Natural killer T cells in liver injury, inflammation and cancer

Expert Review of Gastroenterology and Hepatology

Volumn 9, Issue 8, 2015, Pages 1077-1085

  Wang, Hua ^a   Yin, Shi ^a  

^a ANHUI MEDICAL UNIVERSITY   (China)

Author keywords

liver cancer; liver fibrosis; liver injury; liver regeneration; NKT cells

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 22; INTERLEUKIN 4; NATURAL KILLER CELL RECEPTOR NKG2D; STAT6 PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ALCOHOL LIVER CIRRHOSIS; CD8+ T LYMPHOCYTE; CHRONIC LIVER DISEASE; CYTOKINE PRODUCTION; HEPATITIS; HUMAN; LIVER CANCER; LIVER CARCINOGENESIS; LIVER FIBROSIS; LIVER INJURY; LIVER NECROSIS; LIVER REGENERATION; NATURAL KILLER T CELL; NONALCOHOLIC FATTY LIVER; NONHUMAN; REVIEW; STELLATE CELL; T LYMPHOCYTE ACTIVATION; TUMOR GROWTH; ANIMAL; IMMUNOLOGY; LIVER CIRRHOSIS; LIVER TUMOR; PHYSIOLOGY; TOXIC HEPATITIS;

ANIMALS; DRUG-INDUCED LIVER INJURY; HEPATITIS; HUMANS; LIVER CIRRHOSIS; LIVER NEOPLASMS; LIVER REGENERATION; NATURAL KILLER T-CELLS;

EID: 84937574974     PISSN: 17474124     EISSN: 17474132     Source Type: Journal    
DOI: 10.1586/17474124.2015.1056738     Document Type: Review

References (110)

