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Chapter 17 : Intracellular Trafficking of Legionella pneumophila within Phagocytic Cells

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Intracellular Trafficking of Legionella pneumophila within Phagocytic Cells, Page 1 of 2

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Abstract:

A number of bacterial pathogens replicate within macrophages during host infections. Bacteria that establish a novel intracellular route either destroy the nascent phagosomal membrane to gain access to the host cell cytosol or else are targeted to a special membrane-bound compartment that allows exclusion of antimicrobial factors, and presumably access to nutrients. This latter group of pathogens includes , , species, and the eukaryotic parasite . The nascent phagosome formed by the coil has a distinct protein composition, an interesting observation likely to be important for subsequent events during intracellular growth. From a number of studies on the behavior of within phagocytic cells, it is apparent that the phagosome bearing the microorganism is routed within the cell in a fashion distinct from that seen for phagosomes bearing nonpathogens. Protease mutants also appear to have virulences equal to those of wild-type microorganisms, although this result should be interpreted cautiously since partial differences in virulence or histopathology between the mutant and wild type may be difficult to detect in the guinea pig model. At this point, however, it can be said that the protease is dispensable for the intracellular trafficking pathway of . Perhaps , by disrupting the phagosomal membrane, causes a series of similar localized changes, with the result that the microorganism is eventually targeted to its replicative niche.

Citation: Isberg R. 1994. Intracellular Trafficking of Legionella pneumophila within Phagocytic Cells, p 263-278. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch17

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Major Histocompatibility Complex Class I
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References

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1. Abu Kwaik, Y.,, B. I. Eisenstein,, and N. C. Engleberg. 1993. Phenotypic modulation by Legionella pneumophila upon infection of macrophages. Infect. Immun. 61:13201329.
2. Baskerville, A.,, J. W. Conlan,, L. A. Ashworth,, and A. B. Dowsett. 1986. Pulmonary damage caused by a protease from Legionella pneumophila. Br. J. Exp. Pathol. 67:527536.
3. Bellinger-Kawahara, C.,, and M. A. Horwitz. 1990. Complement component C3 fixes selectively to the major outer membrane protein (MOMP) of Legionella pneumophila and mediates phagocytosis of liposome-MOMP complexes by human monocytes. J. Exp. Med. 172:12011210.
4. Berger, K.,, and R. R. Isberg. 1993. Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol. Microbiol. 7:719.
5. Berger, K.,, and R. R. Isberg. Unpublished data.
6. Berger, K. H.,, J. J. Merriam,, and R. R. Isberg. Submitted for publication.
7. Blander, S. J.,, R. F. Breiman,, and M. A. Horwitz. 1989. A live avirulent mutant Legionella pneumophila vaccine induces protective immunity against lethal aerosol challenge. J. Clin. Invest. 83: 810815.
8. Blander, S. J.,, and M. A. Horwitz. 1989. Vaccination with the major secretory protein of Legionella pneumophila induces cell-mediated and protective immunity in a guinea pig model of Legionnaires' disease. J. Exp. Med. 169:691705.
9. Blander, S. J.,, L. Szeto,, H. A. Shuman,, and M. A. Horwitz. 1990. An immunoprotective molecule, the major secretory protein of Legionella pneumophila, is not a virulence factor in a guinea pig model of Legionnaires' disease. J. Clin. Invest. 86:817824.
10. Bole, D. G.,, R. Dowin,, M. Doriaux,, and J. D. Jamieson. 1990. Immunocytochemical localization of BiP to the rough endoplasmic reticulum: evidence for protein sorting by selective retention. J. Biol. Chem. 265:68796883.
11. Cha, Y.,, S. M. Holland,, and J. T. August. 1990. The cDNA sequence of mouse LAMP-2. Evidence for two classes of lysosomal membrane glycoproteins. J. Biol. Chem. 265:50085013.
12. Chavrier, P.,, R. G. Parton,, H. P. Hauri,, K. Simons,, and M. Zerial. 1990. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62:317329.
13. Cianciotto, N. P.,, B. I. Eisenstein,, C. H. Mody,, and N. C. Engleberg. 1990. A mutation in the mip gene results in an attenuation of Legionella pneumophila virulence. J. Infect. Dis. 162:121126.
