Embryonic temperature affects muscle fibre recruitment in adult zebrafish

genome-wide changes in gene and microRNA expression associated with the transition from hyperplastic to hypertrophic growth phenotypes

Ian A Johnston, Hung-Tai Lee, Daniel J Macqueen, Karthikeyani Paranthaman, Cintia Kawashima, Attia Anwar, James R Kinghorn, Tamas Dalmay

Research output: Contribution to journalArticle

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Abstract

We investigated the effects of embryonic temperature (ET) treatments (22, 26 and 31°C) on the life-time recruitment of fast myotomal muscle fibres in zebrafish Danio rerio L. reared at 26/27°C from hatching. Fast muscle fibres were produced until 25 mm total length (TL) at 22°C ET, 28 mm TL at 26°C ET and 23 mm TL at 31°C ET. The final fibre number (FFN) showed an optimum at 26°C ET (3600) and was 19% and 14% higher than for the 22°C ET (3000) and 31°C ET (3100) treatments, respectively. Further growth to the maximum TL of ∼48 mm only involved fibre hypertrophy. Microarray experiments were used to determine global changes in microRNA (miRNA) and mRNA expression associated with the transition from the hyperplasic myotube-producing phenotype (M+, 10–12 mm TL) to the hypertrophic growth phenotype (M–, 28–31 mm TL) in fish reared at 26–27°C over the whole life-cycle. The expression of miRNAs and mRNAs obtained from microarray experiments was validated by northern blotting and real-time qPCR in independent samples of fish with the M+ and M– phenotype. Fourteen down-regulated and 15 up-regulated miRNAs were identified in the M– phenotype together with 34 down-regulated and 30 up-regulated mRNAs (>2-fold; P<0.05). The two most abundant categories of down-regulated genes in the M– phenotype encoded contractile proteins (23.5%) and sarcomeric structural/cytoskeletal proteins (14.7%). In contrast, the most highly represented up-regulated transcripts in the M– phenotype were energy metabolism (26.7%) and immune-related (20.0%) genes. The latter were mostly involved in cell–cell interactions and cytokine pathways and included β-2-microglobulin precursor (b2m), an orthologue of complement component 4, invariant chain-like protein 1 (iclp), CD9 antigen-like (cd9l), and tyrosine kinase, non-receptor (tnk2). Five myosin heavy chain genes that were down-regulated in the M– phenotype formed part of a tandem repeat on chromosome 5 and were shown by in situ hybridisation to be specifically expressed in nascent myofibres. Seven up-regulated miRNAs in the M– phenotype showed reciprocal expression with seven mRNA targets identified in miRBase Targets version 5 (http://microrna.sanger.ac.uk/targets/v5/), including asporin (aspn) which was the target for four miRNAs. Eleven down-regulated miRNAs in the M– phenotype had predicted targets for seven up-regulated genes, including dre-miR-181c which had five predicted mRNA targets. These results provide evidence that miRNAs play a role in regulating the transition from the M+ to the M– phenotype and identify some of the genes and regulatory interactions involved.
Original languageEnglish
Pages (from-to)1781-1793
Number of pages13
JournalJournal of Experimental Biology
Volume212
Issue number12
DOIs
Publication statusPublished - 15 Jun 2009

Fingerprint

Zebrafish
MicroRNAs
Danio rerio
microRNA
muscle fibers
phenotype
muscle
genome
Genome
Phenotype
Gene Expression
Muscles
Temperature
gene
Growth
temperature
genes
Messenger RNA
Genes
protein

Keywords

  • Danio rerio
  • microRNA
  • developmental plasticity
  • temperature
  • muscle growth
  • muscle hyperplasia
  • gene expression
  • myosin heavy chains
  • β-2-microglobulin

Cite this

Embryonic temperature affects muscle fibre recruitment in adult zebrafish : genome-wide changes in gene and microRNA expression associated with the transition from hyperplastic to hypertrophic growth phenotypes. / Johnston, Ian A; Lee, Hung-Tai; Macqueen, Daniel J; Paranthaman, Karthikeyani; Kawashima, Cintia; Anwar, Attia; Kinghorn, James R; Dalmay, Tamas.

In: Journal of Experimental Biology, Vol. 212, No. 12, 15.06.2009, p. 1781-1793.

