SpringerLink
Log in

The crosstalk between bacteria and host autophagy: host defense or bacteria offense

  • Minireview
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Xenophagy is a specific selective autophagy for the elimination of intracellular bacteria. Current evidence suggests that the processes for host autophagy system to recognize and eliminate invading bacteria are complex, and vary according to different pathogens. Although both ubiquitin-dependent and ubiquitin-independent autophagy exist in host to defense invading bacteria, successful pathogens have evolved diverse strategies to escape from or paralyze host autophagy system. In this review, we discuss the mechanisms of host autophagy system to recognize and eliminate intracellular pathogens and the mechanisms of different pathogens to escape from or paralyze host autophagy system, with a particular focus on the most extensively studied bacteria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abdullah, M., Greenfield, L.K., Bronte-Tinkew, D., Capurro, M.I., Rizzuti, D., and Jones, N.L. 2019. VacA promotes CagA accumulation in gastric epithelial cells during Helicobacter pylori infection. Sci. Rep. 9, 38.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aikawa, C., Nakajima, S., Karimine, M., Nozawa, T., Minowa-Nozawa, A., Toh, H., Yamada, S., and Nakagawa, I. 2018. NLRX1 negatively regulates Group A Streptococcus invasion and autophagy induction by interacting with the Beclin1-UVRAG complex. Front. Cell Infect. Microbiol. 8, 403.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ammanathan, V., Mishra, P., Chavalmane, A.K., Muthusamy, S., Jadhav, V., Siddamadappa, C., and Manjithaya, R. 2020. Restriction of intracellular Salmonella replication by restoring TFEB-mediated xenophagy. Autophagy 16, 1584–1597.

    Article  CAS  PubMed  Google Scholar 

  • Andersson, A.M., Andersson, B., Lorell, C., Raffetseder, J., Larsson, M., and Blomgran, R. 2016. Autophagy induction targeting mTORC1 enhances Mycobacterium tuberculosis replication in HIV co-infected human macrophages. Sci. Rep. 6, 28171.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anding, A.L. and Baehrecke, E.H. 2017. Cleaning house: selective autophagy of organelles. Dev. Cell 41, 10–22.

    Article  CAS  Google Scholar 

  • Aredia, F. and Scovassi, A.I. 2017. A new function for miRNAs as regulators of autophagy. Future Med. Chem. 9, 25–36.

    Article  CAS  PubMed  Google Scholar 

  • Augenstreich, J., Haanappel, E., Ferré, G., Czaplicki, G., Jolibois, F., Destainville, N., Guilhot, C., Milon, A., Astarie-Dequeker, C., and Chavent, M. 2019. The conical shape of DIM lipids promotes Mycobacterium tuberculosis infection of macrophages. Proc. Natl. Acad. Sci. USA 116, 25649–25658.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bah, A., Sanicas, M., Nigou, J., Guilhot, C., Astarie-Dequeker, C., and Vergne, I. 2020. The lipid virulence factors of Mycobacterium tuberculosis exert multilayered control over autophagy-related pathways in infected human macrophages. Cells 9, 666.

    Article  CAS  PubMed Central  Google Scholar 

  • Barnett, T.C., Liebl, D., Seymour, L.M., Gillen, C.M., Lim, J.Y., Larock, C.N., Davies, M.R., Schulz, B.L., Nizet, V., Teasdale, R.D., et al. 2013. The globally disseminated M1T1 clone of Group A Streptococcus evades autophagy for intracellular replication. Cell Host Microbe 14, 675–682.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Behar, S.M. and Baehrecke, E.H. 2015. Tuberculosis: autophagy is not the answer. Nature 528, 482–483.

    Article  CAS  PubMed  Google Scholar 

  • Birmingham, C.L., Smith, A.C., Bakowski, M.A., Yoshimori, T., and Brumell, J.H. 2006. Autophagy controls Salmonella infection in response to damage to the Salmonella-containing vacuole. J. Biol. Chem. 281, 11374–11383.

