Sirtuins and Sepsis: Cross Talk between Redox and Epigenetic Pathways
Abstract
:1. Introduction
2. Sirtuins and Redox Regulation of Sepsis
2.1. Mitochondrial Redox and Sepsis
Sirtuins and Mitochondrial Redox
2.2. Redox Signaling in Sepsis
2.2.1. Redox Signaling Pathways in Sepsis
2.2.2. Sirtuins and Redox Signaling
3. Sirtuins and Epigenetic Regulation of Sepsis
3.1. Epigenetic Regulation
3.2. Epigenetics Regulation of Sepsis
4. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Torio, C.M.; Andrews, R.M. National inpatient hospital costs: The most expensive conditions by payer, 2011: Sta-tistical brief #160. In Healthcare Cost and Utilization Project (Hcup) Statistical Briefs; Agency for Healthcare Research and Quality: Rockville, MD, USA, 2006. [Google Scholar]
- Reinhart, K.; Daniels, R.; Machado, F.R. O ônus da sepse: Uma chamada em apoio ao Dia Mundial da Sepse 2013. Rev. Bras. Ter. Intensiv. 2013, 25, 3–5. [Google Scholar] [CrossRef] [PubMed]
- Vachharajani, V.T.; Liu, T.; Brown, C.M.; Wang, X.; Buechler, N.L.; Wells, J.D.; Yoza, B.K.; McCall, C.E. SIRT1 inhibition during the hypoinflammatory phenotype of sepsis enhances immunity and improves outcome. J. Leukoc. Biol. 2014, 96, 785–796. [Google Scholar] [CrossRef]
- Boomer, J.S.; To, K.; Chang, K.C.; Takasu, O.; Osborne, D.F.; Walton, A.H.; Bricker, T.L.; Jarman, S.D.; Kreisel, D., 2nd; Krupnick, A.S.; et al. Immunosuppression in Patients Who Die of Sepsis and Multiple Organ Failure. JAMA 2011, 306, 2594–2605. [Google Scholar] [CrossRef] [PubMed]
- Otto, G.P.; Sossdorf, M.; Claus, R.A.; Rödel, J.; Menge, K.; Reinhart, K.; Bauer, M.; Riedemann, N.C. The late phase of sepsis is characterized by an increased microbiological burden and death rate. Crit. Care 2011, 15, R183. [Google Scholar] [CrossRef] [Green Version]
- Marshall, J.C.; Cook, D.J.; Christou, N.V.; Bernard, G.R.; Sprung, C.L.; Sibbald, W.J. Multiple Organ Dysfunction Score. Crit. Care Med. 1995, 23, 1638–1652. [Google Scholar] [CrossRef] [PubMed]
- Tsirigotis, P.; Chondropoulos, S.; Gkirkas, K.; Meletiadis, J.; Dimopoulou, I. Balanced control of both hyper and hypo-inflammatory phases as a new treatment paradigm in sepsis. J. Thorac. Dis. 2016, 8, E312–E316. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Halliwell, B.; Gutteridge, J.M.C. Free Radicals in Biology and Medicine, 4th ed.; Oxford University Press: Oxford, UK, 2007. [Google Scholar]
- Hotchkiss, R.S.; Tinsley, K.W.; Karl, I.E. Role of apoptotic cell death in sepsis. Scand. J. Infect. Dis. 2003, 35, 585–592. [Google Scholar] [CrossRef]
- Vachharajani, V.; McCall, C.E. Epigenetic and metabolic programming of innate immunity in sepsis. Innate Immun. 2019, 25, 267–279. [Google Scholar] [CrossRef]
- Singer, M. The role of mitochondrial dysfunction in sepsis-induced multi-organ failure. Virulence 2013, 5, 66–72. [Google Scholar] [CrossRef] [PubMed]
- Exline, M.C.; Crouser, E.D. Mitochondrial mechanisms of sepsis-induced organ failure. Front. Biosci. 2008, 13, 5030–5041. [Google Scholar] [PubMed]
- Paiva, C.N.; Bozza, M.T. Are Reactive Oxygen Species Always Detrimental to Pathogens? Antioxid. Redox Signal. 2014, 20, 1000–1037. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Murphy, M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417, 1–13. [Google Scholar] [CrossRef] [Green Version]
- He, L.; He, T.; Farrar, S.; Ji, L.; Liu, T.; Ma, X. Antioxidants Maintain Cellular Redox Homeostasis by Elimination of Reactive Oxygen Species. Cell. Physiol. Biochem. 2017, 44, 532–553. [Google Scholar] [CrossRef] [PubMed]
- Asci, A.; Surmeli-Onay, O.; Erkekoglu, P.; Yigit, S.; Yurdakok, M.; Kocer-Gumusel, B. Oxidant and antioxidant status in neonatal proven and clinical sepsis according to selenium status. Pediatr. Int. 2015, 57, 1131–1137. [Google Scholar] [CrossRef] [PubMed]
- Andrades, M.; Morina, A.; Spasić, S.; Spasojević, I. Bench-to-bedside review: Sepsis—From the redox point of view. Crit. Care 2011, 15, 230. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Macdonald, J.; Galley, H.; Webster, N. Oxidative stress and gene expression in sepsis. Br. J. Anaesth. 2003, 90, 221–232. [Google Scholar] [CrossRef] [Green Version]
- Cross, C.E.; Halliwell, B.; Borish, E.T.; Pryor, W.A.; Ames, B.N.; Saul, R.L.; Mccord, J.M.; Harman, D. Oxygen Radicals and Human Disease. Ann. Intern. Med. 1987, 107, 526–545. [Google Scholar] [CrossRef]
- Mantzarlis, K.; Tsolaki, V.; Zakynthinos, E. Role of Oxidative Stress and Mitochondrial Dysfunction in Sepsis and Potential Therapies. Oxidative Med. Cell. Longev. 2017, 2017, 5985209. [Google Scholar] [CrossRef] [PubMed]
- Li, S.; Hu, Q.; Huang, J.; Wu, X.; Ren, J. Mitochondria-Derived Damage-Associated Molecular Patterns in Sepsis: From Bench to Bedside. Oxidative Med. Cell. Longev. 2019, 2019, 6914849. [Google Scholar] [CrossRef]
- Delcuve, G.P.; Rastegar, M.; Davie, J.R. Epigenetic control. J. Cell. Physiol. 2009, 219, 243–250. [Google Scholar] [CrossRef] [PubMed]
- Handy, D.E.; Castro, R.; Loscalzo, J. Epigenetic modifications: Basic mechanisms and role in cardiovascular disease. Circulation 2011, 123, 2145–2156. [Google Scholar] [CrossRef] [Green Version]
- Gibney, E.R.; Nolan, C.M. Epigenetics and gene expression. Heredity 2010, 105, 4–13. [Google Scholar] [CrossRef] [Green Version]
- Binnie, A.; Tsang, J.L.Y.; Hu, P.; Carrasqueiro, G.; Castelo-Branco, P.; Dos Santos, C.C. Epigenetics of Sepsis. Crit. Care Med. 2020, 48, 745–756. [Google Scholar] [CrossRef] [PubMed]
- Castelo-Branco, P.; Choufani, S.; Mack, S.C.; Gallagher, D.; Zhang, C.; Lipman, T.; Zhukova, N.; Walker, E.J.; Martin, D.; Merino, D.; et al. Methylation of the TERT promoter and risk stratification of childhood brain tumours: An integrative genomic and molecular study. Lancet Oncol. 2013, 14, 534–542. [Google Scholar] [CrossRef]
