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Research Article | Host-Microbe Biology

Mycobacterium tuberculosis Type VII Secretion System Effectors Differentially Impact the ESCRT Endomembrane Damage Response

Ekansh Mittal, Michael L. Skowyra, Grace Uwase, Emir Tinaztepe, Alka Mehra, Stefan Köster, Phyllis I. Hanson, Jennifer A. Philips
Samuel I. Miller, Editor
Ekansh Mittal
aDivision of Infectious Diseases, Department of Medicine, Washington University School of Medicine, St. Louis, Missouri, USA
bDepartment of Molecular Microbiology, Washington University School of Medicine, St. Louis, Missouri, USA
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Michael L. Skowyra
cDepartment of Cell Biology and Physiology, Washington University School of Medicine, St. Louis, Missouri, USA
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Grace Uwase
aDivision of Infectious Diseases, Department of Medicine, Washington University School of Medicine, St. Louis, Missouri, USA
bDepartment of Molecular Microbiology, Washington University School of Medicine, St. Louis, Missouri, USA
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Emir Tinaztepe
dDivision of Infectious Diseases, Department of Medicine, New York University School of Medicine, New York, New York, USA
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Alka Mehra
dDivision of Infectious Diseases, Department of Medicine, New York University School of Medicine, New York, New York, USA
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Stefan Köster
dDivision of Infectious Diseases, Department of Medicine, New York University School of Medicine, New York, New York, USA
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Phyllis I. Hanson
cDepartment of Cell Biology and Physiology, Washington University School of Medicine, St. Louis, Missouri, USA
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Jennifer A. Philips
aDivision of Infectious Diseases, Department of Medicine, Washington University School of Medicine, St. Louis, Missouri, USA
bDepartment of Molecular Microbiology, Washington University School of Medicine, St. Louis, Missouri, USA
dDivision of Infectious Diseases, Department of Medicine, New York University School of Medicine, New York, New York, USA
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Samuel I. Miller
University of Washington
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DOI: 10.1128/mBio.01765-18
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  • FIG 1
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    FIG 1

    ESCRT-III is recruited to M. tuberculosis (Mtb) phagosomes in an esxA-dependent manner. (A, E, and I) Immunofluorescence (IF) images of CHMP1A (A) and CHMP4B (E and I) in BMDMs that were uninfected (UI) or infected with PKH-labeled H37Rv (WT) or the ΔesxA mutant or GFP-expressing mc26206 or mc26230 (ΔRD1) for 3 h. Images are maximum-intensity projections. Scale bar, 10 μm. Boxed areas in the merged image are shown in higher magnification in the rightmost panel. (B and F) Three-dimensional renderings of individual bacilli, which are also shown in Movies S1 to S4. (C and G) The percentages of bacteria in CHMP1A- and CHMP4B-positive phagosomes were quantified from over 100 bacteria by an individual blind to sample identity (****, P ≤ 0.0001 for CHMP1A, and **, P ≤ 0.0079 for CHMP4B, Fisher's exact test). Automated image analysis was used to quantify the mean fluorescence intensity (MFI) of CHMP1A (D) and CHMP4B (H and J) colocalized with individual bacilli from 5 fields from a 12-mm coverslip. Data are means ± SEM from one representative experiment of three for H37Rv strains or two independent experiments for mc26206 and mc26230. *, P ≤ 0.05, **, P ≤ 0.01, and ***, P ≤ 0.001, Student's t test.

