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Topographical mapping of α- and β-keratins on developing chicken skin integuments: Functional interaction and evolutionary perspectives
Avian integumentary organs include feathers, scales, claws, and beaks. They cover the body surface and play various functions to help adapt birds to diverse environments. These keratinized structures are mainly composed of corneous materials made of α-keratins, which exist in all vertebrates, and β-...
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Published in: | Proceedings of the National Academy of Sciences - PNAS 2015-12, Vol.112 (49), p.E6770-E6779 |
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container_title | Proceedings of the National Academy of Sciences - PNAS |
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creator | Wu, Ping Ng, Chen Siang Yan, Jie Lai, Yung-Chih Chen, Chih-Kuan Lai, Yu-Ting Wu, Siao-Man Chen, Jiun-Jie Luo, Weiqi Widelitz, Randall B. Li, Wen-Hsiung Chuong, Cheng-Ming |
description | Avian integumentary organs include feathers, scales, claws, and beaks. They cover the body surface and play various functions to help adapt birds to diverse environments. These keratinized structures are mainly composed of corneous materials made of α-keratins, which exist in all vertebrates, and β-keratins,which only exist in birds and reptiles. Here, members of the keratin gene families were used to study how gene family evolution contributes to novelty and adaptation, focusing on tissue morphogenesis. Using chicken as a model, we applied RNA-seq and in situ hybridization to map α- and β-keratin genes in various skin appendages at embryonic developmental stages. The data demonstrate that temporal and spatial α- and β-keratin expression is involved in establishing the diversity of skin appendage phenotypes. Embryonic feathers express a higher proportion of β-keratin genes than other skin regions. In feather filament morphogenesis, β-keratins show intricate complexity in diverse substructures of feather branches. To explore functional interactions, we used a retrovirus transgenic system to ectopically express mutant α- or antisense β-keratin forms. α- and β-keratins show mutual dependence and mutations in either keratin type results in disrupted keratin networks and failure to form proper feather branches. Our data suggest that combinations of α- and β-keratin genes contribute to the morphological and structural diversity of different avian skin appendages, with feather-β-keratins conferring more possible composites in building intrafeather architecture complexity, setting up a platform of morphological evolution of functional forms in feathers. |
doi_str_mv | 10.1073/pnas.1520566112 |
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They cover the body surface and play various functions to help adapt birds to diverse environments. These keratinized structures are mainly composed of corneous materials made of α-keratins, which exist in all vertebrates, and β-keratins,which only exist in birds and reptiles. Here, members of the keratin gene families were used to study how gene family evolution contributes to novelty and adaptation, focusing on tissue morphogenesis. Using chicken as a model, we applied RNA-seq and in situ hybridization to map α- and β-keratin genes in various skin appendages at embryonic developmental stages. The data demonstrate that temporal and spatial α- and β-keratin expression is involved in establishing the diversity of skin appendage phenotypes. Embryonic feathers express a higher proportion of β-keratin genes than other skin regions. In feather filament morphogenesis, β-keratins show intricate complexity in diverse substructures of feather branches. To explore functional interactions, we used a retrovirus transgenic system to ectopically express mutant α- or antisense β-keratin forms. α- and β-keratins show mutual dependence and mutations in either keratin type results in disrupted keratin networks and failure to form proper feather branches. Our data suggest that combinations of α- and β-keratin genes contribute to the morphological and structural diversity of different avian skin appendages, with feather-β-keratins conferring more possible composites in building intrafeather architecture complexity, setting up a platform of morphological evolution of functional forms in feathers.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1520566112</identifier><identifier>PMID: 26598683</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animals ; beta-Keratins - genetics ; Biological Evolution ; Biological Sciences ; Chick Embryo ; Chromosome Mapping ; In Situ Hybridization ; Keratin-13 - genetics ; Keratins - genetics ; PNAS Plus ; RNA, Antisense - pharmacology ; Skin - embryology ; Skin - metabolism</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2015-12, Vol.112 (49), p.E6770-E6779</ispartof><rights>Volumes 1–89 and 106–112, copyright as a collective work only; author(s) retains copyright to individual articles</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c440t-886ecefcbbb5a6c6c202a48426669aab3a4f31966ccf2b7e6617ea028331b0843</citedby><cites>FETCH-LOGICAL-c440t-886ecefcbbb5a6c6c202a48426669aab3a4f31966ccf2b7e6617ea028331b0843</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/112/49.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26466567$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26466567$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793,58238,58471</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26598683$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wu, Ping</creatorcontrib><creatorcontrib>Ng, Chen Siang</creatorcontrib><creatorcontrib>Yan, Jie</creatorcontrib><creatorcontrib>Lai, Yung-Chih</creatorcontrib><creatorcontrib>Chen, Chih-Kuan</creatorcontrib><creatorcontrib>Lai, Yu-Ting</creatorcontrib><creatorcontrib>Wu, Siao-Man</creatorcontrib><creatorcontrib>Chen, Jiun-Jie</creatorcontrib><creatorcontrib>Luo, Weiqi</creatorcontrib><creatorcontrib>Widelitz, Randall B.</creatorcontrib><creatorcontrib>Li, Wen-Hsiung</creatorcontrib><creatorcontrib>Chuong, Cheng-Ming</creatorcontrib><title>Topographical mapping of α- and β-keratins on developing chicken skin integuments: Functional interaction and evolutionary perspectives</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Avian integumentary organs include feathers, scales, claws, and beaks. They cover the body surface and play various functions to help adapt birds to diverse environments. These keratinized structures are mainly composed of corneous materials made of α-keratins, which exist in all vertebrates, and β-keratins,which only exist in birds and reptiles. Here, members of the keratin gene families were used to study how gene family evolution contributes to novelty and adaptation, focusing on tissue morphogenesis. Using chicken as a model, we applied RNA-seq and in situ hybridization to map α- and β-keratin genes in various skin appendages at embryonic developmental stages. The data demonstrate that temporal and spatial α- and β-keratin expression is involved in establishing the diversity of skin appendage phenotypes. Embryonic feathers express a higher proportion of β-keratin genes than other skin regions. In feather filament morphogenesis, β-keratins show intricate complexity in diverse substructures of feather branches. To explore functional interactions, we used a retrovirus transgenic system to ectopically express mutant α- or antisense β-keratin forms. α- and β-keratins show mutual dependence and mutations in either keratin type results in disrupted keratin networks and failure to form proper feather branches. Our data suggest that combinations of α- and β-keratin genes contribute to the morphological and structural diversity of different avian skin appendages, with feather-β-keratins conferring more possible composites in building intrafeather architecture complexity, setting up a platform of morphological evolution of functional forms in feathers.</description><subject>Animals</subject><subject>beta-Keratins - genetics</subject><subject>Biological Evolution</subject><subject>Biological Sciences</subject><subject>Chick Embryo</subject><subject>Chromosome Mapping</subject><subject>In Situ Hybridization</subject><subject>Keratin-13 - genetics</subject><subject>Keratins - genetics</subject><subject>PNAS Plus</subject><subject>RNA, Antisense - pharmacology</subject><subject>Skin - embryology</subject><subject>Skin - metabolism</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><recordid>eNpVkc1u1DAURi0EokNhzQrkJZu01z-5TjZIqCoFqRKLlrXleJypO4kd7EylPhY8SJ-pHmYY2pUXPt-51_4Iec_ghIESp1Mw-YTVHGpExvgLsmDQsgplCy_JAoCrqpFcHpE3Od8CQFs38JoccazbBhuxIFfXcYqrZKYbb81ARzNNPqxo7OnD74qasKQPf6q1S2b2IdMY6NLduSH-hWzJrF2gee0D9WF2q83owpzfkle9GbJ7tz-Pyc-v59dn36rLHxffz75cVlZKmKumQWddb7uuqw1atBy4kWVdRGyN6YSRvWAtorU975QrL1TOAG-EYB00UhyTzzvvtOlGt7RldjKDnpIfTbrX0Xj9_Cb4G72Kd1qiakE0RfBpL0jx18blWY8-WzcMJri4yZopqQQTILCgpzvUpphzcv1hDAO9rUJvq9D_qyiJj0-3O_D__r4AdA9skwcd41q2-hyVgoJ82CG3eY7piUIi1qjEI8innEI</recordid><startdate>20151208</startdate><enddate>20151208</enddate><creator>Wu, Ping</creator><creator>Ng, Chen Siang</creator><creator>Yan, Jie</creator><creator>Lai, Yung-Chih</creator><creator>Chen, Chih-Kuan</creator><creator>Lai, Yu-Ting</creator><creator>Wu, Siao-Man</creator><creator>Chen, Jiun-Jie</creator><creator>Luo, Weiqi</creator><creator>Widelitz, Randall B.</creator><creator>Li, Wen-Hsiung</creator><creator>Chuong, Cheng-Ming</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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20151208</creationdate><title>Topographical mapping of α- and β-keratins on developing chicken skin integuments</title><author>Wu, Ping ; Ng, Chen Siang ; Yan, Jie ; Lai, Yung-Chih ; Chen, Chih-Kuan ; Lai, Yu-Ting ; Wu, Siao-Man ; Chen, Jiun-Jie ; Luo, Weiqi ; Widelitz, Randall B. ; Li, Wen-Hsiung ; Chuong, Cheng-Ming</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c440t-886ecefcbbb5a6c6c202a48426669aab3a4f31966ccf2b7e6617ea028331b0843</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>beta-Keratins - genetics</topic><topic>Biological Evolution</topic><topic>Biological Sciences</topic><topic>Chick Embryo</topic><topic>Chromosome Mapping</topic><topic>In Situ Hybridization</topic><topic>Keratin-13 - genetics</topic><topic>Keratins - genetics</topic><topic>PNAS Plus</topic><topic>RNA, Antisense - pharmacology</topic><topic>Skin - embryology</topic><topic>Skin - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wu, Ping</creatorcontrib><creatorcontrib>Ng, Chen Siang</creatorcontrib><creatorcontrib>Yan, Jie</creatorcontrib><creatorcontrib>Lai, Yung-Chih</creatorcontrib><creatorcontrib>Chen, Chih-Kuan</creatorcontrib><creatorcontrib>Lai, Yu-Ting</creatorcontrib><creatorcontrib>Wu, Siao-Man</creatorcontrib><creatorcontrib>Chen, Jiun-Jie</creatorcontrib><creatorcontrib>Luo, Weiqi</creatorcontrib><creatorcontrib>Widelitz, Randall B.</creatorcontrib><creatorcontrib>Li, Wen-Hsiung</creatorcontrib><creatorcontrib>Chuong, Cheng-Ming</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><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wu, Ping</au><au>Ng, Chen Siang</au><au>Yan, Jie</au><au>Lai, Yung-Chih</au><au>Chen, Chih-Kuan</au><au>Lai, Yu-Ting</au><au>Wu, Siao-Man</au><au>Chen, Jiun-Jie</au><au>Luo, Weiqi</au><au>Widelitz, Randall B.</au><au>Li, Wen-Hsiung</au><au>Chuong, Cheng-Ming</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Topographical mapping of α- and β-keratins on developing chicken skin integuments: Functional interaction and evolutionary perspectives</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2015-12-08</date><risdate>2015</risdate><volume>112</volume><issue>49</issue><spage>E6770</spage><epage>E6779</epage><pages>E6770-E6779</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Avian integumentary organs include feathers, scales, claws, and beaks. They cover the body surface and play various functions to help adapt birds to diverse environments. These keratinized structures are mainly composed of corneous materials made of α-keratins, which exist in all vertebrates, and β-keratins,which only exist in birds and reptiles. Here, members of the keratin gene families were used to study how gene family evolution contributes to novelty and adaptation, focusing on tissue morphogenesis. Using chicken as a model, we applied RNA-seq and in situ hybridization to map α- and β-keratin genes in various skin appendages at embryonic developmental stages. The data demonstrate that temporal and spatial α- and β-keratin expression is involved in establishing the diversity of skin appendage phenotypes. Embryonic feathers express a higher proportion of β-keratin genes than other skin regions. In feather filament morphogenesis, β-keratins show intricate complexity in diverse substructures of feather branches. To explore functional interactions, we used a retrovirus transgenic system to ectopically express mutant α- or antisense β-keratin forms. α- and β-keratins show mutual dependence and mutations in either keratin type results in disrupted keratin networks and failure to form proper feather branches. Our data suggest that combinations of α- and β-keratin genes contribute to the morphological and structural diversity of different avian skin appendages, with feather-β-keratins conferring more possible composites in building intrafeather architecture complexity, setting up a platform of morphological evolution of functional forms in feathers.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>26598683</pmid><doi>10.1073/pnas.1520566112</doi><oa>free_for_read</oa></addata></record> |
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subjects | Animals beta-Keratins - genetics Biological Evolution Biological Sciences Chick Embryo Chromosome Mapping In Situ Hybridization Keratin-13 - genetics Keratins - genetics PNAS Plus RNA, Antisense - pharmacology Skin - embryology Skin - metabolism |
title | Topographical mapping of α- and β-keratins on developing chicken skin integuments: Functional interaction and evolutionary perspectives |
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