Hydrostatic pressure drives sprouting angiogenesis via adherens junction remodelling and YAP signalling.
Hydrostatic Pressure
Adherens Junctions
/ metabolism
Humans
Neovascularization, Physiologic
YAP-Signaling Proteins
/ metabolism
Signal Transduction
Human Umbilical Vein Endothelial Cells
/ metabolism
Adaptor Proteins, Signal Transducing
/ metabolism
Transcription Factors
/ metabolism
Animals
Cadherins
/ metabolism
Endothelial Cells
/ metabolism
Cell Movement
Angiogenesis
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
03 Aug 2024
03 Aug 2024
Historique:
received:
08
11
2023
accepted:
17
07
2024
medline:
4
8
2024
pubmed:
4
8
2024
entrez:
3
8
2024
Statut:
epublish
Résumé
Endothelial cell physiology is governed by its unique microenvironment at the interface between blood and tissue. A major contributor to the endothelial biophysical environment is blood hydrostatic pressure, which in mechanical terms applies isotropic compressive stress on the cells. While other mechanical factors, such as shear stress and circumferential stretch, have been extensively studied, little is known about the role of hydrostatic pressure in the regulation of endothelial cell behavior. Here we show that hydrostatic pressure triggers partial and transient endothelial-to-mesenchymal transition in endothelial monolayers of different vascular beds. Values mimicking microvascular pressure environments promote proliferative and migratory behavior and impair barrier properties that are characteristic of a mesenchymal transition, resulting in increased sprouting angiogenesis in 3D organotypic model systems ex vivo and in vitro. Mechanistically, this response is linked to differential cadherin expression at the adherens junctions, and to an increased YAP expression, nuclear localization, and transcriptional activity. Inhibition of YAP transcriptional activity prevents pressure-induced sprouting angiogenesis. Together, this work establishes hydrostatic pressure as a key modulator of endothelial homeostasis and as a crucial component of the endothelial mechanical niche.
Identifiants
pubmed: 39097636
doi: 10.1038/s42003-024-06604-9
pii: 10.1038/s42003-024-06604-9
doi:
Substances chimiques
YAP-Signaling Proteins
0
Adaptor Proteins, Signal Transducing
0
Transcription Factors
0
YAP1 protein, human
0
Cadherins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
940Subventions
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Swiss National Science Foundation)
ID : 205321_188828
Informations de copyright
© 2024. The Author(s).
Références
Barrasa-Ramos, S., Dessalles, C. A., Hautefeuille, M. & Barakat, A. I. Mechanical regulation of the early stages of angiogenesis. J. R. Soc. Interface 19, 20220360 (2022).
pubmed: 36475392
pmcid: 9727679
doi: 10.1098/rsif.2022.0360
Prystopiuk, V. et al. A two-phase response of endothelial cells to hydrostatic pressure. J. Cell Sci. 131, jcs206920 (2018).
Khurana, R., Simons, M., Martin, J. F. & Zachary, I. C. Role of angiogenesis in cardiovascular disease: a critical appraisal. Circulation 112, 1813–1824 (2005).
pubmed: 16172288
doi: 10.1161/CIRCULATIONAHA.105.535294
Carmeliet, P. Angiogenesis in health and disease. Nat. Med. 9, 653–660 (2003).
pubmed: 12778163
doi: 10.1038/nm0603-653
Xia, C. Y. et al. Analysis of blood flow and local expression of angiogenesis‑associated growth factors in infected wounds treated with negative pressure wound therapy. Mol. Med. Rep. 9, 1749–1754 (2014).
pubmed: 24584462
doi: 10.3892/mmr.2014.1997
Yoshino, D. & Sato, M. Early-stage dynamics in vascular endothelial cells exposed to hydrostatic pressure. J. Biomech. Eng. 2019. 141, 091006.
