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Cognate Interaction Between Endothelial Cells and T Cells

  • Percy A. KnolleEmail author
Chapter
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 43)

Abstract

Endothelial cells lining the blood vessels form a barrier between circulating immune cells and parenchymal tissue. While the molecular mechanisms involved in antigen-independent recruitment of leukocytes into infected tissue have been extensively studied, the mechanisms involving antigen-specific recruitment of T cells into tissue have remained largely elusive. Here I shall review the experimental evidence that endothelial cells function as antigen-presenting cells and in this function contribute first to regulation of immune responses and second, to antigen-specific recruitment of T cells.

Keywords

Endothelial Cell Major Histocompatibility Complex Major Histocompatibility Complex Class Human Endothelial Cell Microvascular Endothelial Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Askenase PW, Szczepanik M, Itakura A, Kiener C, Campos RA (2004) Extravascular T-cell recruitment requires initiation begun by Valpha14+ NKT cells and B-1 B cells. Trends Immunol 25:441–449 PubMedCrossRefGoogle Scholar
  2. 2.
    Bagai R, Valujskikh A, Canaday DH, Bailey E, Lalli PN, Harding CV, Heeger PS (2005) Mouse endothelial cells cross-present lymphocyte-derived antigen on class I MHC via a TAP1- and proteasome-dependent pathway. J Immunol 174:7711–7715 PubMedGoogle Scholar
  3. 3.
    Berg LP, James MJ, Alvarez-Iglesias M, Glennie S, Lechler RI, Marelli-Berg FM (2002) Functional consequences of noncognate interactions between CD4+ memory T lymphocytes and the endothelium. J Immunol 168:3227–3234 PubMedGoogle Scholar
  4. 4.
    Biedermann BC, Pober JS (1998) Human endothelial cells induce and regulate cytolytic T cell differentiation. J Immunol 161:4679–4687 PubMedGoogle Scholar
  5. 5.
    Biedermann BC, Pober JS (1999) Human vascular endothelial cells favor clonal expansion of unusual alloreactive CTL. J Immunol 162:7022–7030 PubMedGoogle Scholar
  6. 6.
    Biedermann BC, Sahner S, Gregor M, Tsakiris DA, Jeanneret C, Pober JS, Gratwohl A (2002) Endothelial injury mediated by cytotoxic T lymphocytes and loss of microvessels in chronic graft versus host disease. Lancet 359:2078–2083 PubMedCrossRefGoogle Scholar
  7. 7.
    Blanas E, Carbone FR, Allison J, Miller JF, Heath WR (1996) Induction of autoimmune diabetes by oral administration of autoantigen. Science 274:1707–1709 PubMedCrossRefGoogle Scholar
  8. 8.
    Boitano S, Safdar Z, Welsh DG, Bhattacharya J, Koval M (2004) Cell–cell interactions in regulating lung function. Am J Physiol Lung Cell Mol Physiol 287:L455–L459 PubMedCrossRefGoogle Scholar
  9. 9.
    Borgonovo B, Casorati G, Frittoli E, Gaffi D, Crimi E, Burastero SE (1997) Recruitment of circulating allergen-specific T lymphocytes to the lung on allergen challenge in asthma. J Allergy Clin Immunol 100:669–678 PubMedCrossRefGoogle Scholar
  10. 10.
    Bowen DG, Zen M, Holz L, Davis T, McCaughan GW, Bertolino P (2004) The site of primary T cell activation is a determinant of the balance between intrahepatic tolerance and immunity. J Clin Invest 114:701–712 PubMedCrossRefGoogle Scholar
  11. 11.
    Brezinschek RI, Oppenheimer-Marks N, Lipsky PE (1999) Activated T cells acquire endothelial cell surface determinants during transendothelial migration. J Immunol 162:1677–1684 PubMedGoogle Scholar
  12. 12.
    Callery MP, Kamei T, Flye MW (1989a) The effect of portacaval shunt on delayed-hypersensitivity responses following antigen feeding. J Surg Res 46:391–394 PubMedCrossRefGoogle Scholar
  13. 13.
