Abstract
Sepsis is a condition of severe organ failure caused by the maladaptive response of the host to an infection. It is a severe complication affecting critically ill patients, which can progress to severe sepsis, septic shock, and ultimately death. As a vital part of the human innate immune system, neutrophils are essential in resisting pathogen invasion, infection, and immune surveillance. Neutrophil-produced reactive oxygen species (ROS) play a pivotal role in organ dysfunction related to sepsis. In recent years, ROS have received a lot of attention as a major cause of sepsis, which can progress to severe sepsis and septic shock. This paper reviews the existing knowledge on the production mechanism of neutrophil ROS in human organ function impairment because of sepsis.
概要
脓毒症是由宿主对感染的不良反应引起的严重器官衰竭的综合征。中性粒细胞作为人类固有免疫系统的重要组成部分,对抵抗病原体入侵、感染和免疫监视至关重要。中性粒细胞产生的活性氧(ROS)在与脓毒症相关的器官功能障碍中起关键作用。脓毒症可发展为严重脓毒症和感染性休克,因此近年来ROS作为脓毒症的一个因素受到了很多关注。本综述旨在总结中性粒细胞ROS在脓毒症器官功能损害中的适当机制,并有望为脓毒症期间破坏性器官功能障碍的发生和发展提供新的线索。
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Avagimyan A, Popov S, Shalnova S, 2022. The pathophysiological basis of diabetic cardiomyopathy development. Curr Probl Cardiol, in press. https://doi.org/10.1016/j.cpcardiol.2022.101156
Bae MH, Park SH, Park CJ, et al., 2016. Flow cytometric measurement of respiratory burst activity and surface expression of neutrophils for septic patient prognosis. Cytom B Clin Cytom, 90(4):368–375. https://doi.org/10.1002/cyto.b.21274
Bateman RM, Sharpe MD, Ellis CG, 2003. Bench-to-bedside review: microvascular dysfunction in sepsis—hemodynamics, oxygen transport, and nitric oxide. Crit Care, 7(5):359. https://doi.org/10.1186/cc2353
Beesley SJ, Weber G, Sarge T, et al., 2018. Septic cardiomyopathy. Crit Care Med, 46(4):625–634. https://doi.org/10.1097/ccm.0000000000002851
Bougaki M, Searles RJ, Kida K, et al., 2010. NOS3 protects against systemic inflammation and myocardial dysfunction in murine polymicrobial sepsis. Shock, 34(3):281–290. https://doi.org/10.1097/SHK.0b013e3181cdc327
Brealey D, Brand M, Hargreaves I, et al., 2002. Association between mitochondrial dysfunction and severity and outcome of septic shock. Lancet, 360(9328):219–223. https://doi.org/10.1016/s0140-6736(02)09459-x
Brealey D, Karyampudi S, Jacques TS, et al., 2004. Mitochondrial dysfunction in a long-term rodent model of sepsis and organ failure. Am J Physiol Regul Integr Comp Physiol, 286(3):R491–R497. https://doi.org/10.1152/ajpregu.00432.2003
Brinkmann V, Reichard U, Goosmann C, et al., 2004. Neutrophil extracellular traps kill bacteria. Science, 303(5663): 1532–1535. https://doi.org/10.1126/science.1092385
Cai H, Harrison DG, 2000. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res, 87(10):840–844. https://doi.org/10.1161/01.RES.87.10.840
Cao ZZ, Qin HQ, Huang YH, et al., 2022. Crosstalk of pyroptosis, ferroptosis, and mitochondrial aldehyde dehydrogenase 2-related mechanisms in sepsis-induced lung injury in a mouse model. Bioengineered, 13(3):4810–4820. https://doi.org/10.1080/21655979.2022.2033381
Catalão CHR, Santos-Júnior NN, da Costa LHA, et al., 2017. Brain oxidative stress during experimental sepsis is attenuated by simvastatin administration. Mol Neurobiol, 54(9):7008–7018. https://doi.org/10.1007/s12035-016-0218-3
Caudrillier A, Kessenbrock K, Gilliss BM, et al., 2012. Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury. J Clin Invest, 122(7):2661–2671. https://doi.org/10.1172/jci61303
Cave AC, Brewer AC, Narayanapanicker A, et al., 2006. NADPH oxidases in cardiovascular health and disease. Antioxid Redox Signal, 8(5–6):691–728. https://doi.org/10.1089/ars.2006.8.691
