Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

Mitophagy and Innate Immunity in Infection

  • Cho, Dong-Hyung (School of Life Sciences, Kyungpook National University) ;
  • Kim, Jin Kyung (Department of Microbiology, Chungnam National University School of Medicine) ;
  • Jo, Eun-Kyeong (Department of Microbiology, Chungnam National University School of Medicine)
  • Received : 2019.12.24
  • Accepted : 2020.01.08
  • Published : 2020.01.31
Download PDF
⟨ Previous Next ⟩

Abstract

Mitochondria have several quality control mechanisms by which they maintain cellular homeostasis and ensure that the molecular machinery is protected from stress. Mitophagy, selective autophagy of mitochondria, promotes mitochondrial quality control by inducing clearance of damaged mitochondria via the autophagic machinery. Accumulating evidence suggests that mitophagy is modulated by various microbial components in an attempt to affect the innate immune response to infection. In addition, mitophagy plays a key role in the regulation of inflammatory signaling, and mitochondrial danger signals such as mitochondrial DNA translocated into the cytosol can lead to exaggerated inflammatory responses. In this review, we present current knowledge on the functional aspects of mitophagy and its crosstalk with innate immune signaling during infection. A deeper understanding of the role of mitophagy could facilitate the development of more effective therapeutic strategies against various infections.

Keywords

References

  1. Amatullah, H., Shan, Y., Beauchamp, B.L., Gali, P.L., Gupta, S., Maron-Gutierrez, T., Speck, E.R., Fox-Robichaud, A.E., Tsang, J.L., Mei, S.H., et al. (2017). DJ-1/PARK7 impairs bacterial clearance in sepsis. Am. J. Respir. Crit. Care Med. 195, 889-905. https://doi.org/10.1164/rccm.201604-0730OC
  2. Asrat, S., de Jesus, D.A., Hempstead, A.D., Ramabhadran, V., and Isberg, R.R. (2014). Bacterial pathogen manipulation of host membrane trafficking. Annu. Rev. Cell Dev. Biol. 30, 79-109. https://doi.org/10.1146/annurev-cellbio-100913-013439
  3. Bento, C.F., Empadinhas, N., and Mendes, V. (2015). Autophagy in the fight against tuberculosis. DNA Cell Biol. 34, 228-242. https://doi.org/10.1089/dna.2014.2745
  4. Bingol, B., Tea, J.S., Phu, L., Reichelt, M., Bakalarski, C.E., Song, Q., Foreman, O., Kirkpatrick, D.S., and Sheng, M. (2014). The mitochondrial deubiquitinase USP30 opposes parkin-mediated mitophagy. Nature 510, 370-375. https://doi.org/10.1038/nature13418
  5. Burman, J.L., Pickles, S., Wang, C., Sekine, S., Vargas, J.N.S., Zhang, Z., Youle, A.M., Nezich, C.L., Wu, X., Hammer, J.A., et al. (2017). Mitochondrial fission facilitates the selective mitophagy of protein aggregates. J. Cell Biol. 216, 3231-3247. https://doi.org/10.1083/jcb.201612106
  6. Chen, G., Han, Z., Feng, D., Chen, Y., Chen, L., Wu, H., Huang, L., Zhou, C., Cai, X., Fu, C., et al. (2014). A regulatory signaling loop comprising the PGAM5 phosphatase and CK2 controls receptor-mediated mitophagy. Mol. Cell 54, 362-377. https://doi.org/10.1016/j.molcel.2014.02.034
  7. Chew, T.S., O'Shea, N.R., Sewell, G.W., Oehlers, S.H., Mulvey, C.M., Crosier, P.S., Godovac-Zimmermann, J., Bloom, S.L., Smith, A.M., and Segal, A.W. (2015). Optineurin deficiency in mice contributes to impaired cytokine secretion and neutrophil recruitment in bacteria-driven colitis. Dis. Model. Mech. 8, 817-829. https://doi.org/10.1242/dmm.020362
  8. Cho, D.H., Nakamura, T., and Lipton, S.A. (2010). Mitochondrial dynamics in cell death and neurodegeneration. Cell. Mol. Life Sci. 67, 3435-3447. https://doi.org/10.1007/s00018-010-0435-2
  9. Choi, Y.B., Shembade, N., Parvatiyar, K., Balachandran, S., and Harhaj, E.W. (2017). TAX1BP1 restrains virus-induced apoptosis by facilitating itchmediated degradation of the mitochondrial adaptor MAVS. Mol. Cell. Biol. 37, e00422-16.
  10. Cloonan, S.M. and Choi, A.M. (2013). Mitochondria: sensors and mediators of innate immune receptor signaling. Curr. Opin. Microbiol. 16, 327-338. https://doi.org/10.1016/j.mib.2013.05.005
  11. Colonne, P.M., Winchell, C.G. and Voth, D.E. (2016). Hijacking host cell highways: Manipulation of the host actin cytoskeleton by obligate intracellular bacterial pathogens. Front. Cell. Infect. Microbiol. 6, 107.
  12. Cui, J., Chen, Y., Wang, H.Y., and Wang, R.F. (2014). Mechanisms and pathways of innate immune activation and regulation in health and cancer. Hum. Vaccin. Immunother. 10, 3270-3285. https://doi.org/10.4161/21645515.2014.979640
  13. Dalrymple, N.A., Cimica, V., and Mackow, E.R. (2015). Dengue virus NS proteins inhibit RIG-I/MAVS signaling by blocking TBK1/IRF3 phosphorylation: Dengue virus serotype 1 NS4A is a unique interferon-regulating virulence determinant. mBio 6, e00553-15.
