Kupffer cells potentiate liver sinusoidal endothelial cell injury in sepsis by ligating programmed cell death ligand-1

Journal of Leukocyte Biology

Volumn 94, Issue 5, 2013, Pages 963-970

  Hutchins, Noelle A ^a,b   Wang, Fei ^b   Wang, Yvonne ^b   Chung, Chun Shiang ^b   Ayala, Alfred ^b  

^a BROWN UNIVERSITY   (United States)

^b RHODE ISLAND HOSPITAL   (United States)

Author keywords

Acute liver failure; Coinhibitory molecules; Hepatic endothelium; Liver immune tolerance; Septic inflammation

Indexed keywords

PROGRAMMED DEATH 1 LIGAND 1; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENDOTHELIUM INJURY; KUPFFER CELL; LIVER CELL DAMAGE; LIVER SINUSOIDAL ENDOTHELIAL CELL INJURY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEPSIS;

ACUTE LIVER FAILURE; COINHIBITORY MOLECULES; HEPATIC ENDOTHELIUM; LIVER IMMUNE TOLERANCE; SEPTIC INFLAMMATION;

ANIMALS; ANTIGENS, CD274; ANTIGENS, CD95; APOPTOSIS; CAPILLARY PERMEABILITY; CELL PROLIFERATION; ENDOTHELIAL CELLS; KUPFFER CELLS; LIVER; MALE; MICE; MICE, INBRED C57BL; SEPSIS; STAT3 TRANSCRIPTION FACTOR;

EID: 84887006158     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0113051     Document Type: Article

References (56)

