The alternative sigma factor σB and the virulence gene regulator PrfA both regulate transcription of Listeria monocytogenes internalins

Applied and Environmental Microbiology

Volumn 73, Issue 9, 2007, Pages 2919-2930

  McGann, Patrick ^a   Wiedmann, Martin ^a   Boor, Kathryn J ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE TRANSCRIPTION; LISTERIA MONOCYTOGENES INTERNALINS; MAMMALIAN TISSUE CULTURE CELLS; VIRULENCE GENE REGULATORS;

CELL ADHESION; GENE ENCODING; MICROORGANISMS; TISSUE;

GENE EXPRESSION;

BACTERIAL PROTEIN; INTERNALIN; INTERNALIN A; INTERNALIN B; INTERNALIN C; INTERNALIN C2; INTERNALIN D; INTERNALIN E; INTERNALIN F; INTERNALIN G; MEMBRANE PROTEIN; POSITIVE REGULATORY FACTOR A; SIGMA FACTOR; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

BACTERIUM; ENVIRONMENTAL STRESS; GENE EXPRESSION; GENETIC ANALYSIS; MAMMAL; POLYMERASE CHAIN REACTION; VIRULENCE;

ARTICLE; BACTERIAL STRAIN; GASTROINTESTINAL TRACT; GENE EXPRESSION; GENETIC TRANSCRIPTION; LISTERIA MONOCYTOGENES; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; IMMUNOHISTOCHEMISTRY; LISTERIA MONOCYTOGENES; MICROSCOPY, ELECTRON, TRANSMISSION; PEPTIDE TERMINATION FACTORS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGMA FACTOR;

LISTERIA MONOCYTOGENES; MAMMALIA;

EID: 34248170594     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02664-06     Document Type: Article

References (64)

