Endothelial cells as antigen-presenting cells: Role in human transplant rejection

Cellular and Molecular Life Sciences

Volumn 54, Issue 9, 1998, Pages 965-978

  Rose, M L ^a  

^a HAREFIELD HOSPITAL   (United Kingdom)

Author keywords

Antigen presentation; Endothelial cells; Rejection; Transplantation

Indexed keywords

B7 ANTIGEN; CD2 ANTIGEN; CD28 ANTIGEN; CYTOKINE; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 3; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ALLOIMMUNITY; ANTIBODY RESPONSE; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; BONE MARROW CELL; ENDOTHELIUM CELL; EPITHELIUM CELL; FIBROBLAST; GRAFT REJECTION; HUMAN; REVIEW; SMOOTH MUSCLE FIBER; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION;

ACUTE DISEASE; ANIMALS; ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; CELLS, CULTURED; CHRONIC DISEASE; CORONARY DISEASE; ENDOTHELIUM, VASCULAR; GRAFT REJECTION; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; ISOANTIGENS; LYMPHOCYTE ACTIVATION; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 0031705761     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s000180050226     Document Type: Review

References (122)

1. Steinmuller D. (1985) Which T cells mediate allograft rejection? Transplantation 40: 229-233
2. Ungureanu-Longrois D., Balligand J. L., Simmons W. W., Okada I., Kobzik L., Lowenstein C. J. et al. (1995) Induction of nitric oxide synthase activity by cytokines in ventricular myocytes is necessary but not sufficient to decrease contractile responses to beta-adrenergic agonists. Circ. Res. 77: 494-502
3. Matsumori A., Yamada T., Suzuki H., Matoba Y. and Sasayama S. (1994) Increased circulating cytokines in patients with myocarditis and cardiomyopathy. Br. Heart J. 72: 561-566
4. Lewis N. P., Tsao P. S., Rickenbacher P. R., Xue C., Johns R. A., Haywood G. A. et al. (1996) Induction of nitric oxide synthase in the human cardiac allograft is associated with contractile dysfunction of the left ventricle. Circulation 93: 720-729
5. Daar A. S., Fuggle S. V., Fabre J. W. and Morris P. J. (1984) The detailed distribution of MHC class II antigens in normal human organs. Transplantation 38: 292-297
6. Rose M. L., Coles M. I., Griffin R. J., Pomerance A. and Yacoub M. H. (1986) Expression of class I and class II major histocompatibilty antigens in normal and transplanted human heart. Transplantation 41: 776-780
7. Page C. S., Rose M. L., Piggott R. and Yacoub M. H. (1992) Heterogeneity of vascular ECs. Am. J. Pathol. 141: 673-683
8. Parker K. E., Dalchau R., Fowler V. J., Priestly C. A., Carter C. A. and Fabre J. W. (1992) Stimulation of CD4+ T lymphocytes by allogeneic MHC peptides presented on autologous antigen presenting cells. Transplantation 53: 918-924
9. Terness P., Dufter C., Otto G. and Opelz G. (1996) Allograft survival following immunisation with membrane bound or soluble peptide MHC class I donor antigens: factors relevant for the induction of rejection by indirect recognition. Transplant. Int. 9: 2-8
10. Liu Z., Colovai A. I., Tugulea S., Reed E. F., Fisher P. E., Mancini D. et al. (1996) Indirect recognition of donor HLA-DR peptides in organ allograft rejection. J. Clin. Invest. 98: 1150-1157
11. Pober J. S., Orosz C. G., Rose M. L. and Savage C. O. S. (1996) Can graft endothelial cells initiate a host anti-graft immune response? Transplantation 61: 343-349