1. Angus, D. C., Linde-Zwirble, W. T., Lidicker, J., Clermont, G., Carcillo, J., Pinsky, M. R. (2001) Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 29, 1303-1310.
2. Canabal, J. M., Kramer, D. J. (2008) Management of sepsis in patients with liver failure. Curr. Opin. Crit. Care 14, 189-197.
3. Aird, W. C. (2003) The role of the endothelium in severe sepsis and multiple organ dysfunction syndrome. Blood 101, 3765-3777.
4. Hutchins, N. A., Chung, C. S., Borgerding, J. N., Ayala, C. A., Ayala, A. (2013) Kupffer cells protect liver sinusoidal endothelial cells from Fasdependent apoptosis in sepsis by down-regulating gp130. Am. J. Pathol. 182, 742-754.
5. Crispe, I. N. (2009) The liver as a lymphoid organ. Annu. Rev. Immunol. 27, 147-163.
6. Tiegs, G., Lohse, A. W. (2010) Immune tolerance: what is unique about the liver. J. Autoimmun. 34, 1-6.
7. Calne, R. Y., Sells, R. A., Pena, J. R., Davis, D. R., Millard, P. R., Herbertson, B. M., Binns, R. M., Davies, D. A. (1969) Induction of immunological tolerance by porcine liver allografts. Nature 223, 472-476.
8. Limmer, A., Ohl, J., Kurts, C., Ljunggren, H. G., Reiss, Y., Groettrup, M., Momburg, F., Arnold, B., Knolle, P. A. (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.
9. Diehl, L., Schurich, A., Grochtmann, R., Hegenbarth, S., Chen, L., Knolle, P. A. (2008) Tolerogenic maturation of liver sinusoidal endothelial cells promotes B7-homolog 1-dependent CD8 T cell tolerance. Hepatology 47, 296-305.
10. Freeman, G. J., Long, A. J., Iwai, Y., Bourque, K., Chernova, T., Nishimura, H., Fitz, L. J., Malenkovich, N., Okazaki, T., Byrne, M. C., Horton, H. F., Fouser, L., Carter, L., Ling, V., Bowman, M. R., Carreno, B. M., Collins, M., Wood, C. R., 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.
11. Day, C. L., Kaufmann, D. E., Kiepiela, P., Brown, J. A., Moodley, E. S., Reddy, S., Mackey, E. W., Miller, J. D., Leslie, A. J., DePierres, C., Mncube, Z., Duraiswamy, J., Zhu, B., Eichbaum, Q., Altfeld, M., Wherry, E. J., Coovadia, H. M., Goulder, P. J., Klenerman, P., Ahmed, R., Freeman, G. J., Walker, B. D. (2006) PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 443, 350-354.
12. Dong, H., Strome, S. E., Salomao, D. R., Tamura, H., Hirano, F., Flies, D. B., Roche, P. C., Lu, J., Zhu, G., Tamada, K., Lennon, V. A., Celis, E., Chen, L. (2002) Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat. Med. 8, 793-800.
13. Huang, X., Venet, F., Wang, Y. L., Lepape, A., Yuan, Z., Chen, Y., Swan, R., Kherouf, H., Monneret, G., Chung, C. S., Ayala, A. (2009) PD-1 expression by macrophages plays a pathologic role in altering microbial clearance and the innate inflammatory response to sepsis. Proc. Natl. Acad. Sci. USA 106, 6303-6308.
14. Brahmamdam, P., Inoue, S., Unsinger, J., Chang, K. C., McDunn, J. E., Hotchkiss, R. S. (2010) Delayed administration of anti-PD-1 antibody reverses immune dysfunction and improves survival during sepsis. J. Leukoc. Biol. 88, 233-240.
15. Zhang, Y., Zhou, Y., Lou, J., Li, J., Bo, L., Zhu, K., Wan, X., Deng, X., Cai, Z. (2010) PD-L1 blockade improves survival in experimental sepsis by inhibiting lymphocyte apoptosis and reversing monocyte dysfunction. Crit. Care 14, R220.
16. Jin, Y., Chauhan, S. K., El Annan, J., Sage, P. T., Sharpe, A. H., Dana, R. (2011) A novel function for programmed death ligand-1 regulation of angiogenesis. Am. J. Pathol. 178, 1922-1929.
17. Rittirsch, D., Huber-Lang, M. S., Flierl, M. A., Ward, P. A. (2009) Immunodesign of experimental sepsis by cecal ligation and puncture. Nat. Protoc. 4, 31-36.
18. Wesche-Soldato, D. E., Chung, C. S., Lomas-Neira, J., Doughty, L. A., Gregory, S. H., Ayala, A. (2005) In vivo delivery of caspase-8 or Fas siRNA improves the survival of septic mice. Blood 106, 2295-2301.
19. Zellweger, R. M., Prestwood, T. R., Shresta, S. (2010) Enhanced infection of liver sinusoidal endothelial cells in a mouse model of antibody-induced severe dengue disease. Cell Host Microbe 7, 128-139.
