scholar]
  65. Kennedy KJ, Smith WS, Miller SD, Karpus WJ. 65.  1997. Induction of antigen-specific tolerance for the treatment of ongoing, relapsing autoimmune encephalomyelitis: a comparison between oral and peripheral tolerance. J. Immunol. 159:1036–44 [Google Scholar]
  66. Slavin AJ, Maron R, Weiner HL. 66.  2001. Mucosal administration of IL-10 enhances oral tolerance in autoimmune encephalomyelitis and diabetes. Int. Immunol. 13:825–33 [Google Scholar]
  67. Azizi A, Kumar A, Diaz-Mitoma F, Mestecky J. 67.  2010. Enhancing oral vaccine potency by targeting intestinal M cells. PLOS Pathog. 6:e1001147 [Google Scholar]
  68. des Rieux A, Fievez V, Garinot M, Schneider YJ, Preat V. 68.  2006. Nanoparticles as potential oral delivery systems of proteins and vaccines: a mechanistic approach. J. Control. Release 116:1–27 [Google Scholar]
  69. Kohli N, Westerveld DR, Ayache AC, Verma A, Shil P. 69.  et al. 2014. Oral delivery of bioencapsulated proteins across blood–brain and blood–retinal barriers. Mol. Ther. 22:535–46 [Google Scholar]
  70. Lee WK, Park JY, Jung S, Yang CW, Kim WU. 70.  et al. 2005. Preparation and characterization of biodegradable nanoparticles entrapping immunodominant peptide conjugated with PEG for oral tolerance induction. J. Control. Release 105:77–88 [Google Scholar]
  71. Kwon KC, Nityanandam R, New JS, Daniell H. 71.  2013. Oral delivery of bioencapsulated exendin-4 expressed in chloroplasts lowers blood glucose level in mice and stimulates insulin secretion in β-TC6 cells. Plant Biotechnol. J. 11:77–86 [Google Scholar]
  72. Su J, Zhu L, Sherman A, Wang X, Lin S. 72.  et al. 2015. Low cost industrial production of coagulation factor IX bioencapsulated in lettuce cells for oral tolerance induction in hemophilia B. Biomaterials 70:84–93 [Google Scholar]
  73. Ma S, Huang Y, Yin Z, Menassa R, Brandle JE, Jevnikar AM. 73.  2004. Induction of oral tolerance to prevent diabetes with transgenic plants requires glutamic acid decarboxylase (GAD) and IL-4. PNAS 101:5680–85 [Google Scholar]
  74. Bowman K, Sarkar R, Raut S, Leong KW. 74.  2008. Gene transfer to hemophilia A mice via oral delivery of FVIII-chitosan nanoparticles. J. Control. Release 132:252–59 [Google Scholar]
  75. Goldmann K, Ensminger SM, Spriewald BM. 75.  2012. Oral gene application using chitosan–DNA nanoparticles induces transferable tolerance. Clin. Vaccine Immunol. 19:1758–64 [Google Scholar]
  76. Merad M, Ginhoux F, Collin M. 76.  2008. Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat. Rev. Immunol. 8:935–47 [Google Scholar]
  77. Apostolou I, von Boehmer H. 77.  2004. In vivo instruction of suppressor commitment in naive T cells. J. Exp. Med. 199:1401–8 [Google Scholar]
  78. Ganguly D, Haak S, Sisirak V, Reizis B. 78.  2013. The role of dendritic cells in autoimmunity. Nat. Rev. Immunol. 13:566–77 [Google Scholar]
  79. Szczepanik M.79.  2014. Skin-induced tolerance as a new needle free therapeutic strategy. Pharmacol. Rep. 66:192–97 [Google Scholar]
  80. Ma W, Chen M, Kaushal S, McElroy M, Zhang Y. 80.  et al. 2012. PLGA nanoparticle–mediated delivery of tumor antigenic peptides elicits effective immune responses. Int. J. Nanomedicine 7:1475–87 [Google Scholar]
  81. Manolova V, Flace A, Bauer M, Schwarz K, Saudan P, Bachmann MF. 81.  2008. Nanoparticles target distinct dendritic cell populations according to their size. Eur. J. Immunol. 38:1404–13 [Google Scholar]
  82. Zhan X, Tran KK, Shen H. 82.  2012. Effect of the poly(ethylene glycol) (PEG) density on the access and uptake of particles by antigen-presenting cells (APCs) after subcutaneous administration. Mol. Pharm. 9:3442–51 [Google Scholar]