    Article  CAS  PubMed  Google Scholar 

  • Capurro, M.I., Greenfield, L.K., Prashar, A., **a, S., Abdullah, M., Wong, H., Zhong, X.Z., Bertaux-Skeirik, N., Chakrabarti, J., Siddiqui, I., et al. 2019. VacA generates a protective intracellular reservoir for Helicobacter pylori that is eliminated by activation of the lysosomal calcium channel TRPML1. Nat. Microbiol. 4, 1411–1423.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casanova, J.E. 2017. Bacterial autophagy: offense and defense at the host-pathogen interface. Cell. Mol. Gastroenterol. Hepatol. 4, 237–243.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cattaneo, R. 2004. Four viruses, two bacteria, and one receptor: membrane cofactor protein (CD46) as pathogens’ magnet. J. Virol. 78, 4385–4388.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cemma, M., Kim, P.K., and Brumell, J.H. 2011. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cerni, S., Shafer, D., To, K., and Venketaraman, V. 2019. Investigating the role of everolimus in mTOR inhibition and autophagy promotion as a potential host-directed therapeutic target in Mycobacterium tuberculosis infection. J. Clin. Med. 8, 232.

    Article  CAS  PubMed Central  Google Scholar 

  • Chai, Q., Wang, X., Qiang, L., Zhang, Y., Ge, P., Lu, Z., Zhong, Y., Li, B., Wang, J., Zhang, L., et al. 2019. A Mycobacterium tuberculosis surface protein recruits ubiquitin to trigger host xenophagy. Nat. Commun. 10, 1973.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chandra, V., Bhagyaraj, E., Nanduri, R., Ahuja, N., and Gupta, P. 2015. NR1D1 ameliorates Mycobacterium tuberculosis clearance through regulation of autophagy. Autophagy 11, 1987–1997.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chauhan, S., Kumar, S., Jain, A., Ponpuak, M., Mudd, M.H., Kimura, T., Choi, S.W., Peters, R., Mandell, M., Bruun, J.A., et al. 2016. TRIMs and galectins globally cooperate and TRIM16 and Galectin-3 co-direct autophagy in endomembrane damage homeostasis. Dev. Cell 39, 13–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, Z., Wang, T., Liu, Z., Zhang, G., Wang, J., Feng, S., and Liang, J. 2015. Inhibition of autophagy by MiR-30A induced by Mycobacteria tuberculosis as a possible mechanism of immune escape in human macrophages. Jpn. J. Infect. Dis. 68, 420–424.

    Article  CAS  PubMed  Google Scholar 

  • Cheng, S., Wang, L., Liu, Q., Qi, L., Yu, K., Wang, Z., Wu, M., Liu, Y., Fu, J., Hu, M., et al. 2017. Identification of a novel Salmonella type III effector by quantitative secretome profiling. Mol. Cell. Proteomics 16, 2219–2228.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choy, A., Dancourt, J., Mugo, B., O’Connor, T.J., Isberg, R.R., Melia, T.J., and Roy, C.R. 2012. The Legionella effector RavZ inhibits host autophagy through irreversible Atg8 deconjugation. Science 338, 1072–1076.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chu, Y., Kang, Y., Yan, C., Yang, C., Zhang, T., Huo, H., and Liu, Y. 2020. LUBAC and OTULIN regulate autophagy initiation and maturation by mediating the linear ubiquitination and the stabilization of ATG13. Autophagy 17, 1688–1699.

    Google Scholar 

  • Ding, S., Qu, Y., Yang, S., Zhao, Y., and Xu, G. 2019. Novel miR-1958 promotes Mycobacterium tuberculosis survival in RAW264.7 cells by inhibiting autophagy via Atg5. J. Microbiol. Biotechnol. 29, 989–998.

    Article  CAS  PubMed  Google Scholar 

  • Dortet, L., Mostowy, S., Samba-Louaka, A., Gouin, E., Nahori, M.A., Wiemer, E.A.C., Dussurget, O., and Cossart, P. 2011. Recruitment of the major vault protein by InlK: a Listeria monocytogenes strategy to avoid autophagy. PLoS Pathog. 7, e1002168.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dupont, N., Lacas-Gervais, S., Bertout, J., Paz, I., Freche, B., Van Nhieu, G.T., van der Goot, F.G., Sansonetti, P.J., and Lafont, F. 2009. Shigella phagocytic vacuolar membrane remnants participate in the cellular response to pathogen invasion and are regulated by autophagy. Cell Host Microbe 6, 137–149.