1. Brennan PJ, Brigl M, Brenner MB. Invariant natural killer T cells: an innate activation scheme linked to diverse effector functions. Nat Rev Immunol 2013;13(2): 101-17
2. Kronenberg M, Gapin L. The unconventional lifestyle of NKT cells. Nat Rev Immunol 2002;2(8):557-68
3. Bendelac A, Savage PB, Teyton L. The biology of NKT cells. Annu Rev Immunol 2007;25:297-336
4. Van Kaer L, Parekh VV, Wu L. Invariant natural killer T cells: bridging innate and adaptive immunity. Cell Tissue Res 2011; 343(1):43-55
5. Wu L, Van Kaer L. Natural killer T cells in health and disease. Front Biosci (Schol Ed) 2011;3:236-51
6. Brigl M, Brenner MB. CD1: antigen presentation and T cell function. Annu Rev Immunol 2004;22:817-90
7. Rossjohn J, Pellicci DG, Patel O, et al. Recognition of CD1d-restricted antigens by natural killer T cells. Nat Rev Immunol 2012;12(12):845-57
8. Berzins SP, Smyth MJ, Baxter AG. Presumed guilty: natural killer T cell defects and human disease. Nat Rev Immunol 2011;11(2):131-42
9. Wilson MT, Johansson C, Olivares-Villagomez D, et al. The response of natural killer T cells to glycolipid antigens is characterized by surface receptor down-modulation and expansion. Proc Natl Acad Sci U S A 2003;100(19):10913-18
10. Leite-de-Moraes MC, Herbelin A, Gouarin C, et al. Fas/Fas ligand interactions promote activation-induced cell death of NK T lymphocytes. J Immunol 2000; 165(8):4367-71
11. Parekh VV, Singh AK, Wilson MT, et al. Quantitative and qualitative differences in the in vivo response of NKT cells to distinct alpha- and beta-anomeric glycolipids. J Immunol 2004;173(6): 3693-706
12. Gao B, Radaeva S, Park O. Liver natural killer and natural killer T cells: immunobiology and emerging roles in liver diseases. J Leukoc Biol 2009;86(3):513-28
13. Godfrey DI, Berzins SP. Control points in NKT-cell development. Nat Rev Immunol 2007;7(7):505-18
14. Kawano T, Cui J, Koezuka Y, et al. CD1d-restricted and TCR-mediated activation of valpha14 NKT cells by glycosylceramides. Science 1997;278(5343): 1626-9
15. Velazquez P, Cameron TO, Kinjo Y, et al. Cutting edge: activation by innate cytokines or microbial antigens can cause arrest of natural killer T cell patrolling of liver sinusoids. J Immunol 2008;180(4):2024-8
16. Winau F, Hegasy G, Weiskirchen R, et al. Ito cells are liver-resident antigen-presenting cells for activating T cell responses. Immunity 2007;26(1):117-29
17. Schmieg J, Yang G, Franck RW, et al. Glycolipid presentation to natural killer T cells differs in an organ-dependent fashion. Proc Natl Acad Sci U S A 2005;102(4): 1127-32
18. Geissmann F, Cameron TO, Sidobre S, et al. Intravascular immune surveillance by CXCR6+ NKT cells patrolling liver sinusoids. PLoS Biol 2005;3(4):e113
19. De Santo C, Salio M, Masri SH, et al. Invariant NKT cells reduce the immunosuppressive activity of influenza A virus-induced myeloid-derived suppressor cells in mice and humans. J Clin Invest 2008;118(12):4036-48
20. Zeissig S, Murata K, Sweet L, et al. Hepatitis B virus-induced lipid alterations contribute to natural killer T cell-dependent protective immunity. Nat Med 2012;18(7): 1060-8
21. Emoto M, Mittrucker HW, Schmits R, et al. Critical role of leukocyte function-associated antigen-1 in liver accumulation of CD4+NKT cells. J Immunol 1999;162(9):5094-8
22. Thomas SY, Scanlon ST, Griewank KG, et al. PLZF induces an intravascular surveillance program mediated by long-lived LFA-1-ICAM-1 interactions. J Exp Med 2011;208(6):1179-88
23. Li Z, Oben JA, Yang S, et al. Norepinephrine regulates hepatic innate immune system in leptin-deficient mice with nonalcoholic steatohepatitis. Hepatology 2004;40(2):434-41
