Alcohol-induced miR-155 and HDAC11 inhibit negative regulators of the TLR4 pathway and lead to increased LPS responsiveness of Kupffer cells in alcoholic liver disease

Journal of Leukocyte Biology

Volumn 102, Issue 2, 2017, Pages 487-498

  Bala, Shashi ^a   Csak, Timea ^a   Kodys, Karen ^a   Catalano, Donna ^a   Ambade, Aditya ^a   Furi, Istvan ^a   Lowe, Patrick ^a   Cho, Yeonhee ^a   Iracheta Vellve, Arvin ^a   Szabo, Gyongyi ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

HDAC11; IRAK M; miR 155; MyD88; TNF

Indexed keywords

ACETALDEHYDE; ALCOHOL; HISTONE DEACETYLASE 11; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 3; INTERLEUKIN 10; LIPOPOLYSACCHARIDE; MICRORNA 155; MYELOID DIFFERENTIATION FACTOR 88; SMALL INTERFERING RNA; SUPPRESSOR OF CYTOKINE SIGNALING 1; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR; HDAC11 PROTEIN, MOUSE; HISTONE DEACETYLASE; MICRORNA; MIRN155 MICRORNA, MOUSE; TLR4 PROTEIN, MOUSE;

ALCOHOL LIVER DISEASE; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; FEMALE; GAIN OF FUNCTION MUTATION; GENE OVEREXPRESSION; GENE SILENCING; INFLAMMATION; KUPFFER CELL; LIVER CELL; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAW 264.7 CELL LINE; REGULATORY MECHANISM; ANIMAL; C57BL MOUSE; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; IMMUNOLOGY; METABOLISM; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HISTONE DEACETYLASES; INFLAMMATION; KUPFFER CELLS; LIPOPOLYSACCHARIDES; LIVER DISEASES, ALCOHOLIC; MICE; MICE, INBRED C57BL; MICRORNAS; RAW 264.7 CELLS; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 85026784656     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3A0716-310R     Document Type: Article

References (62)

