Crosstalk between Dysfunctional Mitochondria and Proinflammatory Responses during Viral Infections
Abstract
:1. Introduction
2. Mitochondrial Structure and Functions
3. Mitochondrial Damage Induced by Viral Infections
3.1. The Increased Mitochondrial Membrane Permeability Induced by Viral Infections Leads to Mitochondrial Damage
3.2. Viral Proteins-Induced Disruption of Mitochondrial Dynamics Leads to Mitochondrial Damage
3.3. The Mitochondria-Mediated Stress Response during Viral Infections Leads to Mitochondrial Damage
4. Proinflammatory Response Induced by Mitochondrial Damage upon Viral Infections
4.1. Mitochondrial Damage Promotes NLRP3 Inflammasome Activation
4.2. Viruses Manipulate the Immune Responses Associated with Mitochondrial Damage
5. Targeted Regulation of Mitochondrial Damage in Antiviral Therapies
5.1. Regulation of Mitochondrial Membrane Permeability in Antiviral Strategies
5.2. Modulation of the Mitophagy Pathway in Response to Viral Infections
6. Conclusions and Perspectives
Author Contributions
Funding
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
AMPK | AMP-activated protein kinase |
ATP | adenosine triphosphate |
ClpP | caseinolytic protease P |
CMPK2 | cytidine monophosphate kinase 2 |
GPX1 | glutathione peroxidase 1 |
NAC | N-acetyl-L-cysteine |
NEK7 | NIMA-related kinase 7 |
NQO2 | quinone oxidoreductase 2 |
PPID | peptidylprolyl isomerase D |
SOD | superoxide dismutase |
References
- Protasoni, M.; Zeviani, M. Mitochondrial structure and bioenergetics in normal and disease conditions. Int. J. Mol. Sci. 2021, 22, 586. [Google Scholar] [CrossRef] [PubMed]
- Palmer, C.S.; Anderson, A.J.; Stojanovski, D. Mitochondrial protein import dysfunction: Mitochondrial disease, neurodegenerative disease and cancer. FEBS Lett. 2021, 595, 1107–1131. [Google Scholar] [CrossRef] [PubMed]
- Lalier, L.; Mignard, V.; Joalland, M.P.; Lanoe, D.; Cartron, P.F.; Manon, S.; Vallette, F.M. TOM20-mediated transfer of Bcl2 from ER to MAM and mitochondria upon induction of apoptosis. Cell Death Dis. 2021, 12, 182. [Google Scholar] [CrossRef] [PubMed]
- Xu, T.; Dong, Q.; Luo, Y.; Liu, Y.; Gao, L.; Pan, Y.; Zhang, D. Porphyromonas gingivalis infection promotes mitochondrial dysfunction through Drp1-dependent mitochondrial fission in endothelial cells. Int. J. Oral Sci. 2021, 13, 28. [Google Scholar] [CrossRef]
- Scheffer, D.; Garcia, A.A.; Lee, L.; Mochly-Rosen, D.; Ferreira, J. Mitochondrial fusion, fission, and mitophagy in cardiac diseases: Challenges and therapeutic opportunities. Antioxid. Redox Signal. 2022, 36, 844–863. [Google Scholar] [CrossRef]
- Boyenle, I.D.; Oyedele, A.K.; Ogunlana, A.T.; Adeyemo, A.F.; Oyelere, F.S.; Akinola, O.B.; Adelusi, T.I.; Ehigie, L.O.; Ehigie, A.F. Targeting the mitochondrial permeability transition pore for drug discovery: Challenges and opportunities. Mitochondrion 2022, 63, 57–71. [Google Scholar] [CrossRef]
- McClain, S.L.; Clippinger, A.J.; Lizzano, R.; Bouchard, M.J. Hepatitis B virus replication is associated with an HBx-dependent mitochondrion-regulated increase in cytosolic calcium levels. J. Virol. 2007, 81, 12061–12065. [Google Scholar] [CrossRef]
- Halestrap, A.P.; Brenner, C. The adenine nucleotide translocase: A central component of the mitochondrial permeability transition pore and key player in cell death. Curr. Med. Chem. 2003, 10, 1507–1525. [Google Scholar] [CrossRef] [PubMed]
