Parental Transfer of the Antimicrobial Protein LBP/BPI Protects Biomphalaria glabrata Eggs against Oomycete Infections

Autor: Michel Ponchet, Benoit Industri, Olga Baron, Pieter van West, Géraldine Dubreuil, Jean-Marc Reichhart, Benjamin Gourbal, Christine Coustau
Přispěvatelé: Réponse immunitaire et developpement chez les insectes (RIDI - UPR 9002), Université de Strasbourg (UNISTRA)-Institut de biologie moléculaire et cellulaire (IBMC), Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM), Oomycete Laboratory, University of Aberdeen, Institut de recherche sur la biologie de l'insecte UMR7261 (IRBI), Université de Tours-Centre National de la Recherche Scientifique (CNRS), Ecologie et évolution des interactions [2011-2014] (2EI), Université de Perpignan Via Domitia (UPVD)-Centre National de la Recherche Scientifique (CNRS), Interactions Biotiques et Santé Végétale (IBSV), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS), ANR [ANR-07-BLAN-0214, ANR-12-EMMA-00O7-01], CNRS, INRA, BBSRC, Ecologie et évolution des interactions (2EI), Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA)-Centre National de la Recherche Scientifique (CNRS), Reichhart, Jean-Marc, Coustau, Christine, Institut de biologie moléculaire et cellulaire (IBMC), Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Université de Tours (UT)-Centre National de la Recherche Scientifique (CNRS)
Jazyk: angličtina
Rok vydání: 2013
Předmět:
Cell Membrane Permeability
Zygote
Virologie
Biomphalaria
antibactérien
0302 clinical medicine
invertébré
Cloning
Molecular
lcsh:QH301-705.5
Oomycete
0303 health sciences
Membrane Glycoproteins
biology
[SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
Microbiology and Parasitology
Blood Proteins
oomycète
Recombinant Proteins
Microbiologie et Parasitologie
Oomycetes
Female
bactérie pathogène
Lipopolysaccharide binding protein
Research Article
lcsh:Immunologic diseases. Allergy
food.ingredient
Offspring
Immunology
Microbial Sensitivity Tests
Infections
Microbiology
03 medical and health sciences
food
Immunity
Virology
Yolk
Escherichia coli
Genetics
Animals
Biomphalaria glabrata
Molecular Biology
lipide
030304 developmental biology
Cell Membrane
biology.organism_classification
Bactericidal/permeability-increasing protein
lcsh:Biology (General)
bactérie gram négatif
biology.protein
Parasitology
protéine recombinante
lcsh:RC581-607
Carrier Proteins
Immunity
Maternally-Acquired
Acute-Phase Proteins
Antimicrobial Cationic Peptides
030215 immunology
Zdroj: PLoS Pathogens
PLoS Pathogens, Public Library of Science, 2013, 9 (12), pp.e1003792. ⟨10.1371/journal.ppat.1003792⟩
Plos Pathogens 12 (9), . (2013)
PLoS Pathogens, Vol 9, Iss 12, p e1003792 (2013)
ISSN: 1553-7366
1553-7374
DOI: 10.1371/journal.ppat.1003792⟩
Popis: 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.
Author Summary Vertebrate immune systems not only protect adult organisms against infections but also increase survival of offspring through parental transfer of innate and adaptive immune factors via the placenta, colostrum and milk or via the egg yolk. This maternal transfer of immunity is critical for species survival as embryos and neonates are immunologically immature and unable to fight off infections at early life stages. Parental immune protection is poorly documented in invertebrates and how the estimated 1.3 million of invertebrate species protect their eggs against pathogens remains an intriguing question. Here, we show that a fresh-water snail, Biomphalaria glabrata massively loads its eggs with a lipopolysaccharide binding protein/bactericidal permeability increasing protein (LBP/BPI) displaying expected antibacterial activities. Remarkably, this snail LBP/BPI also displayed a strong biocidal activity against water molds (oomycetes). This yet unsuspected activity is conserved in human BPI. Gene expression knock-down resulted in the reduction of snail reproductive success and massive death of eggs after water mold infections. This work reveals a novel and conserved biocidal activity for LBP/BPI family members and demonstrates that the snail LBP/BPI represents a major fitness-related protein transferred from parents to their clutches and protecting them from widespread and lethal oomycete infections.
Databáze: OpenAIRE
Externí odkaz: