Simulating the Mammalian Blastocyst - Molecular and Mechanical Interactions Pattern the Embryo
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{"title"=>"Simulating the Mammalian Blastocyst - Molecular and Mechanical Interactions Pattern the Embryo", "type"=>"journal", "authors"=>[{"first_name"=>"Pawel", "last_name"=>"Krupinski", "scopus_author_id"=>"12647443400"}, {"first_name"=>"Vijay", "last_name"=>"Chickarmane", "scopus_author_id"=>"6602384133"}, {"first_name"=>"Carsten", "last_name"=>"Peterson", "scopus_author_id"=>"55574236891"}], "year"=>2011, "source"=>"PLoS Computational Biology", "identifiers"=>{"scopus"=>"2-s2.0-79958174363", "doi"=>"10.1371/journal.pcbi.1001128", "sgr"=>"79958174363", "pmid"=>"21573197", "issn"=>"1553734X", "pui"=>"361907822"}, "id"=>"15f9aefd-3033-3f08-b042-69aae9320b3c", "abstract"=>"Mammalian embryogenesis is a dynamic process involving gene expression and mechanical forces between proliferating cells. The exact nature of these interactions, which determine the lineage patterning of the trophectoderm and endoderm tissues occurring in a highly regulated manner at precise periods during the embryonic development, is an area of debate. We have developed a computational modeling framework for studying this process, by which the combined effects of mechanical and genetic interactions are analyzed within the context of proliferating cells. At a purely mechanical level, we demonstrate that the perpendicular alignment of the animal-vegetal (a-v) and embryonic-abembryonic (eb-ab) axes is a result of minimizing the total elastic conformational energy of the entire collection of cells, which are constrained by the zona pellucida. The coupling of gene expression with the mechanics of cell movement is important for formation of both the trophectoderm and the endoderm. In studying the formation of the trophectoderm, we contrast and compare quantitatively two hypotheses: (1) The position determines gene expression, and (2) the gene expression determines the position. Our model, which couples gene expression with mechanics, suggests that differential adhesion between different cell types is a critical determinant in the robust endoderm formation. In addition to differential adhesion, two different testable hypotheses emerge when considering endoderm formation: (1) A directional force acts on certain cells and moves them into forming the endoderm layer, which separates the blastocoel and the cells of the inner cell mass (ICM). In this case the blastocoel simply acts as a static boundary. (2) The blastocoel dynamically applies pressure upon the cells in contact with it, such that cell segregation in the presence of differential adhesion leads to the endoderm formation. To our knowledge, this is the first attempt to combine cell-based spatial mechanical simulations with genetic networks to explain mammalian embryogenesis. Such a framework provides the means to test hypotheses in a controlled in silico environment.", "link"=>"http://www.mendeley.com/research/simulating-mammalian-blastocyst-molecular-mechanical-interactions-pattern-embryo", "reader_count"=>101, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Student > Doctoral Student"=>3, "Researcher"=>25, "Student > Ph. D. Student"=>32, "Student > Postgraduate"=>2, "Student > Master"=>18, "Student > Bachelor"=>10, "Lecturer"=>1, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Student > Doctoral Student"=>3, "Researcher"=>25, "Student > Ph. D. Student"=>32, "Student > Postgraduate"=>2, "Student > Master"=>18, "Student > Bachelor"=>10, "Lecturer"=>1, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Engineering"=>5, "Biochemistry, Genetics and Molecular Biology"=>14, "Mathematics"=>1, "Medicine and Dentistry"=>7, "Agricultural and Biological Sciences"=>64, "Physics and Astronomy"=>6, "Psychology"=>1, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>5}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>7}, "Physics and Astronomy"=>{"Physics and Astronomy"=>6}, "Psychology"=>{"Psychology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>64}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>14}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Czech Republic"=>1, "United States"=>1, "Brazil"=>2, "France"=>1, "Portugal"=>1, "Germany"=>1}, "group_count"=>9}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/390251", "https://ndownloader.figshare.com/files/390272", "https://ndownloader.figshare.com/files/390294", "https://ndownloader.figshare.com/files/390318", "https://ndownloader.figshare.com/files/390335", "https://ndownloader.figshare.com/files/390353", "https://ndownloader.figshare.com/files/390370", "https://ndownloader.figshare.com/files/390383", "https://ndownloader.figshare.com/files/390397", "https://ndownloader.figshare.com/files/390418", "https://ndownloader.figshare.com/files/390451", "https://ndownloader.figshare.com/files/390618", "https://ndownloader.figshare.com/files/390661", "https://ndownloader.figshare.com/files/390715", "https://ndownloader.figshare.com/files/390779", "https://ndownloader.figshare.com/files/390837", "https://ndownloader.figshare.com/files/390925", "https://ndownloader.figshare.com/files/391007", "https://ndownloader.figshare.com/files/391097"], "description"=>"<div><p>Mammalian embryogenesis is a dynamic process involving gene expression and mechanical forces between proliferating cells. The exact nature of these interactions, which determine the lineage patterning of the trophectoderm and endoderm tissues occurring in a highly regulated manner at precise periods during the embryonic development, is an area of debate. We have developed a computational modeling framework for