Flournoy, J., Ashkanani, S. & Chen, Y. Mechanical regulation of signal transduction in angiogenesis. Front. Cell Dev. Biol. 10, 933474 (2022).
pubmed: 36081909
pmcid: 9447863
doi: 10.3389/fcell.2022.933474
Galie, P. A. et al. Fluid shear stress threshold regulates angiogenic sprouting. Proc. Natl Acad. Sci. USA 111, 7968–7973 (2014).
pubmed: 24843171
pmcid: 4050561
doi: 10.1073/pnas.1310842111
Song, J. W. & Munn, L. L. Fluid forces control endothelial sprouting. Proc. Natl Acad. Sci. USA 108, 15342–15347 (2011).
pubmed: 21876168
pmcid: 3174629
doi: 10.1073/pnas.1105316108
Jufri, N. F., Mohamedali, A., Avolio, A. & Baker, M. S. Mechanical stretch: physiological and pathological implications for human vascular endothelial cells. Vasc. Cell 7, 8 (2015).
pubmed: 26388991
pmcid: 4575492
doi: 10.1186/s13221-015-0033-z
Kretschmer, M., Rüdiger, D. & Zahler, S. Mechanical Aspects of Angiogenesis. Cancers 13, 4987 (2021).
pubmed: 34638470
pmcid: 8508205
doi: 10.3390/cancers13194987
Lancerotto, L. & Orgill, D. P. Mechanoregulation of Angiogenesis in Wound Healing. Adv. Wound Care 3, 626–634 (2014).
doi: 10.1089/wound.2013.0491
Adair, T. H. & Montani, J. P. Angiogenesis. (Morgan & Claypool Life Sciences, San Rafael, CA).
Pappano, A. J. & Withrow, G. W. Cardiovascular Physiology (Elsevier, 2013).
Hall, J. E. Guyton and Hall Textbook of Medical Physiology (Elsevier Health Sciences, 2020).
Dawson, T. Allometric relations and scaling laws for the cardiovascular system of mammals. Systems 2, 168–185 (2014).
doi: 10.3390/systems2020168
White, C. R. & Seymour, R. S. The role of gravity in the evolution of mammalian blood pressure. Evolution 68, 901–908 (2014).
pubmed: 24152198
doi: 10.1111/evo.12298
Sandal, P. H., Damgaard, M. & Secher, N. H. Comments on the review ‘Does mean arterial blood pressure scale with body mass in mammals? Effect of measurement of blood pressure’ Acta Physiol (Oxf). Acta Physiol. 228, e13407 (2020).
doi: 10.1111/apha.13407
Poulsen, C. B., Wang, T., Assersen, K., Iversen, N. K. & Damkjaer, M. Does mean arterial blood pressure scale with body mass in mammals? Effects of measurement of blood pressure. Acta Physiol. 222, e13010 (2018).
doi: 10.1111/apha.13010
Acevedo, A. D., Bowser, S. S., Gerritsen, M. E. & Bizios, R. Morphological and proliferative responses of endothelial cells to hydrostatic pressure: role of fibroblast growth factor. J. Cell Physiol. 157, 603–614 (1993).
pubmed: 8253872
doi: 10.1002/jcp.1041570321
Salwen, S. A., Szarowski, D. H., Turner, J. N. & Bizios, R. Three-dimensional changes of the cytoskeleton of vascular endothelial cells exposed to sustained hydrostatic pressure. Med. Biol. Eng. Comput. 36, 520–527 (1998).
pubmed: 10198540
doi: 10.1007/BF02523225
Schwartz, E. A., Bizios, R., Medow, M. S. & Gerritsen, M. E. Exposure of human vascular endothelial cells to sustained hydrostatic pressure stimulates proliferation - Involvement of the alpha(v) integrins. Circ. Res. 84, 315–322 (1999).
pubmed: 10024305
doi: 10.1161/01.RES.84.3.315
Shin, H. Y., Gerritsen, M. E. & Bizios, R. Regulation of endothelial cell proliferation and apoptosis by cyclic pressure. Ann. Biomed. Eng. 30, 297–304 (2002).
pubmed: 12051615
doi: 10.1114/1.1458595
Sumpio, B. E., Widmann, M. D., Ricotta, J., Awolesi, M. A. & Watase, M. Increased ambient pressure stimulates proliferation and morphologic changes in cultured endothelial cells. J. Cell Physiol. 158, 133–139 (1994).
pubmed: 8263020
doi: 10.1002/jcp.1041580117
Yoshino, D., Sato, K. & Sato, M. Endothelial cell response under hydrostatic pressure condition mimicking pressure therapy. Cell. Mol. Bioeng. 8, 296–303 (2015).
doi: 10.1007/s12195-015-0385-8
Friedrich, E. E. et al. Endothelial cell Piezo1 mediates pressure-induced lung vascular hyperpermeability via disruption of adherens junctions. Proc. Natl Acad. Sci. USA 116, 12980–12985 (2019).