  83. Ludvigsson J, Faresjö M, Hjorth M, Axelsson S, Chéramy M. 83.  et al. 2008. GAD treatment and insulin secretion in recent-onset type 1 diabetes. N. Engl. J. Med. 359:1909–20 [Google Scholar]
  84. Ludvigsson J, Krisky D, Casas R, Battelino T, Castano L. 84.  et al. 2012. GAD65 antigen therapy in recently diagnosed type 1 diabetes mellitus. N. Engl. J. Med. 366:433–42 [Google Scholar]
  85. Daniel C, Weigmann B, Bronson R, von Boehmer H. 85.  2011. Prevention of type 1 diabetes in mice by tolerogenic vaccination with a strong agonist insulin mimetope. J. Exp. Med. 208:1501–10 [Google Scholar]
  86. Northrup L, Sestak JO, Sullivan BP, Thati S, Hartwell BL. 86.  et al. 2014. Co-delivery of autoantigen and B7 pathway modulators suppresses experimental autoimmune encephalomyelitis. AAPS J. 16:1204–13 [Google Scholar]
  87. Idoyaga J, Fiorese C, Zbytnuik L, Lubkin A, Miller J. 87.  et al. 2013. Specialized role of migratory dendritic cells in peripheral tolerance induction. J. Clin. Investig. 123:844–54 [Google Scholar]
  88. Clatworthy MR, Aronin CE, Mathews RJ, Morgan NY, Smith KG, Germain RN. 88.  2014. Immune complexes stimulate CCR7-dependent dendritic cell migration to lymph nodes. Nat. Med. 20:1458–63 [Google Scholar]
  89. Lund AW, Duraes FV, Hirosue S, Raghavan VR, Nembrini C. 89.  et al. 2012. VEGF-C promotes immune tolerance in B16 melanomas and cross-presentation of tumor antigen by lymph node lymphatics. Cell Rep. 1:191–99 [Google Scholar]
  90. Cohen JN, Guidi CJ, Tewalt EF, Qiao H, Rouhani SJ. 90.  et al. 2010. Lymph node–resident lymphatic endothelial cells mediate peripheral tolerance via Aire-independent direct antigen presentation. J. Exp. Med. 207:681–88 [Google Scholar]
  91. Waithman J, Allan RS, Kosaka H, Azukizawa H, Shortman K. 91.  et al. 2007. Skin-derived dendritic cells can mediate deletional tolerance of class I–restricted self-reactive T cells. J. Immunol. 179:4535–41 [Google Scholar]
  92. Engman C, Wen Y, Meng WS, Bottino R, Trucco M, Giannoukakis N. 92.  2015. Generation of antigen-specific Foxp3+ regulatory T-cells in vivo following administration of diabetes-reversing tolerogenic microspheres does not require provision of antigen in the formulation. Clin. Immunol. 160:103–23 [Google Scholar]
  93. Cappellano G, Woldetsadik AD, Orilieri E, Shivakumar Y, Rizzi M. 93.  et al. 2014. Subcutaneous inverse vaccination with PLGA particles loaded with a MOG peptide and IL-10 decreases the severity of experimental autoimmune encephalomyelitis. Vaccine 32:5681–89 [Google Scholar]
  94. Lewis JS, Dolgova NV, Zhang Y, Xia CQ, Wasserfall CH. 94.  et al. 2015. A combination dual-sized microparticle system modulates dendritic cells and prevents type 1 diabetes in prediabetic NOD mice. Clin. Immunol. 160:90–102 [Google Scholar]
  95. Yoon YM, Lewis JS, Carstens MR, Campbell-Thompson M, Wasserfall CH. 95.  et al. 2015. A combination hydrogel microparticle–based vaccine prevents type 1 diabetes in non-obese diabetic mice. Sci. Rep. 5:13155 [Google Scholar]
  96. Glowacki AJ, Gottardi R, Yoshizawa S, Cavalla F, Garlet GP. 96.  et al. 2015. Strategies to direct the enrichment, expansion, and recruitment of regulatory cells for the treatment of disease. Ann. Biomed. Eng. 43:593–602 [Google Scholar]
  97. Alegre ML, Florquin S, Goldman M. 97.  2007. Cellular mechanisms underlying acute graft rejection: time for reassessment. Curr. Opin. Immunol. 19:563–68 [Google Scholar]
  98. Mellor AL, Munn DH. 98.  2008. Creating immune privilege: active local suppression that benefits friends, but protects foes. Nat. Rev. Immunol. 8:74–80 [Google Scholar]
