线粒体DNA在先天性免疫中的作用

doi:10.11843/j.issn.0366-6964.2021.02.002

Abstract

Abstract: Mitochondria are important cellular organelles involved in many different functions and are known as the energy factory of cells. Mitochondria maintain their genetic material, mitochondrial DNA (mtDNA), mtDNA is widely known for its role in oxidative phosphorylation. In recent years, increasing researches show that mtDNA acts as an agonist of the innate immune system and plays an important role in the pathogen infection and the pathologic development of inflammatory diseases. On entering the cytoplasm or extracellular environment, mtDNA can engage multiple pattern-recognition receptors of the innate immune system to trigger pro-inflammatory cytokines secretion and type Ⅰ interferon response. This review summarizes the mechanism of mtDNA to activate innate immunity and its role in the pathogenesis of infection and related diseases, the purpose is to provide theoretical basis for further research on the role and mechanism of mtDNA in pathogen infection and related diseases.

Key words: mitochondrial DNA, innate immunity, infection, inflammatory diseases

CLC Number:

S852.42

SONG Yinjuan, LIAO Yi, ZHOU Xiangmei. The Role of Mitochondrial DNA in Innate Immunity[J]. Acta Veterinaria et Zootechnica Sinica, 2021, 52(2): 286-299.

References 97

[1]	WEST A P, SHADEL G S, GHOSH S. Mitochondria in innate immune responses[J]. Nat Rev Immunol, 2011, 11(6):389-402.
[2]	FUKATA M, VAMADEVAN A S, ABREU M T. Toll-like receptors (TLRs) and nod-like receptors (NLRs) in inflammatory disorders[J]. Semin Immunol, 2009, 21(4):242-253.
[3]	MARAKALALA M J, NDLOVU H. Signaling C-type lectin receptors in antimycobacterial immunity[J]. PLoS Pathog, 2017, 13(6):e1006333.
[4]	GALLUZZI L, KEPP O, KROEMER G. Mitochondria:master regulators of danger signalling[J]. Nat Rev Mol Cell Biol, 2012, 13(12):780-788.
[5]	LANE N, MARTIN W. The energetics of genome complexity[J]. Nature, 2010, 467(7318):929-934.
[6]	MCINERNEY J, PISANI D, O'CONNELL M J. The ring of life hypothesis for eukaryote origins is supported by multiple kinds of data[J]. Philos Trans R Soc Lond B Biol Sci, 2015, 370(1678):20140323.
[7]	SHADEL G S, CLAYTON D A. Mitochondrial DNA maintenance in vertebrates[J]. Annu Rev Biochem, 1997, 66:409-435.
[8]	SHADEL G S, HORVATH T L. Mitochondrial ROS signaling in organismal homeostasis[J]. Cell, 2015, 163(3):560-569.
[9]	WEINBERG S E, SENA L A, CHANDEL N S. Mitochondria in the regulation of innate and adaptive immunity[J]. Immunity, 2015, 42(3):406-417.
[10]	WEST A P. Mitochondrial dysfunction as a trigger of innate immune responses and inflammation[J]. Toxicology, 2017, 391:54-63.
[11]	WANG L Y. Mitochondrial purine and pyrimidine metabolism and beyond[J]. Nucleosides Nucleotides Nucleic Acids, 2016, 35(10-12):578-594.
[12]	THEILEN N T, KUNKEL G H, TYAGI S C. The role of exercise and TFAM in preventing skeletal muscle atrophy[J]. J Cell Physiol, 2017, 232(9):2348-2358.
[13]	ZHONG Z Y, LIANG S, SANCHEZ-LOPEZ E, et al. New mitochondrial DNA synthesis enables NLRP3 inflammasome activation[J]. Nature, 2018, 560(7717):198-203.
[14]	SONG Y J, HUSSAIN T, WANG J, et al. Mitochondrial transcription factor a regulates Mycobacterium bovis-induced IFN-β production by modulating mitochondrial DNA replication in macrophages[J]. J Infect Dis, 2020, 221(3):438-448.
[15]	WEST A P, SHADEL G S. Mitochondrial DNA in innate immune responses and inflammatory pathology[J]. Nat Rev Immunol, 2017, 17(6):363-375.
