Proteomic analysis of Legionella-containing phagosomes isolated from Dictyostelium

International Journal of Medical Microbiology

Volumn 299, Issue 7, 2009, Pages 489-508

  Shevchuk, Olga ^a,b   Batzilla, Christoph ^b   Hägele, Sonja ^c   Kusch, Harald ^c   Engelmann, Susanne ^d   Hecker, Michael ^d   Haas, Albert ^e   Heuner, Klaus ^b   Glöckner, Gernot ^f   Steinert, Michael ^a  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c Abteilung Herz Kreislaufphysiologie   (Germany)

^d UNIVERSITY OF GREIFSWALD   (Germany)

^e UNIVERSITY OF BONN   (Germany)

^f FRITZ LIPMANN INSTITUTE   (Germany)

Author keywords

Dictyostelium discoideum; Legionella pneumophila; Phagosome; Proteome

Indexed keywords

KHELLIN; PROTEIN; PROTEIN KINASE C INHIBITOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RHO FACTOR; RHOGDI PROTEIN; SUPEROXIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATION; CELL FRACTIONATION; CELL ISOLATION; CELL MATURATION; CONTROLLED STUDY; CYTOSOL; DICTYOSTELIUM; DICTYOSTELIUM DISCOIDEUM; DISSECTION; GENOMICS; GROWTH INHIBITION; HOST CELL; KINETICS; LEGIONELLA; LEGIONELLA PNEUMOPHILA; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PHAGOSOME; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEOMICS; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ACTINS; ANIMALS; CELL FRACTIONATION; CYSTEINE PROTEINASE INHIBITORS; DICTYOSTELIUM; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENOMICS; LEGIONELLA; LYSOSOMES; MICROFILAMENT PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, BIOLOGICAL; NADPH OXIDASE; PHAGOSOMES; PROTEIN KINASE INHIBITORS; PROTEOME; PROTEOMICS; PROTOZOAN PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SUPEROXIDES;

EID: 70349095902     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2009.03.006     Document Type: Article

References (53)

