Role for a somatically diversified lectin in resistance of an invertebrate to parasite infection
Invertebrates lack adaptive immune systems homologous to those of vertebrates, yet it is becoming increasingly clear that they can produce diversified antigen recognition molecules. We have previously noted that the snail Biomphalaria glabrata produces a secreted lectin, fibrinogen-related protein 3...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2010-12, Vol.107 (49), p.21087-21092 |
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| container_title | Proceedings of the National Academy of Sciences - PNAS |
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| creator | Hanington, Patrick C. Forys, Michelle A. Dragoo, Jerry W. Zhang, Si-Ming Adema, Coen M. Loker, Eric S. Cooper, Max D. |
| description | Invertebrates lack adaptive immune systems homologous to those of vertebrates, yet it is becoming increasingly clear that they can produce diversified antigen recognition molecules. We have previously noted that the snail Biomphalaria glabrata produces a secreted lectin, fibrinogen-related protein 3 (FREP3), unusual among invertebrate defense molecules because it is somatically diversified by gene conversion and point mutation. Here we implicate FREP3 in playing a central role in resistance to a major group of snail pathogens, digenetic trematodes. FREP3 is up-regulated in three models of resistance of B. glabrata to infection with Schistosoma mansoni or Echinostoma paraensei, and functions as an opsonin favoring phagocytosis by hemocytes. Knock-down of FREP3 in resistant snails using siRNA-mediated interference resulted in increased susceptibility to E. paraensei, providing a direct link between a gastropod immune molecule and resistance to trematodes. FREP3 up-regulation is also associated with heightened responsiveness following priming with attenuated digenetic trematodes (acquired resistance) in this model invertebrate immune system. |
| doi_str_mv | 10.1073/pnas.1011242107 |
| format | Article |
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We have previously noted that the snail Biomphalaria glabrata produces a secreted lectin, fibrinogen-related protein 3 (FREP3), unusual among invertebrate defense molecules because it is somatically diversified by gene conversion and point mutation. Here we implicate FREP3 in playing a central role in resistance to a major group of snail pathogens, digenetic trematodes. FREP3 is up-regulated in three models of resistance of B. glabrata to infection with Schistosoma mansoni or Echinostoma paraensei, and functions as an opsonin favoring phagocytosis by hemocytes. Knock-down of FREP3 in resistant snails using siRNA-mediated interference resulted in increased susceptibility to E. paraensei, providing a direct link between a gastropod immune molecule and resistance to trematodes. FREP3 up-regulation is also associated with heightened responsiveness following priming with attenuated digenetic trematodes (acquired resistance) in this model invertebrate immune system.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1011242107</identifier><identifier>PMID: 21084634</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Adaptive Immunity ; Animals ; Antigens ; Biological Sciences ; Biomphalaria - immunology ; Biomphalaria - parasitology ; Biomphalaria glabrata ; Echinostoma - immunology ; Echinostoma paraensei ; Echinostomiasis ; Gastropoda ; Gene expression ; Hemocytes ; Immune system ; Immunoglobulins - immunology ; Immunology ; Infections ; Invertebrata ; Invertebrates ; Lectins ; Lectins - immunology ; Marine ; Miracidia ; Molecules ; Mollusks ; Mutation ; Opsonin Proteins ; Parasites ; Parasitism ; Phagocytosis ; Proteins ; Schistosoma mansoni ; Schistosoma mansoni - immunology ; Schistosomiasis mansoni ; Snails</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2010-12, Vol.107 (49), p.21087-21092</ispartof><rights>Copyright National Academy of Sciences Dec 7, 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c530t-139c8dd361fdc448dd231de83c7637437d53317825087a830c4acee5f13906523</citedby><cites>FETCH-LOGICAL-c530t-139c8dd361fdc448dd231de83c7637437d53317825087a830c4acee5f13906523</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/107/49.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/25756836$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/25756836$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21084634$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hanington, Patrick C.</creatorcontrib><creatorcontrib>Forys, Michelle A.</creatorcontrib><creatorcontrib>Dragoo, Jerry W.</creatorcontrib><creatorcontrib>Zhang, Si-Ming</creatorcontrib><creatorcontrib>Adema, Coen M.</creatorcontrib><creatorcontrib>Loker, Eric S.</creatorcontrib><creatorcontrib>Cooper, Max D.