Published 6 issues per year
ISSN Print: 0278-940X
ISSN Online: 1943-619X
Indexed in
Mechanics of Endothelial Cell Architecture and Vascular Permeability
ABSTRACT
Blood vessel walls form a selective barrier to the transport of materials between blood and tissue, and the endothelium contributes significantly to this barrier function. The role of the endothelium is particularly important in thin-walled vessels, such as venules, because during tissue inflammation the endothelial junctions widen in localized areas and gaps form, thus compromising the barrier function. The mechanisms of endothelial gap formation are still under question. In this review we describe what is known about the structure of endothelial cell-cell junctions and how this structure can change during inflammation. We then consider two possible mechanisms by which endothelial gaps are formed: active endothelial cell contraction or breakdown of the junctional complex, followed by passive recoil. Using measured values of the mechanical properties of endothelial cells, and the forces to which they are subjected, we calculate that gap formation by breakdown of cellular adhesion, followed by passive recoil, is a feasible mechanism. Finally, since endothelial cell surfaces, including junctions, are coated with a glycocalyx, we consider the question of whether changes in the glycocalyx can markedly increase endothelial permeability. We conclude that gap formation can occur by active contraction or by breakdown of adhesion, depending on the inflammatory mediator, and that the responses of the glycocalyx may also play an important role in the regulation of microvascular permeability.
-
Tatara Tsuneo, Itani Motoi, Sugi Takashi, Fujita Kimihiko, Physical plugging does not account for attenuation of capillary leakage by hydroxyethyl starch 130/0.4: A synthetic gel layer model, Journal of Biomedical Materials Research Part B: Applied Biomaterials, 101B, 1, 2013. Crossref
-
Falk Matthias M., Fong John T., Kells Rachael M., O’Laughlin Michael C., Kowal Tia J., Thévenin Anastasia F., Degradation of Endocytosed Gap Junctions by Autophagosomal and Endo-/lysosomal Pathways: A Perspective, The Journal of Membrane Biology, 245, 8, 2012. Crossref
-
Di Vizio Dolores, Morello Matteo, Dudley Andrew C., Schow Peter W., Adam Rosalyn M., Morley Samantha, Mulholland David, Rotinen Mirja, Hager Martin H., Insabato Luigi, Moses Marsha A., Demichelis Francesca, Lisanti Michael P., Wu Hong, Klagsbrun Michael, Bhowmick Neil A., Rubin Mark A., D'Souza-Schorey Crislyn, Freeman Michael R., Large Oncosomes in Human Prostate Cancer Tissues and in the Circulation of Mice with Metastatic Disease, The American Journal of Pathology, 181, 5, 2012. Crossref
-
Parsons-Wingerter Patrica, Radhakrishan Krishnan, A Two-Dimensional Model of Cell-Cell Aggregation: Application to Hepatocytes Undergoing Random Motion, 41st Aerospace Sciences Meeting and Exhibit, 2003. Crossref
-
Martins‐Green Manuela, Petreaca Melissa, Yao Min, Chapter 8 An Assay System for In Vitro Detection of Permeability in Human “Endothelium”, in Angiogenesis - In Vitro Systems, 443, 2008. Crossref
-
Patterson Carolyn E., Lum Hazel, Johan Groeneveld A.B., Chapter 15 Advances in protection of endothelial barrier function, in Perspectives on Lung Endothelial Barrier Function, 35, 2005. Crossref
