Molecular characterization and expression analysis of the putative interleukin 6 receptor (IL-6Rα and glycoprotein-130) in rainbow trout (Oncorhynchus mykiss)

salmonid IL-6Rα possesses a polymorphic N-terminal Ig domain with variable numbers of two repeats

Maria M Costa, Tiehui Wang, Milena M Monte, Christopher J Secombes

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

Interleukin (IL)-6, the founding member of IL-6 family cytokines, plays non-redundant roles in hematopoiesis and acute phase responses. IL-6 signals via a specific private IL-6Rα and a common beta chain gp130. In this study, we have cloned both the IL-6Rα and gp130 in rainbow trout. The trout gp130 cDNA encodes 906 aa and is similar in size, extracellular domain structure (D1-D6) and presence of intracellular motifs important for signal transduction to tetrapod gp130s. The trout IL-6Rα cDNA encodes for 834 aa and is larger compared to tetrapod IL-6Rαs, as are other fish IL-6Rα molecules due to a large D1 domain. However, the cytokine-binding domain is well conserved across vertebrates, with four conserved cysteine residues in the N-terminal FNIII domain and a WSXWS motif in the C-terminal FNIII domain. Furthermore, a phylogenetic tree analysis confirmed that the reported fish IL-6Rα and gp130 molecules are orthologues to their tetrapod counterparts. The extra large D1 domain of the salmonid IL-6Rα molecules results partially from the insertions of two repetitive sequences of [TS]-[TF]-VSTTT-[ND]-TTSNG and TTVS-[AT]-IKD-[DG]-S-[KD]-N-[GR], respectively. Furthermore the numbers of repetitions of the two motifs were variable in different individuals and cell lines, and even in the same fish allelic polymorphism exists. Trout IL-6Rα was expressed at higher levels than gp130 in a number of tissues examined and the expression of both IL-6Rα and gp130 could be modulated by LPS and Poly I:C in the cell lines studied. The expression patterns of the receptors suggest that high level expression of IL-6Rα is critical for IL-6 responsiveness.
Original languageEnglish
Pages (from-to)229-244
Number of pages16
JournalImmunogenetics
Volume64
Issue number3
Early online date29 Oct 2011
DOIs
Publication statusPublished - Mar 2012

Fingerprint

Interleukin-6 Receptors
Oncorhynchus mykiss
Interleukins
Glycoproteins
Trout
Interleukin-6
Fishes
Complementary DNA
Immunoglobulin Domains
Cytokines
Poly I-C
Cell Line
Acute-Phase Reaction
Nucleic Acid Repetitive Sequences
Hematopoiesis
Cysteine
Vertebrates
Signal Transduction

Keywords

  • amino acid sequence
  • animals
  • cell line
  • cytokine receptor gp130
  • gene expression regulation
  • interleukin-6 Receptor alpha subunit
  • molecular sequence data
  • Oncorhynchus mykiss
  • organ specificity
  • phylogeny
  • polymorphism, genetic
  • protein structure, tertiary
  • repetitive sequences, amino acid
  • sequence alignment
  • sequence analysis, DNA

Cite this

@article{35d171393b254fafad129e39ad90af54,
title = "Molecular characterization and expression analysis of the putative interleukin 6 receptor (IL-6Rα and glycoprotein-130) in rainbow trout (Oncorhynchus mykiss): salmonid IL-6Rα possesses a polymorphic N-terminal Ig domain with variable numbers of two repeats",
abstract = "Interleukin (IL)-6, the founding member of IL-6 family cytokines, plays non-redundant roles in hematopoiesis and acute phase responses. IL-6 signals via a specific private IL-6Rα and a common beta chain gp130. In this study, we have cloned both the IL-6Rα and gp130 in rainbow trout. The trout gp130 cDNA encodes 906 aa and is similar in size, extracellular domain structure (D1-D6) and presence of intracellular motifs important for signal transduction to tetrapod gp130s. The trout IL-6Rα cDNA encodes for 834 aa and is larger compared to tetrapod IL-6Rαs, as are other fish IL-6Rα molecules due to a large D1 domain. However, the cytokine-binding domain is well conserved across vertebrates, with four conserved cysteine residues in the N-terminal FNIII domain and a WSXWS motif in the C-terminal FNIII domain. Furthermore, a phylogenetic tree analysis confirmed that the reported fish IL-6Rα and gp130 molecules are orthologues to their tetrapod counterparts. The extra large D1 domain of the salmonid IL-6Rα molecules results partially from the insertions of two repetitive sequences of [TS]-[TF]-VSTTT-[ND]-TTSNG and TTVS-[AT]-IKD-[DG]-S-[KD]-N-[GR], respectively. Furthermore the numbers of repetitions of the two motifs were variable in different individuals and cell lines, and even in the same fish allelic polymorphism exists. Trout IL-6Rα was expressed at higher levels than gp130 in a number of tissues examined and the expression of both IL-6Rα and gp130 could be modulated by LPS and Poly I:C in the cell lines studied. The expression patterns of the receptors suggest that high level expression of IL-6Rα is critical for IL-6 responsiveness.",
keywords = "amino acid sequence, animals, cell line, cytokine receptor gp130, gene expression regulation, interleukin-6 Receptor alpha subunit, molecular sequence data, Oncorhynchus mykiss, organ specificity, phylogeny, polymorphism, genetic, protein structure, tertiary, repetitive sequences, amino acid, sequence alignment, sequence analysis, DNA",
author = "Costa, {Maria M} and Tiehui Wang and Monte, {Milena M} and Secombes, {Christopher J}",
year = "2012",
month = "3",
doi = "10.1007/s00251-011-0581-1",
language = "English",
volume = "64",
pages = "229--244",
journal = "Immunogenetics",
issn = "0093-7711",
publisher = "Springer Verlag",
number = "3",