1. Bala, S., Marcos, M., Gattu, A., Catalano, D., Szabo, G. (2014) Acute binge drinking increases serum endotoxin and bacterial DNA levels in healthy individuals. PLoS One 9, e96864.
2. Lippai, D., Bala, S., Catalano, D., Kodys, K., Szabo, G. (2014) Micro-RNA-155 deficiency prevents alcohol-induced serum endotoxin increase and small bowel inflammation in mice. Alcohol. Clin. Exp. Res. 38, 2217–2224.
3. Keshavarzian, A., Farhadi, A., Forsyth, C. B., Rangan, J., Jakate, S., Shaikh, M., Banan, A., Fields, J. Z. (2009) Evidence that chronic alcohol exposure promotes intestinal oxidative stress, intestinal hyperpermeability and endotoxemia prior to development of alcoholic steatohepatitis in rats. J. Hepatol. 50, 538–547.
4. Mutlu, E., Keshavarzian, A., Engen, P., Forsyth, C. B., Sikaroodi, M., Gillevet, P. (2009) Intestinal dysbiosis: a possible mechanism of alcohol-induced endotoxemia and alcoholic steatohepatitis in rats. Alcohol. Clin. Exp. Res. 33, 1836–1846.
5. Szabo, G., Petrasek, J., Bala, S. (2012) Innate immunity and alcoholic liver disease. Dig. Dis. 30 (Suppl 1), 55–60.
6. Gao, B., Seki, E., Brenner, D. A., Friedman, S., Cohen, J. I., Nagy, L., Szabo, G., Zakhari, S. (2011) Innate immunity in alcoholic liver disease. Am. J. Physiol. Gastrointest. Liver Physiol. 300, G516–G525.
7. Szabo, G., Bala, S. (2010) Alcoholic liver disease and the gut-liver axis. World J. Gastroenterol. 16, 1321–1329.
8. Yan, A. W., Fouts, D. E., Brandl, J., Stärkel, P., Torralba, M., Schott, E., Tsukamoto, H., Nelson, K. E., Brenner, D. A., Schnabl, B. (2011) Enteric dysbiosis associated with a mouse model of alcoholic liver disease. Hepatology 53, 96–105.
9. Hritz, I., Mandrekar, P., Velayudham, A., Catalano, D., Dolganiuc, A., Kodys, K., Kurt-Jones, E., Szabo, G. (2008) The critical role of toll-like receptor (TLR) 4 in alcoholic liver disease is independent of the common TLR adapter MyD88. Hepatology 48, 1224–1231.
10. Bala, S., Tang, A., Catalano, D., Petrasek, J., Taha, O., Kodys, K., Szabo, G. (2012) Induction of Bcl-3 by acute binge alcohol results in Toll-like receptor 4/LPS tolerance. J. Leukoc. Biol. 92, 611–620.
11. Mandrekar, P., Bala, S., Catalano, D., Kodys, K., Szabo, G. (2009) The opposite effects of acute and chronic alcohol on lipopolysaccharide-induced inflammation are linked to IRAK-M in human monocytes. J. Immunol. 183, 1320–1327.
12. Norkina, O., Dolganiuc, A., Catalano, D., Kodys, K., Mandrekar, P., Syed, A., Efros, M., Szabo, G. (2008) Acute alcohol intake induces SOCS1 and SOCS3 and inhibits cytokine-induced STAT1 and STAT3 signaling in human monocytes. Alcohol. Clin. Exp. Res. 32, 1565–1573.
13. Mandrekar, P., Szabo, G. (2009) Signalling pathways in alcohol-induced liver inflammation. J. Hepatol. 50, 1258–1266.
14. Nahid, M. A., Pauley, K. M., Satoh, M., Chan, E. K. L. (2009) miR-146a is critical for endotoxin-induced tolerance: implication in innate immunity. J. Biol. Chem. 284, 34590–34599.
15. Biswas, S. K., Lopez-Collazo, E. (2009) Endotoxin tolerance: new mechanisms, molecules and clinical significance. Trends Immunol. 30, 475–487.
16. Zacharioudaki, V., Androulidaki, A., Arranz, A., Vrentzos, G., Margioris, A. N., Tsatsanis, C. (2009) Adiponectin promotes endotoxin tolerance in macrophages by inducing IRAK-M expression. J. Immunol. 182, 6444–6451.