12. Janeway C. A. J. and Bottomly K. (1994) Signals and signs for lymphocyte responses. Cell 57: 275-285
13. June C. H., Blustone J. A., Nadler L. M. and Thompson C. B. (1994) The B7 and CD28 receptor families. Immunol. Today 15: 321-331
14. Tan P., Anasetti C., Hansen J. A., Melrose J., Brunvand M., Bradshaw J. et al. (1993) Induction of alloantigen specific hyporesponsiveness in human T lymphocytes by blocking interaction of CD28 with its natural ligand B7/BB1. J. Exp. Med. 177: 165-173
15. Schwartz R. H. (1990) A cell culture model for T lymphocyte clonal anergy. Science 248: 1349-1356
16. Liu Y. and Janeway C. A. J. (1990) Interferon g plays a critical role in induced cell death of effector T cells: a possible third mechanism of self-tolerance. J. Exp. Med. 172: 1735-1739
17. Linsley P. S., Brady W., Urnes M., Grosmire L. S., Damle N. K., and Ledbetter J. A. (1991) CTLA-4 is a second receptor for the B cell activation antigen B7. J. Exp. Med. 147: 561-569
18. Turka L. A., Linsley P. S., Lin H., Brady W., Leiden J. M., Wei R. Q. et al. (1992) T cell activation by the CD28 ligand B7 is required for cardiac allograft rejection in vivo. Proc. Natl. Acad. Sci. USA 89: 11102-11105
19. Lin H., Bolling S. F., Linsley P. S., Wei R. Q., Gordon D., Thompson C. B. et al. (1993) Long-term acceptance of major histocompatibility complex mismatched cardiac allografts induced by CTLA4-Ig plus donor-specific transfusions. J. Exp. Med. 178: 1801-1806
20. Pearson T. C., Alexandre D. Z., Winn K. J., Linsley P. S., Lowry R. P. and Larsen C. P. (1994) Transplantation tolerance induced by CTLA4-Ig. Transplantation 57: 1701-1706
21. Lenschow D. J., Zeng Y., Thistlethwaite J., Montag A., Brady W., Gibson M. G. et al. (1992) Long term survival of xenogeneic pancreatic islet grafts induced by CTLA4-Ig. Science 257: 789-792
22. Fuggle S. V. (1989) MHC antigen expression in vascularised organ allografts: clinical correlations and significance. Transplant. Rev. 3: 81-102
23. So S. K. S., Platt J. L., Ascher N. L. and Snover D. C. (1987) Increased expression of class I major histocompatibilty complex antigens on hepatocytes in rejecting human liver allografts. Transplantation 43: 79-84
24. Fuggle S. V., Errasti P., Daar A. S., Fabre J. W., Ting A., Morris P. J. et al. (1983) Localisation of major histocompatibilty complex (HLA-ABC and DR) antigens in 46 kidneys: differences in HLA-DR staining of tubules among kidneys. Transplantation 35: 385-390
25. Milton A. D., Spencer S. C. and Fabre J. W. (1986) Detailed analysis and demonstration of differences in the kinetics of induction of class I and class II major histocompatibilty complex antigens in rejecting cardiac and kidney allografts in the rat. Transplantation 41: 499-508
26. Arbustini E., Grasso M., Diegoli M., Bramerio M., Foglieni A. S., Albertario M. et al. (1991) Expression of tumour necrosis factor in human acute cardiac rejection. An immunohistochemical and immunoblotting study. Am. J. Pathol. 139: 709-715
27. Cunningham D. A., Dunn M. J., Yacoub M. J. and Rose M. L. (1994) Local production of cytokines in the human cardiac allograft. Transplantation 57: 1333-1337
28. Gao S. J., Schroeder J. S., Alderman E. L., Hunt S. A., Valantine H. A. and Weiederhold V. (1989) Prevalence of accelerated coronary artery disease in heart transplant survivors. Comparison of cyclosporine and azathioprine regimens. Circulation 8: III100-105
