Primed CD8 + T-cell responses to allogeneic endothelial cells are controlled by local complement activation

American Journal of Transplantation

Volumn 9, Issue 8, 2009, Pages 1784-1795

  Raedler, H ^a   Yang, M ^a   Lalli, P N ^b   Medof, M E ^b   Heeger, P S ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Complement activation; Complement component C3; Endothelial cell activation; T cell immunity; T cell immunology

Indexed keywords

CLASSICAL COMPLEMENT PATHWAY C3 C5 CONVERTASE; COMPLEMENT COMPONENT C5A; COMPLEMENT COMPONENT C5A RECEPTOR; DECAY ACCELERATING FACTOR; GAMMA INTERFERON; PERFORIN;

ALLOGRAFT; ALLOIMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL EXPANSION; CELL INTERACTION; CELL PROLIFERATION; CELL SURFACE; COMPLEMENT ACTIVATION; COMPLEMENT ALTERNATIVE PATHWAY; CONTROLLED STUDY; EFFECTOR CELL; ENDOTHELIUM CELL; FLOW CYTOMETRY; HEART GRAFT; HEART TRANSPLANTATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; UPREGULATION;

ANIMALS; ANTIGENS, CD55; CD8-POSITIVE T-LYMPHOCYTES; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; COMPLEMENT C3; COMPLEMENT C3-C5 CONVERTASES; COMPLEMENT C5A; COMPLEMENT SYSTEM PROTEINS; CYTOKINES; ENDOTHELIUM, VASCULAR; FEMALE; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, ANIMAL; RECEPTOR, ANAPHYLATOXIN C5A;

EID: 67650935679     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2009.02723.x     Document Type: Article

References (50)

