Secretive Bacterial Pathogens and the Secretory Pathway

Traffic

Volumn 13, Issue 9, 2012, Pages 1187-1197

  Hilbi, Hubert ^a   Haas, Albert ^b  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

Brucella; Chlamydia; Endosomal pathway; Golgi apparatus; Legionella; Pathogen vacuole; Salmonella; Secretory pathway; Type III secretion system; Type IV secretion system; Vesicle trafficking

Indexed keywords

PHOSPHATIDYLINOSITIDE; RAB PROTEIN; SNARE PROTEIN;

ALPHA HELIX; ARTICLE; BACTERIUM; BRUCELLA ABORTUS; BRUCELLA MELITENSIS; CELL COMPARTMENTALIZATION; CELL COMPOSITION; CELL MIGRATION; CELL SELECTION; CELL VACUOLE; CHLAMYDIA TRACHOMATIS; CHLAMYDOPHILA PNEUMONIAE; ENDOPLASMIC RETICULUM; ENDOSOME; LEGIONELLA PNEUMOPHILA; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SECRETORY PATHWAY; TRANS GOLGI NETWORK;

ANIMALS; BACTERIAL PROTEINS; BRUCELLA; CHLAMYDIA; ENDOSOMES; EUKARYOTIC CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; LEGIONELLA; PROTEIN TRANSPORT; SALMONELLA; SECRETORY PATHWAY;

EID: 84865154655     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2012.01344.x     Document Type: Article

References (110)

