Pathways of major histocompatibility complex allorecognition

Current Opinion in Organ Transplantation

Volumn 13, Issue 4, 2008, Pages 438-444

  Afzali, Behdad ^a   Lombardi, Giovanna ^a   Lechler, Robert I ^a,b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Allorecognition; Direct; Human; Indirect; Mouse; Regulatory T cells; Semi direct; Transplantation

Indexed keywords

ALLOANTIGEN;

ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; CELL FUNCTION; GRAFT REJECTION; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MEDICAL RESEARCH; NONHUMAN; ORGAN TRANSPLANTATION; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE;

ANIMALS; ANTIGEN PRESENTATION; GRAFT REJECTION; GRAFT SURVIVAL; HUMANS; IMMUNE TOLERANCE; ISOANTIGENS; MAJOR HISTOCOMPATIBILITY COMPLEX; ORGAN TRANSPLANTATION; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION, HOMOLOGOUS;

EID: 67649983265     PISSN: 10872418     EISSN: 15317013     Source Type: Journal    
DOI: 10.1097/MOT.0b013e328309ee31     Document Type: Review

References (85)

1. Afzali B, Lechler RI, Hernandez-Fuentes MP. Allorecognition and the alloresponse: clinical implications. Tissue Antigens 2007; 69:545-556.
2. Warrens AN, Lombardi G, Lechler RI. Presentation and recognition of major and minor histocompatibility antigens. Transpl Immunol 1994; 2:103-107.
3. Lechler RI, Batchelor JR. Restoration of immunogenicity to passenger celldepleted kidney allografts by the addition of donor strain dendritic cells. J Exp Med 1982; 155:31-41.
4. Herrera OB, Golshayan D, Tibbott R, et al. A novel pathway of alloantigen presentation by dendritic cells. J Immunol 2004; 173:4828-4837.
5. Whitelegg AM, Oosten LE, Jordan S, et al. Investigation of peptide involvement in T cell allorecognition using recombinant HLA class I multimers. J Immunol 2005; 175:1706-1714.
6. Lindahl KF, Wilson DB. Histocompatibility antigen-activated cytotoxic T lymphocytes. II. Estimates of the frequency and specificity of precursors. J Exp Med 1977; 145:508-522.
7. Ford D, Burger D. Precursor frequency of antigen-specific T cells: effects of sensitization in vivo and in vitro. Cell Immunol 1983; 79:334-344.
8. Pietra BA, Wiseman A, Bolwerk A, et al. CD4 T cell-mediated cardiac allograft rejection requires donor but not host MHC class II. J Clin Invest 2000; 106: 1003-1010.
9. Sandner SE, Salama AD, Houser SL, et al. New TCR transgenic model for tracking allospecific CD4 T-cell activation and tolerance in vivo. Am J Transplant 2003; 3:1242-1250.
10. Larsen CP, Steinman RM, Witmer-Pack M, et al. Migration and maturation of Langerhans cells in skin transplants and explants. J Exp Med 1990; 172: 1483-1493.
11. Lakkis FG, Arakelov A, Konieczny BT, Inoue Y. Immunologic 'ignorance' of vascularized organ transplants in the absence of secondary lymphoid tissue. Nat Med 2000; 6:686-688.
12. Zinkernagel RM, Doherty PC. Restriction of in vitro T cell-mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system. Nature 1974; 248:701-702.
13. Baker RJ, Hernandez-Fuentes MP, Brookes PA, et al. The role of the allograft in the induction of donor-specific T cell hyporesponsiveness. Transplantation 2001; 72:480-485.
14. Suchin EJ, Langmuir PB, Palmer E, et al. Quantifying the frequency of alloreactive T cells in vivo: new answers to an old question. J Immunol 2001; 166:973-981.
15. Lombardi G, Sidhu S, Batchelor JR, Lechler RI. Allorecognition of DR1 by T cells from a DR4/DRw13 responder mimics self-restricted recognition of endogenous peptides. Proc Natl Acad Sci U S A 1989; 86:4190-4194.
16. Malissen M, Trucy J, Letourneur F, et al. A T cell clone expresses two T cell receptor alpha genes but uses one alpha beta heterodimer for allorecognition and self MHC-restricted antigen recognition. Cell 1988; 55:49-59.
17. Archbold JK, Macdonald WA, Miles JJ, et al. Alloreactivity between disparate cognate and allogeneic pMHC-I complexes is the result of highly focused, peptide-dependentstructural mimicry.JBiol Chem2006;281:34324-34332.
