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Research Paper - Basic Science

The autophagy receptor SQSTM1/p62 mediates anti-inflammatory actions of the selective NR3C1/glucocorticoid receptor modulator compound A (CpdA) in macrophages

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Pages 2049-2064 | Received 15 Sep 2017, Accepted 27 Jun 2018, Published online: 14 Sep 2018

References

  • Chatzidionysiou K, Emamikia S, Nam J, et al. Efficacy of glucocorticoids, conventional and targeted synthetic disease-modifying antirheumatic drugs: A systematic literature review informing the 2016 update of the EULAR recommendations for the management of rheumatoid arthritis. Ann Rheum Dis. 2017;76:1102–1107.
  • Fardet L, Petersen I, Nazareth I. Monitoring of patients on long-term glucocorticoid therapy. Medicine (Baltimore). 2015;94:e647.
  • Barnes PJ. Glucocorticosteroids. Handb Exp Pharmacol. 2016;237:93–115.
  • Ratman D, Vanden Berghe W, Dejager L, et al. How glucocorticoid receptors modulate the activity of other transcription factors: A scope beyond tethering. Mol Cell Endocrinol. 2013;380:41–54.
  • Desmet SJ, De Bosscher K. Glucocorticoid receptors: finding the middle ground. J Clin Invest. 2017;127:1136–1145.
  • Meijsing SH. Mechanisms of glucocorticoid-regulated gene transcription. Adv Exp Med Biol. 2015;872:59–81.
  • Hua G, Ganti KP, Chambon P. Glucocorticoid-induced tethered transrepression requires SUMOylation of GR and formation of a SUMO-SMRT/NCoR1-HDAC3 repressing complex. Proc Natl Acad Sci. 2016;113:E635–E643.
  • Sundahl N, Bridelance J, Libert C, et al. Selective glucocorticoid receptor modulation: new directions with non-steroidal scaffolds. Pharmacol Ther. 2015;152:28–41.
  • Gossye V, Elewaut D, Van Beneden K, et al. A plant-derived glucocorticoid receptor modulator attenuates inflammation without provoking ligand-induced resistance. Ann Rheum Dis. 2010;69:291–296.
  • Dewint P, Gossye V, De Bosscher K, et al. A plant-derived ligand favoring monomeric Glucocorticoid receptor conformation with impaired transactivation potential attenuates collagen-induced arthritis. J Immunol. 2008;180:2608–2615.
  • Lesovaya E, Yemelyanov A, Swart AC, et al. Discovery of Compound A - a selective activator of the glucocorticoid receptor with anti-inflammatory and anti-cancer activity. Oncotarget. 2015;6:30730–30744.
  • Saksida T, Vujicic M, Nikolic I, et al. Compound A, a selective glucocorticoid receptor agonist, inhibits immunoinflammatory diabetes, induced by multiple low doses of streptozotocin in mice. Br J Pharmacol. 2014;171:5898–5909.
  • Gavrila A, Chachi L, Tliba O, et al. Effect of the plant derivative Compound A on the production of corticosteroid-resistant chemokines in airway smooth muscle cells. Am J Respir Cell Mol Biol. 2015;53:728–737.
  • De Bosscher K, Vanden Berghe W, Beck IME, et al. A fully dissociated compound of plant origin for inflammatory gene repression. Proc Natl Acad Sci USA. 2005;102:15827–15832.
  • Barcala Tabarrozzi AE, Andreone L, Deckers J, et al. GR-independent down-modulation on GM-CSF bone marrow-derived dendritic cells by the selective glucocorticoid receptor modulator Compound A. Sci Rep. 2016;6:36646.
  • Lu M-C, Ji J-A, Jiang Z-Y, et al. The Keap1-Nrf2-ARE pathway as a potential preventive and therapeutic target: an update. Med Res Rev. 2016;36:924–963.
  • Dodson M, Redmann M, Rajasekaran NS, et al. KEAP1–NRF2 signalling and autophagy in protection against oxidative and reductive proteotoxicity. Biochem J. 2015;469:347–355.
  • Jo C, Gundemir S, Pritchard S, et al. Nrf2 reduces levels of phosphorylated tau protein by inducing autophagy adaptor protein NDP52. Nat Commun. 2014;5:3496.
  • Komatsu M, Kurokawa H, Waguri S, et al. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat Cell Biol. 2010;12:213–223.
  • Jain A, Lamark T, Sjøttem E, et al. 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. 2010;285:22576–22591.
  • Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature. 2011;469:323–335.
  • He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet. 2009;43:67–93.
  • Clark AR, Belvisi MG. Maps and legends: the quest for dissociated ligands of the glucocorticoid receptor. Pharmacol Ther. 2012;134:54–67.
  • Zhong Z, Umemura A, Sanchez-Lopez E, et al. NF-κB restricts inflammasome activation via elimination of damaged mitochondria. Cell. 2016;164:896–910.
  • Lavin Y, Mortha A, Rahman A, et al. Regulation of macrophage development and function in peripheral tissues. Nat Rev Immunol. 2015;15:731–744.