24. Syn WK, Witek RP, Curbishley SM, et al. Role for hedgehog pathway in regulating growth and function of invariant NKT cells. Eur J Immunol 2009;39(7):1879-92
25. Syn WK, Agboola KM, Swiderska M, et al. NKT-associated hedgehog and osteopontin drive fibrogenesis in non-alcoholic fatty liver disease. Gut 2012;61(9):1323-9
26. Godfrey DI, MacDonald HR, Kronenberg M, et al. NKT cells: whats in a name? Nat Rev Immunol 2004;4(3):231-7
27. Billerbeck E, Kang YH, Walker L, et al. Analysis of CD161 expression on human CD8+ T cells defines a distinct functional subset with tissue-homing properties. Proc Natl Acad Sci U S A 2010;107(7):3006-11
28. Karadimitris A, Gadola S, Altamirano M, et al. Human CD1d-glycolipid tetramers generated by in vitro oxidative refolding chromatography. Proc Natl Acad Sci U S A 2001;98(6):3294-8
29. Tilloy F, Treiner E, Park SH, et al. An invariant T cell receptor alpha chain defines a novel TAP-independent major histocompatibility complex class Ib-restricted alpha/beta T cell subpopulation in mammals. J Exp Med 1999;189(12): 1907-21
30. Le Bourhis L, Martin E, Peguillet I, et al. Antimicrobial activity of mucosal-associated invariant T cells. Nat Immunol 2010;1(8): 701-8
31. Treiner E, Lantz O. CD1d- and MR1-restricted invariant T cells: of mice and men. Cur Opin Immunol 2006;18(5): 519-26
32. Tang XZ, Jo J, Tan AT, et al. IL-7 licenses activation of human liver intrasinusoidal mucosal-associated invariant T cells. J Immunol 2013;190(7):3142-52
33. Ussher JE, Bilton M, Attwod E, et al. CD161++ CD8+ T cells, including the MAIT cell subset, are specifically activated by IL-12+IL-18 in a TCR-independent manner. Eur J Immunol 2014;44(1): 195-203
34. Santodomingo-Garzon T, Swain MG. Role of NKT cells in autoimmune liver disease. Autoimmun Rev 2011;10(12):793-800
35. Duwaerts CC, Gregory SH. Targeting the diverse immunological functions expressed by hepatic NKT cells. Expert Opin Ther Targets 2011;15(8):973-88
36. Martin-Murphy BV, Kominsky DJ, Orlicky DJ, et al. Increased susceptibility of natural killer T-cell-deficient mice to acetaminophen-induced liver injury. Hepatology 2013;57(4):1575-84
37. Wang H, Feng D, Park O, et al. Invariant NKT cell activation induces neutrophil accumulation and hepatitis: opposite regulation by IL-4 and IFN-gamma. Hepatology 2013;58(4):1474-85
38. Yin S, Wang H, Bertola A, et al. Activation of invariant natural killer T cells impedes liver regeneration by way of both IFNgamma- and IL-4-dependent mechanisms. Hepatology 2014;60(4):1356-66
39. Malhi H, Guicciardi ME, Gores GJ. Hepatocyte death: a clear and present danger. Physiol Rev 2010;90(3):1165-94
40. Gao B, Jeong WI, Tian Z. Liver: An organ with predominant innate immunity. Hepatology 2008;47(2):729-36
41. Jenne CN, Kubes P. Immune surveillance by the liver. Nat Immunol 2013;14(10): 996-1006
42. Liaskou E, Wilson DV, Oo YH. Innate immune cells in liver inflammation. Mediators Inflamm 2012;2012:949157
43. Biburger M, Tiegs G. Alpha-galactosylceramide-induced liver injury in mice is mediated by TNF-alpha but independent of Kupffer cells. J Immunol 2005;175(3):1540-50
44. Takeda K, Hayakawa Y, Van Kaer L, et al. Critical contribution of liver natural killer T cells to a murine model of hepatitis. Proc Natl Acad Sci U S A 2000;97(10):5498-503
45. Biburger M, Tiegs G. Activation-induced NKT cell hyporesponsiveness protects from alpha-galactosylceramide hepatitis and is independent of active transregulatory factors. J Leukoc Biol 2008;84(1):264-79
46. Jaruga B, Hong F, Sun R, et al. Crucial role of IL-4/STAT6 in T cell-mediated hepatitis: up-regulating eotaxins and IL-5 and recruiting leukocytes. J Immunol 2003;171(6):3233-44
