Vascular Endothelial Cell Biology: An Update

Anne Krüger-Genge, Anna Blocki, Ralf-Peter Franke, Friedrich Jung, Anne Krüger-Genge, Anna Blocki, Ralf-Peter Franke, Friedrich Jung

Abstract

The vascular endothelium, a monolayer of endothelial cells (EC), constitutes the inner cellular lining of arteries, veins and capillaries and therefore is in direct contact with the components and cells of blood. The endothelium is not only a mere barrier between blood and tissues but also an endocrine organ. It actively controls the degree of vascular relaxation and constriction, and the extravasation of solutes, fluid, macromolecules and hormones, as well as that of platelets and blood cells. Through control of vascular tone, EC regulate the regional blood flow. They also direct inflammatory cells to foreign materials, areas in need of repair or defense against infections. In addition, EC are important in controlling blood fluidity, platelet adhesion and aggregation, leukocyte activation, adhesion, and transmigration. They also tightly keep the balance between coagulation and fibrinolysis and play a major role in the regulation of immune responses, inflammation and angiogenesis. To fulfill these different tasks, EC are heterogeneous and perform distinctly in the various organs and along the vascular tree. Important morphological, physiological and phenotypic differences between EC in the different parts of the arterial tree as well as between arteries and veins optimally support their specified functions in these vascular areas. This review updates the current knowledge about the morphology and function of endothelial cells, particularly their differences in different localizations around the body paying attention specifically to their different responses to physical, biochemical and environmental stimuli considering the different origins of the EC.

Keywords: angiogenesis; endothelium; glycocalyx; shear stress; thrombosis.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
(A) Immunostaining of an endothelial cell monolayer (cell nuclei in blue, von Willebrand factor in red, vinculin in green); (B) Endothelial cell borders from the confluent endothelial cell monolayer are stained according to Ranvier with AgNO3 (400-fold primary magnification).
Figure 2
Figure 2
Hemodynamic stresses (τW: wall shear stress, σ: circumferential wall stress) acting on the endothelial cell monolayer. (Q: blood volume flow, η: blood viscosity, r vessel radius, PT: transmural pressure difference).
Figure 3
Figure 3
Factors inducing vasodilation and/or vasoconstriction. (The red circle represents a blood vessel).
Figure 4
Figure 4
Platelet dependent and independent, receptor-mediated activation of endothelial cells.
Figure 5
Figure 5
Buckling of human venous endothelial cells in vitro on extracellular matrix pre-secreted by bovine corneal endothelial cells and displayed by confocal laser scanning microscopy (CLSM) induced by addition of an iodinated radiographic contrast medium (Iopromide-370, 30% v/v) to the cell culture medium [108].
Figure 6
Figure 6
Segmental constriction of a nailfold capillary documented at three time points (final magnification 1:570) [109].
Figure 7
Figure 7
Angiogenesis in brief. VEGF initiates assembly of endothelial cells, PDGF-BB recruits pericytes, whereas angiopoietin-1 and TGF-β stabilize the nascent vessel.
Figure 8
Figure 8
Capillary projection before occlusion and at different phases of capillary remodeling (Reprinted with the permission of [142], S. Karger AG).
Figure 9
Figure 9
Overlay of the former and the remodeled capillary beds by means of a Helmert transformation. (The picture in red shows the capillary bed before occlusion, superimposed by the picture in green with the newly grown capillary (Reprinted with the permission of [127], S. Karger AG)).

References

    1. Gimbrone M.A. Vascular endothelium: nature’s blood container. In: Gimbrone M.A., editor. Vascular endothelium in hemostasis and thrombosis. Churchill Livingstone; New York, NY, USA: 1986. pp. 1–13.
    1. Wolinsky H. A proposal linking clearance of circulating lipoproteins to tissue metabolic activity as a basis for understanding atherogenesis. Circ. Res. 1980;47:301–311. doi: 10.1161/01.RES.47.3.301.
    1. Lee M.-J., Thangada S., Claffey K.P., Ancellin N., Liu C.H., Kluk M., Volpi M., Sha’afi R.I., Hla T. Cell Adherens Junction Assembly and Morphogenesis Induced by Sphingosine-1-Phosphate. Cell. 1999;99:301–312. doi: 10.1016/S0092-8674(00)81661-X.
    1. Geiger B. A 130K protein from chicken gizzard: Its localization at the termini of microfilament bundles in cultured chicken cells. Cell. 1979;18:193–205. doi: 10.1016/0092-8674(79)90368-4.
    1. Michel C.C., Curry F.E. Microvascular Permeability. Physiol. Rev. 1999;79:703–761. doi: 10.1152/physrev.1999.79.3.703.
    1. McMaster P.D., Hudack S. The vessels involved in hydrostatic transudation. J. Exp. Med. 1932;55:417–430. doi: 10.1084/jem.55.3.417.
    1. Crone C. Permeability of single capillaries compared with results from whole-organ studies. Acta Physiol. Scand. Suppl. 1979;463:75–80.
    1. Krogh A. The number and distribution of capillaries in muscles with calculations of the oxygen pressure head necessary for supplying the tissue. J. Physiol. 1919;52:409–415. doi: 10.1113/jphysiol.1919.sp001839.
    1. Aird W.C. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ. Res. 2007;100:158–173. doi: 10.1161/01.RES.0000255691.76142.4a.
