TRIM21 Ubiquitylates SQSTM1/p62 and Suppresses Protein Sequestration to Regulate Redox Homeostasis

Molecular Cell - Tập 61 - Trang 720-733 - 2016
Ji-An Pan1,2,3, Yu Sun1,2,3, Ya-Ping Jiang4, Alex J. Bott1,2,3, Nadia Jaber3, Zhixun Dou3, Bin Yang5, Juei-Suei Chen3, Joseph M. Catanzaro3, Chunying Du6, Wen-Xing Ding7, Maria T. Diaz-Meco8, Jorge Moscat8, Keiko Ozato9, Richard Z. Lin4,10, Wei-Xing Zong1,2,3
1Department of Chemical Biology, Ernest Mario School of Pharmacy, Rutgers University, 164 Frelinghuysen Road, Piscataway, NJ 08854, USA
2Rutgers Cancer Institute of New Jersey, 195 Little Albany Street, New Brunswick, NJ 08903, USA
3Department of Molecular Genetics & Microbiology, Stony Brook University, Stony Brook, NY 11794, USA
4Department of Physiology and Biophysics, Stony Brook University, Stony Brook, NY 11794, USA
5Key Laboratory of Artificial Cells, Tianjin Third Central Hospital, Tianjin 300170, China
6Department of Cancer Biology, University of Cincinnati, Cincinnati, OH 45267, USA
7Department of Pharmacology, Toxicology and Therapeutics, University of Kansas Medical Center, Kansas City, KS 66160, USA
8Cancer Metabolism and Signaling Networks Program, Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA 92037, USA
9Division of Developmental Biology, NICHD, National Institutes of Health, Bethesda, MD 20892, USA
10Department of Veterans Affairs Medical Center, Northport, NY 11768, USA

Tài liệu tham khảo

Barchowsky, 1996, Arsenic induces oxidant stress and NF-kappa B activation in cultured aortic endothelial cells, Free Radic. Biol. Med., 21, 783, 10.1016/0891-5849(96)00174-8 Belch, 1991, Oxygen free radicals and congestive heart failure, Br. Heart J., 65, 245, 10.1136/hrt.65.5.245 Ben-Chetrit, 1988, A 52-kD protein is a novel component of the SS-A/Ro antigenic particle, J. Exp. Med., 167, 1560, 10.1084/jem.167.5.1560 Ben-Chetrit, 1990, Dissociation of immune responses to the SS-A (Ro) 52-kd and 60-kd polypeptides in systemic lupus erythematosus and Sjögren’s syndrome, Arthritis Rheum., 33, 349, 10.1002/art.1780330307 Bernstam, 2000, Molecular aspects of arsenic stress, J. Toxicol. Environ. Health B Crit. Rev., 3, 293, 10.1080/109374000436355 Bjørkøy, 2005, p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death, J. Cell Biol., 171, 603, 10.1083/jcb.200507002 Brauner, 2015, Reduced expression of TRIM21/Ro52 predicts poor prognosis in diffuse large B-cell lymphoma patients with and without rheumatic disease, J. Intern. Med., 278, 323, 10.1111/joim.12375 Chou, 2004, Role of NADPH oxidase in arsenic-induced reactive oxygen species formation and cytotoxicity in myeloid leukemia cells, Proc. Natl. Acad. Sci. USA, 101, 4578, 10.1073/pnas.0306687101 Date, 2002, The antioxidant N-2-mercaptopropionyl glycine attenuates left ventricular hypertrophy in in vivo murine pressure-overload model, J. Am. Coll. Cardiol., 39, 907, 10.1016/S0735-1097(01)01826-5 DeNicola, 2011, Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis, Nature, 475, 106, 10.1038/nature10189 Ding, 2015, Downregulation of TRIM21 contributes to hepatocellular carcinoma carcinogenesis and indicates poor prognosis of cancers, Tumour Biol., 36, 8761, 10.1007/s13277-015-3572-2 Duran, 2008, The signaling adaptor p62 is an important NF-kappaB mediator in tumorigenesis, Cancer Cell, 13, 343, 10.1016/j.ccr.2008.02.001 Espinosa, 2009, Loss of the