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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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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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.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1005015</identifier><identifier>PMID: 26230630</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Bacteria ; Beekeeping ; Bees - immunology ; Blotting, Western ; Chromatography ; Colleges & universities ; E coli ; Egg Proteins - immunology ; Experiments ; Female ; Honey ; Immune system ; Immunoglobulins ; Immunology ; Insects ; Molecular weight ; Ovum - immunology ; Proteins ; Surface Plasmon Resonance ; Vertebrates ; Vitellogenins - immunology</subject><ispartof>PLoS pathogens, 2015-07, Vol.11 (7), p.e1005015-e1005015</ispartof><rights>2015 Salmela et al 2015 Salmela et al</rights><rights>2015 Public Library of Science. 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 credited: Salmela H, Amdam GV, Freitak D (2015) Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin. 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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.</description><subject>Animals</subject><subject>Bacteria</subject><subject>Beekeeping</subject><subject>Bees - immunology</subject><subject>Blotting, Western</subject><subject>Chromatography</subject><subject>Colleges & universities</subject><subject>E coli</subject><subject>Egg Proteins - immunology</subject><subject>Experiments</subject><subject>Female</subject><subject>Honey</subject><subject>Immune system</subject><subject>Immunoglobulins</subject><subject>Immunology</subject><subject>Insects</subject><subject>Molecular weight</subject><subject>Ovum - immunology</subject><subject>Proteins</subject><subject>Surface Plasmon Resonance</subject><subject>Vertebrates</subject><subject>Vitellogenins - immunology</subject><issn>1553-7374</issn><issn>1553-7366</issn><issn>1553-7374</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNpVUk1v1DAQjRCIfsA_QOAjlyz-jJMLEqraslKrcihIVQ-W44_US2IvtlOp_75eNq3ai23NvHkzb_yq6hOCK0Q4-rYJc_RyXG23Mq8QhAwi9qY6RIyRmhNO3754H1RHKW0gpIig5n11gBtMYEPgYXV7HaVP1kQQLFhP0-xdfgA2hglchnxX4jmAK2vTNjo_gHUCl0Y7mY0G906C02Gob8L4F_yKIRvnwR-XzTiGwXjnP1TvrByT-bjcx9Xvs9Prk5_1xdX5-uTHRa0axHJtYWsxR8S0ipq2Z4T2UHOMESUtM7bvuGIaEgRRq3rS4l43VHNFWdNjRbQmx9WXPe92DEkse0kCcQwph4w2BbHeI3SQG1GkTDI-iCCd-B8IcRAyZqdGIwimbaMM4aTpKCyHpbq1CvcGdbBHXeH6vnSb-8loZXyOcnxF-jrj3Z0Ywr2gDKMWskLwdSGI4d9sUhaTS6psTXoT5t3cRWkHGeMFSvdQFUNK0djnNgiKnQue1IqdC8TiglL2-eWIz0VP304eAY26sFA</recordid><startdate>20150701</startdate><enddate>20150701</enddate><creator>Salmela, Heli</creator><creator>Amdam, Gro V</creator><creator>Freitak, Dalial</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20150701</creationdate><title>Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin</title><author>Salmela, Heli ; Amdam, Gro V ; Freitak, Dalial</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c615t-f08f2713e8c4e8b534b0d72214385efb97c5d031018cb382bd64d7c456b2c3dd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Bacteria</topic><topic>Beekeeping</topic><topic>Bees - immunology</topic><topic>Blotting, Western</topic><topic>Chromatography</topic><topic>Colleges & universities</topic><topic>E coli</topic><topic>Egg Proteins - immunology</topic><topic>Experiments</topic><topic>Female</topic><topic>Honey</topic><topic>Immune system</topic><topic>Immunoglobulins</topic><topic>Immunology</topic><topic>Insects</topic><topic>Molecular weight</topic><topic>Ovum - immunology</topic><topic>Proteins</topic><topic>Surface Plasmon Resonance</topic><topic>Vertebrates</topic><topic>Vitellogenins - immunology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Salmela, Heli</creatorcontrib><creatorcontrib>Amdam, Gro V</creatorcontrib><creatorcontrib>Freitak, Dalial</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Salmela, Heli</au><au>Amdam, Gro V</au><au>Freitak, Dalial</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2015-07-01</date><risdate>2015</risdate><volume>11</volume><issue>7</issue><spage>e1005015</spage><epage>e1005015</epage><pages>e1005015-e1005015</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26230630</pmid><doi>10.1371/journal.ppat.1005015</doi><oa>free_for_read</oa></addata></record> |
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subjects | Animals Bacteria Beekeeping Bees - immunology Blotting, Western Chromatography Colleges & universities E coli Egg Proteins - immunology Experiments Female Honey Immune system Immunoglobulins Immunology Insects Molecular weight Ovum - immunology Proteins Surface Plasmon Resonance Vertebrates Vitellogenins - immunology |
title | Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin |
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