Analysis of Gap Gene Regulation in a 3D Organism-Scale Model of the Drosophila melanogaster Embryo
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{"title"=>"Analysis of gap gene regulation in a 3D Organism-Scale model of the Drosophila melanogaster embryo", "type"=>"journal", "authors"=>[{"first_name"=>"James B.", "last_name"=>"Hengenius", "scopus_author_id"=>"53979977200"}, {"first_name"=>"Michael", "last_name"=>"Gribskov", "scopus_author_id"=>"7003537392"}, {"first_name"=>"Ann E.", "last_name"=>"Rundell", "scopus_author_id"=>"20434539900"}, {"first_name"=>"Charless C.", "last_name"=>"Fowlkes", "scopus_author_id"=>"6701549596"}, {"first_name"=>"David M.", "last_name"=>"Umulis", "scopus_author_id"=>"8345158900"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-81155138886", "doi"=>"10.1371/journal.pone.0026797", "pui"=>"362925603", "issn"=>"19326203", "pmid"=>"22110594", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "sgr"=>"81155138886"}, "id"=>"67d9a205-7272-3430-840e-fefc65384de0", "abstract"=>"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.", "link"=>"http://www.mendeley.com/research/analysis-gap-gene-regulation-3d-organismscale-model-drosophila-melanogaster-embryo", "reader_count"=>29, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>4, "Researcher"=>8, "Student > Ph. D. Student"=>9, "Student > Master"=>5, "Student > Bachelor"=>3}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>4, "Researcher"=>8, "Student > Ph. D. Student"=>9, "Student > Master"=>5, "Student > Bachelor"=>3}, "reader_count_by_subject_area"=>{"Engineering"=>5, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>16, "Medicine and Dentistry"=>2, "Physics and Astronomy"=>3}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>5}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Physics and Astronomy"=>{"Physics and Astronomy"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>16}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}}, "reader_count_by_country"=>{"United States"=>1, "United Kingdom"=>1}, "group_count"=>0}

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  • {"files"=>["https://ndownloader.figshare.com/files/711987"], "description"=>"<p>Initial conditions in various models. (<b>A</b>) 1D model initial conditions, reported by Jaeger <i>et al</i>., and used in models and . (<b>B</b>) 1D initial conditions were mapped onto the 3D embryonic geometry (). (<b>C</b>), 1D initial Cad protein distribution, (<b>D</b>) 1D initial Hb protein distribution. Subsequent models incorporated (<b>E</b>) DV-asymmetric interpolated [Bcd] distribution () or (<b>F</b>) smoothed DV-asymmetric interpolated [Bcd] distribution ().</p>", "links"=>[], "tags"=>["3d"], "article_id"=>382349, "categories"=>["Physics", "Biological Sciences", "Developmental Biology"], "users"=>["James B. Hengenius", "Michael Gribskov", "Ann E. Rundell", "Charless C. Fowlkes", "David M. Umulis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026797.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_1D_and_3D_initial_conditions_/382349", "title"=>"1D and 3D initial conditions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-11-16 00:39:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/711870"], "description"=>"<p>Model output was simulated over a 0–100% AP length domain using the optimal GRN reported by Jaeger <i>et al</i>. Solid vertical lines represent the original model boundaries, not used in this simulation. (<b>A</b>) (solid lines) shows qualitative agreement with the Jaeger model (dashed lines) in the 35–92% AP range, but shows discrepancies at either end of the domain due to the movement of boundaries; all species displayed at <i>t</i> = 70 min. (<b>B</b>) The best-fit GRN from Jaeger et al. was locally optimized to improve the agreement of the 0–100% AP length, model (solid lines), and the original Jaeger <i>et al</i>. original model ( dashed lines); all species displayed at <i>t</i> = 70 min. (<b>C</b>) VE protein data for Gt, Hb, Kni, Kr at <i>t</i> = 70 min; VE mRNA data for Tll at <i>t</i> = 70 min; protein data from Jaeger <i>et al</i>. for Cad at <i>t</i> = 56 min. (<b>D</b>) Model output () was also optimized against VE data (RMSE = 13.992); Gt, Hb, Kni, Kr, Tll at <i>t</i> = 70 min; Cad at <i>t</i> = 56 min. Despite modest improvements in model agreement in the 35% and 92% region (<b>C–D</b>), the resulting changes in parameter values were small. (<b>E</b>) Optimized parameter magnitudes vary but signs remained the same in most cases (blue - ; green - ; red - ).