17. Biswas, S. K., Bist, P., Dhillon, M. K., Kajiji, T., Del Fresno, C., Yamamoto, M., Lopez-Collazo, E., Akira, S., Tergaonkar, V. (2007) Role for MyD88-independent, TRIF pathway in lipid A/TLR4-induced endotoxin tolerance. J. Immunol. 179, 4083–4092.
18. Kobayashi, K., Hernandez, L. D., Galán, J. E., Janeway, C. A. Jr., Medzhitov, R., Flavell, R. A. (2002) IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 110, 191–202.
19. Nakagawa, R., Naka, T., Tsutsui, H., Fujimoto, M., Kimura, A., Abe, T., Seki, E., Sato, S., Takeuchi, O., Takeda, K., Akira, S., Yamanishi, K., Kawase, I., Nakanishi, K., Kishimoto, T. (2002) SOCS-1 participates in negative regulation of LPS responses. Immunity 17, 677–687.
20. Frazier, T. H., Stocker, A. M., Kershner, N. A., Marsano, L. S., McClain, C. J. (2011) Treatment of alcoholic liver disease. Therap. Adv. Gastroenterol. 4, 63–81.
21. Szabo, G., Bala, S. (2013) MicroRNAs in liver disease. Nat. Rev. Gastroenterol. Hepatol. 10, 542–552.
22. O’Connell, R. M., Rao, D. S., Baltimore, D. (2012) microRNA regulation of inflammatory responses. Annu. Rev. Immunol. 30, 295–312.
23. O’Connell, R. M., Chaudhuri, A. A., Rao, D. S., Baltimore, D. (2009) Inositol phosphatase SHIP1 is a primary target of miR-155. Proc. Natl. Acad. Sci. USA 106, 7113–7118.
24. Costinean, S., Sandhu, S. K., Pedersen, I. M., Tili, E., Trotta, R., Perrotti, D., Ciarlariello, D., Neviani, P., Harb, J., Kauffman, L. R., Shidham, A., Croce, C. M. (2009) Src homology 2 domain-containing inositol-5-phosphatase and CCAAT enhancer-binding protein beta are targeted by miR-155 in B cells of Emicro-miR-155 transgenic mice. Blood 114, 1374–1382.
25. Jiang, S., Zhang, H. W., Lu, M. H., He, X. H., Li, Y., Gu, H., Liu, M. F., Wang, E. D. (2010) MicroRNA-155 functions as an OncomiR in breast cancer by targeting the suppressor of cytokine signaling 1 gene. Cancer Res. 70, 3119–3127.
26. Tili, E., Michaille, J. J., Cimino, A., Costinean, S., Dumitru, C. D., Adair, B., Fabbri, M., Alder, H., Liu, C. G., Calin, G. A., Croce, C. M. (2007) Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. J. Immunol. 179, 5082–5089.
27. Bala, S., Marcos, M., Kodys, K., Csak, T., Catalano, D., Mandrekar, P., Szabo, G. (2011) Up-regulation of microRNA-155 in macrophages contributes to increased tumor necrosis factor alpha (TNFalpha) production via increased mRNA half-life in alcoholic liver disease. J. Biol. Chem. 286, 1436–1444.
28. Bala, S., Csak, T., Saha, B., Zatsiorsky, J., Kodys, K., Catalano, D., Satishchandran, A., Szabo, G. (2016) The pro-inflammatory effects of miR-155 promote liver fibrosis and alcohol-induced steatohepatitis. J. Hepatol. 64, 1378–1387.
29. Martinez-Nunez, R. T., Louafi, F., Friedmann, P. S., Sanchez-Elsner, T. (2009) MicroRNA-155 modulates the pathogen binding ability of dendritic cells (DCs) by down-regulation of DC-specific intercellular adhesion molecule-3 grabbing non-integrin (DC-SIGN). J. Biol. Chem. 284, 16334–16342.
30. Emmanuilidis, K., Weighardt, H., Maier, S., Gerauer, K., Fleischmann, T., Zheng, X. X., Hancock, W. W., Holzmann, B., Heidecke, C. D. (2001) Critical role of Kupffer cell-derived IL-10 for host defense in septic peritonitis. J. Immunol. 167, 3919–3927.
31. Breous, E., Somanathan, S., Vandenberghe, L. H., Wilson, J. M. (2009) Hepatic regulatory T cells and Kupffer cells are crucial mediators of systemic T cell tolerance to antigens targeting murine liver. Hepatology 50, 612–621.
