CD8+ T cell tolerance following antigen recognition on hepatocytes

Journal of Autoimmunity

Volumn 34, Issue 1, 2010, Pages 15-22

  Holz, Lauren E ^a   Warren, Alessandra ^b   Le Couteur, David G ^b   Bowen, David G ^a   Bertolino, Patrick ^a  

^a ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^b ANZAC Research Institute   (Australia)

Author keywords

Bim; CD8; Hepatocyte; Interleukin 2; Liver

Indexed keywords

ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; APOPTOSIS; CD8+ T LYMPHOCYTE; CELL FATE; CELL FUNCTION; CELL INTERACTION; CELL TYPE; CELLULAR IMMUNITY; CHRONIC ACTIVE HEPATITIS; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; LYMPHOCYTE MIGRATION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE RECIRCULATION; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; CLONAL DELETION; HEPACIVIRUS; HEPATITIS C; HEPATOCYTES; HUMANS; IMMUNE EVASION; IMMUNE TOLERANCE; LYMPHOCYTE ACTIVATION;

EID: 75149189809     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2009.08.005     Document Type: Review

References (62)

1. Wick M.J., Leithauser F., and Reimann J. The hepatic immune system. Crit Rev Immunol 22 (2002) 47-103
2. Warren A., Le Couteur D.G., Fraser R., Bowen D.G., McCaughan G.W., and Bertolino P. T lymphocytes interact with hepatocytes through fenestrations in murine liver sinusoidal endothelial cells. Hepatology 44 (2006) 1182-1190
3. Chen M., Tabaczewski P., Truscott S.M., Van Kaer L., and Stroynowski I. Hepatocytes express abundant surface class I MHC and efficiently use transporter associated with antigen processing, tapasin, and low molecular weight polypeptide proteasome subunit components of antigen processing and presentation pathway. J Immunol 175 (2005) 1047-1055
4. Bertolino P., Trescol-Biemont M.C., and Rabourdin-Combe C. Hepatocytes induce functional activation of naive CD8+ T lymphocytes but fail to promote survival. Eur J Immunol 28 (1998) 221-236
5. Herkel J., Jagemann B., Wiegard C., Lazaro J.F., Lueth S., Kanzler S., et al. MHC class II-expressing hepatocytes function as antigen-presenting cells and activate specific CD4 T lymphocytes. Hepatology 37 (2003) 1079-1085
6. Bertolino P., Trescol-Biemont M.C., Thomas J., Fazekas de St Groth B., Pihlgren M., Marvel J., et al. Death by neglect as a deletional mechanism of peripheral tolerance. Int Immunol 11 (1999) 1225-1238
7. Schönrich G., Momburg F., Malissen M., Schmitt-Verhulst A.M., Malissen B., Hammerling G.J., et al. Distinct mechanisms of extrathymic T cell tolerance due to differential expression of self antigen. Int Immunol 4 (1992) 581-590
8. Morahan G., Brennan F.E., Bhathal P.S., Allison J., Cox K.O., and Miller J.F.A.P. Expression in transgenic mice of class I histocompatibility antigens controlled by the metallothionein promoter. Proc Natl Acad Sci U S A 86 (1989) 3782-3786
9. Bertolino P., Heath W.R., Hardy C.L., Morahan G., and Miller J.F. Peripheral deletion of autoreactive CD8+ T cells in transgenic mice expressing H-2Kb in the liver. Eur J Immunol 25 (1995) 1932-1942
10. Bertolino P., Bowen D.G., McCaughan G.W., and Fazekas De St Groth B. Antigen-specific primary activation of CD8+ T cells within the liver. J Immunol 166 (2001) 5430-5438
11. Bowen D.G., Zen M., Holz L., Davis T., McCaughan G.W., and Bertolino P. The site of primary T cell activation is a determinant of the balance between intrahepatic tolerance immunity. J Clin Investig 114 (2004) 701-712