- Leenen, F.A.D.; Muller, C.P.; Turner, J.D. DNA methylation: Conducting the orchestra from exposure to phenotype? Clin. Epigenet. 2016, 8, 92. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Thangavel, J.; Samanta, S.; Rajasingh, S.; Barani, B.; Xuan, Y.-T.; Dawn, B.; Rajasingh, J. Epigenetic modifiers reduce inflammation and modulate macrophage phenotype during endotoxemia-induced acute lung injury. J. Cell Sci. 2015, 128, 3094–3105. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shih, C.-C.; Liao, M.-H.; Hsiao, T.-S.; Hii, H.-P.; Shen, C.-H.; Chen, S.-J.; Ka, S.-M.; Chang, Y.-L.; Wu, C.-C. Procainamide Inhibits DNA Methylation and Alleviates Multiple Organ Dysfunction in Rats with Endotoxic Shock. PLoS ONE 2016, 11, e0163690. [Google Scholar] [CrossRef] [PubMed]
- Yoza, B.K.; McCall, C.E. Facultative heterochromatin formation at the IL-1 beta promoter in LPS tolerance and sepsis. Cytokine 2011, 53, 145–152. [Google Scholar] [CrossRef] [Green Version]
- Wei, Z.; Batagov, A.O.; Schinelli, S.; Wang, J.; Wang, Y.; EL Fatimy, R.; Rabinovsky, R.; Balaj, L.; Chen, C.C.; Hochberg, F.; et al. Coding and noncoding landscape of extracellular RNA released by human glioma stem cells. Nat. Commun. 2017, 8, 1145. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carson, W.F.; Cavassani, K.A.; Dou, Y.; Kunkel, S.L. Epigenetic regulation of immune cell functions during post-septic immunosuppression. Epigenetics 2011, 6, 273–283. [Google Scholar] [CrossRef] [PubMed]
- Li, L.; Chen, Z.; Fu, W.; Cai, S.; Zeng, Z. Emerging Evidence concerning the Role of Sirtuins in Sepsis. Crit. Care Res. Pract. 2018, 2018, 5489571. [Google Scholar] [CrossRef]
- Haigis, M.C.; Sinclair, D.A. Mammalian Sirtuins: Biological Insights and Disease Relevance. Annu. Rev. Pathol. Mech. Dis. 2010, 5, 253–295. [Google Scholar] [CrossRef] [Green Version]
- Singh, C.K.; Chhabra, G.; Ndiaye, M.A.; Garcia-Peterson, L.M.; Mack, N.J.; Ahmad, N. The Role of Sirtuins in Antioxidant and Redox Signaling. Antioxid. Redox Signal. 2018, 28, 643–661. [Google Scholar] [CrossRef]
- Vachharajani, V.; Liu, T.; Wang, X.; Hoth, J.J.; Yoza, B.K.; McCall, C.E. Sirtuins Link Inflammation and Metabolism. J. Immunol. Res. 2016, 2016, 8167273. [Google Scholar] [CrossRef] [Green Version]
- Jing, H.; Lin, H. Sirtuins in Epigenetic Regulation. Chem. Rev. 2015, 115, 2350–2375. [Google Scholar] [CrossRef] [Green Version]
- Li, T.; Garcia-Gomez, A.; Morante-Palacios, O.; Ciudad, L.; Özkaramehmet, S.; Van Dijck, E.; Rodriguez-Ubreva, J.; Vaquero, A.; Ballestar, E. SIRT1/2 orchestrate acquisition of DNA methylation and loss of histone H3 activating marks to prevent premature activation of inflammatory genes in macrophages. Nucleic Acids Res. 2019, 48, 665–681. [Google Scholar] [CrossRef]
- Hotchkiss, R.R.; Moldawer, L.L.L.; Opal, S.M.; Reinhart, K.; Turnbull, I.I.; Vincent, J.-L. Sepsis and septic shock. Nat. Rev. Dis. Prim. 2016, 2, 16045. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dare, A.J.; Phillips, A.R.; Hickey, A.J.; Mittal, A.; Loveday, B.; Thompson, N.; Windsor, J.A. A systematic review of experimental treatments for mitochondrial dysfunction in sepsis and multiple organ dysfunction syndrome. Free Radic. Biol. Med. 2009, 47, 1517–1525. [Google Scholar] [CrossRef]
- Hayes, M.A.; Timmins, A.C.; Yau, E.H.S.; Palazzo, M.; Watson, D.; Hinds, C.J. Oxygen transport patterns in patients with sepsis syndrome or septic shock. Crit. Care Med. 1997, 25, 926–936. [Google Scholar] [CrossRef]
- Fink, M.P. Cytopathic Hypoxia. Crit. Care Clin. 2001, 17, 219–237. [Google Scholar] [CrossRef]
- Galley, H.F. Oxidative stress and mitochondrial dysfunction in sepsis. Br. J. Anaesth. 2011, 107, 57–64. [Google Scholar] [CrossRef] [Green Version]
- Marshall, J.C.; Vincent, J.-L.; Guyatt, G.; Angus, D.C.; Abraham, E.; Bernard, G.; Bombardier, C.; Calandra, T.; Jørgensen, H.S.; Sylvester, R.; et al. Outcome measures for clinical research in sepsis: A report of the 2nd Cambridge Colloquium of the International Sepsis Forum. Crit. Care Med. 2005, 33, 1708–1716. [Google Scholar] [CrossRef] [PubMed]
- Lange, M.; Connelly, R.; Traber, D.L.; Hamahata, A.; Nakano, Y.; Esechie, A.; Jonkam, C.; Von Borzyskowski, S.; Traber, L.D.; Schmalstieg, F.C.; et al. Time course of nitric oxide synthases, nitrosative stress, and poly(ADP ribosylation) in an ovine sepsis model. Crit. Care 2010, 14, R129. [Google Scholar] [CrossRef] [Green Version]
- Szabó, C.; Cuzzocrea, S.; Zingarelli, B.; O’Connor, M.; Salzman, A.L. Endothelial dysfunction in a rat model of endotoxic shock. Importance of the activation of poly (ADP-ribose) synthetase by peroxynitrite. J. Clin. Investig. 1997, 100, 723–735. [Google Scholar] [CrossRef] [Green Version]
- Belcher, E.; Mitchell, J.; Evans, T. Myocardial dysfunction in sepsis: No role for NO? Heart 2002, 87, 507–509. [Google Scholar] [CrossRef]
- Ozawa, T. Mitochondrial genome mutation in cell death and aging. J. Bioenerget. Biomembr. 1999, 31, 377–390. [Google Scholar] [CrossRef]
- Turrens, J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 2003, 552, 335–344. [Google Scholar] [CrossRef]
- Kakkar, P.; Singh, B.K. Mitochondria: A hub of redox activities and cellular distress control. Mol. Cell. Biochem. 2007, 305, 235–253. [Google Scholar] [CrossRef]
- Dröge, W. Free Radicals in the Physiological Control of Cell Function. Physiol. Rev. 2002, 82, 47–95. [Google Scholar] [CrossRef]
- James, A.M.; Murphy, M.P. How Mitochondrial Damage Affects Cell Function. J. Biomed. Sci. 2002, 9, 475–487. [Google Scholar] [CrossRef] [PubMed]
- Ding, W.-X.; Yin, X.-M. Mitophagy: Mechanisms, pathophysiological roles, and analysis. Biol. Chem. 2012, 393, 547–564. [Google Scholar] [CrossRef] [Green Version]
- Arulkumaran, N.; Deutschman, C.S.; Pinsky, M.R.; Zuckerbraun, B.; Schumacker, P.T.; Gomez, H.; Gomez, A.; Murray, P.; Kellum, J.A. Mitochondrial Function in Sepsis. Shock 2016, 45, 271–281. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zapelini, P.H.; Rezin, G.T.; Cardoso, M.R.; Ritter, C.; Klamt, F.; Moreira, J.C.; Streck, E.L.; Dal-Pizzol, F. Antioxidant treatment reverses mitochondrial dysfunction in a sepsis animal model. Mitochondrion 2008, 8, 211–218. [Google Scholar] [CrossRef]
