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Basic Research Paper

Autophagy induced by AXL receptor tyrosine kinase alleviates acute liver injury via inhibition of NLRP3 inflammasome activation in mice

, , , , , , , , , , & show all
Pages 2326-2343 | Received 23 Dec 2015, Accepted 07 Sep 2016, Published online: 26 Oct 2016

References

  • Rockey DC, Bell PD, Hill JA. Fibrosis- a common pathway to organ injury and failure. N Engl J Med 2015; 372:1138-49; PMID:25785971; http://dx.doi.org/10.1056/NEJMra1300575
  • Seki E, Schwabe RF. Hepatic inflammation and Fibrosis: Functional links and key pathways. Hepatology 2015; 61:1066-79; PMID:25066777; http://dx.doi.org/10.1002/hep.27332
  • Crispe IN. The liver as a lymphoid organ. Annu Rev Immunol 2009; 27:147-63; PMID:19302037; http://dx.doi.org/10.1146/annurev.immunol.021908.132629
  • Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 2012; 22:787-95; http://dx.doi.org/10.1172/JCI59643
  • Scott RS, McMahon EJ, Pop SM, Reap EA, Caricchio R, Cohen PL, Earp HS, Matsushima GK. Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature 2001; 411:207-11; PMID:11346799; http://dx.doi.org/10.1038/35075603
  • Zagórska A, Través PG, Lew ED, Dransfield I, Lemke G. Diversification of TAM receptor tyrosine kinase function. Nat Immunol 2014; 15:920-8; http://dx.doi.org/10.1038/ni.2986
  • Sharif MN, Sosic D, Rothlin CV, Kelly E, Lemke G, Olson EN, Ivashkiv LB. Twist mediates suppression of inflammation by type I IFNs and Axl. J Exp Med 2006; 203:1891-901; PMID:16831897; http://dx.doi.org/10.1084/jem.20051725
  • Rothlin CV, Ghosh S, Zuniga EI, Oldstone MB, Lemke G. TAM receptors are pleiotropic inhibitors of the innate immune response. Cell 2007; 131:1124-36; PMID:18083102; http://dx.doi.org/10.1016/j.cell.2007.10.034
  • Lu Q, Lemke G. Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family. Science 2001; 293:306-11; PMID:11452127; http://dx.doi.org/10.1126/science.1061663
  • Cohen PL, Caricchio R, Abraham V, Camenisch TD, Jennette JC, Roubey RA, Earp HS, Matsushima G, Reap EA. Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J Exp Med 2002; 196:135-40; PMID:12093878; http://dx.doi.org/10.1084/jem.20012094
  • Llacuna L, Bárcena C, Bellido-Martín L, Fernández L, Stefanovic M, Marí M, García-Ruiz C, Fernández-Checa JC, García de Frutos P, Morales A. Growth arrest-specific protin 6 is hepatoprotective against murine ischemia/reperfusion injury. Hepatology 2010; 52:1371-9; PMID:20730776; http://dx.doi.org/10.1002/hep.23833
  • Lafdil F, Chobert MN, Deveaux V, Zafrani ES, Mavier P, Nakano T, Laperche T, Brouillet A. Growth arrest-specific protein 6 deficiency impairs liver tissue repair after acute toxic hepatitis in mice. J Hepatol 2009; 51:55-66; PMID:19443073; http://dx.doi.org/10.1016/j.jhep.2009.02.030
  • Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science 2000; 290:1717-21; PMID:10634780
  • Levine B, Deretic V. Unveiling the roles of autophagy in innate and adaptive immunity. Nat Rev Immunol 2007; 7:767-77; PMID:17767194; http://dx.doi.org/10.1038/nri2161
  • Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451:1069-75; PMID:18305538; http://dx.doi.org/10.1038/nature06639
  • Saitoh T, Fujita N, Jang MH, Uematsu S, Yang BG, Satoh T, Omori H, Noda T, Yamamoto N, Komatsu M, et al. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 2008; 456:264-8; PMID:18849965; http://dx.doi.org/10.1038/nature07383
  • Zhou R, Yazdi AS, Menu P, Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011; 469:221-5; PMID:21124315; http://dx.doi.org/10.1038/nature09663
  • Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, Englert JA, Rabinovitch M, Cernadas M, Kim HP, et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 2011; 12:222-30; PMID:21151103; http://dx.doi.org/10.1038/ni.1980
  • Beth L, Noboru M, Herbert WV. Autophagy in immunity and inflammation. Nature 2011; 469:323-35; PMID:21248839; http://dx.doi.org/10.1038/nature09782
  • Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol 2013; 13:722-37; PMID:24064518; http://dx.doi.org/10.1038/nri3532
  • Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, Adachi H, Adams CM, Adams PD, Adeli K, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 2016; 12:1-222; PMID:26799652; http://dx.doi.org/10.1080/15548627.2015.1100356
  • Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy 2007; 3:542-5; PMID:17611390; http://dx.doi.org/10.4161/auto.4600
  • Mizushima N, Yoshimori T, Ohsumi Y. The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 2011; 27:107-32; PMID:21801009; http://dx.doi.org/10.1146/annurev-cellbio-092910-154005
  • Paccez JD, Vogelsang M, Parker MI, Zerbini LF. The receptor tyrosine kinase Axl in cancer: biological functions and therapeutic implications. Int J Cancer 2014; 134:1024-33; PMID:23649974; http://dx.doi.org/10.1002/ijc.28246
  • Eyers PA, Craxton M, Morrice N, Cohen P, Goedert M. Conversion of SB203580-insensitive MAP kinase family members to drug-sensitive forms by a single amino-acid substitution. Chem Biol 1998; 5:321-8; PMID:9653550; http://dx.doi.org/10.1016/S1074-5521(98)90170-3
  • Li P, Allen H, Banerjee S, Franklin S, Herzog L, Johnston C, McDowell J, Paskind M, Rodman L, Salfeld J, et al. Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell 1995; 80:401-11; PMID:7859282; http://dx.doi.org/10.1016/0092-8674(95)90490-5
  • Sutterwala FS, Ogura Y, Szczepanik M, Lara-Tejero M, Lichtenberger GS, Grant EP, Bertin J, Coyle AJ, Galán JE, Askenase PW, et al. Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 2006; 24:317-27; PMID:16546100; http://dx.doi.org/10.1016/j.immuni.2006.02.004
  • Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 2005; 169:425-34; PMID:15866887; http://dx.doi.org/10.1083/jcb.200412022
  • Yang CS, Kim JJ, Lee HM, Jin HS, Lee SH, Park JH, Kim SJ, Kim JM, Han YM, Lee MS, et al. The AMPK-PPARGC1A pathway is required for antimicrobial host defense through activation of autophagy. Autophagy 2014; 10:785-802; PMID:24598403; http://dx.doi.org/10.4161/auto.28072
  • Guarda G, Braun M, Staehli F, Tardivel A, Mattmann C, Forster I, Farlik M, Decker T, Du Pasquier RA, Romero P, et al. Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 2011; 34:213-23; PMID:21349431; http://dx.doi.org/10.1016/j.immuni.2011.02.006
  • Petrasek J, Bala S, Csak T, Lippai D, Kodys K, Menashy V, Barrieau M, Min SY, Kurt-Jones EA, Szabo G. IL-1 receptor antagonist ameliorates inflammasome-dependent alcoholic steatohepatitis in mice. J Clin Invest 2012; 122:3476-89; PMID:22945633; http://dx.doi.org/10.1172/JCI60777
  • Huang H, Chen HW, Evankovich J, Yan W, Rosborough BR, Nace GW, Ding Q, Loughran P, Beer-Stolz D, Billiar TR, et al. Histones activate the NLRP3 inflammasome in Kupffer cells during sterile inflammatory liver injury. J Immunol 2013; 191:2665-79.
  • Jankovic D, Ganesan J, Bscheider M, Stickel N, Weber FC, Guarda G, Follo M, Pfeifer D, Tardivel A, Ludigs K, et al. The Nlrp3 inflammasome regulates acute graft-versus-host disease. J Exp Med 2013; 210:1899-910; PMID:23980097; http://dx.doi.org/10.1084/jem.20130084
  • Beier JI, Luyendyk JP, Guo L, von Montfort C, Staunton DE, Arteel GE. Fibrin accumulation plays a critical role in the sensitization to lipopolysaccharide-induced liver injury caused by ethanol in mice. Hepatology 2009; 49:1545-53; PMID:19291788; http://dx.doi.org/10.1002/hep.22847
  • Liu K, Zhao E, Ilyas G, Lalazar G, Lin Y, Haseeb M, Tanaka KE, Czaja MJ. Impaired macrophage autophagy increases the immune response in obese mice by promoting proinflammatory macrophage polarization. Autophagy 2015; 11:271-84; PMID:25650776; http://dx.doi.org/10.1080/15548627.2015.1009787
  • Dall'Armi C, Hurtado-Lorenzo A, Tian H, Morel E, Nezu A, Chan RB, Yu WH, Robinson KS, Yeku O, Small SA, et al. The phospholipase D1 pathway modulates macroautophagy. Nat Commun 2010; 1:142; PMID:21266992; http://dx.doi.org/10.1038/ncomms1144
