NK cells suppress experimental cholestatic liver injury by an interleukin-6-mediated, Kupffer cell-dependent mechanism

Journal of Hepatology

Volumn 54, Issue 4, 2011, Pages 746-752

  Cheng, Chao Wen ^a   Duwaerts, Caroline C ^a   Rooijen, Nico Van ^b,c   Wintermeyer, Philip ^a,d   Mott, Stephanie ^a   Gregory, Stephen H ^a  

^a BROWN UNIVERSITY   (United States)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d UNIVERSITY OF WITTEN HERDECKE   (Germany)

Author keywords

Biliary obstruction; Interleukin 6; Kupffer cell; NK cell

Indexed keywords

ALANINE AMINOTRANSFERASE; CD69 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 6; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BILE DUCT LIGATION; BILE DUCT OBSTRUCTION; CELL ACTIVATION; CHOLESTASIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; FLOW CYTOMETRY; IN VITRO STUDY; IN VIVO STUDY; KUPFFER CELL; LIVER INJURY; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; T CELL DEPLETION;

ADAPTIVE IMMUNITY; ANIMALS; CHOLESTASIS; DISEASE MODELS, ANIMAL; FEMALE; INTERFERON-GAMMA; INTERLEUKIN-6; KILLER CELLS, NATURAL; KUPFFER CELLS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECOMBINANT PROTEINS;

EID: 79952702661     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2010.07.018     Document Type: Article

References (38)

