Salmonella-containing vacuoles display centrifugal movement associated with cell-to-cell transfer in epithelial cells

Infection and Immunity

Volumn 77, Issue 3, 2009, Pages 996-1007

  Szeto, Jason ^a,d   Namolovan, Anton ^a   Osborne, Suzanne E ^b   Coombes, Brian K ^b   Brumell, John H ^a,c  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d Sanofi Pasteur   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; KINESIN 1; PROTEIN PIPB2; PROTEIN SIFA; UNCLASSIFIED DRUG; KINESIN; MEMBRANE PROTEIN; PIPB2 PROTEIN, SALMONELLA ENTERICA; SPI 2 PROTEIN, SALMONELLA; SPI-2 PROTEIN, SALMONELLA;

ARTICLE; BACTERIAL INFECTION; CELL TRANSFER; CELL VACUOLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EPITHELIUM CELL; HELA CELL; HUMAN; HUMAN CELL; PATHOGENICITY ISLAND; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; WILD TYPE; CELL COMMUNICATION; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSFECTION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; SALMONELLOSIS;

BACTERIAL PROTEINS; CELL COMMUNICATION; EPITHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HUMANS; KINESIN; MEMBRANE PROTEINS; SALMONELLA ENTERICA; SALMONELLA INFECTIONS; TRANSFECTION; VACUOLES;

EID: 62449093980     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01275-08     Document Type: Article

References (58)

