Liver sinusoidal endothelial cell cross-priming is supported by CD4 T cell-derived IL-2

Journal of Hepatology

Volumn 66, Issue 5, 2017, Pages 978-986

  Wittlich, Michaela ^a   Dudek, Michael ^b   Böttcher, Jan P ^a   Schanz, Oliver ^a   Hegenbarth, Silke ^b   Bopp, Tobias ^c   Schmitt, Edgar ^c   Kurts, Christian ^a   Garbers, Christoph ^d   Rose John, Stefan ^d   Knolle, Percy A ^a,b   Wohlleber, Dirk ^b  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^d UNIVERSITY OF KIEL   (Germany)

Author keywords

CD4 T cell help; IL 6 trans signaling; Liver primed T cells; LSEC

Indexed keywords

CD28 ANTIGEN; CD3 ANTIBODY; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GRANZYME B; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; PATTERN RECOGNITION RECEPTOR; T LYMPHOCYTE RECEPTOR; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR T BET; VASCULAR CELL ADHESION MOLECULE 1; GRANZYME;

ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CROSS PRESENTATION; CYTOKINE RELEASE; ENDOTHELIUM CELL; ENZYME INDUCTION; FEMALE; FLOW CYTOMETRY; HEPATIC STELLATE CELL; LYMPHOCYTE FUNCTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TH1 CELL; ANIMAL; C57BL MOUSE; CELL COMMUNICATION; CELL CULTURE; IMMUNOLOGY; LIVER; PHYSIOLOGY;

ANIMALS; ANTIGEN-PRESENTING CELLS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL COMMUNICATION; CELLS, CULTURED; CROSS-PRIMING; ENDOTHELIAL CELLS; GRANZYMES; INTERLEUKIN-2; LIVER; MICE; MICE, INBRED C57BL;

EID: 85010402409     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2016.12.015     Document Type: Article

References (37)

