A rab-centric perspective of bacterial pathogen-occupied vacuoles

Cell Host and Microbe

Volumn 14, Issue 3, 2013, Pages 256-268

  Sherwood, Racquel Kim ^a   Roy, Craig R ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CITICOLINE; ERBIUM; GUANOSINE TRIPHOSPHATE; RAB PROTEIN; SNARE PROTEIN; SYNTAXIN 1; SYNTAXIN 2;

BACTERIUM; BIOGENESIS; BRUCELLA; CARBOXY TERMINAL SEQUENCE; CELL VACUOLE; CHLAMYDIA; CHLAMYDIASIS; CONFORMATIONAL TRANSITION; COXIELLA BURNETII; DENDRITIC CELL; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HUMAN; HYDROLYSIS; LEGIONELLA PNEUMOPHILA; LOBAR PNEUMONIA; MACROPHAGE; MEMBRANE TRANSPORT; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEOTIDE BINDING SITE; PHAGOCYTOSIS; PRIORITY JOURNAL; Q FEVER; REVIEW; SALMONELLA ENTERICA; SECRETORY VESICLE; TUBERCULOSIS; TYPE III SECRETION SYSTEM; TYPE IV SECRETION SYSTEM;

BACTERIA (MICROORGANISMS);

BACTERIA; HOST-PATHOGEN INTERACTIONS; INCLUSION BODIES; MODELS, BIOLOGICAL; RAB GTP-BINDING PROTEINS; VACUOLES;

EID: 84883885084     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2013.08.010     Document Type: Review

References (143)

1. C.M. Alpuche Aranda, J.A. Swanson, W.P. Loomis, and S.I. Miller Salmonella typhimurium activates virulence gene transcription within acidified macrophage phagosomes Proc. Natl. Acad. Sci. USA 89 1992 10079 10083
2. M. Anitei, and B. Hoflack Bridging membrane and cytoskeleton dynamics in the secretory and endocytic pathways Nat. Cell Biol. 14 2012 11 19
3. K. Arasaki, and C.R. Roy Legionella pneumophila promotes functional interactions between plasma membrane syntaxins and Sec22b Traffic 11 2010 587 600
4. K. Arasaki, D.K. Toomre, and C.R. Roy The Legionella pneumophila effector DrrA is sufficient to stimulate SNARE-dependent membrane fusion Cell Host Microbe 11 2012 46 57
5. G.N. Arenas, A.S. Staskevich, A. Aballay, and L.S. Mayorga Intracellular trafficking of Brucella abortus in J774 macrophages Infect. Immun. 68 2000 4255 4263
6. M.A. Bakowski, V. Braun, G.Y. Lam, T. Yeung, W.D. Heo, T. Meyer, B.B. Finlay, S. Grinstein, and J.H. Brumell The phosphoinositide phosphatase SopB manipulates membrane surface charge and trafficking of the Salmonella-containing vacuole Cell Host Microbe 7 2010 453 462
7. F. Barr, and D.G. Lambright Rab GEFs and GAPs Curr. Opin. Cell Biol. 22 2010 461 470
8. P.A. Beare, S.D. Gilk, C.L. Larson, J. Hill, C.M. Stead, A. Omsland, D.C. Cockrell, D. Howe, D.E. Voth, and R.A. Heinzen Dot/Icm type IVB secretion system requirements for Coxiella burnetii growth in human macrophages MBio 2 2011 e00175-e11
9. W. Berón, M.G. Gutierrez, M. Rabinovitch, and M.I. Colombo Coxiella burnetii localizes in a Rab7-labeled compartment with autophagic characteristics Infect. Immun. 70 2002 5816 5821
10. J. Blümer, J. Rey, L. Dehmelt, T. Mazel, Y.W. Wu, P. Bastiaens, R.S. Goody, and A. Itzen RabGEFs are a major determinant for specific Rab membrane targeting J. Cell Biol. 200 2013 287 300
11. M.L. Boschiroli, S. Ouahrani-Bettache, V. Foulongne, S. Michaux-Charachon, G. Bourg, A. Allardet-Servent, C. Cazevieille, J.P. Liautard, M. Ramuz, and D. O'Callaghan The Brucella suis virB operon is induced intracellularly in macrophages Proc. Natl. Acad. Sci. USA 99 2002 1544 1549
12. E. Boucrot, T. Henry, J.P. Borg, J.P. Gorvel, and S. Méresse The intracellular fate of Salmonella depends on the recruitment of kinesin Science 308 2005 1174 1178
