Cited by 299Angiogenesis and VEGF in CancerCell Adhesion Molecules ResearchCellular Mechanics and Interactions

Intramembrane binding of VE-cadherin to VEGFR2 and VEGFR3 assembles the endothelial mechanosensory complex

Open access
Coon, Brian G., Baeyens, Nicolas, Han, Jinah, Budatha, Madhusudhan, Ross, Tyler D., Fang, Jennifer S., Yun, Sanguk, Thomas, Jeon-Leon +1 more·2015·Journal of Cell Biology

Abstract

Endothelial responses to fluid shear stress are essential for vascular development and physiology, and determine the formation of atherosclerotic plaques at regions of disturbed flow. Previous work identified VE-cadherin as an essential component, along with PECAM-1 and VEGFR2, of a complex that mediates flow signaling. However, VE-cadherin’s precise role is poorly understood. We now show that the transmembrane domain of VE-cadherin mediates an essential adapter function by binding directly to the transmembrane domain of VEGFR2, as well as VEGFR3, which we now identify as another component of the junctional mechanosensory complex. VEGFR2 and VEGFR3 signal redundantly downstream of VE-cadherin. Furthermore, VEGFR3 expression is observed in the aortic endothelium, where it contributes to flow responses in vivo. In summary, this study identifies a novel adapter function for VE-cadherin mediated by transmembrane domain association with VEGFRs.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1083/jcb.201408103

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 71

  1. Andersen O.S., and Koeppe R.E. II 2007 Bilayer thickness and membrane protein function: an energetic perspective. Annu. Rev. Biophys. Biomol. Struct. 36: 107– 130 10.1146/annurev.biophys.36.040306.132643 17263662 · DOI
  2. Bocharov E.V., Mineev K.S., Goncharuk M.V., and Arseniev A.S. 2012 Structural and thermodynamic insight into the process of “weak” dimerization of the ErbB4 transmembrane domain by solution NMR. Biochim. Biophys. Acta. 1818: 2158– 2170 10.1016/j.bbamem.2012.05.001 22579757 · DOI
  3. Calvo C.F., Fontaine R.H., Soueid J., Tammela T., Makinen T., Alfaro-Cervello C., Bonnaud F., Miguez A., Benhaim L., Xu Y., 2011 Vascular endothelial growth factor receptor 3 directly regulates murine neurogenesis. Genes Dev. 25: 831– 844 10.1101/gad.615311 21498572 PMC3078708 · DOI
  4. Carmeliet P., Lampugnani M.G., Moons L., Breviario F., Compernolle V., Bono F., Balconi G., Spagnuolo R., Oosthuyse B., Dewerchin M., 1999 Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell. 98: 147– 157 10.1016/S0092-8674(00)81010-7 10428027 · DOI
  5. Chiu J.J., and Chien S. 2011 Effects of disturbed flow on vascular endothelium: pathophysiological basis and clinical perspectives. Physiol. Rev. 91: 327– 387 10.1152/physrev.00047.2009 21248169 PMC3844671 · DOI · Paper page
  6. Chiu Y.J., McBeath E., and Fujiwara K. 2008 Mechanotransduction in an extracted cell model: Fyn drives stretch- and flow-elicited PECAM-1 phosphorylation. J. Cell Biol. 182: 753– 763 10.1083/jcb.200801062 18710921 PMC2518713 · DOI
  7. Chiu J.J., Usami S., and Chien S. 2009 Vascular endothelial responses to altered shear stress: pathologic implications for atherosclerosis. Ann. Med. 41: 19– 28 10.1080/07853890802186921 18608132 · DOI
  8. Cicha I., Goppelt-Struebe M., Yilmaz A., Daniel W.G., and Garlichs C.D. 2008 Endothelial dysfunction and monocyte recruitment in cells exposed to non-uniform shear stress. Clin. Hemorheol. Microcirc. 39: 113– 119. 18503117