- Yang, Y.; Liang, Y.; Qu, L.; Chen, Z.; Yi, M.; Li, K.; Lemon, S.M. Disruption of innate immunity due to mitochondrial targeting of a picornaviral protease precursor. Proc. Natl. Acad. Sci. USA 2007, 104, 7253–7258. [Google Scholar] [CrossRef] [PubMed]
- Dela, C.C.; Kang, M.J. Mitochondrial dysfunction and damage associated molecular patterns (DAMPs) in chronic inflammatory diseases. Mitochondrion 2018, 41, 37–44. [Google Scholar] [CrossRef] [PubMed]
- Lai, J.H.; Wu, D.W.; Wu, C.H.; Hung, L.F.; Huang, C.Y.; Ka, S.M.; Chen, A.; Ho, L.J. USP18 enhances dengue virus replication by regulating mitochondrial DNA release. Sci. Rep. 2023, 13, 20126. [Google Scholar] [CrossRef] [PubMed]
- Bouchard, M.J.; Schneider, R.J. The enigmatic X gene of hepatitis B virus. J. Virol. 2004, 78, 12725–12734. [Google Scholar] [CrossRef]
- Lee, Y.J.; Lee, C. Porcine deltacoronavirus induces caspase-dependent apoptosis through activation of the cytochrome C-mediated intrinsic mitochondrial pathway. Virus Res. 2018, 253, 112–123. [Google Scholar] [CrossRef] [PubMed]
- Papaianni, E.; El Maadidi, S.; Schejtman, A.; Neumann, S.; Maurer, U.; Marino-Merlo, F.; Mastino, A.; Borner, C. Phylogenetically distant viruses use the same BH3-only protein Puma to trigger Bax/Bak-dependent apoptosis of infected mouse and human cells. PLoS ONE 2015, 10, e126645. [Google Scholar] [CrossRef] [PubMed]
- Zhang, S.; Zeng, L.; Su, B.; Yang, G.; Wang, J.; Ming, S.; Chu, B. The glycoprotein 5 of porcine reproductive and respiratory syndrome virus stimulates mitochondrial ROS to facilitate viral replication. mBio 2023, 14, e265123. [Google Scholar] [CrossRef]
- Aarreberg, L.D.; Esser-Nobis, K.; Driscoll, C.; Shuvarikov, A.; Roby, J.A.; Gale, M.J. Interleukin-1beta induces mtDNA release to activate innate immune signaling via cGAS-STING. Mol. Cell 2019, 74, 801–815. [Google Scholar] [CrossRef]
- Yang, S.; Gorshkov, K.; Lee, E.M.; Xu, M.; Cheng, Y.S.; Sun, N.; Soheilian, F.; de Val, N.; Ming, G.; Song, H.; et al. Zika virus-induced neuronal apoptosis via increased mitochondrial fragmentation. Front. Microbiol. 2020, 11, 598203. [Google Scholar] [CrossRef]
- Huang, C.Y.; Chiang, S.F.; Lin, T.Y.; Chiou, S.H.; Chow, K.C. HIV-1 Vpr triggers mitochondrial destruction by impairing Mfn2-mediated ER-mitochondria interaction. PLoS ONE 2012, 7, e33657. [Google Scholar] [CrossRef]
- Lee, J.H.; Oh, S.J.; Yun, J.; Shin, O.S. Nonstructural protein NS1 of influenza virus disrupts mitochondrial dynamics and enhances mitophagy via ULK1 and BNIP3. Viruses 2021, 13, 1845. [Google Scholar] [CrossRef]
- Kim, S.J.; Khan, M.; Quan, J.; Till, A.; Subramani, S.; Siddiqui, A. Hepatitis B virus disrupts mitochondrial dynamics: Induces fission and mitophagy to attenuate apoptosis. PLoS Pathog. 2013, 9, e1003722. [Google Scholar] [CrossRef]
- Kim, S.J.; Syed, G.H.; Khan, M.; Chiu, W.W.; Sohail, M.A.; Gish, R.G.; Siddiqui, A. Hepatitis C virus triggers mitochondrial fission and attenuates apoptosis to promote viral persistence. Proc. Natl. Acad. Sci. USA 2014, 111, 6413–6418. [Google Scholar] [CrossRef] [PubMed]
- Liu, G.; Zhong, M.; Guo, C.; Komatsu, M.; Xu, J.; Wang, Y.; Kitazato, K. Autophagy is involved in regulating influenza A virus RNA and protein synthesis associated with both modulation of Hsp90 induction and mTOR/p70S6K signaling pathway. Int. J. Biochem. Cell Biol. 2016, 72, 100–108. [Google Scholar] [CrossRef] [PubMed]