  99. Glotz D, Tambur A. 99.  2015. Stratifying patients based on epitope mismatching: ready for primetime?. Am. J. Transplant. 15:2021–22 [Google Scholar]
  100. Spierings E.100.  2014. Minor histocompatibility antigens: past, present, and future. Tissue Antigens 84:374–60 [Google Scholar]
  101. Cobbold S, Waldmann H. 101.  1998. Infectious tolerance. Curr. Opin. Immunol. 10:518–24 [Google Scholar]
  102. Yuan X, Paez-Cortez J, Schmitt-Knosalla I, D'Addio F, Mfarrej B. 102.  et al. 2008. A novel role of CD4 Th17 cells in mediating cardiac allograft rejection and vasculopathy. J. Exp. Med. 205:3133–44 [Google Scholar]
  103. Jordan SC, Choi J, Vo A. 103.  2015. Achieving incompatible transplantation through desensitization: current perspectives and future directions. Immunotherapy 7:377–98 [Google Scholar]
  104. Poggio ED, Clemente M, Hricik DE, Heeger PS. 104.  2006. Panel of reactive T cells as a measurement of primed cellular alloimmunity in kidney transplant candidates. J. Am. Soc. Nephrol. 17:564–72 [Google Scholar]
  105. Lúcia M, Luque S, Crespo E, Melilli E, Cruzado JM. 105.  et al. 2015. Preformed circulating HLA-specific memory B cells predict high risk of humoral rejection in kidney transplantation. Kidney Int. 88:874–87 [Google Scholar]
  106. Scandling JD, Busque S, Dejbakhsh-Jones S, Benike C, Millan MT. 106.  et al. 2008. Tolerance and chimerism after renal and hematopoietic-cell transplantation. N. Engl. J. Med. 358:362–68 [Google Scholar]
  107. Kawai T, Cosimi AB, Spitzer TR, Tolkoff-Rubin N, Suthanthiran M. 107.  et al. 2008. HLA-mismatched renal transplantation without maintenance immunosuppression. N. Engl. J. Med. 358:353–61 [Google Scholar]
  108. Leventhal J, Abecassis M, Miller J, Gallon L, Ravindra K. 108.  et al. 2012. Chimerism and tolerance without GVHD or engraftment syndrome in HLA-mismatched combined kidney and hematopoietic stem cell transplantation. Sci. Transl. Med. 4:124ra28 [Google Scholar]
  109. Leventhal J, Abecassis M, Miller J, Gallon L, Tollerud D. 109.  et al. 2013. Tolerance induction in HLA disparate living donor kidney transplantation by donor stem cell infusion: Durable chimerism predicts outcome. Transplantation 95:169–76 [Google Scholar]
  110. Leventhal JR, Mathew JM, Salomon DR, Kurian SM, Suthanthiran M. 110.  et al. 2013. Genomic biomarkers correlate with HLA-identical renal transplant tolerance. J. Am. Soc. Nephrol. 24:1376–85 [Google Scholar]
  111. Talawila N, Pengel LH. 111.  2015. Does belatacept improve outcomes for kidney transplant recipients? A systematic review. Transpl. Int. 28:1251–64 [Google Scholar]
  112. Li XL, Menoret S, Le Mauff B, Angin M, Anegon I. 112.  2008. Promises and obstacles for the blockade of CD40–CD40L interactions in allotransplantation. Transplantation 86:10–15 [Google Scholar]
  113. Luo X, Tarbell KV, Yang H, Pothoven K, Bailey SL. 113.  et al. 2007. Dendritic cells with TGF-β1 differentiate naive CD4+CD25 T cells into islet-protective Foxp3+ regulatory T cells. PNAS 104:2821–26 [Google Scholar]
  114. Pothoven KL, Kheradmand T, Yang Q, Houlihan JL, Zhang H. 114.  et al. 2010. Rapamycin-conditioned donor dendritic cells differentiate CD4CD25Foxp3 T cells in vitro with TGF-β1 for islet transplantation. Am. J. Transplant. 10:1774–84 [Google Scholar]
  115. Wood KJ, Sakaguchi S. 115.  2003. Regulatory T cells in transplantation tolerance. Nat. Rev. Immunol. 3:199–210 [Google Scholar]
  116. Juvet SC, Whatcott AG, Bushell AR, Wood KJ. 116.  2014. Harnessing regulatory T cells for clinical use in transplantation: the end of the beginning. Am. J. Transplant. 14:750–63 [Google Scholar]