</p>", "links"=>[], "tags"=>["Computational biology", "developmental biology", "physics"], "article_id"=>382234, "categories"=>["Physics", "Biological Sciences", "Developmental Biology"], "users"=>["James B. Hengenius", "Michael Gribskov", "Ann E. Rundell", "Charless C. Fowlkes", "David M. Umulis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026797.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_One_dimensional_model_results_/382234", "title"=>"One-dimensional model results.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-11-16 00:37:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/711782"], "description"=>"<p>The model representation of the gap gene network. The network topology in (<b>A</b>) represents negative (black box, flat line) and positive (white box, arrowhead line) regulatory effects on each target gene (blue). Dashed lines represent near-zero regulatory inputs that may be negligible. This qualitative topology is quantified in (<b>B</b>) as a set of genetic regulatory network (GRN) weight parameters <i>w<sub>b,a</sub></i>, the influence of gene b on gene a. From left to right, each set of seven inputs represent Cad, Gt, Hb, Kni, Kr, Tll, and Bcd. Each cluster of seven interactions represents a target gene Cad, Gt, Hb, Kni, Kr, and Tll.</p>", "links"=>[], "tags"=>["Computational biology", "developmental biology", "physics"], "article_id"=>382137, "categories"=>["Physics", "Biological Sciences", "Developmental Biology"], "users"=>["James B. Hengenius", "Michael Gribskov", "Ann E. Rundell", "Charless C. Fowlkes", "David M. Umulis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026797.g001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Gap_gene_genetic_regulatory_network_/382137", "title"=>"Gap gene genetic regulatory network.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-11-16 00:35:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/712111"], "description"=>"<p>Simulation results in the 3D model. (<b>A–H</b>) Lateral view of VE geometry is shown in rows <b>A–G</b> (Gt, Hb, Kni, Kr, Tll at <i>t</i> = 70 min, Cad at <i>t</i> = 56 min); row <b>H</b> displays RMSE difference between model and VE data summed with all time points. Column 1 shows scaled VE data. Column 2 displays output from evaluated with GRN . Column 3 contains output from incorporating DV-asymmetric Bcd data and GRN ; Column 4 illustrates the effect of the smoothed Bcd interpolant in while considering the same GRN . Column 5 displays output from with reoptimized parameters . White boxes indicate the lateral areas where Jaeger <i>et al</i>. optimized their 1D model. Animations of pattern development are available for column 2 ( , <b><a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0026797#pone.0026797.s004\" target=\"_blank\">Movies S1</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0026797#pone.0026797.s005\" target=\"_blank\">S2</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0026797#pone.0026797.s006\" target=\"_blank\">S3</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0026797#pone.0026797.s007\" target=\"_blank\">S4</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0026797#pone.0026797.s008\" target=\"_blank\">S5</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0026797#pone.0026797.s009\" target=\"_blank\">S6</a></b>) and column 5 (, <b><a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0026797#pone.0026797.s010\" target=\"_blank\">Movies S7</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0026797#pone.0026797.s011\" target=\"_blank\">S8</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0026797#pone.0026797.s012\" target=\"_blank\">S9</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0026797#pone.0026797.s013\" target=\"_blank\">S10</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0026797#pone.0026797.s014\" target=\"_blank\">S11</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0026797#pone.0026797.s015\" target=\"_blank\">S12</a></b>) in the supplementary material.</p>", "links"=>[], "tags"=>["Computational biology", "developmental biology", "physics"], "article_id"=>382474, "categories"=>["Physics", "Biological Sciences", "Developmental Biology"], "users"=>["James B. Hengenius", "Michael Gribskov", "Ann E. Rundell", "Charless C. Fowlkes", "David M. Umulis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026797.g004", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Three_dimensional_model_results_/382474", "title"=>"Three-dimensional model results.