Streptococcus pneumoniae triggers hierarchical autophagy through reprogramming of LAPosome-like vesicles via NDP52-delocalization.

Animals Autophagy Biomarkers Cell Line Cytoplasmic Vesicles / metabolism Fluorescent Antibody Technique Gene Expression Genes, Reporter Host-Pathogen Interactions Humans Mice Models, Biological Nuclear Proteins / metabolism Pneumococcal Infections / metabolism Reactive Oxygen Species / metabolism Streptococcus pneumoniae / physiology

Journal

Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179

Informations de publication

Date de publication:
13 01 2020
Historique:
received: 07 05 2019
accepted: 23 12 2019
entrez: 15 1 2020
pubmed: 15 1 2020
medline: 5 5 2021
Statut: epublish

Résumé

In innate immunity, multiple autophagic processes eliminate intracellular pathogens, but it remains unclear whether noncanonical autophagy and xenophagy are coordinated, and whether they occur concomitantly or sequentially. Here, we show that Streptococcus pneumoniae, a causative of invasive pneumococcal disease, can trigger FIP200-, PI3P-, and ROS-independent pneumococcus-containing LC3-associated phagosome (LAPosome)-like vacuoles (PcLVs) in an early stage of infection, and that PcLVs are indispensable for subsequent formation of bactericidal pneumococcus-containing autophagic vacuoles (PcAVs). Specifically, we identified LC3- and NDP52-delocalized PcLV, which are intermediates between PcLV and PcAV. Atg14L, Beclin1, and FIP200 were responsible for delocalizing LC3 and NDP52 from PcLVs. Thus, multiple noncanonical and canonical autophagic processes are deployed sequentially against intracellular S. pneumoniae. The Atg16L1 WD domain, p62, NDP52, and poly-Ub contributed to PcLV formation. These findings reveal a previously unidentified hierarchical autophagy mechanism during bactericidal xenophagy against intracellular bacterial pathogens, and should improve our ability to control life-threating pneumococcal diseases.

Identifiants

DOI: 10.1038/s42003-020-0753-3 PMID: 31932716 PMC: PMC6957511
pubmed: 31932716
doi: 10.1038/s42003-020-0753-3
pii: 10.1038/s42003-020-0753-3
pmc: PMC6957511
doi:

Substances chimiques

Biomarkers 0
CALCOCO2 protein, human 0
Nuclear Proteins 0
Reactive Oxygen Species 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