pubmed: 31186359
pmcid: 6600969
doi: 10.1073/pnas.1902165116
Ohashi, T., Sugaya, Y., Sakamoto, N. & Sato, M. Hydrostatic pressure influences morphology and expression of VE-cadherin of vascular endothelial cells. J. Biomech. 40, 2399–2405 (2007).
pubmed: 17261311
doi: 10.1016/j.jbiomech.2006.11.023
Shin, H. Y., Underwood, R. M. & Fannon, M. W. Fluid pressure is a magnitude-dependent modulator of early endothelial tubulogenic activity: implications related to a potential tissue-engineering control parameter. Tissue Eng. Part A 18, 2590–2600 (2012).
pubmed: 22793042
pmcid: 3501089
doi: 10.1089/ten.tea.2011.0588
Mammoto, T. et al. Hydrostatic pressure controls angiogenesis through endothelial YAP1 during lung regeneration. Front. Bioeng. Biotechnol. 10, 823642 (2022).
pubmed: 35252132
pmcid: 8896883
doi: 10.3389/fbioe.2022.823642
Yoshino, D., Funamoto, K., Sato, K., Kenry, Sato, M. & Lim, C. T. Hydrostatic pressure promotes endothelial tube formation through aquaporin 1 and Ras-ERK signaling. Commun. Biol. 3, 152 (2020).
pubmed: 32242084
pmcid: 7118103
doi: 10.1038/s42003-020-0881-9
Bellacen, K. & Lewis, E. C. Aortic ring assay. J. Vis. Exp. 33, 1564 (2009).
Ricard, N., Bailly, S., Guignabert, C. & Simons, M. The quiescent endothelium: signalling pathways regulating organ-specific endothelial normalcy. Nat. Rev. Cardiol. 18, 565–580 (2021).
pubmed: 33627876
pmcid: 7903932
doi: 10.1038/s41569-021-00517-4
Shen, H. X. et al. Hydrostatic pressure stimulates the osteogenesis and angiogenesis of MSCs/HUVECs co-culture on porous PLGA scaffolds. Colloids Surf. B Biointerfaces 213, 112419 (2022).
pubmed: 35227994
doi: 10.1016/j.colsurfb.2022.112419
Ohashi, T., Segawa, K., Sakamoto, N. & Sato, M. Effect of hydrostatic pressure on the morphology and expression of VE-Cadherin in HUVEC. Trans. Jpn. Soc. Med. Biol. Eng. 44, 454–459 (2006).
Uxa, S. et al. Ki-67 gene expression. Cell Death Differ. 28, 3357–3370 (2021).
pubmed: 34183782
pmcid: 8629999
doi: 10.1038/s41418-021-00823-x
Brookes, N. H. Riding the cell jamming boundary: geometry, topology, and phase of human corneal endothelium. Exp. Eye Res. 172, 171–180 (2018).
pubmed: 29656016
doi: 10.1016/j.exer.2018.04.007
Haeger, A., Wolf, K., Zegers, M. M. & Friedl, P. Collective cell migration: guidance principles and hierarchies. Trends Cell Biol. 25, 556–566 (2015).
pubmed: 26137890
doi: 10.1016/j.tcb.2015.06.003
Malinverno, C. et al. Endocytic reawakening of motility in jammed epithelia. Nat. Mater. 16, 587–596 (2017).
pubmed: 28135264
pmcid: 5407454
doi: 10.1038/nmat4848
Oldenburg, J. & de Rooij, J. Mechanical control of the endothelial barrier. Cell Tissue Res. 355, 545–555 (2014).
pubmed: 24519624
doi: 10.1007/s00441-013-1792-6
Dorland, Y. L. & Huveneers, S. Cell-cell junctional mechanotransduction in endothelial remodeling. Cell Mol. Life Sci. 74, 279–292 (2017).
pubmed: 27506620
doi: 10.1007/s00018-016-2325-8
Wang, M., He, P., Han, Y., Dong, L. & Yun, C. C. Control of intestinal epithelial permeability by lysophosphatidic acid receptor 5. Cell Mol. Gastroenterol. Hepatol. 12, 1073–1092 (2021).
