Participation of blood vessel cells in human adaptive immune responses

Trends in Immunology

Volumn 33, Issue 1, 2012, Pages 49-57

  Pober, Jordan S ^a   Tellides, George ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; GAMMA INTERFERON; INTERCELLULAR ADHESION MOLECULE 1; VASCULAR CELL ADHESION MOLECULE 1;

ADAPTIVE IMMUNITY; BLOOD VESSEL; CELL HETEROGENEITY; CELL INFILTRATION; CELL INTERACTION; ENDOTHELIUM CELL; HUMAN; INFLAMMATION; NONHUMAN; PERICYTE; REVIEW; SMOOTH MUSCLE FIBER; T LYMPHOCYTE;

ADAPTIVE IMMUNITY; ANIMALS; BLOOD VESSELS; CELL MOVEMENT; ENDOTHELIAL CELLS; HUMANS; T-LYMPHOCYTES;

EID: 84855300285     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2011.09.006     Document Type: Review

References (104)

1. Fabre J.W. Rat kidney allograft model: was it all too good to be true?. Transplantation 1982, 34:223-225.
2. von Willebrand E., et al. Distribution of the major histocompatibility complex antigens in human and rat kidney. Kidney Int. 1985, 27:616-621.
3. Pober J.S., et al. Lymphocytes recognize human vascular endothelial and dermal fibroblast Ia antigens induced by recombinant immune interferon. Nature 1983, 305:726-729.
4. Tellides G., et al. Interferon-gamma elicits arteriosclerosis in the absence of leukocytes. Nature 2000, 403:207-211.
5. Ma W., et al. Interferon-gamma rapidly increases peptide transporter (TAP) subunit expression and peptide transport capacity in endothelial cells. J. Biol. Chem. 1997, 272:16585-16590.
6. Collins T., et al. Immune interferon activates multiple class II major histocompatibility complex genes and the associated invariant chain gene in human endothelial cells and dermal fibroblasts. Proc. Natl. Acad. Sci. U.S.A. 1984, 81:4917-4921.
7. Savage C.O., et al. Human vascular endothelial cells process and present autoantigen to human T cell lines. Int. Immunol. 1995, 7:471-479.
8. Pober J.S., et al. Interactions of T lymphocytes with human vascular endothelial cells: role of endothelial cells surface antigens. Immunobiology 1984, 168:483-494.
9. Hughes C.C., et al. Endothelial cells augment T cell interleukin 2 production by a contact-dependent mechanism involving CD2/LFA-3 interaction. J. Exp. Med. 1990, 171:1453-1467.
10. Shiao S.L., et al. Memory T cells and their costimulators in human allograft injury. J. Immunol. 2005, 175:4886-4896.
11. Mestas J., et al. Endothelial cell co-stimulation through OX40 augments and prolongs T cell cytokine synthesis by stabilization of cytokine mRNA. Int. Immunol. 2005, 17:737-747.
12. Khayyamian S., et al. ICOS-ligand, expressed on human endothelial cells, costimulates Th1 and Th2 cytokine secretion by memory CD4+ T cells. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:6198-6203.
13. Tan P.H., et al. Phenotypic and functional differences between human saphenous vein (HSVEC) and umbilical vein (HUVEC) endothelial cells. Atherosclerosis 2004, 173:171-183.
14. Nocentini G., Riccardi C. GITR: a multifaceted regulator of immunity belonging to the tumor necrosis factor receptor superfamily. Eur. J. Immunol. 2005, 35:1016-1022.
15. Maier C.L., Pober J.S. Human placental pericytes poorly stimulate and actively regulate allogeneic CD4 T cell responses. Arterioscler. Thromb. Vasc. Biol. 2011, 31:183-189.
16. Epperson D.E., Pober J.S. Antigen-presenting function of human endothelial cells. Direct activation of resting CD8 T cells. J. Immunol. 1994, 153:5402-5412.
17. Page C., et al. Human endothelial stimulation of allogeneic T cells via a CTLA-4 independent pathway. Transpl. Immunol. 1994, 2:342-347.