13. E. Brombacher, S. Urwyler, C. Ragaz, S.S. Weber, K. Kami, M. Overduin, and H. Hilbi Rab1 guanine nucleotide exchange factor SidM is a major phosphatidylinositol 4-phosphate-binding effector protein of Legionella pneumophila J. Biol. Chem. 284 2009 4846 4856
14. J.J. Bultema, A.L. Ambrosio, C.L. Burek, and S.M. Di Pietro BLOC-2, AP-3, and AP-1 proteins function in concert with Rab38 and Rab32 proteins to mediate protein trafficking to lysosome-related organelles J. Biol. Chem. 287 2012 19550 19563
15. M. Calero, C.Z. Chen, W. Zhu, N. Winand, K.A. Havas, P.M. Gilbert, C.G. Burd, and R.N. Collins Dual prenylation is required for Rab protein localization and function Mol. Biol. Cell 14 2003 1852 1867
16. V. Campanacci, S. Mukherjee, C.R. Roy, and J. Cherfils Structure of the Legionella effector AnkX reveals the mechanism of phosphocholine transfer by the FIC domain EMBO J. 32 2013 1469 1477
17. E.M. Campoy, F.C. Zoppino, and M.I. Colombo The early secretory pathway contributes to the growth of the Coxiella-replicative niche Infect. Immun. 79 2011 402 413
18. A. Capmany, and M.T. Damiani Chlamydia trachomatis intercepts Golgi-derived sphingolipids through a Rab14-mediated transport required for bacterial development and replication PLoS ONE 5 2010 e14084
19. K.L. Carey, H.J. Newton, A. Lührmann, and C.R. Roy The Coxiella burnetii Dot/Icm system delivers a unique repertoire of type IV effectors into host cells and is required for intracellular replication PLoS Pathog. 7 2011 e1002056
20. I. Cebrian, G. Visentin, N. Blanchard, M. Jouve, A. Bobard, C. Moita, J. Enninga, L.F. Moita, S. Amigorena, and A. Savina Sec22b regulates phagosomal maturation and antigen crosspresentation by dendritic cells Cell 147 2011 1355 1368
21. J. Celli, C. de Chastellier, D.-M. Franchini, J. Pizarro-Cerda, E. Moreno, and J.-P. Gorvel Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum J. Exp. Med. 198 2003 545 556
22. J. Celli, S.P. Salcedo, and J.P. Gorvel Brucella coopts the small GTPase Sar1 for intracellular replication Proc. Natl. Acad. Sci. USA 102 2005 1673 1678
23. E. Chaves-Olarte, C. Guzmán-Verri, S. Méresse, M. Desjardins, J. Pizarro-Cerdá, J. Badilla, J.P. Gorvel, and E. Moreno Activation of Rho and Rab GTPases dissociates Brucella abortus internalization from intracellular trafficking Cell. Microbiol. 4 2002 663 676
24. P. Chavrier, J.P. Gorvel, E. Stelzer, K. Simons, J. Gruenberg, and M. Zerial Hypervariable C-terminal domain of rab proteins acts as a targeting signal Nature 353 1991 769 772
25. C. Chen, S. Banga, K. Mertens, M.M. Weber, I. Gorbaslieva, Y. Tan, Z.Q. Luo, and J.E. Samuel Large-scale identification and translocation of type IV secretion substrates by Coxiella burnetii Proc. Natl. Acad. Sci. USA 107 2010 21755 21760
26. Y. Chen, I. Tascón, M.R. Neunuebel, C. Pallara, J. Brady, L.N. Kinch, J. Fernández-Recio, A.L. Rojas, M.P. Machner, and A. Hierro Structural basis for Rab1 de-AMPylation by the Legionella pneumophila effector SidD PLoS Pathog. 9 2013 e1003382
27. J. Cherfils, and M. Zeghouf Regulation of small GTPases by GEFs, GAPs, and GDIs Physiol. Rev. 93 2013 269 309
28. D.L. Clemens, B.Y. Lee, and M.A. Horwitz Deviant expression of Rab5 on phagosomes containing the intracellular pathogens Mycobacterium tuberculosis and Legionella pneumophila is associated with altered phagosomal fate Infect. Immun. 68 2000 2671 2684