  9. Conway D.E., Breckenridge M.T., Hinde E., Gratton E., Chen C.S., and Schwartz M.A. 2013 Fluid shear stress on endothelial cells modulates mechanical tension across VE-cadherin and PECAM-1. Curr. Biol. 23: 1024– 1030 10.1016/j.cub.2013.04.049 23684974 PMC3676707 · DOI
  10. Cosson P., Perrin J., and Bonifacino J.S. 2013 Anchors aweigh: protein localization and transport mediated by transmembrane domains. Trends Cell Biol. 23: 511– 517 10.1016/j.tcb.2013.05.005 23806646 PMC3783643 · DOI
  11. Dai G., Kaazempur-Mofrad M.R., Natarajan S., Zhang Y., Vaughn S., Blackman B.R., Kamm R.D., García-Cardeña G., and Gimbrone M.A. Jr 2004 Distinct endothelial phenotypes evoked by arterial waveforms derived from atherosclerosis-susceptible and -resistant regions of human vasculature. Proc. Natl. Acad. Sci. USA. 101: 14871– 14876 10.1073/pnas.0406073101 15466704 PMC522013 · DOI
  12. Davies P.F., Civelek M., Fang Y., and Fleming I. 2013 The atherosusceptible endothelium: endothelial phenotypes in complex haemodynamic shear stress regions in vivo. Cardiovasc. Res. 99: 315– 327 10.1093/cvr/cvt101 23619421 PMC3695748 · DOI
  13. Diaz-Rohrer B.B., Levental K.R., Simons K., and Levental I. 2014 Membrane raft association is a determinant of plasma membrane localization. Proc. Natl. Acad. Sci. USA. 111: 8500– 8505 10.1073/pnas.1404582111 24912166 PMC4060687 · DOI
  14. Di Stefano I., Koopmans D.R., and Langille B.L. 1998 Modulation of arterial growth of the rabbit carotid artery associated with experimental elevation of blood flow. J. Vasc. Res. 35: 1– 7 10.1159/000025559 9482690 · DOI
  15. DiMaio D., and Petti L.M. 2013 The E5 proteins. Virology. 445: 99– 114 10.1016/j.virol.2013.05.006 23731971 PMC3772959 · DOI
  16. Endres N.F., Das R., Smith A.W., Arkhipov A., Kovacs E., Huang Y., Pelton J.G., Shan Y., Shaw D.E., Wemmer D.E., 2013 Conformational coupling across the plasma membrane in activation of the EGF receptor. Cell. 152: 543– 556 10.1016/j.cell.2012.12.032 23374349 PMC3718647 · DOI
  17. Eskens F.A., and Verweij J. 2006 The clinical toxicity profile of vascular endothelial growth factor (VEGF) and vascular endothelial growth factor receptor (VEGFR) targeting angiogenesis inhibitors; a review. Eur. J. Cancer. 42: 3127– 3139 10.1016/j.ejca.2006.09.015 17098419 · DOI
  18. Feaver R.E., Gelfand B.D., Wang C., Schwartz M.A., and Blackman B.R. 2010 Atheroprone hemodynamics regulate fibronectin deposition to create positive feedback that sustains endothelial inflammation. Circ. Res. 106: 1703– 1711 10.1161/CIRCRESAHA.109.216283 20378855 PMC2891748 · DOI
  19. Fleming I., Fisslthaler B., Dixit M., and Busse R. 2005 Role of PECAM-1 in the shear-stress-induced activation of Akt and the endothelial nitric oxide synthase (eNOS) in endothelial cells. J. Cell Sci. 118: 4103– 4111 10.1242/jcs.02541 16118242 · DOI
  20. Frangos J.A., McIntire L.V., and Eskin S.G. 1988 Shear stress induced stimulation of mammalian cell metabolism. Biotechnol. Bioeng. 32: 1053– 1060 10.1002/bit.260320812 18587822 · DOI
  21. Galvagni F., Pennacchini S., Salameh A., Rocchigiani M., Neri F., Orlandini M., Petraglia F., Gotta S., Sardone G.L., Matteucci G., 2010 Endothelial cell adhesion to the extracellular matrix induces c-Src-dependent VEGFR-3 phosphorylation without the activation of the receptor intrinsic kinase activity. Circ. Res. 106: 1839– 1848 10.1161/CIRCRESAHA.109.206326 20431062 · DOI
  22. Gavard J., Lambert M., Grosheva I., Marthiens V., Irinopoulou T., Riou J.F., Bershadsky A., and Mège R.M. 2004 Lamellipodium extension and cadherin adhesion: two cell responses to cadherin activation relying on distinct signalling pathways. J. Cell Sci. 117: 257– 270 10.1242/jcs.00857 14657280 · DOI
