The Francisella O-antigen mediates survival in the macrophage cytosol via autophagy avoidance

Cellular Microbiology

Volumn 16, Issue 6, 2014, Pages 862-877

  Case, Elizabeth Di Russo ^a,c   Chong, Audrey ^a   Wehrly, Tara D ^a   Hansen, Bryan ^a   Child, Robert ^a   Hwang, Seungmin ^b,d   Virgin, Herbert W ^b   Celli, Jean ^a,e  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

^e WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; O ANTIGEN; TRANSPOSON;

ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; AUTOPHAGY; BACTERIAL GENE; BACTERIAL VIABILITY; BACTERIUM IDENTIFICATION; BACTERIUM MUTANT; CELL VACUOLE; CONTROLLED STUDY; CYTOSOL; DELETION MUTANT; FRANCISELLA; GENE LOCUS; MACROPHAGE; MANC GENE; MOLECULAR CLONING; MOLECULAR LIBRARY; MOUSE; NONHUMAN; PARASITE SURVIVAL; PHAGOSOME; PRIORITY JOURNAL; SCREENING; WILD TYPE; ANIMAL; C57BL MOUSE; CELL CULTURE; FRANCISELLA TULARENSIS; GENE EXPRESSION REGULATION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; PHYSIOLOGY; TRANSPOSON;

BACTERIA (MICROORGANISMS); FRANCISELLA; FRANCISELLA TULARENSIS; LISTERIA; MURINAE; SHIGELLA;

ANIMALS; AUTOPHAGY; CELLS, CULTURED; CYTOSOL; DNA TRANSPOSABLE ELEMENTS; FRANCISELLA TULARENSIS; HOST-PATHOGEN INTERACTIONS; MACROPHAGES; MICE, INBRED C57BL; MICROBIAL VIABILITY; MUTAGENESIS, INSERTIONAL; O ANTIGENS;

EID: 84898731112     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12246     Document Type: Article

References (37)

