Regression of blood vessels in the ventral velum of <i>Xenopus laevis Daudin</i> during metamorphosis: light microscopic and transmission electron microscopic study

Bartel, H; Lametschwandtner, Alois

doi:10.1046/j.1469-7580.2000.19720157.x

Cited by 14 publications

(9 citation statements)

References 28 publications

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“…1e) or in a multifocal manner (Fig. 1f,g), similar to the process of vascular obliteration observed by others (Bartel and Lametschwandtner, 2000). By means of this "fold" mechanism, the branching angle decreases and the bifurcation point moves either upstream (in arteries) or downstream (in veins).…”

Section: Morphology and Time Seriessupporting

confidence: 80%

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

Djonov

Kurz

Burri

2002

Developmental Dynamics

187

218

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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.

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Section: Morphology and Time Seriessupporting

confidence: 80%

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

Djonov

Kurz

Burri

2002

Developmental Dynamics

187

218

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“…To determine whether apoptosis was occurring equally in the GFP and XR11 transgenic tadpoles, we focused on the ventral velum, a portion of the larval filter feeding apparatus that has a chevron shape in cross section before it dissociates through apoptosis during metamorphosis [45]. As shown in Figure 3K–R, TUNEL-positive nuclei, which are rare in the velums in the absence of T 3 , were prevalent in the velums of both T 3 -treated GFP and XR11 transgenic tadpoles.…”

Section: Resultsmentioning

confidence: 99%

The roles of Bcl-xL in modulating apoptosis during development of Xenopus laevis

et al. 2005

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Background: Apoptosis is a common and essential aspect of development. It is particularly prevalent in the central nervous system and during remodelling processes such as formation of the digits and in amphibian metamorphosis. Apoptosis, which is dependent upon a balance between pro-and anti-apoptotic factors, also enables the embryo to rid itself of cells damaged by gamma irradiation. In this study, the roles of the anti-apoptotic factor Bcl-x L in protecting cells from apoptosis were examined in Xenopus laevis embryos using transgenesis to overexpress the XR11 gene, which encodes Bcl-x L . The effects on developmental, thyroid hormone-induced and γ-radiation-induced apoptosis in embryos were examined in these transgenic animals.

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“…In studies of cyclic angiogenesis and blood vessel regression in the ovary, in 1996, Modlich et al [133] found that capillary endothelial cells detached from the basement membrane singly or in sheets, and most endothelial cells became detached before undergoing apoptosis. Bartel and Lametschwandtner [134], studying regression of capillaries in tadpole epithelium, found that endothelial cells bulged into the lumen, almost plugging the vessel. Many endothelial cells were apoptotic.…”

Section: Endothelial Cell Destructionmentioning

confidence: 99%

A Review of String Vessels or Collapsed, Empty Basement Membrane Tubes

Brown

2010

JAD

106

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String vessels are thin connective tissue strands, remnants of capillaries, with no endothelial cells; they do not carry blood flow. They occur in numerous species, particularly in the central nervous system, but can occur in any tissue where capillaries have died. String vessels are often associated with pathologies such as Alzheimer’s disease, ischemia, and irradiation, but are also found in normal human brains from preterm babies to the aged. They provide a record of the original blood vessel location, but gradually disappear after months or years. There have been numerous studies of string vessels (acellular capillaries) in the retina, because retinal vessels can be seen in great detail in whole mounts after trypsin digestion. Capillary regression occurs by apoptosis, synchronously along capillary segments, with macrophages engulfing apoptotic endothelial cells. Macrophages may cause the apoptosis, or the regression may be triggered by loss of the endothelial cell survival factor VEGF. VEGF expression is induced by hypoxia and promotes capillary growth. Cessation of blood flow eliminates the shear stress that helps maintain endothelial cell survival. Capillaries can re-grow by proliferation and migration of endothelial cells into empty basement membrane tubes, which provide a structural scaffold, replete with signaling molecules. This is a problem in tumor control, but useful for recovery from capillary loss. There is an age-related waning of VEGF expression in response to hypoxia. This causes an age-related decline in cerebral angiogenesis and results in neuronal loss. It may also contribute to the proposed age-related loss of brain reserve.

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Regression of blood vessels in the ventral velum of Xenopus laevis Daudin during metamorphosis: light microscopic and transmission electron microscopic study

Cited by 14 publications

References 28 publications

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

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

The roles of Bcl-xL in modulating apoptosis during development of Xenopus laevis

A Review of String Vessels or Collapsed, Empty Basement Membrane Tubes

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