Identifying the Evolutionary Building Blocks of the Cardiac Conduction System
Publication Date
September 11, 2012
Journal
PLOS ONE
Authors
Bjarke Jensen, Bastiaan J. D. Boukens, Alex V. Postma, Quinn D. Gunst, et al
Volume
7
Issue
9
Pages
e44231
DOI
https://dx.plos.org/10.1371/journal.pone.0044231
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0044231
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/22984480
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3439475
Europe PMC
http://europepmc.org/abstract/MED/22984480
Web of Science
000308638700050
Scopus
84866286055
Mendeley
http://www.mendeley.com/research/identifying-evolutionary-building-blocks-cardiac-conduction-system
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Mendeley | Further Information

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CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/308944", "https://ndownloader.figshare.com/files/309019", "https://ndownloader.figshare.com/files/309085", "https://ndownloader.figshare.com/files/309766", "https://ndownloader.figshare.com/files/309825"], "description"=>"<div><p>The endothermic state of mammals and birds requires high heart rates to accommodate the high rates of oxygen consumption. These high heart rates are driven by very similar conduction systems consisting of an atrioventricular node that slows the electrical impulse and a His-Purkinje system that efficiently activates the ventricular chambers. While ectothermic vertebrates have similar contraction patterns, they do not possess anatomical evidence for a conduction system. This lack amongst extant ectotherms is surprising because mammals and birds evolved independently from reptile-like ancestors. Using conserved genetic markers, we found that the conduction system design of lizard (<em>Anolis carolinensis</em> and <em>A. sagrei</em>), frog (<em>Xenopus laevis</em>) and zebrafish (<em>Danio rerio</em>) adults is strikingly similar to that of embryos of mammals (mouse <em>Mus musculus</em>, and man) and chicken (<em>Gallus gallus</em>). Thus, in ectothermic adults, the slow conducting atrioventricular canal muscle is present, no fibrous insulating plane is formed, and the spongy ventricle serves the dual purpose of conduction and contraction. Optical mapping showed base-to-apex activation of the ventricles of the ectothermic animals, similar to the activation pattern of mammalian and avian embryonic ventricles and to the His-Purkinje systems of the formed hearts. Mammalian and avian ventricles uniquely develop thick compact walls and septum and, hence, form a discrete ventricular conduction system from the embryonic spongy ventricle. Our study uncovers the evolutionary building plan of heart and indicates that the building blocks of the conduction system of adult ectothermic vertebrates and embryos of endotherms are similar.</p> </div>", "links"=>[], "tags"=>["identifying", "evolutionary", "blocks", "cardiac", "conduction"], "article_id"=>120967, "categories"=>["Physiology", "Developmental Biology"], "users"=>["Bjarke Jensen", "Bastiaan J. D. Boukens", "Alex V. Postma", "Quinn D. Gunst", "Maurice J. B. van den Hoff", "Antoon F. M. Moorman", "Tobias Wang", "Vincent M. Christoffels"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0044231.s001", "https://dx.doi.org/10.1371/journal.pone.0044231.s002", "https://dx.doi.org/10.1371/journal.pone.0044231.s003", "https://dx.doi.org/10.1371/journal.pone.0044231.s004", "https://dx.doi.org/10.1371/journal.pone.0044231.s005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Identifying_the_Evolutionary_Building_Blocks_of_the_Cardiac_Conduction_System/120967", "title"=>"Identifying the Evolutionary Building Blocks of the Cardiac Conduction System", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-09-11 00:16:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/579350"], "description"=>"<p>(A) Anatomical works concluded that the specialized cardiac conduction system evolved independently in mammals and birds because similar structures could not be found in ectothermic vertebrates. (B) We are testing the hypothesis that a primordial version of the specialized cardiac conduction system can be found in ectothermic vertebrates.</p>", "links"=>[], "tags"=>["physiology", "developmental biology"], "article_id"=>249842, "categories"=>["Physiology", "Developmental Biology"], "users"=>["Bjarke Jensen", "Bastiaan J. D. Boukens", "Alex V. Postma", "Quinn D. Gunst", "Maurice J. B. van den Hoff", "Antoon F. M. Moorman", "Tobias Wang", "Vincent M. Christoffels"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0044231.