A novel prfA mutation that promotes Listeria monocytogenes cytosol entry but reduces bacterial spread and cytotoxicity

Microbial Pathogenesis

Volumn 45, Issue 4, 2008, Pages 273-281

  Miner, Maurine D ^a,b   Port, Gary C ^a,b   Bouwer, H G Archie ^c   Chang, Jennifer C ^a   Freitag, Nancy E ^a,b,d  

^a UNIVERSITY OF WASHINGTON   (United States)

^b SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^c PORTLAND VA MEDICAL CENTER   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

Author keywords

ActA; Gene expression; PrfA; Virulence regulation

Indexed keywords

ANTIGEN; CD8 ANTIGEN; PRFA PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; EFFECTOR CELL; GENE MUTATION; HOST CELL; LISTERIA MONOCYTOGENES; MOUSE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; WILD TYPE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CYTOSOL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; LISTERIA INFECTIONS; LISTERIA MONOCYTOGENES; MICE; MICE, INBRED BALB C; MUTATION, MISSENSE; PEPTIDE TERMINATION FACTORS; VIRULENCE; VIRULENCE FACTORS;

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

EID: 50949126831     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2008.06.006     Document Type: Article

References (46)

1. Gellin B.G., and Broome C.V. Listeriosis. JAMA 261 (1989) 1313-1320
2. Vazquez-Boland J.A., Kuhn M., Berche P., Chakraborty T., Dominguez-Bernal G., Goebel W., et al. Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14 (2001) 584-640
3. Ramaswamy V., Cresence V.M., Rejitha J.S., Lekshmi M.U., Dharsana K.S., Prasad S.P., et al. Listeria - review of epidemiology and pathogenesis. J Microbiol Immunol Infect 40 (2007) 4-13
4. Posfay-Barbe K.M., and Wald E.R. Listeriosis. Pediatr Rev 25 (2004) 151-159
5. Kreft J., and Vazquez-Boland J.A. Regulation of virulence genes in Listeria. Int J Med Microbiol 291 (2001) 145-157
6. Sheehan B., Kocks C., Dramsi S., Gouin E., Klarsfeld A.D., Mengaud J., et al. Molecular and genetic determinants of the Listeria monocytogenes infectious process. Curr Top Microbiol Immunol 192 (1994) 187-216
7. Dussurget O., Pizarro-Cerda J., and Cossart P. Molecular determinants of Listeria monocytogenes virulence. Annu Rev Microbiol 58 (2004) 587-610
8. Hamon M., Bierne H., and Cossart P. Listeria monocytogenes: a multifaceted model. Nat Rev Microbiol 4 (2006) 423-434
9. Gray M.J., Freitag N.E., and Boor K.J. How the bacterial pathogen Listeria monocytogenes mediates the switch from environmental Dr. Jekyll to pathogenic Mr. Hyde. Infect Immun 74 (2006) 2505-2512
10. Leimeister-Wachter M., Haffner C., Domann E., Goebel W., and Chakraborty T. Identification of a gene that positively regulates expression of listeriolysin, the major virulence factor of Listeria monocytogenes. Proc Natl Acad Sci USA 87 (1990) 8336-8340
11. Leimeister-Wachter M., Goebel W., and Chakraborty T. Mutations affecting hemolysin production in Listeria monocytogenes located outside the listeriolysin gene. FEMS Microbiol Lett 53 (1989) 23-29
12. Chakraborty T., Leimeister-Wachter M., Domann E., Hartl M., Goebel W., Nichterlein T., et al. Coordinate regulation of virulence genes in Listeria monocytogenes requires the product of the prfA gene. J Bacteriol 174 (1992) 568-574
13. Miner M.D., Port G.C., and Freitag N.E. Regulation of Listeria monocytogenes virulence genes. In: Shen H., and Goldfine H. (Eds). Listeria monocytogenes: pathogenesis and host response (2007), Springer-Verlag 139-158
14. Lampidis R., Gross R., Sokolovic Z., Goebel W., and Kreft J. 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 (1994) 141-151
15. Busby S., and Ebright R.H. Transcription activation by catabolite activator protein (CAP). J Mol Biol 293 (1999) 199-213
16. Korner H., Sofia H.J., and Zumft W.G. Phylogeny of the bacterial superfamily of Crp-Fnr transcription regulators: exploiting the metabolic spectrum by controlling alternative gene programs. FEMS Microbiol Rev 27 (2003) 559-592
17. Garges S., and Adhya S. Sites of allosteric shift in the structure of the cyclic AMP receptor protein. Cell 41 (1985) 745-751
18. Harman J.G., Peterkofsky A., and McKenney K. Arginine substituted for leucine at position 195 produces a cyclic AMP-independent form of the Escherichia coli cyclic AMP receptor protein. J Biol Chem 263 (1988) 8072-8077
19. Wong K.K., and Freitag N.E. A novel mutation within the central Listeria monocytogenes regulator PrfA that results in constitutive expression of virulence gene products. J Bacteriol 186 (2004) 6265-6276
20. Ripio M.T., Dominguez-Bernal G., Lara M., Suarez M., and Vazquez-Boland J.A. A Gly145Ser substitution in the transcriptional activator PrfA causes constitutive overexpression of virulence factors in Listeria monocytogenes. J Bacteriol 179 (1997) 1533-1540
21. Shetron-Rama L.M., Mueller K., Bravo J.M., Bouwer H.G., Way S.S., and Freitag N.E. Isolation of Listeria monocytogenes mutants with high-level in vitro expression of host cytosol-induced gene products. Mol Microbiol 48 (2003) 1537-1551
