ATG7 and ATG14 restrict cytosolic and phagosomal Mycobacterium tuberculosis replication in human macrophages.
Journal
Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869
Informations de publication
Date de publication:
05 2023
05 2023
Historique:
received:
24
01
2022
accepted:
24
01
2023
medline:
8
5
2023
pubmed:
25
3
2023
entrez:
24
3
2023
Statut:
ppublish
Résumé
Autophagy is a cellular innate-immune defence mechanism against intracellular microorganisms, including Mycobacterium tuberculosis (Mtb). How canonical and non-canonical autophagy function to control Mtb infection in phagosomes and the cytosol remains unresolved. Macrophages are the main host cell in humans for Mtb. Here we studied the contributions of canonical and non-canonical autophagy in the genetically tractable human induced pluripotent stem cell-derived macrophages (iPSDM), using a set of Mtb mutants generated in the same genetic background of the common lab strain H37Rv. We monitored replication of Mtb mutants that are either unable to trigger canonical autophagy (Mtb ΔesxBA) or reportedly unable to block non-canonical autophagy (Mtb ΔcpsA) in iPSDM lacking either ATG7 or ATG14 using single-cell high-content imaging. We report that deletion of ATG7 by CRISPR-Cas9 in iPSDM resulted in increased replication of wild-type Mtb but not of Mtb ΔesxBA or Mtb ΔcpsA. We show that deletion of ATG14 resulted in increased replication of both Mtb wild type and the mutant Mtb ΔesxBA. Using Mtb reporters and quantitative imaging, we identified a role for ATG14 in regulating fusion of phagosomes containing Mtb with lysosomes, thereby enabling intracellular bacteria restriction. We conclude that ATG7 and ATG14 are both required for restricting Mtb replication in human macrophages.
Identifiants
pubmed: 36959508
doi: 10.1038/s41564-023-01335-9
pii: 10.1038/s41564-023-01335-9
pmc: PMC10159855
doi:
Substances chimiques
ATG7 protein, human
EC 6.2.1.45
Autophagy-Related Protein 7
EC 6.2.1.45
ATG14 protein, human
0
Autophagy-Related Proteins
0
Adaptor Proteins, Vesicular Transport
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
803-818Subventions
Organisme : Cancer Research UK
ID : FC001092
Pays : United Kingdom
Organisme : Wellcome Trust
ID : FC001092
Pays : United Kingdom
Organisme : Medical Research Council
ID : FC001092
Pays : United Kingdom
Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2023. The Author(s).
Références
Deretic, V. Autophagy in immunity and cell-autonomous defense against intracellular microbes. Immunol. Rev. 240, 92–104 (2011).
pubmed: 21349088
pmcid: 3057454
doi: 10.1111/j.1600-065X.2010.00995.x
Gutierrez, M., Master, S. & Singh, S. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119, 753–766 (2004).
pubmed: 15607973
doi: 10.1016/j.cell.2004.11.038
Nakagawa, I. et al. Autophagy defends cells against invading group A Streptococcus. Science 306, 1037–1040 (2004).
pubmed: 15528445
doi: 10.1126/science.1103966
Huang, J. & Brumell, J. H. Bacteria–autophagy interplay: a battle for survival. Nat. Rev. Microbiol. 12, 101–114 (2014).
pubmed: 24384599
pmcid: 7097477
doi: 10.1038/nrmicro3160
Upadhyay, S. & Philips, J. A. LC3-associated phagocytosis: host defense and microbial response. Curr. Opin. Immunol. 60, 81–90 (2019).
pubmed: 31247378
doi: 10.1016/j.coi.2019.04.012
Knodler, L. A. & Celli, J. Eating the strangers within: host control of intracellular bacteria via xenophagy. Cell Microbiol. 13, 1319–1327 (2011).
pubmed: 21740500
pmcid: 3158265
doi: 10.1111/j.1462-5822.2011.01632.x
Jia, J. et al. Galectin-3 coordinates a cellular system for lysosomal repair and removal. Dev. Cell 52, 69–87 e68 (2020).
