Recruitment of both the ESCRT and autophagic machineries to ejecting Mycobacterium marinum.
Dictyostelium discoideum
Mycobacterium marinum
ESCRT
autophagy
ejectosome
Journal
Molecular microbiology
ISSN: 1365-2958
Titre abrégé: Mol Microbiol
Pays: England
ID NLM: 8712028
Informations de publication
Date de publication:
25 May 2023
25 May 2023
Historique:
revised:
24
04
2023
received:
21
02
2023
accepted:
01
05
2023
medline:
26
5
2023
pubmed:
26
5
2023
entrez:
25
5
2023
Statut:
aheadofprint
Résumé
Cytosolic Mycobacterium marinum are ejected from host cells such as macrophages or the amoeba Dictyostelium discoideum in a non-lytic fashion. As described previously, the autophagic machinery is recruited to ejecting bacteria and supports host cell integrity during egress. Here, we show that the ESCRT machinery is also recruited to ejecting bacteria, partially dependent on an intact autophagic pathway. As such, the AAA-ATPase Vps4 shows a distinct localization at the ejectosome structure in comparison to fluorescently tagged Vps32, Tsg101 and Alix. Along the bacterium engaged in ejection, ESCRT and the autophagic component Atg8 show partial colocalization. We hypothesize that both, the ESCRT and autophagic machinery localize to the bacterium as part of a membrane damage response, as well as part of a "frustrated autophagosome" that is unable to engulf the ejecting bacterium.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : DFG Priority Program 2225
Organisme : Deutsche Forschungsgemeinschaft
ID : HA3473/8-1
Organisme : Deutsche Forschungsgemeinschaft
ID : HA3474/3-1
Organisme : Deutsche Forschungsgemeinschaft
ID : HA3474/3-2
Organisme : Health and Medical University Potsdam
Organisme : Leibniz-Gemeinschaft
Informations de copyright
© 2023 The Authors. Molecular Microbiology published by John Wiley & Sons Ltd.
Références
Barisch, C. & Soldati, T. (2017) Breaking fat! How mycobacteria and other intracellular pathogens manipulate host lipid droplets. Biochimie, 141, 54-61.
Carroll P, Schreuder LJ, Muwanguzi-Karugaba J, Wiles S, Robertson BD, Ripoll J, et al. (2010) Sensitive detection of gene expression in mycobacteria under replicating and non-replicating conditions using optimized far-red reporter. PLoS One. 5(3), e9823.
Flieger, A., Frischknecht, F., Häcker, G., Hornef, M.W. & Pradel, G. (2018) Pathways of host cell exit by intracellular pathogens. Microb Cell, 5(12), 525-544.
Friedrich, N., Hagedorn, M., Soldati-Favre, D. & Soldati, T. (2012) Prison break: pathogens' strategies to egress from host cells. Microbiology and Molecular Biology Reviews, 76(4), 707-720.
Gerstenmaier, L., Pilla, R., Herrmann, L., Herrmann, H., Prado, M., Villafano, G.J. et al. (2015) The autophagic machinery ensures nonlytic transmission of mycobacteria. Proceedings of the National Academy of Sciences of the United States of America, 112(7), E687-E692.
Hagedorn, M., Neuhaus, E.M. & Soldati, T. (2006) Optimized fixation and immunofluorescence staining methods for Dictyostelium cells. Methods in Molecular Biology, 346, 327-338.
Hagedorn, M., Rohde, K.H., Russell, D.G. & Soldati, T. (2009) Infection by tubercular mycobacteria is spread by nonlytic ejection from their amoeba hosts. Science, 323(5922), 1729-1733.
Hagedorn, M. & Soldati, T. (2007) Flotillin and RacH modulate the intracellular immunity of Dictyostelium to Mycobacterium marinum infection. Cellular Microbiology, 9(11), 2716-2733.
Houben, D., Demangel, C., van Ingen, J., Perez, J., Baldeon, L., Abdallah, A.M. et al. (2012) ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria. Cellular Microbiology, 14(8), 1287-1298.
Jimenez, A.J., Maiuri, P., Lafaurie-Janvore, J., Divoux, S., Piel, M. & Perez, F. (2014) ESCRT machinery is required for plasma membrane repair. Science, 343(6174), 1247136.
King, J.S., Gueho, A., Hagedorn, M., Gopaldass, N., Leuba, F., Soldati, T. et al. (2013) WASH is required for lysosomal recycling and efficient autophagic and phagocytic digestion. Molecular Biology of the Cell, 24(17), 2714-2726.
