The role of HDAC6 in enhancing macrophage autophagy via the autophagolysosomal pathway to alleviate legionella pneumophila-induced pneumonia

References

• Horwitz MA. Formation of a novel phagosome by the legionnaires’ disease bacterium (legionella pneumophila) in human monocytes. J Exp Med. 1983;158(4):1319–21. doi: 10.1084/jem.158.4.1319
   PubMed Web of Science ®Google Scholar
• Newton HJ, Ang DK, van Driel IR, et al. Molecular pathogenesis of infections caused by legionella pneumophila. Clin Microbiol Rev. 2010;23(2):274–298. doi: 10.1128/CMR.00052-09
   PubMed Web of Science ®Google Scholar
• Mouchtouri VA, Rudge JW. Legionnaires’ disease in hotels and passenger ships: a systematic review of evidence, sources, and contributing factors. J Travel Med. 2015;22(5):325–337. doi: 10.1111/jtm.12225
   PubMed Web of Science ®Google Scholar
• Iliadi V, Staykova J, Iliadis S, et al. Legionella pneumophila: the journey from the environment to the blood. J Clin Med. 2022;11(20):6126. doi: 10.3390/jcm11206126
   PubMed Web of Science ®Google Scholar
• Chidiac C, Che D, Pires-Cronenberger S, et al. Factors associated with hospital mortality in community-acquired legionellosis in France. Eur Respir J. 2012;39(4):963–970. doi: 10.1183/09031936.00076911
   PubMed Web of Science ®Google Scholar
• Oliva G, Sahr T, Buchrieser C. The life cycle of L. pneumophila: cellular differentiation is linked to virulence and metabolism. Front Cell Infect Microbiol. 2018;8:3. doi: 10.3389/fcimb.2018.00003
   PubMed Web of Science ®Google Scholar
• Krakauer T. Inflammasomes, autophagy, and cell death: the trinity of innate host defense against intracellular bacteria. Mediators Inflamm. 2019;2019:2471215. doi: 10.1155/2019/2471215
   PubMed Web of Science ®Google Scholar
• Abdelaziz DH, Khalil H, Cormet-Boyaka E, et al. The cooperation between the autophagy machinery and the inflammasome to implement an appropriate innate immune response: do they regulate each other? Immunol. Rev. 2015;265(1):194–204. doi: 10.1111/imr.12288
   PubMed Web of Science ®Google Scholar
• Choy A, Dancourt J, Mugo B, et al. The legionella effector RavZ inhibits host autophagy through irreversible Atg8 deconjugation. Science. 2012;338(6110):1072–1076. doi: 10.1126/science.1227026
   PubMed Web of Science ®Google Scholar
• Abu Khweek A, Kanneganti A, Guttridge DD, et al. The sphingosine-1-phosphate lyase (LegS2) contributes to the restriction of legionella pneumophila in murine macrophages. PLoS One. 2016;11(1):e0146410. doi: 10.1371/journal.pone.0146410
   PubMed Web of Science ®Google Scholar
• Khweek AA, Caution K, Akhter A, et al. A bacterial protein promotes the recognition of the legionella pneumophila vacuole by autophagy. Eur J Immunol. 2013;43(5):1333–1344. doi: 10.1002/eji.201242835
   PubMed Web of Science ®Google Scholar
• Abdulrahman BA, Khweek AA, Akhter A, et al. Autophagy stimulation by rapamycin suppresses lung inflammation and infection by Burkholderia cenocepacia in a model of cystic fibrosis. Autophagy. 2011;7(11):1359–1370. doi: 10.4161/auto.7.11.17660
   PubMed Web of Science ®Google Scholar
• Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol. 2010;221(1):3–12. doi: 10.1002/path.2697
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Abdalla FC, Abeliovich H, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2012;8(4):445–544. doi: 10.4161/auto.19496
   PubMed Web of Science ®Google Scholar