}

TY - JOUR

T1 - Molecular characterization and expression analysis of the putative interleukin 6 receptor (IL-6Rα and glycoprotein-130) in rainbow trout (Oncorhynchus mykiss)

T2 - salmonid IL-6Rα possesses a polymorphic N-terminal Ig domain with variable numbers of two repeats

AU - Costa, Maria M

AU - Wang, Tiehui

AU - Monte, Milena M

AU - Secombes, Christopher J

PY - 2012/3

Y1 - 2012/3

N2 - Interleukin (IL)-6, the founding member of IL-6 family cytokines, plays non-redundant roles in hematopoiesis and acute phase responses. IL-6 signals via a specific private IL-6Rα and a common beta chain gp130. In this study, we have cloned both the IL-6Rα and gp130 in rainbow trout. The trout gp130 cDNA encodes 906 aa and is similar in size, extracellular domain structure (D1-D6) and presence of intracellular motifs important for signal transduction to tetrapod gp130s. The trout IL-6Rα cDNA encodes for 834 aa and is larger compared to tetrapod IL-6Rαs, as are other fish IL-6Rα molecules due to a large D1 domain. However, the cytokine-binding domain is well conserved across vertebrates, with four conserved cysteine residues in the N-terminal FNIII domain and a WSXWS motif in the C-terminal FNIII domain. Furthermore, a phylogenetic tree analysis confirmed that the reported fish IL-6Rα and gp130 molecules are orthologues to their tetrapod counterparts. The extra large D1 domain of the salmonid IL-6Rα molecules results partially from the insertions of two repetitive sequences of [TS]-[TF]-VSTTT-[ND]-TTSNG and TTVS-[AT]-IKD-[DG]-S-[KD]-N-[GR], respectively. Furthermore the numbers of repetitions of the two motifs were variable in different individuals and cell lines, and even in the same fish allelic polymorphism exists. Trout IL-6Rα was expressed at higher levels than gp130 in a number of tissues examined and the expression of both IL-6Rα and gp130 could be modulated by LPS and Poly I:C in the cell lines studied. The expression patterns of the receptors suggest that high level expression of IL-6Rα is critical for IL-6 responsiveness.

AB - Interleukin (IL)-6, the founding member of IL-6 family cytokines, plays non-redundant roles in hematopoiesis and acute phase responses. IL-6 signals via a specific private IL-6Rα and a common beta chain gp130. In this study, we have cloned both the IL-6Rα and gp130 in rainbow trout. The trout gp130 cDNA encodes 906 aa and is similar in size, extracellular domain structure (D1-D6) and presence of intracellular motifs important for signal transduction to tetrapod gp130s. The trout IL-6Rα cDNA encodes for 834 aa and is larger compared to tetrapod IL-6Rαs, as are other fish IL-6Rα molecules due to a large D1 domain. However, the cytokine-binding domain is well conserved across vertebrates, with four conserved cysteine residues in the N-terminal FNIII domain and a WSXWS motif in the C-terminal FNIII domain. Furthermore, a phylogenetic tree analysis confirmed that the reported fish IL-6Rα and gp130 molecules are orthologues to their tetrapod counterparts. The extra large D1 domain of the salmonid IL-6Rα molecules results partially from the insertions of two repetitive sequences of [TS]-[TF]-VSTTT-[ND]-TTSNG and TTVS-[AT]-IKD-[DG]-S-[KD]-N-[GR], respectively. Furthermore the numbers of repetitions of the two motifs were variable in different individuals and cell lines, and even in the same fish allelic polymorphism exists. Trout IL-6Rα was expressed at higher levels than gp130 in a number of tissues examined and the expression of both IL-6Rα and gp130 could be modulated by LPS and Poly I:C in the cell lines studied. The expression patterns of the receptors suggest that high level expression of IL-6Rα is critical for IL-6 responsiveness.

KW - amino acid sequence

KW - animals

KW - cell line

KW - cytokine receptor gp130

KW - gene expression regulation

KW - interleukin-6 Receptor alpha subunit

KW - molecular sequence data

KW - Oncorhynchus mykiss

KW - organ specificity

KW - phylogeny

KW - polymorphism, genetic

KW - protein structure, tertiary

KW - repetitive sequences, amino acid

KW - sequence alignment

KW - sequence analysis, DNA

U2 - 10.1007/s00251-011-0581-1

DO - 10.1007/s00251-011-0581-1

M3 - Article

VL - 64

SP - 229

EP - 244

JO - Immunogenetics

JF - Immunogenetics

SN - 0093-7711

IS - 3

ER -