- Korenaga, M.; Wang, T.; Li, Y.; Showalter, L.A.; Chan, T.; Sun, J.; Weinman, S.A. Hepatitis C virus core protein inhibits mitochondrial electron transport and increases reactive oxygen species (ROS) production. J. Biol. Chem. 2005, 280, 37481–37488. [Google Scholar] [CrossRef]
- Macho, A.; Calzado, M.A.; Jimenez-Reina, L.; Ceballos, E.; Leon, J.; Munoz, E. Susceptibility of HIV-1-TAT transfected cells to undergo apoptosis. Biochemical Mechanisms. Oncogene 1999, 18, 7543–7551. [Google Scholar] [CrossRef] [PubMed]
- Helle, S.C.; Kanfer, G.; Kolar, K.; Lang, A.; Michel, A.H.; Kornmann, B. Organization and function of membrane contact sites. Biochim. Biophys. Acta 2013, 1833, 2526–2541. [Google Scholar] [CrossRef]
- Simmen, T.; Lynes, E.M.; Gesson, K.; Thomas, G. Oxidative protein folding in the endoplasmic reticulum: Tight links to the mitochondria-associated membrane (MAM). Biochim. Biophys. Acta 2010, 1798, 1465–1473. [Google Scholar] [CrossRef]
- Bosch, M.; Mari, M.; Gross, S.P.; Fernandez-Checa, J.C.; Pol, A. Mitochondrial cholesterol: A connection between caveolin, metabolism, and disease. Traffic 2011, 12, 1483–1489. [Google Scholar] [CrossRef]
- Zhou, R.; Yazdi, A.S.; Menu, P.; Tschopp, J. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011, 469, 221–225. [Google Scholar] [CrossRef]
- de Brito, O.M.; Scorrano, L. An intimate liaison: Spatial organization of the endoplasmic reticulum-mitochondria relationship. EMBO J. 2010, 29, 2715–2723. [Google Scholar] [CrossRef]
- Zhao, M.; Wang, Y.; Li, L.; Liu, S.; Wang, C.; Yuan, Y.; Yang, G.; Chen, Y.; Cheng, J.; Lu, Y.; et al. Mitochondrial ROS promote mitochondrial dysfunction and inflammation in ischemic acute kidney injury by disrupting TFAM-mediated mtDNA maintenance. Theranostics 2021, 11, 1845–1863. [Google Scholar] [CrossRef]
- Lai, J.H.; Wang, M.Y.; Huang, C.Y.; Wu, C.H.; Hung, L.F.; Yang, C.Y.; Ke, P.Y.; Luo, S.F.; Liu, S.J.; Ho, L.J. Infection with the dengue RNA virus activates TLR9 signaling in human dendritic cells. EMBO Rep. 2018, 19, e46182. [Google Scholar] [CrossRef] [PubMed]
- Cervantes-Silva, M.P.; Cox, S.L.; Curtis, A.M. Alterations in mitochondrial morphology as a key driver of immunity and host defence. EMBO Rep. 2021, 22, e53086. [Google Scholar] [CrossRef] [PubMed]
- Chen, H.; Detmer, S.A.; Ewald, A.J.; Griffin, E.E.; Fraser, S.E.; Chan, D.C. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 2003, 160, 189–200. [Google Scholar] [CrossRef]
- Geisler, S.; Holmstrom, K.M.; Skujat, D.; Fiesel, F.C.; Rothfuss, O.C.; Kahle, P.J.; Springer, W. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 2010, 12, 119–131. [Google Scholar] [CrossRef] [PubMed]
- Novak, I.; Kirkin, V.; McEwan, D.G.; Zhang, J.; Wild, P.; Rozenknop, A.; Rogov, V.; Lohr, F.; Popovic, D.; Occhipinti, A.; et al. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 2010, 11, 45–51. [Google Scholar] [CrossRef]
- Yan, C.; Gong, L.; Chen, L.; Xu, M.; Abou-Hamdan, H.; Tang, M.; Desaubry, L.; Song, Z. PHB2 (prohibitin 2) promotes PINK1-PRKN/Parkin-dependent mitophagy by the PARL-PGAM5-PINK1 axis. Autophagy 2020, 16, 419–434. [Google Scholar] [CrossRef]