  14. Deng, Z., Purtell, K., Lachance, V., Wold, M.S., Chen, S., and Yue, Z. (2017). Autophagy receptors and neurodegenerative diseases. Trends Cell Biol. 27, 491-504. https://doi.org/10.1016/j.tcb.2017.01.001
  15. Ding, B., Zhang, L., Li, Z., Zhong, Y., Tang, Q., Qin, Y., and Chen, M. (2017). The matrix protein of human parainfluenza virus type 3 induces mitophagy that suppresses interferon responses. Cell Host Microbe 21, 538-547.e4. https://doi.org/10.1016/j.chom.2017.03.004
  16. Dromparis, P. and Michelakis, E.D. (2013). Mitochondria in vascular health and disease. Annu. Rev. Physiol. 75, 95-126. https://doi.org/10.1146/annurev-physiol-030212-183804
  17. Du, Y., Duan, T., Feng, Y., Liu, Q., Lin, M., Cui, J., and Wang, R.F. (2018). LRRC25 inhibits type I IFN signaling by targeting ISG15-associated RIG-I for autophagic degradation. EMBO J. 37, 351-366. https://doi.org/10.15252/embj.201796781
  18. Gegg, M.E., Cooper, J.M., Chau, K.Y., Rojo, M., Schapira, A.H., and Taanman, J.W. (2010). Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/parkin-dependent manner upon induction of mitophagy. Hum. Mol. Genet. 19, 4861-4870. https://doi.org/10.1093/hmg/ddq419
  19. Geisler, S., Holmstrom, K.M., Skujat, D., Fiesel, F.C., Rothfuss, O.C., Kahle, P.J., and Springer, W. (2010). PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 12, 119-131. https://doi.org/10.1038/ncb2012
  20. Gkikas, I., Palikaras, K., and Tavernarakis, N. (2018). The role of mitophagy in innate immunity. Front. Immunol. 9, 1283. https://doi.org/10.3389/fimmu.2018.01283
  21. Gomes, L.C. and Scorrano, L. (2013). Mitochondrial morphology in mitophagy and macroautophagy. Biochim. Biophys. Acta 1833, 205-212. https://doi.org/10.1016/j.bbamcr.2012.02.012
  22. Gou, H., Zhao, M., Xu, H., Yuan, J., He, W., Zhu, M., Ding, H., Yi, L., and Chen, J. (2017). CSFV induced mitochondrial fission and mitophagy to inhibit apoptosis. Oncotarget 8, 39382-39400. https://doi.org/10.18632/oncotarget.17030
  23. Hara, Y., Yanatori, I., Ikeda, M., Kiyokage, E., Nishina, S., Tomiyama, Y., Toida, K., Kishi, F., Kato, N., Imamura, M., et al. (2014). Hepatitis C virus core protein suppresses mitophagy by interacting with parkin in the context of mitochondrial depolarization. Am. J. Pathol. 184, 3026-3039. https://doi.org/10.1016/j.ajpath.2014.07.024
  24. Hawn, T.R., Shah, J.A., and Kalman, D. (2015). New tricks for old dogs: countering antibiotic resistance in tuberculosis with host-directed therapeutics. Immunol. Rev. 264, 344-362. https://doi.org/10.1111/imr.12255
  25. He, X., Zhu, Y., Zhang, Y., Geng, Y., Gong, J., Geng, J., Zhang, P., Zhang, X., Liu, N., Peng, Y., et al. (2019). RNF34 functions in immunity and selective mitophagy by targeting MAVS for autophagic degradation. EMBO J. 38, e100978.