18. Maher S.E., et al. Porcine endothelial CD86 is a major costimulator of xenogeneic human T cells: cloning, sequencing, and functional expression in human endothelial cells. J. Immunol. 1996, 157:3838-3844.
19. Vandenberghe P., et al. In situ expression of B7/BB1 on antigen-presenting cells and activated B cells: an immunohistochemical study. Int. Immunol. 1993, 5:317-321.
20. Prat A., et al. B7 expression and antigen presentation by human brain endothelial cells: requirement for proinflammatory cytokines. J. Neuropathol. Exp. Neurol. 2000, 59:129-136.
21. Omari K.I., Dorovini-Zis K. Expression and function of the costimulatory molecules B7-1 (CD80) and B7-2 (CD86) in an in vitro model of the human blood-brain barrier. J. Neuroimmunol. 2001, 113:129-141.
22. Ge X., et al. Antibodies to liver sinusoidal endothelial cells modulate immune responses in liver transplantation. Transplant. Proc. 2005, 37:3335-3337.
23. Lozanoska-Ochser B., et al. Expression of CD86 on human islet endothelial cells facilitates T cell adhesion and migration. J. Immunol. 2008, 181:6109-6116.
24. Leifeld L., et al. Enhanced expression of CD80 (B7-1), CD86 (B7-2), and CD40 and their ligands CD28 and CD154 in fulminant hepatic failure. Am. J. Pathol. 1999, 154:1711-1720.
25. Yao S., et al. B7-h2 is a costimulatory ligand for CD28 in human. Immunity 2011, 34:729-740.
26. Karmann K., et al. CD40 on human endothelial cells: inducibility by cytokines and functional regulation of adhesion molecule expression. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:4342-4346.
27. Hollenbaugh D., et al. Expression of functional CD40 by vascular endothelial cells. J. Exp. Med. 1995, 182:33-40.
28. Yellin M.J., et al. Functional interactions of T cells with endothelial cells: the role of CD40L-CD40-mediated signals. J. Exp. Med. 1995, 182:1857-1864.
29. Mazanet M.M., Hughes C.C. B7-H1 is expressed by human endothelial cells and suppresses T cell cytokine synthesis. J. Immunol. 2002, 169:3581-3588.
30. Rodig N., et al. Endothelial expression of PD-L1 and PD-L2 down-regulates CD8+ T cell activation and cytolysis. Eur. J. Immunol. 2003, 33:3117-3126.
31. Oikawa T., et al. Intrahepatic expression of the co-stimulatory molecules programmed death-1, and its ligands in autoimmune liver disease. Pathol. Int. 2007, 57:485-492.
32. Xie Z., et al. Intrahepatic PD-1/PD-L1 up-regulation closely correlates with inflammation and virus replication in patients with chronic HBV infection. Immunol. Invest. 2009, 38:624-638.
33. Chen J., et al. Intrahepatic levels of PD-1/PD-L correlate with liver inflammation in chronic hepatitis B. Inflamm. Res. 2011, 60:47-53.
34. Geiger R., et al. Human naive and memory CD4+ T cell repertoires specific for naturally processed antigens analyzed using libraries of amplified T cells. J. Exp. Med. 2009, 206:1525-1534.
35. Altman, J.D. and Davis, M.M. (2003) MHC-peptide tetramers to visualize antigen-specific T cells. Curr. Protoc. Immunol. Chapter 17, Unit 17.3, 1-33. John Wiley & Sons.
36. Macedo C., et al. Contribution of naive and memory T-cell populations to the human alloimmune response. Am. J. Transplant. 2009, 9:2057-2066.
37. Lombardi G., et al. Are primary alloresponses truly primary?. Int. Immunol. 1990, 2:9-13.
38. Hirschberg H., et al. Antigen-presenting properties of human vascular endothelial cells. J. Exp. Med. 1980, 152:249s-255s.