- Ogura, Y.; Kitada, M.; Koya, D. Sirtuins and Renal Oxidative Stress. Antioxidants 2021, 10, 1198. [Google Scholar] [CrossRef]
- Grabowska, W.; Sikora, E.; Bielak-Zmijewska, A. Sirtuins, a promising target in slowing down the ageing process. Biogerontology 2017, 18, 447–476. [Google Scholar] [CrossRef] [Green Version]
- Liu, T.F.; Vachharajani, V.; Millet, P.; Bharadwaj, M.S.; Molina, A.J.; McCall, C.E. Sequential Actions of SIRT1-RELB-SIRT3 Coordinate Nuclear-Mitochondrial Communication during Immunometabolic Adaptation to Acute Inflammation and Sepsis. J. Biol. Chem. 2015, 290, 396–408. [Google Scholar] [CrossRef] [Green Version]
- Sun, J.; Zhang, J.; Tian, J.; Virzì, G.M.; Digvijay, K.; Cueto, L.; Yin, Y.; Rosner, M.H.; Ronco, C. Mitochondria in Sepsis-Induced AKI. J. Am. Soc. Nephrol. 2019, 30, 1151–1161. [Google Scholar] [CrossRef]
- Tang, B.L. Sirt1 and the Mitochondria. Mol. Cells 2016, 39, 87–95. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McBride, M.A.; Owen, A.M.; Stothers, C.L.; Hernandez, A.; Luan, L.; Burelbach, K.R.; Patil, T.K.; Bohannon, J.K.; Sherwood, E.R.; Patil, N.K. The Metabolic Basis of Immune Dysfunction Following Sepsis and Trauma. Front. Immunol. 2020, 11, 1043. [Google Scholar] [CrossRef]
- Liang, H.; Ward, W.F. PGC-1α: A key regulator of energy metabolism. Adv. Physiol. Educ. 2006, 30, 145–151. [Google Scholar] [CrossRef]
- Wenz, T. Regulation of mitochondrial biogenesis and PGC-1α under cellular stress. Mitochondrion 2013, 13, 134–142. [Google Scholar] [CrossRef]
- Ahn, B.-H.; Kim, H.-S.; Song, S.; Lee, I.H.; Liu, J.; Vassilopoulos, A.; Deng, C.-X.; Finkel, T. A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc. Natl. Acad. Sci. USA 2008, 105, 14447–14452. [Google Scholar] [CrossRef] [Green Version]
- Hallows, W.C.; Yu, W.; Smith, B.; Devires, M.K.; Ellinger, J.; Someya, S.; Shortreed, M.R.; Prolla, T.; Markley, J.L.; Smith, L.M.; et al. Sirt3 Promotes the Urea Cycle and Fatty Acid Oxidation during Dietary Restriction. Mol. Cell 2011, 41, 139–149. [Google Scholar] [CrossRef] [Green Version]
- Hirschey, M.D.; Shimazu, T.; Goetzman, E.; Jing, E.; Schwer, B.; Lombard, D.B.; Grueter, C.A.; Harris, C.; Biddinger, S.; Ilkayeva, O.R.; et al. SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 2010, 464, 121–125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Verdin, E.; Hirschey, M.; Finley, L.W.; Haigis, M.C. Sirtuin regulation of mitochondria: Energy production, apoptosis, and signaling. Trends Biochem. Sci. 2010, 35, 669–675. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Finley, L.W.S.; Haas, W.; Desquiret-Dumas, V.; Wallace, D.C.; Procaccio, V.; Gygi, S.P.; Haigis, M.C. Succinate Dehydrogenase Is a Direct Target of Sirtuin 3 Deacetylase Activity. PLoS ONE 2011, 6, e23295. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jing, E.; Emanuelli, B.; Hirschey, M.D.; Boucher, J.; Lee, K.Y.; Lombard, D.; Verdin, E.M.; Kahn, C.R. Sirtuin-3 (Sirt3) regulates skeletal muscle metabolism and insulin signaling via altered mitochondrial oxidation and reactive oxygen species production. Proc. Natl. Acad. Sci. USA 2011, 108, 14608–14613. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bause, A.S.; Haigis, M.C. SIRT3 regulation of mitochondrial oxidative stress. Exp. Gerontol. 2013, 48, 634–639. [Google Scholar] [CrossRef] [PubMed]
- Qiu, X.; Brown, K.; Hirschey, M.; Verdin, E.; Chen, D. Calorie Restriction Reduces Oxidative Stress by SIRT3-Mediated SOD2 Activation. Cell Metab. 2010, 12, 662–667. [Google Scholar] [CrossRef] [Green Version]
- Someya, S.; Yu, W.; Hallows, W.C.; Xu, J.; Vann, J.M.; Leeuwenburgh, C.; Tanokura, M.; Denu, J.M.; Prolla, T.A. Sirt3 Mediates Reduction of Oxidative Damage and Prevention of Age-Related Hearing Loss under Caloric Restriction. Cell 2010, 143, 802–812. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lei, Y.; Peng, X.; Liu, L.; Dong, Z.; Li, T. Beneficial effect of cyclosporine A on traumatic hemorrhagic shock. J. Surg. Res. 2015, 195, 529–540. [Google Scholar] [CrossRef]
- Li, P.; Meng, X.; Bian, H.; Burns, N.; Zhao, K.-S.; Song, R. Activation of sirtuin 1/3 improves vascular hyporeactivity in severe hemorrhagic shock by alleviation of mitochondrial damage. Oncotarget 2015, 6, 36998–37011. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hafner, A.V.; Dai, J.; Gomes, A.P.; Xiao, C.-Y.; Palmeira, C.M.; Rosenzweig, A.; Sinclair, D.A. Regulation of the mPTP by SIRT3-mediated deacetylation of CypD at lysine 166 suppresses age-related cardiac hypertrophy. Aging 2010, 2, 914–923. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, W.-Y.; Zhang, L.; Sui, M.-X.; Zhu, Y.-H.; Zeng, L. Protective effects of sirtuin 3 in a murine model of sepsis-induced acute kidney injury. Sci. Rep. 2016, 6, 33201. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, W.; Zhang, L.; Chen, R.; Lu, H.; Sui, M.; Zhu, Y.; Zeng, L. SIRT3 Protects Against Acute Kidney Injury via AMPK/mTOR-Regulated Autophagy. Front. Physiol. 2018, 9, 1526. [Google Scholar] [CrossRef]
- Lin, Z.-F.; Xu, H.-B.; Wang, J.-Y.; Lin, Q.; Ruan, Z.; Liu, F.-B.; Jin, W.; Huang, H.-H.; Chen, X. SIRT5 desuccinylates and activates SOD1 to eliminate ROS. Biochem. Biophys. Res. Commun. 2013, 441, 191–195. [Google Scholar] [CrossRef]
- van de Ven, R.A.; Santos, D.; Haigis, M.C. Mitochondrial Sirtuins and Molecular Mechanisms of Aging. Trends Mol. Med. 2017, 23, 320–331. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gertz, M.; Steegborn, C. Using mitochondrial sirtuins as drug targets: Disease implications and available compounds. Cell. Mol. Life Sci. 2016, 73, 2871–2896. [Google Scholar] [CrossRef] [PubMed]
