1932

Abstract

Ubiquitination is a posttranslational modification that regulates a multitude of cellular functions. Pathogens, such as bacteria and viruses, have evolved sophisticated mechanisms that evade or counteract ubiquitin-dependent host responses, or even exploit the ubiquitin system to their own advantage. This is largely done by numerous pathogen virulence factors that encode E3 ligases and deubiquitinases, which are often used as weapons in pathogen–host cell interactions. Moreover, upon pathogen attack, host cellular signaling networks undergo major ubiquitin-dependent changes to protect the host cell, including coordination of innate immunity, remodeling of cellular organelles, reorganization of the cytoskeleton, and reprogramming of metabolic pathways to restrict growth of the pathogen. Here we provide mechanistic insights into ubiquitin regulation of host-pathogen interactions and how it affects bacterial and viral pathogenesis and the organization and response of the host cell.

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2022-09-08
2024-05-06
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Literature Cited

  1. 1.
    Ablasser A, Chen ZJ. 2019. cGAS in action: expanding roles in immunity and inflammation. Science 363:6431eaat8657
    [Google Scholar]
  2. 2.
    Alix E, Godlee C, Cerny O, Blundell S, Tocci R et al. 2020. The tumour suppressor TMEM127 is a Nedd4-family E3 ligase adaptor required by Salmonella SteD to ubiquitinate and degrade MHC class II molecules. Cell Host Microbe 28:154–68
    [Google Scholar]
  3. 3.
    Auer D, Hügelschäffer SD, Fischer AB, Rudel T. 2020. The chlamydial deubiquitinase Cdu1 supports recruitment of Golgi vesicles to the inclusion. Cell. Microbiol. 22:5e13136
    [Google Scholar]
  4. 4.
    Baek K, Scott DC, Schulman BA. 2021. NEDD8 and ubiquitin ligation by cullin-RING E3 ligases. Curr. Opin. Struct. Biol. 67:101–9
    [Google Scholar]
  5. 5.
    Banerjee I, Miyake Y, Nobs SP, Schneider C, Horvath P et al. 2014. Influenza A virus uses the aggresome processing machinery for host cell entry. Science 346:6208473–77
    [Google Scholar]
  6. 6.
    Bernardi KM, Forster ML, Lencer WI, Tsai B. 2008. Derlin-1 facilitates the retro-translocation of cholera toxin. Mol. Biol. Cell 19:3877–84
    [Google Scholar]
  7. 7.
    Bernardi KM, Williams JM, Kikkert M, van Voorden S, Wiertz EJ et al. 2010. The E3 ubiquitin ligases Hrd1 and gp78 bind to and promote cholera toxin retro-translocation. Mol. Biol. Cell 21:1140–51
    [Google Scholar]
  8. 8.
    Bhogaraju S, Kalayil S, Liu Y, Bonn F, Colby T et al. 2016. Phosphoribosylation of ubiquitin promotes serine ubiquitination and impairs conventional ubiquitination. Cell 167:61636–49
    [Google Scholar]
  9. 9.
    Cao Y, Zhu H, He R, Kong L, Shao J et al. 2020. Proteasome, a promising therapeutic target for multiple diseases beyond cancer. Drug Des. Dev. Ther. 14:4327
    [Google Scholar]
  10. 10.
    Carneiro FR, Lepelley A, Seeley JJ, Hayden MS, Ghosh S. 2018. An essential role for ECSIT in mitochondrial complex I assembly and mitophagy in macrophages. Cell Rep. 22:102654–66
    [Google Scholar]
  11. 11.
    Chowdhury SR, Reimer A, Sharan M, Kozjak-Pavlovic V, Eulalio A et al. 2017. Chlamydia preserves the mitochondrial network necessary for replication via microRNA-dependent inhibition of fission. J. Cell Biol. 216:41071–89
    [Google Scholar]
  12. 12.
    Clague MJ, Urbe S, Komander D. 2019. Breaking the chains: deubiquitylating enzyme specificity begets function. Nat. Rev. Mol. Cell Biol. 20:338–52
    [Google Scholar]
  13. 13.