    1. Monahan-Earley R., Dvorak A.M., Aird W.C. Evolutionary origins of the blood vascular system and endothelium. J. Thromb. Haemost. 2013;11:46–66. doi: 10.1111/jth.12253.
    1. Mehta D., Malik A.B. Signaling mechanisms regulating endothelial permeability. Physiol. Rev. 2006;86:279–367. doi: 10.1152/physrev.00012.2005.
    1. Krüger A., Mrowietz C., Lendlein A., Jung F. Interaction of human umbilical vein endothelial cells (HUVEC) with platelets in vitro: Influence of platelet concentration and reactivity. Clin. Hemorheol. Microcirc. 2013;55:111–120.
    1. Tailor A., Cooper D., Granger D.N. Platelet–Vessel Wall Interactions in the Microcirculation. Microcirculation. 2005;12:275–285. doi: 10.1080/10739680590925691.
    1. Moncada S., Higgs E.A., vane J.R. Human arterial and venous tissues generate prostacyclin (prostaglandin X), a potent inhibitor of platelet aggregation. Lancet. 1977;1:18–20. doi: 10.1016/S0140-6736(77)91655-5.
    1. Weksler B.B., Marcus A.J., Jaffe E.A. Synthesis of PGI2 (prostacyclin) by cultured human and bovine endothelial cells. Proc. Nat. Acad. Sci. USA. 1977;74:3922–3926. doi: 10.1073/pnas.74.9.3922.
    1. Furchgott R.F., Zawadzki J.V. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature. 1980;288:373–376. doi: 10.1038/288373a0.
    1. Garland C.J., Hiley C.R., Dora K.A. EDHF: Spreading the influence of the endothelium. Br. J. Pharmacol. 2011;164:839–852. doi: 10.1111/j.1476-5381.2010.01148.x.
    1. Panza J.A., Quyyumi A.A., Brush J.E., Jr., Epstein S.E. Abnormal endothelium-dependent vascular relaxation in patients with essential hypertension. N. Engl. J. Med. 1990;323:22–27. doi: 10.1056/NEJM199007053230105.
    1. Marti C.N., Gheorghiade M., Kalogeropoulos A.P., Georgiopoulou V.V., Quyyumi A.A., Butler J. Endothelial dysfunction, arterial stiffness, and heart failure. J. Am. Coll. Cardiol. 2012;60:1455–1469. doi: 10.1016/j.jacc.2011.11.082.
    1. Lubrano V., Balzan S. Roles of LOX-1 in microvascular dysfunction. Microvasc. Res. 2016;105:132–140. doi: 10.1016/j.mvr.2016.02.006.
    1. Ushiyama A., Kataoka H., Iijima T. Glycocalix and its involvement in clinical pathophysiologies. J. Intens. Care. 2016;4:59. doi: 10.1186/s40560-016-0182-z.
    1. Becker B.F., Chappell D., Bruegger D., Annecke T., Jacob M. Therapeutic strategies targeting the endothelial glycocalyx: Acute deficits, but great potential. Cardiovasc. Res. 2010;87:300–310. doi: 10.1093/cvr/cvq137.
    1. Lipowsky H.H. Microvascular rheology and hemodynamics. Microcirculation. 2005;12:5–15. doi: 10.1080/10739680590894966.
    1. Zeng Y. Endothelial glycocalyx as a critical signaling platform integrating the extracellular hemodynamic forces and chemical signaling. J. Cell Mol. Med. 2017;21:1457–1462. doi: 10.1111/jcmm.13081.
    1. Reitsma S., Slaaf D.W., Vink H., van Zandvoort M.A., oude Egbrink M.G. The endothelial glycocalyx: Composition, functions, and visualization. Pflugers Arch. 2007;454:345–359. doi: 10.1007/s00424-007-0212-8.
    1. Itano N., Sawai T., Yoshida M., Lenas P., Yamada Y., Imagawa M., Shinomura T., Hamaguchi M., Yoshida Y., Ohnuki Y., et al. Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties. J. Biol. Chem. 1999;274:25085–25092. doi: 10.1074/jbc.274.35.25085.
    1. Potter D.R., Jiang J., Damiano E.R. The recovery time course of the endothelial-cell glycocalyx in vivo and its implications in vitro. Circ. Res. 2009;104:1318–1325. doi: 10.1161/CIRCRESAHA.108.191585.
    1. Jacob M., Bruegger D., Rehm M., Stoeckelhuber M., Welsch U., Conzen P., Becker B.F. The endothelial glycocalyx affords compatibility of Starling’s principle and high cardiac interstitial albumin levels. Cardiovasc. Res. 2007;73:575–586. doi: 10.1016/j.cardiores.2006.11.021.
    1. Lebel L. Clearance of hyaluronan from the circulation. Adv. Drug Delivery Rev. 1991;2:221–235. doi: 10.1016/0169-409X(91)90003-U.
    1. Koning N.J., Vonk A.B., Vink H., Boer C. Side-by-side alterations in glycocalyx thickness and perfused microvascular density during acute microcirculatory alterations in cardiac surgery. Microcirculation. 2016;23:69–74. doi: 10.1111/micc.12260.
    1. Fransson L.-Å., Belting M., Cheng F., Jönsson M., Mani K., Sandgren S. Novel aspects of glypican glycobiology. Cell Mol. Life Sci. CMLS. 2004;61:1016–1024. doi: 10.1007/s00018-004-3445-0.