- Torrens-Mas, M.; Pons, D.G.; Sastre-Serra, J.; Oliver, J.; Roca, P. SIRT3 Silencing Sensitizes Breast Cancer Cells to Cytotoxic Treatments Through an Increment in ROS Production. J. Cell. Biochem. 2016, 118, 397–406. [Google Scholar] [CrossRef]
- Qin, K.; Han, C.; Zhang, H.; Li, T.; Li, N.; Cao, X. NAD + dependent deacetylase Sirtuin 5 rescues the innate inflammatory response of endotoxin tolerant macrophages by promoting acetylation of p65. J. Autoimmun. 2017, 81, 120–129. [Google Scholar] [CrossRef]
- Heinonen, T.; Ciarlo, E.; Le Roy, D.; Roger, T. Impact of the Dual Deletion of the Mitochondrial Sirtuins SIRT3 and SIRT5 on Anti-microbial Host Defenses. Front. Immunol. 2019, 10, 2341. [Google Scholar] [CrossRef] [PubMed]
- Tao, J.; Zhang, J.; Ling, Y.; McCall, C.E.; Liu, T.F. Mitochondrial Sirtuin 4 Resolves Immune Tolerance in Monocytes by Rebalancing Glycolysis and Glucose Oxidation Homeostasis. Front. Immunol. 2018, 9, 419. [Google Scholar] [CrossRef] [Green Version]
- McCall, C.E.; Zabalawi, M.; Liu, T.; Martin, A.; Long, D.L.; Buechler, N.L.; Arts, R.J.W.; Netea, M.; Yoza, B.K.; Stacpoole, P.W.; et al. Pyruvate dehydrogenase complex stimulation promotes immunometabolic homeostasis and sepsis survival. JCI Insight 2018, 3, e99292. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arellano, M.; Jiang, J.; Zhou, X.; Zhang, L.; Ye, H.; Wong, D.T.; Hu, S. Current advances in identification of cancer biomarkers in saliva. Front. Biosci. 2009, 1, 296. [Google Scholar] [CrossRef]
- Wu, F.; Schuster, D.P.; Tyml, K.; Wilson, J.X. Ascorbate inhibits NADPH oxidase subunit p47phox expression in microvascular endothelial cells. Free Radic. Biol. Med. 2007, 42, 124–131. [Google Scholar] [CrossRef]
- Fredriksson, K.; Hammarqvist, F.; Strigård, K.; Hultenby, K.; Ljungqvist, O.; Wernerman, J.; Rooyackers, O. Derangements in mitochondrial metabolism in intercostal and leg muscle of critically ill patients with sepsis-induced multiple organ failure. Am. J. Physiol. Metab. 2006, 291, E1044–E1050. [Google Scholar] [CrossRef] [Green Version]
- Ritter, C.; Andrades, M.; Frota, M.L.C.; Bonatto, F.; Pinho, R.A.; Polydoro, M.; Klamt, F.; Pinheiro, C.T.S.; Menna-Barreto, S.S.; Moreira, J.C.F.; et al. Oxidative parameters and mortality in sepsis induced by cecal ligation and perforation. Intensiv. Care Med. 2003, 29, 1782–1789. [Google Scholar] [CrossRef]
- Virdis, A.; Colucci, R.; Fornai, M.; Blandizzi, C.; Duranti, E.; Pinto, S.; Bernardini, N.; Segnani, C.; Antonioli, L.; Taddei, S.; et al. Cyclooxygenase-2 Inhibition Improves Vascular Endothelial Dysfunction in a Rat Model of Endotoxic Shock: Role of Inducible Nitric-Oxide Synthase and Oxidative Stress. J. Pharmacol. Exp. Ther. 2004, 312, 945–953. [Google Scholar] [CrossRef]
- Jacobi, J.; Kristal, B.; Chezar, J.; Shaul, S.M.; Sela, S. Exogenous superoxide mediates pro-oxidative, proinflammatory, and procoagulatory changes in primary endothelial cell cultures. Free Radic. Biol. Med. 2005, 39, 1238–1248. [Google Scholar] [CrossRef] [PubMed]
- Panday, A.; Sahoo, M.; Osorio, D.; Batra, S. NADPH oxidases: An overview from structure to innate immunity-associated pathologies. Cell. Mol. Immunol. 2014, 12, 5–23. [Google Scholar] [CrossRef] [Green Version]
- Joseph, L.C.; Kokkinaki, D.; Valenti, M.-C.; Kim, G.J.; Barca, E.; Tomar, D.; Hoffman, N.E.; Subramanyam, P.; Colecraft, H.M.; Hirano, M.; et al. Inhibition of NADPH oxidase 2 (NOX2) prevents sepsis-induced cardiomyopathy by improving calcium handling and mitochondrial function. JCI Insight 2017, 2, e94248. [Google Scholar] [CrossRef] [PubMed]
- Höcherl, K.; Dreher, F.; Vitzthum, H.; Köhler, J.; Kurtz, A. Cyclosporine A Suppresses Cyclooxygenase-2 Expression in the Rat Kidney. J. Am. Soc. Nephrol. 2002, 13, 2427–2436. [Google Scholar] [CrossRef] [Green Version]
- Winterbourn, C.C. Biological reactivity and biomarkers of the neutrophil oxidant, hypochlorous acid. Toxicology 2002, 181-182, 223–227. [Google Scholar] [CrossRef]
- Rees, M.D.; Whitelock, J.; Malle, E.; Chuang, C.Y.-N.; Iozzo, R.; Nilasaroya, A.; Davies, M. Myeloperoxidase-derived oxidants selectively disrupt the protein core of the heparan sulfate proteoglycan perlecan. Matrix Biol. 2010, 29, 63–73. [Google Scholar] [CrossRef] [Green Version]
- Park, S.Y.; Shin, S.W.; Lee, S.-M.; Park, J.-W. Hypochlorous acid-induced modulation of cellular redox status in HeLa cells. Arch. Pharmacal Res. 2008, 31, 905–910. [Google Scholar] [CrossRef]
- Marinho, H.S.; Real, C.; Cyrne, L.; Soares, H.; Antunes, F. Hydrogen peroxide sensing, signaling and regulation of transcription factors. Redox Biol. 2014, 2, 535–562. [Google Scholar] [CrossRef] [Green Version]
- D’Autréaux, B.; Toledano, M.B. ROS as signalling molecules: Mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 2007, 8, 813–824. [Google Scholar] [CrossRef]
- Barnes, P.J.; Karin, M. Nuclear Factor-κB—A Pivotal Transcription Factor in Chronic Inflammatory Diseases. N. Engl. J. Med. 1997, 336, 1066–1071. [Google Scholar] [CrossRef]
- Jung, Y.; Kim, H.; Min, S.H.; Rhee, S.G.; Jeong, W. Dynein Light Chain LC8 Negatively Regulates NF-κB through the Redox-dependent Interaction with IκBα. J. Biol. Chem. 2008, 283, 23863–23871. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arnalich, F.; Garcia-Palomero, E.; López, J.; Jiménez, M.; Madero, R.; Renart, J.; Vázquez, J.J.; Montiel, C. Predictive Value of Nuclear Factor κB Activity and Plasma Cytokine Levels in Patients with Sepsis. Infect. Immun. 2000, 68, 1942–1945. [Google Scholar] [CrossRef] [Green Version]
- Böhrer, H.; Qiu, F.; Zimmermann, T.; Zhang, Y.; Jllmer, T.; Mannel, D.; Böttiger, B.W.; Stern, D.M.; Waldherr, R.; Saeger, H.D.; et al. Role of NFkappaB in the mortality of sepsis. J. Clin. Investig. 1997, 100, 972–985. [Google Scholar] [CrossRef] [Green Version]
- Nam, N.-H. Naturally Occurring NF-κB Inhibitors. Mini-Rev. Med. Chem. 2006, 6, 945–951. [Google Scholar] [CrossRef]
