Eating the strangers within: Host control of intracellular bacteria via xenophagy

Cellular Microbiology

Volumn 13, Issue 9, 2011, Pages 1319-1327

  Knodler, Leigh A ^a   Celli, Jean ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY PROTEIN 5; GAMMA INTERFERON; PROTEIN P62; UBIQUITIN;

ADAPTATION; ANTIBACTERIAL ACTIVITY; AUTOPHAGOSOME; AUTOPHAGY; HOST PATHOGEN INTERACTION; HUMAN; INNATE IMMUNITY; INTRACELLULAR BACTERIUM; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SHORT SURVEY; XENOPHAGY;

ANIMALS; AUTOPHAGY; BACTERIA; HUMANS; IMMUNITY, INNATE;

BACTERIA (MICROORGANISMS);

EID: 80051813164     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2011.01632.x     Document Type: Short Survey

References (71)

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 USA 104: 6031-6036.
2. Axe, E.L., Walker, S.A., Manifava, M., Chandra, P., Roderick, H.L., Habermann, A., etal. (2008) Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 182: 685-701.
3. Berger, S.B., Romero, X., Ma, C., Wang, G., Faubion, W.A., Liao, G., etal. (2010) SLAM is a microbial sensor that regulates bacterial phagosome functions in macrophages. Nat Immunol 11: 920-927.
4. Beuzon, C.R., Meresse, S., Unsworth, K.E., Ruiz-Albert, J., Garvis, S., Waterman, S.R., etal. (2000) Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J 19: 3235-3249.
5. Bhardwaj, V., Kanagawa, O., Swanson, P.E., and Unanue, E.R. (1998) Chronic Listeria infection in SCID mice: requirements for the carrier state and the dual role of T cells in transferring protection or suppression. J Immunol 160: 376-384.
6. 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.
7. Birmingham, C.L., Canadien, V., Gouin, E., Troy, E.B., Yoshimori, T., Cossart, P., etal. (2007) Listeria monocytogenes evades killing by autophagy during colonization of host cells. Autophagy 3: 442-451.
8. 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.
9. Butchar, J.P., Cremer, T.J., Clay, C.D., Gavrilin, M.A., Wewers, M.D., Marsh, C.B., etal. (2008) Microarray analysis of human monocytes infected with Francisella tularensis identifies new targets of host response subversion. PLoS ONE 3: e2924.
10. 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: 22-26.
11. Checroun, C., Wehrly, T.D., Fischer, E.R., Hayes, S.F., and Celli, J. (2006) Autophagy-mediated reentry of Francisella tularensis into the endocytic compartment after cytoplasmic replication. Proc Natl Acad Sci USA 103: 14578-14583.
12. Cocchiaro, J.L., and Valdivia, R.H. (2009) New insights into Chlamydia intracellular survival mechanisms. Cell Microbiol 11: 1571-1578.
13. Collins, C.A., De Maziere, A., van Dijk, S., Carlsson, F., Klumperman, J., and Brown, E.J. (2009) Atg5-independent sequestration of ubiquitinated mycobacteria. PLoS Pathog 5: e1000430.
14. Delgado, M.A., Elmaoued, R.A., Davis, A.S., Kyei, G., and Deretic, V. (2008) Toll-like receptors control autophagy. EMBO J 27: 1110-1121.
15. Deretic, V. (2005) Autophagy in innate and adaptive immunity. Trends Immunol 26: 523-528.
16. Deretic, V. (2010) Autophagy in infection. Curr Opin Cell Biol 22: 252-262.
17. Deretic, V., and Levine, B. (2009) Autophagy, immunity, and microbial adaptations. Cell Host Microbe 5: 527-549.
18. Dorn, B.R., Dunn, W.A., Jr, and Progulske-Fox, A. (2001) Porphyromonas gingivalis traffics to autophagosomes in human coronary artery endothelial cells. Infect Immun 69: 5698-5708.
19. Dupont, N., Lacas-Gervais, S., Bertout, J., Paz, I., Freche, B., Van Nhieu, G.T., etal. (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.
20. Flannagan, R.S., Cosio, G., and Grinstein, S. (2009) Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat Rev Microbiol 7: 355-366.
21. Franchi, L., Park, J.H., Shaw, M.H., Marina-Garcia, N., Chen, G., Kim, Y.G., and Nunez, G. (2008) Intracellular NOD-like receptors in innate immunity, infection and disease. Cell Microbiol 10: 1-8.
22. Geisler, S., Holmstrom, K.M., Skujat, D., Fiesel, F.C., Rothfuss, O.C., Kahle, P.J., and Springer, W. (2010) PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 12: 119-131.
23. 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.