pubmed: 33975030
pmcid: 8350072
doi: 10.1016/j.jcmgh.2021.05.003
Pramotton, F. M. et al. DYRK1B inhibition exerts senolytic effects on endothelial cells and rescues endothelial dysfunctions. Mech. Ageing Dev. 213, 111836 (2023).
pubmed: 37301518
doi: 10.1016/j.mad.2023.111836
Dejana, E. Endothelial cell-cell junctions: happy together. Nat. Rev. Mol. Cell Biol. 5, 261–270 (2004).
pubmed: 15071551
doi: 10.1038/nrm1357
Wang, L., Chung, J., Gill, S. E. & Mehta, S. Quantification of adherens junction disruption and contiguous paracellular protein leak in human lung endothelial cells under septic conditions. Microcirculation 26, e12528 (2019).
pubmed: 30636088
doi: 10.1111/micc.12528
Bazzoni, G. & Dejana, E. Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol. Rev. 84, 869–901 (2004).
pubmed: 15269339
doi: 10.1152/physrev.00035.2003
Angulo-Urarte, A., van der Wal, T. & Huveneers, S. Cell-cell junctions as sensors and transducers of mechanical forces. Biochim. Biophys. Acta Biomembr. 1862, 183316 (2020).
pubmed: 32360073
doi: 10.1016/j.bbamem.2020.183316
Huveneers, S. et al. Vinculin associates with endothelial VE-cadherin junctions to control force-dependent remodeling. J. Cell Biol. 196, 641–652 (2012).
pubmed: 22391038
pmcid: 3307691
doi: 10.1083/jcb.201108120
Jin, Y. et al. Tyrosine-protein kinase Yes controls endothelial junctional plasticity and barrier integrity by regulating VE-cadherin phosphorylation and endocytosis. Nat. Cardiovasc. Res. 1, 1156–1173 (2022).
pubmed: 37936984
pmcid: 7615285
doi: 10.1038/s44161-022-00172-z
Maeso-Alonso, L. et al. p73 is required for vessel integrity controlling endothelial junctional dynamics through Angiomotin. Cell. Mol. Life Sci. 79, 535 (2022).
Bentley, K. et al. The role of differential VE-cadherin dynamics in cell rearrangement during angiogenesis. Nat. Cell Biol. 16, 309–321 (2014).
pubmed: 24658686
doi: 10.1038/ncb2926
Millan, J. et al. Adherens junctions connect stress fibres between adjacent endothelial cells. BMC Biol. 8, 11 (2010).
pubmed: 20122254
pmcid: 2845098
doi: 10.1186/1741-7007-8-11
Lampugnani, M. G. Endothelial adherens junctions and the actin cytoskeleton: an ‘infinity net’? J. Biol. 9, 16 (2010).
pubmed: 20377920
pmcid: 2871513
doi: 10.1186/jbiol232
Giampietro, C. et al. Overlapping and divergent signaling pathways of N-cadherin and VE-cadherin in endothelial cells. Blood 119, 2159–2170 (2012).
pubmed: 22246030
doi: 10.1182/blood-2011-09-381012
Amsellem, V. et al. ICAM-2 regulates vascular permeability and N-cadherin localization through ezrin-radixin-moesin (ERM) proteins and Rac-1 signalling. Cell Commun. Signal. 12, 12 (2014).
pubmed: 24593809
pmcid: 4015342
doi: 10.1186/1478-811X-12-12
Ferreri, D. M., Minnear, F. L., Yin, T., Kowalczyk, A. P. & Vincent, P. A. N-cadherin levels in endothelial cells are regulated by monolayer maturity and p120 availability. Cell Commun. Adhes. 15, 333–349 (2008).
pubmed: 18979298
pmcid: 2631983
doi: 10.1080/15419060802440377
Wheelock, M. J., Shintani, Y., Maeda, M., Fukumoto, Y. & Johnson, K. R. Cadherin switching. J. Cell Sci. 121, 727–735 (2008).
pubmed: 18322269
doi: 10.1242/jcs.000455
Piera-Velazquez, S. & Jimenez, S. A. Endothelial to mesenchymal transition: role in physiology and in the pathogenesis of human diseases. Physiol. Rev. 99, 1281–1324 (2019).
pubmed: 30864875
pmcid: 6734087
doi: 10.1152/physrev.00021.2018
Clere, N., Renault, S. & Corre, I. Endothelial-to-mesenchymal transition in cancer. Front. Cell Dev. Biol. 8, 747 (2020).