1. Bakardjiev, A. I., B. A. Stacy, S. J. Fisher, and D. A. Portnoy. 2004. Listeriosis in the pregnant guinea pig: a model of vertical transmission. Infect. Immun. 72:489-497.
2. Begley, M., R. D. Sleator, C. G. Gahan, and C. Hill. 2005. Contribution of three bile-associated loci, bsh, pva, and btlB, to gastrointestinal persistence and bile tolerance of Listeria monocytogenes. Infect. Immun. 73:894-904.
3. Behari, J., and P. Youngman. 1998. A homolog of CcpA mediates catabolite control in Listeria monocytogenes but not carbon source regulation of virulence genes. J. Bacteriol. 180:6316-6324.
4. Behari, J., and P. Youngman. 1998. Regulation of hly expression in Listeria monocytogenes by carbon sources and pH occurs through separate mechanisms mediated by PrfA. Infect. Immun. 66:3635-3642.
5. Bergmann, B., D. Raffelsbauer, M. Kuhn, M. Goetz, S. Horn, and W. Goebel. 2002. InlA- but not InlB-mediated internalization of Listeria monocytogenes by non-phagocytic mammalian cells needs the support of other internalins. Mol. Microbiol. 43:557-570.
6. Bishop, D. K., and D. J. Hinrichs. 1987. Adoptive transfer of immunity to Listeria monocytogenes. The influence of in vitro stimulation on lymphocyte subset requirements. J. Immunol. 139:2005-2009.
7. Böckmann, R., C. Dickneite, B. Middendorf, W. Goebel, and Z. Sokolovic. 1996. Specific binding of the Listeria monocytogenes transcriptional regulator PrfA to target sequences requires additional factor(s) and is influenced by iron. Mol. Microbiol. 22:643-653.
8. Bohne, J., H. Kestler, C. Uebele, Z. Sokolovic, and W. Goebel. 1996. Differential regulation of the virulence genes of Listeria monocytogenes by the transcriptional activator PrfA. Mol. Microbiol. 20:1189-1198.
9. Braun, L., B. Ghebrehiwet, and P. Cossart. 2000. gClq-R/p32, a Clq-binding protein, is a receptor for the InlB invasion protein of Listeria monocytogenes. EMBO J. 19:1458-1466.
10. Brehm, K., M. T. Ripio, J. Kreft, and J. A. Vazquez-Boland. 1999. The bvr locus of Listeria monocytogenes mediates virulence gene repression by betaglucosides. J. Bacteriol. 181:5024-5032.
11. Cabanes, D., P. Dehoux, O. Dussurget, L. Frangeul, and P. Cossart. 2002. Surface proteins and the pathogenic potential of Listeria monocytogenes. Trends Microbiol. 10:238-245.
12. Camilli, A., L. G. Tilney, and D. A. Portnoy. 1993. Dual roles of plcA in Listeria monocytogenes pathogenesis. Mol. Microbiol. 8:143-157.
13. Chaturongakul, S., and K. J. Boor. 2004. RsbT and RsbV contribute to sigma B-dependent survival under environmental, energy, and intracellular stress conditions in Listeria monocytogenes. Appl. Environ. Microbiol. 70:5349-5356.
14. Chaturongakul, S., and K. J. Boor. 2006. Sigma B activation under environmental and energy stress conditions in Listeria monocytogenes. Appl. Environ. Microbiol. 72:5197-5203.
15. Dramsi, S., I. Biswas, E. Maguin, L. Braun, P. Mastroeni, and P. Cossart. 1995. Entry of Listeria monocytogenes into hepatocytes requires expression of inlB, a surface protein of the internalin multigene family. Mol. Microbiol. 16:251-261.
16. Dramsi, S., P. Dehoux, M. Lebrun, P. L. Goossens, and P. Cossart. 1997. Identification of four new members of the internalin multigene family of Listeria monocytogenes EGD. Infect. Immun. 65:1615-1625.
17. Dramsi, S., C. Kocks, C. Forestier, and P. Cossart. 1993. Internalin-mediated invasion of epithelial cells by Listeria monocytogenes is regulated by the bacterial growth state, temperature and the pleiotropic activator PrfA. Mol. Microbiol. 9:931-941.
18. Engelbrecht, F., S. K. Chun, C. Ochs, J. Hess, F. Lottspeich, W. Goebel, and Z. Sokolovic. 1996. A new PrfA-regulated gene of Listeria monocytogenes encoding a small, secreted protein which belongs to the family of internalins. Mol. Microbiol. 21:823-837.
19. Farber, J. M., and P. I. Peterkin. 1991. Listeria monocytogenes, a food-borne pathogen. Microbiol. Rev. 55:476-511.
20. Ferreira, A., C. P. O'Byrne, and K. J. Boor. 2001. Role of sigma B in heat, ethanol, acid, and oxidative stress resistance and during carbon starvation in Listeria monocytogenes. Appl. Environ. Microbiol. 67:4454-4457.
21. Fraser, K. R., D. Sue, M. Wiedmann, K. Boor, and C. P. O'Byrne. 2003. Role of sigma B in regulating the compatible solute uptake systems of Listeria monocytogenes: osmotic induction of OpuC is sigma B dependent. Appl. Environ. Microbiol. 69:2015-2022.