1. Lee MC, Miller EA, Goldberg J, Orci L, Schekman R. Bi-directional protein transport between the ER and Golgi. Annu Rev Cell Dev Biol 2004;20:87-123.
2. Lord C, Bhandari D, Menon S, Ghassemian M, Nycz D, Hay J, Ghosh P, Ferro-Novick S. Sequential interactions with Sec23 control the direction of vesicle traffic. Nature 2011;473:181-186.
3. Roy CR, Salcedo SP, Gorvel JP. Pathogen-endoplasmic-reticulum interactions: in through the out door. Nat Rev Immunol 2006;6:136-147.
4. Hickey CM, Wickner W. HOPS initiates vacuole docking by tethering membranes before trans-SNARE complex assembly. Mol Biol Cell 2010;21:2297-2305.
5. Jahn R, Scheller RH. SNAREs - engines for membrane fusion. Nat Rev Mol Cell Biol 2006;7:631-643.
6. Jensen D, Schekman R. COPII-mediated vesicle formation at a glance. J Cell Sci 2011;124:1-4.
7. De Matteis MA, Luini A. Exiting the Golgi complex. Nat Rev Mol Cell Biol 2008;9:273-284.
8. Johannes L, Popoff V. Tracing the retrograde route in protein trafficking. Cell 2008;135:1175-1187.
9. Di Paolo G, De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature 2006;443:651-657.
10. Cosio G, Grinstein S. Analysis of phospho-inositide dynamics during phagocytosis using genetically encoded fluorescent biosensors. Methods Mol Biol 2008;445:287-300.
11. Dowler S, Kular G, Alessi DR. Protein lipid overlay assay. Sci STKE 2002;2002:PL6.
12. 2 on the Golgi complex. Nat Cell Biol 1999;1:280-287.
13. Minogue S, Waugh MG, De Matteis MA, Stephens DJ, Berditchevski F, Hsuan JJ. Phosphatidylinositol 4-kinase is required for endosomal trafficking and degradation of the EGF receptor. J Cell Sci 2006;119:571-581.
14. Graham TR, Burd CG. Coordination of Golgi functions by phosphatidylinositol 4-kinases. Trends Cell Biol 2011;21:113-121.
15. Lowe M. Structure and function of the Lowe syndrome protein OCRL1. Traffic 2005;6:711-719.
16. Liu Y, Boukhelifa M, Tribble E, Morin-Kensicki E, Uetrecht A, Bear JE, Bankaitis VA. The Sac1 phosphoinositide phosphatase regulates Golgi membrane morphology and mitotic spindle organization in mammals. Mol Biol Cell 2008;19:3080-3096.
17. Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001;2:107-117.
18. Jones DH, Morris JB, Morgan CP, Kondo H, Irvine RF, Cockcroft S. Type I phosphatidyl-inositol 4-phosphate 5-kinase directly interacts with ADP-ribosylation factor 1 and is responsible for phosphatidylinositol 4, 5-bisphosphate synthesis in the Golgi compartment. J Biol Chem 2000;275:13962-13966.
19. Shin HW, Nakayama K. Dual control of membrane targeting by PtdIns(4)P and ARF. Trends Biochem Sci 2004;29:513-515.
20. Behnia R, Munro S. Organelle identity and the signposts for membrane traffic. Nature 2005;438:597-604.
21. Simonsen A, Lippe R, Christoforidis S, Gaullier JM, Brech A, Callaghan J, Toh BH, Murphy C, Zerial M, Stenmark H. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 1998;394:494-498.
22. Godi A, Di Campli A, Konstantakopoulos A, Di Tullio G, Alessi DR, Kular GS, Daniele T, Marra P, Lucocq JM, De Matteis MA. FAPPs control Golgi-to-cell-surface membrane traffic by binding to ARF and PtdIns(4)P. Nat Cell Biol 2004;6:393-404.
23. Natarajan P, Liu K, Patil DV, Sciorra VA, Jackson CL, Graham TR. Regulation of a Golgi flippase by phosphoinositides and an ArfGEF. Nat Cell Biol 2009;11:1421-1426.
24. de Graaf P, Zwart WT, van Dijken RA, Deneka M, Schulz TK, Geijsen N, Coffer PJ, Gadella BM, Verkleij AJ, van der Sluijs P, van Bergen en Henegouwen PM. Phosphatidylinositol 4-kinase beta is critical for functional association of Rab11 with the Golgi complex. Mol Biol Cell 2004;15:2038-2047.
25. Mayinger P. Regulation of Golgi function via phosphoinositide lipids. Semin Cell Dev Biol 2009;20:793-800.