pubmed: 31813797
doi: 10.1016/j.devcel.2019.10.025
Thurston, T. L., Ryzhakov, G., Bloor, S., von Muhlinen, N. & Randow, F. The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat. Immunol. 10, 1215–1221 (2009).
pubmed: 19820708
doi: 10.1038/ni.1800
Fiskin, E., Bionda, T., Dikic, I. & Behrends, C. Global analysis of host and bacterial ubiquitinome in response to Salmonella typhimurium infection. Mol. Cell 62, 967–981 (2016).
pubmed: 27211868
doi: 10.1016/j.molcel.2016.04.015
Otten, E. G. et al. Ubiquitylation of lipopolysaccharide by RNF213 during bacterial infection. Nature 594, 111–116 (2021).
pubmed: 34012115
pmcid: 7610904
doi: 10.1038/s41586-021-03566-4
Martinez, J. et al. Molecular characterization of LC3-associated phagocytosis reveals distinct roles for Rubicon, NOX2 and autophagy proteins. Nat. Cell Biol. 17, 893–906 (2015).
pubmed: 26098576
pmcid: 4612372
doi: 10.1038/ncb3192
Koster, S. et al. Mycobacterium tuberculosis is protected from NADPH oxidase and LC3-associated phagocytosis by the LCP protein CpsA. Proc. Natl Acad. Sci. USA 114, E8711–E8720 (2017).
pubmed: 28973896
pmcid: 5642705
doi: 10.1073/pnas.1707792114
Bussi, C. & Gutierrez, M. G. Mycobacterium tuberculosis infection of host cells in space and time. FEMS Microbiol. Rev. https://doi.org/10.1093/femsre/fuz006 (2019).
Lerner, T. R. et al. Mycobacterium tuberculosis replicates within necrotic human macrophages. J. Cell Biol. https://doi.org/10.1083/jcb.201603040 (2017).
Simeone, R. et al. Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathog. 8, e1002507 (2012).
pubmed: 22319448
pmcid: 3271072
doi: 10.1371/journal.ppat.1002507
van der Wel, N. et al. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129, 1287–1298 (2007).
pubmed: 17604718
doi: 10.1016/j.cell.2007.05.059
Augenstreich, J. et al. ESX-1 and phthiocerol dimycocerosates of Mycobacterium tuberculosis act in concert to cause phagosomal rupture and host cell apoptosis. Cell. Microbiol. 19, 1–19 (2017).
doi: 10.1111/cmi.12726
Lerner, T. R. et al. Phthiocerol dimycocerosates promote access to the cytosol and intracellular burden of Mycobacterium tuberculosis in lymphatic endothelial cells. BMC Biol. 16, 1 (2018).
pubmed: 29325545
pmcid: 5795283
doi: 10.1186/s12915-017-0471-6
Quigley, J. et al. The cell wall lipid PDIM contributes to phagosomal escape and host cell exit of Mycobacterium tuberculosis. mBio 8, e00148–17 (2017).
pubmed: 28270579
pmcid: 5340868
doi: 10.1128/mBio.00148-17
Barczak, A. K. et al. Systematic, multiparametric analysis of Mycobacterium tuberculosis intracellular infection offers insight into coordinated virulence. PLoS Pathog. 13, e1006363 (2017).
pubmed: 28505176
pmcid: 5444860
doi: 10.1371/journal.ppat.1006363
Lopez-Jimenez, A. T. et al. The ESCRT and autophagy machineries cooperate to repair ESX-1-dependent damage at the Mycobacterium-containing vacuole but have opposite impact on containing the infection. PLoS Pathog. 14, e1007501 (2018).
pubmed: 30596802
pmcid: 6329560
doi: 10.1371/journal.ppat.1007501
Bernard, E. M. et al. M. tuberculosis infection of human iPSC-derived macrophages reveals complex membrane dynamics during xenophagy evasion. J. Cell Sci. 134, jcs252973 (2020).