• Escoll P, Rolando M, Buchrieser C. Modulation of host autophagy during bacterial infection: sabotaging host munitions for pathogen nutrition. Front Immunol. 2016;7:81. doi: 10.3389/fimmu.2016.00081
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Petroni G, Amaravadi RK, et al. Autophagy in major human diseases. The EMBO Journal. 2021;40(19):e108863. doi: 10.15252/embj.2021108863
   PubMed Web of Science ®Google Scholar
• Chang P, Li H, Hu H, et al. The role of HDAC6 in autophagy and NLRP3 inflammasome. Front Immunol. 2021;12:763831. doi: 10.3389/fimmu.2021.763831
   PubMed Web of Science ®Google Scholar
• Liu P, Xiao J, Wang Y, et al. Posttranslational modification and beyond: interplay between histone deacetylase 6 and heat-shock protein 90. Mol Med. 2021;27(1):110. doi: 10.1186/s10020-021-00375-3
   PubMed Web of Science ®Google Scholar
• Xu S, Chen H, Ni H, et al. Targeting HDAC6 attenuates nicotine-induced macrophage pyroptosis via NF-kappaB/NLRP3 pathway. Atherosclerosis. 2021;317:1–9. doi: 10.1016/j.atherosclerosis.2020.11.021
   PubMed Web of Science ®Google Scholar
• Brijmohan AS, Batchu SN, Majumder S, et al. HDAC6 inhibition promotes transcription factor EB activation and is protective in experimental kidney disease. Front Pharmacol. 2018;9:34. doi: 10.3389/fphar.2018.00034
   PubMed Web of Science ®Google Scholar
• Xu Y, Wan W. Acetylation in the regulation of autophagy. Autophagy. 2023;19(2):379–387. doi: 10.1080/15548627.2022.2062112
   PubMed Web of Science ®Google Scholar
• Zhang L, Zhang Z, Li C, et al. S100A11 promotes liver steatosis via FOXO1-mediated autophagy and Lipogenesis. Cell Mol Gastroenterol Hepatol. 2021b;11(3):697–724. doi: 10.1016/j.jcmgh.2020.10.006
   PubMed Web of Science ®Google Scholar
• Yu L, Chen Y, Tooze SA. Autophagy pathway: cellular and molecular mechanisms. Autophagy. 2018;14(2):207–215. doi: 10.1080/15548627.2017.1378838
   PubMed Web of Science ®Google Scholar
• Li T, Yin L, Kang X, et al. TFEB acetylation promotes lysosome biogenesis and ameliorates alzheimer’s disease–relevant phenotypes in mice. J of Biol. Chem. 2022;298(12):102649. doi: 10.1016/j.jbc.2022.102649
   PubMed Web of Science ®Google Scholar
• Pandey UB, Nie Z, Batlevi Y, et al. HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature. 2007;447(7146):859–863. doi: 10.1038/nature05853
   PubMed Web of Science ®Google Scholar
• Mitchell G, Cheng MI, Chen C, et al. Listeria monocytogenes triggers noncanonical autophagy upon phagocytosis, but avoids subsequent growth-restricting xenophagy. Proc Natl Acad Sci U S A. 2018;115(2):E210–E217. doi: 10.1073/pnas.1716055115
   PubMed Web of Science ®Google Scholar
• Hui Z, Zhou L, Xue Z, et al. Cxxc finger protein 1 positively regulates GM-CSF-Derived macrophage phagocytosis through Csf2ralpha-mediated signaling. Front Immunol. 2018;9. doi: 10.3389/fimmu.2018.01885
   PubMed Web of Science ®Google Scholar
• Brieland J, Freeman P, Kunkel R, et al. Replicative legionella pneumophila lung infection in intratracheally inoculated A/J mice. A murine model of human legionnaires’ disease. Am J Pathol. 1994;145(6):1537–1546.
   PubMed Web of Science ®Google Scholar
• Chen Y, Tateda K, Fujita K, et al. Sequential changes of legionella antigens and bacterial load in the lungs and urines of a mouse model of pneumonia. Diagn Microbiol Infect Dis. 2010;66(3):253–260. doi: 10.1016/j.diagmicrobio.2009.11.001
   PubMed Web of Science ®Google Scholar
• Assouvie A, Daley-Bauer LP, Rousselet G. Growing murine bone marrow-derived macrophages. Methods Mol Biol. 2018;1784:29–33.