[16]	MEHTA M M, WEINBERG S E, CHANDEL N S. Mitochondrial control of immunity:beyond ATP[J]. Nat Rev Immunol, 2017, 17(10):608-620.
[17]	YASUKAWA T, KANG D C. An overview of mammalian mitochondrial DNA replication mechanisms[J]. J Biochem, 2018, 164(3):183-193.
[18]	DHIR A, DHIR S, BOROWSKI L S, et al. Mitochondrial double-stranded RNA triggers antiviral signalling in humans[J]. Nature, 2018, 560(7717):238-242.
[19]	KANG D C, KIM S H, HAMASAKI N. Mitochondrial transcription factor A (TFAM):roles in maintenance of mtDNA and cellular functions[J]. Mitochondrion, 2007, 7(1-2):39-44.
[20]	BESTWICK M L, SHADEL G S. Accessorizing the human mitochondrial transcription machinery[J]. Trends Biochem Sci, 2013, 38(6):283-291.
[21]	ANDREEVA L, HILLER B, KOSTREWA D, et al. cGAS senses long and HMGB/TFAM-bound U-turn DNA by forming protein-DNA ladders[J]. Nature, 2017, 549(7672):394-398.
[22]	JULIAN M W, SHAO G H, BAO S Y, et al. Mitochondrial transcription factor a serves as a danger signal by augmenting plasmacytoid dendritic cell responses to DNA[J]. J Immunol, 2012, 189(1):433-443.
[23]	COLLINS L V, HAJIZADEH S, HOLME E, et al. Endogenously oxidized mitochondrial DNA induces in vivo and in vitro inflammatory responses[J]. J Leukoc Biol, 2004, 75(6):995-1000.
[24]	BARBALAT R, EWALD S E, MOUCHESS M L, et al. Nucleic acid recognition by the innate immune system[J]. Annu Rev Immunol, 2011, 29:185-214.
[25]	LATZ E, SCHOENEMEYER A, VISINTIN A, et al. TLR9 signals after translocating from the ER to CpG DNA in the lysosome[J]. Nat Immunol, 2004, 5(2):190-198.
[26]	ZHANG Q, ITAGAKI K, HAUSER C J. Mitochondrial DNA is released by shock and activates neutrophils via p38 map kinase[J]. Shock, 2010, 34(1):55-59.
[27]	ZHANG Q, RAOOF M, CHEN Y, et al. Circulating mitochondrial DAMPs cause inflammatory responses to injury[J]. Nature, 2010, 464(7285):104-107.
[28]	OKA T, HIKOSO S, YAMAGUCHI O, et al. Mitochondrial DNA that escapes from autophagy causes inflammation and heart failure[J]. Nature, 2012, 485(7397):251-255.
[29]	CAIELLI S, ATHALE S, DOMIC B, et al. Oxidized mitochondrial nucleoids released by neutrophils drive type I interferon production in human lupus[J]. J Exp Med, 2016, 213(5):697-713.
[30]	WEN H T, MIAO E A, TING J P Y. Mechanisms of NOD-like receptor-associated inflammasome activation[J]. Immunity, 2013, 39(3):432-441.
[31]	MAN S M, KANNEGANTI T D. Converging roles of caspases in inflammasome activation, cell death and innate immunity[J]. Nat Rev Immunol, 2016, 16(1):7-21.
[32]	ELLIOTT E I, SUTTERWALA F S. Initiation and perpetuation of NLRP3 inflammasome activation and assembly[J]. Immunol Rev, 2015, 265(1):35-52.
[33]	NAKAHIRA K, HASPEL J A, RATHINAM V A K, et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome[J]. Nat Immunol, 2011, 12(3):222-230.
[34]	SHIMADA K, CROTHER T R, KARLIN J, et al. Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis[J]. Immunity, 2012, 36(3):401-414.
[35]	JABIR M S, HOPKINS L, RITCHIE N D, et al. Mitochondrial damage contributes to Pseudomonas aeruginosa activation of the inflammasome and is downregulated by autophagy[J]. Autophagy, 2015, 11(1):166-182.
[36]	BAE J H, JO Ⅱ S, KIM S J, et al. Circulating cell-free mtDNA contributes to AIM2 inflammasome-mediated chronic inflammation in patients with type 2 diabetes[J]. Cells, 2019, 8(4):328.
[37]	TUMURKHUU G, SHIMADA K, DAGVADORJ J, et al. Ogg1-dependent DNA repair regulates NLRP3 inflammasome and prevents atherosclerosis[J]. Circ Res, 2016, 119(6):e76-e90.