32. Shukla, S. D., Velazquez, J., French, S. W., Lu, S. C., Ticku, M. K., Zakhari, S. (2008) Emerging role of epigenetics in the actions of alcohol. Alcohol. Clin. Exp. Res. 32, 1525–1534.
33. Moghe, A., Joshi-Barve, S., Ghare, S., Gobejishvili, L., Kirpich, I., McClain, C. J., Barve, S. (2011) Histone modifications and alcohol-induced liver disease: are altered nutrients the missing link? World J. Gastroenterol. 17, 2465–2472.
34. Kirpich, I., Zhang, J., Gobejishvili, L., Kharebava, G., Barker, D., Ghare, S., Joshi-Barve, S., McClain, C. J., Barve, S. (2013) Binge ethanol-induced HDAC3 down-regulates Cpt1α expression leading to hepatic steatosis and injury. Alcohol. Clin. Exp. Res. 37, 1920–1929.
35. Villagra, A., Cheng, F., Wang, H. W., Suarez, I., Glozak, M., Maurin, M., Nguyen, D., Wright, K. L., Atadja, P. W., Bhalla, K., Pinilla-Ibarz, J., Seto, E., Sotomayor, E. M. (2009) The histone deacetylase HDAC11 regulates the expression of interleukin 10 and immune tolerance. Nat. Immunol. 10, 92–100.
36. Bala, S., Csak, T., Momen-Heravi, F., Lippai, D., Kodys, K., Catalano, D., Satishchandran, A., Ambros, V., Szabo, G. (2015) Biodistribution and function of extracellular miRNA-155 in mice. Sci. Rep. 5, 10721.
37. Saha, B., Bala, S., Hosseini, N., Kodys, K., Szabo, G. (2015) Krüppel-like factor 4 is a transcriptional regulator of M1/M2 macrophage polarization in alcoholic liver disease. J. Leukoc. Biol. 97, 963–973.
38. Csak, T., Ganz, M., Pespisa, J., Kodys, K., Dolganiuc, A., Szabo, G. (2011) Fatty acid and endotoxin activate inflammasomes in mouse hepatocytes that release danger signals to stimulate immune cells. Hepatology 54, 133–144.
39. Cai, X., Yin, Y., Li, N., Zhu, D., Zhang, J., Zhang, C. Y., Zen, K. (2012) Re-polarization of tumor-associated macrophages to pro-inflammatory M1 macrophages by microRNA-155. J. Mol. Cell Biol. 4, 341–343.
40. Bode, J. G., Ehlting, C., Häussinger, D. (2012) The macrophage response towards LPS and its control through the p38(MAPK)-STAT3 axis. Cell. Signal. 24, 1185–1194.
41. Kühn, R., Löhler, J., Rennick, D., Rajewsky, K., Müller, W. (1993) Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75, 263–274.
42. Takeda, K., Clausen, B. E., Kaisho, T., Tsujimura, T., Terada, N., Förster, I., Akira, S. (1999) Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity 10, 39–49.
43. 2A adenosine receptors and C/EBPbeta are crucially required for IL-10 production by macrophages exposed to Escherichia coli. Blood 110, 2685–2695.
44. He, M., Xu, Z., Ding, T., Kuang, D. M., Zheng, L. (2009) MicroRNA-155 regulates inflammatory cytokine production in tumor-associated macrophages via targeting C/EBPbeta. Cell. Mol. Immunol. 6, 343–352.
45. Enomoto, N., Schemmer, P., Ikejima, K., Takei, Y., Sato, N., Brenner, D. A., Thurman, R. G. (2001) Long-term alcohol exposure changes sensitivity of rat Kupffer cells to lipopolysaccharide. Alcohol. Clin. Exp. Res. 25, 1360–1367.
46. Adachi, Y., Moore, L. E., Bradford, B. U., Gao, W., Thurman, R. G. (1995) Antibiotics prevent liver injury in rats following long-term exposure to ethanol. Gastroenterology 108, 218–224.
47. Yamashina, S., Wheeler, M. D., Rusyn, I., Ikejima, K., Sato, N., Thurman, R. G. (2000) Tolerance and sensitization to endotoxin in Kupffer cells caused by acute ethanol involve interleukin-1 receptor-associated kinase. Biochem. Biophys. Res. Commun. 277, 686–690.
48. Fukui, H. (2005) Relation of endotoxin, endotoxin binding proteins and macrophages to severe alcoholic liver injury and multiple organ failure. Alcohol. Clin. Exp. Res. 29 (Suppl 11), 172S–179S.
