Growth temperature-dependent contributions of response regulators, σb, PrfA, and motility factors to Listeria monocytogenes invasion of Caco-2 cells

Foodborne Pathogens and Disease

Volumn 7, Issue 11, 2010, Pages 1337-1349

  Ivy, Reid A ^a   Chan, Yvonne C ^a   Bowen, Barbara M ^a   Boor, Kathryn J ^a   Wiedmann, Martin ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FLAA PROTEIN; GADA PROTEIN; IN1A PROTEIN; INLA PROTEIN; PLCA PROTEIN; PRFA PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; GENETIC REGULATION; GENETIC TRANSCRIPTION; LISTERIA MONOCYTOGENES; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; TEMPERATURE DEPENDENCE;

BACTERIAL PROTEINS; CACO-2 CELLS; FLAGELLIN; GENE DELETION; HUMANS; LISTERIA MONOCYTOGENES; PEPTIDE TERMINATION FACTORS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGMA FACTOR; TEMPERATURE;

BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES; OCTODON DEGUS;

EID: 78149362633     PISSN: 15353141     EISSN: None     Source Type: Journal    
DOI: 10.1089/fpd.2010.0563     Document Type: Article

References (70)

1. Andersen JB, Roldgaard B, Christensen B, and Licht T. Oxygen restriction increases the infective potential of Listeria monocytogenes in vitro in Caco-2 cells and in vivo in guinea pigs. BMC Microbiol 2007;7:55.
2. Autret N, Raynaud C, Dubail I, Berche P, and Charbit A. Identification of the agr locus of Listeria monocytogenes: role in bacterial virulence. Infect Immun 2003;71:4463-4471.
3. Bakardjiev AI, Stacy BA, Fisher SJ, and Portnoy DA. Listeriosis in the pregnant guinea pig: a model of vertical transmission. Infect Immun 2004;72:489-497.
4. Becker LA, Evans SN, Hutkins RW, and Benson AK. Role of Sigma B in adaptation of Listeria monocytogenes to growth at low temperature. J Bacteriol 2000;182:7083-7087.
5. Bennink R, Peeters M, Van den Maegdenbergh V, Geypens B, Rutgeerts P, De Roo M, and Mortelmans L. Evaluation of small-bowel transit for solid and liquid test meal in healthy men and women. Eur J Nucl Med Mol Imaging 1999;26:1560-1566.
6. Bishop DK and Hinrichs DJ. Adoptive transfer of immunity to Listeria monocytogenes. The influence of in vitro stimulation on lymphocyte subset requirements. J Immunol 1987;139:2005-2009.
7. Brondsted L, Kallipolitis BH, Ingmer H, and Knochel S. kdpE and a putative RsbQ homologue contribute to growth of Listeria monocytogenes at high osmolarity and low temperature. FEMS Microbiol Lett 2003;219:233-239.
8. Camilli A, Tilney LG, and Portnoy DA. Dual roles of plcA in Listeria monocytogenes pathogenesis. Mol Microbiol 1993;8: 143-157.
9. Cetin MS, Zhang C, Hutkins RW, and Benson AK. Regulation of transcription of compatible solute transporters by the general stress sigma factor, Sigma B, in Listeria monocytogenes. J Bacteriol 2004;186:794-802.
10. Chan YC, Boor KJ, and Wiedmann M. Sigma B-dependent and -independent mechanisms contribute to transcription of Listeria monocytogenes cold stress genes during cold shock and cold growth. Appl Environ Microbiol 2007a;73: 6019-6029.
11. Chan YC, Raengpradub S, Boor KJ, and Wiedmann M. Microarraybased characterization of the Listeria monocytogenes cold regulon in log- and stationary-phase cells. Appl Environ Microbiol 2007b;73:6484-6498.
12. Chaturongakul S and Boor KJ. Sigma B activation under environmental and energy stress conditions in Listeria monocytogenes. Appl Environ Microbiol 2006;72:5197-5203.
13. Cheng LW and Portnoy DA. Drosophila S2 cells: an alternative infection model for Listeria monocytogenes. Cell Microbiol 2003;5:875-885.
14. Cotter PD, Emerson N, Gahan CGM, and Hill C. Identification and disruption of lisRK, a genetic locus encoding a twocomponent signal transduction system involved in stress tolerance and virulence in Listeria monocytogenes. J Bacteriol 1999;181:6840-6843.