39. Salomon R.N., et al. Human coronary transplantation-associated arteriosclerosis. Evidence for a chronic immune reaction to activated graft endothelial cells. Am. J. Pathol. 1991, 138:791-798.
40. Savage C.O., et al. Human CD4+ T cells proliferate to HLA-DR+ allogeneic vascular endothelium. Identification of accessory interactions. Transplantation 1993, 56:128-134.
41. Murray A.G., et al. Human vascular smooth muscle cells poorly co-stimulate and actively inhibit allogeneic CD4+ T cell proliferation in vitro. J. Immunol. 1995, 154:151-161.
42. McDouall R.M., et al. Alloproliferation of purified CD4+ T cells to adult human heart endothelial cells, and study of second-signal requirements. Immunology 1996, 89:220-226.
43. Murphy L.L., et al. Single-cell analysis of costimulation by B cells, endothelial cells, and fibroblasts demonstrates heterogeneity in responses of CD4(+) memory T cells. Cell Immunol. 1999, 194:150-161.
44. Rao D.A., et al. Interleukin (IL)-1 promotes allogeneic T cell intimal infiltration and IL-17 production in a model of human artery rejection. J. Exp. Med. 2008, 205:3145-3158.
45. Dengler T.J., et al. Human vascular endothelial cells stimulate a lower frequency of alloreactive CD8+ pre-CTL and induce less clonal expansion than matching B lymphoblastoid cells: development of a novel limiting dilution analysis method based on CFSE labeling of lymphocytes. J. Immunol. 2001, 166:3846-3854.
46. Shiao S.L., et al. Human effector memory CD4+ T cells directly recognize allogeneic endothelial cells in vitro and in vivo. J. Immunol. 2007, 179:4397-4404.
47. Nunez G., et al. Accessory cell function of human endothelial cells. I. A subpopulation of Ia positive cells is required for antigen presentation. J. Immunol. 1983, 131:666-673.
48. Pardi R., Bender J.R. Signal requirements for the generation of CD4+ and CD8+ T-cell responses to human allogeneic microvascular endothelium. Circ. Res. 1991, 69:1269-1279.
49. Marelli-Berg F.M., et al. Major histocompatibility complex class II-expressing endothelial cells induce allospecific nonresponsiveness in naive T cells. J. Exp. Med. 1996, 183:1603-1612.
50. Dengler T.J., Pober J.S. Human vascular endothelial cells stimulate memory but not naive CD8+ T cells to differentiate into CTL retaining an early activation phenotype. J. Immunol. 2000, 164:5146-5155.
51. Biedermann B.C., Pober J.S. Human endothelial cells induce and regulate cytolytic T cell differentiation. J. Immunol. 1998, 161:4679-4687.
52. Biedermann B.C., Pober J.S. Human vascular endothelial cells favor clonal expansion of unusual alloreactive CTL. J. Immunol. 1999, 162:7022-7030.
53. Kummer M., et al. Vascular endothelial cells have impaired capacity to present immunodominant, antigenic peptides: a mechanism of cell type-specific immune escape. J. Immunol. 2005, 174:1947-1953.
54. Rao D.A., et al. IL-1alpha and IL-1beta are endogenous mediators linking cell injury to the adaptive alloimmune response. J. Immunol. 2007, 179:6536-6546.
55. Manavalan J.S., et al. Alloantigen specific CD8+CD28- FOXP3+ T suppressor cells induce ILT3+ ILT4+ tolerogenic endothelial cells, inhibiting alloreactivity. Int. Immunol. 2004, 16:1055-1068.
56. Gleissner C.A., et al. IL-10 inhibits endothelium-dependent T cell costimulation by up-regulation of ILT3/4 in human vascular endothelial cells. Eur. J. Immunol. 2007, 37:177-192.
57. Damle N.K., et al. Proliferation of human T lymphocytes induced with superantigens is not dependent on costimulation by the CD28 counter-receptor B7. J. Immunol. 1993, 150:726-735.
