LegC3, an Effector Protein from Legionella pneumophila, Inhibits Homotypic Yeast Vacuole Fusion In Vivo and In Vitro

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Bennett, Terry L ^a   Kraft, Shannon M ^a   Reaves, Barbara J ^a   Mima, Joji ^b   O'Brien, Kevin M ^a   Starai, Vincent J ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LEGC3 PROTEIN; RAB PROTEIN; SNARE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL VACUOLE; COMPLEX FORMATION; CONTROLLED STUDY; LEGIONELLA PNEUMOPHILA; LYSOSOME; MEMBRANE FUSION; NONHUMAN; SACCHAROMYCES CEREVISIAE;

BACTERIAL PROTEINS; GENE EXPRESSION; LEGIONELLA PNEUMOPHILA; LYSOSOMES; MEMBRANE FUSION; MUTATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; SACCHAROMYCES CEREVISIAE; SNARE PROTEINS; VACUOLES;

EID: 84874223215     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056798     Document Type: Article

References (93)

1. Baumert M, Maycox PR, Navone F, De Camilli P, Jahn R, (1989) Synaptobrevin: an integral membrane protein of 18,000 daltons present in small synaptic vesicles of rat brain. EMBO J 8: 379-384.
2. Trimble WS, Cowan DM, Scheller RH, (1988) VAMP-1: a synaptic vesicle-associated integral membrane protein. Proc Natl Acad Sci U S A 85: 4538-4542.
3. Goud B, Salminen A, Walworth NC, Novick PJ, (1988) A GTP-binding protein required for secretion rapidly associates with secretory vesicles and the plasma membrane in yeast. Cell 53: 753-768.
4. Walworth NC, Goud B, Kabcenell AK, Novick PJ, (1989) Mutational analysis of SEC4 suggests a cyclical mechanism for the regulation of vesicular traffic. EMBO J 8: 1685-1693.
5. Banta LM, Vida TA, Herman PK, Emr SD, (1990) Characterization of yeast Vps33p, a protein required for vacuolar protein sorting and vacuole biogenesis. Mol Cell Biol 10: 4638-4649.
6. Hata Y, Slaughter CA, Sudhof TC, (1993) Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin. Nature 366: 347-351.
7. Pevsner J, Hsu SC, Braun JE, Calakos N, Ting AE, et al. (1994) Specificity and regulation of a synaptic vesicle docking complex. Neuron 13: 353-361.
8. Wada Y, Kitamoto K, Kanbe T, Tanaka K, Anraku Y, (1990) The SLP1 gene of Saccharomyces cerevisiae is essential for vacuolar morphogenesis and function. Mol Cell Biol 10: 2214-2223.
9. Cao X, Ballew N, Barlowe C, (1998) Initial docking of ER-derived vesicles requires Uso1p and Ypt1p but is independent of SNARE proteins. EMBO J 17: 2156-2165.
10. Christoforidis S, McBride HM, Burgoyne RD, Zerial M, (1999) The Rab5 effector EEA1 is a core component of endosome docking. Nature 397: 621-625.
11. Block MR, Glick BS, Wilcox CA, Wieland FT, Rothman JE, (1988) Purification of an N-ethylmaleimide-sensitive protein catalyzing vesicular transport. Proc Natl Acad Sci U S A 85: 7852-7856.
12. Clary DO, Griff IC, Rothman JE, (1990) SNAPs, a family of NSF attachment proteins involved in intracellular membrane fusion in animals and yeast. Cell 61: 709-721.
13. Malhotra V, Orci L, Glick BS, Block MR, Rothman JE, (1988) Role of an N-ethylmaleimide-sensitive transport component in promoting fusion of transport vesicles with cisternae of the Golgi stack. Cell 54: 221-227.
14. Weidman PJ, Melancon P, Block MR, Rothman JE, (1989) Binding of an N-ethylmaleimide-sensitive fusion protein to Golgi membranes requires both a soluble protein(s) and an integral membrane receptor. J Cell Biol 108: 1589-1596.
15. Haas A, Wickner W, (1996) Homotypic vacuole fusion requires Sec17p (yeast alpha-SNAP) and Sec18p (yeast NSF). EMBO J 15: 3296-3305.
16. Mayer A, Wickner W, Haas A, (1996) Sec18p (NSF)-driven release of Sec17p (alpha-SNAP) can precede docking and fusion of yeast vacuoles. Cell 85: 83-94.
17. Christoforidis S, Miaczynska M, Ashman K, Wilm M, Zhao L, et al. (1999) Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat Cell Biol 1: 249-252.
18. Lin RC, Scheller RH, (1997) Structural organization of the synaptic exocytosis core complex. Neuron 19: 1087-1094.
19. Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M, et al. (1998) SNAREpins: minimal machinery for membrane fusion. Cell 92: 759-772.