47. Louis H, Le Moine A, Flamand V, et al. Critical role of interleukin 5 and eosinophils in concanavalin A-induced hepatitis in mice. Gastroenterology 2002;122(7):2001-10
48. Wondimu Z, Santodomingo-Garzon T, Le T, Swain MG. Protective role of interleukin-17 in murine NKT cell-driven acute experimental hepatitis. Am J Pathol 2010;177(5):2334-46
49. Sun R, Tian Z, Kulkarni S, Gao B. IL-6 prevents T cell-mediated hepatitis via inhibition of NKT cells in CD4+ T celland STAT3-dependent manners. J Immunol 2004;172(9):5648-55
50. Vilarinho S, Ogasawara K, Nishimura S, et al. Blockade of NKG2D on NKT cells prevents hepatitis and the acute immune response to hepatitis B virus. Proc Natl Acad Sci U S A 2007;104(46):18187-92
51. Hosoya S, Ikejima K, Takeda K, et al. Innate immune responses involving natural killer and natural killer T cells promote liver regeneration after partial hepatectomy in mice. Am J Physiol Gastrointest Liver Physiol 2013;304(3):G293-9
52. Kawamura T, Takeda K, Kaneda H, et al. NKG2A inhibits invariant NKT cell activation in hepatic injury. J Immunol 2009;182(1):250-8
53. Mathews S, Feng D, Maricic I, et al. Invariant natural killer T cells contribute to chronic-plus-binge ethanol-mediated liver injury by promoting hepatic neutrophil infiltration. Cell Mol Immunol 2015
54. Maricic I, Sheng H, Marrero I, et al. Inhibition of type I natural killer T cells by retinoids or following sulfatide-mediated activation of type II natural killer T cells attenuates alcoholic liver disease in mice. Hepatology 2015;61(4):1357-69
55. Cui K, Yan G, Xu C, et al. Invariant NKT cells promote alcohol-induced steatohepatitis through interleukin-1beta in mice. J Hepatol 2015;62(6):1311-18
56. Pellicoro A, Ramachandran P, Iredale JP, Fallowfield JA. Liver fibrosis and repair: immune regulation of wound healing in a solid organ. Nat Rev Immunol 2014;14(3): 181-94
57. Lee YA, Wallace MC, Friedman SL. Pathobiology of liver fibrosis: a translational success story. Gut 2015;64(5):830-41
58. Puche JE, Saiman Y, Friedman SL. Hepatic stellate cells and liver fibrosis. Comprehensive Physiology 2013;3(4): 1473-92
59. Friedman SL, Sheppard D, Duffield JS, Violette S. Therapy for fibrotic diseases: nearing the starting line. Sci Transl Med 2013;5(167):167sr161
60. Friedman SL. Evolving challenges in hepatic fibrosis. Nat Rev Gastroenterol Hepatol 2010;7(8):425-36
61. Mitra A, Satelli A, Yan J, et al. IL-30 (IL27p28) attenuates liver fibrosis through inducing NKG2D-rae1 interaction between NKT and activated hepatic stellate cells in mice. Hepatology 2014;60(6):2027-39
62. Miyagi T, Takehara T, Tatsumi T, et al. CD1d-mediated stimulation of natural killer T cells selectively activates hepatic natural killer cells to eliminate experimentally disseminated hepatoma cells in murine liver. Int J Cancer 2003;106(1):81-9
63. Jin Z, Sun R, Wei H, et al. Accelerated liver fibrosis in hepatitis B virus transgenic mice: involvement of natural killer T cells. Hepatology 2011;53(1):219-29
64. Ishikawa S, Ikejima K, Yamagata H, et al. CD1d-restricted natural killer T cells contribute to hepatic inflammation and fibrogenesis in mice. J Hepatol 2011;54(6): 1195-204
65. Park O, Jeong WI, Wang L, et al. Diverse roles of invariant natural killer T cells in liver injury and fibrosis induced by carbon tetrachloride. Hepatology 2009;49(5): 1683-94
66. Gao B, Radaeva S. Natural killer and natural killer T cells in liver fibrosis. Biochim Biophys Acta 2013;1832(7):1061-9
67. Radaeva S, Sun R, Jaruga B, et al. Natural killer cells ameliorate liver fibrosis by killing activated stellate cells in NKG2D-dependent and tumor necrosis factor-related apoptosisinducing ligand-dependent manners. Gastroenterology 2006;130(2):435-52
