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Mechanical Force Alters Morphogenetic Movements and Segmental Gene Expression Patterns during Drosophila Embryogenesis

The development of an organism is accompanied by various cellular morphogenetic movements, changes in cellular as well as nuclear morphology and transcription programs. Recent evidence suggests that intra and inter-cellular connections mediated by various adhesion proteins contribute to defining nuc...

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Autores principales: Kumar, Abhishek, Shivashankar, G. V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3310051/
https://www.ncbi.nlm.nih.gov/pubmed/22470437
http://dx.doi.org/10.1371/journal.pone.0033089
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author Kumar, Abhishek
Shivashankar, G. V.
author_facet Kumar, Abhishek
Shivashankar, G. V.
author_sort Kumar, Abhishek
collection PubMed
description The development of an organism is accompanied by various cellular morphogenetic movements, changes in cellular as well as nuclear morphology and transcription programs. Recent evidence suggests that intra and inter-cellular connections mediated by various adhesion proteins contribute to defining nuclear morphology. In addition, three dimensional organization of the cell nucleus regulate the transcription programs. However the link between cellular morphogenetic movements and its coupling to nuclear function in a developmental context is poorly understood. In this paper we use a point perturbation by tissue level laser ablation and sheet perturbation by application of force using magnetic tweezers to alter cellular morphogenetic movements and probe its impact on nuclear morphology and segmental gene expression patterns. Mechanical perturbations during blastoderm stage in a developing Drosophila embryo resulted in localized alterations in nuclear morphology and cellular movement. In addition, global defects in germ-band (GB) extension and retraction are observed when external force is applied during morphogenetic movements, suggesting a long-range physical coupling within the GB layer of cells. Further local application of force resulted in redistribution of non muscle myosin-II in the GB layer. Finally these perturbations lead to altered segmental gene (engrailed) expression patterns later during the development. Our observations suggest that there exists a tight regulation between nuclear morphology and cellular adhesive connections during morphogenetic movement of cells in the embryo. The observed spatial changes in patterning genes, with perturbation, highlight the importance of nuclear integrity to cellular movement in establishing gene expression program in a developmental system.
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spelling pubmed-33100512012-04-02 Mechanical Force Alters Morphogenetic Movements and Segmental Gene Expression Patterns during Drosophila Embryogenesis Kumar, Abhishek Shivashankar, G. V. PLoS One Research Article The development of an organism is accompanied by various cellular morphogenetic movements, changes in cellular as well as nuclear morphology and transcription programs. Recent evidence suggests that intra and inter-cellular connections mediated by various adhesion proteins contribute to defining nuclear morphology. In addition, three dimensional organization of the cell nucleus regulate the transcription programs. However the link between cellular morphogenetic movements and its coupling to nuclear function in a developmental context is poorly understood. In this paper we use a point perturbation by tissue level laser ablation and sheet perturbation by application of force using magnetic tweezers to alter cellular morphogenetic movements and probe its impact on nuclear morphology and segmental gene expression patterns. Mechanical perturbations during blastoderm stage in a developing Drosophila embryo resulted in localized alterations in nuclear morphology and cellular movement. In addition, global defects in germ-band (GB) extension and retraction are observed when external force is applied during morphogenetic movements, suggesting a long-range physical coupling within the GB layer of cells. Further local application of force resulted in redistribution of non muscle myosin-II in the GB layer. Finally these perturbations lead to altered segmental gene (engrailed) expression patterns later during the development. Our observations suggest that there exists a tight regulation between nuclear morphology and cellular adhesive connections during morphogenetic movement of cells in the embryo. The observed spatial changes in patterning genes, with perturbation, highlight the importance of nuclear integrity to cellular movement in establishing gene expression program in a developmental system. Public Library of Science 2012-03-21 /pmc/articles/PMC3310051/ /pubmed/22470437 http://dx.doi.org/10.1371/journal.pone.0033089 Text en Kumar, Shivashankar. 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
Kumar, Abhishek
Shivashankar, G. V.
Mechanical Force Alters Morphogenetic Movements and Segmental Gene Expression Patterns during Drosophila Embryogenesis
title Mechanical Force Alters Morphogenetic Movements and Segmental Gene Expression Patterns during Drosophila Embryogenesis
title_full Mechanical Force Alters Morphogenetic Movements and Segmental Gene Expression Patterns during Drosophila Embryogenesis
title_fullStr Mechanical Force Alters Morphogenetic Movements and Segmental Gene Expression Patterns during Drosophila Embryogenesis
title_full_unstemmed Mechanical Force Alters Morphogenetic Movements and Segmental Gene Expression Patterns during Drosophila Embryogenesis
title_short Mechanical Force Alters Morphogenetic Movements and Segmental Gene Expression Patterns during Drosophila Embryogenesis
title_sort mechanical force alters morphogenetic movements and segmental gene expression patterns during drosophila embryogenesis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3310051/
https://www.ncbi.nlm.nih.gov/pubmed/22470437
http://dx.doi.org/10.1371/journal.pone.0033089
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