Constitutive activation of PrfA tilts the balance of Listeria monocytogenes fitness towards life within the host versus environmental survival

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Bruno Jr , Joseph C ^a   Freitag, Nancy E ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCEROL; MUTANT PROTEIN; PROTEIN PRFA; REGULATOR PROTEIN; SIGMA FACTOR; SIGMA FACTOR SIGB; SODIUM CHLORIDE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CARBON; GLUCOSE; PRFA PROTEIN, LISTERIA MONOCYTOGENES; SIGB PROTEIN, LISTERIA MONOCYTOGENES; TRANSLATION TERMINATION FACTOR;

ACIDITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BROTH DILUTION; CARBON SOURCE; CONTROLLED STUDY; EXPERIMENTAL INFECTION; GROWTH CURVE; HOST CELL; HOST PATHOGEN INTERACTION; IN VITRO STUDY; IN VIVO STUDY; INTESTINE; LISTERIA MONOCYTOGENES; LIVER; MIXED INFECTION; MONOCULTURE; MOUSE; NONHUMAN; OSMOTIC STRESS; PROTEIN FUNCTION; SPLEEN; STOMACH; ALLELE; ANIMAL; BACTERIOPHAGE; C57BL MOUSE; CHEMISTRY; CYTOSOL; GENETICS; METABOLISM; MUTATION; PROTEIN PROCESSING; STEM CELL;

ANIMALIA; BACTERIA (MICROORGANISMS); EUKARYOTA; LISTERIA MONOCYTOGENES;

ALLELES; ANIMALS; BACTERIAL PROTEINS; BACTERIOPHAGES; CARBON; CYTOSOL; GLUCOSE; GLYCEROL; LISTERIA MONOCYTOGENES; MICE; MICE, INBRED C57BL; MUTATION; PEPTIDE TERMINATION FACTORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGMA FACTOR; STEM CELLS;

EID: 78650082185     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015138     Document Type: Article

References (90)

1. Gray ML, Killinger AH (1966) Listeria monocytogenes and listeric infections. Bacteriol Rev 30: 309-382.
2. Gray MJ, Freitag NE, Boor KJ (2006) How the bacterial pathogen Listeria monocytogenes mediates the switch from environmental Dr. Jekyll to pathogenic Mr. Hyde. Infect Immun 74: 2505-2512.
3. Freitag NE, Port GC, Miner MD (2009) Listeria monocytogenes - from saprophyte to intracellular pathogen. Nat Rev Microbiol 7: 623-628.
4. Drevets DA, Bronze MS (2008) Listeria monocytogenes: epidemiology, human disease, and mechanisms of brain invasion. FEMS Immunol Med Microbiol 53: 151-165.
5. Vazquez-Boland JA, Kuhn M, Berche P, Chakraborty T, Dominguez-Bernal G, et al. (2001) Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14: 584-640.
6. Allerberger F, Wagner M (2010) Listeriosis: a resurgent foodborne infection. Clin Microbiol Infect 16: 16-23.
7. Bortolussi R (2008) Listeriosis: a primer. CMAJ 179: 795-797.
8. Swaminathan B, Gerner-Smidt P (2007) The epidemiology of human listeriosis. Microbes Infect 9: 1236-1243.
9. Ryser ET (1999) Foodborne Listeriosis. In: Ryser ET, Marth EH, eds. Listeria, Listeriosis, and Food Safety. 2nd ed. New York, NY: Marcel Dekker, Inc. pp 299-358.
10. Gottlieb SL, Newbern EC, Griffin PM, Graves LM, Hoekstra RM, et al. (2006) Multistate outbreak of Listeriosis linked to turkey deli meat and subsequent changes in US regulatory policy. Clin Infect Dis 42: 29-36.
11. MMWR (2008) Outbreak of Listeria monocytogenes infections associated with pasteurized milk from a local dairy-Massachusetts, 2007. MMWR Morb Mortal Wkly Rep 57: 1097-1100.