29. Johnson J. A. and Kobashigawa J. A. (1995) Quantitative analysis of transplant coronary artery disease with use of intracoronary ultrasound. J. Heart Lung Transplant. 14: S198-202
30. Hosenpud J. D., Shipley G. D. and Wagner C. R. (1992) Cardiac allograft vasculopathy: current concepts, recent developments and future directions. J. Heart Lung Transplant. 11: 9-23
31. Ross R. (1993) The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362: 801-809
32. Barbir M., Banner N., Thompson G. R., Khaghani A., Mitchell A. and Yacoub M. H. (1991). Relationship of immunosuppression and serum lipids to the development of coronary arterial disease in the transplanted heart. Int. J. Cardiol. 32: 51-56
33. Barbir M., Kushwaha S., Hunt B., Mackin A., Thompson G. R., Mitchell A. et al. (1992) Lipoprotein (a) and accelerated coronary artery disease in cardiac transplant recipients. Lancet 340: 1500-1502
34. Kobashigawa J. A., Katznelson S., Laks H., Johnson J. A., Yeatman L., Wang X. M. et al. (1995) Effect of pravastatin on outcome after cardiac transplantation. N. Engl. J. Med. 333: 621-627
35. Gratten M. T., Moreno-Cabral C. E., Starnes V. A., Oyer P. B., Stinson E. B., Shumway N. E. et al. (1989) Cytomegalovirus is associated with cardiac allograft rejection and atherosclerosis. JAMA 261: 3561-3566
36. McDonald K., Rector T. S., Braunlin E. A., Kubo S. H. and Olivari M. T. (1989) Association of coronary artery disease in transplant recipients with cytomegalovirus infection. Am. J. Cardiol. 64: 359-362
37. Loebe M., Schiller S., Zaus O., Warnecke H., Flecke E. and Hetzer R. (1990) Role of cytomegalovirus in the development of coronary artery disease in the transplanted heart. J. Heart Lung Transplant. 9: 707-711
38. Everett J. P., Hershberger R. E., Norman D. J., Chou S., Ratkovec R. M., Cobanoglu A. et al. (1992) Prolonged cytomegalovirus infection with viremia is associated with development of cardiac allograft vasculopathy. J. Heart Lung Transplant. 11: S133-S137
39. Kendall T. J., Wilson R. E., Radio S. J., Kandolph R., Gulizia J. M., Winters G. L. et al. (1992) Cytomegalovirus and other herpesviruses: do they have a role in the development of accelerated coronary artery disease in human heart allografts? J. Heart Lung Transplant. 11: S14-20
40. Beersma F. C., Bijlmakers M. J. E. and Ploegh H. L. (1993) Human cytomegalovirus down regulates HLA class I expression by reducing the stability of class I chains. J. Immunol. 151: 4455-4464
41. Sedmak D. D., Roberts W. H., Stephens R. E., Buesching W. J., Morgan L. A. and Davis D. H. (1990) Inability of cytomegalovirus infection of cultured ECs to induce HLA class II antigen expression. Transplantation 49: 458-462
42. Waldman W. J., Adams P. W., Orosz C. G. and Sedmak D. D. (1992) T lymphocyte activation by cytomegalovirus infected allogeneic cultured human ECs. Transplantation 54: 887-896
43. Tullius S. G. and Tilney N. J. (1995) Both alloantigen-dependent and independent factors influence chronic allograft rejection. Transplantation 59: 313-318
44. Collins T., Lapierre L. A., Fiers W., Strominger J. L. and Pober J. S. (1986) Recombinant human tumour necrosis factor increases mRNA levels and surface expression of HLA-A,B antigens in vascular EC's and dermal fibroblasts in vitro. Proc. Natl. Acad. Sci. USA 83: 446-450