pubmed: 32938685
pmcid: 7710011
doi: 10.1242/jcs.252973
Franco, L. H. et al. The ubiquitin ligase Smurf1 functions in selective autophagy of Mycobacterium tuberculosis and anti-tuberculous host defense. Cell Host Microbe 21, 59–72 (2017).
pubmed: 28017659
doi: 10.1016/j.chom.2016.11.002
Manzanillo, P. S. et al. PARKIN ubiquitin ligase mediates resistance to intracellular pathogens. Nature 501, 512–516 (2013).
pubmed: 24005326
pmcid: 3886920
doi: 10.1038/nature12566
Watson, R. O., Manzanillo, P. S. & Cox, J. S. Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 150, 803–815 (2012).
pubmed: 22901810
pmcid: 3708656
doi: 10.1016/j.cell.2012.06.040
Kimmey, J. M. et al. Unique role for ATG5 in neutrophil-mediated immunopathology during M. tuberculosis infection. Nature 528, 565–569 (2015).
pubmed: 26649827
pmcid: 4842313
doi: 10.1038/nature16451
Behar, S. M. & Baehrecke, E. H. Tuberculosis: autophagy is not the answer. Nature 528, 482–483 (2015).
pubmed: 26649822
doi: 10.1038/nature16324
Chandra, P. et al. Mycobacterium tuberculosis inhibits RAB7 recruitment to selectively modulate autophagy flux in macrophages. Sci. Rep. 5, 16320 (2015).
pubmed: 26541268
pmcid: 4635374
doi: 10.1038/srep16320
Romagnoli, A. et al. ESX-1 dependent impairment of autophagic flux by Mycobacterium tuberculosis in human dendritic cells. Autophagy 8, 1357–1370 (2012).
pubmed: 22885411
pmcid: 3442882
doi: 10.4161/auto.20881
Kaps, I. et al. Energy transfer between fluorescent proteins using a co-expression system in Mycobacterium smegmatis. Gene 278, 115–124 (2001).
pubmed: 11707328
doi: 10.1016/S0378-1119(01)00712-0
Florey, O., Gammoh, N., Kim, S. E., Jiang, X. & Overholtzer, M. V-ATPase and osmotic imbalances activate endolysosomal LC3 lipidation. Autophagy 11, 88–99 (2015).
pubmed: 25484071
doi: 10.4161/15548627.2014.984277
van Wilgenburg, B., Browne, C., Vowles, J. & Cowley, S. A. Efficient, long term production of monocyte-derived macrophages from human pluripotent stem cells under partly-defined and fully-defined conditions. PLoS ONE 8, e71098 (2013).
pubmed: 23951090
pmcid: 3741356
doi: 10.1371/journal.pone.0071098
Hall-Roberts, H. et al. TREM2 Alzheimer’s variant R47H causes similar transcriptional dysregulation to knockout, yet only subtle functional phenotypes in human iPSC-derived macrophages. Alzheimers Res. Ther. 12, 151 (2020).
pubmed: 33198789
pmcid: 7667762
doi: 10.1186/s13195-020-00709-z
Hiatt, J. et al. Efficient generation of isogenic primary human myeloid cells using CRISPR–Cas9 ribonucleoproteins. Cell Rep. 35, 109105 (2021).
pubmed: 33979618
pmcid: 8188731
doi: 10.1016/j.celrep.2021.109105
Barczak, A. K. et al. Systematic, multiparametric analysis of Mycobacterium tuberculosis intracellular infection offers insight into coordinated virulence. PLoS Pathog. 13, 1–27 (2017).
doi: 10.1371/journal.ppat.1006363
Quigley, J. et al. The cell wall lipid PDIM contributes to phagosomal escape and host cell exit of Mycobacterium tuberculosis. mBio 8, 1–12 (2017).
