Selonsertib Inhibits Liver Fibrosis via Downregulation of ASK1/MAPK Pathway of Hepatic Stellate Cells |
Yoon, Young-Chan
(Department of Biomedical Sciences, College of Medicine, and Program in Biomedical Science & Engineering, Inha University)
Fang, Zhenghuan (Department of Biomedical Sciences, College of Medicine, and Program in Biomedical Science & Engineering, Inha University) Lee, Ji Eun (Department of Biomedical Sciences, College of Medicine, and Program in Biomedical Science & Engineering, Inha University) Park, Jung Hee (Department of Biomedical Sciences, College of Medicine, and Program in Biomedical Science & Engineering, Inha University) Ryu, Ji-Kan (Department of Urology, College of Medicine, Inha University) Jung, Kyung Hee (Department of Biomedical Sciences, College of Medicine, and Program in Biomedical Science & Engineering, Inha University) Hong, Soon-Sun (Department of Biomedical Sciences, College of Medicine, and Program in Biomedical Science & Engineering, Inha University) |
1 | Noureddin, M., Anstee, Q. M. and Loomba, R. (2016) Review article: emerging anti-fibrotic therapies in the treatment of non-alcoholic steatohepatitis. Aliment. Pharmacol. Ther. 43, 1109-1123. DOI |
2 | Pellicoro, A., Ramachandran, P., Iredale, J. P. and Fallowfield, J. A. (2014) Liver fibrosis and repair: immune regulation of wound healing in a solid organ. Nat. Rev. Immunol. 14, 181-194. DOI |
3 | Priya, S. and Sudhakaran, P. R. (2008) Cell survival, activation and apoptosis of hepatic stellate cells: modulation by extracellular matrix proteins. Hepatol. Res. 38, 1221-1232. |
4 | Son, G., Hines, I. N., Lindquist, J., Schrum, L. W. and Rippe, R. A. (2009) Inhibition of phosphatidylinositol 3-kinase signaling in hepatic stellate cells blocks the progression of hepatic fibrosis. Hepatology 50, 1512-1523. DOI |
5 | Song, J., Cho, K. J., Cheon, S. Y., Kim, S. H., Park, K. A., Lee, W. T. and Lee, J. E. (2013) Apoptosis signal-regulating kinase 1 (ASK1) is linked to neural stem cell differentiation after ischemic brain injury. Exp. Mol. Med. 45, e69. DOI |
6 | Tobiume, K., Matsuzawa, A., Takahashi, T., Nishitoh, H., Morita, K., Takeda, K., Minowa, O., Miyazono, K., Noda, T. and Ichijo, H. (2001) ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep. 2, 222-228. DOI |
7 | Tsukada, S., Westwick, J. K., Ikejima, K., Sato, N. and Rippe, R. A. (2005) SMAD and p38 MAPK signaling pathways independently regulate alpha1(I) collagen gene expression in unstimulated and transforming growth factor-beta-stimulated hepatic stellate cells. J. Biol. Chem. 280, 10055-10064. DOI |
8 | Wang, Y., Gao, J., Zhang, D., Zhang, J., Ma, J. and Jiang, H. (2010) New insights into the antifibrotic effects of sorafenib on hepatic stellate cells and liver fibrosis. J. Hepatol. 53, 132-144. DOI |
9 | Zhang, C. Y., Yuan, W. G., He, P., Lei, J. H. and Wang, C. X. (2016) Liver fibrosis and hepatic stellate cells: etiology, pathological hallmarks and therapeutic targets. World J. Gastroenterol. 22, 10512-10522. DOI |
10 | Yu, F. X., Teng, Y. Y., Zhu, Q. D., Zhang, Q. Y. and Tang, Y. H. (2014) Inhibitory effects of capsaicin on hepatic stellate cells and liver fibrosis. Biochem. Cell Biol. 92, 406-412. DOI |