58. Ma W., Pober J.S. Human endothelial cells effectively costimulate cytokine production by, but not differentiation of, naive CD4+ T cells. J. Immunol. 1998, 161:2158-2167.
59. Ley K., et al. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 2007, 7:678-689.
60. Vestweber D. Adhesion and signaling molecules controlling the transmigration of leukocytes through endothelium. Immunol. Rev. 2007, 218:178-196.
61. Cinamon G., et al. Shear forces promote lymphocyte migration across vascular endothelium bearing apical chemokines. Nat. Immunol. 2001, 2:515-522.
62. Manes T.D., et al. Endothelial cell-T lymphocyte interactions: IP[corrected]-10 stimulates rapid transendothelial migration of human effort but not central memory CD4+ T cells. Requirements for shear stress and adhesion molecules. Transplantation 2006, 82:S9-S14.
63. Manes T.D., et al. TCR signaling antagonizes rapid IP-10-mediated transendothelial migration of effector memory CD4+ T cells. J. Immunol. 2007, 178:3237-3243.
64. Manes T.D., Pober J.S. Antigen presentation by human microvascular endothelial cells triggers ICAM-1-dependent transendothelial protrusion by, and fractalkine-dependent transendothelial migration of, effector memory CD4+ T cells. J. Immunol. 2008, 180:8386-8392.
65. Manes T.D., et al. Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins block distinct steps in transendothelial migration of effector memory CD4+ T cells by targeting different endothelial proteins. J. Immunol. 2010, 184:5186-5192.
66. Manes T.D., Pober J.S. Identification of endothelial cell junctional proteins and lymphocyte receptors involved in transendothelial migration of human effector memory CD4+ T cells. J. Immunol. 2011, 186:1763-1768.
67. Choy J.C., et al. CXCL12 induction of inducible nitric oxide synthase in human CD8 T cells. J. Heart Lung Transplant. 2008, 27:1333-1339.
68. Choy J.C., et al. Induction of inducible NO synthase in bystander human T cells increases allogeneic responses in the vasculature. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:1313-1318.
69. Choy J.C., Pober J.S. Generation of NO by bystander human CD8 T cells augments allogeneic responses by inhibiting cytokine deprivation-induced cell death. Am. J. Transplant. 2009, 9:2281-2291.
70. Denton M.D., et al. Endothelial cells modify the costimulatory capacity of transmigrating leukocytes and promote CD28-mediated CD4(+) T cell alloactivation. J. Exp. Med. 1999, 190:555-566.
71. Berg L.P., et al. Functional consequences of noncognate interactions between CD4+ memory T lymphocytes and the endothelium. J. Immunol. 2002, 168:3227-3234.
72. Nourshargh S., Marelli-Berg F.M. Transmigration through venular walls: a key regulator of leukocyte phenotype and function. Trends Immunol. 2005, 26:157-165.
73. Zhang P., et al. Human vascular smooth muscle cells lack essential costimulatory molecules to activate allogeneic memory T cells. Arterioscler. Thromb. Vasc. Biol. 2010, 30:1795-1801.
74. Cuffy M.C., et al. Induction of indoleamine 2,3-dioxygenase in vascular smooth muscle cells by interferon-gamma contributes to medial immunoprivilege. J. Immunol. 2007, 179:5246-5254.
75. Johnson B.A., et al. Targeting the immunoregulatory indoleamine 2,3 dioxygenase pathway in immunotherapy. Immunotherapy 2009, 1:645-661.
76. Lebastchi A.H., et al. TGF-β expression by human vascular cells inhibits IFN-γ production and arterial media injury by alloreactive memory T cells. Am. J. Transpl. 2011, (in press). 10.1111/j.1600-6143.2011.03676.x.
77. Dal Canto A.J., et al. IFN-gamma action in the media of the great elastic arteries, a novel immunoprivileged site. J. Clin. Invest. 2001, 107:R15-R22.
78. Karrar A., et al. Human liver sinusoidal endothelial cells induce apoptosis in activated T cells: a role in tolerance induction. Gut 2007, 56:243-252.