pubmed: 32923440
pmcid: 7456955
doi: 10.3389/fcell.2020.00747
Fang, J. S., Hultgren, N. W. & Hughes, C. C. W. Regulation of partial and reversible endothelial-to-mesenchymal transition in angiogenesis. Front Cell Dev. Biol. 9, 702021 (2021).
pubmed: 34692672
pmcid: 8529039
doi: 10.3389/fcell.2021.702021
Rudini, N. et al. VE-cadherin is a critical endothelial regulator of TGF-beta signalling. EMBO J. 27, 993–1004 (2008).
pubmed: 18337748
pmcid: 2323269
doi: 10.1038/emboj.2008.46
Zhao, Y. et al. The VE-Cadherin/beta-catenin signalling axis regulates immune cell infiltration into tumours. Cancer Lett. 496, 1–15 (2021).
pubmed: 32991950
doi: 10.1016/j.canlet.2020.09.026
Giampietro, C. et al. The actin-binding protein EPS8 binds VE-cadherin and modulates YAP localization and signaling. J. Cell Biol. 211, 1177–1192 (2015).
pubmed: 26668327
pmcid: 4687874
doi: 10.1083/jcb.201501089
Choi, H. J. et al. Yes-associated protein regulates endothelial cell contact-mediated expression of angiopoietin-2. Nat. Commun. 6, 6943 (2015).
pubmed: 25962877
doi: 10.1038/ncomms7943
Dupont, S. et al. Role of YAP/TAZ in mechanotransduction. Nature 474, 179–183 (2011).
pubmed: 21654799
doi: 10.1038/nature10137
Hooglugt, A., van der Stoel, M. M., Boon, R. A. & Huveneers, S. Endothelial YAP/TAZ signaling in angiogenesis and tumor vasculature. Front. Oncol. 10, 612802 (2020).
pubmed: 33614496
doi: 10.3389/fonc.2020.612802
Kim, K. I. et al. Beta-catenin overexpression augments angiogenesis and skeletal muscle regeneration through dual mechanism of vascular endothelial growth factor-mediated endothelial cell proliferation and progenitor cell mobilization. Arterioscler Thromb. Vasc. Biol. 26, 91–98 (2006).
pubmed: 16254206
doi: 10.1161/01.ATV.0000193569.12490.4b
Liebner, S. et al. Beta-catenin is required for endothelial-mesenchymal transformation during heart cushion development in the mouse. J. Cell Biol. 166, 359–367 (2004).
pubmed: 15289495
pmcid: 2172268
doi: 10.1083/jcb.200403050
Savorani, C. et al. A dual role of YAP in driving TGFbeta-mediated endothelial-to-mesenchymal transition. J. Cell Sci. 134, jcs251371 (2021).
Daugherty, R. L. & Gottardi, C. J. Phospho-regulation of Beta-catenin adhesion and signaling functions. Physiology 22, 303–309 (2007).
pubmed: 17928543
doi: 10.1152/physiol.00020.2007
Fang, D. et al. Phosphorylation of beta-catenin by AKT promotes beta-catenin transcriptional activity. J. Biol. Chem. 282, 11221–11229 (2007).
pubmed: 17287208
doi: 10.1074/jbc.M611871200
Doble, B. W. & Woodgett, J. R. GSK-3: tricks of the trade for a multi-tasking kinase. J. Cell Sci. 116, 1175–1186 (2003).
pubmed: 12615961
doi: 10.1242/jcs.00384
Neto, F. et al. YAP and TAZ regulate adherens junction dynamics and endothelial cell distribution during vascular development. Elife, 7, e31037 (2018).