11 | Zhang, X. L., Chen, Z. N., Huang, Q. F., Bai, F. C., Nie, J. L., Lu, S. J., Wei, J. B. and Lin, X. (2018) Methyl helicterate inhibits hepatic stellate cell activation through modulation of apoptosis and autophagy. Cell. Physiol. Biochem. 51, 897-908. DOI |
12 | Carpino, G., Morini, S., Ginanni Corradini, S., Franchitto, A., Merli, M., Siciliano, M., Gentili, F., Onetti Muda, A., Berloco, P., Rossi, M., Attili, A. F. and Gaudio, E. (2005) Alpha-SMA expression in hepatic stellate cells and quantitative analysis of hepatic fibrosis in cirrhosis and in recurrent chronic hepatitis after liver transplantation. Dig. Liver Dis. 37, 349-356. DOI |
13 | Amos, L. A., Ma, F. Y., Tesch, G. H., Liles, J. T., Breckenridge, D. G., Nikolic-Paterson, D. J. and Han, Y. (2018) ASK1 inhibitor treatment suppresses p38/JNK signalling with reduced kidney inflammation and fibrosis in rat crescentic glomerulonephritis. J. Cell. Mol. Med. 22, 4522-4533. DOI |
14 | Arriazu, E., Ruiz de Galarreta, M., Cubero, F. J., Varela-Rey, M., Perez de Obanos, M. P., Leung, T. M., Lopategi, A., Benedicto, A., Abraham-Enachescu, I. and Nieto, N. (2014) Extracellular matrix and liver disease. Antioxid. Redox Signal. 21, 1078-1097. DOI |
15 | Baffy, G. (2013) Hepatocellular carcinoma in non-alcoholic fatty liver disease: epidemiology, pathogenesis, and prevention. J. Clin. Transl. Hepatol. 1, 131-137. |
16 | Bataller, R. and Brenner, D. A. (2005) Liver fibrosis. J. Clin. Invest. 115, 209-218. DOI |
17 | Budas, G. R., Boehm, M., Kojonazarov, B., Viswanathan, G., Tian, X., Veeroju, S., Novoyatleva, T., Grimminger, F., Hinojosa-Kirschenbaum, F., Ghofrani, H. A., Weissmann, N., Seeger, W., Liles, J. T. and Schermuly, R. T. (2018) ASK1 inhibition halts disease progression in preclinical models of pulmonary arterial hypertension. Am. J. Respir. Crit. Care Med. 197, 373-385. DOI |
18 | Cuenda, A. and Rousseau, S. (2007) p38 MAP-kinases pathway regulation, function and role in human diseases. Biochim. Biophys. Acta 1773, 1358-1375. DOI |
19 | De Oliveira da Silva, B., Ramos, L. F. and Moraes, K. C. M. (2017) Molecular interplays in hepatic stellate cells: apoptosis, senescence, and phenotype reversion as cellular connections that modulate liver fibrosis. Cell Biol. Int. 41, 946-959. DOI |
20 | Elsharkawy, A. M., Oakley, F. and Mann, D. A. (2005) The role and regulation of hepatic stellate cell apoptosis in reversal of liver fibrosis. Apoptosis 10, 927-939. DOI |
21 | Hatai, T., Matsuzawa, A., Inoshita, S., Mochida, Y., Kuroda, T., Sakamaki, K., Kuida, K., Yonehara, S., Ichijo, H. and Takeda, K. (2000) Execution of apoptosis signal-regulating kinase 1 (ASK1)-induced apoptosis by the mitochondria-dependent caspase activation. J. Biol. Chem. 275, 26576-26581. DOI |
22 | Ikejima, K., Takei, Y., Honda, H., Hirose, M., Yoshikawa, M., Zhang, Y. J., Lang, T., Fukuda, T., Yamashina, S., Kitamura, T. and Sato, N. (2002) Leptin receptor-mediated signaling regulates hepatic fibrogenesis and remodeling of extracellular matrix in the rat. Gastroenterology 122, 1399-1410. DOI |
