Transcription Factor σB Plays an Important Role in the Production of Extracellular Membrane-Derived Vesicles in Listeria monocytogenes

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Lee, Jung Hwa ^a   Choi, Chi Won ^b   Lee, Taewon ^c   Kim, Seung Il ^b   Lee, Je Chul ^a   Shin, Ji Hyun ^d  

^a Kyungpook National University School of Medicine   (South Korea)

^b Korea Basic Science Institute (KBSI)   (South Korea)

^c Korea University   (South Korea)

^d Dankook University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ACID; CELL DIVISION PROTEIN KINASE; INTERNALIN B; MEMBRANE PROTEIN; OPUCA PROTEIN; OPUCC PROTEIN; POLYSACCHARIDE; PROTEOME; SIGMA FACTOR; TRANSCRIPTION FACTOR SIGMAB; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; SIGB PROTEIN, LISTERIA MONOCYTOGENES; VIRULENCE FACTOR;

ARTICLE; BACTERIAL OUTER MEMBRANE; BACTERIAL STRAIN; BACTERIUM MUTANT; BIOSYNTHESIS; CELL DIVISION; CELL METABOLISM; CELL SURVIVAL; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; EXTRACELLULAR MEMBRANE VESICLE; HEAT; IN VITRO STUDY; LISTERIA MONOCYTOGENES; MEMBRANE VESICLE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION; SECRETORY VESICLE; WILD TYPE; CLASSIFICATION; ELECTROSPRAY MASS SPECTROMETRY; EXTRACELLULAR SPACE; GENE ONTOLOGY; LIQUID CHROMATOGRAPHY; METABOLISM; MUTATION; PATHOGENICITY; ULTRASTRUCTURE; WESTERN BLOTTING;

BACTERIAL PROTEINS; BLOTTING, WESTERN; CHROMATOGRAPHY, LIQUID; EXTRACELLULAR SPACE; GENE ONTOLOGY; LISTERIA MONOCYTOGENES; MUTATION; SECRETORY VESICLES; SIGMA FACTOR; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; VIRULENCE FACTORS;

EID: 84882565855     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073196     Document Type: Article

References (47)