    Callery MP, Kamei T, Flye MW (1989b) Kupffer cell blockade inhibits induction of tolerance by the portal venous route. Transplantation 47:1092–1094 PubMedCrossRefGoogle Scholar
  14. 14.
    Campos RA, Szczepanik M, Itakura A, Akahira-Azuma M, Sidobre S, Kronenberg M, Askenase PW (2003) Cutaneous immunization rapidly activates liver invariant Valpha14 NKT cells stimulating B-1 B cells to initiate T cell recruitment for elicitation of contact sensitivity. J Exp Med 198:1785–1796 PubMedCrossRefGoogle Scholar
  15. 15.
    Cantor H, Dumont A (1967) Hepatic suppression of sensitization to antigen absorbed into the portal system. Nature 215:744–745 PubMedCrossRefGoogle Scholar
  16. 16.
    Chen L (2004) Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity. Nat Rev Immunol 4:336–347 PubMedCrossRefGoogle Scholar
  17. 17.
    Chi JT, Chang HY, Haraldsen G, Jahnsen FL, Troyanskaya OG, Chang DS, Wang Z, Rockson SG, van de Rijn M, Botstein D, Brown PO (2003) Endothelial cell diversity revealed by global expression profiling. Proc Natl Acad Sci USA 100:10623–10628 PubMedCrossRefGoogle Scholar
  18. 18.
    Choi J, Enis DR, Koh KP, Shiao SL, Pober JS (2004) T lymphocyte–endothelial cell interactions. Annu Rev Immunol 22:683–709 PubMedCrossRefGoogle Scholar
  19. 19.
    Curtsinger JM, Lins DC, Mescher MF (2003) Signal 3 determines tolerance versus full activation of naive CD8 T cells: dissociating proliferation and development of effector function. J Exp Med 197:1141–1151 PubMedCrossRefGoogle Scholar
  20. 20.
    Curtsinger JM, Valenzuela JO, Agarwal P, Lins D, Mescher MF (2005) Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J Immunol 174:4465–4469 PubMedGoogle Scholar
  21. 21.
    Dengler TJ, Pober JS (2000) Human vascular endothelial cells stimulate memory but not naive CD8+ T cells to differentiate into CTL retaining an early activation phenotype. J Immunol 164:5146–5155 PubMedGoogle Scholar
  22. 22.
    Dengler TJ, Johnson DR, Pober JS (2001) 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 166:3846–3854 PubMedGoogle Scholar
  23. 23.
    Denton MD, Geehan CS, Alexander SI, Sayegh MH, Briscoe DM (1999) Endothelial cells modify the costimulatory capacity of transmigrating leukocytes and promote CD28-mediated CD4(+) T cell alloactivation. J Exp Med 190:555–566 PubMedCrossRefGoogle Scholar
  24. 24.
    Descamps L, Dehouck MP, Torpier G, Cecchelli R (1996) Receptor-mediated transcytosis of transferrin through blood–brain barrier endothelial cells. Am J Physiol 270:H1149–H1158 PubMedGoogle Scholar
  25. 25.
    Dustin ML, Bromley SK, Kan Z, Peterson DA, Unanue ER (1997) Antigen receptor engagement delivers a stop signal to migrating T lymphocytes. Proc Natl Acad Sci USA 94:3909–3913 PubMedCrossRefGoogle Scholar
  26. 26.
    Engelhardt B, Wolburg H (2004) Transendothelial migration of leukocytes: through the front door or around the side of the house? Eur J Immunol 34:2955–2963 PubMedCrossRefGoogle Scholar
  27. 27.
    Freeman GJ, Long AJ, Iwai Y, Bourque K, Chernova T, Nishimura H, Fitz LJ, Malenkovich N, Okazaki T, Byrne MC, Horton HF, Fouser L, Carter L, Ling V, Bowman MR, Carreno BM, Collins M, Wood CR, Honjo T (2000) Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med 192:1027–1034 PubMedCrossRefGoogle Scholar
  28. 28.
    Garcia-Barros M, Paris F, Cordon-Cardo C, Lyden D, Rafii S, Haimovitz-Friedman A, Fuks Z, Kolesnick R (2003) Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 300:1155–1159 PubMedCrossRefGoogle Scholar
  29. 29.
