IL-17 axis driven inflammation in non-alcoholic fatty liver disease progression

Current Drug Targets

Volumn 16, Issue 12, 2015, Pages 1315-1323

  Giles, Daniel A ^a   Moreno Fernandez, Maria E ^a   Divanovic, Senad ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

IL 17; Inflammation; NAFLD; Obesity

Indexed keywords

CXCL1 CHEMOKINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 17; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 6; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; ARTICLE; CYTOKINE PRODUCTION; DISEASE COURSE; HUMAN; IMMUNE RESPONSE; KUPFFER CELL; LIPOTOXICITY; LIVER CELL; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER DISEASE; NATURAL KILLER CELL; NEUTROPHIL; NONALCOHOLIC FATTY LIVER; NONHUMAN; OBESITY; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STELLATE CELL; ANIMAL; COMPLICATION; CYTOLOGY; INFLAMMATION; LIVER; METABOLISM; MOUSE; NON-ALCOHOLIC FATTY LIVER DISEASE; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; DISEASE PROGRESSION; HUMANS; INFLAMMATION; INTERLEUKIN-17; LIVER; MICE; NON-ALCOHOLIC FATTY LIVER DISEASE; OBESITY;

EID: 84946722042     PISSN: 13894501     EISSN: 18735592     Source Type: Journal    
DOI: 10.2174/1389450116666150531153627     Document Type: Article

References (139)

1. [1] Finucane MM, Stevens GA, Cowan MJ, et al. National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9.1 million participants. Lancet 2011; 377(9765): 557-67.
2. [2] Ng M, Fleming T, Robinson M, et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 2014; 384(9945): 766-81.
3. [3] Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of childhood and adult obesity in the United States, 2011-2012. JAMA 2014; 311(8): 806-14.
4. [4] Wang Y, Beydoun MA. The obesity epidemic in the United States- -gender, age, socioeconomic, racial/ethnic, and geographic characteristics: a systematic review and meta-regression analysis. Epidemiol Rev 2007; 29: 6-28.
5. [5] Kassirer JP, Angell M. Losing weight--an ill-fated New Year's resolution. N Engl J Med 1998; 338(1): 52-4.
6. [6] Kang JG, Park CY. Anti-obesity drugs: A review about their effects and safety. Diabetes Metab J. 2012; 36(1): 13-25.
7. [7] Schenk S, Saberi M, Olefsky JM. Insulin sensitivity: modulation by nutrients and inflammation. J Clin Investig 2008, 118(9):2992-3002
8. [8] Strissel KJ, Stancheva Z, Miyoshi H, et al. Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes 2007; 56(12): 2910-8
9. [9] Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Investig 2003; 112(12): 1796-808.
10. [10] Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. Adults. N Engl J Med 2003; 348(17): 1625-38.
11. [11] Kanneganti TD, Dixit VD. Immunological complications of obesity. Nat Immunol 2012; 13(8): 707-12.
12. [12] Vallianou NG, Evangelopoulos AA, Panagiotakos DB, et al. Associations of acute-phase reactants with metabolic syndrome in middle- aged overweight or obese people. Med Sci Monit 2010; 16(2): CR56-60.
13. [13] Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 1993; 259(5091): 87-91.
14. [14] Hotamisligil GS, Arner P, Caro JF, Atkinson RL, Spiegelman BM. Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance. J Clin Investig 1995; 95(5): 2409-15.
15. [15] Sethi JK, Hotamisligil GS. The role of TNF alpha in adipocyte metabolism. Semin Cell Dev Biol 1999; 10(1): 19-29.
16. [16] Heilbronn LK, Campbell LV. Adipose tissue macrophages, low grade inflammation and insulin resistance in human obesity. Curr pharm design 2008; 14(12): 1225-30.
17. [17] Solinas G, Vilcu C, Neels JG, et al. JNK1 in hematopoietically derived cells contributes to diet-induced inflammation and insulin resistance without affecting obesity. Cell Metabol 2007; 6(5): 386-97.