29. D.R. Clifton, K.A. Fields, S.S. Grieshaber, C.A. Dooley, E.R. Fischer, D.J. Mead, R.A. Carabeo, and T. Hackstadt A chlamydial type III translocated protein is tyrosine-phosphorylated at the site of entry and associated with recruitment of actin Proc. Natl. Acad. Sci. USA 101 2004 10166 10171
30. C. Cortes, K.A. Rzomp, A. Tvinnereim, M.A. Scidmore, and B. Wizel Chlamydia pneumoniae inclusion membrane protein Cpn0585 interacts with multiple Rab GTPases Infect. Immun. 75 2007 5586 5596
31. M. de Barsy, A. Jamet, D. Filopon, C. Nicolas, G. Laloux, J.F. Rual, A. Muller, J.C. Twizere, B. Nkengfac, and J. Vandenhaute Identification of a Brucella spp. secreted effector specifically interacting with human small GTPase Rab2 Cell. Microbiol. 13 2011 1044 1058
32. I. Derré, and R.R. Isberg Legionella pneumophila replication vacuole formation involves rapid recruitment of proteins of the early secretory system Infect. Immun. 72 2004 3048 3053
33. I. Derré, M. Pypaert, A. Dautry-Varsat, and H. Agaisse RNAi screen in Drosophila cells reveals the involvement of the Tom complex in Chlamydia infection PLoS Pathog. 3 2007 1446 1458
34. I. Derré, R. Swiss, and H. Agaisse The lipid transfer protein CERT interacts with the Chlamydia inclusion protein IncD and participates to ER-Chlamydia inclusion membrane contact sites PLoS Pathog. 7 2011 e1002092
35. N. Dong, Y. Zhu, Q. Lu, L. Hu, Y. Zheng, and F. Shao Structurally distinct bacterial TBC-like GAPs link Arf GTPase to Rab1 inactivation to counteract host defenses Cell 150 2012 1029 1041
36. R.A. Edwards, G.J. Olsen, and S.R. Maloy Comparative genomics of closely related salmonellae Trends Microbiol. 10 2002 94 99
37. C.A. Elwell, A. Ceesay, J.H. Kim, D. Kalman, and J.N. Engel RNA interference screen identifies Abl kinase and PDGFR signaling in Chlamydia trachomatis entry PLoS Pathog. 4 2008 e1000021
38. C.A. Elwell, S. Jiang, J.H. Kim, A. Lee, T. Wittmann, K. Hanada, P. Melancon, and J.N. Engel Chlamydia trachomatis co-opts GBF1 and CERT to acquire host sphingomyelin for distinct roles during intracellular development PLoS Pathog. 7 2011 e1002198
39. A.W. Ensminger, and R.R. Isberg Legionella pneumophila Dot/Icm translocated substrates: a sum of parts Curr. Opin. Microbiol. 12 2009 67 73
40. G.D. Fairn, and S. Grinstein How nascent phagosomes mature to become phagolysosomes Trends Immunol. 33 2012 397 405
41. K.A. Fields, and T. Hackstadt The chlamydial inclusion: escape from the endocytic pathway Annu. Rev. Cell Dev. Biol. 18 2002 221 245
42. C.L. Francis, T.A. Ryan, B.D. Jones, S.J. Smith, and S. Falkow Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria Nature 364 1993 639 642
43. D.W. Fraser, T.R. Tsai, W. Orenstein, W.E. Parkin, H.J. Beecham, R.G. Sharrar, J. Harris, G.F. Mallison, S.M. Martin, and J.E. McDade Legionnaires' disease: description of an epidemic of pneumonia N. Engl. J. Med. 297 1977 1189 1197
44. R.A. Fratti, J. Chua, I. Vergne, and V. Deretic Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest Proc. Natl. Acad. Sci. USA 100 2003 5437 5442
45. E. Fugier, S.P. Salcedo, C. de Chastellier, M. Pophillat, A. Muller, V. Arce-Gorvel, P. Fourquet, and J.P. Gorvel The glyceraldehyde-3-phosphate dehydrogenase and the small GTPase Rab 2 are crucial for Brucella replication PLoS Pathog. 5 2009 e1000487
46. J.E. Galán Salmonella interactions with host cells: type III secretion at work Annu. Rev. Cell Dev. Biol. 17 2001 53 86
47. E. Galanis, D.M. Lo Fo Wong, M.E. Patrick, N. Binsztein, A. Cieslik, T. Chalermchikit, A. Aidara-Kane, A. Ellis, F.J. Angulo, H.C. Wegener World Health Organization Global Salm-Surv Web-based surveillance and global Salmonella distribution, 2000-2002 Emerg. Infect. Dis. 12 2006 381 388