studying this process, by which the combined effects of mechanical and genetic interactions are analyzed within the context of proliferating cells. At a purely mechanical level, we demonstrate that the perpendicular alignment of the animal-vegetal (a-v) and embryonic-abembryonic (eb-ab) axes is a result of minimizing the total elastic conformational energy of the entire collection of cells, which are constrained by the zona pellucida. The coupling of gene expression with the mechanics of cell movement is important for formation of both the trophectoderm and the endoderm. In studying the formation of the trophectoderm, we contrast and compare quantitatively two hypotheses: (1) The position determines gene expression, and (2) the gene expression determines the position. Our model, which couples gene expression with mechanics, suggests that differential adhesion between different cell types is a critical determinant in the robust endoderm formation. In addition to differential adhesion, two different testable hypotheses emerge when considering endoderm formation: (1) A directional force acts on certain cells and moves them into forming the endoderm layer, which separates the blastocoel and the cells of the inner cell mass (ICM). In this case the blastocoel simply acts as a static boundary. (2) The blastocoel dynamically applies pressure upon the cells in contact with it, such that cell segregation in the presence of differential adhesion leads to the endoderm formation. To our knowledge, this is the first attempt to combine cell-based spatial mechanical simulations with genetic networks to explain mammalian embryogenesis. Such a framework provides the means to test hypotheses in a controlled <em>in silico</em> environment.</p></div>", "links"=>[], "tags"=>["simulating", "mammalian", "blastocyst", "molecular", "interactions", "embryo"], "article_id"=>137056, "categories"=>["Developmental Biology", "Cell Biology", "Biological Sciences", "Biophysics"], "users"=>["Pawel Krupinski", "Vijay Chickarmane", "Carsten Peterson"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1001128.s001", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s002", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s003", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s004", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s005", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s006", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s007", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s008", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s009", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s010", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s011", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s012", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s013", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s014", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s015", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s016", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s017", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s018", "https://dx.doi.org/10.1371/journal.pcbi.1001128.s019"], "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Simulating_the_Mammalian_Blastocyst_Molecular_and_Mechanical_Interactions_Pattern_the_Embryo/137056", "title"=>"Simulating the Mammalian Blastocyst - Molecular and Mechanical Interactions Pattern the Embryo", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-05-05 01:57:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/777002"], "description"=>"<p>The cells next to blastocoelic surface are pushed with forces proportional to their cross section surface area in direction perpendicular to the surface of the blastocoel. The bottom panes show the cross section through the cell mass to visualize the internal pattern. The GATA6 cells are blue and NANOG cells are red. (<b>a</b>) Initial state for the simulation. Both populations of cells are placed in the “salt and pepper” pattern. (<b>b</b>) Effect of random active movements alone. (<b>c</b>) Differential adhesion is able to form layer of GATA6 cells, but position of this layer is not stable with respect to blastocoel often resulting in ill placed endoderm. (<b>d</b>) Addition of stronger adhesion between NANOG cells and trophectoderm provides stabilizing signal which is able to place endoderm in correct position next to blastocoel.</p>", "links"=>[], "tags"=>["simulation", "endoderm", "interactions", "cells", "blastocoel", "movements"], "article_id"=>447367, "categories"=>["Developmental Biology", "Cell Biology", "Computational Biology", "Biophysics"], "users"=>["Pawel Krupinski", "Vijay Chickarmane", "Carsten Peterson"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1001128.g006", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Results_of_simulation_of_endoderm_formation_in_case_of_dynamic_interactions_of_cells_with_blastocoel_and_random_active_movements_of_cells_/447367", "title"=>"Results of simulation of endoderm formation in case of dynamic interactions of cells with blastocoel and random active movements of cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-05 02:02:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/776785"], "description"=>"<p>The core of the simplified genetic network used in the simulations of the both models is based on mutual repression of <i>Cdx2</i> and <i>Oct4</i> and auto-regulation of both transcription factors. In the position-based model (<b>a</b>) outer cells receive an additional signal enhancing the expression of <i>Cdx2</i>. In the polarity-based model (<b>d</b>) this signal is reduced. Instead subcellularly polarized <i>Cdx2</i> mRNA levels can be affected during asymmetric division. (<b>b</b>) Normalized histogram of CDX2 levels in inner and outer cells from the position-based model. One observes a clear shift of distributions towards lower concentrations in inner cells and higher concentrations in outer cells. Both distributions are well separated. (<b>c</b>) Example of CDX2 expression in inner and outer cells at the 32-cell stage in the position-based model. Inner cells (left pane) typically have lower expression of <i>Cdx2</i> resulting from higher expression of <i>Oct4</i>. Outer cells (right pane) on average have higher CDX2 expression. (<b>e</b>) In the polarity-based model the distributions of CDX2 in inner and outer cells are statistically distinct, but show larger number of low CDX2 level cells in the outer position. (<b>f</b>) The polarity-based model results in higher CDX2 expression in outer cells (right pane) than in inner cells (left pane) on average, but typically also yields more outliers.</p>", "links"=>[], "tags"=>["cdx2", "distributions", "embryo", "position-based", "polarity-based", "models"], "article_id"=>447151, "categories"=>["Developmental Biology", "Cell Biology", "Computational Biology", "Biophysics"], "users"=>["Pawel Krupinski", "Vijay Chickarmane", "Carsten Peterson"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1001128.g004", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Separation_of_CDX2_distributions_in_inner_and_outer_cells_with_respect_to_embryo_mass_in_the_position_based_a_b_c_and_polarity_based_models_d_e_f_respectively_/447151", "title"=>"Separation of CDX2 distributions in inner and outer cells, with respect to embryo mass, in the position-based (a, b, c) and polarity-based models (d, e, f) respectively.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-05 01:59:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/776554"], "description"=>"<p>Starting from fertilization (E0), after three rounds of cleavages (E1–E2.5), the blastomers undergo compaction and polarization (E3). Then the trophectoderm outer layer starts to separate from the inner cell mass (ICM) followed by the expansion of the blastocoel and the localization of the ICM to one part of the embryo (E3.5). After this stage the endoderm is formed as a layer separating epiblast from blastocoel (E4.5). After 4.5 embryonic days, the preimplantation embryo contains more than 100 cells.</p>", "links"=>[], "tags"=>["morphological", "lineage", "specification", "steps", "embryonic"], "article_id"=>446923, "categories"=>["Developmental Biology", "Cell Biology", "Computational Biology", "Biophysics"], "users"=>["Pawel Krupinski", "Vijay Chickarmane", "Carsten Peterson"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1001128.g001", "stats"=>{"downloads"=>0, "page_views"=>30, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_view_of_morphological_and_lineage_specification_steps_during_the_early_mouse_embryonic_development_/446923", "title"=>"Schematic view of morphological and lineage specification steps during the early mouse embryonic development.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-05 01:55:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/776899"], "description"=>"<p>(<b>a</b>) Schematic view of the late blastocyst. The differentiated trophectoderm (gray) and endoderm (blue) constrain the epiblast (red). (<b>b</b>) Initial configuration of 12 cells used in all presented simulations. The dotted shape shows the constraining surfaces of trophectoderm and blastocoel. In the middle pane, part of the cells were hidden to exhibit the interior of a cell cluster. The bottom pane shows the view from the blastocoel side. The NANOG and GATA6 cells are positioned in a salt-and-pepper pattern. The cells are allowed to take three rounds of division and move according to mechanical interactions within the constraining surroundings. The daughter cells are assumed to retain the identity (NANOG or GATA6) of their mother cells. In <b>c</b>, <b>d</b>, <b>e</b> and <b>f</b> the final state of the simulation is presented for different cases. (<b>c</b>) Adhesion coefficients are the same for both types of cells making them mechanically equivalent. Both NANOG and GATA6 cells are taking positions inside and outside in the cell cluster. (<b>d</b>) The NANOG cells have stronger self adhesion than GATA6 cells. The cross-adhesion between both cell types is small as compared to the average of the self adhesions. GATA6 cells form a layer of cells outside the NANOG cells next to the boundary. However, localization of this layer is not always close to the blastocoel boundary (middle and bottom panes). This suggest that differential adhesion and boundary constraints are enough to separate the two populations of cells, but are not sufficient to position GATA6 cells in the direct proximity of blastocoel. (<b>e</b>) Combination of differential adhesion and directional movement of GATA6 cells towards a signal from the blastocoel boundary is able to position all the GATA6 cells next to blastocoel boundary. (<b>f</b>) A directional signal alone is not sufficient to achieve the same effect.</p>", "links"=>[], "tags"=>["differential", "adhesion", "gata6", "nanog", "cells", "simulation", "static", "blastocoel", "providing", "positional"], "article_id"=>447260, "categories"=>["Developmental Biology", "Cell Biology", "Computational Biology", "Biophysics"], "users"=>["Pawel Krupinski", "Vijay Chickarmane", "Carsten Peterson"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1001128.g005", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_differential_adhesion_on_separation_of_GATA6_blue_and_NANOG_red_cells_during_simulation_with_static_blastocoel_providing_just_a_positional_restriction_for_blastomers_/447260", "title"=>"Effect of differential adhesion on separation of GATA6 (blue) and NANOG (red) cells during simulation with static blastocoel providing just a positional restriction for blastomers.