Proteome analysis of Legionella vacuoles purified by magnetic immunoseparation reveals secretory and endosomal GTPases

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Volumn 10, Issue 1, 2009, Pages 76-87

  Urwyler, Simon ^a   Nyfeler, Yves ^a   Ragaz, Curdin ^a   Lee, Hookeun ^a,b   Mueller, Lukas N ^a   Aebersold, Ruedi ^a,c,d   Hilbi, Hubert ^a  

^a ETH ZURICH   (Switzerland)

^b Gachon University College of Medicine   (South Korea)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

Author keywords

Dictyostelium; Drosophila; GTPase; Macrophage; Mass spectrometry; Phagocyte; Phosphoinositide; Vesicle trafficking

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; BACTERIAL PROTEIN; BIOLOGICAL MARKER; CALNEXIN; GREEN FLUORESCENT PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE; PROTEIN SIDC; PROTEOME; RAB PROTEIN; RAB7 PROTEIN; RAB8 PROTEIN; RED FLUORESCENT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE TRANSPORT; CELL VACUOLE; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; DICTYOSTELIUM DISCOIDEUM; ENDOSOME; ENZYME ACTIVITY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GOLGI COMPLEX; LEGIONELLA; LEGIONELLA PNEUMOPHILA; LIQUID CHROMATOGRAPHY; MAGNETIC SEPARATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECRETION; PROTEOMICS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; WILD TYPE;

ANIMALS; DICTYOSTELIUM; ENDOSOMES; GTP PHOSPHOHYDROLASES; IMMUNOLOGIC TECHNIQUES; LEGIONELLA PNEUMOPHILA; MAGNETICS; PHAGOCYTES; PROTEOME; SECRETORY PATHWAY; VACUOLES;

EID: 58149183673     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2008.00851.x     Document Type: Article

References (95)