- Zhang, L.; Qin, Y.; Chen, M. Viral strategies for triggering and manipulating mitophagy. Autophagy 2018, 14, 1665–1673. [Google Scholar] [CrossRef]
- Liu, B.; Fang, M.; Hu, Y.; Huang, B.; Li, N.; Chang, C.; Huang, R.; Xu, X.; Yang, Z.; Chen, Z.; et al. Hepatitis B virus X protein inhibits autophagic degradation by impairing lysosomal maturation. Autophagy 2014, 10, 416–430. [Google Scholar] [CrossRef]
- Son, J.; Kim, M.J.; Lee, J.S.; Kim, J.Y.; Chun, E.; Lee, K.Y. Hepatitis B virus X protein promotes liver cancer progression through autophagy induction in response to TLR4 stimulation. Immune Netw. 2021, 21, e37. [Google Scholar] [CrossRef] [PubMed]
- Evans, M.D.; Dizdaroglu, M.; Cooke, M.S. Oxidative DNA damage and disease: Induction, repair and significance. Mutat. Res. 2004, 567, 1–61. [Google Scholar] [CrossRef] [PubMed]
- Pruchniak, M.P.; Arazna, M.; Demkow, U. Biochemistry of oxidative stress. Adv. Exp. Med. Biol. 2016, 878, 9–19. [Google Scholar] [CrossRef]
- Karihtala, P.; Soini, Y. Reactive oxygen species and antioxidant mechanisms in human tissues and their relation to malignancies. APMIS 2007, 115, 81–103. [Google Scholar] [CrossRef]
- Krokan, H.E.; Standal, R.; Slupphaug, G. DNA glycosylases in the base excision repair of DNA. Biochem. J. 1997, 325, 1–16. [Google Scholar] [CrossRef]
- Dizdaroglu, M.; Jaruga, P.; Birincioglu, M.; Rodriguez, H. Free radical-induced damage to DNA: Mechanisms and measurement. Free Radic. Biol. Med. 2002, 32, 1102–1115. [Google Scholar] [CrossRef] [PubMed]
- Hahm, J.Y.; Park, J.; Jang, E.S.; Chi, S.W. 8-Oxoguanine: From oxidative damage to epigenetic and epitranscriptional modification. Exp. Mol. Med. 2022, 54, 1626–1642. [Google Scholar] [CrossRef] [PubMed]
- Memisoglu, A.; Samson, L. Base excision repair in yeast and mammals. Mutat. Res. 2000, 451, 39–51. [Google Scholar] [CrossRef] [PubMed]
- Wilson, D.R.; Sofinowski, T.M.; McNeill, D.R. Repair mechanisms for oxidative DNA damage. Front. Biosci. 2003, 8, d963–d981. [Google Scholar] [CrossRef]
- Kensler, T.W.; Wakabayashi, N.; Biswal, S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 2007, 47, 89–116. [Google Scholar] [CrossRef]
- Holmstrom, K.M.; Finkel, T. Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat. Rev. Mol. Cell Biol. 2014, 15, 411–421. [Google Scholar] [CrossRef] [PubMed]
- Pinti, M.; Gibellini, L.; Liu, Y.; Xu, S.; Lu, B.; Cossarizza, A. Mitochondrial Lon protease at the crossroads of oxidative stress, ageing and cancer. Cell. Mol. Life Sci. 2015, 72, 4807–4824. [Google Scholar] [CrossRef]
- Wang, Y.; Li, X.; Zhao, F. MCU-dependent mROS generation regulates cell metabolism and cell death modulated by the AMPK/PGC-1alpha/SIRT3 signaling pathway. Front. Med. 2021, 8, 674986. [Google Scholar] [CrossRef]
- Janeway, C.J.; Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol. 2002, 20, 197–216. [Google Scholar] [CrossRef] [PubMed]
- Schroder, K.; Tschopp, J. The inflammasomes. Cell 2010, 140, 821–832. [Google Scholar] [CrossRef]
- Lei, X.; Li, S.; Luo, C.; Wang, Y.; Liu, Y.; Xu, Z.; Huang, Q.; Zou, F.; Chen, Y.; Peng, F.; et al. Micheliolide attenuates lipopolysaccharide-induced inflammation by modulating the mROS/NF-kappaB/NLRP3 axis in renal tubular epithelial cells. Mediat. Inflamm. 2020, 2020, 3934769. [Google Scholar] [CrossRef]
- Franchi, L.; Munoz-Planillo, R.; Nunez, G. Sensing and reacting to microbes through the inflammasomes. Nat. Immunol. 2012, 13, 325–332. [Google Scholar] [CrossRef]