    Article  CAS  PubMed  Google Scholar 

  • Etna, M.P., Sinigaglia, A., Grassi, A., Giacomini, E., Romagnoli, A., Pardini, M., Severa, M., Cruciani, M., Rizzo, F., Anastasiadou, E., et al. 2018. Mycobacterium tuberculosis-induced miR-155 subverts autophagy by targeting ATG3 in human dendritic cells. PLoS Pathog. 14, e1006790.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fabri, M., Stenger, S., Shin, D.M., Yuk, J.M., Liu, P.T., Realegeno, S., Lee, H.M., Krutzik, S.R., Schenk, M., Sieling, P.A., et al. 2011. Vitamin D is required for IFN-γ-mediated antimicrobial activity of human macrophages. Sci. Transl. Med. 3, 104ra102.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Floto, R.A., Sarkar, S., Perlstein, E.O., Kampmann, B., Schreiber, S.L., and Rubinsztein, D.C. 2007. Small molecule enhancers of rapamycin-induced TOR inhibition promote autophagy, reduce toxicity in Huntington’s disease models and enhance killing of mycobacteria by macrophages. Autophagy 3, 620–622.

    Article  CAS  PubMed  Google Scholar 

  • Foegeding, N.J., Raghunathan, K., Campbell, A.M., Kim, S.W., Lau, K.S., Kenworthy, A.K., Cover, T.L., and Ohi, M.D. 2019. Intracellular degradation of Helicobacter pylori VacA toxin as a determinant of gastric epithelial cell viability. Infect. Immun. 87, e00783–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Franco, L.H., Nair, V.R., Scharn, C.R., Xavier, R.J., Torrealba, J.R., Shiloh, M.U., and Levine, B. 2017. The ubiquitin ligase Smurf1 functions in selective autophagy of Mycobacterium tuberculosis and anti-tuberculous host defense. Cell Host Microbe 21, 59–72.

    Article  CAS  PubMed  Google Scholar 

  • Gatica, D., Lahiri, V., and Klionsky, D.J. 2018. Cargo recognition and degradation by selective autophagy. Nat. Cell Biol. 20, 233–242.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gomes, L.C. and Dikic, I. 2014. Autophagy in antimicrobial immunity. Mol. Cell 54, 224–233.

    Article  CAS  PubMed  Google Scholar 

  • Greenfield, L.K. and Jones, N.L. 2013. Modulation of autophagy by Helicobacter pylori and its role in gastric carcinogenesis. Trends Microbiol. 21, 602–612.

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez, M.G., Master, S.S., Singh, S.B., Taylor, G.A., Colombo, M.I., and Deretic, V. 2004. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119, 753–766.

    Article  CAS  PubMed  Google Scholar 

  • Haobam, B., Nozawa, T., Minowa-Nozawa, A., Tanaka, M., Oda, S., Watanabe, T., Aikawa, C., Maruyama, F., and Nakagawa, I. 2014. Rab17-mediated recycling endosomes contribute to autophagosome formation in response to Group A Streptococcus invasion. Cell. Microbiol. 16, 1806–1821.

    Article  CAS  PubMed  Google Scholar 

  • Haraga, A., Ohlson, M.B., and Miller, S.I. 2008. Salmonellae interplay with host cells. Nat. Rev. Microbiol. 6, 53–66.

    Article  CAS  PubMed  Google Scholar 

  • Hooi, J.K.Y., Lai, W.Y., Ng, W.K., Suen, M.M.Y., Underwood, F.E., Tanyingoh, D., Malfertheiner, P., Graham, D.Y., Wong, V.W.S., Wu, J.C.Y., et al. 2017. Global Prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology 153, 420–429.

    Article  PubMed  Google Scholar 

  • Huang, J. and Brumell, J.H. 2014. Bacteria-autophagy interplay: a battle for survival. Nat. Rev. Microbiol. 12, 101–114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huett, A., Heath, R.J., Begun, J., Sassi, S.O., Baxt, L.A., Vyas, J.M., Goldberg, M.B., and Xavier, R.J. 2012. The LRR and RING domain protein LRSAM1 is an E3 ligase crucial for ubiquitin-dependent autophagy of intracellular Salmonella Typhimurium. Cell Host Microbe 12, 778–790.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joubert, P.E., Meiffren, G., Grégoire, I.P., Pontini, G., Richetta, C., Flacher, M., Azocar, O., Vidalain, P.O., Vidal, M., Lotteau, V., et al. 2009. Autophagy induction by the pathogen receptor CD46. Cell Host Microbe 6, 354–366.

    Article  PubMed  CAS  Google Scholar 

  • Kim, Y.S., Lee, H.M., Kim, J.K., Yang, C.S., Kim, T.S., Jung, M., **, H.S., Kim, S., Jang, J., Oh, G.T., et al. 2017a. PPAR-α activation mediates innate host defense through induction of TFEB and lipid catabolism. J. Immunol. 198, 3283–3295.

