Formin is associated with left-right asymmetry in the pond snail and the frog

While components of the pathway that establishes left-right asymmetry have been identified in diverse animals, from vertebrates to flies, it is striking that the genes involved in the first symmetry-breaking step remain wholly unknown in the most obviously chiral animals, the gastropod snails. Previ...

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Main Authors: Davison, Angus, McDowell, Gary S., Holden, Jennifer M., Johnson, Harriet F., Koutsovoulos, Georgios D., Liu, M. Maureen, Hulpiau, Paco, Roy, Frans Van, Wade, Christopher M., Banerjee, Ruby, Yang, Fengtang, Chiba, Satoshi, Davey, John W., Jackson, Daniel J., Levin, Michael, Blaxter, Mark L.
Format: Article
Published: Elsevier (Cell Press) 2016
Online Access:https://eprints.nottingham.ac.uk/31985/
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author Davison, Angus
McDowell, Gary S.
Holden, Jennifer M.
Johnson, Harriet F.
Koutsovoulos, Georgios D.
Liu, M. Maureen
Hulpiau, Paco
Roy, Frans Van
Wade, Christopher M.
Banerjee, Ruby
Yang, Fengtang
Chiba, Satoshi
Davey, John W.
Jackson, Daniel J.
Levin, Michael
Blaxter, Mark L.
author_facet Davison, Angus
McDowell, Gary S.
Holden, Jennifer M.
Johnson, Harriet F.
Koutsovoulos, Georgios D.
Liu, M. Maureen
Hulpiau, Paco
Roy, Frans Van
Wade, Christopher M.
Banerjee, Ruby
Yang, Fengtang
Chiba, Satoshi
Davey, John W.
Jackson, Daniel J.
Levin, Michael
Blaxter, Mark L.
author_sort Davison, Angus
building Nottingham Research Data Repository
collection Online Access
description While components of the pathway that establishes left-right asymmetry have been identified in diverse animals, from vertebrates to flies, it is striking that the genes involved in the first symmetry-breaking step remain wholly unknown in the most obviously chiral animals, the gastropod snails. Previously, research on snails was used to show that left-right signalling of Nodal, downstream of symmetry-breaking, may be an ancestral feature of the Bilateria. Here we report that a disabling mutation in one copy of a tandemly duplicated, diaphanous-related formin is perfectly associated with symmetry-breaking in the pond snail. This is supported by the observation that an anti-formin drug treatment converts dextral snail embryos to a sinistral phenocopy, and in frogs, drug inhibition or over-expression by microinjection of formin has a chirality-randomizing effect in early (pre-cilia) embryos. Contrary to expectations based on existing models, we discovered asymmetric gene expression in 2 and 4 cell snail embryos, preceding morphological asymmetry. As the formin-actin filament has been shown to be part of an asymmetry-breaking switch in vitro, together these results are consistent with the view that animals with diverse bodyplans may derive their asymmetries from the same intracellular chiral elements.
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spelling nottingham-319852020-05-04T17:35:32Z https://eprints.nottingham.ac.uk/31985/ Formin is associated with left-right asymmetry in the pond snail and the frog Davison, Angus McDowell, Gary S. Holden, Jennifer M. Johnson, Harriet F. Koutsovoulos, Georgios D. Liu, M. Maureen Hulpiau, Paco Roy, Frans Van Wade, Christopher M. Banerjee, Ruby Yang, Fengtang Chiba, Satoshi Davey, John W. Jackson, Daniel J. Levin, Michael Blaxter, Mark L. While components of the pathway that establishes left-right asymmetry have been identified in diverse animals, from vertebrates to flies, it is striking that the genes involved in the first symmetry-breaking step remain wholly unknown in the most obviously chiral animals, the gastropod snails. Previously, research on snails was used to show that left-right signalling of Nodal, downstream of symmetry-breaking, may be an ancestral feature of the Bilateria. Here we report that a disabling mutation in one copy of a tandemly duplicated, diaphanous-related formin is perfectly associated with symmetry-breaking in the pond snail. This is supported by the observation that an anti-formin drug treatment converts dextral snail embryos to a sinistral phenocopy, and in frogs, drug inhibition or over-expression by microinjection of formin has a chirality-randomizing effect in early (pre-cilia) embryos. Contrary to expectations based on existing models, we discovered asymmetric gene expression in 2 and 4 cell snail embryos, preceding morphological asymmetry. As the formin-actin filament has been shown to be part of an asymmetry-breaking switch in vitro, together these results are consistent with the view that animals with diverse bodyplans may derive their asymmetries from the same intracellular chiral elements. Elsevier (Cell Press) 2016-02-25 Article PeerReviewed Davison, Angus, McDowell, Gary S., Holden, Jennifer M., Johnson, Harriet F., Koutsovoulos, Georgios D., Liu, M. Maureen, Hulpiau, Paco, Roy, Frans Van, Wade, Christopher M., Banerjee, Ruby, Yang, Fengtang, Chiba, Satoshi, Davey, John W., Jackson, Daniel J., Levin, Michael and Blaxter, Mark L. (2016) Formin is associated with left-right asymmetry in the pond snail and the frog. Current Biology . ISSN 1879-0445 (In Press) http://www.cell.com/current-biology/fulltext/S0960-9822(16)00056-7 doi:10.1016/j.cub.2015.12.071 doi:10.1016/j.cub.2015.12.071
spellingShingle Davison, Angus
McDowell, Gary S.
Holden, Jennifer M.
Johnson, Harriet F.
Koutsovoulos, Georgios D.
Liu, M. Maureen
Hulpiau, Paco
Roy, Frans Van
Wade, Christopher M.
Banerjee, Ruby
Yang, Fengtang
Chiba, Satoshi
Davey, John W.
Jackson, Daniel J.
Levin, Michael
Blaxter, Mark L.
Formin is associated with left-right asymmetry in the pond snail and the frog
title Formin is associated with left-right asymmetry in the pond snail and the frog
title_full Formin is associated with left-right asymmetry in the pond snail and the frog
title_fullStr Formin is associated with left-right asymmetry in the pond snail and the frog
title_full_unstemmed Formin is associated with left-right asymmetry in the pond snail and the frog
title_short Formin is associated with left-right asymmetry in the pond snail and the frog
title_sort formin is associated with left-right asymmetry in the pond snail and the frog
url https://eprints.nottingham.ac.uk/31985/
https://eprints.nottingham.ac.uk/31985/
https://eprints.nottingham.ac.uk/31985/