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Background_and_hypothesis_/249842", "title"=>"Background and hypothesis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-11 02:44:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/579490"], "description"=>"<p>Picro-sirius red stain for collagen (red) on 10 µm sections of hearts of adult ectotherms showing the atrioventricular canal to be in full communication (+) with the ventricle. l(r)a, left(right) atrium.</p>", "links"=>[], "tags"=>["atrioventricular", "junction", "ectotherms", "interrupted", "insulating"], "article_id"=>249980, "categories"=>["Physiology", "Developmental Biology"], "users"=>["Bjarke Jensen", "Bastiaan J. D. Boukens", "Alex V. Postma", "Quinn D. Gunst", "Maurice J. B. van den Hoff", "Antoon F. M. Moorman", "Tobias Wang", "Vincent M. Christoffels"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0044231.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_atrioventricular_junction_in_ectotherms_is_not_interrupted_by_an_insulating_plane_/249980", "title"=>"The atrioventricular junction in ectotherms is not interrupted by an insulating plane.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-11 02:46:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/579706"], "description"=>"<p>Numbers in the phylogenetic tree indicate time in millions of years since major splits in tetrapod evolution. (A–E) The hearts of mature ectotherms (blue) and embryonic endotherms (red) maintain complete muscular connection in the atrioventricular canal (avc). (F–J) Markers of fast propagating chamber myocardium (<i>Nppa</i> and <i>Gja5</i>) are absent from the atrioventricular canal (arrowheads). Note that the specimen in H is contracted, obscuring the spongy design otherwise visible. Scale bars in (A–E), 300 µm; (F–J), 100 µm.</p>", "links"=>[], "tags"=>["phenotype", "propagating", "atrioventricular", "canal", "evolutionary"], "article_id"=>250191, "categories"=>["Physiology", "Developmental Biology"], "users"=>["Bjarke Jensen", "Bastiaan J. D. Boukens", "Alex V. Postma", "Quinn D. Gunst", "Maurice J. B. van den Hoff", "Antoon F. M. Moorman", "Tobias Wang", "Vincent M. Christoffels"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0044231.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_phenotype_of_the_slow_propagating_atrioventricular_canal_is_evolutionary_conserved_/250191", "title"=>"The phenotype of the slow propagating atrioventricular canal is evolutionary conserved.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-11 00:03:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/579946"], "description"=>"<p>(A–D) Stage 17/19 <i>Anolis</i> hearts show complementary expressions of <i>Bmp2</i> and <i>Tbx3</i> to <i>Gja5</i> in the developing myocardial atrioventricular canal (arrowheads). (E–H) The developmental expression of <i>Bmp2</i>, <i>Tbx3</i> and <i>Gja5</i> is maintained in the mature myocardial atrioventricular canal (left side shown). la, left atrium; ra, right atrium; ven, ventricle. Scale bars are 100 µm.</p>", "links"=>[], "tags"=>["programme", "amniotes", "maintained", "mature"], "article_id"=>250433, "categories"=>["Physiology", "Developmental Biology"], "users"=>["Bjarke Jensen", "Bastiaan J. D. Boukens", "Alex V. Postma", "Quinn D. Gunst", "Maurice J. B. van den Hoff", "Antoon F. M. Moorman", "Tobias Wang", "Vincent M. Christoffels"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0044231.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_developmental_gene_programme_of_amniotes_is_maintained_in_the_mature_heart_of_Anolis_/250433", "title"=>"The developmental gene programme of amniotes is maintained in the mature heart of <i>Anolis</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-11 00:07:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/580139"], "description"=>"<p>Reconstructions are based on in-situ hybridizations of serial sections, except in human (based on immunohistochemistry, modified from <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0044231#pone.0044231-Sizarov1\" target=\"_blank\">[57]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0044231#pone.0044231-Sizarov2\" target=\"_blank\">[58]</a>). The <i>Tbx3</i> domains are strikingly similar in the early phases of chamber formation (upper panel). The <i>Tbx3</i> expression of the <i>Anolis</i> ventricle is very similar to that associated with ventricular septation (black arrows) in the other amniotes (lower panel).