49. Fujimoto, M., Uemura, M., Nakatani, Y., Tsujita, S., Hoppo, K., Tamagawa, T., Kitano, H., Kikukawa, M., Ann, T., Ishii, Y., Kojima, H., Sakurai, S., Tanaka, R., Namisaki, T., Noguchi, R., Higashino, T., Kikuchi, E., Nishimura, K., Takaya, A., Fukui, H. (2000) Plasma endotoxin and serum cytokine levels in patients with alcoholic hepatitis: relation to severity of liver disturbance. Alcohol. Clin. Exp. Res. 24 (Suppl 4), 48S–54S.
50. Hill, D. B., Barve, S., Joshi-Barve, S., McClain, C. (2000) Increased monocyte nuclear factor-kappaB activation and tumor necrosis factor production in alcoholic hepatitis. J. Lab. Clin. Med. 135, 387–395.
51. Liew, F. Y., Xu, D., Brint, E. K., O’Neill, L. A. (2005) Negative regulation of Toll-like receptor-mediated immune responses. Nat. Rev. Immunol. 5, 446–458.
52. Rauh, M. J., Ho, V., Pereira, C., Sham, A., Sly, L. M., Lam, V., Huxham, L., Minchinton, A. I., Mui, A., Krystal, G. (2005) SHIP represses the generation of alternatively activated macrophages. Immunity 23, 361–374.
53. Wang, N., Liang, H., Zen, K. (2014) Molecular mechanisms that influence the macrophage m1-m2 polarization balance. Front. Immunol. 5, 614.
54. Su, C., Hou, Z., Zhang, C., Tian, Z., Zhang, J. (2011) Ectopic expression of microRNA-155 enhances innate antiviral immunity against HBV infection in human hepatoma cells. Virol. J. 8, 354.
55. O’Connell, R. M., Kahn, D., Gibson, W. S., Round, J. L., Scholz, R. L., Chaudhuri, A. A., Kahn, M. E., Rao, D. S., Baltimore, D. (2010) MicroRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity 33, 607–619.
56. Nazari-Jahantigh, M., Wei, Y., Noels, H., Akhtar, S., Zhou, Z., Koenen, R. R., Heyll, K., Gremse, F., Kiessling, F., Grommes, J., Weber, C., Schober, A. (2012) MicroRNA-155 promotes atherosclerosis by repressing Bcl6 in macrophages. J. Clin. Invest. 122, 4190–4202.
57. Palma, C. A., Al Sheikha, D., Lim, T. K., Bryant, A., Vu, T. T., Jayaswal, V., Ma, D. D. (2014) MicroRNA-155 as an inducer of apoptosis and cell differentiation in acute myeloid leukaemia. Mol.Cancer. 13, 79.
58. Csak, T., Bala, S., Lippai, D., Kodys, K., Catalano, D., Iracheta-Vellve, A., Szabo, G. (2015) MicroRNA-155 deficiency attenuates liver ateatosis and fibrosis without reducing inflammation in a mouse model of steatohepatitis. PLoS One 10, e0129251.
59. Qian, F., Deng, J., Lee, Y. G., Zhu, J., Karpurapu, M., Chung, S., Zheng, J. N., Xiao, L., Park, G. Y., Christman, J. W. (2015) The transcription factor PU.1 promotes alternative macrophage polarization and asthmatic airway inflammation. J. Mol. Cell Biol. 7, 557–567.
60. Yang, L., Kouichi, M., Zhang, B., Matsushita, H., Yang, Y. M., Liang, S., Song, J., Roh, Y. S., Seki, E. (2017) TRIF differentially regulates hepatic steatosis and inflammation/fibrosis in mice. Cell Mol. Gastroenterol. Hepatol. 3, 469–483.
61. Scott, M. J., Liu, S., Shapiro, R. A., Vodovotz, Y., Billiar, T. R. (2009) Endotoxin uptake in mouse liver is blocked by endotoxin pretreatment through a suppressor of cytokine signaling-1-dependent mechanism. Hepatology 49, 1695–1708.
62. Zahs, A., Cook, R. T., Waldschimdt, T. J., Choudhry, M. A., Kovacs, E. J., Bird, M. D. (2012) Alcohol and inflammation and infection: clinical and experimental systems–summary of the 2010 Alcohol and Immunology Research Interest Group Meeting. Alcohol 46, 147–153.