Cernuda-Morollón E, Ridley AJ, 2006. Rho GTPases and leukocyte adhesion receptor expression and function in endothelial cells. Circ Res, 98(6):757–767. https://doi.org/10.1161/01.RES.0000210579.35304.d3
Chelazzi C, Villa G, Mancinelli P, et al., 2015. Glycocalyx and sepsis-induced alterations in vascular permeability. Crit Care, 19:26. https://doi.org/10.1186/s13054-015-0741-z
Chen YH, Jin S, Teng X, et al., 2018. Hydrogen sulfide attenuates LPS-induced acute kidney injury by inhibiting inflammation and oxidative stress. Oxid Med Cell Longev, 2018:6717212. https://doi.org/10.1155/2018/6717212
Cogger VC, Mross PE, Hosie MJ, et al., 2001. The effect of acute oxidative stress on the ultrastructure of the perfused rat liver. Pharmacol Toxicol, 89(6):306–311. https://doi.org/10.1034/j.1600-0773.2001.d01-165.x
Cohen J, 2002. The immunopathogenesis of sepsis. Nature, 420(6917):885–891. https://doi.org/10.1038/nature01326
Drifte G, Dunn-Siegrist I, Tissières P, et al., 2013. Innate immune functions of immature neutrophils in patients with sepsis and severe systemic inflammatory response syndrome. Crit Care Med, 41(3):820–832. https://doi.org/10.1097/CCM.0b013e318274647d
Dunham-Snary KJ, Hong ZG, Xiong PY, et al., 2016. A mitochondrial redox oxygen sensor in the pulmonary vasculature and ductus arteriosus. Pflugers Arch, 468(1):43–58. https://doi.org/10.1007/s00424-015-1736-y
Eidelman LA, Putterman D, Putterman C, et al., 1996. The spectrum of septic encephalopathy. Definitions, etiologies, and mortalities. JAMA, 275(6):470–473. https://doi.org/10.1001/jama.1996.03530300054040
Ely EW, Shintani A, Truman B, et al., 2004. Delirium as a predictor of mortality in mechanically ventilated patients in the intensive care unit. JAMA, 291(14):1753–1762. https://doi.org/10.1001/jama.291.14.1753
Fani F, Regolisti G, Delsante M, et al., 2018. Recent advances in the pathogenetic mechanisms of sepsis-associated acute kidney injury. J Nephrol, 31(3):351–359. https://doi.org/10.1007/s40620-017-0452-4
Fink MP, Evans TW, 2002. Mechanisms of organ dysfunction in critical illness: report from a Round Table Conference held in Brussels. Intensive Care Med, 28(3):369–375. https://doi.org/10.1007/s00134-001-1205-2
Fuchs TA, Brill A, Duerschmied D, et al., 2010. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA, 107(36):15880–15885. https://doi.org/10.1073/pnas.1005743107
Gamal M, Moawad J, Rashed L, et al., 2018. Possible involvement of tetrahydrobiopterin in the disturbance of redox homeostasis in sepsis-induced brain dysfunction. Brain Res, 1685:19–28. https://doi.org/10.1016/j.brainres.2018.02.008
Gan TT, Yang YL, Hu F, et al., 2018. TLR3 regulated poly I: C-induced neutrophil extracellular traps and acute lung injury partly through p38 MAP kinase. Front Microbiol, 9:3174. https://doi.org/10.3389/fmicb.2018.03174
Ge QM, Huang CM, Zhu XY, et al., 2017. Differentially expressed miRNAs in sepsis-induced acute kidney injury target oxidative stress and mitochondrial dysfunction pathways. PLoS ONE, 12(3):e0173292. https://doi.org/10.1371/journal.pone.0173292
Gerin F, Sener U, Erman H, et al., 2016. The effects of quercetin on acute lung injury and biomarkers of inflammation and oxidative stress in the rat model of sepsis. Inflammation, 39(2):700–705. https://doi.org/10.1007/s10753-015-0296-9
Griendling KK, Sorescu D, Ushio-Fukai M, 2000. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res, 86(5):494–501. https://doi.org/10.1161/01.res.86.5.494
Guerci P, Ergin B, Ince C, 2017. The macro- and microcirculation of the kidney. Best Pract Res Clin Anaesthesiol, 31(3):315–329. https://doi.org/10.1016/j.bpa.2017.10.002
Guo RF, Ward PA, 2007. Role of oxidants in lung injury during sepsis. Antioxid Redox Signal, 9(11): 1991–2002. https://doi.org/10.1089/ars.2007.1785