18. [18] Vallerie SN, Furuhashi M, Fucho R, Hotamisligil GS. A predominant role for parenchymal c-Jun amino terminal kinase (JNK) in the regulation of systemic insulin sensitivity. PloS One 2008; 3(9): e3151.
19. [19] Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clini Investig 2006; 116(7): 1793-801.
20. [20] De Taeye BM, Novitskaya T, McGuinness OP, et al. Macrophage TNF-alpha contributes to insulin resistance and hepatic steatosis in diet-induced obesity. Am J Physiol Endocrinol Metabol 2007; 293(3): E713-25.
21. [21] Hirosumi J, Tuncman G, Chang L, et al. A central role for JNK in obesity and insulin resistance. Nature 2002; 420(6913): 333-6.
22. [22] Yuan M, Konstantopoulos N, Lee J, et al. Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of Ikkbeta. Science 2001; 293(5535): 1673-7.
23. [23] Tuncman G, Hirosumi J, Solinas G, Chang L, Karin M, Hotamisligil GS. Functional in vivo interactions between JNK1 and JNK2 isoforms in obesity and insulin resistance. Proc Natl Acad Sci USA 2006; 103(28): 10741-6.
24. [24] Ye J, Gao Z, Yin J, He Q. Hypoxia is a potential risk factor for chronic inflammation and adiponectin reduction in adipose tissue of ob/ob and dietary obese mice. Am J Physiol Endocrinol Metabol 2007; 293(4): E1118-28.
25. [25] Hotamisligil GS. Inflammation and endoplasmic reticulum stress in obesity and diabetes. Int J Obesity 2008; 32 Suppl 7: S52-4
26. [26] Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature 2006; 444(7122): 1022-3.
27. [27] Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 2005; 102(31): 11070-5.
28. [28] Brun P, Castagliuolo I, Leo VD, et al. Increased intestinal permeability in obese mice: new evidence in the pathogenesis of nonalcoholic steatohepatitis. Am J Physiol Gastrointest Liver Physiol 2007; 292(2): G518-25.
29. [29] Cani PD, Amar J, Iglesias MA, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007; 56(7): 1761-72.
30. [30] Miller YI, Viriyakosol S, Worrall DS, Boullier A, Butler S, Witztum JL. Toll-like receptor 4-dependent and -independent cytokine secretion induced by minimally oxidized low-density lipoprotein in macrophages. Arterioscler Thromb Vasc Bio 2005;25(6): 1213-9
31. [31] Huang S, Rutkowsky JM, Snodgrass RG, et al. Saturated fatty acids activate TLR-mediated proinflammatory signaling pathways. J Lipid Res 2012; 53(9): 2002-13.
32. [32] Okamura Y, Watari M, Jerud ES, et al. The extra domain A of fibronectin activates Toll-like receptor 4. J Biol Chem 2001; 276(13): 10229-33.
33. [33] Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002; 418(6894): 191-5.
34. [34] Xu H, Barnes GT, Yang Q, et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003;112(12): 1821-30.
35. [35] Gordon S. Macrophage heterogeneity and tissue lipids. J Clin Invest 2007; 117(1): 89-93.
36. [36] Talukdar S, Oh da Y, Bandyopadhyay G, et al. Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase. Nat Med 2012; 18(9): 1407-12.
37. [37] Bertola A, Ciucci T, Rousseau D, et al. Identification of adipose tissue dendritic cells correlated with obesity-associated insulinresistance and inducing Th17 responses in mice and patients. Diabetes 2012; 61(9): 2238-47.
38. [38] O'Rourke RW, Metcalf MD, White AE, et al. Depot-specific differences in inflammatory mediators and a role for NK cells and IFN-gamma in inflammation in human adipose tissue. Int J Obes 2009; 33(9): 978-90.
39. [39] Ohmura K, Ishimori N, Ohmura Y, et al. Natural killer T cells are involved in adipose tissues inflammation and glucose intolerance in diet-induced obese mice. Arteriosclerosis, thrombosis, and vascular biology. Arterioscler Thromb Vasc Biol 2010; 30(2): 193-9.