20. Nichols BJ, Ungermann C, Pelham HR, Wickner WT, Haas A, (1997) Homotypic vacuolar fusion mediated by t- and v-SNAREs. Nature 387: 199-202.
21. Ungermann C, Sato K, Wickner W, (1998) Defining the functions of trans-SNARE pairs. Nature 396: 543-548.
22. Miaczynska M, Zerial M, (2002) Mosaic organization of the endocytic pathway. Exp Cell Res 272: 8-14.
23. Wang L, Seeley ES, Wickner W, Merz AJ, (2002) Vacuole fusion at a ring of vertex docking sites leaves membrane fragments within the organelle. Cell 108: 357-369.
24. Lang T, Bruns D, Wenzel D, Riedel D, Holroyd P, et al. (2001) SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J 20: 2202-2213.
25. Vogel JP, Andrews HL, Wong SK, Isberg RR, (1998) Conjugative transfer by the virulence system of Legionella pneumophila. Science 279: 873-876.
26. Burstein D, Zusman T, Degtyar E, Viner R, Segal G, et al. (2009) Genome-scale identification of Legionella pneumophila effectors using a machine learning approach. PLoS Pathog 5: e1000508.
27. Campodonico EM, Chesnel L, Roy CR, (2005) A yeast genetic system for the identification and characterization of substrate proteins transferred into host cells by the Legionella pneumophila Dot/Icm system. Mol Microbiol 56: 918-933.
28. Heidtman M, Chen EJ, Moy MY, Isberg RR, (2009) Large-scale identification of Legionella pneumophila Dot/Icm substrates that modulate host cell vesicle trafficking pathways. Cell Microbiol 11: 230-248.
29. Luo ZQ, Isberg RR, (2004) Multiple substrates of the Legionella pneumophila Dot/Icm system identified by interbacterial protein transfer. Proc Natl Acad Sci U S A 101: 841-846.
30. Ninio S, Zuckman-Cholon DM, Cambronne ED, Roy CR, (2005) The Legionella IcmS-IcmW protein complex is important for Dot/Icm-mediated protein translocation. Mol Microbiol 55: 912-926.
31. Horwitz MA, (1983) The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J Exp Med 158: 2108-2126.
32. Horwitz MA, (1983) Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J Exp Med 158: 1319-1331.
33. Nash TW, Libby DM, Horwitz MA, (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.
34. Abu Kwaik Y, (1996) The phagosome containing Legionella pneumophila within the protozoan Hartmannella vermiformis is surrounded by the rough endoplasmic reticulum. Appl Environ Microbiol 62: 2022-2028.
35. Clemens DL, Lee BY, Horwitz MA, (2000) Deviant expression of Rab5 on phagosomes containing the intracellular pathogens Mycobacterium tuberculosis and Legionella pneumophila is associated with altered phagosomal fate. Infect Immun 68: 2671-2684.
36. Fernandez-Moreira E, Helbig JH, Swanson MS, (2006) Membrane vesicles shed by Legionella pneumophila inhibit fusion of phagosomes with lysosomes. Infect Immun 74: 3285-3295.
37. Roy CR, Berger KH, Isberg RR, (1998) Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol Microbiol 28: 663-674.
38. Arasaki K, Roy CR, (2010) Legionella pneumophila promotes functional interactions between plasma membrane syntaxins and Sec22b. Traffic 11: 587-600.
39. Goody RS, Muller MP, Schoebel S, Oesterlin LK, Blumer J, et al. (2011) The versatile Legionella effector protein DrrA. Commun Integr Biol 4: 72-74.
40. Ingmundson A, Delprato A, Lambright DG, Roy CR, (2007) Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature 450: 365-369.
41. Siggers KA, Lesser CF, (2008) The Yeast Saccharomyces cerevisiae: a versatile model system for the identification and characterization of bacterial virulence proteins. Cell Host Microbe 4: 8-15.
42. de Felipe KS, Glover RT, Charpentier X, Anderson OR, Reyes M, et al. (2008) Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog 4: e1000117.
43. Wickner W, (2010) Membrane fusion: five lipids, four SNAREs, three chaperones, two nucleotides, and a Rab, all dancing in a ring on yeast vacuoles. Annu Rev Cell Dev Biol 26: 115-136.
44. Seeley ES, Kato M, Margolis N, Wickner W, Eitzen G, (2002) Genomic analysis of homotypic vacuole fusion. Mol Biol Cell 13: 782-794.
45. Jones EW, (2002) Vacuolar proteases and proteolytic artifacts in Saccharomyces cerevisiae. Methods Enzymol 351: 127-150.
