Chemistry and biology of enzymes in protein glutathionylation

Schieber, 2014, ROS function in redox signaling and oxidative stress, Curr Biol, 24, R453, 10.1016/j.cub.2014.03.034 Garel, 1986, Covalent binding of glutathione to hemoglobin. I. Inhibition of hemoglobin S polymerization, J Biol Chem, 261, 14704, 10.1016/S0021-9258(18)66928-5 Craescu, 1986, Covalent binding of glutathione to hemoglobin. II. Functional consequences and structural changes reflected in NMR spectra, J Biol Chem, 261, 14710, 10.1016/S0021-9258(18)66929-7 Kukulage, 2022, Emerging chemistry and biology in protein glutathionylation, Curr Opin Chem Biol, 71, 102221, 10.1016/j.cbpa.2022.102221 Mailloux, 2020, Protein S-glutathionylation reactions as a global inhibitor of cell metabolism for the desensitization of hydrogen peroxide signals, Redox Biol, 32, 101472, 10.1016/j.redox.2020.101472 Adachi, 2004, S-glutathiolation of Ras mediates redox-sensitive signaling by angiotensin II in vascular smooth muscle cells, J Biol Chem, 279, 29857, 10.1074/jbc.M313320200 Yang, 2020, GSTpi regulates VE-cadherin stabilization through promoting S-glutathionylation of Src, Redox Biol, 30, 101416, 10.1016/j.redox.2019.101416 Abdelsaid, 2012, S-glutathionylation of LMW-PTP regulates VEGF-mediated FAK activation and endothelial cell migration, J Cell Sci, 125, 4751 Sakai, 2012, Reactive oxygen species-induced actin glutathionylation controls actin dynamics in neutrophils, Immunity, 37, 1037, 10.1016/j.immuni.2012.08.017 Reynaert, 2006, Dynamic redox control of NF-kB through glutaredoxin-regulated S-glutathionylation of inhibitory kB kinase beta, Proc Natl Acad Sci USA, 103, 13086, 10.1073/pnas.0603290103 Checconi, 2019, Role of glutathionylation in infection and inflammation, Nutrients, 11, 1952, 10.3390/nu11081952 Velu, 2007, Human p53 is inhibited by glutathionylation of cysteines present in the proximal DNA-binding domain during oxidative stress, Biochemistry, 46, 7765, 10.1021/bi700425y Adachi, 2004, S-glutathiolation by peroxynitrite activates SERCA during arterial relaxation by nitric oxide, Nat Med, 10, 1200, 10.1038/nm1119 Alegre-Cebollada, 2014, S-glutathionylation of cryptic cysteines enhances titin elasticity by blocking protein folding, Cell, 156, 1235, 10.1016/j.cell.2014.01.056 Loescher, 2020, Regulation of titin-based cardiac stiffness by unfolded domain oxidation (UnDOx), Proc Natl Acad Sci USA, 117, 24545, 10.1073/pnas.2004900117 Rashdan, 2020, S-glutathionylation, friend or foe in cardiovascular health and disease, Redox Biol, 37, 101693, 10.1016/j.redox.2020.101693 Chia, 2020, Dysregulation of the glutaredoxin/S-glutathionylation redox axis in lung diseases, Am J Physiol Cell Physiol, 318, C304, 10.1152/ajpcell.00410.2019 Hayes, 2020, Oxidative stress in cancer, Cancer Cell, 38, 167, 10.1016/j.ccell.2020.06.001 Cha, 2017, Protein glutathionylation in the pathogenesis of neurodegenerative diseases, Oxid Med Cell Longev, 2017, 2818565, 10.1155/2017/2818565 Gallogly, 2007, Mechanisms of reversible protein glutathionylation in redox signaling and oxidative stress, Curr Opin Pharmacol, 7, 381, 10.1016/j.coph.2007.06.003 Tew, 2011, The role of glutathione S-transferase P in signaling pathways and S-glutathionylation in cancer, Free Radic Biol Med, 51, 299, 10.1016/j.freeradbiomed.2011.04.013 Shelton, 2005, Glutaredoxin: role in reversible protein S-glutathionylation and regulation of redox signal transduction and protein translocation, Antioxidants Redox Signal, 7, 348, 10.1089/ars.2005.7.348 Menon, 2013, A role for glutathione transferase omega 1 (GSTO1-1) in the glutathionylation cycle, J Biol Chem, 288, 25769, 10.1074/jbc.M113.487785 Board, 2000, Identification, characterization, and crystal structure of the omega class glutathione transferases, J Biol Chem, 275, 24798, 10.1074/jbc.M001706200 Whitbread, 