Salmonella-containing vacuoles: Directing traffic and nesting to grow

Traffic

Volumn 9, Issue 12, 2008, Pages 2022-2031

  Bakowski, Malina A ^a,b   Braun, Virginie ^a   Brumell, John H ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Bacterial invasion; Endosome; Lysosome; Phosphoinositide; Rab GTPase; S. typhimurium; SopB; Type III secretion

Indexed keywords

BACTERIAL PROTEIN; CHOLESTEROL; GLYCOPROTEIN; MEVINOLIN; PROTEIN SOPB; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANTIGEN PRESENTATION; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL IMMUNITY; BACTERIAL INFECTION; BACTERIAL VIRULENCE; CELL MATURATION; CELL MIGRATION; CELL SECRETION; CELL VACUOLE; CELLULAR IMMUNITY; CHOLESTEROL SYNTHESIS; CYTOSKELETON; CYTOSOL; DENDRITIC CELL; DRUG MECHANISM; ENDOCYTOSIS; ENZYME INHIBITION; HUMAN; IMMUNE RESPONSE; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN TRANSPORT; REVIEW; SALMONELLA TYPHIMURIUM;

ANIMALS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CYTOSKELETON; ENDOCYTOSIS; HUMANS; SALMONELLA; VACUOLES;

EID: 56149108652     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2008.00827.x     Document Type: Review

References (93)