    De Leon JA, Qiu J, Nicolai CJ, Counihan JL, Barry KC et al. 2017. Positive and negative regulation of the master metabolic regulator mTORC1 by two families of Legionella pneumophila effectors. Cell Rep. 21:82031–38
    [Google Scholar]
  14. 14.
    de Wispelaere M, Du G, Donovan KA, Zhang T, Eleuteri NA et al. 2019. Small molecule degraders of the hepatitis C virus protease reduce susceptibility to resistance mutations. Nat. Commun. 10:13468
    [Google Scholar]
  15. 15.
    Dejarnac O, Hafirassou ML, Chazal M, Versapuech M, Gaillard J et al. 2018. TIM-1 ubiquitination mediates dengue virus entry. Cell Rep. 23:61779–93
    [Google Scholar]
  16. 16.
    Demiroz D, Platanitis E, Bryant M, Fischer P, Prchal-Murphy M et al. 2021. Listeria monocytogenes infection rewires host metabolism with regulatory input from type I interferons. PLOS Pathog. 17:7e1009697
    [Google Scholar]
  17. 17.
    Deschamps T, Dogrammatzis C, Mullick R, Kalamvoki M. 2017. Cbl E3 ligase mediates the removal of nectin-1 from the surface of herpes simplex virus 1-infected cells. J. Virol. 91:12e00393–17
    [Google Scholar]
  18. 18.
    Dos Santos AM,, Ferrari RG, Conte-Junior CA 2019. Virulence factors in Salmonella Typhimurium: the sagacity of a bacterium. Curr. Microbiol. 76:6762–73
    [Google Scholar]
  19. 19.
    Eckart RA, Bisle S, Schulze-Luehrmann J, Wittmann I, Jantsch J et al. 2014. Antiapoptotic activity of Coxiella burnetii effector protein AnkG is controlled by p32-dependent trafficking. Infect. Immun. 82:72763–71
    [Google Scholar]
  20. 20.
    Edelmann MJ, Kramer HB, Altun M, Kessler BM. 2010. Post-translational modification of the deubiquitinating enzyme otubain 1 modulates active RhoA levels and susceptibility to Yersinia invasion. FEBS J. 277:112515–30
    [Google Scholar]
  21. 21.
    Escoll P, Platon L, Dramé M, Sahr T, Schmidt S et al. 2021. Reverting the mode of action of the mitochondrial FOF1-ATPase by Legionella pneumophila preserves its replication niche. eLife 10:e71978
    [Google Scholar]
  22. 22.
    Escoll P, Song OR, Viana F, Steiner B, Lagache T et al. 2017. Legionella pneumophila modulates mitochondrial dynamics to trigger metabolic repurposing of infected macrophages. Cell Host Microbe 22:3302–16
    [Google Scholar]
  23. 23.
    Fiskin E, Bionda T, Dikic I, Behrends C. 2016. Global analysis of host and bacterial ubiquitinome in response to Salmonella Typhimurium infection. Mol. Cell 62:6967–81
    [Google Scholar]
  24. 24.
    Flöter J, Kaymak I, Schulze A. 2017. Regulation of metabolic activity by p53. Metabolites 7:221
    [Google Scholar]
  25. 25.
    Fujita Y, Krause G, Scheffner M, Zechner D, Leddy HEM et al. 2002. Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat. Cell Biol. 4:3222–31
    [Google Scholar]
  26. 26.
    Galmiche A, Rassow J. 2010. Targeting of Helicobacter pylori VacA to mitochondria. Gut Microbes 1:6392–95
    [Google Scholar]
  27. 27.
    Gatta AT, Carlton JG. 2019. The ESCRT-machinery: closing holes and expanding roles. Curr. Opin. Cell Biol. 59:121–32
    [Google Scholar]
  28. 28.
    Harper JW, Ordureau A, Heo JM. 2018. Building and decoding ubiquitin chains for mitophagy. Nat. Rev. Mol. Cell Biol. 19:293–108
    [Google Scholar]
  29. 29.
