The bimodal lifestyle of intracellular Salmonella in epithelial cells: Replication in the cytosol obscures defects in vacuolar replication

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Malik Kale, Preeti ^a   Winfree, Seth ^a   Steele Mortimer, Olivia ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GROWTH; BACTERIAL REPRODUCTION; BIOGENESIS; CELL VACUOLE; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOSOL; EPITHELIUM CELL; HELA CELL; INTRACELLULAR BACTERIUM; NONHUMAN; SALMONELLA TYPHIMURIUM; TYPE III SECRETION SYSTEM;

CYTOSOL; EPITHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HUMANS; SALMONELLA ENTERICA; VACUOLES;

EID: 84862171547     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038732     Document Type: Article

References (36)

1. Marlovits TC, Stebbins CE, (2010) Type III secretion systems shape up as they ship out. Curr Opin Microbiol 13: 47-52.
2. Steele-Mortimer O, (2008) The Salmonella-containing vacuole: moving with the times. Curr Opin Microbiol 11: 38-45.
3. Beuzon CR, Salcedo SP, Holden DW, (2002) Growth and killing of a Salmonella enterica serovar Typhimurium sifA mutant strain in the cytosol of different host cell lines. Microbiology 148: 2705-2715.
4. Birmingham CL, Smith AC, Bakowski MA, Yoshimori T, Brumell JH, (2006) Autophagy controls Salmonella infection in response to damage to the Salmonella-containing vacuole. J Biol Chem 281: 11374-11383.
5. Brumell JH, Rosenberger CM, Gotto GT, Marcus SL, Finlay BB, (2001) SifA permits survival and replication of Salmonella typhimurium in murine macrophages. Cell Microbiol 3: 75-84.
6. Knodler LA, Vallance BA, Celli J, Winfree S, Hansen B, et al. (2010) Dissemination of invasive Salmonella via bacterial-induced extrusion of mucosal epithelia. Proc Natl Acad Sci USA 107: 17733-17738.
7. Steele-Mortimer O, Brumell JH, Knodler LA, Meresse S, Lopez A, et al. (2002) 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 4: 43-54.
8. Knodler LA, Vallance BA, Hensel M, Jackel D, Finlay BB, et al. (2003) Salmonella type III effectors PipB and PipB2 are targeted to detergent-resistant microdomains on internal host cell membranes. Mol Microbiol 49: 685-704.
9. Bakowski MA, Braun V, Brumell JH, (2008) Salmonella-containing vacuoles: directing traffic and nesting to grow. Traffic 9: 2022-2031.
10. Garcia-del Portillo F, Finlay BB, (1995) Targeting of Salmonella typhimurium to vesicles containing lysosomal membrane glycoproteins bypasses compartments with mannose 6-phosphate receptors. J Cell Biol 129: 81-97.
11. Mota LJ, Ramsden AE, Liu M, Castle JD, Holden DW, (2009) SCAMP3 is a component of the Salmonella-induced tubular network and reveals an interaction between bacterial effectors and post-Golgi trafficking. Cell Microbiol 11: 1236-1253.
12. Bujny MV, Ewels PA, Humphrey S, Attar N, Jepson MA, et al. (2008) Sorting nexin-1 defines an early phase of Salmonella-containing vacuole-remodeling during Salmonella infection. J Cell Sci 121: 2027-2036.
13. Drecktrah D, Knodler LA, Howe D, Steele-Mortimer O, (2007) Salmonella trafficking is defined by continuous dynamic interactions with the endolysosomal system. Traffic 8: 212-225.
14. Steele-Mortimer O, Meresse S, Gorvel JP, Toh BH, Finlay BB, (1999) Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell Microbiol 1: 33-49.
15. Abrahams GL, Muller P, Hensel M, (2006) Functional dissection of SseF, a type III effector protein involved in positioning the salmonella-containing vacuole. Traffic 7: 950-965.
16. Guignot J, Servin AL, (2008) Maintenance of the Salmonella-containing vacuole in the juxtanuclear area: a role for intermediate filaments. Microb Pathog 45: 415-422.