1. Hilbi H, Weber SS, Ragaz C, Nyfeler Y, Urwyler S. Environmental predators as models for bacterial pathogenesis. Environ Microbiol 2007;9:563-575.
2. Steinert M, Heuner K, Buchrieser C, Albert-Weissenberger C, Glockner G. Legionella pathogenicity: Genome structure, regulatory networks and the host cell response. Int J Med Microbiol 2007;297:577-587.
3. Ragaz C, Pietsch H, Urwyler S, Tiaden A, Weber SS, Hilbi H. The Legionella pneumophila phosphatidylinositol-4 phosphate-binding type IV substrate SidC recruits endoplasmic reticulum vesicles to a replication-permissive vacuole. Cell Microbiol 2008;10:2416-2433.
4. Horwitz MA. Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J Exp Med 1983;158:1319-1331.
5. Swanson MS, Isberg RR. Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect Immun 1995;63:3609-3620.
6. Tilney LG, Harb OS, Connelly PS, Robinson CG, Roy CR. 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 2001;114:4637-4650.
7. Kagan JC, Roy CR. Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat Cell Biol 2002;4:945-954.
8. Kagan JC, Stein MP, Pypaert M, Roy CR. Legionella subvert the functions of Rab1 and Sec22b to create a replicative organelle. J Exp Med 2004;199:1201-1211.
9. Derre I, Isberg RR. Legionella pneumophila replication vacuole formation involves rapid recruitment of proteins of the early secretory system. Infect Immun 2004;72:3048-3053.
10. Dorer MS, Kirton D, Bader JS, Isberg RR. RNA interference analysis of Legionella in Drosophila cells: Exploitation of early secretory apparatus dynamics. PLoS Pathog 2006;2:e34.
11. Solomon JM, Isberg RR. Growth of Legionella pneumophila in Dictyostelium discoideum: A novel system for genetic analysis of host-pathogen interactions. Trends Microbiol 2000;8:478-480.
12. Otto GP, Wu MY, Clarke M, Lu H, Anderson OR, Hilbi H, Shuman HA, Kessin RH. Macroautophagy is dispensable for intracellular replication of Legionella pneumophila in Dictyostelium discoideum. Mol Microbiol 2004;51:63-72.
13. Hilbi H, Segal G, Shuman HA. Icm/Dot-dependent upregulation of phagocytosis by Legionella pneumophila. Mol Microbiol 2001;42:603-617.
14. Weber SS, Ragaz C, Reus K, Nyfeler Y, Hilbi H. Legionella pneumophila exploits PI(4) P to anchor secreted effector proteins to the replicative vacuole. PLoS Pathog 2006;2:e46.
15. Brüggemann H, Cazalet C, Buchrieser C. Adaptation of Legionella pneumophila to the host environment: Role of protein secretion, effectors and eukaryotic-like proteins. Curr Opin Microbiol 2006;9:86-94.
16. Hilbi H. Modulation of phosphoinositide metabolism by pathogenic bacteria. Cell Microbiol 2006;8:1697-1706.
17. Ninio S, Roy CR. Effector proteins translocated by Legionella pneumophila: Strength in numbers. Trends Microbiol 2007;15:372-380.
18. Segal G, Feldman M, Zusman T. The Icm/Dot type-IV secretion systems of Legionella pneumophila and Coxiella burnetii. FEMS Microbiol Rev 2005;29:65-81.
19. Nagai H, Kagan JC, Zhu X, Kahn RA, Roy CR. A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 2002;295:679-682.
20. Machner MP, Isberg RR. Targeting of host Rab GTPase function by the intravacuolar pathogen Legionella pneumophila. Dev Cell 2006;11:47-56.
21. Murata T, Delprato A, Ingmundson A, Toomre DK, Lambright DG, Roy CR. The Legionella pneumophila effector protein DrrA is a Rab1 guanine nucleotide-exchange factor. Nat Cell Biol 2006;8:971-977.
22. Machner MP, Isberg RR. A bifunctional bacterial protein links GDI displacement to Rab1 activation. Science 2007;318:974-977.
23. Ingmundson A, Delprato A, Lambright DG, Roy CR. Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature 2007;450:365-369.
24. Chen J, de Felipe KS, Clarke M, Lu H, Anderson OR, Segal G, Shuman HA. Legionella effectors that promote nonlytic release from protozoa. Science 2004;303:1358-1361.
25. Garin J, Diez R, Kieffer S, Dermine JF, Duclos S, Gagnon E, Sadoul R, Rondeau C, Desjardins M. The phagosome proteome: Insight into phagosome functions. J Cell Biol 2001;152:165-180.
26. Gotthardt D, Warnatz HJ, Henschel O, Bruckert F, Schleicher M, Soldati T. High-resolution dissection of phagosome maturation reveals distinct membrane trafficking phases. Mol Biol Cell 2002;13:3508-3520.
27. Gotthardt D, Blancheteau V, Bosserhoff A, Ruppert T, Delorenzi M, Soldati T. Proteomics fingerprinting of phagosome maturation and evidence for the role of a G α during uptake. Mol Cell Proteomics 2006;5:2228-2243.