    Gerdes N, Sukhova GK, Libby P, Reynolds RS, Young JL, Schonbeck U (2002) Expression of interleukin (IL)-18 and functional IL-18 receptor on human vascular endothelial cells, smooth muscle cells, and macrophages: implications for atherogenesis. J Exp Med 195:245–257 PubMedCrossRefGoogle Scholar
  30. 30.
    Greening JE, Tree TI, Kotowicz KT, van Halteren AG, Roep BO, Klein NJ, Peakman M (2003) Processing and presentation of the islet autoantigen GAD by vascular endothelial cells promotes transmigration of autoreactive T cells. Diabetes 52:717–725 PubMedCrossRefGoogle Scholar
  31. 31.
    Grewal IS, Flavell RA (1998) CD40 and CD154 in cell-mediated immunity. Annu Rev Immunol 16:111–135 PubMedCrossRefGoogle Scholar
  32. 32.
    Gutgemann I, Fahrer AM, Altman JD, Davis MM, Chien YH (1998) Induction of rapid T cell activation and tolerance by systemic presentation of an orally administered antigen. Immunity 8:667–673 PubMedCrossRefGoogle Scholar
  33. 33.
    Hawkins BT, Davis TP (2005) The blood–brain barrier/neurovascular unit in health and disease. Pharmacol Rev 57:173–185 PubMedCrossRefGoogle Scholar
  34. 34.
    Haraldsen G, Sollid LM, Bakke O, Farstad IN, Kvale D, Molberg J, Norstein J, Stang E, Brandtzaeg P (1998) Major histocompatibility complex class II-dependent antigen presentation by human intestinal endothelial cells. Gastroenterology 114:649–656 PubMedCrossRefGoogle Scholar
  35. 35.
    Karmann K, Hughes CC, Schechner J, Fanslow WC, Pober JS (1995) CD40 on human endothelial cells: inducibility by cytokines and functional regulation of adhesion molecule expression. Proc Natl Acad Sci USA 92:4342–4346 PubMedCrossRefGoogle Scholar
  36. 36.
    Karmann K, Hughes CC, Fanslow WC, Pober JS (1996) Endothelial cells augment the expression of CD40 ligand on newly activated human CD4+ T cells through a CD2/LFA-3 signaling pathway. Eur J Immunol 26:610–617 PubMedCrossRefGoogle Scholar
  37. 37.
    Katz SC, Pillarisetty VG, Bleier JI, Shah AB, DeMatteo RP (2004) Liver sinusoidal endothelial cells are insufficient to activate T cells. J Immunol 173:230–235 PubMedGoogle Scholar
  38. 38.
    Kawai T, Shimauchi H, Eastcott JW, Smith DJ, Taubman MA (1998) Antigen direction of specific T-cell clones into gingival tissues. Immunology 93:11–19 PubMedCrossRefGoogle Scholar
  39. 39.
    Khayyamian S, Hutloff A, Buchner K, Grafe M, Henn V, Kroczek RA, Mages HW (2002) ICOS-ligand, expressed on human endothelial cells, costimulates Th1 and Th2 cytokine secretion by memory CD4+ T cells. Proc Natl Acad Sci USA 99:6198–6203 PubMedCrossRefGoogle Scholar
  40. 40.
    Knolle PA, Schmitt E, Jin S, Germann T, Duchmann R, Hegenbarth S, Gerken G, Lohse AW (1999) Induction of cytokine production in naive CD4(+) T cells by antigen-presenting murine liver sinusoidal endothelial cells but failure to induce differentiation toward Th1 cells. Gastroenterology 116:1428–1440 PubMedCrossRefGoogle Scholar
  41. 41.
    Kummer M, Lev A, Reiter Y, Biedermann BC (2005) Vascular endothelial cells have impaired capacity to present immunodominant, antigenic peptides: a mechanism of cell type-specific immune escape. J Immunol 174:1947–1953 PubMedGoogle Scholar
  42. 42.
    Kurt-Jones EA, Fiers W, Pober JS (1987) Membrane interleukin 1 induction on human endothelial cells and dermal fibroblasts. J Immunol 139:2317–2324 PubMedGoogle Scholar
  43. 43.