-
Patterson Carolyn E., Matthay Michael A., Chapter 16 Looking to the future as keepers of the dam, in Perspectives on Lung Endothelial Barrier Function, 35, 2005. Crossref
-
Chamorro-Jorganes Aránzazu, Araldi Elisa, Suárez Yajaira, MicroRNAs as pharmacological targets in endothelial cell function and dysfunction, Pharmacological Research, 75, 2013. Crossref
-
Patterson Carolyn E., Matthay Michael A., Chapter 1 The cellular and molecular foundations of pulmonary edema, in Perspectives on Lung Endothelial Barrier Function, 35, 2005. Crossref
-
Patterson Carolyn E., Stamenović Dimitrije, Chapter 2. Molecular architecture of the endothelium, in Perspectives on Lung Endothelial Barrier Function, 35, 2005. Crossref
-
Muradashvili Nino, Lominadze David, Role of fibrinogen in cerebrovascular dysfunction after traumatic brain injury, Brain Injury, 27, 13-14, 2013. Crossref
-
Corcoran Brendan M., Black Alexander, Anderson Heather, McEwan Joanna Dukes, French Anne, Smith Paul, Devine Craig, Identification of surface morphologic changes in the mitral valve leaflets and chordae tendineae of dogs with myxomatous degeneration, American Journal of Veterinary Research, 65, 2, 2004. Crossref
-
Belvitch Patrick, Adyshev Djanybek, Elangovan Venkateswaran R., Brown Mary E., Naureckas Caitlin, Rizzo Alicia N., Siegler Jessica H., Garcia Joe G.N., Dudek Steven M., Proline-rich region of non-muscle myosin light chain kinase modulates kinase activity and endothelial cytoskeletal dynamics, Microvascular Research, 95, 2014. Crossref
-
GUO MINGZHANG, Wu Mack H., Granger Harris J., Yuan Sarah Y., Focal Adhesion Kinase in Neutrophil-Induced Microvascular Hyperpermeability, Microcirculation, 12, 2, 2005. Crossref
-
Brookes Zoë L. S., Kaufman Susan, Effects of atrial natriuretic peptide on the extrasplenic microvasculature and lymphatics in the ratin vivo, The Journal of Physiology, 565, 1, 2005. Crossref
-
Arts C.H.P., de Groot Ph.G., Heijnen-Snyder G.J., Blankensteijn J.D., Eikelboom B.C., Slaper-Cortenbach I.C.M., Application of a clinical grade CD34-mediated method for the enrichment of microvascular endothelial cells from fat tissue, Cytotherapy, 6, 1, 2004. Crossref
-
Wei Liping, Sun Dongdong, Yin Zhiyong, Yuan Yuan, Hwang Andrew, Zhang Yingmei, Si Rui, Zhang Rongqing, Guo Wenyi, Cao Feng, Wang Haichang, A PKC-β inhibitor protects against cardiac microvascular ischemia reperfusion injury in diabetic rats, Apoptosis, 15, 4, 2010. Crossref
-
Muradashvili Nino, Tyagi Neetu, Tyagi Reeta, Munjal Charu, Lominadze David, Fibrinogen alters mouse brain endothelial cell layer integrity affecting vascular endothelial cadherin, Biochemical and Biophysical Research Communications, 413, 4, 2011. Crossref
-
Waschke Jens, Golenhofen Nikola, Kurzchalia Teymuras V., Drenckhahn Detlev, Protein kinase C-mediated endothelial barrier regulation is caveolin-1-dependent, Histochemistry and Cell Biology, 126, 1, 2006. Crossref
-
Durán Walter N, Sánchez Fabiola A, Breslin Jerome W, Microcirculatory Exchange Function, in Microcirculation, 2008. Crossref
-
Wei Liping, Yin Zhiyong, Yuan Yuan, Hwang Andrew, Lee Andrew, Sun Dongdong, Li Fei, Di Chunxia, Zhang Rongqing, Cao Feng, Wang Haichang, A PKC-β inhibitor treatment reverses cardiac microvascular barrier dysfunction in diabetic rats, Microvascular Research, 80, 1, 2010. Crossref
