Roles of autophagy in elimination of intracellular bacterial pathogens

Frontiers in Immunology

Volumn 4, Issue MAY, 2013, Pages

  Jo, Eun Kyeong ^a   Yuk, Jae Min ^a   Shin, Dong Min ^a   Sasakawa, Chihiro ^b  

^a Chungnam National University   (South Korea)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Autophagic receptors; Autophagy; Innate immunity; Listeria; Mycobacteria; Salmonella; Shigella; Xenophagy

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; AUTOPHAGY PROTEIN 5; AUTOPHAGY RELATED PROTEIN 8; BECLIN 1; BETA INTERFERON; CASPASE 3; CASPASE 8; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CATHEPSIN D; GALECTIN 8; GAMMA INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 12; INTERLEUKIN 23; INTERLEUKIN 8; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PEPTIDES AND PROTEINS; PEPTIDOGLYCAN RECOGNITION PROTEIN; PHOSPHOLIPASE C; PROTEIN P62; RAB PROTEIN; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN; VITAMIN D;

ARTICLE; AUTOLYSOSOME; BACTERIAL CLEARANCE; CELL MATURATION; CELL SURVIVAL; HUMAN; INNATE IMMUNITY; INTRACELLULAR BACTERIAL PATHOGEN; LEGIONNAIRE DISEASE; LISTERIOSIS; MYCOBACTERIOSIS; MYCOBACTERIUM BOVIS BCG; NONHUMAN; PATHOGENESIS; PHAGOSOME; PROTEIN AGGREGATION; SALMONELLOSIS; SHIGELLOSIS; TUBERCULOSIS; XENOPHAGY;

EID: 84881030026     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00097     Document Type: Article

References (77)

