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Expanded collectin family in bullfrog (Rana catesbeiana): Identification and characterization of plasma collectins
BLAST searches against databases for the bullfrog (Rana catesbeiana), using the collectin sequence previously identified in tadpoles, revealed the presence of at least 20 members of the collectin gene family. Phylogenetic analysis demonstrated that the bullfrog possesses expanded gene subfamilies en...
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Published in: | Developmental and comparative immunology 2021-09, Vol.122, p.104108-104108, Article 104108 |
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description | BLAST searches against databases for the bullfrog (Rana catesbeiana), using the collectin sequence previously identified in tadpoles, revealed the presence of at least 20 members of the collectin gene family. Phylogenetic analysis demonstrated that the bullfrog possesses expanded gene subfamilies encoding mannose-binding lectin (MBL) and pulmonary surfactant-associated protein D (PSAPD). Two collectins, of 20 kDa (PSAPD1) and 25 kDa (PSAPD6), were purified as a mixture from adult bullfrog plasma using affinity chromatography. These collectins were present as an oligomer of ~400 kDa in their native state, and showed Ca2+-dependent carbohydrate binding with different sugar preferences. Affinity-purified collectins showed weak E. coli agglutination and bactericidal activities, compared with those of plasma. Although both PSAPD1 and PSAPD6 genes were predominantly expressed in the liver, PSAPD1 transcripts were abundant in adults whereas PSAPD6 transcripts were abundant in tadpoles. The findings indicate that two gene subfamilies in the collectin family have diverged structurally, functionally and transcriptionally in the bullfrog. Rapid expansion of the collectin family in bullfrogs may reflect the onset of sub-functionalization of the prototype MBL gene towards tetrapod MBL and PSAPDs, and may be one means of natural adaptation in the innate immune system to various pathogens in both aquatic and terrestrial environments.
•Bullfrog has expanded collectin gene family.•Two bullfrog collectins were isolated from the plasma and characterized.•The plasma collectins structurally, functionally and transcriptionally diverged.•Tetrapod MBL, PSAPA and PSAPD separated in the sarcopterygian lineage. |
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•Bullfrog has expanded collectin gene family.•Two bullfrog collectins were isolated from the plasma and characterized.•The plasma collectins structurally, functionally and transcriptionally diverged.•Tetrapod MBL, PSAPA and PSAPD separated in the sarcopterygian lineage.</description><identifier>ISSN: 0145-305X</identifier><identifier>EISSN: 1879-0089</identifier><identifier>DOI: 10.1016/j.dci.2021.104108</identifier><identifier>PMID: 33909995</identifier><language>eng</language><publisher>United States: Elsevier Ltd</publisher><subject>Affinity ; Affinity chromatography ; Agglutination ; Agglutination - immunology ; Animals ; Aquatic environment ; Bacterial Adhesion - immunology ; Binding ; Calcium ; Calcium ions ; Carbohydrate Metabolism - immunology ; Carbohydrates ; Carbohydrates - immunology ; Collectin ; Collectins ; Collectins - blood ; Collectins - genetics ; Collectins - metabolism ; E coli ; Escherichia coli - immunology ; Evolution ; Expression ; Frogs ; Immune system ; Immunity, Innate - genetics ; Immunity, Innate - immunology ; Innate immunity ; Juveniles ; Larva - immunology ; Mannose ; Mannose-binding lectin ; Mannose-Binding Lectin - blood ; Mannose-Binding Lectin - genetics ; Mannose-Binding Lectin - metabolism ; Molecular structure ; Phylogeny ; Protein D ; Pulmonary Surfactant-Associated Protein D - blood ; Pulmonary Surfactant-Associated Protein D - genetics ; Pulmonary Surfactant-Associated Protein D - metabolism ; Rana catesbeiana ; Rana catesbeiana - metabolism ; Saccharide recognition ; Terrestrial environments ; Transcription</subject><ispartof>Developmental and comparative immunology, 2021-09, Vol.122, p.104108-104108, Article 104108</ispartof><rights>2021 Elsevier Ltd</rights><rights>Copyright © 2021 Elsevier Ltd. All rights reserved.