25

Commentaires et corrections

Type : CommentIn

Références

Mizushima, N., Yoshimori, T. & Ohsumi, Y. The role of Atg proteins in autophagosome formation. Annu Rev. Cell Dev. Biol. 27, 107–132 (2011).
pubmed: 21801009 doi: 10.1146/annurev-cellbio-092910-154005 pmcid: 21801009
Evans, R. J., Sundaramurthy, V. & Frickel, E. M. The interplay of host autophagy and eukaryotic pathogens. Front. Cell Dev. Biol. 6, 118 (2018).
pubmed: 30271774 pmcid: 6146372 doi: 10.3389/fcell.2018.00118
Grumati, P. & Dikic, I. Ubiquitin signaling and autophagy. J. Biol. Chem. 293, 5404–5413 (2017).
pubmed: 29187595 pmcid: 5900779 doi: 10.1074/jbc.TM117.000117
Ogawa, M. et al. A Tecpr1-dependent selective autophagy pathway targets bacterial pathogens. Cell Host Microbe 9, 376–389 (2011).
pubmed: 21575909 doi: 10.1016/j.chom.2011.04.010 pmcid: 21575909
Thurston, T. L., Wandel, M. P., von Muhlinen, N., Foeglein, A. & Randow, F. Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 482, 414–418 (2012).
pubmed: 22246324 pmcid: 3343631 doi: 10.1038/nature10744
Yoshikawa, Y. et al. Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat. Cell Biol. 11, 1233–1240 (2009).
doi: 10.1038/ncb1967
Heckmann, B. L., Boada-Romero, E., Cunha, L. D., Magne, J. & Green, D. R. LC3-Associated Phagocytosis and Inflammation. J. Mol. Biol. 429, 3561–3576 (2017).
pubmed: 28847720 pmcid: 5743439 doi: 10.1016/j.jmb.2017.08.012
Huang, J. et al. Activation of antibacterial autophagy by NADPH oxidases. Proc. Natl Acad. Sci. USA 106, 6226–6231 (2009).
pubmed: 19339495 doi: 10.1073/pnas.0811045106 pmcid: 19339495
Lam, G. Y., Cemma, M., Muise, A. M., Higgins, D. E. & Brumell, J. H. Host and bacterial factors that regulate LC3 recruitment to Listeria monocytogenes during the early stages of macrophage infection. Autophagy 9, 985–995 (2013).
pubmed: 23584039 pmcid: 3722333 doi: 10.4161/auto.24406
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
Mitchell, G. et al. Listeria monocytogenes triggers noncanonical autophagy upon phagocytosis, but avoids subsequent growth-restricting xenophagy. Proc. Natl Acad. Sci. USA 115, E210–E217 (2018).
pubmed: 29279409 doi: 10.1073/pnas.1716055115 pmcid: 29279409
Fletcher, K. et al. The WD40 domain of ATG16L1 is required for its non-canonical role in lipidation of LC3 at single membranes. EMBO J. 37, e97840 (2018).
pubmed: 29317426 pmcid: 5813257 doi: 10.15252/embj.201797840
Kadioglu, A., Weiser, J. N., Paton, J. C. & Andrew, P. W. The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat. Rev. Microbiol. 6, 288–301 (2008).
doi: 10.1038/nrmicro1871
Ogawa, M. et al. Molecular mechanisms of Streptococcus pneumoniae-targeted autophagy via pneumolysin, Golgi-resident Rab41, and Nedd4-1-mediated K63-linked ubiquitination. Cell Microbiol. 20, e12846 (2018).
pubmed: 29582580 doi: 10.1111/cmi.12846 pmcid: 29582580
Fujita, N. et al. Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin. J. Cell Biol. 203, 115–128 (2013).
pubmed: 24100292 pmcid: 3798248 doi: 10.1083/jcb.201304188
Fujita, N. et al. Differential involvement of Atg16L1 in Crohn disease and canonical autophagy: analysis of the organization of the Atg16L1 complex in fibroblasts. J. Biol. Chem. 284, 32602–32609 (2009).
pubmed: 19783656 pmcid: 2781674 doi: 10.1074/jbc.M109.037671
Jefferies, J. M. et al. Presence of nonhemolytic pneumolysin in serotypes of Streptococcus pneumoniae associated with disease outbreaks. J. Infect. Dis. 196, 936–944 (2007).
pubmed: 17703426 doi: 10.1086/520091 pmcid: 17703426
Xiong, Q. et al. The role of ATG16 in autophagy and the ubiquitin proteasome system. Cells 8, E2 (2018).
pubmed: 30577509 doi: 10.3390/cells8010002 pmcid: 30577509
Tan, J. M. J. et al. An ATG16L1-dependent pathway promotes plasma membrane repair and limits Listeria monocytogenes cell-to-cell spread. Nat. Microbiol. 3, 1472–1485 (2018).
pubmed: 30478389 doi: 10.1038/s41564-018-0293-5 pmcid: 30478389
Lystad, A. H. et al. Distinct functions of ATG16L1 isoforms in membrane binding and LC3B lipidation in autophagy-related processes. Nat. Cell Biol. 21, 372–383 (2019).
pubmed: 30778222 pmcid: 7032593 doi: 10.1038/s41556-019-0274-9
Boada-Romero, E. et al. The T300A Crohn’s disease risk polymorphism impairs function of the WD40 domain of ATG16L1. Nat. Commun. 7, 11821 (2016).
pubmed: 27273576 pmcid: 4899871 doi: 10.1038/ncomms11821
Lassen, K. G. et al. Atg16L1 T300A variant decreases selective autophagy resulting in altered cytokine signaling and decreased antibacterial defense. Proc. Natl Acad. Sci. USA 111, 7741–7746 (2014).
pubmed: 24821797 doi: 10.1073/pnas.1407001111 pmcid: 24821797