1. Wiedmann M, Arvik TJ, Hurley RJ, Boor KJ, (1998) General stress transcription factor σB and its role in acid tolerance and virulence of Listeria monocytogenes. J Bacteriol 180: 3650-3656. PubMed: 9658010.
2. Becker LA, Cetin MS, Hutkins RW, Benson AK, (1998) Identification of the gene encoding the alternative sigma factor σB from Listeria monocytogenes and its role in osmotolerance. J Bacteriol 180: 4547-4554. PubMed: 9721294.
3. Sleator RD, Wouters J, Gahan CG, Abee T, Hill C, (2001) Analysis of the role of OpuC, an osmolyte transport system, in salt tolerance and virulence potential of Listeria monocytogenes. Appl Environ Microbiol 67: 2692-2698. doi:10.1128/AEM.67.6.2692-2698.2001. PubMed: 11375182.
4. Ferreira A, O'Byrne CP, Boor KJ, (2001) Role of σB in heat, ethanol, acid, and oxidative stress resistance and during carbon starvation in Listeria monocytogenes. Appl Environ Microbiol 67: 4454-4457. doi:10.1128/AEM.67.10.4454-4457.2001. PubMed: 11571142.
5. Hain T, Hossain H, Chatterjee SS, Machata S, Volk U, et al. (2008) Temporal transcriptomic analysis of the Listeria monocytogenes EGD-e σB regulon. BMC Microbiol 8: 20. doi:10.1186/1471-2180-8-20. PubMed: 18226246.
6. Kazmierczak MJ, Mithoe SC, Boor KJ, Wiedmann M, (2003) Listeria monocytogenes σB regulates stress response and virulence functions. J Bacteriol 185: 5722-5734. doi:10.1128/JB.185.19.5722-5734.2003. PubMed: 13129943.
7. Shin JH, Brody MS, Price CW, (2010) Physical and antibiotic stresses require activation of the RsbU phosphatase to induce the general stress response in Listeria monocytogenes. Microbiology 156: 2660-2669. doi:10.1099/mic.0.041202-0. PubMed: 20558511.
8. Fraser KR, Sue D, Wiedmann M, Boor K, O'Byrne CP, (2003) Role of σB in regulating the compatible solute uptake systems of Listeria monocytogenes: osmotic induction of opuC is σB dependent. Appl Environ Microbiol 69: 2015-2022. doi:10.1128/AEM.69.4.2015-2022.2003. PubMed: 12676677.
9. Shin JH, Kim J, Kim SM, Kim S, Lee JC, et al. (2010) σB-dependent protein induction in Listeria monocytogenes during vancomycin stress. FEMS Microbiol Lett 308: 94-100. doi:10.1111/j.1574-6968.2010.01998.x. PubMed: 20487028.
10. Garner MR, Njaa BL, Wiedmann M, Boor KJ, (2006) Sigma B contributes to Listeria monocytogenes gastrointestinal infection but not to systemic spread in the guinea pig infection model. Infect Immun 74: 876-886. doi:10.1128/IAI.74.2.876-886.2006. PubMed: 16428730.
11. Tjalsma H, Antelmann H, Jongbloed JD, Braun PG, Darmon E, et al. (2004) Proteomics of protein secretion by Bacillus subtilis: separating the "secrets" of the secretome. Microbiol Mol Biol Rev 68: 207-233. doi:10.1128/MMBR.68.2.207-233.2004. PubMed: 15187182.
12. Nieuwland R, Sturk A, (2010) Why do cells release vesicles? Thromb Res 125 (Suppl 1):: S49-S51. doi:10.1016/j.thromres.2010.01.037. PubMed: 20149923.
13. Kadurugamuwa JL, Beveridge TJ, (1995) Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J Bacteriol 177: 3998-4008. PubMed: 7608073.
14. Li Z, Clarke AJ, Beveridge TJ, (1996) A major autolysin of Pseudomonas aeruginosa: subcellular distribution, potential role in cell growth and division and secretion in surface membrane vesicles. J Bacteriol 178: 2479-2488. PubMed: 8626312.
15. Wai SN, Lindmark B, Söderblom T, Takade A, Westermark M, et al. (2003) Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell 115: 25-35. doi:10.1016/S0092-8674(03)00754-2. PubMed: 14532000.
16. Fiocca R, Necchi V, Sommi P, Ricci V, Telford J, et al. (1999) Release of Helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles. Uptake of released toxin and vesicles by gastric epithelium. J Pathol 188: 220-226. doi:10.1002/(SICI)1096-9896(199906)188:2. PubMed: 10398168.
17. Dutta S, Iida K, Takade A, Meno Y, Nair GB, et al. (2004) Release of Shiga toxin by membrane vesicles in Shigella dysenteriae serotype 1 strains and in vitro effects of antimicrobials on toxin production and release. Microbiol Immunol 48: 965-969. PubMed: 15611613.
18. Lee EY, Choi DY, Kim DK, Kim JW, Park JO, et al. (2009) Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles. Proteomics 9: 5425-5436. doi:10.1002/pmic.200900338. PubMed: 19834908.
19. Gurung M, Moon DC, Choi CW, Lee JH, Bae YC, et al. (2011) Staphylococcus aureus produces membrane-derived vesicles that induce host cell death. PLOS ONE 6: e27958. doi:10.1371/journal.pone.0027958. PubMed: 22114730.
20. Dorward DW, Garon CF, (1990) DNA Is Packaged within Membrane-Derived Vesicles of Gram-Negative but Not Gram-Positive Bacteria. Appl Environ Microbiol 56: 1960-1962. PubMed: 16348232.
21. Rivera J, Cordero RJ, Nakouzi AS, Frases S, Nicola A, et al. (2010) Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins. Proc Natl Acad Sci U S A 107: 19002-19007. doi:10.1073/pnas.1008843107. PubMed: 20956325.
22. Marsollier L, Brodin P, Jackson M, Korduláková J, Tafelmeyer P, et al. (2007) Impact of Mycobacterium ulcerans biofilm on transmissibility to ecological niches and Buruli ulcer pathogenesis. PLOS Pathog 3: e62. doi:10.1371/journal.ppat.0030062. PubMed: 17480118.
23. Miller JM, (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