48. F. Garcia-del Portillo, and B.B. Finlay Targeting of Salmonella typhimurium to vesicles containing lysosomal membrane glycoproteins bypasses compartments with mannose 6-phosphate receptors J. Cell Biol. 129 1995 81 97
49. P. Glaziou, D. Falzon, K. Floyd, and M. Raviglione Global epidemiology of tuberculosis Semin. Respir. Crit. Care Med. 34 2013 3 16
50. R.S. Goody, A. Rak, and K. Alexandrov The structural and mechanistic basis for recycling of Rab proteins between membrane compartments Cell. Mol. Life Sci. 62 2005 1657 1670
51. M.B. Goren, P. D'Arcy Hart, M.R. Young, and J.A. Armstrong Prevention of phagosome-lysosome fusion in cultured macrophages by sulfatides of Mycobacterium tuberculosis Proc. Natl. Acad. Sci. USA 73 1976 2510 2514
52. M.G. Gutierrez, C.L. Vázquez, D.B. Munafó, F.C. Zoppino, W. Berón, M. Rabinovitch, and M.I. Colombo Autophagy induction favours the generation and maturation of the Coxiella-replicative vacuoles Cell. Microbiol. 7 2005 981 993
53. M. Hamasaki, N. Furuta, A. Matsuda, A. Nezu, A. Yamamoto, N. Fujita, H. Oomori, T. Noda, T. Haraguchi, and Y. Hiraoka Autophagosomes form at ER-mitochondria contact sites Nature 495 2013 389 393
54. L.D. Hernandez, K. Hueffer, M.R. Wenk, and J.E. Galán Salmonella modulates vesicular traffic by altering phosphoinositide metabolism Science 304 2004 1805 1807
55. M. Horn Chlamydiae as symbionts in eukaryotes Annu. Rev. Microbiol. 62 2008 113 131
56. M.A. Horwitz Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes J. Exp. Med. 158 1983 1319 1331
57. M.A. Horwitz The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes J. Exp. Med. 158 1983 2108 2126
58. D. Howe, J. Melnicákova, I. Barák, and R.A. Heinzen Fusogenicity of the Coxiella burnetii parasitophorous vacuole Ann. N Y Acad. Sci. 990 2003 556 562
59. A. Hubber, and C.R. Roy Modulation of host cell function by Legionella pneumophila type IV effectors Annu. Rev. Cell Dev. Biol. 26 2010 261 283
60. A.H. Hutagalung, and P.J. Novick Role of Rab GTPases in membrane traffic and cell physiology Physiol. Rev. 91 2011 119 149
61. A. Ingmundson, A. Delprato, D.G. Lambright, and C.R. Roy Legionella pneumophila proteins that regulate Rab1 membrane cycling Nature 450 2007 365 369
62. E. Itakura, C. Kishi-Itakura, and N. Mizushima The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes Cell 151 2012 1256 1269
63. S. Jean, and A.A. Kiger Coordination between RAB GTPase and phosphoinositide regulation and functions Nat. Rev. Mol. Cell Biol. 13 2012 463 470
64. T.J. Jewett, E.R. Fischer, D.J. Mead, and T. Hackstadt Chlamydial TARP is a bacterial nucleator of actin Proc. Natl. Acad. Sci. USA 103 2006 15599 15604
65. J.C. Kagan, and C.R. Roy Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites Nat. Cell Biol. 4 2002 945 954
66. J.C. Kagan, M.P. Stein, M. Pypaert, and C.R. Roy Legionella subvert the functions of Rab1 and Sec22b to create a replicative organelle J. Exp. Med. 199 2004 1201 1211
67. B. Kasmapour, A. Gronow, C.K. Bleck, W. Hong, and M.G. Gutierrez Size-dependent mechanism of cargo sorting during lysosome-phagosome fusion is controlled by Rab34 Proc. Natl. Acad. Sci. USA 109 2012 20485 20490
68. D. Kostrewa, A. D'Arcy, B. Takacs, and M. Kamber Crystal structures of Streptococcus pneumoniae N-acetylglucosamine-1-phosphate uridyltransferase, GlmU, in apo form at 2.33 A resolution and in complex with UDP-N- acetylglucosamine and Mg(2+) at 1.96 A resolution J. Mol. Biol. 305 2001 279 289