-
Mints Miriam, Hultenby Kjell, Zetterberg Eva, Blomgren Bo, Falconer Christian, Rogers Rick, Palmblad Jan, Wall discontinuities and increased expression of vascular endothelial growth factor-A and vascular endothelial growth factor receptors 1 and 2 in endometrial blood vessels of women with menorrhagia, Fertility and Sterility, 88, 3, 2007. Crossref
-
Wolka Anne M, Huber Jason D, Davis Thomas P, Pain and the blood–brain barrier: obstacles to drug delivery, Advanced Drug Delivery Reviews, 55, 8, 2003. Crossref
-
Bammens Bert, Urea and Uremic Solutes: How Does Peritoneal Dialysis Work?, Seminars in Nephrology, 31, 2, 2011. Crossref
-
Yu Yang, Lv Ning, Lu Zheng, Zheng Yan-Yan, Zhang Wen-Cheng, Chen Chen, Peng Ya-Jing, He Wei-Qi, Meng Fan-Qing, Zhu Min-Sheng, Chen Hua-Qun, Deletion of myosin light chain kinase in endothelial cells has a minor effect on the lipopolysaccharide-induced increase in microvascular endothelium permeability in mice, FEBS Journal, 279, 8, 2012. Crossref
-
Dhar-Mascareño Manya, Cárcamo Juan M., Golde David W., Hypoxia–reoxygenation-induced mitochondrial damage and apoptosis in human endothelial cells are inhibited by vitamin C, Free Radical Biology and Medicine, 38, 10, 2005. Crossref
-
Durán Walter N., Sánchez Fabiola A., Breslin Jerome W., Microcirculatory Exchange Function, in Comprehensive Physiology, 2008. Crossref
-
Lund A.K., Oxidants and Endothelial Dysfunction, in Comprehensive Toxicology, 2010. Crossref
-
Vlachou E., Gosling P., Moiemen N.S., Microalbuminuria: A marker of endothelial dysfunction in thermal injury, Burns, 32, 8, 2006. Crossref
-
Nowatzki Jenifer, de Sene Reginaldo Vieira, Paludo Katia Sabrina, Veiga Silvio Sanches, Oliver Constance, Jamur Maria Célia, Nader Helena Bonciani, Trindade Edvaldo S., Franco Célia Regina C., Brown spider venom toxins interact with cell surface and are endocytosed by rabbit endothelial cells, Toxicon, 56, 4, 2010. Crossref
-
Yu Hang, Wang Ping, An Ping, Yixue Xue, Recombinant Human Angiopoietin-1 Ameliorates the Expressions of ZO-1, Occludin, VE-cadherin, and PKCα Signaling after Focal Cerebral Ischemia/Reperfusion in Rats, Journal of Molecular Neuroscience, 46, 1, 2012. Crossref
-
Feinberg Adam W., Schumacher James F., Brennan Anthony B., Engineering high-density endothelial cell monolayers on soft substrates, Acta Biomaterialia, 5, 6, 2009. Crossref
-
Yuan Sarah Y., Protein kinase signaling in the modulation of microvascular permeability, Vascular Pharmacology, 39, 4-5, 2002. Crossref
-
Trache Andreea, Trzeciakowski Jerome P., Gardiner Lesley, Sun Zhe, Muthuchamy Mariappan, Guo Mingzhang, Yuan Sarah Y., Meininger Gerald A., Histamine Effects on Endothelial Cell Fibronectin Interaction Studied by Atomic Force Microscopy, Biophysical Journal, 89, 4, 2005. Crossref
-
Williams Donna A., Change in shear stress (Δτ)/hydraulic conductivity (Lp) relationship after pronase treatment of individual capillaries in situ, Microvascular Research, 73, 1, 2007. Crossref
-
Lukyanenko Valeriy, Therapeutic Nano-Object Delivery to Subdomains of Cardiac Myocytes, in Organelle-Specific Pharmaceutical Nanotechnology, 2010. Crossref
-
Pfaltzgraff Elise R., Bader David M., Heterogeneity in vascular smooth muscle cell embryonic origin in relation to adult structure, physiology, and disease, Developmental Dynamics, 244, 3, 2015. Crossref
