Horiguchi K, Hanada T, Fukui Y, Chishti AH (2006) Transport of PIP3 by GAKIN, a kinesin-3 family protein, regulates neuronal cell polarity. J Cell Biol 174:425–436. https://doi.org/10.1083/jcb.200604031

Article  CAS  PubMed  PubMed Central  Google Scholar 

Claesson-Welsh L, Dejana E, McDonald DM (2020) Permeability of the endothelial barrier: identifying and reconciling controversies. Trends Mol Med 27:314–331. https://doi.org/10.1016/j.molmed.2020.11.006

Article  CAS  PubMed  PubMed Central  Google Scholar 

Duong CN, Vestweber D (2020) Mechanisms ensuring endothelial junction integrity beyond VE-cadherin. Front Physiol 11:519. https://doi.org/10.3389/fphys.2020.00519

Article  PubMed  PubMed Central  Google Scholar 

Eelen G, Treps L, Li X, Carmeliet P (2020) Basic and therapeutic aspects of angiogenesis updated. Circ Res 127:310–329. https://doi.org/10.1161/circresaha.120.316851

Article  CAS  PubMed  Google Scholar 

Apte RS, Chen DS, Ferrara N (2019) VEGF in signaling and disease: beyond discovery and development. Cell 176:1248–1264. https://doi.org/10.1016/j.cell.2019.01.021

Article  CAS  PubMed  PubMed Central  Google Scholar 

Yamada KH, Kang H, Malik AB (2017) Antiangiogenic therapeutic potential of peptides derived from the molecular motor KIF13B that transports VEGFR2 to plasmalemma in endothelial cells. Am J Pathol 187:214–224. https://doi.org/10.1016/j.ajpath.2016.09.010

Article  CAS  PubMed  PubMed Central  Google Scholar 

Waters SB, Zhou C, Nguyen T et al (2021) VEGFR2 trafficking by KIF13B is a novel therapeutic target for wet age-related macular degeneration. Invest Ophth Vis Sci 62:5. https://doi.org/10.1167/iovs.62.2.5

Article  CAS  Google Scholar 

Simons M, Gordon E, Claesson-Welsh L (2016) Mechanisms and regulation of endothelial VEGF receptor signalling. Nat Rev Mol Cell Bio 17:611–625. https://doi.org/10.1038/nrm.2016.87

Article  CAS  Google Scholar 

Nakayama M, Nakayama A, van Lessen M et al (2013) Spatial regulation of VEGF receptor endocytosis in angiogenesis. Nat Cell Biol 15:249–260. https://doi.org/10.1038/ncb2679

Article  CAS  PubMed  PubMed Central  Google Scholar 

Sawamiphak S, Seidel S, Essmann CL et al (2010) Ephrin-B2 regulates VEGFR2 function in developmental and tumour angiogenesis. Nature 465:487–491. https://doi.org/10.1038/nature08995

Article  CAS  PubMed  Google Scholar 

Lanahan AA, Hermans K, Claes F et al (2010) VEGF receptor 2 endocytic trafficking regulates arterial morphogenesis. Dev Cell 18:713–724. https://doi.org/10.1016/j.devcel.2010.02.016

Article  CAS  PubMed  PubMed Central  Google Scholar 

Lanahan AA, Lech D, Dubrac A et al (2014) PTP1b is a physiologic regulator of vascular endothelial growth factor signaling in endothelial cells. Circulation 130:902–909. https://doi.org/10.1161/circulationaha.114.009683

Article  CAS  PubMed  PubMed Central  Google Scholar 

Ballmer-Hofer K, Andersson AE, Ratcliffe LE, Berger P (2011) Neuropilin-1 promotes VEGFR-2 trafficking through Rab11 vesicles thereby specifying signal output. Blood 118:816–826. https://doi.org/10.1182/blood-2011-01-328773

Article  CAS  PubMed  Google Scholar 

Manickam V, Tiwari A, Jung JJ et al (2011) Regulation of vascular endothelial growth factor receptor 2 trafficking and angiogenesis by Golgi localized t-SNARE syntaxin 6. Blood 117:1425–1435. https://doi.org/10.1182/blood-2010-06-291690

Article  CAS  PubMed  PubMed Central  Google Scholar 

Tiwari A, Jung JJ, Inamdar SM et al (2013) The myosin motor Myo1c is required for VEGFR2 delivery to the cell surface and for angiogenic signaling. Am J Physiol Heart Circ Physiol 304:H687–H696. https://doi.org/10.1152/ajpheart.00744.2012

Article  CAS  PubMed  Google Scholar 

Yamada KH, Nakajima Y, Geyer M et al (2014) KIF13B regulates angiogenesis through Golgi to plasma membrane trafficking of VEGFR2. J Cell Sci 127:4518–4530. https://doi.org/10.1242/jcs.156109

Article  CAS  PubMed  PubMed Central  Google Scholar 

Waters SB, Dominguez JR, Cho H-D et al (2021) KIF13B-mediated VEGFR2 trafficking is essential for vascular leakage and metastasis in vivo. Life Sci Alliance 5:e202101170. https://doi.org/10.26508/lsa.202101170

