A novel C-terminal mutation resulting in constitutive activation of the Listeria monocytogenes central virulence regulatory factor PrfA

Microbiology

Volumn 157, Issue 11, 2011, Pages 3138-3149

  Xayarath, Bobbi ^a   Smart, Jennifer I ^a   Mueller, Kimberly J ^a   Freitag, Nancy E ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; TRANSCRIPTION FACTOR; TRANSCRIPTIONAL ACTIVATOR PRFA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL MUTATION; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BACTERIUM REPLICATION; BINDING AFFINITY; BROTH DILUTION; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; DNA BINDING; ENZYME ACTIVITY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; LISTERIA MONOCYTOGENES; MUTAGENESIS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; TRANSCRIPTION INITIATION; WESTERN BLOTTING;

ANIMALS; BACTERIAL PROTEINS; CELLS, CULTURED; DNA-BINDING PROTEINS; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; LISTERIA MONOCYTOGENES; MICE; MUTATION; PEPTIDE TERMINATION FACTORS; PROTEIN STRUCTURE, TERTIARY; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES; MAMMALIA; MUS;

EID: 80155164880     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.049957-0     Document Type: Article

References (59)

1. Alonzo, F., III, Port, G. C., Cao, M. & Freitag, N. E. (2009). The posttranslocation chaperone PrsA2 contributes to multiple facets of Listeria monocytogenes pathogenesis. Infect Immun 77, 2612-2623.
2. Bitar, A. P., Cao, M. & Marquis, H. (2008). The metalloprotease of Listeria monocytogenes is activated by intramolecular autocatalysis. J Bacteriol 190, 107-111.
3. Bruno, J. C., Jr & Freitag, N. E. (2010). Constitutive activation of PrfA tilts the balance of Listeria monocytogenes fitness towards life within the host versus environmental survival. PLoS ONE 5, e15138.
4. Camilli, A., Paynton, C. R. & Portnoy, D. A. (1989). Intracellular methicillin selection of Listeria monocytogenes mutants unable to replicate in a macrophage cell line. Proc Natl Acad Sci U S A 86, 5522-5526.
5. Camilli, A., Tilney, L. G. & Portnoy, D. A. (1993). Dual roles of plcA in Listeria monocytogenes pathogenesis. Mol Microbiol 8, 143-157.
6. Centers for Disease Control and Prevention (2004). Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food - selected sites, United States, 2003. MMWR Morb Mortal Wkly Rep 53, 338-343.
7. Cossart, P. (2007). Listeriology (1926-2007): the rise of a model pathogen. Microbes Infect 9, 1143-1146.
8. Cossart, P. & Toledo-Arana, A. (2008). Listeria monocytogenes, a unique model in infection biology: an overview. Microbes Infect 10, 1041-1050.
9. Czuprynski, C. J. (2005). Listeria monocytogenes: silage, sandwiches and science. Anim Health Res Rev 6, 211-217.
10. Delgado, A. R. (2008). Listeriosis in pregnancy. J Midwifery Womens Health 53, 255-259.
11. Drevets, D. A. & Bronze, M. S. (2008). Listeria monocytogenes: epidemiology, human disease, and mechanisms of brain invasion. FEMS Immunol Med Microbiol 53, 151-165.
12. Dussurget, O. (2008). New insights into determinants of Listeria monocytogenes virulence. Int Rev Cell Mol Biol 270, 1-38.
13. Eiting, M., Hagelüken, G., Schubert, W. D. & Heinz, D. W. (2005). The mutation G145S in PrfA, a key virulence regulator of Listeria monocytogenes, increases DNA-binding affinity by stabilizing the HTH motif. Mol Microbiol 56, 433-446.
14. Freitag, N. E. (2006). From hot dogs to host cells: how the bacterial pathogen Listeria monocytogenes regulates virulence gene expression. Future Microbiol 1, 89-101.
15. Freitag, N. E. & Portnoy, D. A. (1994). Dual promoters of the Listeria monocytogenes prfA transcriptional activator appear essential in vitro but are redundant in vivo. Mol Microbiol 12, 845-853.
16. Freitag, N. E., Port, G. C. & Miner, M. D. (2009). Listeria monocytogenes - from saprophyte to intracellular pathogen. Nat Rev Microbiol 7, 623-628.
17. Gandhi, M. & Chikindas, M. L. (2007). Listeria: a foodborne pathogen that knows how to survive. Int J Food Microbiol 113, 1-15.
18. Gray, M. J., Freitag, N. E. & Boor, K. J. (2006). How the bacterial pathogen Listeria monocytogenes mediates the switch from environmental Dr. Jekyll to pathogenic Mr. Hyde. Infect Immun 74, 2505-2512.