- Dinarello, C.A. Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 2009, 27, 519–550. [Google Scholar] [CrossRef] [PubMed]
- Fink, S.L.; Cookson, B.T. Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol. 2006, 8, 1812–1825. [Google Scholar] [CrossRef] [PubMed]
- Liu, Q.; Zhang, D.; Hu, D.; Zhou, X.; Zhou, Y. The role of mitochondria in NLRP3 inflammasome activation. Mol. Immunol. 2018, 103, 115–124. [Google Scholar] [CrossRef]
- Shimada, K.; Crother, T.R.; Karlin, J.; Dagvadorj, J.; Chiba, N.; Chen, S.; Ramanujan, V.K.; Wolf, A.J.; Vergnes, L.; Ojcius, D.M.; et al. Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity 2012, 36, 401–414. [Google Scholar] [CrossRef]
- He, Y.; Hara, H.; Nunez, G. Mechanism and regulation of NLRP3 inflammasome activation. Trends Biochem. Sci. 2016, 41, 1012–1021. [Google Scholar] [CrossRef]
- Elliott, E.I.; Miller, A.N.; Banoth, B.; Iyer, S.S.; Stotland, A.; Weiss, J.P.; Gottlieb, R.A.; Sutterwala, F.S.; Cassel, S.L. Cutting edge: Mitochondrial assembly of the NLRP3 inflammasome complex is initiated at priming. J. Immunol. 2018, 200, 3047–3052. [Google Scholar] [CrossRef] [PubMed]
- Maynard, S.; Schurman, S.H.; Harboe, C.; de Souza-Pinto, N.C.; Bohr, V.A. Base excision repair of oxidative DNA damage and association with cancer and aging. Carcinogenesis 2009, 30, 2–10. [Google Scholar] [CrossRef] [PubMed]
- Khan, S.; Godfrey, V.; Zaki, M.H. Cytosolic nucleic acid sensors in inflammatory and autoimmune disorders. Int. Rev. Cell Mol. Biol. 2019, 344, 215–253. [Google Scholar] [CrossRef]
- Riley, J.S.; Tait, S.W. Mitochondrial DNA in inflammation and immunity. EMBO Rep. 2020, 21, e49799. [Google Scholar] [CrossRef] [PubMed]
- Decout, A.; Katz, J.D.; Venkatraman, S.; Ablasser, A. The cGAS-STING pathway as a therapeutic target in inflammatory diseases. Nat. Rev. Immunol. 2021, 21, 548–569. [Google Scholar] [CrossRef] [PubMed]
- Coll, R.C.; Holley, C.L.; Schroder, K. Author Correction: Mitochondrial DNA synthesis fuels NLRP3 inflammasome. Cell Res. 2018, 28, 1202. [Google Scholar] [CrossRef] [PubMed]
- Hall, C.J.; Sanderson, L.E.; Lawrence, L.M.; Pool, B.; van der Kroef, M.; Ashimbayeva, E.; Britto, D.; Harper, J.L.; Lieschke, G.J.; Astin, J.W.; et al. Blocking fatty acid-fueled mROS production within macrophages alleviates acute gouty inflammation. J. Clin. Investig. 2018, 128, 1752–1771. [Google Scholar] [CrossRef] [PubMed]
- Abais, J.M.; Xia, M.; Zhang, Y.; Boini, K.M.; Li, P.L. Redox regulation of NLRP3 inflammasomes: ROS as trigger or effector? Antioxid. Redox Signal. 2015, 22, 1111–1129. [Google Scholar] [CrossRef]
- Bauernfeind, F.; Bartok, E.; Rieger, A.; Franchi, L.; Nunez, G.; Hornung, V. Cutting edge: Reactive oxygen species inhibitors block priming, but not activation, of the NLRP3 inflammasome. J. Immunol. 2011, 187, 613–617. [Google Scholar] [CrossRef] [PubMed]
- Kagan, V.E.; Tyurin, V.A.; Jiang, J.; Tyurina, Y.Y.; Ritov, V.B.; Amoscato, A.A.; Osipov, A.N.; Belikova, N.A.; Kapralov, A.A.; Kini, V.; et al. Cytochrome C acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat. Chem. Biol. 2005, 1, 223–232. [Google Scholar] [CrossRef]
- Schofield, J.H.; Schafer, Z.T. Mitochondrial reactive oxygen species and mitophagy: A complex and nuanced relationship. Antioxid. Redox Signal. 2021, 34, 517–530. [Google Scholar] [CrossRef] [PubMed]