12. Derkow K., Loddenkemper C., Mintern J., Kruse N., Klugewitz K., Berg T., et al. Differential priming of CD8 CD4 T-cells in animal models of autoimmune hepatitis cholangitis. Hepatology 46 (2004) 1155-1165
13. Klein I., and Crispe I.N. Complete differentiation of CD8+ T cells activated locally within the transplanted liver. J Exp Med 203 (2006) 437-447
14. Wuensch S.A., Pierce R.H., and Crispe I.N. Local intrahepatic CD8+ T cell activation by a non-self-antigen results in full functional differentiation. J Immunol 177 (2006) 1689-1697
15. Franco A., Barnaba V., Natali P., Balsano C., Musca A., and Balsano F. Expression of class I and class II major histocompatibility complex antigens on human hepatocytes. Hepatology 8 (1988) 449-454
16. Ando K., Guidotti L.G., Cerny A., Ishikawa T., and Chisari F.V. CTL access to tissue antigen is restricted in vivo. J Immunol 153 (1994) 482-488
17. Bowen D.G., McCaughan G.W., and Bertolino P. Intrahepatic immunity: a tale of two sites?. Trends Immunol 26 (2005) 512-517
18. MacPhee P.J., Schmidt E.E., and Groom A.C. Intermittence of blood flow in liver sinusoids, studied by high-resolution in vivo microscopy. Am J Physiol 269 (1995) G692-G698
19. Bertolino P., McCaughan G.W., and Bowen D.G. Role of primary intrahepatic T-cell activation in the 'liver tolerance effect'. Immunol Cell Biol 80 (2002) 84-92
20. Wisse E., De Zanger R.B., Charels K., Van Der Smissen P., and McCuskey R.S. The liver sieve: considerations concerning the structure and function of endothelial fenestrae, the sinusoidal wall and the space of disse. Hepatology 5 (1985) 683-692
21. Cogger V.C., Muller M., Fraser R., McLean A.J., Khan J., and Le Couteur D.G. The effects of oxidative stress on the liver sieve. J Hepatol 41 (2004) 370-376
22. Limmer A., Sacher T., Alferink J., Nichterlein T., Arnold B., and Hammerling G.J. A two-step model for the induction of organ-specific autoimmunity. Novartis Found Symp 215 (1998) 159-167 discussion 167-171
23. Guerder S., Rincon M., and Schmitt-Verhulst A.M. Regulation of activator protein-1 and NF-kappa B in CD8+ T cells exposed to peripheral self-antigens. J Immunol 166 (2001) 4399-4407
24. Wong J., Johnston B., Lee S.S., Bullard D.C., Smith C.W., Beaudet A.L., et al. A minimal role for selectins in the recruitment of leukocytes into the inflamed liver microvasculature. J Clin Investig 99 (1997) 2782-2790
25. Holz L.E., Benseler V., Bowen D.G., Bouillet P., Strasser A., O'Reilly L., et al. Intrahepatic murine CD8 T-cell activation associates with a distinct phenotype leading to Bim-dependent death. Gastroenterology 135 (2008) 989-997
26. Roebuck K.A., and Finnegan A. Regulation of intercellular adhesion molecule-1 (CD54) gene expression. J Leukoc Biol 66 (1999) 876-888
27. Schuh K., Twardzik T., Kneitz B., Heyer J., Schimpl A., and Serfling E. The interleukin 2 receptor alpha chain/CD25 promoter is a target for nuclear factor of activated T cells. J Exp Med 188 (1998) 1369-1373
28. Lopez-Cabrera M., Munoz E., Blazquez M.V., Ursa M.A., Santis A.G., and Sanchez-Madrid F. Transcriptional regulation of the gene encoding the human C-type lectin leukocyte receptor AIM/CD69 and functional characterization of its tumor necrosis factor-alpha-responsive elements. J Biol Chem 270 (1995) 21545-21551