    Hartmann H, Eltzschig HK, Wurz H, Hantke K, Rakin A et al. 2008. Hypoxia-independent activation of HIF-1 by Enterobacteriaceae and their siderophores. Gastroenterology 134:3756–67
    [Google Scholar]
  30. 30.
    Herr RA, Harris J, Fang S, Wang X, Hansen TH 2009. Role of the RING-CH domain of viral ligase mK3 in ubiquitination of non-lysine and lysine MHC I residues. Traffic 10:91301–17
    [Google Scholar]
  31. 31.
    Hershko A, Ciechanover A, Varshavsky A. 2000. The ubiquitin system. Nat. Med. 6:101073–81
    [Google Scholar]
  32. 32.
    Hsu F, Luo X, Qiu J, Teng YB, Jin J et al. 2014. The Legionella effector SidC defines a unique family of ubiquitin ligases important for bacterial phagosomal remodeling. PNAS 111:2910538–43
    [Google Scholar]
  33. 33.
    Hu Z, Crews CM. 2021. Recent developments in PROTAC-mediated protein degradation: from bench to clinic. ChemBioChem 23:2e202100270
    [Google Scholar]
  34. 34.
    Inoue T, Moore P, Tsai B. 2011. How viruses and toxins disassemble to enter host cells. Annu. Rev. Microbiol. 65:287–305
    [Google Scholar]
  35. 35.
    Inturi R, Mun K, Singethan K, Schreiner S, Punga T. 2018. Human adenovirus infection causes cellular E3 ubiquitin ligase MKRN1 degradation involving the viral core protein pVII. J. Virol. 92:3e01154–17
    [Google Scholar]
  36. 36.
    Ivanov SS, Roy CR. 2009. Modulation of ubiquitin dynamics and suppression of DALIS formation by the Legionella pneumophila Dot/Icm system. Cell. Microbiol. 11:2261–78
    [Google Scholar]
  37. 37.
    Jabir MS, Hopkins L, Ritchie ND, Ullah I, Bayes HK et al. 2015. Mitochondrial damage contributes to Pseudomonas aeruginosa activation of the inflammasome and is downregulated by autophagy. Autophagy 11:1166–82
    [Google Scholar]
  38. 38.
    Jiang L, Wang P, Song X, Zhang H, Ma S. 2021. Salmonella Typhimurium reprograms macrophage metabolism via T3SS effector SopE2 to promote intracellular replication and virulence. Nat. Commun. 12:1879
    [Google Scholar]
  39. 39.
    Jiang Y, Su S, Zhang Y, Qian J, Liu P. 2019. Control of mTOR signaling by ubiquitin. Oncogene 38:213989–4001
    [Google Scholar]
  40. 40.
    Johnson N, West M, Odorizzi G. 2017. Regulation of yeast ESCRT-III membrane scission activity by the Doa4 ubiquitin hydrolase. Mol. Biol. Cell 28:5661–72
    [Google Scholar]
  41. 41.
    Juliana C, Fernandes-Alnemri T, Kang S, Farias A, Qin F et al. 2012. Non-transcriptional priming and deubiquitination regulate NLRP3 inflammasome activation. J. Biol. Chem. 287:4336617–22
    [Google Scholar]
  42. 42.
    Keller CW, Loi M, Ligeon LA, Gannagé M, Lünemann JD et al. 2018. Endocytosis regulation by autophagy proteins in MHC restricted antigen presentation. Curr. Opin. Immunol. 52:68–73
    [Google Scholar]
  43. 43.
    Kitao T, Nagai H, Kubori T. 2020. Divergence of Legionella effectors reversing conventional and unconventional ubiquitination. Front. Cell. Infect. Microbiol. 10:448
    [Google Scholar]
  44. 44.
    Klingenbeck L, Eckart RA, Berens C, Lührmann A. 2013. The Coxiella burnetii type IV secretion system substrate CaeB inhibits intrinsic apoptosis at the mitochondrial level. Cell. Microbiol. 15:4675–87
    [Google Scholar]
  45. 45.
    Knight M, Stanley S. 2019. HIF-1α as a central mediator of cellular resistance to intracellular pathogens. Curr. Opin. Immunol. 60:111–16
    [Google Scholar]
  46. 46.
