Systemic inflammatory response syndrome is triggered by mitochondrial damage (Review)
- Authors:
- Can Kong
- Wei Song
- Tao Fu
-
Affiliations: Department of Gastrointestinal Surgery II, Renmin Hospital of Wuhan University, Wuhan, Hubei 430060, P.R. China - Published online on: March 1, 2022 https://doi.org/10.3892/mmr.2022.12663
- Article Number: 147
-
Copyright: © Kong et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Itagaki K, Riça I, Konecna B, Kim HI, Park J, Kaczmarek E and Hauser CJ: Role of mitochondria-derived danger signals released after injury in systemic inflammation and sepsis. Antioxid Redox Signal. 35:1273–1290. 2021. View Article : Google Scholar : PubMed/NCBI | |
Kang J, Kim S, Cho H and Lee S: DAMPs activating innate immune responses in sepsis. Ageing Res Rev. 24:54–65. 2015. View Article : Google Scholar : PubMed/NCBI | |
Khwaja B, Thankam FG and Agrawal DK: Mitochondrial DAMPs and altered mitochondrial dynamics in OxLDL burden in atherosclerosis. Mol Cell Biochem. 476:1915–1928. 2021. View Article : Google Scholar : PubMed/NCBI | |
Schneck E, Edinger F, Hecker M, Sommer N, Pak O, Weissmann N, Hecker A, Reichert M, Markmann M, Sander M and Koch C: Blood levels of free-circulating mitochondrial DNA in septic shock and postsurgical systemic inflammation and its influence on coagulation: A secondary analysis of a prospective observational study. J Clin Med. 9:20562020. View Article : Google Scholar : PubMed/NCBI | |
Jiménez-Sousa MA, Tamayo E, Guzmán-Fulgencio M, Heredia M, Fernández-Rodríguez A, Gómez E, Almansa R, Gómez-Herreras JI, García-Álvarez M, Gutiérrez-Junco S, et al: Mitochondrial DNA haplogroups are associated with severe sepsis and mortality in patients who underwent major surgery. J Infect. 70:20–29. 2015. View Article : Google Scholar : PubMed/NCBI | |
Hu Q, Ren J, Wu J, Li G, Wu X, Liu S, Wang G, Gu G and Li J: Elevated levels of plasma mitochondrial DNA are associated with clinical outcome in intra-abdominal infections caused by severe trauma. Surg Infect (Larchmt). 18:610–618. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kung CT, Hsiao SY, Tsai TC, Su CM, Chang WN, Huang CR, Wang HC, Lin WC, Chang HW, Lin YJ, et al: Plasma nuclear and mitochondrial DNA levels as predictors of outcome in severe sepsis patients in the emergency room. J Transl Med. 10:1302012. View Article : Google Scholar : PubMed/NCBI | |
Li S, Hu Q, Huang J, Wu X and Ren J: Mitochondria-derived damage-associated molecular patterns in sepsis: From bench to bedside. Oxid Med Cell Longev. 2019:69148492019. View Article : Google Scholar : PubMed/NCBI | |
West AP and Shadel GS: Mitochondrial DNA in innate immune responses and inflammatory pathology. Nat Rev Immunol. 17:363–375. 2017. View Article : Google Scholar : PubMed/NCBI | |
Ryoo IG and Kwak MK: Regulatory crosstalk between the oxidative stress-related transcription factor Nfe2l2/Nrf2 and mitochondria. Toxicol Appl Pharmacol. 359:24–33. 2018. View Article : Google Scholar : PubMed/NCBI | |
Pihán P, Carreras-Sureda A and Hetz C: BCL-2 family: Integrating stress responses at the ER to control cell demise. Cell Death Differ. 24:1478–1487. 2017. View Article : Google Scholar : PubMed/NCBI | |
Picca A, Calvani R, Coelho-Junior HJ and Marzetti E: Cell death and inflammation: The role of mitochondria in health and disease. Cells. 10:5372021. View Article : Google Scholar : PubMed/NCBI | |
