Immune tolerance in liver disease

Hepatology

Volumn 60, Issue 6, 2014, Pages 2109-2117

  Crispe, Ian N ^a  

^a UNIVERSITY OF WASHINGTON MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BONE MARROW CELL; DENDRITIC CELL; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; KUPFFER CELL; LIVER DISEASE; LYMPHOCYTE ACTIVATION; PHYSIOLOGY; T LYMPHOCYTE;

ANIMALS; DENDRITIC CELLS; HUMANS; IMMUNE TOLERANCE; KUPFFER CELLS; LIVER DISEASES; LYMPHOCYTE ACTIVATION; MYELOID CELLS; T-LYMPHOCYTES;

EID: 84911887407     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.27254     Document Type: Review

References (98)

1. Calne RY, Sells RA, Pena JR, Davis DR, Millard PR, Herbertson BM, et al. Induction of immunological tolerance by porcine liver allografts. Nature 1969;223:472-476.
2. Calne RY, White HJ, Binns RM, Herbertson BM, Millard PR, Pena J, et al. Immunosuppressive effects of the orthotopically transplanted porcine liver. Transplant Proc 1969;1:321-324.
3. Calne RY. Immunological tolerance-the liver effect. Immunol Rev 2000;174:280-282.
4. + T cells within the liver. J Immunol 2001;166:5430-5438.
5. + T cells activated locally within the transplanted liver. J Exp Med 2006;203:437-447.
6. Qian S, Lu L, Fu F, Li Y, Li W, Starzl TE, et al. Apoptosis within spontaneously accepted mouse liver allografts: evidence for deletion of cytotoxic T cells and implications for tolerance induction. J Immunol 1997;158:4654-4661.
7. + T lymphocytes but fail to promote survival. Eur J Immunol 1998;28:221-236.
8. + memory T cells. Nature 2006;441:890-893.
9. + T cell help can be essential for primary CD8+ T cell responses in vivo. J Immunol 2003;171:6339-6343.
10. Sun JC, Bevan MJ. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 2003;300:339-342.
11. + T cells after acute infection. Nat Immunol 2004;5:927-933.
12. Barber DL, Wherry EJ, Masopust D, Zhu B, Allison JP, Sharpe AH, et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 2006;439:682-687.
13. Mays LE, Wang L, Lin J, Bell P, Crawford A, Wherry EJ, Wilson JM. AAV8 induces tolerance in murine muscle as a result of poor APC transduction, T cell exhaustion, and minimal MHCI upregulation on target cells. Mol Ther 2014;22:28-41.
14. Decman V, Laidlaw BJ, Doering TA, Leng J, Ertl HC, Goldstein DR, Wherry EJ. Defective CD8 T cell responses in aged mice are due to quantitative and qualitative changes in virus-specific precursors. J Immunol 2012;188:1933-1941.
15. Radziewicz H, Ibegbu CC, Fernandez ML, Workowski KA, Obideen K, Wehbi M, et al. Liver-infiltrating lymphocytes in chronic human hepatitis C virus infection display an exhausted phenotype with high levels of PD-1 and low levels of CD127 expression. J Virol 2007;81:2545-2553.
16. + T cell responses in chronic HCV infection in blood and liver identified by antigen-specific upregulation of CD154. J Hepatol 2010;52:800-811.
17. Shoukry NH, Sidney J, Sette A, Walker CM. Conserved hierarchy of helper T cell responses in a chimpanzee during primary and secondary hepatitis C virus infections. J Immunol 2004;172:483-492.
18. + T cells in chronic hepatitis C virus infection. J Immunol 2002;169:3447-3458.
19. + T lymphocytes after infection with hepatitis C virus. J Virol 2001;75:5550-5558.
20. Saha B, Choudhary MC, Sarin SK. Expression of inhibitory markers is increased on effector memory T cells during hepatitis C virus/HIV coinfection as compared to hepatitis C virus or HIV monoinfection. AIDS 2013;27:2191-2200.
21. Albert ML, Pearce SF, Francisco LM, Sauter B, Roy P, Silverstein RL, Bhardwaj N. Immature dendritic cells phagocytose apoptotic cells via alphavbeta5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J Exp Med 1998;188:1359-1368.
