Experimental and theoretical modelling of blind-ended vessels within a developing angiogenic plexus.

Luciano A Guerreiro-Lucas, S. Rares Pop, Maria J C Machado and Ying Liang Ma, Sarah L Waters, Giles Richardson, Kurt Saetzler, Oliver E Jensen, Christopher Mitchell

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

Angiogenic sprouts at the leading edge of an expanding vascular plexus are recognised as major regulators of the structure of the developing network. Early in sprout development, a vascular lumen is often evident which communicates with the parent vessel while the distal tip is blind-ended. Here we describe the temporal evolution of blind-ended vessels (BEVs) in a small wound made in the panniculus carnosus muscle of a mouse viewed in a dorsal skin-fold window-chamber model with intra-vital microscopy during the most active period of angiogenesis (days 5-8 after injury). Although these structures have been mentioned anecdotally in previous studies, we observed BEVs to be frequent, albeit transient, features of plexus formation. Plasma leakage into the surrounding extracellular matrix occurring from these immature conduits could play an important role in preparing hypoxic tissue for vascular invasion. Although sprout growth is likely to be regulated by its flow environment, the parameters regulating flow into and through BEVs have not been characterised in situ. Longitudinal data from individual animals show that the number of BEVs filled with plasma alone peaks at day 7, when they can exceed 150 mum in length. Additionally, BEVs greater than 40 mum in length are more likely to be filled with stationary erythrocytes than with plasma alone. Using a mathematical model, we show how the flux of 150kD fluorinated (FITC-) dextran through an individual plasma-filled BEV is related to its geometry being determined primarily by its surface area; by fitting theoretical intensity values to experimental data we assess the permeability of the vessel to FITC-dextran. Plasma skimming provides a mechanistic explanation for the observation that BEVs with larger surface area are more likely to recruit erythrocytes.
LanguageEnglish
Pages161-168
JournalMicrovasc Res
Volume76
DOIs
Publication statusPublished - Jul 2008

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vessel
modeling
plasma
surface area
temporal evolution
leakage
microscopy
skin
muscle
permeability
fold
geometry
matrix
animal

Cite this

Guerreiro-Lucas, L. A., Pop, S. R., Ma, M. J. C. M. Y. L., Waters, S. L., Richardson, G., Saetzler, K., ... Mitchell, C. (2008). Experimental and theoretical modelling of blind-ended vessels within a developing angiogenic plexus. Microvasc Res, 76, 161-168. https://doi.org/10.1016/j.mvr.2008.06.005
Guerreiro-Lucas, Luciano A ; Pop, S. Rares ; Ma, Maria J C Machado and Ying Liang ; Waters, Sarah L ; Richardson, Giles ; Saetzler, Kurt ; Jensen, Oliver E ; Mitchell, Christopher. / Experimental and theoretical modelling of blind-ended vessels within a developing angiogenic plexus. In: Microvasc Res. 2008 ; Vol. 76. pp. 161-168.
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Guerreiro-Lucas, LA, Pop, SR, Ma, MJCMYL, Waters, SL, Richardson, G, Saetzler, K, Jensen, OE & Mitchell, C 2008, 'Experimental and theoretical modelling of blind-ended vessels within a developing angiogenic plexus.', Microvasc Res, vol. 76, pp. 161-168. https://doi.org/10.1016/j.mvr.2008.06.005

Experimental and theoretical modelling of blind-ended vessels within a developing angiogenic plexus. / Guerreiro-Lucas, Luciano A; Pop, S. Rares; Ma, Maria J C Machado and Ying Liang; Waters, Sarah L; Richardson, Giles; Saetzler, Kurt; Jensen, Oliver E; Mitchell, Christopher.

In: Microvasc Res, Vol. 76, 07.2008, p. 161-168.

Research output: Contribution to journalArticle

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AU - Guerreiro-Lucas, Luciano A

AU - Pop, S. Rares

AU - Ma, Maria J C Machado and Ying Liang

AU - Waters, Sarah L

AU - Richardson, Giles

AU - Saetzler, Kurt

AU - Jensen, Oliver E

AU - Mitchell, Christopher

PY - 2008/7

Y1 - 2008/7

N2 - Angiogenic sprouts at the leading edge of an expanding vascular plexus are recognised as major regulators of the structure of the developing network. Early in sprout development, a vascular lumen is often evident which communicates with the parent vessel while the distal tip is blind-ended. Here we describe the temporal evolution of blind-ended vessels (BEVs) in a small wound made in the panniculus carnosus muscle of a mouse viewed in a dorsal skin-fold window-chamber model with intra-vital microscopy during the most active period of angiogenesis (days 5-8 after injury). Although these structures have been mentioned anecdotally in previous studies, we observed BEVs to be frequent, albeit transient, features of plexus formation. Plasma leakage into the surrounding extracellular matrix occurring from these immature conduits could play an important role in preparing hypoxic tissue for vascular invasion. Although sprout growth is likely to be regulated by its flow environment, the parameters regulating flow into and through BEVs have not been characterised in situ. Longitudinal data from individual animals show that the number of BEVs filled with plasma alone peaks at day 7, when they can exceed 150 mum in length. Additionally, BEVs greater than 40 mum in length are more likely to be filled with stationary erythrocytes than with plasma alone. Using a mathematical model, we show how the flux of 150kD fluorinated (FITC-) dextran through an individual plasma-filled BEV is related to its geometry being determined primarily by its surface area; by fitting theoretical intensity values to experimental data we assess the permeability of the vessel to FITC-dextran. Plasma skimming provides a mechanistic explanation for the observation that BEVs with larger surface area are more likely to recruit erythrocytes.

AB - Angiogenic sprouts at the leading edge of an expanding vascular plexus are recognised as major regulators of the structure of the developing network. Early in sprout development, a vascular lumen is often evident which communicates with the parent vessel while the distal tip is blind-ended. Here we describe the temporal evolution of blind-ended vessels (BEVs) in a small wound made in the panniculus carnosus muscle of a mouse viewed in a dorsal skin-fold window-chamber model with intra-vital microscopy during the most active period of angiogenesis (days 5-8 after injury). Although these structures have been mentioned anecdotally in previous studies, we observed BEVs to be frequent, albeit transient, features of plexus formation. Plasma leakage into the surrounding extracellular matrix occurring from these immature conduits could play an important role in preparing hypoxic tissue for vascular invasion. Although sprout growth is likely to be regulated by its flow environment, the parameters regulating flow into and through BEVs have not been characterised in situ. Longitudinal data from individual animals show that the number of BEVs filled with plasma alone peaks at day 7, when they can exceed 150 mum in length. Additionally, BEVs greater than 40 mum in length are more likely to be filled with stationary erythrocytes than with plasma alone. Using a mathematical model, we show how the flux of 150kD fluorinated (FITC-) dextran through an individual plasma-filled BEV is related to its geometry being determined primarily by its surface area; by fitting theoretical intensity values to experimental data we assess the permeability of the vessel to FITC-dextran. Plasma skimming provides a mechanistic explanation for the observation that BEVs with larger surface area are more likely to recruit erythrocytes.

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DO - 10.1016/j.mvr.2008.06.005

M3 - Article

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Guerreiro-Lucas LA, Pop SR, Ma MJCMYL, Waters SL, Richardson G, Saetzler K et al. Experimental and theoretical modelling of blind-ended vessels within a developing angiogenic plexus. Microvasc Res. 2008 Jul;76:161-168. https://doi.org/10.1016/j.mvr.2008.06.005