Evidence implicating the 5′ untranslated region of Listeria monocytogenes actA in the regulation of bacterial actin-based motility

Cellular Microbiology

Volumn 6, Issue 2, 2004, Pages 155-166

  Wong, Kendy K Y ^a   Bouwer, H G Archie ^b   Freitag, Nancy E ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b PORTLAND VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; MESSENGER RNA; VIRULENCE FACTOR;

5' UNTRANSLATED REGION; ACTIN FILAMENT; ANIMAL CELL; BACTERIUM MUTANT; CELL MOTILITY; CELL TRANSPORT; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOSOL; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INDUCTION; HOST; LISTERIA MONOCYTOGENES; MONOLAYER CULTURE; MOUSE; NONHUMAN; PHASE TRANSITION; PREDICTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ASSEMBLY; PROTEIN POLYMERIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN SYNTHESIS; RAT; REVIEW;

ANIMALIA; BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES;

EID: 1642513704     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1462-5822.2003.00348.x     Document Type: Review

References (63)

1. Arnold, T.E., Yu, J., and Belasco, J.G. (1998) mRNA stabilization by the ompA 5′ untranslated region: two protective elements hinder distinct pathways for mRNA degradation. RNA 4: 319-330.
2. Bockmann, R., Dickneite, C., Goebel, W., and Bohne, J. (2000) PrfA mediates specific binding of RNA polymerase of Listeria monocytogenes to PrfA-dependent virulence gene promoters resulting in a transcriptionally active complex. Mol Microbiol 36: 487-497.
3. Boujemaa-Paterski, R., Gouin, E., Hansen, G., Samarin, S., Le Clainche, C., Didry, D., et al. (2001) Listeria protein ActA mimics WASp family proteins: it activates filament barbed end branching by Arp2/3 complex. Biochemistry 40: 11390-11404.
4. Bricker, A.L., and Belasco, J.G. (1999) Importance of a 5′ stem-loop for longevity of papA mRNA in Escherichia coli. J Bacteriol 181: 3587-3590.
5. Brundage, R.A., Smith, G.A., Camilli, A., Theriot, J.A., and Portnoy, D.A. (1993) Expression and phosphorylation of the Listeria monocytogenes ActA protein in mammalian cells. Proc Natl Acad Sci USA 90: 11890-11894.
6. Bubert, A., Sokolovic, Z., Chun, S.K., Papatheodorou, L., Simm, A., and Goebel, W. (1999) Differential expression of Listeria monocytogenes virulence genes in mammalian host cells. Mol Gen Genet 261: 323-336.
7. Cameron, L.A., Footer, M.J., van Oudenaarden, A., and Theriot, J.A. (1999) Motility of ActA protein-coated microspheres driven by actin polymerization. Proc Natl Acad Sci USA 96: 4908-4913.
8. Camilli, A., Paynton, C.R., and Portnoy, D.A. (1989) Intracellular methicillin selection of Listeria monocytogenes mutants unable to replicate in a macrophage cell line. Proc Natl Acad Sci USA 86: 5522-5526.
9. Chakraborty, T., Ebel, F., Domann, E., Niebuhr, K., Gerstel, B., Pistor, S., et al. (1995) A focal adhesion factor directly linking intracellularly motile Listeria monocytogenes and Listeria ivanovii to the actin-based cytoskeleton of mammalian cells. EMBO J 14: 1314-1321.
10. Condon, C. (2003) RNA processing and degradation in Bacillus subtilis. Microbiol Mol Biol Rev 67: 157-174.
11. Cossart, P. (1995) Actin-based bacterial motility. Curr Opin Cell Biol 7: 94-101.
12. Cossart, P., and Kocks, C. (1994) The actin based motility of the facultative intracellular pathogen Listeria monocytogenes. Mol Microbiol 13: 395-402.
13. Domann, E., Wehland, J., Rohde, M., Pistor, S., Hartl, M., Goebel, W., et al. (1992) A novel bacterial virulence gene in Listeria monocytogenes required for host cell microfilament interaction with homology to the proline-rich region of vinculin. EMBO J 11: 1981-1990.
14. Emory, S.A., Bouvet, P., and Belasco, J.G. (1992) A 5′-terminal stem-loop structure can stabilize mRNA in Escherichia coli. Genes Dev 6: 135-148.
15. Freitag, N.E. (2000) Genetic tools for use with Listeria monocytogenes. In Gram-Positive Pathogens. Fischetti, V.A., Novick, R.P., Ferretti, J.J., Portnoy, D.A., and Rood, J.I. (eds). Washington, DC: American Society for Microbiology Press, pp. 488-498.
16. Freitag, N.E., and Jacobs, K.E. (1999) Examination of Listeria monocytogenes intracellular gene expression by using the green fluorescent protein of Aequorea victoria. Infect Immun 67: 1844-1852.