Research output: Contribution to journalArticle

Johnston, Ian A ; Lee, Hung-Tai ; Macqueen, Daniel J ; Paranthaman, Karthikeyani ; Kawashima, Cintia ; Anwar, Attia ; Kinghorn, James R ; Dalmay, Tamas. / Embryonic temperature affects muscle fibre recruitment in adult zebrafish : genome-wide changes in gene and microRNA expression associated with the transition from hyperplastic to hypertrophic growth phenotypes. In: Journal of Experimental Biology. 2009 ; Vol. 212, No. 12. pp. 1781-1793.
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abstract = "We investigated the effects of embryonic temperature (ET) treatments (22, 26 and 31°C) on the life-time recruitment of fast myotomal muscle fibres in zebrafish Danio rerio L. reared at 26/27°C from hatching. Fast muscle fibres were produced until 25 mm total length (TL) at 22°C ET, 28 mm TL at 26°C ET and 23 mm TL at 31°C ET. The final fibre number (FFN) showed an optimum at 26°C ET (3600) and was 19{\%} and 14{\%} higher than for the 22°C ET (3000) and 31°C ET (3100) treatments, respectively. Further growth to the maximum TL of ∼48 mm only involved fibre hypertrophy. Microarray experiments were used to determine global changes in microRNA (miRNA) and mRNA expression associated with the transition from the hyperplasic myotube-producing phenotype (M+, 10–12 mm TL) to the hypertrophic growth phenotype (M–, 28–31 mm TL) in fish reared at 26–27°C over the whole life-cycle. The expression of miRNAs and mRNAs obtained from microarray experiments was validated by northern blotting and real-time qPCR in independent samples of fish with the M+ and M– phenotype. Fourteen down-regulated and 15 up-regulated miRNAs were identified in the M– phenotype together with 34 down-regulated and 30 up-regulated mRNAs (>2-fold; P<0.05). The two most abundant categories of down-regulated genes in the M– phenotype encoded contractile proteins (23.5{\%}) and sarcomeric structural/cytoskeletal proteins (14.7{\%}). In contrast, the most highly represented up-regulated transcripts in the M– phenotype were energy metabolism (26.7{\%}) and immune-related (20.0{\%}) genes. The latter were mostly involved in cell–cell interactions and cytokine pathways and included β-2-microglobulin precursor (b2m), an orthologue of complement component 4, invariant chain-like protein 1 (iclp), CD9 antigen-like (cd9l), and tyrosine kinase, non-receptor (tnk2). Five myosin heavy chain genes that were down-regulated in the M– phenotype formed part of a tandem repeat on chromosome 5 and were shown by in situ hybridisation to be specifically expressed in nascent myofibres. Seven up-regulated miRNAs in the M– phenotype showed reciprocal expression with seven mRNA targets identified in miRBase Targets version 5 (http://microrna.sanger.ac.uk/targets/v5/), including asporin (aspn) which was the target for four miRNAs. Eleven down-regulated miRNAs in the M– phenotype had predicted targets for seven up-regulated genes, including dre-miR-181c which had five predicted mRNA targets. These results provide evidence that miRNAs play a role in regulating the transition from the M+ to the M– phenotype and identify some of the genes and regulatory interactions involved.",
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TY - JOUR

T1 - Embryonic temperature affects muscle fibre recruitment in adult zebrafish

T2 - genome-wide changes in gene and microRNA expression associated with the transition from hyperplastic to hypertrophic growth phenotypes

