Visualising the Cardiovascular System of Embryos of Biomedical Model Organisms with High Resolution Episcopic Microscopy (HREM)

The article will briefly introduce the high-resolution episcopic microscopy (HREM) technique and will focus on its potential for researching cardiovascular development and remodelling in embryos of biomedical model organisms. It will demonstrate the capacity of HREM for analysing the cardiovascular system of normally developed and genetically or experimentally malformed zebrafish, frog, chick and mouse embryos in the context of the whole specimen and will exemplarily show the possibilities HREM offers for comprehensive visualisation of the vasculature of adult human skin. Finally, it will provide examples of the successful application of HREM for identifying cardiovascular malformations in genetically altered mouse embryos produced in the deciphering the mechanisms of developmental disorders (DMDD) program.

[1]  G. Müller,et al.  [3-dimensional reconstruction of histological serial sections using a computer]. , 1996, Wiener klinische Wochenschrift.

[2]  M. Bennett,et al.  Pan‐myocardial expression of Cre recombinase throughout mouse development , 2007, Genesis.

[3]  W. Weninger,et al.  Some Mice Feature 5th Pharyngeal Arch Arteries and Double-Lumen Aortic Arch Malformations , 2012, Cells Tissues Organs.

[4]  C. Miller,et al.  Multimodal optical microscopy methods reveal polyp tissue morphology and structure in Caribbean reef building corals. , 2014, Journal of visualized experiments : JoVE.

[5]  Gerd B Müller,et al.  MicroCT for molecular imaging: Quantitative visualization of complete three‐dimensional distributions of gene products in embryonic limbs , 2011, Developmental dynamics : an official publication of the American Association of Anatomists.

[6]  J. Schneider,et al.  Making the mouse embryo transparent: identifying developmental malformations using magnetic resonance imaging. , 2004, Birth defects research. Part C, Embryo today : reviews.

[7]  G. Andelfinger Genetic factors in congenital heart malformation , 2008, Clinical genetics.

[8]  R. Ramirez-Solis,et al.  Highly variable penetrance of abnormal phenotypes in embryonic lethal knockout mice , 2016, Mechanisms of Development.

[9]  E. Olson A decade of discoveries in cardiac biology , 2004, Nature Medicine.

[10]  W. Weninger,et al.  The dermal arteries in the cutaneous angiosome of the descending genicular artery , 2018, Journal of anatomy.

[11]  R. Henkelman,et al.  3D imaging, registration, and analysis of the early mouse embryonic vasculature , 2013, Developmental dynamics : an official publication of the American Association of Anatomists.

[12]  G. Johnson,et al.  High-resolution magnetic resonance histology of the embryonic and neonatal mouse: A 4D atlas and morphologic database , 2008, Proceedings of the National Academy of Sciences.

[13]  J. Hecksher-Sørensen,et al.  Optical Projection Tomography as a Tool for 3D Microscopy and Gene Expression Studies , 2002, Science.

[14]  Marc Modat,et al.  Magnetic resonance virtual histology for embryos: 3D atlases for automated high-throughput phenotyping , 2011, NeuroImage.

[15]  Jeffrey L. Wrana,et al.  Baf60c is essential for function of BAF chromatin remodelling complexes in heart development , 2004, Nature.

[16]  Constantine Butakoff,et al.  Quantification of the detailed cardiac left ventricular trabecular morphogenesis in the mouse embryo , 2018, Medical Image Anal..

[17]  R E Jacobs,et al.  Towards a microMRI atlas of mouse development. , 1999, Computerized medical imaging and graphics : the official journal of the Computerized Medical Imaging Society.

[18]  B. Metscher MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues , 2009, BMC Physiology.

[19]  R. Mark Henkelman,et al.  A novel 3D mouse embryo atlas based on micro-CT , 2012, Development.

[20]  D. Srivastava Making or Breaking the Heart: From Lineage Determination to Morphogenesis , 2006, Cell.

[21]  David L. Thomas,et al.  Cardiac phenotyping in ex vivo murine embryos using µMRI , 2009, NMR in biomedicine.

