Integration of Nodal and BMP Signals in the Heart Requires FoxH1 to Create Left–Right Differences in Cell Migration Rates That Direct Cardiac Asymmetry
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{"title"=>"Integration of Nodal and BMP Signals in the Heart Requires FoxH1 to Create Left-Right Differences in Cell Migration Rates That Direct Cardiac Asymmetry", "type"=>"journal", "authors"=>[{"first_name"=>"Kari F.", "last_name"=>"Lenhart", "scopus_author_id"=>"24314616100"}, {"first_name"=>"Nathalia G.", "last_name"=>"Holtzman", "scopus_author_id"=>"25031348000"}, {"first_name"=>"Jessica R.", "last_name"=>"Williams", "scopus_author_id"=>"36520269400"}, {"first_name"=>"Rebecca D.", "last_name"=>"Burdine", "scopus_author_id"=>"6602681393"}], "year"=>2013, "source"=>"PLoS Genetics", "identifiers"=>{"pmid"=>"23358434", "sgr"=>"84873495850", "doi"=>"10.1371/journal.pgen.1003109", "scopus"=>"2-s2.0-84873495850", "pui"=>"368295345", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "issn"=>"15537390"}, "id"=>"fee56e20-c4df-30e0-bde0-6c0ab0b24d3e", "abstract"=>"Failure to properly establish the left-right (L/R) axis is a major cause of congenital heart defects in humans, but how L/R patterning of the embryo leads to asymmetric cardiac morphogenesis is still unclear. We find that asymmetric Nodal signaling on the left and Bmp signaling act in parallel to establish zebrafish cardiac laterality by modulating cell migration velocities across the L/R axis. Moreover, we demonstrate that Nodal plays the crucial role in generating asymmetry in the heart and that Bmp signaling via Bmp4 is dispensable in the presence of asymmetric Nodal signaling. In addition, we identify a previously unappreciated role for the Nodal-transcription factor FoxH1 in mediating cell responsiveness to Bmp, further linking the control of these two pathways in the heart. The interplay between these TGFβ pathways is complex, with Nodal signaling potentially acting to limit the response to Bmp pathway activation and the dosage of Bmp signals being critical to limit migration rates. These findings have implications for understanding the complex genetic interactions that lead to congenital heart disease in humans.", "link"=>"http://www.mendeley.com/research/integration-nodal-bmp-signals-heart-requires-foxh1-create-leftright-differences-cell-migration-rates", "reader_count"=>43, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>3, "Researcher"=>8, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>1, "Student > Master"=>7, "Student > Bachelor"=>7, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>3, "Researcher"=>8, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>1, "Student > Master"=>7, "Student > Bachelor"=>7, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>11, "Agricultural and Biological Sciences"=>25, "Medicine and Dentistry"=>3, "Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>25}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>11}, "Unspecified"=>{"Unspecified"=>3}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Argentina"=>1, "United States"=>1, "Chile"=>1}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/477989", "https://ndownloader.figshare.com/files/477993", "https://ndownloader.figshare.com/files/477996", "https://ndownloader.figshare.com/files/477998", "https://ndownloader.figshare.com/files/478004", "https://ndownloader.figshare.com/files/478011"], "description"=>"<div><p>Failure to properly establish the left–right (L/R) axis is a major cause of congenital heart defects in humans, but how L/R patterning of the embryo leads to asymmetric cardiac morphogenesis is still unclear. We find that asymmetric Nodal signaling on the left and Bmp signaling act in parallel to establish zebrafish cardiac laterality by modulating cell migration velocities across the L/R axis. Moreover, we demonstrate that Nodal plays the crucial role in generating asymmetry in the heart and that Bmp signaling via Bmp4 is dispensable in the presence of asymmetric Nodal signaling. In addition, we identify a previously unappreciated role for the Nodal-transcription factor FoxH1 in mediating cell responsiveness to Bmp, further linking the control of these two pathways in the heart. The interplay between these TGFβ pathways is complex, with Nodal signaling potentially acting to limit the response to Bmp pathway activation and the dosage of Bmp signals being critical to limit migration rates. These findings have implications for understanding the complex genetic interactions that lead to congenital heart disease in humans.</p> </div>", "links"=>[], "tags"=>["nodal", "bmp", "signals", "requires", "foxh1", "differences", "rates", "cardiac", "asymmetry"], "article_id"=>154200, "categories"=>["Developmental Biology"], "users"=>["Kari F. Lenhart", "Nathalia G. Holtzman", "Jessica R. Williams", "Rebecca D. Burdine"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003109.s001", "https://dx.doi.org/10.1371/journal.pgen.1003109.s002", "https://dx.doi.org/10.1371/journal.pgen.1003109.s003", "https://dx.doi.org/10.1371/journal.pgen.1003109.s004", "https://dx.doi.org/10.1371/journal.pgen.1003109.s005", "https://dx.doi.org/10.1371/journal.pgen.1003109.s006"], "stats"=>{"downloads"=>8, "page_views"=>70, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Integration_of_Nodal_and_BMP_Signals_in_the_Heart_Requires_FoxH1_to_Create_Left_Right_Differences_in_Cell_Migration_Rates_That_Direct_Cardiac_Asymmetry__/154200", "title"=>"Integration of Nodal and BMP Signals in the Heart Requires FoxH1 to Create Left–Right Differences in Cell Migration Rates That Direct Cardiac Asymmetry", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-01-24 01:10:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/500659"], "description"=>"<p>1: Nodal signaling to the myocardium through the transcription factor FoxH1 is required to asymmetrically increase cardiac migration rates specifically on the left of the cardiac cone. 2: The Bmp pathway is bilaterally activated in the endocardium but only effectively limits migration rates in the absence of strong inductive cues from Nodal signaling on the right of the cardiac cone. This leads to a non-cell autonomous decrease in myocardial migration rates on the right of the cone. 3: The Nodal pathway generally limits Bmp pathway activation in the heart, potentially through competition for access to proteins common to both pathways. 4: FoxH1 is also required in a Nodal-independent manner in the heart to mediate cardiac cell responsiveness to Bmp signals.</p>", "links"=>[], "tags"=>["opposing", "nodal", "bmp", "signaling", "asymmetric", "cardiac"], "article_id"=>171181, "categories"=>["Developmental Biology"], "users"=>["Kari F. Lenhart", "Nathalia G. Holtzman", "Jessica R. Williams", "Rebecca D. Burdine"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003109.g004", "stats"=>{"downloads"=>3, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Model_of_the_opposing_roles_for_Nodal_and_Bmp_signaling_during_asymmetric_cardiac_morphogenesis_/171181", "title"=>"Model of the opposing roles for Nodal and Bmp signaling during asymmetric cardiac morphogenesis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-01-24 00:19:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/500411"], "description"=>"<p>Embryos were scored for laterality of cardiac jogging between 24 and 30 hpf. A–C: Dorsal views of the heart at 24 hpf showing jogging laterality phenotypes by RNA in situ hybridizations using the <i>myl7</i> probe D: WT embryos exhibit primarily left-directed cardiac jog, as do <i>bmp4<sup>Y180</sup></i> mutants (I) lacking both maternal and zygotic <i>bmp4</i> (MZ<i>bmp4</i>). E,F: While WT embryos injected with <i>spaw</i> morpholino <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003109#pgen.1003109-Baker1\" target=\"_blank\">[9]</a> and late-zygotic (LZ) <i>oep</i> mutants display randomized jogging laterality, H: MZ<i>bmp4<sup>Y180</sup></i> mutants injected with <i>spaw</i> morpholino lack significant jogging asymmetries. I: Loss of <i>bmp4</i> alone does not affect jogging laterality and resembles WT (D) suggesting Bmp is dispensable for correct jogging when asymmetric Nodal signals are present. J: Jogging laterality in the absence of Spaw is highly sensitive to the level of Bmp4 present, as loss of a single functional copy of <i>bmp4</i> in embryos deficient for Spaw is sufficient to result in predominantly midline jogging phenotypes. K: <i>midway</i> mutants homozygous for a nonsense mutation in the Nodal transcription factor FoxH1 display jogging phenotypes similar to what is observed in embryos lacking both Nodal and Bmp signaling. We note that a discrepancy exists between the randomized jogging of <i>spaw</i> morphants and the predominantly midline jogging of SB-505124-treated embryos (G). As described in more detail in the discussion, these phenotypic differences are likely due to the more global inhibition of TGFβ signaling achieved through drug treatment and we believe reflects the involvement of a second, as yet unidentified, TGFβ ligand in establishing jogging laterality. MO: morpholino. Het: Heterozygotes. Mut: Mutant. Asterisk: jogging data presented supplementary to <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003109#pgen.1003109-Baker1\" target=\"_blank\">[9]</a>.</p>", "links"=>[], "tags"=>["laterality"], "article_id"=>170939, "categories"=>["Developmental Biology"], "users"=>["Kari F. Lenhart", "Nathalia G. Holtzman", "Jessica R. Williams", "Rebecca D. Burdine"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003109.g002", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Jogging_laterality_phenotypes_/170939", "title"=>"Jogging laterality phenotypes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-01-24 00:15:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/500244"], "description"=>"<p>A–G: First frame of time lapse movies taken from a dorsal view of <i>Tg(myl7:eGFP)</i> embryos overlaid with cell trajectories. Yellow tracks: left cells. White tracks: center cells. Red tracks: right cells. A: All cells exhibit trajectories directed toward the anterior and left in WT embryos. B: Bilateral expression of <i>spaw</i> in <i>ntl</i> morphants leads to loss of L/R asymmetry in cardiac cell migrations. C–G: L/R directionality is also absent in embryos C: lacking the Nodal ligand <i>spaw</i>; D: treated with the SB-505124 Nodal inhibitor drug E: lacking <i>spaw</i> and one functional copy of <i>bmp4</i>; F: injected with both <i>bmp4</i> and <i>spaw</i> morpholinos; and