</p>", "links"=>[], "tags"=>["reconstructions", "amniotes"], "article_id"=>250631, "categories"=>["Physiology", "Developmental Biology"], "users"=>["Bjarke Jensen", "Bastiaan J. D. Boukens", "Alex V. Postma", "Quinn D. Gunst", "Maurice J. B. van den Hoff", "Antoon F. M. Moorman", "Tobias Wang", "Vincent M. Christoffels"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0044231.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Three_dimensional_reconstructions_of_Tbx3_yellow_expression_in_amniotes_reveal_a_shared_design_/250631", "title"=>"Three-dimensional reconstructions of <i>Tbx3</i> (yellow) expression in amniotes reveal a shared design.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-11 00:10:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/580273"], "description"=>"<p><i>Nppa</i> is expressed in a complementary pattern. a, atrium; ven, ventricle.</p>", "links"=>[], "tags"=>["atrioventricular", "canal", "formed", "zebrafish"], "article_id"=>250766, "categories"=>["Physiology", "Developmental Biology"], "users"=>["Bjarke Jensen", "Bastiaan J. D. Boukens", "Alex V. Postma", "Quinn D. Gunst", "Maurice J. B. van den Hoff", "Antoon F. M. Moorman", "Tobias Wang", "Vincent M. Christoffels"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0044231.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tbx2_expression_in_the_atrioventricular_canal_of_the_formed_heart_of_the_zebrafish_in_situ_hybridization_/250766", "title"=>"<i>Tbx2</i> expression in the atrioventricular canal of the formed heart of the zebrafish (<i>in-situ</i> hybridization).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-11 00:12:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/580399"], "description"=>"<p><i>Tbx2</i> is expressed in the atrioventricular canal and base of the myocardial outflow tract and complementary to <i>Nppa</i>, marker of chamber myocardium. In ectotherms primitive myocardium (p), remnants of the embryonic heart tube, can be recognized by its smooth surface as opposed to the trabeculated myocardium (t) formed during chamber formation. The primitive myocardium of the ventricular base of st 48 <i>Xenopus</i> hearts already has the adult configuration. The trabecular component is far from fully developed. a, atrium; avc, atrioventricular canal; c, conus arteriosus (myocardial outflow tract); p, primitive (atrabecular) myocardium; t, ventricular trabeculated myocardium; ven, ventricle.</p>", "links"=>[], "tags"=>["physiology", "developmental biology"], "article_id"=>250890, "categories"=>["Physiology", "Developmental Biology"], "users"=>["Bjarke Jensen", "Bastiaan J. D. Boukens", "Alex V. Postma", "Quinn D. Gunst", "Maurice J. B. van den Hoff", "Antoon F. M. Moorman", "Tobias Wang", "Vincent M. Christoffels"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0044231.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tbx2_expression_in_situ_hybridization_in_developing_Xenopus_st_48_/250890", "title"=>"<i>Tbx2</i> expression (in-situ hybridization) in developing <i>Xenopus</i> (st 48).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-11 00:14:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/580548"], "description"=>"<p>The development of the compact walls (<i>Nppa</i> and <i>Gja5</i> negative) of mammals and birds leaves the trabeculated myocardium (<i>Nppa</i> and <i>Gja5</i> positive) as a thin inner lining of the ventricular lumina in the fully formed hearts. <i>Nppa</i> is not expressed birds<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0044231#pone.0044231-Houweling2\" target=\"_blank\">[36]</a>. Scalebars, 100 µm. ivs, interventricular septum; lv, left ventricle.</p>", "links"=>[], "tags"=>["compact"], "article_id"=>251042, "categories"=>["Physiology", "Developmental Biology"], "users"=>["Bjarke Jensen", "Bastiaan J. D. Boukens", "Alex V. Postma", "Quinn D. Gunst", "Maurice J. B. van den Hoff", "Antoon F. M. Moorman", "Tobias Wang", "Vincent M. Christoffels"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0044231.g008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Development_of_compact_walls_/251042", "title"=>"Development of compact walls.