    Article  CAS  PubMed  Google Scholar 

  • Kim, I.J., Lee, J., Oh, S.J., Yoon, M.S., Jang, S.S., Holland, R.L., Reno, M.L., Hamad, M.N., Maeda, T., Chung, H.J., et al. 2018a. Helicobacter pylori infection modulates host cell metabolism through VacA-dependent inhibition of mTORC1. Cell Host Microbe 23, 583–593.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, J.K., Lee, H.M., Park, K.S., Shin, D.M., Kim, T.S., Kim, Y.S., Suh, H.W., Kim, S.Y., Kim, I.S., Kim, J.M., et al. 2017b. MIR144* inhibits antimicrobial responses against Mycobacterium tuberculosis in human monocytes and macrophages by targeting the autophagy protein DRAM2. Autophagy 13, 423–441.

    Article  CAS  PubMed  Google Scholar 

  • Kim, S.Y., Yang, C.S., Lee, H.M., Kim, J.K., Kim, Y.S., Kim, Y.R., Kim, J.S., Kim, T.S., Yuk, J.M., Dufour, C.R., et al. 2018b. ESRRA (estrogen-related receptor alpha) is a key coordinator of transcriptional and post-translational activation of autophagy to promote innate host defense. Autophagy 14, 152–168.

    Article  CAS  PubMed  Google Scholar 

  • Kim, J.K., Yuk, J.M., Kim, S.Y., Kim, T.S., **, H.S., Yang, C.S., and Jo, E.K. 2015. MicroRNA-125a inhibits autophagy activation and antimicrobial responses during mycobacterial infection. J. Immunol. 194, 5355–5365.

    Article  CAS  PubMed  Google Scholar 

  • Kimmey, J.M., Huynh, J.P., Weiss, L.A., Park, S., Kambal, A., Debnath, J., Virgin, H.W., and Stallings, C.L. 2015. Unique role for ATG5 in neutrophil-mediated immunopathology during M. tuberculosis infection. Nature 528, 565–569.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kohler, L.J. and Roy, C.R. 2017. Autophagic targeting and avoidance in intracellular bacterial infections. Curr. Opin. Microbiol. 35, 36–41.

    Article  PubMed  Google Scholar 

  • Komatsu, M., Waguri, S., Koike, M., Sou, Y.S., Ueno, T., Hara, T., Mizushima, N., Iwata, J., Ezaki, J., Murata, S., et al. 2007. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131, 1149–1163.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, R., Sahu, S.K., Kumar, M., Jana, K., Gupta, P., Gupta, U.D., Kundu, M., and Basu, J. 2016. MicroRNA 17-5p regulates autophagy in Mycobacterium tuberculosis-infected macrophages by targeting Mcl-1 and STAT3. Cell. Microbiol. 18, 679–691.

    Article  CAS  PubMed  Google Scholar 

  • LaRock, D.L., Chaudhary, A., and Miller, S.I. 2015. Salmonellae interactions with host processes. Nat. Rev. Microbiol. 13, 191–205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lau, N., Haeberle, A.L., O’Keeffe, B.J., Latomanski, E.A., Celli, J., Newton, H.J., and Knodler, L.A. 2019. SopF, a phosphoinositide binding effector, promotes the stability of the nascent Salmonella-containing vacuole. PLoS Pathog. 15, e1007959.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Linares, J.F., Duran, A., Yajima, T., Pasparakis, M., Moscat, J., and Diaz-Meco, M.T. 2013. K63 polyubiquitination and activation of mTOR by the p62-TRAF6 complex in nutrient-activated cells. Mol. Cell 51, 283–296.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, F., Chen, J., Wang, P., Li, H., Zhou, Y., Liu, H., Liu, Z., Zheng, R., Wang, L., Yang, H., et al. 2018. MicroRNA-27a controls the intracellular survival of Mycobacterium tuberculosis by regulating calcium-associated autophagy. Nat. Commun. 9, 4295.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu, G., Wan, Q., Li, J., Hu, X., Gu, X., and Xu, S. 2020. Silencing miR-125b-5p attenuates inflammatory response and apoptosis inhibition in mycobacterium tuberculosis-infected human macrophages by targeting DNA damage-regulated autophagy modulator 2 (DRAM2). Cell Cycle 19, 3182–3194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Merle, N.S., Noe, R., Halbwachs-Mecarelli, L., Fremeaux-Bacchi, V., and Roumenina, L.T. 2015. Complement system part II: role in immunity. Front. Immunol. 6, 257.