1. Apicella, M.A., Post, D.M., Fowler, A.C., Jones, B.D., Rasmussen, J.A., Hunt, J.R., etal. (2010) Identification, characterization and immunogenicity of an O-antigen capsular polysaccharide of Francisella tularensis. PLoS ONE 5: e11060.
2. 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.
3. Chong, A., Wehrly, T.D., Nair, V., Fischer, E.R., Barker, J.R., Klose, K.E., and Celli, J. (2008) The early phagosomal stage of Francisella tularensis determines optimal phagosomal escape and Francisella pathogenicity island protein expression. Infect Immun 76: 5488-5499.
4. Chong, A., Wehrly, T.D., Child, R., Hansen, B., Hwang, S., Virgin, H.W., and Celli, J. (2012) Cytosolic clearance of replication-deficient mutants reveals Francisella tularensis interactions with the autophagic pathway. Autophagy 8: 1342-1356.
5. Clemens, D.L., Lee, B.Y., and Horwitz, M.A. (2004) Virulent and avirulent strains of Francisella tularensis prevent acidification and maturation of their phagosomes and escape into the cytoplasm in human macrophages. Infect Immun 72: 3204-3217.
6. Clemens, D.L., Lee, B.Y., and Horwitz, M.A. (2012) O-antigen-deficient Francisella tularensis Live Vaccine Strain mutants are ingested via an aberrant form of looping phagocytosis and show altered kinetics of intracellular trafficking in human macrophages. Infect Immun 80: 952-967.
7. Dortet, L., Mostowy, S., Samba-Louaka, A., Gouin, E., Nahori, M.A., Wiemer, E.A., etal. (2011) Recruitment of the major vault protein by InlK: a Listeria monocytogenes strategy to avoid autophagy. PLoS Pathog 7: e1002168.
8. Gal, J., Strom, A.L., Kwinter, D.M., Kilty, R., Zhang, J., Shi, P., etal. (2009) Sequestosome 1/p62 links familial ALS mutant SOD1 to LC3 via an ubiquitin-independent mechanism. J Neurochem 111: 1062-1073.
9. Gunn, J.S., and Ernst, R.K. (2007) The structure and function of Francisella lipopolysaccharide. Ann N Y Acad Sci 1105: 202-218.
10. Hajjar, A.M., Harvey, M.D., Shaffer, S.A., Goodlett, D.R., Sjostedt, A., Edebro, H., etal. (2006) Lack of in vitro and in vivo recognition of Francisella tularensis subspecies lipopolysaccharide by Toll-like receptors. Infect Immun 74: 6730-6738.
11. Huett, A., Heath, R.J., Begun, J., Sassi, S.O., Baxt, L.A., Vyas, J.M., etal. (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.
12. Kampen, H., Rotzel, D.C., Kurtenbach, K., Maier, W.A., and Seitz, H.M. (2004) Substantial rise in the prevalence of Lyme borreliosis spirochetes in a region of western Germany over a 10-year period. Appl Environ Microbiol 70: 1576-1582.
13. Kraft, C., Peter, M., and Hofmann, K. (2010) Selective autophagy: ubiquitin-mediated recognition and beyond. Nat Cell Biol 12: 836-841.
14. Lai, X.H., Shirley, R.L., Crosa, L., Kanistanon, D., Tempel, R., Ernst, R.K., etal. (2010) Mutations of Francisella novicida that alter the mechanism of its phagocytosis by murine macrophages. PLoS ONE 5: e11857.
15. Larsson, P., Oyston, P.C.F., Chain, P., Chu, M.C., Duffield, M., Fuxelius, H.H., etal. (2005) The complete genome sequence of Francisella tularensis, the causative agent of tularemia. Nat Genet 37: 153-159.
16. Lindemann, S.R., Peng, K., Long, M.E., Hunt, J.R., Apicella, M.A., Monack, D.M., etal. (2011) Francisella tularensis Schu S4 O-antigen and capsule biosynthesis gene mutants induce early cell death in human macrophages. Infect Immun 79: 581-594.
17. Maier, T.M., Havig, A., Casey, M., Nano, F.E., Frank, D.W., and Zahrt, T.C. (2004) Construction and characterization of a highly efficient Francisella shuttle plasmid. Appl Environ Microbiol 70: 7511-7519.
18. Maier, T.M., Pechous, R., Casey, M., Zahrt, T.C., and Frank, D.W. (2006) In vivo Himar1-based transposon mutagenesis of Francisella tularensis. Appl Environ Microbiol 72: 1878-1885.
19. Maier, T.M., Casey, M.S., Becker, R.H., Dorsey, C.W., Glass, E.M., Maltsev, N., etal. (2007) Identification of Francisella tularensis Himar1-based transposon mutants defective for replication in macrophages. Infect Immun 75: 5376-5389.
20. von Muhlinen, N., Thurston, T., Ryzhakov, G., Bloor, S., and Randow, F. (2010) NDP52, a novel autophagy receptor for ubiquitin-decorated cytosolic bacteria. Autophagy 6: 288-289.
21. Nakayasu, E.S., Tempel, R., Cambronne, X.A., Petyuk, V.A., Jones, M.B., Gritsenko, M.A., etal. (2013) Comparative phosphoproteomics reveals components of host cell invasion and post-transcriptional regulation during Francisella infection. Mol Cell Proteomics 12: 3297-3309.
22. Ogawa, M., Yoshimori, T., Suzuki, T., Sagara, H., Mizushima, N., and Sasakawa, C. (2005) Escape of intracellular Shigella from autophagy. Science 307: 727-731.
23. Overell, R.W., Weisser, K.E., and Cosman, D. (1988) Stably transmitted triple-promoter retroviral vectors and their use in transformation of primary mammalian cells. Mol Cell Biol 8: 1803-1808.
24. 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.
25. Peng, K., Broz, P., Jones, J., Joubert, L.M., and Monack, D. (2011) Elevated AIM2-mediated pyroptosis triggered by hypercytotoxic Francisella mutant strains is attributed to increased intracellular bacteriolysis. Cell Microbiol 13: 1586-1600.
26. Phillips, N.J., Schilling, B., McLendon, M.K., Apicella, M.A., and Gibson, B.W. (2004) Novel modification of lipid A of Francisella tularensis. Infect Immun 72: 5340-5348.
27. Prior, J.L., Prior, R.G., Hitchen, P.G., Diaper, H., Griffin, K.F., Morris, H.R., etal. (2003) Characterization of the O antigen gene cluster and structural analysis of the O antigen of Francisella tularensis subsp. tularensis. J Med Microbiol 52: 845-851.
28. Raynaud, C., Meibom, K.L., Lety, M.A., Dubail, I., Candela, T., Frapy, E., and Charbit, A. (2007) Role of the wbt locus of Francisella tularensis in lipopolysaccharide O-antigen biogenesis and pathogenicity. Infect Immun 75: 536-541.
29. Sorokin, V.M., Pavlovich, N.V., and Prozorova, L.A. (1996) Francisella tularensis resistance to bactericidal action of normal human serum. FEMS Immunol Med Microbiol 13: 249-252.
30. Steele, S., Brunton, J., Ziehr, B., Taft-Benz, S., Moorman, N., and Kawula, T. (2013) Francisella tularensis harvests nutrients derived via ATG5-independent autophagy to support intracellular growth. PLoS Pathog 8: e1003562.
31. Wang, X., Ribeiro, A.A., Guan, Z., McGrath, S.C., Cotter, R.J., and Raetz, C.R. (2006) Structure and biosynthesis of free lipid A molecules that replace lipopolysaccharide in Francisella tularensis subsp. novicida. Biochemistry 45: 14427-14440.
32. Wehrly, T.D., Chong, A., Virtaneva, K., Sturdevant, D.E., Child, R., Edwards, J.A., etal. (2009) Intracellular biology and virulence determinants of Francisella tularensis revealed by transcriptional profiling inside macrophages. Cell Microbiol 11: 1128-1150.
33. Yang, Z., and Klionsky, D.J. (2010) Eaten alive: a history of macroautophagy. Nat Cell Biol 12: 814-822.
34. 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.
35. Zhao, Z., Thackray, L.B., Miller, B.C., Lynn, T.M., Becker, M.M., Ward, E., etal. (2007) Coronavirus replication does not require the autophagy gene ATG5. Autophagy 3: 581-585.
36. 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.
37. 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.