    Lacorre DA, Baekkevold ES, Garrido I, Brandtzaeg P, Haraldsen G, Amalric F, Girard JP (2004) Plasticity of endothelial cells: rapid dedifferentiation of freshly isolated high endothelial venule endothelial cells outside the lymphoid tissue microenvironment. Blood 103:4164–4172 PubMedCrossRefGoogle Scholar
  44. 44.
    Lenschow DJ, Walunas TL, Bluestone JA (1996) CD28/B7 system of T cell costimulation. Annu Rev Immunol 14:233–258 PubMedCrossRefGoogle Scholar
  45. 45.
    Lienenluke B, Germann T, Kroczek RA, Hecker M (2000) CD154 stimulation of interleukin-12 synthesis in human endothelial cells. Eur J Immunol 30:2864–2870 PubMedCrossRefGoogle Scholar
  46. 46.
    Limmer A, Sacher T, Alferink J, Kretschmar M, Schonrich G, Nichterlein T, Arnold B, Hammerling GJ (1998) Failure to induce organ-specific autoimmunity by breaking of tolerance: importance of the microenvironment. Eur J Immunol 28:2395–2406 PubMedCrossRefGoogle Scholar
  47. 47.
    Limmer A, Ohl J, Kurts C, Ljunggren HG, Reiss Y, Groettrup M, Momburg F, Arnold B, Knolle PA (2000) Efficient presentation of exogenous antigen by liver endothelial cells to CD8+ T cells results in antigen-specific T-cell tolerance. Nat Med 6:1348–1354 PubMedCrossRefGoogle Scholar
  48. 48.
    Limmer A, Ohl J, Wingender G, Berg M, Jüngerkes F, Schumak B, Djandji D, Scholz K, Klevenz A, Hegenbarth S, Momburg F, Hämmerling GJ, Arnold B, Knolle PA (2005) Cross-presentation of oral antigens by liver sinusoidal endothelial cells leads to CD8 T cell tolerance. Eur J Immunol 35:2970–2981 PubMedCrossRefGoogle Scholar
  49. 49.
    Liu Y, Shaw SK, Ma S, Yang L, Luscinskas FW, Parkos CA (2004) Regulation of leukocyte transmigration: cell surface interactions and signaling events. J Immunol 172:7–13 PubMedGoogle Scholar
  50. 50.
    Lohse AW, Knolle PA, Bilo K, Uhrig A, Waldmann C, Ibe M, Schmitt E, Gerken G, Meyer zum Buschenfelde KH (1996) Antigen-presenting function and B7 expression of murine sinusoidal endothelial cells and Kupffer cells. Gastroenterology 110:1175–1181 PubMedCrossRefGoogle Scholar
  51. 51.
    Ma W, Pober JS (1998) Human endothelial cells effectively costimulate cytokine production by, but not differentiation of, naive CD4+ T cells. J Immunol 161:2158–2167 PubMedGoogle Scholar
  52. 52.
    Mackay CR (1993) Homing of naive, memory and effector lymphocytes. Curr Opin Immunol 5:423–427 PubMedCrossRefGoogle Scholar
  53. 53.
    Mahboubi K, Biedermann BC, Carroll JM, Pober JS (2000) IL-11 activates human endothelial cells to resist immune-mediated injury. J Immunol 164:3837–3846 PubMedGoogle Scholar
  54. 54.
    Marelli-Berg FM, Jarmin SJ (2004) Antigen presentation by the endothelium: a green light for antigen-specific T cell trafficking? Immunol Lett 93:109–113 PubMedCrossRefGoogle Scholar
  55. 55.
    Marelli-Berg FM, Hargreaves RE, Carmichael P, Dorling A, Lombardi G, Lechler RI (1996) Major histocompatibility complex class II-expressing endothelial cells induce allospecific nonresponsiveness in naive T cells. J Exp Med 183:1603–1612 PubMedCrossRefGoogle Scholar
  56. 56.
    Marelli-Berg FM, Frasca L, Weng L, Lombardi G, Lechler RI (1999) Antigen recognition influences transendothelial migration of CD4+ T cells. J Immunol 162:696–703 PubMedGoogle Scholar
  57. 57.