24. Gutierrez, M.G., Vazquez, C.L., Munafo, D.B., Zoppino, F.C., Beron, W., Rabinovitch, M., and Colombo, M.I. (2005) Autophagy induction favours the generation and maturation of the Coxiella-replicative vacuoles. Cell Microbiol 7: 981-993.
25. Huang, J., Canadien, V., Lam, G.Y., Steinberg, B.E., Dinauer, M.C., Magalhaes, M.A., etal. (2009) Activation of antibacterial autophagy by NADPH oxidases. Proc Natl Acad Sci USA 106: 6226-6231.
26. Huang, J., Birmingham, C.L., Shahnazari, S., Shiu, J., Zheng, Y.T., Smith, A.C., etal. (2011) Antibacterial autophagy occurs at PI(3)P-enriched domains of the endoplasmic reticulum and requires Rab1 GTPase. Autophagy 7: 17-26.
27. Itakura, E., and Mizushima, N. (2010) Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins. Autophagy 6: 764-776.
28. Kageyama, S., Omori, H., Saitoh, T., Sone, T., Guan, J.L., Akira, S., etal. (2011) The LC3 recruitment mechanism is separate from Atg9L1-dependent membrane formation in the autophagic response against Salmonella. Mol Biol Cell doi 10.1091/mbc.E10-11-0893
29. Kim, P.K., Hailey, D.W., Mullen, R.T., and Lippincott-Schwartz, J. (2008) Ubiquitin signals autophagic degradation of cytosolic proteins and peroxisomes. Proc Natl Acad Sci USA 105: 20567-20574.
30. Kirkin, V., McEwan, D.G., Novak, I., and Dikic, I. (2009a) A role for ubiquitin in selective autophagy. Mol Cell 34: 259-269.
31. Kirkin, V., Lamark, T., Sou, Y.S., Bjorkoy, G., Nunn, J.L., Bruun, J.A., etal. (2009b) A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol Cell 33: 505-516.
32. Knodler, L.A., Vallance, B.A., Celli, J., Winfree, S., Hansen, B., Montero, M., and Steele-Mortimer, O. (2010) Dissemination of invasive Salmonella via bacterial-induced extrusion of mucosal epithelia. Proc Natl Acad Sci USA 107: 17733-17738.
33. Kumar, D., Nath, L., Kamal, M.A., Varshney, A., Jain, A., Singh, S., and Rao, K.V. (2010) Genome-wide analysis of the host intracellular network that regulates survival of Mycobacterium tuberculosis. Cell 140: 731-743.
34. Levine, B. (2005) Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell 120: 159-162.
35. Levine, B., and Kroemer, G. (2008) Autophagy in the pathogenesis of disease. Cell 132: 27-42.
36. Levine, B., Mizushima, N., and Virgin, H.W. (2011) Autophagy in immunity and inflammation. Nature 469: 323-335.
37. Meyer-Morse, N., Robbins, J.R., Rae, C.S., Mochegova, S.N., Swanson, M.S., Zhao, Z., etal. (2010) Listeriolysin O is necessary and sufficient to induce autophagy during Listeria monocytogenes infection. PLoS ONE 5: e8610.
38. Moreau, K., Lacas-Gervais, S., Fujita, N., Sebbane, F., Yoshimori, T., Simonet, M., and Lafont, F. (2010) Autophagosomes can support Yersinia pseudotuberculosis replication in macrophages. Cell Microbiol 12: 1108-1123.
39. Nakagawa, I., Amano, A., Mizushima, N., Yamamoto, A., Yamaguchi, H., Kamimoto, T., etal. (2004) Autophagy defends cells against invading group A Streptococcus. Science 306: 1037-1040.
40. Nishida, Y., Arakawa, S., Fujitani, K., Yamaguchi, H., Mizuta, T., Kanaseki, T., etal. (2009) Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 461: 654-658.
41. Novak, I., Kirkin, V., McEwan, D.G., Zhang, J., Wild, P., Rozenknop, A., etal. (2010) Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep 11: 45-51.
42. Ogawa, M., Yoshimori, T., Suzuki, T., Sagara, H., Mizushima, N., and Sasakawa, C. (2005) Escape of intracellular Shigella from autophagy. Science 307: 727-731.
43. Pankiv, S., Clausen, T.H., Lamark, T., Brech, A., Bruun, J.A., Outzen, H., etal. (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282: 24131-24145.
44. Perrin, A.J., Jiang, X., Birmingham, C.L., So, N.S., and Brumell, J.H. (2004) Recognition of bacteria in the cytosol of mammalian cells by the ubiquitin system. Curr Biol 14: 806-811.
45. Pizarro-Cerda, J., Meresse, S., Parton, R.G., van der Goot, G., Sola-Landa, A., Lopez-Goni, I., etal. (1998a) Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect Immun 66: 5711-5724.
46. Pizarro-Cerda, J., Moreno, E., Sanguedolce, V., Mege, J.L., and Gorvel, J.P. (1998b) Virulent Brucella abortus prevents lysosome fusion and is distributed within autophagosome-like compartments. Infect Immun 66: 2387-2392.
