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      Microvascular anatomy of the non‐lobulated liver of adult Xenopus laevis : A scanning electron microscopic study of vascular casts

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          Abstract

          The microvascular anatomy of the non‐lobulated liver of adult Xenopus laevis was studied by scanning electron microscopy of vascular corrosion casts. Hepatic portal veins and hepatic arteries entered hepatic lobes at the hiluses, hepatic veins left at these sites. Intraparenchymal, hepatic portal veins branched up to 10 times before terminal portal venules supplied liver sinusoids. Hepatic arteries closely followed portal vessels. Arteriolar side branches formed anastomoses with close by portal venules (arteriolar‐portal anastomoses; APAs), liver sinusoids (arteriolar‐sinusoidal anastomoses; ASAs), and peribiliary plexus vessels. Distally, hepatic arteries anastomosed with terminal portal venules having >100 μm in diameter. Liver sinusoids formed a dense three‐dimensional network displaying signs of non‐sprouting and sprouting angiogenesis evidenced by “holes” and blind ending tapering cast vascular structures (sprouts), respectively. Sinusoids drained via efferent hepatic veins. Right and left hepatic veins drained into the posterior caval vein. Locally, a dense honeycomb‐like 3D‐meshwork of resin structures was found around terminal portal venules and hepatic arteries. These networks were fed by hepatic arterioles and drained into adjacent terminal portal venules. As their morphologies differed significantly from sinusoids and they were found at sites where diffuse lymphoid tissue is described, we are convinced that they represent the vasculature of diffuse lymphoid tissue areas. Frequencies and diameter ratios of hepatic portal venules versus hepatic arterioles anastomosing with the former (APAs) implicate that the arterial supply contributes to the oxygenation of parenchymal and stromal cells rather than to a significant increase in blood flow towards hepatic sinusoids.

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          Most cited references49

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          Vascular remodeling by intussusceptive angiogenesis.

          Intussusception (growth within itself) is an alternative to the sprouting mode of angiogenesis. The protrusion of opposing microvascular walls into the capillary lumen creates a contact zone between endothelial cells. The endothelial bilayer is perforated, intercellular contacts are reorganized, and a transluminal pillar with an interstitial core is formed, which is soon invaded by myofibroblasts and pericytes leading to its rapid enlargement by the deposition of collagen fibrils. Intussusception has been implicated in three processes of vascular growth and remodeling. (1) Intussusceptive microvascular growth permits rapid expansion of the capillary plexus, furnishing a large endothelial surface for metabolic exchange. (2) Intussusceptive arborization causes changes in the size, position, and form of preferentially perfused capillary segments, creating a hierarchical tree. (3) Intussusceptive branching remodeling (IBR) leads to modification of the branching geometry of supplying vessels, optimizing pre- and postcapillary flow properties. IBR can also lead to the removal of branches by pruning in response to changes in metabolic needs. None of the three modes requires the immediate proliferation of endothelial cells but rather the rearrangement and plastic remodeling of existing ones. Intussusception appears to be triggered immediately after the formation of the primitive capillary plexus by vasculogenesis or sprouting. The advantage of this mechanism of growth over sprouting is that blood vessels are generated more rapidly in an energetically and metabolically more economic manner, as extensive cell proliferation, basement membrane degradation, and invasion of the surrounding tissue are not required; the capillaries thereby formed are less leaky. This process occurs without disrupting organ function. Improvements in our understanding of the process should enable the development of novel pro- and anti-angiogenic therapeutic treatments.
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            Intussusceptive angiogenesis: its emergence, its characteristics, and its significance.

            This review shall familiarize the reader with the various aspects of intussusceptive angiogenesis (IA). The basic event in IA is the formation of transvascular tissue pillars. Depending on location, timing, and frequency of pillar emergence, the IA process has different outcomes. In capillaries, a primary IA function is to expand the capillary bed in size and complexity (intussusceptive microvascular growth). It represents an alternative to capillary sprouting. Highly ordered pillar formation in a developing capillary network leads to the formation of vascular trees (intussusceptive arborization). In small arteries and veins, pillar formation at the vessels' branching angles leads either to remodeling of the branching geometry or even to vascular pruning (intussusceptive branching remodeling). It appears essential that future angiogenic research considers always both phenomena, sprouting and intussusception. Vascularization of tissues, organs, and tumors rely heavily on both mechanisms; neglecting one or the other would obscure our understanding of the angiogenesis process. (c) 2004 Wiley-Liss, Inc.
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              Morphological mechanisms for regulating blood flow through hepatic sinusoids.