  23. Giampietro C., Taddei A., Corada M., Sarra-Ferraris G.M., Alcalay M., Cavallaro U., Orsenigo F., Lampugnani M.G., and Dejana E. 2012 Overlapping and divergent signaling pathways of N-cadherin and VE-cadherin in endothelial cells. Blood. 119: 2159– 2170 10.1182/blood-2011-09-381012 22246030 · DOI
  24. Gimbrone M.A. Jr, and García-Cardeña G. 2013 Vascular endothelium, hemodynamics, and the pathobiology of atherosclerosis. Cardiovasc. Pathol. 22: 9– 15 10.1016/j.carpath.2012.06.006 22818581 PMC4564111 · DOI
  25. Goel R., Schrank B.R., Arora S., Boylan B., Fleming B., Miura H., Newman P.J., Molthen R.C., and Newman D.K. 2008 Site-specific effects of PECAM-1 on atherosclerosis in LDL receptor-deficient mice. Arterioscler. Thromb. Vasc. Biol. 28: 1996– 2002 10.1161/ATVBAHA.108.172270 18669884 PMC3013511 · DOI
  26. Gu W., Brännström T., Jiang W., Bergh A., and Wester P. 2001 Vascular endothelial growth factor-A and -C protein up-regulation and early angiogenesis in a rat photothrombotic ring stroke model with spontaneous reperfusion. Acta Neuropathol. 102: 216– 226. 11585245
  27. Hahn C., and Schwartz M.A. 2009 Mechanotransduction in vascular physiology and atherogenesis. Nat. Rev. Mol. Cell Biol. 10: 53– 62 10.1038/nrm2596 19197332 PMC2719300 · DOI
  28. Hahn C., Orr A.W., Sanders J.M., Jhaveri K.A., and Schwartz M.A. 2009 The subendothelial extracellular matrix modulates JNK activation by flow. Circ. Res. 104: 995– 1003 10.1161/CIRCRESAHA.108.186486 19286608 PMC2702158 · DOI
  29. Hahn C., Wang C., Orr A.W., Coon B.G., and Schwartz M.A. 2011 JNK2 promotes endothelial cell alignment under flow. PLoS ONE. 6: e24338 10.1371/journal.pone.0024338 21909388 PMC3164210 · DOI
  30. Haiko P., Makinen T., Keskitalo S., Taipale J., Karkkainen M.J., Baldwin M.E., Stacker S.A., Achen M.G., and Alitalo K. 2008 Deletion of vascular endothelial growth factor C (VEGF-C) and VEGF-D is not equivalent to VEGF receptor 3 deletion in mouse embryos. Mol. Cell. Biol. 28: 4843– 4850 10.1128/MCB.02214-07 18519586 PMC2493372 · DOI
  31. Harry B.L., Sanders J.M., Feaver R.E., Lansey M., Deem T.L., Zarbock A., Bruce A.C., Pryor A.W., Gelfand B.D., Blackman B.R., 2008 Endothelial cell PECAM-1 promotes atherosclerotic lesions in areas of disturbed flow in ApoE-deficient mice. Arterioscler. Thromb. Vasc. Biol. 28: 2003– 2008 10.1161/ATVBAHA.108.164707 18688018 PMC2651147 · DOI
  32. Hove J.R., Köster R.W., Forouhar A.S., Acevedo-Bolton G., Fraser S.E., and Gharib M. 2003 Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature. 421: 172– 177 10.1038/nature01282 12520305 · DOI
  33. Hwang J., Saha A., Boo Y.C., Sorescu G.P., McNally J.S., Holland S.M., Dikalov S., Giddens D.P., Griendling K.K., Harrison D.G., and Jo H. 2003 Oscillatory shear stress stimulates endothelial production of O2- from p47phox-dependent NAD(P)H oxidases, leading to monocyte adhesion. J. Biol. Chem. 278: 47291– 47298 10.1074/jbc.M305150200 12958309 · DOI
  34. Jin Z.G., Ueba H., Tanimoto T., Lungu A.O., Frame M.D., and Berk B.C. 2003 Ligand-independent activation of vascular endothelial growth factor receptor 2 by fluid shear stress regulates activation of endothelial nitric oxide synthase. Circ. Res. 93: 354– 363 10.1161/01.RES.0000089257.94002.96 12893742 · DOI
  35. Jongstra-Bilen J., Haidari M., Zhu S.N., Chen M., Guha D., and Cybulsky M.I. 2006 Low-grade chronic inflammation in regions of the normal mouse arterial intima predisposed to atherosclerosis. J. Exp. Med. 203: 2073– 2083 10.1084/jem.20060245 16894012 PMC2118407 · DOI