68. Melhem A, Muhanna N, Bishara A, et al. Anti-fibrotic activity of NK cells in experimental liver injury through killing of activated HSC. J Hepatol 2006;45(1):60-71
69. Krizhanovsky V, Yon M, Dickins RA, et al. Senescence of activated stellate cells limits liver fibrosis. Cell 2008;134(4):657-67
70. Muhanna N, Abu Tair L, Doron S, et al. Amelioration of hepatic fibrosis by NK cell activation. Gut 2011;60(1):90-8
71. Muhanna N, Doron S, Wald O, et al. Activation of hepatic stellate cells after phagocytosis of lymphocytes: A novel pathway of fibrogenesis. Hepatology 2008; 48(3):963-77
72. Jeong WI, Park O, Suh YG, et al. Suppression of innate immunity (natural killer cell/interferon-gamma) in the advanced stages of liver fibrosis in mice. Hepatology 2011;53(4):1342-51
73. Jeong WI, Park O, Gao B. Abrogation of the antifibrotic effects of natural killer cells/interferon-gamma contributes to alcohol acceleration of liver fibrosis. Gastroenterology 2008;134(1):248-58
74. Jeong WI, Park O, Radaeva S, Gao B. STAT1 inhibits liver fibrosis in mice by inhibiting stellate cell proliferation and stimulating NK cell cytotoxicity. Hepatology 2006;44(6):1441-51
75. Wu SJ, Yang YH, Tsuneyama K, et al. Innate immunity and primary biliary cirrhosis: activated invariant natural killer T cells exacerbate murine autoimmune cholangitis and fibrosis. Hepatology 2011; 53(3):915-25
76. Wehr A, Baeck C, Heymann F, et al. Chemokine receptor CXCR6-dependent hepatic NK T Cell accumulation promotes inflammation and liver fibrosis. J Immunol 2013;190(10):5226-36
77. Syn WK, Oo YH, Pereira TA, et al. Accumulation of natural killer T cells in progressive nonalcoholic fatty liver disease. Hepatology 2010;51(6):1998-2007
78. de Lalla C, Galli G, Aldrighetti L, et al. Production of profibrotic cytokines by invariant NKT cells characterizes cirrhosis progression in chronic viral hepatitis. J Immunol 2004;173(2):1417-25
79. Kremer M, Thomas E, Milton RJ, et al. Kupffer cell and interleukin-12-dependent loss of natural killer T cells in hepatosteatosis. Hepatology 2010;51(1): 130-41
80. Guebre-Xabier M, Yang S, Lin HZ, et al. Altered hepatic lymphocyte subpopulations in obesity-related murine fatty livers: potential mechanism for sensitization to liver damage. Hepatology 2000;31(3): 633-40
81. Tajiri K, Shimizu Y, Tsuneyama K, Sugiyama T. Role of liver-infiltrating CD3 +CD56+ natural killer T cells in the pathogenesis of nonalcoholic fatty liver disease. Eur J Gastroenterol Hepatol 2009; 21(6):673-80
82. Michalopoulos GK. Advances in liver regeneration. Expert Rev Gastroenterol Hepatol 2014;8(8):897-907
83. Michalopoulos GK. Liver regeneration after partial hepatectomy: critical analysis of mechanistic dilemmas. Am J Pathol 2010; 176(1):2-13
84. Michalopoulos GK. Principles of liver regeneration and growth homeostasis. Compr Physiol 2013;3(1):485-513
85. Fausto N, Campbell JS, Riehle KJ. Liver regeneration. J Hepatol 2012;57(3):692-4
86. Fausto N. Involvement of the innate immune system in liver regeneration and injury. J Hepatol 2006;45(3):347-9
87. Van Sweringen HL, Sakai N, Tevar AD, et al. CXC chemokine signaling in the liver: impact on repair and regeneration. Hepatology 2011;54(4):1445-53
88. Tumanov AV, Koroleva EP, Christiansen PA, et al. T cell-derived lymphotoxin regulates liver regeneration. Gastroenterology 2009;136(2):694-704
89. Rao R, Graffeo CS, Gulati R, et al. Interleukin 17-producing gammadeltaT cells promote hepatic regeneration in mice. Gastroenterology 2014;147(2):473-84
90. Sun R, Gao B. Negative regulation of liver regeneration by innate immunity (natural killer cells/interferon-gamma). Gastroenterology 2004;127(5):1525-39
