Morphological patterns of angiogenesis in ovarian follicle capillary networks. A scanning electron microscopy study of corrosion cast.
To describe the morphological characteristics of the ovarian follicle (F) capillary neoformation and regression, the angiogenic figures were studied by means of scanning electron microscopy of corrosion casts in developing and mature F of rabbit, pig, and cow. Developing F showed gradual neoformation of thecal capillaries characterized by budding and then sprouting, likely from preexisting interstitial vessels. Postcapillary venules frequently showed vasoconstriction rings (sphincters). Vasodilation followed capillary elongation. Mature F, in addition to vessel elongation and dilation, also presented infolding of dilated capillary walls, followed by capillary duplication and sinusoidalization. Periovulatory F mainly showed functional changes, such as capillary dilation, signs of iperpermeabilization, and ischemia, the latter being limited to the apical follicular area. Vessel regression was characterized by thinning of capillaries and presence of avascular areas within the atretic F wall at any stage. This study showed two main types of angiogenic patterns. (a) longitudinal elongation (in series, sprouting angiogenesis) characterizing the initial phase of F development and (b) parallel duplication (in parallel, infolding or intussusceptive angiogenesis), ending in capillary lateral replication or splitting, secondary to functional microvascular changes. Indirect evidence of the establishment of postcapillary resistances contributing to capillary remodeling, was also shown. It is concluded that the sequence of capillary neoformation in mammalian ovarian F occurs in six steps: (1) budding, (2) sprouting (and elongation), (3) dilation, (4) infolding (intussusception), (5) duplication (splitting and elongation), and (6) sinusoidalization. Capillary regression hits F at any stage and characterizes F atresia.
Macchiarelli
Guido
G
Department of Experimental Medicine, University of L'Aquila, L'Aquila, Italy. guido.macchiarelli@cc.univaq.it
Jiang
Jin-Yi
JY
Nottola
Stefania A
SA
Sato
Eimei
E
D000818:Animals; D002196:Capillaries / Q000648:ultrastructure*; D002417:Cattle; D016319:Corrosion Casting / Q000379:methods*; D005260:Female; D008855:Microscopy, Electron, Scanning; D018919:Neovascularization, Physiologic / Q000502:physiology*; D006080:Ovarian Follicle / Q000098:blood supply* / Q000648:ultrastructure; D011817:Rabbits; D013552:Swine