40. [40] Yang H, Youm YH, Vandanmagsar B, et al. Obesity increases the production of proinflammatory mediators from adipose tissue T cells and compromises TCR repertoire diversity: implications for systemic inflammation and insulin resistance. J Immunol 2010; 185(3): 1836-45.
41. [41] Winer DA, Winer S, Shen L, et al. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat Med 2011; 17(5): 610-7.
42. [42] Wu D, Molofsky AB, Liang HE, et al. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 2011; 332(6026): 243-7.
43. [43] Liu J, Divoux A, Sun J, et al. Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nat Med 2009; 15(8): 940-5.
44. [44] Tiniakos DG, Vos MB, Brunt EM. Nonalcoholic fatty liver disease: pathology and pathogenesis. Annu Rev Pathol 2010; 5: 145-71.
45. [45] Cohen JC, Horton JD, Hobbs HH. Human fatty liver disease: old questions and new insights. Science 2011; 332(6037): 1519-23.
46. [46] Browning JD, Szczepaniak LS, Dobbins R, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 2004; 40(6): 1387-95.
47. [47] Adams LA, Angulo P. Recent concepts in non-alcoholic fatty liver disease. Diabetic medicine. Diabet Med 2005; 22(9): 1129-33.
48. [48] Schwimmer JB, Deutsch R, Kahen T, Lavine JE, Stanley C, Behling C. Prevalence of fatty liver in children and adolescents. Pediatrics 2006; 118(4): 1388-93.
49. [49] Angulo P, Keach JC, Batts KP, Lindor KD. Independent predictors of liver fibrosis in patients with nonalcoholic steatohepatitis. Hepatology 1999; 30(6): 1356-62.
50. [50] Rinella ME. Will the increased prevalence of nonalcoholic steatohepatitis (NASH) in the age of better hepatitis C virus therapy make NASH the deadlier disease? Hepatology 2011;54(4): 1118-20
51. [51] Farrell GC, van Rooyen D, Gan L, Chitturi S. NASH is an inflammatory disorder: pathogenic, prognostic and therapeutic implications. Gut Liver 2012; 6(2): 149-71.
52. [52] Sakaguchi S, Takahashi S, Sasaki T, Kumagai T, Nagata K. Progression of alcoholic and non-alcoholic steatohepatitis: common metabolic aspects of innate immune system and oxidative stress. Drug Metab Pharmacokinet 2011; 26(1): 30-46.
53. [53] Davidson A, Diamond B. Autoimmune diseases. N Engl J Med 2001; 345(5): 340-50.
54. [54] O'Shea JJ, Ma A, Lipsky P. Cytokines and autoimmunity. Nat Rev Immunol 2002; 2(1): 37-45.
55. [55] Carter-Kent C, Zein NN, Feldstein AE. Cytokines in the pathogenesis of fatty liver and disease progression to steatohepatitis: implications for treatment. Am J Gastroenterol 2008;103(4): 1036-42
56. [56] Gaffen SL. Structure and signalling in the IL-17 receptor family. Nat Rev Immunol 2009; 9(8): 556-67.
57. [57] Cua DJ, Tato CM. Innate IL-17-producing cells: the sentinels of the immune system. Nat Rev Immunol 2010; 10(7):479-89.
58. [58] Ge D, You Z. Expression of interleukin-17RC protein in normal human tissues. Int Arch Med 2008; 1(1): 19.
59. [59] Lafdil F, Wang H, Park O, et al. Myeloid STAT3 inhibits T cellmediated hepatitis by regulating T helper 1 cytokine and interleukin- 17 production. Gastroenterology 2009;137(6): 2125-35 e1-2.
60. [60] Lemmers A, Moreno C, Gustot T, et al. The interleukin-17 pathway is involved in human alcoholic liver disease. Hepatology 2009; 49(2): 646-57.
