Divergent regulation of insulin-like growth factor binding protein genes in cultured Atlantic salmon myotubes under different models of catabolism and anabolism

Daniel Garcia de la serrana Castillo, Eduardo N Fuentes, Samuel A M Martin, Ian A Johnston, Daniel J MacQueen

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

Much attention has been given to insulin-like growth factor (Igf) pathways that regulate the balance of skeletal muscle protein synthesis and breakdown in response to a range of extrinsic and intrinsic signals. However, we have a less complete understanding of how the same signals modulate muscle mass upstream of such signalling, through a family of functionally-diverse Igf-binding proteins (Igfbps) that modify the availability of Igfs to the cell receptor Igf1r. We exposed cultured myotubes from Atlantic salmon (Salmo salar L.) to treatments recapturing three catabolic signals: inflammation (interleukin-1β), stress (dexamethasone) and fasting (amino acid deprivation), plus one anabolic signal: recovery of muscle mass post-fasting (supplementation of fasted myotubes with Igf-I and amino acids). The intended phenotype of treatments was confirmed by significant changes in myotube diameter and immunofluorescent staining of structural proteins. We quantified the mRNA-level regulation of the full expressed Igf and Igfbp gene complement across a post-treatment time course, along with marker genes for muscle structural protein synthesis, as well as muscle breakdown, via the ubiquitin-proteasome and autophagy systems. Our results highlight complex, non-overlapping responses of Igfbp family members to the different treatments, suggesting that the profile of expressed Igfbps is differentially regulated by distinct signals promoting similar muscle remodelling phenotypes. We also demonstrate divergent regulation of salmonid-specific gene duplicates of igfbp5b1 and igfbp5b2 under distinct catabolic and anabolic conditions. Overall, this study increases our understanding of the regulation of Igfbp genes in response to signals that promote remodelling of skeletal muscle.
Original languageEnglish
Pages (from-to)53-65
Number of pages13
JournalGeneral and Comparative Endocrinology
Volume247
Early online date19 Jan 2017
DOIs
Publication statusPublished - 1 Jun 2017

Fingerprint

Salmo salar
Insulin-Like Growth Factor Binding Proteins
insulin-like growth factor binding proteins
Skeletal Muscle Fibers
Muscles
muscles
metabolism
Muscle Proteins
Somatomedins
Genes
structural proteins
somatomedins
Fasting
Skeletal Muscle
genes
Duplicate Genes
fasting
skeletal muscle
Phenotype
Amino Acids

Keywords

  • skeletal muscle
  • myotubes
  • cell culture
  • insulin-like growth factor system
  • Igf binding proteins
  • Atlantic salmon
  • dexamethasone
  • Interleukin-1β
  • amino acids

Cite this

Divergent regulation of insulin-like growth factor binding protein genes in cultured Atlantic salmon myotubes under different models of catabolism and anabolism. / de la serrana Castillo, Daniel Garcia ; Fuentes, Eduardo N; Martin, Samuel A M; Johnston, Ian A; MacQueen, Daniel J.

In: General and Comparative Endocrinology, Vol. 247, 01.06.2017, p. 53-65.

Research output: Contribution to journalArticle

@article{714077b44484436b8c7c10b59dc6c927,
title = "Divergent regulation of insulin-like growth factor binding protein genes in cultured Atlantic salmon myotubes under different models of catabolism and anabolism",
abstract = "Much attention has been given to insulin-like growth factor (Igf) pathways that regulate the balance of skeletal muscle protein synthesis and breakdown in response to a range of extrinsic and intrinsic signals. However, we have a less complete understanding of how the same signals modulate muscle mass upstream of such signalling, through a family of functionally-diverse Igf-binding proteins (Igfbps) that modify the availability of Igfs to the cell receptor Igf1r. We exposed cultured myotubes from Atlantic salmon (Salmo salar L.) to treatments recapturing three catabolic signals: inflammation (interleukin-1β), stress (dexamethasone) and fasting (amino acid deprivation), plus one anabolic signal: recovery of muscle mass post-fasting (supplementation of fasted myotubes with Igf-I and amino acids). The intended phenotype of treatments was confirmed by significant changes in myotube diameter and immunofluorescent staining of structural proteins. We quantified the mRNA-level regulation of the full expressed Igf and Igfbp gene complement across a post-treatment time course, along with marker genes for muscle structural protein synthesis, as well as muscle breakdown, via the ubiquitin-proteasome and autophagy systems. Our results highlight complex, non-overlapping responses of Igfbp family members to the different treatments, suggesting that the profile of expressed Igfbps is differentially regulated by distinct signals promoting similar muscle remodelling phenotypes. We also demonstrate divergent regulation of salmonid-specific gene duplicates of igfbp5b1 and igfbp5b2 under distinct catabolic and anabolic conditions. Overall, this study increases our understanding of the regulation of Igfbp genes in response to signals that promote remodelling of skeletal muscle.",
keywords = "skeletal muscle, myotubes, cell culture, insulin-like growth factor system, Igf binding proteins, Atlantic salmon, dexamethasone, Interleukin-1β, amino acids",
author = "{de la serrana Castillo}, {Daniel Garcia} and Fuentes, {Eduardo N} and Martin, {Samuel A M} and Johnston, {Ian A} and MacQueen, {Daniel J}",
note = "Acknowledgments This work received funding from the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland) and their support is gratefully acknowledged. MASTS is funded by the Scottish Funding Council (grant reference HR09011) and contributing institutions.",
year = "2017",
month = "6",
day = "1",
doi = "10.1016/j.ygcen.2017.01.017",
language = "English",
volume = "247",
pages = "53--65",
journal = "General and Comparative Endocrinology",
issn = "0016-6480",
publisher = "Academic Press Inc.",