  36. Joukov V., Pajusola K., Kaipainen A., Chilov D., Lahtinen I., Kukk E., Saksela O., Kalkkinen N., and Alitalo K. 1996 A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J. 15: 290– 298. 8617204 PMC449944
  37. Karkkainen M.J., Ferrell R.E., Lawrence E.C., Kimak M.A., Levinson K.L., McTigue M.A., Alitalo K., and Finegold D.N. 2000 Missense mutations interfere with VEGFR-3 signalling in primary lymphoedema. Nat. Genet. 25: 153– 159 10.1038/75997 10835628 · DOI
  38. Kubo H., Fujiwara T., Jussila L., Hashi H., Ogawa M., Shimizu K., Awane M., Sakai Y., Takabayashi A., Alitalo K., 2000 Involvement of vascular endothelial growth factor receptor-3 in maintenance of integrity of endothelial cell lining during tumor angiogenesis. Blood. 96: 546– 553. 10887117
  39. Lampugnani M.G., Orsenigo F., Gagliani M.C., Tacchetti C., and Dejana E. 2006 Vascular endothelial cadherin controls VEGFR-2 internalization and signaling from intracellular compartments. J. Cell Biol. 174: 593– 604 10.1083/jcb.200602080 16893970 PMC2064264 · DOI
  40. Langille B.L., and O’Donnell F. 1986 Reductions in arterial diameter produced by chronic decreases in blood flow are endothelium-dependent. Science. 231: 405– 407 10.1126/science.3941904 3941904 · DOI
  41. Liu Y., Sweet D.T., Irani-Tehrani M., Maeda N., and Tzima E. 2008 Shc coordinates signals from intercellular junctions and integrins to regulate flow-induced inflammation. J. Cell Biol. 182: 185– 196 10.1083/jcb.200709176 18606845 PMC2447891 · DOI
  42. Lucitti J.L., Jones E.A., Huang C., Chen J., Fraser S.E., and Dickinson M.E. 2007 Vascular remodeling of the mouse yolk sac requires hemodynamic force. Development. 134: 3317– 3326 10.1242/dev.02883 17720695 PMC4260474 · DOI
  43. Maciag T., Cerundolo J., Ilsley S., Kelley P.R., and Forand R. 1979 An endothelial cell growth factor from bovine hypothalamus: identification and partial characterization. Proc. Natl. Acad. Sci. USA. 76: 5674– 5678 10.1073/pnas.76.11.5674 293671 PMC411712 · DOI
  44. Manni S., Mineev K.S., Usmanova D., Lyukmanova E.N., Shulepko M.A., Kirpichnikov M.P., Winter J., Matkovic M., Deupi X., Arseniev A.S., and Ballmer-Hofer K. 2014 Structural and functional characterization of alternative transmembrane domain conformations in VEGF receptor 2 activation. Structure. 22: 1077– 1089 10.1016/j.str.2014.05.010 24980797 · DOI
  45. Mattsson E.J., Kohler T.R., Vergel S.M., and Clowes A.W. 1997 Increased blood flow induces regression of intimal hyperplasia. Arterioscler. Thromb. Vasc. Biol. 17: 2245– 2249 10.1161/01.ATV.17.10.2245 9351396 · DOI
  46. Moore D.T., Berger B.W., and DeGrado W.F. 2008 Protein-protein interactions in the membrane: sequence, structural, and biological motifs. Structure. 16: 991– 1001 10.1016/j.str.2008.05.007 18611372 PMC3771515 · DOI
  47. Nam D., Ni C.W., Rezvan A., Suo J., Budzyn K., Llanos A., Harrison D., Giddens D., and Jo H. 2009 Partial carotid ligation is a model of acutely induced disturbed flow, leading to rapid endothelial dysfunction and atherosclerosis. Am. J. Physiol. Heart Circ. Physiol. 297: H1535– H1543 10.1152/ajpheart.00510.2009 19684185 PMC2770764 · DOI
  48. Navarro P., Ruco L., and Dejana E. 1998 Differential localization of VE- and N-cadherins in human endothelial cells: VE-cadherin competes with N-cadherin for junctional localization. J. Cell Biol. 140: 1475– 1484 10.1083/jcb.140.6.1475 9508779 PMC2132661 · DOI
  49. Nawroth R., Poell G., Ranft A., Kloep S., Samulowitz U., Fachinger G., Golding M., Shima D.T., Deutsch U., and Vestweber D. 2002 VE-PTP and VE-cadherin ectodomains interact to facilitate regulation of phosphorylation and cell contacts. EMBO J. 21: 4885– 4895 10.1093/emboj/cdf497 12234928 PMC126293 · DOI