  • FIG 2
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    FIG 2

    EsxH antagonizes ESCRT-III recruitment. (A, B, and C) IF images of CHMP1A (A), CHMP1B (B), and CHMP4B (C) with DsRed-expressing H37Rv or ΔesxH and Δpe5-ppe4 (Δppe) mutants 3 hpi in BMDMs. Images are maximum-intensity projections. Scale bar, 10 μm. Boxed areas in the merged image are shown in higher magnification in the rightmost panel. Mtb, M. tuberculosis. (D to H) Automated image analysis was used to quantify the MFI of CHMP1A (D and E), CHMP1B (F), and CHMP4B (G and H) colocalized with individual bacilli in 5 fields from a 12-mm coverslip. In panels E and H, BMDMs were infected with the PKH-labeled ΔesxH or ΔesxH::esxH mutant for 3 h. Data are means ± SEM from one representative experiment from three (for the WT and ΔesxH mutant in panels A to D, F, and G and the Δpe5-ppe4 mutant in panels A, C, D, and G) or two (for panels E and H and the Δpe5-ppe4 mutant in panels B and F) independent experiments. *, P ≤ 0.05, **, P ≤ 0.01, ***, P ≤ 0.001, and ****, P ≤ 0.0001, Student’s t test. ns, not significant.

  • FIG 3
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    FIG 3

    EsxG-EsxH alters phagosomal GAL3, ubiquitin, and LAMP1. (A, C, and E) IF images of GAL3 (A), ubiquitin (FK2 antibody) (C), and LAMP1 (E) in BMDMs that were infected with DsRed-expressing H37Rv (WT) or the ΔesxH mutant for 3 h. Images are maximum-intensity projections. Scale bar, 10 μm. Boxed areas in the merged image are shown in higher magnification in the rightmost panel. Mtb, M. tuberculosis. (B, D, and F) Automated image analysis was used to quantify the MFI of GAL3 (B), ubiquitin (D), and LAMP1 (F) colocalized with individual bacilli from 5 fields of a 12-mm coverslip. Data are means ± SEM from one representative experiment from three (A, B, E, and F) or two (C and D) independent experiments. ****, P ≤ 0.0001, Student's t test.

  • FIG 4
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    FIG 4

    EsxG-EsxH impairs ESCRT-III recruitment to damaged lysosomes. (A and C) HeLa cells transfected with M. tuberculosis (Mtb) EsxG-EsxH (GH) or the vector control were treated with LLOME or the solvent control and stained for CHMP1B (A) or CHMP4A (C). ESCRT-III and EsxG-EsxH are shown in green and red, respectively. EsxG-EsxH was visualized with an anti-EsxG-EsxH monoclonal antibody. (B and D) Automated image analysis was used to quantify the number of CHMP1B (A) or CHMP4A (B) punctae on 30 macrophages per sample. Data are means ± SEM from one representative experiment from at least three independent experiments. ***, P ≤ 0.001, and ****, P ≤ 0.0001, Student's t test. (E) HeLa cells were transfected with Mtb EsxG-EsxH and loaded with SRB. Live-cell imaging was used to visualize SRB before and after addition of LLOME, after which cells were fixed and stained to visualize EsxG-EsxH (green) and CHMP4A (magenta). Image panels of representative cells are shown at the times indicated from each recording. Individual cells are outlined by white dashed lines. Images are maximum-intensity projections. Scale bars, 10 µm. (F and G) Automated image analysis was used to quantify the number of CHMP4A punctae, the reduction in SRB signal, and the MFI of EsxG-EsxH on a per cell basis. The number of CHMP4A punctae and the reduction is SRB signal were compared in cells with an EsxG-EsxH MFI greater than and less than 500. Data are means ± SEM from one representative experiment from at least three independent experiments. ***, P ≤ 0.001, Student’s t test. ns, not significant. (H) HeLa cells transfected with Mtb or M. smegmatis (Msmeg) EsxG-EsxH were treated with LLOME, and CHMP4A and EsxG-EsxH were visualized. Automated image analysis was used to quantify the EsxG-EsxH MFI and the number of CHMP4A punctae in individual cells. The correlation between EsxG-EsxH expression and number of CHMP4A punctae is shown (R value). Data are means ± SEM from four independent experiments in which at least 100 cells were evaluated.