15. Di Bonaventura G, Piccolomini R, Paludi D, D'Orio V, Vergara A, Conter M, and Ianieri A. Influence of temperature on biofilm formation by Listeria monocytogenes on various foodcontact surfaces: relationship with motility and cell surface hydrophobicity. J Appl Microbiol 2008;104:1552-1561.
16. Dons L, Eriksson E, Jin Y, Rottenberg ME, Kristensson K, Larsen CN, Bresciani J, and Olsen JE. Role of flagellin and the twocomponent CheA/CheY system of Listeria monocytogenes in host cell invasion and virulence. Infect Immun 2004;72:3237-3244.
17. Dramsi S, Kocks C, Forestier C, and Cossart P. Internalinmediated invasion of epithelial cells by Listeria monocytogenes is regulated by the bacterial growth state, temperature and the pleiotropic activator PrfA. Mol Microbiol 1993;9:931-941.
18. Freitag NE, Rong L, and Portnoy DA. Regulation of the PrfA transcriptional activator of Listeria monocytogenes: multiple promoter elements contribute to intracellular growth and cellto- cell spread. Infect Immun 1993;61:2537-2544.
19. Garner MR, James KE, Callahan MC, Wiedmann M, and Boor KJ. Exposure to salt and organic acids increases the ability of Listeria monocytogenes to invade Caco-2 cells but decreases its ability to survive gastric stress. Appl Environ Microbiol 2006a;72:5384-5395.
20. Garner MR, Njaa BL, Wiedmann M, and Boor KJ. Sigma B contributes to Listeria monocytogenes gastrointestinal infection but not to systemic spread in the guinea pig infection model. Infect Immun 2006b;74:876-886.
21. Gilbreth SE, Benson AK, and Hutkins RW. Catabolite repression and virulence gene expression in Listeria monocytogenes. Curr Microbiol 2004;49:95-98.
22. Grundling A, Burrack LS, Bouwer HGA, and Higgins DE. From the cover: Listeria monocytogenes regulates flagellar motility gene expression through MogR, a transcriptional repressor required for virulence. PNAS 2004;101:12318-12323.
23. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, Eng JK, Akira S, Underhill DM, and Aderem A. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 2001;410:1099-1103.
24. Isberg RR, Swain A, and Falkow S. Analysis of expression and thermoregulation of the Yersinia pseudotuberculosis inv gene with hybrid proteins. Infect Immun 1988;56:2133-2138.
25. Johansson J, Mandin P, Renzoni A, Chiaruttini C, Springer M, and Cossart P. An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 2002;110:551-561.
26. Kallipolitis BH and Ingmer H. Listeria monocytogenes response regulators important for stress tolerance and pathogenesis. FEMS Microbiol Lett 2001;204:111-115.
27. Kallipolitis BH, Ingmer H, Gahan CG, Hill C, and Sogaard- Andersen L. CesRK, a two-component signal transduction system in Listeria monocytogenes, responds to the presence of cell wall-acting antibiotics and affects {beta}-lactam resistance. Antimicrob Agents Chemother 2003;47:3421-3429.
28. Kazmierczak MJ, Mithoe SC, Boor KJ, and Wiedmann M. Listeria monocytogenes Sigma B regulates stress response and virulence functions. J Bacteriol 2003;185:5722-5734.
29. Kazmierczak MJ, Wiedmann M, and Boor KJ. Contributions of Listeria monocytogenes Sigma B and PrfA to expression of virulence and stress response genes during extra- and intracellular growth. Microbiology 2006;152:1827-1838.
30. Kim H, Boor KJ, and Marquis H. Listeria monocytogenes Sigma B contributes to invasion of human intestinal epithelial cells. Infect Immun 2004;72:7374-7378.
31. Kim H, Marquis H, and Boor KJ. Sigma B contributes to Listeria monocytogenes invasion by controlling expression of inlA and inlB. Microbiology 2005;151:3215-3222.
32. Knudsen GM, Olsen JE, and Dons L. Characterization of DegU, a response regulator in Listeria monocytogenes, involved in regulation of motility and contributes to virulence. FEMS Microbiol Lett 2004;240:171-179.
33. Konkel ME and Tilly K. Temperature-regulated expression of bacterial virulence genes. Microb Infect 2000;2:157-166.
34. Larsen MH, Kallipolitis BH, Christiansen JK, Olsen JE, and Ingmer H. The response regulator ResD modulates virulence gene expression in response to carbohydrates in Listeria monocytogenes. Mol Microbiol 2006;61:1622-1635.
