Identification and subcellular localization of the Legionella pneumophila IcmX protein: A factor essential for establishment of a replicative organelle in eukaryotic host cells

Infection and Immunity

Volumn 68, Issue 7, 2000, Pages 3971-3982

  Matthews, Miguelina ^a   Roy, Craig R ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN ICMX; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL GROWTH; GENETIC ANALYSIS; NONHUMAN; PATHOGENICITY; PHAGOSOME; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT;

ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; CELLS, CULTURED; DNA PRIMERS; GENE DELETION; GENES, BACTERIAL; HUMANS; LEGIONELLA; LEGIONELLA PNEUMOPHILA; MACROPHAGES; MICE; ORGANELLES; PERIPLASM; PHAGOSOMES; SPECIES SPECIFICITY; U937 CELLS; VIRULENCE;

EID: 0033932228     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.68.7.3971-3982.2000     Document Type: Article

References (58)

1. Abath, F. G., A. M. Almeida, and L. C. Ferreira. 1992. Identification of surface-exposed Yersinia pestis proteins by radio-iodination and biotinylation. J. Med. Microbiol. 37:420-424.
2. Abu Kwaik, Y., C. Venkataraman, O. S. Harb, and L. Y. Gao. 1998. Signal transduction in the protozoan host Hartmannella vermiformis upon attachment and invasion by Legionella micdadei. Appl. Environ. Microbiol. 64: 3134-3139.
3. Andrews, H. L., J. P. Vogel, and R. R. Isberg. 1998. Identification of linked Legionella pneumophila genes essential for intracellular growth and evasion of the endocytic pathway. Infect. Immun. 66:950-958.
4. Baron, C., M. Llosa, S. Zhou, and P. C. Zambryski. 1997. VirB1, a component of the T-complex transfer machinery of Agrobacterium tumefaciens, is processed to a C-terminal secreted product, VirB1. J. Bacteriol. 179:1203-1210.
5. Berger, K. H., 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.
6. Bornstein, N., D. Marmet, M. Surgot, M. Nowicki, H. Meugnier, J. Fleurette, E. Ageron, F. Grimont, P. A. Grimont, W. L. Thacker, et al. 1989. Legionella gratiana sp. nov. isolated from French spa water. Res. Microbiol. 140:541-552.
7. Bradburne, J. A., P. Godfrey, J. H. Choi, and J. N. Mathis. 1993. In vivo labeling of Escherichia coli cell envelope proteins with N-hydroxysuccinimide esters of biotin. Appl. Environ. Microbiol. 59:663-668.
8. Brand, B. C., A. B. Sadosky, and H. A. Shuman. 1994. The Legionella pneumophila icm locus: a set of genes required for intracellular multiplication in human macrophages. Mol. Microbiol. 14:797-808.
9. Brenner, D. J., A. G. Steigerwalt, and J. E. McDade. 1979. Classification of the Legionnaires' disease bacterium: Legionella pneumophila, genus novum, species nova, of the family Legionellaceae, family nova. Ann. Intern. Med. 90:655-658.
10. Celada, A., P. W. Gray, E. Rinderknecht, and R. D. Schreiber. 1984. Evidence for a gamma-interferon receptor that regulates macrophage tumoricidal activity. J. Exp. Med. 160:55-74.
11. Chen, J. W., W. Pan, M. P. D'Souza, and J. T. August. 1985. Lysosome-associated membrane proteins: characterization of LAMP-1 of macrophage P388 and mouse embryo 3T3 cultured cells. Arch. Biochem. Biophys. 239: 574-586.
12. Cianciotto, N. P., J. M. Bangsborg, B. I. Eisenstein, and N. C. Engleberg. 1990. Identification of mip-like genes in the genus Legionella. Infect. Immun. 58:2912-2918.
13. Cianciotto, N. P., and B. S. Fields. 1992. Legionella pneumophila mip gene potentiates intracellular infection of protozoa and human macrophages. Proc. Natl. Acad. Sci. USA 89:5188-5191.