14. Cianciotto, N. P.,, B. I. Eisenstein,, C. H. Mody,, G. B. Toews,, and N. C. Engleberg. 1989. A Legionella pneumophila gene encoding a species-specific surface protein potentiates initiation of intracellular infection. Infect. Immun. 57:12551262.
15. Clemens, D. L.,, and M. A. Horwltz. 1992. Membrane sorting during phagocytosis: selective exclusion of major histocompatibility complex molecules but not complement receptor CR3 during conventional and coiling phagocytosis. J.Exp. Med. 175:13171326.
16. Davis, G. S.,, W. C. Winn, Jr.,, D. W. Gump,, and H. N. Beaty. 1983. The kinetics of early inflammatory events during experimental pneumonia due to Legionella pneumophila in guinea pigs. J. Infect. Dis. 148:823835.
17. Detilieux, P. G.,, B. L. Deyoe,, and N. F. Cheville. 1990. Penetration and intracellular growth of Brucella abortus in nonphagocytic cells in vitro. Infect. Immun. 58:23202328.
18. Dunn, W. A., Jr. 1990. Studies on the mechanisms of autophagy: formation of the autophagic vacuole. J. Cell Biol. 110:19351945.
19. Dunn, W. A., Jr. 1992. Studies on the mechanisms of autophagy: maturation of the autophagic vacuole. J. Cell. Physiol. 152:458466.
20. Eissenberg, L. G.,, P. B. Wyrick,, C. H. Davis,, and J. W. Rumpp. 1983. Chlamydia psittaci elementary body envelopes: ingestion and inhibition of phagolysosome fusion. Infect. Immun. 40: 741751.
21. Engleberg, N. N.,, C. Carter,, D. R. Weber,, N. P. Cianciotto,, and B. I. Eisenstein. 1989. DNA sequence of mip, a Legionella pneumophila gene associated with macrophage infectivity. Infect. Immun. 57:12631270.
22. Engleberg, N. C.,, E. Pearlman,, D. Dixon,, and B. I. Eisenstein. 1986. Antibodies isolated by using cloned surface antigens recognize antigenically related components of Legionella pneumophila and other Legionella species. J. Immunol. 136:14151417.
23. Engleberg, N. C.,, E. Fearlman,, and B. I. Eisenstein. 1984. Legionella pneumophila surface antigens cloned and expressed in Escherichia coli are translocated to the host cell surface and interact with specific anti-Legionella antibodies. J. Bacteriol. 160:199203.
24. Fallon, R. J.,, and T. J. Rowbotham. 1990. Microbiological investigations into an outbreak of Pontiac fever due to Legionella micdadei associated with use of a whirlpool. J. Clin. Pathol. 43: 479483.
25. Fields, B. S.,, J. M. Barbaree,, E. B. Shorts,, J. C. Feeley,, W. E. Morrill,, G. N. Sanden,, and M. J. Dykstra. 1986. Comparison of guinea pig and protozoan models for determining virulence of Legionella species. Infect. Immun. 53:553559.
26. Fields, B. S.,, S. R. Fields,, J. N. Loy,, E. H. White,, W. L. Steffens,, and E. B. Shotts. 1993. Attachment and entry oí Legionella pneumophila in Hartmannella vermiformis. J. Infect. Dis. 167:11461150.
27. Fields, B. S.,, E. B. Shotts,, J. C. Feeley,, G. W. Gorman,, and W. T. Martin. 1984. Proliferation of Legionella pneumophila as an intracellular parasite of the ciliated protozoan Tetrahymena pyri-formis. Appl. Environ. Microbiol. 47:467471.
28. Finlay, B. B.,, S. Ruschowski,, and S. Dedhar. 1991. Cytoskeletal rearrangements accompanying Salmonella entry into epithelial cells. J. Cell Sci. 99:283296.
29. Fischer, G.,, H. Bang,, B. Ludwig,, K. Mann,, and J. Hacker. 1992. Mip protein of Legionella pneumophila exhibits peptidyl-prolyl-cis/trans isomerase (PPIase) activity. Mol. Microbiol. 6:13751383.
30. Hacker, J.,, and G. Fischer. 1993. Immunophilins: structure-function relationship and possible role in microbial pathogenicity. Mol. Microbiol. 10:445456.