    PubMed  PubMed Central  Google Scholar 

  • Mesquita, F.S., Thomas, M., Sachse, M., Santos, A.J., Figueira, R., and Holden, D.W. 2012. The Salmonella deubiquitinase SseL inhibits selective autophagy of cytosolic aggregates. PLoS Pathog. 8, e1002743.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mizushima, N. and Komatsu, M. 2011. Autophagy: renovation of cells and tissues. Cell 147, 728–741.

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa, I., Amano, A., Mizushima, N., Yamamoto, A., Yamaguchi, H., Kamimoto, T., Nara, A., Funao, J., Nakata, M., Tsuda, K., et al. 2004. Autophagy defends cells against invading Group A Streptococcus. Science 306, 1037–1040.

    Article  CAS  PubMed  Google Scholar 

  • Nakajima, S., Aikawa, C., Nozawa, T., Minowa-Nozawa, A., Toh, H., and Nakagawa, I. 2017. Bcl-xL Affects Group A Streptococcus-induced autophagy directly, by inhibiting fusion between autophagosomes and lysosomes, and indirectly, by inhibiting bacterial internalization via interaction with Beclin 1-UVRAG. PLoS ONE 12, e0170138.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nakajima, K., Nozawa, T., Minowa-Nozawa, A., Toh, H., Yamada, S., Aikawa, C., and Nakagawa, I. 2019. RAB30 regulates PI4KB (phosphatidylinositol 4-kinase beta)-dependent autophagy against Group A Streptococcus. Autophagy 15, 466–477.

    Article  CAS  PubMed  Google Scholar 

  • Neumann, Y., Bruns, S.A., Rohde, M., Prajsnar, T.K., Foster, S.J., and Schmitz, I. 2016. Intracellular Staphylococcus aureus eludes selective autophagy by activating a host cell kinase. Autophagy 12, 2069–2084.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nozawa, T., Aikawa, C., Goda, A., Maruyama, F., Hamada, S., and Nakagawa, I. 2012. The small GTPases Rab9A and Rab23 function at distinct steps in autophagy during Group A Streptococcus infection. Cell. Microbiol. 14, 1149–1165.

    Article  CAS  PubMed  Google Scholar 

  • Ogawa, M., Yoshikawa, Y., Mimuro, H., Hain, T., Chakraborty, T., and Sasakawa, C. 2011. Autophagy targeting of Listeria monocytogenes and the bacterial countermeasure. Autophagy 7, 310–314.

    Article  CAS  PubMed  Google Scholar 

  • Ouimet, M., Koster, S., Sakowski, E., Ramkhelawon, B., van Solingen, C., Oldebeken, S., Karunakaran, D., Portal-Celhay, C., Sheedy, F.J., Ray, T.D., et al. 2016. Mycobacterium tuberculosis induces the miR-33 locus to reprogram autophagy and host lipid metabolism. Nat. Immunol. 17, 677–686.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paik, S., Kim, J.K., Chung, C., and Jo, E.K. 2019. Autophagy: a new strategy for host-directed therapy of tuberculosis. Virulence 10, 448–459.

    Article  CAS  PubMed  Google Scholar 

  • Palucci, I. and Delogu, G. 2018. Host directed therapies for tuberculosis: futures strategies for an ancient disease. Chemotherapy 63, 172–180.

    Article  CAS  PubMed  Google Scholar 

  • Peng, H., Yang, J., Li, G., You, Q., Han, W., Li, T., Gao, D., **e, X., Lee, B.H., Du, J., et al. 2017. Ubiquitylation of p62/sequestosome1 activates its autophagy receptor function and controls selective autophagy upon ubiquitin stress. Cell Res. 27, 657–674.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Philpott, D.J., Sorbara, M.T., Robertson, S.J., Croitoru, K., and Girardin, S.E. 2014. NOD proteins: regulators of inflammation in health and disease. Nat. Rev. Immunol. 14, 9–23.

    Article  CAS  PubMed  Google Scholar 

  • Qu, Y., Ding, S., Ma, Z., Jiang, D., Xu, X., Zhang, Y., Zhang, A., and Xu, G. 2019. MiR-129-3p favors intracellular BCG survival in RAW264.7 cells by inhibiting autophagy via Atg4b. Cell. Immunol. 337, 22–32.