19. Harman, J. G. (2001). Allosteric regulation of the cAMP receptor protein. Biochim Biophys Acta 1547, 1-17.
20. Harman, J. G., McKenney, K. & Peterkofsky, A. (1986). Structure-function analysis of three cAMP-independent forms of the cAMP receptor protein. J Biol Chem 261, 16332-16339.
21. Herler, M., Bubert, A., Goetz, M., Vega, Y., Vazquez-Boland, J. A. & Goebel, W. (2001). Positive selection of mutations leading to loss or reduction of transcriptional activity of PrfA, the central regulator of Listeria monocytogenes virulence. J Bacteriol 183, 5562-5570.
22. Ireton, K. & Cossart, P. (1997). Host-pathogen interactions during entry and actin-based movement of Listeria monocytogenes. Annu Rev Genet 31, 113-138.
23. Joseph, B. & Goebel, W. (2007). Life of Listeria monocytogenes in the host cells' cytosol. Microbes Infect 9, 1188-1195.
24. Kreft, J., Vázquez-Boland, J. A., Altrock, S., Dominguez-Bernal, G. & Goebel, W. (2002). Pathogenicity islands and other virulence elements in Listeria. Curr Top Microbiol Immunol 264, 109-125.
25. Lampidis, R., Gross, R., Sokolovic, Z., Goebel, W. & Kreft, J. (1994). The virulence regulator protein of Listeria ivanovii is highly homologous to PrfA from Listeria monocytogenes and both belong to the Crp-Fnr family of transcription regulators. Mol Microbiol 13, 141-151.
26. Lauer, P., Chow, M. Y., Loessner, M. J., Portnoy, D. A. & Calendar, R. (2002). Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. J Bacteriol 184, 4177-4186.
27. Lecuit, M. (2007). Human listeriosis and animal models. Microbes Infect 9, 1216-1225.
28. Lynch, M., Painter, J., Woodruff, R., Braden, C. & Centers for Disease Control and Prevention (2006). Surveillance for foodborne-disease outbreaks - United States, 1998-2002. MMWR Surveill Summ 55, 1-42.
29. Marquis, H., Doshi, V. & Portnoy, D. A. (1995). The broad-range phospholipase C and a metalloprotease mediate listeriolysin Oindependent escape of Listeria monocytogenes from a primary vacuole in human epithelial cells. Infect Immun 63, 4531-4534.
30. Marr, A. K., Joseph, B., Mertins, S., Ecke, R., Müller-Altrock, S. & Goebel, W. (2006). Overexpression of PrfA leads to growth inhibition of Listeria monocytogenes in glucose-containing culture media by interfering with glucose uptake. J Bacteriol 188, 3887-3901.
31. Mead, P. S., Dunne, E. F., Graves, L., Wiedmann, M., Patrick, M., Hunter, S., Salehi, E., Mostashari, F., Craig, A. & other authors (2006). Nationwide outbreak of listeriosis due to contaminated meat. Epidemiol Infect 134, 744-751.
32. Mertins, S., Joseph, B., Goetz, M., Ecke, R., Seidel, G., Sprehe, M., Hillen, W., Goebel, W. & Müller-Altrock, S. (2007). Interference of components of the phosphoenolpyruvate phosphotransferase system with the central virulence gene regulator PrfA of Listeria monocytogenes. J Bacteriol 189, 473-490.
33. Miner, M. D., Port, G. C., Bouwer, H. G., Chang, J. C. & Freitag, N. E. (2008a). A novel prfA mutation that promotes Listeria monocytogenes cytosol entry but reduces bacterial spread and cytotoxicity. Microb Pathog 45, 273-281.
34. Miner, M. D., Port, G. C. & Freitag, N. E. (2008b). Functional impact of mutational activation on the Listeria monocytogenes central virulence regulator PrfA. Microbiology 154, 3579-3589.
35. Mueller, K. J. & Freitag, N. E. (2005). Pleiotropic enhancement of bacterial pathogenesis resulting from the constitutive activation of the Listeria monocytogenes regulatory factor PrfA. Infect Immun 73, 1917-1926.
36. O'Neil, H. S. & Marquis, H. (2006). Listeria monocytogenes flagella are used for motility, not as adhesins, to increase host cell invasion. Infect Immun 74, 6675-6681.
37. Port, G. C. & Freitag, N. E. (2007). Identification of novel Listeria monocytogenes secreted virulence factors following mutational activation of the central virulence regulator, PrfA. Infect Immun 75, 5886-5897.
38. Portnoy, D. A., Jacks, P. S. & Hinrichs, D. J. (1988). Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med 167, 1459-1471.
39. Ramaswamy, V., Cresence, V. M., Rejitha, J. S., Lekshmi, M. U., Dharsana, K. S., Prasad, S. P. & Vijila, H. M. (2007). Listeria - review of epidemiology and pathogenesis. J Microbiol Immunol Infect 40, 4-13.