  • FIG 5
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    FIG 5

    EsxG-EsxH relocalizes in response to membrane damage. HeLa cells transfected with M. tuberculosis (Mtb) EsxG-EsxH were treated with LLOME, and CHMP1B (A) or CHMP4A (B) (red) and EsxG-EsxH (green) was visualized by IF. (C) HeLa cells expressing Mtb EsxG-EsxH were treated with LLOME or the solvent control for 2.5 min. EsxG-EsxH is shown in red. (D) HeLa cells expressing Mtb EsxG-EsxH were treated with LLOME for 1.0 min and then incubated in excess LLOME-free medium for 5 to 30 min as indicated and stained for CHMP4A (green) and EsxG-EsxH (red). (E) Automated image analysis was used to quantify the number of CHMP4A punctae on 30 macrophages per sample from panel D. Data are means ± SEM from one representative experiment from at least two independent experiments. ***, P ≤ 0.001, Student's t test. (F and G) HeLa cells expressing Ms EsxG-EsxH (green) (F) or LacZ (vector control [red]) (G) were treated with LLOME or the solvent control. (H) U2OS cells transfected with Mtb EsxG-EsxH were treated with silica (SiO2) nanoparticles for 15 min and stained for CHMP4A (red) and EsxG-EsxH (green). White arrows indicate the silica nanoparticles. (A to H) Both EsxG-EsxH and LacZ were detected with anti-V5 antibody. Nuclei were stained with DAPI. Images are maximum-intensity projections. Scale bar 10 μm.

  • FIG 6
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    FIG 6

    EsxG-EsxH alters HRS localization during infection. (A) BMDMs were uninfected (UI) or infected with H37Rv (WT), the ΔesxH or ΔesxG mutant, or the ΔesxG complemented strain for 3 h, and HRS was examined by IF. Mtb, M. tuberculosis. (B) The number of HRS punctae was quantified. Data are means ± SEM from three independent experiments. ****, P < 0.0001, and ***, P ≤ 0.0005, one-way ANOVA with Tukey’s multiple-comparison test. ns, not significant. (C) BMDMs were uninfected or infected with the WT or ΔesxH mutant for 1 to 4 h at a multiplicity of infection (MOI) of 10 to 50 as indicated. HRS and β-actin were examined by Western blotting. (D) Immunoelectron microscopy of BMDMs infected for 3 h with the WT and ΔesxH mutant. Red arrows indicate anti-HRS gold particles on M. tuberculosis phagosomes, while vesicular and cytosolic gold particles are indicated with orange and black arrows, respectively. Bacteria are labeled “B.” (E) The subcellular localization of anti-HRS gold particles was quantified from two independent experiments by an investigator blind to sample identity. At least 25 images with at least 174 bacilli per sample were analyzed. The number of anti-HRS gold particles in each sample is indicated (n). ****, P <0.0001, Fisher’s exact test.

  • FIG 7
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    FIG 7

    HRS is not required for ESCRT-III endomembrane damage response. (A and B) HRS does not assemble with ESCRT machinery on LLOME-disrupted endolysosomes. U20S cells were treated with LLOME or the solvent control for 10 min and then stained for HRS and EEA1 (A) or for HRS and CHMP4A (B). Boxed areas are magnified at right. The middle two columns show each indicated stain in grayscale; overlap of both stains in leftmost and rightmost columns appears white. Individual cells are outlined by white dashed lines; scale bars equal 10 μm (2 μm in magnified views). (C) RAW cells were treated with siRNA to deplete HRS or TSG101 for 2 days. Macrophages were then treated with LLOME for 15 min, and ubiquitin (FK2 antibody [red]) and CHMP4B (green) were examined. FK2-positive cells are outlined by white dashed lines. (D and E) Automated image analysis was used to quantify the mean fluorescent intensity (MFI) of FK2 (D) or the number of CHMP4B (E) punctae on 50 macrophages per sample. The number of CHMP4B punctae was compared in cells with FK2 MFI greater than and less than 700. Data are means ± SEM from one representative experiment from at least two independent experiments. ****, P ≤ 0.0001, Student’s t test. ns, not significant. (F) HeLa cells were transfected with M. tuberculosis (Mtb) EsxG-EsxH or vector control, preincubated for 1 h with BAPTA-AM, and then treated with LLOME for 15 min and stained for CHMP4A (green) and EsxG-EsxH (red). EsxG-EsxH was detected with anti-V5 antibody. Nuclei were stained with DAPI. Images are maximum-intensity projections. Scale bar, 10 μm.