61. [61] Shen F, Gaffen SL. Structure-function relationships in the IL-17 receptor: implications for signal transduction and therapy. Cytokine 2008; 41(2): 92-104.
62. [62] Iwakura Y, Ishigame H, Saijo S, Nakae S. Functional specialization of interleukin-17 family members. Immunity 2011; 34(2): 149-62.
63. [63] Cesaratto L, Vascotto C, Calligaris S, Tell G. The importance of redox state in liver damage. Ann Hepatol 2004; 3(3): 86-92.
64. [64] Rensen SS, Bieghs V, Xanthoulea S, et al. Neutrophil-derived myeloperoxidase aggravates non-alcoholic steatohepatitis in lowdensity lipoprotein receptor-deficient mice. PloS One 2012; 7(12): e52411.
65. [65] Gujral JS, Liu J, Farhood A, Hinson JA, Jaeschke H. Functional importance of ICAM-1 in the mechanism of neutrophil-induced liver injury in bile duct-ligated mice. Am J Physiol Gastrointest Liver Physiol 2004; 286(3): G499-507.
66. [66] Tan Z, Qian X, Jiang R, et al. IL-17A plays a critical role in the pathogenesis of liver fibrosis through hepatic stellate cell activation. J Immunol 2013; 191(4): 1835-44.
67. [67] Du WJ, Zhen JH, Zeng ZQ, et al. Expression of interleukin-17 associated with disease progression and liver fibrosis with hepatitis B virus infection: IL-17 in HBV infection. Diagn Pathol 2013; 8: 40.
68. [68] Balanescu P, Ladaru A, Voiosu T, Nicolau A, Ene M, Balanescu E. Th17 and IL-17 immunity in chronic hepatitis C infection. Rom J Intern Med 2012; 50(1): 13-8.
69. [69] Lan RY, Salunga TL, Tsuneyama K, et al. Hepatic IL-17 responses in human and murine primary biliary cirrhosis. J Autoimmun 2009; 32(1): 43-51.
70. [70] Qian C, Jiang T, Zhang W, et al. Increased IL-23 and IL-17 expression by peripheral blood cells of patients with primary biliary cirrhosis. Cytokine 2013; 64(1): 172-80.
71. [71] Zhang JP, Yan J, Xu J, et al. Increased intratumoral IL-17- producing cells correlate with poor survival in hepatocellular carcinoma patients. J Hepatol 2009; 50(5): 980-9.
72. [72] Fabrega E, Lopez-Hoyos M, San Segundo D, Casafont F, Pons- Romero F. Changes in the serum levels of interleukin- 17/interleukin-23 during acute rejection in liver transplantation. Liver Transpl 2009; 15(6): 629-33.
73. [73] Xie XJ, Ye YF, Zhou L, et al. Th17 promotes acute rejection following liver transplantation in rats. J Zhejiang Univ Sci B 2010; 11(11): 819-27.
74. [74] Nagata T, McKinley L, Peschon JJ, Alcorn JF, Aujla SJ, Kolls JK. Requirement of IL-17RA in Con A induced hepatitis and negative regulation of IL-17 production in mouse T cells. J Immunol 2008; 181(11): 7473-9.
75. [75] Yan S, Wang L, Liu N, Wang Y, Chu Y. Critical role of interleukin- 17/interleukin-17 receptor axis in mediating Con A-induced hepatitis. Immunol Cell Biol 2012; 90(4): 421-8.
76. [76] Meng F, Wang K, Aoyama T, et al. Interleukin-17 signaling in inflammatory, Kupffer cells, and hepatic stellate cells exacerbates liver fibrosis in mice. Gastroenterology 2012;143(3): 765-76 e1-3
77. [77] Winer S, Paltser G, Chan Y, et al. Obesity predisposes to Th17 bias. Eur J Immunol 2009; 39(9): 2629-35.
78. [78] Sumarac-Dumanovic M, Stevanovic D, Ljubic A, et al. Increased activity of interleukin-23/interleukin-17 proinflammatory axis in obese women. Int J Obes 2009; 33(1): 151-6.