    1. Iozzo R.V. Proteoglycans: Structure, function, and role in neoplasia. Lab. Invest. 1985;53:373–396.
    1. Curry F.E., Adamson R.H. Endothelial glycocalyx: Permeability barrier and mechanosensor. Ann. Biomed. Eng. 2012;40:828–839. doi: 10.1007/s10439-011-0429-8.
    1. van den Berg B.M., Nieuwdorp M., Stroes E.S., Vink H. Glycocalyx and endothelial (dys) function: From mice to men. Pharmacol. Rep. 2006;58:75–80.
    1. Pries A.R., Secomb T.W., Gaehtgens P. The endothelial surface layer. Pflugers Arch. 2000;440:653–666. doi: 10.1007/s004240000307.
    1. Levick J. Capillary filtration-absorption balance reconsidered in light of dynamic extravascular factors. Exp. Physiol. 1991;76:825–857. doi: 10.1113/expphysiol.1991.sp003549.
    1. Lipowsky H.H., Lescanic A. Inhibition of inflammation induced shedding of the endothelial glycocalyx with low molecular weight heparin. Microvasc. Res. 2017;112:72–78. doi: 10.1016/j.mvr.2017.03.007.
    1. Tarbell J.M., Pahakis M. Mechanotransduction and the glycocalyx. J. Intern. Med. 2006;259:339–350. doi: 10.1111/j.1365-2796.2006.01620.x.
    1. Tesauro M., Cardillo C. Obesity, blood vessels and metabolic syndrome. Acta Physiol. (Oxf). 2011;203:279–286. doi: 10.1111/j.1748-1716.2011.02290.x.
    1. Reinhart W.H. Shear-dependence of endothelial functions. Experientia. 1994;50:87–93. doi: 10.1007/BF01984940.
    1. Resnick N., Gimbrone M.A. Hemodynamic forces are complex regulators of endothelial gene expression. FASEB J. 1995;9:874–882. doi: 10.1096/fasebj.9.10.7615157.
    1. Xiao Z., Zhang Z., Ranjan V., Diamond S.L. Shear stress induction of the endothelial nitric oxide synthase gene is calcium-dependent but not calcium-activated. J. Cell Physiol. 1997;171:205–211. doi: 10.1002/(SICI)1097-4652(199705)171:2<205::AID-JCP11>;2-C.
    1. Nerem R.M., Alexander R.W., Chappell D.C., Medford R.M., Varner S.E., Taylor W.R. The study of the influence of flow on vascular endothelial biology. Am. J. Med. Sci. 1998;316:169–175.
    1. Chien S. Effects of disturbed flow on endothelial cells. Ann. Biomed. Eng. 2008;36:554–562. doi: 10.1007/s10439-007-9426-3.
    1. Franke R.P., Gräfe M., Schnittler H., Seiffge D., Mittermayer C., Drenckhahn D. Induction of human vascular endothelial stress fibres by fluid shear stress. Nature. 1984;307:648–649. doi: 10.1038/307648a0.
    1. Tzima E., Irani-Tehrani M., Kiosses W.B., Dejana E., Schultz D.A., Engelhardt B., Cao G., DeLisser H., Schwartz M.A. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature. 2005;437:426–431. doi: 10.1038/nature03952.
    1. Gudi S., Huvar I., White C.R., McKnight N.L., Dusserre N., Boss G.R., Frangos J.A. Rapid activation of Ras by fluid flow is mediated by Galpha(q) and Gbetagamma subunits of heterotrimeric G proteins in human endothelial cells. Arterioscler. Thromb. Vasc. Biol. 2003;23:994–1000. doi: 10.1161/01.ATV.0000073314.51987.84.
    1. Hierck B.P., Van der Heiden K., Alkemade F.E., Van de Pas S., Van Thienen J.V., Groenendijk B.C., Bax W.H., Van der Laarse A., Deruiter M.C., Horrevoets A.J., et al. Primary cilia sensitize endothelial cells for fluid shear stress. Dev Dyn. 2008;237:725–735. doi: 10.1002/dvdy.21472.
    1. Yu J., Bergaya S., Murata T., Alp I.F., Bauer M.P., Lin M.I., Drab M., Kurzchalia T.V., Stan R.V., Sessa W.C. Direct evidence for the role of caveolin-1 and caveolae in mechanotransduction and remodeling of blood vessels. J. Clin. Invest. 2006;116:1284–1291. doi: 10.1172/JCI27100.
    1. Jalali S., del Pozo M.A., Chen K., Miao H., Li Y., Schwartz M.A., Shyy J.Y., Chien S. Integrin-mediated mechanotransduction requires its dynamic interaction with specific extracellular matrix (ECM) ligands. Proc Natl Acad Sci. USA. 2001;98:1042–1046. doi: 10.1073/pnas.98.3.1042.
    1. Pahakis M.Y., Kosky J.R., Dull R.O., Tarbell J.M. The role of endothelial glycocalyx components in mechanotransduction of fluid shear stress. Biochem. Biophys. Res. Commun. 2007;355:228–233. doi: 10.1016/j.bbrc.2007.01.137.
    1. Drenckhahn D., Gress T., Franke R.P. Vascular endothelial stress fibres: Their potential role in protecting the vessel wall from rheological damage. Klin Wochenschr. 1986;64:986–988.
