Parental transfer of the antimicrobial protein LBP/BPI protects Biomphalaria glabrata eggs against oomycete infections.
Parental transfer of the antimicrobial protein LBP/BPI protects Biomphalaria glabrata eggs against oomycete infections.
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DOI:
10.1371/journal.ppat.1003792
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发表时间:
2013
期刊:
影响因子:
6.7
通讯作者:
Coustau C
中科院分区:
文献类型:
--
作者:
Baron OL;van West P;Industri B;Ponchet M;Dubreuil G;Gourbal B;Reichhart JM;Coustau C
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. 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.
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影响因子:
1.6
作者:
Gardsvoll, Henrik;Hansen, Line V.;Ploug, Michael
通讯作者:
Ploug, Michael
影响因子:
5.1
作者:
Galiana, Eric;Fourre, Sandra;Engler, Gilbert
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作者:
Benkendorff, K;Davis, AR;Bremner, J
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Bremner, J
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作者:
GAZZANOSANTORO, H;PARENT, JB;CONLON, PJ
通讯作者:
CONLON, PJ
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作者:
Barbault, F;Landon, C;Vovelle, F
通讯作者:
Vovelle, F