1. Alonso, S., Pethe, K., Russell, D. G., and Purdy, G. E. (2007). Lysosomal killing of Mycobacterium mediated by ubiquitin-derived peptides is enhanced by autophagy. Proc. Natl. Acad. Sci. U.S.A. 104, 6031-6036.
2. Amer, A. O., and Swanson, M. S. (2005). Autophagy is an immediate macrophage response to Legionella pneumophila. Cell. Microbiol. 7, 765-778.
3. Ashida, H., Ogawa, M., Mimuro, H., Kobayashi, T., Sanada, T., and Sasakawa, C. (2011). Shigella are versatile mucosal pathogens that circumvent the host innate immune system. Curr. Opin. Immunol. 23, 448-455.
4. Bakowski, M. A., Braun, V., and Brumell, J. H. (2008). Salmonella-containing vacuoles: directing traffic and nesting to grow. Traffic 9, 2022-2031.
5. Banga, S., Gao, P., Shen, X., Fiscus, V., Zong, W. X., Chen, L., et al. (2007). Legionella pneumophila inhibits macrophage apoptosis by targeting pro-death members of the Bcl2 protein family. Proc. Natl. Acad. Sci. U.S.A. 104, 5121-5126.
6. Barbuddhe, S. B., and Chakraborty, T. (2009). Listeria as an enteroinvasive gastrointestinal pathogen. Curr. Top. Microbiol. Immunol. 337, 173-195.
7. Basu, J., Shin, D. M., and Jo, E. K. (2012). Mycobacterial signaling through toll-like receptors. Front. Cell. Infect. Microbiol. 2:145. doi:10.3389/fcimb.2012.00145
8. Behrends, C., Sowa, M. E., Gygi, S. P., and Harper, J. W. (2010). Network organization of the human autophagy system. Nature 466, 68-76.
9. Birmingham, C. L., Canadien, V., Gouin, E., Troy, E. B., Yoshimori, T., Cossart, P., et al. (2007). Listeria monocytogenes evades killing by autophagy during colonization of host cells. Autophagy 3, 442-451.
10. Birmingham, C. L., Canadien, V., Kaniuk, N. A., Steinberg, B. E., Higgins, D. E., and Brumell, J. H. (2008). Listeriolysin O allows Listeria monocytogenes replication in macrophage vacuoles. Nature 451, 350-354.
11. 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.
12. Chen, D., Fan, W., Lu, Y., Ding, X., Chen, S., and Zhong, Q. (2012). A mammalian autophagosome maturation mechanism mediated by Tecpr1 and the Atg12-Atg5 conjugate. Mol. Cell 45, 629-641.
13. Choy, A., Dancourt, J., Mugo, B., O'Connor, T. J., Isberg, R. R., Melia, T. J., et al. (2012). The Legionella effector Ravz inhibits host autophagy through irreversible Atg8 deconjugation. Science 338, 1072-1076.
14. Collins, C. A., and Brown, E. J. (2010). Cytosol as battleground: ubiquitin as a weapon for both host and pathogen. Trends Cell Biol. 20, 205-213.
15. Deretic, V. (2008). Autophagy, an immunologic magic bullet: Mycobacterium tuberculosis phagosome maturation block and how to bypass it. Future Microbiol. 3, 517-524.
16. Deretic, V. (2011). Autophagy in immunity and cell-autonomous defense against intracellular microbes. Immunol. Rev. 240, 92-104.
17. Deretic, V., and Levine, B. (2009). Autophagy, immunity, and microbial adaptations. Cell Host Microbe 5, 527-549.
18. Deretic, V., Singh, S., Master, S., Harris, J., Roberts, E., Kyei, G., et al. (2006). Mycobacterium tuberculosis inhibition of phagolysosome biogenesis and autophagy as a host defence mechanism. Cell. Microbiol. 8, 719-727.
19. Dong, N., Zhu, Y., Lu, Q., Hu, L., Zheng, Y., and Shao, F. (2012). Structurally distinct bacterial Tbc-like gaps link Arf Gtpase to Rab1 inactivation to counteract host defenses. Cell 150, 1029-1041.
20. Dortet, L., Mostowy, S., Samba-Louaka, A., Gouin, E., Nahori, M. A., Wiemer, E. A., et al. (2011). Recruitment of the major vault protein by Inlk: a Listeria monocytogenes strategy to avoid autophagy. PLoS Pathog. 7:e1002168. doi:10.1371/journal.ppat.1002168
21. Dubuisson, J. F., and Swanson, M. S. (2006). Mouse infection by Legionella, a model to analyze autophagy. Autophagy 2, 179-182.
22. Dupont, N., Lacas-Gervais, S., Bertout, J., Paz, I., Freche, B., Van Nhieu, G. T., et al. (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.
23. Fujita, N., and Yoshimori, T. (2011). Ubiquitination-mediated autophagy against invading bacteria. Curr. Opin. Cell Biol. 23, 492-497.
24. Harriff, M. J., Purdy, G. E., and Lewinsohn, D. M. (2012). Escape from the phagosome: the explanation for Mhc-I processing of mycobacterial antigens? Front. Immunol. 3:40. doi:10.3389/fimmu.2012.00040
25. Huynh, K. K., Joshi, S. A., and Brown, E. J. (2011). A delicate dance: host response to mycobacteria. Curr. Opin. Immunol. 23, 464-472.
26. Joshi, A. D., and Swanson, M. S. (2011). Secrets of a successful pathogen: Legionella resistance to progression along the autophagic pathway. Front. Microbiol. 2:138. doi:10.3389/fmicb.2011.00138