  117. Tan J, Wu W, Xu X, Liao L, Zheng F. 117.  et al. 2012. Induction therapy with autologous mesenchymal stem cells in living-related kidney transplants: a randomized controlled trial. JAMA 307:1169–77 [Google Scholar]
  118. Luan Y, Mosheir E, Menon MC, Wilson D, Woytovich C. 118.  et al. 2013. Monocytic myeloid-derived suppressor cells accumulate in renal transplant patients and mediate CD4+ Foxp3+ Treg expansion. Am. J. Transplant. 13:3123–31 [Google Scholar]
  119. Ochando J, Conde P, Bronte V. 119.  2015. Monocyte-derived suppressor cells in transplantation. Curr. Transplant. Rep. 2:176–83 [Google Scholar]
  120. Conde P, Rodriguez M, van der Touw W, Jimenez A, Burns M. 120.  et al. 2015. Immunity 421143–58 [Google Scholar]
  121. Bryant J, Lerret NM, Wang JJ, Kang HK, Tasch J. 121.  et al. 2014. Preemptive donor apoptotic cell infusions induce IFN-γ-producing myeloid-derived suppressor cells for cardiac allograft protection. J. Immunol. 192:6092–101 [Google Scholar]
  122. Gibly RF, Graham JG, Luo X, Lowe WL Jr, Hering BJ, Shea LD. 122.  2011. Advancing islet transplantation: from engraftment to the immune response. Diabetologia 54:2494–505 [Google Scholar]
  123. Forrester JV, Xu H, Lambe T, Cornall R. 123.  2008. Immune privilege or privileged immunity?. Mucosal Immunol. 1:372–81 [Google Scholar]
  124. Dumont CM, Park J, Shea LD. 124.  2015. Controlled release strategies for modulating immune responses to promote tissue regeneration. J. Control. Release 219:155–56 [Google Scholar]
  125. Hlavaty KA, Gibly RF, Zhang X, Rives CB, Graham JG. 125.  et al. 2014. Enhancing human islet transplantation by localized release of trophic factors from PLG scaffolds. Am. J. Transplant. 14:1523–32 [Google Scholar]
  126. Liu JMH, Zhang J, Zhang X, Hlavaty KA, Ricci CF. 126.  et al. 2015. Transforming growth factor β1 delivery from microporous scaffolds decreases inflammation post-implant and enhances function of transplanted islets. Biomaterials 80:11–19 [Google Scholar]
  127. Chen T, Yuan J, Duncanson S, Hibert ML, Kodish BC. 127.  et al. 2015. Alginate encapsulant incorporating CXCL12 supports long-term allo- and xenoislet transplantation without systemic immune suppression. Am. J. Transplant. 15:618–27 [Google Scholar]
  128. Bischoff L, Alvarez S, Dai DL, Soukhatcheva G, Orban PC, Verchere CB. 128.  2015. Cellular mechanisms of CCL22-mediated attenuation of autoimmune diabetes. J. Immunol. 194:3054–64 [Google Scholar]
  129. Graham JG, Zhang X, Goodman A, Pothoven K, Houlihan J. 129.  et al. 2013. PLG scaffold delivered antigen-specific regulatory T cells induce systemic tolerance in autoimmune diabetes. Tissue Eng. A 19:1465–75 [Google Scholar]
  130. Lau HT, Yu M, Fontana A, Stoeckert CJ Jr. 130.  1996. Prevention of islet allograft rejection with engineered myoblasts expressing FasL in mice. Science 273:109–12 [Google Scholar]
  131. Pearl-Yafe M, Kaminitz A, Yolcu ES, Yaniv I, Stein J, Askenasy N. 131.  2007. Pancreatic islets under attack: cellular and molecular effectors. Curr. Pharm. Des. 13:749–60 [Google Scholar]
  132. Plenter RJ, Grazia TJ, Nelson DP, Zamora MR, Gill RG, Pietra BA. 132.  2015. Ectopic expression of Fas ligand on cardiomyocytes renders cardiac allografts resistant to CD4+ T-cell mediated rejection. Cell Immunol. 293:30–33 [Google Scholar]
  133. Yolcu ES, Zhao H, Bandura-Morgan L, Lacelle C, Woodward KB. 133.  et al. 2011. Pancreatic islets engineered with SA-FasL protein establish robust localized tolerance by inducing regulatory T cells in mice. J. Immunol. 187:5901–9 [Google Scholar]