lupus autoantigen Ro52/Trim21 induces tissue inflammation and systemic autoimmunity by disregulating the IL-23-Th17 pathway, J. Exp. Med., 206, 1661, 10.1084/jem.20090585 Harder, 2015, Molecular mechanisms of Nrf2 regulation and how these influence chemical modulation for disease intervention, Biochem. Soc. Trans., 43, 680, 10.1042/BST20150020 Huang, 2010, A quantitative assay for mitochondrial fusion using Renilla luciferase complementation, Mitochondrion, 10, 559, 10.1016/j.mito.2010.05.003 Ichimura, 2013, Phosphorylation of p62 activates the Keap1-Nrf2 pathway during selective autophagy, Mol. Cell, 51, 618, 10.1016/j.molcel.2013.08.003 Ishii, 1996, Murine peritoneal macrophages induce a novel 60-kDa protein with structural similarity to a tyrosine kinase p56lck-associated protein in response to oxidative stress, Biochem. Biophys. Res. Commun., 226, 456, 10.1006/bbrc.1996.1377 Itakura, 2011, p62 Targeting to the autophagosome formation site requires self-oligomerization but not LC3 binding, J. Cell Biol., 192, 17, 10.1083/jcb.201009067 Jaber, 2012, Class III PI3K Vps34 plays an essential role in autophagy and in heart and liver function, Proc. Natl. Acad. Sci. USA, 109, 2003, 10.1073/pnas.1112848109 Jain, 2010, p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription, J. Biol. Chem., 285, 22576, 10.1074/jbc.M110.118976 James, 2007, Structural basis for PRYSPRY-mediated tripartite motif (TRIM) protein function, Proc. Natl. Acad. Sci. USA, 104, 6200, 10.1073/pnas.0609174104 Kang, 2004, Caspase-independent cell death by arsenic trioxide in human cervical cancer cells: reactive oxygen species-mediated poly(ADP-ribose) polymerase-1 activation signals apoptosis-inducing factor release from mitochondria, Cancer Res., 64, 8960, 10.1158/0008-5472.CAN-04-1830 Katsuragi, 2015, p62/SQSTM1 functions as a signaling hub and an autophagy adaptor, FEBS J., 282, 4672, 10.1111/febs.13540 Kim, 2009, The sequestosome 1/p62 attenuates cytokine gene expression in activated macrophages by inhibiting IFN regulatory factor 8 and TNF receptor-associated factor 6/NF-kappaB activity, J. Immunol., 182, 2131, 10.4049/jimmunol.0802755 Kobayashi, 2004, Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2, Mol. Cell. Biol., 24, 7130, 10.1128/MCB.24.16.7130-7139.2004 Komatsu, 2005, Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice, J. Cell Biol., 169, 425, 10.1083/jcb.200412022 Komatsu, 2010, The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1, Nat. Cell Biol., 12, 213, 10.1038/ncb2021 Lau, 2010, A noncanonical mechanism of Nrf2 activation by autophagy deficiency: direct interaction between Keap1 and p62, Mol. Cell. Biol., 30, 3275, 10.1128/MCB.00248-10 Lim, 2015, Proteotoxic stress induces phosphorylation of p62/SQSTM1 by ULK1 to regulate selective autophagic clearance of protein aggregates, PLoS Genet., 11, e1004987, 10.1371/journal.pgen.1004987 Linares, 2011, Phosphorylation of p62 by cdk1 controls the timely transit of cells through mitosis and tumor cell proliferation, Mol. Cell. Biol., 31, 105, 10.1128/MCB.00620-10 Lynn, 1998, Arsenite stimulates poly(ADP-ribosylation) by generation of nitric oxide, Free Radic. Biol. Med., 24, 442, 10.1016/S0891-5849(97)00279-7 Mallery, 2010, Antibodies mediate intracellular immunity through tripartite motif-containing 21 (TRIM21), Proc. Natl. Acad. Sci. USA, 107, 19985, 10.1073/pnas.1014074107 