22. Lutz M, Schuler G. Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol 2002;23:445-449.
23. Mosmann TR, Livingstone AM. Dendritic cells: the immune information management experts. Nat Immunol 2004;5:564-566.
24. Kingham TP, Chaudhry UI, Plitas G, Katz SC, Raab J, DeMatteo RP. Murine liver plasmacytoid dendritic cells become potent immunostimulatory cells after Flt-3 ligand expansion. Hepatology 2007;45:445-454.
25. Nattermann J, Zimmermann H, Iwan A, von Lilienfeld-Toal M, Leifeld L, Nischalke HD, et al. Hepatitis C virus E2 and CD81 interaction may be associated with altered trafficking of dendritic cells in chronic hepatitis C. Hepatology 2006;44:945-954.
26. Velazquez VM, Hon H, Ibegbu C, Knechtle SJ, Kirk AD, Grakoui A. Hepatic enrichment and activation of myeloid dendritic cells during chronic hepatitis C virus infection. Hepatology 2012;56:2071-2081.
27. Takahashi K, Asabe S, Wieland S, Garaigorta U, Gastaminza P, Isogawa M, Chisari FV. Plasmacytoid dendritic cells sense hepatitis C virus-infected cells, produce interferon, and inhibit infection. Proc Natl Acad Sci U S A 2010;107:7431-7436.
28. Kelly A, Fahey R, Fletcher JM, Keogh C, Carroll AG, Siddachari R, et al. CD141(+) myeloid dendritic cells are enriched in healthy human liver. J Hepatol 2014;60:135-142.
29. Haniffa M, Shin A, Bigley V, McGovern N, Teo P, See P, et al. Human tissues contain CD141hi cross-presenting dendritic cells with functional homology to mouse CD103+ nonlymphoid dendritic cells. Immunity 2012;37:60-73.
30. Yoshio S, Kanto T, Kuroda S, Matsubara T, Higashitani K, Kakita N, et al. Human blood dendritic cell antigen 3 (BDCA3)(+) dendritic cells are a potent producer of interferon-lambda in response to hepatitis C virus. Hepatology 2013;57:1705-1715.
31. Hsu W, Shu SA, Gershwin E, Lian ZX. The current immune function of hepatic dendritic cells. Cell Mol Immunol 2007;4:321-328.
32. Sumpter TL, Abe M, Tokita D, Thomson AW. Dendritic cells, the liver, and transplantation. Hepatology 2007;46:2021-2031.
33. Ezzelarab M, Thomson AW. Tolerogenic dendritic cells and their role in transplantation. Semin Immunol 2011;23:252-263.
34. Matta BM, Raimondi G, Rosborough BR, Sumpter TL, Thomson AW. IL-27 production and STAT3-dependent upregulation of B7-H1 mediate immune regulatory functions of liver plasmacytoid dendritic cells. J Immunol 2012;188:5227-5237.
35. Liu H, Bakthavatsalam R, Meng Z, Li Z, Li W, Perkins JD, Reyes J. PD-L1 signal on liver dendritic cells is critical for Foxp3(+)CD4(+)CD25(+) Treg and liver tolerance induction in mice. Transplant Proc 2013;45:1853-1855.
36. Higashitani K, Kanto T, Kuroda S, Yoshio S, Matsubara T, Kakita N, et al. Association of enhanced activity of indoleamine 2, 3-dioxygenase in dendritic cells with the induction of regulatory T cells in chronic hepatitis C infection. J Gastroenterol 2013;48:660-670.
37. Sun X, Gong ZJ, Wang ZW, Li T, Zhang JY, Sun HC, et al. IDO-competent-DCs induced by IFN-gamma attenuate acute rejection in rat liver transplantation. J Clin Immunol 2012;32:837-847.
38. Jurgens B, Hainz U, Fuchs D, Felzmann T, Heitger A. Interferon-gamma-triggered indoleamine 2, 3-dioxygenase competence in human monocyte-derived dendritic cells induces regulatory activity in allogeneic T cells. Blood 2009;114:3235-3243.
39. Pillarisetty VG, Katz SC, Bleier JI, Shah AB, Dematteo RP. Natural killer dendritic cells have both antigen presenting and lytic function and in response to CpG produce IFN-gamma via autocrine IL-12. J Immunol 2005;174:2612-2618.
40. Terme M, Mignot G, Ullrich E, Bonmort M, Minard-Colin V, Jacquet A, et al. The dendritic cell-like functions of IFN-producing killer dendritic cells reside in the CD11b+ subset and are licensed by tumor cells. Cancer Res 2009;69:6590-6597.
