Inhibition of thrombospondin-1 reduces glutathione activity and worsens acute liver injury during acetaminophen hepatotoxicity in mice

Toxicology and Applied Pharmacology - Tập 409 - Trang 115323 - 2020
Gabriel Frampton1,2, Priyanka Reddy1, Brandi Jefferson1, Malaika Ali1, Durreshahwar Khan1, Matthew McMillin1,2
1Central Texas Veterans Health Care System, Austin, TX, United States of America
2The University of Texas at Austin Dell Medical School, Department of Internal Medicine, Austin, TX, United States of America

Tài liệu tham khảo

Abdollah, 1997, TbetaRI phosphorylation of Smad2 on Ser465 and Ser467 is required for Smad2-Smad4 complex formation and signaling, J. Biol. Chem., 272, 27678, 10.1074/jbc.272.44.27678 Akino, 2018, Activation of Nrf2 might reduce oxidative stress in human granulosa cells, Mol. Cell. Endocrinol., 470, 96, 10.1016/j.mce.2017.10.002 Bachhawat, 2018, The glutathione cycle: glutathione metabolism beyond the gamma-glutamyl cycle, IUBMB Life, 70, 585, 10.1002/iub.1756 Baenziger, 1972, Isolation and properties of a thrombin-sensitive protein of human platelets, J. Biol. Chem., 247, 2723, 10.1016/S0021-9258(19)45271-X Bernal, 2015, Acute liver failure: a curable disease by 2024?, J. Hepatol., 62, S112, 10.1016/j.jhep.2014.12.016 Bird, 2018, TGFbeta inhibition restores a regenerative response in acute liver injury by suppressing paracrine senescence, Sci. Transl. Med., 10, 10.1126/scitranslmed.aan1230 Chen, 2000, The cell biology of thrombospondin-1, Matrix Biol., 19, 597, 10.1016/S0945-053X(00)00107-4 Chen, 2016, Thrombospondin-1 might be a therapeutic target to suppress RB cells by regulating the DNA double-strand breaks repair, Oncotarget, 7, 6105, 10.18632/oncotarget.6835 Crawford, 1998, Thrombospondin-1 is a major activator of TGF-beta1 in vivo, Cell., 93, 1159, 10.1016/S0092-8674(00)81460-9 Cunha, 2016, Thrombospondin 1 protects pancreatic beta-cells from lipotoxicity via the PERK-NRF2 pathway, Cell Death Differ., 23, 1995, 10.1038/cdd.2016.89 Daubon, 2019, Deciphering the complex role of thrombospondin-1 in glioblastoma development, Nat. Commun., 10, 1146, 10.1038/s41467-019-08480-y DeMorrow, 2008, The endocannabinoid anandamide inhibits cholangiocarcinoma growth via activation of the noncanonical Wnt signaling pathway, Am. J. Physiol. Gastrointest. Liver Physiol., 295, G1150, 10.1152/ajpgi.90455.2008 Ebisawa, 2001, Smurf1 interacts with transforming growth factor-beta type I receptor through Smad7 and induces receptor degradation, J. Biol. Chem., 276, 12477, 10.1074/jbc.C100008200 El-Youssef, 1999, Increased expression of transforming growth factor-beta1 and thrombospondin-1 in congenital hepatic fibrosis: possible role of the hepatic stellate cell, J. Pediatr. Gastroenterol. Nutr., 28, 386, 10.1097/00005176-199904000-00008 Fan, 2018, Isoorientin ameliorates APAP-induced hepatotoxicity via activation Nrf2 antioxidative pathway: the involvement of AMPK/Akt/GSK3beta, Front. Pharmacol., 9, 1334, 10.3389/fphar.2018.01334 Frampton, 2012, Interleukin-6-driven progranulin expression increases cholangiocarcinoma growth by an Akt-dependent mechanism, Gut., 61, 268, 10.1136/gutjnl-2011-300643 Grant, 2018, Direct comparison of the thioacetamide and azoxymethane models of type a hepatic encephalopathy in mice, Gene Expr., 18, 171, 10.3727/105221618X15287315176503 Jefferson, 2020, Thrombospondin-1 exacerbates acute liver failure and hepatic encephalopathy pathology in mice by activating transforming growth factor beta1, Am. J. Pathol., 190, 347, 10.1016/j.ajpath.2019.10.003 Jin, 2019, Quercetin attenuates toosendanin-induced hepatotoxicity through inducing the Nrf2/GCL/GSH antioxidant signaling pathway, Acta Pharmacol. Sin., 40, 75, 10.1038/s41401-018-0024-8 Kavsak, 2000, Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation, Mol. Cell, 6, 1365, 10.1016/S1097-2765(00)00134-9 Khalil, 1999, TGF-beta: from latent to active, Microbes Infect., 1, 1255, 10.1016/S1286-4579(99)00259-2 Kim, 2017, Disturbed flow promotes arterial stiffening through thrombospondin-1, Circulation, 136, 1217, 