[22]  K. Kadler,et al.  Slow Stretching That Mimics Embryonic Growth Rate Stimulates Structural and Mechanical Development of Tendon-Like Tissue In Vitro , 2011, Developmental dynamics : an official publication of the American Association of Anatomists.

[23]  M. Reddington,et al.  Surface imaging microscopy, an automated method for visualizing whole embryo samples in three dimensions at high resolution , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[24]  J. Epstein,et al.  Rapid 3D Phenotyping of Cardiovascular Development in Mouse Embryos by Micro-CT With Iodine Staining , 2010, Circulation. Cardiovascular imaging.

[25]  W. Weninger,et al.  High-Resolution Episcopic Microscopy Data-Based Measurements of the Arteries of Mouse Embryos: Evaluation of Significance and Reproducibility under Routine Conditions , 2011, Cells Tissues Organs.

[26]  W. Weninger,et al.  High-Resolution Episcopic Microscopy (HREM): A Tool for Visualizing Skin Biopsies , 2014, Microscopy and Microanalysis.

[27]  J Streicher,et al.  External marker‐based automatic congruencing: A new method of 3D reconstruction from serial sections , 1997, The Anatomical record.

[28]  M. Labow,et al.  Noninvasive, in utero imaging of mouse embryonic heart development with 40-MHz echocardiography. , 1998, Circulation.

[29]  James Sharpe,et al.  Optical projection tomography as a new tool for studying embryo anatomy , 2003, Journal of anatomy.

[30]  K. Schughart,et al.  Computer-based three-dimensional visualization of developmental gene expression , 2000, Nature Genetics.

[31]  R. Jacobs,et al.  Three-dimensional digital mouse atlas using high-resolution MRI. , 2001, Developmental biology.

[32]  Wolfgang J Weninger,et al.  Embedding embryos for high-resolution episcopic microscopy (HREM). , 2012, Cold Spring Harbor protocols.

[33]  James C Moon,et al.  Morphogenesis of myocardial trabeculae in the mouse embryo , 2016, Journal of anatomy.

[34]  Wolfgang J Weninger,et al.  Imaging heart development using high-resolution episcopic microscopy , 2011, Current opinion in genetics & development.

[35]  Raksha Raghunathan,et al.  Optical coherence tomography for embryonic imaging: a review , 2016, Journal of biomedical optics.

[36]  Richard Baldock,et al.  Deciphering the Mechanisms of Developmental Disorders (DMDD): a new programme for phenotyping embryonic lethal mice , 2013, Disease Models & Mechanisms.

[37]  S. Neubauer,et al.  Identification of cardiac malformations in mice lacking Ptdsr using a novel high-throughput magnetic resonance imaging technique , 2004, BMC Developmental Biology.

[38]  Johannes Streicher,et al.  A new episcopic method for rapid 3-D reconstruction: applications in anatomy and embryology , 1998, Anatomy and Embryology.

[39]  H. Baldwin,et al.  Making a heart: advances in understanding the mechanisms of cardiac development , 2016, Current opinion in pediatrics.

[40]  S Lee Adamson,et al.  Embryonic and neonatal phenotyping of genetically engineered mice. , 2006, ILAR journal.

[41]  S. Neubauer,et al.  Rapid identification and 3D reconstruction of complex cardiac malformations in transgenic mouse embryos using fast gradient echo sequence magnetic resonance imaging. , 2003, Journal of molecular and cellular cardiology.

[42]  M. Brueckner,et al.  Genetics and Genomics of Congenital Heart Disease. , 2017, Circulation research.

[43]  R Mark Henkelman,et al.  Diffusible iodine‐based contrast‐enhanced computed tomography (diceCT): an emerging tool for rapid, high‐resolution, 3‐D imaging of metazoan soft tissues , 2016, Journal of anatomy.

[44]  O. Genin,et al.  Effects of storage conditions on hatchability, embryonic survival and cytoarchitectural properties in broiler from young and old flocks , 2018, Poultry science.