Homer, C. R., Richmond, A. L., Rebert, N. A., Achkar, J. P. & McDonald, C. ATG16L1 and NOD2 interact in an autophagy-dependent antibacterial pathway implicated in Crohn’s disease pathogenesis. Gastroenterology 139, 1630–1641 (2010). 1641 e1631-1632.
pubmed: 20637199 pmcid: 2967588 doi: 10.1053/j.gastro.2010.07.006
Travassos, L. H. et al. Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry. Nat. Immunol. 11, 55–62 (2010).
pubmed: 19898471 doi: 10.1038/ni.1823 pmcid: 19898471
Long, M. D., Martin, C., Sandler, R. S. & Kappelman, M. D. Increased risk of pneumonia among patients with inflammatory bowel disease. Am. J. Gastroenterol. 108, 240–248 (2013).
pubmed: 23295276 pmcid: 4624299 doi: 10.1038/ajg.2012.406
Casella, G. et al. Pulmonary diseases associated with inflammatory bowel diseases. J. Crohns Colitis 4, 384–389 (2010).
pubmed: 21122533 doi: 10.1016/j.crohns.2010.02.005 pmcid: 21122533
Verlhac, P. et al. Autophagy receptor NDP52 regulates pathogen-containing autophagosome maturation. Cell Host Microbe 17, 515–525 (2015).
pubmed: 25771791 doi: 10.1016/j.chom.2015.02.008 pmcid: 25771791
Surve, M. V. et al. Heterogeneity in pneumolysin expression governs the fate of Streptococcus pneumoniae during blood-brain barrier trafficking. PLoS Pathog. 14, e1007168 (2018).
pubmed: 30011336 pmcid: 6062133 doi: 10.1371/journal.ppat.1007168
Mostowy, S. et al. p62 and NDP52 proteins target intracytosolic Shigella and Listeria to different autophagy pathways. J. Biol. Chem. 286, 26987–26995 (2011).
pubmed: 21646350 pmcid: 3143657 doi: 10.1074/jbc.M111.223610
Cemma, M., Kim, P. K. & Brumell, J. H. The ubiquitin-binding adaptor proteins p62/SQSTM1 and NDP52 are recruited independently to bacteria-associated microdomains to target Salmonella to the autophagy pathway. Autophagy 7, 341–345 (2011).
pubmed: 21079414 pmcid: 3060414 doi: 10.4161/auto.7.3.14046
Maejima, I. et al. Autophagy sequesters damaged lysosomes to control lysosomal biogenesis and kidney injury. EMBO J. 32, 2336–2347 (2013).
pubmed: 23921551 pmcid: 3770333 doi: 10.1038/emboj.2013.171
Li, M. et al. AMDE-1 is a dual function chemical for autophagy activation and inhibition. PLoS ONE 10, e0122083 (2015).
pubmed: 25894744 pmcid: 4403922 doi: 10.1371/journal.pone.0122083
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 pmcid: 25484071
Yahiro, K. et al. Low-density lipoprotein receptor-related protein-1 (LRP1) mediates autophagy and apoptosis caused by Helicobacter pylori VacA. J. Biol. Chem. 287, 31104–31115 (2012).
pubmed: 22822085 pmcid: 3438942 doi: 10.1074/jbc.M112.387498
Kobayashi, N. et al. Segregation of TRAF6-mediated signaling pathways clarifies its role in osteoclastogenesis. EMBO J. 20, 1271–1280 (2001).
pubmed: 11250893 pmcid: 145527 doi: 10.1093/emboj/20.6.1271
Katoh, Y., Nozaki, S., Hartanto, D., Miyano, R. & Nakayama, K. Architectures of multisubunit complexes revealed by a visible immunoprecipitation assay using fluorescent fusion proteins. J. Cell Sci. 128, 2351–2362 (2015).
pubmed: 25964651 doi: 10.1242/jcs.168740 pmcid: 25964651
Kabeya, Y. et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720–5728 (2000).
pubmed: 11060023 pmcid: 305793 doi: 10.1093/emboj/19.21.5720
Hara, T. et al. FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J. Cell Biol. 181, 497–510 (2008).
pubmed: 18443221 pmcid: 2364687 doi: 10.1083/jcb.200712064
Cheong, H., Lindsten, T., Wu, J., Lu, C. & Thompson, C. B. Ammonia-induced autophagy is independent of ULK1/ULK2 kinases. Proc. Natl Acad. Sci. USA 108, 11121–11126 (2011).
pubmed: 21690395 doi: 10.1073/pnas.1107969108 pmcid: 21690395
Kuma, A. et al. The role of autophagy during the early neonatal starvation period. Nature 432, 1032–1036 (2004).
pubmed: 15525940 doi: 10.1038/nature03029 pmcid: 15525940
Jacquemin, G. et al. Granzyme B-induced mitochondrial ROS are required for apoptosis. Cell Death Differ. 22, 862–874 (2015).
pubmed: 25361078 doi: 10.1038/cdd.2014.180 pmcid: 25361078
Saitoh, T. et al. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 456, 264–268 (2008).
pubmed: 18849965 doi: 10.1038/nature07383 pmcid: 18849965
Komatsu, M. et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131, 1149–1163 (2007).
pubmed: 18083104 doi: 10.1016/j.cell.2007.10.035 pmcid: 18083104
Yamamoto, S., Izumiya, H., Morita, M., Arakawa, E. & Watanabe, H. Application of lambda red recombination system to Vibrio cholerae genetics: simple methods for inactivation and modification of chromosomal genes. Gene 438, 57–64 (2009).
pubmed: 19268696 doi: 10.1016/j.gene.2009.02.015 pmcid: 19268696