35. Lecuit M, Dramsi S, Gottardi C, Fedor-Chaiken M, Gumbiner B, and Cossart P. A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes. EMBO J 1999;18:3956-3963.
36. Leimeister-Wachter M, Domann E, and Chakraborty T. The expression of virulence genes in Listeria monocytogenes is thermoregulated. J Bacteriol 1992;174:947-952.
37. Lingnau A, Domann E, Hudel M, Bock M, Nichterlein T,Wehland J, and Chakraborty T. Expression of the Listeria monocytogenes EGD inlA and inlB genes, whose products mediate bacterial entry into tissue culture cell lines, by PrfA-dependent and -independent mechanisms. Infect Immun 1995;63:3896-3903.
38. Liu S, Graham JE, Bigelow L, Morse PD II, and Wilkinson BJ.Identification of Listeria monocytogenes genes expressed in response to growth at low temperature. Appl Environ Microbiol 2002;68:1697-1705.
39. Mandin P, Fsihi H, Dussurget O, Vergassola M, Milohanic E, Toledo-Arana A, Lasa I, Johansson J, and Cossart P. VirR, a response regulator critical for Listeria monocytogenes virulence. Mol Microbiol 2005;57:1367-1380.
40. Mauder N, Williams T, Fritsch F, Kuhn M, and Beier D. Response regulator DegU of Listeria monocytogenes controls temperature-responsive flagellar gene expression in its unphosphorylated state. J Bacteriol 2008;190:4777-4781.
41. Maurelli AT. Temperature regulation of virulence genes in pathogenic bacteria: a general strategy for human pathogens? Microb Pathog 1989;7:1-10.
42. McGann P, Ivanek R, Wiedmann M, and Boor KJ. Temperaturedependent expression of Listeria monocytogenes internalin and internalin-like genes suggests functional diversity of these proteins among the Listeriae. Appl Environ Microbiol 2007a; 73:2806-2814.
43. McGann P, Raengpradub S, Ivanek R, Wiedmann M, and Boor KJ. Differential regulation of Listeria monocytogenes internalin and internalin-like genes by Sigma B and PrfA as revealed by subgenomic microarray analyses. Foodborne Pathog Dis 2008;5:417-435.
44. McGann P, Wiedmann M, and Boor KJ. The alternative sigma factor Sigma B and the virulence gene regulator PrfA both regulate transcription of Listeria monocytogenes internalins. Appl Environ Microbiol 2007b;73:2919-2930.
45. Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C, Griffin PM, and Tauxe RV. Food-related illness and death in the United States. Emerg Infect Dis 1999;5:607-625.
46. Michel E, Mengaud J, Galsworthy S, and Cossart P. Characterization of a large motility gene cluster containing the cheR, motAB genes of Listeria monocytogenes and evidence that PrfA downregulates motility genes. FEMS Microbiol Lett 1998; 169:341-347.
47. Milenbachs AA, Brown DP, Moors M, and Youngman P. Carbon- source regulation of virulence gene expression in Listeria monocytogenes. Mol Microbiol 1997;23:1075-1085.
48. Milohanic E, Glaser P, Coppee J-Y, Frangeul L, Vega Y, Vazquez- Boland JA, Kunst F, Cossart P, and Buchrieser C. Transcriptome analysis of Listeria monocytogenes identifies three groups of genes differently regulated by PrfA. Mol Microbiol 2003;47:1613-1625.
49. Ollinger J, Wiedmann M, and Boor KJ. SigB- and PrfA-dependent transcription of genes previously classified as putative constituents of the Listeria monocytogenes PrfA Regulon. Foodborne Pathog Dis 2008;5:281-293.
50. O'Neil HS and Marquis H. Listeria monocytogenes flagella are used for motility, not as adhesins, to increase host cell invasion. Infect Immun 2006;74:6675-6681.
51. Pal A, Labuza TP, and Diez-Gonzalez F. Comparison of primary predictive models to study the growth of Listeria monocytogenes at low temperatures in liquid cultures and selection of fastest growing ribotypes in meat and turkey product slurries. Food Microbiol 2008;25:460-470.
52. Raengpradub S, Wiedmann M, and Boor KJ. Comparative analysis of the Sigma B-dependent stress responses in Listeria monocytogenes and Listeria innocua strains exposed to selected stress conditions. Appl Environ Microbiol 2008;74: 158-171.