Zhang, Q. et al. Shear stress inhibits cardiac microvascular endothelial cells apoptosis to protect against myocardial ischemia reperfusion injury via YAP/miR-206/PDCD4 signaling pathway. Biochem. Pharm. 186, 114466 (2021).
pubmed: 33610591
doi: 10.1016/j.bcp.2021.114466
Matsuo, E. et al. Substrate stiffness modulates endothelial cell function via the YAP-Dll4-Notch1 pathway. Exp. Cell Res. 408, 112835 (2021).
pubmed: 34543658
doi: 10.1016/j.yexcr.2021.112835
Gordon, E., Schimmel, L. & Frye, M. The importance of mechanical forces for in vitro endothelial cell biology. Front. Physiol. 11, 684 (2020).
pubmed: 32625119
pmcid: 7314997
doi: 10.3389/fphys.2020.00684
Wahlsten, A. et al. Multiscale mechanical analysis of the elastic modulus of skin. Acta Biomater. 170, 155–168 (2023).
pubmed: 37598792
doi: 10.1016/j.actbio.2023.08.030
Otto, T. & Fandrey, J. Hypoxia induced gene expression: the specificity switch! Cell Cycle 14, 1491 (2015).
pubmed: 25751236
pmcid: 4614514
doi: 10.1080/15384101.2015.1024587
Pragallapati, S. & Manyam, R. Glucose transporter 1 in health and disease. J. Oral. Maxillofac. Pathol. 23, 443–449 (2019).
pubmed: 31942129
pmcid: 6948067
doi: 10.4103/jomfp.JOMFP_22_18
Kim, J. et al. YAP/TAZ regulates sprouting angiogenesis and vascular barrier maturation. J. Clin. Investig 127, 3441–3461 (2017).
pubmed: 28805663
pmcid: 5669570
doi: 10.1172/JCI93825
Gao, Y. et al. YAP inhibits squamous transdifferentiation of Lkb1-deficient lung adenocarcinoma through ZEB2-dependent DNp63 repression. Nat. Commun. 5, 4629 (2014).
pubmed: 25115923
doi: 10.1038/ncomms5629
Zhang, Y. et al. YAP promotes migration and invasion of human glioma cells. J. Mol. Neurosci. 64, 262–272 (2018).
pubmed: 29306996
doi: 10.1007/s12031-017-1018-6
Chen, C. C., Mo, F. E. & Lau, L. F. The angiogenic factor Cyr61 activates a genetic program for wound healing in human skin fibroblasts. J. Biol. Chem. 276, 47329–47337 (2001).
pubmed: 11584015
doi: 10.1074/jbc.M107666200
Seghezzi, G. et al. Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: an autocrine mechanism contributing to angiogenesis. J. Cell Biol. 141, 1659–1673 (1998).
pubmed: 9647657
pmcid: 2132998
doi: 10.1083/jcb.141.7.1659
Shibuya, M. Vascular Endothelial Growth Factor (VEGF) and its receptor (VEGFR) signaling in angiogenesis: a crucial target for anti- and pro-angiogenic therapies. Genes Cancer 2, 1097–1105 (2011).
pubmed: 22866201
pmcid: 3411125
doi: 10.1177/1947601911423031
Kovacic, J. C. et al. Endothelial to mesenchymal transition in cardiovascular disease: JACC state-of-the-art review. J. Am. Coll. Cardiol. 73, 190–209 (2019).
pubmed: 30654892
pmcid: 6865825
doi: 10.1016/j.jacc.2018.09.089
Giraud, J. et al. Verteporfin targeting YAP1/TAZ-TEAD transcriptional activity inhibits the tumorigenic properties of gastric cancer stem cells. Int. J. Cancer 146, 2255–2267 (2020).
pubmed: 31489619
doi: 10.1002/ijc.32667
Wei, H. et al. Verteporfin suppresses cell survival, angiogenesis and vasculogenic mimicry of pancreatic ductal adenocarcinoma via disrupting the YAP-TEAD complex. Cancer Sci. 108, 478–487 (2017).
pubmed: 28002618
pmcid: 5378285
doi: 10.1111/cas.13138
Urner, S., Kelly-Goss, M., Peirce, S. M. & Lammert, E. Mechanotransduction in blood and lymphatic vascular development and disease. Adv. Pharm. 81, 155–208 (2018).
doi: 10.1016/bs.apha.2017.08.009
Dessalles, C. A., Leclech, C., Castagnino, A. & Barakat, A. I. Integration of substrate- and flow-derived stresses in endothelial cell mechanobiology. Commun. Biol. 4, 764 (2021).
pubmed: 34155305
pmcid: 8217569
doi: 10.1038/s42003-021-02285-w
le Noble, F. et al. Flow regulates arterial-venous differentiation in the chick embryo yolk sac. Development 131, 361–375 (2004).
pubmed: 14681188
doi: 10.1242/dev.00929
Moyon, D., Pardanaud, L., Yuan, L., Breant, C. & Eichmann, A. Plasticity of endothelial cells during arterial-venous differentiation in the avian embryo. Development 128, 3359–3370 (2001).
pubmed: 11546752
doi: 10.1242/dev.128.17.3359
Bai, H. et al. Adult human vein grafts retain plasticity of vessel identity. Ann. Vasc. Surg. 68, 468–475 (2020).
pubmed: 32422286
doi: 10.1016/j.avsg.2020.04.046
Mack, J. J. et al. NOTCH1 is a mechanosensor in adult arteries. Nat. Commun. 8, 1620 (2017).