    Kobayashi S, Yoshii K, Phongphaew W, Muto M, Hirano M et al. 2020. West Nile virus capsid protein inhibits autophagy by AMP-activated protein kinase degradation in neurological disease development. PLOS Pathog. 16:1e1008238
    [Google Scholar]
  47. 47.
    Kotewicz KM, Ramabhadran V, Sjoblom N, Vogel JP, Haenssler E et al. 2017. A single Legionella effector catalyzes a multistep ubiquitination pathway to rearrange tubular endoplasmic reticulum for replication. Cell Host Microbe 21:2169–81
    [Google Scholar]
  48. 48.
    Lachance V, Angers S, Parent JL. 2014. New insights in the regulation of Rab GTPases by G protein-coupled receptors. Small GTPases 5:4e983872
    [Google Scholar]
  49. 49.
    Lachmandas E, Beigier-Bompadre M, Cheng SC, Kumar V, van Laarhoven A et al. 2016. Rewiring cellular metabolism via the AKT/mTOR pathway contributes to host defence against Mycobacterium tuberculosis in human and murine cells. Eur. J. Immunol. 46:112574–86
    [Google Scholar]
  50. 50.
    Le Sage V, Cinti A, Amorim R, Mouland AJ 2016. Adapting the stress response: viral subversion of the mTOR signaling pathway. Viruses 8:6152
    [Google Scholar]
  51. 51.
    Li P, Jiang W, Yu Q, Liu W, Zhou P et al. 2017. Ubiquitination and degradation of GBPs by a Shigella effector to suppress host defence. Nature 551:7680378–83
    [Google Scholar]
  52. 52.
    Lin YH, Doms AG, Cheng E, Kim B, Evans TR et al. 2015. Host cell-catalyzed S-palmitoylation mediates Golgi targeting of the Legionella ubiquitin ligase GobX. J. Biol. Chem. 290:4225766–81
    [Google Scholar]
  53. 53.
    Liu X, Xu F, Ren L, Zhao F, Huang Y et al. 2021. MARCH8 inhibits influenza A virus infection by targeting viral M2 protein for ubiquitination-dependent degradation in lysosomes. Nat. Commun. 12:14427
    [Google Scholar]
  54. 54.
    Liu Y, Mukherjee R, Bonn F, Colby T, Matic I et al. 2021. Serine-ubiquitination regulates Golgi morphology and the secretory pathway upon Legionella infection. Cell Death Differ 28:102957–69
    [Google Scholar]
  55. 55.
    Maculins T, Fiskin E, Bhogaraju S, Dikic I. 2016. Bacteria-host relationship: ubiquitin ligases as weapons of invasion. Cell Res. 26:4499–510
    [Google Scholar]
  56. 56.
    Manasanch EE, Orlowski RZ. 2017. Proteasome inhibitors in cancer therapy. Nat. Rev. Clin. Oncol. 14:7417–33
    [Google Scholar]
  57. 57.
    Manzanillo PS, Ayres JS, Watson RO, Collins AC, Souza G et al. 2013. The ubiquitin ligase parkin mediates resistance to intracellular pathogens. Nature 501:7468512–16
    [Google Scholar]
  58. 58.
    Meng B, Lever AM. 2021. The interplay between ESCRT and viral factors in the enveloped virus life cycle. Viruses 13:2324
    [Google Scholar]
  59. 59.
    Mills EL, Kelly B, O'Neill LA. 2017. Mitochondria are the powerhouses of immunity. Nat. Immunol. 18:5488–98
    [Google Scholar]
  60. 60.
    Morreale FE, Kleine S, Leodolter J, Ovchinnikov S, Kley J et al. 2021. BacPROTACs mediate targeted protein degradation in bacteria. bioRxiv 2021.06.09.447781, Jun. 10
  61. 61.
    Mostowy S, Bonazzi M, Hamon MA, Tham TN, Mallet A et al. 2010. Entrapment of intracytosolic bacteria by septin cage-like structures. Cell Host Microbe 8:5433–44
    [Google Scholar]
  62. 62.