[45]  D. Herndon,et al.  High-resolution episcopic microscopy (HREM): a useful technique for research in wound care. , 2015, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[46]  Kirill V Larin,et al.  Dynamic imaging and quantitative analysis of cranial neural tube closure in the mouse embryo using optical coherence tomography. , 2017, Biomedical optics express.

[47]  W. Weninger,et al.  High-resolution Episcopic Microscopy (HREM) - Simple and Robust Protocols for Processing and Visualizing Organic Materials , 2017, Journal of visualized experiments : JoVE.

[48]  D. Srivastava,et al.  Genetic basis for congenital heart defects: current knowledge: a scientific statement from the American Heart Association Congenital Cardiac Defects Committee, Council on Cardiovascular Disease in the Young: endorsed by the American Academy of Pediatrics. , 2007, Circulation.

[49]  M. Capecchi,et al.  Virtual Histology of Transgenic Mouse Embryos for High-Throughput Phenotyping , 2006, PLoS genetics.

[50]  B. Metscher MicroCT for developmental biology: A versatile tool for high‐contrast 3D imaging at histological resolutions , 2009, Developmental dynamics : an official publication of the American Association of Anatomists.

[51]  Mark Henkelman,et al.  Angiopoietin-1 is essential in mouse vasculature during development and in response to injury. , 2011, The Journal of clinical investigation.

[52]  Diego Rasskin-Gutman,et al.  High-resolution episcopic microscopy: a rapid technique for high detailed 3D analysis of gene activity in the context of tissue architecture and morphology , 2006, Anatomy and Embryology.

[53]  A. Joyner,et al.  Three‐dimensional micro‐MRI analysis of cerebral artery development in mouse embryos , 2009, Magnetic resonance in medicine.

[54]  Jacqueline K. White,et al.  Placentation defects are highly prevalent in embryonic lethal mouse mutants , 2018, Nature.

[55]  Colin K. L. Phoon,et al.  Imaging Tools for the Developmental Biologist: Ultrasound Biomicroscopy of Mouse Embryonic Development , 2006, Pediatric Research.

[56]  Robert Wilson,et al.  Deciphering the mechanisms of developmental disorders: phenotype analysis of embryos from mutant mouse lines , 2015, Nucleic Acids Res..

[57]  Mary E. Dickinson,et al.  Three-dimensional microCT imaging of mouse development from early post-implantation to early postnatal stages , 2016, Developmental biology.

[58]  Orlando Aristizábal,et al.  Embryonic Heart Failure in NFATc1−/− Mice: Novel Mechanistic Insights From In Utero Ultrasound Biomicroscopy , 2004, Circulation research.

[59]  V. Tybulewicz,et al.  Genetic dissection of Down syndrome-associated congenital heart defects using a new mouse mapping panel , 2015, eLife.

[60]  W. Weninger,et al.  Generation of volume data by episcopic three-dimensional imaging of embryos. , 2012, Cold Spring Harbor protocols.

[61]  R. M. Henkelman,et al.  Mouse embryonic phenotyping by morphometric analysis of MR images , 2010, Physiological genomics.

[62]  W. Weninger,et al.  Measurements of the diameters of the great arteries and semi‐lunar valves of chick and mouse embryos , 2009, Journal of microscopy.

[63]  Chen Wu,et al.  Applicability, usability, and limitations of murine embryonic imaging with optical coherence tomography and optical projection tomography. , 2016, Biomedical optics express.

[64]  D. Adams,et al.  Phenotyping structural abnormalities in mouse embryos using high-resolution episcopic microscopy , 2014, Disease Models & Mechanisms.

[65]  Robert H. Anderson,et al.  Clarification of the identity of the mammalian fifth pharyngeal arch artery , 2013, Clinical anatomy.

[66]  W. Weninger,et al.  The dermal arteries of the human thumb pad , 2013, Journal of anatomy.

[67]  M. Ameloot,et al.  Imaging the zebrafish dentition: from traditional approaches to emerging technologies. , 2015, Zebrafish.