24. Jin JS, Kwon SO, Moon DC, Gurung M, Lee JH, et al. (2011) Acinetobacter baumannii secretes cytotoxic outer membrane protein A via outer membrane vesicles. PLOS ONE 6: e17027. doi:10.1371/journal.pone.0017027. PubMed: 21386968.
25. Kim YH, Cho K, Yun SH, Kim JY, Kwon KH, et al. (2006) Analysis of aromatic catabolic pathways in Pseudomonas putida KT 2440 using a combined proteomic approach: 2-DE/MS and cleavable isotope-coded affinity tag analysis. Proteomics 6: 1301-1318. doi:10.1002/pmic.200500329. PubMed: 16470664.
26. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. Gene Ontology Consortium Nat Genet 25: 25-29.
27. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57. PubMed: 19131956.
28. Huang da W, Sherman BT, Lempicki RA, (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1-13. doi:10.1093/nar/gkp505. PubMed: 19033363.
29. Raengpradub S, Wiedmann M, Boor KJ, (2008) Comparative analysis of the σB-dependent stress responses in Listeria monocytogenes and Listeria innocua strains exposed to selected stress conditions. Appl Environ Microbiol 74: 158-171. doi:10.1128/AEM.00951-07. PubMed: 18024685.
30. Chatterjee SS, Hossain H, Otten S, Kuenne C, Kuchmina K, et al. (2006) Intracellular gene expression profile of Listeria monocytogenes. Infect Immun 74: 1323-1338. doi:10.1128/IAI.74.2.1323-1338.2006. PubMed: 16428782.
31. Bauman SJ, Kuehn MJ, (2009) Pseudomonas aeruginosa vesicles associate with and are internalized by human lung epithelial cells. BMC Microbiol 9: 26. doi:10.1186/1471-2180-9-26. PubMed: 19192306.
32. Wai SN, Takade A, Amako K, (1995) The release of outer membrane vesicles from the strains of enterotoxigenic Escherichia coli. Microbiol Immunol 39: 451-456. PubMed: 8569529.
33. Rolhion N, Barnich N, Claret L, Darfeuille-Michaud A, (2005) Strong decrease in invasive ability and outer membrane vesicle release in Crohn's disease-associated adherent-invasive Escherichia coli strain LF82 with the yfgL gene deleted. J Bacteriol 187: 2286-2296. doi:10.1128/JB.187.7.2286-2296.2005. PubMed: 15774871.
34. Parida SK, Domann E, Rohde M, Müller S, Darji A, et al. (1998) Internalin B is essential for adhesion and mediates the invasion of Listeria monocytogenes into human endothelial cells. Mol Microbiol 28: 81-93. PubMed: 9593298.
35. Pentecost M, Kumaran J, Ghosh P, Amieva MR, (2010) Listeria monocytogenes internalin B activates junctional endocytosis to accelerate intestinal invasion. PLOS Pathog 6: e1000900. PubMed: 20485518.
36. Schwab U, Bowen B, Nadon C, Wiedmann M, Boor KJ, (2005) The Listeria monocytogenes prfAP2 promoter is regulated by sigma B in a growth phase dependent manner. FEMS Microbiol Lett 245: 329-336. doi:10.1016/j.femsle.2005.03.025. PubMed: 15837390.
37. Portnoy DA, Jacks PS, Hinrichs DJ, (1988) Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med 167: 1459-1471. doi:10.1084/jem.167.4.1459. PubMed: 2833557.
38. Gedde MM, Higgins DE, Tilney LG, Portnoy DA, (2000) Role of listeriolysin O in cell-to-cell spread of Listeria monocytogenes. Infect Immun 68: 999-1003. doi:10.1128/IAI.68.2.999-1003.2000. PubMed: 10639481.
39. Sue D, Fink D, Wiedmann M, Boor KJ, (2004) σB-dependent gene induction and expression in Listeria monocytogenes during osmotic and acid stress conditions simulating the intestinal environment. Microbiology 150: 3843-3855. doi:10.1099/mic.0.27257-0. PubMed: 15528669.
40. Wemekamp-Kamphuis HH, Wouters JA, Sleator RD, Gahan CG, Hill C, et al. (2002) Multiple deletions of the osmolyte transporters BetL, Gbu, and OpuC of Listeria monocytogenes affect virulence and growth at high osmolarity. Appl Environ Microbiol 68: 4710-4716.
41. Wemekamp-Kamphuis HH, Sleator RD, Wouters JA, Hill C, Abee T, (2004) Molecular and physiological analysis of the role of osmolyte transporters BetL, Gbu, and OpuC in growth of Listeria monocytogenes at low temperatures. Appl Environ Microbiol 70: 2912-2918.
42. Azizoglu RO, Kathariou S, (2010) Temperature-dependent requirement for catalase in aerobic growth of Listeria monocytogenes F2365. Appl Environ Microbiol 76: 6998-7003. doi:10.1128/AEM.01223-10. PubMed: 20817809.
43. van der Veen S, Hain T, Wouters JA, Hossain H, de Vos WM, et al. (2007) The heat-shock response of Listeria monocytogenes comprises genes involved in heat shock, cell division, cell wall synthesis, and the SOS response. Microbiology 153: 3593-3607. doi:10.1099/mic.0.2007/006361-0. PubMed: 17906156.
44. Kim SH, Gorski L, Reynolds J, Orozco E, Fielding S, et al. (2006) Role of uvrA in the growth and survival of Listeria monocytogenes under UV radiation and acid and bile stress. J Food Protect 69: 3031-3036. PubMed: 17186676.
45. van der Veen S, Abee T, (2011) Contribution of Listeria monocytogenes RecA to acid and bile survival and invasion of human intestinal Caco-2 cells. Int J Med Microbiol 301: 334-340. doi:10.1016/j.ijmm.2010.11.006. PubMed: 21273119.
46. Costerton JW, Stewart PS, Greenberg EP, (1999) Bacterial biofilms: a common cause of persistent infections. Science 284: 1318-1322. doi:10.1126/science.284.5418.1318. PubMed: 10334980.
47. Schooling SR, Beveridge TJ, (2006) Membrane vesicles: an overlooked component of the matrices of biofilms. J Bacteriol 188: 5945-5957. doi:10.1128/JB.00257-06. PubMed: 16885463.