20. Katz, S. C., Pillarisetty, V. G., Bleier, J. I., Shah, A. B., DeMatteo, R. P. (2004) Liver sinusoidal endothelial cells are insufficient to activate T cells. J. Immunol. 173, 230-235.
21. Hotchkiss, R. S., Coopersmith, C. M., McDunn, J. E., Ferguson, T. A. (2009) The sepsis seesaw: tilting toward immunosuppression. Nat. Med. 15, 496-497.
22. Wolfle, S. J., Strebovsky, J., Bartz, H., Sahr, A., Arnold, C., Kaiser, C., Dalpke, A. H., Heeg, K. (2011) PD-L1 expression on tolerogenic APCs is controlled by STAT-3. Eur. J. Immunol. 41, 413-424.
23. Haga, S., Terui, K., Zhang, H. Q., Enosawa, S., Ogawa, W., Inoue, H., Okuyama, T., Takeda, K., Akira, S., Ogino, T., Irani, K., Ozaki, M. (2003) Stat3 protects against Fas-induced liver injury by redox-dependent and-independent mechanisms. J. Clin. Invest. 112, 989-998.
24. Wesche-Soldato, D. E., Chung, C. S., Gregory, S. H., Salazar-Mather, T. P., Ayala, C. A., Ayala, A. (2007) CD8 T cells promote inflammation and apoptosis in the liver after sepsis: role of Fas-FasL. Am. J. Pathol. 171, 87-96.
25. Lohse, A. W., Knolle, P. A., Bilo, K., Uhrig, A., Waldmann, C., Ibe, M., Schmitt, E., Gerken, G., Meyer Zum Buschenfelde, H. (1996) Antigenpresenting function and B7 expression of murine sinusoidal endothelial cells and Kupffer cells. Gastroenterology 110, 1175-1181.
26. Ishida, Y., Agata, Y., Shibahara, K., Honjo, T. (1992) Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J. 11, 3887-3895.
27. Barber, D. L., Wherry, E. J., Masopust, D., Zhu, B., Allison, J. P., Sharpe, A. H., Freeman, G. J., Ahmed, R. (2006) Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439, 682-687.
28. Yancopoulos, G. D., Davis, S., Gale, N. W., Rudge, J. S., Wiegand, S. J., Holash, J. (2000) Vascular-specific growth factors and blood vessel formation. Nature 407, 242-248.
29. Scholzen, T., Gerdes, J. (2000) The Ki-67 protein: from the known and the unknown. J. Cell. Physiol. 182, 311-322.
30. Antoine, N., Greimers, R., De Roanne, C., Kusaka, M., Heinen, E., Simar, L. J., Castronovo, V. (1994) AGM-1470, a potent angiogenesis inhibitor, prevents the entry of normal but not transformed endothelial cells into the G1 phase of the cell cycle. Cancer Res. 54, 2073-2076.
31. Kurniali, P. C., O'Gara, K., Wang, X., Wang, L. J., Somasundar, P., Falanga, V., Espat, N. J., Katz, S. C. (2012) The effects of sorafenib on liver regeneration in a model of partial hepatectomy. J. Surg. Res. 178, 242-247.
32. Lee, S. H., Starkey, P. M., Gordon, S. (1985) Quantitative analysis of total macrophage content in adult mouse tissues. Immunochemical studies with monoclonal antibody F4/80. J. Exp. Med. 161, 475-489.
33. Schurich, A., Berg, M., Stabenow, D., Bottcher, J., Kern, M., Schild, H. J., Kurts, C., Schuette, V., Burgdorf, S., Diehl, L., Limmer, A., Knolle, P. A. (2010) Dynamic regulation of CD8 T cell tolerance induction by liver sinusoidal endothelial cells. J. Immunol. 184, 4107-4114.
34. Carambia, A., Frenzel, C., Bruns, O. T., Schwinge, D., Reimer, R., Hohenberg, H., Huber, S., Tiegs, G., Schramm, C., Lohse, A. W., Herkel, J. (2012) Inhibition of inflammatory CD4 T cell activity by murine liver sinusoidal endothelial cells. J. Hepatol. 58, 112-118.
35. Rodig, N., Ryan, T., Allen, J. A., Pang, H., Grabie, N., Chernova, T., Greenfield, E. A., Liang, S. C., Sharpe, A. H., Lichtman, A. H., Freeman, G. J. (2003) Endothelial expression of PD-L1 and PD-L2 down-regulates CD8 T cell activation and cytolysis. Eur. J. Immunol. 33, 3117-3126.
36. Kassel, R., Cruise, M. W., Iezzoni, J. C., Taylor, N. A., Pruett, T. L., Hahn, Y. S. (2009) Chronically inflamed livers up-regulate expression of inhibitory B7 family members. Hepatology 50, 1625-1637.
37. Wang, B. J., Bao, J. J., Wang, J. Z., Wang, Y., Jiang, M., Xing, M. Y., Zhang, W. G., Qi, J. Y., Roggendorf, M., Lu, M. J., Yang, D. L. (2011) Immunostaining of PD-1/PD-Ls in liver tissues of patients with hepatitis and hepatocellular carcinoma. World J. Gastroenterol. 17, 3322-3329.