  26. Heo, J.M., Ordureau, A., Paulo, J.A., Rinehart, J., and Harper, J.W. (2015). The PINK1-PARKIN mitochondrial ubiquitylation pathway drives a program of OPTN/NDP52 recruitment and TBK1 activation to promote mitophagy. Mol. Cell 60, 7-20. https://doi.org/10.1016/j.molcel.2015.08.016
  27. Hino, K., Nishina, S., Sasaki, K., and Hara, Y. (2019). Mitochondrial damage and iron metabolic dysregulation in hepatitis C virus infection. Free Radic. Biol. Med. 133, 193-199. https://doi.org/10.1016/j.freeradbiomed.2018.09.044
  28. Hirota, Y., Tamashita, S., Kurihara, Y., Jin, X., Aihara, M., Saigusa, T., Kang, D., and Kanki, T. (2015). Mitophagy is primarily due to alterative autophagy and requires the MAPK1 and MAPK14 signaling pathways. Autophagy 11, 332-343. https://doi.org/10.1080/15548627.2015.1023047
  29. Hollville, E., Carroll, R.G., Cullen, S.P., and Martin, S.J. (2014). Bcl-2 family proteins participate in mitochondrial quality control by regulating Parkin/PINK1-dependent mitophagy. Mol. Cell 55, 451-466. https://doi.org/10.1016/j.molcel.2014.06.001
  30. Hu, Y.W., Zhang, J., Wu, X.M., Cao, L., Nie, P., and Chang, M.X. (2018). TANK-Binding Kinase 1 (TBK1) isoforms negatively regulate type I interferon induction by inhibiting TBK1-IRF3 interaction and IRF3 phosphorylation. Front. Immunol. 9, 84. https://doi.org/10.3389/fimmu.2018.00084
  31. Ishii, K.J., Koyama, S., Nakagawa, A., Coban, C., and Akira, S. (2008). Host innate immune receptors and beyond: making sense of microbial infections. Cell Host Microbe 3, 352-363. https://doi.org/10.1016/j.chom.2008.05.003
  32. Jabir, M.S., Hopkins, L., Ritchie, N.D., Ullah, I., Bayes, H.K., Li, D., Tourlomousis, P., Lupton, A., Puleston, D., Simon, A.K., et al. (2015). Mitochondrial damage contributes to Pseudomonas aeruginosa activation of the inflammasome and is downregulated by autophagy. Autophagy 11, 166-182. https://doi.org/10.4161/15548627.2014.981915
  33. Jabir, M.S., Ritchie, N.D., Li, D., Bayes, H.K., Tourlomousis, P., Puleston, D., Lupton, A., Hopkins, L., Simon, A.K., Bryant, C., et al. (2014). Caspase-1 cleavage of the TLR adaptor TRIF inhibits autophagy and beta-interferon production during Pseudomonas aeruginosa infection. Cell Host Microbe 15, 214-227. https://doi.org/10.1016/j.chom.2014.01.010
  34. Jassey, A., Liu, C.H., Changou, C.A., Richardson, C.D., Hsu, H.Y., and Lin, L.T. (2019). Hepatitis C virus non-structural protein 5A (NS5A) disrupts mitochondrial dynamics and induces mitophagy. Cells 8, E290. https://doi.org/10.3390/cells8040290
  35. Jin, H.S., Suh, H.W., Kim, S.J., and Jo, E.K. (2017a). Mitochondrial control of innate immunity and inflammation. Immune Netw. 17, 77-88. https://doi.org/10.4110/in.2017.17.2.77
  36. Jin, S., Tian, S., Luo, M., Xie, W., Liu, T., Duan, T., Wu, Y., and Cui, J. (2017b). Tetherin suppresses type I interferon signaling by targeting MAVS for NDP52-mediated selective autophagic degradation in human cells. Mol. Cell 68, 308-322.e4. https://doi.org/10.1016/j.molcel.2017.09.005
  37. Jin, S.M., Lazarou, M., Wang, C., Kane, L.A., Narendra, D.P., and Youle, R.J. (2010). Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J. Cell Biol. 191, 933-942. https://doi.org/10.1083/jcb.201008084
  38. Jing, K., Shin, S., Jeong, S., Kim, S., Song, K.S., Park, J.H., Heo, J.Y., Seo, K.S., Park, S.K., Kweon, G.R., et al. (2014). Docosahexaenoic acid induces the degradation of HPV E6/E7 oncoproteins by activating the ubiquitin-proteasome system. Cell Death Dis. 5, e1524. https://doi.org/10.1038/cddis.2014.477
  39. Kang, R., Zeng, L., Xie, Y., Yan, Z., Zhou, B., Cao, L., Klionsky, D.J., Tracey, K.J., Li, J., Wang, H., et al. (2016). A novel PINK1- and PARK2-dependent protective neuroimmune pathway in lethal sepsis. Autophagy 12, 2374-2385. https://doi.org/10.1080/15548627.2016.1239678
  40. Kawai, T. and Akira, S. (2011). Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34, 637-650. https://doi.org/10.1016/j.immuni.2011.05.006
  41. Kim, M.J., Bae, S.H., Ryu, J.C., Kwon, Y., Oh, J.H., Kwon, J., Moon, J.S., Kim, K., Miyawaki, A., Lee, M.G., et al. (2016). SESN2/sestrin2 suppresses sepsis by inducing mitophagy and inhibiting NLRP3 activation in macrophages. Autophagy 12, 1272-1291. https://doi.org/10.1080/15548627.2016.1183081
  42. Kim, S.J., Jang, J.Y., Kim, E.J., Cho, E.K., Ahn, D.G., Kim, C., Park, H.S., Jeong, S.W., Lee, S.H., Kim, S.G., et al. (2017). Ginsenoside Rg3 restores hepatitis C virus-induced aberrant mitochondrial dynamics and inhibits virus propagation. Hepatology 66, 758-771. https://doi.org/10.1002/hep.29177
  43. Kim, S.J., Khan, M., Quan, J., Till, A., Subramani, S., and Siddiqui, A. (2013a). Hepatitis B virus disrupts mitochondrial dynamics: induces fission and mitophagy to attenuate apoptosis. PLoS Pathog. 9, e1003722. https://doi.org/10.1371/journal.ppat.1003722
  44. Kim, S.J., Syed, G.H., and Siddiqui, A. (2013b). Hepatitis C virus induces the mitochondrial translocation of Parkin and subsequent mitophagy. PLoS Pathog. 9, e1003285. https://doi.org/10.1371/journal.ppat.1003285
  45. Kim, S.J., Syed, G.H., Khan, M., Chiu, W.W., Sohail, M.A., Gish, R.G., and Siddiqui, A. (2014). Hepatitis C virus triggers mitochondrial fission and attenuates apoptosis to promote viral persistence. Proc. Natl. Acad. Sci. U. S. A. 111, 6413-6418. https://doi.org/10.1073/pnas.1321114111
  46. Klein, C. and Westenberger, A. (2012). Genetics of Parkinson's disease. Cold Spring Harb. Perspect. Med. 2, a008888. https://doi.org/10.1101/cshperspect.a008888
  47. Krakauer, T. (2019). Inflammasomes, autophagy, and cell death: the trinity of innate host defense against intracellular bacteria. Mediators Inflamm. 2019, 2471215.
