The intersection of the extrinsic hedgehog and WNT/wingless signals with the intrinsic Hox code underpins branching pattern and tube shape diversity in the drosophila airways.

The tubular networks of the Drosophila respiratory system and our vasculature show distinct branching patterns and tube shapes in different body regions. These local variations are crucial for organ function and organismal fitness. Organotypic patterns and tube geometries in branched networks are ty...

Full description

Bibliographic Details
Main Authors: Ryo Matsuda, Chie Hosono, Kaoru Saigo, Christos Samakovlis
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-01-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC4304712?pdf=render
id doaj-32be8bdcd97c4fa19f78bda8ba4d87f0
record_format Article
spelling doaj-32be8bdcd97c4fa19f78bda8ba4d87f02020-11-24T21:40:44ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042015-01-01111e100492910.1371/journal.pgen.1004929The intersection of the extrinsic hedgehog and WNT/wingless signals with the intrinsic Hox code underpins branching pattern and tube shape diversity in the drosophila airways.Ryo MatsudaChie HosonoKaoru SaigoChristos SamakovlisThe tubular networks of the Drosophila respiratory system and our vasculature show distinct branching patterns and tube shapes in different body regions. These local variations are crucial for organ function and organismal fitness. Organotypic patterns and tube geometries in branched networks are typically controlled by variations of extrinsic signaling but the impact of intrinsic factors on branch patterns and shapes is not well explored. Here, we show that the intersection of extrinsic hedgehog(hh) and WNT/wingless (wg) signaling with the tube-intrinsic Hox code of distinct segments specifies the tube pattern and shape of the Drosophila airways. In the cephalic part of the airways, hh signaling induces expression of the transcription factor (TF) knirps (kni) in the anterior dorsal trunk (DTa1). kni represses the expression of another TF spalt major (salm), making DTa1 a narrow and long tube. In DTa branches of more posterior metameres, Bithorax Complex (BX-C) Hox genes autonomously divert hh signaling from inducing kni, thereby allowing DTa branches to develop as salm-dependent thick and short tubes. Moreover, the differential expression of BX-C genes is partly responsible for the anterior-to-posterior gradual increase of the DT tube diameter through regulating the expression level of Salm, a transcriptional target of WNT/wg signaling. Thus, our results highlight how tube intrinsic differential competence can diversify tube morphology without changing availabilities of extrinsic factors.http://europepmc.org/articles/PMC4304712?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Ryo Matsuda
Chie Hosono
Kaoru Saigo
Christos Samakovlis
spellingShingle Ryo Matsuda
Chie Hosono
Kaoru Saigo
Christos Samakovlis
The intersection of the extrinsic hedgehog and WNT/wingless signals with the intrinsic Hox code underpins branching pattern and tube shape diversity in the drosophila airways.
PLoS Genetics
author_facet Ryo Matsuda
Chie Hosono
Kaoru Saigo
Christos Samakovlis
author_sort Ryo Matsuda
title The intersection of the extrinsic hedgehog and WNT/wingless signals with the intrinsic Hox code underpins branching pattern and tube shape diversity in the drosophila airways.
title_short The intersection of the extrinsic hedgehog and WNT/wingless signals with the intrinsic Hox code underpins branching pattern and tube shape diversity in the drosophila airways.
title_full The intersection of the extrinsic hedgehog and WNT/wingless signals with the intrinsic Hox code underpins branching pattern and tube shape diversity in the drosophila airways.
title_fullStr The intersection of the extrinsic hedgehog and WNT/wingless signals with the intrinsic Hox code underpins branching pattern and tube shape diversity in the drosophila airways.
title_full_unstemmed The intersection of the extrinsic hedgehog and WNT/wingless signals with the intrinsic Hox code underpins branching pattern and tube shape diversity in the drosophila airways.
title_sort intersection of the extrinsic hedgehog and wnt/wingless signals with the intrinsic hox code underpins branching pattern and tube shape diversity in the drosophila airways.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2015-01-01
description The tubular networks of the Drosophila respiratory system and our vasculature show distinct branching patterns and tube shapes in different body regions. These local variations are crucial for organ function and organismal fitness. Organotypic patterns and tube geometries in branched networks are typically controlled by variations of extrinsic signaling but the impact of intrinsic factors on branch patterns and shapes is not well explored. Here, we show that the intersection of extrinsic hedgehog(hh) and WNT/wingless (wg) signaling with the tube-intrinsic Hox code of distinct segments specifies the tube pattern and shape of the Drosophila airways. In the cephalic part of the airways, hh signaling induces expression of the transcription factor (TF) knirps (kni) in the anterior dorsal trunk (DTa1). kni represses the expression of another TF spalt major (salm), making DTa1 a narrow and long tube. In DTa branches of more posterior metameres, Bithorax Complex (BX-C) Hox genes autonomously divert hh signaling from inducing kni, thereby allowing DTa branches to develop as salm-dependent thick and short tubes. Moreover, the differential expression of BX-C genes is partly responsible for the anterior-to-posterior gradual increase of the DT tube diameter through regulating the expression level of Salm, a transcriptional target of WNT/wg signaling. Thus, our results highlight how tube intrinsic differential competence can diversify tube morphology without changing availabilities of extrinsic factors.
url http://europepmc.org/articles/PMC4304712?pdf=render
work_keys_str_mv AT ryomatsuda theintersectionoftheextrinsichedgehogandwntwinglesssignalswiththeintrinsichoxcodeunderpinsbranchingpatternandtubeshapediversityinthedrosophilaairways
AT chiehosono theintersectionoftheextrinsichedgehogandwntwinglesssignalswiththeintrinsichoxcodeunderpinsbranchingpatternandtubeshapediversityinthedrosophilaairways
AT kaorusaigo theintersectionoftheextrinsichedgehogandwntwinglesssignalswiththeintrinsichoxcodeunderpinsbranchingpatternandtubeshapediversityinthedrosophilaairways
AT christossamakovlis theintersectionoftheextrinsichedgehogandwntwinglesssignalswiththeintrinsichoxcodeunderpinsbranchingpatternandtubeshapediversityinthedrosophilaairways
AT ryomatsuda intersectionoftheextrinsichedgehogandwntwinglesssignalswiththeintrinsichoxcodeunderpinsbranchingpatternandtubeshapediversityinthedrosophilaairways
AT chiehosono intersectionoftheextrinsichedgehogandwntwinglesssignalswiththeintrinsichoxcodeunderpinsbranchingpatternandtubeshapediversityinthedrosophilaairways
AT kaorusaigo intersectionoftheextrinsichedgehogandwntwinglesssignalswiththeintrinsichoxcodeunderpinsbranchingpatternandtubeshapediversityinthedrosophilaairways
AT christossamakovlis intersectionoftheextrinsichedgehogandwntwinglesssignalswiththeintrinsichoxcodeunderpinsbranchingpatternandtubeshapediversityinthedrosophilaairways
_version_ 1725924932989222912