28. Sturgill-Koszycki S, Haddix PL, Russell DG. The interaction between Mycobacterium and the macrophage analyzed by two-dimensional polyacrylamide gel electrophoresis. Electrophoresis 1997;18:2558-2565.
29. Mills SD, Finlay BB. 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 1998;77:35-47.
30. Luhrmann A, Haas A. A method to purify bacteria-containing phagosomes from infected macrophages. Methods Cell Sci 2000;22:329-341.
31. Fernandez-Mora E, Polidori M, Luhrmann A, Schaible UE, Haas A. Maturation of Rhodococcus equi-containing vacuoles is arrested after completion of the early endosome stage. Traffic 2005;6:635-653.
32. Kima PE, Dunn W. Exploiting calnexin expression on phagosomes to isolate Leishmania parasitophorous vacuoles. Microb Pathog 2005;38:139-145.
33. Robinson CG, Roy CR. Attachment and fusion of endoplasmic reticulum with vacuoles containing Legionella pneumophila. Cell Microbiol 2006;8:793-805.
34. Luo ZQ, Isberg RR. Multiple substrates of the Legionella pneumophila Dot/ Icm system identified by interbacterial protein transfer. Proc Natl Acad Sci U S A 2004;101:841-846.
35. Weber SS, Ragaz C, Hilbi H. The inositol polyphosphate 5-phosphatase OCRL1 restricts growth of Legionella, localizes to the replicative vacuole and binds to the bacterial effector LpnE. Cell Microbiol [Epub ahead of print].
36. Fajardo M, Schleicher M, Noegel A, Bozzaro S, Killinger S, Heuner K, Hacker J, Steinert M. Calnexin, calreticulin and cytoskeleton-associated proteins modulate uptake and growth of Legionella pneumophila in Dictyostelium discoideum. Microbiology 2004;150:2825-2835.
37. Hägele S, Kohler R, Merkert H, Schleicher M, Hacker J, Steinert M. Dictyostelium discoideum: A new host model system for intracellular pathogens of the genus Legionella. Cell Microbiol 2000;2:165-171.
38. Skriwan C, Fajardo M, Hagele S, Horn M, Wagner M, Michel R, Krohne G, Schleicher M, Hacker J, Steinert M. Various bacterial pathogens and symbionts infect the amoeba Dictyostelium discoideum. Int J Med Microbiol 2002;291:615-624.
39. Veiga E, Guttman JA, Bonazzi M, Boucrot E, Toledo-Arana A, Lin AE, Enninga J, Pizarro-Cerda J, Finlay BB, Kirchhausen T, Cossart P. Invasive and adherent bacterial pathogens co-opt host clathrin for infection. Cell Host Microbe 2007;2:340-351.
40. Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001;2:107-117.
41. Powell RR, Temesvari LA. Involvement of a Rab8-like protein of Dictyostelium discoideum, Sas1, in the formation of membrane extensions, secretion and adhesion during development. Microbiology 2004;150:2513-2525.
42. Henry L, Sheff DR. Rab8 regulates basolateral secretory, but not recycling, traffic at the recycling endosome. Mol Biol Cell 2008;19:2059-2068.
43. Bravo-Cordero JJ, Marrero-Diaz R, Megias D, Genis L, Garcia-Grande A, Garcia MA, Arroyo AG, Montoya MC. MT1-MMP proinvasive activity is regulated by a novel Rab8-dependent exocytic pathway. EMBO J 2007;26:1499-1510.
44. Faust F, Gomez-Lazaro M, Borta H, Agricola B, Schrader M. Rab8 is involved in zymogen granule formation in pancreatic acinar AR42J cells. Traffic 2008;9:964-979.
45. Ang AL, Folsch H, Koivisto UM, Pypaert M, Mellman I. The Rab8 GTPase selectively regulates AP-1B-dependent basolateral transport in polarized Madin-Darby canine kidney cells. J Cell Biol 2003;163:339-350.
46. Sato T, Mushiake S, Kato Y, Sato K, Sato M, Takeda N, Ozono K, Miki K, Kubo Y, Tsuji A, Harada R, Harada A. The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature 2007;448:366-369.
47. Buczynski G, Bush J, Zhang L, Rodriguez-Paris J, Cardelli J. Evidence for a recycling role for Rab7 in regulating a late step in endocytosis and in retention of lysosomal enzymes in Dictyostelium discoideum. Mol Biol Cell 1997;8:1343-1360.
48. Harris E, Wang N, Wu Wl WL, Weatherford A, De Lozanne A, Cardelli J. Dictyostelium LvsB mutants model the lysosomal defects associated with Chediak-Higashi syndrome. Mol Biol Cell 2002;13:656-669.
49. Clemens DL, Lee BY, Horwitz MA. Mycobacterium tuberculosis and Legionella pneumophila phagosomes exhibit arrested maturation despite acquisition of Rab7. Infect Immun 2000;68:5154-5166.
50. Harris E, Cardelli J. RabD, a Dictyostelium Rab14-related GTPase, regulates phagocytosis and homotypic phagosome and lysosome fusion. J Cell Sci 2002;115:3703-3713.