King, J.S., Veltman, D.M. & Insall, R.H. (2011) The induction of autophagy by mechanical stress. Autophagy, 7(12), 1490-1499.
Koliwer-Brandl, H., Knobloch, P., Barisch, C., Welin, A., Hanna, N., Soldati, T. et al. (2019) Distinct Mycobacterium marinum phosphatases determine pathogen vacuole phosphoinositide pattern, phagosome maturation, and escape to the cytosol. Cellular Microbiology, 21(6), e13008.
Lopez-Jimenez, A.T., Cardenal-Munoz, E., Leuba, F., Gerstenmaier, L., Barisch, C., Hagedorn, M. et al. (2018) 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 Pathogens, 14(12), e1007501.
Mehra, A., Zahra, A., Thompson, V., Sirisaengtaksin, N., Wells, A., Porto, M. et al. (2013) Mycobacterium tuberculosis type VII secreted effector EsxH targets host ESCRT to impair trafficking. PLoS Pathogens, 9(10), e1003734.
Meßling, S., Matthias, J., Xiong, Q., Fischer, S. & Eichinger, L. (2017) The two Dictyostelium discoideum autophagy 8 proteins have distinct autophagic functions. European Journal of Cell Biology, 96(4), 312-324.
Mittal, E., Skowyra, M.L., Uwase, G., Tinaztepe, E., Mehra, A., Köster, S. et al. (2018) Mycobacterium tuberculosis type VII secretion system effectors differentially impact the ESCRT endomembrane damage response. mBio, 9(6), e01765-18.
Philips, J.A., Porto, M.C., Wang, H., Rubin, E.J. & Perrimon, N. (2008) ESCRT factors restrict mycobacterial growth. Proceedings of the National Academy of Sciences of the United States of America, 105(8), 3070-3075.
Portal-Celhay, C., Tufariello, J.M., Srivastava, S., Zahra, A., Klevorn, T., Grace, P.S. et al. (2016) Mycobacterium tuberculosis EsxH inhibits ESCRT-dependent CD4(+) T-cell activation. Nature Microbiology, 2, 16232.
Rasband, W.S. (1997-2018) ImageJ. U.S. National Institute of Health, Bethesda, MD, USA. https://imagej.nih.gov/ij/
Raykov, L., Mottet, M., Nitschke, J. & Soldati, T. (2021) The Dictyostelium discoideum E3 ubiquitin ligase TrafE coordinates endolysosomal damage response and cell-autonomous immunity to Mycobacterium marinum. bioRxiv, 2021-06. Available from: https://doi.org/10.1101/2021.2006.2029.450281
Rusten, T.E. & Stenmark, H. (2009) How do ESCRT proteins control autophagy? Journal of Cell Science, 122(Pt 13), 2179-2183.
Simeone, R., Bobard, A., Lippmann, J., Bitter, W., Majlessi, L., Brosch, R. et al. (2012) Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathogens, 8(2), e1002507.
Takahashi, Y., He, H., Tang, Z., Hattori, T., Liu, Y., Young, M.M. et al. (2018) An autophagy assay reveals the ESCRT-III component CHMP2A as a regulator of phagophore closure. Nature Communications, 9(1), 2855.
Takahashi, Y., Liang, X., Hattori, T., Tang, Z., He, H., Chen, H. et al. (2019) VPS37A directs ESCRT recruitment for phagophore closure. The Journal of Cell Biology, 218(10), 3336-3354.
van der Wel, N., Hava, D., Houben, D., Fluitsma, D., van Zon, M., Pierson, J. et al. (2007) M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell, 129(7), 1287-1298.
Vietri, M., Radulovic, M. & Stenmark, H. (2020) The many functions of ESCRTs. Nature Reviews. Molecular Cell Biology, 21(1), 25-42.
Westman, J., Plumb, J., Licht, A., Yang, M., Allert, S., Naglik, J.R. et al. (2022) Calcium-dependent ESCRT recruitment and lysosome exocytosis maintain epithelial integrity during Candida albicans invasion. Cell Reports, 38(1), 110187.
Wollert, T. & Hurley, J.H. (2010) Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature, 464(7290), 864-869.
Zhen, Y., Spangenberg, H., Munson, M.J., Brech, A., Schink, K.O., Tan, K.W. et al. (2020) ESCRT-mediated phagophore sealing during mitophagy. Autophagy, 16(5), 826-841.