    Mostowy S, Shenoy AR. 2015. The cytoskeleton in cell-autonomous immunity: structural determinants of host defence. Nat. Rev. Immunol. 15:9559–73
    [Google Scholar]
  63. 63.
    Mukherjee R, Majumder P, Chakrabarti O. 2017. MGRN1-mediated ubiquitination of α-tubulin regulates microtubule dynamics and intracellular transport. Traffic 18:12791–807
    [Google Scholar]
  64. 64.
    Noack J, Bernasconi R, Molinari M. 2014. How viruses hijack the ERAD tuning machinery. J. Virol. 88:1810272–75
    [Google Scholar]
  65. 65.
    Nunnari J, Suomalainen A. 2012. Mitochondria: in sickness and in health. Cell 148:61145–59
    [Google Scholar]
  66. 66.
    Olagnier D, Farahani E, Thyrsted J, Blay-Cadanet J, Herengt A et al. 2020. SARS-CoV2-mediated suppression of NRF2-signaling reveals potent antiviral and anti-inflammatory activity of 4-octyl-itaconate and dimethyl fumarate. Nat. Commun. 11:14938 Erratum 2020. Nat. Commun. 11:15419
    [Google Scholar]
  67. 67.
    Peyssonnaux C, Datta V, Cramer T, Doedens A, Theodorakis EA et al. 2005. HIF-1α expression regulates the bactericidal capacity of phagocytes. J. Clin. Investig. 115:71806–15
    [Google Scholar]
  68. 68.
    Philips JA, Porto MC, Wang H, Rubin EJ, Perrimon N. 2008. ESCRT factors restrict mycobacterial growth. PNAS 105:83070–75
    [Google Scholar]
  69. 69.
    Piscatelli H, Kotkar SA, McBee ME, Muthupalani S, Schauer DB et al. 2011. The EHEC type III effector NleL is an E3 ubiquitin ligase that modulates pedestal formation. PLOS ONE 6:4e19331
    [Google Scholar]
  70. 70.
    Pohl C, Dikic I. 2019. Cellular quality control by the ubiquitin-proteasome system and autophagy. Science 366:818–22
    [Google Scholar]
  71. 71.
    Qiu J, Luo ZQ. 2017. Hijacking of the host ubiquitin network by Legionella pneumophila. Front. Cell. Infect. Microbiol. 7:487
    [Google Scholar]
  72. 72.
    Radhakrishnan GK, Harms JS, Splitter GA. 2011. Modulation of microtubule dynamics by a TIR domain protein from the intracellular pathogen Brucella melitensis. Biochem. J. 439:179–83
    [Google Scholar]
  73. 73.
    Ravid T, Hochstrasser M. 2008. Diversity of degradation signals in the ubiquitin–proteasome system. Nat. Rev. Mol. Cell Biol. 9:679–89
    [Google Scholar]
  74. 74.
    Reddick LE, Alto NM. 2014. Bacteria fighting back: how pathogens target and subvert the host innate immune system. Mol. Cell 54:321–28
    [Google Scholar]
  75. 75.
    Reiter KH, Klevit RE. 2018. Characterization of RING-Between-RING E3 ubiquitin transfer mechanisms. The Ubiquitin Proteasome System T Mayor, G Kleiger 3–17 New York: Humana
    [Google Scholar]
  76. 76.
    Ren G, Zhang X, Xiao Y, Zhang W, Wang Y et al. 2019. ABRO1 promotes NLRP3 inflammasome activation through regulation of NLRP3 deubiquitination. EMBO J. 38:6e100376
    [Google Scholar]
  77. 77.
    Ribet D, Cossart P. 2018. Ubiquitin, SUMO, and NEDD8: key targets of bacterial pathogens. Trends Cell Biol. 28:11926–40
    [Google Scholar]
  78. 78.
    Roche PA, Furuta K. 2015. The ins and outs of MHC class II-mediated antigen processing and presentation. Nat. Rev. Immunol. 15:4203–16
    [Google Scholar]
  79. 79.
