Cell Autonomy of HIF Effects in Drosophila: Tracheal Cells Sense Hypoxia and Induce Terminal Branch Sprouting

Drosophila tracheal terminal branches are plastic and have the capacity to sprout out projections toward oxygen-starved areas, in a process analogous to mammalian angiogenesis. This response involves the upregulation of FGF/Branchless in hypoxic tissues, which binds its receptor Breathless on trache...

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Autores principales: Centanin, L., Dekanty, A., Romero, N., Irisarri, M., Gorr, T.A., Wappner, P.
Formato: Artículo publishedVersion
Publicado: 2008
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Acceso en línea:http://hdl.handle.net/20.500.12110/paper_15345807_v14_n4_p547_Centanin
https://repositoriouba.sisbi.uba.ar/gsdl/cgi-bin/library.cgi?a=d&c=artiaex&d=paper_15345807_v14_n4_p547_Centanin_oai
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id I28-R145-paper_15345807_v14_n4_p547_Centanin_oai
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spelling I28-R145-paper_15345807_v14_n4_p547_Centanin_oai2024-08-16 Centanin, L. Dekanty, A. Romero, N. Irisarri, M. Gorr, T.A. Wappner, P. 2008 Drosophila tracheal terminal branches are plastic and have the capacity to sprout out projections toward oxygen-starved areas, in a process analogous to mammalian angiogenesis. This response involves the upregulation of FGF/Branchless in hypoxic tissues, which binds its receptor Breathless on tracheal cells. Here, we show that extra sprouting depends on the Hypoxia-Inducible Factor (HIF)-α homolog Sima and on the HIF-prolyl hydroxylase Fatiga that operates as an oxygen sensor. In mild hypoxia, Sima accumulates in tracheal cells, where it induces breathless, and this induction is sufficient to provoke tracheal extra sprouting. In nontracheal cells, Sima contributes to branchless induction, whereas overexpression of Sima fails to attract terminal branch outgrowth, suggesting that HIF-independent components are also required for full induction of the ligand. We propose that the autonomous response to hypoxia that occurs in tracheal cells enhances tracheal sensitivity to increasing Branchless levels, and that this mechanism is a cardinal step in hypoxia-dependent tracheal sprouting. © 2008 Elsevier Inc. All rights reserved. Fil:Centanin, L. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Dekanty, A. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Romero, N. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Irisarri, M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Wappner, P. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. application/pdf http://hdl.handle.net/20.500.12110/paper_15345807_v14_n4_p547_Centanin info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by/2.5/ar Dev. Cell 2008;14(4):547-558 DEVBIO cell protein fibroblast growth factor receptor hypoxia inducible factor alpha ligand procollagen proline 2 oxoglutarate 4 dioxygenase protein Fatiga transcription factor transcription factor Branchless transcription factor Breathless transcription factor Sima unclassified drug angiogenesis animal cell article cell hypoxia controlled study Drosophila embryo gene overexpression nonhuman organogenesis oxygen sensing phenotype priority journal protein expression protein localization tissue oxygenation trachea wild type Animals Anoxia Body Patterning DNA-Binding Proteins Drosophila melanogaster Drosophila Proteins Fibroblast Growth Factors Gene Expression Regulation, Developmental Hypoxia-Inducible Factor 1, alpha Subunit Larva Oxygen Phenotype Procollagen-Proline Dioxygenase Protein-Tyrosine Kinases Receptors, Fibroblast Growth Factor Mammalia Cell Autonomy of HIF Effects in Drosophila: Tracheal Cells Sense Hypoxia and Induce Terminal Branch Sprouting info:eu-repo/semantics/article info:ar-repo/semantics/artículo info:eu-repo/semantics/publishedVersion https://repositoriouba.sisbi.uba.ar/gsdl/cgi-bin/library.cgi?a=d&c=artiaex&d=paper_15345807_v14_n4_p547_Centanin_oai
institution Universidad de Buenos Aires
institution_str I-28
repository_str R-145
collection Repositorio Digital de la Universidad de Buenos Aires (UBA)
topic DEVBIO
cell protein
fibroblast growth factor receptor
hypoxia inducible factor alpha
ligand
procollagen proline 2 oxoglutarate 4 dioxygenase
protein Fatiga
transcription factor
transcription factor Branchless
transcription factor Breathless
transcription factor Sima
unclassified drug
angiogenesis
animal cell
article
cell hypoxia
controlled study
Drosophila
embryo
gene overexpression
nonhuman
organogenesis
oxygen sensing
phenotype
priority journal
protein expression
protein localization
tissue oxygenation
trachea
wild type
Animals
Anoxia
Body Patterning
DNA-Binding Proteins
Drosophila melanogaster
Drosophila Proteins
Fibroblast Growth Factors
Gene Expression Regulation, Developmental
Hypoxia-Inducible Factor 1, alpha Subunit
Larva
Oxygen
Phenotype
Procollagen-Proline Dioxygenase
Protein-Tyrosine Kinases
Receptors, Fibroblast Growth Factor
Mammalia
spellingShingle DEVBIO
cell protein
fibroblast growth factor receptor
hypoxia inducible factor alpha
ligand
procollagen proline 2 oxoglutarate 4 dioxygenase
protein Fatiga
transcription factor
transcription factor Branchless
transcription factor Breathless
transcription factor Sima
unclassified drug
angiogenesis
animal cell
article
cell hypoxia
controlled study
Drosophila
embryo
gene overexpression
nonhuman
organogenesis
oxygen sensing
phenotype
priority journal
protein expression
protein localization
tissue oxygenation
trachea
wild type
Animals
Anoxia
Body Patterning
DNA-Binding Proteins
Drosophila melanogaster
Drosophila Proteins
Fibroblast Growth Factors
Gene Expression Regulation, Developmental
Hypoxia-Inducible Factor 1, alpha Subunit
Larva
Oxygen
Phenotype
Procollagen-Proline Dioxygenase
Protein-Tyrosine Kinases
Receptors, Fibroblast Growth Factor
Mammalia
Centanin, L.