Auteurs

Michinaga Ogawa (M)

Department of Bacteriology I, National Institute of Infectious Diseases, 1-23-1, Toyama, Shinjuku-ku, Tokyo, 162-8640, Japan. micogawa@nih.go.jp.
ORCID: 0000-0001-6883-6443

Naoki Takada (N)

Department of Bacteriology I, National Institute of Infectious Diseases, 1-23-1, Toyama, Shinjuku-ku, Tokyo, 162-8640, Japan.
Department of Life Science and Medical Bioscience, Waseda University, 2-2 Wakamatsu-cho, Shinjuku-ku, Tokyo, 162-8480, Japan.

Sayaka Shizukuishi (S)

Department of Bacteriology I, National Institute of Infectious Diseases, 1-23-1, Toyama, Shinjuku-ku, Tokyo, 162-8640, Japan.
Department of Microbiology, Yokohama City University Graduate School of Medicine, 3-9 Fukuura, Kanazawa-ku, Yokohama-shi, Kanagawa, 236-0004, Japan.

Mikado Tomokiyo (M)

Department of Bacteriology I, National Institute of Infectious Diseases, 1-23-1, Toyama, Shinjuku-ku, Tokyo, 162-8640, Japan.
School of Veterinary Medicine, Azabu University, Fuchinobe, Sagamihara-shi, Kanagawa, 229-8501, Japan.

Bin Chang (B)

Department of Bacteriology I, National Institute of Infectious Diseases, 1-23-1, Toyama, Shinjuku-ku, Tokyo, 162-8640, Japan.

Mitsutaka Yoshida (M)

Laboratory of Morphology and Image Analysis, Research Support Center, Juntendo University, 2-1-1, Hongo, Bunkyo-ku, Tokyo, 113-8421, Japan.

Soichiro Kakuta (S)

Laboratory of Morphology and Image Analysis, Research Support Center, Juntendo University, 2-1-1, Hongo, Bunkyo-ku, Tokyo, 113-8421, Japan.
Department of Cellular and Molecular Neuropathology, Graduate School of Medicine, Juntendo University, 2-1-1, Hongo, Bunkyo-ku, Tokyo, 113-8421, Japan.

Isei Tanida (I)

Department of Cellular and Molecular Neuropathology, Graduate School of Medicine, Juntendo University, 2-1-1, Hongo, Bunkyo-ku, Tokyo, 113-8421, Japan.