Article  CAS  PubMed  PubMed Central  Google Scholar 

Smith R, Ninchoji T, Gordon E et al (2020) Vascular permeability in retinopathy is regulated by VEGFR2 Y949 signaling to VE-cadherin. Elife 9:e54056. https://doi.org/10.7554/elife.54056

Article  CAS  PubMed  PubMed Central  Google Scholar 

Orsenigo F, Giampietro C, Ferrari A et al (2012) Phosphorylation of VE-cadherin is modulated by haemodynamic forces and contributes to the regulation of vascular permeability in vivo. Nat Commun 3:1208. https://doi.org/10.1038/ncomms2199

Article  CAS  PubMed  Google Scholar 

Adam AP, Sharenko AL, Pumiglia K, Vincent PA (2010) Src-induced tyrosine phosphorylation of VE-cadherin is not sufficient to decrease barrier function of endothelial monolayers. J Biol Chem 285:7045–7055. https://doi.org/10.1074/jbc.m109.079277

Article  CAS  PubMed  PubMed Central  Google Scholar 

Wessel F, Winderlich M, Holm M et al (2014) Leukocyte extravasation and vascular permeability are each controlled in vivo by different tyrosine residues of VE-cadherin. Nat Immunol 15:223–230. https://doi.org/10.1038/ni.2824

Article  CAS  PubMed  Google Scholar 

Nitzsche A, Pietilä R, Love DT et al (2021) Paladin is a phosphoinositide phosphatase regulating endosomal VEGFR2 signalling and angiogenesis. Embo Rep 22:e50218. https://doi.org/10.15252/embr.202050218

Article  CAS  PubMed  Google Scholar 

Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Bio 10:513–525. https://doi.org/10.1038/nrm2728

Article  CAS  Google Scholar 

Zhu W, Shi DS, Winter JM et al (2017) Small GTPase ARF6 controls VEGFR2 trafficking and signaling in diabetic retinopathy. J Clin Invest 127:4569–4582. https://doi.org/10.1172/jci91770

Article  PubMed  PubMed Central  Google Scholar 

Basagiannis D, Zografou S, Murphy C et al (2016) VEGF induces signalling and angiogenesis by directing VEGFR2 internalisation through macropinocytosis. J Cell Sci 129:4091–4104. https://doi.org/10.1242/jcs.188219

Article  CAS  PubMed  Google Scholar 

Lampugnani MG, Orsenigo F, Gagliani MC et al (2006) Vascular endothelial cadherin controls VEGFR-2 internalization and signaling from intracellular compartments. J Cell Biol 174:593–604. https://doi.org/10.1083/jcb.200602080

Article  CAS  PubMed  PubMed Central  Google Scholar 

Fantin A, Lampropoulou A, Senatore V et al (2017) VEGF165-induced vascular permeability requires NRP1 for ABL-mediated SRC family kinase activation. J Exp Med 214:1049–1064. https://doi.org/10.1084/jem.20160311

Article  CAS  PubMed  PubMed Central  Google Scholar 

Gong Y, Li J, Sun Y et al (2015) Optimization of an image-guided laser-induced choroidal neovascularization model in mice. PLoS ONE 10:e0132643. https://doi.org/10.1371/journal.pone.0132643

Article  CAS  PubMed  PubMed Central  Google Scholar 

Zhou HJ, Xu Z, Wang Z et al (2018) SUMOylation of VEGFR2 regulates its intracellular trafficking and pathological angiogenesis. Nat Commun 9:3303. https://doi.org/10.1038/s41467-018-05812-2

Article  CAS  PubMed  PubMed Central  Google Scholar 

Ash D, Sudhahar V, Youn S-W et al (2021) The P-type ATPase transporter ATP7A promotes angiogenesis by limiting autophagic degradation of VEGFR2. Nat Commun 12:3091. https://doi.org/10.1038/s41467-021-23408-1

Article  CAS  PubMed  PubMed Central  Google Scholar 

Kofler N, Corti F, Rivera-Molina F et al (2018) The Rab-effector protein RABEP2 regulates endosomal trafficking to mediate vascular endothelial growth factor receptor-2 (VEGFR2)-dependent signaling. J Biol Chem 293:4805–4817. https://doi.org/10.1074/jbc.m117.812172

Article  CAS  PubMed  PubMed Central  Google Scholar 

Smith GA, Fearnley GW, Abdul-Zani I et al (2016) VEGFR2 trafficking, signaling and proteolysis is regulated by the ubiquitin isopeptidase USP8. Traffic 17:53–65. https://doi.org/10.1111/tra.12341

Article  CAS  PubMed  Google Scholar 

Maghsoudlou A, Meyer RD, Rezazadeh K et al (2016) RNF121 inhibits angiogenic growth factor signaling by restricting cell surface expression of VEGFR-2. Traffic 17:289–300. https://doi.org/10.1111/tra.12353

Article  CAS  PubMed  Google Scholar 

Huckaba TM, Gennerich A, Wilhelm JE et al (2011) Kinesin-73 is a processive motor that localizes to Rab5-containing organelles. J Biol Chem 286:7457–7467. https://doi.org/10.1074/jbc.m110.167023

Article  CAS