69. B. Ku, K.H. Lee, W.S. Park, C.S. Yang, J. Ge, S.G. Lee, S.S. Cha, F. Shao, W. Do Heo, J.U. Jung, and B.H. Oh VipD of Legionella pneumophila targets activated Rab5 and Rab22 to interfere with endosomal trafficking in macrophages PLoS Pathog. 8 2012 e1003082
70. C. Kuijl, M. Pilli, S.K. Alahari, H. Janssen, P.S. Khoo, K.E. Ervin, M. Calero, S. Jonnalagadda, R.H. Scheller, J. Neefjes, and J.R. Junutula Rac and Rab GTPases dual effector Nischarin regulates vesicle maturation to facilitate survival of intracellular bacteria EMBO J. 32 2013 713 727
71. G.B. Kyei, I. Vergne, J. Chua, E. Roberts, J. Harris, J.R. Junutula, and V. Deretic Rab14 is critical for maintenance of Mycobacterium tuberculosis phagosome maturation arrest EMBO J. 25 2006 5250 5259
72. Z. Lifshitz, D. Burstein, M. Peeri, T. Zusman, K. Schwartz, H.A. Shuman, T. Pupko, and G. Segal Computational modeling and experimental validation of the Legionella and Coxiella virulence-related type-IVB secretion signal Proc. Natl. Acad. Sci. USA 110 2013 E707 E715
73. Z.Q. Luo Legionella secreted effectors and innate immune responses Cell. Microbiol. 14 2012 19 27
74. S. Lyons, L. Wang, J.E. Casanova, S.V. Sitaraman, D. Merlin, and A.T. Gewirtz Salmonella typhimurium transcytoses flagellin via an SPI2-mediated vesicular transport pathway J. Cell Sci. 117 2004 5771 5780
75. M.P. Machner, and R.R. Isberg Targeting of host Rab GTPase function by the intravacuolar pathogen Legionella pneumophila Dev. Cell 11 2006 47 56
76. G.V. Mallo, M. Espina, A.C. Smith, M.R. Terebiznik, A. Alemán, B.B. Finlay, L.E. Rameh, S. Grinstein, and J.H. Brumell SopB promotes phosphatidylinositol 3-phosphate formation on Salmonella vacuoles by recruiting Rab5 and Vps34 J. Cell Biol. 182 2008 741 752
77. M. Maurin, and D. Raoult Q fever Clin. Microbiol. Rev. 12 1999 518 553
78. J.A. McDonough, H.J. Newton, S. Klum, R. Swiss, H. Agaisse, and C.R. Roy Host pathways important for Coxiella burnetii infection revealed by genome-wide RNA interference screening MBio 4 2013 e00606 e00612
79. K. McGourty, T.L. Thurston, S.A. Matthews, L. Pinaud, L.J. Mota, and D.W. Holden Salmonella inhibits retrograde trafficking of mannose-6-phosphate receptors and lysosome function Science 338 2012 963 967
80. E. Mihai Gazdag, A. Streller, I. Haneburger, H. Hilbi, I.R. Vetter, R.S. Goody, and A. Itzen Mechanism of Rab1b deactivation by the Legionella pneumophila GAP LepB EMBO Rep. 14 2013 199 205
81. E. Mizuno-Yamasaki, F. Rivera-Molina, and P. Novick GTPase networks in membrane traffic Annu. Rev. Biochem. 81 2012 637 659
82. S. Mukherjee, X. Liu, K. Arasaki, J. McDonough, J.E. Galán, and C.R. Roy Modulation of Rab GTPase function by a protein phosphocholine transferase Nature 477 2011 103 106
83. M.P. Müller, H. Peters, J. Blümer, W. Blankenfeldt, R.S. Goody, and A. Itzen The Legionella effector protein DrrA AMPylates the membrane traffic regulator Rab1b Science 329 2010 946 949
84. T. Murata, A. Delprato, A. Ingmundson, D.K. Toomre, D.G. Lambright, and C.R. Roy The Legionella pneumophila effector protein DrrA is a Rab1 guanine nucleotide-exchange factor Nat. Cell Biol. 8 2006 971 977
85. H. Nagai, J.C. Kagan, X. Zhu, R.A. Kahn, and C.R. Roy A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes Science 295 2002 679 682