31. Hart, C. A.,, and T. Makin. 1991. Legionella in hospitals: a review. J. Hosp. Infect. Suppl.A:481489.
32. Hoffman, P. S.,, M. Ripley,, and R. Weeratna. 1992. Cloning and nucleotide sequence of a gene (ompS) encoding the major outer membrane protein of Legionella pneumophila. J. Bacteriol. 174: 914920.
33. Horwitz, M. A. 1983. Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J. Exp. Med. 158:13191331.
34. Horwitz, M. A. 1983. The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J. Exp. Med. 158:21082126.
35. Horwitz, M. A. 1984. Phagocytosis of the Legionnaires' disease bacterium (Legionella pneumophila) occurs by a novel mechanism: engulfment within a pseudopod coil. Cell 36:2733.
36. Horwitz, M. A. 1987. Characterization of avirulent mutants of Legionella pneumophila that survive but do not multiply within human monocytes. J. Exp. Med. 166:13101328.
37. Horwitz, M. A.,, and F. R. Maxfield. 1984. Legionella pneumophila inhibits acidification of its phagosome in human monocytes. J. Cell Biol. 99:19361943.
38. Horwitz, M. A.,, and S. C. Silverstein. 1980. Legionnaires' disease bacterium (Legionella pneumophila) multiples intracellularly in human monocytes. J. Clin. Invest. 66:441450.
39. Horwitz, M. A.,, and S. C. Silverstein 1983. Intracellular multiplication of Legionnaires' disease bacteria (Legionella pneumophila) in human monocytes is reversibly inhibited by erythromycin and rifampin. J. Clin. Invest. 71:1526.
40. Hurley, M. C.,, K. Balazovich,, M. Albano,, N. C. Engleberg,, and B. I. Eisenstein,. 1993. Legionella pneumophila Mip inhibits protein kinase C, p. 6970. In J. M. Barbaree,, R. F. Breiman,, and A. P. Dufour (ed.), Legionella: Current Status and Emerging Perspectives. American Society for Microbiology, Washington, D.C..
41. Joiner, K. Personal communication.
42. Joiner, K. A.,, S. A. Fuhrman,, H. M. Miettinen,, L. H. Kasper,, and I. Mellman. 1990. Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science 249:641646.
43. Kishimoto, R. A.,, J. D. White,, F. G. Shirey,, V. G. McGann,, R. F. Berendt,, E. W. Larson,, and K. W. Hedlund. 1981. In vitro responses of guinea pig peritoneal macrophages to Legionella pneumophila. Infect. Immun. 31:12091213.
44. Liu, J.,, J. D. Farmer, Jr.,, W. S. Lane,, J. Friedman,, I. Weissman,, and S. L. Schreiber. 1991. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66:807815.
45. Lukacs, G. L.,, O. D. Rotstein,, and S. Grinstein. 1990. Phagosomal acidification is mediated by a vacuolar-type H( + )-ATPase in murine macrophages. J. Biol. Chem. 265:2109921107.
46. Lundemose, A. G.,, D. A. Rouch,, S. Birkelund,, G. Christiansen,, and J. H. Pearce. 1992. Chlamydia trachomatis Mip-like protein. Mol. Microbiol. 6:25392548.
47. Mahan, M. J.,, J. M. Slauch,, and J. J. Mekalanos. 1993. Selection of bacterial virulence genes that are specifically induced in host tissues. Science 259:686688.
48. Marra, A.,, S. J. Blander,, M. A. Horwitz,, and H. A. Shuman. 1992. Identification of a Legionella pneumophila locus required for intracellular multiplication in human macrophages. Proc. Natl. Acad. Sci. USA 89:96079611.
49. Marra, A.,, M. A. Horwitz,, and H. A. Shuman. 1990. The HL-60 model for the interaction of human macrophages with the Legionnaires' disease bacterium. J. Immunol. 144:27382744.
50. Maurelli, A. T.,, and P. J. Sansonetti. 1988. Genetic determinants of Shigella pathogenicity. Annu. Rev. Microbiol. 42:127150.
51. McCusker, K. T.,, B. A. Braaten,, M. W. Cho,, and D. A. Low. 1991. Legionella pneumophila inhibits protein synthesis in Chinese hamster ovary cells. Infect. Immun. 59:240246.