45. Lapierre L. A., Fiers W. and Pober J. S. (1988) Three distinct classes of regulatory cytokines control endothelial cell MHC antigen expression: interactions with immune (γ) interferon differentiate the effects of tumor necrosis factor and lymphotoxin form those of leukocyte (α) and fibroblast (β) interferons. J. Exp. Med. 167: 794-804
46. Batten P., Yacoub M. H. and Rose M. L. (1996) Effect of human cytokines (IFN-γ, TNF-α, IL-1β, IL-4) on porcine ECs: induction of MHC and adhesion molecules and functional significance of these changes. Immunology 87: 127-133
47. Collins T., Korman A. J., Wake C. T., Boss J. M., Kappes D. J., Fiers W. et al. (1984) Immune interferon activates multiple class II major histocompatibilty complex genes and the associated invariant chain gene in human ECs and dermal fibroblasts. Proc. Natl. Acad. Sci. USA 81: 4917-4921
48. Panek R. B., Lee Y.-J. and Benveniste E. N. (1995). TGF-β suppression of IFN-γ induced class II MHC gene expression does not involve inhibition of phosphorylation of JAK1, JAK2 or signal transducers and activators of transcription, or modification of IFN-γ enhanced factor X expression. J. Immunol. 154: 610-619
49. Nanden D. and Reiner N. E. (1997). TGF-β attenuates the class II transactivator and reveals an accessory pathway of IFN-γ action. J. Immunol. 158: 1095-1101
50. McDouall R. M., Batten P., McCormack A., Yacoub M. H. and Rose M. L. (1997) MHC class II expression on human microvascular endothelial cells: exquisite sensitivity to IFNγ and NK cells. Transplantation 64: 1175-1180
51. McDouall R. M., Yacoub M. H. and Rose M. L. (1996) Isolation, culture and characterisation of MHC class II positive microvascular ECs from the human heart. Microvasc. Res. 51: 137-152
52. Groenewegen C., Buurman W. A. and van der Linden C. J. (1985) Lymphokine dependence of in vivo expression of MHC class II antigens by endothelium. Nature 316: 361-363
53. Goes N., Sims T., Urmson J., Vincent D., Ramassar V. and Halloran P. F. (1995) Disturbed MHC regulation in the IFNγ knockout mouse. Evidence for three states of MHC expression with distinct roles for IFNγ. J. Immunol. 155: 4559-4566
54. Watson C. A., Petzelbauer P., Zhou J., Pardi R. and Bender J. (1995) Contact dependent endothelial class II gene activation induced by NK cells is mediated by IFN gamma dependent and independent mechanisms. J. Immunol. 154: 3222-3233
55. Savage C. O. S., Hughes C. C. W., McIntyre B. W., Picard J. K. and Pober J. S. (1993) Human CD4+ T cells proliferate to HLA-DR + allogeneic vascular endothelium: identification of accessory interactions. Transplantation 56: 128-134
56. Page C. S., Holloway N., Smith H., Yacoub M. H. and Rose M. L. (1994) Alloproliferative responses of purified CD4+ and CD8+ T cell subsets to human vascular ECs in the absence of contaminating accessory cells. Transplantation 57: 1628-1637
57. Page C. S., Thompson C., Yacoub M. H. and Rose M. L. (1994) Human endothelial cell stimulation of allogeneic T cells via a CTLA-4 independent pathway. Transplant. Immunol. 1994: 2: 342-347
58. Epperson D. E. and Pober J. S. (1994) Antigen-presenting function of human endothelial cells. Direct activation of resting CD8+ T cells. J. Immunol. 153: 5402-5412
59. McDouall R. M., Page C. S., Hafizi H., Yacoub M. H. and Rose M. L. (1996) Alloproliferation of purified CD4+ T cells to adult human heart ECs and study of second signal requirements. Immunology 89: 220-226