Guo SQ, Zhang Y, Wang ZF, et al., 2017. Intraperitoneal gardiquimod protects against hepatotoxicity through inhibition of oxidative stress and inflammation in mice with sepsis. JBiochem Mol Toxicol, 31(8):e21923. https://doi.org/10.1002/jbt.21923
Hadem J, Bockmeyer CL, Lukasz A, et al., 2012. Angiopoietin-2 in acute liver failure. Crit Care Med, 40(5):1499–1505. https://doi.org/10.1097/CCM.0b013e318241e34e
Haileselassie B, Su E, Pozios I, et al., 2017. Myocardial oxidative stress correlates with left ventricular dysfunction on strain echocardiography in a rodent model of sepsis. Intensive Care Med Exp, 5:21. https://doi.org/10.1186/s40635-017-0134-5
Hong GL, Zheng D, Zhang LL, et al., 2018. Administration of nicotinamide riboside prevents oxidative stress and organ injury in sepsis. Free Radic Biol Med, 123:125–137. https://doi.org/10.1016/j.freeradbiomed.2018.05.073
Hordijk PL, 2006. Endothelial signalling events during leukocyte transmigration. FEBS J, 273(19):4408–4415. https://doi.org/10.1111/j.1742-4658.2006.05440.x
Hou MY, Wu XJ, Zhao ZY, et al., 2022. Endothelial cell-targeting, ROS-ultrasensitive drug/siRNA co-delivery nanocomplexes mitigate early-stage neutrophil recruitment for the anti-inflammatory treatment of myocardial ischemia reperfusion injury. Acta Biomater, 143:344–355. https://doi.org/10.1016/j.actbio.2022.02.018
Iantorno M, Campia U, di Daniele N, et al., 2014. Obesity, inflammation and endothelial dysfunction. J Biol Regul Homeost Agents, 28(2):169–176.
Jaganjac M, Cipak A, Schaur RJ, et al., 2016. Pathophysiology of neutrophil-mediated extracellular redox reactions. Front Biosci (Landmark Ed), 21(4):839–855. https://doi.org/10.2741/4423
Kim J, Bae JS, 2016. Tumor-associated macrophages and neutrophils in tumor microenvironment. Mediators Inflamm, 2016:6058147. https://doi.org/10.1155/2016/6058147
Kumar A, 2014. An alternate pathophysiologic paradigm of sepsis and septic shock: implications for optimizing antimicrobial therapy. Virulence, 5(1):80–97. https://doi.org/10.4161/viru.26913
Kurepa J, Smalle JA, 2019. Oxidative stress-induced formation of covalently linked ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit dimer in tobacco plants. BMC Res Notes, 12:112. https://doi.org/10.1186/s13104-019-4153-z
Kurian AG, Singh RK, Lee JH, et al., 2022. Surface-engineered hybrid gelatin methacryloyl with nanoceria as reactive oxygen species responsive matrixes for bone therapeutics. ACS Appl Bio Mater, 5(3):1130–1138. https://doi.org/10.1021/acsabm.1c01189
Lambeth JD, 2004. NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol, 4(3):181–189. https://doi.org/10.1038/nri1312
Landry DW, Levin HR, Gallant EM, et al., 1997. Vasopressin deficiency contributes to the vasodilation of septic shock. Circulation, 95(5):1122–1125. https://doi.org/10.1161/01.cir.95.5.1122
Landskron G, de la Fuente M, Thuwajit P, et al., 2014. Chronic inflammation and cytokines in the tumor microenvironment. J Immunol Res, 2014:149185. https://doi.org/10.1155/2014/149185
Larsen FS, 2019. Artificial liver support in acute and acute-on-chronic liver failure. Curr Opin Crit Care, 25(2): 187–191. https://doi.org/10.1097/mcc.0000000000000584
Lee KS, Kim SR, Park SJ, et al., 2006. Hydrogen peroxide induces vascular permeability via regulation of vascular endothelial growth factor. Am J Respir Cell Mol Biol, 35(2):190–197. https://doi.org/10.1165/rcmb.2005-0482OC
Li F, Lang FF, Zhang HL, et al., 2016. Role of TFEB mediated autophagy, oxidative stress, inflammation, and cell death in endotoxin induced myocardial toxicity of young and aged mice. Oxid Med Cell Longev, 2016: 5380319. https://doi.org/10.1155/2016/5380319
Li JM, Shah AM, 2004. Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology. Am J Physiol Regul Integr Comp Physiol, 287(5):R1014–R1030. https://doi.org/10.1152/ajpregu.00124.2004