    1. Jin Z.G., Ueba H., Tanimoto T., Lungu A.O., Frame M.D., Berk B.C. Ligand-independent activation of vascular endothelial growth factor receptor 2 by fluid shear stress regulates activation of endothelial nitric oxide synthase. Circ. Res. 2003;93:354–363. doi: 10.1161/01.RES.0000089257.94002.96.
    1. Banerjee S.S., Lin Z., Atkins G.B., Greif D.M., Rao R.M., Kumar A., Feinberg M.W., Chen Z., Simon D.I., Luskinskas F.W., et al. KLF2 Is a Novel Transcriptional Regulator of Endothelial Proinflammatory Activation. J. Exp. Med. 2004;199:1305–1315. doi: 10.1084/jem.20031132.
    1. Simionescu M., Simionescu N., Santoro F., Palade G.E. Differentiated microdomains of the luminal plasmalemma of murine muscle capillaries: Segmental variations in young and old animals. J. Cell Biol. 1985;100:1396–1407. doi: 10.1083/jcb.100.5.1396.
    1. Gerritsen M.E., Printz M.P. Sites of prostaglandin synthesis in the bovine heart and isolated bovine coronary microvessels. Circ. Res. 1981;49:1152–1163. doi: 10.1161/01.RES.49.5.1152.
    1. Hauser S., Jung F., Pietzsch J. Human Endothelial Cell Models in Biomaterial Research. Trends Biotechnol. 2017;35:265–277. doi: 10.1016/j.tibtech.2016.09.007.
    1. Johnson A.R. Human pulmonary endothelial cells in culture. Activities of cells from arteries and cells from veins. J. Clin. Invest. 1980;65:841–850. doi: 10.1172/JCI109736.
    1. Michiels C. Endothelial Cell Functions. J. Cell. Physiol. 2003;196:430–443. doi: 10.1002/jcp.10333.
    1. Gori T. Endothelial Function: A Short Guide for the Interventional Cardiologist. Int. J. Mol. Sci. 2018;19:3838. doi: 10.3390/ijms19123838.
    1. Miura H., Gutterman D.D. Human coronary arteriolar dilation to arachidonic acid depends on cytochrome P-450 monooxygenase and Ca2+ activated K+ channels. Circ. Res. 1998;83:501–507. doi: 10.1161/01.RES.83.5.501.
    1. Goto K., Ohtsubo T., Kitazono T. Endothelium-Dependent Hyperpolarization (EDH) in Hypertension: The Role of Endothelial Ion Channels. Int. J. Mol. Sci. 2018;19:315. doi: 10.3390/ijms19010315.
    1. Palmer R.M., Ferrige A.G., Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 1987;327:524–526. doi: 10.1038/327524a0.
    1. Loh Y.C., Tan C.S., Ch’ng Y.S., Yeap Z.Q., Ng C.H., Yam M.F. Overview of the Microenvironment of Vasculature in Vascular Tone Regulation. Int. J. Mol. Sci. 2018;19:120.
    1. Fleming I., Bauersachs J., Busse R. Paracrine functions of the coronary vascular endothelium. Mol. Cell. Biochem. 1996;157:137–145. doi: 10.1007/BF00227892.
    1. Ahmad A., Dempsey S.K., Daneva Z., Azam M., Li N., Li P-LRitter J.K. Role of Nitric Oxide in the Cardiovascular and Renal Systems. Int. J. Mol. Sci. 2018;19:2605. doi: 10.3390/ijms19092605.
    1. Komori K., Vanhoutte P.M. Endothelium-derived hyperpolarizing factor. Blood Vessels. 1990;27:238–245. doi: 10.1159/000158815.
    1. Zeldin D.C. Epoxygenase pathways of arachidonic acid metabolism. J. Biol. Chem. 2001;276:36059–36062. doi: 10.1074/jbc.R100030200.
    1. Jung F., Schulz C., Blaschke F., Muller D.N., Mrowietz C., Franke R.P., Lendlein A., Schunck W.H. Effect of cytochrome P450-dependent epoxyeicosanoids on Ristocetin-induced thrombocyte aggregation. Clin. Hemorheol. Microcirc. 2012;52:403–416.
    1. Chen J.K., Capdevila J., Harris R.C. Overexpression of C-terminal Src kinase blocks 14,15-epoxyeicosatrienoic acid-induced tyrosine phosphorylation and mitogenesis. J. Biol. Chem. 2000;275:13789–13792. doi: 10.1074/jbc.275.18.13789.
    1. Node K., Huo Y., Ruan X., Yang B., Spiecker M., Ley K., Zeldin D.C., Liao J.K. Anti-inflammatory properties of cytochrome P450 epoxygenase-derived eicosanoids. Science. 1999;285:1276–1279. doi: 10.1126/science.285.5431.1276.
    1. Panigrahy D., Kalish B.T., Huang S., Bielenberg D.R., Le H.D., Yang J., Edin M.L., Lee C.R., Benny O., Mudge D.K., et al. Epoxyeicosanoids promote organ and tissue regeneration. Proc. Natl. Acad. Sci. USA. 2013;110:13528–13533. doi: 10.1073/pnas.1311565110.
    1. Sun J., Sui X., Bradbury J.A., Zeldin D.C., Conte M.S., Liao J.K. Inhibition of vascular smooth muscle cell migration by cytochrome p450 epoxygenase-derived eicosanoids. Circ. Res. 2002;90:1020–1027. doi: 10.1161/01.RES.0000017727.35930.33.
