Pleiotropic enhancement of bacterial pathogenesis resulting from the constitutive activation of the Listeria monocytogenes regulatory factor PrfA

Infection and Immunity

Volumn 73, Issue 4, 2005, Pages 1917-1926

  Mueller, Kimberly J ^a   Freitag, Nancy E ^a,b  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BACTERIAL PROTEIN; CELL SURFACE PROTEIN; GENE PRODUCT; HEMOLYSIN; LISTERIOLYSIN; PHOSPHOLIPASE; PROTEIN ACTA; PROTEIN INLA; PROTEIN INLB; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PRFA; UNCLASSIFIED DRUG; BACTERIAL TOXIN; HEAT SHOCK PROTEIN; HLYA PROTEIN, LISTERIA MONOCYTOGENES; PEPTIDE CHAIN TERMINATION RELEASE FACTOR 1; PEPTIDE CHAIN-TERMINATION RELEASE FACTOR 1; TRANSACTIVATOR PROTEIN; TRANSLATION TERMINATION FACTOR;

ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL VIRULENCE; CELL MEMBRANE; CELL VACUOLE; CONTROLLED STUDY; CYTOSOL; DNA SEQUENCE; EPITHELIUM CELL; GENE EXPRESSION; HOST CELL; HUMAN; HUMAN CELL; LISTERIA MONOCYTOGENES; NONHUMAN; PATHOGENESIS; PHENOTYPE; PLEIOTROPY; PRFA GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; VIRULENCE;

ACTINS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CELL MEMBRANE; CYTOSOL; HEAT-SHOCK PROTEINS; HEMOLYSIN PROTEINS; HUMANS; LISTERIA MONOCYTOGENES; PEPTIDE TERMINATION FACTORS; TRANS-ACTIVATORS; VACUOLES; VIRULENCE;

EID: 16244408601     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.4.1917-1926.2005     Document Type: Article

References (65)