doi: 10.1128/mBio.00148-17
Tan, S., Sukumar, N., Abramovitch, R. B., Parish, T. & Russell, D. G. Mycobacterium tuberculosis responds to chloride and pH as synergistic cues to the immune status of its host cell. PLoS Pathog. 9, e1003282 (2013).
pubmed: 23592993
pmcid: 3616970
doi: 10.1371/journal.ppat.1003282
Castillo, E. F. et al. Autophagy protects against active tuberculosis by suppressing bacterial burden and inflammation. Proc. Natl Acad. Sci. USA 109, E3168–E3176 (2012).
pubmed: 23093667
pmcid: 3503152
doi: 10.1073/pnas.1210500109
Flynn, J. L. Lessons from experimental Mycobacterium tuberculosis infections. Microbes Infect. 8, 1179–1188 (2006).
pubmed: 16513383
doi: 10.1016/j.micinf.2005.10.033
MacMicking, J. D. et al. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc. Natl Acad. Sci. USA 94, 5243–5248 (1997).
pubmed: 9144222
pmcid: 24663
doi: 10.1073/pnas.94.10.5243
Schmidt-Supprian, M. & Rajewsky, K. Vagaries of conditional gene targeting. Nat. Immunol. 8, 665–668 (2007).
pubmed: 17579640
doi: 10.1038/ni0707-665
Kramnik, I., Dietrich, W. F., Demant, P. & Bloom, B. R. Genetic control of resistance to experimental infection with virulent Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 97, 8560–8565 (2000).
pubmed: 10890913
pmcid: 26987
doi: 10.1073/pnas.150227197
Ji, D. X. et al. Type I interferon-driven susceptibility to Mycobacterium tuberculosis is mediated by IL-1Ra. Nat. Microbiol 4, 2128–2135 (2019).
pubmed: 31611644
pmcid: 6879852
doi: 10.1038/s41564-019-0578-3
Kreibich, S. et al. Autophagy proteins promote repair of endosomal membranes damaged by the Salmonella Type Three Secretion System 1. Cell Host Microbe 18, 527–537 (2015).
pubmed: 26567507
doi: 10.1016/j.chom.2015.10.015
Diao, J. et al. ATG14 promotes membrane tethering and fusion of autophagosomes to endolysosomes. Nature 520, 563–566 (2015).
pubmed: 25686604
pmcid: 4442024
doi: 10.1038/nature14147
Kim, H. J. et al. Beclin-1-interacting autophagy protein Atg14L targets the SNARE-associated protein Snapin to coordinate endocytic trafficking. J. Cell Sci. 125, 4740–4750 (2012).
pubmed: 22797916
pmcid: 4074282
Murphy, K. C. et al. ORBIT: a new paradigm for genetic engineering of mycobacterial chromosomes. mBio 9, e01467-18 (2018).
pubmed: 30538179
pmcid: 6299477
doi: 10.1128/mBio.01467-18
Takaki, K., Davis, J. M., Winglee, K. & Ramakrishnan, L. Evaluation of the pathogenesis and treatment of Mycobacterium marinum infection in zebrafish. Nat. Protoc. 8, 1114–1124 (2013).
pubmed: 23680983
pmcid: 3919459
doi: 10.1038/nprot.2013.068
Astarie-Dequeker, C. et al. Phthiocerol dimycocerosates of M. tuberculosis participate in macrophage invasion by inducing changes in the organization of plasma membrane lipids. PLoS Pathog. 5, e1000289 (2009).
pubmed: 19197369
pmcid: 2632888
doi: 10.1371/journal.ppat.1000289
Hodgkins, A. et al. WGE: a CRISPR database for genome engineering. Bioinformatics 31, 3078–3080 (2015).
pubmed: 25979474
pmcid: 4565030
doi: 10.1093/bioinformatics/btv308
Skarnes, W. C., Pellegrino, E. & McDonough, J. A. Improving homology-directed repair efficiency in human stem cells. Methods 164–165, 18–28 (2019).
pubmed: 31216442
doi: 10.1016/j.ymeth.2019.06.016