    Rodríguez-Pérez F, Manford AG, Pogson A, Ingersoll AJ, Martínez-González B et al. 2021. Ubiquitin-dependent remodeling of the actin cytoskeleton drives cell fusion. Dev. Cell 56:5588–601
    [Google Scholar]
  80. 80.
    Rothchild AC, Olson GS, Nemeth J, Amon LM, Mai D et al. 2019. Alveolar macrophages generate a noncanonical NRF2-driven transcriptional response to Mycobacterium tuberculosis in vivo. Sci. Immunol. 4:37eaaw6693
    [Google Scholar]
  81. 81.
    Roy CR. 2002. Exploitation of the endoplasmic reticulum by bacterial pathogens. Trends Microbiol. 10:9418–24
    [Google Scholar]
  82. 82.
    Sarbanes SL, Blomen VA, Lam E, Heissel S, Luna JM et al. 2021. E3 ubiquitin ligase Mindbomb 1 facilitates nuclear delivery of adenovirus genomes. PNAS 118:1e2015794118
    [Google Scholar]
  83. 83.
    Schweiggert J, Habeck G, Hess S, Mikus F, Beloshistov R et al. 2021. SCFFbxw5 targets kinesin-13 proteins to facilitate ciliogenesis. EMBO J. 40:18e107735
    [Google Scholar]
  84. 84.
    Shi CS, Qi HY, Boularan C, Huang NN, Abu-Asab M et al. 2014. SARS-coronavirus open reading frame-9b suppresses innate immunity by targeting mitochondria and the MAVS/TRAF3/TRAF6 signalosome. J. Immunol. 193:63080–89
    [Google Scholar]
  85. 85.
    Shin D, Bhattacharya A, Cheng YL, Alonso MC, Mehdipour AR et al. 2020. Bacterial OTU deubiquitinases regulate substrate ubiquitination upon Legionella infection. eLife 9:e58277
    [Google Scholar]
  86. 86.
    Shin D, Mukherjee R, Liu Y, Gonzalez A, Bonn F et al. 2020. Regulation of phosphoribosyl-linked serine ubiquitination by deubiquitinases DupA and DupB. Mol. Cell 77:1164–79
    [Google Scholar]
  87. 87.
    Shin D, Na W, Lee JH, Kim G, Baek J et al. 2017. Site-specific monoubiquitination downregulates Rab5 by disrupting effector binding and guanine nucleotide conversion. eLife 6:e29154
    [Google Scholar]
  88. 88.
    Song Y, Brady ST. 2015. Post-translational modifications of tubulin: pathways to functional diversity of microtubules. Trends Cell Biol. 25:3125–36
    [Google Scholar]
  89. 89.
    Stavru F, Palmer AE, Wang C, Youle RJ, Cossart P. 2013. Atypical mitochondrial fission upon bacterial infection. PNAS 110:4016003–8
    [Google Scholar]
  90. 90.
    Steele S, Brunton J, Ziehr B, Taft-Benz S, Moorman N et al. 2013. Francisella tularensis harvests nutrients derived via ATG5-independent autophagy to support intracellular growth. PLOS Pathog. 9:8e1003562
    [Google Scholar]
  91. 91.
    Strickland M, Nyenhuis D, Watanabe SM, Tjandra N, Carter CA. 2021. Novel Tsg101 binding partners regulate viral L domain trafficking. Viruses 13:61147
    [Google Scholar]
  92. 92.
    Su WC, Chen YC, Tseng CH, Hsu PWC, Tung KF et al. 2013. Pooled RNAi screen identifies ubiquitin ligase Itch as crucial for influenza A virus release from the endosome during virus entry. PNAS 110:4317516–21
    [Google Scholar]
  93. 93.
    Suzuki S, Mimuro H, Kim M, Ogawa M, Ashida H et al. 2014. Shigella IpaH7.8 E3 ubiquitin ligase targets glomulin and activates inflammasomes to demolish macrophages. PNAS 111:40E4254–63
    [Google Scholar]
  94. 94.
    Sweet CR, Conlon J, Golenbock DT, Goguen J, Silverman N. 2007. YopJ targets TRAF proteins to inhibit TLR-mediated NF-κB, MAPK and IRF3 signal transduction. Cell. Microbiol. 9:112700–15
    [Google Scholar]
  95. 95.