22. Freitag, N. E., L. Rong, and D. A. Portnoy. 1993. Regulation of the PrfA transcriptional activator of Listeria monocytogenes: multiple promoter elements contribute to intracellular growth and cell-to-cell spread. Infect. Immun. 61:2537-2544.
23. Garner, M. R., K. E. James, M. C. Callahan, M. Wiedmann, and K. J. Boor. 2006. 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. 72:5384-5395.
24. Gellin, B. G., and C. V. Broome. 1989. Listeriosis. JAMA 261:1313-1320.
25. Gilbreth, S. E., A. K. Benson, and R. W. Hutkins. 2004. Catabolite repression and virulence gene expression in Listeria monocytogenes. Curr. Microbiol. 49:95-98.
26. Han, Y., D. Zhou, X. Pang, L. Zhang, Y. Song, Z. Tong, J. Bao, E. Dai, J. Wang, Z. Guo, J. Zhai, Z. Du, X. Wang, P. Huang, and R. Yang. 2005. Comparative transcriptome analysis of Yersinia pestis in response to hyperosmotic and high-salinity stress. Res. Microbiol. 156:403-415.
27. Heusipp, G., M. A. Schmidt, and V. L. Miller. 2003. Identification of rpoE and nadB as host responsive elements of Yersinia enterocolitica. FEMS Microbiol. Lett. 226:291-298.
28. Huillet, E., S. Larpin, P. Pardon, and P. Berche. 1999. Identification of a new locus in Listeria monocytogenes involved in cellobiose-dependent repression of hly expression. FEMS Microbiol. Lett. 174:265-272.
29. Ireton, K., B. Payrastre, H. Chap, W. Ogawa, H. Sakaue, M. Kasuga, and P. Cossart. 1996. A role for phosphoinositide 3-kinase in bacterial invasion. Science 274:780-782.
30. Ireton, K., B. Payrastre, and P. Cossart. 1999. The Listeria monocytogenes protein InlB is an agonist of mammalian phosphoinositide 3-kinase. J. Biol. Chem. 274:17025-17032.
31. Jonquières, R., J. Pizarro-Cerda, and P. Cossart. 2001. Synergy between the N- and C-terminal domains of InlB for efficient invasion of non-phagocytic cells by Listeria monocytogenes. Mol. Microbiol. 42:955-965.
32. Kazmierczak, M. J., S. C. Mithoe, K. J. Boor, and M. Wiedmann. 2003. Listeria monocytogenes sigma B regulates stress response and virulence functions. J. Bacteriol. 185:5722-5734.
33. Kazmierczak, M. J., M. Wiedmann, and K. J. Boor. 2006. Contributions of Listeria monocytogenes sigma B and PrfA to expression of virulence and stress response genes during extra- and intracellular growth. Microbiology 152:1827-1838.
34. Khelef, N., M. Lecuit, H. Bierne, and P. Cossart. 2006. Species specificity of the Listeria monocytogenes InlB protein. Cell Microbiol. 8:457-470.
35. Kim, H., K. J. Boor, and H. Marquis. 2004. Listeria monocytogenes sigma B contributes to invasion of human intestinal epithelial cells. Infect. Immun. 72:7374-7378.
36. Kim, H., H. Marquis, and K. J. Boor. 2005. Sigma B contributes to Listeria monocytogenes invasion by controlling expression of inlA and inlB. Microbiology 151:3215-3222.
37. Kreft, J., and J. A Vazquez-Boland. 2001. Regulation of virulence genes in Listeria. Int. J. Med. Microbiol. 91:145-157.
38. Lecuit, M., S. Dramsi, C. Gottardi, M. Fedor-Chaiken, B. Gumbiner, and P. Cossart. 1999. A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes. EMBO J. 18:3956-3963.
39. Lecuit, M., D. M. Nelson, S. D. Smith, H. Khun, M. Huerre, M. C. Vacher-Lavenu, J. I. Gordon, and P. Cossart. 2004. Targeting and crossing of the human maternofetal barrier by Listeria monocytogenes: role of internalin interaction with trophoblast E-cadherin. Proc. Natl. Acad. Sci. USA 101:6152-6157.
40. Lecuit, M., S. Vandormael-Pournin, J. Lefort, M. Huerre, P. Gounon, C. Dupuy, C. Babinet, and P. Cossart. 2001. A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science 292:1722-1725.
41. Leimeister-Wachter, M., E. Domann, and T. Chakraborty. 1992. The expression of virulence genes in Listeria monocytogenes is thermoregulated. J. Bacteriol. 174:947-952.
42. Luo, Q., M. Rauch, A. K. Marr, S. Muller-Altrock, and W. Goebel. 2004. In vitro transcription of the Listeria monocytogenes virulence genes inlC and mpl reveals overlapping PrfA-dependent and -independent promoters that are differentially activated by GTP. Mol. Microbiol. 52:39-52.
43. McLauchlin, J. 1997. Animal and human listeriosis: a shared problem? Vet. J. 153:3-5.
44. Mengaud, J., S. Dramsi, E. Gouin, J. A. Vazquez-Boland, G. Milon, and P. Cossart. 1991. Pleiotropic control of Listeria monocytogenes virulence factors by a gene that is autoregulated. Mol. Microbiol. 5:2273-2283.
