Spatiotemporal compartmentalization of key physiological processes during muscle precursor differentiation

Ertuǧrul M. Özbudak, Olivier Tassy, Olivier Pourquié

Research output: Contribution to journalArticle

27 Citations (Scopus)

Abstract

The development of multicellular organisms is controlled by transcriptional networks. Understanding the role of these networks requires a full understanding of transcriptome regulation during embryogenesis. Several microarray studies have characterized the temporal evolution of the transcriptome during development in different organisms [Wang QT, et al. (2004) Dev Cell 6:133-144; Furlong EE, Andersen EC, Null B, White KP, Scott MP (2001) Science 293:1629-1633; Mitiku N, Baker JC (2007) Dev Cell 13:897-907]. In all cases, however, experiments were performed on whole embryos, thus averaging gene expression among many different tissues. Here, we took advantage of the local synchrony of the differentiation process in the paraxial mesoderm. This approach provides a unique opportunity to study the systems-level properties of muscle differentiation. Using high-resolution, spatiotemporal profiling of the early stages of muscle development in the zebrafish embryo, we identified a major reorganization of the transcriptome taking place in the presomitic mesoderm. We further show that the differentiation process is associated with a striking modular compartmentalization of the transcription of essential components of cellular physiological programs. Particularly, weidentify a tight segregation of cell cycle/DNA metabolic processes and translation/oxidative metabolism at the tissue level, highly reminiscent of the yeast metabolic cycle. These results should expand more investigations into the developmental control of metabolism.

Original languageEnglish (US)
Pages (from-to)4224-4229
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume107
Issue number9
DOIs
StatePublished - Mar 2 2010

Fingerprint

Physiological Phenomena
Transcriptome
Mesoderm
Muscles
Embryonic Structures
Muscle Development
Gene Regulatory Networks
Zebrafish
Embryonic Development
Cell Cycle
Yeasts
Gene Expression
DNA

Keywords

  • Mesoderm
  • Metabolism
  • Stem cell
  • Transcription factors

ASJC Scopus subject areas

  • General

Cite this

Spatiotemporal compartmentalization of key physiological processes during muscle precursor differentiation. / Özbudak, Ertuǧrul M.; Tassy, Olivier; Pourquié, Olivier.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 107, No. 9, 02.03.2010, p. 4224-4229.

Research output: Contribution to journalArticle

@article{20338d4679bf4db191553564af7e34b9,
title = "Spatiotemporal compartmentalization of key physiological processes during muscle precursor differentiation",
abstract = "The development of multicellular organisms is controlled by transcriptional networks. Understanding the role of these networks requires a full understanding of transcriptome regulation during embryogenesis. Several microarray studies have characterized the temporal evolution of the transcriptome during development in different organisms [Wang QT, et al. (2004) Dev Cell 6:133-144; Furlong EE, Andersen EC, Null B, White KP, Scott MP (2001) Science 293:1629-1633; Mitiku N, Baker JC (2007) Dev Cell 13:897-907]. In all cases, however, experiments were performed on whole embryos, thus averaging gene expression among many different tissues. Here, we took advantage of the local synchrony of the differentiation process in the paraxial mesoderm. This approach provides a unique opportunity to study the systems-level properties of muscle differentiation. Using high-resolution, spatiotemporal profiling of the early stages of muscle development in the zebrafish embryo, we identified a major reorganization of the transcriptome taking place in the presomitic mesoderm. We further show that the differentiation process is associated with a striking modular compartmentalization of the transcription of essential components of cellular physiological programs. Particularly, weidentify a tight segregation of cell cycle/DNA metabolic processes and translation/oxidative metabolism at the tissue level, highly reminiscent of the yeast metabolic cycle. These results should expand more investigations into the developmental control of metabolism.",
keywords = "Mesoderm, Metabolism, Stem cell, Transcription factors",
author = "{\"O}zbudak, {Ertuǧrul M.} and Olivier Tassy and Olivier Pourqui{\'e}",
year = "2010",
month = "3",
day = "2",
doi = "10.1073/pnas.0909375107",
language = "English (US)",
volume = "107",
pages = "4224--4229",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "9",

}

TY - JOUR

T1 - Spatiotemporal compartmentalization of key physiological processes during muscle precursor differentiation

AU - Özbudak, Ertuǧrul M.

AU - Tassy, Olivier

AU - Pourquié, Olivier

PY - 2010/3/2

Y1 - 2010/3/2

N2 - The development of multicellular organisms is controlled by transcriptional networks. Understanding the role of these networks requires a full understanding of transcriptome regulation during embryogenesis. Several microarray studies have characterized the temporal evolution of the transcriptome during development in different organisms [Wang QT, et al. (2004) Dev Cell 6:133-144; Furlong EE, Andersen EC, Null B, White KP, Scott MP (2001) Science 293:1629-1633; Mitiku N, Baker JC (2007) Dev Cell 13:897-907]. In all cases, however, experiments were performed on whole embryos, thus averaging gene expression among many different tissues. Here, we took advantage of the local synchrony of the differentiation process in the paraxial mesoderm. This approach provides a unique opportunity to study the systems-level properties of muscle differentiation. Using high-resolution, spatiotemporal profiling of the early stages of muscle development in the zebrafish embryo, we identified a major reorganization of the transcriptome taking place in the presomitic mesoderm. We further show that the differentiation process is associated with a striking modular compartmentalization of the transcription of essential components of cellular physiological programs. Particularly, weidentify a tight segregation of cell cycle/DNA metabolic processes and translation/oxidative metabolism at the tissue level, highly reminiscent of the yeast metabolic cycle. These results should expand more investigations into the developmental control of metabolism.

AB - The development of multicellular organisms is controlled by transcriptional networks. Understanding the role of these networks requires a full understanding of transcriptome regulation during embryogenesis. Several microarray studies have characterized the temporal evolution of the transcriptome during development in different organisms [Wang QT, et al. (2004) Dev Cell 6:133-144; Furlong EE, Andersen EC, Null B, White KP, Scott MP (2001) Science 293:1629-1633; Mitiku N, Baker JC (2007) Dev Cell 13:897-907]. In all cases, however, experiments were performed on whole embryos, thus averaging gene expression among many different tissues. Here, we took advantage of the local synchrony of the differentiation process in the paraxial mesoderm. This approach provides a unique opportunity to study the systems-level properties of muscle differentiation. Using high-resolution, spatiotemporal profiling of the early stages of muscle development in the zebrafish embryo, we identified a major reorganization of the transcriptome taking place in the presomitic mesoderm. We further show that the differentiation process is associated with a striking modular compartmentalization of the transcription of essential components of cellular physiological programs. Particularly, weidentify a tight segregation of cell cycle/DNA metabolic processes and translation/oxidative metabolism at the tissue level, highly reminiscent of the yeast metabolic cycle. These results should expand more investigations into the developmental control of metabolism.

KW - Mesoderm

KW - Metabolism

KW - Stem cell

KW - Transcription factors

UR - http://www.scopus.com/inward/record.url?scp=77749254890&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77749254890&partnerID=8YFLogxK

U2 - 10.1073/pnas.0909375107

DO - 10.1073/pnas.0909375107

M3 - Article

C2 - 20160088

AN - SCOPUS:77749254890

VL - 107

SP - 4224

EP - 4229

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 9

ER -