1. [1] Schoenberger, S.P., Toes, R.E., van der Voort, E.I., Offringa, R., Melief, C.J., T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 393 (1998), 480–483.
2. [2] Bennett, S.R., Carbone, F.R., Karamalis, F., Flavell, R.A., Miller, J.F., Heath, W.R., Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 393 (1998), 478–480.
3. [3] Burgdorf, S., Scholz, C., Kautz, A., Tampe, R., Kurts, C., Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation. Nat Immunol 9 (2008), 558–566.
4. [4] Bousso, P., Robey, E., Dynamics of CD8+ T cell priming by dendritic cells in intact lymph nodes. Nat Immunol 4 (2003), 579–585.
5. [5] Castellino, F., Huang, A.Y., Altan-Bonnet, G., Stoll, S., Scheinecker, C., Germain, R.N., Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell-dendritic cell interaction. Nature 440 (2006), 890–895.
6. [6] Janssen, E.M., Lemmens, E.E., Wolfe, T., Christen, U., von Herrath, M.G., Schoenberger, S.P., CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 421 (2003), 852–856.
7. [7] Greyer, M., Whitney, P.G., Stock, A.T., Davey, G.M., Tebartz, C., Bachem, A., et al. T cell help amplifies innate signals in CD8(+) DCs for optimal CD8(+) T cell priming. Cell Reports 14 (2016), 586–597.
8. [8] Sun, J.C., Bevan, M.J., Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 300 (2003), 339–342.
9. [9] Shedlock, D.J., Shen, H., Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300 (2003), 337–339.
10. [10] Knolle, P.A., Schmitt, E., Jin, S., Germann, T., Duchmann, R., Hegenbarth, S., et al. 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 (1999), 1428–1440.
11. [11] Limmer, A., Ohl, J., Kurts, C., Ljunggren, H.G., Reiss, Y., Groettrup, M., et al. Efficient presentation of exogenous antigen by liver endothelial cells to CD8+ T cells results in antigen-specific T-cell tolerance. Nat Med 6 (2000), 1348–1354.
12. [12] Carambia, A., Freund, B., Schwinge, D., Heine, M., Laschtowitz, A., Huber, S., et al. TGF-beta-dependent induction of CD4(+)CD25(+)Foxp3(+) Tregs by liver sinusoidal endothelial cells. J Hepatol 61 (2014), 594–599.
13. [13] Neumann, K., Rudolph, C., Neumann, C., Janke, M., Amsen, D., Scheffold, A., Liver sinusoidal endothelial cells induce immunosuppressive IL-10-producing Th1 cells via the Notch pathway. Eur J Immunol 45 (2015), 2008–2016.
14. [14] Böttcher, J.P., Schanz, O., Wohlleber, D., Abdullah, Z., Debey-Pascher, S., Staratschek-Jox, A., et al. Liver-primed memory T cells generated under noninflammatory conditions provide anti-infectious immunity. Cell Reports 3 (2013), 779–795.
15. [15] Böttcher, J.P., Schanz, O., Garbers, C., Zaremba, A., Hegenbarth, S., Kurts, C., et al. IL-6 trans-signaling-dependent rapid development of cytotoxic CD8(+) T cell function. Cell Reports 8 (2014), 1318–1327.
16. [16] Rose-John, S., IL-6 trans-signaling via the soluble IL-6 receptor: importance for the pro-inflammatory activities of IL-6. Int J Biol Sci 8 (2012), 1237–1247.
17. [17] Diehl, L., Schurich, A., Grochtmann, R., Hegenbarth, S., Chen, L., Knolle, P.A., Tolerogenic maturation of liver sinusoidal endothelial cells promotes B7-homolog 1-dependent CD8+ T cell tolerance. Hepatology 47 (2008), 296–305.
18. [18] Fischer, M., Goldschmitt, J., Peschel, C., Brakenhoff, J.P., Kallen, K.J., Wollmer, A., et al. I. A bioactive designer cytokine for human hematopoietic progenitor cell expansion. Nat Biotechnol 15 (1997), 142–145.
19. [19] Schroers, A., Hecht, O., Kallen, K.J., Pachta, M., Rose-John, S., Grotzinger, J., Dynamics of the gp130 cytokine complex: a model for assembly on the cellular membrane. Protein Sci 14 (2005), 783–790.
20. [20] Schurich, A., Bottcher, J.P., Burgdorf, S., Penzler, P., Hegenbarth, S., Kern, M., et al. Distinct kinetics and dynamics of cross-presentation in liver sinusoidal endothelial cells compared to dendritic cells. Hepatology 50 (2009), 909–919.
21. [21] Semmling, V., Lukacs-Kornek, V., Thaiss, C.A., Quast, T., Hochheiser, K., Panzer, U., et al. Alternative cross-priming through CCL17-CCR4-mediated attraction of CTLs toward NKT cell-licensed DCs. Nat Immunol 11 (2010), 313–320.
22. [22] Crispe, I.N., The liver as a lymphoid organ. Annu Rev Immunol 27 (2009), 147–163.
23. [23] Thomson, A.W., Knolle, P.A., Antigen-presenting cell function in the tolerogenic liver environment. Nat Rev Immunol 10 (2010), 753–766.
24. [24] Lohse, A.W., Knolle, P.A., Bilo, K., Uhrig, A., Waldmann, C., Ibe, M., et al. Antigen-presenting function and B7 expression of murine sinusoidal endothelial cells and Kupffer cells. Gastroenterology 110 (1996), 1175–1181.
25. [25] Kurts, C., Robinson, B.W., Knolle, P.A., Cross-priming in health and disease. Nat Rev Immunol 10 (2010), 403–414.
26. [26] Eickhoff, S., Brewitz, A., Gerner, M.Y., Klauschen, F., Komander, K., Hemmi, H., et al. Robust anti-viral immunity requires multiple distinct T cell-dendritic cell interactions. Cell 162 (2015), 1322–1337.
27. [27] von Oppen, N., Schurich, A., Hegenbarth, S., Stabenow, D., Tolba, R., Weiskirchen, R., et al. Systemic antigen cross-presented by liver sinusoidal endothelial cells induces liver-specific CD8 T-cell retention and tolerization. Hepatology 49 (2009), 1664–1672.
28. [28] Guidotti, L.G., Inverso, D., Sironi, L., Di Lucia, P., Fioravanti, J., Ganzer, L., et al. Immunosurveillance of the liver by intravascular effector CD8(+) T cells. Cell 161 (2015), 486–500.
29. [29] Intlekofer, A.M., Takemoto, N., Kao, C., Banerjee, A., Schambach, F., Northrop, J.K., et al. Requirement for T-bet in the aberrant differentiation of unhelped memory CD8+ T cells. J Exp Med 204 (2007), 2015–2021.
30. [30] Bannard, O., Kraman, M., Fearon, D.T., Secondary replicative function of CD8+ T cells that had developed an effector phenotype. Science 323 (2009), 505–509.
31. [31] Williams, M.A., Tyznik, A.J., Bevan, M.J., Interleukin-2 signals during priming are required for secondary expansion of CD8+ memory T cells. Nature 441 (2006), 890–893.
32. [32] Janas, M.L., Groves, P., Kienzle, N., Kelso, A., IL-2 regulates perforin and granzyme gene expression in CD8+ T cells independently of its effects on survival and proliferation. J Immunol 175 (2005), 8003–8010.
33. [33] Tamang, D.L., Redelman, D., Alves, B.N., Vollger, L., Bethley, C., Hudig, D., Induction of granzyme B and T cell cytotoxic capacity by IL-2 or IL-15 without antigens: multiclonal responses that are extremely lytic if triggered and short-lived after cytokine withdrawal. Cytokine 36 (2006), 148–159.
34. [34] Schurich, A., Berg, M., Stabenow, D., Bottcher, J., Kern, M., Schild, H.J., et al. Dynamic regulation of CD8 T cell tolerance induction by liver sinusoidal endothelial cells. J Immunol 184 (2010), 4107–4114.
35. [35] Wieland, S., Thimme, R., Purcell, R.H., Chisari, F.V., Genomic analysis of the host response to hepatitis B virus infection. Proc Natl Acad Sci U S A 101 (2004), 6669–6674.
36. [36] Meylan, E., Curran, J., Hofmann, K., Moradpour, D., Binder, M., Bartenschlager, R., et al. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437 (2005), 1167–1172.
37. [37] Gehring, A.J., Haniffa, M., Kennedy, P.T., Ho, Z.Z., Boni, C., Shin, A., et al. Mobilizing monocytes to cross-present circulating viral antigen in chronic infection. J Clin Invest 123 (2013), 3766–3776.