38. Xie, Z., Chen, Y., Zhao, S., Yang, Z., Yao, X., Guo, S., Yang, C., Fei, L., Zeng, X., Ni, B., Wu, Y. (2009) Intrahepatic PD-1/PD-L1 up-regulation closely correlates with inflammation and virus replication in patients with chronic HBV infection. Immunol. Invest. 38, 624-638.
39. Larrubia, J. R., Benito-Martinez, S., Miquel, J., Calvino, M., Sanz-de-Villalobos, E., Parra-Cid, T. (2009) Costimulatory molecule programmed death-1 in the cytotoxic response during chronic hepatitis C. World J. Gastroenterol. 15, 5129-5140.
40. Zhang, H. G., Su, X., Liu, D., Liu, W., Yang, P., Wang, Z., Edwards, C. K., Bluethmann, H., Mountz, J. D., Zhou, T. (1999) Induction of specific T cell tolerance by Fas ligand-expressing antigen-presenting cells. J. Immunol. 162, 1423-1430.
41. Askenasy, N., Yolcu, E. S., Yaniv, I., Shirwan, H. (2005) Induction of tolerance using Fas ligand: a double-edged immunomodulator. Blood 105, 1396-1404.
42. Van Parijs, L., Ibraghimov, A., Abbas, A. K. (1996) The roles of costimulation and Fas in T cell apoptosis and peripheral tolerance. Immunity 4, 321-328.
43. Wajant, H. (2002) The Fas signaling pathway: more than a paradigm. Science 296, 1635-1636.
44. Keir, M. E., Butte, M. J., Freeman, G. J., Sharpe, A. H. (2008) PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 26, 677-704.
45. Uda, Y., Hirano, T., Son, G., Iimuro, Y., Uyama, N., Yamanaka, J., Mori, A., Arii, S., Fujimoto, J. (2013) Angiogenesis is crucial for liver regeneration after partial hepatectomy. Surgery 153, 70-77.
46. Wang, L., Wang, X., Xie, G., Wang, L., Hill, C. K., DeLeve, L. D. (2012) Liver sinusoidal endothelial cell progenitor cells promote liver regeneration in rats. J. Clin. Invest. 122, 1567-1573.
47. Yano, K., Liaw, P. C., Mullington, J. M., Shih, S. C., Okada, H., Bodyak, N., Kang, P. M., Toltl, L., Belikoff, B., Buras, J., Simms, B. T., Mizgerd, J. P., Carmeliet, P., Karumanchi, S. A., Aird, W. C. (2006) Vascular endothelial growth factor is an important determinant of sepsis morbidity and mortality. J. Exp. Med. 203, 1447-1458.
48. Iwai, Y., Terawaki, S., Ikegawa, M., Okazaki, T., Honjo, T. (2003) PD-1 inhibits antiviral immunity at the effector phase in the liver. J. Exp. Med. 198, 39-50.
49. Zhang, Y., Li, J., Lou, J., Zhou, Y., Bo, L., Zhu, J., Zhu, K., Wan, X., Cai, Z., Deng, X. (2011) Upregulation of programmed death-1 on T cells and programmed death ligand-1 on monocytes in septic shock patients. Crit. Care 15, R70.
50. Oikawa, T., Takahashi, H., Ishikawa, T., Hokari, A., Otsuki, N., Azuma, M., Zeniya, M., Tajiri, H. (2007) Intrahepatic expression of the co-stimulatory molecules programmed death-1, and its ligands in autoimmune liver disease. Pathol. Int. 57, 485-492.
51. Wu, K., Kryczek, I., Chen, L., Zou, W., Welling, T. H. (2009) Kupffer cell suppression of CD8 T cells in human hepatocellular carcinoma is mediated by B7-H1/programmed death-1 interactions. Cancer Res. 69, 8067-8075.
52. Latchman, Y. E., Liang, S. C., Wu, Y., Chernova, T., Sobel, R. A., Klemm, M., Kuchroo, V. K., Freeman, G. J., Sharpe, A. H. (2004) PD-L1-deficient mice show that PD-L1 on T cells, antigen-presenting cells, and host tissues negatively regulates T cells. Proc. Natl. Acad. Sci. USA 101, 10691-10696.
53. Goyert, S. M., Silver, J. (2010) Editorial: PD-1, a new target for sepsis treatment: better late than never. J. Leukoc. Biol. 88, 225-226.
54. Loke, P., Allison, J. P. (2003) PD-L1 and PD-L2 are differentially regulated by Th1 and Th2 cells. Proc. Natl. Acad. Sci. USA 100, 5336-5341.
55. Heymann, F., Trautwein, C., Tacke, F. (2009) Monocytes and macrophages as cellular targets in liver fibrosis. Inflamm. Allergy Drug Targets 8, 307-318.
56. Karlmark, K. R., Weiskirchen, R., Zimmermann, H. W., Gassler, N., Ginhoux, F., Weber, C., Merad, M., Luedde, T., Trautwein, C., Tacke, F. (2009) Hepatic recruitment of the inflammatory Gr1 monocyte subset upon liver injury promotes hepatic fibrosis. Hepatology 50, 261-274.