NF-κB1 deficiency stimulates the progression of non-alcoholic steatohepatitis (NASH) in mice by promoting NKT-cell-mediated responses

Clinical Science

Volumn 124, Issue 4, 2013, Pages 279-287

  Locatelli, Irene ^a   Sutti, Salvatore ^a   Vacchiano, Marco ^a   Bozzola, Cristina ^a   Albano, Emanuele ^a  

^a UNIVERSITY OF EASTERN PIEDMONT   (Italy)

Author keywords

Liver fibrosis; Liver inflammation; Natural killer T cell (NKT cell); Non alcoholic fatty liver disease

Indexed keywords

CHOLINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 12P40; MESSENGER RNA; METHIONINE; MONOCYTE CHEMOTACTIC PROTEIN 1; OSTEOPONTIN; PROCOLLAGEN; PROTEIN P50; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TUMOR NECROSIS FACTOR ALPHA; BIOLOGICAL MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL INFILTRATION; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; FLOW CYTOMETRY; LIVER CELL; MOUSE; NATURAL KILLER CELL; NONALCOHOLIC FATTY LIVER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STELLATE CELL; T LYMPHOCYTE; UPREGULATION; WILD TYPE; ANIMAL; C57BL MOUSE; DIET; FATTY LIVER; IMMUNOLOGY; LIVER CIRRHOSIS; MACROPHAGE; METABOLISM; MOUSE MUTANT; NATURAL KILLER T CELL; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; BIOLOGICAL MARKERS; DIET; FATTY LIVER; FLOW CYTOMETRY; LIVER CIRRHOSIS; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NATURAL KILLER T-CELLS; NF-KAPPA B P50 SUBUNIT; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84872223447     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20120289     Document Type: Article

References (42)

