Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1995 Jul;63(7):2729–2737. doi: 10.1128/iai.63.7.2729-2737.1995

iactA of Listeria ivanovii, although distantly related to Listeria monocytogenes actA, restores actin tail formation in an L. monocytogenes actA mutant.

E Gouin 1, P Dehoux 1, J Mengaud 1, C Kocks 1, P Cossart 1
PMCID: PMC173365  PMID: 7790091

Abstract

A gene homologous to the actA gene of Listeria monocytogenes was cloned from Listeria ivanovii (strain CLIP257) by chromosome walking starting from the ilo gene that encodes the pore-forming toxin ivanolysin. The nucleotide sequence revealed that this gene, named iactA, encodes a protein of 1,044 amino acids (IactA) comprising a central region with seven highly conserved tandem proline-rich repeats of 47 amino acids. Although IactA and ActA share an overall similar structure, these two proteins are only distantly related. Like ActA, IactA migrates aberrantly on sodium dodecyl sulfate gels. When expressed in an L. monocytogenes actA deletion mutant strain, iactA restored actin polymerization.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Arakawa T., Frieden C. Interaction of microtubule-associated proteins with actin filaments. Studies using the fluorescence-photobleaching recovery technique. J Biol Chem. 1984 Oct 10;259(19):11730–11734. [PubMed] [Google Scholar]
  3. Asai D. J., Thompson W. C., Wilson L., Dresden C. F., Schulman H., Purich D. L. Microtubule-associated proteins (MAPs): a monoclonal antibody to MAP 1 decorates microtubules in vitro but stains stress fibers and not microtubules in vivo. Proc Natl Acad Sci U S A. 1985 Mar;82(5):1434–1438. doi: 10.1073/pnas.82.5.1434. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bernardini M. L., Mounier J., d'Hauteville H., Coquis-Rondon M., Sansonetti P. J. Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra- and intercellular spread through interaction with F-actin. Proc Natl Acad Sci U S A. 1989 May;86(10):3867–3871. doi: 10.1073/pnas.86.10.3867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bohne J., Sokolovic Z., Goebel W. Transcriptional regulation of prfA and PrfA-regulated virulence genes in Listeria monocytogenes. Mol Microbiol. 1994 Mar;11(6):1141–1150. doi: 10.1111/j.1365-2958.1994.tb00390.x. [DOI] [PubMed] [Google Scholar]
  6. Brendel V., Bucher P., Nourbakhsh I. R., Blaisdell B. E., Karlin S. Methods and algorithms for statistical analysis of protein sequences. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2002–2006. doi: 10.1073/pnas.89.6.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brundage R. A., Smith G. A., Camilli A., Theriot J. A., Portnoy D. A. Expression and phosphorylation of the Listeria monocytogenes ActA protein in mammalian cells. Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11890–11894. doi: 10.1073/pnas.90.24.11890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Casadaban M. J., Cohen S. N. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol. 1980 Apr;138(2):179–207. doi: 10.1016/0022-2836(80)90283-1. [DOI] [PubMed] [Google Scholar]
  9. Cooper R. F., Dennis S. M. Further characterization of Listeria monocytogenes serotype 5. Can J Microbiol. 1978 May;24(5):598–599. doi: 10.1139/m78-097. [DOI] [PubMed] [Google Scholar]
  10. Cossart P. Actin-based bacterial motility. Curr Opin Cell Biol. 1995 Feb;7(1):94–101. doi: 10.1016/0955-0674(95)80050-6. [DOI] [PubMed] [Google Scholar]
  11. Cossart P., Kocks C. The actin-based motility of the facultative intracellular pathogen Listeria monocytogenes. Mol Microbiol. 1994 Aug;13(3):395–402. doi: 10.1111/j.1365-2958.1994.tb00434.x. [DOI] [PubMed] [Google Scholar]
  12. Coune A. Liposomes as drug delivery system in the treatment of infectious diseases. Potential applications and clinical experience. Infection. 1988 May-Jun;16(3):141–147. doi: 10.1007/BF01644088. [DOI] [PubMed] [Google Scholar]
  13. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Domann E., Leimeister-Wächter M., Goebel W., Chakraborty T. Molecular cloning, sequencing, and identification of a metalloprotease gene from Listeria monocytogenes that is species specific and physically linked to the listeriolysin gene. Infect Immun. 1991 Jan;59(1):65–72. doi: 10.1128/iai.59.1.65-72.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Domann E., Wehland J., Rohde M., Pistor S., Hartl M., Goebel W., Leimeister-Wächter M., Wuenscher M., Chakraborty T. 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. 1992 May;11(5):1981–1990. doi: 10.1002/j.1460-2075.1992.tb05252.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fujii T., Watanabe M., Ogoma Y., Kondo Y., Arai T. Microtubule-associated proteins, MAP 1A and MAP 1B, interact with F-actin in vitro. J Biochem. 1993 Dec;114(6):827–829. doi: 10.1093/oxfordjournals.jbchem.a124263. [DOI] [PubMed] [Google Scholar]