1. Hansen-Wester I, Hensel M. Salmonella pathogenicity islands encoding type III secretion systems. Microbes Infect 2001; 3: 549-559.
2. Lostroh CP, Lee CA. The Salmonella pathogenicity island-1 type III secretion system. Microbes Infect 2001; 3: 1281-1291.
3. Santos RL, Zhang S, Tsolis RM, Kingsley RA, Adams LG, Baumler AJ. Animal models of Salmonella infections: Enteritis versus typhoid fever. Microbes Infect 2001; 3: 1335-1344.
4. Wallis TS, Galyov EE. Molecular basis of Salmonella-induced enteritis. Mol Microbiol 2000; 36: 997-1005.
5. Hensel M. Salmonella pathogenicity island 2. Mol Microbiol 2000; 36: 1015-1023.
6. Waterman SR, Holden DW. Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol 2003; 5: 501-511.
7. Brawn LC, Hayward RD, Koronakis V. Salmonella SPI1 effector SipA persists after entry and cooperates with a SPI2 effector to regulate phagosome maturation and intracellular replication. Cell Host Microbe 2007; 1: 63-75.
8. Coburn B, Li Y, Owen D, Vallance BA, Finlay BB. Salmonella enterica serovar Typhimurium pathogenicity island 2 is necessary for complete virulence in a mouse model of infectious enterocolitis. Infect Immun 2005; 73: 3219-3227.
9. Hapfelmeier S, Hardt WD. A mouse model for S. typhimurium-induced enterocolitis. Trends Microbiol 2005; 13: 497-503.
10. Steele-Mortimer O, Brumell JH, Knodler LA, Meresse S, Lopez A, Finlay BB. The invasion-associated type III secretion system of Salmonella enterica serovar Typhimurium is necessary for intracellular proliferation and vacuole biogenesis in epithelial cells. Cell Microbiol 2002; 4: 43-54.
11. Wasylnka JA, Bakowski MA, Szeto J, Ohlson MB, Trimble WS, Miller SI, Brumell JH. Role for myosin II in regulating positioning of Salmonella-containing vacuoles and intracellular replication. Infect Immun 2008; 76: 2722-2735.
12. Steele-Mortimer O, Meresse S, Gorvel JP, Toh BH, Finlay BB. Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell Microbiol 1999; 1: 33-49.
13. Garcia-del Portillo F, Zwick MB, Leung KY, Finlay BB. Salmonella induces the formation of filamentous structures containing lysosomal membrane glycoproteins in epithelial cells. Proc Natl Acad Sci U S A 1993; 90: 10544-10548.
14. Garcia-del Portillo F, Zwick MB, Leung KY, Finlay BB. Intracellular replication of Salmonella within epithelial cells is associated with filamentous structures containing lysosomal membrane glycoproteins. Infect Agents Dis 1993; 2: 227-231.
15. Meresse S, Steele-Mortimer O, Finlay BB, Gorvel JP. The rab7 GTPase controls the maturation of Salmonella typhimurium-containing vacuoles in HeLa cells. EMBO J 1999; 18: 4394-4403.
16. Garcia-del Portillo F, Finlay BB. Targeting of Salmonella typhimurium to vesicles containing lysosomal membrane glycoproteins bypasses compartments with mannose 6-phosphate receptors. J Cell Biol 1995; 129: 81-97.
17. Brumell JH, Tang P, Mills SD, Finlay BB. Characterization of Salmonella-induced filaments (Sifs) reveals a delayed interaction between Salmonella-containing vacuoles and late endocytic compartments. Traffic 2001; 2: 643-653.
18. Rathman M, Barker LP, Falkow S. The unique trafficking pattern of Salmonella typhimurium-containing phagosomes in murine macrophages is independent of the mechanism of bacterial entry. Infect Immun 1997; 65: 1475-1485.
19. Garvis SG, Beuzon CR, Holden DW. A role for the PhoP/Q regulon in inhibition of fusion between lysosomes and Salmonella-containing vacuoles in macrophages. Cell Microbiol 2001; 3: 731-744.
20. Steele-Mortimer O. The Salmonella-containing vacuole: Moving with the times. Curr Opin Microbiol 2008; 11: 38-45.
21. Grosshans BL, Ortiz D, Novick P. Rabs and their effectors: Achieving specificity in membrane traffic. Proc Natl Acad Sci U S A 2006; 103: 11821-11827.
22. Smith AC, Heo WD, Braun V, Jiang X, Macrae C, Casanova JE, Scidmore MA, Grinstein S, Meyer T, Brumell JH. A network of Rab GTPases controls phagosome maturation and is modulated by Salmonella enterica serovar Typhimurium. J Cell Biol 2007; 176: 263-268.
23. 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.
24. Smith AC, Cirulis JT, Casanova JE, Scidmore MA, Brumell JH. Interaction of the Salmonella-containing vacuole with the endocytic recycling system. J Biol Chem 2005; 280: 24634-24641.
25. Heo WD, Inoue T, Park WS, Kim ML, Park BO, Wandless TJ, Meyer T. PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 2006; 314: 1458-1461.