10.1161/CIRCULATIONAHA.116.026361 Kumar, 2017, TGF-beta activation by bone marrow-derived thrombospondin-1 causes Schistosoma- and hypoxia-induced pulmonary hypertension, Nat. Commun., 8, 15494, 10.1038/ncomms15494 Kuo, 2008, Gamma-H2AX - a novel biomarker for DNA double-strand breaks, In Vivo, 22, 305 Liu, 2016, Smad2 and Smad3 have differential sensitivity in relaying TGFbeta signaling and inversely regulate early lineage specification, Sci. Rep., 6, 21602, 10.1038/srep21602 Livak, 2001, Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method, Methods., 25, 402, 10.1006/meth.2001.1262 Lopez-Dee, 2011, Thrombospondin-1: multiple paths to inflammation, Mediat. Inflamm., 2011, 296069, 10.1155/2011/296069 Lv, 2019, Corilagin alleviates acetaminophen-induced hepatotoxicity via enhancing the AMPK/GSK3beta-Nrf2 signaling pathway, Cell Commun. Signal., 17, 2, 10.1186/s12964-018-0314-2 Matkowskyj, 1999, Azoxymethane-induced fulminant hepatic failure in C57BL/6J mice: characterization of a new animal model, Am. J. Phys., 277, G455 McMillin, 2019, The TGFbeta1 receptor antagonist GW788388 reduces JNK activation and protects against acetaminophen hepatotoxicity in mice, Toxicol. Sci., 170, 549, 10.1093/toxsci/kfz122 Mirochnik, 2008, Thrombospondin and apoptosis: molecular mechanisms and use for design of complementation treatments, Curr. Drug Targets, 9, 851, 10.2174/138945008785909347 Mosher, 1982, Synthesis and secretion of thrombospondin by cultured human endothelial cells, J. Cell Biol., 93, 343, 10.1083/jcb.93.2.343 Munger, 1997, Latent transforming growth factor-beta: structural features and mechanisms of activation, Kidney Int., 51, 1376, 10.1038/ki.1997.188 Munger, 1999, The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis, Cell., 96, 319, 10.1016/S0092-8674(00)80545-0 Neuschwander-Tetri, 2006, Induced thrombospondin expression in the mouse pancreas during pancreatic injury, Int. J. Biochem. Cell Biol., 38, 102, 10.1016/j.biocel.2005.08.008 Qu, 2018, Thrombospondin-1 protects against pathogen-induced lung injury by limiting extracellular matrix proteolysis, JCI Insight, 3, 10.1172/jci.insight.96914 Raucy, 1989, Acetaminophen activation by human liver cytochromes P450IIE1 and P450IA2, Arch. Biochem. Biophys., 271, 270, 10.1016/0003-9861(89)90278-6 Resovi, 2014, Current understanding of the thrombospondin-1 interactome, Matrix Biol., 37, 83, 10.1016/j.matbio.2014.01.012 Ribeiro, 1999, The activation sequence of thrombospondin-1 interacts with the latency-associated peptide to regulate activation of latent transforming growth factor-beta, J. Biol. Chem., 274, 13586, 10.1074/jbc.274.19.13586 Schultz-Cherry, 1993, Thrombospondin causes activation of latent transforming growth factor-beta secreted by endothelial cells by a novel mechanism, J. Cell Biol., 122, 923, 10.1083/jcb.122.4.923 Seif, 2018, Neutrophil-Mediated Proteolysis of thrombospondin-1 promotes platelet adhesion and string formation, Thromb. Haemost., 118, 2074, 10.1055/s-0038-1675229 Shi, 2004, GADD34-PP1c recruited by Smad7 dephosphorylates TGFbeta type I receptor, J. Cell Biol., 164, 291, 10.1083/jcb.200307151 Starlinger, 2011, Platelet-stored angiogenesis factors: clinical monitoring is prone to artifacts, Dis. Markers, 31, 55, 10.1155/2011/535109 Suzuki, 2015, Upregulation of thrombospondin 1 expression in synovial tissues and plasma of rheumatoid arthritis: role of transforming growth factor-beta1 toward fibroblast-like synovial cells, J. Rheumatol., 42, 943, 10.3899/jrheum.141292 Wang, 2018, Fucoidan alleviates acetaminophen-induced hepatotoxicity via oxidative stress inhibition and Nrf2 translocation, Int. J. Mol. Sci., 19, 10.3390/ijms19124050 Warren, 2018, Activation of latent transforming growth factor-beta1, a conserved function for pregnancy-specific beta 1-glycoproteins, Mol. Hum. Reprod., 24, 602, 10.1093/molehr/gay044 Yu, 2000, Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis, Genes Dev., 14, 163, 10.1101/gad.14.2.163 Zhang, 1996, Receptor-associated mad homologues synergize as effectors of the TGF-beta response, Nature., 383, 168, 10.1038/383168a0