Bock FJ and Tait SWG: Mitochondria as multifaceted regulators of cell death. Nat Rev Mol Cell Biol. 21:85–100. 2020. View Article : Google Scholar : PubMed/NCBI | |
Campbell KJ and Tait SWG: Targeting BCL-2 regulated apoptosis in cancer. Open Biol. 8:1800022018. View Article : Google Scholar : PubMed/NCBI | |
Hu Q, Ren H, Ren J, Liu Q, Wu J, Wu X, Li G, Wang G, Gu G, Guo K, et al: Released mitochondrial DNA following intestinal ischemia reperfusion induces the inflammatory response and gut barrier dysfunction. Sci Rep. 8:73502018. View Article : Google Scholar : PubMed/NCBI | |
Wenceslau CF, Szasz T, McCarthy CG, Baban B, NeSmith E and Webb RC: Mitochondrial N-formyl peptides cause airway contraction and lung neutrophil infiltration via formyl peptide receptor activation. Pulm Pharmacol Ther. 37:49–56. 2016. View Article : Google Scholar : PubMed/NCBI | |
Hepokoski M, Wang J, Li K, Li Y, Gupta P, Mai T, Moshensky A, Alotaibi M, Crotty Alexander LE, Malhotra A and Singh P: Altered lung metabolism and mitochondrial DAMPs in lung injury due to acute kidney injury. Am J Physiol Lung Cell Mol Physiol. 320:L821–L831. 2021. View Article : Google Scholar : PubMed/NCBI | |
McIlroy DJ, Bigland M, White AE, Hardy BM, Lott N, Smith DW and Balogh ZJ: Cell necrosis-independent sustained mitochondrial and nuclear DNA release following trauma surgery. J Trauma Acute Care Surg. 78:282–288. 2015. View Article : Google Scholar : PubMed/NCBI | |
Pencovich N, Nevo N, Weiser R, Bonder E, Bogoch Y and Nachmany I: Postoperative rise of circulating mitochondrial DNA is associated with inflammatory response in patients following pancreaticoduodenectomy. Eur Surg Res. 62:18–24. 2021. View Article : Google Scholar : PubMed/NCBI | |
Csóka B, Németh ZH, Szabó I, Davies DL, Varga ZV, Pálóczi J, Falzoni S, Di Virgilio F, Muramatsu R, Yamashita T, et al: Macrophage P2X4 receptors augment bacterial killing and protect against sepsis. JCI Insight. 3:e994312018. View Article : Google Scholar : PubMed/NCBI | |
Csóka B, Németh ZH, Törő G, Idzko M, Zech A, Koscsó B, Spolarics Z, Antonioli L, Cseri K, Erdélyi K, et al: Extracellular ATP protects against sepsis through macrophage P2X7 purinergic receptors by enhancing intracellular bacterial killing. FASEB J. 29:3626–3637. 2015. View Article : Google Scholar : PubMed/NCBI | |
Konecna B, Park J, Kwon WY, Vlkova B, Zhang Q, Huang W, Kim HI, Yaffe MB, Otterbein LE, Itagaki K and Hauser CJ: Monocyte exocytosis of mitochondrial danger-associated molecular patterns in sepsis suppresses neutrophil chemotaxis. J Trauma Acute Care Surg. 90:46–53. 2021. View Article : Google Scholar : PubMed/NCBI | |
Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, Junger W, Brohi K, Itagaki K and Hauser CJ: Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature. 464:104–107. 2010. View Article : Google Scholar : PubMed/NCBI | |
Kaczmarek E, Hauser CJ, Kwon WY, Riça I, Chen L, Sandler N, Otterbein LE, Campbell Y, Cook CH, Yaffe MB, et al: A subset of five human mitochondrial formyl peptides mimics bacterial peptides and functionally deactivates human neutrophils. J Trauma Acute Care. 85:936–943. 2018. View Article : Google Scholar : PubMed/NCBI | |