Li Q, Mao M, Qiu YL, et al., 2016. Key role of ROS in the process of 15-lipoxygenase/15-hydroxyeicosatetraenoiccid-induced pulmonary vascular remodeling in hypoxia pulmonary hypertension. PLoS ONE, 11(2):e0149164. https://doi.org/10.1371/journal.pone.0149164
Li Q, Zhong XF, Yao WC, et al., 2022. Inhibitor of glutamine metabolism V9302 promotes ROS-induced autophagic degradation of B7H3 to enhance antitumor immunity. J Biol Chem, 298(4):101753. https://doi.org/10.1016/j.jbc.2022.101753
Li XY, Fang P, Li YF, et al., 2016. Mitochondrial reactive oxygen species mediate lysophosphatidylcholine-induced endothelial cell activation. Arterioscler Thromb Vasc Biol, 36(6):1090–1100. https://doi.org/10.1161/atvbaha.115.306964
Liu H, Wu J, Yao JY, et al., 2017. The role of oxidative stress in decreased acetylcholinesterase activity at the neuromuscular junction of the diaphragm during sepsis. Oxid Med Cell Longev, 2017:9718615. https://doi.org/10.1155/2017/9718615
Livaditi O, Kotanidou A, Psarra A, et al., 2006. Neutrophil CD64 expression and serum IL-8: sensitive early markers of severity and outcome in sepsis. Cytokine, 36(5–6): 283–290. https://doi.org/10.1016/j.cyto.2007.02.007
Mariampillai K, Granger B, Amelin D, et al., 2018. Development of a new classification system for idiopathic inflammatory myopathies based on clinical manifestations and myositis-specific autoantibodies. JAMA Neurol, 75(12):1528–1537. https://doi.org/10.1001/jamaneurol.2018.2598
Marin-Esteban V, Turbica I, Dufour G, et al., 2012. Afa/Dr diffusely adhering Escherichia coli strain C1845 induces neutrophil extracellular traps that kill bacteria and damage human enterocyte-like cells. Infect Immun, 80(5):1891–1899. https://doi.org/10.1128/iai.00050-12
Martin L, Derwall M, Al Zoubi S, et al., 2019. The septic heart: current understanding of molecular mechanisms and clinical implications. Chest, 155(2):427–437. https://doi.org/10.1016/j.chest.2018.08.1037
McCracken JM, Allen LAH, 2014. Regulation of human neutrophil apoptosis and lifespan in health and disease. J Cell Death, 7:15–23. https://doi.org/10.4137/jcd.S11038
Mills EL, Kelly B, Logan A, et al., 2016. Succinate dehydrogenase supports metabolic repurposing of mitochondria to drive inflammatory macrophages. Cell, 167(2):457–470.e13. https://doi.org/10.1016/j.cell.2016.08.064
Morgan MJ, Liu ZG, 2011. Crosstalk of reactive oxygen species and NF-κB signaling. Cell Res, 21(1):103–115. https://doi.org/10.1038/cr.2010.178
Morrell ED, Kellum JA, Pastor-Soler NM, et al., 2014. Septic acute kidney injury: molecular mechanisms and the importance of stratification and targeting therapy. Crit Care, 18(5):501. https://doi.org/10.1186/s13054-014-0501-5
Ostermann M, Liu K, Kashani K, 2019. Fluid management in acute kidney injury. Chest, 156(3):594–603. https://doi.org/10.1016/j.chest.2019.04.004
Peerapornratana S, Manrique-Caballero CL, Gómez H, et al., 2019. Acute kidney injury from sepsis: current concepts, epidemiology, pathophysiology, prevention and treatment. Kidney Int, 96(5):1083–1099. https://doi.org/10.1016/j.kint.2019.05.026
Perl M, Lomas-Neira J, Chung CS, et al., 2008. Epithelial cell apoptosis and neutrophil recruitment in acute lung injury—a unifying hypothesis? What we have learned from small interfering RNAs. Mol Med, 14(7–8):465–475. https://doi.org/10.2119/2008-00011.Perl
Post EH, Kellum JA, Bellomo R, et al., 2017. Renal perfusion in sepsis: from macro- to microcirculation. Kidney Int, 91(1):45–60. https://doi.org/10.1016/j.kint.2016.07.032
Rea IM, Gibson DS, McGilligan V, et al., 2018. Age and age-related diseases: role of inflammation triggers and cytokines. Front Immunol, 9:586. https://doi.org/10.3389/fimmu.2018.00586