26. Newton HJ, Ang DK, van Driel IR, Hartland EL. Molecular pathogenesis of infections caused by Legionella pneumophila. Clin Microbiol Rev 2010;23:274-298.
27. Hilbi H, Hoffmann C, Harrison CF. Legionella spp. outdoors: colonization, communication and persistence. Environ Microbiol Rep 2011;3:286-296.
28. Tiaden A, Spirig T, Hilbi H. Bacterial gene regulation by alpha-hydroxyketone signaling. Trends Microbiol 2010;18:288-297.
29. Isberg RR, O'Connor TJ, Heidtman M. The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat Rev Microbiol 2009;7:13-24.
30. Urwyler S, Nyfeler Y, Ragaz C, Lee H, Mueller LN, Aebersold R, Hilbi H. Proteome analysis of Legionella vacuoles purified by magnetic immunoseparation reveals secretory and endosomal GTPases. Traffic 2009;10:76-87.
31. Shevchuk O, Batzilla C, Hagele S, Kusch H, Engelmann S, Hecker M, Haas A, Heuner K, Glöckner G, Steinert M. Proteomic analysis of Legionella-containing phagosomes isolated from Dictyostelium. Int J Med Microbiol 2009;299:489-508.
32. Hubber A, Roy CR. Modulation of host cell function by Legionella pneumophila type IV effectors. Annu Rev Cell Dev Biol 2010;26:261-283.
33. 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.
34. Hilbi H, Weber S, Finsel I. Anchors for effectors: subversion of phosphoinositide lipids by Legionella. Front Microbiol 2011;2:91.
35. 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.
36. Brombacher E, Urwyler S, Ragaz C, Weber SS, Kami K, Overduin M, Hilbi H. Rab1 guanine nucleotide exchange factor SidM is a major phosphatidylinositol 4-phosphate-binding effector protein of Legionella pneumophila. J Biol Chem 2009;284:4846-4856.
37. Schoebel S, Blankenfeldt W, Goody RS, Itzen A. High-affinity binding of phosphatidylinositol 4-phosphate by Legionella pneumophila DrrA. EMBO Rep 2010;11:598-604.
38. Weber SS, Ragaz C, Hilbi H. The inositol polyphosphate 5-phosphatase OCRL1 restricts intracellular growth of Legionella, localizes to the replicative vacuole and binds to the bacterial effector LpnE. Cell Microbiol 2009;11:442-460.
39. 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.
40. Machner MP, Isberg RR. Targeting of host Rab GTPase function by the intravacuolar pathogen Legionella pneumophila. Dev Cell 2006;11:47-56.
41. Machner MP, Isberg RR. A bifunctional bacterial protein links GDI displacement to Rab1 activation. Science 2007;318:974-977.
42. Schoebel S, Oesterlin LK, Blankenfeldt W, Goody RS, Itzen A. RabGDI displacement by DrrA from Legionella is a consequence of its guanine nucleotide exchange activity. Mol Cell 2009;36:1060-1072.
43. Ingmundson A, Delprato A, Lambright DG, Roy CR. Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature 2007;450:365-369.
44. Müller MP, Peters H, Blumer J, Blankenfeldt W, Goody RS, Itzen A. The Legionella effector protein DrrA AMPylates the membrane traffic regulator Rab1b. Science 2010;329:946-949.
45. Mukherjee S, Liu X, Arasaki K, McDonough J, Galan JE, Roy CR. Modulation of Rab GTPase function by a protein phosphocholine transferase. Nature 2011;477:103-106.
46. Tan Y, Luo ZQ. Legionella pneumophila SidD is a deAMPylase that modifies Rab1. Nature 2011;475:506-509.
47. Neunuebel MR, Chen Y, Gaspar AH, Backlund PS Jr, Yergey A, Machner MP. De-AMPylation of the small GTPase Rab1 by the pathogen Legionella pneumophila. Science 2011;333:453-456.
48. Pan X, Lührmann A, Satoh A, Laskowski-Arce MA, Roy CR. Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors. Science 2008;320:1651-1654.
49. Tan Y, Arnold RJ, Luo ZQ. Legionella pneumophila regulates the small GTPase Rab1 activity by reversible phosphoryl-cholination. Proc Natl Acad Sci U S A 2011;108:21212-21217.
50. Schoebel S, Cichy AL, Goody RS, Itzen A. Protein LidA from Legionella is a Rab GTPase supereffector. Proc Natl Acad Sci U S A 2011;108:17945-17950.