17. Gellin, B.G., and Broome, C.V. (1989) Listeriosis. J Am Med Assoc 261: 1313-1320.
18. Goldberg, M.B. (2001) Actin-based motility of intracellular microbial pathogens. Microbiol Mol Biol Rev 65: 595-626.
19. Gray, M.L., and Killinger, A.H. (1966) Listeria monocytogenes and listeric infections. Bacteriol Rev 30: 309-382.
20. Horton, R. (1993) In vitro recombination and mutagenesis of DNA. In PCR Protocols: Current Methods and Applications. White, B. (ed.). Totowa, NJ: Humana Press, pp. 251-260.
21. Johansson, J., Mandin, P., Renzoni, A., Chiaruttini, C., Springer, M., and Cossart, P. (2002) An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 110: 551.
22. Kocks, C., Gouin, E., Tabouret, M., Berche, P., Ohayon, H., and Cossart, P. (1992) L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68: 521-531.
23. Kocks, C., Marchand, J.B., Gouin, E., d'Hauteville, H., Sansonetti, P.J., Carlier, M.F., and Cossart, P. (1995) The unrelated surface proteins ActA of Listeria monocytogenes and IcsA of Shigella flexneri are sufficient to confer actin-based motility on Listeria innocua and Escherichia coli respectively. Mol Microbiol 18: 413-423.
24. Kreft, J., and Vazquez-Boland, J.A. (2001) Regulation of virulence genes in Listeria. Int J Med Microbiol 291: 145-157.
25. Lai, E.C. (2003) RNA sensors and riboswitches: self-regulating messages. Curr Biol 13: R285-R291.
26. Lauer, P., Theriot, J.A., Skoble, J., Welch, M.D., and Portnoy, D.A. (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.
27. Loisel, T.P., Boujemaa, R., Pantaloni, D., and Carlier, M.F. (1999) Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401: 613-616.
28. Lorber, B. (1997) Listeriosis. Clin Infect Dis 24: 1-9.
29. Magdalena, J., and Goldberg, M.B. (2002) Quantification of Shigella IcsA required for bacterial actin polymerization. Cell Motil Cytoskeleton 51: 187-196.
30. Mandal, M., Boese, B., Barrick, J.E., Winkler, W.C., and Breaker, R.R. (2003) Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113: 577-586.
31. Marquis, H., Goldfine, H., and Portnoy, D.A. (1997) Proteolytic pathways of activation and degradation of a bacterial phospholipase C during intracellular infection by Listeria monocytogenes. J Cell Biol 137: 1381-1392.
32. Mathews, D.H., Sabina, J., Zuker, M., and Turner, D.H. (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 288: 911-940.
33. Moors, M.A., Levitt, B., Youngman, P., and Portnoy, D.A. (1999a) Expression of listeriolysin O and ActA by intracellular and extracellular Listeria monocytogenes. Infect Immun 67: 131-139.
34. Moors, M.A., Auerbuch, V., and Portnoy, D.A. (1999b) Stability of the Listeria monocytogenes ActA protein in mammalian cells is regulated by the N-end rule pathway. Cell Microbiol 1: 249-257.
35. Mounier, J., Ryter, A., Coquis-Rondon, M., and Sansonetti, P.J. (1990) Intracellular and cell-to-cell spread of Listeria monocytogenes involves interaction with F-actin in the enterocyte-like cell line Caco-2. Infect Immun 58: 1048-1058.
36. Mourrain, P., Lasa, I., Gautreau, A., Gouin, E., Pugsley, A., and Cossart, P. (1997) ActA is a dimer. Proc Natl Acad Sci USA 94: 10034-10039.
37. Niebuhr, K., Ebel, F., Frank, R., Reinhard, M., Domann, E., Carl, U.D., et al. (1997) A novel proline-rich motif present in ActA of Listeria monocytogenes and cytoskeletal proteins is the ligand for the EVH1 domain, a protein module present in the Ena/VASP family. EMBO J 16: 5433-5444.
38. Noireaux, V., Golsteyn, R.M., Friederich, E., Prost, J., Antony, C., Louvard, D., and Sykes, C. (2000) Growing an actin gel on spherical surfaces. Biophys J 78: 1643-1654.
39. Pistor, S., Grobe, L., Sechi, A.S., Domann, E., Gerstel, B., Machesky, L.M., et al. (2000) Mutations of arginine residues within the 146-KKRRK-150 motif of the ActA protein of Listeria monocytogenes abolish intracellular motility by interfering with the recruitment of the Arp2/3 complex. J Cell Sci 113: 3277-3287.
40. Portnoy, D.A., Jacks, P.S., and Hinrichs, D.J. (1988) Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med 167: 1459-1471.