Rudd KE, Johnson SC, Agesa KM, et al., 2020. Global, regional, and national sepsis incidence and mortality, 1990–2017: analysis for the global burden of disease study. Lancet, 395(10219):200–211. https://doi.org/10.1016/s0140-6736(19)32989-7
Saffarzadeh M, Juenemann C, Queisser MA, et al., 2012. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLoS ONE, 7(2):e32366. https://doi.org/10.1371/journal.pone.0032366
Sakaguchi S, Furusawa S, 2006. Oxidative stress and septic shock: metabolic aspects of oxygen-derived free radicals generated in the liver during endotoxemia. FEMS Immunol Med Microbiol, 47(2):167–177. https://doi.org/10.1111/j.1574-695X.2006.00072.x
Singer M, 2014. The role of mitochondrial dysfunction in sepsis-induced multi-organ failure. Virulence, 5(1):66–72. https://doi.org/10.4161/viru.26907
Singer M, Deutschman CS, Seymour CW, et al., 2016. The third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA, 315(8):801–810. https://doi.org/10.1001/jama.2016.0287
Smith IO, Liu XH, Smith LA, et al., 2009. Nanostructured polymer scaffolds for tissue engineering and regenerative medicine. Wiley Interdiscip Rev Nanomed Nanobiotechnol, 1(2):226–236. https://doi.org/10.1002/wnan.26
Starczewska MH, Mon W, Shirley P, 2017. Anaesthesia in patients with liver disease. Curr Opin Anaesthesiol, 30(3): 392–398. https://doi.org/10.1097/aco.0000000000000470
Suresh K, Shimoda LA, 2017. Endothelial cell reactive oxygen species and Ca2+ signaling in pulmonary hypertension. In: Wang YX (Ed.), Pulmonary Vasculature Redox Signaling in Health and Disease. Springer, Cham, p.299–314. https://doi.org/10.1007/978-3-319-63245-2_18
Tan CY, Aziz M, Wang P, 2021. The vitals of nets. J Leukoc Biol, 110(4):797–808. https://doi.org/10.1002/JLB.3RU0620-375R
Tang GM, Yang HY, Chen J, et al., 2017. Metformin ameliorates sepsis-induced brain injury by inhibiting apoptosis, oxidative stress and neuroinflammation via the PI3K/Akt signaling pathway. Oncotarget, 8(58):97977–97989. https://doi.org/10.18632/oncotarget.20105
Thieblemont N, Wright HL, Edwards SW, et al., 2016. Human neutrophils in auto-immunity. Semin Immunol, 28(2): 159–173. https://doi.org/10.1016/j.smim.2016.03.004
Vaisbich MH, Pache de Faria Guimaraes L, Shimizu MHM, et al., 2011. Oxidative stress in cystinosis patients. Nephron Extra, 1(1):73–77. https://doi.org/10.1159/000331445
Wang JC, Bennett M, 2012. Aging and atherosclerosis: mechanisms, functional consequences, and potential therapeutics for cellular senescence. Circ Res, 111(2):245–259. https://doi.org/10.1161/circresaha.111.261388
Wang YX, Zang QS, Liu ZJ, et al., 2011. Regulation of VEGF-induced endothelial cell migration by mitochondrial reactive oxygen species. Am J Physiol Cell Physiol, 301(3): C695–C704. https://doi.org/10.1152/ajpcell.00322.2010
Wang Z, Holthoff JH, Seely KA, et al., 2012. Development of oxidative stress in the peritubular capillary microenvironment mediates sepsis-induced renal microcirculatory failure and acute kidney injury. Am J Pathol, 180(2): 505–516. https://doi.org/10.1016/j.ajpath.2011.10.011
Wilson CL, Jurk D, Fullard N, et al., 2015. NFκB1 is a suppressor of neutrophil-driven hepatocellular carcinoma. Nat Commun, 6:6818. https://doi.org/10.1038/ncomms7818
Winterbourn CC, Kettle AJ, Hampton MB, 2016. Reactive oxygen species and neutrophil function. Annu Rev Biochem, 85:765–792. https://doi.org/10.1146/annurev-biochem-060815-014442
Yan J, Li S, Li SL, 2014. The role of the liver in sepsis. Int Rev Immunol, 33(6):498–510. https://doi.org/10.3109/08830185.2014.889129
Yin R, Wang H, Li C, et al., 2022. Induction of apoptosis and autosis in cardiomyocytes by the combination of homocysteine and copper via NOX-mediated p62 expression. Cell Death Discov, 8:75. https://doi.org/10.1038/s41420-022-00870-4