    1. Node K., Ruan X.L., Dai J., Yang S.X., Graham L., Zeldin D.C., Liao J.K. Activation of Galpha s mediates induction of tissue-type plasminogen activator gene transcription by epoxyeicosatrienoic acids. J. Biol. Chem. 2001;276:15983–15989. doi: 10.1074/jbc.M100439200.
    1. Wang H., Lin L., Jiang J., Wang Y., Lu Z.Y., Bradbury J.A., Lih F.B., Wang D.W., Zeldin D.C. Up-regulation of endothelial nitric-oxide synthase by endothelium-derived hyperpolarizing factor involves mitogen-activated protein kinase and protein kinase C signaling pathways. J. Pharmacol. Exp. Ther. 2003;307:753–764. doi: 10.1124/jpet.103.052787.
    1. Luksha L., Luksha N., Kublickas M., Nisell H., Kublickiene K. Diverse mechanisms of endothelium-derived hyperpolarizing factor-mediated dilatation in small myometrial arteries in normal human pregnancy and preeclampsia. Biol. Reprod. 2010;83:728–735. doi: 10.1095/biolreprod.110.084426.
    1. Tomioka H., Hattori Y., Fukao M., Sato A., Liu M., Sakuma I., Kitabatake A., Kanno M. Relaxation in different-sized rat blood vessels mediated by endothelium-derived hyperpolarizing factor: Importance of processes mediating precontractions. J. Vasc. Res. 1999;36:311–320. doi: 10.1159/000025659.
    1. Huang A., Sun D., Smith C.J., Connetta J.A., Shesely E.G., Koller A., Kaley G. In eNOS knockout mice skeletal muscle arteriolar dilation to acetylcholine is mediated by EDHF. Am. J. Physiol. Heart Circ. Physiol. 2000;278:H762–H768. doi: 10.1152/ajpheart.2000.278.3.H762.
    1. Feletou M., Vanhoutte P.M. Endothelium-derived hyperpolarizing factor: Where are we now? Arterioscler. Thromb. Vasc. Biol. 2006;26:1215–1225. doi: 10.1161/01.ATV.0000217611.81085.c5.
    1. Félétou M., Vanhoutte P.M. Endothelium-dependent hyperpolarization of canine coronary smooth muscle. Br. J. Pharmacol. 1988;93:515–524. doi: 10.1111/j.1476-5381.1988.tb10306.x.
    1. Garland C.J., Dora K.A. EDH: Endothelium-dependent hyperpolarization and microvascular signaling. Acta Physiol. 2017;219:152–161. doi: 10.1111/apha.12649.
    1. Vanhoutte P.M. TE Endothelium-dependent contractions: When a good guy turns bad! J. Physiol. 2008;15:5295–5304. doi: 10.1113/jphysiol.2008.161430.
    1. Yanagisawa M., Kurihara H., Kimura S., Tomobe Y., Kobayashi M., Mitsui Y., Yazaki Y., Goto K., Masaki T. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature. 1988;332:411–415. doi: 10.1038/332411a0.
    1. Kedzierski R.M., Yanagisawa M. Endothelin system: The double-edged sword in health and disease. Annu. Rev. Pharmacol. Toxicol. 2001;41:851–876. doi: 10.1146/annurev.pharmtox.41.1.851.
    1. Rubanyi G.M., Botelho L.H. Endothelins. FASEB J. 1991;5:2713–2720. doi: 10.1096/fasebj.5.12.1916094.
    1. Stern D.M., Nawroth P.P. Modulation of endothelial cell hemostatic properties by tumor necrosis factor. J. Exp. Med. 1986;163:740–745.
    1. Colucci M., Balconi G., Lorenzet R., Pietra A., Locati D., Donati M.B., Semeraro N. Cultured human endothelial cells generate tissue factor in response to endotoxin. J. Clin. Invest. 1983;71:1893–1896. doi: 10.1172/JCI110945.
    1. Lyberg T., Qaldal K.S., Evensen S.A., Prydz H. Cellular cooperation in endothelial cell thromboplastin synthesis. Br. J. Haematol. 1983;53:89–95. doi: 10.1111/j.1365-2141.1983.tb01989.x.
    1. Moore K.L., Bang N.U., Esmon C.T., Esmon N.L. The thrombogenic endothelial cells. Two endotoxin-mediated mechanisms [abstr] Clin Res. 1985;33:35Oa.
    1. Bevilacqua M.P., Pober J.S., Majeau G.R., Cotran R.S., Gimbrone M.A. Interleukin-1 biosynthesis and cell surface expression of procoagulant activity in human vascular endothelial cells. J. Exp. Med. 1984;60:618–623. doi: 10.1084/jem.160.2.618.
    1. Galdal K.S., Lyberg T., Evensen S.A., Nllson E., Prydz H. Thrombin induces thromboplastin synthesis in cultured vascular endothelial cells. Thromb. Haemost. 1985;54:373–376. doi: 10.1055/s-0038-1657742.
    1. Ramasamy I. Inherited bleeding disorders: Disorders of platelet adhesion and aggregation. Crit. Rev. Oncol. Hematol. 2004;49:1–35. doi: 10.1016/S1040-8428(03)00117-3.