   PubMedGoogle Scholar
• Amer AO, Swanson MS. Autophagy is an immediate macrophage response to Legionella pneumophila. Cell Microbiol. 2005;7(6):765–778. doi: 10.1111/j.1462-5822.2005.00509.x
   PubMed Web of Science ®Google Scholar
• Randow F, Youle RJ. Self and nonself: how autophagy targets mitochondria and bacteria. Cell Host Microbe. 2014;15(4):403–411. doi: 10.1016/j.chom.2014.03.012
   PubMed Web of Science ®Google Scholar
• Li Z, Liu S, Fu T, et al. Microtubule destabilization caused by silicate via HDAC6 activation contributes to autophagic dysfunction in bone mesenchymal stem cells. Stem Cell Res Ther. 2019;10(1):351. doi: 10.1186/s13287-019-1441-4
   PubMed Web of Science ®Google Scholar
• Magupalli VG, Negro R, Tian Y, et al. HDAC6 mediates an aggresome-like mechanism for NLRP3 and pyrin inflammasome activation. Science. 2020;369(6510). doi: 10.1126/science.aas8995
   PubMed Web of Science ®Google Scholar
• Horndahl J, Svard R, Berntsson P, et al. HDAC6 inhibitor ACY-1083 shows lung epithelial protective features in COPD. PLoS One. 2022;17(10):e0266310. doi: 10.1371/journal.pone.0266310
   PubMed Web of Science ®Google Scholar
• Su Y, Han W, Kovacs-Kasa A, et al. HDAC6 activates ERK in airway and pulmonary vascular remodeling of chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol. 2021;65(6):603–614. doi: 10.1165/rcmb.2020-0520OC
   PubMed Web of Science ®Google Scholar
• Liu L, Zhou X, Shetty S, et al. HDAC6 inhibition blocks inflammatory signaling and caspase-1 activation in LPS-induced acute lung injury. Toxicol Appl Pharmacol. 2019;370:178–183. doi: 10.1016/j.taap.2019.03.017
   PubMed Web of Science ®Google Scholar
• Zhou T, Jia D, Han J, et al. HDAC6 inhibition alleviates acute pulmonary embolism: a possible future therapeutic option. Folia Histochem Cytobiol. 2023;61(1):56–67. doi: 10.5603/FHC.a2023.0006
   PubMed Web of Science ®Google Scholar
• Moreno-Gonzalo O, Ramirez-Huesca M, Blas-Rus N, et al. HDAC6 controls innate immune and autophagy responses to TLR-mediated signalling by the intracellular bacteria listeria monocytogenes. PLoS Pathog. 2017;13(12):e1006799. doi: 10.1371/journal.ppat.1006799
   PubMed Web of Science ®Google Scholar
• Youn GS, Ju SM, Choi SY, et al. HDAC6 mediates HIV-1 tat-induced proinflammatory responses by regulating MAPK-NF-kappaB/AP-1 pathways in astrocytes. Glia. 2015;63(11):1953–1965. doi: 10.1002/glia.22865
   PubMed Web of Science ®Google Scholar
• New M, Sheikh S, Bekheet M, et al. TLR adaptor protein MYD88 mediates sensitivity to HDAC inhibitors via a cytokine-dependent mechanism. Cancer Res. 2016;76(23):6975–6987. doi: 10.1158/0008-5472.CAN-16-0504
   PubMed Web of Science ®Google Scholar
• Youn GS, Lee KW, Choi SY, et al. Overexpression of HDAC6 induces pro-inflammatory responses by regulating ROS-MAPK-NF-kappaB/AP-1 signaling pathways in macrophages. Free Radic Biol Med. 2016;97:14–23. doi: 10.1016/j.freeradbiomed.2016.05.014
   PubMed Web of Science ®Google Scholar
• Zhang F, Yu S, Chai Q, et al. HDAC6 contributes to human resistance against mycobacterium tuberculosis infection via mediating innate immune responses. FASEB J. 2021a;35(11):e22009. doi: 10.1096/fj.202100614R
   PubMed Web of Science ®Google Scholar
• Rosenjack J, Hodges CA, Darrah RJ, et al. HDAC6 depletion improves cystic fibrosis mouse airway responses to bacterial challenge. Sci Rep. 2019;9(1):10282. doi: 10.1038/s41598-019-46555-4
   PubMedGoogle Scholar
• Rymut SM, Harker A, Corey DA, et al. Reduced microtubule acetylation in cystic fibrosis epithelial cells. Amer. J of Physiol.-Lung Cell. and mol. Physiol. 2013;305(6):L419–431. doi: 10.1152/ajplung.00411.2012
   PubMed Web of Science ®Google Scholar
