1887

Abstract

is an important food-borne bacterial pathogen and listeriosis can result in abortions in pregnant women. The bacterium can colonize food-processing environments, where specific molecular subtypes can persist for years. The purpose of this study was to determine the virulence potential of a group of food-processing persistent strains encoding a premature stop codon in (encoding internalin A) by using two orally dosed models, pregnant mice and pregnant guinea pigs. A food-processing persistent strain of invaded placentas ( = 58; 10 % positive) and fetuses (3 % positive) of pregnant mice ( = 9 animals per strain), similar to a genetically manipulated murinized strain, EGD-e InlA ( = 61; 3 and 2 %, respectively). In pregnant guinea pigs ( = 9 animals per bacterial strain), a maternofetal strain (from a human fetal clinical fatal case) was isolated from 34 % of placenta samples ( = 50), whereas both food-processing persistent strains were found in 5 % of placenta samples ( = 36 or 37). One of the food-processing persistent strains, N53-1, was found in up to 8 % of guinea pig fetal liver and brain samples, whereas the maternofetal control was found in 6 % of fetal tissue samples. As the food-processing persistent strains carry a premature stop codon in but are invasive in orally dosed pregnant mice and guinea pigs, we hypothesize that listerial crossing of the placental barrier can occur by a mechanism that is independent of an interaction between E-cadherin and InlA.

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2013-12-01
2020-01-29
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References

  1. Autio T. , Hielm S. , Miettinen M. K. , Sjöberg A. M. , Aarnisalo K. , Björkroth J. , Mattila-Sandholm T. , Korkeala H. . ( 1999; ). Sources of Listeria monocytogenes contamination in a cold-smoked rainbow trout processing plant detected by pulsed-field gel electrophoresis typing. . Appl Environ Microbiol 65:, 150–155.[PubMed]
    [Google Scholar]
  2. Bakardjiev A. I. , Stacy B. A. , Fisher S. J. , Portnoy D. A. . ( 2004; ). Listeriosis in the pregnant guinea pig: a model of vertical transmission. . Infect Immun 72:, 489–497. [CrossRef] [PubMed]
    [Google Scholar]
  3. Bakardjiev A. I. , Stacy B. A. , Portnoy D. A. . ( 2005; ). Growth of Listeria monocytogenes in the guinea pig placenta and role of cell-to-cell spread in fetal infection. . J Infect Dis 191:, 1889–1897. [CrossRef] [PubMed]
    [Google Scholar]
  4. Chambel L. , Sol M. , Fernandes I. , Barbosa M. , Zilhão I. , Barata B. , Jordan S. , Perni S. , Shama G. . & other authors ( 2007; ). Occurrence and persistence of Listeria spp. in the environment of ewe and cow’s milk cheese dairies in Portugal unveiled by an integrated analysis of identification, typing and spatial-temporal mapping along production cycle. . Int J Food Microbiol 116:, 52–63. [CrossRef] [PubMed]
    [Google Scholar]
  5. Disson O. , Grayo S. , Huillet E. , Nikitas G. , Langa-Vives F. , Dussurget O. , Ragon M. , Le Monnier A. , Babinet C. . & other authors ( 2008; ). Conjugated action of two species-specific invasion proteins for fetoplacental listeriosis. . Nature 455:, 1114–1118. [CrossRef] [PubMed]
    [Google Scholar]
  6. 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 Microbiol 16:, 251–261. [CrossRef] [PubMed]
    [Google Scholar]
  7. Drevets D. A. , Schawang J. E. , Dillon M. J. , Lerner M. R. , Bronze M. S. , Brackett D. J. . ( 2008; ). Innate responses to systemic infection by intracellular bacteria trigger recruitment of Ly-6Chigh monocytes to the brain. . J Immunol 181:, 529–536.[PubMed] [CrossRef]
    [Google Scholar]