AU - Johnston, Ian A

AU - Lee, Hung-Tai

AU - Macqueen, Daniel J

AU - Paranthaman, Karthikeyani

AU - Kawashima, Cintia

AU - Anwar, Attia

AU - Kinghorn, James R

AU - Dalmay, Tamas

PY - 2009/6/15

Y1 - 2009/6/15

N2 - We investigated the effects of embryonic temperature (ET) treatments (22, 26 and 31°C) on the life-time recruitment of fast myotomal muscle fibres in zebrafish Danio rerio L. reared at 26/27°C from hatching. Fast muscle fibres were produced until 25 mm total length (TL) at 22°C ET, 28 mm TL at 26°C ET and 23 mm TL at 31°C ET. The final fibre number (FFN) showed an optimum at 26°C ET (3600) and was 19% and 14% higher than for the 22°C ET (3000) and 31°C ET (3100) treatments, respectively. Further growth to the maximum TL of ∼48 mm only involved fibre hypertrophy. Microarray experiments were used to determine global changes in microRNA (miRNA) and mRNA expression associated with the transition from the hyperplasic myotube-producing phenotype (M+, 10–12 mm TL) to the hypertrophic growth phenotype (M–, 28–31 mm TL) in fish reared at 26–27°C over the whole life-cycle. The expression of miRNAs and mRNAs obtained from microarray experiments was validated by northern blotting and real-time qPCR in independent samples of fish with the M+ and M– phenotype. Fourteen down-regulated and 15 up-regulated miRNAs were identified in the M– phenotype together with 34 down-regulated and 30 up-regulated mRNAs (>2-fold; P<0.05). The two most abundant categories of down-regulated genes in the M– phenotype encoded contractile proteins (23.5%) and sarcomeric structural/cytoskeletal proteins (14.7%). In contrast, the most highly represented up-regulated transcripts in the M– phenotype were energy metabolism (26.7%) and immune-related (20.0%) genes. The latter were mostly involved in cell–cell interactions and cytokine pathways and included β-2-microglobulin precursor (b2m), an orthologue of complement component 4, invariant chain-like protein 1 (iclp), CD9 antigen-like (cd9l), and tyrosine kinase, non-receptor (tnk2). Five myosin heavy chain genes that were down-regulated in the M– phenotype formed part of a tandem repeat on chromosome 5 and were shown by in situ hybridisation to be specifically expressed in nascent myofibres. Seven up-regulated miRNAs in the M– phenotype showed reciprocal expression with seven mRNA targets identified in miRBase Targets version 5 (http://microrna.sanger.ac.uk/targets/v5/), including asporin (aspn) which was the target for four miRNAs. Eleven down-regulated miRNAs in the M– phenotype had predicted targets for seven up-regulated genes, including dre-miR-181c which had five predicted mRNA targets. These results provide evidence that miRNAs play a role in regulating the transition from the M+ to the M– phenotype and identify some of the genes and regulatory interactions involved.

AB - We investigated the effects of embryonic temperature (ET) treatments (22, 26 and 31°C) on the life-time recruitment of fast myotomal muscle fibres in zebrafish Danio rerio L. reared at 26/27°C from hatching. Fast muscle fibres were produced until 25 mm total length (TL) at 22°C ET, 28 mm TL at 26°C ET and 23 mm TL at 31°C ET. The final fibre number (FFN) showed an optimum at 26°C ET (3600) and was 19% and 14% higher than for the 22°C ET (3000) and 31°C ET (3100) treatments, respectively. Further growth to the maximum TL of ∼48 mm only involved fibre hypertrophy. Microarray experiments were used to determine global changes in microRNA (miRNA) and mRNA expression associated with the transition from the hyperplasic myotube-producing phenotype (M+, 10–12 mm TL) to the hypertrophic growth phenotype (M–, 28–31 mm TL) in fish reared at 26–27°C over the whole life-cycle. The expression of miRNAs and mRNAs obtained from microarray experiments was validated by northern blotting and real-time qPCR in independent samples of fish with the M+ and M– phenotype. Fourteen down-regulated and 15 up-regulated miRNAs were identified in the M– phenotype together with 34 down-regulated and 30 up-regulated mRNAs (>2-fold; P<0.05). The two most abundant categories of down-regulated genes in the M– phenotype encoded contractile proteins (23.5%) and sarcomeric structural/cytoskeletal proteins (14.7%). In contrast, the most highly represented up-regulated transcripts in the M– phenotype were energy metabolism (26.7%) and immune-related (20.0%) genes. The latter were mostly involved in cell–cell interactions and cytokine pathways and included β-2-microglobulin precursor (b2m), an orthologue of complement component 4, invariant chain-like protein 1 (iclp), CD9 antigen-like (cd9l), and tyrosine kinase, non-receptor (tnk2). Five myosin heavy chain genes that were down-regulated in the M– phenotype formed part of a tandem repeat on chromosome 5 and were shown by in situ hybridisation to be specifically expressed in nascent myofibres. Seven up-regulated miRNAs in the M– phenotype showed reciprocal expression with seven mRNA targets identified in miRBase Targets version 5 (http://microrna.sanger.ac.uk/targets/v5/), including asporin (aspn) which was the target for four miRNAs. Eleven down-regulated miRNAs in the M– phenotype had predicted targets for seven up-regulated genes, including dre-miR-181c which had five predicted mRNA targets. These results provide evidence that miRNAs play a role in regulating the transition from the M+ to the M– phenotype and identify some of the genes and regulatory interactions involved.

KW - Danio rerio

KW - microRNA

KW - developmental plasticity

KW - temperature

KW - muscle growth

KW - muscle hyperplasia

KW - gene expression

KW - myosin heavy chains

KW - β-2-microglobulin

U2 - 10.1242/jeb.029918

DO - 10.1242/jeb.029918

M3 - Article

VL - 212

SP - 1781

EP - 1793

JO - Journal of Experimental Biology

JF - Journal of Experimental Biology

SN - 0022-0949

IS - 12

ER -