Parental transfer of the antimicrobial protein LBP/BPI protects Biomphalaria glabrata eggs against oomycete infections

Olga Lucia Baron, Pieter van West, Benoit Industri, Michel Ponchet, Geraldine Dubreuil, Benjamin Gourbal, Jean-Marc Reichhart, Christine Coustau

Research output: Contribution to journalArticle

30 Citations (Scopus)
3 Downloads (Pure)

Abstract

Vertebrate females transfer antibodies via the placenta, colostrum and milk or via the egg yolk to protect their immunologically immature offspring against pathogens. This evolutionarily important transfer of immunity is poorly documented in invertebrates and basic questions remain regarding the nature and extent of parental protection of offspring. In this study, we show that a lipopolysaccharide binding protein/bactericidal permeability increasing protein family member from the invertebrate Biomphalaria glabrata (BgLBP/BPI1) is massively loaded into the eggs of this freshwater snail. Native and recombinant proteins displayed conserved LPS-binding, antibacterial and membrane permeabilizing activities. A broad screening of various pathogens revealed a previously unknown biocidal activity of the protein against pathogenic water molds (oomycetes), which is conserved in human BPI. RNAi-dependent silencing of LBP/BPI in the parent snails resulted in a significant reduction of reproductive success and extensive death of eggs through oomycete infections. This work provides the first functional evidence that a LBP/BPI is involved in the parental immune protection of invertebrate offspring and reveals a novel and conserved biocidal activity for LBP/BPI family members.

Original languageEnglish
Article numbere1003792
Number of pages10
JournalPLoS Pathogens
Volume9
Issue number12
DOIs
Publication statusPublished - 19 Dec 2013

Keywords

  • bactericidal/permeability-increasing protein
  • lipopolysaccharide-binding-protein
  • gram-negative bacteria
  • LPS-binding
  • host-defense
  • saprolegnia-parasitica
  • schistosoma-mansoni
  • structural-analysis
  • albumin gland
  • drosophila

Cite this

Parental transfer of the antimicrobial protein LBP/BPI protects Biomphalaria glabrata eggs against oomycete infections. / Baron, Olga Lucia; van West, Pieter; Industri, Benoit; Ponchet, Michel; Dubreuil, Geraldine; Gourbal, Benjamin; Reichhart, Jean-Marc; Coustau, Christine.

In: PLoS Pathogens, Vol. 9, No. 12, e1003792, 19.12.2013.

Research output: Contribution to journalArticle

Baron, OL, van West, P, Industri, B, Ponchet, M, Dubreuil, G, Gourbal, B, Reichhart, J-M & Coustau, C 2013, 'Parental transfer of the antimicrobial protein LBP/BPI protects Biomphalaria glabrata eggs against oomycete infections' PLoS Pathogens, vol. 9, no. 12, e1003792. https://doi.org/10.1371/journal.ppat.1003792
Baron, Olga Lucia ; van West, Pieter ; Industri, Benoit ; Ponchet, Michel ; Dubreuil, Geraldine ; Gourbal, Benjamin ; Reichhart, Jean-Marc ; Coustau, Christine. / Parental transfer of the antimicrobial protein LBP/BPI protects Biomphalaria glabrata eggs against oomycete infections. In: PLoS Pathogens. 2013 ; Vol. 9, No. 12.
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abstract = "Vertebrate females transfer antibodies via the placenta, colostrum and milk or via the egg yolk to protect their immunologically immature offspring against pathogens. This evolutionarily important transfer of immunity is poorly documented in invertebrates and basic questions remain regarding the nature and extent of parental protection of offspring. In this study, we show that a lipopolysaccharide binding protein/bactericidal permeability increasing protein family member from the invertebrate Biomphalaria glabrata (BgLBP/BPI1) is massively loaded into the eggs of this freshwater snail. Native and recombinant proteins displayed conserved LPS-binding, antibacterial and membrane permeabilizing activities. A broad screening of various pathogens revealed a previously unknown biocidal activity of the protein against pathogenic water molds (oomycetes), which is conserved in human BPI. RNAi-dependent silencing of LBP/BPI in the parent snails resulted in a significant reduction of reproductive success and extensive death of eggs through oomycete infections. This work provides the first functional evidence that a LBP/BPI is involved in the parental immune protection of invertebrate offspring and reveals a novel and conserved biocidal activity for LBP/BPI family members.",
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