    1. Cines D.B., Pollak E.S., Buck C.A., Loscalzo J., Zimmerman G.A., McEver R.P., Pober J.S., Wick T.M., Konkle B.A., Schwartz B.S., et al. Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood. 1998;91:3527–3561.
    1. de Graaf J.C., Banga J.D., Moncada S., Palmer R.M., de Groot P.G., Sixma J.J. Nitric oxide functions as an inhibitor of platelet adhesion under flow conditions. Circulation. 1992;85:2284–2290. doi: 10.1161/01.CIR.85.6.2284.
    1. Pearson J.D., Carleton J.S., Gordon J.L. Metabolism of adenine nucleotides by ectoenzymes of vascular endothelial and smooth muscle cells in culture. Biochem. J. 1980;190:421–429. doi: 10.1042/bj1900421.
    1. Michal F., Thorp R.H. Enhanced adenosine inhibition of platelet aggregation in the presence of cardiac glycosides. Nature. 1966;209:208–209. doi: 10.1038/209208a0.
    1. Sadler J.E. Thrombomodulin structure and function. Thromb. Haemost. 1997;78:392–395. doi: 10.1055/s-0038-1657558.
    1. Stern D.M., Esposito C., Gerlach H., Gerlach M., Ryan J., Handley D., Nawroth P. Endothelium and regulation of coagulation. Diabetes Care. 1991;14:160–166. doi: 10.2337/diacare.14.2.160.
    1. Esmon C.T. The endothelial cell protein C receptor. Thromb. Haemost. 2000;83:639–643. doi: 10.1055/s-0037-1613883.
    1. Esmon C.T. Thrombomodulin as a model of molecular mechanisms that modulate protease specificity and function at the vessel surface. FASEB J. 1995;9:946–955. doi: 10.1096/fasebj.9.10.7615164.
    1. Kato H. Regulation of functions of vascular wall cells by tissue factor pathway inhibitor: Basic and clinical aspects. Arterioscler. Thromb. Vasc. Biol. 2002;22:539–548. doi: 10.1161/.
    1. Mackman N. New insights into the mechanisms of venous thrombosis. J. Clin. Invest. 2012;122:2331–2336. doi: 10.1172/JCI60229.
    1. Aird W.C. Endothelial cell heterogeneity. Crit. Care Med. 2003;31:221–230. doi: 10.1097/01.CCM.0000057847.32590.C1.
    1. Pries A.R., Kuebler W.M. The Vascular Endothelium I. Springer; Berlin/Heidelberg, Germany: 2006. Normal endothelium; pp. 1–40.
    1. Lin F.J., Tsai M.J., Tsai S.Y. Artery and vein formation: A tug of war between different forces. EMBO Rep. 2007;8:920–924. doi: 10.1038/sj.embor.7401076.
    1. Chi J.T., Chang H.Y., Haraldsen G., Jahnsen F.L., Troyanskaya O.G., Chang D.S., Wang Z., Rockson S.G., van de Rijn M., Botstein D., et al. Endothelial cell diversity revealed by global expression profiling. Proc. Natl. Acad. Sci. USA. 2003;100:10623–10628. doi: 10.1073/pnas.1434429100.
    1. Carver L.A., Schnitzer J.E. Proteomic mapping of endothelium and vascular targeting in vivo. In: William C., Aird M.D., editors. Endothelial Biomedicine. Cambridge University Press; Cambridge, UK: 2007. pp. 881–897.
    1. Franke R.P., Fuhrmann R., Hiebl B., Jung F. Influence of various radiographic contrast media on the buckling of endothelial cells. Microvasc. Res. 2008;76:110–113. doi: 10.1016/j.mvr.2008.05.002.
    1. Jung F. From hemorheology to microcirculation and regenerative medicine: Fåhraeus Lecture 2009. Clin. Hemorheol. Microcirc. 2010;45:79–99.
    1. Mai J., Virtue A., Shen J., Wang H., Yang X.F. An evolving new paradigm: Endothelial cells – conditional innate immune cells. J. Hematol. Oncol. 2013;6:61–74. doi: 10.1186/1756-8722-6-61.
    1. Freudenberg N., Riese K.H., Freudenberg M.A. The vascular endothelial system. Structure-function-pathology-reaction to endotoxin shock-methods of investigation. Veröff. Pathol. 1983;120:1–114.
    1. Thorgeirsson G., Robertson A.L., Jr. The vascular endothelium-pathobiologic significance. Am. J. Pathol. 1978;93:803–848.
    1. Gebrane-Younes J., Drouet L., Caen J.P., Orcel L. Heterogeneous distribution of Weibel-Palade bodies and von Willebrand factor along the porcine vascular tree. Am. J. Pathol. 1991;139:1471–1484.
    1. Hawkins B.T., Davis T.P. The Blood-Brain Barrier/Neurovascular Unit in Health and Disease. Pharmacol. Rev. 2005;57:173–185. doi: 10.1124/pr.57.2.4.
    1. Mackie K., Lai Y., Nairn A.C., Greengard P., Pitt B.R., Lazo J.S. Protein phosphorylation in cultured endothelial cells. J. Cell Physiol. 1986;128:367–374. doi: 10.1002/jcp.1041280304.
    1. Snopko R., Guffy T., Rafelson M., Hall E. Serum stimulation of prostacyclin synthesis in aortically, venously and microvascularly derived endothelial cells. Clin. Physiol. Biochem. 1987;5:70–76.