79. [79] Ahmed M, Gaffen SL. IL-17 in obesity and adipogenesis. Cytokine Growth Factor Rev 2010; 21(6): 449-53.
80. [80] Zuniga LA, Shen WJ, Joyce-Shaikh B, et al. IL-17 regulates adipogenesis, glucose homeostasis, and obesity. J Immunol 2010; 185(11): 6947-59.
81. [81] Harley IT, Stankiewicz TE, Giles DA, et al. IL-17 signaling accelerates the progression of nonalcoholic fatty liver disease in mice. Hepatology 2014; 59(5): 1830-9.
82. [82] Xu R, Tao A, Zhang S, Zhang M. Neutralization of interleukin-17 attenuates high fat diet-induced non-alcoholic fatty liver disease in mice. Acta Biochim Biophys Sin (Shanghai) 2013; 45(9): 726-33.
83. [83] Tang Y, Bian Z, Zhao L, et al. Interleukin-17 exacerbates hepatic steatosis and inflammation in non-alcoholic fatty liver disease. Clin Exp Immunol 2011; 166(2): 281-90.
84. [84] Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006; 444(7122): 1027-31.
85. [85] Abu-Shanab A, Quigley EM. The role of the gut microbiota in nonalcoholic fatty liver disease. Nat Rev Gastroenterol Hepatol 2010; 7(12): 691-701.
86. [86] Backhed F, Ding H, Wang T, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 2004; 101(44): 15718-23.
87. [87] Rabot S, Membrez M, Bruneau A, et al. Germ-free C57BL/6J mice are resistant to high-fat-diet-induced insulin resistance and have altered cholesterol metabolism. Proc Natl Acad Sci USA 2010; 24(12): 4948-59.
88. [88] Henao-Mejia J, Elinav E, Jin C, et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature 2012; 482(7384): 179-85.
89. [89] Ivanov II, Atarashi K, Manel N, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009;139(3):485-98
90. [90] Ivanov II, Frutos Rde L, Manel N, et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 2008; 4(4): 337-49.
91. [91] Gaboriau-Routhiau V, Rakotobe S, Lecuyer E, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 2009; 31(4): 677-89.
92. [92] Lee YK, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA 2011; 108 Suppl 1: 4615-22.
93. [93] Kriegel MA, Sefik E, Hill JA, Wu HJ, Benoist C, Mathis D. Naturally transmitted segmented filamentous bacteria segregate with diabetes protection in nonobese diabetic mice. Proc Natl Acad Sci USA 2011; 108(28): 11548-53.
94. [94] Wu HJ, Ivanov II, Darce J, et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 2010; 32(6): 815-27.
95. [95] Yin Y, Wang Y, Zhu L, et al. Comparative analysis of the distribution of segmented filamentous bacteria in humans, mice and chickens. ISME J 2013; 7(3): 615-21.
96. [96] Musa S, Moran C, Rahman T. Clostridium difficile infection and liver disease. J Gastrointestin Liver Dis 2010; 19(3):303-10.
97. [97] Chambers JC, Zhang W, Sehmi J, et al. Genome-wide association study identifies loci influencing concentrations of liver enzymes in plasma. Nat Genet 2011; 43(11): 1131-8.
98. [98] Middelberg RP, Benyamin B, de Moor MH, et al. Loci affecting gamma-glutamyl transferase in adults and adolescents show age x SNP interaction and cardiometabolic disease associations. Hum Mol Genet 2012; 21(2): 446-55.
99. [99] Alkhouri N, Morris-Stiff G, Campbell C, et al. Neutrophil to lymphocyte ratio: a new marker for predicting steatohepatitis and fibrosis in patients with nonalcoholic fatty liver disease. Liver Int 2012; 32(2): 297-302.
100. [100] Racanelli V, Rehermann B. The liver as an immunological organ. Hepatology 2006; 43(2 Suppl 1): S54-62.
