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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...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2015
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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. |
format | Online Article Text |
id | pubmed-4521805 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
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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