18. Shoskes DA, Wood KJ. Indirect presentation of MHC antigens in transplantation. Immunol Today 1994; 15:32-38.
19. Taylor AL, Negus SL, Negus M, et al. Pathways of helper CD4 T cell allorecognition in generating alloantibody and CD8 T cell alloimmunity. Transplantation 2007; 83:931-937.
20. Steele DJ, Laufer TM, Smiley ST, et al. Two levels of help for B cell alloantibody production. J Exp Med 1996; 183:699-703.
21. Inaba K, Turley S, Yamaide F, et al. Efficient presentation of phagocytosed cellular fragments on the major histocompatibility complex class II products of dendritic cells. J Exp Med 1998; 188:2163-2173.
22. Auchincloss H Jr, Lee R, Shea S, et al. The role of 'indirect' recognition in initiating rejection of skin grafts from major histocompatibility complex class II-deficient mice. Proc Natl Acad Sci U S A 1993; 90:3373-3377.
23. Fangmann J, Dalchau R, Fabre JW. Rejection of skin allografts by indirect allorecognition of donor class I major histocompatibility complex peptides. J Exp Med 1992; 175:1521-1529.
24. Sayegh MH, Perico N, Imberti O, et al. Thymic recognition of class II major histocompatibility complex allopeptides induces donor-specific unresponsiveness to renal allografts. Transplantation 1993; 56:461-465.
25. Tugulea S, Ciubotariu R, Colovai AI, et al. New strategies for early diagnosis of heart allograft rejection. Transplantation 1997; 64:842-847.
26. Liu Z, Braunstein NS, Suciu-Foca N. T cell recognition of allopeptides in context of syngeneic MHC. J Immunol 1992; 148:35-40.
27. Liu Z, Colovai AI, Tugulea S, et al. Indirect recognition of donor HLA-DR peptides in organ allograft rejection. J Clin Invest 1996; 98:1150-1157.
28. Dalchau R, Fangmann J, Fabre JW. Allorecognition of isolated, denatured chains of class I and class II major histocompatibility complex molecules. Evidence for an important role for indirect allorecognition in transplantation. Eur J Immunol 1992; 22:669-677.
29. Vella JP, Spadafora-Ferreira M, Murphy B, et al. Indirect allorecognition of major histocompatibility complex allopeptides in human renal transplant recipients with chronic graft dysfunction. Transplantation 1997; 64:795-800.
30. Benichou G, Valujskikh A, Heeger PS. Contributions of direct and indirect T cell alloreactivity during allograft rejection in mice. J Immunol 1999; 162: 352-358.
31. Mason PD, Robinson CM, Lechler RI. Detection of donor-specific hypore-sponsiveness following late failure of human renal allografts. Kidney Int 1996; 50:1019-1025.
32. HornickPI, Mason PD, Yacoub MH, et al. Assessment of the contribution that direct allorecognition makes to the progression of chronic cardiac transplant rejection in humans. Circulation 1998; 97:1257-1263.
33. Hornick PI, Mason PD, Baker RJ, et al. Significant frequencies of T cells with indirect antidonor specificity in heart graft recipients with chronic rejection. Circulation 2000; 101:2405-2410.
34. Frasca L, Amendola A, Hornick P, et al. Role of donor and recipient antigen-presenting cells in priming and maintaining T cells with indirect allospecificity. Transplantation 1998; 66:1238-1243.
35. Ridge JP, Di RF, Matzinger P. A conditioned dendritic cell can be a temporal bridge between aCD4+T-helper and a T-killer cell. Nature 1998; 393:474-478.
36. LeeRS, Grusby MJ,GlimcherLH, et al. Indirect recognition by helper cells can induce donor-specific cytotoxic T lymphocytes in vivo. J Exp Med 1994; 179:865-872.
37. Wise MP, Bemelman F, Cobbold SP, Waldmann H. Linked suppression of skin graft rejection can operate through indirect recognition. J Immunol 1998; 161:5813-5816.
38. Smyth LA, Afzali B, Tsang J, et al. Intercellular transfer of MHC and immunological molecules: molecular mechanisms and biological significance. Am J Transplant 2007; 7:1442-1449.