2005, Characterization of the omega class of glutathione transferases, Methods Enzymol, 401, 78, 10.1016/S0076-6879(05)01005-0 Board, 2016, Structure, function and disease relevance of omega-class glutathione transferases, Arch Toxicol, 90, 1049, 10.1007/s00204-016-1691-1 Hughes, 2019, Glutathione transferase omega-1 regulates NLRP3 inflammasome activation through NEK7 deglutathionylation, Cell Rep, 29, 151, 10.1016/j.celrep.2019.08.072 Hughes, 2017, Glutathione and glutathione transferase omega 1 as key posttranslational regulators in macrophages, Microbiol Spectr, 5, 10.1128/microbiolspec.MCHD-0044-2016 Li, 2021, ASC deglutathionylation is a checkpoint for NLRP3 inflammasome activation, J Exp Med, 218, 10.1084/jem.20202637 Menon, 2015, GSTO1-1 modulates metabolism in macrophages activated through the LPS and TLR4 pathway, J Cell Sci, 128, 1982, 10.1242/jcs.167858 Xu, 2020, Deletion of glutathione S-transferase omega 1 activates type I interferon genes and downregulates tissue factor, Cancer Res, 80, 3692, 10.1158/0008-5472.CAN-20-0530 Wang, 2021, Glutathione S-transferase omega 1 promotes the proliferation, migration and invasion, and inhibits the apoptosis of non-small cell lung cancer cells, via the JAK/STAT3 signaling pathway, Mol Med Rep, 23, 71, 10.3892/mmr.2020.11709 Cha, 2022, Therapeutic modulation of GSTO activity rescues FUS-associated neurotoxicity via deglutathionylation in ALS disease models, Dev Cell, 57, 783, 10.1016/j.devcel.2022.02.022 Cha, 2022, Knockdown of glutathione S-transferase leads to mislocalization and accumulation of cabeza, a drosophila homolog of FUS, in the brain, J Neurogenet, 1 Crozat, 1993, Fusion of CHOP to a novel RNA-binding protein in human myxoid liposarcoma, Nature, 363, 640, 10.1038/363640a0 Dormann, 2013, Fused in sarcoma (FUS): an oncogene goes awry in neurodegeneration, Mol Cell Neurosci, 56, 475, 10.1016/j.mcn.2013.03.006 Vance, 2009, Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6, Science, 323, 1208, 10.1126/science.1165942 Sun, 2011, Molecular determinants and genetic modifiers of aggregation and toxicity for the ALS disease protein FUS/TLS, PLoS Biol, 9, 10.1371/journal.pbio.1000614 Sun, 2020, Physiological and pathological roles of mammalian NEK7, Front Physiol, 11, 606996, 10.3389/fphys.2020.606996 He, 2016, NEK7 is an essential mediator of NLRP3 activation downstream of potassium efflux, Nature, 530, 354, 10.1038/nature16959 Swanson, 2019, The NLRP3 inflammasome: molecular activation and regulation to therapeutics, Nat Rev Immunol, 19, 477, 10.1038/s41577-019-0165-0 Parker, 2016, Antitumour actions of interferons: implications for cancer therapy, Nat Rev Cancer, 16, 131, 10.1038/nrc.2016.14 Kasthuri, 2009, Role of tissue factor in cancer, J Clin Oncol, 27, 4834, 10.1200/JCO.2009.22.6324 Lu, 2017, Chemotherapy-induced Ca(2+) release stimulates breast cancer stem cell enrichment, Cell Rep, 18, 1946, 10.1016/j.celrep.2017.02.001 Manupati, 2019, Glutathione S-transferase omega 1 inhibition activates JNK-mediated apoptotic response in breast cancer stem cells, FEBS J, 286, 2167, 10.1111/febs.14813 Xie, 2018, Reviewing hit discovery literature for difficult targets: glutathione transferase omega-1 as an example, J Med Chem, 61, 7448, 10.1021/acs.jmedchem.8b00318 Ramkumar, 2016, Mechanistic evaluation and transcriptional signature of a glutathione S-transferase omega 1 inhibitor, Nat Commun, 7, 13084, 10.1038/ncomms13084 Xie, 2020, Development of benzenesulfonamide derivatives as potent glutathione transferase omega-1 inhibitors, J Med Chem, 63, 2894, 10.1021/acs.jmedchem.9b01391 Dai, 2019, Structure-based design of N-(5-phenylthiazol-2-yl)acrylamides as novel and potent glutathione S-transferase omega 1 inhibitors, J Med Chem, 62, 3068, 10.1021/acs.jmedchem.8b01960 Mortenson, 2018, “Inverse drug discovery” strategy to