52. Meyer, R. D. 1983. Legionella infections: a review of five years of research. Rev. Infect. Dis. 5: 258278.
53. Mintz, C. S.,, J. X. Chen,, and H. A. Shuman. 1988. Isolation and characterization of auxotrophic mutants of Legionella pneumophila that fail to multiply in human monocytes. Infect. Immun. 56: 14491455.
54. Mintz, C. S.,, R. D. Miller,, N. S. Gutgsell,, and T. Malek. 1993. Legionella pneumophila protease inactivates interleukin-2 and cleaves CD4 on human T cells. Infect. Immun. 61:34163421.
55. Moffat, J. F.,, and L. S. Tompkins. 1992. A quantitative model of intracellular growth of Legionella pneumophila in Acanthamoeba castellana. Infect. Immun. 60:296301.
56. Nash, T. W.,, D. M. Libby,, and M. A. Horwitz. 1984. Interaction between the Legionnaires' disease bacterium (Legionella pneumophila) and human alveolar macrophages. Influence of antibody, lymphokines, and hydrocortisone. J. Clin. Invest.74:771782.
57. Nguyen, M. H.,, J. E. Stout,, and V. L. Yu. 1991. Legionellosis. Infect. Dis. Clin. North Am. 5: 561584.
58. Oaks, E. V.,, M. E. Wingfield,, and S. B. Formal. 1985. Plaque formation by virulent Shigella flexneri. Infect. Immun. 48:124129.
59. Pace, J.,, M. J. Hayman,, and J. E. Galan. 1993. Signal transduction and invasion of epithelial cells by S. typhimurium. Cell 72:505514.
60. Payne, N. R., and M. A. Horwitz. 1987. Phagocytosis of Legionella pneumophila is mediated by human monocyte complement receptors. J. Exp. Med. 166:13771389.
61. Pearlman, E.,, N. C. Engleberg,, and B. I. Eisenstein. 1985. Identification of protein antigens of Legionella pneumophila serogroup 1. Infect. Immun. 47:7479.
62. Pearlman, E.,, A. H. Jiwa,, N. C. Engleberg,, and B. I. Eisenstein. 1988. Growth of Legionella pneumophila in a human macrophage-like (U937) cell line. Microb. Pathog. 5:8795.
63. Portnoy, D. A.,, P. S. Jacks,, and D. J. Hinrichs. 1988. Role of hemolysin for the intracellular growth of Listeria monocytogenes. J. Exp. Med. 167:14591471.
64. Quinn, F. D.,, M. G. Keen,, and L. S. Tompkins. 1989. Genetic, immunological, and cytotoxic comparisons of Legionella proteolytic activities. Infect. Immun. 57:27192725.
65. Quinn, F. D.,, and L. S. Tompkins. 1989. Analysis of a cloned sequence of Legionella pneumophila encoding a 38 kD metalloprotease possessing haemolytic and cytotoxic activities. Mol. Microbiol. 3:797805.
66. Rabinowitz, S.,, H. Horstmann,, S. Gordon,, and G. Griffiths. 1992. Immunocytochemical characterization of the endocytic and phagolysosomal compartments in peritoneal macrophages. J. Cell Biol. 116:95112.
67. Racoostn, E. L.,, and J. A. Swanson. 1993. Macropinosome maturation and fusion with tubular lysosomes in macrophages. J. Cell Biol. 121:10111020.
68. Rankin, S.,, and R. R. Isberg. 1993. Identification of Legionella pneumophila loci expressed in response to an intracellular environment. Infect. Agents Dis., 2:269271.
69. Rittig, M. G.,, A. Krause,, T. Haupl,, U. E. Schaible,, M. Modolell,, M. D. Kramer,, E. Lutjen-Drecoll,, M. M. Simon,, and G. R. Burmester. 1992. Coiling phagocytosis is the preferential phagocytic mechanism for Borrelia burgdorferi. Infect. Immun. 60:42054212.
70. Rowbotham, T. J. 1983. Isolation of Legionella pneumophila from clinical specimens via amoebae, and the interaction of those and other isolates with amoebae. J. Clin. Pathol. 36:978986.
71. Roy, C.,, and R. Isberg. Unpublished data.
72. Sadosky, A. B.,, L. A. Wiater,, and H. A. Shuman. 1993. Identification of Legionella pneumophila genes required for growth within and killing of human macrophages. Infect. Immun. 61:53615373.