41. Ripio, M.T., Dominguez-Bernal, G., Suarez, M., Brehm, K., Berche, P., and Vazquez-Boland, J.A. (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.
42. Sanger, J.M., Sanger, J.W., and Southwick, F.S. (1992) Host cell actin assembly is necessary and likely to provide the propulsive force for intracellular movement of Listeria monocytogenes. Infect Immun 60: 3609-3619.
43. Schlax, P.J., and Worhunsky, D.J. (2003) Translational repression mechanisms in prokaryotes. Mol Microbiol 48: 1157-1169.
44. Sechi, A.S., Wehland, J., and Small, J.V. (1997) The isolated comet tail pseudopodium of Listeria monocytogenes: a tail of two actin filament populations, long and axial and short and random. J Cell Biol 137: 155-167.
45. Sheehan, B., Kocks, C., Dramsi, S., Gouin, E., Klarsfeld, A.D., Mengaud, J., and Cossart, P. (1994) Molecular and genetic determinants of the Listeria monocytogenes infectious process. Curr Topics Microbiol 192: 187-216.
46. Shetron-Rama, L.M., Marquis, H., Bouwer, H.G., and Freitag, N.E. (2002) Intracellular induction of Listeria monocytogenes actA expression. Infect Immun 70: 1087-1096.
47. Shetron-Rama, L.M., Mueller, K., Bravo, J.M., Bouwer, H.G., Way, S.S., and 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.
48. Skoble, J., Portnoy, D.A., and Welch, M.D. (2000) Three regions within ActA promote Arp2/3 complex-mediated actin nucleation and Listeria monocytogenes motility. J Cell Biol 150: 527-538.
49. de Smit, M.H., and van Duin, J. (1994) Control of translation by mRNA secondary structure in Escherichia coli. A quantitative analysis of literature data. J Mol Biol 244: 144-150.
50. Smith, G.A., Portnoy, D.A., and Theriot, J.A. (1995) Asymmetric distribution of the Listeria monocytogenes ActA protein is required and sufficient to direct actin-based motility. Mol Microbiol 17: 945-951.
51. Smith, G.A., Theriot, J.A., and Portnoy, D.A. (1996) The tandem repeat domain in the Listeria monocytogenes ActA protein controls the rate of actin-based motility, the percentage of moving bacteria, and the localization of vasodilator-stimulated phosphoprotein and profilin. J Cell Biol 135: 647-660.
52. Smith, K., and Youngman, P. (1992) Use of a new integrational vector to investigate compartment-specific expression of the Bacillus subtilis spollM gene. Biochimie 74: 705-711.
53. Suarez, M., Gonzalez-Zorn, B., Vega, Y., Chico-Calero, I., and Vazquez-Boland, J.A. (2001) A role for ActA in epithelial cell invasion by Listeria monocytogenes. Cell Microbiol 3: 853-864.
54. Sun, A.N., Camilli, A., and 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.
55. Theriot, J.A., Mitchison, T.J., Tilney, L.G., and Portnoy, D.A. (1992) The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization. Nature 357: 257-260.
56. Vazquez-Boland, J.A., Kuhn, M., Berche, P., Chakraborty, T., Dominguez-Bernal, G., Goebel, W., et al. (2001) Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14: 584-640.
57. Welch, M.D., Iwamatsu, A., and Mitchison, T.J. (1997) Actin polymerization is induced by Arp2/3 protein complex at the surface of Listeria monocytogenes. Nature 385: 265-269.
58. Welch, M.D., Rosenblatt, J., Skoble, J., Portnoy, D.A., and Mitchison, T.J. (1998) Interaction of human Arp2/3 complex and the Listeria monocytogenes ActA protein in actin filament nucleation. Science 281: 105-108.
59. Yamanaka, K., Mitta, M., and Inouye, M. (1999) Mutation analysis of the 5′ untranslated region of the cold shock cspA mRNA of Escherichia coli. J Bacteriol 181: 6284-6291.
60. Youngman, P. (1987) Plasmid vectors for recovering and exploiting Tn917 transpositions in Bacillus and other gram-positive bacteria. In Plasmids: a Practical Approach. Hardy, K. (ed.). Oxford: IRL Press, pp. 79-103.
61. Zalevsky, J., Grigorova, I., and Mullins, R.D. (2001) Activation of the Arp2/3 complex by the Listeria Acta protein. ActA binds two actin monomers and three subunits of the Arp2/3 complex. J Biol Chem 276: 3468-3475.
62. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 1-10.
63. Zuker, M., Jaeger, J.A., and Turner, D.H. (1991) A comparison of optimal and suboptimal RNA secondary structures predicted by free energy minimization with structures determined by phylogenetic comparison. Nucleic Acids Res 19: 2707-2714.