- Wartenberg, M.; Hoffmann, E.; Schwindt, H.; Grünheck, F.; Petros, J.; Arnold, J.R.S.; Hescheler, J.; Sauer, H. Reactive oxygen species-linked regulation of the multidrug resistance transporter P-glycoprotein in Nox-1 overexpressing prostate tumor spheroids. FEBS Lett. 2005, 579, 4541–4549. [Google Scholar] [CrossRef] [Green Version]
- Yin, G.Q.; Du, K.H.; Gu, F.R.; Fang, Z.X.; Tang, J.Q.; Zhong, B.; Zhu, X.Y.; Wu, Y.W.; Lu, C.P. Early-phase Endotoxic Shock-induced Myocardial Injury Increases iNOS and Selectin Expression in Macaque Primate. Heart Lung Circ. 2007, 16, 85–92. [Google Scholar] [CrossRef]
- Sato, K.; Miyakawa, K.; Takeya, M.; Hattori, R.; Yui, Y.; Sunamoto, M.; Ichimori, Y.; Ushio, Y.; Takahashi, K. Im-munohistochemical expression of inducible nitric oxide synthase (inos) in reversible endotoxic shock studied by a novel monoclonal antibody against rat inos. J. Leukoc. Biol. 1995, 57, 36–44. [Google Scholar] [CrossRef]
- Evans, T.; Carpenter, A.; Kinderman, H.; Cohen, J. Evidence of increased nitric oxide production in patients with the sepsis syndrome. Circ. Shock. 1993, 41, 71–88. [Google Scholar]
- Thimmulappa, R.K.; Lee, H.; Rangasamy, T.; Reddy, S.P.; Yamamoto, M.; Kensler, T.W.; Biswal, S. Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J. Clin. Investig. 2006, 116, 984–995. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, J.-M.; Moehlenkamp, J.D.; Hanson, J.M.; Johnson, J.A. Nrf2-Dependent Activation of the Antioxidant Responsive Element by tert-Butylhydroquinone Is Independent of Oxidative Stress in IMR-32 Human Neuroblastoma Cells. Biochem. Biophys. Res. Commun. 2001, 280, 286–292. [Google Scholar] [CrossRef]
- Alam, J.; Wicks, C.; Stewart, D.; Gong, P.; Touchard, C.; Otterbein, S.; Choi, A.M.; Burow, M.E.; Tou, J.-S. Mechanism of Heme Oxygenase-1 Gene Activation by Cadmium in MCF-7 Mammary Epithelial Cells. J. Biol. Chem. 2000, 275, 27694–27702. [Google Scholar] [CrossRef] [Green Version]
- Kim, Y.-C.; Masutani, H.; Yamaguchi, Y.; Itoh, K.; Yamamoto, M.; Yodoi, J. Hemin-induced Activation of the Thioredoxin Gene by Nrf2. J. Biol. Chem. 2001, 276, 18399–18406. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, W.; Yu, S.; Liu, T.; Kim, J.-H.; Blank, V.; Li, H.; Kong, A.-N.T. Heterodimerization with small Maf proteins enhances nuclear retention of Nrf2 via masking the NESzip motif. Biochim. Biophys. Acta (BBA) Bioenerg. 2008, 1783, 1847–1856. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kong, X.; Thimmulappa, R.; Kombairaju, P.; Biswal, S. NADPH Oxidase-Dependent Reactive Oxygen Species Mediate Amplified TLR4 Signaling and Sepsis-Induced Mortality in Nrf2-Deficient Mice. J. Immunol. 2010, 185, 569–577. [Google Scholar] [CrossRef] [Green Version]
- Deng, Z.; Pardi, R.; Cheadle, W.; Xiang, X.; Zhang, S.; Shah, S.V.; Grizzle, W.; Miller, D.; Mountz, J.; Zhang, H.-G. Plant homologue constitutive photomorphogenesis 9 (COP9) signalosome subunit CSN5 regulates innate immune responses in macrophages. Blood 2011, 117, 4796–4804. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kolls, J.K. Oxidative stress in sepsis: A redox redux. J. Clin. Investig. 2006, 116, 860–863. [Google Scholar] [CrossRef] [PubMed]
- Radak, Z.; Koltai, E.; Taylor, A.W.; Higuchi, M.; Kumagai, S.; Ohno, H.; Goto, S.; Boldogh, I. Redox-regulating sirtuins in aging, caloric restriction, and exercise. Free Radic. Biol. Med. 2013, 58, 87–97. [Google Scholar] [CrossRef] [PubMed]
- Schafer, F.Q.; Buettner, G. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 2001, 30, 1191–1212. [Google Scholar] [CrossRef]
- Wang, X.; Buechler, N.L.; Long, D.L.; Furdui, C.M.; Yoza, B.K.; McCall, C.E.; Vachharajani, V. Cysteine thiol oxidation on SIRT2 regulates inflammation in obese mice with sepsis. Inflammation 2018, 42, 156–169. [Google Scholar] [CrossRef]
- Long, D.; Wu, H.; Tsang, A.W.; Poole, L.B.; Yoza, B.K.; Wang, X.; Vachharajani, V.; Furdui, C.M.; McCall, C.E. The Oxidative State of Cysteine Thiol 144 Regulates the SIRT6 Glucose Homeostat. Sci. Rep. 2017, 7, 11005. [Google Scholar] [CrossRef]
- Yeung, F.; Hoberg, J.E.; Ramsey, C.S.; Keller, M.D.; Jones, D.R.; Frye, R.A.; Mayo, M.W. Modulation of NF-κB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 2004, 23, 2369–2380. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rothgiesser, K.M.; Erener, S.; Waibel, S.; Lüscher, B.; Hottiger, M.O. SIRT2 regulates NF-κB-dependent gene expression through deacetylation of p65 Lys310. J. Cell Sci. 2010, 123, 4251–4258. [Google Scholar] [CrossRef] [Green Version]
- Pahl, H.L. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 1999, 18, 6853–6866. [Google Scholar] [CrossRef] [Green Version]
- Gao, R.; Chen, J.; Hu, Y.; Li, Z.; Wang, S.; Shetty, S.; Fu, J. Sirt1 Deletion Leads to Enhanced Inflammation and Aggravates Endotoxin-Induced Acute Kidney Injury. PLoS ONE 2014, 9, e98909. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, X.; Buechler, N.L.; Yoza, B.K.; McCall, C.E.; Vachharajani, V.T. Resveratrol attenuates microvascular inflammation in sepsis via SIRT-1-Induced modulation of adhesion molecules in ob/ob mice. Obesity 2015, 23, 1209–1217. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, X.; Buechler, N.L.; Martin, A.; Wells, J.; Yoza, B.; McCall, C.E.; Vachharajani, V. Correction: Sirtuin-2 Regulates Sepsis Inflammation in ob/ob Mice. PLoS ONE 2016, 11, e0162560. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sasaki, T.; Maier, B.; Koclega, K.D.; Chruszcz, M.; Gluba, W.; Stukenberg, P.T.; Minor, W.; Scrable, H. Phosphorylation Regulates SIRT1 Function. PLoS ONE 2008, 3, e4020. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shih, L.-J.; Wang, J.-Y.; Jheng, J.-Y.; Siao, A.-C.; Lin, Y.-Y.; Tsuei, Y.-W.; Kuo, Y.-C.; Chuu, C.-P.; Kao, Y.-H. Betel Nut Arecoline Induces Different Phases of Growth Arrest between Normal and Cancerous Prostate Cells through the Reactive Oxygen Species Pathway. Int. J. Mol. Sci. 2020, 21, 9219. [Google Scholar] [CrossRef]