  • Chikh A, Sanzà P, Raimondi C, Akinduro O, Warnes G, Chiorino G, Byrne C, Harwood CA, Bergamaschi D. iASPP is a novel autophagy inhibitor in keratinocytes. J Cell Sci 2014; 127:3079-93; PMID:24777476; http://dx.doi.org/10.1242/jcs.144816
  • Linger RM, Keating AK, Earp HS, Graham DK. TAM receptor tyrosine kinases: biologic functions, signaling, and potential therapeutic targeting in human cancer. Adv Cancer Res 2008; 100:35-83; PMID:18620092; http://dx.doi.org/10.1016/S0065-230X(08)00002-X
  • Demarchi F, Verardo R, Varnum B, Brancolini C, Schneider C. Gas6 anti-apoptotic signaling requires NF-kappa B activation. J Biol Chem 2001; 276:31738-44; PMID:11425860; http://dx.doi.org/10.1074/jbc.M104457200
  • Stutz A, Golenbock DT, Latz E. Inflammasomes: too big to miss. J Clin Invest 2009; 119:3502-11; PMID:19955661; http://dx.doi.org/10.1172/JCI40599
  • Schroder K, Tschopp J. The inflammasomes. Cell 2010; 140:821-32; PMID:20303873; http://dx.doi.org/10.1016/j.cell.2010.01.040
  • Bensaad K, Cheung EC, Vousden KH. Modulation of intracellular ROS levels by TIGAR controls autophagy. EMBO J 2009; 28:3015-26; PMID:19713938; http://dx.doi.org/10.1038/emboj.2009.242
  • Wree A, Eguchi A, McGeough MD, Pena CA, Johnson CD, Canbay A, Hoffman HM, Feldstein AE. NLRP3 inflammasome activation results in hepatocyte pyroptosis, liver inflammation, and fibrosis in mice. Hepatology 2014; 59:898-910; PMID:23813842; http://dx.doi.org/10.1002/hep.26592
  • Fourcot A, Couchie D, Chobert MN, Zafrani ES, Mavier P, Laperche Y, Brouillet A. Gas6 deficiency prevents liver inflammation, steatohepatitis, and fibrosis in mice. Am J Physiol Gastrointest Liver Physiol 2011; 300:G1043-53; PMID:21350191; http://dx.doi.org/10.1152/ajpgi.00311.2010
  • Bárcena C, Stefanovic M, Tutusaus A, Joannas L, Menéndez A, García-Ruiz C, Sancho-Bru P, Marí M, Caballeria J, Rothlin CV, et al. Gas6/Axl pathway is activated in chronic liver disease and its targeting reduces fibrosis via hepatic stellate cell inactivation. J Hepatol 2015; 63:670-8.
  • Park HJ, Lee SJ, Kim SH, Han J, Bae J, Kim SJ, Park CG, Chun T. IL-10 inhibits the starvation induced autophagy in macrophages via class I phosphatidylinositol 3-kinase (PI3K) pathway. Mol Immunol 2011; 48:720-7; PMID:21095008; http://dx.doi.org/10.1016/j.molimm.2010.10.020
  • Pineda-Torra I, Gage M, de Juan A, Pello OM. Isolation, culture, and polarization of murine bone marrow-derived and peritoneal macrophages. Methods Mol Biol 2015; 1339:101-9; PMID:26445783; http://dx.doi.org/10.1007/978-1-4939-2929-0_6
  • Sander LE, Sackett SD, Dierssen U, Beraza N, Linke RP, Müller M, Blander JM, Tacke F, Trautwein C. Hepatic acute-phase proteins control innate immune responses during infection by promoting myeloid-derived suppressor cell function. J Exp Med 2010; 207:1453-64; PMID:20530204; http://dx.doi.org/10.1084/jem.20091474
  • Lodder J, Denaës T, Chobert MN, Wan J, El-Benna J, Pawlotsky JM, Lotersztajn S, Teixeira-Clerc F. Macrophage autophagy protects against liver fibrosis in mice. Autophagy 2015; 11:1280-92; PMID:26061908; http://dx.doi.org/10.1080/15548627.2015.1058473
  • Lu Y, Leung TM, Ward SC, Nieto N. Partial deletion of argininosuccinate synthase protects from pyrazole plus LPS-induced liver injury by decreasing nitrosative stress. Am J Physiol Gastrointest Liver Physiol 2012; 302:G287-95; PMID:22052013; http://dx.doi.org/10.1152/ajpgi.00375.2011
  • Xu H, Garver H, Fernandes R, Galligan JJ, Fink GD. Altered L-type Ca2+ channel activity contributes to exacerbated hypoperfusion and mortality in smooth muscle cell BK channel-deficient septic mice. Am J Physiol Regul Integr Comp Physiol 2014; 307:R138-48; PMID:24829499; http://dx.doi.org/10.1152/ajpregu.00117.2014
  • Mao K, Chen S, Chen M, Ma Y, Wang Y, Huang B, He Z, Zeng Y, Hu Y, Sun S, et al. Nitric oxide suppresses NLRP3 inflammasome activation and protects against LPS-induced septic shock. Cell Res 2013; 23:201-12; PMID:23318584; http://dx.doi.org/10.1038/cr.2013.6

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