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-11-16 00:41:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/360915", "https://ndownloader.figshare.com/files/360960", "https://ndownloader.figshare.com/files/361023", "https://ndownloader.figshare.com/files/361079", "https://ndownloader.figshare.com/files/361125", "https://ndownloader.figshare.com/files/361158", "https://ndownloader.figshare.com/files/361184", "https://ndownloader.figshare.com/files/361219", "https://ndownloader.figshare.com/files/361251", "https://ndownloader.figshare.com/files/361290", "https://ndownloader.figshare.com/files/361334", "https://ndownloader.figshare.com/files/361374", "https://ndownloader.figshare.com/files/361410", "https://ndownloader.figshare.com/files/361440", "https://ndownloader.figshare.com/files/361466", "https://ndownloader.figshare.com/files/361495", "https://ndownloader.figshare.com/files/361512", "https://ndownloader.figshare.com/files/361562"], "description"=>"<div><p>The axial bodyplan of <em>Drosophila melanogaster</em> is determined during a process called morphogenesis. Shortly after fertilization, maternal <em>bicoid</em> 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.</p> </div>", "links"=>[], "tags"=>["3d", "organism-scale", "embryo"], "article_id"=>131352, "categories"=>["Physics", "Biological Sciences", "Developmental Biology"], "users"=>["James B. Hengenius", "Michael Gribskov", "Ann E. Rundell", "Charless C. Fowlkes", "David M. Umulis"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0026797.s001", "https://dx.doi.org/10.1371/journal.pone.0026797.s002", "https://dx.doi.org/10.1371/journal.pone.0026797.s003", "https://dx.doi.org/10.1371/journal.pone.0026797.s004", "https://dx.doi.org/10.1371/journal.pone.0026797.s005", "https://dx.doi.org/10.1371/journal.pone.0026797.s006", "https://dx.doi.org/10.1371/journal.pone.0026797.s007", "https://dx.doi.org/10.1371/journal.pone.0026797.s008", "https://dx.doi.org/10.1371/journal.pone.0026797.s009", "https://dx.doi.org/10.1371/journal.pone.0026797.s010", "https://dx.doi.org/10.1371/journal.pone.0026797.s011", "https://dx.doi.org/10.1371/journal.pone.0026797.s012", "https://dx.doi.org/10.1371/journal.pone.0026797.s013", "https://dx.doi.org/10.1371/journal.pone.0026797.s014", "https://dx.doi.org/10.1371/journal.pone.0026797.s015", "https://dx.doi.org/10.1371/journal.pone.0026797.s016", "https://dx.doi.org/10.1371/journal.pone.0026797.s017", "https://dx.doi.org/10.1371/journal.pone.0026797.s018"], "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Analysis_of_Gap_Gene_Regulation_in_a_3D_Organism_Scale_Model_of_the_Drosophila_melanogaster_Embryo/131352", "title"=>"Analysis of Gap Gene Regulation in a 3D Organism-Scale Model of the <em>Drosophila melanogaster</em> Embryo", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-11-16 00:22:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/712244"], "description"=>"<p> Parametric noise alters model output. Lateral view of VE geometry for all genes is shown in rows <b>A–G</b> (all outputs at <i>t</i> = 70 min). Each column displays output at t = 70 min evaluated with GRN . Columns 2–5 represent randomly chosen sample output when a normally distributed noise vector ε is added to the GRN parameter set (denoted θ). ε has mean of 0 and variance that scales with θ.</p>", "links"=>[], "tags"=>["robust", "grn"], "article_id"=>382611, "categories"=>["Physics", "Biological Sciences", "Developmental Biology"], "users"=>["James B. Hengenius", "Michael Gribskov", "Ann E. Rundell", "Charless C. Fowlkes", "David M. Umulis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026797.g005", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Model_is_not_robust_to_noise_in_GRN_parameters_/382611", "title"=>"Model is not robust to noise in GRN parameters.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-11-16 00:43:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/712346"], "description"=>"<p>*optimized by fitting model output to Virtual Embryo data unless otherwise noted.</p>", "links"=>[], "tags"=>["variants", "corresponding", "optimal", "parameter"], "article_id"=>382706, "categories"=>["Physics", "Biological Sciences", "Developmental Biology"], "users"=>["James B. Hengenius", "Michael Gribskov", "Ann E. Rundell", "Charless C. Fowlkes", "David M. Umulis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0026797.t001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Model_Variants_and_Corresponding_Optimal_Parameter_Sets_/382706", "title"=>"Model Variants and Corresponding Optimal Parameter Sets.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-11-16 00:45:06"}

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Relative Metric

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