[38]	MCARTHUR K, WHITEHEAD L W, HEDDLESTON J M, et al. BAK/BAX macropores facilitate mitochondrial herniation and mtDNA efflux during apoptosis[J]. Science, 2018, 359(6378):eaao6047.
[39]	ALLAM R, LAWLOR K E, YU E C W, et al. Mitochondrial apoptosis is dispensable for NLRP3 inflammasome activation but non-apoptotic caspase-8 is required for inflammasome priming[J]. EMBO Rep, 2014, 15(9):982-990.
[40]	HUANG L S, HONG Z G, WU W, et al. mtDNA activates cGAS signaling and suppresses the YAP-mediated endothelial cell proliferation program to promote inflammatory injury[J]. Immunity, 2020, 52(3):475-486.e5.
[41]	YU J J, NAGASU H, MURAKAMI T, et al. Inflammasome activation leads to Caspase-1-dependent mitochondrial damage and block of mitophagy[J]. Proc Natl Acad Sci U S A, 2014, 111(43):15514-15519.
[42]	ZHONG Z Y, UMEMURA A, SANCHEZ-LOPEZ E, et al. NF-κB restricts inflammasome activation via elimination of damaged mitochondria[J]. Cell, 2016, 164(5):896-910.
[43]	SUBRAMANIAN N, NATARAJAN K, CLATWORTHY M R, et al. The adaptor MAVS promotes NLRP3 mitochondrial localization and inflammasome activation[J]. Cell, 2013, 153(2):348-361.
[44]	CHEN Q, SUN L J, CHEN Z J J. Regulation and function of the cGAS-STING pathway of cytosolic DNA sensing[J]. Nat Immunol, 2016, 17(10):1142-1149.
[45]	COLLINS A C, CAI H C, LI T, et al. Cyclic GMP-AMP synthase is an innate immune DNA sensor for Mycobacterium tuberculosis[J]. Cell Host Microbe, 2015, 17(6):820-828.
[46]	GAO D X, WU J X, WU Y T, et al. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses[J]. Science, 2013, 341(6148):903-906.
[47]	BARBER G N. STING:infection, inflammation and cancer[J]. Nat Rev Immunol, 2015, 15(12):760-770.
[48]	CROW Y J, MANEL N. Aicardi-Goutières syndrome and the type I interferonopathies[J]. Nat Rev Immunol, 2015, 15(7):429-440.
[49]	RONGVAUX A, JACKSON R, HARMAN C C D, et al. Apoptotic caspases prevent the induction of type I interferons by mitochondrial DNA[J]. Cell, 2014, 159(7):1563-1577.
[50]	WHITE M J, MCARTHUR K, METCALF D, et al. Apoptotic caspases suppress mtDNA-induced STING-mediated type I IFN production[J]. Cell, 2014, 159(7):1549-1562.
[51]	GARCIA N, CHÁVEZ E. Mitochondrial DNA fragments released through the permeability transition pore correspond to specific gene size[J]. Life Sci, 2007, 81(14):1160-1166.
[52]	PATRUSHEV M, KASYMOV V, PATRUSHEVA V, et al. Mitochondrial permeability transition triggers the release of mtDNA fragments[J]. Cell Mol Life Sci, 2004, 61(24):3100-3103.
[53]	CARROLL E C, JIN L, MORI A, et al. The vaccine adjuvant chitosan promotes cellular immunity via DNA sensor cGAS-STING-dependent induction of type I interferons[J]. Immunity, 2016, 44(3):597-608.
[54]	HOWELL J, SAWHNEY R, TESTRO A, et al. Cyclosporine and tacrolimus have inhibitory effects on toll-like receptor signaling after liver transplantation[J]. Liver Transpl, 2013, 19(10):1099-1107.
[55]	NISHIYAMA S, MANABE N, KUBOTA Y, et al. Cyclosporin A inhibits the early phase of NF-κB/RelA activation induced by CD28 costimulatory signaling to reduce the IL-2 expression in human peripheral T cells[J]. Int Immunopharmacol, 2005, 5(4):699-710.
[56]	KANNEGANTI T D, KUNDU M, GREEN D R. Innate immune recognition of mtDNA-an undercover signal?[J]. Cell Metab, 2015, 21(6):793-794.
[57]	ALAVIAN K N, BEUTNER G, LAZROVE E, et al. An uncoupling channel within the c-subunit ring of the F1FO ATP synthase is the mitochondrial permeability transition pore[J]. Proc Natl Acad Sci U S A, 2014, 111(29):10580-10585.
