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Chapter 17 : Intracellular Trafficking of Legionella pneumophila within Phagocytic Cells

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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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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: 1320 1329.
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: 527 536.
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: 1201 1210.
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: 7 19.
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: 810 815.
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: 691 705.
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: 817 824.
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: 6879 6883.
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: 5008 5013.
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: 317 329.
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: 121 126.
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: 1255 1262.
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: 1317 1326.
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: 823 835.
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: 2320 2328.
18. Dunn, W. A., Jr. 1990. Studies on the mechanisms of autophagy: formation of the autophagic vacuole. J. Cell Biol. 110: 1935 1945.
19. Dunn, W. A., Jr. 1992. Studies on the mechanisms of autophagy: maturation of the autophagic vacuole. J. Cell. Physiol. 152: 458 466.
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: 741 751.
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: 1263 1270.
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: 1415 1417.
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: 199 203.
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: 479 483.
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: 553 559.
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: 1146 1150.
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: 467 471.
28. Finlay, B. B.,, S. Ruschowski,, and S. Dedhar. 1991. Cytoskeletal rearrangements accompanying Salmonella entry into epithelial cells. J. Cell Sci. 99: 283 296.
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: 1375 1383.
30. Hacker, J.,, and G. Fischer. 1993. Immunophilins: structure-function relationship and possible role in microbial pathogenicity. Mol. Microbiol. 10: 445 456.
31. Hart, C. A.,, and T. Makin. 1991. Legionella in hospitals: a review. J. Hosp. Infect. Suppl.A: 481 489.
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: 914 920.
33. Horwitz, M. A. 1983. Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J. Exp. Med. 158: 1319 1331.
34. Horwitz, M. A. 1983. The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J. Exp. Med. 158: 2108 2126.
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: 27 33.
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: 1310 1328.
37. Horwitz, M. A.,, and F. R. Maxfield. 1984. Legionella pneumophila inhibits acidification of its phagosome in human monocytes. J. Cell Biol. 99: 1936 1943.
38. Horwitz, M. A.,, and S. C. Silverstein. 1980. Legionnaires' disease bacterium (Legionella pneumophila) multiples intracellularly in human monocytes. J. Clin. Invest. 66: 441 450.
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: 15 26.
40. Hurley, M. C.,, K. Balazovich,, M. Albano,, N. C. Engleberg,, and B. I. Eisenstein,. 1993. Legionella pneumophila Mip inhibits protein kinase C, p. 69 70. 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: 641 646.
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: 1209 1213.
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: 807 815.
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: 21099 21107.
46. Lundemose, A. G.,, D. A. Rouch,, S. Birkelund,, G. Christiansen,, and J. H. Pearce. 1992. Chlamydia trachomatis Mip-like protein. Mol. Microbiol. 6: 2539 2548.
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: 686 688.
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: 9607 9611.
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: 2738 2744.
50. Maurelli, A. T.,, and P. J. Sansonetti. 1988. Genetic determinants of Shigella pathogenicity. Annu. Rev. Microbiol. 42: 127 150.
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: 240 246.
52. Meyer, R. D. 1983. Legionella infections: a review of five years of research. Rev. Infect. Dis. 5: 258 278.
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: 1449 1455.
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: 3416 3421.
55. Moffat, J. F.,, and L. S. Tompkins. 1992. A quantitative model of intracellular growth of Legionella pneumophila in Acanthamoeba castellana. Infect. Immun. 60: 296 301.
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: 771 782.
57. Nguyen, M. H.,, J. E. Stout,, and V. L. Yu. 1991. Legionellosis. Infect. Dis. Clin. North Am. 5: 561 584.
58. Oaks, E. V.,, M. E. Wingfield,, and S. B. Formal. 1985. Plaque formation by virulent Shigella flexneri. Infect. Immun. 48: 124 129.
59. Pace, J.,, M. J. Hayman,, and J. E. Galan. 1993. Signal transduction and invasion of epithelial cells by S. typhimurium. Cell 72: 505 514.
60. Payne, N. R., and M. A. Horwitz. 1987. Phagocytosis of Legionella pneumophila is mediated by human monocyte complement receptors. J. Exp. Med. 166: 1377 1389.
61. Pearlman, E.,, N. C. Engleberg,, and B. I. Eisenstein. 1985. Identification of protein antigens of Legionella pneumophila serogroup 1. Infect. Immun. 47: 74 79.
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: 87 95.
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: 1459 1471.
64. Quinn, F. D.,, M. G. Keen,, and L. S. Tompkins. 1989. Genetic, immunological, and cytotoxic comparisons of Legionella proteolytic activities. Infect. Immun. 57: 2719 2725.
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: 797 805.
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: 95 112.
67. Racoostn, E. L.,, and J. A. Swanson. 1993. Macropinosome maturation and fusion with tubular lysosomes in macrophages. J. Cell Biol. 121: 1011 1020.
68. Rankin, S.,, and R. R. Isberg. 1993. Identification of Legionella pneumophila loci expressed in response to an intracellular environment. Infect. Agents Dis., 2: 269 271.
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: 4205 4212.
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: 978 986.
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: 5361 5373.
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: 760 764.
75. Skinner, A. R.,, C. M. Anand,, A. Malic,, and J. B. Kurtz. 1983. Acanthamoebae and environmental spread of Legionella pneumophila. Lancet li: 289 290.
76. Storz, G.,, L. A. Tartaglia,, S. B. Farr,, and B. N. Ames. 1990. Bacterial defenses against oxidative stress. Trends Genet. 6: 363 368.
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: 678 681.
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: 3770 3778.
79. Swanson, J.,, E. Burke,, and S. C. Silverstein. 1987. Tubular lysosomes accompany stimulated pinocytosis in macrophages. J. Cell Biol. 104: 1217 1222.
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: 224 226.
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: 2585 2592.
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: 709 719.
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: 2677 2682.
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: 257 264.
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: 1135 1143.
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: 2016 2023.
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: 405 409.
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: 89 98.
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: 428 432.

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