12. MMWR (2009) Preliminary FoodNet Data on the incidence of infection with pathogens transmitted commonly through food-10 States, 2008. MMWR Morb Mortal Wkly Rep 58: 333-337.
13. Fenlon DR (1999) Listeria monocytogenes in the Natural Environment. In: Ryser ET, Marth EH, eds. Listeria, listeriosis, and food safety. 2nd ed. New York, NY: Marcel Dekker. pp 21-38.
14. Abram F, Starr E, Karatzas KA, Matlawska-Wasowska K, Boyd A, et al. (2008) Identification of components of the sigma B regulon in Listeria monocytogenes that contribute to acid and salt tolerance. Appl Environ Microbiol 74: 6848-6858.
15. Schmid B, Klumpp J, Raimann E, Loessner MJ, Stephan R, et al. (2009) Role of cold shock proteins in growth of Listeria monocytogenes under cold and osmotic stress conditions. Appl Environ Microbiol 75: 1621-1627.
16. Oliver HF, Orsi RH, Wiedmann M, Boor KJ (2010) Listeria monocytogenes {sigma}B has a small core regulon and a conserved role in virulence but makes differential contributions to stress tolerance across a diverse collection of strains. Appl Environ Microbiol 76: 4216-4232.
17. Barbuddhe SB, Chakraborty T (2009) Listeria as an enteroinvasive gastrointestinal pathogen. Curr Top Microbiol Immunol 337: 173-195.
18. Scortti M, Monzo HJ, Lacharme-Lora L, Lewis DA, Vazquez-Boland JA (2007) The PrfA virulence regulon. Microbes Infect 9: 1196-1207.
19. Freitag NE, Rong L, Portnoy DA (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.
20. Leimeister-Wachter M, Haffner C, Domann E, Goebel W, Chakraborty T (1990) Identification of a gene that positively regulates expression of listeriolysin, the major virulence factor of Listeria monocytogenes. Proc Natl Acad Sci U S A 87: 8336-8340.
21. Korner H, Sofia HJ, Zumft WG (2003) Phylogeny of the bacterial superfamily of Crp-Fnr transcription regulators: exploiting the metabolic spectrum by controlling alternative gene programs. FEMS Microbiol Rev 27: 559-592.
22. Vega Y, Dickneite C, Ripio MT, Bockmann R, Gonzalez-Zorn B, et al. (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.
23. 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.
24. Freitag NE, Portnoy DA (1994) Dual promoters of the Listeria monocytogenes prfA transcriptional activator appear essential in vitro but are redundant in vivo. Mol Microbiol 12: 845-853.
25. 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.
26. Rauch M, Luo Q, Muller-Altrock S, Goebel W (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.
27. Leimeister-Wachter M, Domann E, Chakraborty T (1992) The expression of virulence genes in Listeria monocytogenes is thermoregulated. J Bacteriol 174: 947-952.
28. Johansson J, Mandin P, Renzoni A, Chiaruttini C, Springer M, et al. (2002) An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 110: 551-561.
29. Renzoni A, Klarsfeld A, Dramsi S, Cossart P (1997) Evidence that PrfA, the pleiotropic activator of virulence genes in Listeria monocytogenes, can be present but inactive. Infect Immun 65: 1515-1518.
30. Miner MD, Port GC, Bouwer HG, Chang JC, Freitag NE (2008) A novel prfA mutation that promotes Listeria monocytogenes cytosol entry but reduces bacterial spread and cytotoxicity. Microb Pathog 45: 273-281.
31. Vega Y, Rauch M, Banfield MJ, Ermolaeva S, Scortti M, et al. (2004) New Listeria monocytogenes prfA* mutants, transcriptional properties of PrfA* proteins and structure-function of the virulence regulator PrfA. Mol Microbiol 52: 1553-1565.
