Dynamic analysis of vascular morphogenesis using transgenic quail embryos.

Yuki Sato, Greg Poynter, David Huss, Michael B. Filla, Andras Czirok, Brenda J. Rongish, Charles D. Little, Scott E. Fraser, Rusty Lansford

Research output: Contribution to journalArticle

Abstract

One of the least understood and most central questions confronting biologists is how initially simple clusters or sheet-like cell collectives can assemble into highly complex three-dimensional functional tissues and organs. Due to the limits of oxygen diffusion, blood vessels are an essential and ubiquitous presence in all amniote tissues and organs. Vasculogenesis, the de novo self-assembly of endothelial cell (EC) precursors into endothelial tubes, is the first step in blood vessel formation. Static imaging and in vitro models are wholly inadequate to capture many aspects of vascular pattern formation in vivo, because vasculogenesis involves dynamic changes of the endothelial cells and of the forming blood vessels, in an embryo that is changing size and shape. We have generated Tie1 transgenic quail lines Tg(tie1:H2B-eYFP) that express H2B-eYFP in all of their endothelial cells which permit investigations into early embryonic vascular morphogenesis with unprecedented clarity and insight. By combining the power of molecular genetics with the elegance of dynamic imaging, we follow the precise patterning of endothelial cells in space and time. We show that during vasculogenesis within the vascular plexus, ECs move independently to form the rudiments of blood vessels, all while collectively moving with gastrulating tissues that flow toward the embryo midline. The aortae are a composite of somatic derived ECs forming its dorsal regions and the splanchnic derived ECs forming its ventral region. The ECs in the dorsal regions of the forming aortae exhibit variable mediolateral motions as they move rostrally; those in more ventral regions show significant lateral-to-medial movement as they course rostrally. The present results offer a powerful approach to the major challenge of studying the relative role(s) of the mechanical, molecular, and cellular mechanisms of vascular development. In past studies, the advantages of the molecular genetic tools available in mouse were counterbalanced by the limited experimental accessibility needed for imaging and perturbation studies. Avian embryos provide the needed accessibility, but few genetic resources. The creation of transgenic quail with labeled endothelia builds upon the important roles that avian embryos have played in previous studies of vascular development.

Original languageEnglish
Article numbere12674
JournalPLoS One
Volume5
Issue number9
Publication statusPublished - 2010
Externally publishedYes

Fingerprint

Quail
Endothelial cells
Blood vessels
quails
Morphogenesis
blood vessels
Dynamic analysis
morphogenesis
Blood Vessels
embryo (animal)
Embryonic Structures
genetically modified organisms
Tissue
Imaging techniques
endothelial cells
Endothelial Cells
image analysis
Self assembly
aorta
molecular genetics

All Science Journal Classification (ASJC) codes

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Sato, Y., Poynter, G., Huss, D., Filla, M. B., Czirok, A., Rongish, B. J., ... Lansford, R. (2010). Dynamic analysis of vascular morphogenesis using transgenic quail embryos. PLoS One, 5(9), [e12674].

Dynamic analysis of vascular morphogenesis using transgenic quail embryos. / Sato, Yuki; Poynter, Greg; Huss, David; Filla, Michael B.; Czirok, Andras; Rongish, Brenda J.; Little, Charles D.; Fraser, Scott E.; Lansford, Rusty.

In: PLoS One, Vol. 5, No. 9, e12674, 2010.

Research output: Contribution to journalArticle

Sato, Y, Poynter, G, Huss, D, Filla, MB, Czirok, A, Rongish, BJ, Little, CD, Fraser, SE & Lansford, R 2010, 'Dynamic analysis of vascular morphogenesis using transgenic quail embryos.', PLoS One, vol. 5, no. 9, e12674.
Sato Y, Poynter G, Huss D, Filla MB, Czirok A, Rongish BJ et al. Dynamic analysis of vascular morphogenesis using transgenic quail embryos. PLoS One. 2010;5(9). e12674.
Sato, Yuki ; Poynter, Greg ; Huss, David ; Filla, Michael B. ; Czirok, Andras ; Rongish, Brenda J. ; Little, Charles D. ; Fraser, Scott E. ; Lansford, Rusty. / Dynamic analysis of vascular morphogenesis using transgenic quail embryos. In: PLoS One. 2010 ; Vol. 5, No. 9.
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