- Rizvi, S.H.M.; Shao, D.; Tsukahara, Y.; Pimentel, D.R.; Weisbrod, R.M.; Hamburg, N.M.; McComb, M.E.; Matsui, R.; Bachschmid, M.M. Oxidized GAPDH transfers S-glutathionylation to a nuclear protein Sirtuin-1 leading to apoptosis. Free Radic. Biol. Med. 2021, 174, 73–83. [Google Scholar] [CrossRef]
- Shao, D.; Fry, J.; Han, J.; Hou, X.; Pimentel, D.R.; Matsui, R.; Cohen, R.A.; Bachschmid, M.M. A Redox-resistant Sirtuin-1 Mutant Protects against Hepatic Metabolic and Oxidant Stress. J. Biol. Chem. 2014, 289, 7293–7306. [Google Scholar] [CrossRef] [Green Version]
- Kornberg, M.; Sen, N.; Hara, M.R.; Juluri, K.R.; Nguyen, J.V.K.; Snowman, A.M.; Law, L.; Hester, L.D.; Snyder, S.H. GAPDH mediates nitrosylation of nuclear proteins. Nature 2010, 12, 1094–1100. [Google Scholar] [CrossRef] [Green Version]
- Jung, S.-B.; Kim, C.-S.; Kim, Y.-R.; Naqvi, A.; Yamamori, T.; Kumar, S.; Kumar, A.; Irani, K. Redox Factor-1 Activates Endothelial SIRTUIN1 through Reduction of Conserved Cysteine Sulfhydryls in Its Deacetylase Domain. PLoS ONE 2013, 8, e65415. [Google Scholar] [CrossRef] [Green Version]
- Santos, L.; Escande, C.; Denicola, A. Potential Modulation of Sirtuins by Oxidative Stress. Oxidative Med. Cell. Longev. 2015, 2016, 9831825. [Google Scholar] [CrossRef] [Green Version]
- Kim, J.-E.; Chen, J.; Lou, Z. DBC1 is a negative regulator of SIRT1. Nature 2008, 451, 583–586. [Google Scholar] [CrossRef] [PubMed]
- Kim, E.-J.; Kho, J.-H.; Kang, M.-R.; Um, S.-J. Active Regulator of SIRT1 Cooperates with SIRT1 and Facilitates Suppression of p53 Activity. Mol. Cell 2007, 28, 277–290. [Google Scholar] [CrossRef]
- Yuan, J.; Luo, K.; Liu, T.; Lou, Z. Regulation of SIRT1 activity by genotoxic stress. Genes Dev. 2012, 26, 791–796. [Google Scholar] [CrossRef] [Green Version]
- Yang, X.; Park, S.-H.; Chang, H.-C.; Shapiro, J.S.; Vassilopoulos, A.; Sawicki, K.T.; Chen, C.; Shang, M.; Burridge, P.W.; Epting, C.L.; et al. Sirtuin 2 regulates cellular iron homeostasis via deacetylation of transcription factor NRF2. J. Clin. Investig. 2017, 127, 1505–1516. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cao, W.; Hong, Y.; Chen, H.; Wu, F.; Wei, X.; Ying, W. SIRT2 mediates NADH-induced increases in Nrf2, GCL, and glutathione by modulating Akt phosphorylation in PC12 cells. FEBS Lett. 2016, 590, 2241–2255. [Google Scholar] [CrossRef] [Green Version]
- Xue, F.; Huang, J.-W.; Ding, P.-Y.; Zang, H.-G.; Kou, Z.-J.; Li, T.; Fan, J.; Peng, Z.-W.; Yan, W.-J. Nrf2/antioxidant defense pathway is involved in the neuroprotective effects of Sirt1 against focal cerebral ischemia in rats after hyperbaric oxygen preconditioning. Behav. Brain Res. 2016, 309, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Pan, H.; Guang-Hui, L.; Liu, X.; Li, J.; Wang, L.; Wu, J.; Weizhou, Z.; Zhang, W.; Ren, R.; Zhang, W.; et al. SIRT6 safeguards human mesenchymal stem cells from oxidative stress by coactivating NRF2. Cell Res. 2016, 26, 190–205. [Google Scholar] [CrossRef]
- Wang, F.; Nguyen, M.; Qin, F.X.-F.; Tong, Q. SIRT2 deacetylates FOXO3a in response to oxidative stress and caloric restriction. Aging Cell 2007, 6, 505–514. [Google Scholar] [CrossRef]
- Klotz, L.-O.; Sánchez-Ramos, C.; Prieto, I.; Urbánek, P.; Steinbrenner, H.; Monsalve, M. Redox regulation of FoxO transcription factors. Redox Biol. 2015, 6, 51–72. [Google Scholar] [CrossRef] [Green Version]
- Kops, G.; Dansen, T.B.; Polderman, P.E.; Saarloos, I.; Wirtz, K.W.A.; Coffer, P.J.; Huang, T.-T.; Bos, J.L.; Medema, R.; Burgering, B. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 2002, 419, 316–321. [Google Scholar] [CrossRef]
- Yang, J.; Gupta, V.; Carroll, K.; Liebler, D.C. Site-specific mapping and quantification of protein S-sulphenylation in cells. Nat. Commun. 2014, 5, 4776. [Google Scholar] [CrossRef] [Green Version]
- Feng, J.; Yan, P.-F.; Zhao, H.-Y.; Zhang, F.-C.; Zhao, W.-H.; Feng, M. SIRT6 suppresses glioma cell growth via induction of apoptosis, inhibition of oxidative stress and suppression of JAK2/STAT3 signaling pathway activation. Oncol. Rep. 2015, 35, 1395–1402. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rezazadeh, S.; Yang, D.; Tombline, G.; Simon, M.; Regan, S.P.; Seluanov, A.; Gorbunova, V. SIRT6 promotes transcription of a subset of NRF2 targets by mono-ADP-ribosylating BAF170. Nucleic Acids Res. 2019, 47, 7914–7928. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mostoslavsky, R.; Chua, K.F.; Lombard, D.; Pang, W.W.; Fischer, M.R.; Gellon, L.; Liu, P.; Mostoslavsky, G.; Franco, S.; Murphy, M.M.; et al. Genomic Instability and Aging-like Phenotype in the Absence of Mammalian SIRT6. Cell 2006, 124, 315–329. [Google Scholar] [CrossRef] [Green Version]
- Stirzaker, C.; Taberlay, P.; Statham, A.L.; Clark, S.J. Mining cancer methylomes: Prospects and challenges. Trends Genet. 2014, 30, 75–84. [Google Scholar] [CrossRef] [PubMed]
- Moore, L.D.; Le, T.; Fan, G. DNA Methylation and Its Basic Function. Neuropsychopharmacology 2013, 38, 23–38. [Google Scholar] [CrossRef] [Green Version]
- Jaenisch, R.; Bird, A. Epigenetic regulation of gene expression: How the genome integrates intrinsic and environmental signals. Nat. Genet. 2003, 33, 245–254. [Google Scholar] [CrossRef] [PubMed]
- García-Guede, A.; Vera, O.; Ibáñez-De-Caceres, I. When Oxidative Stress Meets Epigenetics: Implications in Cancer Development. Antioxidants 2020, 9, 468. [Google Scholar] [CrossRef] [PubMed]
- Castelo-Branco, P.; Leão, R.; Lipman, T.; Campbell, B.; Lee, D.; Price, A.; Zhang, C.; Heidari, A.; Stephens, D.; Boerno, S.; et al. A cancer specific hypermethylation signature of the TERT promoter predicts biochemical relapse in prostate cancer: A retrospective cohort study. Oncotarget 2016, 7, 57726–57736. [Google Scholar] [CrossRef] [Green Version]