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-05 02:01:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/776702"], "description"=>"<p>In the case of the two-cell embryo constrained by the elliptical pellucid zone (<b>a</b>) the positioning of the cells is consistently on opposite sides of the longest axis of ellipsoid by purely mechanical interactions and independent of the direction of the first division. The second polar body (a small cell with little genetic content positioned on the side of blastomers) is a product of the last meiotic division of the oocyte and marks polarization of the maternal mRNA. The blastocoel, which is modeled as a slowly expanding sphere inside of the embryo (<b>b</b>), positions itself preferentially at one end of the same axis. The frequency of this effect depends upon the elongation ratio of the pellucid zone and parameters of the model. However, it is consistently above 50% suggesting that orientation of the embryonic-abembryonic axis is mechanically biased as well.</p>", "links"=>[], "tags"=>["two-cell", "embryo", "symmetry", "axis", "embryonic-abembryonic", "ellipsoidal", "pellucid"], "article_id"=>447065, "categories"=>["Developmental Biology", "Cell Biology", "Computational Biology", "Biophysics"], "users"=>["Pawel Krupinski", "Vijay Chickarmane", "Carsten Peterson"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1001128.g003", "stats"=>{"downloads"=>2, "page_views"=>30, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Alignment_of_the_two_cell_embryo_symmetry_axis_and_embryonic_abembryonic_axis_with_the_long_axis_of_ellipsoidal_pellucid_zone_/447065", "title"=>"Alignment of the two-cell embryo symmetry axis and embryonic-abembryonic axis with the long axis of ellipsoidal pellucid zone.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-05 01:57:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/777081"], "description"=>"<p>The simulation starts from 12 to 14 ICM cells half of which are NANOG and another half GATA6. The cells are allowed to take three rounds of divisions and then their position (endoderm or epiblast) and gene expression (GATA6 or NANOG) is recorded. Number of mispositioned GATA6 (NANOG) cells relative to the total number of epiblast (endoderm) cells is presented for simulations of different separation mechanisms. Numbers for each model are averages of 6 simulations. In random model (first column) cells are labeled as GATA6 and NANOG but there is no difference in their adhesion strengths or directional movement. The differential adhesion model (second column) assume that GATA6 cells have slightly lower self-adhesion than NANOG cells. Cross-adhesion between both types is small as well. The directional movement model without differential adhesion (third column) features constant force drawing the GATA6 cells towards endoderm position. The lowest number of misplaced cells is obtained by combination of differential adhesion and directional signal (fourth column).</p>", "links"=>[], "tags"=>["mispositioned", "cells", "epiblast", "nanog"], "article_id"=>447452, "categories"=>["Developmental Biology", "Cell Biology", "Computational Biology", "Biophysics"], "users"=>["Pawel Krupinski", "Vijay Chickarmane", "Carsten Peterson"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1001128.t001", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_relative_number_of_mispositioned_cells_GATA6_cells_in_epiblast_and_NANOG_cells_in_endoderm_at_the_end_of_simulation_/447452", "title"=>"The relative number of mispositioned cells (GATA6 cells in epiblast and NANOG cells in endoderm) at the end of simulation.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-05-05 02:04:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/776634"], "description"=>"<p>(<b>a</b>) The number of inner cells in the simulations at the 32-cell stage (E3.5 in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1001128#pcbi-1001128-g001\" target=\"_blank\">Figure 1</a>) as a function of the blastomeres sizes. As the diameter of the cells increases, geometrical constraints force more cells to position themselves inside the cluster. (<b>b</b>) Average elastic deformation energy of the blastomeres (energy of the springs simulating elastic response of the cells) as a function of time in a typical simulation. The sharp peaks in energy correspond to cell division events. We observe a decline of the deformation energy perceived by blastomeres as the number of cells increase. Particularly large drop in energy takes place at 4- to 8-cell transition. The 32-cell stage shows the lowest deformation energy in this picture. Interestingly, these are the stages of development when morula compaction and blastocoel formation happen.</p>", "links"=>[], "tags"=>["geometrical"], "article_id"=>447009, "categories"=>["Developmental Biology", "Cell Biology", "Computational Biology", "Biophysics"], "users"=>["Pawel Krupinski", "Vijay Chickarmane", "Carsten Peterson"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1001128.g002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Examples_of_geometrical_and_mechanical_effects_in_embryogenesis_/447009", "title"=>"Examples of geometrical and mechanical effects in embryogenesis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-05 01:56:49"}

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Relative Metric

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