  50. Nayak L., Lin Z., and Jain M.K. 2011 “Go with the flow”: how Krüppel-like factor 2 regulates the vasoprotective effects of shear stress. Antioxid. Redox Signal. 15: 1449– 1461 10.1089/ars.2010.3647 20919941 PMC3144441 · DOI
  51. Nigro P., Abe J., and Berk B.C. 2011 Flow shear stress and atherosclerosis: a matter of site specificity. Antioxid. Redox Signal. 15: 1405– 1414 10.1089/ars.2010.3679 21050140 PMC3144425 · DOI
  52. Olsson A.K., Dimberg A., Kreuger J., and Claesson-Welsh L. 2006 VEGF receptor signalling - in control of vascular function. Nat. Rev. Mol. Cell Biol. 7: 359– 371 10.1038/nrm1911 16633338 · DOI · Paper page
  53. Orr A.W., Sanders J.M., Bevard M., Coleman E., Sarembock I.J., and Schwartz M.A. 2005 The subendothelial extracellular matrix modulates NF-κB activation by flow: a potential role in atherosclerosis. J. Cell Biol. 169: 191– 202 10.1083/jcb.200410073 15809308 PMC2171897 · DOI
  54. Orr A.W., Ginsberg M.H., Shattil S.J., Deckmyn H., and Schwartz M.A. 2006 Matrix-specific suppression of integrin activation in shear stress signaling. Mol. Biol. Cell. 17: 4686– 4697 10.1091/mbc.E06-04-0289 16928957 PMC1635406 · DOI
  55. Orr A.W., Hahn C., Blackman B.R., and Schwartz M.A. 2008 p21-activated kinase signaling regulates oxidant-dependent NF-κB activation by flow. Circ. Res. 103: 671– 679 10.1161/CIRCRESAHA.108.182097 18669917 PMC2697905 · DOI
  56. Osawa M., Masuda M., Kusano K., and Fujiwara K. 2002 Evidence for a role of platelet endothelial cell adhesion molecule-1 in endothelial cell mechanosignal transduction: is it a mechanoresponsive molecule? J. Cell Biol. 158: 773– 785 10.1083/jcb.200205049 12177047 PMC2174013 · DOI
  57. Piedra J., Miravet S., Castaño J., Pálmer H.G., Heisterkamp N., García de Herreros A., and Duñach M. 2003 p120 Catenin-associated Fer and Fyn tyrosine kinases regulate β-catenin Tyr-142 phosphorylation and β-catenin-α-catenin interaction. Mol. Cell. Biol. 23: 2287– 2297 10.1128/MCB.23.7.2287-2297.2003 12640114 PMC150740 · DOI
  58. Pitulescu M.E., Schmidt I., Benedito R., and Adams R.H. 2010 Inducible gene targeting in the neonatal vasculature and analysis of retinal angiogenesis in mice. Nat. Protoc. 5: 1518– 1534 10.1038/nprot.2010.113 20725067 · DOI
  59. Pohl U., Holtz J., Busse R., and Bassenge E. 1986 Crucial role of endothelium in the vasodilator response to increased flow in vivo. Hypertension. 8: 37– 44 10.1161/01.HYP.8.1.37 3080370 · DOI
  60. Privratsky J.R., Newman D.K., and Newman P.J. 2010 PECAM-1: conflicts of interest in inflammation. Life Sci. 87: 69– 82 10.1016/j.lfs.2010.06.001 20541560 PMC2917326 · DOI
  61. Sharpe H.J., Stevens T.J., and Munro S. 2010 A comprehensive comparison of transmembrane domains reveals organelle-specific properties. Cell. 142: 158– 169 10.1016/j.cell.2010.05.037 20603021 PMC2928124 · DOI
  62. Stevens H.Y., Melchior B., Bell K.S., Yun S., Yeh J.C., and Frangos J.A. 2008 PECAM-1 is a critical mediator of atherosclerosis. Dis. Model. Mech. 1: 175– 181 10.1242/dmm.000547 19048083 PMC2562188 · DOI
  63. Tammela T., Zarkada G., Wallgard E., Murtomäki A., Suchting S., Wirzenius M., Waltari M., Hellström M., Schomber T., Peltonen R., 2008 Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature. 454: 656– 660 10.1038/nature07083 18594512 · DOI
  64. Tedgui A., and Mallat Z. 2001 Anti-inflammatory mechanisms in the vascular wall. Circ. Res. 88: 877– 887 10.1161/hh0901.090440 11348996 · DOI