  8. Gaillard J. L. , Berche P. , Frehel C. , Gouin E. , Cossart P. . ( 1991; ). Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from Gram-positive cocci. . Cell 65:, 1127–1141. [CrossRef] [PubMed]
    [Google Scholar]
  9. Gillespie I. A. , McLauchlin J. , Grant K. A. , Little C. L. , Mithani V. , Penman C. , Lane C. , Regan M. . ( 2006; ). Changing pattern of human listeriosis, England and Wales, 2001–2004. . Emerg Infect Dis 12:, 1361–1366. [CrossRef] [PubMed]
    [Google Scholar]
  10. Hansen C. H. , Vogel B. F. , Gram L. . ( 2006; ). Prevalence and survival of Listeria monocytogenes in Danish aquatic and fish-processing environments. . J Food Prot 69:, 2113–2122.[PubMed]
    [Google Scholar]
  11. Hildebrand F. , Nguyen T. L. A. , Brinkman B. , Yunta R. G. , Cauwe B. , Vandenabeele P. , Liston A. , Raes J. . ( 2013; ). Inflammation-associated enterotypes, host genotype, cage and inter-individual effects drive gut microbiota variation in common laboratory mice. . Genome Biol 14:, R4. [CrossRef] [PubMed]
    [Google Scholar]
  12. Hoffman A. D. , Gall K. L. , Norton D. M. , Wiedmann M. . ( 2003; ). Listeria monocytogenes contamination patterns for the smoked fish processing environment and for raw fish. . J Food Prot 66:, 52–60.[PubMed]
    [Google Scholar]
  13. Holch A. , Gottlieb C. T. , Larsen M. H. , Ingmer H. , Gram L. . ( 2010; ). Poor invasion of trophoblastic cells but normal plaque formation in fibroblastic cells despite actA deletion in a group of Listeria monocytogenes strains persisting in some food processing environments. . Appl Environ Microbiol 76:, 3391–3397. [CrossRef] [PubMed]
    [Google Scholar]
  14. Holch A. , Webb K. , Lukjancenko O. , Ussery D. , Rosenthal B. M. , Gram L. . ( 2013; ). Genome sequencing identifies two nearly unchanged strains of persistent Listeria monocytogenes isolated at two different fish processing plants sampled 6 years apart. . Appl Environ Microbiol 79:, 2944–2951. [CrossRef] [PubMed]
    [Google Scholar]
  15. Hufeldt M. R. , Nielsen D. S. , Vogensen F. K. , Midtvedt T. , Hansen A. K. . ( 2010; ). Variation in the gut microbiota of laboratory mice is related to both genetic and environmental factors. . Comp Med 60:, 336–347.[PubMed]
    [Google Scholar]
  16. Jacquet C. , Doumith M. , Gordon J. I. , Martin P. M. V. , Cossart P. , Lecuit M. . ( 2004; ). A molecular marker for evaluating the pathogenic potential of foodborne Listeria monocytogenes . . J Infect Dis 189:, 2094–2100. [CrossRef] [PubMed]
    [Google Scholar]
  17. Jensen A. , Larsen M. H. , Ingmer H. , Vogel B. F. , Gram L. . ( 2007; ). Sodium chloride enhances adherence and aggregation and strain variation influences invasiveness of Listeria monocytogenes strains. . J Food Prot 70:, 592–599.[PubMed]
    [Google Scholar]
  18. Jensen A. , Thomsen L. E. , Jørgensen R. L. , Larsen M. H. , Roldgaard B. B. , Christensen B. B. , Vogel B. F. , Gram L. , Ingmer H. . ( 2008a; ). Processing plant persistent strains of Listeria monocytogenes appear to have a lower virulence potential than clinical strains in selected virulence models. . Int J Food Microbiol 123:, 254–261. [CrossRef] [PubMed]
    [Google Scholar]
  19. Jensen A. , Williams D. , Irvin E. A. , Gram L. , Smith M. A. . ( 2008b; ). A processing plant persistent strain of Listeria monocytogenes crosses the fetoplacental barrier in a pregnant guinea pig model. . J Food Prot 71:, 1028–1034.[PubMed]
    [Google Scholar]
  20. Kastbjerg V. G. , Gram L. . ( 2009; ). Model systems allowing quantification of sensitivity to disinfectants and comparison of disinfectant susceptibility of persistent and presumed nonpersistent Listeria monocytogenes . . J Appl Microbiol 106:, 1667–1681. [CrossRef] [PubMed]