51. Temesvari L, Rodriguez-Paris J, Bush J, Steck TL, Cardelli J. Characterization of lysosomal membrane proteins of Dictyostelium discoideum. A complex population of acidic integral membrane glycoproteins, Rab GTP-binding proteins and vacuolar ATPase subunits. J Biol Chem 1994;269:25719-25727.
52. Kyei GB, Vergne I, Chua J, Roberts E, Harris J, Junutula JR, Deretic V. Rab14 is critical for maintenance of Mycobacterium tuberculosis phagosome maturation arrest. EMBO J 2006;25:5250-5259.
53. Molmeret M, Santic M, Asare R, Carabeo RA, Abu Kwaik Y. Rapid escape of the dot/icm mutants of Legionella pneumophila into the cytosol of mammalian and protozoan cells. Infect Immun 2007;75:3290-3304.
54. Sturgill-Koszycki S, Swanson MS. Legionella pneumophila replication vacuoles mature into acidic, endocytic organelles. J Exp Med 2000;192:1261-1272.
55. 2 on the Golgi complex. Nat Cell Biol 1999;1:280-287.
56. Mampel J, Spirig T, Weber SS, Haagensen JAJ, Molin S, Hilbi H. Planktonic replication is essential for biofilm formation by Legionella pneumophila in a complex medium under static and dynamic flow conditions. Appl Environ Microbiol 2006;72:2885-2895.
57. Troll H, Malchow D, Muller-Taubenberger A, Humbel B, Lottspeich F, Ecke M, Gerisch G, Schmid A, Benz R. Purification, functional characterization, and cDNA sequencing of mitochondrial porin from Dictyostelium discoideum. J Biol Chem 1992;267:21072-21079.
58. Lee H, Yi EC, Wen B, Reily TP, Pohl L, Nelson S, Aebersold R, Goodlett DR. Optimization of reversed-phase microcapillary liquid chromatography for quantitative proteomics. J Chromatogr B Analyt Technol Biomed Life Sci 2004;803:101-110.
59. Chisholm RL, Gaudet P, Just EM, Pilcher KE, Fey P, Merchant SN, Kibbe WA. dictyBase, the model organism database for Dictyostelium discoideum. Nucleic Acids Res 2006;34:D423-D427.
60. Keller A, Nesvizhskii AI, Kolker E, Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 2002;74:5383-5392.
61. Nesvizhskii AI, Keller A, Kolker E, Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 2003;75:4646-4658.
62. Keller A, Eng J, Zhang N, Li XJ, Aebersold R. A uniform proteomics MS/MS analysis platform utilizing open XML file formats. Mol Syst Biol 2005;1:2005-0017.
63. Saraste J, Lahtinen U, Goud B. Localization of the small GTP-binding protein Rab1p to early compartments of the secretory pathway. J Cell Sci 1995;108:1541-1552.
64. Hattula K, Furuhjelm J, Tikkanen J, Tanhuanpaa K, Laakkonen P, Peranen J. Characterization of the Rab8-specific membrane traffic route linked to protrusion formation. J Cell Sci 2006;119:4866-4877.
65. Roland JT, Kenworthy AK, Peranen J, Caplan S, Goldenring JR. Myosin Vb interacts with Rab8a on a tubular network containing EHD1 and EHD3. Mol Biol Cell 2007;18:2828-2837.
66. Bush J, Franek K, Daniel J, Spiegelman GB, Weeks G, Cardelli J. Cloning and characterization of five novel Dictyostelium discoideum rab-related genes. Gene 1993;136:55-60.
67. Reinders Y, Schulz I, Graf R, Sickmann A. Identification of novel centrosomal proteins in Dictyostelium discoideum by comparative proteomic approaches. J Proteome Res 2006;5:589-598.
68. Bolourani P, Spiegelman GB, Weeks G. Delineation of the roles played by RasG and RasC in cAMP-dependent signal transduction during the early development of Dictyostelium discoideum. Mol Biol Cell 2006;17:4543-4550.
69. Rivero F, Illenberger D, Somesh BP, Dislich H, Adam N, Meyer AK. Defects in cytokinesis, actin reorganization and the contractile vacuole in cells deficient in RhoGDI. EMBO J 2002;21:4539-4549.
70. Ruscetti T, Cardelli JA, Niswonger ML, O'Halloran TJ. Clathrin heavy chain functions in sorting and secretion of lysosomal enzymes in Dictyostelium discoideum. J Cell Biol 1994;126:343-352.
71. Arnoult D, Tatischeff I, Estaquier J, Girard M, Sureau F, Tissier JP, Grodet A, Dellinger M, Traincard F, Kahn A, Ameisen JC, Petit PX. On the evolutionary conservation of the cell death pathway: Mitochondrial release of an apoptosis-inducing factor during Dictyostelium discoideum cell death. Mol Biol Cell 2001;12:3016-3030.
72. Matto-Yelin M, Aitken A, Ravid S. 14-3-3 inhibits the Dictyostelium myosin II heavy-chain-specific protein kinase C activity by a direct interaction: Identification of the 14-3-3 binding domain. Mol Biol Cell 1997;8:1889-1899.