- Orning, P.; Weng, D.; Starheim, K.; Ratner, D.; Best, Z.; Lee, B.; Brooks, A.; Xia, S.; Wu, H.; Kelliher, M.A.; et al. Pathogen blockade of TAK1 triggers caspase-8-dependent cleavage of gasdermin D and cell death. Science 2018, 362, 1064–1069. [Google Scholar] [CrossRef]
- Iyer, S.S.; He, Q.; Janczy, J.R.; Elliott, E.I.; Zhong, Z.; Olivier, A.K.; Sadler, J.J.; Knepper-Adrian, V.; Han, R.; Qiao, L.; et al. Mitochondrial cardiolipin is required for NLRP3 inflammasome activation. Immunity 2013, 39, 311–323. [Google Scholar] [CrossRef] [PubMed]
- Macchioni, L.; Petricciuolo, M.; Davidescu, M.; Fettucciari, K.; Scarpelli, P.; Vitale, R.; Gatticchi, L.; Orvietani, P.L.; Marchegiani, A.; Marconi, P.; et al. Palmitate lipotoxicity in enteric glial cells: Lipid remodeling and mitochondrial ROS are responsible for release outside mitochondria. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 2018, 1863, 895–908. [Google Scholar] [CrossRef]
- Means, R.E.; Katz, S.G. Balancing life and death: BCL-2 family members at diverse ER-mitochondrial contact sites. FEBS J. 2022, 289, 7075–7112. [Google Scholar] [CrossRef] [PubMed]
- Shi, C.S.; Qi, H.Y.; Boularan, C.; Huang, N.N.; Abu-Asab, M.; Shelhamer, J.H.; Kehrl, J.H. SARS-coronavirus open reading frame-9b suppresses innate immunity by targeting mitochondria and the MAVS/TRAF3/TRAF6 signalosome. J. Immunol. 2014, 193, 3080–3089. [Google Scholar] [CrossRef] [PubMed]
- Choi, H.J.; Park, A.; Kang, S.; Lee, E.; Lee, T.A.; Ra, E.A.; Lee, J.; Lee, S.; Park, B. Human cytomegalovirus-encoded US9 targets MAVS and STING signaling to evade type I interferon immune responses. Nat. Commun. 2018, 9, 125. [Google Scholar] [CrossRef]
- Li, X.D.; Sun, L.; Seth, R.B.; Pineda, G.; Chen, Z.J. Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein off the mitochondria to evade innate immunity. Proc. Natl. Acad. Sci. USA 2005, 102, 17717–17722. [Google Scholar] [CrossRef] [PubMed]
- Lau, L.; Gray, E.E.; Brunette, R.L.; Stetson, D.B. DNA tumor virus oncogenes antagonize the cGAS-STING DNA-sensing pathway. Science 2015, 350, 568–571. [Google Scholar] [CrossRef]
- Luo, X.; Donnelly, C.R.; Gong, W.; Heath, B.R.; Hao, Y.; Donnelly, L.A.; Moghbeli, T.; Tan, Y.S.; Lin, X.; Bellile, E.; et al. HPV16 drives cancer immune escape via NLRX1-mediated degradation of STING. J. Clin. Investig. 2020, 130, 1635–1652. [Google Scholar] [CrossRef] [PubMed]
- Oka, T.; Hikoso, S.; Yamaguchi, O.; Taneike, M.; Takeda, T.; Tamai, T.; Oyabu, J.; Murakawa, T.; Nakayama, H.; Nishida, K.; et al. Mitochondrial DNA that escapes from autophagy causes inflammation and heart failure. Nature 2012, 485, 251–255. [Google Scholar] [CrossRef] [PubMed]
- Mouton-Liger, F.; Rosazza, T.; Sepulveda-Diaz, J.; Ieang, A.; Hassoun, S.M.; Claire, E.; Mangone, G.; Brice, A.; Michel, P.P.; Corvol, J.C.; et al. Parkin deficiency modulates NLRP3 inflammasome activation by attenuating an A20-dependent negative feedback loop. Glia 2018, 66, 1736–1751. [Google Scholar] [CrossRef] [PubMed]
- Li, L.; Tan, J.; Miao, Y.; Lei, P.; Zhang, Q. ROS and autophagy: Interactions and molecular regulatory mechanisms. Cell. Mol. Neurobiol. 2015, 35, 615–621. [Google Scholar] [CrossRef] [PubMed]
