An ATG16L1-dependent pathway promotes plasma membrane repair and limits Listeria monocytogenes cell-to-cell spread

Tan, Joel M J; Mellouk, Nora; Osborne, Suzanne E.; Ammendolia, Dustin A.; Dyer, Diana; Ren, Li; Brunen, Diede; Rijn, Jorik M. van; Huang, Ju; Czuczman, Mark A.; Cemma, Marija; Won, Amy; Yip, Christopher M.; Xavier, Ramnik J.; MacDuff, Donna A.; Reggiori, Fulvio; Debnath, Jayanta; Yoshimori, Tamotsu; Kim, Peter K.; Fairn, Gregory D.; Coyaud, Étienne; Raught, Brian; Muise, Aleixo M.; Higgins, Darren E.; Brumell, John H.

doi:10.1038/s41564-018-0293-5

Cited by 60 publications

(61 citation statements)

References 61 publications

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“…16 Jurkat T cells, U937, and THP-1 were incubated with HIS6X-GFP-D4, and analyzed by flow cytometry to quantify outer leaflet plasma membrane cholesterol. 22 U937 and THP-1 cells displayed comparable binding affinities to D4. In contrast, D4 binding to Jurkat T cells was significantly elevated ( Figure 3A).…”

Section: Pneumolysin Shows Preferential Binding To the Plasma Membrmentioning

confidence: 88%

“…We established the ratio of PLY-pores to microvesicles by Cryo-EM. 22 Cells were incubated for 10 minutes with HIS6X-GFP-D4, washed and immediately analyzed by FACS. Their total number per microvesicle did not differ significantly in the three vesicle fractions (Supplemental Figure S3C).…”

Section: Distinct Differences In the Speed Of Microvesicle Sheddingmentioning

confidence: 99%

“…A, Jurkat T cells, U937, and THP-1 cells were stimulated with HIS6X-GFP-D4 as described. 22 Cells were incubated for 10 minutes with HIS6X-GFP-D4, washed and immediately analyzed by FACS. Mean ± SEM is shown (n = 6).…”

Section: Distinct Differences In the Speed Of Microvesicle Sheddingmentioning

confidence: 99%

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Bacterial pore‐forming toxin pneumolysin: Cell membrane structure and microvesicle shedding capacity determines differential survival of immune cell types

et al. 2019

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Bacterial infectious diseases can lead to death or to serious illnesses. These outcomes are partly the consequence of pore-forming toxins, which are secreted by the pathogenic bacteria (eg, pneumolysin of Streptococcus pneumoniae). Pneumolysin binds to cholesterol within the plasma membrane of host cells and assembles to form transmembrane pores, which can lead to Ca 2+ influx and cell death. Membrane repair mechanisms exist that limit the extent of damage. Immune cells which are essential to fight bacterial infections critically rely on survival mechanisms after detrimental pneumolysin attacks. This study investigated the susceptibility of different immune cell types to pneumolysin. As a model system, we used the lymphoid T-cell line Jurkat, and myeloid cell lines U937 and THP-1. We show that Jurkat T cells are highly susceptible to pneumolysin attack. In contrast, myeloid THP-1 and U937 cells are less susceptible to pneumolysin. In line with these findings, human primary T cells are shown to be more susceptible to pneumolysin attack than monocytes.Differences in susceptibility to pneumolysin are due to (I) preferential binding of pneumolysin to Jurkat T cells and (II) cell type specific plasma membrane repair capacity. Myeloid cell survival is mostly dependent on Ca 2+ induced expelling of damaged plasma membrane areas as microvesicles. Thus, in myeloid cells, first-line defense cells in bacterial infections, a potent cellular repair machinery ensures cell survival after pneumolysin attack. In lymphoid cells, which are important at later stages of infections, less efficient repair mechanisms and enhanced toxin binding renders the cells more sensitive to pneumolysin. K E Y W O R D Sbacterial pore-forming toxins, host-defense, lymphoid immune cells, myeloid immune cells, plasma membrane repair 1666 | LARPIN et AL.