• Chattopadhyay S, Fensterl V, Zhang Y, et al. Inhibition of viral pathogenesis and promotion of the septic shock response to bacterial infection by IRF-3 are regulated by the acetylation and phosphorylation of its coactivators. MBio. 2013;4(2):4. doi: 10.1128/mBio.00636-12
   Web of Science ®Google Scholar
• Deng Q, Zhao T, Pan B, et al. Protective effect of tubastatin a in CLP-Induced lethal sepsis. Inflammation. 2018;41(6):2101–2109. doi: 10.1007/s10753-018-0853-0
   PubMed Web of Science ®Google Scholar
• Abd El Maksoud AI, Elebeedy D, et al. Methylomic changes of autophagy-related genes by legionella effector Lpg2936 in infected macrophages. Front Cell Dev Biol. 2019;7:390. doi: 10.3389/fcell.2019.00390
   PubMed Web of Science ®Google Scholar
• Park SW, Jun YW, Jeon P, et al. LIR motifs and the membrane-targeting domain are complementary in the function of RavZ. BMB Rep. 2019;52(12):700–705. doi: 10.5483/BMBRep.2019.52.12.211
   PubMed Web of Science ®Google Scholar
• Joshi AD, Swanson MS. Secrets of a successful pathogen: legionella resistance to progression along the autophagic pathway. Front Microbiol. 2011;2:138. doi: 10.3389/fmicb.2011.00138
   PubMed Web of Science ®Google Scholar
• Lee JY, Kawaguchi Y, Li M, et al. Uncoupling of protein aggregation and neurodegeneration in a mouse amyotrophic lateral sclerosis model. Neurodegener Dis. 2015;15(6):339–349. doi: 10.1159/000437208
   PubMed Web of Science ®Google Scholar
• Chang YY, Neufeld TP, Schmid SL. An Atg1/Atg13 complex with multiple roles in TOR-mediated autophagy regulation. Mol Biol Cell. 2009;20(7):2004–2014. doi: 10.1091/mbc.e08-12-1250
   PubMed Web of Science ®Google Scholar
• Jung CH, Jun CB, Ro SH, et al. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell. 2009;20(7):1992–2003. doi: 10.1091/mbc.e08-12-1249
   PubMed Web of Science ®Google Scholar
• Ganley IG, Lam du H, Wang J, et al. ULK1·ATG13·FIP200 complex mediates mTOR signaling and is essential for autophagy. J Biol Chem. 2009;284(18):12297–12305. doi: 10.1074/jbc.M900573200
   PubMed Web of Science ®Google Scholar
• Dooley HC, Razi M, Polson HE, et al. WIPI2 links LC3 conjugation with PI3P, autophagosome formation, and pathogen clearance by recruiting Atg12–5-16L1. Molecular Cell. 2014;55(2):238–252. doi: 10.1016/j.molcel.2014.05.021
   PubMed Web of Science ®Google Scholar
• Su H, Yang F, Wang Q, et al. VPS34 acetylation controls its lipid kinase activity and the initiation of canonical and non-canonical autophagy. Mol. Cell. 2017;67(6):907–921 e907. doi: 10.1016/j.molcel.2017.07.024
   PubMed Web of Science ®Google Scholar
• Sun T, Li X, Zhang P, et al. Acetylation of beclin 1 inhibits autophagosome maturation and promotes tumour growth. Nat Commun. 2015;6(1):7215. doi: 10.1038/ncomms8215
   PubMedGoogle Scholar
• Kim TW, Lee HG. Apigenin induces autophagy and cell death by targeting EZH2 under hypoxia conditions in gastric cancer cells. Int J Mol Sci. 2021;22(24):13455. doi: 10.3390/ijms222413455
   PubMed Web of Science ®Google Scholar
• Booth L, Roberts JL, Rais R, et al. Valproate augments Niraparib killing of tumor cells. Cancer Biol Ther. 2018;19(9):797–808. doi: 10.1080/15384047.2018.1472190
   PubMed Web of Science ®Google Scholar
• Ye X, Zhou XJ, Zhang H. Exploring the role of autophagy-related gene 5 (ATG5) yields important insights into autophagy in autoimmune/autoinflammatory diseases. Front Immunol. 2018;9:2334. doi: 10.3389/fimmu.2018.02334
   PubMed Web of Science ®Google Scholar
• Erbil S, Oral O, Mitou G, et al. RACK1 is an interaction partner of ATG5 and a novel regulator of autophagy. J Biol Chem. 2016;291(32):16753–16765. doi: 10.1074/jbc.M115.708081
   PubMed Web of Science ®Google Scholar
• Lee IH, Finkel T. Regulation of autophagy by the p300 acetyltransferase. J Biol Chem. 2009;284(10):6322–6328. doi: 10.1074/jbc.M807135200
