The hypoxia-inducible transcription factor pathway regulates oxygen sensing in the simplest animal, Trichoplax adhaerens

Christoph Loenarz; Mathew L Coleman; Anna Boleininger; Bernd Schierwater; Peter W H Holland; Peter J Ratcliffe; Christopher J Schofield

doi:10.1038/embor.2010.170

The hypoxia-inducible transcription factor pathway regulates oxygen sensing in the simplest animal, Trichoplax adhaerens

Christoph Loenarz, Mathew L Coleman, Anna Boleininger, Bernd Schierwater, Peter W H Holland, Peter J Ratcliffe, Christopher J Schofield

Research output: Contribution to journal › Article › peer-review

150 Citations (Scopus)

Abstract

The hypoxic response in humans is mediated by the hypoxia-inducible transcription factor (HIF), for which prolyl hydroxylases (PHDs) act as oxygen-sensing components. The evolutionary origins of the HIF system have been previously unclear. We demonstrate a functional HIF system in the simplest animal, Trichoplax adhaerens: HIF targets in T. adhaerens include glycolytic and metabolic enzymes, suggesting a role for HIF in the adaptation of basal multicellular animals to fluctuating oxygen levels. Characterization of the T. adhaerens PHDs and cross-species complementation assays reveal a conserved oxygen-sensing mechanism. Cross-genomic analyses rationalize the relative importance of HIF system components, and imply that the HIF system is likely to be present in all animals, but is unique to this kingdom.

Original language	English
Pages (from-to)	63-70
Number of pages	8
Journal	EMBO Reports
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/embor.2010.170
Publication status	Published - Jan 2011

Keywords

Amino Acid Sequence
Animals
Hypoxia-Inducible Factor 1
Molecular Sequence Data
Oxygen
Phylogeny
Placozoa
Procollagen-Proline Dioxygenase
Transcriptional Activation
Von Hippel-Lindau Tumor Suppressor Protein

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10.1038/embor.2010.170

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title = "The hypoxia-inducible transcription factor pathway regulates oxygen sensing in the simplest animal, Trichoplax adhaerens",

abstract = "The hypoxic response in humans is mediated by the hypoxia-inducible transcription factor (HIF), for which prolyl hydroxylases (PHDs) act as oxygen-sensing components. The evolutionary origins of the HIF system have been previously unclear. We demonstrate a functional HIF system in the simplest animal, Trichoplax adhaerens: HIF targets in T. adhaerens include glycolytic and metabolic enzymes, suggesting a role for HIF in the adaptation of basal multicellular animals to fluctuating oxygen levels. Characterization of the T. adhaerens PHDs and cross-species complementation assays reveal a conserved oxygen-sensing mechanism. Cross-genomic analyses rationalize the relative importance of HIF system components, and imply that the HIF system is likely to be present in all animals, but is unique to this kingdom.",

keywords = "Amino Acid Sequence, Animals, Hypoxia-Inducible Factor 1, Molecular Sequence Data, Oxygen, Phylogeny, Placozoa, Procollagen-Proline Dioxygenase, Transcriptional Activation, Von Hippel-Lindau Tumor Suppressor Protein",

author = "Christoph Loenarz and Coleman, {Mathew L} and Anna Boleininger and Bernd Schierwater and Holland, {Peter W H} and Ratcliffe, {Peter J} and Schofield, {Christopher J}",

year = "2011",

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doi = "10.1038/embor.2010.170",

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AU - Loenarz, Christoph

AU - Coleman, Mathew L

AU - Boleininger, Anna

AU - Schierwater, Bernd

AU - Holland, Peter W H

AU - Ratcliffe, Peter J

AU - Schofield, Christopher J

PY - 2011/1

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N2 - The hypoxic response in humans is mediated by the hypoxia-inducible transcription factor (HIF), for which prolyl hydroxylases (PHDs) act as oxygen-sensing components. The evolutionary origins of the HIF system have been previously unclear. We demonstrate a functional HIF system in the simplest animal, Trichoplax adhaerens: HIF targets in T. adhaerens include glycolytic and metabolic enzymes, suggesting a role for HIF in the adaptation of basal multicellular animals to fluctuating oxygen levels. Characterization of the T. adhaerens PHDs and cross-species complementation assays reveal a conserved oxygen-sensing mechanism. Cross-genomic analyses rationalize the relative importance of HIF system components, and imply that the HIF system is likely to be present in all animals, but is unique to this kingdom.

AB - The hypoxic response in humans is mediated by the hypoxia-inducible transcription factor (HIF), for which prolyl hydroxylases (PHDs) act as oxygen-sensing components. The evolutionary origins of the HIF system have been previously unclear. We demonstrate a functional HIF system in the simplest animal, Trichoplax adhaerens: HIF targets in T. adhaerens include glycolytic and metabolic enzymes, suggesting a role for HIF in the adaptation of basal multicellular animals to fluctuating oxygen levels. Characterization of the T. adhaerens PHDs and cross-species complementation assays reveal a conserved oxygen-sensing mechanism. Cross-genomic analyses rationalize the relative importance of HIF system components, and imply that the HIF system is likely to be present in all animals, but is unique to this kingdom.

KW - Amino Acid Sequence

KW - Animals

KW - Hypoxia-Inducible Factor 1

KW - Molecular Sequence Data

KW - Oxygen

KW - Phylogeny

KW - Placozoa

KW - Procollagen-Proline Dioxygenase

KW - Transcriptional Activation

KW - Von Hippel-Lindau Tumor Suppressor Protein

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DO - 10.1038/embor.2010.170

M3 - Article

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SN - 1469-221X

VL - 12

SP - 63

EP - 70

JO - EMBO Reports

JF - EMBO Reports

IS - 1

ER -

The hypoxia-inducible transcription factor pathway regulates oxygen sensing in the simplest animal, Trichoplax adhaerens

Abstract

Keywords

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