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Characteristic and functional analysis of toll-like receptors (TLRs) in the lophotrocozoan, Crassostrea gigas, reveals ancient origin of TLR-mediated innate immunity.

The evolution of TLR-mediated innate immunity is a fundamental question in immunology. Here, we report the characterization and functional analysis of four TLR members in the lophotrochozoans Crassostrea gigas (CgTLRs). All CgTLRs bear a conserved domain organization and have a close relationship wi... Full description

Journal Title: PloS one 2013, Vol.8(10), p.e76464
Main Author: Zhang, Yang
Other Authors: He, Xiaocui , Yu, Feng , Xiang, Zhiming , Li, Jun , Thorpe, Karen L , Yu, Ziniu
Format: Electronic Article Electronic Article
Language: English
Subjects:
ID: E-ISSN: 1932-6203 ; DOI: 10.1371/journal.pone.0076464
Link: http://search.proquest.com/docview/1443414563/?pq-origsite=primo
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title: Characteristic and functional analysis of toll-like receptors (TLRs) in the lophotrocozoan, Crassostrea gigas, reveals ancient origin of TLR-mediated innate immunity.
format: Article
creator:
  • Zhang, Yang
  • He, Xiaocui
  • Yu, Feng
  • Xiang, Zhiming
  • Li, Jun
  • Thorpe, Karen L
  • Yu, Ziniu
subjects:
  • Amino Acid Sequence–Immunology
  • Animals–Classification
  • Cell Degranulation–Genetics
  • Cell Line–Immunology
  • Crassostrea–Metabolism
  • Cytokines–Genetics
  • Evolution, Molecular–Metabolism
  • Gene Expression–Immunology
  • Gene Expression Profiling–Metabolism
  • Genes, Reporter–Chemistry
  • Hemocytes–Metabolism
  • Humans–Genetics
  • Immunity, Innate–Metabolism
  • Ligands–Chemistry
  • Models, Molecular–Metabolism
  • Molecular Sequence Data–Pharmacology
  • Multigene Family–Antagonists & Inhibitors
  • Myeloid Differentiation Factor 88–Chemistry
  • Nf-Kappa B–Genetics
  • Peptides–Metabolism
  • Phylogeny–Metabolism
  • Protein Binding–Metabolism
  • Protein Conformation–Metabolism
  • Protein Transport–Metabolism
  • Signal Transduction–Metabolism
  • Toll-Like Receptors–Metabolism
  • Cytokines
  • Ligands
  • Myeloid Differentiation Factor 88
  • Nf-Kappa B
  • Peptides
  • Toll-Like Receptors
ispartof: PloS one, 2013, Vol.8(10), p.e76464
description: The evolution of TLR-mediated innate immunity is a fundamental question in immunology. Here, we report the characterization and functional analysis of four TLR members in the lophotrochozoans Crassostrea gigas (CgTLRs). All CgTLRs bear a conserved domain organization and have a close relationship with TLRs in ancient non-vertebrate chordates. In HEK293 cells, every CgTLR could constitutively activate NF-[kappa]B responsive reporter, but none of the PAMPs tested could stimulate CgTLR-activated NF-[kappa]B induction. Subcellular localization showed that CgTLR members have similar and dual distribution on late endosomes and plasma membranes. Moreover, CgTLRs and CgMyD88 mRNA show a consistent response to multiple PAMP challenges in oyster hemocytes. As CgTLR-mediated NF-[kappa]B activation is dependent on CgMyD88, we designed a blocking peptide for CgTLR signaling that would inhibit CgTLR-CgMyD88 dependent NF-[kappa]B activation. This was used to demonstrate that a Vibrio parahaemolyticus infection-induced enhancement of degranulation and increase of cytokines TNF mRNA in hemocytes, could be inhibited by blocking CgTLR signaling. In summary, our study characterized the primitive TLRs in the lophotrocozoan C. gigas and demonstrated a fundamental role of TLR signaling in infection-induced hemocyte activation. This provides further evidence for an ancient origin of TLR-mediated innate immunity.
language: eng
source:
identifier: E-ISSN: 1932-6203 ; DOI: 10.1371/journal.pone.0076464
fulltext: fulltext
issn:
  • 19326203
  • 1932-6203
url: Link


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titleCharacteristic and functional analysis of toll-like receptors (TLRs) in the lophotrocozoan, Crassostrea gigas, reveals ancient origin of TLR-mediated innate immunity.
creatorZhang, Yang ; He, Xiaocui ; Yu, Feng ; Xiang, Zhiming ; Li, Jun ; Thorpe, Karen L ; Yu, Ziniu
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identifierE-ISSN: 1932-6203 ; DOI: 10.1371/journal.pone.0076464
subjectAmino Acid Sequence–Immunology ; Animals–Classification ; Cell Degranulation–Genetics ; Cell Line–Immunology ; Crassostrea–Metabolism ; Cytokines–Genetics ; Evolution, Molecular–Metabolism ; Gene Expression–Immunology ; Gene Expression Profiling–Metabolism ; Genes, Reporter–Chemistry ; Hemocytes–Metabolism ; Humans–Genetics ; Immunity, Innate–Metabolism ; Ligands–Chemistry ; Models, Molecular–Metabolism ; Molecular Sequence Data–Pharmacology ; Multigene Family–Antagonists & Inhibitors ; Myeloid Differentiation Factor 88–Chemistry ; Nf-Kappa B–Genetics ; Peptides–Metabolism ; Phylogeny–Metabolism ; Protein Binding–Metabolism ; Protein Conformation–Metabolism ; Protein Transport–Metabolism ; Signal Transduction–Metabolism ; Toll-Like Receptors–Metabolism ; Cytokines ; Ligands ; Myeloid Differentiation Factor 88 ; Nf-Kappa B ; Peptides ; Toll-Like Receptors
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descriptionThe evolution of TLR-mediated innate immunity is a fundamental question in immunology. Here, we report the characterization and functional analysis of four TLR members in the lophotrochozoans Crassostrea gigas (CgTLRs). All CgTLRs bear a conserved domain organization and have a close relationship with TLRs in ancient non-vertebrate chordates. In HEK293 cells, every CgTLR could constitutively activate NF-[kappa]B responsive reporter, but none of the PAMPs tested could stimulate CgTLR-activated NF-[kappa]B induction. Subcellular localization showed that CgTLR members have similar and dual distribution on late endosomes and plasma membranes. Moreover, CgTLRs and CgMyD88 mRNA show a consistent response to multiple PAMP challenges in oyster hemocytes. As CgTLR-mediated NF-[kappa]B activation is dependent on CgMyD88, we designed a blocking peptide for CgTLR signaling that would inhibit CgTLR-CgMyD88 dependent NF-[kappa]B activation. This was used to demonstrate that a Vibrio parahaemolyticus infection-induced enhancement of degranulation and increase of cytokines TNF mRNA in hemocytes, could be inhibited by blocking CgTLR signaling. In summary, our study characterized the primitive TLRs in the lophotrocozoan C. gigas and demonstrated a fundamental role of TLR signaling in infection-induced hemocyte activation. This provides further evidence for an ancient origin of TLR-mediated innate immunity.
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titleCharacteristic and functional analysis of toll-like receptors (TLRs) in the lophotrocozoan, Crassostrea gigas, reveals ancient origin of TLR-mediated innate immunity.
authorZhang, Yang ; He, Xiaocui ; Yu, Feng ; Xiang, Zhiming ; Li, Jun ; Thorpe, Karen L ; Yu, Ziniu
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