14. Coers, J., C. Monahan, and C. R. Roy. 1999. Modulation of phagosome biogenesis by Legionella pneumophila creates an organelle permissive for intracellular growth. Nat. Cell Biol. 1:451-453.
15. Collazo, C. M., and J. E. Galan. 1997. The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell. Mol. Microbiol. 24:747-756.
16. Collazo, C. M., and J. E. Galan. 1996. Requirement for exported proteins in secretion through the invasion-associated type III system of Salmonella typhimurium. Infect. Immun. 64:3524-3531.
17. Dreyfus, L. A., and B. H. Iglewski. 1986. Purification and characterization of an extracellular protease of Legionella pneumophila. Infect. Immun. 51:736-743.
18. Edelstein, P. H., M. A. Edelstein, F. Higa, and S. Falkow. 1999. Discovery of virulence genes of Legionella pneumophila by using signature tagged mutagenesis in a guinea pig pneumonia model. Proc. Natl. Acad. Sci. USA 96:8190-8195.
19. Feeley, J. C., R. J. Gibson, G. W. Gorman, N. C. Langford, J. K. Rasheed, D. C. Mackel, and W. B. Blaine. 1979. Charcoal-yeast extract agar: primary isolation medium for Legionella pneumophila. J. Clin. Microbiol. 10:437-441.
20. Fields, B. S. 1996. The molecular ecology of legionellae. Trends Microbiol. 4:286-490.
21. Gao, L. Y., O. S. Harb, and Y. Abu Kwaik. 1997. Utilization of similar mechanisms by Legionella pneumophila to parasitize two evolutionarily distant host cells, mammalian macrophages and protozoa. Infect. Immun. 65: 4738-4746.
22. Gao, L. Y., O. S. Harb, and Y. A. Kwaik. 1998. Identification of macrophage-specific infectivity loci (mil) of Legionella pneumophila that are not required for infectivity of protozoa. Infect. Immun. 66:883-892.
23. Guan, K. L., and J. E. Dixon. 1991. Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal. Biochem. 192:262-267.
24. Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor, N.Y.
25. Hebert, G. A., C. W. Moss, L. K. McDougal, F. M. Bozeman, R. M. McKinney, and D. J. Brenner. 1980. The rickettsia-like organisms TATLOCK (1943) and HEBA (1959): bacteria phenotypically similar to but genetically distinct from Legionella pneumophila and the WIGA bacterium. Ann. Intern. Med. 92:45-52.
26. Hoffman, C. S., and A. Wright. 1985. Fusions of secreted proteins to alkaline phosphatase: an approach for studying protein secretion. Proc. Natl. Acad. Sci. USA 82:5107-5111.
27. 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.
28. Horwitz, M. A. 1983. The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome lysosome fusion in human monocytes. J. Exp. Med. 158:2108-2126.
29. Horwitz, M. A., and S. C. Silverstein. 1980. Legionnaires' disease bacterium (Legionella pneumophila) multiplies intracellularly in human monocytes. J. Clin. Investig. 66:441-450.
30. Joshi, A. D., and M. S. Swanson. 1999. Comparative analysis of Legionella pneumophila and Legionella micdadei virulence traits. Infect. Immun. 67: 4134-4142.
31. Kirby, J. E., J. P. Vogel, H. L. Andrews, and R. R. Isberg. 1998. Evidence for pore-forming ability by Legionella pneumophila. Mol. Microbiol. 27:323-336.
32. Kolter, R., M. Inuzuka, and D. R. Helinski. 1978. Trans-complementation-dependent replication of a low molecular weight origin fragment from plasmid R6K. Cell 15:1199-1208.
33. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
34. Manoil, C., and J. Beckwith. 1986. A genetic approach to analyzing membrane protein topology. Science 233:1403-1408.
35. 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.
36. McDade, J. E., D. J. Brenner, and F. M. Bozeman. 1979. Legionnaires' disease bacterium isolated in 1947. Ann. Intern. Med. 90:659-661.