    Marelli-Berg FM, Scott D, Bartok I, Peek E, Dyson J, Lechler RI (2000a) Activated murine endothelial cells have reduced immunogenicity for CD8+ T cells: a mechanism of immunoregulation? J Immunol 165:4182–4189 PubMedGoogle Scholar
  58. 58.
    Marelli-Berg FM, Peek E, Lidington EA, Stauss HJ, Lechler RI (2000b) Isolation of endothelial cells from murine tissue. J Immunol Methods 244:205–215 PubMedCrossRefGoogle Scholar
  59. 59.
    Marelli-Berg FM, James MJ, Dangerfield J, Dyson J, Millrain M, Scott D, Simpson E, Nourshargh S, Lechler RI (2004) Cognate recognition of the endothelium induces HY-specific CD8+ T-lymphocyte transendothelial migration (diapedesis) in vivo. Blood 103:3111–3116 PubMedCrossRefGoogle Scholar
  60. 60.
    Mazanet MM, Hughes CC (2002) B7-H1 is expressed by human endothelial cells and suppresses T cell cytokine synthesis. J Immunol 169:3581–3588 PubMedGoogle Scholar
  61. 61.
    McDouall RM, Batten P, McCormack A, Yacoub MH, Rose ML (1997) MHC class II expression on human heart microvascular endothelial cells: exquisite sensitivity to interferon-gamma and natural killer cells. Transplantation 64:1175–1180 PubMedCrossRefGoogle Scholar
  62. 62.
    Mehta D, Bhattacharya J, Matthay MA, Malik AB (2004) Integrated control of lung fluid balance. Am J Physiol Lung Cell Mol Physiol 287:L1081–L1090 PubMedCrossRefGoogle Scholar
  63. 63.
    Miyasaka M, Tanaka T (2004) Lymphocyte trafficking across high endothelial venules: dogmas and enigmas. Nat Rev Immunol 4:360–370 PubMedCrossRefGoogle Scholar
  64. 64.
    Muczynski KA, Ekle DM, Coder DM, Anderson SK (2003) Normal human kidney HLA-DR-expressing renal microvascular endothelial cells: characterization, isolation, and regulation of MHC class II expression. J Am Soc Nephrol 14:1336–1348 PubMedCrossRefGoogle Scholar
  65. 65.
    Nourshargh S, Marelli-Berg FM (2005) Transmigration through venular walls: a key regulator of leukocyte phenotype and function. Trends Immunol 26:157–165 PubMedCrossRefGoogle Scholar
  66. 66.
    Pasqualini R, Ruoslahti E (1996) Organ targeting in vivo using phage display peptide libraries. Nature 380:364–366 PubMedCrossRefGoogle Scholar
  67. 67.
    Peng HJ, Turner MW, Strobel S (1989) The kinetics of oral hyposensitization to a protein antigen are determined by immune status and the timing, dose and frequency of antigen administration. Immunology 67:425–430 PubMedGoogle Scholar
  68. 68.
    Podgrabinska S, Braun P, Velasco P, Kloos B, Pepper MS, Skobe M (2002) Molecular characterization of lymphatic endothelial cells. Proc Natl Acad Sci USA 99:16069–16074 PubMedCrossRefGoogle Scholar
  69. 69.
    Rodig N, Ryan T, Allen JA, Pang H, Grabie N, Chernova T, Greenfield EA, Liang SC, Sharpe AH, Lichtman AH, Freeman GJ (2003) Endothelial expression of PD-L1 and PD-L2 down-regulates CD8+ T cell activation and cytolysis. Eur J Immunol 33:3117–3126 PubMedCrossRefGoogle Scholar
  70. 70.
    Sancho D, Yanez-Mo M, Tejedor R, Sanchez-Madrid F (1999) Activation of peripheral blood T cells by interaction and migration through endothelium: role of lymphocyte function antigen-1/intercellular adhesion molecule-1 and interleukin-15. Blood 93:886–896 PubMedGoogle Scholar
  71. 71.
    Savinov AY, Wong FS, Stonebraker AC, Chervonsky AV (2003) Presentation of antigen by endothelial cells and chemoattraction are required for homing of insulin-specific CD8+ T cells. J Exp Med 197:643–656 PubMedCrossRefGoogle Scholar
  72. 72.