17. Meresse S, Steele-Mortimer O, Finlay BB, Gorvel JP, (1999) The rab7 GTPase controls the maturation of Salmonella typhimurium-containing vacuoles in HeLa cells. EMBO J 18: 4394-4403.
18. Rathman M, Barker LP, Falkow S, (1997) The unique trafficking pattern of Salmonella typhimurium-containing phagosomes in murine macrophages is independent of the mechanism of bacterial entry. Infect Immun 65: 1475-1485.
19. Beuzon CR, Meresse S, Unsworth KE, Ruiz-Albert J, Garvis S, et al. (2000) Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J 19: 3235-3249.
20. Ruiz-Albert J, Yu XJ, Beuzon CR, Blakey AN, Galyov EE, et al. (2002) Complementary activities of SseJ and SifA regulate dynamics of the Salmonella typhimurium vacuolar membrane. Mol Microbiol 44: 645-661.
21. Garcia-del Portillo F, Zwick MB, Leung KY, Finlay BB, (1993) Salmonella induces the formation of filamentous structures containing lysosomal membrane glycoproteins in epithelial cells. Proc Natl Acad Sci USA 90: 10544-10548.
22. Buckner MM, Croxen MA, Arena ET, Finlay BB, (2011) A comprehensive study of the contribution of Salmonella enterica serovar Typhimurium SPI2 effectors to bacterial colonization, survival, and replication in typhoid fever, macrophage, and epithelial cell infection models. Virulence 2: 208-216.
23. Freeman JA, Ohl ME, Miller SI, (2003) The Salmonella enterica serovar typhimurium translocated effectors SseJ and SifB are targeted to the Salmonella-containing vacuole. Infect Immun 71: 418-427.
24. Guy RL, Gonias LA, Stein MA, (2000) Aggregation of host endosomes by Salmonella requires SPI2 translocation of SseFG and involves SpvR and the fms-aroE intragenic region. Mol Microbiol 37: 1417-1435.
25. Coombes BK, Brown NF, Kujat-Choy S, Vallance BA, Finlay BB, (2003) SseA is required for translocation of Salmonella pathogenicity island-2 effectors into host cells. Microb Infect 5: 561-570.
26. Brumell JH, Tang P, Mills SD, Finlay BB, (2001) Characterization of Salmonella-induced filaments (Sifs) reveals a delayed interaction between Salmonella-containing vacuoles and late endocytic compartments. Traffic 2: 643-653.
27. Ibarra JA, Knodler LA, Sturdevant DE, Virtaneva K, Carmody AB, et al. (2010) Induction of Salmonella pathogenicity island 1 under different growth conditions can affect Salmonella-host cell interactions in vitro. Microbiology 156: 1120-1133.
28. Deiwick J, Salcedo SP, Boucrot E, Gilliland SM, Henry T, et al. (2006) The translocated Salmonella effector proteins SseF and SseG interact and are required to establish an intracellular replication niche. Infect Immun 74: 6965-6972.
29. Kerr MC, Wang JT, Castro NA, Hamilton NA, Town L, et al. (2010) Inhibition of the PtdIns(5) kinase PIKfyve disrupts intracellular replication of Salmonella. EMBO J 29: 1331-1347.
30. Cirillo DM, Valdivia RH, Monack DM, Falkow S, et al. (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.
31. Hensel M, Shea JE, Raupach B, Monack D, Falkow S, (1997) Functional analysis of ssaJ and the ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella Pathogenicity Island 2. Mol Microbiol 24: 155-167.
32. Hensel M, Shea JE, Waterman SR, Mundy R, Nikolaus T, et al. (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.
33. Ochman H, Soncini FC, Solomon F, Groisman EA, (1996) Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci USA 93: 7800-7804.
34. Hautefort I, Thompson A, Eriksson-Ygberg S, Parker ML, Lucchini S, et al. (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.
35. Drecktrah D, Levine-Wilkinson S, Dam T, Winfree S, Knodler LA, et al. (2008) Dynamic behavior of Salmonella-induced membrane tubules in epithelial cells. Traffic 9: 2117-2129.
36. Preibisch S, Saalfeld S, Tomancak P, (2009) Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics 25: 1463-1465.