1. Alvarez-Dominguez, C., J. A. Vazquez-Boland, E. Carrasco-Marin, P. Lopez-Mato, and F. Leyva-Cobian. 1997. Host cell heparan sulfate proteoglycans mediate attachment and entry of Listeria monocytogenes, and the listerial surface protein ActA is involved in heparan sulfate receptor recognition. Infect. Immun. 65:78-88.
2. 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.
3. 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.
4. 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.
5. Braun, L., H. Ohayon, and P. Cossart. 1998. The InIB protein of Listeria monocytogenes is sufficient to promote entry into mammalian cells. Mol. Microbiol. 27:1077-1087.
6. Brehm, K., M. T. Ripio, J. Kreft, and J. A. Vazquez-Boland. 1999. The bvr locus of Listeria monocytogenes mediates virulence gene repression by beta-glucosides. J. Bacteriol. 181:5024-5032.
7. Brundage, R. A., G. A. Smith, A. Camilli, J. A. Theriot, and D. A. Portnoy. 1993. Expression and phosphorylation of the Listeria monocytogenes ActA protein in mammalian cells. Proc. Nad. Acad. Sci. USA 90:11890-11894.
8. Bubert, A., Z. Sokolovic, S.-K. Chun, L. Papatheodorou, A. Simm, and W. Goebel. 1999. Differential expression of Listeria monocytogenes virulence genes in mammalian host cells. Mol. Gen. Genet. 261:323-336.
9. Camilli, A., C. R. Paynton, and D. A. Portnoy. 1989. Intracellular methicillin selection of Listeria monocytogenes mutants unable to replicate in a macrophage cell line. Proc. Natl. Acad. Sci. USA 86:5522-5526.
10. Camilli, A., L. G. Tilney, and D. A. Portnoy. 1993. Dual roles of plcA in Listeria monocytogenes pathogenesis. Mol. Microbiol. 8:143-157.
11. Conte, M. P., G. Petrone, A. M. Di Biase, C. Longhi, M. Penta, A. Tinari, F. Superti, G. Fabozzi, P. Visca, and L. Seganti. 2002. Effect of add adaptation on the fate of Listeria monocytogenes in THP-1 human macrophages activated by gamma interferon. Infect. Immun. 70:4369-4378.
12. Cossart, P., J. Pizarro-Cerda, and M. Lecuit. 2003. Invasion of mammalian cells by Listeria monocytogenes: functional mimicry to subvert cellular functions. Trends Cell Biol. 13:23-31.
13. Cossart, P., and P. J. Sansonetti. 2004. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304:242-248.
14. Dabiri, G. A., J. M. Sanger, D. A. Portnoy, and F. S. Southwick. 1990. Listeria monocytogenes moves rapidly through the host cytoplasm by inducing directional actin assembly. Proc. Natl. Acad. Sci. USA 87:6068-6072.
15. Decatur, A. L., and D. A. Portnoy. 2000. A PEST-like sequence in listeriolysin O essential for Listeria monocytogenes pathogenicity. Science 290:992-995.
16. Dramsi, S., and P. Cossart. 2003. Listeriolysin O-mediated calcium influx potentiates entry of Listeria monocytogenes into the human Hep-2 epithelial cell line. Infect. Immun. 71:3614-3618.
17. Farber, J. M., and P. I. Peterkin. 1991. Listeria monocytogenes, a food-borne pathogen. Microbiol. Rev. 55:476-511.
18. Freitag, N. E. 2000. Genetic tools for use with Listeria monocytogenes, p. 488-498. In V. A. Fischetti, R. P. Novick, J. J. Ferretti, D. A. Portnoy, and J. I. Rood (ed.), Gram-positive pathogens. ASM Press, Washington D.C.
19. Freitag, N. E., and K. E. Jacobs. 1999. Examination of Listeria monocytogenes intracellular gene expression by using the green fluorescent protein of Aequorea victoria. Infect. Immun. 67:1844-1852.
20. Freitag, N. E., L. Kong, 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.
21. Freitag, N. E., P. Youngman, and D. A. Portnoy. 1992. Transcriptional activation of the Listeria monocytogenes hemolysin gene in Bacillus subtilis. J. Bacteriol. 174:1293-1298.
22. Gaillard, J. L., P. Berche, C. Frehel, E. Gouin, and P. Cossart. 1991. Entry of Listeria monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell 65:1127-1141.
23. Gaillard, J. L., P. Berche, and P. Sansonetti. 1986. Transposon mutagenesis as a tool to study the role of hemolysin in the virulence of Listeria monocytogenes. Infect. Immun. 52:50-55.