</rights><rights>Copyright Elsevier Science Ltd. Sep 2021</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c333t-bc21288d63b64d5264b7f27642ba749dbbff6497fb9adbac6081dd4c892e05523</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33909995$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Okada, Masako</creatorcontrib><creatorcontrib>Akimoto, Takanori</creatorcontrib><creatorcontrib>Ishihara, Akinori</creatorcontrib><creatorcontrib>Yamauchi, Kiyoshi</creatorcontrib><title>Expanded collectin family in bullfrog (Rana catesbeiana): Identification and characterization of plasma collectins</title><title>Developmental and comparative immunology</title><addtitle>Dev Comp Immunol</addtitle><description>BLAST searches against databases for the bullfrog (Rana catesbeiana), using the collectin sequence previously identified in tadpoles, revealed the presence of at least 20 members of the collectin gene family. Phylogenetic analysis demonstrated that the bullfrog possesses expanded gene subfamilies encoding mannose-binding lectin (MBL) and pulmonary surfactant-associated protein D (PSAPD). Two collectins, of 20 kDa (PSAPD1) and 25 kDa (PSAPD6), were purified as a mixture from adult bullfrog plasma using affinity chromatography. These collectins were present as an oligomer of ~400 kDa in their native state, and showed Ca2+-dependent carbohydrate binding with different sugar preferences. Affinity-purified collectins showed weak E. coli agglutination and bactericidal activities, compared with those of plasma. Although both PSAPD1 and PSAPD6 genes were predominantly expressed in the liver, PSAPD1 transcripts were abundant in adults whereas PSAPD6 transcripts were abundant in tadpoles. The findings indicate that two gene subfamilies in the collectin family have diverged structurally, functionally and transcriptionally in the bullfrog. Rapid expansion of the collectin family in bullfrogs may reflect the onset of sub-functionalization of the prototype MBL gene towards tetrapod MBL and PSAPDs, and may be one means of natural adaptation in the innate immune system to various pathogens in both aquatic and terrestrial environments.
•Bullfrog has expanded collectin gene family.•Two bullfrog collectins were isolated from the plasma and characterized.•The plasma collectins structurally, functionally and transcriptionally diverged.•Tetrapod MBL, PSAPA and PSAPD separated in the sarcopterygian lineage.</description><subject>Affinity</subject><subject>Affinity chromatography</subject><subject>Agglutination</subject><subject>Agglutination - immunology</subject><subject>Animals</subject><subject>Aquatic environment</subject><subject>Bacterial Adhesion - immunology</subject><subject>Binding</subject><subject>Calcium</subject><subject>Calcium ions</subject><subject>Carbohydrate Metabolism - immunology</subject><subject>Carbohydrates</subject><subject>Carbohydrates - immunology</subject><subject>Collectin</subject><subject>Collectins</subject><subject>Collectins - blood</subject><subject>Collectins - genetics</subject><subject>Collectins - metabolism</subject><subject>E coli</subject><subject>Escherichia coli - immunology</subject><subject>Evolution</subject><subject>Expression</subject><subject>Frogs</subject><subject>Immune system</subject><subject>Immunity, Innate - genetics</subject><subject>Immunity, Innate - immunology</subject><subject>Innate immunity</subject><subject>Juveniles</subject><subject>Larva - immunology</subject><subject>Mannose</subject><subject>Mannose-binding lectin</subject><subject>Mannose-Binding Lectin - blood</subject><subject>Mannose-Binding Lectin - genetics</subject><subject>Mannose-Binding Lectin - metabolism</subject><subject>Molecular structure</subject><subject>Phylogeny</subject><subject>Protein D</subject><subject>Pulmonary Surfactant-Associated Protein D - blood</subject><subject>Pulmonary Surfactant-Associated Protein D - genetics</subject><subject>Pulmonary Surfactant-Associated Protein D - metabolism</subject><subject>Rana catesbeiana</subject><subject>Rana catesbeiana - metabolism</subject><subject>Saccharide recognition</subject><subject>Terrestrial environments</subject><subject>Transcription</subject><issn>0145-305X</issn><issn>1879-0089</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp9kV1LHTEQhoO06NH2B3hTAr3Riz3mc3dTr0RsKwiCWOhdyGebQ3ZzmuxK9dc3h9UWeuHczGR45mUyLwDHGK0xwu3ZZm1NWBNEcH0zjPo9sMJ9JxqEevEGrBBmvKGIfz8Ah6VsUI0eo31wQKlAQgi-Avnq91aN1lloUozOTGGEXg0hPsJa6TlGn9MPeHKnRgWNmlzRLtT69BO8tm6cgg-1G9IIqwo0P1VWZnI5PC3N5OE2qjKof_LlHXjrVSzu_XM-At8-X91ffm1ubr9cX17cNIZSOjXaEEz63rZUt8xy0jLdedK1jGjVMWG19r5lovNaKKuVaevfrGWmF8Qhzgk9AieL7janX7MrkxxCMS5GNbo0F0k4Fj3iHeUV_fgfuklzHut2leKIM97yHYUXyuRUSnZebnMYVH6UGMmdIXIjqyFyZ4hcDKkzH56VZz04-3fixYEKnC-Aq6d4CC7LYoIbjbMh13tJm8Ir8n8AoCObyw</recordid><startdate>202109</startdate><enddate>202109</enddate><creator>Okada, Masako</creator><creator>Akimoto, Takanori</creator><creator>Ishihara, Akinori</creator><creator>Yamauchi, Kiyoshi</creator><general>Elsevier Ltd</general><general>Elsevier Science Ltd</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>7QL</scope><scope>7T5</scope><scope>C1K</scope><scope>H94</scope><scope>7X8</scope></search><sort><creationdate>202109</creationdate><title>Expanded collectin family in bullfrog (Rana catesbeiana): Identification and characterization of plasma collectins</title><author>Okada, Masako ; Akimoto, Takanori ; Ishihara, Akinori ; Yamauchi, Kiyoshi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c333t-bc21288d63b64d5264b7f27642ba749dbbff6497fb9adbac6081dd4c892e05523</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Affinity</topic><topic>Affinity chromatography</topic><topic>Agglutination</topic><topic>Agglutination - immunology</topic><topic>Animals</topic><topic>Aquatic environment</topic><topic>Bacterial Adhesion - immunology</topic><topic>Binding</topic><topic>Calcium</topic><topic>Calcium ions</topic><topic>Carbohydrate Metabolism - immunology</topic><topic>Carbohydrates</topic><topic>Carbohydrates - immunology</topic><topic>Collectin</topic><topic>Collectins</topic><topic>Collectins - blood</topic><topic>Collectins - genetics</topic><topic>Collectins - metabolism</topic><topic>E coli</topic><topic>Escherichia coli - immunology</topic><topic>Evolution</topic><topic>Expression</topic><topic>Frogs</topic><topic>Immune system</topic><topic>Immunity, Innate - genetics</topic><topic>Immunity, Innate - immunology</topic><topic>Innate immunity</topic><topic>Juveniles</topic><topic>Larva - immunology</topic><topic>Mannose</topic><topic>Mannose-binding lectin</topic><topic>Mannose-Binding Lectin - blood</topic><topic>Mannose-Binding Lectin - genetics</topic><topic>Mannose-Binding Lectin - metabolism</topic><topic>Molecular structure</topic><topic>Phylogeny</topic><topic>Protein D</topic><topic>Pulmonary Surfactant-Associated Protein D - blood</topic><topic>Pulmonary Surfactant-Associated Protein D - genetics</topic><topic>Pulmonary Surfactant-Associated Protein D - metabolism</topic><topic>Rana catesbeiana</topic><topic>Rana catesbeiana - metabolism</topic><topic>Saccharide recognition</topic><topic>Terrestrial environments</topic><topic>Transcription</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Okada, Masako</creatorcontrib><creatorcontrib>Akimoto, Takanori</creatorcontrib><creatorcontrib>Ishihara, Akinori</creatorcontrib><creatorcontrib>Yamauchi, Kiyoshi</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Immunology Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Developmental and comparative immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Okada, Masako</au><au>Akimoto, Takanori</au><au>Ishihara, Akinori</au><au>Yamauchi, Kiyoshi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Expanded collectin family in bullfrog (Rana catesbeiana): Identification and characterization of plasma collectins</atitle><jtitle>Developmental and comparative immunology</jtitle><addtitle>Dev Comp Immunol</addtitle><date>2021-09</date><risdate>2021</risdate><volume>122</volume><spage>104108</spage><epage>104108</epage><pages>104108-104108</pages><artnum>104108</artnum><issn>0145-305X</issn><eissn>1879-0089</eissn><abstract>BLAST searches against databases for the bullfrog (Rana catesbeiana), using the collectin sequence previously identified in tadpoles, revealed the presence of at least 20 members of the collectin gene family. Phylogenetic analysis demonstrated that the bullfrog possesses expanded gene subfamilies encoding mannose-binding lectin (MBL) and pulmonary surfactant-associated protein D (PSAPD). Two collectins, of 20 kDa (PSAPD1) and 25 kDa (PSAPD6), were purified as a mixture from adult bullfrog plasma using affinity chromatography. These collectins were present as an oligomer of ~400 kDa in their native state, and showed Ca2+-dependent carbohydrate binding with different sugar preferences. Affinity-purified collectins showed weak E. coli agglutination and bactericidal activities, compared with those of plasma. Although both PSAPD1 and PSAPD6 genes were predominantly expressed in the liver, PSAPD1 transcripts were abundant in adults whereas PSAPD6 transcripts were abundant in tadpoles. The findings indicate that two gene subfamilies in the collectin family have diverged structurally, functionally and transcriptionally in the bullfrog. Rapid expansion of the collectin family in bullfrogs may reflect the onset of sub-functionalization of the prototype MBL gene towards tetrapod MBL and PSAPDs, and may be one means of natural adaptation in the innate immune system to various pathogens in both aquatic and terrestrial environments.
•Bullfrog has expanded collectin gene family.•Two bullfrog collectins were isolated from the plasma and characterized.•The plasma collectins structurally, functionally and transcriptionally diverged.•Tetrapod MBL, PSAPA and PSAPD separated in the sarcopterygian lineage.</abstract><cop>United States</cop><pub>Elsevier Ltd</pub><pmid>33909995</pmid><doi>10.1016/j.dci.2021.104108</doi><tpages>1</tpages></addata></record> |
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subjects | Affinity Affinity chromatography Agglutination Agglutination - immunology Animals Aquatic environment Bacterial Adhesion - immunology Binding Calcium Calcium ions Carbohydrate Metabolism - immunology Carbohydrates Carbohydrates - immunology Collectin Collectins Collectins - blood Collectins - genetics Collectins - metabolism E coli Escherichia coli - immunology Evolution Expression Frogs Immune system Immunity, Innate - genetics Immunity, Innate - immunology Innate immunity Juveniles Larva - immunology Mannose Mannose-binding lectin Mannose-Binding Lectin - blood Mannose-Binding Lectin - genetics Mannose-Binding Lectin - metabolism Molecular structure Phylogeny Protein D Pulmonary Surfactant-Associated Protein D - blood Pulmonary Surfactant-Associated Protein D - genetics Pulmonary Surfactant-Associated Protein D - metabolism Rana catesbeiana Rana catesbeiana - metabolism Saccharide recognition Terrestrial environments Transcription |
title | Expanded collectin family in bullfrog (Rana catesbeiana): Identification and characterization of plasma collectins |
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