1. Herberman RB, Nunn ME, Holden HT, Lavrin DH. Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic and allogeneic tumors. II. Characterization of effector cells. Int J Cancer 1975;16:230-239.
2. Vales-Gomez M, Reyburn H, Strominger J. Interaction between the human NK receptors and their ligands. Crit Rev Immunol 2000;20:223-244. (Pubitemid 30645021)
3. Piccioli D, Sbrana S, Melandri E, Valiante NM. Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells. J Exp Med 2002;195:335-341. (Pubitemid 34461491)
4. Martin-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, Lanzavecchia A, et al. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol 2004;5:1260-1265. (Pubitemid 41057741)
5. Godshall CJ, Scott MJ, Burch PT, Peyton JC, Cheadle WG. Natural killer cells participate in bacterial clearance during septic peritonitis through interactions with macrophages. Shock 2003;19:144-149.
6. bright NK cells are enriched at inflammatory sites and can engage with monocytes in a reciprocal program of activation. J Immunol 2004;173:6418-6426.
7. + natural T cells with distinct cytotoxic activities and Th1, Th2, and Th0 cytokine secretion patterns. J Immunol 1999;163:2314-2321.
8. Klugewitz K, Adams DH, Emoto M, Eulenburg K, Hamann A. The composition of intrahepatic lymphocytes: shaped by selective recruitment? Trends Immunol 2004;25:590-594.
9. Muhlen KA, Schumann J, Wittke F, Stenger S, van Rooijen N, van Kaer L, et al. NK cells, but not NKT cells, are involved in Pseudomonas aeruginosa exotoxin A-induced hepatotoxicity in mice. J Immunol 2004;172:3034-3041. (Pubitemid 38263692)
10. Dong Z, Wei H, Sun R, Hu Z, Gao B, Tian Z. Involvement of natural killer cells in PolyI:C-induced liver injury. J Hepatol 2004;41:966-973. (Pubitemid 39575664)
11. Gehring S, Dickson EM, San Martin ME, van Rooijen N, Papa EF, Harty MW, et al. Kupffer cells abrogate cholestatic liver injury in mice. Gastroenterology 2006;130:810-822. (Pubitemid 43374530)
12. Kopf M, Baumann H, Freer G, Freudenberg M, Lamers M, Kishimoto T, et al. Impaired immune and acute-phase response in interleukin-6-deficient mice. Nature 1994;368:339-341.
13. Cui J, Shin T, Kawano T, Sato H, Kondo E, Toura I, et al. Requirement for Vα14 NKT cells in IL-12-mediated rejection of tumors. Science 1997;278:1623-1626. (Pubitemid 27516281)
14. Wintermeyer P, Cheng CW, Gehring S, Hoffman BL, Holub M, Brossay L, et al. Invariant natural killer T cells suppress the neutrophil inflammatory response in a mouse model of cholestatic liver damage. Gastroenterology 2009;136:1048-1059.
15. Holub M, Cheng CW, Mott S, Wintermeyer P, van Rooijen N, Gregory SH. Neutrophils sequestered in the liver suppress the proinflammatory response of Kupffer cells to systemic bacterial infection. J Immunol 2009;183:3309-3316.
16. +NKT cells to the liver. J Immunol 2000;165:1729-1732.
17. Vanderkerken K, Bouwens L, van Rooijen N, Van den Berg K, Baekeland M, Wisse E. The role of Kupffer cells in the differentiation process of hepatic NK cells. Hepatology 1995;22:283-290.
18. Sheth K, Bankey P. The liver as an immune organ. Curr Opin Crit Care 2001;7:99-104. (Pubitemid 32411398)
19. Crispe IN, Giannandrea M, Klein I, John B, Sampson B, Wuensch S. Cellular and molecular mechanisms of liver tolerance. Immunol Rev 2006;213:101-118. (Pubitemid 44401496)
20. Racanelli V, Rehermann B. The liver as an immunological organ. Hepatology 2006;43:S54-S62.
21. Billiar TR, Maddaus MA, West MA, Dunn DL, Simmons RL. The role of intestinal flora on the interactions between nonparenchymal cells and hepatocytes in coculture. J Surg Res 1988;44:397-403.
22. Bilzer M, Roggel F, Gerbes AL. Role of Kupffer cells in host defense and liver disease. Liver Int 2006;26:1175-1186. (Pubitemid 44741204)
23. Tu Z, Bozorgzadeh A, Pierce RH, Kurtis J, Crispe IN, Orloff MS. TLR-dependent cross talk between human Kupffer cells and NK cells. J Exp Med 2008;205:233-244. (Pubitemid 351185729)
24. Sewnath ME, van der PT, van Noorden CJ, ten Kate FJ, Gouma DJ. Endogenous interferon γ protects against cholestatic liver injury in mice. Hepatology 2002;36:1466-1477.
25. Ezure T, Sakamoto T, Tsuji H, Lunz III JG, Murase N, Fung JJ, et al. The development and compensation of biliary cirrhosis in interleukin-6-deficient mice. Am J Pathol 2000;156:1627-1639. (Pubitemid 30646701)
26. Wuestefeld T, Klein C, Streetz KL, Betz U, Lauber J, Buer J, et al. Interleukin-6/glycoprotein 130-dependent pathways are protective during liver regeneration. J Biol Chem 2003;278:11281-11288. (Pubitemid 36792685)
27. Schoemaker MH, Gommans WM, de la Rosa LC, Homan M, Klok P, Trautwein C, et al. Resistance of rat hepatocytes against bile acid-induced apoptosis in cholestatic liver injury is due to nuclear factor-kappa B activation. J Hepatol 2003;39:153-161. (Pubitemid 36920549)
28. Gujral JS, Liu J, Farhood A, Jaeschke H. Reduced oncotic necrosis in Fas receptor-deficient C57BL/6J-lpr mice after bile duct ligation. Hepatology 2004;40:998-1007. (Pubitemid 39288134)
29. Wang H, Park O, Lafdil F, Shen K, Horiguchi N, Yin S, et al. Interplay of hepatic and myeloid signal transducer and activator of transcription 3 in facilitating liver regeneration via tempering innate immunity. Hepatology 2010;51:1354-1362.
30. Sun R, Park O, Horiguchi N, Kulkarni S, Jeong WI, Sun HY, et al. STAT1 contributes to dsRNA inhibition of liver regeneration after partial hepatectomy in mice. Hepatology 2006;44:955-966. (Pubitemid 46489560)
31. Notas G, Kisseleva T, Brenner D. NK and NKT cells in liver injury and fibrosis. Clin Immunol 2009;130:16-26.
32. Kahraman A, Barreyro FJ, Bronk SF, Werneburg NW, Mott JL, Akazawa Y, et al. TRAIL mediates liver injury by the innate immune system in the bile duct-ligated mouse. Hepatology 2008;47:1317-1330. (Pubitemid 351547918)
33. McMahon CW, Zajac AJ, Jamieson AM, Corral L, Hammer GE, Ahmed R, et al. Viral and bacterial infections induce expression of multiple NK cell receptors in responding CD8(+) T cells. J Immunol 2002;169:1444-1452. (Pubitemid 34809189)
34. Chen L, Calomeni E, Wen J, Ozato K, Shen R, Gao JX. Natural killer dendritic cells are an intermediate of developing dendritic cells. J Leukoc Biol 2007;81:1422-1433. (Pubitemid 46827965)
35. Scott MJ, Hoth JJ, Gardner SA, Peyton JC, Cheadle WG. Natural killer cell activation primes macrophages to clear bacterial infection. Am Surg 2003;69:679-686.
36. Melhem A, Muhanna N, Bishara A, Alvarez CE, Ilan Y, Bishara T, et al. Anti- fibrotic activity of NK cells in experimental liver injury through killing of activated HSC. J Hepatol 2006;45:60-71. (Pubitemid 43850614)
37. Radaeva S, Sun R, Jaruga B, Nguyen VT, Tian Z, Gao B. Natural killer cells ameliorate liver fibrosis by killing activated stellate cells in NKG2D-dependent and tumor necrosis factor-related apoptosis-inducing ligand-dependent manners. Gastroenterology 2006;130:435-452. (Pubitemid 43202042)
38. Seki S, Habu Y, Kawamura T, Takeda K, Dobashi H, Ohkawa T, et al. The liver as a crucial organ in the first line of host defense: the roles of Kupffer cells, natural killer (NK) cells and NK1.1 Ag+ T cells in T helper 1 immune responses. Immunol Rev 2000;174:35-46. (Pubitemid 30201377)