  17. Gaillard J. L., Berche P., Frehel C., Gouin E., Cossart P. Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell. 1991 Jun 28;65(7):1127–1141. doi: 10.1016/0092-8674(91)90009-n. [DOI] [PubMed] [Google Scholar]
  18. Gehrung S., Snyder M. The SPA2 gene of Saccharomyces cerevisiae is important for pheromone-induced morphogenesis and efficient mating. J Cell Biol. 1990 Oct;111(4):1451–1464. doi: 10.1083/jcb.111.4.1451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Goebel S. J., Johnson G. P., Perkus M. E., Davis S. W., Winslow J. P., Paoletti E. The complete DNA sequence of vaccinia virus. Virology. 1990 Nov;179(1):247-66, 517-63. doi: 10.1016/0042-6822(90)90294-2. [DOI] [PubMed] [Google Scholar]
  20. Goldberg M. B., Bârzu O., Parsot C., Sansonetti P. J. Unipolar localization and ATPase activity of IcsA, a Shigella flexneri protein involved in intracellular movement. J Bacteriol. 1993 Apr;175(8):2189–2196. doi: 10.1128/jb.175.8.2189-2196.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Goossens P. L., Milon G. Induction of protective CD8+ T lymphocytes by an attenuated Listeria monocytogenes actA mutant. Int Immunol. 1992 Dec;4(12):1413–1418. doi: 10.1093/intimm/4.12.1413. [DOI] [PubMed] [Google Scholar]
  22. Gormley E., Mengaud J., Cossart P. Sequences homologous to the listeriolysin O gene region of Listeria monocytogenes are present in virulent and avirulent haemolytic species of the genus Listeria. Res Microbiol. 1989 Nov-Dec;140(9):631–643. doi: 10.1016/0923-2508(89)90195-2. [DOI] [PubMed] [Google Scholar]
  23. Gouin E., Mengaud J., Cossart P. The virulence gene cluster of Listeria monocytogenes is also present in Listeria ivanovii, an animal pathogen, and Listeria seeligeri, a nonpathogenic species. Infect Immun. 1994 Aug;62(8):3550–3553. doi: 10.1128/iai.62.8.3550-3553.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Griffith L. M., Pollard T. D. The interaction of actin filaments with microtubules and microtubule-associated proteins. J Biol Chem. 1982 Aug 10;257(15):9143–9151. [PubMed] [Google Scholar]
  25. Haas A., Dumbsky M., Kreft J. Listeriolysin genes: complete sequence of ilo from Listeria ivanovii and of lso from Listeria seeligeri. Biochim Biophys Acta. 1992 Feb 28;1130(1):81–84. doi: 10.1016/0167-4781(92)90466-d. [DOI] [PubMed] [Google Scholar]
  26. Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol. 1983 Jun 5;166(4):557–580. doi: 10.1016/s0022-2836(83)80284-8. [DOI] [PubMed] [Google Scholar]
  27. Hiller G., Jungwirth C., Weber K. Fluorescence microscopical analysis of the life cycle of vaccinia virus in chick embryo fibroblasts. Virus-cytoskeleton interactions. Exp Cell Res. 1981 Mar;132(1):81–87. doi: 10.1016/0014-4827(81)90085-9. [DOI] [PubMed] [Google Scholar]
  28. Hiller G., Weber K., Schneider L., Parajsz C., Jungwirth C. Interaction of assembled progeny pox viruses with the cellular cytoskeleton. Virology. 1979 Oct 15;98(1):142–153. doi: 10.1016/0042-6822(79)90533-6. [DOI] [PubMed] [Google Scholar]
  29. Karunasagar I., Krohne G., Goebel W. Listeria ivanovii is capable of cell-to-cell spread involving actin polymerization. Infect Immun. 1993 Jan;61(1):162–169. doi: 10.1128/iai.61.1.162-169.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kocks C., Cossart P. Directional actin assembly by Listeria monocytogenes at the site of polar surface expression of the actA gene product involving the actin-bundling protein plastin (fimbrin). Infect Agents Dis. 1993 Aug;2(4):207–209. [PubMed] [Google Scholar]
  31. Kocks C., Gouin E., Tabouret M., Berche P., Ohayon H., Cossart P. L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell. 1992 Feb 7;68(3):521–531. doi: 10.1016/0092-8674(92)90188-i. [DOI] [PubMed] [Google Scholar]
  32. Kocks C., Hellio R., Gounon P., Ohayon H., Cossart P. Polarized distribution of Listeria monocytogenes surface protein ActA at the site of directional actin assembly. J Cell Sci. 1993 Jul;105(Pt 3):699–710. doi: 10.1242/jcs.105.3.699. [DOI] [PubMed] [Google Scholar]
  33. Kreft J., Dumbsky M., Theiss S. The actin-polymerization protein from Listeria ivanovii is a large repeat protein which shows only limited amino acid sequence homology to ActA from Listeria monocytogenes. FEMS Microbiol Lett. 1995 Feb 15;126(2):113–121. doi: 10.1111/j.1574-6968.1995.tb07403.x. [DOI] [PubMed] [Google Scholar]
