A Caudal Proliferating Growth Center Contributes to Both Poles of the Forming Heart Tube

Recent studies have shown that the primary heart tube continues to grow by addition of cells from the coelomic wall. This growth occurs concomitantly with embryonic folding and formation of the coelomic cavity, making early heart formation morphologically complex. A scarcity of data on localized gro...

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Bibliographic Details
Published in:Circulation research 2009-01, Vol.104 (2), p.179-188
Main Authors: van den Berg, Gert, Abu-Issa, Radwan, de Boer, Bouke A, Hutson, Mary R, de Boer, Piet A.J, Soufan, Alexandre T, Ruijter, Jan M, Kirby, Margaret L, van den Hoff, Maurice J.B, Moorman, Antoon F.M
Format: Article
Language:English
Subjects:
Animals
Biological and medical sciences
Bromodeoxyuridine - metabolism
Cell Cycle
Cell Differentiation
Cell Movement
Cell Proliferation
Chick Embryo
Fundamental and applied biological sciences. Psychology
Heart - embryology
Heart Ventricles - embryology
Homeodomain Proteins - metabolism
Image Processing, Computer-Assisted
Imaging, Three-Dimensional
Immunohistochemistry
LIM-Homeodomain Proteins
Mesoderm - cytology
Models, Anatomic
Models, Cardiovascular
Myocardium - cytology
Myocardium - metabolism
Organogenesis
Pericardium - embryology
Time Factors
Transcription Factors
Vertebrates: cardiovascular system
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Summary:Recent studies have shown that the primary heart tube continues to grow by addition of cells from the coelomic wall. This growth occurs concomitantly with embryonic folding and formation of the coelomic cavity, making early heart formation morphologically complex. A scarcity of data on localized growth parameters further hampers the understanding of cardiac growth. Therefore, we investigated local proliferation during early heart formation. Firstly, we determined the cell cycle length of primary myocardium of the early heart tube to be 5.5 days, showing that this myocardium is nonproliferating and implying that initial heart formation occurs solely by addition of cells. In line with this, we show that the heart tube rapidly lengthens at its inflow by differentiation of recently divided precursor cells. To track the origin of these cells, we made quantitative 3D reconstructions of proliferation in the forming heart tube and the mesoderm of its flanking coelomic walls. These reconstructions show a single, albeit bilateral, center of rapid proliferation in the caudomedial pericardial back wall. This center expresses Islet1. Cell tracing showed that cells from this caudal growth center, besides feeding into the venous pole of the heart, also move cranially via the dorsal pericardial mesoderm and differentiate into myocardium at the arterial pole. Inhibition of caudal proliferation impairs the formation of both the atria and the right ventricle. These data show how a proliferating growth center in the caudal coelomic wall elongates the heart tube at both its venous and arterial pole, providing a morphological mechanism for early heart formation.
ISSN:0009-7330
1524-4571
DOI:10.1161/CIRCRESAHA.108.185843