60. Savage C. O. S. and Brooks C. J. (1995). Human vascular ECs do not induce anergy in allogeneic CD4+ T cells unless costimulation is prevented. Transplantation 60: 734-740
61. Rose M. L., Navarette C., Yacoub M. H. and Festenstein H. (1988) Persistence of donor specific class II antigens in allografted human heart two years after transplantation. Human Immunol. 23: 179-182
62. Murray A. G., Khodadoust M. M., Pober J. S. and Bothwell A. L. M. (1994) Porcine aortic ECs activate human T cells: direct presentation of MHC antigens and costimulation by ligands for human CD2 and CD28. Immunity 1: 57-63
63. Seino K., Azuma M., Bashuda H., Fukao K., Yagita H. and Okumura K. (1995) CD86 (B70/B7 2) on ECs co-stimulates allogeneic CD4+ T cells. Int. Immunol. 7: 1331-1337
64. Savage C. O. S., Hughes C. C. W., Pepinsky R. S., Wallner B. P., Freedman A. S. and Pober J. S. (1991) Endothelial cell lymphocyte function associated antigen-3 and an unidentified ligand act in concert to provide costimulation to human peripheral blood CD4+ T cells. Cell. Immunol. 137: 150-163
65. Arulanandam A. R., Moingeon P., Concino M. F., Recny M. A., Kato K., Yagita H. et al. (1993) A soluble multimeric recombinant CD2 protein identifies CD48 as a low affinity ligand for human CD2: divergence of CD2 ligands during evolution of humans and mice. J. Exp. Med. 177: 1439-1450
66. Kawai K., Shahinian A., Mak T. W. and Ohashi P. S. (1996) Skin allograft rejection in CD28-deficient mice. Transplantation 61: 352-355
67. Kaplon A. G., Hochman P. S., Michler R. E., Kwiatkowski P. A., Edwards N. M., Berger C. L. et al. (1996) Short course single agent therapy with an LFA-3-IgG1 fusion protein prolongs primate cardiac allograft survival. Transplantation 61: 356-363
68. Isobe I. M., Suzuki J., Yamazaki S., Horie S., Okubo Y. and Sekiguchi M. (1997) Assessment of tolerance induction to cardiac allograft by anti-ICAM-1 and anti-LFA-1 monoclonal antibodies. J. Heart Lung Transplant. 16: 1149-1156
69. VanSeventer G. A., Shimizy Y., Horgan K. J. and Shaw S. (1990) The LFA-1 ligand ICAM-1 provides a costimulatory signal for T cell receptor mediated activation of resting T cells. J. Immunol. 144: 4579-4586
70. Damle N. and Aruffo A. (1991) Vascular cell adhesion molecule induces T cell antigen receptor dependent activation by CD4+ T lymphocytes. Proc. Natl. Acad. Sci. 88: 6403-6407
71. Karmann K., Hughes C. C. W., Schechner J., Fanslow W. C. and Pober J. S. (1995) CD40 on human ECs: inducibility by cytokines and functional regulation of adhesion molecule expression. Proc. Natl. Acad. Sci. 92: 4342-4346
72. Taylor P. M., Rose M. L., Yacoub M. H. and Piggott R. (1992) Induction of vascular adhesion molecules during rejection of human cardiac allografts. Transplantation 54: 451-457
73. Briscoe D. M., Schoen F. J., Rice G. E., Bevilacqua M. P., Ganz P. and Pober J. S. (1991). Induced expression of endothelial-leukocyte adhesion molecules in human cardiac allografts. Transplantation 51: 537-539
74. Pober J. S., Bevilacqua M. P., Mendrick D. L., Lapierre L. A., Fiers W. and Gimbrone M. A. (1986) Two distinct monokines, interleukin 1 and tumour necrosis factor, each independently induce biosynthesis and transient expression of the same antigen on the surface of cultured ECs. J. Immunol. 136: 1680-1687
75. Luscinskas F. W., Ding H. and Lichtman A. H. (1995) P-selectin and vascular adhesion molecule 1 mediate rolling and arrest, respectively, of CD4+ T lymphocytes on tumour necrosis factor a activated vascular endothelium under flow. J. Exp. Med. 181: 1179-1186