              R McCuskey (2000)
              This review summarizes what is known about the various morphological sites that regulate the distribution of blood flow to and from the sinusoids in the hepatic microvascular system. These sites potentially include the various segments of the afferent portal venules and hepatic arterioles, the sinusoids themselves, and central and hepatic venules. Given the paucity of smooth muscle in the walls of these vessels, various sinusoidal lining cells have been suggested to play a role in regulating the diameters of sinusoids and influencing the distribution and velocity of blood flow in these vessels. While sinusoidal endothelial cells have been demonstrated to be contractile and to exhibit sphincter function, attention has recently focused on the perisinusoidal stellate cell as the cell responsible for controlling the sinusoidal diameter. A very recent study, however, suggested that the principal site of vasoconstriction elicited by ET-1 was the pre-terminal portal venule. This raised the question of whether or not the diameters of sinusoids might decrease due to passive recoil when inflow is reduced or eliminated and intra-sinusoidal pressure falls. In more recent in vivo microscopic studies, clamping of the portal vein dramatically reduced sinusoidal blood flow as well as the diameters of sinusoids. The sinusoidal lumens rapidly returned to their initial diameters upon restoration of portal blood flow suggesting that sinusoidal blood pressure normally distends the sinusoidal wall which can recoil when the pressure drops. Stellate cells may be responsible for this reaction given the nature of their attachment to parenchymal cells by obliquely oriented microprojections from the lateral edges of their subendothelial processes. This suggests that care must be exercised when interpreting the mechanism for the reduction of sinusoidal diameters following drug administration without knowledge of changes occurring to the portal venous and hepatic inflow.

                Author and article information

                Contributors
                alois.lametschwandtner@sbg.ac.at
                Journal
                Anat Rec (Hoboken)
                Anat Rec (Hoboken)
                10.1002/(ISSN)1932-8494
                AR
                Anatomical Record (Hoboken, N.j. : 2007)
                John Wiley & Sons, Inc. (Hoboken, USA )
                1932-8486
                1932-8494
                24 May 2021
                February 2022
                : 305
                : 2 ( doiID: 10.1002/ar.v305.2 )
                : 243-253
                Affiliations
                [ 1 ] Department of Biosciences University of Salzburg, Vascular and Exercise Biology Research Group Salzburg Austria
                [ 2 ] Department of Biomedicine University of Basel Basel Switzerland
                Author notes
                [*] [* ] Correspondence

                Alois Lametschwandtner, Department of Biosciences, University of Salzburg, Vascular and Exercise Biology Research Group, Hellbrunnerstrasse 34, A‐5020 Salzburg, Austria.

                Email: alois.lametschwandtner@ 123456sbg.ac.at

                Author information
                https://orcid.org/0000-0001-8057-9304
                Article
                AR24649
                10.1002/ar.24649
                9292344
                33943032
                d8909d1e-a04f-42dd-aa00-c0d9a25d42b1
                © 2021 The Authors. The Anatomical Record published by Wiley Periodicals LLC on behalf of American Association for Anatomy.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

                History
                : 21 March 2021
                : 23 January 2021
                : 06 April 2021
                Page count
                Figures: 7, Tables: 0, Pages: 11, Words: 6350
                Funding
                Funded by: Universität Salzburg , doi 10.13039/501100005644;
                Categories
                Full Length Article
                FULL LENGTH ARTICLE
                COVER / Gastrointestinal Biology
                Custom metadata
                2.0
                February 2022
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.1.7 mode:remove_FC converted:18.07.2022

                Anatomy & Physiology
                liver,microvasculature,scanning electron microscopy,vascular casts,xenopus
                Anatomy & Physiology
                liver, microvasculature, scanning electron microscopy, vascular casts, xenopus

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