51. Neunuebel MR, Mohammadi S, Jarnik M, Machner MP. Legionella pneumophila LidA affects nucleotide binding and activity of the host GTPase Rab1. J Bacteriol 2012;194:1389-1400. Epub ahead of print; doi: 10.1128/JB.06306-11.
52. Kagan JC, Roy CR. Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat Cell Biol 2002;4:945-954.
53. 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.
54. Arasaki K, Roy CR. Legionella pneumophila promotes functional interactions between plasma membrane syntaxins and Sec22b. Traffic 2010;11:587-600.
55. Arasaki K, Toomre DK, Roy CR. The Legionella pneumophila effector DrrA Is sufficient to stimulate SNARE-dependent membrane fusion. Cell Host Microbe 2012;11:46-57.
56. 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.
57. Paumet F, Wesolowski J, Garcia-Diaz A, Delevoye C, Aulner N, Shuman HA, Subtil A, Rothman JE. Intracellular bacteria encode inhibitory SNARE-like proteins. PLoS One 2009;4:e7375.
58. Liu Y, Luo ZQ. The Legionella pneumophila effector SidJ is required for efficient recruitment of endoplasmic reticulum proteins to the bacterial phagosome. Infect Immun 2007;75:592-603.
59. Celli J, Gorvel JP. Organelle robbery: Brucella interactions with the endoplasmic reticulum. Curr Opin Microbiol 2004;7:93-97.
60. Celli J, de Chastellier C, Franchini DM, Pizarro-Cerda J, Moreno E, Gorvel JP. Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum. J Exp Med 2003;198:545-556.
61. Delrue RM, Martinez-Lorenzo M, Lestrate P, Danese I, Bielarz V, Mertens P, De Bolle X, Tibor A, Gorvel JP, Letesson JJ. Identification of Brucella spp. genes involved in intracellular trafficking. Cell Microbiol 2001;3:487-497.
62. Comerci DJ, Martinez-Lorenzo MJ, Sieira R, Gorvel JP, Ugalde RA. Essential role of the VirB machinery in the maturation of the Brucella abortus-containing vacuole. Cell Microbiol 2001;3:159-168.
63. de Jong MF, Sun YH, den Hartigh AB, van Dijl JM, Tsolis RM. Identification of VceA and VceC, two members of the VjbR regulon that are translocated into macrophages by the Brucella type IV secretion system. Mol Microbiol 2008;70:1378-1396.
64. Marchesini MI, Herrmann CK, Salcedo SP, Gorvel JP, Comerci DJ. In search of Brucella abortus type IV secretion substrates: screening and identification of four proteins translocated into host cells through VirB system. Cell Microbiol 2011;13:1261-1274.
65. de Barsy M, Jamet A, Filopon D, Nicolas C, Laloux G, Rual JF, Muller A, Twizere JC, Nkengfac B, Vandenhaute J, Hill DE, Salcedo SP, Gorvel JP, Letesson JJ, De Bolle X. Identification of a Brucella spp. secreted effector specifically interacting with human small GTPase Rab2. Cell Microbiol 2011;13:1044-1058.
66. Fugier E, Salcedo SP, de Chastellier C, Pophillat M, Muller A, Arce-Gorvel V, Fourquet P, Gorvel JP. The glyceraldehyde-3-phosphate dehydrogenase and the small GTPase Rab 2 are crucial for Brucella replication. PLoS Pathog 2009;5:e1000487.
67. Starr T, Ng TW, Wehrly TD, Knodler LA, Celli J. Brucella intracellular replication requires trafficking through the late endosomal/ lysosomal compartment. Traffic 2008;9:678-694.
68. Celli J, Salcedo SP, Gorvel JP. Brucella coopts the small GTPase Sar1 for intracellular replication. Proc Natl Acad Sci U S A 2005;102:1673-1678.
69. Qin QM, Pei J, Ancona V, Shaw BD, Ficht TA, de Figueiredo P. RNAi screen of endoplasmic reticulum-associated host factors reveals a role for IRE1alpha in supporting Brucella replication. PLoS Pathog 2008;4:e1000110.
70. Horn M. Chlamydiae as symbionts in eukaryotes. Annu Rev Microbiol 2008;62:113-131.
71. Muschiol S, Bailey L, Gylfe A, Sundin C, Hultenby K, Bergstrom S, Elofsson M, Wolf-Watz H, Normark S, Henriques-Normark B. A small-molecule inhibitor of type III secretion inhibits different stages of the infectious cycle of Chlamydia trachomatis. Proc Natl Acad Sci U S A 2006;103:14566-14571.