  • Menegon S, Columbano A, Giordano S. The dual roles of NRF2 in cancer. Trends Mol Med. 2016;22:578–593.
  • Sun X, Ou Z, Chen R, et al. Activation of the p62-Keap1-NRF2 pathway protects against ferroptosis in hepatocellular carcinoma cells. Hepatology. 2016;63:173–184.
  • Jubb AW, Young RS, Hume DA, et al. Enhancer turnover is associated with a divergent transcriptional response to glucocorticoid in mouse and human macrophages. J Immunol. 2016;196:813–822.
  • Lazarou M, Sliter DA, Kane LA, et al. The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature. 2015;524:309–314.
  • Frank B, Marcu A, De Oliveira Almeida Petersen AL, et al. Autophagic digestion of Leishmania major by host macrophages is associated with differential expression of BNIP3, CTSE, and the miRNAs miR-101c, miR-129, and miR-210. Parasites and Vectors. 2015;8:404.
  • Jiang H, Cheng D, Liu W, et al. Protein kinase C inhibits autophagy and phosphorylates LC3. Biochem Biophys Res Commun. 2010;395:471–476.
  • Riccardi C. GILZ as a mediator of the anti-inflammatory effects of glucocorticoids. Front Endocrinol (Lausanne). 2015;6:1–6.
  • Smallie T, Ross EA, Ammit AJ, et al. Dual-specificity phosphatase 1 and tristetraprolin cooperate to regulate macrophage responses to lipopolysaccharide. J Immunol. 2015;195:277–288.
  • Lasa M, Abraham SM, Boucheron C, et al. Dexamethasone causes sustained expression of mitogen-activated protein kinase (MAPK) phosphatase 1 and phosphatase-mediated inhibition of MAPK p38. Mol Cell Biol. 2002;22:7802–7811.
  • Van Bogaert T, Vandevyver S, Dejager L, et al. Tumor necrosis factor inhibits glucocorticoid receptor function in mice: a strong signal toward lethal shock. J Biol Chem. 2011;286:26555–26567.
  • Auphan N, DiDonato JA, Rosette C, et al. Immunosuppression by glucocorticoids: inhibition of NF-kappaB activity through induction of IkappaB synthesis. Science. 1995;270:286–290.
  • Reber LL, Daubeuf F, Plantinga M, et al. A dissociated glucocorticoid receptor modulator reduces airway hyperresponsiveness and inflammation in a mouse model of asthma. J Immunol. 2012;188:3478–3487.
  • Beck IM, Drebert ZJ, Hoya-Arias R, et al. Compound A, a selective Glucocorticoid receptor modulator, enhances heat shock protein Hsp70 gene promoter activation. PLoS One. 2013;8:e69115.
  • Ki SH, Cho IJ, Choi DW, et al. Glucocorticoid receptor (GR) -associated SMRT binding to C/EBPβ TAD and Nrf2 Neh4/5 : role of SMRT recruited to GR in GSTA2 gene repression. Mol Cell Biol. 2005;25:4150–4165.
  • Alam MM, Okazaki K, Nguyen LTT, et al. Glucocorticoid receptor signaling represses the antioxidant response by inhibiting histone acetylation mediated by the transcriptional activator NRF2. J Biol Chem. 2017;292:7519–7530.
  • Kim JY, Ozato K. 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. 2009;182:2131–2140.
  • Kobayashi EH, Suzuki T, Funayama R, et al. Nrf2 suppresses macrophage inflammatory response by blocking proinflammatory cytokine transcription. Nat Commun. 2016;7:11624.
  • Sergin I, Bhattacharya S, Emanuel R, et al. Inclusion bodies enriched for p62 and polyubiquitinated proteins in macrophages protect against atherosclerosis. Sci Signal. 2016;9:1–14.
  • Moscat J, Diaz-Meco MT. p62 at the crossroads of autophagy, apoptosis, and cancer. Cell. 2009;137:1001–1004.
  • Zhang X, Jin JY, Wu J, et al. RNA-Seq and ChIP-Seq reveal SQSTM1/p62 as a key mediator of JunB suppression of NF-κB-dependent inflammation. J Invest Dermatol. 2015;135:1016–1024.
  • Fracchiolla D, Sawa-Makarska J, Zens B, et al. Mechanism of cargo-directed Atg8 conjugation during selective autophagy. Elife. 2016;5:e18544.
  • Katsuragi Y, Ichimura Y, Komatsu M. p62/SQSTM1 functions as a signaling hub and an autophagy adaptor. FEBS J. 2015;282:4672–4678.
  • Pankiv S, Lamark T, Bruun JA, et al. Nucleocytoplasmic shuttling of p62/SQSTM1 and its role in recruitment of nuclear polyubiquitinated proteins to promyelocytic leukemia bodies. J Biol Chem. 2010;285:5941–5953.
  • Louw A, Swart P, De KSS, et al. Mechanism for the stabilization in vivo of the aziridine precursor 2-(4-Acetoxyphenyl)-2-chloro-N-methyl-ethylammonium chloride by serum proteins. Biochem Pharmacol. 1997;53:189–197.
  • Ratman D, Mylka V, Bougarne N, et al. Chromatin recruitment of activated AMPK drives fasting response genes co-controlled by GR and PPARα. Nucleic Acids Res. 2016;44:10539–10553.
  • Hellemans J, Vandesompele J. Selection of reliable reference genes for RT-qPCR analysis. Methods Mol Biol. 2014;1160:19–26.
  • Shaid S, Brandts CH, Serve H, et al. Ubiquitination and selective autophagy. Cell Death Differ. 2013;20:21–30.