Dekanty, A.
Romero, N.
Irisarri, M.
Gorr, T.A.
Wappner, P.
Cell Autonomy of HIF Effects in Drosophila: Tracheal Cells Sense Hypoxia and Induce Terminal Branch Sprouting
topic_facet DEVBIO
cell protein
fibroblast growth factor receptor
hypoxia inducible factor alpha
ligand
procollagen proline 2 oxoglutarate 4 dioxygenase
protein Fatiga
transcription factor
transcription factor Branchless
transcription factor Breathless
transcription factor Sima
unclassified drug
angiogenesis
animal cell
article
cell hypoxia
controlled study
Drosophila
embryo
gene overexpression
nonhuman
organogenesis
oxygen sensing
phenotype
priority journal
protein expression
protein localization
tissue oxygenation
trachea
wild type
Animals
Anoxia
Body Patterning
DNA-Binding Proteins
Drosophila melanogaster
Drosophila Proteins
Fibroblast Growth Factors
Gene Expression Regulation, Developmental
Hypoxia-Inducible Factor 1, alpha Subunit
Larva
Oxygen
Phenotype
Procollagen-Proline Dioxygenase
Protein-Tyrosine Kinases
Receptors, Fibroblast Growth Factor
Mammalia
description Drosophila tracheal terminal branches are plastic and have the capacity to sprout out projections toward oxygen-starved areas, in a process analogous to mammalian angiogenesis. This response involves the upregulation of FGF/Branchless in hypoxic tissues, which binds its receptor Breathless on tracheal cells. Here, we show that extra sprouting depends on the Hypoxia-Inducible Factor (HIF)-α homolog Sima and on the HIF-prolyl hydroxylase Fatiga that operates as an oxygen sensor. In mild hypoxia, Sima accumulates in tracheal cells, where it induces breathless, and this induction is sufficient to provoke tracheal extra sprouting. In nontracheal cells, Sima contributes to branchless induction, whereas overexpression of Sima fails to attract terminal branch outgrowth, suggesting that HIF-independent components are also required for full induction of the ligand. We propose that the autonomous response to hypoxia that occurs in tracheal cells enhances tracheal sensitivity to increasing Branchless levels, and that this mechanism is a cardinal step in hypoxia-dependent tracheal sprouting. © 2008 Elsevier Inc. All rights reserved.
format Artículo
Artículo
publishedVersion
author Centanin, L.
Dekanty, A.
Romero, N.
Irisarri, M.
Gorr, T.A.
Wappner, P.
author_facet Centanin, L.
Dekanty, A.
Romero, N.
Irisarri, M.
Gorr, T.A.
Wappner, P.
author_sort Centanin, L.
title Cell Autonomy of HIF Effects in Drosophila: Tracheal Cells Sense Hypoxia and Induce Terminal Branch Sprouting
title_short Cell Autonomy of HIF Effects in Drosophila: Tracheal Cells Sense Hypoxia and Induce Terminal Branch Sprouting
title_full Cell Autonomy of HIF Effects in Drosophila: Tracheal Cells Sense Hypoxia and Induce Terminal Branch Sprouting
title_fullStr Cell Autonomy of HIF Effects in Drosophila: Tracheal Cells Sense Hypoxia and Induce Terminal Branch Sprouting
title_full_unstemmed Cell Autonomy of HIF Effects in Drosophila: Tracheal Cells Sense Hypoxia and Induce Terminal Branch Sprouting
title_sort cell autonomy of hif effects in drosophila: tracheal cells sense hypoxia and induce terminal branch sprouting
publishDate 2008
url http://hdl.handle.net/20.500.12110/paper_15345807_v14_n4_p547_Centanin
https://repositoriouba.sisbi.uba.ar/gsdl/cgi-bin/library.cgi?a=d&c=artiaex&d=paper_15345807_v14_n4_p547_Centanin_oai
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