[68]  Honey B. Golden,et al.  In utero assessment of cardiovascular function in the embryonic mouse heart using high-resolution ultrasound biomicroscopy. , 2012, Methods in molecular biology.

[69]  D. Adams,et al.  Morphology, topology and dimensions of the heart and arteries of genetically normal and mutant mouse embryos at stages S21–S23 , 2017, Journal of anatomy.

[70]  Jean-François Colas,et al.  Live optical projection tomography , 2009, Organogenesis.

[71]  V. Hamburger,et al.  A series of normal stages in the development of the chick embryo. 1951. , 2012, Developmental dynamics : an official publication of the American Association of Anatomists.

[72]  T. Mohun,et al.  Clarifying the morphology of the ostium primum defect , 2015, Journal of anatomy.

[73]  M. Torres,et al.  Growth and Morphogenesis during Early Heart Development in Amniotes , 2017, Journal of cardiovascular development and disease.

[74]  Edward Z. Zhang,et al.  Dual modality optical coherence and whole-body photoacoustic tomography imaging of chick embryos in multiple development stages. , 2014, Biomedical optics express.

[75]  Robert H. Anderson,et al.  The independence of the infundibular building blocks in the setting of double-outlet right ventricle , 2017, Cardiology in the Young.

[76]  Philipp Schneider,et al.  Simultaneous visualisation of calcified bone microstructure and intracortical vasculature using synchrotron X-ray phase contrast-enhanced tomography , 2017, Scientific Reports.

[77]  Robert H. Anderson,et al.  The anatomy and development of normal and abnormal coronary arteries* , 2015, Cardiology in the Young.

[78]  Robert H. Anderson,et al.  Insights regarding the normal and abnormal formation of the atrial and ventricular septal structures , 2016, Clinical anatomy.

[79]  W. Weninger,et al.  Metric characterization of the aortic arch of early mouse fetuses and of a fetus featuring a double lumen aortic arch malformation. , 2013, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[80]  B R Smith,et al.  Magnetic resonance microscopy in cardiac development , 2001, Microscopy research and technique.

[81]  L. Kamolz,et al.  Simultaneous dermal matrix and autologous split‐thickness skin graft transplantation in a porcine wound model: A three‐dimensional histological analysis of revascularization , 2014, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[82]  W. Denk,et al.  Serial Block-Face Scanning Electron Microscopy to Reconstruct Three-Dimensional Tissue Nanostructure , 2004, PLoS biology.

[83]  Amy Slender,et al.  Down's syndrome-like cardiac developmental defects in embryos of the transchromosomic Tc1 mouse , 2010, Cardiovascular research.

[84]  S. Dunwoodie,et al.  Cited2 is required both for heart morphogenesis and establishment of the left-right axis in mouse development , 2005, Development.

[85]  Lei Xi,et al.  Label-free photoacoustic imaging of the cardio-cerebrovascular development in the embryonic zebrafish. , 2017, Biomedical optics express.

[86]  W. Weninger,et al.  Phenotyping transgenic embryos: a rapid 3-D screening method based on episcopic fluorescence image capturing , 2002, Nature Genetics.

[87]  W. Weninger,et al.  Visualizing Vertebrate Embryos with Episcopic 3D Imaging Techniques , 2009, TheScientificWorldJournal.

[88]  W. Weninger,et al.  Comparative study of regenerative effects of mesenchymal stem cells derived from placental amnion, chorion and umbilical cord on dermal wounds. , 2018, Placenta.

[89]  T. Starborg,et al.  Serial block face scanning electron microscopy in cell biology: Applications and technology. , 2019, Tissue & cell.

[90]  J. Bangham,et al.  A predictive model of asymmetric morphogenesis from 3D reconstructions of mouse heart looping dynamics , 2017, eLife.

[91]  S. Geyer,et al.  A Chick Embryo With a yet Unclassified Type of Cephalothoracopagus Malformation and a Hypothesis for Explaining its Genesis , 2013, Anatomia, histologia, embryologia.