[58]	BERNARDI P, RASOLA A, FORTE M, et al. The mitochondrial permeability transition pore:channel formation by F-ATP synthase, integration in signal transduction, and role in pathophysiology[J]. Physiol Rev, 2015, 95(4):1111-1155.
[59]	MATILLA I, ALFONSO C, RIVAS G, et al. The conjugative DNA translocase TrwB is a structure-specific DNA-binding protein[J]. J Biol Chem, 2010, 285(23):17537-17544.
[60]	WEST A P, KHOURY-HANOLD W, STARON M, et al. Mitochondrial DNA stress primes the antiviral innate immune response[J]. Nature, 2015, 520(7548):553-557.
[61]	AARREBERG LD, ESSER-NOBIS K, DRISCOLL C, et al. Interleukin-1β induces mtDNA release to activate innate immune signaling via cGAS-STING[J]. Mol Cell, 2019, 74(4):801-815.e6.
[62]	MAYER-BARBER K D, ANDRADE B B, OLAND S D, et al. Host-directed therapy of tuberculosis based on interleukin-1 and type I interferon crosstalk[J]. Nature, 2014, 511(7507):99-103.
[63]	LOOD C, BLANCO L P, PURMALEK M M, et al. Neutrophil extracellular traps enriched in oxidized mitochondrial DNA are interferogenic and contribute to lupus-like disease[J]. Nat Med, 2016, 22(2):146-153.
[64]	MCILROY D J, JARNICKI A G, AU G G, et al. Mitochondrial DNA neutrophil extracellular traps are formed after trauma and subsequent surgery[J]. J Crit Care, 2014, 29(6):1133.e1-1133.e5.
[65]	WEST A P, BRODSKY I E, RAHNER C, et al. TLR signalling augments macrophage bactericidal activity through mitochondrial ROS[J]. Nature, 2011, 472(7344):476-480.
[66]	PAZMANDI K, AGOD Z, KUMAR B V, et al. Oxidative modification enhances the immunostimulatory effects of extracellular mitochondrial DNA on plasmacytoid dendritic cells[J]. Free Radic Biol Med, 2014, 77:281-290.
[67]	MATYSZEWSKI M, MORRONE S R, SOHN J. Digital signaling network drives the assembly of the AIM2-ASC inflammasome[J]. Proc Natl Acad Sci U S A, 2018, 115(9):E1963-E1972.
[68]	MORRONE S R, MATYSZEWSKI M, YU X, et al. Assembly-driven activation of the AIM2 foreign-dsDNA sensor provides a polymerization template for downstream ASC[J]. Nat Commun, 2015, 6:7827.
[69]	JIN T C, PERRY A, JIANG J S, et al. Structures of the HIN domain:DNA complexes reveal ligand binding and activation mechanisms of the AIM2 inflammasome and IFI16 receptor[J]. Immunity, 2012, 36(4):561-571.
[70]	LUECKE S, HOLLEUFER A, CHRISTENSEN M H, et al. cGAS is activated by DNA in a length-dependent manner[J]. EMBO Rep, 2017, 18(10):1707-1715.
[71]	WANG L Y, LIEBMEN M N, WANG X D. Roles of mitochondrial DNA signaling in immune responses[M]//SUN H Z, WANG X D. Mitochondrial DNA and Diseases. Singapore:Springer, 2017, 1038:39-53.
[72]	HU B, JIN C C, LI H B, et al. The DNA-sensing AIM2 inflammasome controls radiation-induced cell death and tissue injury[J]. Science, 2016, 354(6313):765-768.
[73]	CHEN J Q, CHEN Z J J. PtdIns4P on dispersed trans-Golgi network mediates NLRP3 inflammasome activation[J]. Nature, 2018, 564(7734):71-76.
[74]	GENTILI M, LAHAYE X, NADALIN F, et al. The N-terminal domain of cGAS determines preferential association with centromeric DNA and innate immune activation in the nucleus[J]. Cell Rep, 2019, 26(9):2377-2393.e13.
[75]	BARNETT K C, CORONAS-SERNA J M, ZHOU W, et al. Phosphoinositide interactions position cGAS at the plasma membrane to ensure efficient distinction between self- and viral DNA[J]. Cell, 2019, 176(6):1432-1446.e11.
[76]	WANG Y T, NING X H, GAO P F, et al. Inflammasome activation triggers caspase-1-mediated cleavage of cGAS to regulate responses to DNA virus infection[J]. Immunity, 2017, 46(3):393-404.