    Article  CAS  PubMed  Google Scholar 

  • Queiroz, A. and Riley, L.W. 2017. Bacterial immunostat: Mycobacterium tuberculosis lipids and their role in the host immune response. Rev. Soc. Bras. Med. Trop. 50, 9–18.

    Article  PubMed  Google Scholar 

  • Quigley, J., Hughitt, V.K., Velikovsky, C.A., Mariuzza, R.A., El-Sayed, N.M., and Briken, V. 2017. The cell wall lipid PDIM contributes to phagosomal escape and host cell exit of Mycobacterium tuberculosis. mBio 8, e00148–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raju, D., Hussey, S., Ang, M., Terebiznik, M.R., Sibony, M., Galindo-Mata, E., Gupta, V., Blanke, S.R., Delgado, A., Romero-Gallo, J., et al. 2012. Vacuolating cytotoxin and variants in Atg16L1 that disrupt autophagy promote Helicobacter pylori infection in humans. Gastroenterology 142, 1160–1171.

    Article  CAS  PubMed  Google Scholar 

  • Ravenhill, B.J., Boyle, K.B., von Muhlinen, N., Ellison, C.J., Masson, G.R., Otten, E.G., Foeglein, A., Williams, R., and Randow, F. 2019. The cargo receptor NDP52 initiates selective autophagy by recruiting the ULK complex to cytosol-invading bacteria. Mol. Cell 74, 320–329.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rekha, R.S., Rao Muvva, S.S.V., Wan, M., Raqib, R., Bergman, P., Brighenti, S., Gudmundsson, G.H., and Agerberth, B. 2015. Phenylbutyrate induces LL-37-dependent autophagy and intracellular killing of Mycobacterium tuberculosis in human macrophages. Autophagy 11, 1688–1699.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ricci, V. 2016. Relationship between VacA toxin and host cell autophagy in Helicobacter pylori infection of the human stomach: a few answers, many questions. Toxins 8, 203.

    Article  PubMed Central  CAS  Google Scholar 

  • Rikihis, Y. 1984. Glycogen autophagosomes in polymorphonuclear leukocytes induced by rickettsiae. Anat. Rec. 208, 319–327.

    Article  Google Scholar 

  • Rolando, M., Escoll, P., Nora, T., Botti, J., Boitez, V., Bedia, C., Daniels, C., Abraham, G., Stogios, P.J., Skarina, T., et al. 2016. Legionella pneumophila S1P-lyase targets host sphingolipid metabolism and restrains autophagy. Proc. Natl. Acad. Sci. USA 113, 1901–1906.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sahu, S.K., Kumar, M., Chakraborty, S., Banerjee, S.K., Kumar, R., Gupta, P., Jana, K., Gupta, U.D., Ghosh, Z., Kundu, M., et al. 2017. MicroRNA 26a (miR-26a)/KLF4 and CREB-C/EBPβ regulate innate immune signaling, the polarization of macrophages and the trafficking of Mycobacterium tuberculosis to lysosomes during infection. PLoS Pathog. 13, e1006410.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sharma, V., Verma, S., Seranova, E., Sarkar, S., and Kumar, D. 2018. Selective autophagy and xenophagy in infection and disease. Front. Cell. Dev. Biol. 6, 147.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sheedlo, M.J., Qiu, J., Tan, Y., Paul, L.N., Luo, Z.Q., and Das, C. 2015. Structural basis of substrate recognition by a bacterial deubiquitinase important for dynamics of phagosome ubiquitination. Proc. Natl. Acad. Sci. USA 112, 15090–15095.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shui, W., Petzold, C.J., Redding, A., Liu, J., Pitcher, A., Sheu, L., Hsieh, T.Y., Keasling, J.D., and Bertozzi, C.R. 2011. Organelle membrane proteomics reveals differential influence of mycobacterial lipoglycans on macrophage phagosome maturation and autophagosome accumulation. J. Proteome Res. 10, 339–348.

    Article  CAS  PubMed  Google Scholar 

  • Silwal, P., Kim, Y.S., Basu, J., and Jo, E.K. 2020. The roles of micro-RNAs in regulation of autophagy during bacterial infection. Semin. Cell Dev. Biol. 101, 51–58.

    Article  CAS  PubMed  Google Scholar 

  • Simon, H.U., Friis, R., Tait, S.W.G., and Ryan, K.M. 2017. Retrograde signaling from autophagy modulates stress responses. Sci. Signal 10, eaag2791.

    Article  PubMed  Google Scholar 

  • Singh, P. and Subbian, S. 2018. Harnessing the mTOR pathway for tuberculosis treatment. Front. Microbiol. 9, 70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siqueira, M.D.S., Ribeiro, R.M., and Travassos, L.H. 2018. Autophagy and its interaction with intracellular bacterial pathogens. Front. Immunol. 9, 935.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sorbara, M.T., Foerster, E.G., Tsalikis, J., Abdel-Nour, M., Mangiapane, J., Sirluck-Schroeder, I., Tattoli, I., van Dalen, R., Isenman, D.E., Rohde, J.R., et al. 2018. Complement C3 drives autophagy-dependent restriction of cyto-invasive bacteria. Cell Host Microbe 23, 644–652.

    Article  CAS  PubMed  Google Scholar 

  • Terebiznik, M.R., Raju, D., Vazquez, C.L., Torbricki, K., Kulkarni, R., Blanke, S.R., Yoshimori, T., Colombo, M.I., and Jones, N.L. 2009. Effect of Helicobacter pylori’s vacuolating cytotoxin on the autophagy pathway in gastric epithelial cells. Autophagy 5, 370–379.

    Article  CAS  PubMed  Google Scholar 

  • Thurston, T.L., Wandel, M.P., von Muhlinen, N., Foeglein, A., and Randow, F. 2012. Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 482, 414–418.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Travassos, L.H., Carneiro, L.A., Ramjeet, M., Hussey, S., Kim, Y.G., Magalhães, J.G., Yuan, L., Soares, F., Chea, E., Le Bourhis, L., et al. 2010. Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry. Nat. Immunol. 11, 55–62.

    Article  CAS  PubMed  Google Scholar 

  • van Wijk, S.J.L., Fricke, F., Herhaus, L., Gupta, J., Hotte, K., Pampaloni, F., Grumati, P., Kaulich, M., Sou, Y.S., Komatsu, M., et al. 2017. Linear ubiquitination of cytosolic Salmonella Typhimurium activates NF-κB and restricts bacterial proliferation. Nat. Microbiol. 2, 17066.

    Article  CAS  PubMed  Google Scholar 

  • Vergne, I., Chua, J., Singh, S.B., and Deretic, V. 2004. Cell biology of Mycobacterium tuberculosis phagosome. Annu. Rev. Cell Dev. Biol. 20, 367–394.

    Article  CAS  PubMed  Google Scholar 

  • Vergne, I., Gilleron, M., and Nigou, J. 2014. Manipulation of the endocytic pathway and phagocyte functions by Mycobacterium tuberculosis lipoarabinomannan. Front. Cell. Infect. Microbiol. 4, 187.

    PubMed  Google Scholar 

  • Verlhac, P., Grégoire, I.P., Azocar, O., Petkova, D.S., Baguet, J., Viret, C., and Faure, M. 2015. Autophagy receptor NDP52 regulates pathogen-containing autophagosome maturation. Cell Host Microbe 17, 515–525.

    Article  CAS  PubMed  Google Scholar 

  • Walker, M.J., Barnett, T.C., McArthur, J.D., Cole, J.N., Gillen, C.M., Henningham, A., Sriprakash, K.S., Sanderson-Smith, M.L., and Nizet, V. 2014. Disease manifestations and pathogenic mechanisms of Group A Streptococcus. Clin. Microbiol. Rev. 27, 264–301.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang, J., Yang, K., Zhou, L., Minhaowu, Wu, Y., Zhu, M., Lai, X., Chen, T., Feng, L., Li, M., Huang, C., et al. 2013. MicroRNA-155 promotes autophagy to eliminate intracellular mycobacteria by targeting Rheb. PLoS Pathog. 9, e1003697.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Watson, R.O., Manzanillo, P.S., and Cox, J.S. 2012. Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 150, 803–815.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wild, P., Farhan, H., McEwan, D.G., Wagner, S., Rogov, V.V., Brady, N.R., Richter, B., Korac, J., Waidmann, O., Choudhary, C., et al. 2011. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 333, 228–233.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilkinson, D.S., Jariwala, J.S., Anderson, E., Mitra, K., Meisenhelder, J., Chang, J.T., Ideker, T., Hunter, T., Nizet, V., Dillin, A., et al. 2015. Phosphorylation of LC3 by the Hippo kinases STK3/STK4 is essential for autophagy. Mol. Cell 57, 55–68.