73. Graf R. DdNek2, the first non-vertebrate homologue of human Nek2, is involved in the formation of microtubule-organizing centers. J Cell Sci 2002;115:1919-1929.
74. Murphy MB, Levi SK, Egelhoff TT. Molecular characterization and immunolocalization of Dictyostelium discoideum protein phosphatase 2A. FEBS Lett 1999;456:7-12.
75. Li G, Foote C, Alexander S, Alexander H. Sphingosine-1-phosphate lyase has a central role in the development of Dictyostelium discoideum. Development 2001;128:3473-3483.
76. Morita T, Amagai A, Maeda Y. Unique behavior of a Dictyostelium homologue of TRAP-1, coupling with differentiation of D. discoideum cells. Exp Cell Res 2002;280:45-54.
77. Hagedorn M, Soldati T. Flotillin and RacH modulate the intracellular immunity of Dictyostelium to Mycobacterium marinum infection. Cell Microbiol 2007;9:2716-2733.
78. Cornillon S, Dubois A, Bruckert F, Lefkir Y, Marchetti A, Benghezal M, De Lozanne A, Letourneur F, Cosson P. Two members of the beige/CHS (BEACH) family are involved at different stages in the organization of the endocytic pathway in Dictyostelium. J Cell Sci 2002;115:737-744.
79. Coukell MB, Moniakis J, Cameron AM. The patB gene of Dictyostelium discoideum encodes a P-type H(+)-ATPase isoform essential for growth and development under acidic conditions. Microbiology 1997;143:3877-3888.
80. Lu H, Clarke M. Dynamic properties of Legionella-containing phagosomes in Dictyostelium amoebae. Cell Microbiol 2005;7:995-1007.
81. Müller-Taubenberger A, Lupas AN, Li H, Ecke M, Simmeth E, Gerisch G. Calreticulin and calnexin in the endoplasmic reticulum are important for phagocytosis. EMBO J 2001;20:6772-6782.
82. Journet A, Chapel A, Jehan S, Adessi C, Freeze H, Klein G, Garin J. Characterization of Dictyostelium discoideum cathepsin D. J Cell Sci 1999;112:3833-3843.
83. Monnat J, Hacker U, Geissler H, Rauchenberger R, Neuhaus EM, Maniak M, Soldati T. Dictyostelium discoideum protein disulfide isomerase, an endoplasmic reticulum resident enzyme lacking a KDEL-type retrieval signal. FEBS Lett 1997;418:357-362.
84. Nijtmans LG, Artal SM, Grivell LA, Coates PJ. The mitochondrial PHB complex: Roles in mitochondrial respiratory complex assembly, ageing and degenerative disease. Cell Mol Life Sci 2002;59:143-155.
85. Nishii W, Ueki T, Miyashita R, Kojima M, Kim YT, Sasaki N, Murakami-Murofushi K, Takahashi K. Structural and enzymatic characterization of physarolisin (formerly physaropepsin) proves that it is a unique serine-carboxyl proteinase. Biochem Biophys Res Commun 2003;301:1023-1029.
86. Homma K, Yoshida Y, Nakano A. Evidence for recycling of cytochrome P450 sterol 14-demethylase from the cis-Golgi compartment to the endoplasmic reticulum (ER) upon saturation of the ER-retention mechanism. J Biochem 2000;127:747-754.
87. Weiner OH, Murphy J, Griffiths G, Schleicher M, Noegel AA. The actin-binding protein comitin (p24) is a component of the Golgi apparatus. J Cell Biol 1993;123:23-34.
88. Bosgraaf L, van Haastert PJ. The regulation of myosin II in Dictyostelium. Eur J Cell Biol 2006;85:969-979.
89. Wuestehube LJ, Luna EJ. F-actin binds to the cytoplasmic surface of ponticulin, a 17-kD integral glycoprotein from Dictyostelium discoideum plasma membranes. J Cell Biol 1987;105:1741-1751.
90. Faix J, Steinmetz M, Boves H, Kammerer RA, Lottspeich F, Mintert U, Murphy J, Stock A, Aebi U, Gerisch G. Cortexillins, major determinants of cell shape and size, are actin-bundling proteins with a parallel coiled-coil tail. Cell 1996;86:631-642.
91. Schneider N, Weber I, Faix J, Prassler J, Müller-Taubenberger A, Kohler J, Burghardt E, Gerisch G, Marriott G. A Lim protein involved in the progression of cytokinesis and regulation of the mitotic spindle. Cell Motil Cytoskeleton 2003;56:130-139.
92. Madigan SJ, Katz ER. Identification and characterization of catA, a mutation causing catalase deficiency in Dictyostelium discoideum. J Bacteriol 1989;171:1492-1495.
93. Akaza Y, Tsuji A, Yasukawa H. Analysis of the gene encoding copper/zinc superoxide dismutase homolog in Dictyostelium discoideum. Biol Pharm Bull 2002;25:1528-1532.
94. Janssen KP, Rost R, Eichinger L, Schleicher M. Characterization of CD36/ LIMPII homologues in Dictyostelium discoideum. J Biol Chem 2001;276:38899-38910.
95. van Zon A, Mossink MH, Scheper RJ, Sonneveld P, Wiemer EA. The vault complex. Cell Mol Life Sci 2003;60:1828-1837.