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Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin

Insect immune systems can recognize specific pathogens and prime offspring immunity. High specificity of immune priming can be achieved when insect females transfer immune elicitors into developing oocytes. The molecular mechanism behind this transfer has been a mystery. Here, we establish that the...

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Detalles Bibliográficos
Autores principales: Salmela, Heli, Amdam, Gro V., Freitak, Dalial
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4521805/
https://www.ncbi.nlm.nih.gov/pubmed/26230630
http://dx.doi.org/10.1371/journal.ppat.1005015
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author Salmela, Heli
Amdam, Gro V.
Freitak, Dalial
author_facet Salmela, Heli
Amdam, Gro V.
Freitak, Dalial
author_sort Salmela, Heli
collection PubMed
description Insect immune systems can recognize specific pathogens and prime offspring immunity. High specificity of immune priming can be achieved when insect females transfer immune elicitors into developing oocytes. The molecular mechanism behind this transfer has been a mystery. Here, we establish that the egg-yolk protein vitellogenin is the carrier of immune elicitors. Using the honey bee, Apis mellifera, model system, we demonstrate with microscopy and western blotting that vitellogenin binds to bacteria, both Paenibacillus larvae – the gram-positive bacterium causing American foulbrood disease – and to Escherichia coli that represents gram-negative bacteria. Next, we verify that vitellogenin binds to pathogen-associated molecular patterns; lipopolysaccharide, peptidoglycan and zymosan, using surface plasmon resonance. We document that vitellogenin is required for transport of cell-wall pieces of E. coli into eggs by imaging tissue sections. These experiments identify vitellogenin, which is distributed widely in oviparous species, as the carrier of immune-priming signals. This work reveals a molecular explanation for trans-generational immunity in insects and a previously undescribed role for vitellogenin.
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spelling pubmed-45218052015-08-06 Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin Salmela, Heli Amdam, Gro V. Freitak, Dalial PLoS Pathog Research Article Insect immune systems can recognize specific pathogens and prime offspring immunity. High specificity of immune priming can be achieved when insect females transfer immune elicitors into developing oocytes. The molecular mechanism behind this transfer has been a mystery. Here, we establish that the egg-yolk protein vitellogenin is the carrier of immune elicitors. Using the honey bee, Apis mellifera, model system, we demonstrate with microscopy and western blotting that vitellogenin binds to bacteria, both Paenibacillus larvae – the gram-positive bacterium causing American foulbrood disease – and to Escherichia coli that represents gram-negative bacteria. Next, we verify that vitellogenin binds to pathogen-associated molecular patterns; lipopolysaccharide, peptidoglycan and zymosan, using surface plasmon resonance. We document that vitellogenin is required for transport of cell-wall pieces of E. coli into eggs by imaging tissue sections. These experiments identify vitellogenin, which is distributed widely in oviparous species, as the carrier of immune-priming signals. This work reveals a molecular explanation for trans-generational immunity in insects and a previously undescribed role for vitellogenin. Public Library of Science 2015-07-31 /pmc/articles/PMC4521805/ /pubmed/26230630 http://dx.doi.org/10.1371/journal.ppat.1005015 Text en © 2015 Salmela et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Salmela, Heli
Amdam, Gro V.
Freitak, Dalial
Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin
title Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin
title_full Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin
title_fullStr Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin
title_full_unstemmed Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin
title_short Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin
title_sort transfer of immunity from mother to offspring is mediated via egg-yolk protein vitellogenin
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4521805/
https://www.ncbi.nlm.nih.gov/pubmed/26230630
http://dx.doi.org/10.1371/journal.ppat.1005015
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