86. M.R. Neunuebel, Y. Chen, A.H. Gaspar, P.S. Backlund Jr., A. Yergey, and M.P. Machner De-AMPylation of the small GTPase Rab1 by the pathogen Legionella pneumophila Science 333 2011 453 456
87. H.J. Newton, J.A. McDonough, and C.R. Roy Effector protein translocation by the Coxiella burnetii Dot/Icm type IV secretion system requires endocytic maturation of the pathogen-occupied vacuole PLoS ONE 8 2013 e54566
88. B. Nkengfac, J. Pouyez, E. Bauwens, J. Vandenhaute, J.J. Letesson, J. Wouters, and X. De Bolle Structural analysis of Brucella abortus RicA substitutions that do not impair interaction with human Rab2 GTPase BMC Biochem. 13 2012 16
89. F.A. Norris, M.P. Wilson, T.S. Wallis, E.E. Galyov, and P.W. Majerus SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase Proc. Natl. Acad. Sci. USA 95 1998 14057 14059
90. P. Novick, and M. Zerial The diversity of Rab proteins in vesicle transport Curr. Opin. Cell Biol. 9 1997 496 504
91. D. O'Callaghan, C. Cazevieille, A. Allardet-Servent, M.L. Boschiroli, G. Bourg, V. Foulongne, P. Frutos, Y. Kulakov, and M. Ramuz A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretion systems is essential for intracellular survival of Brucella suis Mol. Microbiol. 33 1999 1210 1220
92. X. Pan, A. Lührmann, A. Satoh, M.A. Laskowski-Arce, and C.R. Roy Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors Science 320 2008 1651 1654
93. X. Pan, A. Lührmann, A. Satoh, M.A. Laskowski-Arce, and C.R. Roy Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors Science 320 2008 1651 1654
94. J.C. Patel, and J.E. Galán Manipulation of the host actin cytoskeleton by Salmonella - all in the name of entry Curr. Opin. Microbiol. 8 2005 10 15
95. J.C. Patel, K. Hueffer, T.T. Lam, and J.E. Galán Diversification of a Salmonella virulence protein function by ubiquitin-dependent differential localization Cell 137 2009 283 294
96. J.B. Pereira-Leal, and M.C. Seabra The mammalian Rab family of small GTPases: definition of family and subfamily sequence motifs suggests a mechanism for functional specificity in the Ras superfamily J. Mol. Biol. 301 2000 1077 1087
97. N. Perskvist, K. Roberg, A. Kulyté, and O. Stendahl Rab5a GTPase regulates fusion between pathogen-containing phagosomes and cytoplasmic organelles in human neutrophils J. Cell Sci. 115 2002 1321 1330
98. J. Pizarro-Cerdá, S. Méresse, R.G. Parton, G. van der Goot, A. Sola-Landa, I. Lopez-Goñi, E. Moreno, and J.P. Gorvel Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes Infect. Immun. 66 1998 5711 5724
99. I.D. Pokrovskaya, J.W. Szwedo, A. Goodwin, T.V. Lupashina, U.M. Nagarajan, and V.V. Lupashin Chlamydia trachomatis hijacks intra-Golgi COG complex-dependent vesicle trafficking pathway Cell. Microbiol. 14 2012 656 668
100. C.R. Raetz, and S.L. Roderick A left-handed parallel beta helix in the structure of UDP-N-acetylglucosamine acyltransferase Science 270 1995 997 1000
101. A. Rejman Lipinski, J. Heymann, C. Meissner, A. Karlas, V. Brinkmann, T.F. Meyer, and D. Heuer Rab6 and Rab11 regulate Chlamydia trachomatis development and golgin-84-dependent Golgi fragmentation PLoS Pathog. 5 2009 e1000615
102. E.A. Roberts, J. Chua, G.B. Kyei, and V. Deretic Higher order Rab programming in phagolysosome biogenesis J. Cell Biol. 174 2006 923 929
103. P.S. Romano, M.G. Gutierrez, W. Berón, M. Rabinovitch, and M.I. Colombo The autophagic pathway is actively modulated by phase II Coxiella burnetii to efficiently replicate in the host cell Cell. Microbiol. 9 2007 891 909