DeMaio, L., Chang, Y. S., Gardner, T. W., Tarbell, J. M. & Antonetti, D. A. Shear stress regulates occludin content and phosphorylation. Am. J. Physiol. Heart Circ. Physiol. 281, H105–H113 (2001).
pubmed: 11406474
doi: 10.1152/ajpheart.2001.281.1.H105
Lampugnani, M. G. & Dejana, E. Adherens junctions in endothelial cells regulate vessel maintenance and angiogenesis. Thromb. Res. 120, S1–S6 (2007).
pubmed: 18023702
doi: 10.1016/S0049-3848(07)70124-X
Wang, W. Y., Lin, D., Jarman, E. H., Polacheck, W. J. & Baker, B. M. Functional angiogenesis requires microenvironmental cues balancing endothelial cell migration and proliferation. Lab a Chip 20, 1153–1166 (2020).
doi: 10.1039/C9LC01170F
Taddei, A. et al. Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5. Nat. Cell Biol. 10, 923–934 (2008).
pubmed: 18604199
doi: 10.1038/ncb1752
Luo, Y. & Radice, G. L. N-cadherin acts upstream of VE-cadherin in controlling vascular morphogenesis. J. Cell Biol. 169, 29–34 (2005).
pubmed: 15809310
pmcid: 2171890
doi: 10.1083/jcb.200411127
Alberici Delsin, L. E. et al. MAP4K4 regulates forces at cell-cell and cell-matrix adhesions to promote collective cell migration. Life Sci Alliance, 6, 202302196 (2023).
Rabiet, M. J. et al. Thrombin-induced increase in endothelial permeability is associated with changes in cell-to-cell junction organization. Arterioscler Thromb. Vasc. Biol. 16, 488–496 (1996).
pubmed: 8630677
doi: 10.1161/01.ATV.16.3.488
Welch-Reardon, K. M., Wu, N. & Hughes, C. C. A role for partial endothelial-mesenchymal transitions in angiogenesis? Arterioscler Thromb. Vasc. Biol. 35, 303–308 (2015).
pubmed: 25425619
doi: 10.1161/ATVBAHA.114.303220
Loh, C. Y. et al. The E-Cadherin and N-Cadherin Switch in Epithelial-to-Mesenchymal Transition: Signaling, Therapeutic Implications, and Challenges. Cells 8, 1118 (2019).
Haase, K., M. R., Gillrie, C., Hajal, C. & Kamm, R. D. Pericytes contribute to dysfunction in a human 3d model of placental microvasculature through VEGF-Ang-Tie2 Signaling. Adv. Sci. 6, 1900878 (2019).
Polacheck, W. J., Kutys, M. L., Tefft, J. B. & Chen, C. S. Microfabricated blood vessels for modeling the vascular transport barrier. Nat. Protoc. 14, 1425–1454 (2019).
pubmed: 30953042
pmcid: 7046311
doi: 10.1038/s41596-019-0144-8
Ershov, D. et al. TrackMate 7: integrating state-of-the-art segmentation algorithms into tracking pipelines. Nat. Methods 19, 829–832 (2022).
pubmed: 35654950
doi: 10.1038/s41592-022-01507-1
Al-Nuaimi, D., Lendenmann, T. Image processing code for immunofluorescence microscopy images. ETH Zürich Res. Collection, 2024.
Pramotton, F. M. et al. Optimized topological and topographical expansion of epithelia. ACS Biomater. Sci. Eng. 5, 3922–3934 (2019).
pubmed: 33438431
doi: 10.1021/acsbiomaterials.8b01346
Rezakhaniha, R. et al. Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy. Biomech. Model Mechanobiol. 11, 461–473 (2012).
pubmed: 21744269
doi: 10.1007/s10237-011-0325-z