1887

Abstract

is a genetically heterogeneous species, which is divided into evolutionary lineages and clonal complexes (CCs). Not all isolates are equally likely to cause disease, with CC1, and in particular sequence type (ST) 1, being the most prevalent complex in human and ruminant infections and more specifically in neurolisteriosis. While the major factors that determine neurotropism are unknown, the CC1 strains harbour listeriolysin S () and particular alleles of internalin () F and , which are not present in CCs commonly isolated from food and the environment. The aim of this study was to analyse the role of these factors in cellular infection.

A ST1 field strain (JF5203) from CC1 isolated from a bovine rhombencephalitis case was used to create deletion mutants. These were tested alongside the parental strain and EGD-e (CC9), in different culture models representing targets (neurons, microglia, placenta, intestine and macrophages). The phenotype was assessed by quantification of c.f.u. from cell lysates and immunofluorescence analysis.

Compared to EGD-e, the ST1 strain JF5203 was hyperinvasive and exhibited increased intercellular spread. However, deletion of , or 1, had no significant effect on infection or growth in the culture models tested.

Our results underline the importance of using relevant clinical strains when investigating virulence. We show that despite the association with CC1, , and 1 are not involved in the hyperinvasiveness and efficient intercellular spread of ST1 in various cell types.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000529
2017-07-01
2024-11-06
Loading full text...

Full text loading...

/deliver/fulltext/jmm/66/7/1053.html?itemId=/content/journal/jmm/10.1099/jmm.0.000529&mimeType=html&fmt=ahah