32. Shetron-Rama LM, Mueller K, Bravo JM, Bouwer HG, Way SS, et al. (2003) Isolation of Listeria monocytogenes mutants with high-level in vitro expression of host cytosol-induced gene products. Mol Microbiol 48: 1537-1551.
33. Wong KK, Freitag NE (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.
34. Ripio MT, Dominguez-Bernal G, Lara M, Suarez M, Vazquez-Boland JA (1997) A Gly145Ser substitution in the transcriptional activator PrfA causes constitutive overexpression of virulence factors in Listeria monocytogenes. J Bacteriol 179: 1533-1540.
35. Ripio MT, Dominguez-Bernal G, Suarez M, Brehm K, Berche P, et al. (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.
36. Monk IR, Gahan CG, Hill C (2008) Tools for functional postgenomic analysis of Listeria monocytogenes. Appl Environ Microbiol 74: 3921-3934.
37. Mueller KJ, Freitag NE (2005) Pleiotropic enhancement of bacterial pathogenesis resulting from the constitutive activation of the Listeria monocytogenes regulatory factor PrfA. Infect Immun 73: 1917-1926.
38. Xayarath B, Marquis H, Port GC, Freitag NE (2009) Listeria monocytogenes CtaP is a multifunctional cysteine transport-associated protein required for bacterial pathogenesis. Mol Microbiol 74: 956-973.
39. Alonzo F 3rd, Port GC, Cao M, Freitag NE (2009) The posttranslocation chaperone PrsA2 contributes to multiple facets of Listeria monocytogenes pathogenesis. Infect Immun 77: 2612-2623.
40. Port GC, Freitag NE (2007) Identification of novel Listeria monocytogenes secreted virulence factors following mutational activation of the central virulence regulator, PrfA. Infect Immun 75: 5886-5897.
41. Miner MD, Port GC, Freitag NE (2008) Functional impact of mutational activation on the Listeria monocytogenes central virulence regulator PrfA. Microbiology 154: 3579-3589.
42. Moors MA, Levitt B, Youngman P, Portnoy DA (1999) Expression of listeriolysin O and ActA by intracellular and extracellular Listeria monocytogenes. Infect Immun 67: 131-139.
43. Marr AK, Joseph B, Mertins S, Ecke R, Muller-Altrock S, et al. (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.
44. Stoll R, Mertins S, Joseph B, Muller-Altrock S, Goebel W (2008) Modulation of PrfA activity in Listeria monocytogenes upon growth in different culture media. Microbiology 154: 3856-3876.
45. Joseph B, Mertins S, Stoll R, Schar J, Umesha KR, et al. (2008) Glycerol metabolism and PrfA activity in Listeria monocytogenes. J Bacteriol 190: 5412-5430.
46. Rocourt J (1999) The Genus Listeria and Listeria monocytogenes: Phylogenetic Position, Taxonomy, and Identification. In: Ryser ET, Marth EH, eds. Listeria, Listeriosis, and Food Safety. New York, NY: Marcel Dekker, Inc. pp 1-20.
47. Walecka E, Molenda J, Bania J (2009) The impact of environmental stress on Listeria monocytogenes virulence. Pol J Vet Sci 12: 575-579.
48. Blackman IC, Frank JF (1996) Growth of Listeria monocytogenes as a biofilm on various food-processing surfaces. J Food Prot 59: 827-831.
49. Gahan CG, Hill C (2005) Gastrointestinal phase of Listeria monocytogenes infection. J Appl Microbiol 98: 1345-1353.
50. Begley M, Sleator RD, Gahan CG, Hill C (2005) Contribution of three bileassociated loci, bsh, pva, and btlB, to gastrointestinal persistence and bile tolerance of Listeria monocytogenes. Infect Immun 73: 894-904.
51. Davis MJ, Coote PJ, O'Byrne CP (1996) Acid tolerance in Listeria monocytogenes: the adaptive acid tolerance response (ATR) and growth-phase-dependent acid resistance. Microbiology 142(Pt 10): 2975-2982.