identify proteins that are targeted by latent electrophiles as exemplified by aryl fluorosulfates, J Am Chem Soc, 140, 200, 10.1021/jacs.7b08366 Wormer, 2019, A cyclopropene electrophile that targets glutathione S-transferase omega-1 in cells, Angew Chem Int Ed Engl, 58, 11918, 10.1002/anie.201907520 Jackson, 2017, Covalent modifiers: a chemical perspective on the reactivity of alpha,beta-unsaturated carbonyls with thiols via hetero-Michael addition reactions, J Med Chem, 60, 839, 10.1021/acs.jmedchem.6b00788 Tsuboi, 2011, Potent and selective inhibitors of glutathione S-transferase omega 1 that impair cancer drug resistance, J Am Chem Soc, 133, 16605, 10.1021/ja2066972 Lillig, 2008, Glutaredoxin systems, Biochim Biophys Acta, 1780, 1304, 10.1016/j.bbagen.2008.06.003 Gallogly, 2009, Mechanistic and kinetic details of catalysis of thiol-disulfide exchange by glutaredoxins and potential mechanisms of regulation, Antioxidants Redox Signal, 11, 1059, 10.1089/ars.2008.2291 Begas, 2017, Glutaredoxin catalysis requires two distinct glutathione interaction sites, Nat Commun, 8, 14835, 10.1038/ncomms14835 Guo, 2021, Oxidative stress-induced FABP5 S-glutathionylation protects against acute lung injury by suppressing inflammation in macrophages, Nat Commun, 12, 7094, 10.1038/s41467-021-27428-9 Luo, 2022, NF-kappaB inactivation attenuates the M1 macrophage polarization in experimental necrotizing enterocolitis by glutaredoxin-1 deficiency, Cell Biol Int, 46, 1886, 10.1002/cbin.11861 Ahn, 2022, Glutaredoxin 1 controls monocyte reprogramming during nutrient stress and protects mice against obesity and atherosclerosis in a sex-specific manner, Nat Commun, 13, 790, 10.1038/s41467-022-28433-2 Manuel, 2021, Dysregulation of pyruvate kinase M2 promotes inflammation in a mouse model of obese allergic asthma, Am J Respir Cell Mol Biol, 64, 709, 10.1165/rcmb.2020-0512OC Anathy, 2018, Reducing protein oxidation reverses lung fibrosis, Nat Med, 24, 1128, 10.1038/s41591-018-0090-y Xi, 2021, The anti-fibrotic drug pirfenidone inhibits liver fibrosis by targeting the small oxidoreductase glutaredoxin-1, Sci Adv, 7, 10.1126/sciadv.abg9241 Tsukahara, 2022, Administration of glutaredoxin-1 attenuates liver fibrosis caused by aging and non-alcoholic steatohepatitis, Antioxidants, 11, 867, 10.3390/antiox11050867 Massague, 2012, TGFbeta signalling in context, Nat Rev Mol Cell Biol, 13, 616, 10.1038/nrm3434 Strasser, 2009, The many roles of FAS receptor signaling in the immune system, Immunity, 30, 180, 10.1016/j.immuni.2009.01.001 Anathy, 2009, Redox amplification of apoptosis by caspase-dependent cleavage of glutaredoxin 1 and S-glutathionylation of Fas, J Cell Biol, 184, 241, 10.1083/jcb.200807019 Sun, 2021, Contribution of glutaredoxin-1 to Fas S-glutathionylation and inflammation in ethanol-induced liver injury, Life Sci, 264, 118678, 10.1016/j.lfs.2020.118678 Gorelenkova Miller, 2017, Novel chloroacetamido compound CWR-J02 is an anti-inflammatory glutaredoxin-1 inhibitor, PLoS One, 12, 10.1371/journal.pone.0187991 Haffo, 2018, Inhibition of the glutaredoxin and thioredoxin systems and ribonucleotide reductase by mutant p53-targeting compound APR-246, Sci Rep, 8, 12671, 10.1038/s41598-018-31048-7 Kekulandara, 2018, Redox-Inactive peptide disrupting Trx1-Ask1 interaction for selective activation of stress signaling, Biochemistry, 57, 772, 10.1021/acs.biochem.7b01083 van der Donk, 2014, Structure and mechanism of lanthipeptide biosynthetic enzymes, Curr Opin Struct Biol, 29, 58, 10.1016/j.sbi.2014.09.006 He, 2017, LanCL proteins are not involved in lanthionine synthesis in mammals, Sci Rep, 7, 40980, 10.1038/srep40980 Chung, 2007, Identification of lanthionine synthase C-like protein-1 as a prominent glutathione binding protein expressed in the mammalian central nervous system, Biochemistry, 46, 3262, 