39. Bedford P, Garner K, Knight SC. MHC class II molecules transferred between allogeneic dendritic cells stimulate primary mixed leukocyte reactions. Int Immunol 1999; 11:1739-1744.
40. Smyth LA, Herrera OB, Golshayan D, et al. A novel pathway of antigen presentation by dendritic and endothelial cells: implications for allorecognition and infectious diseases. Transplantation 2006; 82:S15-S18.
41. Game DS, Rogers NJ, Lechler RI. Acquisition of HLA-DR and costimulatory molecules by T cells from allogeneic antigen presenting cells. Am J Transplant 2005; 5:1614-1625.
42. Harshyne LA, Watkins SC, Gambotto A, Barratt-Boyes SM. Dendritic cells acquire antigens from live cells for cross-presentation to CTL. J Immunol 2001; 166:3717-3723.
43. Morelli AE, LarreginaAT, Shufesky WJ, et al. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood 2004; 104:3257-3266.
44. Denzer K, van EM, Kleijmeer MJ, et al. Follicular dendritic cells carry MHC class II-expressing microvesicles at their surface. J Immunol 2000; 165: 1259-1265.
45. Pimenta-Araujo R, Mascarell L, Huesca M, et al. Embryonic thymic epithelium naturally devoid of APCs is acutely rejected in the absence of indirect recognition. J Immunol 2001; 167:5034-5041.
46. Mandelbrot DA, Kishimoto K, Auchincloss H Jr, et al. Rejection of mouse cardiac allografts by costimulation in trans. J Immunol 2001; 167:1174 -1178.
47. GraziaRoncarolo M, Gregori S, Battaglia M, et al. Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol Rev 2006; 212:28-50.
48. Weiner HL. Induction and mechanism of action of transforming growth factor-beta-secreting Th3 regulatory cells. Immunol Rev 2001; 182:207-214.
49. Lu L, Werneck MBF, Cantor H. The immunoregulatory effects of Qa-1. Immunol Rev 2006; 212:51 -59.
50. Cortesini R, LeMaoult J, Ciubotariu R, Cortesini NSF. CD8+CD28- T suppressor cells and the induction of antigen-specific, antigen-presenting cellmediated suppression of Th reactivity. Immunol Rev 2001; 182:201 -206.
51. Rifa'i M, Kawamoto Y, Nakashima I, Suzuki H. Essential roles of CD8+CD122+ regulatory T cells in the maintenance of T cell homeostasis. J Exp Med 2004; 200:1123-1134.
52. Zhang ZX, Yang L, Young KJ, et al. Identification of a previously unknown antigen-specific regulatory T cell and its mechanism of suppression. Nat Med 2000; 6:782-789.
53. Sakaguchi S, Sakaguchi N, Asano M, et al. 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. J Immunol 1995; 155:1151 -1164.
54. Sakaguchi S, Toda M, Asano M, et al.T cell-mediated maintenance of natural self-tolerance: its breakdown as a possible cause of various autoimmune diseases. J Autoimmun 1996; 9:211 -220.
55. Wildin RS, Ramsdell F, Peake J, et al. X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy. Nat Genet 2001; 27:18-20.
56. Wood KJ, Sakaguchi S. Regulatory T cells in transplantation tolerance. Nat Rev Immunol 2003; 3:199-210.
57. Graca L, Cobbold SP, Waldmann H. Identification of regulatory T cells in tolerated allografts. J Exp Med 2002; 195:1641 -1646.
58. Graca L, Thompson S, Lin CY, et al. Both CD4(+)CD25(+) and CD4(+)CD25(-) regulatory cells mediate dominant transplantation tolerance. J Immunol 2002; 168:5558-5565.
59. Hall BM, Pearce NW, Gurley KE, Dorsch SE. Specific unresponsiveness in rats with prolonged cardiac allograft survival after treatment with cyclosporine. III. Further characterization of the CD4+ suppressor cell and its mechanisms of action. J Exp Med 1990; 171:141 -157.
60. Jordan MS, Boesteanu A, Reed AJ, et al. Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat Immunol 2001; 2:301 -306.
61. Apostolou I, Sarukhan A, Klein L, von Boehmer H. Origin of regulatory T cells with known specificity for antigen. Nature Immunol 2002; 3:756-763.
62. Romagnoli P, Hudrisier D, van Meerwijk JP. Preferential recognition of self antigens despite normal thymic deletion of CD4(+)CD25(+) regulatory T cells. J Immunol 2002; 168:1644-1648.