24. Garges, S., and S. Adhya. 1988. Cyclic AMP-induced conformational change of cyclic AMP receptor protein (CRP): intragenic suppressors of cyclic AMP-independent CRP mutations. J. Bacteriol. 170:1417-1422.
25. Glomski, I. J., M. M. Gedde, A. W. Tsang, J. A. Swanson, and D. A. Portnoy. 2002. The Listeria monocytogenes hemolysin has an acidic pH optimum to compartmentalize activity and prevent damage to infected host cells. J. Cell Biol. 156:1029-1038.
26. Gray, M. L., and A. H. Killinger. 1966. Listeria monocytogenes and listeric infections. Bacteriol. Rev. 30:309-382.
27. Grundling, A., M. D. Gonzalez, and D. E. Higgins. 2003. Requirement of the Listeria monocytogenes broad-range phospholipase PC-PLC during infection of human epithelial cells. J. Bacteriol. 185:6295-6307.
28. Ireton, K., and P. Cossart. 1997. Host-pathogen interactions during entry and actin-based movement of Listeria monocytogenes. Annu. Rev. Genet. 31:113-138.
29. 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.
30. Johansson, J., P, Mandin, A. Renzoni, C. Chiaruttini, M. Springer, and P. Cossart. 2002. An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 110:551.
31. Jones, S., and D. A. Portnoy. 1994. Characterization of Listeria monocytogenes pathogenesis in a strain expressing perfringolysin O in place of listeriolysin O. Infect. Immun. 62:5608-5613.
32. Kathariou, S., P. Metz, H. Hof, and W. Goebel. 1987. Tn916-induced mutations in the hemolysin determinant affecting virulence of Listeria monocytogenes. J. Bacteriol. 169:1291-1297.
33. Kreft, J., and J. A. Vazquez-Boland. 2001. Regulation of virulence genes in Listeria. Int. J. Med. Microbiol. 291:145-157.
34. Lacayo, C. I., and J. A. Theriot. 2004. Listeria monocytogenes actin-based motility varies depending on subcellular location: a kinematic probe for cytoarchitecture. Mol. Biol. Cell 15:2164-2175.
35. Lauer, P., J. A. Theriot, J. Skoble, M. D. Welch, and D. A. Portnoy. 2001. Systematic mutational analysis of the amino-terminal domain of the Listeria monocytogenes ActA protein reveals novel functions in actin-based motility. Mol. Microbiol. 42:1163-1177.
36. Leimeister-Wachter, M., C. Haffner, E. Domann, W. Goebel, and T. Chakraborty. 1990. Identification of a gene that positively regulates expression of listeriolysin, the major virulence factor of Listeria monocytogenes. Proc. Natl. Acad. Sci. USA 87:8336-8340.
37. Lety, M. A., C. Frehel, P. Berche, and A. Charbit. 2002. Critical role of the N-terminal residues of listeriolysin O in phagosomal escape and virulence of Listeria monocytogenes. Mol. Microbiol. 46:367-379.
38. Marquis, H., V. Doshi, and D. A. Portnoy. 1995. The broad-range phospholipase C and a metalloprotease mediate listeriolysin O-independent escape of Listeria monocytogenes from a primary vacuole in human epithelial cells. Infect. Immun. 63:4531-4534.
39. Marquis, H., and E. J. Hager. 2000. pH-regulated activation and release of a bacteria-associated phospholipase C during intracellular infection by Listeria monocytogenes. Mol. Microbiol. 35:289-298.
40. 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.
41. 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 Listeria monocytogenes into epithelial cells. Cell 84:923-932.
42. Millenbachs, 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.
43. Moors, M. A., B. Levitt, P. Youngman, and D. A. Portnoy. 1999. Expression of listeriolysin O and ActA by intracellular and extracellular Listeria monocytogenes. Infect. Immun. 67:131-139.
44. Mounier, J., A. Ryter, M. Coquis-Rondon, and P. J. Sansonetti. 1990. Intracellular and cell-to-cell spread of Listeria monocytogenes involves interaction with F-actin in the enterocytelike cell line Caco-2. Infect. Immun. 58:1048-1058.
45. Myers, J. T., A. W. Tsang, and J. A. Swanson. 2003. Localized reactive oxygen and nitrogen intermediates inhibit escape of Listeria monocytogenes from vacuoles in activated macrophages. J. Immunol. 171:5447-5453.