26. Galyov EE, Wood MW, Rosqvist R, Mullan PB, Watson PR, Hedges S, Wallis TS. A secreted effector protein of Salmonella dublin is translocated into eukaryotic cells and mediates inflammation and fluid secretion in infected ileal mucosa. Mol Microbiol 1997; 25: 903-912.
27. Drecktrah D, Knodler LA, Galbraith K, Steele-Mortimer O. The Salmonella SPI1 effector SopB stimulates nitric oxide production long after invasion. Cell Microbiol 2005; 7: 105-113.
28. Marcus SL, Knodler LA, Finlay BB. Salmonella enterica serovar Typhimurium effector SigD/SopB is membrane-associated and ubiquitinated inside host cells. Cell Microbiol 2002; 4: 435-446.
29. Giacomodonato MN, Uzzau S, Bacciu D, Caccuri R, Sarnacki SH, Rubino S, Cerquetti MC. SipA, SopA, SopB, SopD and SopE2 effector proteins of Salmonella enterica serovar Typhimurium are synthesized at late stages of infection in mice. Microbiology 2007; 153: 1221-1228.
30. Lawley TD, Chan K, Thompson LJ, Kim CC, Govoni GR, Monack DM. Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog 2006; 2: E11.
31. Norris FA, Wilson MP, Wallis TS, Galyov EE, Majerus PW. SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc Natl Acad Sci U S A 1998; 95: 14057-14059.
32. Feng Y, Wente SR, Majerus PW. Overexpression of the inositol phosphatase SopB in human 293 cells stimulates cellular chloride influx and inhibits nuclear mRNA export. Proc Natl Acad Sci U S A 2001; 98: 875-879.
33. Zhou D, Chen LM, Hernandez L, Shears SB, Galan JE. A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol Microbiol 2001; 39: 248-259.
34. Mason D, Mallo GV, Terebiznik MR, Payrastre B, Finlay BB, Brumell JH, Rameh L, Grinstein S. Alteration of epithelial structure and function associated with PtdIns(4,5)P2 degradation by a bacterial phosphatase. J Gen Physiol 2007; 129: 267-283.
35. Terebiznik MR, Vieira OV, Marcus SL, Slade A, Yip CM, Trimble WS, Meyer T, Finlay BB, Grinstein S. Elimination of host cell PtdIns(4,5)P(2) by bacterial SigD promotes membrane fission during invasion by Salmonella. Nat Cell Biol 2002; 4: 766-773.
36. Mallo GV, Espina M, Smith AC, Terebiznik MR, Alemán A, Finlay BB, Rameh LE, Grinstein S, Brumell JH. SopB promotes phosphatidylinositol 3-phosphate formation on Salmonella vacuoles by recruiting Rab5 and Vps34. J Cell Biol 2008; 182: 741-752.
37. Knodler LA, Finlay BB, Steele-Mortimer O. The Salmonella effector protein SopB protects epithelial cells from apoptosis by sustained activation of Akt. J Biol Chem 2005; 280: 9058-9064.
38. Steele-Mortimer O, Knodler LA, Marcus SL, Scheid MP, Goh B, Pfeifer CG, Duronio V, Finlay BB. Activation of Akt/protein kinase B in epithelial cells by the Salmonella typhimurium effector sigD. J Biol Chem 2000; 275: 37718-37724.
39. Patel JC, Galan JE. Differential activation and function of Rho GTPases during Salmonella-host cell interactions. J Cell Biol 2006; 175: 453-463.
40. Friebel A, Ilchmann H, Aepfelbacher M, Ehrbar K, Machleidt W, Hardt WD. SopE and SopE2 from Salmonella typhimurium activate different sets of RhoGTPases of the host cell. J Biol Chem 2001; 276: 34035-34040.
41. Rogers LD, Kristensen AR, Boyle EC, Robinson DP, Ly RT, Finlay BB, Foster LJ. Identification of cognate host targets and specific ubiquitylation sites on the Salmonella SPI-1 effector SopB/SigD. J Proteomics 2008; 71: 97-108.
42. Hardt WD, Chen LM, Schuebel KE, Bustelo XR, Galan JE. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 1998; 93: 815-826.
43. Cain RJ, Hayward RD, Koronakis V. Deciphering interplay between Salmonella invasion effectors. PLoS Pathog 2008; 4: E1000037.
44. Pendaries C, Tronchere H, Arbibe L, Mounier J, Gozani O, Cantley L, Fry MJ, Gaits-lacovoni F, Sansonetti PJ, Payrastre B. PtdIns5P activates the host cell PI3-kinase/Akt pathway during Shigella flexneri infection. EMBO J 2006; 25: 1024-1034.
45. Hernandez LD, Hueffer K, Wenk MR, Galan JE. Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 2004; 304: 1805-1807.
46. Bakowski MA, Cirulis JT, Brown NF, Finlay BB, Brumell JH. SopD acts cooperatively with SopB during Salmonella enterica serovar Typhimurium invasion. Cell Microbiol 2007; 9: 2839-2855.
47. Yeung T, Grinstein S. Lipid signaling and the modulation of surface charge during phagocytosis. Immunol Rev 2007; 219: 17-36.