Mathew, 2009, Autophagy suppresses tumorigenesis through elimination of p62, Cell, 137, 1062, 10.1016/j.cell.2009.03.048 Matsumoto, 2011, Serine 403 phosphorylation of p62/SQSTM1 regulates selective autophagic clearance of ubiquitinated proteins, Mol. Cell, 44, 279, 10.1016/j.molcel.2011.07.039 McEwan, 2013, Intracellular antibody-bound pathogens stimulate immune signaling via the Fc receptor TRIM21, Nat. Immunol., 14, 327, 10.1038/ni.2548 Moscat, 2009, p62 at the crossroads of autophagy, apoptosis, and cancer, Cell, 137, 1001, 10.1016/j.cell.2009.05.023 Nisole, 2005, TRIM family proteins: retroviral restriction and antiviral defence, Nat. Rev. Microbiol., 3, 799, 10.1038/nrmicro1248 Pan, 2011, Inhibition of protein degradation induces apoptosis through a microtubule-associated protein 1 light chain 3-mediated activation of caspase-8 at intracellular membranes, Mol. Cell. Biol., 31, 3158, 10.1128/MCB.05460-11 Pankiv, 2007, p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy, J. Biol. Chem., 282, 24131, 10.1074/jbc.M702824200 Puissant, 2010, Resveratrol promotes autophagic cell death in chronic myelogenous leukemia cells via JNK-mediated p62/SQSTM1 expression and AMPK activation, Cancer Res., 70, 1042, 10.1158/0008-5472.CAN-09-3537 Sayin, 2014, Antioxidants accelerate lung cancer progression in mice, Sci. Transl. Med., 6, 221ra15, 10.1126/scitranslmed.3007653 Schafer, 2009, Antioxidant and oncogene rescue of metabolic defects caused by loss of matrix attachment, Nature, 461, 109, 10.1038/nature08268 Seibenhener, 2004, Sequestosome 1/p62 is a polyubiquitin chain binding protein involved in ubiquitin proteasome degradation, Mol. Cell. Biol., 24, 8055, 10.1128/MCB.24.18.8055-8068.2004 Shin, 1998, P62 and the sequestosome, a novel mechanism for protein metabolism, Arch. Pharm. Res., 21, 629, 10.1007/BF02976748 Song, 2005, The B30.2(SPRY) domain of the retroviral restriction factor TRIM5alpha exhibits lineage-specific length and sequence variation in primates, J. Virol., 79, 6111, 10.1128/JVI.79.10.6111-6121.2005 Tanji, 2014, Phosphorylation of serine 349 of p62 in Alzheimer’s disease brain, Acta Neuropathol. Commun., 2, 50, 10.1186/2051-5960-2-50 Vadlamudi, 1998, Genomic structure and promoter analysis of the p62 gene encoding a non-proteasomal multiubiquitin chain binding protein, FEBS Lett., 435, 138, 10.1016/S0014-5793(98)01021-7 von Harsdorf, 1999, Signaling pathways in reactive oxygen species-induced cardiomyocyte apoptosis, Circulation, 99, 2934, 10.1161/01.CIR.99.22.2934 Wada, 2006, Autoantigen Ro52 is an E3 ubiquitin ligase, Biochem. Biophys. Res. Commun., 339, 415, 10.1016/j.bbrc.2005.11.029 Wilson, 2003, PB1 domain-mediated heterodimerization in NADPH oxidase and signaling complexes of atypical protein kinase C with Par6 and p62, Mol. Cell, 12, 39, 10.1016/S1097-2765(03)00246-6 Yoshimi, 2009, Gene disruption study reveals a nonredundant role for TRIM21/Ro52 in NF-kappaB-dependent cytokine expression in fibroblasts, J. Immunol., 182, 7527, 10.4049/jimmunol.0804121 Zhang, 2004, Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex, Mol. Cell. Biol., 24, 10941, 10.1128/MCB.24.24.10941-10953.2004 Zhao, 2001, Transcript map and complete genomic sequence for the 310 kb region of minimal allele loss on chromosome segment 11p15.5 in non-small-cell lung cancer, Oncogene, 20, 8154, 10.1038/sj.onc.1205027