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-11 00:17:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/580735"], "description"=>"<p>(A, D, G, J) Markers of fast propagating myocardium (<i>Nppa</i> and <i>Gja5</i>) are homogenously expressed in the ventricular trabeculated myocardium from base to apex (ap). (B, E, H) Ventricular activation occurs from base to apex. Early activation is red, late activation is blue. Note that the time-colour coding in panel E is different from that in panels B and H. (K) In species with thick compact myocardium, surface breakthrough of the activation front is earlier in the apical region than in the base. (C, F, I, L) Graphs show the average activation time of the apex and base and the total ventricular activation time. Note that in zebrafish, Xenopus and Anolis, the ventricular base is activated earlier than the apex whereas in mice the ventricular base is activated later than the apex (* Significantly different (one-way ANOVA P<0.05)). n is 3, 6, 9 and 2, respectively. Scale bars in (B, E, H, K) indicate respectively 0.2, 1, 0.5 and 0.1 millimetre. avc, atrioventricular canal; ven, ventricle.</p>", "links"=>[], "tags"=>["ventricles", "activated"], "article_id"=>251230, "categories"=>["Physiology", "Developmental Biology"], "users"=>["Bjarke Jensen", "Bastiaan J. D. Boukens", "Alex V. Postma", "Quinn D. Gunst", "Maurice J. B. van den Hoff", "Antoon F. M. Moorman", "Tobias Wang", "Vincent M. Christoffels"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0044231.g009"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Trabeculated_ventricles_are_activated_from_base_to_apex_/251230", "title"=>"Trabeculated ventricles are activated from base to apex.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-11 00:20:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/580916"], "description"=>"<p>(A–C) The trabecular myocardium gives rise to the His-Purkinje system in mammals and birds and remains activated from base to apex. (C) On the epicardial surface of septated and thick-walled ventricles, as in the formed hearts of mammals and birds, activation is seen to occur from apex to base and the luminal base-to-apex activation is obscured.</p>", "links"=>[], "tags"=>["trabecular", "myocardium", "activated", "apex"], "article_id"=>251404, "categories"=>["Physiology", "Developmental Biology"], "users"=>["Bjarke Jensen", "Bastiaan J. D. Boukens", "Alex V. Postma", "Quinn D. Gunst", "Maurice J. B. van den Hoff", "Antoon F. M. Moorman", "Tobias Wang", "Vincent M. Christoffels"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0044231.g010"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_trabecular_myocardium_is_activated_from_base_to_apex_in_all_vertebrates_/251404", "title"=>"The trabecular myocardium is activated from base to apex in all vertebrates.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-11 00:23:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/581036"], "description"=>"<p>In the formed hearts of mammals and birds, epicardial ventricular activation is from apex to base.</p>1<p>Left-to-right activation is only reported in broad-hearted turtles.</p>2<p>Arbel et al (1977) using ventrally placed electrodes find that as the apex becomes activated the current spreads towards the base. As they could not evaluate if the base was activated earlier, and since the zebrafish outflow region is indeed activated later than the apex their results may be in agreement with the present study.</p>*<p>Species where first point of activation definitely was neither base nor apex. From <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0044231#pone.0044231-Mullen1\" target=\"_blank\">[33]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0044231#pone.0044231-Arbel1\" target=\"_blank\">[59]</a>–<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0044231#pone.0044231-ZhaoXian1\" target=\"_blank\">[81]</a>.</p>", "links"=>[], "tags"=>["activation", "ectothermic", "vertebrates", "investigated", "optical", "markers"], "article_id"=>251523, "categories"=>["Physiology", "Developmental Biology"], "users"=>["Bjarke Jensen", "Bastiaan J. D. Boukens", "Alex V. Postma", "Quinn D. Gunst", "Maurice J. B. van den Hoff", "Antoon F. M. Moorman", "Tobias Wang", "Vincent M. Christoffels"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0044231.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ventricular_activation_pattern_in_ectothermic_vertebrates_investigated_by_optical_mapping_OP_ECG_ECG_electrodes_E_or_markers_M_/251523", "title"=>"Ventricular activation pattern in ectothermic vertebrates investigated by optical mapping(<sup>OP</sup>), ECG(<sup>ECG</sup>), electrodes(<sup>E</sup>) or markers (<sup>M</sup>).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-09-11 00:25:23"}

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