73. Shuman, H. Personal communication.
74. Sibley, L. D.,, E. Weidner,, and J. L. Kraehenbuhl. 1985. Phagosome acidification blocked by intracellular Toxoplasma gondii. Infect. Immun. 49:760764.
75. Skinner, A. R.,, C. M. Anand,, A. Malic,, and J. B. Kurtz. 1983. Acanthamoebae and environmental spread of Legionella pneumophila. Lancet li:289290.
76. Storz, G.,, L. A. Tartaglia,, S. B. Farr,, and B. N. Ames. 1990. Bacterial defenses against oxidative stress. Trends Genet. 6:363368.
77. Sturgill-Koskycki, S.,, P. H. Schlesinger,, P. Chakraborty,, P. Haddix,, H. L. Collins,, S. Gluck,, A. K. Fok,, R. D. Allen,, J. Heuser,, and D. G. Russell. 1994. Mycobacteria resist acidification of their phagosomes by selectively blocking incorporation of the vesicular proton-ATPase. Science 263: 678681.
78. Sun, A. N.,, A. Camilli,, and D. A. Portnoy. 1990. Isolation of Listeria monocytogenes small plaque mutants defective for intracellular growth and cell-to-cell spread. Infect. Immun. 58:37703778.
79. Swanson, J.,, E. Burke,, and S. C. Silverstein. 1987. Tubular lysosomes accompany stimulated pinocytosis in macrophages. J. Cell Biol. 104:12171222.
80. Swanson, M. Unpublished data.
81. Swanson, M.,, and R. Isberg. Unpublished data.
82. Swanson, M. S.,, and R. R. Isberg. 1993. Formation of the Legionella pneumophila replicative phagosome. Infect. Agents Dis. 2:224226.
83. Szeto, L.,, and H. A. Shuman. 1990. The Legionella pneumophila major secretory protein, a protease, is not required for intracellular growth or cell killing. Infect. Immun. 58:25852592.
84. Tartaglia, L. A.,, G. Storz,, and B. N. Ames. 1989. Identification and molecular analysis of oxyR-regulated promoters important for the bacterial adaptation to oxidative stress. J. Mol. Biol. 210: 709719.
85. Wadowsky, R. M.,, L. J. Butter,, M. K. Cook,, S. M. Verma,, M. A. Paul,, B. S. Fields,, G. Keleti,, J. L. Sykora,, and R. B. Yee. 1988. Growth-supporting activity for Legionella pneumophila in tap water cultures and implication of Hartmannella amoebae as growth factors. Appl. Environ. Microbiol. 54:26772682.
86. Williams, A.,, A. Baskerville,, A. B. Dowsett,, and J. W. Conlan. 1987. Immunocytochemical demonstration of the association between Legionella pneumophila, its tissue-destructive protease, and pulmonary lesions in experimental Legionnaires' disease. J. Pathol. 153:257264.
87. Wintermeyer, E.,, U. Rdest,, B. Ludwig,, A. Debes,, and J. Hacker. 1991. Characterization of legiolysin (lly), responsible for haemolytic activity, colour production and fluorescence of Legionella pneumophila. Mol. Microbiol. 5:11351143.
88. Wright, S. D.,, and S. C. Silverstein. 1983. Receptors for C3b and C3bi promote phagocytosis but not the release of toxic oxygen from human phagocytes. J. Exp. Med. 158:20162023.
89. Yamamoto, Y.,, T. W. Klein,, and H. Friedman. 1991. Legionella pneumophila growth in macrophages from susceptible mice is genetically controlled. Proc. Soc. Exp. Biol. Med. 196:405409.
90. Yamamoto, Y.,, T. W. Klein,, C. A. Newton,, and H. Friedman. 1988. Interaction of Legionella pneumophila with peritoneal macrophages from various mouse strains. Adv. Exp. Med. Biol. 239: 8998.
91. Yoshida, S.,, Y. Goto,, Y. Mizuguchi,, K. Nomoto,, and E. Skamene. 1991. Genetic control of natural resistance in mouse macrophages regulating intracellular Legionella pneumophila multiplication in vitro. Infect. Immun. 59:428432.

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