104. V. Roux, M. Bergoin, N. Lamaze, and D. Raoult Reassessment of the taxonomic position of Rickettsiella grylli Int. J. Syst. Bacteriol. 47 1997 1255 1257
105. C.R. Roy, K.H. Berger, and R.R. Isberg Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake Mol. Microbiol. 28 1998 663 674
106. K.A. Rzomp, L.D. Scholtes, B.J. Briggs, G.R. Whittaker, and M.A. Scidmore Rab GTPases are recruited to chlamydial inclusions in both a species-dependent and species-independent manner Infect. Immun. 71 2003 5855 5870
107. K.A. Rzomp, A.R. Moorhead, and M.A. Scidmore The GTPase Rab4 interacts with Chlamydia trachomatis inclusion membrane protein CT229 Infect. Immun. 74 2006 5362 5373
108. D. Salomon, and K. Orth What Pathogens Have Taught Us about Posttranslational Modifications Cell Host & Microbe 14 2013 269 279 this issue
109. S. Schoebel, L.K. Oesterlin, W. Blankenfeldt, R.S. Goody, and A. Itzen RabGDI displacement by DrrA from Legionella is a consequence of its guanine nucleotide exchange activity Mol. Cell 36 2009 1060 1072
110. S. Schoebel, A.L. Cichy, R.S. Goody, and A. Itzen Protein LidA from Legionella is a Rab GTPase supereffector Proc. Natl. Acad. Sci. USA 108 2011 17945 17950
111. G. Segal Identification of legionella effectors using bioinformatic approaches Methods Mol. Biol. 954 2013 595 602
112. G. Segal, M. Feldman, and T. Zusman The Icm/Dot type-IV secretion systems of Legionella pneumophila and Coxiella burnetii FEMS Microbiol. Rev. 29 2005 65 81
113. R. Seshadri, I.T. Paulsen, J.A. Eisen, T.D. Read, K.E. Nelson, W.C. Nelson, N.L. Ward, H. Tettelin, T.M. Davidsen, and M.J. Beanan Complete genome sequence of the Q-fever pathogen Coxiella burnetii Proc. Natl. Acad. Sci. USA 100 2003 5455 5460
114. S. Seto, K. Tsujimura, and Y. Koide Rab GTPases regulating phagosome maturation are differentially recruited to mycobacterial phagosomes Traffic 12 2011 407 420
115. J.E. Shea, M. Hensel, C. Gleeson, and D.W. Holden Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium Proc. Natl. Acad. Sci. USA 93 1996 2593 2597
116. N. Shohdy, J.A. Efe, S.D. Emr, and H.A. Shuman Pathogen effector protein screening in yeast identifies Legionella factors that interfere with membrane trafficking Proc. Natl. Acad. Sci. USA 102 2005 4866 4871
117. U. Sivars, D. Aivazian, and S.R. Pfeffer Yip3 catalyses the dissociation of endosomal Rab-GDI complexes Nature 425 2003 856 859
118. A.C. Smith, W.D. Heo, V. Braun, X. Jiang, C. Macrae, J.E. Casanova, M.A. Scidmore, S. Grinstein, T. Meyer, and J.H. Brumell A network of Rab GTPases controls phagosome maturation and is modulated by Salmonella enterica serovar Typhimurium J. Cell Biol. 176 2007 263 268
119. S. Spanò, and J.E. Galán A Rab32-dependent pathway contributes to Salmonella typhi host restriction Science 338 2012 960 963
120. S. Spanò, J.E. Ugalde, and J.E. Galán Delivery of a Salmonella Typhi exotoxin from a host intracellular compartment Cell Host Microbe 3 2008 30 38
121. S. Spanò, X. Liu, and J.E. Galán Proteolytic targeting of Rab29 by an effector protein distinguishes the intracellular compartments of human-adapted and broad-host Salmonella Proc. Natl. Acad. Sci. USA 108 2011 18418 18423
122. T. Starr, T.W. Ng, T.D. Wehrly, L.A. Knodler, and J. Celli Brucella intracellular replication requires trafficking through the late endosomal/lysosomal compartment Traffic 9 2008 678 694
123. M.A. Stein, K.Y. Leung, M. Zwick, F. Garcia-del Portillo, and B.B. Finlay Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells Mol. Microbiol. 20 1996 151 164
124. H. Stenmark Rab GTPases as coordinators of vesicle traffic Nat. Rev. Mol. Cell Biol. 10 2009 513 525
125. H. Stenmark, A. Valencia, O. Martinez, O. Ullrich, B. Goud, and M. Zerial Distinct structural elements of rab5 define its functional specificity EMBO J. 13 1994 575 583
126. H.Y. Suh, D.W. Lee, K.H. Lee, B. Ku, S.J. Choi, J.S. Woo, Y.G. Kim, and B.H. Oh Structural insights into the dual nucleotide exchange and GDI displacement activity of SidM/DrrA EMBO J. 29 2010 496 504
127. Y. Tan, and Z.Q. Luo Legionella pneumophila SidD is a deAMPylase that modifies Rab1 Nature 475 2011 506 509
128. Y. Tan, R.J. Arnold, and Z.Q. Luo Legionella pneumophila regulates the small GTPase Rab1 activity by reversible phosphorylcholination Proc. Natl. Acad. Sci. USA 108 2011 21212 21217
129. M.R. Terebiznik, O.V. Vieira, S.L. Marcus, A. Slade, C.M. Yip, W.S. Trimble, T. Meyer, B.B. Finlay, and S. Grinstein Elimination of host cell PtdIns(4,5)P(2) by bacterial SigD promotes membrane fission during invasion by Salmonella Nat. Cell Biol. 4 2002 766 773
130. E.J. Tisdale, and M.R. Jackson Rab2 protein enhances coatomer recruitment to pre-Golgi intermediates J. Biol. Chem. 273 1998 17269 17277
131. R.H. Valdivia Chlamydia effector proteins and new insights into chlamydial cellular microbiology Curr. Opin. Microbiol. 11 2008 53 59
132. R.H. Valdivia, and S. Falkow Fluorescence-based isolation of bacterial genes expressed within host cells Science 277 1997 2007 2011
133. P. van der Sluijs, M. Hull, P. Webster, P. Mâle, B. Goud, and I. Mellman The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway Cell 70 1992 729 740
134. I. Vergne, J. Chua, H.H. Lee, M. Lucas, J. Belisle, and V. Deretic Mechanism of phagolysosome biogenesis block by viable Mycobacterium tuberculosis Proc. Natl. Acad. Sci. USA 102 2005 4033 4038
135. L.E. Via, D. Deretic, R.J. Ulmer, N.S. Hibler, L.A. Huber, and V. Deretic Arrest of mycobacterial phagosome maturation is caused by a block in vesicle fusion between stages controlled by rab5 and rab7 J. Biol. Chem. 272 1997 13326 13331
136. O.V. Vieira, R.E. Harrison, C.C. Scott, H. Stenmark, D. Alexander, J. Liu, J. Gruenberg, A.D. Schreiber, and S. Grinstein Acquisition of Hrs, an essential component of phagosomal maturation, is impaired by mycobacteria Mol. Cell. Biol. 24 2004 4593 4604
137. K. von Bargen, J.P. Gorvel, and S.P. Salcedo Internal affairs: investigating the Brucella intracellular lifestyle FEMS Microbiol. Rev. 36 2012 533 562
138. D.E. Voth, and R.A. Heinzen Lounging in a lysosome: the intracellular lifestyle of Coxiella burnetii Cell. Microbiol. 9 2007 829 840
139. A.H. Williams, R.M. Immormino, D.T. Gewirth, and C.R.H. Raetz Structure of UDP-N-acetylglucosamine acyltransferase with a bound antibacterial pentadecapeptide Proc. Natl. Acad. Sci. USA 103 2006 10877 10882
140. M.L. Yarbrough, and K. Orth AMPylation is a new post-translational modiFICation Nat. Chem. Biol. 5 2009 378 379
141. Q. Yu, L. Hu, Q. Yao, Y. Zhu, N. Dong, D.C. Wang, and F. Shao Structural analyses of Legionella LepB reveal a new GAP fold that catalytically mimics eukaryotic RasGAP Cell Res. 23 2013 775 787
142. M. Zerial, and H. McBride Rab proteins as membrane organizers Nat. Rev. Mol. Cell Biol. 2 2001 107 117
143. Y. Zhu, L. Hu, Y. Zhou, Q. Yao, L. Liu, and F. Shao Structural mechanism of host Rab1 activation by the bifunctional Legionella type IV effector SidM/DrrA Proc. Natl. Acad. Sci. USA 107 2010 4699 4704