22. Vega Y., Rauch M., Banfield M.J., Ermolaeva S., Scortti M., Goebel W., et al. New Listeria monocytogenes prfA* mutants, transcriptional properties of PrfA* proteins and structure-function of the virulence regulator PrfA. Mol Microbiol 52 (2004) 1553-1565
23. Ripio M.T., Dominguez-Bernal G., Suarez M., Brehm K., Berche P., and Vazquez-Boland J.A. 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 (1996) 371-384
24. Freitag N.E., Rong L., and Portnoy D.A. Regulation of the prfA transcriptional activator of Listeria monocytogenes: multiple promoter elements contribute to intracellular growth and cell-to-cell spread. Infect Immun 61 (1993) 2537-2544
25. Lauer P., Chow M.Y., Loessner M.J., Portnoy D.A., and Calendar R. Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. J Bacteriol 184 (2002) 4177-4186
26. Brundage R.A., Smith G.A., Camilli A., Theriot J.A., and Portnoy D.A. Expression and phosphorylation of the Listeria monocytogenes ActA protein in mammalian cells. Proc Natl Acad Sci U S A 90 (1993) 11890-11894
27. Sun A.N., Camilli A., and Portnoy D.A. Isolation of Listeria monocytogenes small-plaque mutants defective for intracellular growth and cell-to-cell spread. Infect Immun 58 (1990) 3770-3778
28. Theriot J.A., Mitchison T.J., Tilney L.G., and Portnoy D.A. The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization. Nature 357 (1992) 257-260
29. Chary V.K., Amaya E.I., and Piggot P.J. Neomycin- and spectinomycin-resistance replacement vectors for Bacillus subtilis. FEMS Microbiol Lett 153 (1997) 135-139
30. Shetron-Rama L.M., Marquis H., Bouwer H.G., and Freitag N.E. Intracellular induction of Listeria monocytogenes actA expression. Infect Immun 70 (2002) 1087-1096
31. Mueller K.J., and Freitag N.E. Pleiotropic enhancement of bacterial pathogenesis resulting from the constitutive activation of the Listeria monocytogenes regulatory factor PrfA. Infect Immun 73 (2005) 1917-1926
32. Kingdon G.C., and Sword C.P. Biochemical and immunological effects of Listeria monocytogenes hemolysin. Infect Immun 1 (1970) 363-372
33. Camilli A., Paynton C.R., and Portnoy D.A. Intracellular methicillin selection of Listeria monocytogenes mutants unable to replicate in a macrophage cell line. Proc Natl Acad Sci U S A 86 (1989) 5522-5526
34. Wong K.K., Bouwer H.G., and Freitag N.E. Evidence implicating the 5′ untranslated region of Listeria monocytogenes actA in the regulation of bacterial actin-based motility. Cell Microbiol 6 (2004) 155-166
35. Youngman P. Plasmid vectors for recovering and exploiting Tn917 transpositions in Bacillus and other Gram-positive bacteria. In: Hardy K. (Ed). Plasmids: A Practical Approach (1987), IRL Press, Oxford 79-103
36. Moors M.A., Levitt B., Youngman P., and Portnoy D.A. Expression of listeriolysin O and ActA by intracellular and extracellular Listeria monocytogenes. Infect Immun 67 (1999) 131-139
37. Portnoy D.A., Jacks S.P., and Hinrichs D.J. Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med 167 (1988) 1459-1471
38. Decatur A.L., and Portnoy D.A. A PEST-like sequence in listeriolysin O essential for Listeria monocytogenes pathogenicity. Science 290 (2000) 992-995
39. Nato F., Reich K., Lhopital S., Rouyre S., Geoffroy C., Mazie J.C., et al. Production and characterization of neutralizing and nonneutralizing monoclonal antibodies against listeriolysin O. Infect Immun 59 (1991) 4641-4646
40. Bubert A., Sokolovic Z., Chun S.K., Papatheodorou L., Simm A., and Goebel W. Differential expression of Listeria monocytogenes virulence genes in mammalian host cells. Mol Gen Genet 261 (1999) 323-336
41. Freitag N.E., and Jacobs K.E. Examination of Listeria monocytogenes intracellular gene expression by using the green fluorescent protein of Aequorea victoria. Infect Immun 67 (1999) 1844-1852
42. Karow M.L., and Piggot P.J. Construction of gusA transcriptional fusion vectors for Bacillus subtilis and their utilization for studies of spore formation. Gene 163 (1995) 69-74
43. Ermolaeva S., Novella S., Vega Y., Ripio M.T., Scortti M., and Vazquez-Boland J.A. Negative control of Listeria monocytogenes virulence genes by a diffusible autorepressor. Mol Microbiol 52 (2004) 601-611
44. Glomski Ij M., Gedde M., Tsang A.W., Swanson J.A., and Portnoy D.A. The Listeria monocytogenes hemolysin has an acidic pH optimum to compartmentalize activity and prevent damage to infected host cells. J Cell Biol 156 (2002) 1029-1038
45. Eiting M., Hageluken G., Schubert W.D., and Heinz D.W. The mutation G145S in PrfA, a key virulence regulator of Listeria monocytogenes, increases DNA-binding affinity by stabilizing the HTH motif. Mol Microbiol 56 (2005) 433-446
46. Jones S., and Portnoy D.A. Characterization of Listeria monocytogenes pathogenesis in a strain expressing perfringolysin O in place of listeriolysin O. Infect Immun 62 (1994) 5608-5613