101. [101] Berlanga A, Guiu-Jurado E, Porras JA, Auguet T. Molecular pathways in non-alcoholic fatty liver disease. Clin Exp Gastroenterol 2014; 7: 221-39.
102. [102] Meli R, Raso MG, Calignano A. Role of innate immune response in non-alcoholic Fatty liver disease: metabolic complications and therapeutic tools. Front Immunol 2014; 5: 177.
103. [103] Yi HS, Jeong WI. Interaction of hepatic stellate cells with diverse types of immune cells: foe or friend? J Gastroenterol Hepatol 2013; 28 Suppl 1: 99-104.
104. [104] Weiskirchen R, Tacke F. Cellular and molecular functions of hepatic stellate cells in inflammatory responses and liver immunology. Hepatobiliary Surg Nutr 2014; 3(6): 344-63.
105. [105] Zhan YT, An W. Roles of liver innate immune cells in nonalcoholic fatty liver disease. World J Gastroenterol 2010;16(37):4652-60
106. [106] Wenfeng Z, Yakun W, Di M, Jianping G, Chuanxin W, Chun H. Kupffer cells: increasingly significant role in nonalcoholic fatty liver disease. Ann Hepatol 2014; 13(5): 489-95.
107. [107] Kodama Y, Kisseleva T, Iwaisako K, et al. c-Jun N-terminal kinase-1 from hematopoietic cells mediates progression from hepatic steatosis to steatohepatitis and fibrosis in mice. Gastroenterology 2009;137(4):1467-77 e5
108. [108] Kono H, Fujii H, Ogiku M, et al. Role of IL-17A in neutrophil recruitment and hepatic injury after warm ischemia-reperfusion mice. J Immunol 2011; 187(9): 4818-25.
109. [109] Chen Y, Wei H, Sun R, Dong Z, Zhang J, Tian Z. Increased susceptibility to liver injury in hepatitis B virus transgenic mice involves NKG2D-ligand interaction and natural killer cells. Hepatology 2007; 46(3): 706-15.
110. [110] Sun R, Gao B. Negative regulation of liver regeneration by innate immunity (natural killer cells/interferon-gamma). Gastroenterology 2004; 127(5): 1525-39.
111. [111] 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.
112. [112] Doherty DG, O'Farrelly C. Innate and adaptive lymphoid cells in the human liver. Immunol Rev 2000; 174: 5-20.
113. [113] 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 apoptosisinducing ligand-dependent manners. Gastroenterology 2006; 130(2): 435-52.
114. [114] Passos ST, Silver JS, O'Hara AC, Sehy D, Stumhofer JS, Hunter CA. IL-6 promotes NK cell production of IL-17 during toxoplasmosis. J Immunol 2010; 184(4): 1776-83.
115. [115] He J, Lang G, Ding S, Li L. Pathological role of interleukin-17 in poly I: C-induced hepatitis. PloS One 2013; 8(9): e73909.
116. [116] O'Shea D, Cawood TJ, O'Farrelly C, Lynch L. Natural killer cells in obesity: impaired function and increased susceptibility to the effects of cigarette smoke. PloS One 2010; 5(1): e8660.
117. [117] Lamas O, Martinez JA, Marti A. Energy restriction restores the impaired immune response in overweight (cafeteria) rats. J Nutr Biochem 2004; 15(7): 418-25.
118. [118] Kahraman A, Schlattjan M, Kocabayoglu P, et al. Major histocompatibility complex class I-related chains A and B (MIC A/B): a novel role in nonalcoholic steatohepatitis. Hepatology 2010; 51(1): 92-102.
119. [119] Jaeschke H, Farhood A, Smith CW. Neutrophils contribute to ischemia/reperfusion injury in rat liver in vivo. FASEB J 1990; 4(15): 3355-9.
120. [120] Hewett JA, Schultze AE, VanCise S, Roth RA. Neutrophil depletion protects against liver injury from bacterial endotoxin. Lab investig 1992; 66(3): 347-61.