40. Ripio, M. T., Domínguez-Bernal, G., Lara, M., Suárez, M. & Vazquez-Boland, J. A. (1997). A Gly145Ser substitution in the transcriptional activator PrfA causes constitutive overexpression of virulence factors in Listeria monocytogenes. J Bacteriol 179, 1533-1540.
41. Roche, S. M., Gracieux, P., Albert, I., Gouali, M., Jacquet, C., Martin, P. M. & Velge, P. (2003). Experimental validation of low virulence in field strains of Listeria monocytogenes. Infect Immun 71, 3429-3436.
42. Scortti, M., Monzó, H. J., Lacharme-Lora, L., Lewis, D. A. & Vázquez-Boland, J. A. (2007). The PrfA virulence regulon. Microbes Infect 9, 1196-1207.
43. Shetron-Rama, L. M., Marquis, H., Bouwer, H. G. & Freitag, N. E. (2002). Intracellular induction of Listeria monocytogenes actA expression. Infect Immun 70, 1087-1096.
44. Shetron-Rama, L. M., Mueller, K., Bravo, J. M., Bouwer, H. G., Way, S. S. & Freitag, N. E. (2003). Isolation of Listeria monocytogenes mutants with high-level in vitro expression of host cytosol-induced gene products. Mol Microbiol 48, 1537-1551.
45. Smith, M. A., Takeuchi, K., Anderson, G., Ware, G. O., McClure, H. M., Raybourne, R. B., Mytle, N. & Doyle, M. P. (2008). Dose-response model for Listeria monocytogenes-induced stillbirths in nonhuman primates. Infect Immun 76, 726-731.
46. Smith, B., Kemp, M., Ethelberg, S., Schiellerup, P., Bruun, B. G., Gerner-Smidt, P. & Christensen, J. J. (2009). Listeria monocytogenes: maternal-foetal infections in Denmark 1994-2005. Scand J Infect Dis 41, 21-25.
47. Sun, A. N., Camilli, A. & Portnoy, D. A. (1990). Isolation of Listeria monocytogenes small-plaque mutants defective for intracellular growth and cell-to-cell spread. Infect Immun 58, 3770-3778.
48. Swaminathan, B. & Gerner-Smidt, P. (2007). The epidemiology of human listeriosis. Microbes Infect 9, 1236-1243.
49. Swaminathan, B., Gerner-Smidt, P. & Whichard, J. M. (2006). Foodborne disease trends and reports. Foodborne Pathog Dis 3, 316-318.
50. Tan, G. S., Kelly, P., Kim, J. & Wartell, R. M. (1991). Comparison of cAMP receptor protein (CRP) and a cAMP-independent form of CRP by Raman spectroscopy and DNA binding. Biochemistry 30, 5076-5080.
51. Toledo-Arana, A., Dussurget, O., Nikitas, G., Sesto, N., Guet-Revillet, H., Balestrino, D., Loh, E., Gripenland, J., Tiensuu, T. & other authors (2009). The Listeria transcriptional landscape from saprophytism to virulence. Nature 459, 950-956.
52. Vázquez-Boland, J. A., Kuhn, M., Berche, P., Chakraborty, T., Domínguez-Bernal, G., Goebel, W., González-Zorn, B., Wehland, J. & Kreft, J. (2001). Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14, 584-640.
53. Vega, Y., Dickneite, C., Ripio, M. T., Böckmann, R., González-Zorn, B., Novella, S., Domínguez-Bernal, G., Goebel, W. & Vázquez-Boland, J. A. (1998). Functional similarities between the Listeria monocytogenes virulence regulator PrfA and cyclic AMP receptor protein: the PrfA* (Gly145Ser) mutation increases binding affinity for target DNA. J Bacteriol 180, 6655-6660.
54. Vega, Y., Rauch, M., Banfield, M. J., Ermolaeva, S., Scortti, M., Goebel, W. & Vázquez-Boland, J. A. (2004). New Listeria monocytogenes prfA* mutants, transcriptional properties of PrfA* proteins and structure-function of the virulence regulator PrfA. Mol Microbiol 52, 1553-1565.
55. Velge, P., Herler, M., Johansson, J., Roche, S. M., Témoin, S., Fedorov, A. A., Gracieux, P., Almo, S. C., Goebel, W. & Cossart, P. (2007). A naturally occurring mutation K220T in the pleiotropic activator PrfA of Listeria monocytogenes results in a loss of virulence due to decreasing DNA-binding affinity. Microbiology 153, 995-1005.
56. Wong, K. K. & Freitag, N. E. (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.
57. Wong, K. K., Bouwer, H. G. & Freitag, N. E. (2004). Evidence implicating the 59 untranslated region of Listeria monocytogenes actA in the regulation of bacterial actin-based motility. Cell Microbiol 6, 155-166.
58. Xayarath, B., Marquis, H., Port, G. C. & Freitag, N. E. (2009). Listeria monocytogenes CtaP is a multifunctional cysteine transport-associated protein required for bacterial pathogenesis. Mol Microbiol 74, 956-973.
59. Youngman, P. (1987). Plasmid vectors recovering and exploiting Tn917 transposons in Bacillus and other Gram-positive bacteria. In Plasmids: a Practical Approach, 1st edn, pp 79-103. Edited by K. G. Hardy. Oxford: IRL Press.