-
Kaestner Lars, Tian Qinghai, Kaiser Elisabeth, Xian Wenying, Müller Andreas, Oberhofer Martin, Ruppenthal Sandra, Sinnecker Daniel, Tsutsui Hidekazu, Miyawaki Atsushi, Moretti Alessandra, Lipp Peter, Genetically Encoded Voltage Indicators in Circulation Research, International Journal of Molecular Sciences, 16, 9, 2015. Crossref
-
Panasenko Grigory, Volpert Vitaly, Homogenization of a one-dimensional diffusion - discrete absorption equation with feedback, Applicable Analysis, 95, 7, 2016. Crossref
-
Abukabda Alaeddin B., Stapleton Phoebe A., McBride Carroll R., Yi Jinghai, Nurkiewicz Timothy R., Heterogeneous Vascular Bed Responses to Pulmonary Titanium Dioxide Nanoparticle Exposure, Frontiers in Cardiovascular Medicine, 4, 2017. Crossref
-
Lund AK., Oxidants and Endothelial Dysfunction, in Comprehensive Toxicology, 2018. Crossref
-
Juchem Gerd, Weiss Dominik R., Knott Maria, Senftl Anton, Förch Stefan, Fischlein Theodor, Kreuzer Eckart, Reichart Bruno, Laufer Stefan, Nees Stephan, Regulation of coronary venular barrier function by blood borne inflammatory mediators and pharmacological tools: insights from novel microvascular wall models, American Journal of Physiology-Heart and Circulatory Physiology, 302, 3, 2012. Crossref
-
Waschke J., Curry F. E., Adamson R. H., Drenckhahn D., Regulation of actin dynamics is critical for endothelial barrier functions, American Journal of Physiology-Heart and Circulatory Physiology, 288, 3, 2005. Crossref
-
de Arêdes Brum Carla, Duarte Igor Dimitri Gama, Webb R. Clinton, Leite Romulo, Disruption of microtubular network attenuates histamine-induced dilation in rat mesenteric vessels, American Journal of Physiology-Cell Physiology, 288, 2, 2005. Crossref
-
Fierabracci Alessandra, Insights into the Diagnostic Potential of Extracellular Vesicles and Their miRNA Signature from Liquid Biopsy as Early Biomarkers of Diabetic Micro/Macrovascular Complications, International Journal of Molecular Sciences, 18, 9, 2017. Crossref
-
Adamson R. H., Ly J. C., Sarai R. K., Lenz J. F., Altangerel A., Drenckhahn D., Curry F. E., Epac/Rap1 pathway regulates microvascular hyperpermeability induced by PAF in rat mesentery, American Journal of Physiology-Heart and Circulatory Physiology, 294, 3, 2008. Crossref
-
Irwin D. C., Tissot van Patot M. C., Tucker A., Bowen R., Direct ANP inhibition of hypoxia-induced inflammatory pathways in pulmonary microvascular and macrovascular endothelial monolayers, American Journal of Physiology-Lung Cellular and Molecular Physiology, 288, 5, 2005. Crossref
-
Mochizuki Seiichi, Vink Hans, Hiramatsu Osamu, Kajita Tatsuya, Shigeto Fumiyuki, Spaan Jos A. E., Kajiya Fumihiko, Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release, American Journal of Physiology-Heart and Circulatory Physiology, 285, 2, 2003. Crossref
-
Mikhail Marianne, Vachon Pierre H., D’Orléans-Juste Pedro, Jacques Danielle, Bkaily Ghassan, Role of endothelin-1 and its receptors, ETAand ETB, in the survival of human vascular endothelial cells, Canadian Journal of Physiology and Pharmacology, 95, 10, 2017. Crossref
-
Penna Claudia, Pagliaro Pasquale, Chromogranin A-Derived Peptides in Cardiac Pre- and Post-conditioning, in Chromogranins: from Cell Biology to Physiology and Biomedicine, 2017. Crossref