G: homozygous <i>midway</i> mutants. H: Numbers within each bar indicate the number of cells tracked on the left, center and right for all embryos of each genotype. The number of embryos utilized in analysis is indicated (n = ) for each genotype. WT embryos exhibit differences in average cell velocities along the L/R axis, with left cells migrating significantly faster than right cells. Bilateral exposure to Spaw leads to significant increases in average velocities in left and right cells of <i>ntl</i> morphants, while loss of Spaw and global inhibition of Nodal signaling through drug treatment results in significantly decreased rates of migration. In embryos with diminished Bmp signaling along with loss of Spaw, average cell velocities are significantly increased compared with loss of Spaw alone. Error bars in H indicate standard error of the mean. MO: morpholino. Het: Heterozygotes.</p>", "links"=>[], "tags"=>["velocities", "migrating", "cells", "cardiac"], "article_id"=>170764, "categories"=>["Developmental Biology"], "users"=>["Kari F. Lenhart", "Nathalia G. Holtzman", "Jessica R. Williams", "Rebecca D. Burdine"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003109.g001", "stats"=>{"downloads"=>2, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Trajectories_and_average_velocities_of_migrating_cells_within_the_cardiac_cone_/170764", "title"=>"Trajectories and average velocities of migrating cells within the cardiac cone.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-01-24 00:12:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/500521"], "description"=>"<p>Immunofluorescence images for activated Smad1/5/8 (A,B,D,E,G,H,J,K,P–P″) in <i>Tg(myl7:eGFP)</i> embryos (myocardial GFP in B,E,H,K,P–P′″) or in <i>Tg</i>(<i>kdrl</i>:<i>egfp</i>) embryos (endocardial GFP in Q–Q″). C,F,I,L: Schematics of B, E, H and I using IMARIS surface tool. GFP signal in green; p-Smad1/5/8 positive cells are labeled according to intensity using the red (low) to yellow (high) spectrum ranging from an intensity value of 35–65, respectively. All images are dorsal views except for optical cross sections generated in IMARIS along the anterior/posterior axis (P′, Q′) or across the myocardium (P″, Q″). A–C: p-Smad1/5/8 fluorescence intensity is higher on the left of the WT cardiac cone (n = 6). D–F: p-Smad1/5/8 fluorescence intensity on both sides of the cone in <i>spaw</i> morphants is similar to that observed in cells on the left in WT (n = 6). G–I: <i>midway</i> mutants exhibit reduced fluorescence intensities and numbers of p-Smad1/5/8 positive cells, while p-Smad levels elsewhere in the embryo are seemingly unaffected (data not shown, n = 3). J–L: <i>bmp4</i> and <i>spaw</i> double morphants exhibit diminished p-Smad1/5/8 compared with WT (n = 6) but not as severe as observed in <i>midway</i> mutants. M: Comparison of the average fluorescence intensities of p-Smad1/5/8 positive cells on the left and right of the cardiac cone. N: Comparison of the average number of p-Smad1/5/8 positive cells on the left and right of the cardiac cone. O: Comparison of the average number of p-Smad1/5/8 positive cells in the entire cardiac field. P–P″: The myocardium shows little to no overlap of p-Smad1/5/8 positive cells (red) with the green of the myocardium. Q–Q″: Conversely, p-Smad1/5/8 (red) is observed to colocalize with the GFP positive endothelial cells in <i>Tg</i>(<i>kdrl</i>:<i>egfp</i>), indicated with arrowheads in Q′ and Q″, indicating that Bmp signals more strongly to the endocardium. Error bars indicate standard error of the mean. L: Low. H: High. MO: Morpholino. Het: heterozygote.</p>", "links"=>[], "tags"=>["bmp", "pathway", "fluorescence"], "article_id"=>171041, "categories"=>["Developmental Biology"], "users"=>["Kari F. Lenhart", "Nathalia G. Holtzman", "Jessica R. Williams", "Rebecca D. Burdine"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003109.g003", "stats"=>{"downloads"=>3, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Quantitation_of_Bmp_pathway_activity_by_average_fluorescence_intensity_and_number_of_p_Smad1_5_8_positive_cells_/171041", "title"=>"Quantitation of Bmp pathway activity by average fluorescence intensity and number of p-Smad1/5/8 positive cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-01-24 00:17:21"}

PMC Usage Stats | Further Information

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Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences", "average_usage"=>[269, 466, 588, 697, 800, 896, 988, 1076, 1165, 1254, 1340, 1417]}, {"subject_area"=>"/Biology and life sciences/Developmental biology", "average_usage"=>[275, 472, 605, 720, 822, 921, 1013, 1106, 1200, 1289, 1378, 1459, 1531]}, {"subject_area"=>"/Biology and life sciences/Organisms", "average_usage"=>[281, 484, 611, 728, 835, 934, 1030, 1123, 1214, 1299, 1383, 1464]}, {"subject_area"=>"/Medicine and health sciences", "average_usage"=>[264, 460, 584, 692, 794, 887, 978, 1067, 1154, 1241, 1328, 1408, 1474]}, {"subject_area"=>"/Medicine and health sciences/Anatomy and physiology", "average_usage"=>[253, 430]}, {"subject_area"=>"/Physical sciences", "average_usage"=>[254, 431, 547, 651, 748, 842, 932, 1017, 1098, 1178, 1259, 1336, 1404]}]}
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