52. O'Byrne CP, Karatzas KA (2008) The role of sigma B (sigma B) in the stress adaptations of Listeria monocytogenes: overlaps between stress adaptation and virulence. Adv Appl Microbiol 65: 115-140.
53. Milohanic E, Glaser P, Coppee JY, Frangeul L, Vega Y, et al. (2003) Transcriptome analysis of Listeria monocytogenes identifies three groups of genes differently regulated by PrfA. Mol Microbiol 47: 1613-1625.
54. Dussurget O, Cabanes D, Dehoux P, Lecuit M, Buchrieser C, et al. (2002) Listeria monocytogenes bile salt hydrolase is a PrfA-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis. Mol Microbiol 45: 1095-1106.
55. Sleator RD, Wemekamp-Kamphuis HH, Gahan CG, Abee T, Hill C (2005) A PrfA-regulated bile exclusion system (BilE) is a novel virulence factor in Listeria monocytogenes. Mol Microbiol 55: 1183-1195.
56. Kazmierczak MJ, Wiedmann M, Boor KJ (2006) Contributions of Listeria monocytogenes sigmaB and PrfA to expression of virulence and stress response genes during extra- and intracellular growth. Microbiology 152: 1827-1838.
57. 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.
58. Ollinger J, Bowen B, Wiedmann M, Boor KJ, Bergholz TM (2009) Listeria monocytogenes sigmaB modulates PrfA-mediated virulence factor expression. Infect Immun 77: 2113-2124.
59. Kim H, Marquis H, Boor KJ (2005) SigmaB contributes to Listeria monocytogenes invasion by controlling expression of inlA and inlB. Microbiology 151: 3215-3222.
60. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, et al. (2009) The Listeria transcriptional landscape from saprophytism to virulence. Nature 459: 950-956.
61. Wollert T, Pasche B, Rochon M, Deppenmeier S, van den Heuvel J, et al. (2007) Extending the host range of Listeria monocytogenes by rational protein design. Cell 129: 891-902.
62. Bubert A, Sokolovic Z, Chun SK, Papatheodorou L, Simm A, et al. (1999) Differential expression of Listeria monocytogenes virulence genes in mammalian host cells. Mol Gen Genet 261: 323-336.
63. Freitag NE, Jacobs KE (1999) Examination of Listeria monocytogenes intracellular gene expression by using the green fluorescent protein of Aequorea victoria. Infect Immun 67: 1844-1852.
64. Roche SM, Gracieux P, Milohanic E, Albert I, Virlogeux-Payant I, et al. (2005) Investigation of specific substitutions in virulence genes characterizing phenotypic groups of low-virulence field strains of Listeria monocytogenes. Appl Environ Microbiol 71: 6039-6048.
65. Velge P, Herler M, Johansson J, Roche SM, Temoin S, et al. (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.
66. Lemon KP, Freitag NE, Kolter R (2010) The virulence regulator PrfA promotes biofilm formation by Listeria monocytogenes. J Bacteriol 192: 3969-3976.
67. Park SF, Kroll RG (1993) Expression of listeriolysin and phosphatidylinositolspecific phospholipase C is repressed by the plant-derived molecule cellobiose in Listeria monocytogenes. Mol Microbiol 8: 653-661.
68. Milenbachs AA, Brown DP, Moors M, Youngman P (1997) Carbon-source regulation of virulence gene expression in Listeria monocytogenes. Mol Microbiol 23: 1075-1085.
69. Eylert E, Schar J, Mertins S, Stoll R, Bacher A, et al. (2008) Carbon metabolism of Listeria monocytogenes growing inside macrophages. Mol Microbiol 69: 1008-1017.
70. Eisenreich W, Dandekar T, Heesemann J, Goebel W (2010) Carbon metabolism of intracellular bacterial pathogens and possible links to virulence. Nat Rev Microbiol 8: 401-412.
71. Ripio MT, Vazquez-Boland JA, Vega Y, Nair S, Berche P (1998) Evidence for expressional crosstalk between the central virulence regulator PrfA and the stress response mediator ClpC in Listeria monocytogenes. FEMS Microbiol Lett 158: 45-50.
72. Rouquette C, Ripio MT, Pellegrini E, Bolla JM, Tascon RI, et al. (1996) Identification of a ClpC ATPase required for stress tolerance and in vivo survival of Listeria monocytogenes. Mol Microbiol 21: 977-987.
73. Soderholm JD, Perdue MH (2001) Stress and gastrointestinal tract. II. Stress and intestinal barrier function. Am J Physiol Gastrointest Liver Physiol 280: G7-G13.
74. Kim H, Boor KJ, Marquis H (2004) Listeria monocytogenes sigmaB contributes to invasion of human intestinal epithelial cells. Infect Immun 72: 7374-7378.
75. Lingnau A, Domann E, Hudel M, Bock M, Nichterlein T, et al. (1995) 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 63: 3896-3903.
76. Mengaud J, Dramsi S, Gouin E, Vazquez-Boland JA, Milon G, et al. (1991) Pleiotropic control of Listeria monocytogenes virulence factors by a gene that is autoregulated. Mol Microbiol 5: 2273-2283.
77. Bohne J, Kestler H, Uebele C, Sokolovic Z, Goebel W (1996) Differential regulation of the virulence genes of Listeria monocytogenes by the transcriptional activator PrfA. Mol Microbiol 20: 1189-1198.
78. Sheehan B, Klarsfeld A, Msadek T, Cossart P (1995) Differential activation of virulence gene expression by PrfA, the Listeria monocytogenes virulence regulator. J Bacteriol 177: 6469-6476.
79. Lalic-Multhaler M, Bohne J, Goebel W (2001) In vitro transcription of PrfAdependent and -independent genes of Listeria monocytogenes. Mol Microbiol 42: 111-120.
80. Bishop DK, Hinrichs DJ (1987) Adoptive transfer of immunity to Listeria monocytogenes. The influence of in vitro stimulation on lymphocyte subset requirements. J Immunol 139: 2005-2009.
81. Edman DC, Pollock MB, Hall ER (1968) Listeria monocytogenes L forms. I. Induction maintenance, and biological characteristics. J Bacteriol 96: 352-357.
82. Hodgson DA (2000) Generalized transduction of serotype 1/2 and serotype 4b strains of Listeria monocytogenes. Mol Microbiol 35: 312-323.
83. Lennox ES (1955) Transduction of linked genetic characters of the host by bacteriophage P1. Virology 1: 190-206.
84. Wiedmann M, Arvik TJ, Hurley RJ, Boor KJ (1998) General stress transcription factor sigmaB and its role in acid tolerance and virulence of Listeria monocytogenes. J Bacteriol 180: 3650-3656.
85. Smith K, Youngman P (1992) Use of a new integrational vector to investigate compartment-specific expression of the Bacillus subtilis spoIIM gene. Biochimie 74: 705-711.
86. Park SF, Stewart GS (1990) High-efficiency transformation of Listeria monocytogenes by electroporation of penicillin-treated cells. Gene 94: 129-132.
87. Lauer P, Chow MY, Loessner MJ, Portnoy DA, Calendar R (2002) Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. J Bacteriol 184: 4177-4186.
88. Youngman P (1987) Plasmid vectors for recovering and exploiting Tn917 transpositions in Bacillus and other Gram-positive bacteria. In: Hardy KG, ed. Plasmids: A practical approach. Oxford: IRL Press. pp 79-103.
89. Shetron-Rama LM, Marquis H, Bouwer HG, Freitag NE (2002) Intracellular induction of Listeria monocytogenes actA expression. Infect Immun 70: 1087-1096.
90. Auerbuch V, Lenz LL, Portnoy DA (2001) Development of a competitive index assay to evaluate the virulence of Listeria monocytogenes actA mutants during primary and secondary infection of mice. Infect Immun 69: 5953-5957.