Experimental and Theoretical Evidence for Bidirectional Signaling via Core Planar Polarity Protein Complexes in Drosophila
Summary: In developing tissues, sheets of cells become planar polarized, enabling coordination of cell behaviors. It has been suggested that “signaling” of polarity information between cells may occur either bidirectionally or monodirectionally between the molecules Frizzled (Fz) and Van Gogh (Vang)...
Main Authors: | , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Elsevier
2019-07-01
|
Series: | iScience |
Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004219302044 |
_version_ | 1818277192323301376 |
---|---|
author | Katherine H. Fisher David Strutt Alexander G. Fletcher |
author_facet | Katherine H. Fisher David Strutt Alexander G. Fletcher |
author_sort | Katherine H. Fisher |
collection | DOAJ |
description | Summary: In developing tissues, sheets of cells become planar polarized, enabling coordination of cell behaviors. It has been suggested that “signaling” of polarity information between cells may occur either bidirectionally or monodirectionally between the molecules Frizzled (Fz) and Van Gogh (Vang). Using computational modeling we find that both bidirectional and monodirectional signaling models reproduce known non-autonomous phenotypes derived from patches of mutant tissue of key molecules but predict different phenotypes from double mutant tissue, which have previously given conflicting experimental results. Furthermore, we re-examine experimental phenotypes in the Drosophila wing, concluding that signaling is most likely bidirectional. Our modeling suggests that bidirectional signaling can be mediated either indirectly via bidirectional feedbacks between asymmetric intercellular protein complexes or directly via different affinities for protein binding in intercellular complexes, suggesting future avenues for investigation. Our findings offer insight into mechanisms of juxtacrine cell signaling and how tissue-scale properties emerge from individual cell behaviors. : Biological Sciences; Developmental Biology; In Silico Biology Subject Areas: Biological Sciences, Developmental Biology, In Silico Biology |
first_indexed | 2024-12-12T22:57:38Z |
format | Article |
id | doaj.art-40cab3b0c3784dbd9045661f93d3af6f |
institution | Directory Open Access Journal |
issn | 2589-0042 |
language | English |
last_indexed | 2024-12-12T22:57:38Z |
publishDate | 2019-07-01 |
publisher | Elsevier |
record_format | Article |
series | iScience |
spelling | doaj.art-40cab3b0c3784dbd9045661f93d3af6f2022-12-22T00:08:53ZengElsevieriScience2589-00422019-07-01174966Experimental and Theoretical Evidence for Bidirectional Signaling via Core Planar Polarity Protein Complexes in DrosophilaKatherine H. Fisher0David Strutt1Alexander G. Fletcher2Department of Biomedical Science, University of Sheffield, Firth Court, Western Bank, Sheffield S10 2TN, UKDepartment of Biomedical Science, University of Sheffield, Firth Court, Western Bank, Sheffield S10 2TN, UK; Corresponding authorSchool of Mathematics and Statistics, University of Sheffield, Hicks Building, Hounsfield Road, Sheffield S3 7RH, UK; Bateson Centre, University of Sheffield, Firth Court, Western Bank, Sheffield S10 2TN, UK; Corresponding authorSummary: In developing tissues, sheets of cells become planar polarized, enabling coordination of cell behaviors. It has been suggested that “signaling” of polarity information between cells may occur either bidirectionally or monodirectionally between the molecules Frizzled (Fz) and Van Gogh (Vang). Using computational modeling we find that both bidirectional and monodirectional signaling models reproduce known non-autonomous phenotypes derived from patches of mutant tissue of key molecules but predict different phenotypes from double mutant tissue, which have previously given conflicting experimental results. Furthermore, we re-examine experimental phenotypes in the Drosophila wing, concluding that signaling is most likely bidirectional. Our modeling suggests that bidirectional signaling can be mediated either indirectly via bidirectional feedbacks between asymmetric intercellular protein complexes or directly via different affinities for protein binding in intercellular complexes, suggesting future avenues for investigation. Our findings offer insight into mechanisms of juxtacrine cell signaling and how tissue-scale properties emerge from individual cell behaviors. : Biological Sciences; Developmental Biology; In Silico Biology Subject Areas: Biological Sciences, Developmental Biology, In Silico Biologyhttp://www.sciencedirect.com/science/article/pii/S2589004219302044 |
spellingShingle | Katherine H. Fisher David Strutt Alexander G. Fletcher Experimental and Theoretical Evidence for Bidirectional Signaling via Core Planar Polarity Protein Complexes in Drosophila iScience |
title | Experimental and Theoretical Evidence for Bidirectional Signaling via Core Planar Polarity Protein Complexes in Drosophila |
title_full | Experimental and Theoretical Evidence for Bidirectional Signaling via Core Planar Polarity Protein Complexes in Drosophila |
title_fullStr | Experimental and Theoretical Evidence for Bidirectional Signaling via Core Planar Polarity Protein Complexes in Drosophila |
title_full_unstemmed | Experimental and Theoretical Evidence for Bidirectional Signaling via Core Planar Polarity Protein Complexes in Drosophila |
title_short | Experimental and Theoretical Evidence for Bidirectional Signaling via Core Planar Polarity Protein Complexes in Drosophila |
title_sort | experimental and theoretical evidence for bidirectional signaling via core planar polarity protein complexes in drosophila |
url | http://www.sciencedirect.com/science/article/pii/S2589004219302044 |
work_keys_str_mv | AT katherinehfisher experimentalandtheoreticalevidenceforbidirectionalsignalingviacoreplanarpolarityproteincomplexesindrosophila AT davidstrutt experimentalandtheoreticalevidenceforbidirectionalsignalingviacoreplanarpolarityproteincomplexesindrosophila AT alexandergfletcher experimentalandtheoreticalevidenceforbidirectionalsignalingviacoreplanarpolarityproteincomplexesindrosophila |