-
Waschke J., Drenckhahn D., Adamson R. H., Barth H., Curry F. E., cAMP protects endothelial barrier functions by preventing Rac-1 inhibition, American Journal of Physiology-Heart and Circulatory Physiology, 287, 6, 2004. Crossref
-
Kim Joanna, Cooper John A., Yap Alpha, Septins regulate junctional integrity of endothelial monolayers, Molecular Biology of the Cell, 29, 14, 2018. Crossref
-
Fernández-Hernando Carlos, Suárez Yajaira, MicroRNAs in endothelial cell homeostasis and vascular disease, Current Opinion in Hematology, 25, 3, 2018. Crossref
-
Belvitch Patrick, Htwe Yu Maw, Brown Mary E., Dudek Steven, Cortical Actin Dynamics in Endothelial Permeability, in Membranes in Pulmonary Vascular Disease, 82, 2018. Crossref
-
Michiels Carine, Endothelial cell functions, Journal of Cellular Physiology, 196, 3, 2003. Crossref
-
Blaurock-Möller Nancy, Gröger Marko, Siwczak Fatina, Dinger Julia, Schmerler Diana, Mosig Alexander S., Kiehntopf Michael, CAAP48, a New Sepsis Biomarker, Induces Hepatic Dysfunction in an in vitro Liver-on-Chip Model, Frontiers in Immunology, 10, 2019. Crossref
-
Carpick Robert W., Batteas James D., Scanning Probe Studies of Nanoscale Adhesion Between Solids in the Presence of Liquids and Monolayer Films, in Springer Handbook of Nanotechnology, 2004. Crossref
-
Carpick Robert, Batteas James, Boer Maarten, Scanning Probe Studies of Nanoscale Adhesion Between Solids in the Presence of Liquids and Monolayer Films, in Springer Handbook of Nanotechnology, 2007. Crossref
-
Bhattacharya Bishwajit, Maerz Linda L., Fluid and Electrolytes, in Surgical Metabolism, 2020. Crossref
-
Groten Tanja, Pierce Amy A., Huen Arthur C., Schnaper H. William, 17 β‐estradiol transiently disrupts adherens junctions in endothelial cells, The FASEB Journal, 19, 10, 2005. Crossref
-
Flessner Michael F., Endothelial Glycocalyx and the Peritoneal Barrier, Peritoneal Dialysis International: Journal of the International Society for Peritoneal Dialysis, 28, 1, 2008. Crossref
-
Bedenbender Katrin, Schmeck Bernd T., Endothelial Ribonuclease 1 in Cardiovascular and Systemic Inflammation, Frontiers in Cell and Developmental Biology, 8, 2020. Crossref
-
Kim Joanna, Cooper John A., Junctional Localization of Septin 2 Is Required for Organization of Junctional Proteins in Static Endothelial Monolayers, Arteriosclerosis, Thrombosis, and Vascular Biology, 2020. Crossref
-
Villalba Nuria, Baby Sheon, Yuan Sarah Y., The Endothelial Glycocalyx as a Double-Edged Sword in Microvascular Homeostasis and Pathogenesis, Frontiers in Cell and Developmental Biology, 9, 2021. Crossref
-
Belvitch Patrick, Brown Mary E., Brinley Brittany N., Letsiou Eleftheria, Rizzo Alicia N., Garcia Joe G.N., Dudek Steven M., The ARP 2/3 complex mediates endothelial barrier function and recovery, Pulmonary Circulation, 7, 1, 2017. Crossref
-
Tarbell John M., Mass Transport in Arteries and the Localization of Atherosclerosis, Annual Review of Biomedical Engineering, 5, 1, 2003. Crossref
-
Neubauer Katharina, Zieger Barbara, Role of Septins in Endothelial Cells and Platelets, Frontiers in Cell and Developmental Biology, 9, 2021. Crossref
-