   PubMed Web of Science ®Google Scholar
• Maskey D, Yousefi S, Schmid I, et al. ATG5 is induced by DNA-damaging agents and promotes mitotic catastrophe independent of autophagy. Nat Commun. 2013;4(1):2130. doi: 10.1038/ncomms3130
   PubMedGoogle Scholar
• Jiang X, Huang Y, Liang X, et al. Metastatic prostate cancer-associated P62 inhibits autophagy flux and promotes epithelial to mesenchymal transition by sustaining the level of HDAC6. Prostate. 2018;78(6):426–434. doi: 10.1002/pros.23487
   PubMed Web of Science ®Google Scholar
• Chen Q, Yue F, Li W, et al. Potassium Bisperoxo(1,10-phenanthroline)oxovanadate (bpV(phen)) induces apoptosis and pyroptosis and disrupts the P62-HDAC6 protein interaction to suppress the acetylated microtubule-dependent degradation of autophagosomes. J Biol Chem. 2015;290(43):26051–26058. doi: 10.1074/jbc.M115.653568
   PubMed Web of Science ®Google Scholar
• Li W, Dai Y, Shi B, et al. LRPPRC sustains yap-P27-mediated cell ploidy and P62-HDAC6-mediated autophagy maturation and suppresses genome instability and hepatocellular carcinomas. Oncogene. 2020;39(19):3879–3892. doi: 10.1038/s41388-020-1257-9
   PubMed Web of Science ®Google Scholar
• Yang Y, Wang Q, Song D, et al. Lysosomal dysfunction and autophagy blockade contribute to autophagy-related cancer suppressing peptide-induced cytotoxic death of cervical cancer cells through the AMPK/mTOR pathway. J Exp Clin Cancer Res. 2020;39(1):197. doi: 10.1186/s13046-020-01701-z
   PubMed Web of Science ®Google Scholar
• Huang R, Liu W. Identifying an essential role of nuclear LC3 for autophagy. Autophagy. 2015;11(5):852–853. doi: 10.1080/15548627.2015.1038016
   PubMed Web of Science ®Google Scholar
• Liu KP, Zhou D, Ouyang DY, et al. LC3B-II deacetylation by histone deacetylase 6 is involved in serum-starvation-induced autophagic degradation. Biochem Biophys Res Commun. 2013;441(4):970–975. doi: 10.1016/j.bbrc.2013.11.007
   PubMed Web of Science ®Google Scholar
• Hamalisto S, Jaattela M. Lysosomes in cancer-living on the edge (of the cell). Curr Opin Cell Biol. 2016;39:69–76. doi: 10.1016/j.ceb.2016.02.009
   PubMed Web of Science ®Google Scholar
• Zhang L, Wang K, Lei Y, et al. Redox signaling: potential arbitrator of autophagy and apoptosis in therapeutic response. Free Radic Biol Med. 2015;89:452–465. doi: 10.1016/j.freeradbiomed.2015.08.030
   PubMed Web of Science ®Google Scholar
• Hyttinen JM, Niittykoski M, Salminen A, et al. Maturation of autophagosomes and endosomes: a key role for Rab7. Biochim. et Biophys. Act. (BBA) - mol. Cell Res. 2013;1833(3):503–510. doi: 10.1016/j.bbamcr.2012.11.018
   PubMed Web of Science ®Google Scholar
• Eskelinen EL. Roles of LAMP-1 and LAMP-2 in lysosome biogenesis and autophagy. Mol Aspects Med. 2006;27(5–6):495–502. doi: 10.1016/j.mam.2006.08.005
   PubMedGoogle Scholar
• Huynh KK, Eskelinen EL, Scott CC, et al. LAMP proteins are required for fusion of lysosomes with phagosomes. EMBO J. 2007;26(2):313–324. doi: 10.1038/sj.emboj.7601511
   PubMed Web of Science ®Google Scholar
• Thomas DR, Newton P, Lau N, et al. Interfering with autophagy: the opposing strategies deployed by legionella pneumophila and Coxiella burnetii effector proteins. Front Cell Infect Microbiol. 2020;10:599762. doi: 10.3389/fcimb.2020.599762
   PubMed Web of Science ®Google Scholar
• Naujoks J, Lippmann J, Suttorp N, et al. Innate sensing and cell-autonomous resistance pathways in Legionella pneumophila infection. Int J Med Microbiol. 2018;308(1):161–167. doi: 10.1016/j.ijmm.2017.10.004
   PubMed Web of Science ®Google Scholar
• Schator D, Mondino S, Berthelet J, et al. Legionella para-effectors target chromatin and promote bacterial replication. Nat Commun. 2023;14(1):2154. doi: 10.1038/s41467-023-37885-z
   PubMed Web of Science ®Google Scholar