- Ausio, J.; Van Holde, K. The histones of the sperm of Spisula solidissima include a novel, cysteine-containing H-1 histone. Cell Differ. 1988, 23, 175–189. [Google Scholar] [CrossRef]
- Portela, A.; Esteller, M. Epigenetic modifications and human disease. Nat. Biotechnol. 2010, 28, 1057–1068. [Google Scholar] [CrossRef] [PubMed]
- Bannister, A.J.; Kouzarides, T. Regulation of chromatin by histone modifications. Cell Res. 2011, 21, 381–395. [Google Scholar] [CrossRef] [PubMed]
- Lau, P.N.I.; Cheung, P. Histone code pathway involving H3 S28 phosphorylation and K27 acetylation activates transcription and antagonizes polycomb silencing. Proc. Natl. Acad. Sci. USA 2011, 108, 2801–2806. [Google Scholar] [CrossRef] [Green Version]
- Dawson, M.A.; Bannister, A.; Gottgens, B.; Foster, S.; Bartke, T.; Green, A.; Kouzarides, T. JAK2 phosphorylates histone H3Y41 and excludes HP1α from chromatin. Nature 2009, 461, 819–822. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cohen-Armon, M.; Visochek, L.; Rozensal, D.; Kalal, A.; Geistrikh, I.; Klein, R.; Bendetz-Nezer, S.; Yao, Z.; Seger, R. DNA-Independent PARP-1 Activation by Phosphorylated ERK2 Increases Elk1 Activity: A Link to Histone Acetylation. Mol. Cell 2007, 25, 297–308. [Google Scholar] [CrossRef] [PubMed]
- Moss, E.; Halkos, M.E. Cost effectiveness of robotic mitral valve surgery. Ann. Cardiothorac. Surg. 2017, 6, 33–37. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gill, G. Something about SUMO inhibits transcription. Curr. Opin. Genet. Dev. 2005, 15, 536–541. [Google Scholar] [CrossRef]
- Yang, S.-H.; Sharrocks, A.D. SUMO Promotes HDAC-Mediated Transcriptional Repression. Mol. Cell 2004, 13, 611–617. [Google Scholar] [CrossRef]
- Meas, R.; Mao, P. Histone ubiquitylation and its roles in transcription and DNA damage response. DNA Repair 2015, 36, 36–42. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, J.; Guermah, M.; McGinty, R.K.; Lee, J.-S.; Tang, Z.; Milne, T.A.; Shilatifard, A.; Muir, T.W.; Roeder, R.G. RAD6-Mediated Transcription-Coupled H2B Ubiquitylation Directly Stimulates H3K4 Methylation in Human Cells. Cell 2009, 137, 459–471. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Keppler, B.R.; Archer, T.K. Chromatin-modifying enzymes as therapeutic targets—Part 1. Expert Opin. Ther. Targets 2008, 12, 1301–1312. [Google Scholar] [CrossRef] [Green Version]
- Cedar, H.; Bergman, Y. Linking DNA methylation and histone modification: Patterns and paradigms. Nat. Rev. Genet. 2009, 10, 295–304. [Google Scholar] [CrossRef]
- Esteller, M. Non-coding RNAs in human disease. Nat. Rev. Genet. 2011, 12, 861–874. [Google Scholar] [CrossRef] [PubMed]
- Calvano, S.E.; Xiao, D.R.W.; Richards, R.M.; Felciano, H.V.; Baker, R.J.; Cho, R.O.; Chen, B.H.; Brownstein, J.P.; Cobb, S.; Tschoeke, K. A network-based analysis of systemic inflammation in humans. Nature 2005, 437, 1032–1037. [Google Scholar] [CrossRef]
- Novakovic, B.; Habibi, E.; Wang, S.-Y.; Arts, R.J.; Davar, R.; Megchelenbrink, W.; Kim, B.; Kuznetsova, T.; Kox, M.; Zwaag, J.; et al. β-Glucan Reverses the Epigenetic State of LPS-Induced Immunological Tolerance. Cell 2016, 167, 1354–1368. [Google Scholar] [CrossRef] [Green Version]
- Ghizzoni, M.; Haisma, H.J.; Maarsingh, H.; Dekker, F.J. Histone acetyltransferases are crucial regulators in NF-κB mediated inflammation. Drug Discov. Today 2011, 16, 504–511. [Google Scholar] [CrossRef] [Green Version]
- Barnes, P.J.; Adcock, I.; Ito, K. Histone acetylation and deacetylation: Importance in inflammatory lung diseases. Eur. Respir. J. 2005, 25, 552–563. [Google Scholar] [CrossRef]
- Marmorstein, R.; Zhou, M.-M. Writers and Readers of Histone Acetylation: Structure, Mechanism, and Inhibition. Cold Spring Harb. Perspect. Biol. 2014, 6, a018762. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hull, E.E.; Montgomery, M.; Leyva, K.J. HDAC Inhibitors as Epigenetic Regulators of the Immune System: Impacts on Cancer Therapy and Inflammatory Diseases. BioMed Res. Int. 2016, 2016, 8797206. [Google Scholar] [CrossRef] [Green Version]
- El Gazzar, M.; Liu, T.; Yoza, B.K.; McCall, C.E. Dynamic and Selective Nucleosome Repositioning during Endotoxin Tolerance. J. Biol. Chem. 2010, 285, 1259–1271. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sullivan, K.E.; Reddy, A.B.M.; Dietzmann, K.; Suriano, A.R.; Kocieda, V.P.; Stewart, M.; Bhatia, M. Epigenetic Regulation of Tumor Necrosis Factor Alpha. Mol. Cell. Biol. 2007, 27, 5147–5160. [Google Scholar] [CrossRef] [Green Version]
- Hopp, L.; Loeffler-Wirth, H.; Nersisyan, L.; Arakelyan, A.; Binder, H. Footprints of Sepsis Framed Within Community Acquired Pneumonia in the Blood Transcriptome. Front. Immunol. 2018, 9, 1620. [Google Scholar] [CrossRef] [PubMed]
- Cao, Q.; Wang, X.; Jia, L.; Mondal, A.K.; Diallo, A.; Hawkins, G.A.; Das, S.; Parks, J.S.; Yu, L.; Shi, H.; et al. Inhibiting DNA Methylation by 5-Aza-2′-deoxycytidine Ameliorates Atherosclerosis Through Suppressing Macrophage Inflammation. Endocrinology 2014, 155, 4925–4938. [Google Scholar] [CrossRef] [Green Version]
- Falcão-Holanda, R.B.; Brunialti, M.K.C.; Jasiulionis, M.G.; Salomão, R. Epigenetic Regulation in Sepsis, Role in Pathophysiology and Therapeutic Perspective. Front. Med. 2021, 8, 685333. [Google Scholar] [CrossRef] [PubMed]
- Pellegrina, D.V.D.S.; Severino, P.; Barbeiro, H.V.; De Souza, H.P.; Machado, M.C.C.; Pinheiro-Da-Silva, F.; Reis, E.M. Insights into the Function of Long Noncoding RNAs in Sepsis Revealed by Gene Co-Expression Network Analysis. Non-Coding RNA 2017, 3, 5. [Google Scholar] [CrossRef]
- Scicluna, B.P.; Uhel, F.; Van Vught, L.A.; Wiewel, M.A.; Hoogendijk, A.J.; Baessman, I.; Franitza, M.; Nürnberg, P.; Horn, J.; Cremer, O.L.; et al. The leukocyte non-coding RNA landscape in critically ill patients with sepsis. eLife 2020, 9, e58597. [Google Scholar] [CrossRef] [PubMed]
- Biswas, S.K.; Lopez-Collazo, E. Endotoxin tolerance: New mechanisms, molecules and clinical significance. Trends Immunol. 2009, 30, 475–487. [Google Scholar] [CrossRef]