121. [121] Molnar RG, Wang P, Ayala A, Ganey PE, Roth RA, Chaudry IH. The role of neutrophils in producing hepatocellular dysfunction during the hyperdynamic stage of sepsis in rats. J Surg Res 1997; 73(2): 117-22.
122. [122] Bautista AP. Chronic alcohol intoxication induces hepatic injury through enhanced macrophage inflammatory protein-2 production and intercellular adhesion molecule-1 expression in the liver. Hepatology 1997; 25(2): 335-42.
123. [123] Hubscher SG. Histological assessment of non-alcoholic fatty liver disease. Histopathology 2006; 49(5): 450-65.
124. [124] Witowski J, Pawlaczyk K, Breborowicz A, et al. IL-17 stimulates intraperitoneal neutrophil infiltration through the release of GRO alpha chemokine from mesothelial cells. J Immunol 2000; 165(10): 5814-21.
125. [125] Prause O, Laan M, Lotvall J, Linden A. Pharmacological modulation of interleukin-17-induced GCP-2-, GRO-alpha- and interleukin- 8 release in human bronchial epithelial cells. Eur J Pharmacol 2003; 462(1-3): 193-8.
126. [126] Taylor PR, Roy S, Leal SM, et al. Activation of neutrophils by autocrine IL-17A-IL-17RC interactions during fungal infection is regulated by IL-6, IL-23, RORgammat and dectin-2. Nature Immunol 2014; 15(2): 143-51.
127. [127] Exley MA, Koziel MJ. To be or not to be NKT: natural killer T cells in the liver. Hepatology. 2004; 40(5):1033-40.
128. [128] Tajiri K, Shimizu Y, Tsuneyama K, Sugiyama T. Role of liverinfiltrating CD3+CD56+ natural killer T cells in the pathogenesis of nonalcoholic fatty liver disease. Eur J Gastroenterol Hepatol 2009; 21(6): 673-80.
129. [129] Xu CF, Yu CH, Li YM, Xu L, Du J, Shen Z. Association of the frequency of peripheral natural killer T cells with nonalcoholic fatty liver disease. World J Gastroenterol 2007; 13(33): 4504-8.
130. [130] Guebre-Xabier M, Yang S, Lin HZ, Schwenk R, Krzych U, Diehl AM. Altered hepatic lymphocyte subpopulations in obesity-related murine fatty livers: potential mechanism for sensitization to liver damage. Hepatology 2000; 31(3):633-40.
131. [131] Elinav E, Pappo O, Sklair-Levy M, et al. Adoptive transfer of regulatory NKT lymphocytes ameliorates non-alcoholic steatohepatitis and glucose intolerance in ob/ob mice and is associated with intrahepatic CD8 trapping. J Pathol 2006; 209(1): 121-8.
132. [132] 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.
133. [133] De Vito R, Alisi A, Masotti A, et al. Markers of activated inflammatory cells correlate with severity of liver damage in children with nonalcoholic fatty liver disease. Int J Mol Med 2012; 30(1): 49-56.
134. [134] 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.
135. [135] Hammerich L, Tacke F. Interleukins in chronic liver disease: lessons learned from experimental mouse models. Clin Exper Gastroenterol 2014; 7: 297-306.
136. [136] Hammerich L, Heymann F, Tacke F. Role of IL-17 and Th17 cells in liver diseases. Clin Dev Immunol 2011; 345803
137. [137] Mathews JA, Wurmbrand AP, Ribeiro L, Neto FL, Shore SA. Induction of IL-17A precedes development of airway hyperresponsi veness during diet-induced obesity and correlates with complement factor D. Front Immunol 2014; 5: 440.
138. [138] Chen Y, Tian J, Tian X, et al. Adipose tissue dendritic cells enhances inflammation by prompting the generation of Th17 cells. PloS one. 2014; 9(3): e92450.
139. [139] Gaffen SL, Jain R, Garg AV, Cua DJ. The IL-23-IL-17 immune axis: from mechanisms to therapetherapeutic testing. Nat Rev Immunol 2014; 14(9):585-600