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Vertical Signalling Involves Transmission of Hox Information from Gastrula Mesoderm to Neurectoderm

Development and patterning of neural tissue in the vertebrate embryo involves a set of molecules and processes whose relationships are not fully understood. Classical embryology revealed a remarkable phenomenon known as vertical signalling, a gastrulation stage mechanism that copies anterior-posteri...

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Autores principales: Bardine, Nabila, Lamers, Gerda, Wacker, Stephan, Donow, Cornelia, Knoechel, Walter, Durston, Antony
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4267835/
https://www.ncbi.nlm.nih.gov/pubmed/25514127
http://dx.doi.org/10.1371/journal.pone.0115208
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author Bardine, Nabila
Lamers, Gerda
Wacker, Stephan
Donow, Cornelia
Knoechel, Walter
Durston, Antony
author_facet Bardine, Nabila
Lamers, Gerda
Wacker, Stephan
Donow, Cornelia
Knoechel, Walter
Durston, Antony
author_sort Bardine, Nabila
collection PubMed
description Development and patterning of neural tissue in the vertebrate embryo involves a set of molecules and processes whose relationships are not fully understood. Classical embryology revealed a remarkable phenomenon known as vertical signalling, a gastrulation stage mechanism that copies anterior-posterior positional information from mesoderm to prospective neural tissue. Vertical signalling mediates unambiguous copying of complex information from one tissue layer to another. In this study, we report an investigation of this process in recombinates of mesoderm and ectoderm from gastrulae of Xenopus laevis. Our results show that copying of positional information involves non cell autonomous autoregulation of particular Hox genes whose expression is copied from mesoderm to neurectoderm in the gastrula. Furthermore, this information sharing mechanism involves unconventional translocation of the homeoproteins themselves. This conserved primitive mechanism has been known for three decades but has only recently been put into any developmental context. It provides a simple, robust way to pattern the neurectoderm using the Hox pattern already present in the mesoderm during gastrulation. We suggest that this mechanism was selected during evolution to enable unambiguous copying of rather complex information from cell to cell and that it is a key part of the original ancestral mechanism mediating axial patterning by the highly conserved Hox genes.
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spelling pubmed-42678352014-12-26 Vertical Signalling Involves Transmission of Hox Information from Gastrula Mesoderm to Neurectoderm Bardine, Nabila Lamers, Gerda Wacker, Stephan Donow, Cornelia Knoechel, Walter Durston, Antony PLoS One Research Article Development and patterning of neural tissue in the vertebrate embryo involves a set of molecules and processes whose relationships are not fully understood. Classical embryology revealed a remarkable phenomenon known as vertical signalling, a gastrulation stage mechanism that copies anterior-posterior positional information from mesoderm to prospective neural tissue. Vertical signalling mediates unambiguous copying of complex information from one tissue layer to another. In this study, we report an investigation of this process in recombinates of mesoderm and ectoderm from gastrulae of Xenopus laevis. Our results show that copying of positional information involves non cell autonomous autoregulation of particular Hox genes whose expression is copied from mesoderm to neurectoderm in the gastrula. Furthermore, this information sharing mechanism involves unconventional translocation of the homeoproteins themselves. This conserved primitive mechanism has been known for three decades but has only recently been put into any developmental context. It provides a simple, robust way to pattern the neurectoderm using the Hox pattern already present in the mesoderm during gastrulation. We suggest that this mechanism was selected during evolution to enable unambiguous copying of rather complex information from cell to cell and that it is a key part of the original ancestral mechanism mediating axial patterning by the highly conserved Hox genes. Public Library of Science 2014-12-16 /pmc/articles/PMC4267835/ /pubmed/25514127 http://dx.doi.org/10.1371/journal.pone.0115208 Text en © 2014 Bardine et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Bardine, Nabila
Lamers, Gerda
Wacker, Stephan
Donow, Cornelia
Knoechel, Walter
Durston, Antony
Vertical Signalling Involves Transmission of Hox Information from Gastrula Mesoderm to Neurectoderm
title Vertical Signalling Involves Transmission of Hox Information from Gastrula Mesoderm to Neurectoderm
title_full Vertical Signalling Involves Transmission of Hox Information from Gastrula Mesoderm to Neurectoderm
title_fullStr Vertical Signalling Involves Transmission of Hox Information from Gastrula Mesoderm to Neurectoderm
title_full_unstemmed Vertical Signalling Involves Transmission of Hox Information from Gastrula Mesoderm to Neurectoderm
title_short Vertical Signalling Involves Transmission of Hox Information from Gastrula Mesoderm to Neurectoderm
title_sort vertical signalling involves transmission of hox information from gastrula mesoderm to neurectoderm
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4267835/
https://www.ncbi.nlm.nih.gov/pubmed/25514127
http://dx.doi.org/10.1371/journal.pone.0115208
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