Analysis of gap gene regulation in a 3D organism-scale model of the Drosophila melanogaster embryo.

The axial bodyplan of Drosophila melanogaster is determined during a process called morphogenesis. Shortly after fertilization, maternal bicoid mRNA is translated into Bicoid (Bcd). This protein establishes a spatially graded morphogen distribution along the anterior-posterior (AP) axis of the embry...

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Autores principales:	James B Hengenius, Michael Gribskov, Ann E Rundell, Charless C Fowlkes, David M Umulis
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2011
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/5b87a993f9824fc88258f3f66d8c6d88
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spelling	oai:doaj.org-article:5b87a993f9824fc88258f3f66d8c6d882021-11-18T07:34:14ZAnalysis of gap gene regulation in a 3D organism-scale model of the Drosophila melanogaster embryo.1932-620310.1371/journal.pone.0026797https://doaj.org/article/5b87a993f9824fc88258f3f66d8c6d882011-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22110594/?tool=EBIhttps://doaj.org/toc/1932-6203The axial bodyplan of Drosophila melanogaster is determined during a process called morphogenesis. Shortly after fertilization, maternal bicoid mRNA is translated into Bicoid (Bcd). This protein establishes a spatially graded morphogen distribution along the anterior-posterior (AP) axis of the embryo. Bcd initiates AP axis determination by triggering expression of gap genes that subsequently regulate each other's expression to form a precisely controlled spatial distribution of gene products. Reaction-diffusion models of gap gene expression on a 1D domain have previously been used to infer complex genetic regulatory network (GRN) interactions by optimizing model parameters with respect to 1D gap gene expression data. Here we construct a finite element reaction-diffusion model with a realistic 3D geometry fit to full 3D gap gene expression data. Though gap gene products exhibit dorsal-ventral asymmetries, we discover that previously inferred gap GRNs yield qualitatively correct AP distributions on the 3D domain only when DV-symmetric initial conditions are employed. Model patterning loses qualitative agreement with experimental data when we incorporate a realistic DV-asymmetric distribution of Bcd. Further, we find that geometry alone is insufficient to account for DV-asymmetries in the final gap gene distribution. Additional GRN optimization confirms that the 3D model remains sensitive to GRN parameter perturbations. Finally, we find that incorporation of 3D data in simulation and optimization does not constrain the search space or improve optimization results.James B HengeniusMichael GribskovAnn E RundellCharless C FowlkesDavid M UmulisPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 6, Iss 11, p e26797 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q James B Hengenius Michael Gribskov Ann E Rundell Charless C Fowlkes David M Umulis Analysis of gap gene regulation in a 3D organism-scale model of the Drosophila melanogaster embryo.
description	The axial bodyplan of Drosophila melanogaster is determined during a process called morphogenesis. Shortly after fertilization, maternal bicoid mRNA is translated into Bicoid (Bcd). This protein establishes a spatially graded morphogen distribution along the anterior-posterior (AP) axis of the embryo. Bcd initiates AP axis determination by triggering expression of gap genes that subsequently regulate each other's expression to form a precisely controlled spatial distribution of gene products. Reaction-diffusion models of gap gene expression on a 1D domain have previously been used to infer complex genetic regulatory network (GRN) interactions by optimizing model parameters with respect to 1D gap gene expression data. Here we construct a finite element reaction-diffusion model with a realistic 3D geometry fit to full 3D gap gene expression data. Though gap gene products exhibit dorsal-ventral asymmetries, we discover that previously inferred gap GRNs yield qualitatively correct AP distributions on the 3D domain only when DV-symmetric initial conditions are employed. Model patterning loses qualitative agreement with experimental data when we incorporate a realistic DV-asymmetric distribution of Bcd. Further, we find that geometry alone is insufficient to account for DV-asymmetries in the final gap gene distribution. Additional GRN optimization confirms that the 3D model remains sensitive to GRN parameter perturbations. Finally, we find that incorporation of 3D data in simulation and optimization does not constrain the search space or improve optimization results.
format	article
author	James B Hengenius Michael Gribskov Ann E Rundell Charless C Fowlkes David M Umulis
author_facet	James B Hengenius Michael Gribskov Ann E Rundell Charless C Fowlkes David M Umulis
author_sort	James B Hengenius
title	Analysis of gap gene regulation in a 3D organism-scale model of the Drosophila melanogaster embryo.
title_short	Analysis of gap gene regulation in a 3D organism-scale model of the Drosophila melanogaster embryo.
title_full	Analysis of gap gene regulation in a 3D organism-scale model of the Drosophila melanogaster embryo.
title_fullStr	Analysis of gap gene regulation in a 3D organism-scale model of the Drosophila melanogaster embryo.
title_full_unstemmed	Analysis of gap gene regulation in a 3D organism-scale model of the Drosophila melanogaster embryo.
title_sort	analysis of gap gene regulation in a 3d organism-scale model of the drosophila melanogaster embryo.
publisher	Public Library of Science (PLoS)
publishDate	2011
url	https://doaj.org/article/5b87a993f9824fc88258f3f66d8c6d88
work_keys_str_mv	AT jamesbhengenius analysisofgapgeneregulationina3dorganismscalemodelofthedrosophilamelanogasterembryo AT michaelgribskov analysisofgapgeneregulationina3dorganismscalemodelofthedrosophilamelanogasterembryo AT annerundell analysisofgapgeneregulationina3dorganismscalemodelofthedrosophilamelanogasterembryo AT charlesscfowlkes analysisofgapgeneregulationina3dorganismscalemodelofthedrosophilamelanogasterembryo AT davidmumulis analysisofgapgeneregulationina3dorganismscalemodelofthedrosophilamelanogasterembryo
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Analysis of gap gene regulation in a 3D organism-scale model of the Drosophila melanogaster embryo.

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