- Shalova, I.N.; Lim, J.Y.; Chittezhath, M.; Zinkernagel, A.S.; Beasley, F.; Hernández-Jiménez, E.; Toledano, V.; Cubillos-Zapata, C.; Rapisarda, A.; Chen, J.; et al. Human Monocytes Undergo Functional Re-programming during Sepsis Mediated by Hypoxia-Inducible Factor-1α. Immunity 2015, 42, 484–498. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- El Gazzar, M.; Yoza, B.K.; Chen, X.; Hu, J.; Hawkins, G.A.; McCall, C.E. G9a and HP1 Couple Histone and DNA Methylation to TNFα Transcription Silencing during Endotoxin Tolerance. J. Biol. Chem. 2008, 283, 32198–32208. [Google Scholar] [CrossRef] [Green Version]
- Chan, C.; Li, L.; McCall, C.E.; Yoza, B.K. Endotoxin Tolerance Disrupts Chromatin Remodeling and NF-κB Transactivation at the IL-1β Promoter. J. Immunol. 2005, 175, 461–468. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- El Gazzar, M.; McCall, C.E. MicroRNAs Distinguish Translational from Transcriptional Silencing during Endotoxin Tolerance. J. Biol. Chem. 2010, 285, 20940–20951. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- El Gazzar, M.; Church, A.; Liu, T.; McCall, C.E. MicroRNA-146a regulates both transcription silencing and translation disruption of TNF-α during TLR4-induced gene reprogramming. J. Leukoc. Biol. 2011, 90, 509–519. [Google Scholar] [CrossRef] [PubMed]
- Zhu, X.; Meyers, A.; Long, D.; Ingram, B.; Liu, T.; Yoza, B.K.; Vachharajani, V.; McCall, C.E. Frontline Science: Monocytes sequentially rewire metabolism and bioenergetics during an acute inflammatory response. J. Leukoc. Biol. 2018, 105, 215–228. [Google Scholar] [CrossRef] [PubMed]
- Liu, T.F.; Vachharajani, V.; Yoza, B.K.; McCall, C.E. NAD+-dependent Sirtuin 1 and 6 Proteins Coordinate a Switch from Glucose to Fatty Acid Oxidation during the Acute Inflammatory Response. J. Biol. Chem. 2012, 287, 25758–25769. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, T.F.; Yoza, B.K.; El Gazzar, M.; Vachharajani, V.; McCall, C.E. NAD+-dependent SIRT1 Deacetylase Participates in Epigenetic Reprogramming during Endotoxin Tolerance. J. Biol. Chem. 2011, 286, 9856–9864. [Google Scholar] [CrossRef] [Green Version]
- Martin, A.N.; Alexander-Miller, M.; Yoza, B.K.; Vachharajani, V.; McCall, C.E. Sirtuin1 Targeting Reverses Innate and Adaptive Immune Tolerance in Septic Mice. J. Immunol. Res. 2018, 2018, 2402593. [Google Scholar] [CrossRef]
- Lyn-Kew, K.; Rich, E.; Zeng, X.; Wen, H.; Kunkel, S.L.; Newstead, M.W.; Bhan, U.; Standiford, T.J. IRAK-M Regulates Chromatin Remodeling in Lung Macrophages during Experimental Sepsis. PLoS ONE 2010, 5, e11145. [Google Scholar] [CrossRef]
- El Gazzar, M.; Yoza, B.K.; Chen, X.; Garcia, B.A.; Young, N.L.; McCall, C.E. Chromatin-Specific Remodeling by HMGB1 and Linker Histone H1 Silences Proinflammatory Genes during Endotoxin Tolerance. Mol. Cell. Biol. 2009, 29, 1959–1971. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McCall, C.E.; Yoza, B.; Liu, T.; El Gazzar, M. Gene-Specific Epigenetic Regulation in Serious Infections with Systemic Inflammation. J. Innate Immun. 2010, 2, 395–405. [Google Scholar] [CrossRef] [Green Version]
- El Gazzar, M.; Yoza, B.K.; Hu, J.Y.-Q.; Cousart, S.L.; McCall, C.E. Epigenetic Silencing of Tumor Necrosis Factor α during Endotoxin Tolerance. J. Biol. Chem. 2007, 282, 26857–26864. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Eskandarian, H.A.; Impens, F.; Nahori, M.-A.; Soubigou, G.; Coppée, J.-Y.; Cossart, P.; Hamon, M.A. A Role for SIRT2-Dependent Histone H3K18 Deacetylation in Bacterial Infection. Science 2013, 341, 1238858. [Google Scholar] [CrossRef]
- Pereira, J.M.; Chevalier, C.; Chaze, T.; Gianetto, Q.; Impens, F.; Matondo, M.; Cossart, P.; Hamon, M.A. Infection Reveals a Modification of SIRT2 Critical for Chromatin Association. Cell Rep. 2018, 23, 1124–1137. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Choi, S.-E.; Kemper, J.K. Regulation of SIRT1 by MicroRNAs. Mol. Cells 2013, 36, 385–392. [Google Scholar] [CrossRef]
- Yamakuchi, M. MicroRNA Regulation of SIRT1. Front. Physiol. 2012, 3, 68. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bai, X.-Z.; Zhang, J.-L.; Liu, Y.; Zhang, W.; Li, X.-Q.; Wang, K.-J.; Cao, M.-Y.; Zhang, J.-N.; Han, F.; Shi, J.-H.; et al. MicroRNA-138 Aggravates Inflammatory Responses of Macrophages by Targeting SIRT1 and Regulating the NF-κB and AKT Pathways. Cell. Physiol. Biochem. 2018, 49, 489–500. [Google Scholar] [CrossRef] [PubMed]
- Chen, S.; Ding, R.; Hu, Z.; Yin, X.; Xiao, F.; Zhang, W.; Yan, S.; Lv, C. MicroRNA-34a Inhibition Alleviates Lung Injury in Cecal Ligation and Puncture Induced Septic Mice. Front. Immunol. 2020, 11, 1829. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Guan, H.; Zhang, J.-L.; Zheng, Z.; Wang, H.-T.; Tao, K.; Han, S.-C.; Su, L.-L.; Hu, D. Acute downregulation of miR-199a attenuates sepsis-induced acute lung injury by targeting SIRT1. Am. J. Physiol. Physiol. 2018, 314, C449–C455. [Google Scholar] [CrossRef] [PubMed] [Green Version]
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Gandhirajan, A.; Roychowdhury, S.; Vachharajani, V. Sirtuins and Sepsis: Cross Talk between Redox and Epigenetic Pathways. Antioxidants 2022, 11, 3. https://doi.org/10.3390/antiox11010003
Gandhirajan A, Roychowdhury S, Vachharajani V. Sirtuins and Sepsis: Cross Talk between Redox and Epigenetic Pathways. Antioxidants. 2022; 11(1):3. https://doi.org/10.3390/antiox11010003
Chicago/Turabian StyleGandhirajan, Anugraha, Sanjoy Roychowdhury, and Vidula Vachharajani. 2022. "Sirtuins and Sepsis: Cross Talk between Redox and Epigenetic Pathways" Antioxidants 11, no. 1: 3. https://doi.org/10.3390/antiox11010003
APA StyleGandhirajan, A., Roychowdhury, S., & Vachharajani, V. (2022). Sirtuins and Sepsis: Cross Talk between Redox and Epigenetic Pathways. Antioxidants, 11(1), 3. https://doi.org/10.3390/antiox11010003