37. McDade, J. E., C. C. Shepard, D. W. Fraser, T. R. Tsai, M. A. Redus, and W. R. Dowdle. 1977. Legionnaires' disease: isolation of a bacterium and demonstration of its role in other respiratory diseases. N. Engl. J. Med. 297:1197-1203.
38. 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.
39. Merriam, J. J., R. Mathur, R. Maxfield-Boumil, and R. R. Isberg. 1997. Analysis of the Legionella pneumophila fliI gene: intracellular growth of a defined mutant defective for flagellum biosynthesis. Infect. Immun. 65:2497-2501.
40. Morales, V. M., A. Backman, and M. Bagdasarian. 1991. A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants. Gene 97:39-47.
41. Obert, S. O., R. J. Connor, S. Schmid, and P. Hearing. 1994. The adenovirus E4-6/7 protein transactivates the E2 promoter by inducing dimerization of a heteromeric E2F complex. Mol. Cell. Biol. 14:1333-1346.
42. Pasculle, A. W., J. C. Feeley, R. J. Gibson, L. G. Cordes, R. L. Myerowitz, C. M. Patton, G. W. Gorman, C. L. Carmack, J. W. Ezzell, and J. N. Dowling. 1980. Pittsburgh pneumonia agent: direct isolation from human lung tissue. J. Infect. Dis. 141:727-732.
43. Pearlman, E., 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.
44. Ratcliff, R. M., S. C. Donnellan, J. A. Lanser, P. A. Manning, and M. W. Heuzenroeder. 1997. Interspecies sequence differences in the Mip protein from the genus Legionella: implications for function and evolutionary relatedness. Mol. Microbiol. 25:1149-1158.
45. Roy, C. R. 1999. Trafficking of the Legionella pneumophila phagosome. ASM News 65:416-421.
46. Roy, C. R., K. Berger, and R. R. Isberg. 1998. Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol. Microbiol. 28:663-674.
47. Roy, C. R., and R. R. Isberg. 1997. Topology of Legionella pneumophila DotA: an inner membrane protein required for replication in macrophages. Infect. Immun. 65:571-578.
48. 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.
49. Segal, G., M. Purcell, and H. A. Shuman. 1998. Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc. Natl. Acad. Sci. USA 95:1669-1674.
50. Segal, G., and H. A. Shuman. 1997. Characterization of a new region required for macrophage killing by Legionella pneumophila. Infect. Immun. 65:5057-5066.
51. Segal, G., and H. A. Shuman. 1998. How is the intracellular fate of the Legionella pneumophila phagosome determined? Trends Microbiol. 6:253-255.
52. Segal, G., and H. A. Shuman. 1999. Legionella pneumophila utilizes the same genes to multiply within Acanthamoeba castellanii and human macrophages. Infect. Immun. 67:2117-2124.
53. Segal, G., and H. A. Shuman. 1999. Possible origin of the Legionella pneumophila virulence genes and their relation to Coxiella burnetii. Mol. Microbiol. 33:669-670.
54. Sinai, A. P., and K. A. Joiner. 1997. Safe haven: the cell biology of nonfusogenic pathogen vacuoles. Annu. Rev. Microbiol. 51:415-462.
55. Vogel, J. P., H. L. Andrews, S. K. Wong, and R. R. Isberg. 1998. Conjugative transfer by the virulence system of Legionella pneumophila. Science 279:873-876.
56. Vogel, J. P., and R. R. Isberg. 1999. Cell biology of Legionella pneumophila. Curr. Opin. Microbiol. 2:30-34.
57. Wiater, L. A., K. Dunn, F. R. Maxfield, and H. A. Shuman. 1998. Early events in phagosome establishment are required for intracellular survival of Legionella pneumophila. Infect. Immun. 66:4450-4460.
58. Zuckman, D. M., J. B. Hung, and C. R. Roy. 1999. Pore-forming activity is not sufficient for Legionella pneumophila phagosome trafficking and intracellular growth. Mol. Microbiol. 32:990-1001.