</creatorcontrib><title>Role for a somatically diversified lectin in resistance of an invertebrate to parasite infection</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Invertebrates lack adaptive immune systems homologous to those of vertebrates, yet it is becoming increasingly clear that they can produce diversified antigen recognition molecules. We have previously noted that the snail Biomphalaria glabrata produces a secreted lectin, fibrinogen-related protein 3 (FREP3), unusual among invertebrate defense molecules because it is somatically diversified by gene conversion and point mutation. Here we implicate FREP3 in playing a central role in resistance to a major group of snail pathogens, digenetic trematodes. FREP3 is up-regulated in three models of resistance of B. glabrata to infection with Schistosoma mansoni or Echinostoma paraensei, and functions as an opsonin favoring phagocytosis by hemocytes. Knock-down of FREP3 in resistant snails using siRNA-mediated interference resulted in increased susceptibility to E. paraensei, providing a direct link between a gastropod immune molecule and resistance to trematodes. FREP3 up-regulation is also associated with heightened responsiveness following priming with attenuated digenetic trematodes (acquired resistance) in this model invertebrate immune system.</description><subject>Adaptive Immunity</subject><subject>Animals</subject><subject>Antigens</subject><subject>Biological Sciences</subject><subject>Biomphalaria - immunology</subject><subject>Biomphalaria - parasitology</subject><subject>Biomphalaria glabrata</subject><subject>Echinostoma - immunology</subject><subject>Echinostoma paraensei</subject><subject>Echinostomiasis</subject><subject>Gastropoda</subject><subject>Gene expression</subject><subject>Hemocytes</subject><subject>Immune system</subject><subject>Immunoglobulins - immunology</subject><subject>Immunology</subject><subject>Infections</subject><subject>Invertebrata</subject><subject>Invertebrates</subject><subject>Lectins</subject><subject>Lectins - immunology</subject><subject>Marine</subject><subject>Miracidia</subject><subject>Molecules</subject><subject>Mollusks</subject><subject>Mutation</subject><subject>Opsonin Proteins</subject><subject>Parasites</subject><subject>Parasitism</subject><subject>Phagocytosis</subject><subject>Proteins</subject><subject>Schistosoma mansoni</subject><subject>Schistosoma mansoni - immunology</subject><subject>Schistosomiasis mansoni</subject><subject>Snails</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkkuLFDEUhYMoTtu6dqUEN67KSXLz3Agy-IIBQXQdM6mUpqlO2iQ9MP_elN1Oq5sJCbncfOdALgehp5S8okTB-S652itKGWe9cQ-tKDF0kNyQ-2hFCFOD5oyfoUe1bgghRmjyEJ11VnMJfIW-fc5zwFMu2OGat65F7-b5Bo_xOpQapxhGPAffYsJ9l1BjbS75gPOE3dLrWAtXxbWAW8Y7V1yNvY5pWlQ5PUYPJjfX8OR4r9HXd2-_XHwYLj-9_3jx5nLwAkgbKBivxxEknUbPeS8Z0DFo8EqC4qBGAUCVZoJo5TQQz50PQUxdSKRgsEavD767_dU2jD6kVtxsdyVuXbmx2UX770uKP-z3fG2hj4UZ2g1eHg1K_rkPtdltrD7Ms0sh76s1RFGujdF3klpIJRX0dSdJpTLACO_ki__ITd6X1CfWIUUlmH7W6PwA-ZJrLWG6_R4ldsmDXfJgT3noiud_T-WW_xOADuAjsChPdspy85taPJ4dkE1tuZwshBJSg4Rf65XFEg</recordid><startdate>20101207</startdate><enddate>20101207</enddate><creator>Hanington, Patrick C.</creator><creator>Forys, Michelle A.</creator><creator>Dragoo, Jerry W.</creator><creator>Zhang, Si-Ming</creator><creator>Adema, Coen M.</creator><creator>Loker, Eric S.</creator><creator>Cooper, Max D.</creator><general>National Academy of Sciences</general><general>National Acad Sciences</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>5PM</scope></search><sort><creationdate>20101207</creationdate><title>Role for a somatically diversified lectin in resistance of an invertebrate to parasite infection</title><author>Hanington, Patrick C. ; 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We have previously noted that the snail Biomphalaria glabrata produces a secreted lectin, fibrinogen-related protein 3 (FREP3), unusual among invertebrate defense molecules because it is somatically diversified by gene conversion and point mutation. Here we implicate FREP3 in playing a central role in resistance to a major group of snail pathogens, digenetic trematodes. FREP3 is up-regulated in three models of resistance of B. glabrata to infection with Schistosoma mansoni or Echinostoma paraensei, and functions as an opsonin favoring phagocytosis by hemocytes. Knock-down of FREP3 in resistant snails using siRNA-mediated interference resulted in increased susceptibility to E. paraensei, providing a direct link between a gastropod immune molecule and resistance to trematodes. 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| subjects | Adaptive Immunity Animals Antigens Biological Sciences Biomphalaria - immunology Biomphalaria - parasitology Biomphalaria glabrata Echinostoma - immunology Echinostoma paraensei Echinostomiasis Gastropoda Gene expression Hemocytes Immune system Immunoglobulins - immunology Immunology Infections Invertebrata Invertebrates Lectins Lectins - immunology Marine Miracidia Molecules Mollusks Mutation Opsonin Proteins Parasites Parasitism Phagocytosis Proteins Schistosoma mansoni Schistosoma mansoni - immunology Schistosomiasis mansoni Snails |
| title | Role for a somatically diversified lectin in resistance of an invertebrate to parasite infection |
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