47. Polson, H.E., de Lartigue, J., Rigden, D.J., Reedijk, M., Urbe, S., Clague, M.J., and Tooze, S.A. (2010) Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy 6: 506-522.
48. Ponpuak, M., Davis, A.S., Roberts, E.A., Delgado, M.A., Dinkins, C., Zhao, Z., etal. (2010) Delivery of cytosolic components by autophagic adaptor protein p62 endows autophagosomes with unique antimicrobial properties. Immunity 32: 329-341.
49. Pujol, C., Klein, K.A., Romanov, G.A., Palmer, L.E., Cirota, C., Zhao, Z., and Bliska, J.B. (2009) Yersinia pestis can reside in autophagosomes and avoid xenophagy in murine macrophages by preventing vacuole acidification. Infect Immun 77: 2251-2261.
50. Qin, Q.M., Pei, J., Ancona, V., Shaw, B.D., Ficht, T.A., and de Figueiredo, P. (2008) RNAi screen of endoplasmic reticulum-associated host factors reveals a role for IRE1alpha in supporting Brucella replication. PLoS Pathog 4: e1000110.
51. Radtke, A.L., Delbridge, L.M., Balachandran, S., Barber, G.N., and O'Riordan, M.X. (2007) TBK1 protects vacuolar integrity during intracellular bacterial infection. PLoS Pathog 3: e29.
52. Randow, F. (2011) How cells deploy ubiquitin and autophagy to defend their cytosol from bacterial invasion. Autophagy 7: 304-309.
53. Rich, K.A., Burkett, C., and Webster, P. (2003) Cytoplasmic bacteria can be targets for autophagy. Cell Microbiol 5: 455-468.
54. Romano, P.S., Gutierrez, M.G., Beron, W., Rabinovitch, M., and Colombo, M.I. (2007) The autophagic pathway is actively modulated by phase II Coxiella burnetii to efficiently replicate in the host cell. Cell Microbiol 9: 891-909.
55. Roy, D., Liston, D.R., Idone, V.J., Di, A., Nelson, D.J., Pujol, C., etal. (2004) A process for controlling intracellular bacterial infections induced by membrane injury. Science 304: 1515-1518.
56. Roy, C.R., Salcedo, S.P., and Gorvel, J.P. (2006) Pathogen-endoplasmic-reticulum interactions: in through the out door. Nat Rev Immunol 6: 136-147.
57. Sanjuan, M.A., Dillon, C.P., Tait, S.W., Moshiach, S., Dorsey, F., Connell, S., etal. (2007) Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450: 1253-1257.
58. Shahnazari, S., Yen, W.L., Birmingham, C.L., Shiu, J., Namolovan, A., Zheng, Y.T., etal. (2010) A diacylglycerol-dependent signaling pathway contributes to regulation of antibacterial autophagy. Cell Host Microbe 8: 137-146.
59. Shin, D.M., Jeon, B.Y., Lee, H.M., Jin, H.S., Yuk, J.M., Song, C.H., etal. (2010) Mycobacterium tuberculosis eis regulates autophagy, inflammation, and cell death through redox-dependent signaling. PLoS Pathog 6: e1001230.
60. 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.
61. Steele-Mortimer, O. (2008) The Salmonella-containing vacuole: moving with the times. Curr Opin Microbiol 11: 38-45.
62. Swanson, M.S., and Isberg, R.R. (1995) Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect Immun 63: 3609-3620.
63. 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.
64. Travassos, L.H., Carneiro, L.A., Ramjeet, M., Hussey, S., Kim, Y.G., Magalhaes, J.G., etal. (2010) Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry. Nat Immunol 11: 55-62.
65. Virgin, H.W., and Levine, B. (2009) Autophagy genes in immunity. Nat Immunol 10: 461-470.
66. Xu, Y., Jagannath, C., Liu, X.D., Sharafkhaneh, A., Kolodziejska, K.E., and Eissa, N.T. (2007) Toll-like receptor 4 is a sensor for autophagy associated with innate immunity. Immunity 27: 135-144.
67. Yamaguchi, H., Nakagawa, I., Yamamoto, A., Amano, A., Noda, T., and Yoshimori, T. (2009) An initial step of GAS-containing autophagosome-like vacuoles formation requires Rab7. PLoS Pathog 5: e1000670.
68. Yano, T., Mita, S., Ohmori, H., Oshima, Y., Fujimoto, Y., Ueda, R., etal. (2008) Autophagic control of Listeria through intracellular innate immune recognition in drosophila. Nat Immunol 9: 908-916.
69. Yoshikawa, Y., Ogawa, M., Hain, T., Yoshida, M., Fukumatsu, M., Kim, M., etal. (2009) Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat Cell Biol 11: 1233-1240.
70. Zhao, Z., Fux, B., Goodwin, M., Dunay, I.R., Strong, D., Miller, B.C., etal. (2008) Autophagosome-independent essential function for the autophagy protein Atg5 in cellular immunity to intracellular pathogens. Cell Host Microbe 4: 458-469.
71. 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.