10.1021/bi061888s Siodlak, 2015, alpha,beta-Dehydroamino acids in naturally occurring peptides, Amino Acids, 47, 1, 10.1007/s00726-014-1846-4 Townsend, 2014, A comparison of reversible versus irreversible protein glutathionylation, Adv Cancer Res, 122, 177, 10.1016/B978-0-12-420117-0.00005-0 Zhu, 2007, Structural insights into the enzymatic mechanism of the pathogenic MAPK phosphothreonine lyase, Mol Cell, 28, 899, 10.1016/j.molcel.2007.11.011 Chambers, 2018, Selectivity within a family of bacterial phosphothreonine lyases, Biochemistry, 57, 3790, 10.1021/acs.biochem.8b00534 Lai, 2021, LanCLs add glutathione to dehydroamino acids generated at phosphorylated sites in the proteome, Cell, 184, 2680, 10.1016/j.cell.2021.04.001 Ongpipattanakul, 2023, The mechanism of thia-Michael addition catalyzed by LanC enzymes, Proc Natl Acad Sci USA, 120, 10.1073/pnas.2217523120 Sturla, 2009, LANCL2 is necessary for abscisic acid binding and signaling in human granulocytes and in rat insulinoma cells, J Biol Chem, 284, 28045, 10.1074/jbc.M109.035329 Bassaganya-Riera, 2011, Abscisic acid regulates inflammation via ligand-binding domain-independent activation of peroxisome proliferator-activated receptor gamma, J Biol Chem, 286, 2504, 10.1074/jbc.M110.160077 Zeng, 2014, Lanthionine synthetase C-like protein 2 (LanCL2) is a novel regulator of Akt, Mol Biol Cell, 25, 3954, 10.1091/mbc.e14-01-0004 Wang, 2018, LanCL1 protects prostate cancer cells from oxidative stress via suppression of JNK pathway, Cell Death Dis, 9, 197, 10.1038/s41419-017-0207-0 Lu, 2012, Computational modeling-based discovery of novel classes of anti-inflammatory drugs that target lanthionine synthetase C-like protein 2, PLoS One, 7 Carbo, 2016, N-bis(benzimidazolylpicolinoyl)piperazine (BT-11): a novel lanthionine synthetase C-like 2-based therapeutic for inflammatory bowel disease, J Med Chem, 59, 10113, 10.1021/acs.jmedchem.6b00412 Leber, 2018, Activation of LANCL2 by BT-11 ameliorates IBD by supporting regulatory T cell stability through immunometabolic mechanisms, Inflamm Bowel Dis, 24, 1978, 10.1093/ibd/izy167 Leber, 2019, Nonclinical toxicology and toxicokinetic profile of an oral lanthionine synthetase C-like 2 (LANCL2) agonist, BT-11, Int J Toxicol, 38, 96, 10.1177/1091581819827509 Leber, 2020, The safety, tolerability, and pharmacokinetics profile of BT-11, an oral, gut-restricted lanthionine synthetase C-like 2 agonist investigational new drug for inflammatory bowel disease: a randomized, double-blind, placebo-controlled phase I clinical trial, Inflamm Bowel Dis, 26, 643 VanHecke, 2019, Proteomic identification of protein glutathionylation in cardiomyocytes, J Proteome Res, 18, 1806, 10.1021/acs.jproteome.8b00986 VanHecke, 2020, Isotopically labeled clickable glutathione to quantify protein S-glutathionylation, Chembiochem, 21, 853, 10.1002/cbic.201900528 Kramer, 2018, Fatiguing contractions increase protein S-glutathionylation occupancy in mouse skeletal muscle, Redox Biol, 17, 367, 10.1016/j.redox.2018.05.011 Wang, 2021, iCysMod: an integrative database for protein cysteine modifications in eukaryotes, Briefings Bioinf, 22, bbaa400, 10.1093/bib/bbaa400 Scalcon, 2022, Mitochondrial depletion of glutaredoxin 2 induces metabolic dysfunction-associated fatty liver disease in mice, Redox Biol, 51, 102277, 10.1016/j.redox.2022.102277 Li, 2022, Mitochondrial Glrx2 knockout augments acetaminophen-induced hepatotoxicity in mice, Antioxidants, 11, 1643, 10.3390/antiox11091643 van de Wetering, 2021, Glutathione-S-transferase P promotes glycolysis in asthma in association with oxidation of pyruvate kinase M2, Redox Biol, 47, 102160, 10.1016/j.redox.2021.102160 Jones, 2016, Glutathione S-transferase pi modulates NF-kB activation and pro-inflammatory responses in lung epithelial cells, Redox Biol, 8, 375, 10.1016/j.redox.2016.03.005