Fang C, Wei X and Wei Y: Mitochondrial DNA in the regulation of innate immune responses. Protein Cell. 7:11–16. 2016. View Article : Google Scholar : PubMed/NCBI | |
Wu Z, Sainz AG and Shadel GS: Mitochondrial DNA: Cellular genotoxic stress sentinel. Trends Biochem Sci. 46:812–821. 2021. View Article : Google Scholar : PubMed/NCBI | |
Riley JS and Tait SW: Mitochondrial DNA in inflammation and immunity. EMBO Rep. 21:e497992020. View Article : Google Scholar : PubMed/NCBI | |
Garrabou G, Morén C, López S, Tobías E, Cardellach F, Miró O and Casademont J: The effects of sepsis on mitochondria. J Infect Dis. 205:392–400. 2012. View Article : Google Scholar : PubMed/NCBI | |
Bonekamp NA and Larsson NG: SnapShot: Mitochondrial nucleoid. Cell. 172:388–388.e1. 2018. View Article : Google Scholar : PubMed/NCBI | |
van der Slikke EC, Star BS, van Meurs M, Henning RH, Moser J and Bouma HR: Sepsis is associated with mitochondrial DNA damage and a reduced mitochondrial mass in the kidney of patients with sepsis-AKI. Crit Care. 25:362021. View Article : Google Scholar : PubMed/NCBI | |
Nakahira K, Kyung SY, Rogers AJ, Gazourian L, Youn S, Massaro AF, Quintana C, Osorio JC, Wang Z, Zhao Y, et al: Circulating mitochondrial DNA in patients in the ICU as a marker of mortality: Derivation and validation. PLoS Med. 10:e10015772013. View Article : Google Scholar : PubMed/NCBI | |
Busani S, De Biasi S, Nasi M, Paolini A, Venturelli S, Tosi M, Girardis M and Cossarizza A: Increased plasma levels of mitochondrial DNA and normal inflammasome gene expression in monocytes characterize patients with septic shock due to multidrug resistant bacteria. Front Immunol. 11:7682020. View Article : Google Scholar : PubMed/NCBI | |
Zhang WZ, Hoffman KL, Schiffer KT, Oromendia C, Rice MC, Barjaktarevic I, Peters SP, Putcha N, Bowler RP, Wells JM, et al: Association of plasma mitochondrial DNA with COPD severity and progression in the SPIROMICS cohort. Respir Res. 22:1262021. View Article : Google Scholar : PubMed/NCBI | |
Faust HE, Reilly JP, Anderson BJ, Ittner CAG, Forker CM, Zhang P, Weaver BA, Holena DN, Lanken PN, Christie JD, et al: Plasma mitochondrial DNA levels are associated with ARDS in trauma and sepsis patients. Chest. 157:67–76. 2020. View Article : Google Scholar : PubMed/NCBI | |
McIlroy DJ, Minahan K, Keely S, Lott N, Hansbro P, Smith DW and Balogh ZJ: Reduced deoxyribonuclease enzyme activity in response to high postinjury mitochondrial DNA concentration provides a therapeutic target for systemic inflammatory response syndrome. J Trauma Acute Care Surg. 85:354–358. 2018. View Article : Google Scholar : PubMed/NCBI | |
Boyapati RK, Dorward DA, Tamborska A, Kalla R, Ventham NT, Doherty MK, Whitfield PD, Gray M, Loane J, Rossi AG, et al: Mitochondrial DNA is a pro-inflammatory damage-associated molecular pattern released during active IBD. Inflamm Bowel Dis. 24:2113–2122. 2018. View Article : Google Scholar : PubMed/NCBI | |
Bliksøen M, Mariero LH, Torp MK, Baysa A, Ytrehus K, Haugen F, Seljeflot I, Vaage J, Valen G and Stensløkken KO: Extracellular mtDNA activates NF-κB via toll-like receptor 9 and induces cell death in cardiomyocytes. Basic Res Cardiol. 111:422016. View Article : Google Scholar : PubMed/NCBI | |
Simmons JD, Lee Y, Mulekar S, Kuck JL, Brevard SB, Gonzalez RP, Gillespie MN and Richards WO: Elevated levels of plasma mitochondrial DNA DAMPs are linked to clinical outcome in severely injured human subjects. Ann Surg. 258:591–598. 2013. View Article : Google Scholar : PubMed/NCBI | |
