Gastrulation is arguably the most important process that occurs during embryogenesis of higher animals. This all-important process results in the formation of a third primary cell layer, from the ancient two-layered body plan of lower animals — higher animals being those species more advanced than the flat worms. The overwhelming preponderance of our present understanding is derived from interpretation of static images — despite the fact that gastrulation is a period of vast morphological change. However, any valid understanding of early embryogenesis, in warm-blooded animals, must take into account the continuous motion of cells and more to the point, tissues. [Much is known about gastrulation in cold-blooded animal embryos].
Not long after gastrulation begins, bird and mouse embryos commence vasculogenesis — the formation of the first blood vessels. The embryo continues vasculogenesis for 12-14 hours as gastrulation continues to form new mesoderm — the tissue from which blood vessels are made. The process of forming an interconnected network of tubes occurs within a thin layer of fibronectin-containing extracellular matrix. What has been largely ignored is that primordial vascular cells, forming a network, do so in an environment that is always in motion. In short, the biophysical and biomechanical mechanisms that impact vasculogenesis are not understood.
From a mechanics perspective, one of the more difficult challenges in studying vascular pattern formation in vivo is separating cell-autonomous displacement (i.e. motility) from large-scale (tissue-level) morphogenetic displacements. We recently developed a computational tissue-fate mapping method based on particle image velocimetry (PIV). This method allows the displacements of virtual material particles in the embryo to be tracked automatically, using the extracellular matrix substrate fibronectin as a passive in situ mesodermal tissue marker.
Our recent PIV data demonstrate that the cell-autonomous component or “local” cell motility can be separated from displacements caused by large-scale (tissue-level) morphogenetic deformations. To our knowledge, these are the first data that directly show relative motion between gastrulating mesodermal cells, the extracellular matrix and primordial vessel cells. The results of computational tissue-fate mapping experiments reveal regional patterns of mesodermal plate motion relative to the vertebral axis (midline); and also a significant amount of tissue rotation toward the midline. Our data suggest that the motion of cells may be highly correlated with the direction of maximum principal stretch in the lateral mesoderm. We speculate that tissue-level deformations may align extracellular matrix fibrils, specifically fibronectin, and that these "tracks", may provide directionality cues necessary for proper mesoderm formation and vascular patterning.
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