1. Lazo, M. and Clark, J. M. (2008) The epidemiology of nonalcoholic fatty liver disease: a global perspective. Semin. Liver Dis. 28, 339-350
2. Marra, F., Gastaldelli, A., Svegliati-Baroni, G., Tell, G. and Tiribelli, C. (2008) Molecular basis and mechanisms of progression of non-alcoholic steatohepatitis. Trends Mol. Med. 14, 72-81
3. Tilg, H. and Mochen, A. R. (2010) Evolution of inflammation in non-alcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology 52, 1836-1846
4. Baker, R. G., Hayden, M. S. and Ghosh, S. (2011) NF-kB, inflammation and metabolic disease. Cell Metab. 13, 11-22
5. Romics, Jr, L., Kodys, K., Dolganiuc, A., Graham, L., Velayudham, A., Mandrekar, P. and Szabo, G. (2004) Diverse regulation of NF-κB and peroxisome proliferator-activated receptors in murine nonalcoholic fatty liver. Hepatology 40, 376-385
6. Dela Pe{ogonek}na, A., Leclercq, I., Field, J., George, J., Jones, B. and Farrell, G. (2005) NF-κB activation, rather than TNF, mediates hepatic inflammation in a murine dietary model of steatohepatitis. Gastroenterology 129, 1663-1674
7. Ribeiro, P. S., Cortez-Pinto, H., Soĺa, S., Castro, R. E., Ramalho, R. M., Baptista, A., Moura, M. C., Camilo, M. E. and Rodrigues, C. M. (2004) Hepatocyte apoptosis, expression of death receptors, and activation of NF-κB in the liver of nonalcoholic and alcoholic steatohepatitis patients. Am. J. Gastroenterol. 99, 1708-1717
8. Leclercq, I. A., Farrell, G. C., Sempoux, C., dela Pe{ogonek}na, A. and Horsmans, Y. (2004) Curcumin inhibits NF-κB activation and reduces the severity of experimental steatohepatitis in mice. J. Hepatol. 41, 926-934
9. Vallabhapurapu, S. and Karin, M. (2009) Regulation and function of NF-κB transcription factors in the immune system. Annu. Rev. Immunol. 27, 693-733
10. Panzer, U., Steinmetz, O. M., Turner, J. E., Meyer-Schwesinger, C., von Ruffer, C., Meyer, T. N., Zahner, G., Ǵomez-Guerrero, C., Schmid, R. M., Helmchen, U. et al. (2009) Resolution of renal inflammation: a new role for NF-κB1 (p50) in inflammatory kidney diseases. Am. J. Physiol. Renal Physiol. 297, F429-F439
11. Beinke, S. and Ley, S. C. (2004) Functions of NF-κB1 and NF-κB2 in immune cell biology. Biochem. J. 382, 393-409
12. Pereira, S. G. and Oakley, F. (2008) Nuclear factor-κB1: regulation and function. Int. J. Biochem. Cell Biol. 40, 1425-1430
13. Karban, A. S., Okazaki, T., Panhuysen, C. I., Gallegos, T., Potter, J. J., Bailey-Wilson, J. E., Silverberg, M. S., Duerr, R. H., Cho, J. H., Gregersen, P. K. et al. (2004) Functional annotation of a novel NFKB1 promoter polymorphism that increases risk for ulcerative colitis. Hum. Mol. Gen. 13, 35-45
14. Zhou, B., Rao, L., Peng, Y., Wang, Y., Qie, M., Zhang, Z., Song, Y. and Zhang, L. (2010) A functional promoter polymorphism in NFKB1 increases susceptibility to endometriosis. DNA Cell Biol. 29, 235-239
15. Zou, Y. F., Wang, F., Feng, X. L., Tao, J. H., Zhu, J. M., Pan, F. M. and Su, H. (2011) Association of NFKB1-94ins/delATTG promoter polymorphism with susceptibility to autoimmune and inflammatory diseases: a meta-analysis. Tissue Antigens 77, 9-17
16. Marcos, M., Pastor, I., Gonźalez-Sarmiento, R. and Laso, F. J. (2009) A functional polymorphism of the NFKB1 gene increases the risk for alcoholic liver cirrhosis in patients with alcohol dependence. Alcohol Clin. Exp. Res. 33, 1857-1862
17. Kato, A., Edwards, M. J. and Lentsch, A. B. (2002) Gene deletion of NF-κ B p50 does not alter the hepatic inflammatory response to ischemia/reperfusion. J. Hepatol. 37, 48-55
18. DeAngelis, R. A., Kovalovich, K., Cressman, D. E. and Taub, R. (2001) Normal liver regeneration in p50/nuclear factor κB1 knockout mice. Hepatology 33, 915-924
19. Oakley, F., Mann, J., Nailard, S., Smart, D. E., Mungalsingh, N., Constandinou, C., Ali, S., Wilson, S. J., Millward-Sadler, H., Iredale, J. P. and Mann, D. A. (2005) Nuclear factor-κB1 (p50) limits the inflammatory and fibrogenic responses to chronic injury. Am. J. Pathol. 166, 695-708
20. Tang, T., Zhang, J., Yin, J., Gawronska-Kozak, B., Jung, D. Y., Ko, H. J., Ong, H., Kim, J. K., Mynatt, R., Martin, R. J. et al. (2010) Uncoupling of inflammation and insulin resistance by NF-κB in transgenic mice through elevated energy expenditure. J. Biol. Chem. 285, 4637-4644
21. Kleiner, D. E., Brunt, E. M., Van Natta, M., Behling, C., Contos, M. J., Cummings, O. W., Ferrell, L. D., Liu, Y. C., Torbenson, M. S., Unalp-Arida, A. et al. (2005) Nonalcoholic steatohepatitis clinical research network. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41, 1313-1321
22. Crispe, N. I. (1997) Isolation of mouse intrahepatic lymphocytes. Curr. Protoc. Immunol., Chapter 3, Unit 3.21