48. Dukes JD, Lee H, Hagen R, Reaves BJ, Layton AN, Galyov EE, Whitley P. The secreted Salmonella dublin phosphoinositide phosphatase, SopB, localizes to PtdIns(3)P-containing endosomes and perturbs normal endosome to lysosome trafficking. Biochem J 2006; 395: 239-247.
49. Kuijl C, Savage ND, Marsman M, Tuin AW, Janssen L, Egan DA, Ketema M, van den Nieuwendijk R, van den Eeden SJ, Geluk A, Poot A, van der Marel G, Beijersbergen RL, Overkleeft H, Ottenhoff TH, et al. Intracellular bacterial growth is controlled by a kinase network around PKB/AKT1. Nature 2007; 450: 725-730.
50. Meresse S, Unsworth KE, Habermann A, Griffiths G, Fang F, Martinez-Lorenzo MJ, Waterman SR, Gorvel JP, Holden DW. Remodelling of the actin cytoskeleton is essential for replication of intravacuolar Salmonella. Cell Microbiol 2001; 3: 567-577.
51. Miao EA, Brittnacher M, Haraga A, Jeng RL, Welch MD, Miller SI. Salmonella effectors translocated across the vacuolar membrane interact with the actin cytoskeleton. Mol Microbiol 2003; 48: 401-415.
52. Poh J, Odendall C, Spanos A, Boyle C, Liu M, Freemont P, Holden DW. SteC is a Salmonella kinase required for SPI-2-dependent F-actin remodelling. Cell Microbiol 2008; 10: 20-30.
53. Tezcan-Merdol D, Engstrand L, Rhen M. Salmonella enterica SpvB-mediated ADP-ribosylation as an activator for host cell actin degradation. Int J Med Microbiol 2005; 295: 201-212.
54. Tezcan-Merdol D, Nyman T, Lindberg U, Haag F, Koch-Nolte F, Rhen M. Actin is ADP-ribosylated by the Salmonella enterica virulence-associated protein SpvB. Mol Microbiol 2001; 39: 606-619.
55. Lesnick ML, Reiner NE, Fierer J, Guiney DG. The Salmonella spvB virulence gene encodes an enzyme that ADP-ribosylates actin and destabilizes the cytoskeleton of eukaryotic cells. Mol Microbiol 2001; 39: 1464-1470.
56. Brumell JH, Goosney DL, Finlay BB. SifA, a type III secreted effector of Salmonella typhimurium, directs Salmonella-induced filament (Sif) formation along microtubules. Traffic 2002; 3: 407-415.
57. 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.
58. Kuhle V, Jackel D, Hensel M. Effector proteins encoded by Salmonella pathogenicity island 2 interfere with the microtubule cytoskeleton after translocation into host cells. Traffic 2004; 5: 356-370.
59. Ramsden AE, Holden DW, Mota LJ. Membrane dynamics and spatial distribution of Salmonella-containing vacuoles. Trends Microbiol 2007; 15: 516-524.
60. Guignot J, Caron E, Beuzon C, Bucci C, Kagan J, Roy C, Holden DW. Microtubule motors control membrane dynamics of Salmonella-containing vacuoles. J Cell Sci 2004; 117: 1033-1045.
61. Harrison RE, Brumell JH, Khandani A, Bucci C, Scott CC, Jiang X, Finlay BB, Grinstein S. Salmonella impairs RILP recruitment to Rab7 during maturation of invasion vacuoles. Mol Biol Cell 2004; 15: 3146-3154.
62. Marsman M, Jordens I, Kuijl C, Janssen L, Neefjes J. Dynein-mediated vesicle transport controls intracellular Salmonella replication. Mol Biol Cell 2004; 15: 2954-2964.
63. 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.
64. Henry T, Couillault C, Rockenfeller P, Boucrot E, Dumont A, Schroeder N, Hermant A, Knodler LA, Lecine P, Steele-Mortimer O, Borg JP, Gorvel JP, Meresse S. The Salmonella effector protein PipB2 is a linker for kinesin-1. Proc Natl Acad Sci U S A 2006; 103: 13497-13502.
65. Hashim S, Mukherjee K, Raje M, Basu SK, Mukhopadhyay A. Live Salmonella modulate expression of Rab proteins to persist in a specialized compartment and escape transport to lysosomes. J Biol Chem 2000; 275: 16281-16288.
66. Ishibashi Y, Arai T. Specific inhibition of phagosome-lysosome fusion in murine macrophages mediated by Salmonella typhimurium infection. FEMS Microbiol Immunol 1990; 2: 35-43.
67. Buchmeier NA, Heffron F. Inhibition of macrophage phagosome-lysosome fusion by Salmonella typhimurium. Infect Immun 1991; 59: 2232-2238.
68. Carrol ME, Jackett PS, Aber VR, Lowrie DB. Phagolysosome formation, cyclic adenosine 3′:5′-monophosphate and the fate of Salmonella typhimurium within mouse peritoneal macrophages. J Gen Microbiol 1979; 110: 421-429.
69. Oh YK, Alpuche-Aranda C, Berthiaume E, Jinks T, Miller SI, Swanson JA. Rapid and complete fusion of macrophage lysosomes with phagosomes containing Salmonella typhimurium. Infect Immun 1996; 64: 3877-3883.
70. Drecktrah D, Knodler LA, Howe D, Steele-Mortimer O. Salmonella trafficking is defined by continuous dynamic interactions with the endolysosomal system. Traffic 2007; 8: 212-225.