- Newman, L.E.; Shadel, G.S. Mitochondrial DNA Release in Innate Immune Signaling. Annu. Rev. Biochem. 2023, 92, 299–332. [Google Scholar] [CrossRef] [PubMed]
- Averbeck, D.; Rodriguez-Lafrasse, C. Role of Mitochondria in Radiation Responses: Epigenetic, Metabolic, and Signaling Impacts. Int. J. Mol. Sci. 2021, 22, 11047. [Google Scholar] [CrossRef] [PubMed]
- Banoth, B.; Cassel, S.L. Mitochondria in innate immune signaling. Transl. Res. 2018, 202, 52–68. [Google Scholar] [CrossRef] [PubMed]
- Wang, T.; Weinman, S.A. Interactions between hepatitis C virus and mitochondria: Impact on pathogenesis and innate immunity. Curr. Pathobiol. Rep. 2013, 1, 179–187. [Google Scholar] [CrossRef]
- Liu, H.; Zhu, Z.; Xue, Q.; Yang, F.; Li, Z.; Xue, Z.; Cao, W.; He, J.; Guo, J.; Liu, X.; et al. Innate sensing of picornavirus infection involves cGAS-STING-mediated antiviral responses triggered by mitochondrial DNA release. PLoS Pathog. 2023, 19, e1011132. [Google Scholar] [CrossRef]
- Yu, C.H.; Davidson, S.; Harapas, C.R.; Hilton, J.B.; Mlodzianoski, M.J.; Laohamonthonkul, P.; Louis, C.; Low, R.; Moecking, J.; De Nardo, D.; et al. TDP-43 triggers mitochondrial DNA release via mPTP to activate cGAS/STING in ALS. Cell 2020, 183, 636–649. [Google Scholar] [CrossRef]
- Endlicher, R.; Drahota, Z.; Stefkova, K.; Cervinkova, Z.; Kucera, O. The mitochondrial permeability transition pore-current knowledge of its structure, function, and regulation, and optimized methods for evaluating its functional state. Cells 2023, 12, 1273. [Google Scholar] [CrossRef]
- Quarato, G.; D’Aprile, A.; Gavillet, B.; Vuagniaux, G.; Moradpour, D.; Capitanio, N.; Piccoli, C. The cyclophilin inhibitor alisporivir prevents hepatitis C virus-mediated mitochondrial dysfunction. Hepatology 2012, 55, 1333–1343. [Google Scholar] [CrossRef]
- Lampl, S.; Janas, M.K.; Donakonda, S.; Brugger, M.; Lohr, K.; Schneider, A.; Manske, K.; Sperl, L.E.; Klager, S.; Kuster, B.; et al. Reduced mitochondrial resilience enables non-canonical induction of apoptosis after TNF receptor signaling in virus-infected hepatocytes. J. Hepatol. 2020, 73, 1347–1359. [Google Scholar] [CrossRef] [PubMed]
- Fu, C.; Cao, N.; Liu, W.; Zhang, Z.; Yang, Z.; Zhu, W.; Fan, S. Crosstalk between mitophagy and innate immunity in viral infection. Front. Microbiol. 2022, 13, 1064045. [Google Scholar] [CrossRef]
- Picca, A.; Calvani, R.; Coelho-Junior, H.J.; Marzetti, E. Cell death and inflammation: The role of mitochondria in health and disease. Cells 2021, 10, 537. [Google Scholar] [CrossRef] [PubMed]
- Lee, J.; Ou, J.J. HCV-induced autophagy and innate immunity. Front. Immunol. 2024, 15, 1305157. [Google Scholar] [CrossRef] [PubMed]
- Wang, R.; Zhu, Y.; Ren, C.; Yang, S.; Tian, S.; Chen, H.; Jin, M.; Zhou, H. Influenza A virus protein PB1-F2 impairs innate immunity by inducing mitophagy. Autophagy 2021, 17, 496–511. [Google Scholar] [CrossRef] [PubMed]
- Fan, S.; Wu, K.; Zhao, M.; Yuan, J.; Ma, S.; Zhu, E.; Chen, Y.; Ding, H.; Yi, L.; Chen, J. LDHB inhibition induces mitophagy and facilitates the progression of CSFV infection. Autophagy 2021, 17, 2305–2324. [Google Scholar] [CrossRef] [PubMed]
- Vo, M.T.; Choi, Y.B. Herpesvirus regulation of selective autophagy. Viruses 2021, 13, 820. [Google Scholar] [CrossRef]
