Yersinia pestis can reside in autophagosomes and avoid xenophagy in murine macrophages by preventing vacuole acidification

Infection and Immunity

Volumn 77, Issue 6, 2009, Pages 2251-2261

  Pujol, Céline ^a,c   Klein, Kathryn A ^a   Romanov, Galina A ^a   Palmer, Lance E ^a,d   Cirota, Carol ^a   Zhao, Zijiang ^b   Bliska, James B ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UR1282   (France)

^d SIEMENS CORPORATE RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; BIOLOGICAL MARKER;

ACIDIFICATION; ARTICLE; AUTOPHAGY; BACTERIAL COUNT; BACTERIAL SURVIVAL; CELL VACUOLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; FLUORESCENCE MICROSCOPY; GENE DELETION; IMMUNOBLOTTING; LYSOSOME; MACROPHAGE; MACROPHAGE ACTIVATION; NONHUMAN; PH; PHAGOSOME; PRIORITY JOURNAL; YERSINIA PESTIS; ANIMAL; C57BL MOUSE; CHEMISTRY; IMMUNOLOGY; MICROBIAL VIABILITY; MICROBIOLOGY; MOUSE; PHYSIOLOGY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANIMALS; BIOLOGICAL MARKERS; COLONY COUNT, MICROBIAL; HYDROGEN-ION CONCENTRATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MICROBIAL VIABILITY; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; PHAGOSOMES; YERSINIA PESTIS;

EID: 66549126665     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00068-09     Document Type: Article

References (53)