    1. Franke R.P., Fuhrmann R., Mrowietz C., Hiebl B., Jung F. Do radiographic contrast media (Iodixanol or Iomeprol) induce a perturbation of human arterial and/or venous endothelial cells in vitro on extracellular matrix? Clin. Hemorheol. Microcirc. 2012;50:49–54.
    1. Franke R.P., Fuhrmann R., Hiebl B., Jung F. Influence of radiographic contrast media (iodixanol und iomeprol) on the morphology of human arterial and venous endothelial cells on extracellular matrix in vitro. Clin Hemorheol Microcirc. 2011;48:41–56.
    1. Defilippi P., Vanhinsbergh V., Bertolotto A., Rossino P., Silengo L., Tarone G. Differential distribution and modulation of expression of alpha1/beta1 integrin on human endothelial-cells. J Cell Biol. 1991;114:855–863. doi: 10.1083/jcb.114.4.855.
    1. Keuschnigg J., Henttinen T., Auvinen K., Karikoski M., Salmi M., Jalkanen S. The prototype endothelial marker PAL-E is a leukocyte trafficking molecule. Blood. 2009;114:478–484. doi: 10.1182/blood-2008-11-188763.
    1. Hoepken S., Fuhrmann R., Jung F., Franke R.P. Shear resistance of human umbilical endothelial cells on different materials covered with or without extracellular matrix: Controlled in-vitro study. Clin Hemorheol Microcirc. 2009;43:157–166.
    1. Krüger-Genge A., Schulz C., Kratz K., Lendlein A., Jung F. Comparison of two substrate materials used as negative control in endothelialization studies: Glass versus polymeric tissue culture plate. Clin Hemorheol Microcirc. 2018;69:437–445. doi: 10.3233/CH-189904.
    1. Carmeliet P., Jain R.K. Molecular mechanisms and clinical applications of angiogenesis. Nature. 2011;473:298–307. doi: 10.1038/nature10144.
    1. Munaron L., Fiorio Pla A. Endothelial calcium machinery and angiogenesis: Understanding physiology to interfere with pathology. Curr Med Chem. 2009;16:4691–4703. doi: 10.2174/092986709789878210.
    1. Moccia F., Dragoni S., Lodola F., Bonetti E., Bottino C., Guerra G., Laforenza U., Rosti V., Tanzi F. Store-dependent Ca(2+) entry in endothelial progenitor cells as a perspective tool to enhance cell-based therapy and adverse tumour vascularization. Curr Med Chem. 2012;19:5802–5818. doi: 10.2174/092986712804143240.
    1. Jain R.K. Molecular regulation of vessel maturation. Nat Med. 2003;9:685–693. doi: 10.1038/nm0603-685.
    1. Jung F., Franke R.P., Mrowietz C., Wolf S., Kiesewetter H. Capillary occlusion and secondary angiogenesis in a patient with Raynaud’s phenomenon. J Vasc Res. 1992;29:71–74. doi: 10.1159/000158935.
    1. Blocki A., Beyer S., Jung F., Raghunath M. The controversial origin of pericytes during angiogenesis - Implications for cell-based therapeutic angiogenesis and cell-based therapies. Clin Hemorheol Microcirc. 2018;69:215–232. doi: 10.3233/CH-189132.
    1. Beyer S., Koch M., Lee Y.H., Jung F., Blocki A. An In Vitro Model of Angiogenesis during Wound Healing Provides Insights into the Complex Role of Cells and Factors in the Inflammatory and Proliferation Phase. Int J Mol Sci. 2018;19:2913. doi: 10.3390/ijms19102913.
    1. Blocki A., Wang Y., Koch M., Goralczyk A., Beyer S., Agarwal N., Lee M., Moonshi S., Dewavrin J.Y., Peh P., et al. Sourcing of an alternative pericyte-like cell type from peripheral blood in clinically relevant numbers for therapeutic angiogenic applications. Mol Ther. 2015;23:510–522. doi: 10.1038/mt.2014.232.
    1. Barrientos S., Stojadinovic O., Golinko M.S., Brem H., Tomic-Canic M. Growth factors and cytokines in wound healing. Wound Repair Regen. 2008;16:585–601. doi: 10.1111/j.1524-475X.2008.00410.x.
    1. Werner S., Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev. 2003;83:835–870. doi: 10.1152/physrev.2003.83.3.835.
    1. Kobayashi H., Lin P.C. Angiogenesis links chronic inflammation with cancer. Methods Mol Biol. 2009;511:185–191.
    1. Kundu J.K., Surh Y.J. Inflammation: Gearing the journey to cancer. Mutat Res. 2008;659:15–30. doi: 10.1016/j.mrrev.2008.03.002.
    1. Cheng R., Ma J.X. Angiogenesis in diabetes and obesity. Rev Endocr Metab Disord. 2015;16:67–75. doi: 10.1007/s11154-015-9310-7.
    1. Ribot J., Caliaperoumal G., Paquet J., Boisson-Vidal C., Petite H., Anagnostou F. Type 2 diabetes alters mesenchymal stem cell secretome composition and angiogenic properties. J Cell Mol Med. 2017;21:349–363. doi: 10.1111/jcmm.12969.
    1. Hughes C.C. Endothelial-stromal interactions in angiogenesis. Curr Opin Hematol. 2008;15:204–209. doi: 10.1097/MOH.0b013e3282f97dbc.