41. Sun Z, Wada T, Maemura K, Uchikura K, Hoshino S, Diehl AM, Klein AS. Hepatic allograft-derived Kupffer cells regulate T cell response in rats. Liver Transpl 2003;9:489-497.
42. Chen Y, Liu Z, Liang S, Luan X, Long F, Chen J, et al. Role of Kupffer cells in the induction of tolerance of orthotopic liver transplantation in rats. Liver Transpl 2008;14:823-836.
43. + T cells in human hepatocellular carcinoma is mediated by B7-H1/programmed death-1 interactions. Cancer Res 2009;69:8067-8075.
44. Erhardt A, Biburger M, Papadopoulos T, Tiegs G. IL-10, regulatory T cells, and Kupffer cells mediate tolerance in concanavalin A-induced liver injury in mice. Hepatology 2007;45:475-485.
45. Woodson SE, Freiberg AN, Holbrook MR. Differential cytokine responses from primary human Kupffer cells following infection with wild-type or vaccine strain yellow fever virus. Virology 2011;412:188-195.
46. Zhang M, Xu S, Han Y, Cao X. Apoptotic cells attenuate fulminant hepatitis by priming Kupffer cells to produce interleukin-10 through membrane-bound TGF-beta. Hepatology 2011;53:306-316.
47. Yan ML, Wang YD, Tian YF, Lai ZD, Yan LN. Inhibition of allogeneic T-cell response by Kupffer cells expressing indoleamine 2, 3-dioxygenase. World J Gastroenterol 2010;16:636-640.
48. Perez RV, Swanson C, Morgan M, Erickson K, Hubbard NE, German JB. Portal venous transfusion up-regulates Kupffer cell cyclooxygenase activity: a mechanism of immunosuppression in organ transplantation. Transplantation 1997;64:135-139.
49. Callery MP, Mangino MJ, Flye MW. Arginine-specific suppression of mixed lymphocyte culture reactivity by Kupffer cells-a basis of portal venous tolerance. Transplantation 1991;51:1076-1080.
50. Liu ZJ, Yan LN, Li XH, Xu FL, Chen XF, You HB, Gong JP. Up-regulation of IRAK-M is essential for endotoxin tolerance induced by a low dose of lipopolysaccharide in Kupffer cells. J Surg Res 2008;150:34-39.
51. Uhrig A, Banafsche R, Kremer M, Hegenbarth S, Hamann A, Neurath M, et al. Development and functional consequences of LPS tolerance in sinusoidal endothelial cells of the liver. J Leukoc Biol 2005;77:626-633.
52. Tacke F, Zimmermann HW. Macrophage heterogeneity in liver injury and fibrosis. J Hepatol 2014;60:1090-1096.
53. Huang LR, Wohlleber D, Reisinger F, Jenne CN, Cheng RL, Abdullah Z, et al. Intrahepatic myeloid-cell aggregates enable local proliferation of CD8(+) T cells and successful immunotherapy against chronic viral liver infection. Nat Immunol 2013;14:574-583.
54. Klein I, Cornejo JC, Polakos NK, John B, Wuensch SA, Topham DJ, et al. Kupffer cell heterogeneity: functional properties of bone marrow derived and sessile hepatic macrophages. Blood 2007;110:4077-4085.
55. Macatangay BJ, Landay AL, Rinaldo CR. MDSC: a new player in HIV immunopathogenesis. AIDS 2012;26:1567-1569.
56. Brandau S, Moses K, Lang S. The kinship of neutrophils and granulocytic myeloid-derived suppressor cells in cancer: cousins, siblings or twins? Semin Cancer Biol 2013;23:171-182.
57. Kapanadze T, Gamrekelashvili J, Ma C, Chan C, Zhao F, Hewitt S, et al. Regulation of accumulation and function of myeloid derived suppressor cells in different murine models of hepatocellular carcinoma. J Hepatol 2013;59:1007-1013.
58. Cohen PA, Ko JS, Storkus WJ, Spencer CD, Bradley JM, Gorman JE, et al. Myeloid-derived suppressor cells adhere to physiologic STAT3- vs STAT5-dependent hematopoietic programming, establishing diverse tumor-mediated mechanisms of immunologic escape. Immunol Invest 2012;41:680-710.