72. Wolf K, Betts HJ, Chellas-Gery B, Hower S, Linton CN, Fields KA. Treatment of Chlamydia trachomatis with a small molecule inhibitor of the Yersinia type III secretion system disrupts progression of the chlamydial developmental cycle. Mol Microbiol 2006;61:1543-1555.
73. Rockey DD, Grosenbach D, Hruby DE, Peacock MG, Heinzen RA, Hackstadt T. Chlamydia psittaci IncA is phosphorylated by the host cell and is exposed on the cytoplasmic face of the developing inclusion. Mol Microbiol 1997;24:217-228.
74. Subtil A, Delevoye C, Balana ME, Tastevin L, Perrinet S, Dautry-Varsat A. A directed screen for chlamydial proteins secreted by a type III mechanism identifies a translocated protein and numerous other new candidates. Mol Microbiol 2005;56:1636-1647.
75. Subtil A, Parsot C, Dautry-Varsat A. Secretion of predicted Inc proteins of Chlamydia pneumoniae by a heterologous type III machinery. Mol Microbiol 2001;39:792-800.
76. Hackstadt T, Scidmore-Carlson MA, Shaw EI, Fischer ER. The Chlamydia trachomatis IncA protein is required for homotypic vesicle fusion. Cell Microbiol 1999;1:119-130.
77. Delevoye C, Nilges M, Dehoux P, Paumet F, Perrinet S, Dautry-Varsat A, Subtil A. SNARE protein mimicry by an intracellular bacterium. PLoS Pathog 2008;4:e1000022.
78. Derre I, Swiss R, Agaisse H. The lipid transfer protein CERT interacts with the Chlamydia inclusion protein IncD and participates to ER-Chlamydia inclusion membrane contact sites. PLoS Pathog 2011;7:e1002092.
79. Elwell CA, Jiang S, Kim JH, Lee A, Wittmann T, Hanada K, Melancon P, Engel JN. Chlamydia trachomatis co-opts GBF1 and CERT to acquire host sphingomyelin for distinct roles during intracellular development. PLoS Pathog 2011;7:e1002198.
80. Scidmore MA, Hackstadt T. Mammalian 14-3-3 beta associates with the Chlamydia trachomatis inclusion membrane via its interaction with IncG. Mol Microbiol 2001;39:1638-1650.
81. Verbeke P, Welter-Stahl L, Ying S, Hansen J, Hacker G, Darville T, Ojcius DM. Recruitment of BAD by the Chlamydia trachomatis vacuole correlates with host-cell survival. PLoS Pathog 2006;2:e45.
82. Rzomp KA, Moorhead AR, Scidmore MA. The GTPase Rab4 interacts with Chlamydia trachomatis inclusion membrane protein CT229. Infect Immun 2006;74:5362-5373.
83. Cortes C, Rzomp KA, Tvinnereim A, Scidmore MA, Wizel B. Chlamydia pneumoniae inclusion membrane protein Cpn0585 interacts with multiple Rab GTPases. Infect Immun 2007;75:5586-5596.
84. Hackstadt T, Scidmore MA, Rockey DD. Lipid metabolism in Chlamydia trachomatis-infected cells: directed trafficking of Golgi-derived sphingolipids to the chlamydial inclusion. Proc Natl Acad Sci U S A 1995;92:4877-4881.
85. Hackstadt T, Rockey DD, Heinzen RA, Scidmore MA. Chlamydia trachomatis interrupts an exocytic pathway to acquire endogenously synthesized sphingomyelin in transit from the Golgi apparatus to the plasma membrane. EMBO J 1996;15:964-977.
86. Heuer D, Rejman Lipinski A, Machuy N, Karlas A, Wehrens A, Siedler F, Brinkmann V, Meyer TF. Chlamydia causes fragmentation of the Golgi compartment to ensure reproduction. Nature 2009;457:731-735.
87. Christian JG, Heymann J, Paschen SA, Vier J, Schauenburg L, Rupp J, Meyer TF, Hacker G, Heuer D. Targeting of a chlamydial protease impedes intracellular bacterial growth. PLoS Pathog 2011;7:e1002283.
88. Rejman Lipinski A, Heymann J, Meissner C, Karlas A, Brinkmann V, Meyer TF, Heuer D. Rab6 and Rab11 regulate Chlamydia trachomatis development and golgin-84-dependent Golgi fragmentation. PLoS Pathog 2009;5:e1000615.
89. Rzomp KA, Scholtes LD, Briggs BJ, Whittaker GR, Scidmore MA. Rab GTPases are recruited to chlamydial inclusions in both a species-dependent and species-independent manner. Infect Immun 2003;71:5855-5870.