[77]	SWANSON K V, JUNKINS R D, KURKJIAN C J, et al. A noncanonical function of cGAMP in inflammasome priming and activation[J]. J Exp Med, 2017, 214(12):3611-3626.
[78]	CHIMIENTI G, PICCA A, SIRAGO G, et al. Increased TFAM binding to mtDNA damage hot spots is associated with mtDNA loss in aged rat heart[J]. Free Radic Biol Med, 2018, 124:447-453.
[79]	YOSHIDA Y, IZUMI H, ISE T, et al. Human mitochondrial transcription factor A binds preferentially to oxidatively damaged DNA[J]. Biochem Biophys Res Commun, 2002, 295(4):945-951.
[80]	MOK B Y, DE MORAES M H, ZENG J, et al. A bacterial cytidine deaminase toxin enables CRISPR-free mitochondrial base editing[J]. Nature, 2020, 583(7817):631-637.
[81]	YONEYAMA M, ONOMOTO K, JOGI M, et al. Viral RNA detection by RIG-I-like receptors[J]. Curr Opin Immunol, 2015, 32:48-53.
[82]	SCHOGGINS J W, MACDUFF D A, IMANAKA N, et al. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity[J]. Nature, 2014, 505(7485):691-695.
[83]	SUN B, SUNDSTRÖM K B, CHEW J J, et al. Dengue virus activates cGAS through the release of mitochondrial DNA[J]. Sci Rep, 2017, 7(1):3594.
[84]	LAI J H, WANG M Y, HUANG C Y, et al. Infection with the dengue RNA virus activates TLR9 signaling in human dendritic cells[J]. EMBO Rep, 2018, 19(8):e46182.
[85]	AGUIRRE S, MAESTRE A M, PAGNI S, et al. DENV inhibits type I IFN production in infected cells by cleaving human STING[J]. PLoS Pathog, 2012, 8(10):e1002934.
[86]	MORIYAMA M, KOSHIBA T, ICHINOHE T. Influenza A virus M2 protein triggers mitochondrial DNA-mediated antiviral immune responses[J]. Nat Commun, 2019, 10(1):4624.
[87]	VON KÖCKRITZ-BLICKWEDE M, NIZET V. Innate immunity turned inside-out:antimicrobial defense by phagocyte extracellular traps[J]. J Mol Med (Berlin, Germany), 2009, 87(8):775-783.
[88]	YOUSEFI S, GOLD J A, ANDINA N, et al. Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense[J]. Nat Med, 2008, 14(9):949-953.
[89]	YOUSEFI S, MORSHED M, AMINI P, et al. Basophils exhibit antibacterial activity through extracellular trap formation[J]. Allergy, 2015, 70(9):1184-1188.
[90]	SAFFRAN H A, PARE J M, CORCORAN J A, et al. Herpes simplex virus eliminates host mitochondrial DNA[J]. EMBO Rep, 2007, 8(2):188-193.
[91]	WATSON R O, BELL S L, MACDUFF D A, et al. The cytosolic sensor cGAS detects Mycobacterium tuberculosis DNA to induce type I interferons and activate autophagy[J]. Cell Host Microbe, 2015, 17(6):811-819.
[92]	WIENS K E, ERNST J D. The mechanism for type I interferon induction by Mycobacterium tuberculosis is bacterial strain-dependent[J]. PLoS Pathog, 2016, 12(8):e1005809.
[93]	ZHANG Z Y, MENG P, HAN Y J, et al. Mitochondrial DNA-LL-37 complex promotes atherosclerosis by escaping from autophagic recognition[J]. Immunity, 2015, 43(6):1137-1147.
[94]	GARCIA-MARTINEZ I, SANTORO N, CHEN Y L, et al. Hepatocyte mitochondrial DNA drives nonalcoholic steatohepatitis by activation of TLR9[J]. J Clin Invest, 2016, 126(3):859-864.
[95]	YOUNOSSI Z M, KOENIG A B, ABDELATIF D, et al. Global epidemiology of nonalcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes[J]. Hepatology, 2016, 64(1):73-84.
[96]	YU Y S, LIU Y, AN W S, et al. STING-mediated inflammation in Kupffer cells contributes to progression of nonalcoholic steatohepatitis[J]. J Clin Invest, 2019, 129(2):546-555.
[97]	MRIDHA A R, WREE A, ROBERTSON A A B, et al. NLRP3 inflammasome blockade reduces liver inflammation and fibrosis in experimental NASH in mice[J]. J Hepatol, 2017, 66(5):1037-1046.

The Role of Mitochondrial DNA in Innate Immunity

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