STK4 regulates TLR pathways and protects against chronic inflammation-related hepatocellular carcinoma

Journal of Clinical Investigation

Volumn 125, Issue 11, 2015, Pages 4239-4254

  Li, Weiyun ^a   Xiao, Jun ^a   Zhou, Xin ^a   Xu, Ming ^b   Hu, Chaobo ^a   Xu, Xiaoyan ^a   Lu, Yao ^a   Liu, Chang ^a   Xue, Shengjie ^a   Nie, Lei ^c   Zhang, Haibin ^d   Li, Zhiqi ^e   Zhang, Yanbo ^a   Ji, Fu ^b   Hui, Lijian ^a   Tao, Wufan ^f   Wei, Bin ^a,g   Wang, Hongyan ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c HUBEI CANCER HOSPITAL   (China)

^d SECOND MILITARY MEDICAL UNIVERSITY   (China)

^e FUDAN UNIVERSITY   (China)

^f FUDAN UNIVERSITY   (China)

^g WUHAN INSTITUTE OF VIROLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 6; PROTEIN SERINE THREONINE KINASE; PROTEIN SERINE THREONINE KINASE 4; STAT3 PROTEIN; SYNAPTOTAGMIN I; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG; CARBON TETRACHLORIDE; CYTOKINE; DIETHYLNITROSAMINE; IL6 PROTEIN, HUMAN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE; IRAK1 PROTEIN, HUMAN; IRAK1 PROTEIN, MOUSE; LIPOPOLYSACCHARIDE; RELA PROTEIN, HUMAN; STAT3 PROTEIN, HUMAN; STK4 PROTEIN, HUMAN; STK4 PROTEIN, MOUSE; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR RELA; TUMOR PROTEIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CHRONIC INFLAMMATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYMATIC DEGRADATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INFLAMMATION; LIVER CELL CARCINOMA; LIVER FIBROSIS; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; ANIMAL HEPATITIS; BIOSYNTHESIS; BLOOD; CARCINOMA, HEPATOCELLULAR; CHEMICALLY INDUCED; CHEMISTRY; COMPLICATION; DEFICIENCY; ESCHERICHIA COLI INFECTION; FEMALE; GENETICS; GERMFREE ANIMAL; HEK293 CELL LINE; IMMUNOLOGY; INNATE IMMUNITY; LIVER NEOPLASMS; LIVER NEOPLASMS, EXPERIMENTAL; LUNG; MALE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; SECRETION (PROCESS);

ANIMALS; CARBON TETRACHLORIDE; CARCINOMA, HEPATOCELLULAR; CYTOKINES; DIETHYLNITROSAMINE; ESCHERICHIA COLI INFECTIONS; FEMALE; HEK293 CELLS; HEPATITIS, ANIMAL; HUMANS; IMMUNITY, INNATE; INTERFERON-BETA; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; LIVER NEOPLASMS; LIVER NEOPLASMS, EXPERIMENTAL; LUNG; MACROPHAGES; MALE; MICE; NEOPLASM PROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; SPECIFIC PATHOGEN-FREE ORGANISMS; STAT3 TRANSCRIPTION FACTOR; TOLL-LIKE RECEPTORS; TRANSCRIPTION FACTOR RELA;

EID: 84946762064     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI81203     Document Type: Article

References (60)