46. Haas A, Conradt B, Wickner W, (1994) G-protein ligands inhibit in vitro reactions of vacuole inheritance. J Cell Biol 126: 87-97.
47. Haas A, (1995) A quantitative assay to measure homotypic fusion in vitro. Methods Cell Sci 17: 283-294.
48. Slusarewicz P, Xu Z, Seefeld K, Haas A, Wickner WT, (1997) I2B is a small cytosolic protein that participates in vacuole fusion. Proc Natl Acad Sci U S A 94: 5582-5587.
49. Schwartz ML, Merz AJ, (2009) Capture and release of partially zipped trans-SNARE complexes on intact organelles. J Cell Biol 185: 535-549.
50. Starai VJ, Jun Y, Wickner W, (2007) Excess vacuolar SNAREs drive lysis and Rab bypass fusion. Proc Natl Acad Sci U S A 104: 13551-13558.
51. Wang L, Merz AJ, Collins KM, Wickner W, (2003) Hierarchy of protein assembly at the vertex ring domain for yeast vacuole docking and fusion. J Cell Biol 160: 365-374.
52. Jun Y, Thorngren N, Starai VJ, Fratti RA, Collins K, et al. (2006) Reversible, cooperative reactions of yeast vacuole docking. EMBO J 25: 5260-5269.
53. Albert S, Will E, Gallwitz D, (1999) Identification of the catalytic domains and their functionally critical arginine residues of two yeast GTPase-activating proteins specific for Ypt/Rab transport GTPases. EMBO J 18: 5216-5225.
54. Starai VJ, Hickey CM, Wickner W, (2008) HOPS proofreads the trans-SNARE complex for yeast vacuole fusion. Mol Biol Cell 19: 2500-2508.
55. Starai VJ, Jun Y, Wickner W, (2007) Excess vacuolar SNAREs drive lysis and Rab bypass fusion. Proc Natl Acad Sci U S A 104: 13551-13558.
56. Li J, Xu H, Bentley WE, Rao G, (2002) Impediments to secretion of green fluorescent protein and its fusion from Saccharomyces cerevisiae. Biotechnology progress 18: 831-838.
57. Merz AJ, Wickner WT, (2004) Trans-SNARE interactions elicit Ca2+ efflux from the yeast vacuole lumen. J Cell Biol 164: 195-206.
58. Mima J, Hickey CM, Xu H, Jun Y, Wickner W, (2008) Reconstituted membrane fusion requires regulatory lipids, SNAREs and synergistic SNARE chaperones. EMBO J 27: 2031-2042.
59. Price A, Seals D, Wickner W, Ungermann C, (2000) The docking stage of yeast vacuole fusion requires the transfer of proteins from a cis-SNARE complex to a Rab/Ypt protein. J Cell Biol 148: 1231-1238.
60. Banuelos MG, Moreno DE, Olson DK, Nguyen Q, Ricarte F, et al. (2010) Genomic analysis of severe hypersensitivity to hygromycin B reveals linkage to vacuolar defects and new vacuolar gene functions in Saccharomyces cerevisiae. Curr Genet 56: 121-137.
61. Webb GC, Hoedt M, Poole LJ, Jones EW, (1997) Genetic interactions between a pep7 mutation and the PEP12 and VPS45 genes: evidence for a novel SNARE component in transport between the Saccharomyces cerevisiae Golgi complex and endosome. Genetics 147: 467-478.
62. Paumet F, Wesolowski J, Garcia-Diaz A, Delevoye C, Aulner N, et al. (2009) Intracellular bacteria encode inhibitory SNARE-like proteins. PLoS One 4: e7375.
63. Hackstadt T, Scidmore-Carlson MA, Shaw EI, Fischer ER, (1999) The Chlamydia trachomatis IncA protein is required for homotypic vesicle fusion. Cell Microbiol 1: 119-130.
64. Delevoye C, Nilges M, Dehoux P, Paumet F, Perrinet S, et al. (2008) SNARE protein mimicry by an intracellular bacterium. PLoS Pathog 4: e1000022.
65. Cheever ML, Kutateladze TG, Overduin M, (2006) Increased mobility in the membrane targeting PX domain induced by phosphatidylinositol 3-phosphate. Protein Sci 15: 1873-1882.
66. Thorngren N, Collins KM, Fratti RA, Wickner W, Merz AJ, (2004) A soluble SNARE drives rapid docking, bypassing ATP and Sec17/18p for vacuole fusion. EMBO J 23: 2765-2776.
67. Xu Z, Wickner W, (1996) Thioredoxin is required for vacuole inheritance in Saccharomyces cerevisiae. J Cell Biol 132: 787-794.
68. Collins KM, Wickner WT, (2007) Trans-SNARE complex assembly and yeast vacuole membrane fusion. Proc Natl Acad Sci U S A 104: 8755-8760.