1. Achtman, M., G. Morelli, P. Zhu, T. Wirth, I. Diehl, B. Kusecek, A. J. Vogler, D. M. Wagner, C. J. Allender, W. R. Easterday, V. Chenal-Francisque, P. Worsham, N. R. Thomson, J. Parkhill, L. E. Lindler, E. Carniel, and P. Keim. 2004. Microevolution and history of the plague bacillus, Yersinia pestis. Proc. Natl. Acad. Sci. USA 101:17837-17842.
2. Alexeyev, M. F. 1995. Three kanamycin resistance gene cassettes with different polylinkers. BioTechniques 18:52, 54, 56.
3. Amano, A., I. Nakagawa, and T. Yoshimori. 2006. Autophagy in innate immunity against intracellular bacteria. J. Biochem. 140:161-166. (Pubitemid 44618901)
4. Birmingham, C. L., V. Canadien, N. A. Kaniuk, B. E. Steinberg, D. E. Higgins, and J. H. Brumell. 2008. Listeriolysin O allows Listeria monocytogenes replication in macrophage vacuoles. Nature 451:350-354.
5. Cavanaugh, D. C., and R. Randall. 1959. The role of multiplication of Pasteurella pestis in mononuclear phagocytes in the pathogenesis of fleaborne plague. J. Immunol. 85:348-363.
6. Charnetzky, W. T., and W. W. Shuford. 1985. Survival and growth of Yersinia pestis within macrophages and an effect of the loss of the 47-megadalton plasmid on growth in macrophages. Infect. Immun. 47:234-241.
7. Checroun, C., T. D. Wehrly, E. R. Fischer, S. F. Hayes, and J. Celli. 2006. Autophagy-mediated reentry of Francisella tularensis into the endocytic compartment after cytoplasmic replication. Proc. Natl. Acad. Sci. USA 103:14578-14583.
8. Du, Y., R. Rosqvist, and A. Forsberg. 2002. Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect. Immun. 70:1453-1460.
9. Duclos, S., and M. Desjardins. 2000. Subversion of a young phagosome: the survival strategies of intracellular pathogens. Cell. Microbiol. 2:365-377.
10. Ernst, R. K., T. Guina, and S. I. Miller. 1999. How intracellular bacteria survive: surface modifications that promote resistance to host innate immune responses. J. Infect. Dis. 179:S326-S330.
11. Finegold, M. J. 1969. Pneumonic plague in monkeys. An electron microscopic study. Am. J. Pathol. 54:167-185.
12. Gong, S., S. W. Bearden, V. A. Geoffroy, J. D. Fetherston, and R. D. Perry. 2001. Characterization of the Yersinia pestis Yfu ABC inorganic iron transport system. Infect. Immun. 69:2829-2837.
13. Grabenstein, J. P., H. S. Fukuto, L. E. Palmer, and J. B. Bliska. 2006. Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infect. Immun. 74:3727-3741.
14. Grabenstein, J. P., M. Marceau, C. Pujol, M. Simonet, and J. B. Bliska. 2004. The response regulator PhoP of Yersinia pseudotuberculosis is important for replication in macrophages and for virulence. Infect. Immun. 72:4973-4984.
15. Groisman, E. A. 2001. The pleiotropic two-component regulatory system PhoP-PhoQ. J. Bacteriol. 183:1835-1842. (Pubitemid 32225978)
16. Hernandez, L. D., M. Pypaert, R. A. Flavell, and J. E. Galan. 2003. A Salmonella protein causes macrophage cell death by inducing autophagy. J. Cell Biol. 163:1123-1131.
17. Huynh, K. K., and S. Grinstein. 2007. Regulation of vacuolar pH and its modulation by some microbial species. Microbiol. Mol. Biol. Rev. 71:452-462.
18. Janssen, W. A., and M. J. Surgalla. 1969. Plague bacillus: survival within host phagocytes. Science 163:950-952.
19. Klionsky, D. J., H. Abeliovich, P. Agostinis, D. K. Agrawal, G. Aliev, D. S. Askew, M. Baba, E. H. Baehrecke, B. A. Bahr, A. Ballabio, B. A. Bamber, D. C. Bassham, E. Bergamini, X. Bi, M. Biard-Piechaczyk, J. S. Blum, D. E. Bredesen, J. L. Brodsky, J. H. Brumell, U. T. Brunk, W. Bursch, N. Camougrand, E. Cebollero, F. Cecconi, Y. Chen, L. S. Chin, A. Choi, C. T. Chu, J. Chung, P. G. Clarke, R. S. Clark, S. G. Clarke, C. Clave, J. L. Cleveland, P. Codogno, M. I. Colombo, A. Coto-Montes, J. M. Cregg, A. M. Cuervo, J. Debnath, F. Demarchi, P. B. Dennis, P. A. Dennis, V. Deretic, R. J. Devenish, F. Di