71. Uchiya K, Barbieri MA, Funato K, Shah AH, Stahl PD, Groisman EA. A Salmonella virulence protein that inhibits cellular trafficking. EMBO J 1999; 18: 3924-3933.
72. Shotland Y, Kramer H, Groisman EA. The Salmonella SpiC protein targets the mammalian Hook3 protein function to alter cellular trafficking. Mol Microbiol 2003; 49: 1565-1576.
73. Walenta JH, Didier AJ, Liu X, Kramer H. The Golgi-associated hook3 protein is a member of a novel family of microtubule-binding proteins. J Cell Biol 2001; 152: 923-934.
74. Freeman JA, Rappl C, Kuhle V, Hensel M, Miller SI. SpiC is required for translocation of Salmonella pathogenicity island 2 effectors and secretion of translocon proteins SseB and SseC. J Bacteriol 2002; 184: 4971-4980.
75. Yu XJ, Ruiz-Albert J, Unsworth KE, Garvis S, Liu M, Holden DW. SpiC is required for secretion of Salmonella pathogenicity island 2 type III secretion system proteins. Cell Microbiol 2002; 4: 531-540.
76. 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.
77. Lombardi D, Soldati T, Riederer MA, Goda Y, Zerial M, Pfeffer SR. Rab9 functions in transport between late endosomes and the trans Golgi network. EMBO J 1993; 12: 677-682.
78. Catron DM, Sylvester MD, Lange Y, Kadekoppala M, Jones BD, Monack DM, Falkow S, Haldar K. The Salmonella-containing vacuole is a major site of intracellular cholesterol accumulation and recruits the GPI-anchored protein CD55. Cell Microbiol 2002; 4: 315-328.
79. Catron DM, Lange Y, Borensztajn J, Sylvester MD, Jones BD, Haldar K. Salmonella enterica serovar Typhimurium requires nonsterol precursors of the cholesterol biosynthetic pathway for intracellular proliferation. Infect Immun 2004; 72: 1036-1042.
80. Ohlson MB, Fluhr K, Birmingham CL, Brumell JH, Miller SI. SseJ deacylase activity by Salmonella enterica serovar Typhimurium promotes virulence in mice. Infect Immun 2005; 73: 6249-6259.
81. Nawabi P, Catron DM, Haldar K. Esterification of cholesterol by a type III secretion effector during intracellular Salmonella infection. Mol Microbiol 2008; 68: 173-185.
82. Cheminay C, Mohlenbrink A, Hensel M. Intracellular Salmonella inhibit antigen presentation by dendritic cells. J Immunol 2005; 174: 2892-2899.
83. Mitchell EK, Mastroeni P, Kelly AP, Trowsdale J. Inhibition of cell surface MHC class II expression by Salmonella. Eur J Immunol 2004; 34: 2559-2567.
84. Tobar JA, Carreno LJ, Bueno SM, Gonzalez PA, Mora JE, Quezada SA, Kalergis AM. Virulent Salmonella enterica serovar typhimurium evades adaptive immunity by preventing dendritic cells from activating T cells. Infect Immun 2006; 74: 6438-6448.
85. van der Velden AW, Dougherty JT, Starnbach MN. Down-modulation of TCR expression by Salmonella enterica serovar Typhimurium. J Immunol 2008; 180: 5569-5574.
86. van der Velden AW, Copass MK, Starnbach MN. Salmonella inhibit T cell proliferation by a direct, contact-dependent immunosuppressive effect. Proc Natl Acad Sci U S A 2005; 102: 17769-17774.
87. Schoehn G, Di Guilmi AM, Lemaire D, Attree I, Weissenhorn W, Dessen A. Oligomerization of type III secretion proteins PopB and PopD precedes pore formation in Pseudomonas. EMBO J 2003; 22: 4957-4967.
88. Viboud GI, Bliska JB. A bacterial type III secretion system inhibits actin polymerization to prevent pore formation in host cell membranes. EMBO J 2001; 20: 5373-5382.
89. Roy D, Liston DR, Idone VJ, Di A, Nelson DJ, Pujol C, Bliska JB, Chakrabarti S, Andrews NW. A process for controlling intracellular bacterial infections induced by membrane injury. Science 2004; 304: 1515-1518.
90. Birmingham CL, Smith AC, Bakowski MA, Yoshimori T, Brumell JH. Autophagy controls Salmonella infection in response to damage to the Salmonella-containing vacuole. J Biol Chem 2006; 281: 11374-11383.
91. Perrin AJ, Jiang X, Birmingham CL, So NS, Brumell JH. Recognition of bacteria in the cytosol of Mammalian cells by the ubiquitin system. Curr Biol 2004; 14: 806-811.
92. Beuzon CR, Salcedo SP, Holden DW. Growth and killing of a Salmonella enterica serovar Typhimurium sifA mutant strain in the cytosol of different host cell lines. Microbiology 2002; 148: 2705-2715.
93. Brumell JH, Tang P, Zaharik ML, Finlay BB. Disruption of the Salmonella-containing vacuole leads to increased replication of Salmonella enterica serovar typhimurium in the cytosol of epithelial cells. Infect Immun 2002; 70: 3264-3270.