  • FIG 8
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    FIG 8

    Model depicting how the presence of ESCRT at the M. tuberculosis phagosome is determined by ESX-1 and ESX-3. (A) In WT bacilli, ESX-1 effectors generate phagosomal damage. EsxG-EsxH antagonizes recruitment of HRS, ESCRT-III, and GAL3 to the phagosome. EsxG-EsxH alters HRS localization during infection, which might impair ESCRT-III recruitment in the context of receptor trafficking, but is unlikely to account for ESCRT-III inhibition in response to endomembrane damage. (B) During infection with a ΔesxA mutant, there is reduced phagosome damage. Without phagosomal perforation, M. tuberculosis is impaired in its ability to manipulate cellular trafficking and immune responses, and therefore, the bacilli are cleared. (C) Infection with ΔesxH mutants results in enhanced recruitment of HRS, ESCRT-III, and GAL3 to bacilli, which interferes with the bacterial virulence program.

Supplemental Material

  • Figures
  • FIG S1

    ESCRT-III is recruited to damaged endolysosomes in macrophages. BMDMs were treated with 1 mM LLOME or solvent control for 15 min. Immunofluorescence microscopy shows CHMP1A (A), CHMP1B (B), and CHMP4B (C) in green. Images are maximum-intensity projections. Nuclei were stained with DAPI. Scale bar, 10 μm. Download FIG S1, JPG file, 1.9 MB.

    Copyright © 2018 Mittal et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • MOVIE S1

    CHMP1A in WT M. tuberculosis-infected cells. The movie shows the three-dimensional immunofluorescence image of CHMP1A in BMDMs infected with WT M. tuberculosis, as shown in the left panel of Fig. 1B. Download Movie S1, MOV file, 3.2 MB.

    Copyright © 2018 Mittal et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • MOVIE S2

    CHMP1A in ΔesxA mutant-infected cells. The movie shows the three-dimensional immunofluorescence image of CHMP1A in BMDMs infected with the ΔesxA mutant, as shown in the right panel of Fig. 1B. Download Movie S2, MOV file, 3.7 MB.

    Copyright © 2018 Mittal et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • MOVIE S3

    CHMP4B in WT M. tuberculosis-infected cells. The movie shows the three-dimensional immunofluorescence image of CHMP4B in BMDMs infected with WT M. tuberculosis, as shown in the left panel of Fig. 1F. Download Movie S3, MOV file, 2.3 MB.

    Copyright © 2018 Mittal et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • MOVIE S4

    CHMP4B in ΔesxA mutant-infected cells. The movie shows the three-dimensional immunofluorescence image of CHMP4B in BMDMs infected with the ΔesxA mutant, as shown in the right panel of Fig. 1F. Download Movie S4, MOV file, 2.6 MB.

    Copyright © 2018 Mittal et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S2

    ESCRT-III recruitment to WT and ΔesxH phagosomes in heavily infected macrophages. Shown are IF images of CHMP1A (A) and CHMP1B (B) in BMDMs that were heavily infected with the DsRED-expressing H37Rv (WT) and ΔesxH mutant for 3 h. Images are maximum-intensity projections. Scale bar, 10 μm. Mtb, M. tuberculosis. (C) BMDMs were uninfected or infected with the WT or ΔesxH mutant for 2 to 4 h at a multiplicity of infection (MOI) of 10 to 50 as indicated. CHMP1A, CHMP1B, and β-actin were examined by Western blotting. Download FIG S2, JPG file, 2.5 MB.

