Cardiac Myocyte Diversity and a Fibroblast Network in the Junctional Region of the Zebrafish Heart Revealed by Transmission and Serial Block-Face Scanning Electron Microscopy

Handle URI:
http://hdl.handle.net/10754/325323
Title:
Cardiac Myocyte Diversity and a Fibroblast Network in the Junctional Region of the Zebrafish Heart Revealed by Transmission and Serial Block-Face Scanning Electron Microscopy
Authors:
Lafontant, Pascal J.; Behzad, Ali Reza; Brown, Evelyn; Landry, Paul; Hu, Norman; Burns, Alan R.
Abstract:
The zebrafish has emerged as an important model of heart development and regeneration. While the structural characteristics of the developing and adult zebrafish ventricle have been previously studied, little attention has been paid to the nature of the interface between the compact and spongy myocardium. Here we describe how these two distinct layers are structurally and functionally integrated. We demonstrate by transmission electron microscopy that this interface is complex and composed primarily of a junctional region occupied by collagen, as well as a population of fibroblasts that form a highly complex network. We also describe a continuum of uniquely flattened transitional cardiac myocytes that form a circumferential plate upon which the radially-oriented luminal trabeculae are anchored. In addition, we have uncovered within the transitional ring a subpopulation of markedly electron dense cardiac myocytes. At discrete intervals the transitional cardiac myocytes form contact bridges across the junctional space that are stabilized through localized desmosomes and fascia adherentes junctions with adjacent compact cardiac myocytes. Finally using serial block-face scanning electron microscopy, segmentation and volume reconstruction, we confirm the three-dimensional nature of the junctional region as well as the presence of the sheet-like fibroblast network. These ultrastructural studies demonstrate the previously unrecognized complexity with which the compact and spongy layers are structurally integrated, and provide a new basis for understanding development and regeneration in the zebrafish heart. © 2013 Lafontant et al.
KAUST Department:
Advanced Nanofabrication, Imaging and Characterization Core Lab
Citation:
Lafontant PJ, Behzad AR, Brown E, Landry P, Hu N, et al. (2013) Cardiac Myocyte Diversity and a Fibroblast Network in the Junctional Region of the Zebrafish Heart Revealed by Transmission and Serial Block-Face Scanning Electron Microscopy. PLoS ONE 8: e72388. doi:10.1371/journal.pone.0072388.
Publisher:
Public Library of Science
Journal:
PLoS ONE
Issue Date:
23-Aug-2013
DOI:
10.1371/journal.pone.0072388
PubMed ID:
24058412
PubMed Central ID:
PMC3751930
Type:
Article
ISSN:
19326203
Appears in Collections:
Articles; Advanced Nanofabrication, Imaging and Characterization Core Lab

Full metadata record

DC FieldValue Language
dc.contributor.authorLafontant, Pascal J.en
dc.contributor.authorBehzad, Ali Rezaen
dc.contributor.authorBrown, Evelynen
dc.contributor.authorLandry, Paulen
dc.contributor.authorHu, Normanen
dc.contributor.authorBurns, Alan R.en
dc.date.accessioned2014-08-27T09:46:57Zen
dc.date.available2014-08-27T09:46:57Zen
dc.date.issued2013-08-23en
dc.identifier.citationLafontant PJ, Behzad AR, Brown E, Landry P, Hu N, et al. (2013) Cardiac Myocyte Diversity and a Fibroblast Network in the Junctional Region of the Zebrafish Heart Revealed by Transmission and Serial Block-Face Scanning Electron Microscopy. PLoS ONE 8: e72388. doi:10.1371/journal.pone.0072388.en
dc.identifier.issn19326203en
dc.identifier.pmid24058412en
dc.identifier.doi10.1371/journal.pone.0072388en
dc.identifier.urihttp://hdl.handle.net/10754/325323en
dc.description.abstractThe zebrafish has emerged as an important model of heart development and regeneration. While the structural characteristics of the developing and adult zebrafish ventricle have been previously studied, little attention has been paid to the nature of the interface between the compact and spongy myocardium. Here we describe how these two distinct layers are structurally and functionally integrated. We demonstrate by transmission electron microscopy that this interface is complex and composed primarily of a junctional region occupied by collagen, as well as a population of fibroblasts that form a highly complex network. We also describe a continuum of uniquely flattened transitional cardiac myocytes that form a circumferential plate upon which the radially-oriented luminal trabeculae are anchored. In addition, we have uncovered within the transitional ring a subpopulation of markedly electron dense cardiac myocytes. At discrete intervals the transitional cardiac myocytes form contact bridges across the junctional space that are stabilized through localized desmosomes and fascia adherentes junctions with adjacent compact cardiac myocytes. Finally using serial block-face scanning electron microscopy, segmentation and volume reconstruction, we confirm the three-dimensional nature of the junctional region as well as the presence of the sheet-like fibroblast network. These ultrastructural studies demonstrate the previously unrecognized complexity with which the compact and spongy layers are structurally integrated, and provide a new basis for understanding development and regeneration in the zebrafish heart. © 2013 Lafontant et al.en
dc.language.isoenen
dc.publisherPublic Library of Scienceen
dc.rightsThis is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.en
dc.rightsArchived with thanks to PLoS ONEen
dc.subjectactinen
dc.subjectcardiac myosinen
dc.subjectcollagenen
dc.subjectactin filamenten
dc.subjectanimal cellen
dc.subjectanimal tissueen
dc.subjectbiodiversityen
dc.subjectcaveolaen
dc.subjectcell interactionen
dc.subjectcell junctionen
dc.subjectcell subpopulationen
dc.subjectcell ultrastructureen
dc.subjectcellular, subcellular and molecular biological phenomena and functionsen
dc.subjectdesmosomeen
dc.subjectelectron dense transitional cardiac myocyteen
dc.subjectelectron translucent transitional cardiac myocyteen
dc.subjectfasciaen
dc.subjectfibroblast networken
dc.subjectfilopodiumen
dc.subjectheart muscle cellen
dc.subjectimage reconstructionen
dc.subjectphenotypeen
dc.subjectscanning electron microscopyen
dc.subjectserial block face scanning electron microscopyen
dc.subjectstructure analysisen
dc.subjectthree dimensional imagingen
dc.subjecttransitional cell ringen
dc.subjecttransmission electron microscopyen
dc.subjectultrastructureen
dc.subjectzebra fishen
dc.subjectCollagenen
dc.subjectFibroblastsen
dc.subjectMicroscopy, Electron, Scanningen
dc.subjectMicroscopy, Electron, Transmissionen
dc.subjectMyocardiumen
dc.subjectMyocytes, Cardiacen
dc.subjectZebrafishen
dc.titleCardiac Myocyte Diversity and a Fibroblast Network in the Junctional Region of the Zebrafish Heart Revealed by Transmission and Serial Block-Face Scanning Electron Microscopyen
dc.typeArticleen
dc.contributor.departmentAdvanced Nanofabrication, Imaging and Characterization Core Laben
dc.identifier.journalPLoS ONEen
dc.identifier.pmcidPMC3751930en
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionDepartment of Biology, DePauw University, Greencastle, IN, United Statesen
dc.contributor.institutionCollege of Optometry, University of Houston, Houston, TX, United Statesen
dc.contributor.institutionDepartment of Pediatrics, University of Utah School of Medicine, Salt Lake City, UT, United Statesen
dc.contributor.institutionDepartment of Pediatrics, Baylor College of Medicine, Houston, TX, United Statesen
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorBehzad, Ali Rezaen
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