  134. Hume PS, Anseth KS. 134.  2010. Inducing local T cell apoptosis with anti-Fas-functionalized polymeric coatings fabricated via surface-initiated photopolymerizations. Biomaterials 31:3166–74 [Google Scholar]
  135. Chen JJ, Sun Y, Nabel GJ. 135.  1998. Regulation of the proinflammatory effects of Fas ligand (CD95L). Science 282:1714–17 [Google Scholar]
  136. Yolcu ES, Askenasy N, Singh NP, Cherradi SE, Shirwan H. 136.  2002. Cell membrane modification for rapid display of proteins as a novel means of immunomodulation: FasL-decorated cells prevent islet graft rejection. Immunity 17:795–808 [Google Scholar]
  137. Luo X, Pothoven KL, McCarthy D, DeGutes M, Martin A. 137.  et al. 2008. ECDI-fixed allogeneic splenocytes induce donor-specific tolerance for long-term survival of islet transplants via two distinct mechanisms. PNAS 105:14527–32 [Google Scholar]
  138. Wang S, Tasch J, Kheradmand T, Ulaszek J, Ely S. 138.  et al. 2013. Transient B-cell depletion combined with apoptotic donor splenocytes induces xeno-specific T- and B-cell tolerance to islet xenografts. Diabetes 62:3143–50 [Google Scholar]
  139. Luo X, Pothoven KL, McCarthy D, DeGutes M, Martin A. 139.  et al. 2008. ECDI-fixed allogeneic splenocytes induce donor-specific tolerance for long-term survival of islet transplants via two distinct mechanisms. PNAS 105:14527–32 [Google Scholar]
  140. Wang S, Zhang X, Zhang L, Bryant J, Kheradmand T. 140.  et al. 2014. Preemptive tolerogenic delivery of donor antigens for permanent allogeneic islet graft protection. Cell Transplant 24:1155–65 [Google Scholar]
  141. Eagar TN, Karandikar NJ, Bluestone J, Miller SD. 141.  2002. The role of CTLA-4 in induction and maintenance of peripheral T cell tolerance. Eur. J. Immnol. 32:972–81 [Google Scholar]
  142. Tanaka K, Albin MJ, Yuan X, Yamaura K, Habicht A. 142.  et al. 2007. PDL1 is required for peripheral transplantation tolerance and protection from chronic allograft rejection. J. Immunol. 179:5204–10 [Google Scholar]
  143. Kheradmand T, Wang S, Bryant J, Tasch JJ, Lerret N. 143.  et al. 2012. Ethylenecarbodiimide-fixed donor splenocyte infusions differentially target direct and indirect pathways of allorecognition for induction of transplant tolerance. J. Immunol. 189:804–12 [Google Scholar]
  144. Wells AD, Li XC, Li Y, Walsh MC, Zheng XX. 144.  et al. 1999. Requirement for T-cell apoptosis in the induction of peripheral transplantation tolerance. Nat. Med. 5:1303–7 [Google Scholar]
  145. Chen G, Kheradmand T, Bryant J, Wang S, Tasch J. 145.  et al. 2012. Intragraft CD11b+IDO+ cells mediate cardiac allograft tolerance by ECDI-fixed donor splenocyte infusions. Am. J. Transplant. 12:2920–29 [Google Scholar]
  146. Bryant J, Hlavaty KA, Zhang X, Yap WT, Zhang L. 146.  et al. 2014. Nanoparticle delivery of donor antigens for transplant tolerance in allogeneic islet transplantation. Biomaterials 35:8887–94 [Google Scholar]
  147. Iyoda T, Shimoyama S, Liu K, Omatsu Y, Akiyama Y. 147.  et al. 2002. The CD8+ dendritic cell subset selectively endocytoses dying cells in culture and in vivo. J. Exp. Med. 195:1289–302 [Google Scholar]
  148. Huang L, Lemos HP, Li L, Li M, Chandler PR. 148.  et al. 2012. Engineering DNA nanoparticles as immunomodulatory reagents that activate regulatory T cells. J. Immunol. 188:4913–20 [Google Scholar]
  149. Peterson JC, Nordstrom RJ, Long RK. 149.  1976. Subtle source of contamination in spectrophones. Appl. Opt. 15:2974–76 [Google Scholar]
  150. Bandyopadhyay A, Fine RL, Demento S, Bockenstedt LK, Fahmy TM. 150.  2011. The impact of nanoparticle ligand density on dendritic-cell targeted vaccines. Biomaterials 32:3094–105 [Google Scholar]
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