1. Hussain SP, Harris CC. Inflammation and cancer: an ancient link with novel potentials. Int J Cancer. 2007;121(11):2373-2380.
2. Yang L, Karin M. Roles of tumor suppressors in regulating tumor-associated inflammation. Cell Death Differ. 2014;21(11):1677-1686.
3. Dapito DH, et al. Promotion of hepatocellular carcinoma by the intestinal microbiota and TLR4. Cancer Cell. 2012;21(4):504-516.
4. Aksoy E, et al. The p110delta isoform of the kinase PI(3)K controls the subcellular com-partmentalization of TLR4 signaling and protects from endotoxic shock. Nat Immunol. 2012;13(11):1045-1054.
5. Liew FY, Xu D, Brint EK, O'Neill LA. Negative regulation of toll-like receptor-mediated immune responses. Nat Rev Immunol. 2005;5(6):446-458.
6. Zhang Y, et al. Activation of vascular endo-thelial growth factor receptor-3 in macrophages restrains TLR4-NF-κB signaling and protects against endotoxin shock. Immunity. 2014;40(4):501-514.
7. Bard-Chapeau EA, et al. Ptpn11/Shp2 acts as a tumor suppressor in hepatocellular carcinogene-sis. Cancer Cell. 2011;19(5):629-639.
8. Gautheron J, Luedde T. A novel player in inflammation and cancer: the deubiquitinase CYLD controls HCC development. J Hepatol. 2012;57(5):937-939.
9. Takahashi H, Ogata H, Nishigaki R, Broide DH, Karin M. Tobacco smoke promotes lung tum-origenesis by triggering IKKβ- and JNK1-depen-dent inflammation. Cancer Cell. 2010;17(1):89-97.
10. Li L, et al. A unique role for p53 in the regulation of M2 macrophage polarization. Cell Death Differ. 2015;22(7):1081-1093.
11. Cooks T, et al. Mutant p53 prolongs NF-κB activation and promotes chronic inflammation and inflammation-associated colorectal cancer. Cancer Cell. 2013;23(5):634-646.
12. Wu H, et al. Integration of Hippo signaling and the unfolded protein response to restrain liver overgrowth and tumorigenesis. Nat Commun. 2015;6:6239.
13. Zhou D, et al. Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell. 2009;16(5):425-438.
14. Kim TS, Lee DH, Kim SK, Shin SY, Seo EJ, Lim DS. Mammalian sterile 20-like kinase 1 suppresses lymphoma development by promoting faithful chromosome segregation. Cancer Res. 2012;72(20):5386-5395.
15. Nehme NT, et al. MST1 mutations in autosomal recessive primary immunodeficiency characterized by defective naive T-cell survival. Blood. 2012;119(15):3458-3468.
16. Zhou D, et al. The Nore1B/Mst1 complex restrains antigen receptor-induced proliferation of naive T cells. Proc Natl Acad Sci USA. 2008;105(51):20321-20326.
17. Katagiri K, Imamura M, Kinashi T. Spatiotemporal regulation of the kinase Mst1 by binding protein RAPL is critical for lymphocyte polarity and adhesion. Nat Immunol. 2006;7(9):919-928.
18. Zhang YB, Wang HY. Integrin signaling and function in immune cells. Immunology. 2012;135(4):268-275.
19. Wang HY, Lim D, Rudd CE. Immunopathologies linked to integrin signaling. Semin Immunopathol. 2010;32(2):173-182.
20. Raab M, et al. T cell receptor "inside-out" pathway via signaling module SKAP1-RapL regulates T cell motility and interactions in lymph nodes. Immunity. 2010;32(4):541-556.
21. Wang H, Rudd CE. SKAP-55, SKAP-55-related and ADAP adaptors modulate integrin-medi-ated immune-cell adhesion. Trends Cell Biol. 2008;18(10):486-493.
22. + cytotoxic T lymphocytes for enhanced anti-tumor immuno-therapy. EMBO Mol Med. 2015;7(6):754-769.
23. Schneider H, et al. Adaptor SKAP-55 binds p21 activating exchange factor RasGRP1 and negatively regulates the p21-ERK pathway in T-cells. PLoS One. 2008;3(3):e1718.
24. MacIver NJ, et al. The liver kinase B1 is a central regulator of T cell development, activation, and metabolism. J Immunol. 2011;187(8):4187-4198.
25. Zhang YG, et al. Axin1 prevents Salmonella inva-siveness and inflammatory response in intestinal epithelial cells. PLoS One. 2012;7(4):e34942.
26. Bleriot C, Dupuis T, Jouvion G, Eberl G, Disson O, Lecuit M. Liver-resident macrophage necroptosis orchestrates type 1 microbicidal inflammation and type-2-mediated tissue repair during bacterial infection. Immunity. 2015;42(1):145-158.
27. Mencin A, Kluwe J, Schwabe RF. Toll-like receptors as targets in chronic liver diseases. Gut. 2009;58(5):704-720.
28. Liaunardy-Jopeace A, Gay NJ. Molecular and cellular regulation of toll-like receptor-4 activity induced by lipopolysaccharide ligands. Front Immunol. 2014;5:473.
29. McGettrick AF, O'Neill LA. Localisation and trafficking of Toll-like receptors: an important mode of regulation. Curr Opin Immunol. 2010;22(1):20-27.
30. Cinar B, et al. The pro-apoptotic kinase Mst1 and its caspase cleavage products are direct inhibitors of Akt1. EMBO J. 2007;26(21):4523-4534.