1. Pober JS, Kluger MS, Schechner JS. Human endothelial cell presentation of antigen and the homing of memory/effector T cells to skin. Ann N Y Acad Sci 2001 941 : 12 25.
2. Briscoe DM, Alexander SI, Lichtman AH. Interactions between T lymphocytes and endothelial cells in allograft rejection. Curr Opin Immunol 1998 10 : 525 531.
3. Briscoe DM, Ganz P, Alexander SI et al. The problem of chronic rejection: Influence of leukocyte-endothelial interactions. Kidney Int Suppl 1997 58 : S22 S27.
4. Tedesco F, Fischetti F, Pausa M, Dobrina A, Sim RB, Daha MR. Complement-endothelial cell interactions: Pathophysiological implications. Mol immunol 1999 36 : 261 268.
5. Bagai R, Valujskikh A, Canaday DH et al. Mouse endothelial cells cross-present lymphocyte-derived antigen on class I MHC via a TAP1- and proteasome-dependent pathway. J Immunol 2005 174 : 7711 7715.
6. Valujskikh A, Heeger PS. Emerging roles of endothelial cells in transplant rejection. Curr Opin Immunol 2003 15 : 493 498.
7. +) T cells mediate graft rejection via a distinct effector pathway. Nat Immunol 2002 3 : 844 851.
8. + 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.
9. + T cells to differentiate into CTL retaining an early activation phenotype. J Immunol 2000 164 : 5146 5155.
10. + direct allorecognition in graft rejection. J Immunol 2004 173 : 3027 3034.
11. + T lymphocytes in a B7-dependent fashion. J Immunol 2002 169 : 6154 6161.
12. + T cells and trigger acute rejection: An alternative mechanism of allorecognition. Nat Med 2002 8 : 233 239.
13. Shiao SL, McNiff JM, Pober JS. Memory T cells and their costimulators in human allograft injury. J Immunol 2005 175 : 4886 4896.
14. Briscoe DM, DesRoches LE, Kiely JM, Lederer JA, Lichtman AH. Antigen-dependent activation of T helper cell subsets by endothelium. Transplantation 1995 59 : 1638 1641.
15. Kirkiles-Smith NC, Tereb DA, Kim RW et al. Endothelial cell activation by tumor necrosis factor elicits human antiporcine cell-mediated rejection responses. Transplant proc 2001 33 : 412 413.
16. Madge LA, Pober JS. TNF signaling in vascular endothelial cells. Exp Mol Pathol 2001 70 : 317 325.
17. Lalli PN, Strainic MG, Yang M, Lin F, Medof ME, Heeger PS. Locally produced C5a binds to T cell-expressed C5aR to enhance effector T-cell expansion by limiting antigen-induced apoptosis. Blood 2008 112 : 1759 1766.
18. Zhou W, Medof ME, Heeger PS, Sacks S. Graft-derived complement as a mediator of transplant injury. Curr Opin Immunol 2007 19 : 569 576.
19. + T cells. Immunity 2008 28 : 425 435.
20. Heeger PS, Lalli PN, Lin F et al. Decay-accelerating factor modulates induction of T cell immunity. J Exp Med 2005 201 : 1523 1530.
21. Lalli PN, Strainic MG, Lin F, Medof ME, Heeger PS. Decay accelerating factor can control T cell differentiation into IFN-gamma-producing effector cells via regulating local C5a-induced IL-12 production. J Immunol 2007 179 : 5793 5802.
22. Liu J, Lin F, Strainic MG et al. IFN-gamma and IL-17 production in experimental autoimmune encephalomyelitis depends on local APC-T cell complement production. J Immunol 2008 180 : 5882 5889.
23. Pavlov V, Raedler H, Yuan S et al. Donor deficiency of decay-accelerating factor accelerates murine T cell-mediated cardiac allograft rejection. J Immunol 2008 181 : 4580 4589.
24. Gasque P, Singhrao SK, Neal JW, Gotze O, Morgan BP. Expression of the receptor for complement C5a (CD88) is up-regulated on reactive astrocytes, microglia, and endothelial cells in the inflamed human central nervous system. Am J Pathol 1997 150 : 31 41.
25. Kawakami Y, Watanabe Y, Yamaguchi M, Sakaguchi H, Kono I, Ueki A. TNF-alpha stimulates the biosynthesis of complement C3 and factor B by human umbilical cord vein endothelial cells. Cancer lett 1997 116 : 21 26.
26. Coulpier M, Andreev S, Lemercier C et al. Activation of the endothelium by IL-1 alpha and glucocorticoids results in major increase of complement C3 and factor B production and generation of C3a. Clin Exp Immunol 1995 101 : 142 149.
27. Dauchel H, Julen N, Lemercier C et al. Expression of complement alternative pathway proteins by endothelial cells. Differential regulation by interleukin 1 and glucocorticoids. Eur J Immunol 1990 20 : 1669 1675.
28. Foreman KE, Vaporciyan AA, Bonish BK et al. C5a-induced expression of P-selectin in endothelial cells. J Clin Invest 1994 94 : 1147 1155.
29. Ripoche J, Mitchell JA, Erdei A et al. Interferon gamma induces synthesis of complement alternative pathway proteins by human endothelial cells in culture. J Exp Med 1988 168 : 1917 1922.
30. Schraufstatter IU, Trieu K, Sikora L, Sriramarao P, DiScipio R. Complement C3a and C5a induce different signal transduction cascades in endothelial cells. J Immunol 2002 169 : 2102 2110.
31. Banz Y, Cung T, Korchagina EY, Bovin NV, Haeberli A, Rieben R. Endothelial cell protection and complement inhibition in xenotransplantation: A novel in vitro model using whole blood. Xenotransplantation 2005 12 : 434 443.
32. Sheerin NS, Zhou W, Adler S, Sacks SH. TNF-alpha regulation of C3 gene expression and protein biosynthesis in rat glomerular endothelial cells. Kidney Int 1997 51 : 703 710.
33. Brunn GJ, Saadi S, Platt JL. Differential regulation of endothelial cell activation by complement and interleukin 1alpha. Circ Res 2006 98 : 793 800.
34. Verbakel CA, van Duikeren S, de Bruin RW, Marquet RL, Ijzermans JN. Human decay-accelerating factor expressed on rat hearts inhibits leukocyte adhesion. Transpl Int 2003 16 : 168 172.
35. Verbakel CA, de Bruin RW, Bonthuis F et al. Contrast in the efficacy of hDAF mouse hearts between ex vivo perfusion and transplantation into primates. Xenotransplantation 2001 8 : 284 291.
36. Lin F, Fukuoka Y, Spicer A et al. Tissue distribution of products of the mouse decay-accelerating factor (DAF) genes. Exploitation of a Daf1 knock-out mouse and site-specific monoclonal antibodies. Immunology 2001 104 : 215 225.
37. Asai S, Sato T, Tada T et al. Absence of procarboxypeptidase R induces complement-mediated lethal inflammation in lipopolysaccharide-primed mice. J Immunol 2004 173 : 4669 4674.
38. Cai Z, Sprent J. Resting and activated T cells display different requirements for CD8 molecules. J Exp Med 1994 179 : 2005 2015.
39. Pober JS, Sessa WC. Evolving functions of endothelial cells in inflammation. Nat Rev Immunol 2007 7 : 803 815.
40. Kroshus TJ, Rollins SA, Dalmasso AP et al. Complement inhibition with an anti-C5 monoclonal antibody prevents acute cardiac tissue injury in an ex vivo model of pig-to-human xenotransplantation. Transplantation 1995 60 : 1194 1202.
41. + memory T cells in vitro with immunosuppressants. Transplantation 2006 82 : 1352 1361.
42. Lombardi G, Sidhu S, Daly M, Batchelor JR, Makgoba W, Lechler RI. Are primary alloresponses truly primary? Int Immunol 1990 2 : 9 13.
43. Sallusto F, Geginat J, Lanzavecchia A. Central memory and effector memory T cell subsets: Function, generation, and maintenance. Annu Rev Immunol 2004 22 : 745 763.
44. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999 401 : 708 712.
45. Valujskikh A. The challenge of inhibiting alloreactive T-cell memory. Am J Transplant 2006 6 : 647 651.
46. Valujskikh A. Targeting T-cell memory: where do we stand? Curr Opin Organ Transplant 2008 13 : 344 349.
47. Pearl JP, Parris J, Hale DA et al. Immunocompetent T-cells with a memory-like phenotype are the dominant cell type following antibody-mediated T-cell depletion. Am J Transplant 2005 5 : 465 474.
48. Rother RP, Arp J, Jiang J et al. C5 blockade with conventional immunosuppression induces long-term graft survival in presensitized recipients. Am J Transplant 2008 8 : 1129 1142.
49. Wang H, Arp J, Liu W et al. Inhibition of terminal complement components in presensitized transplant recipients prevents antibody-mediated rejection leading to long-term graft survival and accommodation. J Immunol 2007 179 : 4451 4463.
50. Gueler F, Rong S, Gwinner W et al. Complement 5a Receptor Inhibition Improves Renal Allograft Survival. J Am Soc Nephrol 2008 19 : 2301 2312.