    Tada T, Zhang Y, Koyama T, Tobiume M, Tsunetsugu-Yokota Y et al. 2015. MARCH8 inhibits HIV-1 infection by reducing virion incorporation of envelope glycoproteins. Nat. Med. 21:121502–7
    [Google Scholar]
  96. 96.
    Ushijima Y, Goshima F, Kimura H, Nishiyama Y. 2009. Herpes simplex virus type 2 tegument protein UL56 relocalizes ubiquitin ligase Nedd4 and has a role in transport and/or release of virions. Virol. J. 6:168
    [Google Scholar]
  97. 97.
    Van Den Boomen DJ, Timms RT, Grice GL, Stagg HR, Skødt K et al. 2014. TMEM129 is a Derlin-1 associated ERAD E3 ligase essential for virus-induced degradation of MHC-I. PNAS 111:3111425–30
    [Google Scholar]
  98. 98.
    Wandel MP, Pathe C, Werner EI, Ellison CJ, Boyle KB et al. 2017. GBPs inhibit motility of Shigella flexneri but are targeted for degradation by the bacterial ubiquitin ligase IpaH9.8. Cell Host Microbe 22:4507–18
    [Google Scholar]
  99. 99.
    Wang Q, Huang L, Hong Z, Lv Z, Mao Z et al. 2017. The E3 ubiquitin ligase RNF185 facilitates the cGAS-mediated innate immune response. PLOS Pathog. 13:3e1006264
    [Google Scholar]
  100. 100.
    Wang Q, Liu X, Cui Y, Tang Y, Chen W et al. 2014. The E3 ubiquitin ligase AMFR and INSIG1 bridge the activation of TBK1 kinase by modifying the adaptor STING. Immunity 41:6919–33
    [Google Scholar]
  101. 101.
    Wang Q, Peng Z, Long H, Deng X, Huang K. 2019. Polyubiquitylation of α-tubulin at K304 is required for flagellar disassembly in Chlamydomonas. J. Cell Sci. 132:6jcs229047
    [Google Scholar]
  102. 102.
    Weber J, Polo S, Maspero E. 2019. HECT E3 ligases: a tale with multiple facets. Front. Physiol. 10:370
    [Google Scholar]
  103. 103.
    West AP, Brodsky IE, Rahner C, Woo DK, Erdjument-Bromage H et al. 2011. TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 472:7344476–80
    [Google Scholar]
  104. 104.
    Wyatt EV, Diaz K, Griffin AJ, Rasmussen JA, Crane DD et al. 2016. Metabolic reprogramming of host cells by virulent Francisella tularensis for optimal replication and modulation of inflammation. J. Immunol. 196:104227–36
    [Google Scholar]
  105. 105.
    Yau R, Rape M. 2016. The increasing complexity of the ubiquitin code. Nat. Cell Biol. 18:579–86
    [Google Scholar]
  106. 106.
    Yoo YS, Park YJ, Lee HS, Oanh NTK, Cho MY et al. 2019. Mitochondria ubiquitin ligase, MARCH5 resolves hepatitis B virus X protein aggregates in the liver pathogenesis. Cell Death. Dis. 10:938
    [Google Scholar]
  107. 107.
    Yoo YS, Park YY, Kim JH, Cho H, Kim SH et al. 2015. The mitochondrial ubiquitin ligase MARCH5 resolves MAVS aggregates during antiviral signalling. Nat. Commun. 6:7910
    [Google Scholar]
  108. 108.
    Zhang Y, Sharma L, Losier A, Ifedigbo E, Sauler M et al. 2019. Role of PINK1 mediated mitophagy during Streptococcus pneumoniae pneumonia. Am. J. Resp. Crit. Care Med. 199:A7239 (Abstr.)
    [Google Scholar]
  109. 109.
    Zhou R, Yazdi AS, Menu P, Tschopp J. 2011. A role for mitochondria in NLRP3 inflammasome activation. Nature 469:7329221–25
    [Google Scholar]
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