Sano, J. F. Dice, M. Difiglia, S. Dinesh-Kumar, C. W. Distelhorst, M. Djavaheri-Mergny, F. C. Dorsey, W. Droge, M. Dron, W. A. Dunn, Jr., M. Duszenko, N. T. Eissa, Z. Elazar, A. Esclatine, E. L. Eskelinen, L. Fesus, K. D. Finley, J. M. Fuentes, J. Fueyo, K. Fujisaki, B. Galliot, F. B. Gao, D. A. Gewirtz, S. B. Gibson, A. Gohla, A. L. Goldberg, R. Gonzalez, C. Gonzalez-Estevez, S. Gorski, R. A. Gottlieb, D. Haussinger, Y. W. He, K. Heidenreich, J. A. Hill, M. Hoyer-Hansen, X. Hu, W. P. Huang, A. Iwasaki, M. Jaattela, W. T. Jackson, X. Jiang, S. Jin, T. Johansen, J. U. Jung, M. Kadowaki, C. Kang, A. Kelekar, D. H. Kessel, J. A. Kiel, H. P. Kim, A. Kimchi, T. J. Kinsella, K. Kiselyov, K. Kitamoto, E. Knecht, M. Komatsu, E. Kominami, S. Kondo, A. L. Kovacs, G. Kroemer, C. Y. Kuan, R. Kumar, M. Kundu, J. Landry, M. Laporte, W. Le, H. Y. Lei, M. J. Lenardo, B. Levine, A. Lieberman, K. L. Lim, F. C. Lin, W. Liou, L. F. Liu, G. Lopez-Berestein, C. Lopez-Otin, B. Lu, K. F. Macleod, W. Malorni, W. Martinet, K. Matsuoka, J. Mautner, A. J. Meijer, A. Melendez, P. Michels, G. Miotto, W. P. Mistiaen, N. Mizushima, B. Mograbi, I. Monastyrska, M. N. Moore, P. I. Moreira, Y. Moriyasu, T. Motyl, C. Munz, L. O. Murphy, N. I. Naqvi, T. P. Neufeld, I. Nishino, R. A. Nixon, T. Noda, B. Nurnberg, M. Ogawa, N. L. Oleinick, L. J. Olsen, B. Ozpolat, S. Paglin, G. E. Palmer, I. Papassideri, M. Parkes, D. H. Perlmutter, G. Perry, M. Piacentini, R. Pinkas-Kramarski, M. Prescott, T. Proikas-Cezanne, N. Raben, A. Rami, F. Reggiori, B. Rohrer, D. C. Rubinsztein, K. M. Ryan, J. Sadoshima, H. Sakagami, Y. Sakai, M. Sandri, C. Sasakawa, M. Sass, C. Schneider, P. O. Seglen, O. Seleverstov, J. Settleman, J. J. Shacka, I. M. Shapiro, A. Sibirny, E. C. Silva-Zacarin, H. U. Simon, C. Simone, A. Simonsen, M. A. Smith, K. Spanel-Borowski, V. Srinivas, M. Steeves, H. Stenmark, P. E. Stromhaug, C. S. Subauste, S. Sugimoto, D. Sulzer, T. Suzuki, M. S. Swanson, I. Tabas, F. Takeshita, N. J. Talbot, Z. Talloczy, K. Tanaka, I. Tanida, G. S. Taylor, J. P. Taylor, A. Terman, G. Tettamanti, C. B. Thompson, M. Thumm, A. M. Tolkovsky, S. A. Tooze, R. Truant, L. V. Tumanovska, Y. Uchiyama, T. Ueno, N. L. Uzcategui, I. van der Klei, E. C. Vaquero, T. Vellai, M. W. Vogel, H. G. Wang, P. Webster, J. W. Wiley, Z. Xi, G. Xiao, J. Yahalom, J. M. Yang, G. Yap, X. M. Yin, T. Yoshimori, L. Yu, Z. Yue, M. Yuzaki, O. Zabirnyk, X. Zheng, X. Zhu, and R. L. Deter. 2008. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4:151-175.
20. Lathem, W. W., S. D. Crosby, V. L. Miller, and W. E. Goldman. 2005. Progression of primary pneumonic plague: a mouse model of infection, pathology, and bacterial transcriptional activity. Proc. Natl. Acad. Sci. USA 102:17786-17791.
21. Levine, B., and V. Deretic. 2007. Unveiling the roles of autophagy in innate and adaptive immunity. Nat. Rev. Immunol. 7:767-777.
22. Lilo, S., Y. Zheng, and J. B. Bliska. 2008. Caspase-1 activation in macrophages infected with Yersinia pestis KIM requires the type III secretion system effector YopJ. Infect. Immun. 76:3911-3923.
23. Lukaszewski, R. A., D. J. Kenny, R. Taylor, D. G. Rees, M. G. Hartley, and P. C. Oyston. 2005. Pathogenesis of Yersinia pestis infection in BALB/c mice: effects on host macrophages and neutrophils. Infect. Immun. 73:7142-7150.
24. Meresse, S., O. Steele-Mortimer, E. Moreno, M. Desjardins, B. Finlay, and J. P. Gorvel. 1999. Controlling the maturation of pathogen-containing vacuoles: a matter of life and death. Nat. Cell Biol. 1:E183-E188.
25. Meyer, K. F. 1950. Immunity in plague; a critical consideration of some recent studies. J. Immunol. 64:139-163.
26. Mizushima, N., B. Levine, A. M. Cuervo, and D. J. Klionsky. 2008. Autophagy fights disease through cellular self-digestion. Nature 451:1069-1075.
27. Mizushima, N., and T. Yoshimori. 2007. How to interpret LC3 immunoblotting. Autophagy 3:542-545. (Pubitemid 350060049)
28. Morales, V. M., A. Bäckman, and M. Bugdasarian. 1991. A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants. Gene 97:39-47.
29. Ogawa, M., and C. Sasakawa. 2006. Bacterial evasion of the autophagic defense system. Curr. Opin. Microbiol. 9:62-68.
30. Oyston, P. C. F., N. Dorrell, K. Williams, S.-R. Li, M. Green, R. W. Titball, and B. Wren. 2000. The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect. Immun. 68:3419-3425. (Pubitemid 30340439)