  48. Kurose, I., Miura, S., Fukumura, D., Yonei, Y., Saito, H., Tada, S., Suematsu, M., and Tsuchiya, M. (1993). Nitric oxide mediates Kupffer cell-induced reduction of mitochondrial energization in hepatoma cells: a comparison with oxidative burst. Cancer Res. 53, 2676-2682.
  49. Lazarou, M., Sliter, D.A., Kane, L.A., Sarraf, S.A., Wang, C., Burman, J.L., Sideris, D.P., Fogel, A.I., and Youle, R.J. (2015). The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature 524, 309-314. https://doi.org/10.1038/nature14893
  50. Li, J., Ma, C., Long, F., Yang, D., Liu, X., Hu, Y., Wu, C., Wang, B., Wang, M., Chen, Y., et al. (2019). Parkin impairs antiviral immunity by suppressing the mitochondrial reactive oxygen species-Nlrp3 axis and antiviral inflammation. iScience 16, 468-484. https://doi.org/10.1016/j.isci.2019.06.008
  51. Li, S., Wang, J., Zhou, A., Khan, F.A., Hu, L., and Zhang, S. (2016). Porcine reproductive and respiratory syndrome virus triggers mitochondrial fission and mitophagy to attenuate apoptosis. Oncotarget 7, 56002-56012. https://doi.org/10.18632/oncotarget.10817
  52. Li, S., Wu, H., Han, D., Ma, S., Fan, W., Wang, Y., Zhang, R., Fan, M., Huang, Y., Fu, X., et al. (2018). A novel mechanism of mesenchymal stromal cellmediated protection against sepsis: restricting inflammasome activation in macrophages by increasing mitophagy and decreasing mitochondrial ROS. Oxid. Med. Cell. Longev. 2018, 3537609.
  53. Liu, L., Feng, D., Chen, G., Chen, M., Zheng, Q., Song, P., Ma, Q., Zhu, C., Wang, R., Qi, W., et al. (2012a). Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat. Cell Biol. 14, 177-185. https://doi.org/10.1038/ncb2422
  54. Liu, S., Sawada, T., Lee, S., Yu, W., Silverio, G., Alapatt, P., Millan, I., Shen, A., Saxton, W., Kanao, T., et al. (2012b). Parkinson's disease-associated kinase PINK1 regulates Miro protein level and axonal transport of mitochondria. PLoS Genet. 8, e1002537. https://doi.org/10.1371/journal.pgen.1002537
  55. Mannam, P., Shinn, A.S., Srivastava, A., Neamu, R.F., Walker, W.E., Bohanon, M., Merkel, J., Kang, M.J., Dela Cruz, C.S., Ahasic, A.M., et al. (2014). MKK3 regulates mitochondrial biogenesis and mitophagy in sepsis-induced lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 306, L604-L619. https://doi.org/10.1152/ajplung.00272.2013
  56. Martinon, F., Mayor, A., and Tschopp, J. (2009). The inflammasomes: guardians of the body. Annu. Rev. Immunol. 27, 229-265. https://doi.org/10.1146/annurev.immunol.021908.132715
  57. Matheoud, D., Cannon, T., Voisin, A., Penttinen, A.M., Ramet, L., Fahmy, A.M., Ducrot, C., Laplante, A., Bourque, M.J., Zhu, L., et al. (2019). Intestinal infection triggers Parkinson's disease-like symptoms in Pink1(-/-) mice. Nature 571, 565-569. https://doi.org/10.1038/s41586-019-1405-y
  58. McGuire, V.A. and Arthur, J.S. (2015). Subverting toll-like receptor signaling by bacterial pathogens. Front. Immunol. 6, 607.