53. Raffelsbauer D, Bubert A, Engelbrecht F, Scheinpflug J, Simm A, Hess J, Kaufmann SH, and Goebel W. The gene cluster inlC2DE of Listeria monocytogenes contains additional new internalin genes and is important for virulence in mice. Mol Gen Genet 1998;260:144-158.
54. Ripio MT, Brehm K, Lara M, Suarez M, and Vazquez-Boland JA. Glucose-1-phosphate utilization by Listeria monocytogenes is PrfA dependent and coordinately expressed with virulence factors. J Bacteriol 1997;179:7174-7180.
55. Ripio MT, DomÌnguez-Bernal G, Suárez M, Brehm K, Berche P, and Vázquez-Boland JA. Transcriptional activation of virulence genes in wild-type strains of Listeria monocytogenes in response to a change in the extracellular medium composition. Res Microbiol 1996;147:371-384.
56. Scortti M, Monzo HJ, Lacharme-Lora L, Lewis DA, and Vazquez- Boland JA. The PrfA virulence regulon. Microb Infect 2007;9:1196-1207.
57. Shen A and Higgins DE. The MogR transcriptional repressor regulates nonhierarchal expression of flagellar motility genes and virulence in Listeria monocytogenes. PLoS Pathog 2006; 2:0283-0295.
58. Shun Z, Silverberg A, Chang C, and Ouyang P. Dunnett's manyto- one test and least square means. J Biopharm Stat 2003; 13:17-28.
59. Sleator RD and Hill C. A novel role for the LisRK two-component regulatory system in listerial osmotolerance. Clin Microbiol Infect 2005;11:599-601.
60. Smith K and Youngman P. Use of a new integrational vector to investigate compartment-specific expression of the Bacillus subtilis spollM gene. Biochimie 1992;74:705-711.
61. Sue D, Boor KJ, and Wiedmann M. Sigma B-dependent expression patterns of compatible solute transporter genes opuCA and lmo1421 and the conjugated bile salt hydrolase gene bsh in Listeria monocytogenes. Microbiology 2003; 149:3247-3256.
62. Sue D, Fink D, Wiedmann M, and Boor KJ. Sigma B-dependent gene induction and expression in Listeria monocytogenes during osmotic and acid stress conditions simulating the intestinal environment. Microbiology 2004; 150:3843-3855.
63. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, Balestrino D, Loh E, Gripenland J, Tiensuu T, Vaitkevicius K, Barthelemy M, Vergassola M, Nahori M-A, Soubigou G, Regnault B, Coppee J-Y, Lecuit M, Johansson J, and Cossart P. The Listeria transcriptional landscape from saprophytism to virulence. Nature 2009;459:950-956.
64. Torres D, Barrier M, Bihl F, Quesniaux VJF, Maillet I, Akira S, Ryffel B, and Erard F. Toll-like Receptor 2 is required for optimal control of Listeria monocytogenes infection. Infect Immun 2004;72:2131-2139.
65. van der Veen S, Hain T, Wouters JA, Hossain H, de Vos WM, Abee T, Chakraborty T, and Wells-Bennik MHJ. The heat-shock response of Listeria monocytogenes comprises genes involved in heat shock, cell division, cell wall synthesis, and the SOS response. Microbiology 2007;153:3593-3607.
66. Way SS, Thompson LJ, Lopes JE, Hajjar AM, Kollmann TR, Freitag NE, and Wilson CB. Characterization of flagellin expression and its role in Listeria monocytogenes infection and immunity. Cell Microbiol 2004;6:235-242.
67. Wiedmann M, Arvik TJ, Hurley RJ, and Boor KJ. General stress transcription factor Sigma B and its role in acid tolerance and virulence of Listeria monocytogenes. J Bacteriol 1998;180:3650-3656.
68. Williams T, Bauer S, Beier D, and Kuhn M. Construction and characterization of Listeria monocytogenes mutants with in-frame deletions in the response regulator genes identified in the genome sequence. Infect Immun 2005a;73:3152-3159.
69. Williams T, Joseph B, Beier D, Goebel W, and Kuhn M. Response regulator DegU of Listeria monocytogenes regulates the expression of flagella-specific genes. FEMS Microbiol Lett 2005b;252:287-298.
70. Young GM, Badger JL, and Miller VL. Motility is required to initiate host cell invasion by Yersinia enterocolitica. Infect Immun 2000;68:4323-4326.