Yu JJ, Auwerx J, 2010. Protein deacetylation by SIRT1: an emerging key post-translational modification in metabolic regulation. Pharmacol Res, 62(1):35–41. https://doi.org/10.1016/j.phrs.2009.12.006
Zanotti-Cavazzoni SL, Hollenberg SM, 2009. Cardiac dysfunction in severe sepsis and septic shock. Curr Opin Crit Care, 15(5):392–397. https://doi.org/10.1097/MCC.0b013e3283307a4e
Zarbato GF, de Souza Goldim MP, Giustina AD, et al., 2018. Dimethyl fumarate limits neuroinflammation and oxidative stress and improves cognitive impairment after polymicrobial sepsis. Neurotox Res, 34(3):418–430. https://doi.org/10.1007/s12640-018-9900-8
Zeng M, He WM, Li LJ, et al., 2015. Ghrelin attenuates sepsis-associated acute lung injury oxidative stress in rats. Inflammation, 38(2):683–690. https://doi.org/10.1007/s10753-014-9977-z
Zeng MY, Miralda I, Armstrong CL, et al., 2019. The roles of NADPH oxidase in modulating neutrophil effector responses. Mol Oral Microbiol, 34(2):27–38. https://doi.org/10.1111/omi.12252
Zhang XL, Yu L, Xu HX, 2016. Lysosome calcium in ROS regulation of autophagy. Autophagy, 12(10):1954–1955. https://doi.org/10.1080/15548627.2016.1212787
Zhang ZY, Zhang H, Chen R, et al., 2018. Oral supplementation with ursolic acid ameliorates sepsis-induced acute kidney injury in a mouse model by inhibiting oxidative stress and inflammatory responses. Mol Med Rep, 17(5): 7142–7148. https://doi.org/10.3892/mmr.2018.8767
Zheng JL, Yuan SS, Wu CW, et al., 2016. Acute exposure to waterborne cadmium induced oxidative stress and immunotoxicity in the brain, ovary and liver of zebrafish (Danio rerio). Aquat Toxicol, 180:36–44. https://doi.org/10.1016/j.aquatox.2016.09.012
Zhong WH, Qian KJ, Xiong JB, et al., 2016. Curcumin alleviates lipopolysaccharide induced sepsis and liver failure by suppression of oxidative stress-related inflammation via PI3K/AKT and NF-κB related signaling. Biomed Pharmacother, 83:302–313. https://doi.org/10.1016/j.biopha.2016.06.036
Zhu LS, Luo D, Liu Y, 2020. Effect of the nano/microscale structure of biomaterial scaffolds on bone regeneration. Int J Oral Sci, 12:6. https://doi.org/10.1038/s41368-020-0073-y
Zhu W, Lu Q, Wan L, et al., 2016. Sodium tanshinone II A sulfonate ameliorates microcirculatory disturbance of small intestine by attenuating the production of reactie oxygen species in rats with sepsis. Chin J Integr Med, 22(10):745–751. https://doi.org/10.1007/s11655-015-2083-8
Zorov DB, Juhaszova M, Sollott SJ, 2014. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol Rev, 94(3):909–950. https://doi.org/10.1152/physrev.00026.2013
Acknowledgments
We would like to thank the medical and nursing staff from the Department of Critical Care Medicine, Beijing Ditan Hospital, Beijing, China, for their valuable comments during the course of this study.
Author information
Authors and Affiliations
Contributions
Jiaqi LU designed and wrote the manuscript. Jingyuan LIU participated in searching and summarizing the relevant literature. Ang LI provided the theme and design, and edited the manuscript. All authors have read and approved the final manuscript.
Corresponding author
Additional information
Compliance with ethics guidelines
Jiaqi LU, Jingyuan LIU, and Ang LI declare that they have no conflict of interest.
This article does not contain any studies with human or animal subjects performed by the authors.
Rights and permissions
About this article
Cite this article
Lu, J., Liu, J. & Li, A. Roles of neutrophil reactive oxygen species (ROS) generation in organ function impairment in sepsis. J. Zhejiang Univ. Sci. B 23, 437–450 (2022). https://doi.org/10.1631/jzus.B2101075
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1631/jzus.B2101075