Segmental territories along the cardinal veins generate lymph sacs via a ballooning mechanism during embryonic lymphangiogenesis in mice

François, Mathias, Short, Kieran, Secker, Genevieve A., Combes, Alexander, Schwarz, Quenten, Davidson, Tara-Lynn, Smyth, Ian, Hong, Young-Kwon, Harvey, Natasha L. and Koopman, Peter (2012) Segmental territories along the cardinal veins generate lymph sacs via a ballooning mechanism during embryonic lymphangiogenesis in mice. Developmental Biology, 264 2: 89-98. doi:10.1016/j.ydbio.2011.12.032

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Author François, Mathias
Short, Kieran
Secker, Genevieve A.
Combes, Alexander
Schwarz, Quenten
Davidson, Tara-Lynn
Smyth, Ian
Hong, Young-Kwon
Harvey, Natasha L.
Koopman, Peter
Title Segmental territories along the cardinal veins generate lymph sacs via a ballooning mechanism during embryonic lymphangiogenesis in mice
Journal name Developmental Biology   Check publisher's open access policy
ISSN 0012-1606
1095-564X
Publication date 2012-04-15
Year available 2011
Sub-type Article (original research)
DOI 10.1016/j.ydbio.2011.12.032
Volume 264
Issue 2
Start page 89
End page 98
Total pages 10
Place of publication Maryland Heights, MO, U.S.A.
Publisher Academic Press
Collection year 2012
Language eng
Formatted abstract
During lymphangiogenesis in the mammalian embryo, a subset of vascular endothelial cells in the cardinal veins is reprogrammed to adopt a lymphatic endothelial fate. The prevailing model of lymphangiogenesis contends that these lymphatic precursor cells migrate away from the cardinal veins and reassemble peripherally as lymph sacs from which a lymphatic vasculature is generated. However, this model fails to account for a number of observations that, as a result, have remained anecdotal. Here, we use optical projection tomography, confocal microscopy and in vivo live imaging to uncover three key stages of lymphatic vascular morphogenesis in the mouse embryo at high resolution. First, we define territories or “pre-lymphatic clusters” of Prox1-positive lymphatic endothelial progenitor cells along the antero-posterior axis of the cardinal veins. Second, these pre-lymphatic clusters undergo progressive extrusion (“ballooning”) to generate primitive lymph sacs. Third, lymphatic vessels emerge by a combination of mechanisms including sprouting from the lymph sacs and direct delamination of streams of cells from the cardinal veins. Our data support a new model for lymphatic vascular patterning and morphogenesis, as a basis for identifying the molecular cues governing these processes.

Highlights: ► Dynamic assembly of clusters of lymphatic endothelial progenitors in the veins. ► Pre-lymphatic clusters distribute along the anteroposterior axis of the veins. ► Pre-lymphatic clusters give rise to the primitive lymphatic vasculature. ► The lymphatic plexus forms via a combination of ballooning and vascular sprouting. ► A novel model for the morphogenesis of the lymphatic vasculature.
Keyword LYVE1
Prox1
Lymphangiogenesis
Cluster
Lymphatic endothelial cells
Spatial organization
Optical projection tomography
Live imaging
Q-Index Code C1
Q-Index Status Confirmed Code
Institutional Status UQ
Additional Notes Available online 29 December 2011

Document type: Journal Article
Sub-type: Article (original research)
Collections: Official 2012 Collection
Institute for Molecular Bioscience - Publications
 
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Created: Wed, 18 Jan 2012, 10:39:46 EST by Susan Allen on behalf of Institute for Molecular Bioscience