1. Al-Khodor S., Price C.T., Habyarimana F., Kalia A., and Abu Kwaik Y. A Dot/Icm-translocated ankyrin protein of Legionella pneumophila is required for intracellular proliferation within human macrophages and protozoa. Mol. Microbiol. 70 (2008) 908-923
2. Cazalet C., Rusniok C., Brüggemann H., Zidane N., Magnier A., Ma L., Tichit M., Jarraud S., Bouchier C., Vandenesch F., Kunst F., Etienne J., Glaser P., and Buchrieser C. Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat. Genet. 36 (2004) 1165-1173
3. Chen J., Reyes M., Clarke M., and Shuman H.A. Host cell-dependent secretion and translocation of the LepA and LepB effectors of Legionella pneumophila. Cell Microbiol. 9 (2007) 1660-1671
4. Chen G., Zhuchenko O., and Kuspa A. Immune-like phagocyte activity in the social amoeba. Science 317 (2007) 678-681
5. Chisholm R.L., Gaudet P., Just E.M., Pilcher K.E., Fey P., Merchant S.N., and Kibbe W.A. dictyBase, the model organism database for Dictyostelium discoideum. Nucleic Acids Res. 34 (2006) D423-427
6. Clarke M., Bazari W.L., and Kayman S.C. Isolation and properties of calmodulin from Dictyostelium discoideum. J. Bacteriol. 141 (1980) 397-400
7. de Felipe K.S., Glover R.T., Charpentier X., Anderson O.R., Reyes M., Pericone C.D., and Shuman H.A. Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog. 4 (2008) e1000117
8. Derre I., and Isberg R.R. LidA, a translocated substrate of the Legionella pneumophila type IV secretion system, interferes with the early secretory pathway. Infect. Immun. 73 (2005) 4370-4380
9. Dovas A., and Couchman J.R. RhoGDI: multiple functions in the regulation of Rho family GTPase activities. Biochem. J. 390 (2005) 1-9
10. D'Souza-Schorey C., Boshans R.L., McDonough M., Stahl P.D., and Van Aelst L. A role for POR1, a Rac1-interacting protein, in ARF6-mediated cytoskeletal rearrangements. Embo J. 16 (1997) 5445-5454
11. Duhon D., and Cardelli J. The regulation of phagosome maturation in Dictyostelium. J. Muscle Res. Cell Motil. 23 (2002) 803-808
12. Edelstein P.H. Improved semiselective medium for isolation of Legionella pneumophila from contaminated clinical and environmental specimens. J. Clin. Microbiol. 14 (1981) 298-303
13. Egawa K., Klein T.W., Yamamoto Y., Newton C.A., and Friedman H. Cyclic AMP inhibition of lipopolysaccharide-induced restriction of Legionella pneumophila growth in macrophage cultures. Infect. Immun. 60 (1992) 1936-1940
14. Eymann C., Dreisbach A., Albrecht D., Bernhardt J., Becher D., Gentner S., Tam le T., Büttner K., Buurman G., Scharf C., Venz S., Völker U., and Hecker M. A comprehensive proteome map of growing Bacillus subtilis cells. Proteomics 4 (2004) 2849-2876
15. Fajardo M., Schleicher M., Noegel A., Bozzaro S., Killinger S., Heuner K., Hacker J., and Steinert M. Calnexin, calreticulin and cytoskeleton-associated proteins modulate uptake and growth of Legionella pneumophila in Dictyostelium discoideum. Microbiology 150 (2004) 2825-2835
16. Farbrother P., Wagner C., Na J., Tunggal B., Morio T., Urushihara H., Tanaka Y., Schleicher M., Steinert M., and Eichinger L. Dictyostelium transcriptional host cell response upon infection with Legionella. Cell Microbiol. 8 (2006) 438-456
17. Fernandez-Mora E., Polidori M., Lührmann A., Schaible U.E., and Haas A. Maturation of Rhodococcus equi-containing vacuoles is arrested after completion of the early endosome stage. Traffic 6 (2005) 635-653
18. Goldsbrough A.P., Bulleid N.J., Freedman R.B., and Flavell R.B. Conformational differences between two wheat (Triticum aestivum) 'high-molecular-weight' glutenin subunits are due to a short region containing six amino acid differences. Biochem. J. 263 (1989) 837-842
19. Gotthardt D., Warnatz H.J., Henschel O., Bruckert F., Schleicher M., and Soldati T. High-resolution dissection of phagosome maturation reveals distinct membrane trafficking phases. Mol. Biol. Cell 13 (2002) 3508-3520
20. Gotthardt D., Blancheteau V., Bosserhoff A., Ruppert T., Delorenzi M., and Soldati T. Proteomics fingerprinting of phagosome maturation and evidence for the role of a Galpha during uptake. Mol. Cell Proteom. 5 (2006) 2228-2243
21. Grogan A., Reeves E., Keep N., Wientjes F., Totty N.F., Burlingame A.L., Hsuan J.J., and Segal A.W. Cytosolic phox proteins interact with and regulate the assembly of coronin in neutrophils. J. Cell Sci. 110 (1997) 3071-3081
22. Hägele S., Köhler R., Merkert H., Schleicher M., Hacker J., and Steinert M. Dictyostelium discoideum: a new host model system for intracellular pathogens of the genus Legionella. Cell Microbiol. 2 (2000) 165-171
23. Harada T., Miyake M., and Imai Y. Evasion of Legionella pneumophila from the bactericidal system by reactive oxygen species (ROS) in macrophages. Microbiol. Immunol. 51 (2007) 1161-1170
24. Hilbi H., Weber S.S., Ragaz C., Nyfeler Y., and Urwyler S. Environmental predators as models for bacterial pathogenesis. Environ. Microbiol. 9 (2007) 563-575
25. Jepras R.I., Fitzgeorge R.B., and Baskerville A. A comparison of virulence of two strains of Legionella pneumophila based on experimental aerosol infection of guinea-pigs. J. Hyg. (Lond.) 95 (1985) 29-38
26. Ivanov S.S., and Roy C.R. Modulation of ubiquitin dynamics and suppression of DALIS formation by the Legionella pneumophila Dot/Icm system. Cell Microbiol. 11 (2009) 261-278