1. Abrahams, G. L., and M. Hensel. 2006. Manipulating cellular transport and immune responses: dynamic interactions between intracellular Salmonella enterica and its host cells. Cell Microbiol. 8:728-737.
2. Abrahams, G. L., P. Muller, and M. Hensel. 2006. Functional dissection of SseF, a type III effector protein involved in positioning the Salmonella-containing vacuole. Traffic 7:950-965.
3. Alberti-Segui, C., K. R. Goeden, and D. E. Higgins. 2007. Differential function of Listeria monocytogenes listeriolysin O and phospholipases C in vacuolar dissolution following cell-to-cell spread. Cell Microbiol. 9:179-195.
4. Birmingham, C. L., X. Jiang, M. B. Ohlson, S. I. Miller, and J. H. Brumell. 2005. Salmonella-induced filament formation is a dynamic phenotype induced by rapidly replicating Salmonella enterica serovar Typhimurium in epithelial cells. Infect. Immun. 73:1204-1208.
5. Boucrot, E., T. Henry, J. P. Borg, J. P. Gorvel, and S. Meresse. 2005. The intracellular fate of Salmonella depends on the recruitment of kinesin. Science 308:1174-1178.
6. Brawn, L. C., R. D. Hayward, and V. Koronakis. 2007. Salmonella SPI1 effector SipA persists after entry and cooperates with a SPI2 effector to regulate phagosome maturation and intracellular replication. Cell Host Microbe 1:63-75.
7. Brown, N. F., J. Szeto, X. Jiang, B. K. Coombes, B. B. Finlay, and J. H. Brumell. 2006. Mutational analysis of Salmonella translocated effector members SifA and SopD2 reveals domains implicated in translocation, subcellular localization and function. Microbiology 152:2323-2343.
8. Brumell, J. H., D. L. Goosney, and B. B. Finlay. 2002. SifA, a type III secreted effector of Salmonella Typhimurium, directs Salmonella-induced filament (Sif) formation along microtubules. Traffic 3:407-415.
9. Brumell, J. H., C. M. Rosenberger, G. T. Gotto, S. L. Marcus, and B. B. Finlay. 2001. SifA permits survival and replication of Salmonella typhimurium in murine macrophages. Cell Microbiol. 3:75-84.
10. Cirillo, D. M., R. H. Valdivia, D. M. Monack, and S. Falkow. 1998. Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol. Microbiol. 30:175-188.
11. Coombes, B. K., N. F. Brown, Y. Valdez, J. H. Brumell, and B. B. Finlay. 2004. Expression and secretion of Salmonella pathogenicity island-2 virulence genes in response to acidification exhibit differential requirements of a functional type III secretion apparatus and SsaL. J. Biol. Chem. 279:49804-49815.
12. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
13. Deiwick, J., S. P. Salcedo, E. Boucrot, S. M. Gilliland, T. Henry, N. Petermann, S. Waterman, J. P. Gorvel, D. W. Holden, and S. Meresse. 2006. The translocated Salmonella effector proteins SseF and SseG interact and are required to establish an intracellular replication niche. Infect. Immun. 74:6965-6972.
14. Drecktrah, D., L. A. Knodler, K. Galbraith, and O. Steele-Mortimer. 2005. The Salmonella SPI1 effector SopB stimulates nitric oxide production long after invasion. Cell Microbiol. 7:105-113.
15. Drecktrah, D., L. A. Knodler, D. Howe, and O. Steele-Mortimer. 2007. Salmonella trafficking is defined by continuous dynamic interactions with the endolysosomal system. Traffic 8:212-225.
16. Dunlap, N. E., W. H. Benjamin, Jr., R. D. McCall, Jr., A. B. Tilden, and D. E. Briles. 1991. A "safe-site: for Salmonella typhimurium is within splenic cells during the early phase of infection in mice. Microb. Pathog. 10:297-310.
17. Duong, N., S. Osborne, V. H. Bustamante, A. M. Tomljenovic, J. L. Puente, and B. K. Coombes. 2007. Thermosensing coordinates a cis-regulatory module for transcriptional activation of the intracellular virulence system in Salmonella enterica serovar Typhimurium. J. Biol. Chem. 282:34077-34084.
18. Eriksson, S., S. Lucchini, A. Thompson, M. Rhen, and J. C. Hinton. 2003. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 47:103-118.
19. Galan, J. E. 2001. Salmonella interactions with host cells: type III secretion at work. Annu. Rev. Cell Dev. Biol. 17:53-86.
20. Garcia-del Portillo, F., M. B. Zwick, K. Y. Leung, and B. B. Finlay. 1993. Salmonella induces the formation of filamentous structures containing lysosomal membrane glycoproteins in epithelial cells. Proc. Natl. Acad. Sci. USA 90:10544-10548.
21. Guignot, J., E. Caron, C. Beuzon, C. Bucci, J. Kagan, C. Roy, and D. W. Holden. 2004. Microtubule motors control membrane dynamics of Salmonella-containing vacuoles. J. Cell Sci. 117:1033-1045.
22. Guiney, D. G. 2005. The role of host cell death in Salmonella infections. Curr. Top. Microbiol. Immunol. 289:131-150.
23. Haraga, A., M. B. Ohlson, and S. I. Miller. 2008. Salmonellae interplay with host cells. Nat. Rev. Microbiol. 6:53-66.
24. Harrison, R. E., J. H. Brumell, A. Khandani, C. Bucci, C. C. Scott, X. Jiang, B. B. Finlay, and S. Grinstein. 2004. Salmonella impairs RILP recruitment to Rab7 during maturation of invasion vacuoles. Mol. Biol. Cell. 15:3146-3154.
25. Hautefort, I., A. Thompson, S. Eriksson-Ygberg, M. L. Parker, S. Lucchini, V. Danino, R. J. Bongaerts, N. Ahmad, M. Rhen, and J. C. Hinton. 2008. During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell Microbiol. 10:958-984.
26. Henry, T., C. Couillault, P. Rockenfeller, E. Boucrot, A. Dumont, N. Schroeder, A. Hermant, L. A. Knodler, P. Lecine, O. Steele-Mortimer, J. P. Borg, J. P. Gorvel, and S. Meresse. 2006. The Salmonella effector protein PipB2 is a linker for kinesin-1. Proc. Natl. Acad. Sci. USA 103:13497- 13502.
27. Henry, T., J. P. Gorvel, and S. Meresse. 2006. Molecular motors hijacking by intracellular pathogens. Cell Microbiol. 8:23-32.