63. HsiehCS, Liang Y,TyznikAJ,et al. Recognition of the peripheral self by naturally arising CD25+ CD4+ T cell receptors. Immunity 2004; 21:267-277.
64. Jiang S, Camara N, Lombardi G, Lechler RI. Induction of allopeptide-specific human CD4+CD25+regulatory T cells ex vivo. Blood 2003; 102:2180-2186.
65. Tafuri A, Alferink J, Moller P, et al. T cell awareness of paternal alloantigens during pregnancy. Science 1995; 270:630-633.
66. Hunt JS. Stranger in a strange land. Immunol Rev 2006; 213:36-47.
67. Aluvihare VR, Kallikourdis M, Betz AG. Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 2004; 5:266-271.
68. Nelson JL, Ostensen M. Pregnancy and rheumatoid arthritis. Rheum Dis Clin North Am 1997; 23:195-212.
69. Confavreux C, Hutchinson M, Hours MM, et al. Rate of pregnancy-related relapse in multiple sclerosis. Pregnancy in Multiple Sclerosis Group. N Engl J Med 1998; 339:285-291.
70. Sanchez-Fueyo A, Sandner S, Habicht A, et al. Specificity of CD4+CD25+ regulatory T cell function in alloimmunity. J Immunol 2006; 176:329-334.
71. Tang Q, Adams JY, Tooley AJ, et al. Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat Immunol 2006; 7:83-92.
72. Aramaki O, Shirasugi N, Akiyama Y, et al. Induction of operational tolerance and generation of regulatory cells after intratracheal delivery of alloantigen combined with nondepleting anti-CD4 monoclonal antibody. Transplantation 2003; 76:1305-1314.
73. Shirasugi N, IkedaY, Akiyama Y, et al. Induction of hyporesponsiveness to fully allogeneic cardiac grafts by intratracheal delivery of alloantigen. Transplantation 2001; 71:561 -564.
74. Chai JG, James E, Dewchand H, et al. Transplantation tolerance induced by intranasal administration of HY peptides. Blood 2004; 103:3951-3959.
75. Sayegh MH, Khoury SJ, Hancock WW, et al. Induction of immunity and oral tolerance with polymorphic class II major histocompatibility complex allopeptides in the rat. Proc Natl Acad Sci USA 1992; 89:7762-7766.
76. van MA, Herber M, Wood KJ, Jones ND. Cutting edge: CD4+CD25+ alloantigen-specific immunoregulatory cells that can prevent CD8+ T cellmediated graft rejection: implications for anti-CD154 immunotherapy. J Immunol 2002; 169:5401-5404.
77. Quezada SA, Fuller B, Jarvinen LZ, et al. Mechanisms of donor-specific transfusion tolerance: preemptive induction of clonal T-cell exhaustion via indirect presentation. Blood 2003; 102:1920-1926.
78. Yamada A, Chandraker A, LauferTM, et al. Recipient MHC class II expression is required to achieve long-term survival of murine cardiac allografts after costimulatory blockade. J Immunol 2001; 167:5522-5526.
79. Spadafora-Ferreira M, Caldas C, Fae KC, et al. CD4+CD25+Foxp3+ indirect alloreactive T cells from renal transplant patients suppress both the direct and indirect pathways of allorecognition. Scand J Immunol 2007; 66:352-361.
80. Sanchez-Fueyo A, Domenig CM, Mariat C, et al. Influence of direct and indirect allorecognition pathways on CD4+CD25+ regulatory T-cell function in transplantation. Transpl Int 2007; 20:534-541.
81. Karim M, Kingsley CI, Bushell AR, et al. Alloantigen-induced CD25+CD4+ regulatory T cells can develop in vivo from CD25-CD4+ precursors in a thymus-independent process. J Immunol 2004; 172:923-928.
82. Ochando JC, Homma C, Yang Y, et al. Alloantigen-presenting plasmacytoid dendritic cells mediate tolerance to vascularized grafts. Nat Immunol 2006; 7:652-662.
83. Game DS, Hernandez-Fuentes MP, Chaudhry AN, Lechler RI. CD4+CD25+ regulatory T cells do not significantly contribute to direct pathway hyporesponsiveness in stable renal transplant patients. J Am Soc Nephrol 2003; 14:1652-1661.
84. Salama AD, Najafian N, Clarkson MR, et al. Regulatory CD25+ T cells in human kidney transplant recipients. J Am Soc Nephrol 2003; 14:1643-1651.
85. Zheng XX, Sanchez-Fueyo A, Sho M, et al. Favorably tipping the balance between cytopathic and regulatory T cells to create transplantation tolerance. Immunity 2003; 19:503-514.