}

TY - JOUR

T1 - Divergent regulation of insulin-like growth factor binding protein genes in cultured Atlantic salmon myotubes under different models of catabolism and anabolism

AU - de la serrana Castillo, Daniel Garcia

AU - Fuentes, Eduardo N

AU - Martin, Samuel A M

AU - Johnston, Ian A

AU - MacQueen, Daniel J

N1 - Acknowledgments This work received funding from the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland) and their support is gratefully acknowledged. MASTS is funded by the Scottish Funding Council (grant reference HR09011) and contributing institutions.

PY - 2017/6/1

Y1 - 2017/6/1

N2 - Much attention has been given to insulin-like growth factor (Igf) pathways that regulate the balance of skeletal muscle protein synthesis and breakdown in response to a range of extrinsic and intrinsic signals. However, we have a less complete understanding of how the same signals modulate muscle mass upstream of such signalling, through a family of functionally-diverse Igf-binding proteins (Igfbps) that modify the availability of Igfs to the cell receptor Igf1r. We exposed cultured myotubes from Atlantic salmon (Salmo salar L.) to treatments recapturing three catabolic signals: inflammation (interleukin-1β), stress (dexamethasone) and fasting (amino acid deprivation), plus one anabolic signal: recovery of muscle mass post-fasting (supplementation of fasted myotubes with Igf-I and amino acids). The intended phenotype of treatments was confirmed by significant changes in myotube diameter and immunofluorescent staining of structural proteins. We quantified the mRNA-level regulation of the full expressed Igf and Igfbp gene complement across a post-treatment time course, along with marker genes for muscle structural protein synthesis, as well as muscle breakdown, via the ubiquitin-proteasome and autophagy systems. Our results highlight complex, non-overlapping responses of Igfbp family members to the different treatments, suggesting that the profile of expressed Igfbps is differentially regulated by distinct signals promoting similar muscle remodelling phenotypes. We also demonstrate divergent regulation of salmonid-specific gene duplicates of igfbp5b1 and igfbp5b2 under distinct catabolic and anabolic conditions. Overall, this study increases our understanding of the regulation of Igfbp genes in response to signals that promote remodelling of skeletal muscle.

AB - Much attention has been given to insulin-like growth factor (Igf) pathways that regulate the balance of skeletal muscle protein synthesis and breakdown in response to a range of extrinsic and intrinsic signals. However, we have a less complete understanding of how the same signals modulate muscle mass upstream of such signalling, through a family of functionally-diverse Igf-binding proteins (Igfbps) that modify the availability of Igfs to the cell receptor Igf1r. We exposed cultured myotubes from Atlantic salmon (Salmo salar L.) to treatments recapturing three catabolic signals: inflammation (interleukin-1β), stress (dexamethasone) and fasting (amino acid deprivation), plus one anabolic signal: recovery of muscle mass post-fasting (supplementation of fasted myotubes with Igf-I and amino acids). The intended phenotype of treatments was confirmed by significant changes in myotube diameter and immunofluorescent staining of structural proteins. We quantified the mRNA-level regulation of the full expressed Igf and Igfbp gene complement across a post-treatment time course, along with marker genes for muscle structural protein synthesis, as well as muscle breakdown, via the ubiquitin-proteasome and autophagy systems. Our results highlight complex, non-overlapping responses of Igfbp family members to the different treatments, suggesting that the profile of expressed Igfbps is differentially regulated by distinct signals promoting similar muscle remodelling phenotypes. We also demonstrate divergent regulation of salmonid-specific gene duplicates of igfbp5b1 and igfbp5b2 under distinct catabolic and anabolic conditions. Overall, this study increases our understanding of the regulation of Igfbp genes in response to signals that promote remodelling of skeletal muscle.

KW - skeletal muscle

KW - myotubes

KW - cell culture

KW - insulin-like growth factor system

KW - Igf binding proteins

KW - Atlantic salmon

KW - dexamethasone

KW - Interleukin-1β

KW - amino acids

U2 - 10.1016/j.ygcen.2017.01.017

DO - 10.1016/j.ygcen.2017.01.017

M3 - Article

VL - 247

SP - 53

EP - 65

JO - General and Comparative Endocrinology

JF - General and Comparative Endocrinology

SN - 0016-6480

ER -