  34. Kuhn M., Goebel W. Identification of an extracellular protein of Listeria monocytogenes possibly involved in intracellular uptake by mammalian cells. Infect Immun. 1989 Jan;57(1):55–61. doi: 10.1128/iai.57.1.55-61.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  36. Lampidis R., Gross R., Sokolovic Z., Goebel W., 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. 1994 Jul;13(1):141–151. doi: 10.1111/j.1365-2958.1994.tb00409.x. [DOI] [PubMed] [Google Scholar]
  37. Lett M. C., Sasakawa C., Okada N., Sakai T., Makino S., Yamada M., Komatsu K., Yoshikawa M. virG, a plasmid-coded virulence gene of Shigella flexneri: identification of the virG protein and determination of the complete coding sequence. J Bacteriol. 1989 Jan;171(1):353–359. doi: 10.1128/jb.171.1.353-359.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Makino S., Sasakawa C., Kamata K., Kurata T., Yoshikawa M. A genetic determinant required for continuous reinfection of adjacent cells on large plasmid in S. flexneri 2a. Cell. 1986 Aug 15;46(4):551–555. doi: 10.1016/0092-8674(86)90880-9. [DOI] [PubMed] [Google Scholar]
  39. Marck C. 'DNA Strider': a 'C' program for the fast analysis of DNA and protein sequences on the Apple Macintosh family of computers. Nucleic Acids Res. 1988 Mar 11;16(5):1829–1836. doi: 10.1093/nar/16.5.1829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Mengaud J., Vicente M. F., Chenevert J., Pereira J. M., Geoffroy C., Gicquel-Sanzey B., Baquero F., Perez-Diaz J. C., Cossart P. Expression in Escherichia coli and sequence analysis of the listeriolysin O determinant of Listeria monocytogenes. Infect Immun. 1988 Apr;56(4):766–772. doi: 10.1128/iai.56.4.766-772.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Michel E., Reich K. A., Favier R., Berche P., Cossart P. Attenuated mutants of the intracellular bacterium Listeria monocytogenes obtained by single amino acid substitutions in listeriolysin O. Mol Microbiol. 1990 Dec;4(12):2167–2178. doi: 10.1111/j.1365-2958.1990.tb00578.x. [DOI] [PubMed] [Google Scholar]
  42. Niebuhr K., Chakraborty T., Rohde M., Gazlig T., Jansen B., Köllner P., Wehland J. Localization of the ActA polypeptide of Listeria monocytogenes in infected tissue culture cell lines: ActA is not associated with actin "comets". Infect Immun. 1993 Jul;61(7):2793–2802. doi: 10.1128/iai.61.7.2793-2802.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Noble M., Lewis S. A., Cowan N. J. The microtubule binding domain of microtubule-associated protein MAP1B contains a repeated sequence motif unrelated to that of MAP2 and tau. J Cell Biol. 1989 Dec;109(6 Pt 2):3367–3376. doi: 10.1083/jcb.109.6.3367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Pistor S., Chakraborty T., Niebuhr K., Domann E., Wehland J. The ActA protein of Listeria monocytogenes acts as a nucleator inducing reorganization of the actin cytoskeleton. EMBO J. 1994 Feb 15;13(4):758–763. doi: 10.1002/j.1460-2075.1994.tb06318.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Pollard T. D., Selden S. C., Maupin P. Interaction of actin filaments with microtubules. J Cell Biol. 1984 Jul;99(1 Pt 2):33s–37s. doi: 10.1083/jcb.99.1.33s. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Sheehan B., Kocks C., Dramsi S., Gouin E., Klarsfeld A. D., Mengaud J., Cossart P. Molecular and genetic determinants of the Listeria monocytogenes infectious process. Curr Top Microbiol Immunol. 1994;192:187–216. doi: 10.1007/978-3-642-78624-2_9. [DOI] [PubMed] [Google Scholar]
  48. Stokes G. V. High-voltage electron microscope study of the release of vaccinia virus from whole cells. J Virol. 1976 May;18(2):636–643. doi: 10.1128/jvi.18.2.636-643.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Vazquez-Boland J. A., Kocks C., Dramsi S., Ohayon H., Geoffroy C., Mengaud J., Cossart P. Nucleotide sequence of the lecithinase operon of Listeria monocytogenes and possible role of lecithinase in cell-to-cell spread. Infect Immun. 1992 Jan;60(1):219–230. doi: 10.1128/iai.60.1.219-230.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Vulliet P. R., Hall F. L., Mitchell J. P., Hardie D. G. Identification of a novel proline-directed serine/threonine protein kinase in rat pheochromocytoma. J Biol Chem. 1989 Sep 25;264(27):16292–16298. [PubMed] [Google Scholar]
  51. Wuenscher M. D., Köhler S., Bubert A., Gerike U., Goebel W. The iap gene of Listeria monocytogenes is essential for cell viability, and its gene product, p60, has bacteriolytic activity. J Bacteriol. 1993 Jun;175(11):3491–3501. doi: 10.1128/jb.175.11.3491-3501.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES