Characterization of the TLR family in branchiostoma lanceolatum and discovery of a novel TLR22-like involved in dsRNA recognition in amphioxus

Toll-like receptors (TLRs) are important for raising innate immune responses in both invertebrates and vertebrates. Amphioxus belongs to an ancient chordate lineage which shares key features with vertebrates. The genomic research on TLR genes in Branchiostoma floridae and Branchiostoma belcheri reve...

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Authors: Ji, Jie, Ramos Vicente, David, Navas Pérez, Enrique, Herrera Úbeda, Carlos, Lizcano, José Miguel, Garcia Fernández, Jordi, Escrivà, Hector, Bayés, Àlex, Roher Armentia, Nerea
Format: article
Status:Published version
Publication Date:2018
Country:España
Institution:Universidad de Barcelona
Repository:Dipòsit Digital de la UB
OAI Identifier:oai:diposit.ub.edu:2445/129476
Online Access:https://hdl.handle.net/2445/129476
Access Level:Open access
Keyword:Amfiox
Proteïnes
Branchiostoma lanceolatum
Proteins
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spelling Characterization of the TLR family in branchiostoma lanceolatum and discovery of a novel TLR22-like involved in dsRNA recognition in amphioxusJi, JieRamos Vicente, DavidNavas Pérez, EnriqueHerrera Úbeda, CarlosLizcano, José MiguelGarcia Fernández, JordiEscrivà, HectorBayés, ÀlexRoher Armentia, NereaAmfioxProteïnesBranchiostoma lanceolatumProteinsToll-like receptors (TLRs) are important for raising innate immune responses in both invertebrates and vertebrates. Amphioxus belongs to an ancient chordate lineage which shares key features with vertebrates. The genomic research on TLR genes in Branchiostoma floridae and Branchiostoma belcheri reveals the expansion of TLRs in amphioxus. However, the repertoire of TLRs in Branchiostoma lanceolatum has not been studied and the functionality of amphioxus TLRs has not been reported. We have identified from transcriptomic data 30 new putative TLRs in B. lanceolatum and all of them are transcribed in adult amphioxus. Phylogenetic analysis showed that the repertoire of TLRs consists of both non-vertebrate and vertebrate-like TLRs. It also indicated a lineage-specific expansion in orthologous clusters of the vertebrate TLR11 family. We did not detect any representatives of the vertebrate TLR1, TLR3, TLR4, TLR5 and TLR7 families. To gain insight into these TLRs, we studied in depth a particular TLR highly similar to a B. belcheri gene annotated as bbtTLR1. The phylogenetic analysis of this novel BlTLR showed that it clusters with the vertebrate TLR11 family and it might be more related to TLR13 subfamily according to similar domain architecture. Transient and stable expression in HEK293 cells showed that the BlTLR localizes on the plasma membrane, but it did not respond to the most common mammalian TLR ligands. However, when the ectodomain of BlTLR is fused to the TIR domain of human TLR2, the chimeric protein could indeed induce NF-κB transactivation in response to the viral ligand Poly I:C, also indicating that in amphioxus, specific accessory proteins are needed for downstream activation. Based on the phylogenetic, subcellular localization and functional analysis, we propose that the novel BlTLR might be classified as an antiviral receptor sharing at least partly the functions performed by vertebrate TLR22. TLR22 is thought to be viral teleost-specific TLR but here we demonstrate that teleosts and amphioxus TLR22-like probably shared a common ancestor. Additional functional studies with other lancelet TLR genes will enrich our understanding of the immune response in amphioxus and will provide a unique perspective on the evolution of the immune system.Frontiers Media2018info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfhttps://hdl.handle.net/2445/129476Articles publicats en revistes (Genètica, Microbiologia i Estadística)reponame:Dipòsit Digital de la UBinstname:Universidad de BarcelonaInglésReproducció del document publicat a: https://doi.org/10.3389/fimmu.2018.02525Frontiers in Immunology, 2018, vol. 9, p. 2525https://doi.org/10.3389/fimmu.2018.02525cc-by (c) Ji, J. et al., 2018http://creativecommons.org/licenses/by/3.0/esinfo:eu-repo/semantics/openAccessoai:diposit.ub.edu:2445/1294762026-05-27T06:46:51Z
dc.title.none.fl_str_mv Characterization of the TLR family in branchiostoma lanceolatum and discovery of a novel TLR22-like involved in dsRNA recognition in amphioxus
title Characterization of the TLR family in branchiostoma lanceolatum and discovery of a novel TLR22-like involved in dsRNA recognition in amphioxus
spellingShingle Characterization of the TLR family in branchiostoma lanceolatum and discovery of a novel TLR22-like involved in dsRNA recognition in amphioxus
Ji, Jie
Amfiox
Proteïnes
Branchiostoma lanceolatum
Proteins
title_short Characterization of the TLR family in branchiostoma lanceolatum and discovery of a novel TLR22-like involved in dsRNA recognition in amphioxus
title_full Characterization of the TLR family in branchiostoma lanceolatum and discovery of a novel TLR22-like involved in dsRNA recognition in amphioxus
title_fullStr Characterization of the TLR family in branchiostoma lanceolatum and discovery of a novel TLR22-like involved in dsRNA recognition in amphioxus
title_full_unstemmed Characterization of the TLR family in branchiostoma lanceolatum and discovery of a novel TLR22-like involved in dsRNA recognition in amphioxus
title_sort Characterization of the TLR family in branchiostoma lanceolatum and discovery of a novel TLR22-like involved in dsRNA recognition in amphioxus
dc.creator.none.fl_str_mv Ji, Jie
Ramos Vicente, David
Navas Pérez, Enrique
Herrera Úbeda, Carlos
Lizcano, José Miguel
Garcia Fernández, Jordi
Escrivà, Hector
Bayés, Àlex
Roher Armentia, Nerea
author Ji, Jie
author_facet Ji, Jie
Ramos Vicente, David
Navas Pérez, Enrique
Herrera Úbeda, Carlos
Lizcano, José Miguel
Garcia Fernández, Jordi
Escrivà, Hector
Bayés, Àlex
Roher Armentia, Nerea
author_role author
author2 Ramos Vicente, David
Navas Pérez, Enrique
Herrera Úbeda, Carlos
Lizcano, José Miguel
Garcia Fernández, Jordi
Escrivà, Hector
Bayés, Àlex
Roher Armentia, Nerea
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Amfiox
Proteïnes
Branchiostoma lanceolatum
Proteins
topic Amfiox
Proteïnes
Branchiostoma lanceolatum
Proteins
description Toll-like receptors (TLRs) are important for raising innate immune responses in both invertebrates and vertebrates. Amphioxus belongs to an ancient chordate lineage which shares key features with vertebrates. The genomic research on TLR genes in Branchiostoma floridae and Branchiostoma belcheri reveals the expansion of TLRs in amphioxus. However, the repertoire of TLRs in Branchiostoma lanceolatum has not been studied and the functionality of amphioxus TLRs has not been reported. We have identified from transcriptomic data 30 new putative TLRs in B. lanceolatum and all of them are transcribed in adult amphioxus. Phylogenetic analysis showed that the repertoire of TLRs consists of both non-vertebrate and vertebrate-like TLRs. It also indicated a lineage-specific expansion in orthologous clusters of the vertebrate TLR11 family. We did not detect any representatives of the vertebrate TLR1, TLR3, TLR4, TLR5 and TLR7 families. To gain insight into these TLRs, we studied in depth a particular TLR highly similar to a B. belcheri gene annotated as bbtTLR1. The phylogenetic analysis of this novel BlTLR showed that it clusters with the vertebrate TLR11 family and it might be more related to TLR13 subfamily according to similar domain architecture. Transient and stable expression in HEK293 cells showed that the BlTLR localizes on the plasma membrane, but it did not respond to the most common mammalian TLR ligands. However, when the ectodomain of BlTLR is fused to the TIR domain of human TLR2, the chimeric protein could indeed induce NF-κB transactivation in response to the viral ligand Poly I:C, also indicating that in amphioxus, specific accessory proteins are needed for downstream activation. Based on the phylogenetic, subcellular localization and functional analysis, we propose that the novel BlTLR might be classified as an antiviral receptor sharing at least partly the functions performed by vertebrate TLR22. TLR22 is thought to be viral teleost-specific TLR but here we demonstrate that teleosts and amphioxus TLR22-like probably shared a common ancestor. Additional functional studies with other lancelet TLR genes will enrich our understanding of the immune response in amphioxus and will provide a unique perspective on the evolution of the immune system.
publishDate 2018
dc.date.none.fl_str_mv 2018
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/2445/129476
url https://hdl.handle.net/2445/129476
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Reproducció del document publicat a: https://doi.org/10.3389/fimmu.2018.02525
Frontiers in Immunology, 2018, vol. 9, p. 2525
https://doi.org/10.3389/fimmu.2018.02525
dc.rights.none.fl_str_mv cc-by (c) Ji, J. et al., 2018
http://creativecommons.org/licenses/by/3.0/es
info:eu-repo/semantics/openAccess
rights_invalid_str_mv cc-by (c) Ji, J. et al., 2018
http://creativecommons.org/licenses/by/3.0/es
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv Articles publicats en revistes (Genètica, Microbiologia i Estadística)
reponame:Dipòsit Digital de la UB
instname:Universidad de Barcelona
instname_str Universidad de Barcelona
reponame_str Dipòsit Digital de la UB
collection Dipòsit Digital de la UB
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15.300719

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