29. Castellanos M.C., Munoz C., Montoya M.C., Lara-Pezzi E., Lopez-Cabrera M., and de Landazuri M.O. Expression of the leukocyte early activation antigen CD69 is regulated by the transcription factor AP-1. J Immunol 159 (1997) 5463-5473
30. Liu R., Zhao X., Gurney T.A., and Landau N.R. Functional analysis of the proximal CCR5 promoter. AIDS Res Hum Retrovir 14 (1998) 1509-1519
31. Diehn M., Alizadeh A.A., Rando O.J., Liu C.L., Stankunas K., Botstein D., et al. Genomic expression programs and the integration of the CD28 costimulatory signal in T cell activation. Proc Natl Acad Sci U S A 99 (2002) 11796-11801
32. Akbar A.N., Borthwick N.J., Wickremasinghe R.G., Panayoitidis P., Pilling D., Bofill M., et al. Interleukin-2 receptor common gamma-chain signaling cytokines regulate activated T cell apoptosis in response to growth factor withdrawal: selective induction of anti-apoptotic (bcl-2, bcl-xL) but not pro-apoptotic (bax, bcl-xS) gene expression. Eur J Immunol 26 (1996) 294-299
33. Krammer P.H., Arnold R., and Lavrik I.N. Life and death in peripheral T cells. Nat Rev Immunol 7 (2007) 532-542
34. Oltvai Z.N., Milliman C.L., and Korsmeyer S.J. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74 (1993) 609-619
35. Puthalakath H., and Strasser A. Keeping killers on a tight leash: transcriptional and post-translational control of the pro-apoptotic activity of BH3-only proteins. Cell Death Differ 9 (2002) 505-512
36. Huang L., Soldevila G., Leeker M., Flavell R., and Crispe I.N. The liver eliminates T cells undergoing antigen-triggered apoptosis in vivo. Immunity 1 (1994) 741-749
37. Mehal W.Z., Juedes A.E., and Crispe I.N. Selective retention of activated CD8+ T cells by the normal liver. J Immunol 163 (1999) 3202-3210
38. Ward S.M., Jonsson J.R., Sierro S., Clouston A.D., Lucas M., Vargas A.L., et al. Virus-specific CD8+ T lymphocytes within the normal human liver. Eur J Immunol 34 (2004) 1526-1531
39. Keating R., Yue W., Rutigliano J.A., So J., Olivas E., Thomas P.G., et al. Virus-Specific CD8+ T cells in the liver: armed ready to kill. J Immunol 178 (2007) 2737-2745
40. Crispe I.N., Giannandrea M., Klein I., John B., Sampson B., and Wuensch S. Cellular and molecular mechanisms of liver tolerance. Immunol Rev 213 (2006) 101-118
41. Bertolino P., and Holz L.E. Toll-like receptor-3 and the regulation of intrahepatic immunity: implications for interferon-alpha therapy. Hepatology 45 (2007) 250-251
42. Shoukry N.H., Cawthon A.G., and Walker C.M. Cell-mediated immunity and the outcome of hepatitis C virus infection. Annu Rev Microbiol 58 (2004) 391-424
43. Thimme R., Bukh J., Spangenberg H.C., Wieland S., Pemberton J., Steiger C., et al. Viral and immunological determinants of hepatitis C virus clearance, persistence, and disease. Proc Natl Acad Sci U S A 99 (2002) 15661-15668
44. Krawczynski K., Beach M.J., Bradley D.W., Kuo G., di Bisceglie A.M., Houghton M., et al. Hepatitis C virus antigen in hepatocytes: immunomorphologic detection and identification. Gastroenterology 103 (1992) 622-629
45. Neveu B., Debeaupuis E., Echasserieau K., le Moullac-Vaidye B., Gassin M., Jegou L., et al. Selection of high-avidity CD8 T cells correlates with control of hepatitis C virus infection. Hepatology 48 (2008) 713-722
46. Radziewicz H., Ibegbu C.C., Hon H., Osborn M.K., Obideen K., Wehbi M., et al. Impaired HCV specific effector CD8+ T cells undergo massive apoptosis in the peripheral blood during acute HCV infection and in the liver during the chronic phase of infection. J Virol 82 (2008) 9808-9822
47. Lopes A.R., Kellam P., Das A., Dunn C., Kwan A., Turner J., et al. Bim-mediated deletion of antigen-specific CD8 T cells in patients unable to control HBV infection. J Clin Investig 118 (2008) 1835-1845
48. Ochsenbein A.F., Sierro S., Odermatt B., Pericin M., Karrer U., Hermans J., et al. Roles of tumour localization, second signals and cross priming in cytotoxic T-cell induction. Nature 411 (2001) 1058-1064
49. Bertolino P., Bowen D., and McCaughan G. Immunological parameters determining adaptive immune responses to hepatitis C virus infection. In: Jirillo E. (Ed). The use of IFNs in HCV disease: from biology to clinical application. NY: Springer (2007) p. 339-70
50. Das A., Hoare M., Davies N., Lopes A.R., Dunn C., Kennedy P.T., et al. Functional skewing of the global CD8 T cell population in chronic hepatitis B virus infection. J Exp Med 205 (2008) 2111-2124
51. Roth E., Steininger R., Winkler S., Langle F., Grunberger T., Fugger R., et al. L-Arginine deficiency after liver transplantation as an effect of arginase efflux from the graft. Influence on nitric oxide metabolism. Transplantation 57 (1994) 665-669
52. Modolell M., Corraliza I.M., Link F., Soler G., and Eichmann K. Reciprocal regulation of the nitric oxide synthase/arginase balance in mouse bone marrow-derived macrophages by TH1 and TH2 cytokines. Eur J Immunol 25 (1995) 1101-1104
53. Thimme R., Oldach D., Chang K.M., Steiger C., Ray S.C., and Chisari F.V. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J Exp Med 194 (2001) 1395-1406
54. Ehl S., Klenerman P., Zinkernagel R.M., and Bocharov G. The impact of variation in the number of CD8 (+) T-cell precursors on the outcome of virus infection. Cell Immunol 189 (1998) 67-73
55. Zinkernagel R.M. Localization dose and time of antigens determine immune reactivity. Semin Immunol 12 (2000) 163-171 discussion 257-344
56. Vergani D., and Mieli-Vergani G. Viral hepatitis: virus/host interaction. J Gastroenterol Hepatol 19 (2004) S307-S310
57. Mattingly J.A. Immunologic suppression after oral administration of antigen. III. Activation of suppressor-inducer cells in the Peyer's patches. Cell Immunol 86 (1984) 46-52
58. Sun J.B., Czerkinsky C., and Holmgren J. Sublingual 'oral tolerance' induction with antigen conjugated to cholera toxin B subunit generates regulatory T cells that induce apoptosis and depletion of effector T cells. Scand J Immunol 66 (2007) 278-286
59. Sulzberger M.B. Arsphenamine hypersensitiveness in guinea pigs. II. Experiments demonstrating the role of the skin, both as originator and as site of the hypersensitiveness. Arch Dermatol Syphilol 22 (1930) 839-849
60. Chase M.W. Inhibition of experimental drug allergy by prior feeding of the sensitizing agent. Proc Soc Exp Biol Med 61 (1946) 257-259
61. Triger D.R., Cynamon M.H., and Wright R. Studies on hepatic uptake of antigen. I. Comparison of inferior vena cava and portal vein route of immunization. Immunology 25 (1973) 941-950
62. Yang R., Liu Q., Grosfeld J.L., and Pescovitz M.D. Intestinal venous drainage through the liver is a prerequisite for oral tolerance induction. J Pediatr Surg 29 (1994) 1145-1148