Taghavi Sharven, Abdullah Sarah, Duchesne Juan, Pociask Derek, Kolls Jay, Jackson-Weaver Olan, Interleukin 22 mitigates endothelial glycocalyx shedding after lipopolysaccharide injury, Journal of Trauma and Acute Care Surgery, 90, 2, 2021. Crossref
-
Li Tian-Xiao, Liu Rui-Huan, Wang Xiao-Bing, Luo Jun, Luo Jian-Guang, Kong Ling-Yi, Yang Ming-Hua, Hypoxia-Protective Azaphilone Adducts from Peyronellaea glomerata, Journal of Natural Products, 81, 5, 2018. Crossref
-
Jo Myung Hyun, Kim Byoung Choul, Sung Keewon, Panettieri Reynold A., An Steven S., Liu Jian, Ha Taekjip, Molecular Nanomechanical Mapping of Histamine-Induced Smooth Muscle Cell Contraction and Shortening, ACS Nano, 15, 7, 2021. Crossref
-
Medina-Leyte Diana Jhoseline, Zepeda-García Oscar, Domínguez-Pérez Mayra, González-Garrido Antonia, Villarreal-Molina Teresa, Jacobo-Albavera Leonor, Endothelial Dysfunction, Inflammation and Coronary Artery Disease: Potential Biomarkers and Promising Therapeutical Approaches, International Journal of Molecular Sciences, 22, 8, 2021. Crossref
-
Knezevic Ivana I., Predescu Sanda A., Neamu Radu F., Gorovoy Matvey S., Knezevic Nebojsa M., Easington Cordus, Malik Asrar B., Predescu Dan N., Tiam1 and Rac1 Are Required for Platelet-activating Factor-induced Endothelial Junctional Disassembly and Increase in Vascular Permeability, Journal of Biological Chemistry, 284, 8, 2009. Crossref
-
Yuan Sarah Y., Wu Mack H., Ustinova Elena E., Guo Mingzhang, Tinsley John H., de Lanerolle Primal, Xu Wenjuan, Myosin Light Chain Phosphorylation in Neutrophil-Stimulated Coronary Microvascular Leakage, Circulation Research, 90, 11, 2002. Crossref
-
Chen Chia-Chi, Chen Li-Li, Hsu Yu-Ting, Liu Ko-Jiunn, Fan Chi-Shuan, Huang Tze-Sing, The Endothelin-Integrin Axis Is Involved in Macrophage-induced Breast Cancer Cell Chemotactic Interactions with Endothelial Cells, Journal of Biological Chemistry, 289, 14, 2014. Crossref
-
Kahles Timo, Luedike Peter, Endres Matthias, Galla Hans-Joachim, Steinmetz Helmuth, Busse Rudi, Neumann-Haefelin Tobias, Brandes Ralf P., NADPH Oxidase Plays a Central Role in Blood-Brain Barrier Damage in Experimental Stroke, Stroke, 38, 11, 2007. Crossref
-
Mangiafico Marco, Caff Andrea, Costanzo Luca, The Role of Heparin in COVID-19: An Update after Two Years of Pandemics, Journal of Clinical Medicine, 11, 11, 2022. Crossref
-
Tremblay P-L, Auger F A, Huot J, Regulation of transendothelial migration of colon cancer cells by E-selectin-mediated activation of p38 and ERK MAP kinases, Oncogene, 25, 50, 2006. Crossref
-
Maheshwari Akhil, Mezu-Ndubuisi Olachi J, Role of the Endothelium in Neonatal Diseases, Newborn, 1, 1, 2022. Crossref
-
Hocke Andreas C., Temmesfeld-Wollbrueck Bettina, Schmeck Bernd, Berger Katharina, Frisch Eckehard M., Witzenrath Martin, Brell Bernhard, Suttorp Norbert, Hippenstiel Stefan, Perturbation of endothelial junction proteins by Staphylococcus aureus α-toxin: inhibition of endothelial gap formation by adrenomedullin, Histochemistry and Cell Biology, 126, 3, 2006. Crossref
-
Kurulgan Demirci Eylem, Demirci Taylan, Linder Peter, Trzewik Juergen, Gierkowski Jessica Ricarda, Gossmann Matthias, Kayser Peter, Porst Dariusz, Digel Ilya, Artmann Gerhard Michael, Temiz Artmann Aysegul, rhAPC reduces the endothelial cell permeability via a decrease of contractile tensions induced by endothelial cells, Journal of Bioscience and Bioengineering, 114, 2, 2012. Crossref