    1. Verma R.P., Hansch C. Matrix metalloproteinases (MMPs): Chemical-biological functions and (Q)SARs. Bioorg. Med. Chem. 2007;15:2223–2268. doi: 10.1016/j.bmc.2007.01.011.
    1. Tang H., Lee M., Kim E.H., Bishop D., Rodgers G.M. siRNA-knockdown of ADAMTS-13 modulates endothelial cell angiogenesis. Microvasc Res. 2017;113:65–70. doi: 10.1016/j.mvr.2017.05.007.
    1. Rickert D., Lendlein A., Kelch S., Moses M.A., Franke R.P. Expression of MMPs and TIMPs in primary epithelial cell cultures of the upper aerodigestive tract seeded on the surface of a novel polymeric biomaterial. Clin Hemorheol Microcirc. 2005;32:117–128.
    1. Rhodes J.M., Simons M. The extracellular matrix and blood vessel formation: Not just a scaffold. J Cell Mol Med. 2007;11:176–205. doi: 10.1111/j.1582-4934.2007.00031.x.
    1. Jung F., Franke R.P., Mrowietz C., Wolf S., Kiesewetter H., Wenzel E. Capillary occlusion and secondary angiogenesis: Case report. Int J Microcirc Clin Exp. 1992;11:167–170.
    1. Baer-Suryadinata C., Bollinger A. Transcapillary diffusion of Na-fluorescein measured by a ‘large window technique’ in skin areas of the forefoot. Int J Microcirc Clin Exp. 1985;4:217–228.
    1. Eelen G., Cruys B., Welti J., De Bock K., Carmeliet P. Control of vessel sprouting by genetic and metabolic determinants. Trends Endocrinol Metab. 2013;24:589–596. doi: 10.1016/j.tem.2013.08.006.
    1. Ghesquiere B., Wong B.W., Kuchnio A., Carmeliet P. Metabolism of stromal and immune cells in health and disease. Nature. 2014;511:167–176. doi: 10.1038/nature13312.
    1. Jakobsson L., Franco C.A., Bentley K., Collins R.T., Ponsioen B., Aspalter I.M., Rosewell I., Busse M., Thurston G., Medvinsky A., et al. Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat Cell Biol. 2010;12:943–953. doi: 10.1038/ncb2103.
    1. Potente M., Gerhardt H., Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell. 2011;146:873–887. doi: 10.1016/j.cell.2011.08.039.
    1. Phng L.K., Gerhardt H. Angiogenesis: A team effort coordinated by notch. Dev. Cell. 2009;16:196–208. doi: 10.1016/j.devcel.2009.01.015.
    1. You C., Zhao K., Dammann P., Keyvani K., Kreitschmann-Andermahr I., Sure U., Zhu Y. EphB4 forward signaling mediates angiogenesis caused by CCM3/PDCD10-ablation. J Cell Mol Med. 2017;21:1848–1858. doi: 10.1111/jcmm.13105.
    1. Bentley K., Jones M., Cruys B. Predicting the future: Towards symbiotic computational and experimental angiogenesis research. Exp Cell Res. 2013;319:1240–1246. doi: 10.1016/j.yexcr.2013.02.001.
    1. Kiriakidis S., Henze A.T., Kruszynska-Ziaja I., Skobridis K., Theodorou V., Paleolog E.M., Mazzone M. Factor-inhibiting HIF-1 (FIH-1) is required for human vascular endothelial cell survival. FASEB J. 2015;29:2814–2827. doi: 10.1096/fj.14-252379.
    1. Anderson J.M., McNally A.K. Biocompatibility of implants: Lymphocyte/ macrophage interactions. Semin Immunopathol. 2011;33:221–233. doi: 10.1007/s00281-011-0244-1.
    1. Andrade S.P., Ferreira M.A. The Sponge Implant Model of Angiogenesis. Methods Mol Biol. 2016;1430:333–343.
    1. DiEgidio P., Friedman H.I., Gourdie R.G., Riley A.E., Yost M.J., Goodwin R.L. Biomedical implant capsule formation: Lessons learned and the road ahead. Ann Plast Surg. 2014;73:451–460. doi: 10.1097/SAP.0000000000000287.
    1. Klopfleisch R., Jung F. The pathology of the foreign body reaction against biomaterials. J. Biomed. Mater. Res. A. 2017;105:927–940. doi: 10.1002/jbm.a.35958.
    1. Anderson J.M., Rodriguez A., Chang D.T. Foreign body reaction to biomaterials. Semin. Immunol. 2008;20:86–100. doi: 10.1016/j.smim.2007.11.004.
    1. Ullm S., Krüger A., Tondera C., Gebauer T.P., Neffe A.T., Lendlein A., Jung F., Pietzsch J. Biocompatibility and inflammatory response in vitro and in vivo to gelatin-based biomaterials with tailorable elastic properties. Biomaterials. 2014;35:9755–9766. doi: 10.1016/j.biomaterials.2014.08.023.
    1. Fu B.M. Tumor Metastasis in the Microcirculation. Adv Exp Med Biol. 2018;1097:201–218.
    1. Hekimian K., Meisezahl S., Trompelt K., Rabenstein C., Pachmann K. Epithelial cell dissemination and re-adhesion: Analysis of factors contributing to metastasis formation in breast cancer. ISRN Oncol. 2012;2012:601810.

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