1887

Abstract

is a foodborne pathogen able to infect humans and many other mammalian species, leading to serious, often fatal disease. We have previously identified a five-gene locus in the genome of EGD-e which comprised three contiguous genes encoding paralogous type I signal peptidases. In the present study, we focused on the two distal genes of the locus ( and ), encoding proteins sharing significant similarities with the YlqF and RnhB proteins, respectively, of . could complement an thermosensitive growth phenotype, suggesting that it encodes a functional RNase H. Strikingly, inactivation of provoked a strong attenuation of virulence in the mouse model, and kinetic studies in infected mice revealed that multiplication of the mutant in target organs was significantly impaired. However, the mutation did not impair intracellular multiplication or cell-to-cell spread in cell culture models. Transcriptional profiles obtained with an -overexpressing strain were compared to those of the wild-type strain, using microarray analyses. The data obtained suggest a pleiotropic regulatory role of Lmo1273 and possible links with amino acid uptake.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.022277-0
2009-03-01
2020-07-13
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/3/891.html?itemId=/content/journal/micro/10.1099/mic.0.022277-0&mimeType=html&fmt=ahah

References

  1. Arnaud M., Chastanet A., Débarbouillé M.. 2004; New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol70:6887–6891
    [Google Scholar]
  2. Arudchandran A., Cerritelli S., Narimatsu S., Itaya M., Shin D. Y., Shimada Y., Crouch R. J.. 2000; The absence of ribonuclease H1 or H2 alters the sensitivity of Saccharomyces cerevisiae to hydroxyurea, caffeine and ethyl methanesulphonate: implications for roles of RNases H in DNA replication and repair. Genes Cells5:789–802
    [Google Scholar]
  3. Bayliss C. D., Sweetman W. A., Moxon E. R.. 2005; Destabilization of tetranucleotide repeats in Haemophilus influenzae mutants lacking RnaseHI or the Klenow domain of PolI. Nucleic Acids Res33:400–408
    [Google Scholar]
  4. Bigot A., Botton E., Dubail I., Charbit A.. 2006; A homolog of Bacillus subtilis trigger factor in Listeria monocytogenes is involved in stress tolerance and bacterial virulence. Appl Environ Microbiol72:6623–6631
    [Google Scholar]
  5. Bonnemain C., Raynaud C., Reglier-Poupet H., Dubail I., Frehel C., Lety M. A., Berche P., Charbit A.. 2004; Differential roles of multiple signal peptidases in the virulence of Listeria monocytogenes. Mol Microbiol51:1251–1266
    [Google Scholar]
  6. Chatterjee S. S., Hossain H., Otten S., Kuenne C., Kuchmina K., Machata S., Domann E., Chakraborty T., Hain T.. 2006; Intracellular gene expression profile of Listeria monocytogenes. Infect Immun74:1323–1338
    [Google Scholar]
  7. Condon C.. 2003; RNA processing and degradation in Bacillus subtilis. Microbiol Mol Biol Rev67:157–174
    [Google Scholar]
  8. Crouch R. J.. 1990; Ribonuclease H: from discovery to 3D structure. New Biol2:771–777
    [Google Scholar]
  9. de Chastellier C., Berche P.. 1994; Fate of Listeria monocytogenes in murine macrophages: evidence for simultaneous killing and survival of intracellular bacteria. Infect Immun62:543–553
    [Google Scholar]
  10. Dramsi S., Biswas I., Maguin E., Braun L., Mastroeni P., Cossart P.. 1995; Entry of Listeria monocytogenes into hepatocytes requires expression of InIB, a surface protein of the internalin multigene family. Mol Microbiol16:251–261
    [Google Scholar]
  11. Engelbrecht F., Dominguez-Bernal G., Hess J., Dickneite C., Greiffenberg L., Lampidis R., Raffelsbauer D., Daniels J. J., Kreft J.. other authors 1998; A novel PrfA-regulated chromosomal locus, which is specific for Listeria ivanovii, encodes two small, secreted internalins and contributes to virulence in mice. Mol Microbiol30:405–417
    [Google Scholar]
  12. Farber J. M., Peterkin P. I.. 1991; Listeria monocytogenes, a food-borne pathogen. Microbiol Rev55:476–511
    [Google Scholar]
  13. Finney D. J.. 1971; Statistical aspects of monitoring for dangers in drug therapy. Methods Inf Med10:237–245
    [Google Scholar]
  14. Frehel C., Leduc M.. 1987; Cytochemical localization of lipopolysaccharides during peptidoglycan degradation of Escherichia coli cells. J Bacteriol169:210–217
    [Google Scholar]
  15. Fukushima S., Itaya M., Kato H., Ogasawara N., Yoshikawa H.. 2007; Reassessment of the in vivo functions of DNA polymerase I and RNase H in bacterial cell growth. J Bacteriol189:8575–8583
    [Google Scholar]
  16. Glaser P., Frangeul L., Buchrieser C., Rusniok C., Amend A., Baquero F., Berche P., Bloecker H., Brandt P.. other authors 2001; Comparative genomics of Listeria species. Science294:849–852
    [Google Scholar]
  17. Hain T., Steinweg C., Kuenne C. T., Billion A., Ghai R., Chatterjee S. S., Domann E., Kärst U., Goesmann A.. other authors 2006; Whole-genome sequence of Listeria welshimeri reveals common steps in genome reduction with Listeria innocua as compared to Listeria monocytogenes. J Bacteriol188:7405–7415
    [Google Scholar]
  18. Hain T., Hossain H., Chatterjee S. S., Machata S., Volk U., Wagner S., Brors B., Haas S., Kuenne C. T.. other authors 2008; Temporal transcriptomic analysis of the Listeria monocytogenes EGD-e sigmaB regulon. BMC Microbiol8:20
    [Google Scholar]
  19. Hamon M., Bierne H., Cossat P.. 2006; Listeria monocytogenes: a multifaceted model. Nat Rev Microbiol4:423–434
    [Google Scholar]
  20. Haruki M., Tsunaka Y., Morikawa M., Kanaya S.. 2002; Cleavage of a DNA-RNA-DNA/DNA chimeric substrate containing a single ribonucleotide at the DNA-RNA junction with prokaryotic RNases HII. FEBS Lett531:204–208
    [Google Scholar]
  21. Itaya M., Omori A., Kanaya R., Crouch J., Tanaka T., Kondo K.. 1999; Isolation of RNase H genes that are essential for growth of Bacillus subtilis 168. J Bacteriol181:2118–2123
    [Google Scholar]
  22. Joseph B., Przybilla K., Stuhler C., Schauer K., Slaghuis J., Fuchs T. M., Goebel W.. 2006; Identification of Listeria monocytogenes genes contributing to intracellular replication by expression profiling and mutant screening. J Bacteriol188:556–568
    [Google Scholar]
  23. Katayanagi K., Miyagawa M., Matsushima M., Ishikawa M., Kanaya S., Ikehara M., Matsuzaki T., Morikawa K.. 1990; Three-dimensional structure of ribonuclease H from E. coli. Nature347:306–309
    [Google Scholar]
  24. Kazmierczak M. J., Mithoe S. C., Boor K. J., Wiedman M.. 2003; Listeria monocytogenes sigma B regulates stress response and virulence functions. J Bacteriol185:5722–5734
    [Google Scholar]
  25. Klarsfeld A. D., Goossens P. L., Cossart P.. 1994; Five Listeria monocytogenes genes preferentially expressed in infected mammalian cells:plcA, purH, purD, pyrE and an arginine ABC transporter gene, arpJ. Mol Microbiol13:585–597
    [Google Scholar]
  26. Lauer P., Chow M. J., Loessner M. J., Portnoy D. A., Calendar R.. 2002; Construction, characterization and use of two Listeria monocytogenes site-specific phage integration vectors. J Bacteriol184:4177–4186
    [Google Scholar]
  27. Lingnau A., Domann E., Hudel M., Bock M., Nichterlein T., Wehland J., Chakraborty T.. 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 Immun63:3896–3903
    [Google Scholar]
  28. Matsuo Y., Morimoto T., Kuwano M., Loh P. C., Oshima T., Ogasawara N.. 2006; The GTP-binding protein YlqF participates in the late step of 50S ribosomal subunit assembly in Bacillus subtilis. J Biol Chem281:8110–8117
    [Google Scholar]
  29. Morimoto T., Loh P. C., Hirai T., Asai K., Kobayashi K., Moriya S., Ogasawara N.. 2002; Six GTP-binding proteins of the Era/Obg family are essential for cell growth in Bacillus subtilis. Microbiology148:3539–3552
    [Google Scholar]
  30. Ohtani N., Haruki M., Morikawa M., Crouch J., Itaya M., Kanaya R.. 1999a; Identification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII from Bacillus subtilis: classification of RNase H into three families. Biochemistry38:605–618
    [Google Scholar]
  31. Ohtani N., Haruki M., Morikawa M., Kanaya S.. 1999b; Molecular diversities of RNases H. J Biosci Bioeng88:12–19
    [Google Scholar]
  32. Park S. F., Stewart G. S.. 1990; High efficiency transformation of Listeria monocytogenes by electroporation of penicillin-treated cells. Gene94:129–132
    [Google Scholar]
  33. Pucciarelli M. G., Calvo E., Sabet C., Bierne H., Cossart P., Garcia-del Portillo F.. 2005; Identification of substrates of the Listeria monocytogenes sortases A and B by a non-gel proteomic analysis. Proteomics5:4808–4817
    [Google Scholar]
  34. Qiu J., Qian Y., Frank P., Wintersberger U., Shen B.. 1999; Saccharomyces cerevisiae RNase H(35) functions in RNA primer removal during lagging-strand DNA synthesis, most efficiently in cooperation with Rad27 nuclease. Mol Cell Biol19:8361–8371
    [Google Scholar]
  35. Raynaud C., Charbit A.. 2005; Regulation of expression of type I signal peptidases in Listeria monocytogenes. Microbiology151:3769–3776
    [Google Scholar]
  36. Rydberg B., Game J.. 2002; Excision of misincorporated ribonucleotides in DNA by RNase H (type 2) and FEN-1 in cell-free extracts. Proc Natl Acad Sci U S A99:16654–16659
    [Google Scholar]
  37. Sabet C., Toledo-Arana A., Personnic N., Lecuit M., Dubrac S., Poupel O., Gouin E., Nahori M. A., Cossart P., Bierne H.. 2008; The Listeria monocytogenes virulence factor InlJ is specifically expressed in vivo and behaves as an adhesin. Infect Immun76:1368–1378
    [Google Scholar]
  38. Stintzi A.. 2003; Gene expression profile of Campylobacter jejuni in response to growth temperature variations. J Bacteriol185:2009–2016
    [Google Scholar]
  39. Uicker W. C., Schaefer L., Koenigsknecht M., Britton R. A.. 2007; The essential GTPase YqeH is required for proper ribosome assembly in Bacillus subtilis. J Bacteriol189:2926–2929
    [Google Scholar]
  40. Vazquez-Boland J. A., Kuhn M., Berche P., Chakraborty T., Dominguez-Bernal G., Goebel W., Gonzalez-Zorn B.. 2001; Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev14:584–640
    [Google Scholar]
  41. Vieira J., Messing J.. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene33:103–119
    [Google Scholar]
  42. Zhang Y. B., Ayalew S., Lacks S. A.. 1997; The rnhB gene encoding RNase HII of Streptococcus pneumoniae and evidence of conserved motifs in eucaryotic genes. J Bacteriol179:3828–3836
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.022277-0
Loading
/content/journal/micro/10.1099/mic.0.022277-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error