References

  1. Hernandez-Milian A, Payeras-Cifre A. What is new in Listeriosis?. Biomed Res Int 2014; 2014:1–7 [View Article]
    [Google Scholar]
  2. de Noordhout CM, Devleesschauwer B, Angulo FJ, Verbeke G, Haagsma J et al. The global burden of listeriosis: a systematic review and meta-analysis. Lancet Infect Dis 2014; 14:1073–1082 [View Article][PubMed]
    [Google Scholar]
  3. Listeriology CP. The rise of a model pathogen. Microbes Infect 2007; 9:1143–1146 [CrossRef]
    [Google Scholar]
  4. Camejo A, Carvalho F, Reis O, Leitão E, Sousa S et al. The arsenal of virulence factors deployed by Listeria monocytogenes to promote its cell infection cycle. Virulence 2011; 2:379–394 [View Article][PubMed]
    [Google Scholar]
  5. Vázquez-Boland JA, Kuhn M, Berche P, Chakraborty T, Domínguez-Bernal G et al. Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 2001; 14:584–640 [View Article][PubMed]
    [Google Scholar]
  6. Bécavin C, Bouchier C, Lechat P, Archambaud C, Creno S et al. Comparison of widely used Listeria monocytogenes strains EGD, 10403S, and EGD-e highlights genomic variations underlying differences in pathogenicity. MBio 2014; 5:e00969-14 [View Article][PubMed]
    [Google Scholar]
  7. Ragon M, Wirth T, Hollandt F, Lavenir R, Lecuit M et al. A new perspective on Listeria monocytogenes evolution. PLoS Pathog 2008; 4:e1000146 [View Article][PubMed]
    [Google Scholar]
  8. Balandyté L, Brodard I, Frey J, Oevermann A, Abril C. Ruminant rhombencephalitis-associated Listeria monocytogenes alleles linked to a multilocus variable-number tandem-repeat analysis complex. Appl Environ Microbiol 2011; 77:8325–8335 [View Article][PubMed]
    [Google Scholar]
  9. Maury MM, Tsai YH, Charlier C, Touchon M, Chenal-Francisque V et al. Uncovering Listeria monocytogenes hypervirulence by harnessing its biodiversity. Nat Genet 2016; 48:308–313 [View Article][PubMed]
    [Google Scholar]
  10. Dreyer M, Aguilar-Bultet L, Rupp S, Guldimann C, Stephan R et al. Listeria monocytogenes sequence type 1 is predominant in ruminant rhombencephalitis. Sci Rep 2016; 6:36419 [View Article][PubMed]
    [Google Scholar]
  11. Kim SH, Bakko MK, Knowles D, Borucki MK. Oral inoculation of A/J mice for detection of invasiveness differences between Listeria monocytogenes epidemic and environmental strains. Infect Immun 2004; 72:4318–4321 [View Article][PubMed]
    [Google Scholar]
  12. Guldimann C, Bärtschi M, Frey J, Zurbriggen A, Seuberlich T et al. Increased spread and replication efficiency of Listeria monocytogenes in organotypic brain-slices is related to multilocus variable number of tandem repeat analysis (MLVA) complex. BMC Microbiol 2015; 15:134 [View Article][PubMed]
    [Google Scholar]
  13. Cotter PD, Draper LA, Lawton EM, Daly KM, Groeger DS et al. Listeriolysin S, a novel peptide haemolysin associated with a subset of lineage I Listeria monocytogenes. PLoS Pathog 2008; 4:e1000144-10 [View Article][PubMed]
    [Google Scholar]
  14. Bierne H, Sabet C, Personnic N, Cossart P. Internalins: a complex family of leucine-rich repeat-containing proteins in Listeria monocytogenes. Microbes Infect 2007; 9:1156–1166 [View Article][PubMed]
    [Google Scholar]
  15. Dramsi S, Dehoux P, Lebrun M, Goossens PL, Cossart P. Identification of four new members of the internalin multigene family of Listeria monocytogenes EGD. Infect Immun 1997; 65:1615–1625[PubMed]
    [Google Scholar]
  16. Kirchner M, Higgins DE. Inhibition of ROCK activity allows InlF-mediated invasion and increased virulence of Listeria monocytogenes. Mol Microbiol 2008; 68:749–767 [View Article][PubMed]
    [Google Scholar]
  17. Jia Y, Nightingale KK, Boor KJ, Ho A, Wiedmann M et al. Distribution of internalin gene profiles of Listeria monocytogenes isolates from different sources associated with phylogenetic lineages. Foodborne Pathog Dis 2007; 4:222–232 [View Article][PubMed]
    [Google Scholar]
  18. Sabet C, Lecuit M, Cabanes D, Cossart P, Bierne H. LPXTG protein InlJ, a newly identified internalin involved in Listeria monocytogenes virulence. Infect Immun 2005; 73:6912–6922 [View Article][PubMed]
    [Google Scholar]
  19. Sabet C, Toledo-Arana A, Personnic N, Lecuit M, Dubrac S et al. The Listeria monocytogenes virulence factor InlJ is specifically expressed in vivo and behaves as an adhesin. Infect Immun 2008; 76:1368–1378 [View Article][PubMed]
    [Google Scholar]
  20. Quereda JJ, Dussurget O, Nahori MA, Ghozlane A, Volant S et al. Bacteriocin from epidemic Listeria strains alters the host intestinal microbiota to favor infection. Proc Natl Acad Sci USA 2016; 113:5706–5711 [View Article][PubMed]
    [Google Scholar]
  21. Guldimann C, Lejeune B, Hofer S, Leib SL, Frey J et al. Ruminant organotypic brain-slice cultures as a model for the investigation of CNS listeriosis. Int J Exp Pathol 2012; 93:259–268 [View Article][PubMed]
    [Google Scholar]
  22. Stabel JR, Stabel TJ. Immortalization and characterization of bovine peritoneal macrophages transfected with SV40 plasmid DNA. Vet Immunol Immunopathol 1995; 45:211–220 [View Article][PubMed]
    [Google Scholar]