27. Kim, J. J., Lee, H. M., Shin, D. M., Kim, W., Yuk, J. M., Jin, H. S., et al. (2012). Host cell autophagy activated by antibiotics is required for their effective antimycobacterial drug action. Cell Host Microbe 11, 457-468.
28. Kirkin, V., Lamark, T., Sou, Y. S., Bjorkoy, G., Nunn, J. L., Bruun, J. A., et al. (2009). A role for Nbr1 in autophagosomal degradation of ubiquitinated substrates. Mol. Cell 33, 505-516.
29. Korac, J., Schaeffer, V., Kovacevic, I., Clement, A. M., Jungblut, B., Behl, C., et al. (2013). Ubiquitin-independent function of optineurin in autophagic clearance of protein aggregates. J. Cell. Sci. 126, 580-592.
30. Lamark, T., Kirkin, V., Dikic, I., and Johansen, T. (2009). Nbr1 and P62 as cargo receptors for selective autophagy of ubiquitinated targets. Cell Cycle 8, 1986-1990.
31. Lambrechts, A., Gevaert, K., Cossart, P., Vandekerckhove, J., and Van Troys, M. (2008). Listeria comet tails: the actin-based motility machinery at work. Trends Cell Biol. 18, 220-227.
32. Lee, M. S., Cherla, R. P., Jenson, M. H., Leyva-Illades, D., Martinez-Moczygemba, M., and Tesh, V. L. (2011). Shiga toxins induce autophagy leading to differential signalling pathways in toxin-sensitive and toxin-resistant human cells. Cell. Microbiol. 13, 1479-1496.
33. Levine, B. (2005). Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell 120, 159-162.
34. Levine, B., Mizushima, N., and Virgin, H. W. (2011). Autophagy in immunity and inflammation. Nature 469, 323-335.
35. Manzanillo, P. S., Shiloh, M. U., Portnoy, D. A., and Cox, J. S. (2012). Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 11, 469-480.
36. Matsuda, F., Fujii, J., and Yoshida, S. (2009). Autophagy induced by 2-Deoxy-D-Glucose suppresses intracellular multiplication of Legionella pneumophila in a/J mouse macrophages. Autophagy 5, 484-493.
37. Meyer-Morse, N., Robbins, J. R., Rae, C. S., Mochegova, S. N., Swanson, M. S., Zhao, Z., et al. (2010). Listeriolysin O is necessary and sufficient to induce autophagy during Listeria monocytogenes infection. PLoS ONE 5:e8610. doi:10.1371/journal.pone.0008610
38. Moors, M. A., Levitt, B., Youngman, P., and Portnoy, D. A. (1999). Expression of Listeriolysin O and acta by intracellular and extracellular Listeria monocytogenes. Infect. Immun. 67, 131-139.
39. Mostowy, S., Bonazzi, M., Hamon, M. A., Tham, T. N., Mallet, A., Lelek, M., et al. (2010). Entrapment of intracytosolic bacteria by septin cage-like structures. Cell Host Microbe 8, 433-444.
40. Mostowy, S., Sancho-Shimizu, V., Hamon, M. A., Simeone, R., Brosch, R., Johansen, T., et al. (2011). P62 and Ndp52 proteins target intracytosolic Shigella and Listeria to different autophagy pathways. J. Biol. Chem. 286, 26987-26995.
41. Noda, T., Kageyama, S., Fujita, N., and Yoshimori, T. (2012). Three-axis model for Atg recruitment in autophagy against Salmonella. Int. J. Cell. Biol. 2012, 389562.
42. Ogawa, M., Nakagawa, I., Yoshikawa, Y., Hain, T., Chakraborty, T., and Sasakawa, C. (2009). Streptococcus-, Shigella-, and Listeria-induced autophagy. Meth. Enzymol. 452, 363-381.
43. Ogawa, M., Yoshikawa, Y., Kobayashi, T., Mimuro, H., Fukumatsu, M., Kiga, K., et al. (2011a). A Tecpr1-dependent selective autophagy pathway targets bacterial pathogens. Cell Host Microbe 9, 376-389.
44. Ogawa, M., Yoshikawa, Y., Mimuro, H., Hain, T., Chakraborty, T., and Sasakawa, C. (2011b). Autophagy targeting of Listeria monocytogenes and the bacterial countermeasure. Autophagy 7, 310-314.
45. Ogawa, M., Yoshimori, T., Suzuki, T., Sagara, H., Mizushima, N., and Sasakawa, C. (2005). Escape of intracellular Shigella from autophagy. Science 307, 727-731.
46. Philips, J. A. (2008). Mycobacterial manipulation of vacuolar sorting. Cell. Microbiol. 10, 2408-2415.
47. Pilli, M., Arko-Mensah, J., Ponpuak, M., Roberts, E., Master, S., Mandell, M. A., et al. (2012). Tbk-1 promotes autophagy-mediated antimicrobial defense by controlling autophagosome maturation. Immunity 37, 223-234.
48. Purdy, G. E., and Russell, D. G. (2007). Lysosomal ubiquitin and the demise of Mycobacterium tuberculosis. Cell. Microbiol. 9, 2768-2774.
49. Py, B. F., Lipinski, M. M., and Yuan, J. (2007). Autophagy limits Listeria monocytogenes intracellular growth in the early phase of primary infection. Autophagy 3, 117-125.
50. Romagnoli, A., Etna, M. P., Giacomini, E., Pardini, M., Remoli, M. E., Corazzari, M., et al. (2012). Esx-1 dependent impairment of autophagic flux by Mycobacterium tuberculosis in human dendritic cells. Autophagy 8, 1357-1370.
51. Schnupf, P., and Portnoy, D. A. (2007). Listeriolysin O: a phagosome-specific lysin. Microbes Infect. 9, 1176-1187.
52. Schroeder, N., Mota, L. J., and Meresse, S. (2011). Salmonella-induced tubular networks. Trends Microbiol. 19, 268-277.
53. Shahnazari, S., Yen, W. L., Birmingham, C. L., Shiu, J., Namolovan, A., Zheng, Y. T., et al. (2010). A diacylglycerol-dependent signaling pathway contributes to regulation of antibacterial autophagy. Cell Host Microbe 8, 137-146.
54. Shaid, S., Brandts, C. H., Serve, H., and Dikic, I. (2013). Ubiquitination and selective autophagy. Cell Death Differ. 20, 21-30.
55. Singh, S. B., Davis, A. S., Taylor, G. A., and Deretic, V. (2006). Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 313, 1438-1441.
56. Steinhauser, C., Heigl, U., Tchikov, V., Schwarz, J., Gutsmann, T., Seeger, K., et al. (2013). Lipid-labeling facilitates a novel magnetic isolation procedure to characterize pathogen-containing phagosomes. Traffic 14, 321-336.
57. Swanson, M. S., and Molofsky, A. B. (2005). Autophagy and inflammatory cell death, partners of innate immunity. Autophagy 1, 174-176.
58. Tattoli, I., Sorbara, M. T., Vuckovic, D., Ling, A., Soares, F., Carneiro, L. A., et al. (2012). Amino acid starvation induced by invasive bacterial pathogens triggers an innate host defense program. Cell Host Microbe 11, 563-575.
59. Thurston, T. L., Ryzhakov, G., Bloor, S., von Muhlinen, N., and Randow, F. (2009). The Tbk1 adaptor and autophagy receptor Ndp52 restricts the proliferation of ubiquitin-coated bacteria. Nat. Immunol. 10, 1215-1221.
60. 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.
61. Travassos, L. H., Carneiro, L. A., Ramjeet, M., Hussey, S., Kim, Y. G., Magalhaes, J. G., 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.
62. Tung, S. M., Unal, C., Ley, A., Pena, C., Tunggal, B., Noegel, A. A., et al. (2010). Loss of dictyostelium Atg9 results in a pleiotropic phenotype affecting growth, development, phagocytosis and clearance and replication of Legionella pneumophila. Cell. Microbiol. 12, 765-780.
63. Tweten, R. K. (2005). Cholesterol-dependent cytolysins, a family of versatile pore-forming toxins. Infect. Immun. 73, 6199-6209.
64. 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, 1287-1298.
65. Vazquez-Boland, J. A., Kuhn, M., Berche, P., Chakraborty, T., Dominguez-Bernal, G., Goebel, W., et al. (2001). Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 14, 584-640.
66. 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.
67. Vergne, I., Singh, S., Roberts, E., Kyei, G., Master, S., Harris, J., et al. (2006). Autophagy in immune defense against Mycobacterium tuberculosis. Autophagy 2, 175-178.
68. Virgin, H. W., and Levine, B. (2009). Autophagy genes in immunity. Nat. Immunol. 10, 461-470.
69. von Muhlinen, N., Akutsu, M., Ravenhill, B. J., Foeglein, A., Bloor, S., Rutherford, T. J., et al. (2012). Lc3c, bound selectively by a noncanonical Lir motif in Ndp52, is required for antibacterial autophagy. Mol. Cell. 48, 329-342.
70. 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.
71. Wild, P., Farhan, H., McEwan, D. G., Wagner, S., Rogov, V. V., Brady, N. R., et al. (2011). Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 333, 228-233.
72. Yang, C. S., Song, C. H., Lee, J. S., Jung, S. B., Oh, J. H., Park, J., et al. (2006). Intracellular network of phosphatidylinositol 3-kinase, mammalian target of the rapamycin/70 Kda ribosomal S6 kinase 1, and mitogen-activated protein kinases pathways for regulating mycobacteria-induced Il-23 expression in human macrophages. Cell. Microbiol. 8, 1158-1171.
73. Yano, T., Mita, S., Ohmori, H., Oshima, Y., Fujimoto, Y., Ueda, R., et al. (2008). Autophagic control of Listeria through intracellular innate immune recognition in drosophila. Nat. Immunol. 9, 908-916.
74. Yoshikawa, Y., Ogawa, M., Hain, T., Chakraborty, T., and Sasakawa, C. (2009). Listeria monocytogenes acta is a key player in evading autophagic recognition. Autophagy 5, 1220-1221.
75. Yuk, J. M., and Jo, E. K. (2011). Toll-like receptors and innate immunity. J. Bacteriol. Virol. 41, 225-235.
76. Zhao, Z., Fux, B., Goodwin, M., Dunay, I. R., Strong, D., Miller, B. C., et al. (2008). Autophagosome-independent essential function for the autophagy protein Atg5 in cellular immunity to intracellular pathogens. Cell Host Microbe 4, 458-469.
77. 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.