    Copyright © 2018 Mittal et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S3

    Lysosomal trafficking of the Δpe5-ppe4 mutant and ΔesxH::esxH complemented strain. (A and C) IF images of LAMP1 in BMDMs infected with (A) mCherry-expressing ΔesxH and ΔesxH::esxH strains or (C) the DsRed-expressing H37Rv (WT) and Δpe5-ppe4 (Δppe) mutant 3 hpi. Images are maximum-intensity projections. Scale bar, 10 μm. Mtb, M. tuberculosis. (B and D) Automated image analysis was used to quantify the MFI of LAMP1 colocalized with individual bacilli in 5 different fields. Data are means ± SEM from one representative experiment from at least two independent experiments. *, P ≤ 0.05; ****, P ≤ 0.0001. Download FIG S3, JPG file, 2.0 MB.

    Copyright © 2018 Mittal et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S4

    ESCRT-III is recruited to damaged endolysosomes in HeLa cells. HeLa cells were treated with 1 mM LLOME or the solvent control for 15 min. IF shows ALIX (A), CHMP1B (B), CHMP4A (C), and IST1 (D) in green. Images are maximum-intensity projections. Nuclei were stained with DAPI. Scale bar, 10 μm. Download FIG S4, JPG file, 2.1 MB.

    Copyright © 2018 Mittal et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S5

    M. tuberculosis (Mtb) EsxG-EsxH dos not alter total cellular ESCRT levels. HeLa cells transfected with M. tuberculosis EsxG-EsxH were treated with or without LLOME for 15 min, and total cellular extracts were analyzed by Western blotting with the indicated antibodies. Download FIG S5, JPG file, 1.1 MB.

    Copyright © 2018 Mittal et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S6

    HRS and EEA1 in the ΔesxH and Δpe5-ppe4 mutants. (A) IF images of HRS in BMDMs infected with the DsRed-expressing H37Rv or ΔesxH and Δpe5-ppe4 (Δppe) mutants for 3 h. Images are maximum-intensity projections. Scale bar, 10 μm. Mtb, M. tuberculosis. (B) Automated image analysis was used to quantify the number of HRS punctae in 30 macrophages per sample. (C and D) IF images of EEA1 in BMDMs that were uninfected or infected with indicated strains for 3 h. The number of EEA1 punctae was quantified 3 hpi. Data are means ± SEM from one representative experiment from at least three independent experiments. *, P ≤ 0.05, and ***, P ≤ 0.001, Student’s t test. ns, not significant. Download FIG S6, JPG file, 1.4 MB.

    Copyright © 2018 Mittal et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Mycobacterium tuberculosis Type VII Secretion System Effectors Differentially Impact the ESCRT Endomembrane Damage Response
Ekansh Mittal, Michael L. Skowyra, Grace Uwase, Emir Tinaztepe, Alka Mehra, Stefan Köster, Phyllis I. Hanson, Jennifer A. Philips
mBio Nov 2018, 9 (6) e01765-18; DOI: 10.1128/mBio.01765-18

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Mycobacterium tuberculosis Type VII Secretion System Effectors Differentially Impact the ESCRT Endomembrane Damage Response
Ekansh Mittal, Michael L. Skowyra, Grace Uwase, Emir Tinaztepe, Alka Mehra, Stefan Köster, Phyllis I. Hanson, Jennifer A. Philips
mBio Nov 2018, 9 (6) e01765-18; DOI: 10.1128/mBio.01765-18
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    • ABSTRACT
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KEYWORDS

ESCRT
endomembrane damage
Mycobacterium tuberculosis
type VII secretion system
phagosomes

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