- Li, X.; Hou, P.; Ma, W.; Wang, X.; Wang, H.; Yu, Z.; Chang, H.; Wang, T.; Jin, S.; Wang, X.; et al. SARS-CoV-2 ORF10 suppresses the antiviral innate immune response by degrading MAVS through mitophagy. Cell. Mol. Immunol. 2022, 19, 67–78. [Google Scholar] [CrossRef]
- Zhang, B.; Xu, S.; Liu, M.; Wei, Y.; Wang, Q.; Shen, W.; Lei, C.Q.; Zhu, Q. The nucleoprotein of influenza A virus inhibits the innate immune response by inducing mitophagy. Autophagy 2023, 19, 1916–1933. [Google Scholar] [CrossRef]
- Lu, P.; Zheng, H.; Meng, H.; Liu, C.; Duan, L.; Zhang, J.; Zhang, Z.; Gao, J.; Zhang, Y.; Sun, T. Mitochondrial DNA induces nucleus pulposus cell pyroptosis via the TLR9-NF-kappaB-NLRP3 axis. J. Transl. Med. 2023, 21, 389. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.; Zheng, Y.; Huang, J.; Li, J. Mitophagy in antiviral immunity. Front. Cell. Dev. Biol. 2021, 9, 723108. [Google Scholar] [CrossRef] [PubMed]
- Lee, J.K.; Shin, O.S. Zika virus modulates mitochondrial dynamics, mitophagy, and mitochondria-derived vesicles to facilitate viral replication in trophoblast cells. Front. Immunol. 2023, 14, 1203645. [Google Scholar] [CrossRef]
- He, Z.; Guo, L.; Shu, Y.; Fang, Q.; Zhou, H.; Liu, Y.; Liu, D.; Lu, L.; Zhang, X.; Ding, X.; et al. Autophagy protects auditory hair cells against neomycin-induced damage. Autophagy 2017, 13, 1884–1904. [Google Scholar] [CrossRef]
- Luo, P.; An, Y.; He, J.; Xing, X.; Zhang, Q.; Liu, X.; Chen, Y.; Yuan, H.; Chen, J.; Wong, Y.K.; et al. Icaritin with autophagy/mitophagy inhibitors synergistically enhances anticancer efficacy and apoptotic effects through PINK1/Parkin-mediated mitophagy in hepatocellular carcinoma. Cancer Lett. 2024, 587, 216621. [Google Scholar] [CrossRef] [PubMed]
Types of Mitochondrial Damage | Viruses/Viral Proteins | Targeted Pathways/Functional Roles | References |
---|---|---|---|
Increased mitochondrial membrane permeability | PDCoV | BAX-mediated MOMP | [13] |
HSV-1 and SFV | Triggering MOMP through the Puma protein | [14] | |
PRRSV GP5 | Activation of IP3R-GRP75-VDAC1 | [15] | |
DENV | Release of the proinflammatory cytokines-induced mtDNA | [16] | |
Disruption of mitochondrial dynamics | ZIKV | Reduction of the MFN2 protein | [17] |
HIV Vpr | Reduction of the Vpr-related MFN2 | [18] | |
Influenza virus NS1 | The fragmentation of mitochondria | [19] | |
HBV/HCV | PRKN-dependent mitochondrial autophagy | [20,21] | |
IAV | Regulation of autophagy-related signaling pathways | [22] | |
Mitochondrial stress | HCV E1, E2, and NS3 | Inhibition of electron transfer | [23] |
HIV Tat | The Tat protein is translocated from nucleus to mitochondria | [24] |
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Sun, Z.; Wang, Y.; Jin, X.; Li, S.; Qiu, H.-J. Crosstalk between Dysfunctional Mitochondria and Proinflammatory Responses during Viral Infections. Int. J. Mol. Sci. 2024, 25, 9206. https://doi.org/10.3390/ijms25179206
Sun Z, Wang Y, Jin X, Li S, Qiu H-J. Crosstalk between Dysfunctional Mitochondria and Proinflammatory Responses during Viral Infections. International Journal of Molecular Sciences. 2024; 25(17):9206. https://doi.org/10.3390/ijms25179206
Chicago/Turabian StyleSun, Zitao, Yanjin Wang, Xin Jin, Su Li, and Hua-Ji Qiu. 2024. "Crosstalk between Dysfunctional Mitochondria and Proinflammatory Responses during Viral Infections" International Journal of Molecular Sciences 25, no. 17: 9206. https://doi.org/10.3390/ijms25179206