91. Minagawa M, Oya H, Yamamoto S, et al. Intensive expansion of natural killer T cells in the early phase of hepatocyte regeneration after partial hepatectomy in mice and its association with sympathetic nerve activation. Hepatology 2000;31(4):907-15
92. Dong Z, Zhang J, Sun R, et al. Impairment of liver regeneration correlates with activated hepatic NKT cells in HBV transgenic mice. Hepatology 2007;45(6):1400-12
93. Nakashima H, Inui T, Habu Y, et al. Activation of mouse natural killer T cells accelerates liver regeneration after partial hepatectomy. Gastroenterology 2006;131(5): 1573-83
94. Sun R, Park O, Horiguchi N, et al. STAT1 contributes to dsRNA inhibition of liver regeneration after partial hepatectomy in mice. Hepatology 2006;44(4):955-66
95. DeAngelis RA, Markiewski MM, Kourtzelis I, et al. A complement-IL-4 regulatory circuit controls liver regeneration. J Immunol 2012;188(2):641-8
96. Goh YP, Henderson NC, Heredia JE, et al. Eosinophils secrete IL-4 to facilitate liver regeneration. Proc Natl Acad Sci USA 2013;110(24):9914-19
97. Vivier E, Ugolini S, Blaise D, et al. Targeting natural killer cells and natural killer T cells in cancer. Nat Rev Immunol 2012;12(4):239-52
98. Metelitsa LS, Weinberg KI, Emanuel PD, Seeger RC. Expression of CD1d by myelomonocytic leukemias provides a target for cytotoxic NKT cells. Leukemia 2003; 17(6):1068-77
99. Song L, Asgharzadeh S, Salo J, et al. Valpha24-invariant NKT cells mediate antitumor activity via killing of tumor-associated macrophages. J Clin Invest 2009;119(6):1524-36
100. Terabe M, Swann J, Ambrosino E, et al. A nonclassical non-Valpha14Jalpha18 CD1d-restricted (type II) NKT cell is sufficient for down-regulation of tumor immunosurveillance. J Exp Med 2005; 202(12):1627-33
101. Tahir SM, Cheng O, Shaulov A, et al. Loss of IFN-gamma production by invariant NK T cells in advanced cancer. J Immunol 2001;167(7):4046-50
102. Tachibana T, Onodera H, Tsuruyama T, et al. Increased intratumor Valpha24-positive natural killer T cells: a prognostic factor for primary colorectal carcinomas. Clin Cancer Res 2005;11(20): 7322-7
103. Schneiders FL, de Bruin RC, van den Eertwegh AJ, et al. Circulating invariant natural killer T-cell numbers predict outcome in head and neck squamous cell carcinoma: updated analysis with 10-year follow-up. J Clin Oncol 2012; 30(5):567-70
104. Tatsumi T, Takehara T, Yamaguchi S, et al. Intrahepatic delivery of alpha-galactosylceramide-pulsed dendritic cells suppresses liver tumor. Hepatology 2007;45(1):22-30
105. Anson M, Crain-Denoyelle AM, Baud V, et al. Oncogenic beta-catenin triggers an inflammatory response that determines the aggressiveness of hepatocellular carcinoma in mice. J Clin Invest 2012;122(2):586-99
106. Wolf MJ, Adili A, Piotrowitz K, et al. Metabolic activation of intrahepatic CD8+ T cells and NKT cells causes nonalcoholic steatohepatitis and liver cancer via cross-talk with hepatocytes. Cancer Cell 2014;26(4): 549-64
107. Bricard G, Cesson V, Devevre E, et al. Enrichment of human CD4+ V(alpha)24/Vbeta11 invariant NKT cells in intrahepatic malignant tumors. J Immunol 2009;182(8): 5140-51
108. Crowe NY, Coquet JM, Berzins SP, et al. Differential antitumor immunity mediated by NKT cell subsets in vivo. J Exp Med 2005;202(9):1279-88
109. Schneiders FL, Scheper RJ, von Blomberg BM, et al. Clinical experience with alpha-galactosylceramide (KRN7000) in patients with advanced cancer and chronic hepatitis B/C infection. Clin Immunol 2011;140(2):130-41
110. Veldt BJ, van der Vliet HJ, von Blomberg BM, et al. Randomized placebo controlled Phase I/II trial of alpha-galactosylceramide for the treatment of chronic hepatitis C. J Heptol 2007;47(3): 356-65