Dynamic positional fate map of the primary heart-forming region
Abstract
Here we show the temporal–spatial orchestration of early heart morphogenesis at cellular level resolution, in vivo, and reconcile conflicting positional fate mapping data regarding the primary heart-forming field(s). We determined the positional fates of precardiac cells using a precision electroporation approach in combination with wide-field time-lapse microscopy in the quail embryo, a warm-blooded vertebrate (HH Stages 4 through 10). Contrary to previous studies, the results demonstrate the existence of a "continuous" circle-shaped heart field that spans the midline, appearing at HH Stage 4, which then expands to form a wide arc of progenitors at HH Stages 5–7. Our time-resolved image data show that a subset of these cardiac progenitor cells do not overlap with the expression of common cardiogenic factors, Nkx-2.5 and Bmp-2, until HH Stage 10, when a tubular heart has formed, calling into question when cardiac fate is specified and by which key factors. Sub-groups and anatomical bands (cohorts) of heart precursor cells dramatically change their relative positions in a process largely driven by endodermal folding and other large-scale tissue deformations. Thus, our novel dynamic positional fate maps resolve the origin of cardiac progenitor cells in amniotes. The data also establish the concept that tissue motion contributes significantly to cellular position fate — i.e., much of the cellular displacement that occurs during assembly of a midline heart tube (HH Stage 9) is NOT due to "migration" (autonomous motility), a commonly held belief. Computational analysis of our time-resolved data lays the foundation for more precise analyses of how cardiac gene regulatory networks correlate with early heart tissue morphogenesis in birds and mammals.
Additional Information
Copyright © 2009 Elsevier. Received 30 November 2007; revised 22 May 2009; accepted 26 May 2009. Available online 2 June 2009. We thank Dr. Charles Little (University of Kansas Medical Center) for the helpful and provocative discussions, and Drs. Olivier Pourquié and Bertrand Bénazéraf (Stowers Institute for Medical Research, Kansas City, MO) for their assistance with in situ hybridization analysis. This study was supported by an American Heart Association fellowship (0620105Z, CC), an award from the G. Harold and Leila Y. Mathers Charitable Foundation (BJR), an award from the University of Kansas Medical Center Research Institute (BJR) and a NIH award HL085694 (BJR). Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.ydbio.2009.05.570.Attached Files
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Additional details
- Eprint ID
- 15332
- DOI
- 10.1016/j.ydbio.2009.05.570
- Resolver ID
- CaltechAUTHORS:20090826-112854456
- 0620105Z
- American Heart Association
- G. Harold and Leila Y. Mathers Charitable Foundation
- University of Kansas Medical Center Research Institute
- HL085694
- NIH
- Created
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2009-09-11Created from EPrint's datestamp field
- Updated
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2021-11-08Created from EPrint's last_modified field