  59. Meng, G., Xia, M., Wang, D., Chen, A., Wang, Y., Wang, H., Yu, D., and Wei, J. (2014). Mitophagy promotes replication of oncolytic Newcastle disease virus by blocking intrinsic apoptosis in lung cancer cells. Oncotarget 5, 6365-6374. https://doi.org/10.18632/oncotarget.2219
  60. Mohamud, Y., Qu, J., Xue, Y.C., Liu, H., Deng, H., and Luo, H. (2019). CALCOCO2/NDP52 and SQSTM1/p62 differentially regulate coxsackievirus B3 propagation. Cell Death Differ. 26, 1062-1076. https://doi.org/10.1038/s41418-018-0185-5
  61. Mohanty, A., Tiwari-Pandey, R., and Pandey, N.R. (2019). Mitochondria: the indispensable players in innate immunity and guardians of the inflammatory response. J. Cell Commun. Signal. 13, 303-318. https://doi.org/10.1007/s12079-019-00507-9
  62. Montava-Garriga, L. and Ganley, I.G. (2020). Outstanding questions in mitophagy: what we do and do not know. J. Mol. Biol. 432, 206-230. https://doi.org/10.1016/j.jmb.2019.06.032
  63. Murray, P.J. and Wynn, T.A. (2011). Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11, 723-737. https://doi.org/10.1038/nri3073
  64. Nagi, M., Tanabe, K., Nakayama, H., Ueno, K., Yamagoe, S., Umeyama, T., Ohno, H., and Miyazaki, Y. (2016). Iron-depletion promotes mitophagy to maintain mitochondrial integrity in pathogenic yeast Candida glabrata. Autophagy 12, 1259-1271. https://doi.org/10.1080/15548627.2016.1183080
  65. Narendra, D., Tanaka, A., Suen, D.F., and Youle, R.J. (2008). Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183, 795-803. https://doi.org/10.1083/jcb.200809125
  66. Narendra, D.P., Jin, S.M., Tanaka, A., Suen, D.F., Gautier, C.A., Shen, J., Cookson, M.R., and Youle, R.J. (2010). PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 8, e1000298. https://doi.org/10.1371/journal.pbio.1000298
  67. Ney, P.A. (2015). Mitochondrial autophagy: origins, significance, and role of BNIP3 and NIX. Biochim. Biophys. Acta 1853, 2775-2783. https://doi.org/10.1016/j.bbamcr.2015.02.022
  68. Niller, H.H., Masa, R., Venkei, A., Meszaros, S., and Minarovits, J. (2017). Pathogenic mechanisms of intracellular bacteria. Curr. Opin. Infect. Dis. 30, 309-315. https://doi.org/10.1097/QCO.0000000000000363
  69. Novak, I., Kirkin, V., McEwan, D.G., Zhang, J., Wild, P., Rozenknop, A., Rogov, V., Lohr, F., Popovic, D., Occhipinti, A., et al. (2010). Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 11, 45-51. https://doi.org/10.1038/embor.2009.256
  70. Ogawa, M., Mimuro, H., Yoshikawa, Y., Ashida, H., and Sasakawa, C. (2011). Manipulation of autophagy by bacteria for their own benefit. Microbiol. Immunol. 55, 459-471. https://doi.org/10.1111/j.1348-0421.2011.00343.x
  71. Ojeda, D.S., Grasso, D., Urquiza, J., Till, A., Vaccaro, M.I., and Quarleri, J. (2018). Cell death is counteracted by mitophagy in HIV-productively infected astrocytes but is promoted by inflammasome activation among non-productively infected cells. Front. Immunol. 9, 2633. https://doi.org/10.3389/fimmu.2018.02633
  72. Oka, T., Hikoso, S., Yamaguchi, O., Taneike, M., Takeda, T., Tamai, T., Oyabu, J., Murakawa, T., Nakayama, H., Nishida, K., et al. (2012). Mitochondrial DNA that escapes from autophagy causes inflammation and heart failure. Nature 485, 251-255. https://doi.org/10.1038/nature10992
  73. Paik, S., Kim, J.K., Chung, C., and Jo, E.K. (2018). Autophagy: a new strategy for host-directed therapy of tuberculosis. Virulence 10, 1-12. https://doi.org/10.1080/21505594.2018.1551708
  74. Pareja, M.E. and Colombo, M.I. (2013). Autophagic clearance of bacterial pathogens: molecular recognition of intracellular microorganisms. Front. Cell. Infect. Microbiol. 3, 54.
  75. Pickles, S., Vigie, P., and Youle, R.J. (2018). Mitophagy and quality control mechanisms in mitochondrial maintenance. Curr. Biol. 28, R170-R185. https://doi.org/10.1016/j.cub.2018.01.004
  76. Pilli, M., Arko-Mensah, J., Ponpuak, M., Roberts, E., Master, S., Mandell, M.A., Dupont, N., Ornatowski, W., Jiang, S., Bradfute, S.B., et al. (2012). TBK-1 promotes autophagy-mediated antimicrobial defense by controlling autophagosome maturation. Immunity 37, 223-234. https://doi.org/10.1016/j.immuni.2012.04.015
  77. Piquereau, J., Godin, R., Deschenes, S., Bessi, V.L., Mofarrahi, M., Hussain, S.N., and Burelle, Y. (2013). Protective role of PARK2/Parkin in sepsis-induced cardiac contractile and mitochondrial dysfunction. Autophagy 9, 1837-1851. https://doi.org/10.4161/auto.26502
  78. Quinsay, M.N., Thomas, R.L., Lee, Y., and Gustafsson, A.B. (2010). Bnip3-mediated mitochondrial autophagy is independent of the mitochondrial permeability transition pore. Autophagy 6, 855-862. https://doi.org/10.4161/auto.6.7.13005
  79. Rademann, P., Weidinger, A., Drechsler, S., Meszaros, A., Zipperle, J., Jafarmadar, M., Dumitrescu, S., Hacobian, A., Ungelenk, L., Rostel, F., et al. (2017). Mitochondria-targeted antioxidants SkQ1 and MitoTEMPO failed to exert a long-term beneficial effect in murine polymicrobial sepsis. Oxid. Med. Cell. Longev. 2017, 6412682.