28. Hensel, M., J. E. Shea, S. R. Waterman, R. Mundy, T. Nikolaus, G. Banks, A. Vazquez-Torres, C. Gleeson, F. C. Fang, and D. W. Holden. 1998. Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol. Microbiol. 30:163-174.
29. Hoiseth, S. K., and B. A. Stocker. 1981. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291:238-239.
30. Hybiske, K., and R. S. Stephens. 2008. Exit strategies of intracellular pathogens. Nat. Rev. Microbiol. 6:99-110.
31. Hybiske, K., and R. S. Stephens. 2007. Mechanisms of host cell exit by the intracellular bacterium Chlamydia. Proc. Natl. Acad. Sci. USA 104:11430-11435.
32. Jiang, X., O. W. Rossanese, N. F. Brown, S. Kujat-Choy, J. E. Galan, B. B. Finlay, and J. H. Brumell. 2004. The related effector proteins SopD and SopD2 from Salmonella enterica serovar Typhimurium contribute to virulence during systemic infection of mice. Mol. Microbiol. 54:1186-1198.
33. Knodler, L. A., and O. Steele-Mortimer. 2003. Taking possession: biogenesis of the Salmonella-containing vacuole. Traffic 4:587-599.
34. Knodler, L. A., and O. Steele-Mortimer. 2005. The Salmonella effector PipB2 affects late endosome/lysosome distribution to mediate Sif extension. Mol. Biol. Cell 16:4108-4123.
35. Knodler, L. A., B. A. Vallance, M. Hensel, D. Jackel, B. B. Finlay, and O. Steele-Mortimer. 2003. Salmonella type III effectors PipB and PipB2 are targeted to detergent-resistant microdomains on internal host cell membranes. Mol. Microbiol. 49:685-704.
36. Kuhle, V., G. L. Abrahams, and M. Hensel. 2006. Intracellular Salmonella enterica redirect exocytic transport processes in a Salmonella pathogenicity island 2-dependent manner. Traffic 7:716-730.
37. Marsman, M., I. Jordens, C. Kuijl, L. Janssen, and J. Neefjes. 2004. Dyneinmediated vesicle transport controls intracellular Salmonella replication. Mol. Biol. Cell 15:2954-2964.
38. Mastroeni, P., and M. Sheppard. 2004. Salmonella infections in the mouse model: host resistance factors and in vivo dynamics of bacterial spread and distribution in the tissues. Microbes Infect. 6:398-405.
39. Miao, E. A., C. A. Scherer, R. M. Tsolis, R. A. Kingsley, L. G. Adams, A. J. Baumler, and S. I. Miller. 1999. Salmonella typhimurium leucine-rich repeat proteins are targeted to the SPI1 and SPI2 type III secretion systems. Mol. Microbiol. 34:850-864.
40. Ochman, H., F. C. Soncini, F. Solomon, and E. A. Groisman. 1996. Identification of a pathogenicity island required for Salmonella survival in host cells. Proc. Natl. Acad. Sci. USA 93:7800-7804.
41. Ramsden, A. E., D. W. Holden, and L. J. Mota. 2007. Membrane dynamics and spatial distribution of Salmonella-containing vacuoles. Trends Microbiol. 15:516-524.
42. Ramsden, A. E., L. J. Mota, S. Munter, S. L. Shorte, and D. W. Holden. 2007. The SPI-2 type III secretion system restricts motility of Salmonella-containing vacuoles. Cell Microbiol. 9:2517-2529.
43. Richter-Dahlfors, A., A. M. Buchan, and B. B. Finlay. 1997. Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J. Exp. Med. 186:569-580.
44. Rietdorf, J., A. Ploubidou, I. Reckmann, A. Holmstrom, F. Frischknecht, M. Zettl, T. Zimmermann, and M. Way. 2001. Kinesin-dependent movement on microtubules precedes actin-based motility of vaccinia virus. Nat. Cell Biol. 3:992-1000.
45. Salcedo, S. P., and D. W. Holden. 2003. SseG, a virulence protein that targets Salmonella to the Golgi network. EMBO J. 22:5003-5014.
46. Salcedo, S. P., M. Noursadeghi, J. Cohen, and D. W. Holden. 2001. Intracellular replication of Salmonella typhimurium strains in specific subsets of splenic macrophages in vivo. Cell Microbiol. 3:587-597.
47. Sano, G., Y. Takada, S. Goto, K. Maruyama, Y. Shindo, K. Oka, H. Matsui, and K. Matsuo. 2007. Flagella facilitate escape of Salmonella from oncotic macrophages. J. Bacteriol. 189:8224-8232.
48. Shea, J. E., M. Hensel, C. Gleeson, and D. W. Holden. 1996. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 93:2593-2597.
49. Sheppard, M., C. Webb, F. Heath, V. Mallows, R. Emilianus, D. Maskell, and P. Mastroeni. 2003. Dynamics of bacterial growth and distribution within the liver during Salmonella infection. Cell Microbiol. 5:593-600.
50. Steele-Mortimer, O., S. Méresse, J.-P. Gorvel, B.-H. Toh, and B. B. Finlay. 1999. Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell. Microbiol. 1:33-51.
51. Stein, M. A., K. Y. Leung, M. Zwick, F. Garcia-del Portillo, and B. B. Finlay. 1996. Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells. Mol. Microbiol. 20:151-164.
52. Stevens, J. M., E. E. Galyov, and M. P. Stevens. 2006. Actin-dependent movement of bacterial pathogens. Nat. Rev. Microbiol. 4:91-101.
53. Suchland, R. J., D. D. Rockey, S. K. Weeks, D. T. Alzhanov, and W. E. Stamm. 2005. Development of secondary inclusions in cells infected by Chlamydia trachomatis. Infect. Immun. 73:3954-3962.
54. Takeuchi, A. 1967. Electron microscope studies of experimental Salmonella infection. I. Penetration into the intestinal epithelium by Salmonella typhimurium. Am. J. Pathol. 50:109-136.
55. Tsolis, R. M., R. A. Kingsley, S. M. Townsend, T. A. Ficht, L. G. Adams, and A. J. Baumler. 1999. Of mice, calves, and men. Comparison of the mouse typhoid model with other Salmonella infections. Adv. Exp. Med. Biol. 473:261-274.
56. Wang, R. F., and S. R. Kushner. 1991. Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100:195-199.
57. Wasylnka, J. A., M. A. Bakowski, J. Szeto, M. B. Ohlson, W. S. Trimble, S. I. Miller, and J. H. Brumell. 2008. Role for myosin II in regulating positioning of Salmonella-containing vacuoles and intracellular replication. Infect. Immun. 76:2722-2735.
58. Waterman, S. R., and D. W. Holden. 2003. Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol. 5:501-511.