79. Suarez Y., et al. Alloimmunity to human endothelial cells derived from cord blood progenitors. J. Immunol. 2007, 179:7488-7496.
80. Crisan M., et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008, 3:301-313.
81. Uccelli A., et al. Mesenchymal stem cells in health and disease. Nat. Rev. Immunol. 2008, 8:726-736.
82. Pober J.S., et al. Immunopathology of human T cell responses to skin, artery and endothelial cell grafts in the human peripheral blood lymphocyte/severe combined immunodeficient mouse. Springer Semin. Immunopathol. 2003, 25:167-180.
83. Shultz L.D., et al. Humanized mice in translational biomedical research. Nat. Rev. Immunol. 2007, 7:118-130.
84. Jin S.W., Patterson C. The opening act: vasculogenesis and the origins of circulation. Arterioscler. Thromb. Vasc. Biol. 2009, 29:623-629.
85. Majesky M.W. Developmental basis of vascular smooth muscle diversity. Arterioscler. Thromb. Vasc. Biol. 2007, 27:1248-1258.
86. Liu M., et al. Regulation of arterial-venous differences in tumor necrosis factor responsiveness of endothelial cells by anatomic context. Am. J. Pathol. 2008, 172:1088-1099.
87. Aird W.C. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ. Res. 2007, 100:158-173.
88. Aird W.C. Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circ. Res. 2007, 100:174-190.
89. Abbott N.J. Astrocyte-endothelial interactions and blood-brain barrier permeability. J. Anat. 2002, 200:629-638.
90. Majesky M.W., et al. The adventitia: a dynamic interface containing resident progenitor cells. Arterioscler. Thromb. Vasc. Biol. 2011, 31:1530-1539.
91. Yoder M.C. Is endothelium the origin of endothelial progenitor cells?. Arterioscler. Thromb. Vasc. Biol. 2010, 30:1094-1103.
92. Hirschi K.K., et al. Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler. Thromb. Vasc. Biol. 2008, 28:1584-1595.
93. DeLeve L.D. Hepatic microvasculature in liver injury. Semin. Liver Dis. 2007, 27:390-400.
94. Mestas J., Hughes C.C. Of mice and not men: differences between mouse and human immunology. J. Immunol. 2004, 172:2731-2738.
95. Takei Y., et al. Central role for interferon-gamma receptor in the regulation of renal MHC expression. J. Am. Soc. Nephrol. 2000, 11:250-261.
96. Kato K., et al. CD48 is a counter-receptor for mouse CD2 and is involved in T cell activation. J. Exp. Med. 1992, 176:1241-1249.
97. Kreisel D., et al. Mouse vascular endothelium activates CD8+ T lymphocytes in a B7-dependent fashion. J. Immunol. 2002, 169:6154-6161.
98. Kreisel D., et al. Vascular endothelium does not activate CD4+ direct allorecognition in graft rejection. J. Immunol. 2004, 173:3027-3034.
99. Krupnick A.S., et al. Murine vascular endothelium activates and induces the generation of allogeneic CD4+25+Foxp3+ regulatory T cells. J. Immunol. 2005, 175:6265-6270.
100. Kreisel D., et al. Non-hematopoietic allograft cells directly activate CD8+ T cells and trigger acute rejection: an alternative mechanism of allorecognition. Nat. Med. 2002, 8:233-239.
101. Fabry Z., et al. Differential activation of Th1 and Th2 CD4+ cells by murine brain microvessel endothelial cells and smooth muscle/pericytes. J. Immunol. 1993, 151:38-47.
102. Swanson B.J., et al. A small population of vasculitogenic T cells expands and has skewed T cell receptor usage after culture with syngeneic smooth muscle cells. J. Autoimmun. 2003, 20:125-133.
103. Yao L., et al. Divergent inducible expression of P-selectin and E-selectin in mice and primates. Blood 1999, 94:3820-3828.
104. Lebastchi, A.H. et al. (2011) Activation of human vascular cells decreases their expression of transforming growth factor-beta. Atherosclerosis (in press).