Proliferation pattern of capillary endothelial cells in chorioallantoic membrane development indicates local growth control, which is counteracted by vascular endothelial growth factor application

Kurz, Haymo; Ambrosy, Sonja; Wilting, Jörg; Marmé, Dieter; Christ, Bodo

doi:10.1002/aja.1002030206

Cited by 65 publications

(57 citation statements)

References 45 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…5A-D) are compatible with those in real microvascular networks (Clark, 1991;Ellsworth et al, 1987;Honda and Yoshizato, 1997;Kurz et al, 1995;Less et al, 1997;Lichtenbeld et al, 1996;Lipowsky et al, 1978;Lipowsky and Zweifach, 1974;Pries et al, 1990Pries et al, , 1997Renkin, 1988). Moreover, in our random data samples, we find high pressure and low shear stress in and near the capillary region, because some branches may be (temporarily) not perfused -a situation that frequently occurs in living systems.…”

Section: Hemodynamics and Biomass Distributionsupporting

confidence: 87%

Structural and biophysical simulation of angiogenesis and vascular remodeling

Gödde

Kurz

2001

Developmental Dynamics

Self Cite

View full text Add to dashboard Cite

The purpose of this report is to introduce a new computer model for the simulation of microvascular growth and remodeling into arteries and veins that imitates angiogenesis and blood flow in real vascular plexuses. A C؉؉ computer program was developed based on geometric and biophysical initial and boundary conditions. Geometry was defined on a two-dimensional isometric grid by using defined sources and drains and elementary bifurcations that were able to proliferate or to regress under the influence of random and deterministic processes. Biophysics was defined by pressure, flow, and velocity distributions in the network by using the nodal-admittance-matrix-method, and accounting for hemodynamic peculiarities like Fahraeus-Lindqvist effect and exchange with extravascular tissue. The proposed model is the first to simulate interdigitation between the terminal branches of arterial and venous trees. This was achieved by inclusion of vessel regression and anastomosis in the capillary plexus and by remodeling in dependence from hemodynamics. The choice of regulatory properties influences the resulting vascular patterns. The model predicts interdigitating arteriovenous patterning if shear stress-dependent but not pressure-dependent remodeling was applied. By approximating the variability of natural vascular patterns, we hope to better understand homogeneity of transport, spatial distribution of hemodynamic properties and biomass allocation to the vascular wall or blood during development, or during evolution of circulatory systems.

show abstract

Section: Hemodynamics and Biomass Distributionsupporting

confidence: 87%

Structural and biophysical simulation of angiogenesis and vascular remodeling

Gödde

Kurz

2001

Developmental Dynamics

Self Cite

View full text Add to dashboard Cite

show abstract

“…The former has been implicated in vascular remodeling within adult tissues (Maisonpierre et al, 1997), whereas the latter is known to be essential for pericyte recruitment in the retina (Benjamin et al, 1998), brain (Hellstrom et al, 1999, and placenta (Ohlsson et al, 1999). Notably, the application of PDGF-B to fully developed CAMs leads to an abundant formation of larger pre-and postcapillary microvessels but does not amplify capillary meshes (Oh et al, 1998), whereas exogenous VEGF-A affects the capillary plexus and terminal feeding vessels, but has no influence on larger microvessels (Wilting et al, 1993;Kurz et al, 1995). Our assumption that endothelial cells respond to local challenges when initiating IBR is strongly supported by two recent observations: endothelial grafting in the chick-quail system showed that expression of the arterial marker ephrin-B2 depends on hemodynamics or local environment (Othman-Hassan et al, 2001); and serial section histology demonstrated intussusceptive remodeling in conditions of severely altered blood flow during tissue repair or tumor angiogenesis (Patan et al, 2001a,b).…”

Section: Possible Molecular Mechanisms Involved In Vascular Remodelingmentioning

confidence: 99%

“…In the CAM, intussusceptive microvascular growth (IMG; Caduff et al, 1986;Burri and Tarek, 1990) expands the capillary plexus (Patan et al, 1993;Schlatter et al, 1997) from which arterial and venous feeding vessels emerge by means of intussusceptive arborization (IAR) (Djonov et al, 2000a,b). The vascular bed of the CAM expands at an extraordinary speed for approximately 1 week by means of IMG and endothelial proliferation in capillaries, the later process ceasing at around incubation day 12 (E12) (Kurz et al, 1995). Simultaneously, the vascular bed is transformed from a single layer of capillaries into a twolayered system (by means of IAR): the gas-exchanging capillary plexus invades the chorionic epithelium, whereas arteries and veins remain "underneath" the capillary plexus displaying a typical bifurcation pattern.…”