23 | Hayakawa, R., Hayakawa, T., Takeda, K. and Ichijo, H. (2012) Therapeutic targets in the ASK1-dependent stress signaling pathways. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 88, 434-453. DOI |
24 | Higashi, T., Friedman, S. L. and Hoshida, Y. (2017) Hepatic stellate cells as key target in liver fibrosis. Adv. Drug Deliv. Rev. 121, 27-42. DOI |
25 | Ichijo, H., Nishida, E., Irie, K., ten Dijke, P., Saitoh, M., Moriguchi, T., Takagi, M., Matsumoto, K., Miyazono, K. and Gotoh, Y. (1997) Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 275, 90-94. DOI |
26 | Kanda, T., Goto, T., Hirotsu, Y., Moriyama, M. and Omata, M. (2019) Molecular mechanisms driving progression of liver cirrhosis towards hepatocellular carcinoma in chronic hepatitis B and C infections: a review. Int. J. Mol. Sci. 20, 1358. DOI |
27 | Kanda, T., Matsuoka, S., Yamazaki, M., Shibata, T., Nirei, K., Takahashi, H., Kaneko, T., Fujisawa, M., Higuchi, T., Nakamura, H., Matsumoto, N., Yamagami, H., Ogawa, M., Imazu, H., Kuroda, K. and Moriyama, M. (2018) Apoptosis and non-alcoholic fatty liver diseases. World J. Gastroenterol. 24, 2661-2672. DOI |
28 | Lee, J. H., Lee, H., Joung, Y. K., Jung, K. H., Choi, J. H., Lee, D. H., Park, K. D. and Hong, S. S. (2011) The use of low molecular weight heparin-pluronic nanogels to impede liver fibrosis by inhibition the TGF-beta/Smad signaling pathway. Biomaterials 32, 1438-1445. DOI |
29 | Kluwe, J., Pradere, J. P., Gwak, G. Y., Mencin, A., De Minicis, S., Osterreicher, C. H., Colmenero, J., Bataller, R. and Schwabe, R. F. (2010) Modulation of hepatic fibrosis by c-Jun-N-terminal kinase inhibition. Gastroenterology 138, 347-359. DOI |
30 | Kovalic, A. J., Satapathy, S. K. and Chalasani, N. (2018) Targeting incretin hormones and the ASK-1 pathway as therapeutic options in the treatment of non-alcoholic steatohepatitis. Hepatol. Int. 12, 97-106. DOI |
31 | Liles, J. T., Corkey, B. K., Notte, G. T., Budas, G. R., Lansdon, E. B., Hinojosa-Kirschenbaum, F., Badal, S. S., Lee, M., Schultz, B. E., Wise, S., Pendem, S., Graupe, M., Castonguay, L., Koch, K. A., Wong, M. H., Papalia, G. A., French, D. M., Sullivan, T., Huntzicker, E. G., Ma, F. Y., Nikolic-Paterson, D. J., Altuhaifi, T., Yang, H., Fogo, A. B. and Breckenridge, D. G. (2018) ASK1 contributes to fibrosis and dysfunction in models of kidney disease. J. Clin. Invest. 128, 4485-4500. DOI |
32 | Loomba, R., Lawitz, E., Mantry, P. S., Jayakumar, S., Caldwell, S. H., Arnold, H., Diehl, A. M., Djedjos, C. S., Han, L., Myers, R. P., Subramanian, G. M., McHutchison, J. G., Goodman, Z. D., Afdhal, N. H. and Charlton M.R.; GS-US-384-1497 Investigators (2018) The ASK1 inhibitor selonsertib in patients with nonalcoholic steatohepatitis: a randomized, phase 2 trial. Hepatology 67, 549-559. DOI |
33 | Nakagawa, H., Maeda, S., Hikiba, Y., Ohmae, T., Shibata, W., Yanai, A., Sakamoto, K., Ogura, K., Noguchi, T., Karin, M., Ichijo, H. and Omata, M. (2008) Deletion of apoptosis signal-regulating kinase 1 attenuates acetaminophen-induced liver injury by inhibiting c-Jun N-terminal kinase activation. Gastroenterology 135, 1311-1321. DOI |