  65. Therien A.G., Grant F.E., and Deber C.M. 2001 Interhelical hydrogen bonds in the CFTR membrane domain. Nat. Struct. Biol. 8: 597– 601 10.1038/89631 11427889 · DOI
  66. Tzima E., Irani-Tehrani M., Kiosses W.B., Dejana E., Schultz D.A., Engelhardt B., Cao G., DeLisser H., and Schwartz M.A. 2005 A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature. 437: 426– 431 10.1038/nature03952 16163360 · DOI
  67. Vestweber D. 2008 VE-cadherin: the major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arterioscler. Thromb. Vasc. Biol. 28: 223– 232 10.1161/ATVBAHA.107.158014 18162609 · DOI
  68. Wang Y., Nakayama M., Pitulescu M.E., Schmidt T.S., Bochenek M.L., Sakakibara A., Adams S., Davy A., Deutsch U., Lüthi U., 2010 Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature. 465: 483– 486 10.1038/nature09002 20445537 · DOI
  69. Wang C., Baker B.M., Chen C.S., and Schwartz M.A. 2013 Endothelial cell sensing of flow direction. Arterioscler. Thromb. Vasc. Biol. 33: 2130– 2136 10.1161/ATVBAHA.113.301826 23814115 PMC3812824 · DOI
  70. Warfel N.A., Niederst M., and Newton A.C. 2011 Disruption of the interface between the pleckstrin homology (PH) and kinase domains of Akt protein is sufficient for hydrophobic motif site phosphorylation in the absence of mTORC2. J. Biol. Chem. 286: 39122– 39129 10.1074/jbc.M111.278747 21908613 PMC3234737 · DOI
  71. Witmer A.N., van Blijswijk B.C., Dai J., Hofman P., Partanen T.A., Vrensen G.F., and Schlingemann R.O. 2001 VEGFR-3 in adult angiogenesis. J. Pathol. 195: 490– 497 10.1002/path.969 11745682 · DOI

Cited by

Sorted by citations

Authors
Coon, B. G., Baeyens, N., Han, J., Budatha, M., Ross, T. D., Fang, J. S., Yun, S., Thomas, J.-L., & Schwartz, M. A.
Affiliations
  • Yale University (US)
  • Centre National de la Recherche Scientifique (FR)
Corresponding author
Schwartz, Martin A.
Venue
Journal of Cell Biology
Published
2015-03-23
Volume
208
Issue
7
Pages
975-986
ISSN
  • 0021-9525 (ISSN-L)
  • 1540-8140
OpenAlex
W2161020445
Cited by
299
References
1
Citations by year
2026: 16 · 2025: 17 · 2024: 26 · 2023: 21 · 2022: 29 · 2021: 32 · 2020: 36 · 2019: 29 · 2018: 24 · 2017: 29 · 2016: 29 · 2015: 11
FWCI
13.45
Type
journal article
Language
en
Open access
Licence
cc-by-nc-sa
Locations
  • The Journal of Cell Biology (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
  • Research Explorer (The University of Manchester) (publishedVersion, other-oa)
  • Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) (submittedVersion, other-oa)
Funders
  • National Institutes of Health (UL1TR000142)
  • National Heart, Lung, and Blood Institute (R01HL075092, T32HL007950)
  • National Center for Advancing Translational Sciences
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
  • Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
Keywords
VE-cadherin, VEGFR2, VEGFR-3, fluid shear stress, endothelial junctions, CD31, aortic endothelium, atherosclerosis, flow disturbance
MeSH terms
Cadherin 5, Animals, Cell Movement, Cells, Cultured, Endothelium, Vascular, Humans, Mice, Inbred C57BL, Stress, Physiological, Stress, Mechanical, Antigens, CD, Cadherins, Protein Structure, Tertiary, Neovascularization, Physiologic, Platelet Endothelial Cell Adhesion Molecule-1, RNA Interference, RNA, Small Interfering, Vascular Endothelial Growth Factor Receptor-2, Vascular Endothelial Growth Factor Receptor-3, Mechanotransduction, Cellular, Mice, HEK293 Cells, Plaque, Atherosclerotic, Human Umbilical Vein Endothelial Cells

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review