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Convergent Evolution of Mucosal Immune Responses at the Buccal Cavity of Teleost Fish
The buccal mucosa (BM) is a critical first line of defense in terrestrial animals. To gain further insights into the evolutionary origins and primordial roles of BM in teleosts here we show that rainbow trout, a teleost fish, contains a diffuse mucosal associated lymphoid tissue (MALT) within its bu...
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Published in: | iScience 2019-09, Vol.19, p.821-835 |
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creator | Yu, Yong-Yao Kong, Wei-Guang Xu, Hao-Yue Huang, Zhen-Yu Zhang, Xiao-Ting Ding, Li-Guo Dong, Shuai Yin, Guang-Mei Dong, Fen Yu, Wei Cao, Jia-Feng Meng, Kai-Feng Liu, Xia Fu, Yu Zhang, Xue-zhen Zhang, Yong-an Sunyer, J. Oriol Xu, Zhen |
description | The buccal mucosa (BM) is a critical first line of defense in terrestrial animals. To gain further insights into the evolutionary origins and primordial roles of BM in teleosts here we show that rainbow trout, a teleost fish, contains a diffuse mucosal associated lymphoid tissue (MALT) within its buccal cavity. Upon parasite infection, a fish immunoglobulin specialized in mucosal immunity (sIgT) was induced to a high degree, and parasite-specific sIgT responses were mainly detected in the buccal mucus. Moreover, we show that the trout buccal microbiota is prevalently coated with sIgT. Overall our findings revealed that the MALT is present in the BM of a non-tetrapod species. As fish IgT and mucus-producing cells are evolutionarily unrelated to mammalian IgA and salivary glands, respectively, our findings indicate that mucosal immune responses in the BM of teleost fish and tetrapods evolved through a process of convergent evolution.
[Display omitted]
•A mucosal associated lymphoid tissue is identified in teleost buccal cavity•Local immune responses can be induced in teleost buccal mucosa•Teleost IgT plays important roles in defending against buccal pathogen•Microbiota in teleost buccal mucosa is prevalently coated with secreted IgT
Biological Sciences; Immunology; Omics; Transcriptomics |
doi_str_mv | 10.1016/j.isci.2019.08.034 |
format | article |
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[Display omitted]
•A mucosal associated lymphoid tissue is identified in teleost buccal cavity•Local immune responses can be induced in teleost buccal mucosa•Teleost IgT plays important roles in defending against buccal pathogen•Microbiota in teleost buccal mucosa is prevalently coated with secreted IgT
Biological Sciences; Immunology; Omics; Transcriptomics</description><identifier>ISSN: 2589-0042</identifier><identifier>EISSN: 2589-0042</identifier><identifier>DOI: 10.1016/j.isci.2019.08.034</identifier><identifier>PMID: 31499339</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Biological Sciences ; Immunology ; Omics ; Transcriptomics</subject><ispartof>iScience, 2019-09, Vol.19, p.821-835</ispartof><rights>2019 The Author(s)</rights><rights>Copyright © 2019 The Author(s). Published by Elsevier Inc. All rights reserved.</rights><rights>2019 The Author(s) 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c587t-40be0c1a5f9a36b6092d490e821502d34ebcad891154a1b85b02137cb9c264373</citedby><cites>FETCH-LOGICAL-c587t-40be0c1a5f9a36b6092d490e821502d34ebcad891154a1b85b02137cb9c264373</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6734174/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S2589004219303128$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,3549,27924,27925,45780,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31499339$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yu, Yong-Yao</creatorcontrib><creatorcontrib>Kong, Wei-Guang</creatorcontrib><creatorcontrib>Xu, Hao-Yue</creatorcontrib><creatorcontrib>Huang, Zhen-Yu</creatorcontrib><creatorcontrib>Zhang, Xiao-Ting</creatorcontrib><creatorcontrib>Ding, Li-Guo</creatorcontrib><creatorcontrib>Dong, Shuai</creatorcontrib><creatorcontrib>Yin, Guang-Mei</creatorcontrib><creatorcontrib>Dong, Fen</creatorcontrib><creatorcontrib>Yu, Wei</creatorcontrib><creatorcontrib>Cao, Jia-Feng</creatorcontrib><creatorcontrib>Meng, Kai-Feng</creatorcontrib><creatorcontrib>Liu, Xia</creatorcontrib><creatorcontrib>Fu, Yu</creatorcontrib><creatorcontrib>Zhang, Xue-zhen</creatorcontrib><creatorcontrib>Zhang, Yong-an</creatorcontrib><creatorcontrib>Sunyer, J. Oriol</creatorcontrib><creatorcontrib>Xu, Zhen</creatorcontrib><title>Convergent Evolution of Mucosal Immune Responses at the Buccal Cavity of Teleost Fish</title><title>iScience</title><addtitle>iScience</addtitle><description>The buccal mucosa (BM) is a critical first line of defense in terrestrial animals. To gain further insights into the evolutionary origins and primordial roles of BM in teleosts here we show that rainbow trout, a teleost fish, contains a diffuse mucosal associated lymphoid tissue (MALT) within its buccal cavity. Upon parasite infection, a fish immunoglobulin specialized in mucosal immunity (sIgT) was induced to a high degree, and parasite-specific sIgT responses were mainly detected in the buccal mucus. Moreover, we show that the trout buccal microbiota is prevalently coated with sIgT. Overall our findings revealed that the MALT is present in the BM of a non-tetrapod species. As fish IgT and mucus-producing cells are evolutionarily unrelated to mammalian IgA and salivary glands, respectively, our findings indicate that mucosal immune responses in the BM of teleost fish and tetrapods evolved through a process of convergent evolution.
[Display omitted]
•A mucosal associated lymphoid tissue is identified in teleost buccal cavity•Local immune responses can be induced in teleost buccal mucosa•Teleost IgT plays important roles in defending against buccal pathogen•Microbiota in teleost buccal mucosa is prevalently coated with secreted IgT
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Oriol</au><au>Xu, Zhen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Convergent Evolution of Mucosal Immune Responses at the Buccal Cavity of Teleost Fish</atitle><jtitle>iScience</jtitle><addtitle>iScience</addtitle><date>2019-09-27</date><risdate>2019</risdate><volume>19</volume><spage>821</spage><epage>835</epage><pages>821-835</pages><issn>2589-0042</issn><eissn>2589-0042</eissn><abstract>The buccal mucosa (BM) is a critical first line of defense in terrestrial animals. To gain further insights into the evolutionary origins and primordial roles of BM in teleosts here we show that rainbow trout, a teleost fish, contains a diffuse mucosal associated lymphoid tissue (MALT) within its buccal cavity. Upon parasite infection, a fish immunoglobulin specialized in mucosal immunity (sIgT) was induced to a high degree, and parasite-specific sIgT responses were mainly detected in the buccal mucus. Moreover, we show that the trout buccal microbiota is prevalently coated with sIgT. Overall our findings revealed that the MALT is present in the BM of a non-tetrapod species. As fish IgT and mucus-producing cells are evolutionarily unrelated to mammalian IgA and salivary glands, respectively, our findings indicate that mucosal immune responses in the BM of teleost fish and tetrapods evolved through a process of convergent evolution.
[Display omitted]
•A mucosal associated lymphoid tissue is identified in teleost buccal cavity•Local immune responses can be induced in teleost buccal mucosa•Teleost IgT plays important roles in defending against buccal pathogen•Microbiota in teleost buccal mucosa is prevalently coated with secreted IgT
Biological Sciences; Immunology; Omics; Transcriptomics</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>31499339</pmid><doi>10.1016/j.isci.2019.08.034</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Biological Sciences Immunology Omics Transcriptomics |
title | Convergent Evolution of Mucosal Immune Responses at the Buccal Cavity of Teleost Fish |
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