Evidence for intussusceptive capillary growth in the chicken chorio-allantoic membrane (CAM)

Abstract

The aim of our investigations was to test whether the chicken chorio-allantoic membrane (CAM) could be an adequate in vivo model for a new mode of capillary growth, originally described in the rat lung and termed intussusceptive microvascular growth. According to that concept the capillary system does not grow by sprouting of vessels, but expands by insertion of transcapillary tissue pillars or posts which form new intercapillary meshes. In the present study, we observed slender transcapillary tissue pillars with diameters around 1 microns in the CAM by in vivo microscopy, and analyzed their ultrastructure by transmission electron microscopic investigation of serial sections. The pillars corresponded in size to those previously described in rat lung microvasculature. On day 7, the pillar core contained endothelial-, endothelial-like cells and collagen fibers, and on day 12 additionally chorionic epithelial cells. As a hypothesis we propose that slender cytoplasmic extensions of endothelial cells, heavily interdigitated in the post area and often projecting into the vascular lumen, could initiate the first step of pillar formation, i.e., interconnect opposite capillary walls. During both stages of development endothelial-like cells were observed in close relationship with the pillars. These cells seem to be relevant for tissue post completion and growth, as they were found to invade the core of the pillars. From the localization of the interendothelial junctions in the post region, a certain similarity to the concept proposed for the lung can be found. The observations confirm that the CAM is a very suitable material for the in vivo investigation of intussusceptive capillary growth.

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

“…It is thought that the pillars then increase in diameter and become a capillary mesh. Patan et al (1993) observed the same morphological transformation during IMG in the CAM (Fig. 1).…”

Intussusceptive angiogenesis: Its emergence, its characteristics, and its significance

“…Observations made both in the lung and in the chorioallantoic membrane (CAM) of the chicken revealed some additional modes of transluminal pillar formation (Patan et al, 1993(Patan et al, , 1997. These variants are schematically represented in Figure 5, which illustrates the various ways by which transluminal pillars can be formed.…”

“…Therefore, we turned to the in vivo model of the shell-free chicken culture technique established by Auerbach and coworkers (1974). With this approach, it was repeatedly possible to demonstrate the in vivo appearance of transcapillary pillars within relatively short periods of observation (Patan et al, 1993;Kö nig et al, 1997).…”

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

“…Tissue pillars formed in this manner lead, in the first instance, to rapid expansion of the primary capillary plexus: intussusceptive microvascular growth (IMG, Burri and Tarek, 1990;Patan et al, 1993;Schlatter et al., 1997); and then to the formation of arterial and venous feeding vessels: intussusceptive arborization (IAR, Djonov et al, 2000a,b). In addition, as we describe in the present study, intussusceptive processes occur also in vessels of larger diameter and contribute to remodeling and pruning at points of bifurcation: intussusceptive branching remodeling (IBR).…”

“…It originates from fusion of the angiogenic mesodermal allantois with the ectodermal chorion and, thus, corresponds to the placenta of mammals. 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).…”