  23. Takenouchi T, Iwamaru Y, Sato M, Yokoyama T, Kitani H. Establishment of an SV40 large T antigen-immortalized bovine brain cell line and its neuronal differentiation by dibutyryl-cyclic AMP. Cell Biol Int 2009; 33:187–191 [View Article][PubMed]
    [Google Scholar]
  24. Bridger PS, Menge C, Leiser R, Tinneberg HR, Pfarrer CD. Bovine caruncular epithelial cell line (BCEC-1) isolated from the placenta forms a functional epithelial barrier in a polarised cell culture model. Placenta 2007; 28:1110–1117 [View Article][PubMed]
    [Google Scholar]
  25. Rupp S, Aguilar-Bultet L, Jagannathan V, Guldimann C, Drögemüller C et al. A naturally occurring prfA truncation in a Listeria monocytogenes field strain contributes to reduced replication and cell-to-cell spread. Vet Microbiol 2015; 179:91–101 [View Article][PubMed]
    [Google Scholar]
  26. Glaser P, Frangeul L, Buchrieser C, Rusniok C, Amend A et al. Comparative genomics of Listeria species. Science 2001; 294:849–852 [View Article][PubMed]
    [Google Scholar]
  27. Arnaud M, Chastanet A, Débarbouillé M. New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 2004; 70:6887–6891 [View Article][PubMed]
    [Google Scholar]
  28. Henke D, Rupp S, Gaschen V, Stoffel MH, Frey J et al. Listeria monocytogenes spreads within the brain by actin-based intra-axonal migration. Infect Immun 2015; 83:2409–2419 [View Article][PubMed]
    [Google Scholar]
  29. Lauer P, Chow MY, Loessner MJ, Portnoy DA, Calendar R. Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. J Bacteriol 2002; 184:4177–4186 [View Article][PubMed]
    [Google Scholar]
  30. Behrens S, Widder S, Mannala GK, Qing X, Madhugiri R et al. Ultra deep sequencing of Listeria monocytogenes sRNA transcriptome revealed new antisense RNAs. PLoS One 2014; 9:e83979 [View Article][PubMed]
    [Google Scholar]
  31. Suo Y, Liu Y, Zhou X, Huang Y, Shi C et al. Impact of sod on the expression of stress-related genes in Listeria monocytogenes 4b G with/without paraquat treatment. J Food Sci 2014; 79:M1745–M1749 [View Article][PubMed]
    [Google Scholar]
  32. Gaillard JL, Berche P, Mounier J, Richard S, Sansonetti P. In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect Immun 1987; 55:2822–2829[PubMed]
    [Google Scholar]
  33. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 2012; 9:676–682 [View Article][PubMed]
    [Google Scholar]
  34. Rengarajan M, Hayer A, Theriot JA. Endothelial cells use a formin-dependent phagocytosis-like process to internalize the bacterium Listeria monocytogenes. PLoS Pathog 2016; 12:e1005603 [View Article][PubMed]
    [Google Scholar]
  35. Roberts AJ, Wiedmann M. Allelic exchange and site-directed mutagenesis probe the contribution of ActA amino-acid variability to phosphorylation and virulence-associated phenotypes among Listeria monocytogenes strains. FEMS Microbiol Lett 2006; 254:300–307 [View Article][PubMed]
    [Google Scholar]
  36. Moura A, Criscuolo A, Pouseele H, Maury MM, Leclercq A et al. Whole genome-based population biology and epidemiological surveillance of Listeria monocytogenes. Nat Microbiol 2016; 2:16185 [View Article][PubMed]
    [Google Scholar]
  37. Mackaness GB. Cellular resistance to infection. J Exp Med 1962; 116:381–406 [CrossRef]
    [Google Scholar]
  38. Dramsi S, Lévi S, Triller A, Cossart P. Entry of Listeria monocytogenes into neurons occurs by cell-to-cell spread: an in vitro study. Infect Immun 1998; 66:4461–4468[PubMed]
    [Google Scholar]
  39. Drevets DA. Dissemination of Listeria monocytogenes by infected phagocytes. Infect Immun 1999; 67:3512–3517[PubMed]
    [Google Scholar]
  40. Drevets DA, Dillon MJ, Schawang JS, van Rooijen N, Ehrchen J et al. The Ly-6Chigh monocyte subpopulation transports Listeria monocytogenes into the brain during systemic infection of mice. J Immunol 2004; 172:4418–4424 [View Article][PubMed]
    [Google Scholar]
  41. Kocks C, Gouin E, Tabouret M, Berche P, Ohayon H et al. L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 1992; 68:521–531 [View Article][PubMed]
    [Google Scholar]
  42. Stabel JR, Stabel TJ. Immortalization and characterization of bovine peritoneal macrophages transfected with SV40 plasmid DNA. Vet Immunol Immunopathol 1995; 45:211–220 [View Article][PubMed]
    [Google Scholar]
  43. Lull ME, Block ML. Microglial activation and chronic neurodegeneration. Neurotherapeutics 2010; 7:354–365 [View Article][PubMed]
    [Google Scholar]
  44. Tsai YH, Orsi RH, Nightingale KK, Wiedmann M. Listeria monocytogenes internalins are highly diverse and evolved by recombination and positive selection. Infect Genet Evol 2006; 6:378–389 [View Article][PubMed]
    [Google Scholar]
  45. Cantinelli T, Chenal-Francisque V, Diancourt L, Frezal L, Leclercq A et al. "Epidemic clones" of Listeria monocytogenes are widespread and ancient clonal groups. J Clin Microbiol 2013; 51:3770–3779 [View Article][PubMed]
    [Google Scholar]
/content/journal/jmm/10.1099/jmm.0.000529
Loading
/content/journal/jmm/10.1099/jmm.0.000529
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
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