  80. Randow, F. and Munz, C. (2012). Autophagy in the regulation of pathogen replication and adaptive immunity. Trends Immunol. 33, 475-487. https://doi.org/10.1016/j.it.2012.06.003
  81. Rawat, P., Teodorof-Diedrich, C., and Spector, S.A. (2019). Human immunodeficiency virus Type-1 single-stranded RNA activates the NLRP3 inflammasome and impairs autophagic clearance of damaged mitochondria in human microglia. Glia 67, 802-824. https://doi.org/10.1002/glia.23568
  82. Richter, B., Sliter, D.A., Herhaus, L., Stolz, A., Wang, C., Beli, P., Zaffagnini, G., Wild, P., Martens, S., Wagner, S.A., et al. (2016). Phosphorylation of OPTN by TBK1 enhances its binding to Ub chains and promotes selective autophagy of damaged mitochondria. Proc. Natl. Acad. Sci. U. S. A. 113, 4039-4044. https://doi.org/10.1073/pnas.1523926113
  83. Schulze-Osthoff, K., Bakker, A.C., Vanhaesebroeck, B., Beyaert, R., Jacob, W.A., and Fiers, W. (1992). Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions. Evidence for the involvement of mitochondrial radical generation. J. Biol. Chem. 267, 5317-5323. https://doi.org/10.1016/S0021-9258(18)42768-8
  84. Shi, G. and McQuibban, G.A. (2017). The mitochondrial rhomboid protease PARL is regulated by PDK2 to integrate mitochondrial quality control and metabolism. Cell Rep. 18, 1458-1472. https://doi.org/10.1016/j.celrep.2017.01.029
  85. Shi, J., Wong, J., Piesik, P., Fung, G., Zhang, J., Jagdeo, J., Li, X., Jan, E., and Luo, H. (2013). Cleavage of sequestosome 1/p62 by an enteroviral protease results in disrupted selective autophagy and impaired NFKB signaling. Autophagy 9, 1591-1603. https://doi.org/10.4161/auto.26059
  86. Silva, M.T. (2011). Macrophage phagocytosis of neutrophils at inflammatory/infectious foci: a cooperative mechanism in the control of infection and infectious inflammation. J. Leukoc. Biol. 89, 675-683. https://doi.org/10.1189/jlb.0910536
  87. Sin, J., McIntyre, L., Stotland, A., Feuer, R., and Gottlieb, R.A. (2017). Coxsackievirus B escapes the infected cell in ejected mitophagosomes. J. Virol. 91, e01347-17.
  88. Sliter, D.A., Martinez, J., Hao, L., Chen, X., Sun, N., Fischer, T.D., Burman, J.L., Li, Y., Zhang, Z., Narendra, D.P., et al. (2018). Parkin and PINK1 mitigate STING-induced inflammation. Nature 561, 258-262. https://doi.org/10.1038/s41586-018-0448-9
  89. Snell, L.M., McGaha, T.L., and Brooks, D.G. (2017). Type I interferon in chronic virus infection and cancer. Trends Immunol. 38, 542-557. https://doi.org/10.1016/j.it.2017.05.005
  90. Sorbara, M.T. and Girardin, S.E. (2015). Emerging themes in bacterial autophagy. Curr. Opin. Microbiol. 23, 163-170. https://doi.org/10.1016/j.mib.2014.11.020
  91. Srivastava, A., McGinniss, J., Wong, Y., Shinn, A.S., Lam, T.T., Lee, P.J., and Mannam, P. (2015). MKK3 deletion improves mitochondrial quality. Free Radic. Biol. Med. 87, 373-384. https://doi.org/10.1016/j.freeradbiomed.2015.06.024
  92. Sumpter, R., Jr. and Levine, B. (2010). Autophagy and innate immunity: triggering, targeting and tuning. Semin. Cell Dev. Biol. 21, 699-711. https://doi.org/10.1016/j.semcdb.2010.04.003
  93. Sun, S., Sursal, T., Adibnia, Y., Zhao, C., Zheng, Y., Li, H., Otterbein, L.E., Hauser, C.J., and Itagaki, K. (2013). Mitochondrial DAMPs increase endothelial permeability through neutrophil dependent and independent pathways. PLoS One 8, e59989. https://doi.org/10.1371/journal.pone.0059989
  94. Tal, M.C. and Iwasaki, A. (2011). Mitoxosome: a mitochondrial platform for cross-talk between cellular stress and antiviral signaling. Immunol. Rev. 243, 215-234. https://doi.org/10.1111/j.1600-065X.2011.01038.x
  95. Tang, D., Kang, R., Coyne, C.B., Zeh, H.J., and Lotze, M.T. (2012). PAMPs and DAMPs: signal 0s that spur autophagy and immunity. Immunol. Rev. 249, 158-175. https://doi.org/10.1111/j.1600-065X.2012.01146.x
  96. Taylor, D.E., Ghio, A.J., and Piantadosi, C.A. (1995). Reactive oxygen species produced by liver mitochondria of rats in sepsis. Arch. Biochem. Biophys. 316, 70-76. https://doi.org/10.1006/abbi.1995.1011
  97. Teodorof-Diedrich, C. and Spector, S.A. (2018). Human immunodeficiency virus type 1 gp120 and Tat induce mitochondrial fragmentation and incomplete mitophagy in human neurons. J. Virol. 92, e00993-18.
  98. To, E.E., Erlich, J.R., Liong, F., Luong, R., Liong, S., Esaq, F., Oseghale, O., Anthony, D., McQualter, J., Bozinovski, S., et al. (2019). Mitochondrial reactive oxygen species contribute to pathological inflammation during influenza A virus infection in mice. Antioxid. Redox Signal. 2019 Jul 12 [Epub]. doi: 10.1089/ars.2019.7727.
  99. Tsao, N., Kuo, C.F., Cheng, M.H., Lin, W.C., Lin, C.F., and Lin, Y.S. (2019). Streptolysin S induces mitochondrial damage and macrophage death through inhibiting degradation of glycogen synthase kinase-3beta in Streptococcus pyogenes infection. Sci. Rep. 9, 5371. https://doi.org/10.1038/s41598-019-41853-3
  100. Tschurtschenthaler, M. and Adolph, T.E. (2018). The selective autophagy receptor Optineurin in Crohn's disease. Front. Immunol. 9, 766. https://doi.org/10.3389/fimmu.2018.00766
  101. Vo, M.T., Smith, B.J., Nicholas, J., and Choi, Y.B. (2019). Activation of NIXmediated mitophagy by an interferon regulatory factor homologue of human herpesvirus. Nat. Commun. 10, 3203. https://doi.org/10.1038/s41467-019-11164-2
  102. Wang, K., Ma, H., Liu, H., Ye, W., Li, Z., Cheng, L., Zhang, L., Lei, Y., Shen, L., and Zhang, F. (2019a). The glycoprotein and nucleocapsid protein of Hantaviruses manipulate autophagy flux to restrain host innate immune responses. Cell Rep. 27, 2075-2091.e5. https://doi.org/10.1016/j.celrep.2019.04.061
  103. Wang, Y., Serricchio, M., Jauregui, M., Shanbhag, R., Stoltz, T., Di Paolo, C.T., Kim, P.K., and McQuibban, G.A. (2015). Deubiquitinating enzymes regulate PARK2-mediated mitophagy. Autophagy 11, 595-606. https://doi.org/10.1080/15548627.2015.1034408
  104. Wang, Z.T., Lu, M.H., Zhang, Y., Ji, W.L., Lei, L., Wang, W., Fang, L.P., Wang, L.W., Yu, F., Wang, J., et al. (2019b). Disrupted-in-schizophrenia-1 protects synaptic plasticity in a transgenic mouse model of Alzheimer's disease as a mitophagy receptor. Aging Cell 18, e12860. https://doi.org/10.1111/acel.12860
  105. Wei, Y., Chiang, W.C., Sumpter, R., Jr., Mishra, P., and Levine, B. (2017). Prohibitin 2 is an inner mitochondrial membrane mitophagy receptor. Cell 168, 224-238.e10. https://doi.org/10.1016/j.cell.2016.11.042
  106. Weidberg, H. and Elazar, Z. (2011). TBK1 mediates crosstalk between the innate immune response and autophagy. Sci. Signal. 4, pe39. https://doi.org/10.1126/scisignal.2001430
  107. Wong, Y.C. and Holzbaur, E.L. (2014). Optineurin is an autophagy receptor for damaged mitochondria in parkin-mediated mitophagy that is disrupted by an ALS-linked mutation. Proc. Natl. Acad. Sci. U. S. A. 111, E4439-E4448. https://doi.org/10.1073/pnas.1405752111
  108. Wu, W., Tian, W., Hu, Z., Chen, G., Huang, L., Li, W., Zhang, X., Xue, P., Zhou, C., Liu, L., et al. (2014). ULK1 translocates to mitochondria and phosphorylates FUNDC1 to regulate mitophagy. EMBO Rep. 15, 566-575. https://doi.org/10.1002/embr.201438501
  109. Xia, M., Gonzalez, P., Li, C., Meng, G., Jiang, A., Wang, H., Gao, Q., Debatin, K.M., Beltinger, C., and Wei, J. (2014a). Mitophagy enhances oncolytic measles virus replication by mitigating DDX58/RIG-I-like receptor signaling. J. Virol. 88, 5152-5164. https://doi.org/10.1128/JVI.03851-13
  110. Xia, M., Meng, G., Jiang, A., Chen, A., Dahlhaus, M., Gonzalez, P., Beltinger, C., and Wei, J. (2014b). Mitophagy switches cell death from apoptosis to necrosis in NSCLC cells treated with oncolytic measles virus. Oncotarget 5, 3907-3918. https://doi.org/10.18632/oncotarget.2028
  111. Xian, H., Yang, S., Jin, S., Zhang, Y. and Cui, J. (2019). LRRC59 modulates type I interferon signaling by restraining the SQSTM1/p62-mediated autophagic degradation of pattern recognition receptor DDX58/RIG-I. Autophagy 2019 May 22 [Epub]. doi: 10.1080/15548627.2019.1615303.
  112. Xu, Y., Shen, J., and Ran, Z. (2019). Emerging views of mitophagy in immunity and autoimmune diseases. Autophagy 16, 3-17.
  113. Yoo, S.M. and Jung, Y.K. (2018). A molecular approach to mitophagy and mitochondrial dynamics. Mol. Cells 41, 18-26. https://doi.org/10.14348/MOLCELLS.2018.2277
  114. Yoshizumi, T., Ichinohe, T., Sasaki, O., Otera, H., Kawabata, S., Mihara, K., and Koshiba, T. (2014). Influenza A virus protein PB1-F2 translocates into mitochondria via Tom40 channels and impairs innate immunity. Nat. Commun. 5, 4713. https://doi.org/10.1038/ncomms5713
  115. Youle, R.J. and van der Bliek, A.M. (2012). Mitochondrial fission, fusion, and stress. Science 337, 1062-1065. https://doi.org/10.1126/science.1219855
  116. Zachari, M., Gudmundsson, S.R., Li, Z., Manifava, M., Shah, R., Smith, M., Stronge, J., Karanasios, E., Piunti, C., Kishi-Itakura, C., et al. (2019). Selective autophagy of mitochondria on a ubiquitin-endoplasmic-reticulum platform. Dev. Cell 50, 627-643.e5. https://doi.org/10.1016/j.devcel.2019.06.016
  117. Zhang, Q., Kuang, H., Chen, C., Yan, J., Do-Umehara, H.C., Liu, X.Y., Dada, L., Ridge, K.M., Chandel, N.S., and Liu, J. (2015). The kinase Jnk2 promotes stress-induced mitophagy by targeting the small mitochondrial form of the tumor suppressor ARF for degradation. Nat. Immunol. 16, 458-466. https://doi.org/10.1038/ni.3130
  118. Zhang, R., Varela, M., Vallentgoed, W., Forn-Cuni, G., van der Vaart, M., and Meijer, A.H. (2019a). The selective autophagy receptors Optineurin and p62 are both required for zebrafish host resistance to mycobacterial infection. PLoS Pathog. 15, e1007329. https://doi.org/10.1371/journal.ppat.1007329
  119. Zhang, X., Yuan, D., Sun, Q., Xu, L., Lee, E., Lewis, A.J., Zuckerbraun, B.S., and Rosengart, M.R. (2017). Calcium/calmodulin-dependent protein kinase regulates the PINK1/Parkin and DJ-1 pathways of mitophagy during sepsis. FASEB J. 31, 4382-4395. https://doi.org/10.1096/fj.201601096RRR
  120. Zhang, Y., Yao, Y., Qiu, X., Wang, G., Hu, Z., Chen, S., Wu, Z., Yuan, N., Gao, H., Wang, J., et al. (2019b). Listeria hijacks host mitophagy through a novel mitophagy receptor to evade killing. Nat. Immunol. 20, 433-446. https://doi.org/10.1038/s41590-019-0324-2
  121. Zhao, C. and Zhao, W. (2019). TANK-binding kinase 1 as a novel therapeutic target for viral diseases. Expert Opin. Ther. Targets 23, 437-446. https://doi.org/10.1080/14728222.2019.1601702
  122. Zhou, D., Zhou, M., Wang, Z., Fu, Y., Jia, M., Wang, X., Liu, M., Zhang, Y., Sun, Y., Lu, Y., et al. (2019a). PGRN acts as a novel regulator of mitochondrial homeostasis by facilitating mitophagy and mitochondrial biogenesis to prevent podocyte injury in diabetic nephropathy. Cell Death Dis. 10, 524. https://doi.org/10.1038/s41419-019-1754-3
  123. Zhou, J., Yang, R., Zhang, Z., Liu, Q., Zhang, Y., Wang, Q., and Yuan, H. (2019b). Mitochondrial protein PINK1 positively regulates RLR signaling. Front. Immunol. 10, 1069. https://doi.org/10.3389/fimmu.2019.01069
  124. Zhu, L., Mou, C., Yang, X., Lin, J., and Yang, Q. (2016). Mitophagy in TGEV infection counteracts oxidative stress and apoptosis. Oncotarget 7, 27122-27141. https://doi.org/10.18632/oncotarget.8345
  125. Zou, J., Li, W., Misra, A., Yue, F., Song, K., Chen, Q., Guo, G., Yi, J., Kimata, J.T., and Liu, L. (2015). The viral restriction factor tetherin prevents leucine-rich pentatricopeptide repeat-containing protein (LRPPRC) from association with beclin 1 and B-cell CLL/lymphoma 2 (Bcl-2) and enhances autophagy and mitophagy. J. Biol. Chem. 290, 7269-7279. https://doi.org/10.1074/jbc.M114.627679

Cited by

  1. Possible Role of Mitochondrial DNA Mutations in Chronification of Inflammation: Focus on Atherosclerosis vol.9, pp.4, 2020, https://doi.org/10.3390/jcm9040978
  2. Inflammasome and Mitophagy Connection in Health and Disease vol.21, pp.13, 2020, https://doi.org/10.3390/ijms21134714
  3. Melasolv induces melanosome autophagy to inhibit pigmentation in B16F1 cells vol.15, pp.9, 2020, https://doi.org/10.1371/journal.pone.0239019
  4. Peroxisome quality control and dysregulated lipid metabolism in neurodegenerative diseases vol.52, pp.9, 2020, https://doi.org/10.1038/s12276-020-00503-9
  5. Lysophosphatidylcholine Enhances Bactericidal Activity by Promoting Phagosome Maturation via the Activation of the NF-κB Pathway during Salmonella Infection in Mouse Macrophages vol.43, pp.12, 2020, https://doi.org/10.14348/molcells.2020.0030
  6. The FMRFamide Neuropeptide FLP-20 Acts as a Systemic Signal for Starvation Responses in Caenorhabditis elegans vol.44, pp.7, 2020, https://doi.org/10.14348/molcells.2021.0051
  7. Roles of IκB kinases and TANK-binding kinase 1 in hepatic lipid metabolism and nonalcoholic fatty liver disease vol.53, pp.11, 2020, https://doi.org/10.1038/s12276-021-00712-w