76. Spertini O., Luscinskas F. W., Kansas G. S., Munro J. M., Griffin J. D. et al. (1991) Leukocyte adhesion molecule-1 (LAM-1, L-selectin) interacts with an inducible endothelial cell ligand to support leukocyte adhesion. J. Immunol. 147: 2565-2573
77. Yamada A., Nikaido T., Nojima Y., Schlossman S. and Morimoto C. (1991) Activation of human CD4+ T lymphocytes. Interaction of fibronectin with VLA-5 receptor on CD4 cells induces the AP-1 transcription factor. J. Immunol. 146: 53-56
78. Germain R. N. and Margulies D. H. (1993) The biochemistry and cell biology of antigen processing and presentation. Ann. Rev. Immunol. 11: 403-450
79. Epperson D. E., Arnold D., Spies T., Cresswell P., Pober J. S. and Johnson D. R. (1992) Cytokines increase transporter in antigen processing-1 (TAP-1) expression more rapidly than HLA class I expression in ECs. J. Immunol. 149: 3297-3301
80. Clayberger C., Uyehara T., Hardy B., Eaton J., Karasele M. and Krensky A. M. (1985) Target specificity and cell surface structures involved in the human cytolytic T cell response to endothelial cells. J. Immunol. 135: 12-18
81. Pardi R. and Bender J. R. (1991) Signal requirements for the generation of CD4+ and CD8+ T cell responses to human allogeneic microvascular endothelium. Circ. Res. 69: 1269-1279
82. Ayalon O., Hughes E. A., Creswell P., Lee J., O'Donnel L., Pardi R. et al. (1998) Induction of transporter associated with antigen processing by interferon g confers endothelial cell cytoprotection against natural killer-mediated lysis. Proc. Natl. Acad. Sci. USA 95: 2435-2440
83. Fling S. P., Arp B. and Pious D. (1994) HLA-DMA and DMB genes are both required for the MHC class II/peptide complex formation in antigen presenting cells. Nature 368: 554-558
84. Ceman S., Rudersdorf R. A., Peteran J. M. and DeMars A. (1995) DMA and DMB are the only genes in the class II region of the human MHC needed for class II associated antigen processing. J. Immunol. 154: 2545-2556
85. Vora M., Yssel H., de Vries J. E. and Karasek M. A. (1994) Antigen presentation by human dermal microvascular ECs. Immunoregulatory effects of IFNγ-and IL-10. J. Immunol. 152: 5734-5741
86. Savage C. O. S., Brooks C. J., Harcourt G. C., Picard J. K., King W., Sansom D. M. et al. (1995) Human vascular endothelial cells process and present autoantigen to human T cell lines. Int. Immunol. 7: 471-479
87. Lechler R. I. and Batchelor J. R. (1982) Restoration of immungenicity of passenger cell depleted kidney allografts by the addition of donor strain dendritic cells. J. Exp. Med. 155: 31-41
88. Vandenberghe P., Freeman G. J., Nadler L. M., Fletcher M. C., Kamoun M., Turka L. A. et al. (1992) Antibody and B7/BB1-mediated ligation of the CD28 receptor induces tyrosine phosphorylation in human T cells. J. Exp. Med. 175: 951-960
89. Lindstein T., June C. H., Ledbetter J. A., Stella G. and Thompson C. B. (1989) Regulation of lymphokine messenger RNA stability by a surface mediated T cell activation pathway. Science 244: 339-343
90. King P. D., Sadra A., Han A., Liu X. R., Sunder-Plassmann R., Reinherz E. L. et al. (1996) CD2 signalling in T cells involves tyrosine phosphorylation and activation of the Tec family kinase, EMT/ITK/TSK. Int. Immunol. 8: 1707-1714