    Article  CAS  PubMed  Google Scholar 

  • Wu, Y.W. and Li, F. 2019. Bacterial interaction with host autophagy. Virulence 10, 352–362.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu, Y., Zhou, P., Cheng, S., Lu, Q., Nowak, K., Hopp, A.K., Li, L., Shi, X., Zhou, Z., Gao, W., et al. 2019. A bacterial effector reveals the V-ATPase-ATG16L1 axis that initiates xenophagy. Cell 178, 552–566.

    Article  CAS  PubMed  Google Scholar 

  • Yahiro, K., Akazawa, Y., Nakano, M., Suzuki, H., Hisatune, J., Isomoto, H., Sap, J., Noda, M., Moss, J., and Hirayama, T. 2015. Helicobacter pylori VacA induces apoptosis by accumulation of connexin 43 in autophagic vesicles via a Rac1/ERK-dependent pathway. Cell Death Discov. 1, 15035.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yahiro, K., Satoh, M., Nakano, M., Hisatsune, J., Isomoto, H., Sap, J., Suzuki, H., Nomura, F., Noda, M., Moss, J., et al. 2012. Low-density lipoprotein receptor-related protein-1 (LRP1) mediates autophagy and apoptosis caused by Helicobacter pylori VacA. J. Biol. Chem. 287, 31104–31115.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshikawa, Y., Ogawa, M., Hain, T., Yoshida, M., Fukumatsu, M., Kim, M., Mimuro, H., Nakagawa, I., Yanagawa, T., Ishii, T., et al. 2009. Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat. Cell Biol. 11, 1233–1240.

    Article  CAS  PubMed  Google Scholar 

  • Yuan, Q., Chen, H., Yang, Y., Fu, Y., and Yi, Z. 2020. miR-18a promotes Mycobacterial survival in macrophages via inhibiting autophagy by down-regulation of ATM. J. Cell. Mol. Med. 24, 2004–2012.

    Article  CAS  PubMed  Google Scholar 

  • Yuk, J.M., Shin, D.M., Lee, H.M., Yang, C.S., **, H.S., Kim, K.K., Lee, Z.W., Lee, S.H., Kim, J.M., and Jo, E.K. 2009. Vitamin D3 induces autophagy in human monocytes/macrophages via cathelicidin. Cell Host Microbe 6, 231–243.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, R., Varela, M., Vallentgoed, W., Forn-Cuni, G., van der Vaart, M., and Meijer, A.H. 2019. The selective autophagy receptors Optineurin and p62 are both required for zebrafish host resistance to mycobacterial infection. PLoS Pathog. 15, e1007329.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng, Y.T., Shahnazari, S., Brech, A., Lamark, T., Johansen, T., and Brumell, J.H. 2009. The adaptor protein p62/SQSTM1 targets invading bacteria to the autophagy pathway. J. Immunol. 183, 5909–5916.

    Article  CAS  PubMed  Google Scholar 

  • Zulauf, K.E., Sullivan, J.T., and Braunstein, M. 2018. The SecA2 pathway of Mycobacterium tuberculosis exports effectors that work in concert to arrest phagosome and autophagosome maturation. PLoS Pathog. 14, e1007011.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Funds of China (81903138, 31871198), Cooperative Innovation Center of Engineering and New Products for Developmental Biology of Hunan Province (20134486), and the Opening Fund of The National & Local Joint Engineering Laboratory of Animal Peptide Drug Development (Hunan Normal University, National Development and Reform Commission).

Author information

Authors and Affiliations

  1. Center for Biomedical Aging, National & Local Joint Engineering Laboratory of Animal Peptide Drug Development, College of Life Sciences, Hunan Normal University, Changsha, Hunan, 410081, P. R. China

    Lin Zheng, Fang Wei & Guolin Li

  2. Key Laboratory of Hunan Province for Model Animal and Stem Cell Biology, School of Medicine, Hunan Normal University, Changsha, Human, 410081, P. R. China

    Guolin Li

Authors
  1. Lin Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fang Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guolin Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

F.W. and L.Z. wrote the manuscript, and F.W. and G.L. revised the manuscript.

Corresponding authors

Correspondence to Fang Wei or Guolin Li.

Ethics declarations

Authors declare that they are no conflicts of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zheng, L., Wei, F. & Li, G. The crosstalk between bacteria and host autophagy: host defense or bacteria offense. J Microbiol. 60, 451–460 (2022). https://doi.org/10.1007/s12275-022-2009-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-022-2009-z

Keywords

Search

Navigation