31. Palmer, L. E., S. Hobbie, J. E. Galan, and J. B. Bliska. 1998. YopJ of Yersinia pseudotuberculosis is required for the inhibition of macrophage TNFα production and the downregulation of the MAP kinases p38 and JNK. Mol. Microbiol. 27:953-965.
32. Pear, W. S., A. M. Scott, and G. P. Nolan (ed.). 1997. Generation of high titer, helper-free retroviruses by transient transfection. Humana Press, Totowa, NJ.
33. Perry, R. D., and J. D. Fetherston. 1997. Yersinia pestis - etiologic agent of plague. Clin. Microbiol. Rev. 10:35-66.
34. Perry, R. D., M. L. Pendrak, and P. Schuetze. 1990. Identification and cloning of a hemin storage locus involved in the pigmentation phenotype of Yersinia pestis. J. Bacteriol. 172:5929-5937. (Pubitemid 20317134)
35. Prentice, M. B., and L. Rahalison. 2007 Plague. Lancet 369:1196-1207.
36. Pujol, C., and J. B. Bliska. 2003. The ability to replicate in macrophages is conserved between Yersinia pestis and Yersinia pseudotuberculosis. Infect. Immun. 71:5892-5899.
37. Pujol, C., J. P. Grabenstein, R. D. Perry, and J. B. Bliska. 2005. Replication of Yersinia pestis in interferon gamma-activated macrophages requires ripA, a gene encoded in the pigmentation locus. Proc. Natl. Acad. Sci. USA 102:12909-12914.
38. Rohde, K., R. M. Yates, G. E. Purdy, and D. G. Russell. 2007. Mycobacterium tuberculosis and the environment within the phagosome. Immunol. Rev. 219:37-54.
39. Sato, S. B., and S. Toyama. 1994. Interference with the endosomal acidification by a monoclonal antibody directed toward the 116 (100)-kD subunit of the vacuolar type proton pump. J. Cell Biol. 127:39-53.
40. Sebbane, F., D. Gardner, D. Long, B. B. Gowen, and B. J. Hinnebusch. 2005. Kinetics of disease progression and host response in a rat model of bubonic plague. Am. J. Pathol. 166:1427-1439.
41. Shaner, N. C., R. E. Campbell, P. A. Steinbach, B. N. Giepmans, A. E. Palmer, and R. Y. Tsien. 2004. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22:1567-1572.
42. Shenoy, A. R., B. H. Kim, H. P. Choi, T. Matsuzawa, S. Tiwari, and J. D. MacMicking. 2007. Emerging themes in IFN-gamma-induced macrophage immunity by the p47 and p65 GTPase families. Immunobiology 212:771-784. (Pubitemid 350246255)
43. Simonet, M., and S. Falkow. 1992. Invasin expression in Yersinia pseudotuberculosis. Infect. Immun. 60:4414-4417.
44. Steinberg, T. H., and J. A. Swanson. 1994. Measurement of phagosomelysosome fusion and phagosomal pH. Methods Enzymol. 236:147-160.
45. Straley, S. C., and P. A. Harmon. 1984. Growth in mouse peritoneal macrophages of Yersinia pestis lacking established virulence determinants. Infect. Immun. 45:649-654.
46. Straley, S. C., and P. A. Harmon. 1984. Yersinia pestis grows within phagolysosomes in mouse peritoneal macrophages. Infect. Immun. 45:655-659.
47. +-ATPase activity. Microb. Pathog. 27:253-263.
48. Vergne, I., J. Chua, S. B. Singh, and V. Deretic. 2004. Cell biology of Mycobacterium tuberculosis phagosome. Annu. Rev. Cell Dev. Biol. 20:367-394.
49. Viboud, G. I., and J. B. Bliska. 2005. Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu. Rev. Microbiol. 59:69-89.
50. Vieira, O. V., R. J. Botelho, and S. Grinstein. 2002. Phagosome maturation: aging gracefully. Biochem. J. 366:689-704.
51. Welkos, S., M. L. M. Pitt, M. Martinez, A. Friedlander, P. Vogel, and R. Tammariello. 2002. Determination of the virulence of the pigmentation-deficient and pigmentation-/plasminogen activator-deficient strains of Yersinia pestis in non-human primate and mouse models of pneumonic plague. Vaccine 20:2206-2214.
52. Welkos, S. L., A. M. Friedlander, and K. J. Davis. 1997. Studies on the role of plasminogen activator in systemic infection by virulent Yersinia pestis strain C092. Microb. Pathog. 23:211-223.
53. Zhao, Z., L. B. Thackray, B. C. Miller, T. M. Lynn, M. M. Becker, E. Ward, N. N. Mizushima, M. R. Denison, and H. W. T. Virgin. 2007. Coronavirus replication does not require the autophagy gene ATG5. Autophagy 3:581-585. (Pubitemid 350060054)