    [Google Scholar]
  21. Keto-Timonen R. , Tolvanen R. , Lundén J. , Korkeala H. . ( 2007; ). An 8-year surveillance of the diversity and persistence of Listeria monocytogenes in a chilled food processing plant analyzed by amplified fragment length polymorphism. . J Food Prot 70:, 1866–1873.[PubMed]
    [Google Scholar]
  22. Khelef N. , Lecuit M. , Bierne H. , Cossart P. . ( 2006; ). Species specificity of the Listeria monocytogenes InlB protein. . Cell Microbiol 8:, 457–470. [CrossRef] [PubMed]
    [Google Scholar]
  23. Lamont R. F. , Sobel J. , Mazaki-Tovi S. , Kusanovic J. P. , Vaisbuch E. , Kim S. K. , Uldbjerg N. , Romero R. . ( 2011; ). Listeriosis in human pregnancy: a systematic review. . J Perinat Med 39:, 227–236. [CrossRef] [PubMed]
    [Google Scholar]
  24. Le Monnier A. , Join-Lambert O. F. , Jaubert F. , Berche P. , Kayal S. . ( 2006; ). Invasion of the placenta during murine listeriosis. . Infect Immun 74:, 663–672. [CrossRef] [PubMed]
    [Google Scholar]
  25. Le Monnier A. , Autret N. , Join-Lambert O. F. , Jaubert F. , Charbit A. , Berche P. , Kayal S. . ( 2007; ). ActA is required for crossing of the fetoplacental barrier by Listeria monocytogenes . . Infect Immun 75:, 950–957. [CrossRef] [PubMed]
    [Google Scholar]
  26. Lecuit M. , Ohayon H. , Braun L. , Mengaud J. , Cossart P. . ( 1997; ). Internalin of Listeria monocytogenes with an intact leucine-rich repeat region is sufficient to promote internalization. . Infect Immun 65:, 5309–5319.[PubMed]
    [Google Scholar]
  27. Lecuit M. , Dramsi S. , Gottardi C. , Fedor-Chaiken M. , Gumbiner B. , Cossart P. . ( 1999; ). A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes . . EMBO J 18:, 3956–3963. [CrossRef] [PubMed]
    [Google Scholar]
  28. Lecuit M. , Vandormael-Pournin S. , Lefort J. , Huerre M. , Gounon P. , Dupuy C. , Babinet C. , Cossart P. . ( 2001; ). A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. . Science 292:, 1722–1725. [CrossRef] [PubMed]
    [Google Scholar]
  29. Lecuit M. , Nelson D. M. , Smith S. D. , Khun H. , Huerre M. , Vacher-Lavenu M. C. , Gordon J. I. , Cossart P. . ( 2004; ). Targeting and crossing of the human maternofetal barrier by Listeria monocytogenes: role of internalin interaction with trophoblast E-cadherin. . Proc Natl Acad Sci U S A 101:, 6152–6157. [CrossRef] [PubMed]
    [Google Scholar]
  30. Licht T. R. , Ebersbach T. , Frokiaer H. . ( 2012; ). Prebiotics for prevention of gut infections. . Trends Food Sci Technol 23:, 70–82. [CrossRef]
    [Google Scholar]
  31. MacGowan A. P. , Bowker K. , McLauchlin J. , Bennett P. M. , Reeves D. S. . ( 1994; ). The occurrence and seasonal changes in the isolation of Listeria spp. in shop bought food stuffs, human faeces, sewage and soil from urban sources. . Int J Food Microbiol 21:, 325–334. [CrossRef] [PubMed]
    [Google Scholar]
  32. Mengaud J. , Ohayon H. , Gounon P. , Mege, R.M. , Cossart P. . ( 1996; ). E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. . Cell 84:, 923–932. [CrossRef] [PubMed]
    [Google Scholar]
  33. Monk I. R. , Casey P. G. , Hill C. , Gahan C. G. M. . ( 2010; ). Directed evolution and targeted mutagenesis to murinize Listeria monocytogenes internalin A for enhanced infectivity in the murine oral infection model. . BMC Microbiol 10:, 318. [CrossRef] [PubMed]
    [Google Scholar]
  34. Nightingale K. K. , Ivy R. A. , Ho A. J. , Fortes E. D. , Njaa B. L. , Peters R. M. , Wiedmann M. . ( 2008; ). inlA premature stop codons are common among Listeria monocytogenes isolates from foods and yield virulence-attenuated strains that confer protection against fully virulent strains. . Appl Environ Microbiol 74:, 6570–6583. [CrossRef] [PubMed]