90. Moorhead AM, Jung JY, Smirnov A, Kaufer S, Scidmore MA. Multiple host proteins that function in phosphatidylinositol-4 phosphate metabolism are recruited to the chlamydial inclusion. Infect Immun 2010;78:1990-2007.
91. Steele-Mortimer O. The Salmonella-containing vacuole: moving with the times. Curr Opin Microbiol 2008;11:38-45.
92. Kuhle V, Abrahams GL, Hensel M. Intracellular Salmonella enterica redirect exocytic transport processes in a Salmonella pathogenicity island 2-dependent manner. Traffic 2006;7:716-730.
93. Schroeder N, Mota LJ, Meresse S. Salmonella-induced tubular networks. Trends Microbiol 2011;19:268-277.
94. Mota LJ, Ramsden AE, Liu M, Castle JD, Holden DW. SCAMP3 is a component of the Salmonella-induced tubular network and reveals an interaction between bacterial effectors and post-Golgi trafficking. Cell Microbiol 2009;11:1236-1253.
95. Boucrot E, Henry T, Borg JP, Gorvel JP, Meresse S. The intracellular fate of Salmonella depends on the recruitment of kinesin. Science 2005;308:1174-1178.
96. Salcedo SP, Holden DW. SseG, a virulence protein that targets Salmonella to the Golgi network. EMBO J 2003;22:5003-5014.
97. Deiwick J, Salcedo SP, Boucrot E, Gilliland SM, Henry T, Petermann N, Waterman SR, Gorvel JP, Holden DW, Meresse S. The translocated Salmonella effector proteins SseF and SseG interact and are required to establish an intracellular replication niche. Infect Immun 2006;74:6965-6972.
98. Abrahams GL, Muller P, Hensel M. Functional dissection of SseF, a type III effector protein involved in positioning the Salmonella-containing vacuole. Traffic 2006;7:950-965.
99. Ramsden AE, Mota LJ, Munter S, Shorte SL, Holden DW. The SPI-2 type III secretion system restricts motility of Salmonella-containing vacuoles. Cell Microbiol 2007;9:2517-2529.
100. Van Engelenburg SB, Palmer AE. Imaging type-III secretion reveals dynamics and spatial segregation of Salmonella effectors. Nat Methods 2010;7:325-330.
101. Weber SS, Ragaz C, Hilbi H. Pathogen trafficking pathways and host phosphoinositide metabolism. Mol Microbiol 2009;71:1341-1352.
102. 2 by bacterial SigD promotes membrane fission during invasion by Salmonella. Nat Cell Biol 2002;4:766-773.
103. Bakowski MA, Braun V, Lam GY, Yeung T, Heo WD, Meyer T, Finlay BB, Grinstein S, Brumell JH. The phosphoinositide phosphatase SopB manipulates membrane surface charge and trafficking of the Salmonella-containing vacuole. Cell Host Microbe 2010;7:453-462.
104. Hernandez LD, Hueffer K, Wenk MR, Galan JE. Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 2004;304:1805-1807.
105. Bujny MV, Ewels PA, Humphrey S, Attar N, Jepson MA, Cullen PJ. Sorting nexin-1 defines an early phase of Salmonella-containing vacuole-remodeling during Salmonella infection. J Cell Sci 2008;121:2027-2036.
106. Braun V, Wong A, Landekic M, Hong WJ, Grinstein S, Brumell JH. Sorting nexin 3 (SNX3) is a component of a tubular endosomal network induced by Salmonella and involved in maturation of the Salmonella-containing vacuole. Cell Microbiol 2010;12:1352-1367.
107. Alvarez-Dominguez C, Barbieri AM, Beron W, Wandinger-Ness A, Stahl PD. Phagocytosed live Listeria monocytogenes influences Rab5-regulated in vitro phagosome-endosome fusion. J Biol Chem 1996;271:13834-13843.
108. Becken U, Jeschke A, Veltman K, Haas A. Cell-free fusion of bacteria-containing phagosomes with endocytic compartments. Proc Natl Acad Sci U S A 2010;107:20726-20731.
109. Rexach MF, Latterich M, Schekman RW. Characteristics of endoplasmic reticulum-derived transport vesicles. J Cell Biol 1994;126:1133-1148.
110. Balch WE, Glick BS, Rothman JE. Sequential intermediates in the pathway of intercompartmental transport in a cell-free system. Cell 1984;39:525-536.