Harrington JS, Choi AM and Nakahira K: Mitochondrial DNA in Sepsis. Curr Opin Crit Care. 23:284–290. 2017. View Article : Google Scholar : PubMed/NCBI | |
Liu Q, Zhang D, Hu D, Zhou X and Zhou Y: The role of mitochondria in NLRP3 inflammasome activation. Mol Immunol. 103:115–124. 2018. View Article : Google Scholar : PubMed/NCBI | |
Zhou L and Tan L: Role of mitochondrial DNA in acute lung injury/acute respiratory distress syndrome induced by sepsis. Zhonghua Wei Zhong Bing Ji Jiu Yi Xue. 32:253–256. 2020.(In Chinese). PubMed/NCBI | |
Shepard CR: TLR9 in MAFLD and NASH: At the intersection of inflammation and metabolism. Front Endocrinol (Lausanne). 11:6136392021. View Article : Google Scholar : PubMed/NCBI | |
Medeiros TC and Graef M: Autophagy determines mtDNA copy number dynamics during starvation. Autophagy. 15:178–179. 2019. View Article : Google Scholar : PubMed/NCBI | |
Pickles S, Vigié P and Youle RJ: Mitophagy and quality control mechanisms in mitochondrial maintenance. Curr Biol. 28:R170–R185. 2018. View Article : Google Scholar : PubMed/NCBI | |
Zhang JZ, Liu Z, Liu J, Ren JX and Sun TS: Mitochondrial DNA induces inflammation and increases TLR9/NF-κB expression in lung tissue. Int J Mol Med. 33:817–824. 2014. View Article : Google Scholar : PubMed/NCBI | |
Lin JY, Jing R, Lin F, Ge WY, Dai HJ and Pan L: High tidal volume induces mitochondria damage and releases mitochondrial DNA to aggravate the ventilator-induced lung injury. Front Immunol. 9:14772018. View Article : Google Scholar : PubMed/NCBI | |
Jing R, Hu ZK, Lin F, He S, Zhang SS, Ge WY, Dai HJ, Du XK, Lin JY and Pan LH: Mitophagy-mediated mtDNA release aggravates stretching-induced inflammation and lung epithelial cell injury via the TLR9/MyD88/NF-κB pathway. Front Cell Dev Biol. 8:8192020. View Article : Google Scholar : PubMed/NCBI | |
Bueno M, Lai YC, Romero Y, Brands J, St Croix CM, Kamga C, Corey C, Herazo-Maya JD, Sembrat J, Lee JS, et al: PINK1 deficiency impairs mitochondrial homeostasis and promotes lung fibrosis. J Clin Invest. 125:521–538. 2015. View Article : Google Scholar : PubMed/NCBI | |
Shimada K, Crother TR, Karlin J, Dagvadorj J, Chiba N, Chen S, Ramanujan VK, Wolf AJ, Vergnes L, Ojcius DM, et al: Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity. 36:401–414. 2012. View Article : Google Scholar : PubMed/NCBI | |
Sok SPM, Ori D, Wada A, Okude H, Kawasaki T, Momota M, Nagoor NH and Kawai T: 1′-Acetoxychavicol acetate inhibits NLRP3-dependent inflammasome activation via mitochondrial ROS suppression. Int Immunol. 33:373–386. 2021. View Article : Google Scholar : PubMed/NCBI | |
Li S, Li H, Zhang YL, Xin QL, Guan ZQ, Chen X, Zhang XA, Li XK, Xiao GF, Lozach PY, et al: SFTSV infection induces BAK/BAX-dependent mitochondrial DNA release to trigger NLRP3 inflammasome activation. Cell Rep. 30:4370–4385.e7. 2020. View Article : Google Scholar : PubMed/NCBI | |
Xian H, Liu Y, Rundberg Nilsson A, Gatchalian R, Crother TR, Tourtellotte WG, Zhang Y, Aleman-Muench GR, Lewis G, et al: Metformin inhibition of mitochondrial ATP and DNA synthesis abrogates NLRP3 inflammasome activation and pulmonary inflammation. Immunity. 54:1463–1477. 2021. View Article : Google Scholar : PubMed/NCBI | |