69. Stroupe C, Collins KM, Fratti RA, Wickner W, (2006) Purification of active HOPS complex reveals its affinities for phosphoinositides and the SNARE Vam7p. EMBO J 25: 1579-1589.
70. Merz AJ, Wickner WT, (2004) Resolution of organelle docking and fusion kinetics in a cell-free assay. Proc Natl Acad Sci U S A 101: 11548-11553.
71. Sutton RB, Fasshauer D, Jahn R, Brunger AT, (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395: 347-353.
72. Fasshauer D, Sutton RB, Brunger AT, Jahn R, (1998) Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc Natl Acad Sci U S A 95: 15781-15786.
73. Katz L, Brennwald P, (2000) Testing the 3Q:1R "rule": mutational analysis of the ionic "zero" layer in the yeast exocytic SNARE complex reveals no requirement for arginine. Mol Biol Cell 11: 3849-3858.
74. Fratti RA, Collins KM, Hickey CM, Wickner W, (2007) Stringent 3Q.1R composition of the SNARE 0-layer can be bypassed for fusion by compensatory SNARE mutation or by lipid bilayer modification. J Biol Chem 282: 14861-14867.
75. Struck DK, Hoekstra D, Pagano RE, (1981) Use of resonance energy transfer to monitor membrane fusion. Biochemistry 20: 4093-4099.
76. Mima J, Wickner W, (2009) Complex lipid requirements for SNARE- and SNARE chaperone-dependent membrane fusion. J Biol Chem 284: 27114-27122.
77. Mima J, Wickner W, (2009) Phosphoinositides and SNARE chaperones synergistically assemble and remodel SNARE complexes for membrane fusion. Proc Natl Acad Sci U S A 106: 16191-16196.
78. Scott BL, Van Komen JS, Irshad H, Liu S, Wilson KA, et al. (2004) Sec1p directly stimulates SNARE-mediated membrane fusion in vitro. J Cell Biol 167: 75-85.
79. Shen J, Tareste DC, Paumet F, Rothman JE, Melia TJ, (2007) Selective activation of cognate SNAREpins by Sec1/Munc18 proteins. Cell 128: 183-195.
80. Stroupe C, Hickey CM, Mima J, Burfeind AS, Wickner W, (2009) Minimal membrane docking requirements revealed by reconstitution of Rab GTPase-dependent membrane fusion from purified components. Proc Natl Acad Sci U S A 106: 17626-17633.
81. Buchmeier NA, Heffron F, (1991) Inhibition of macrophage phagosome-lysosome fusion by Salmonella typhimurium. Infect Immun 59: 2232-2238.
82. Scidmore MA, Fischer ER, Hackstadt T, (2003) Restricted fusion of Chlamydia trachomatis vesicles with endocytic compartments during the initial stages of infection. Infect Immun 71: 973-984.
83. Kaiser CA, Preuss D, Grisafi P, Botstein D, (1987) Many random sequences functionally replace the secretion signal sequence of yeast invertase. Science 235: 312-317.
84. Rothman JE, (1994) Intracellular membrane fusion. Adv Second Messenger Phosphoprotein Res 29: 81-96.
85. Toonen RF, Verhage M, (2003) Vesicle trafficking: pleasure and pain from SM genes. Trends Cell Biol 13: 177-186.
86. Ivanov SS, Charron G, Hang HC, Roy CR, (2010) Lipidation by the host prenyltransferase machinery facilitates membrane localization of Legionella pneumophila effector proteins. J Biol Chem 285: 34686-34698.
87. Weber SS, Ragaz C, Reus K, Nyfeler Y, Hilbi H, (2006) Legionella pneumophila exploits PI(4)P to anchor secreted effector proteins to the replicative vacuole. PLoS Pathog 2: e46.
88. Hubber A, Roy CR, (2010) Modulation of host cell function by Legionella pneumophila type IV effectors. Annu Rev Cell Dev Biol 26: 261-283.
89. Collins KM, Thorngren NL, Fratti RA, Wickner WT, (2005) Sec17p and HOPS, in distinct SNARE complexes, mediate SNARE complex disruption or assembly for fusion. EMBO J 24: 1775-1786.
90. Gerrard SR, Mecklem AB, Stevens TH, (2000) The yeast endosomal t-SNARE, Pep12p, functions in the absence of its transmembrane domain. Traffic 1: 45-55.
91. Vida TA, Emr SD, (1995) A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol 128: 779-792.
92. von der Haar T, (2007) Optimized protein extraction for quantitative proteomics of yeasts. PLoS One 2: e1078.
93. Reese C, Heise F, Mayer A, (2005) Trans-SNARE pairing can precede a hemifusion intermediate in intracellular membrane fusion. Nature 436: 410-414.