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Section: Pneumolysin Shows Preferential Binding To the Plasma Membrmentioning

confidence: 88%

Section: Distinct Differences In the Speed Of Microvesicle Sheddingmentioning

confidence: 99%

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Bacterial pore‐forming toxin pneumolysin: Cell membrane structure and microvesicle shedding capacity determines differential survival of immune cell types

et al. 2019

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“…Non-canonical autophagy in epithelial cells may reduce IAV replication by increasing transfer of endocytosed virus to 15 lysosomes for degradation. This may involve increased fusion with lysosomes following recruitment of LC3 by TMEM59 36 , or by maintaining membrane repair during virus entry, as observed for S. Typhimurium and Listeria monocytogenes 7,37 . A p22 phox -NOX2 pathway that recruits LC3 to vacuoles containing S. Typhimuriumin epithelial cells 38 may also be activated during IAV entry and hamper lethal infection.…”

Section: Discussionmentioning

confidence: 99%

The WD and linker domains of ATG16L1 required for non-canonical autophagy limit lethal respiratory infection by influenza A virus at epithelial surfaces

Wang

Zhang

Jefferson

et al. 2020

Preprint

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† These authors contributed equally to this work 20 15 extensive viral replication throughout the lungs, cytokine dysregulation, fulminant pneumonia and lung inflammation leading to high mortality associated with virulent strains. Conditional mouse models and ex vivo analysis showed that protection against IAV infection of lung required non-canonical autophagy within epithelial barriers but was independent of phagocytes and other leukocytes. This establishes non-canonical 20 autophagy pathways in epithelial cells as a novel innate defence mechanism that can restrict IAV infection at mucosal surfaces.

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“…This resulted in less efficient lysosomal exocytosis, which is needed for efficient plasma membrane repair. Interestingly, MEFs harbouring the ATG16L1 T300A allele, which was previously found to increase the risk of Crohn's disease (CD), were also less efficient in plasma membrane repair (Serramito-Gómez et al, 2016, Tan et al, 2018. There is also evidence that ATG16L1 modulates the balance between NOD2-induced xenophagy versus cytokine production.…”

Section: Further Autophagy-independent Functions Of Atg5 Atg12 and Amentioning

confidence: 98%

Dictyostelium discoideum and autophagy – a perfect pair

Fischer¹,

Eichinger²

2019

Int. J. Dev. Biol.

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Autophagy is subdivided into chaperone-mediated autophagy, microautophagy and macroautophagy and is a highly conserved intracellular degradative pathway. It is crucial for cellular homeostasis and also serves as a response to different stresses. Here we focus on macroautophagy, which targets damaged organelles and large protein assemblies, as well as pathogenic intracellular microbes for destruction. During this process, cytosolic material becomes enclosed in newly generated double-membrane vesicles, the so-called autophagosomes. Upon maturation, the autophagosome fuses with the lysosome for degradation of the cargo. The basic molecular machinery that controls macroautophagy works in a sequential order and consists of the ATG1 complex, the PtdIns3K complex, the membrane delivery system, two ubiquitin-like conjugation systems, and autophagy adaptors and receptors. Since the different stages of macroautophagy from initiation to final degradation of cargo are tightly regulated and highly conserved across eukaryotes, simple model organisms in combination with a wide range of techniques contributed significantly to advance our understanding of this complex dynamic process. Here, we present the social amoeba Dictyostelium discoideum as an advantageous and relevant experimental model system for the analysis of macroautophagy.KEY WORDS: autophagy, ubiquitin-proteasome system (UPS), LC3-associated phagocytosis, proteaphagy Int. J. Dev. Biol. 63: 485-495 (2019)

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An ATG16L1-dependent pathway promotes plasma membrane repair and limits Listeria monocytogenes cell-to-cell spread

Cited by 60 publications

References 61 publications

Bacterial pore‐forming toxin pneumolysin: Cell membrane structure and microvesicle shedding capacity determines differential survival of immune cell types

Bacterial pore‐forming toxin pneumolysin: Cell membrane structure and microvesicle shedding capacity determines differential survival of immune cell types

The WD and linker domains of ATG16L1 required for non-canonical autophagy limit lethal respiratory infection by influenza A virus at epithelial surfaces

Dictyostelium discoideum and autophagy – a perfect pair

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