27. Kalamidas S.A., Kuehnel M.P., Peyron P., Rybin V., Rauch S., Kotoulas O.B., Houslay M., Hemmings B.A., Gutierrez M.G., Anes E., and Griffiths G. cAMP synthesis and degradation by phagosomes regulate actin assembly and fusion events: consequences for mycobacteria. J. Cell Sci. 119 (2006) 3686-3694
28. Kaul D. Coronin-1A epigenomics governs mycobacterial persistence in tuberculosis. FEMS Microbiol. Lett. 278 (2008) 10-14
29. Kima P.E., and Dunn W. Exploiting calnexin expression on phagosomes to isolate Leishmania parasitophorous vacuoles. Microb. Pathog. 38 (2005) 139-145
30. Kubori T., Hyakutake A., and Nagai H. Legionella translocates an E3 ubiquitin ligase that has multiple U-boxes with distinct functions. Mol. Microbiol. 67 (2008) 1307-1319
31. Li Z., Solomon J.M., and Isberg R.R. Dictyostelium discoideum strains lacking the RtoA protein are defective for maturation of the Legionella pneumophila replication vacuole. Cell Microbiol. 7 (2005) 431-442
32. Lu H., and Clarke M. Dynamic properties of Legionella-containing phagosomes in Dictyostelium amoebae. Cell Microbiol. 7 (2005) 995-1007
33. Lührmann A., and Haas A. A method to purify bacteria-containing phagosomes from infected macrophages. Methods Cell Sci. 22 (2000) 329-341
34. Machner M.P., and Isberg R.R. Targeting of host Rab GTPase function by the intravacuolar pathogen Legionella pneumophila. Dev. Cell. 11 (2006) 47-56
35. Mills S.D., and Finlay B.B. Isolation and characterization of Salmonella typhimurium and Yersinia pseudotuberculosis-containing phagosomes from infected mouse macrophages: Y. pseudotuberculosis traffics to terminal lysosomes where they are degraded. Eur. J. Cell. Biol. 77 (1998) 35-47
36. Molmeret M., Horn M., Wagner M., Santic M., and Abu Kwaik Y. Amoebae as training grounds for intracellular bacterial pathogens. Appl. Environ. Microbiol. 71 (2005) 20-28
37. Murata T., Delprato A., Ingmundson A., Toomre D.K., Lambright D.G., and Roy C.R. The Legionella pneumophila effector protein DrrA is a Rab1 guanine nucleotide-exchange factor. Nat. Cell Biol. 8 (2006) 971-977
38. Nagai H., Kagan J.C., Zhu X., Kahn R.A., and Roy C.R. A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 295 (2002) 679-682
39. North M.J., Nicol K., Sands T.W., and Cotter D.A. Acid-activatable cysteine proteinases in the cellular slime mold Dictyostelium discoideum. J. Biol. Chem. 271 (1996) 14462-14467
40. Ott M., Messner P., Heesemann J., Marre R., and Hacker J. Temperature-dependent expression of flagella in Legionella. J. Gen. Microbiol. 137 (1991) 1955-1961
41. Ragaz C., Pietsch H., Urwyler S., Tiaden A., Weber S.S., and Hilbi H. The Legionella pneumophila phosphatidylinositol-4 phosphate-binding type IV substrate SidC recruits endoplasmic reticulum vesicles to a replication-permissive vacuole. Cell Microbiol. 10 (2008) 2416-2433
42. Richardson J.M., Woychik N.A., Ebert D.L., Dimond R.L., and Cardelli J.A. Inhibition of early but not late proteolytic processing events leads to the missorting and oversecretion of precursor forms of lysosomal enzymes in Dictyostelium discoideum. J. Cell Biol. 107 (1988) 2097-2107
43. Rodriguez-Paris J.M., Nolta K.V., and Steck T.L. Characterization of lysosomes isolated from Dictyostelium discoideum by magnetic fractionation. J. Biol. Chem. 268 (1993) 9110-9116
44. Skriwan C., Fajardo M., Hägele S., Horn M., Wagner M., Michel R., Krohne G., Schleicher M., Hacker J., and Steinert M. Various bacterial pathogens and symbionts infect the amoeba Dictyostelium discoideum. Int. J. Med. Microbiol. 291 (2002) 615-624
45. Solomon J.M., Rupper A., Cardelli J.A., and Isberg R.R. Intracellular growth of Legionella pneumophila in Dictyostelium discoideum, a system for genetic analysis of host-pathogen interactions. Infect. Immun. 68 (2000) 2939-2947
46. Steinert M., and Heuner K. Dictyostelium as host model for pathogenesis. Cell. Microbiol. 7 (2005) 307-314
47. Steinert M., Heuner K., Buchrieser C., Albert-Weissenberger C., and Glöckner G. Legionella pathogenicity: genome structure, regulatory networks and the host cell response. Int. J. Med. Microbiol. 297 (2007) 577-587
48. Sturgill-Koszycki S., Haddix P.L., and Russell D.G. The interaction between Mycobacterium and the macrophage analyed by two-dimensional poly-acrylamide gel electrophoresis. Electrophoresis 18 (1997) 2558-2565
49. Tilney L.G., Harb O.S., Connelly P.S., Robinson C.G., and Roy C.R. How the parasitic bacterium Legionella pneumophila modifies its phagosome and transforms it into rough ER: implications for conversion of plasma membrane to the ER membrane. J. Cell Sci. 114 (2001) 4637-4650
50. Towbin H., Staehelin T., and Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76 (1979) 4350-4354
51. Ünal C., and Steinert M. Dictyostelium discoideum as a model to study host-pathogen interactions. Methods Mol. Biol. 346 (2006) 507-515
52. Urwyler S., Nyfeler Y., Ragaz C., Lee H., Mueller L.N., Aebersold R., and Hilbi H. Proteome analysis of Legionella vacuoles purified by magnetic immuno-separation reveals secretory and endosomal GTPases. Traffic 10 (2009) 76-87
53. Weber S.S., Ragaz C., Reus K., Nyfeler Y., and Hilbi H. Legionella pneumophila exploits PI(4)P to anchor secreted effector proteins to the replicative vacuole. PLoS Pathog. 2 (2006) e46