Section: Introductionmentioning

confidence: 99%

Optimality in the developing vascular system: Branching remodeling by means of intussusception as an efficient adaptation mechanism

Djonov

Kurz

Burri

2002

Developmental Dynamics

Self Cite

189

218

View full text Add to dashboard Cite

The theory of bifurcating vascular systems predicts vessel diameters that are related to optimality criteria like minimization of pumping energy or of building material. However, mechanisms for producing the postulated optimality have not been described so far, and quantitative data on bifurcation diameters during development are scarce. We used an embryonic vascular bed that rapidly grows and adapts to changing hemodynamic conditions, the chicken chorioallantoic membrane (CAM), and correlated vascular cast and tissue section morphology with in vivo time-lapse video monitoring. The bifurcation exponent ⌬ and associated parameters were quantitatively assessed in arterial and venous microvessels ranging in diameter from 30 to 100 m. We observed emergence of optimality by means of intussusception, i.e., formation of transvascular tissue pillars. In addition to intussusceptive microvascular growth (IMG ‫؍‬ expansion of capillary networks) and intussusceptive arborization (IAR ‫؍‬ formation of feeding vessels from capillaries) the observed intussusception at bifurcations represents a third variant of nonsprouting angiogenesis. We call it intussusceptive branching remodeling (IBR). IBR occurred in vessels of considerable diameter by means of two alternative mechanisms: either through pillars arising close to a bifurcation, which increased in girth until they merged with the connective tissue in the bifurcation angle; or through pillars arising at some distance from the bifurcation point, which then expanded by formation of ingrowing tissue folds until they became connected to the tissue of the bifurcation angle. Morphologic evidence suggests that IBR is a wide-spread phenomenon, taking place also in lung, intestinal, kidney, eye, etc., vasculature. Irrespective of the mode followed, IBR led to a branching pattern close to the predicted optimum, ⌬ ‫؍‬ 3.0. Significant differences were observed between ⌬ at arterial bifurcations (2.70 to 2.90) and ⌬ at venous bifurcations (2.93 to 3.75). IBR, by means of eccentric pillar formation and fusion, was also involved in vascular pruning. Experimental changes in CAM hemodynamics (by locally increasing blood flow) induced onset of IBR within less than 1 hr. Our study provides morphologic and quantitative evidence that a similar cellular machinery is used for all three variants of vascular intussusception, IMG, IAR, and IBR. It thus provides a mechanism of efficiently generating complex blood transport systems from limited genetic information. Differential quantitative outcome of IBR in arteries and veins, and the experimental induction of IBR strongly suggest that hemodynamic factors can instruct embryonic vascular remodeling toward optimality.

show abstract

“…At day 11, this falls to 2% and remains low throughout the remaining incubation period. An investigation by Kurz et al (1995) of the presence of bromodeoxyuridine-labeled endothelial cells in the growing CAM from day 6 to day 15 revealed a significant (Ͼ50%) loss of proliferative activity at day 10 (intermediate phase) in comparison with day 6 (sprouting phase). After day 10, proliferative activity decreased further, and at days 14 and 15 (late phase), dividing cells were Ͻ10% of the value of day 6.…”

Section: Morphometric Evaluation Of Cam Vascular Growthmentioning

confidence: 99%

Chorioallantoic membrane capillary bed: A useful target for studying angiogenesis and anti‐angiogenesis in vivo

et al. 2001

View full text Add to dashboard Cite

The chick embryo chorioallantoic membrane (CAM) is an extraembryonic membrane that is commonly used in vivo to study both angiogenesis and anti-angiogenesis. This review 1) summarizes the current knowledge about the structure of the CAM's capillary bed; 2) discusses the controversy about the existence of a single blood sinus or a capillary plexus underlying the chorionic epithelium; 3) describes a new model of the CAM vascular growth, namely the intussusceptive mode; 4) reports findings regarding the role played by endogenous fibroblast growth factor-2 in CAM vascularization; and 5) addresses the use and limitations of the CAM as a model for studying angiogenesis and anti-angiogenesis. Anat Rec 264: [317][318][319][320][321][322][323][324] 2001.

show abstract

Proliferation pattern of capillary endothelial cells in chorioallantoic membrane development indicates local growth control, which is counteracted by vascular endothelial growth factor application

Cited by 65 publications

References 45 publications

Structural and biophysical simulation of angiogenesis and vascular remodeling

Structural and biophysical simulation of angiogenesis and vascular remodeling

Optimality in the developing vascular system: Branching remodeling by means of intussusception as an efficient adaptation mechanism

Chorioallantoic membrane capillary bed: A useful target for studying angiogenesis and anti‐angiogenesis in vivo

Contact Info

Product

Resources

About