91. Gollob J. A., Li J., Kawasaki H., Daley J. F., Groves C., Reinherz E. L. et al. (1996) Molecular interactions between CD58 and CD2 counter receptors mediates the ability of monocytes to augment T cell activation by IL-12. J. Immunol. 157: 1886-1893
92. Bravery C. A., Batten R. Yacoub M. H. and Rose M. L. (1995) Direct recognition of SLA and HLA-like class II antigens on porcine endothelium by human T cells results in T cell activation and release of Interleukin-2. Transplantation 60: 1024-1033
93. Hughes C. C. W. and Pober J. S. (1993) Costimulation of peripheral blood T cell activation by human ECs. Enhanced IL-2 transcription correlates with increased c-fos synthesis and increased fos content of AP-1. J. Immunol. 150: 3148-3160
94. June C. H., Ledbetter J. A., Gillespie M. M., Lindsten T. and Thompson C. B. (1987) T cell proliferation involving the CD28 pathway is associated with cyclosporine resistant interleukin-2 gene expression. Mol. Cell Biol. 7: 4472-4481
95. Adams P. W., Lee S. H. Waldman W. J., Sedmak D. D., Morgan C. J., Ward J. S. et al. (1992) Alloantigenicity of human endothelial cells. I. Frequency and phenotype of human T helper lymphocytes that can react to allogeneic endothelial cells. J. Immunol. 148: 3753-3760
96. Pober J. S., Ma W., Biedermann B. and Libby P. (1997) Vascular cells have limited capacities to activate and differentiate T cells: implications for transplant vascular sclerosis. Transplant. Immunol. 5: 251-255
97. Cunningham A. C., Zhang J.-G., Moy J. V., Ali S. and Kirby J. A. (1997) A comparison of the antigen-presenting capabilities of class II MHC expressing human lung epithelial and ECs. Immunology 91: 458-463
98. Marelli-Berg F. M., Weetman A., Frasca L., Deacock S., Imami N., Lombardi G. et al. (1997) Antigen presentation by epithelial cells induces anergic immunoregulatory CD45RO+ T cells and deletion of CD45RA+ T cells. J. Immunol. 159: 5853-5861
99. Murray A. G., Libby P. and Pober J. S. (1995) Human vascular smooth muscle cells poorly stimulate and actively inhibit allogeneic CD4+ T cell proliferation in vitro. J. Immunol. 154: 151-161
100. Marelli-Berg F. M., Hargreaves R. E. G., Carmichael P., Dorling A., Lombardi G. and Lechler R. I. (1996) Major histocompatibility complex class II expressing endothelial cells induce allospecific non-responsiveness in naive T cells. J. Exp. Med. 183: 1603-1612
101. St. Louis J. D., Lederer J. A. and Lichtman A. H. (1993). Costimulator deficient antigen presentation by an endothelial cell line induces a non-proliferative T cell activation response without anergy. J. Exp. Med. 178: 1597-1605
102. Russel P. S., Chase C. M., Winn H. J. and Colvin R. B. (1994). Coronary atherosclerosis in transplanted mouse hearts. I. Time course and immunogenetics and immunopathological considerations. Am J. Pathol. 144: 260-274
103. Shi C., Lee W. S., He Q., Zhang D., Fletcher D. L., Newell J. B. et al. (1996) Immunologic basis of transplant-associated arteriosclerosis. Proc. Natl. Acad. Sci. USA 93: 4051-4056
104. Mach F., Schonbeck U., Sukhova G. K., Bourcier T., Bonnefoy J. Y., Pober J. S. et al. (1997) Functional CD40 ligand is expressed on human vascular ECs, smooth muscle cells and macrophages: implications for CD40-CD40 ligand signalling in atherosclerosis. Proc. Natl. Acad. Sci. USA 94: 1931-1936
105. Hancock W. W., Sayegh M. H., Zheng X. G., Peach R., Linsley P. S. and Turka L. A. (1996) Costimulatory function and expression of CD40 ligand. CD80 and CD86 in vascularised murine cardiac allograft rejection. Proc. Natl. Acad. Sci. USA 93: 13967-13972