    Scavelli C, Weber E, Agliano M, Cirulli T, Nico B, Vacca A, Ribatti D (2004) Lymphatics at the crossroads of angiogenesis and lymphangiogenesis. J Anat 204:433–449 PubMedCrossRefGoogle Scholar
  73. 73.
    Shamri R, Grabovsky V, Gauguet JM, Feigelson S, Manevich E, Kolanus W, Robinson MK, Staunton DE, von Andrian UH, Alon R (2005) Lymphocyte arrest requires instantaneous induction of an extended LFA-1 conformation mediated by endothelium-bound chemokines. Nat Immunol 6:497–506 PubMedCrossRefGoogle Scholar
  74. 74.
    Smedsrod B (2004) Clearance function of scavenger endothelial cells. Comp Hepatol 3 Suppl 1:S22 Google Scholar
  75. 75.
    Smith ME, Thomas JA (1990) Cellular expression of lymphocyte function associated antigens and the intercellular adhesion molecule-1 in normal tissue. J Clin Pathol 43:893–900 PubMedCrossRefGoogle Scholar
  76. 76.
    Suitters AJ, Rose ML, Dominguez MJ, Yacoub MH (1990) Selection for donor-specific cytotoxic T lymphocytes within the allografted human heart. Transplantation 49:1105–1109 PubMedCrossRefGoogle Scholar
  77. 77.
    Tavassoli M, Kishimoto T, Soda R, Kataoka M, Harjes K (1986) Liver endothelium mediates the uptake of iron–transferrin complex by hepatocytes. Exp Cell Res 165:369–379 PubMedCrossRefGoogle Scholar
  78. 78.
    Tay SS, McCormack A, Lawson C, Rose ML (2003) IFN-gamma reverses the stop signal allowing migration of antigen-specific T cells into inflammatory sites. J Immunol 170:3315–3322 PubMedGoogle Scholar
  79. 79.
    Valujskikh A, Heeger PS (2003) Emerging roles of endothelial cells in transplant rejection. Curr Opin Immunol 15:493–498 PubMedCrossRefGoogle Scholar
  80. 80.
    Vermijlen D, Luo D, Froelich CJ, Medema JP, Kummer JA, Willems E, Braet F, Wisse E (2002) Hepatic natural killer cells exclusively kill splenic/blood natural killer-resistant tumor cells by the perforin/granzyme pathway. J Leukoc Biol 72:668–676 PubMedGoogle Scholar
  81. 81.
    Vora M, Yssel H, de Vries JE, Karasek MA (1994) Antigen presentation by human dermal microvascular endothelial cells. Immunoregulatory effect of IFN-gamma and IL-10. J Immunol 152:5734–5741 PubMedGoogle Scholar
  82. 82.
    Wake K, Kawai Y, Smedsrod B (2001) Re-evaluation of the reticulo-endothelial system. Ital J Anat Embryol 106:261–269 PubMedGoogle Scholar
  83. 83.
    Watanabe T, Yoshida M, Shirai Y, Yamori M, Yagita H, Itoh T, Chiba T, Kita T, Wakatsuki Y (2002) Administration of an antigen at a high dose generates regulatory CD4+ T cells expressing CD95 ligand and secreting IL-4 in the liver. J Immunol 168:2188–2199 PubMedGoogle Scholar
  84. 84.
    Watanabe T, Katsukura H, Shirai Y, Yamori M, Nishi T, Chiba T, Kita T, Wakatsuki Y (2003) A liver tolerates a portal antigen by generating CD11c+ cells, which select Fas ligand+ Th2 cells via apoptosis. Hepatology 38:403–412 PubMedCrossRefGoogle Scholar
  85. 85.
    Zeevi A, Fung J, Zerbe TR, Kaufman C, Rabin BS, Griffith BP, Hardesty RL, Duquesnoy RJ (1986) Allospecificity of activated T cells grown from endomyocardial biopsies from heart transplant patients. Transplantation 41:620–626 PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2006

Authors and Affiliations

  1. 1.Institute for Molecular Medicine and Experimental ImmunologyFriedrich-Wilhelms-Universität BonnBonnGermany

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