46. Park, S. F., G. S. A. B. Stewart, and R. G. Kroll. 1992. The use of bacterial luciferase for monitoring the environmental regulation of expression of genes encoding virulence factors in Listeria monocytogenes. J. Gen. Microbiol. 138:2619-2627.
47. Paschen, A., K. E. Dittmar, R. Grenningloh, M. Rohde, D. Schadendorf, E. Domann, T. Chakraborty, and S. Weiss. 2000. Human dendritic cells infected by Listeria monocytogenes: induction of maturation, requirements for phagolysosomal escape and antigen presentation capacity. Eur. J. Immunol. 30:3447-3456.
48. Portnoy, D. A., T. Chakraborty, W. Goebel, and P. Cossart. 1992. Molecular determinants of Listeria monocytogenes pathogenesis. Infect. Immun. 60: 1263-1267.
49. Portnoy, D. A., P. S. Jacks, and D. J. Hinrichs. 1988. Role of hemolysin for the intracellular growth of Listeria monocytogenes. J. Exp. Med. 167:1459-1471.
50. Portnoy, D. A., R. D. Schreiber, P. Connelly, and L. G. Tilney. 1989. Gamma Interferon limits access of Listeria monocytogenes to the macrophage cytoplasm. J. Exp. Med. 170:2141-2146.
51. Ripio, M.-T., G. Dominguez-Bernal, M. Lara, M. Suarez, and J.-A. Vazquez-Boland. 1997. A Gly145Ser substitution in the transcriptional activator PrfA causes constitutive overexpression of virulence factors in Listeria monocytogenes. J. Bacteriol. 179:1533-1540.
52. Sanger, J. M., B. Mittal, F. S. Southwick, and J. W. Sanger. 1990. Analysis of intracellular motility and actin polymerization induced by Listeria monocytogenes in PtK2 cells. J. Cell Biol. 111:415A.
53. Shetron-Rama, L. M., H. Marquis, H. G. A. Bouwer, and N. E. Freitag. 2002. Intracellular induction of Listeria monocytogenes actA expression. Infect. Immun. 70:1087-1096.
54. 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.
55. Smith, G. A., H. Marquis, S. Jones, N. C. Johnston, D. A. Portnoy, and H. Goldfine. 1995. The two distinct phospholipases C of Listeria monocytogenes have overlapping roles in escape from a vacuole and cell-to-cell spread. Infect. Immun. 63:4231-4237.
56. Smith, K., and P. Youngman. 1992. Use of a new integrational vector to investigate compartment-specific expression of the Bacillus subtilis spoIIM gene. Biochimie 74:705-711.
57. Suarez, M., B. Gonzalez-Zorn, Y. Vega, I. Chico-Calero, and J. A. Vazquez-Boland. 2001. A role for ActA in epithelial cell invasion by Listeria monocytogenes. Cell Microbiol. 3:853-864.
58. Theriot, J. A., T. J. Mitchison, L. G. Tilney, and D. A. Portnoy. 1992. The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization. Nature 357:257-260.
59. Thirumuruhan, R., K. Rajasnankar, A. A. Fedorov, T. Dodatko, M. R. Chance, P. Cossart, and S. C. Almo. 2003. Crystal structure of PrfA, the transcriptional regulator in Listeria monocytogenes. Protein Data Bank accession code 1OMI (http://www.rscb.org.pdb/).
60. Tilney, L. G., and D. A. Portnoy. 1989. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 109:1597-1608.
61. Vazquez-Boland, J. A., G. Dominguez-Bernal, B. Gonzalez-Zorn, J. Kreft, and W. Goebel. 2001. Pathogenicity islands and virulence evolution in Listeria. Microbes Infect. 3:571-584.
62. Vazquez-Boland, J. A., M. Kuhn, P. Berche, T. Chakraborty, G. Dominguez-Bernal, W. Goebel, B. Gonzalez-Zorn, J. Wehland, and J. Kreft. 2001. Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 14:584-640.
63. Vega, Y., C. Dickneite, M.-T. Ripio, R. Böckmann, B. Gonzalez-Zorn, S. Novella, G. Gominguez-Bernal, W. Goebel, and W. Vazquez-Boland. 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.
64. Wadsworth, S. J., and H. Goldfine. 2002. Mobilization of protein kinase C in macrophages induced by Listeria monocytogenes affects its internalization and escape from the phagosome. Infect. Immun. 70:4650-4660.
65. Wong, K. K., H. G. Bouwer, and N. E. Freitag. 2004. Evidence implicating the 5′ untranslated region of Listeria monocytogenes actA in the regulation of bacterial actin-based motility. Cell Microbiol. 6:155-166.