Wu Y, Hao C, Liu X, Han G, Yin J, Zou Z, Zhou J and Xu C: MitoQ protects against liver injury induced by severe burn plus delayed resuscitation by suppressing the mtDNA-NLRP3 axis. Int Immunopharmacol. 80:1061892020. View Article : Google Scholar : PubMed/NCBI | |
Ishikawa H and Barber GN: STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature. 455:674–678. 2008. View Article : Google Scholar : PubMed/NCBI | |
Bryant JD, Lei Y, VanPortfliet JJ, Winters AD and West AP: Assessing mitochondrial DNA release into the cytosol and subsequent activation of innate immune-related pathways in mammalian cells. Curr Protoc. 2:e3722022. View Article : Google Scholar : PubMed/NCBI | |
Luo W, Wang Y, Zhang L, Ren P, Zhang C, Li Y, Azares AR, Zhang M, Guo J, Ghaghada KB, et al: Critical role of cytosolic DNA and its sensing adaptor STING in aortic degeneration, dissection, and rupture. Circulation. 141:42–66. 2020. View Article : Google Scholar : PubMed/NCBI | |
Wan D, Jiang W and Hao J: Research advances in how the cGAS-STING pathway controls the cellular inflammatory response. Front Immunol. 11:6152020. View Article : Google Scholar : PubMed/NCBI | |
Hu Q, Ren H, Li G, Wang D, Zhou Q, Wu J, Zheng J, Huang J, Slade DA, Wu X and Ren J: STING-mediated intestinal barrier dysfunction contributes to lethal sepsis. Ebiomedicine. 41:497–508. 2019. View Article : Google Scholar : PubMed/NCBI | |
Vringer E and Tait SW: Mitochondria and inflammation: Cell death heats up. Front Cell Dev Biol. 7:1002019. View Article : Google Scholar : PubMed/NCBI | |
Comish PB, Liu M, Huebinger R, Carlson D, Kang R and Tang D: The cGAS-STING pathway connects mitochondrial damage to inflammation in burn-induced acute lung injury in rat. Burns. 48:168–175. 2022. View Article : Google Scholar : PubMed/NCBI | |
Liu Q, Wu J, Zhang X, Li X, Wu X, Zhao Y and Ren J: Circulating mitochondrial DNA-triggered autophagy dysfunction via STING underlies sepsis-related acute lung injury. Cell Death Dis. 12:6732021. View Article : Google Scholar : PubMed/NCBI | |
Sliter DA, Martinez J, Hao L, Chen X, Sun N, Fischer TD, Burman JL, Li Y, Zhang Z, Narendra DP, et al: Parkin and PINK1 mitigate STING-induced inflammation. Nature. 561:258–262. 2018. View Article : Google Scholar : PubMed/NCBI | |
Banoth B and Cassel SL: Mitochondria in innate immune signaling. Transl Res. 202:52–68. 2018. View Article : Google Scholar : PubMed/NCBI | |
Ye RD, Boulay F, Wang JM, Dahlgren C, Gerard C, Parmentier M, Serhan CN and Murphy PM: International Union of Basic and Clinical Pharmacology. LXXIII. Nomenclature for the formyl peptide receptor (FPR) family. Pharmacol Rev. 61:119–161. 2009. View Article : Google Scholar : PubMed/NCBI | |
He HQ and Ye RD: The formyl peptide receptors: Diversity of ligands and mechanism for recognition. Molecules. 22:4552017. View Article : Google Scholar : PubMed/NCBI | |
Wenceslau CF, McCarthy CG, Goulopoulou S, Szasz T, NeSmith EG and Webb RC: Mitochondrial-derived N-formyl peptides: Novel links between trauma, vascular collapse and sepsis. Med Hypotheses. 81:532–535. 2013. View Article : Google Scholar : PubMed/NCBI | |
Wenceslau CF, McCarthy CG, Szasz T, Goulopoulou S and Webb RC: Mitochondrial N-formyl peptides induce cardiovascular collapse and sepsis-like syndrome. Am J Physiol Heart Circ Physiol. 308:H768–H777. 2015. View Article : Google Scholar : PubMed/NCBI | |
