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      Biology of Vascular Endothelial Growth Factor C in the Morphogenesis of Lymphatic Vessels

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          Abstract

          Because virtually all tissues contain blood vessels, the importance of hemevascularization has been long recognized in regenerative medicine and tissue engineering. However, the lymphatic vasculature has only recently become a subject of interest. Central to the task of growing a lymphatic network are lymphatic endothelial cells (LECs), which constitute the innermost layer of all lymphatic vessels. The central molecule that directs proliferation and migration of LECs during embryogenesis is vascular endothelial growth factor C (VEGF-C). VEGF-C is therefore an important ingredient for LEC culture and attempts to (re)generate lymphatic vessels and networks. During its biosynthesis VEGF-C undergoes a stepwise proteolytic processing, during which its properties and affinities for its interaction partners change. Many of these fundamental aspects of VEGF-C biosynthesis have only recently been uncovered. So far, most—if not all—applications of VEGF-C do not discriminate between different forms of VEGF-C. However, for lymphatic regeneration and engineering purposes, it appears mandatory to understand these differences, since they relate, e.g., to important aspects such as biodistribution and receptor activation potential. In this review, we discuss the molecular biology of VEGF-C as it relates to the growth of LECs and lymphatic vessels. However, the properties of VEGF-C are similarly relevant for the cardiovascular system, since both old and recent data show that VEGF-C can have a profound effect on the blood vasculature.

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          Most cited references91

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          The placental mammal ancestor and the post-K-Pg radiation of placentals.

          To discover interordinal relationships of living and fossil placental mammals and the time of origin of placentals relative to the Cretaceous-Paleogene (K-Pg) boundary, we scored 4541 phenomic characters de novo for 86 fossil and living species. Combining these data with molecular sequences, we obtained a phylogenetic tree that, when calibrated with fossils, shows that crown clade Placentalia and placental orders originated after the K-Pg boundary. Many nodes discovered using molecular data are upheld, but phenomic signals overturn molecular signals to show Sundatheria (Dermoptera + Scandentia) as the sister taxon of Primates, a close link between Proboscidea (elephants) and Sirenia (sea cows), and the monophyly of echolocating Chiroptera (bats). Our tree suggests that Placentalia first split into Xenarthra and Epitheria; extinct New World species are the oldest members of Afrotheria.
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            Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3.

            Vascular endothelial growth factor receptor-3 (VEGFR-3/Flt4) binds two known members of the VEGF ligand family, VEGF-C and VEGF-D, and has a critical function in the remodelling of the primary capillary vasculature of midgestation embryos. Later during development, VEGFR-3 regulates the growth and maintenance of the lymphatic vessels. In the present study, we have isolated and cultured stable lineages of blood vascular and lymphatic endothelial cells from human primary microvascular endothelium by using antibodies against the extracellular domain of VEGFR-3. We show that VEGFR-3 stimulation alone protects the lymphatic endothelial cells from serum deprivation-induced apoptosis and induces their growth and migration. At least some of these signals are transduced via a protein kinase C-dependent activation of the p42/p44 MAPK signalling cascade and via a wortmannin-sensitive induction of Akt phosphorylation. These results define the critical role of VEGF-C/VEGFR-3 signalling in the growth and survival of lymphatic endothelial cells. The culture of isolated lymphatic endothelial cells should now allow further studies of the molecular properties of these cells.
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              Development and plasticity of meningeal lymphatic vessels

              Antila et al. show that meningeal lymphatic vessels in mice develop postnatally. Interruption of VEGF-C/VEGFR3 signal transduction arrests their development. In adult mice, VEGFR3 deletion and VEGFR3 blockers, including a clinically available tyrosine kinase inhibitor, induce regression of meningeal lymphatic vessels.
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                Author and article information

                Contributors
                Journal
                Front Bioeng Biotechnol
                Front Bioeng Biotechnol
                Front. Bioeng. Biotechnol.
                Frontiers in Bioengineering and Biotechnology
                Frontiers Media S.A.
                2296-4185
                12 February 2018
                2018
                : 6
                : 7
                Affiliations
                [1] 1Translational Cancer Biology Research Program, University of Helsinki , Helsinki, Finland
                [2] 2Wihuri Research Institute, Biomedicum Helsinki , Helsinki, Finland
                Author notes

                Edited by: Wolfgang Holnthoner, Ludwig Boltzmann Gesellschaft (LBG), Austria

                Reviewed by: Joaquim Miguel Oliveira, University of Minho, Portugal; Mikaël M. Martino, Monash University, Australia; Arnaud Scherberich, University Hospital Basel, Switzerland

                *Correspondence: Michael Jeltsch, michael@ 123456jeltsch.org

                Specialty section: This article was submitted to Tissue Engineering and Regenerative Medicine, a section of the journal Frontiers in Bioengineering and Biotechnology

                Article
                10.3389/fbioe.2018.00007
                5816233
                29484295
                c2834bac-b006-46da-b83a-b91677987c1e
                Copyright © 2018 Rauniyar, Jha and Jeltsch.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 01 November 2017
                : 19 January 2018
                Page count
                Figures: 5, Tables: 1, Equations: 0, References: 134, Pages: 12, Words: 9744
                Funding
                Funded by: Academy of Finland 10.13039/501100002341
                Award ID: 304042, 303778, 273612, 265982
                Funded by: K. Albin Johanssons Stiftelse 10.13039/501100009067
                Funded by: Magnus Ehrnroothin Säätiö 10.13039/501100004155
                Funded by: Helsingin Yliopisto 10.13039/100007797
                Categories
                Bioengineering and Biotechnology
                Review

                vascular endothelial growth factor c,lymphatic vessels,lymphedema,tissue engineering,a disintegrin and metalloproteinase with thrombospondin motifs 3,collagen and calcium binding egf domains 1,growth factors,vegf receptors

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