Akihide Ryo (A)

Department of Microbiology, Yokohama City University Graduate School of Medicine, 3-9 Fukuura, Kanazawa-ku, Yokohama-shi, Kanagawa, 236-0004, Japan.

Jun-Lin Guan (JL)

Department of Cancer Biology, University of Cincinnati College of Medicine, CARE/Crawley Building, Suite E-870 3230 Eden Avenue, Cincinnati, OH, 45267, USA.

Haruko Takeyama (H)

Department of Life Science and Medical Bioscience, Waseda University, 2-2 Wakamatsu-cho, Shinjuku-ku, Tokyo, 162-8480, Japan.
Computational Bio Big-Data Open Innovation Laboratory, AIST-Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo, 169-0072, Japan.
Research Organization for Nano & Life Innovation, Waseda University, 513 Wasedatsurumaki-cho, Shinjuku-ku, Tokyo, 162-0041, Japan.
Institute for Advanced Research of Biosystem Dynamics, Waseda Research Institute for Science and Engineering, Graduate School of Advanced Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo, 169-8555, Japan.

Makoto Ohnishi (M)

Department of Bacteriology I, National Institute of Infectious Diseases, 1-23-1, Toyama, Shinjuku-ku, Tokyo, 162-8640, Japan.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female

Evaluation of Low-Value Services Across Major Medicare Advantage Insurers and Traditional Medicare.

Ciara Duggan, Adam L Beckman, Ishani Ganguli et al.
1.00
Humans United States Aged Cross-Sectional Studies Medicare Part C

Effectiveness of Virtual Yoga for Chronic Low Back Pain: A Randomized Clinical Trial.

Hallie Tankha, Devyn Gaskins, Amanda Shallcross et al.
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Streptococcus pneumoniae triggers hierarchical...
questionsmedicales.fr › Phénomènes physiologiques cellulaires › Autophagie › Streptococcus pneumoniae triggers hierarchical...
questionsmedicales.fr › Facteurs biologiques › Marqueurs biologiques › Streptococcus pneumoniae triggers hierarchical...
questionsmedicales.fr › Cellules › Cellules cultivées › Lignée cellulaire › Streptococcus pneumoniae triggers hierarchical...
questionsmedicales.fr › Cellules › Structures cellulaires › Espace intracellulaire › Cytoplasme › Structures cytoplasmiques › Organites › Vésicules cytoplasmiques › Streptococcus pneumoniae triggers hierarchical...
questionsmedicales.fr › Techniques d'investigation › Techniques immunologiques › Technique d'immunofluorescence › Streptococcus pneumoniae triggers hierarchical...
questionsmedicales.fr › Phénomènes génétiques › Expression des gènes › Streptococcus pneumoniae triggers hierarchical...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Composants de génome › Gènes › Gènes rapporteurs › Streptococcus pneumoniae triggers hierarchical...
questionsmedicales.fr › Phénomènes biologiques › Interactions hôte-microbes › Interactions hôte-pathogène › Streptococcus pneumoniae triggers hierarchical...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Streptococcus pneumoniae triggers hierarchical...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Streptococcus pneumoniae triggers hierarchical...
questionsmedicales.fr › Techniques d'investigation › Modèles théoriques › Modèles biologiques › Streptococcus pneumoniae triggers hierarchical...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines nucléaires › Streptococcus pneumoniae triggers hierarchical...
questionsmedicales.fr › Infection › Infections bactériennes et mycoses › Infections bactériennes › Infections bactériennes à Gram positif › Infections à streptocoques › Infections à pneumocoques › Streptococcus pneumoniae triggers hierarchical...
questionsmedicales.fr › Produits chimiques inorganiques › Composés de l'oxygène › Espèces réactives de l'oxygène › Streptococcus pneumoniae triggers hierarchical...
questionsmedicales.fr › Bactéries › Bactéries à Gram positif › Lactobacillales › Streptococcaceae › Streptococcus › Streptococcus pneumoniae › Streptococcus pneumoniae triggers hierarchical...