23. Cao, S., Zhang, X., Edwards, J. P. and Mosser, D. M. (2006) NF-κB1 (p50) homodimers differentially regulate pro- and anti-inflammatory cytokines in macrophages. J. Biol. Chem. 281, 26041-26050
24. Elsharkawy, A. M., Oakley, F., Lin, F., Packham, G., Mann, D. A. and Mann, J. (2010) The NF-κB p50:p50:HDAC-1 repressor complex orchestrates transcriptional inhibition of multiple pro-inflammatory genes. J. Hepatol. 53, 519-527
25. Porta, C., Rimordi, M., Raes, G., Brys, L., Grezzi, P., Di Liberto, D., Dieli, F., Ghisletti, S., Natoli, G., De Baetselier, P. et al. (2009) Tolerance and M2 (alternative) macrophage polarization are related processes orchestrated by p50 nuclear factor κB. Proc. Natl. Acad. Sci. U.S.A. 106, 14978-14983
26. Steel, J. C., Waldmann, T. A. and Morris, J. C. (2012) Interleukin-15 biology and its therapeutic implications in cancer. Trends Pharmacol. Sci. 33, 35-41
27. Syn, W. K., Oo, Y. H., Pereira, T. A., Karaca, G. F., Jung, Y., Omenetti, A., Witek, R. P., Choi, S. S., Guy, C. D., Fearing, C. M. et al. (2010) Accumulation of natural killer T cells in progressive non-alcoholic fatty liver disease. Hepatology 51, 1998-2007
28. Syn, W. K., Agboola, K. M., Swiderska, M., Michelotti, G. A., Liaskou, E., Pang, H., Xie, G., Philips, G., Chan, I. S., Karaca, G. F. et al. (2012) NKT-associated hedgehog and osteopontin drive fibrogenesis in non-alcoholic fatty liver disease. Gut 9, 1323-1329
29. Li, Z., Soloski, M. K. and Diehl, A. M. (2005) Dietary factors alter hepatic innate immune system in mice with nonalcoholic fatty liver disease. Hepatology 42, 880-885
30. Kremer, M., Thomas, E., Milton, R. J., Perry, A. W., van Rooijen, N., Wheeler, M. D., Zacks, S., Fried, M., Rippe, R. A. and Hines, I. N (2010) Kupffer cell and interleukin-12-dependent loss of natural killer T cells in hepatosteatosis. Hepatology 51, 130-141
31. Miyagi, T., Takehara, T., Uemura, A., Nishio, K., Shimizu, S., Kodama, T., Hikita, H., Li, W., Sasakawa, A., Tatsumi, T. et al. (2010) Absence of invariant natural killer T cells deteriorates liver inflammation and fibrosis in mice fed high-fat diet. J. Gastroenterol. 45, 1247-1254
32. Tajiri, K., Shimizu, Y., Tsuneyama, K. and Sugiyama, T. (2009) Role of liver-infiltrating CD3+ CD56+ natural killer T cells in the pathogenesis of nonalcoholic fatty liver disease. Eur. J. Gastroenterol. Hepatol. 21, 673-80
33. Stankovic, S., Gugasyan, R., Kyparissoudis, K., Grumont, R., Banerjee, A., Tsichlis, P., Gerondakis, S. and Godfrey, D. I. (2011) Distinct roles in NKT cell maturation and function for the different transcription factors in the classical NF-κB pathway. Immunol. Cell Biol. 89, 294-303
34. Correia, M. P., Cardoso, E. M., Pereira, C. F., Neves, R., Uhrberg, M. and Arosa, F. A. (2009) Hepatocytes and IL-15: a favorable microenvironment for T cell survival and CD8+ T cell differentiation. J. Immunol. 182, 6149-6159
35. Suzuki, A., McCall, S., Choi, S. S., Sicklick, J. K., Huang, J., Qi, Y., Zdanowicz, M., Camp, T., Li, Y. X. and Diehl, A. M. (2006) Interleukin-15 increases hepatic regenerative activity. J. Hepatol. 45, 410-418
36. Morimoto, J., Kon, S., Matsui, Y. and Uede, T. (2010) Osteopontin as a target molecule for the treatment of inflammatory diseases. Curr. Drug Targets 11, 494-505
37. Diao, H., Kon, S., Iwabuchi, K., Kimura, C., Morimoto, J., Ito, D., Segawa, T., Maeda, M., Hamuro, J., Nakayama, T. et al. (2004) Osteopontin as a mediator of NKT cell function in T cell-mediated liver diseases. Immunity 21, 539-550
38. Syn, W. K., Choi, S. S., Liaskou, E., Karaca, G. F., Agboola, K. M., Oo, Y. H., Mi, Z., Pereira, T. A., Zdanowicz, M., Malladi, P. et al. (2011) Osteopontin is induced by hedgehog pathway activation and promotes fibrosis progression in nonalcoholic steatohepatitis. Hepatology 53, 106-115
39. Sahai, A., Malladi, P., Melin-Aldana, H., Green, R. M. and Whitington, P. F. (2004) Upregulation of osteopontin expression is involved in the development of nonalcoholic steatohepatitis in a dietary murine model. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G264-G273
40. Zeyda, M., Gollinger, K., Todoric, J., Kiefer, F. W., Keck, M., Aszmann, O., Prager, G., Zlabinger, G. J., Petzelbauer, P. and Stulnig, T. M. (2011) Osteopontin is an activator of human adipose tissue macrophages and directly affects adipocyte function. Endocrinology 152, 2219-2227
41. Rangnekar, A. S., Lammert, F., Igolnikov, A. and Green, R. M. (2006) Quantitative trait loci analysis of mice administered the methionine-choline deficient dietary model of experimental steatohepatitis. Liver Int. 26, 1000-1005
42. Vβ3 engagement and PI3K-pAkt-NFκB signaling. Hepatology 55, 594-608