106. Clipstone N. A. and Crabtree G. R. (1992) Identification of calcineurin as a key signalling enzyme in T lymphocyte activation. Nature 357: 695-697
107. Han C. W., Imamura M., Hashino S., Zhu X., Tanaka J., Imai K. et al. (1995) Differential effects of the immunosuppressants cyclosporin A, FK506 and KM2210 on cytokine expression. Bone Marrow Transplant. 15: 733-739
108. Morris R. E. (1991) Rapamycin: FK506's fraternal twin or distant cousin? Immunol. Today 12: 137-140
109. Rose M. L. (1993) Antibody mediated rejection following cardiac transplantation. Transplant. Rev. 7: 140-152
110. Rose E. A., Smith C. R., Petrossian G. A., Barr M. L. and Reemtsma K. (1989) Humoral immune responses after cardiac transplantation: correlation with fatal rejection and graft atherosclerosis. Surgery 106: 203-208
111. Suciu-Foca N., Reed E., Marboe C., Harris P., Yu P. X., Sun Y. K. et al. (1991) The role of anti-HLA antibodies in heart transplantation. Transplantation 51: 716-724
112. Dunn M. J., Crisp S. J., Rose M. L., Taylor P. M. and Yacoub M. H. (1992) Antiendothelial antibodies and coronary artery disease after cardiac transplantation. Lancet 339: 1566-1570
113. Al Hussein K. A., Talbot D., Proud D., Taylor R. M. R. and Shenton B. K. (1995) The clinical significance of post transplantation non-HLA antibodies in renal transplantation. Transplant. Int. 8: 214-220
114. Ferry B. L., Welsh K. I., Dunn M. J., Law D. L., Proctor J., Chapel H. et al. (1997) Anti-cell surface endothelial antibodies in sera from cardiac and kidney transplant recipients: association with chronic rejection. Transplant. Immunol. 5: 17-24
115. Wheeler C. H., Collins A., Dunn M. J., Crisp S. J., Yacoub M. H. and Rose M. L. (1995) Characterisation of endothelial antigens associated with transplant associated coronary artery disease. J. Heart Lung Transplant. 14: S188-197
116. Baum H., Davies H. and Peakman M. (1996) Molecular mimicry in the MHC: hidden clues to autoimmunity? Immunol. Today 17: 64-70
117. Rose M. L. (1996) Role of antibody and indirect antigen presentation in transplant associated coronary artery disease. J. Heart Lung Transplant. 15: 342-349
118. Russel P. S., Chase C. M., Winn H. J. and Colvin R. B. (1994) Coronary atherosclerosis in transplanted mouse hearts. II. Importance of humoral immunity. J. Immunol. 152: 5134-5141
119. Leung D. Y., Collins M. T., Lapierre L. A., Geha R. S. and Pober J. S. (1986) Immunoglobulin M antibodies present in the acute phase of Kawasaki syndrome lyse cultured vascular endothelial cells stimulated by gamma interferon. J. Clin. Invest. 77: 1428-1435
120. Carvalho D., Savage C. O. S., Black C. M. and Pearson J. D. (1996) IgG antiendothelial cell autoantibodies from scleroderma patients induce leukocyte adhesion to human vascular endothelial cells in vitro. J. Clin. Invest. 97: 1-9
121. Pidwell D. W., Heller M. J., Gabler D. and Orosz C. (1995) In vitro stimulation of human ECs by sera from a subpopulation of high percentage panel reactive antibody patients. Transplantation 60: 563-569
122. Harris P. E., Bian H. and Reed E. F. (1997). Induction of high affinity growth factor receptor and proliferation in human endothelial cells by anti-HLA antibodies: a possible mechanism for transplant atherosclerosis. J. Immunol. 159: 5697-5704