Dorward DA, Lucas CD, Doherty MK, Chapman GB, Scholefield EJ, Conway Morris A, Felton JM, Kipari T, Humphries DC, Robb CT, et al: Novel role for endogenous mitochondrial formylated peptide-driven formyl peptide receptor 1 signalling in acute respiratory distress syndrome. Thorax. 72:928–936. 2017. View Article : Google Scholar : PubMed/NCBI | |
Ueda S, Shimasaki M, Ichiseki T, Hirata H, Kawahara N and Ueda Y: Mitochondrial transcription factor A added to osteocytes in a stressed environment has a cytoprotective effect. Int J Med Sci. 17:1293–1299. 2020. View Article : Google Scholar : PubMed/NCBI | |
Schindler SM, Frank MG, Annis JL, Maier SF and Klegeris A: Pattern recognition receptors mediate pro-inflammatory effects of extracellular mitochondrial transcription factor A (TFAM). Mol Cell Neurosci. 89:71–79. 2018. View Article : Google Scholar : PubMed/NCBI | |
West AP, Khoury-Hanold W, Staron M, Tal MC, Pineda CM, Lang SM, Bestwick M, Duguay BA, Raimundo N, MacDuff DA, et al: Mitochondrial DNA stress primes the antiviral innate immune response. Nature. 520:553–557. 2015. View Article : Google Scholar : PubMed/NCBI | |
van der Flier LG and Clevers H: Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol. 71:241–260. 2009. View Article : Google Scholar : PubMed/NCBI | |
Rath E, Moschetta A and Haller D: Mitochondrial function-gatekeeper of intestinal epithelial cell homeostasis. Nat Rev Gastroenterol Hepatol. 15:497–516. 2018. View Article : Google Scholar : PubMed/NCBI | |
Zhang X, Wu J, Liu Q, Li X, Li S, Chen J, Hong Z, Wu X, Zhao Y and Ren J: mtDNA-STING pathway promotes necroptosis-dependent enterocyte injury in intestinal ischemia reperfusion. Cell Death Dis. 11:10502020. View Article : Google Scholar : PubMed/NCBI | |
Druml W: Intestinal cross-talk: The gut as motor of multiple organ failure. Med Klin Intensivmed Notfmed. 113:470–477. 2018.(In German). View Article : Google Scholar : PubMed/NCBI | |
Hu Q, Ren J, Li G, Wu J, Wu X, Wang G, Gu G, Ren H, Hong Z and Li J: The mitochondrially targeted antioxidant MitoQ protects the intestinal barrier by ameliorating mitochondrial DNA damage via the Nrf2/ARE signaling pathway. Cell Death Dis. 9:4032018. View Article : Google Scholar : PubMed/NCBI | |
Chelakkot C, Ghim J and Ryu SH: Mechanisms regulating intestinal barrier integrity and its pathological implications. Exp Mol Med. 50:1–9. 2018. View Article : Google Scholar : PubMed/NCBI | |
Marchiando AM, Shen L, Graham WV, Weber CR, Schwarz BT, Austin JN II, Raleigh DR, Guan Y, Watson AJ, Montrose MH and Turner JR: Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J Cell Biol. 189:111–126. 2010. View Article : Google Scholar : PubMed/NCBI | |
Odenwald MA and Turner JR: The intestinal epithelial barrier: A therapeutic target? Nat Rev Gastroenterol Hepatol. 14:9–21. 2017. View Article : Google Scholar : PubMed/NCBI | |
Assimakopoulos SF, Triantos C, Thomopoulos K, Fligou F, Maroulis I, Marangos M and Gogos CA: Gut-origin sepsis in the critically ill patient: Pathophysiology and treatment. Infection. 46:751–760. 2018. View Article : Google Scholar : PubMed/NCBI | |
Zhou M, Aziz M and Wang P: Damage-associated molecular patterns as double-edged swords in sepsis. Antioxid Redox Signal. 35:1308–1323. 2021. View Article : Google Scholar : PubMed/NCBI |