45. Mengaud, J., H. Ohayon, P. Gounon, R. M. Mege, and P. Cossart. 1996. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84:923-932.
46. Milenbachs, A. A., D. P. Brown, M. Moors, and P. Youngman. 1997. Carbon-source regulation of virulence gene expression in Listeria monocytogenes. Mol. Microbiol. 23:1075-1085.
47. Milenbachs Lukowiak, A., K. J. Mueller, N. E. Freitag, and P. Youngman. 2004. Deregulation of Listeria monocytogenes virulence gene expression by two distinct and semi-independent pathways. Microbiology 150:321-333.
48. Milohanic, E., P. Glaser, J. Y. Coppee, L. Frangeul, Y. Vega, J. A Vazquez-Boland, F. Kunst, P. Cossart, and C. Buchrieser. 2003. Transcriptome analysis of Listeria monocytogenes identifies three groups of genes differently regulated by PrfA. Mol. Microbiol. 47:1613-1625.
49. Nadon, C. A., B. M. Bowen, M. Wiedmann, and K. J. Boor. 2002. Sigma B contributes to PrfA-mediated virulence in Listeria monocytogenes. Infect. Immun. 70:3948-3952.
50. Parida, S. K., E. Domann, M. Rohde, S. Muller, A. Darji, T. Hain, J. Wehland, and T. Chakraborty. 1998. Internalin B is essential for adhesion and mediates the invasion of Listeria monocytogenes into human endothelial cells. Mol. Microbiol. 28:81-93.
51. Park, S. F., and R. G. Kroll. 1993. Expression of listeriolysin and phosphatidylinositol-specific phospholipase C is repressed by the plant-derived molecule cellobiose in Listeria monocytogenes. Mol. Microbiol. 8:653-661.
52. Rauch, M., Q. Luo, S. Muller-Altrock, and W. Goebel. 2005. SigB-dependent in vitro transcription of prfA and some newly identified genes of Listeria monocytogenes whose expression is affected by PrfA in vivo. J. Bacteriol. 187:800-804.
53. Renzoni, A., A. Klarsfeld, S. Dramsi, and P. Cossart. 1997. Evidence that PrfA, the pleiotropic activator of virulence genes in Listeria monocytogenes, can be present but inactive. Infect. Immun. 65:1515-1518.
54. Ripio, M. T., G. Dominguez-Bernal, M. Suarez, K. Brehm, P. Berche, and J. A. Vazquez-Boland. 1996. Transcriptional activation of virulence genes in wild-type strains of Listeria monocytogenes in response to a change in the extracellular medium composition. Res. Microbiol. 147:371-384.
55. Schwab, U., B. Bowen, C. Nadon, M. Wiedmann, and K. J. Boor. 2005. The Listeria monocytogenes prfAP2 promoter is regulated by sigma B in a growth phase dependent manner. FEMS Microbiol. Lett. 245:329-336.
56. Sheehan, B., A. Klarsfeld, T. Msadek, and P. Cossart. 1995. Differential activation of virulence gene expression by PrfA, the Listeria monocytogenes virulence regulator. J. Bacteriol. 177:6469-6476.
57. Shetron-Rama, L. M., K. Mueller, J. M. Bravo, H. G. Bouwer, S. S. Way, and N. E. Freitag. 2003. Isolation of Listeria monocytogenes mutants with high-level in vitro expression of host cytosol-induced gene products. Mol. Microbiol. 48:1537-1551.
58. Sleator, R. D., H. H. Wemekamp-Kamphuis, C. G. Gahan, T. Abee, and C. Hill. 2005. A PrfA-regulated bile exclusion system (BilE) is a novel virulence factor in Listeria monocytogenes. Mol. Microbiol. 55:1183-1195.
59. Sue, D., K. J. Boor, and M. Wiedmann. 2003. 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 149:3247-3256.
60. Sue, D., D. Fink, M. Wiedmann, and K. J. Boor. 2004. Sigma B-dependent gene induction and expression in Listeria monocytogenes during osmotic and acid stress conditions simulating the intestinal environment. Microbiology 150:3843-3855.
61. Tsai, Y. H., R. H. Orsi, K. K. Nightingale, and M. Wiedmann. 2006. Listeria monocytogenes internalins are highly diverse and evolved by recombination and positive selection. Infect. Genet. Evol. 6:378-389.
62. Vandesompele, J., K. De Preter, F. Pattyn, B. Poppe, N. Van Roy, A. De Paepe, and F. Speleman. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3:RESEARCH0034.
63. Wiedmann, M., T. J. Arvik, R. J. Hurley, and K. J. Boor. 1998. General stress transcription factor sigma B and its role in acid tolerance and virulence of Listeria monocytogenes. J. Bacteriol. 180:3650-3656.
64. Wong, K. K., and N. E. Freitag. 2004. A novel mutation within the central Listeria monocytogenes regulator PrfA that results in constitutive expression of virulence gene products. J. Bacteriol. 186:6265-6276.