    [Google Scholar]
  35. Norton D. M. , Scarlett J. M. , Horton K. , Sue D. , Thimothe J. , Boor K. J. , Wiedmann M. . ( 2001; ). Characterization and pathogenic potential of Listeria monocytogenes isolates from the smoked fish industry. . Appl Environ Microbiol 67:, 646–653. [CrossRef] [PubMed]
    [Google Scholar]
  36. Petersen A. , Bergström A. , Andersen J. B. , Hansen M. , Lahtinen S. J. , Wilcks A. , Licht T. R. . ( 2010; ). Analysis of the intestinal microbiota of oligosaccharide fed mice exhibiting reduced resistance to Salmonella infection. . Benef Microbes 1:, 271–281. [CrossRef] [PubMed]
    [Google Scholar]
  37. Robbins J. R. , Skrzypczynska K. M. , Zeldovich V. B. , Kapidzic M. , Bakardjiev A. I. . ( 2010; ). Placental syncytiotrophoblast constitutes a major barrier to vertical transmission of Listeria monocytogenes . . PLoS Pathog 6:, e1000732. [CrossRef] [PubMed]
    [Google Scholar]
  38. Roldgaard B. B. , Andersen J. B. , Hansen T. B. , Christensen B. B. , Licht T. R. . ( 2009; ). Comparison of three Listeria monocytogenes strains in a guinea-pig model simulating food-borne exposure. . FEMS Microbiol Lett 291:, 88–94. [CrossRef] [PubMed]
    [Google Scholar]
  39. Rørvik L. M. , Caugant D. A. , Yndestad M. . ( 1995; ). Contamination pattern of Listeria monocytogenes and other Listeria spp. in a salmon slaughterhouse and smoked salmon processing plant. . Int J Food Microbiol 25:, 19–27. [CrossRef] [PubMed]
    [Google Scholar]
  40. Smith B. , Kemp M. , Ethelberg S. , Schiellerup P. , Bruun B. G. , Gerner-Smidt P. , Christensen J. J. . ( 2009; ). Listeria monocytogenes: maternal–foetal infections in Denmark 1994-2005. . Scand J Infect Dis 41:, 21–25. [CrossRef] [PubMed]
    [Google Scholar]
  41. Van Stelten A. , Simpson J. M. , Chen Y. , Scott V. N. , Whiting R. C. , Ross W. H. , Nightingale K. K. . ( 2011; ). Significant shift in median guinea pig infectious dose shown by an outbreak-associated Listeria monocytogenes epidemic clone strain and a strain carrying a premature stop codon mutation in inlA . . Appl Environ Microbiol 77:, 2479–2487. [CrossRef] [PubMed]
    [Google Scholar]
  42. Vázquez-Boland J. A. , Kuhn M. , Berche P. , Chakraborty T. , Domínguez-Bernal G. , Goebel W. , González-Zorn B. , Wehland J. , Kreft J. . ( 2001; ). Listeria pathogenesis and molecular virulence determinants. . Clin Microbiol Rev 14:, 584–640. [CrossRef] [PubMed]
    [Google Scholar]
  43. Vogel B. F. , Jørgensen L. V. , Ojeniyi B. , Huss H. H. , Gram L. . ( 2001; ). Diversity of Listeria monocytogenes isolates from cold-smoked salmon produced in different smokehouses as assessed by random amplified polymorphic DNA analyses. . Int J Food Microbiol 65:, 83–92. [CrossRef] [PubMed]
    [Google Scholar]
  44. Vogel B. F. , Hansen L. T. , Mordhorst H. , Gram L. . ( 2010; ). The survival of Listeria monocytogenes during long term desiccation is facilitated by sodium chloride and organic material. . Int J Food Microbiol 140:, 192–200. [CrossRef] [PubMed]
    [Google Scholar]
  45. Wulff G. , Gram L. , Ahrens P. , Vogel B. F. . ( 2006; ). One group of genetically similar Listeria monocytogenes strains frequently dominates and persists in several fish slaughter- and smokehouses. . Appl Environ Microbiol 72:, 4313–4322. [CrossRef] [PubMed]
    [Google Scholar]
  46. Zeldovich V. B. , Robbins J. R. , Kapidzic M. , Lauer P. , Bakardjiev A. I. . ( 2011; ). Invasive extravillous trophoblasts restrict intracellular growth and spread of Listeria monocytogenes . . PLoS Pathog 7:, e1002005. [CrossRef] [PubMed]
    [Google Scholar]
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