59. Yen BL, Yen ML, Hsu PJ, Liu KJ, Wang CJ, Bai CH, Sytwu HK. Multipotent human mesenchymal stromal cells mediate expansion of myeloid-derived suppressor cells via hepatocyte growth factor/c-Met and STAT3. Stem Cell Reports 2013;1:139-151.
60. Chen S, Akbar SM, Abe M, Hiasa Y, Onji M. Immunosuppressive functions of hepatic myeloid-derived suppressor cells of normal mice and in a murine model of chronic hepatitis B virus. Clin Exp Immunol 2011;166:134-142.
61. Limmer A, Ohl J, Wingender G, Berg M, Jungerkes F, Schumak B, et al. Cross-presentation of oral antigens by liver sinusoidal endothelial cells leads to CD8 T cell tolerance. Eur J Immunol 2005;35:2970-2981.
62. Warren A, Bertolino P, Benseler V, Fraser R, McCaughan GW, Le Couteur DG. Marked changes of the hepatic sinusoid in a transgenic mouse model of acute immune-mediated hepatitis. J Hepatol 2007;46:239-246.
63. Knolle PA, Limmer A. Control of immune responses by savenger liver endothelial cells. Swiss Med Wkly 2003;133:501-506.
64. + T cells by liver sinusoidal endothelial cells induces CD25low forkhead box protein 3- regulatory T cells suppressing autoimmune hepatitis. Hepatology 2009;50:1904-1913.
65. Tang L, Yang J, Liu W, Tang X, Chen J, Zhao D, et al. Liver sinusoidal endothelial cell lectin, LSECtin, negatively regulates hepatic T-cell immune response. Gastroenterology 2009;137:1498-1508.e1-e5.
66. Ebrahimkhani MR, Mohar I, Crispe IN. Cross-presentation of antigen by diverse subsets of murine liver cells. Hepatology 2011;54:1379-1387.
67. + T cell tolerance. Eur J Immunol 2006;36:2960-2970.
68. Winau F, Hegasy G, Weiskirchen R, Weber S, Cassan C, Sieling PA, et al. Ito cells are liver-resident antigen-presenting cells for activating T cell responses. Immunity 2007;26:117-129.
69. Chen CH, Kuo LM, Chang Y, Wu W, Goldbach C, Ross MA, et al. In vivo immune modulatory activity of hepatic stellate cells in mice. Hepatology 2006;44:1171-1181.
70. Charles R, Chou HS, Wang L, Fung JJ, Lu L, Qian S. Human hepatic stellate cells inhibit T-cell response through B7-H1 pathway. Transplantation 2013;96:17-24.
71. Yang HR, Chou HS, Gu X, Wang L, Brown KE, Fung JJ, et al. Mechanistic insights into immunomodulation by hepatic stellate cells in mice: a critical role of interferon-gamma signaling. Hepatology 2009;50:1981-1991.
72. + regulatory T cells by production of retinoic acid. J Immunol 2013;190:2009-2016.
73. Hochst B, Schildberg FA, Sauerborn P, Gabel YA, Gevensleben H, Goltz D, et al. Activated human hepatic stellate cells induce myeloid derived suppressor cells from peripheral blood monocytes in a CD44-dependent fashion. J Hepatol 2013;59:528-535.
74. Thompson C, Powrie F. Regulatory T cells. Curr Opin Pharmacol 2004;4:408-414.
75. + regulatory T cells. J Immunol 2006;177:6952-6961.
76. Li W, Carper K, Zheng XX, Kuhr CS, Reyes JD, Liang Y, et al. The role of Foxp3+ regulatory T cells in liver transplant tolerance. Transplant Proc 2006;38:3205-3206.
77. Yang ZF, Ngai P, Lau CK, Ho DW, Tam KH, Lam CT, et al. Induction of long-term liver allograft survival by delayed immunosuppression is dependent on interleukin-10. Liver Transpl 2007;13:571-578.
78. Demirkiran A, Baan CC, Kok A, Metselaar HJ, Tilanus HW, van der Laan LJ. Intrahepatic detection of FOXP3 gene expression after liver transplantation using minimally invasive aspiration biopsy. Transplantation 2007;83:819-823.
79. + regulatory T cells detach from the graft and circulate in recipients after liver transplantation. J Immunol 2007;178:6066-6072.
80. Flye MW, Duffy BF, Phelan DL, Ratner LE, Mohanakumar T. Protective effects of liver transplantation on a simultaneously transplanted kidney in a highly sensitized patient. Transplantation 1990;50:1051-1054.
81. + cells accompany allograft rejection in pediatric liver allograft recipients. Pediatr Transplant 2009;13:70-80.
82. + regulatory T cells in an IL-2-dependent manner. Transplantation 2008;86:1492-1502.
83. Oo YH, Weston CJ, Lalor PF, Curbishley SM, Withers DR, Reynolds GM, et al. Distinct roles for CCR4 and CXCR3 in the recruitment and positioning of regulatory T cells in the inflamed human liver. J Immunol 2010;184:2886-2898.
84. Riezu-Boj JI, Larrea E, Aldabe R, Guembe L, Casares N, Galeano E, et al. Hepatitis C virus induces the expression of CCL17 and CCL22 chemokines that attract regulatory T cells to the site of infection. J Hepatol 2011;54:422-431.
85. Loo YM, Owen DM, Li K, Erickson AK, Johnson CL, Fish PM, et al. Viral and therapeutic control of IFN-beta promoter stimulator 1 during hepatitis C virus infection. Proce Natl Acad Sci U S A 2006;103:6001-6006.
86. Ferreon JC, Ferreon AC, Li K, Lemon SM. Molecular determinants of TRIF proteolysis mediated by the hepatitis C virus NS3/4A protease. J Biol Chem 2005;280:20483-20492.
87. Qu L, Feng Z, Yamane D, Liang Y, Lanford RE, Li K, Lemon SM. Disruption of TLR3 signaling due to cleavage of TRIF by the hepatitis A virus protease-polymerase processing intermediate, 3CD. PLoS Pathog 2011;7:e1002169.
88. Lazear HM, Lancaster A, Wilkins C, Suthar MS, Huang A, Vick SC, et al. IRF-3, IRF-5, and IRF-7 coordinately regulate the type I IFN response in myeloid dendritic cells downstream of MAVS signaling. PLoS Pathog 2013;9:e1003118.
89. Hahn CS, Cho YG, Kang BS, Lester IM, Hahn YS. The HCV core protein acts as a positive regulator of fas-mediated apoptosis in a human lymphoblastoid T cell line. Virology 2000;276:127-137.
90. Large MK, Kittlesen DJ, Hahn YS. Suppression of host immune response by the core protein of hepatitis C virus: possible implications for hepatitis C virus persistence. J Immunol 1999;162:931-938.
91. Tu Z, Pierce RH, Kurtis J, Kuroki Y, Crispe IN, Orloff MS. Hepatitis C virus core protein subverts the antiviral activities of human Kupffer cells. Gastroenterology 2010;138:305-314.
92. Sene D, Levasseur F, Abel M, Lambert M, Camous X, Hernandez C, et al. Hepatitis C virus (HCV) evades NKG2D-dependent NK cell responses through NS5A-mediated imbalance of inflammatory cytokines. PLoS Pathog 2010;6:e1001184.
93. Diehl GE, Yue HH, Hsieh K, Kuang AA, Ho M, Morici LA, et al. TRAIL-R as a negative regulator of innate immune cell responses. Immunity 2004;21:877-889.
94. de Paus RA, van Wengen A, Schmidt I, Visser M, Verdegaal EM, van Dissel JT, van de Vosse E. Inhibition of the type I immune responses of human monocytes by IFN-alpha and IFN-beta. Cytokine 2013;61:645-655.
95. Takahara T, Fukuyama Y, Saito S, Ogino T, Miyajima N, Kohase M. Il-1, EGF, and HGF suppress the antiviral activity of interferon in primary monkey hepatic parenchymal cells. Jpn J Infect Dis 1999;52:45-48.
96. Guidotti LG, Chisari FV. To kill or to cure: options in host defense against viral infection. Curr Opin Immunol 1996;8:478-483.
97. Guidotti LG, Chisari FV. Noncytolytic control of viral infections by the innate and adaptive immune response. Annu Rev Immunol 2001;19:65-91.
98. Rehermann B, Chang KM, McHutchison JG, Kokka R, Houghton M, Chisari FV. Quantitative analysis of the peripheral blood cytotoxic T lymphocyte response in patients with chronic hepatitis C virus infection. J Clin Invest 1996;98:1432-1440.