31. Du X, et al. Mst1/Mst2 regulate development and function of regulatory T cells through modulation of Foxo1/Foxo3 stability in autoimmune disease. J Immunol. 2014;192(4):1525-1535.
32. An H, et al. Phosphatase SHP-1 promotes TLR- and RIG-I-activated production of type I interferon by inhibiting the kinase IRAK1. Nat Immunol. 2008;9(5):542-550.
33. Bruni D, Sebastia J, Dunne S, Schroder M, Butler MP. A novel IRAK1-IKKε signaling axis limits the activation of TAK1-IKKβ downstream of TLR3. J Immunol. 2013;190(6):2844-2856.
34. Murakami Y, Mizoguchi F, Saito T, Miyasaka N, Kohsaka H. p16(INK4a) exerts an anti-inflammatory effect through accelerated IRAK1 degradation in macrophages. J Immunol. 2012;189(10):5066-5072.
35. Yamin TT, Miller DK. The interleukin-1 receptor-associated kinase is degraded by protea-somes following its phosphorylation. J Biol Chem. 1997;272(34):21540-21547.
36. Gottipati S, Rao NL, Fung-Leung WP. IRAK1: A critical signaling mediator of innate immunity. Cell Signal. 2008;20(2):269-276.
37. Johnson C, Han Y, Hughart N, McCarra J, Alpini G, Meng F. Interleukin-6 and its receptor, key players in hepatobiliary inflamzmation and cancer. Transl Gastrointest Cancer. 2012;1(1):58-70.
38. Mano Y, et al. Tumor-associated macrophage promotes tumor progression via STAT3 signaling in hepatocellular carcinoma. Pathobiology. 2013;80(3):146-154.
39. Naugler WE, et al. Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science. 2007;317(5834):121-124.
40. Nikolaou K, Tsagaratou A, Eftychi C, Kollias G, Mosialos G, Talianidis I. Inactivation of the deubiquitinase CYLD in hepatocytes causes apoptosis, inflammation, fibrosis, and cancer. Cancer Cell. 2012;21(6):738-750.
41. Lin FC, Young HA. Interferons: Success in anti-viral immunotherapy. Cytokine Growth Factor Rev. 2014;25(4):369-376.
42. Bataller R, Brenner DA. Liver fibrosis. J Clin Invest. 2005;115(2):209-218.
43. Son G, Kremer M, Hines IN. Contribution of gut bacteria to liver pathobiology. Gastroenterol Res Pract. 2010;2010:453563.
44. Agha-Amiri K, Klauck S, Malfertheiner P. Bacterial infection is frequent in human hepatocellular carcinoma (HCC), but not in liver cirrhosis. Gas-troenterology. 2000;118(4 part 1):A321.
45. Schmitz R, et al. TNFAIP3 (A20) is a tumor suppressor gene in Hodgkin lymphoma and primary mediastinal B cell lymphoma. J Exp Med. 2009;206(5):981-989.
46. Ma A, Malynn BA. A20: linking a complex regulator of ubiquitylation to immunity and human disease. Nat Rev Immunol. 2012;12(11):774-785.
47. Bignell GR, et al. Identification of the familial cylindromatosis tumour-suppressor gene. Nat Genet. 2000;25(2):160-165.
48. Yoshida H, Jono H, Kai H, Li JD. The tumor suppressor cylindromatosis (CYLD) acts as a negative regulator for toll-like receptor 2 signaling via negative cross-talk with TRAF6 AND TRAF7. J Biol Chem. 2005;280(49):41111-41121.
49. Stifter SA, Feng CG. Interfering with immunity: detrimental role of type I IFNs during infection. J Immunol. 2015;194(6):2455-2465.
50. Perry AK, Chen G, Zheng D, Tang H, Cheng G. The host type I interferon response to viral and bacterial infections. Cell Res. 2005;15(6):407-422.
51. Takeyasu M, et al. Long-term interferon monother-apy reduces the risk of HCV-associated hepatocel-lular carcinoma. J Med Virol. 2012;84(8):1199-1207.
52. Sakurai T, et al. Hepatocyte necrosis induced by oxidative stress and IL-1α release mediate carcinogen-induced compensatory proliferation and liver tumorigenesis. Cancer Cell. 2008;14(2):156-165.
53. Abdollahpour H, et al. The phenotype of human STK4 deficiency. Blood. 2012;119(15):3450-3457.
54. Crequer A, et al. Inherited MST1 deficiency underlies susceptibility to EV-HPV infections. PLoS O ne. 2012;7(8):e44010.
55. Zuo M, Li C, Lin J, Javle M. LLL12, a novel small inhibitor targeting STAT3 for hepatocellular carcinoma therapy. Oncotarget. 2015; 6(13):10940-10949.
56. He G, Karin M. NF-κB and STAT3 - key players in liver inflammation and cancer. Cell Res. 2011;21(1):159-168.
57. Arsura M, Cavin LG. Nuclear factor-κB and liver carcinogenesis. Cancer Lett. 2005;229(2):157-169.
58. Li Z, et al. Inhibition of IRAK1/4 sensitizes T cell acute lymphoblastic leukemia to chemotherapies. J Clin Invest. 2015;125(3):1081-1097.
59. Saeki I, et al. Bortezomib induces tumor-specific cell death and growth inhibition in hepatocellular carcinoma and improves liver fibrosis. J Gas-troenterol. 2013;48(6):738-750.
60. Zhai XH, Yu JK, Yang FQ, Zheng S. Identification of a new protein biomarker for colorectal cancer diagnosis. Mol Med Rep. 2012;6(2):444-448.