Endosome-to-plasma membrane recycling of VEGFR2 receptor tyrosine kinase regulates endothelial function and blood vessel formation

Cells

Volumn 3, Issue 2, 2014, Pages 363-385

  Jopling, Helen M ^a   Odell, Adam F ^a   Pellet Many, Caroline ^b   Latham, Antony M ^a   Frankel, Paul ^b   Sivaprasadarao, Asipu ^a   Walker, John H ^a   Zachary, Ian C ^b   Ponnambalam, Sreenivasan ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Angiogenesis; Endothelial; Rab11a; Rab4a; Signalling; VEGF A; VEGFR2

Indexed keywords

RAB PROTEIN; RAB11A ACTIVITY; RAB4A PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL MEMBRANE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOCYTOSIS; ENDOTHELIUM CELL; FLOW CYTOMETRY; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; INTRACELLULAR SIGNALING; NONHUMAN; RNA INTERFERENCE; TRANSGENIC ZEBRAFISH; UMBILICAL VEIN ENDOTHELIAL CELL;

EID: 84923076860     PISSN: None     EISSN: 20734409     Source Type: Journal    
DOI: 10.3390/cells3020363     Document Type: Article

References (59)

1. Berger, P.; Ballmer-Hofer, K. The reception and the party after: how vascular endothelial growth factor receptor 2 explores cytoplasmic space. Swiss Med. Wkly. 2011, 141, w13318.
2. Horowitz, A.; Seerapu, H. R. Regulation of VEGF signaling by membrane traffic. Cell. Signal. 2012, 24, 1810-1820.
3. Nakayama, M.; Berger, P. Coordination of VEGF receptor trafficking and signaling by coreceptors. Exp. Cell. Res. 2013, 319, 1340-1347.
4. Maxfield, F. R.; McGraw, T. E. Endocytic recycling. Nat. Rev. Mol. Cell. Biol 2004, 5, 121-132.
5. Jones, M. C.; Caswell, P. T.; Norman, J. C. Endocytic recycling pathways: emerging regulators of cell migration. Curr. Opin. Cell Biol. 2006, 18, 549-557.
6. Gampel, A.; Moss, L.; Jones, M. C.; Brunton, V.; Norman, J. C.; Mellor, H. VEGF regulates the mobilization of VEGFR2/KDR from an intracellular endothelial storage compartment. Blood 2006, 108, 2624-2631.
7. Koch, S.; Tugues, S.; Li, X.; Gualandi, L.; Claesson-Welsh, L. Signal transduction by vascular endothelial growth factor receptors. Biochem. J. 2011, 437, 169-183.
8. Zachary, I.; Morgan, R. D. Therapeutic angiogenesis for cardiovascular disease: Biological context, challenges, prospects. Heart 2011, 97, 181-189.
9. Harper, S. J.; Bates, D. O. VEGF-A splicing: the key to anti-angiogenic therapeutics? Nat. Rev. Cancer 2008, 8, 880-887.
10. Carmeliet, P.; Ferreira, V.; Breier, G.; Pollefeyt, S.; Kieckens, L.; Gertsenstein, M.; Fahrig, M.; Vandenhoeck, A.; Harpal, K.; Eberhardt, C.; et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996, 380, 435-439.
11. Ferrara, N.; Carver-Moore, K.; Chen, H.; Dowd, M.; Lu, L.; O'Shea, K. S.; Powell-Braxton, L.; Hillan, K. J.; Moore, M. W. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996, 380, 439-442.
12. Ewan, L. C.; Jopling, H. M.; Jia, H.; Mittar, S.; Bagherzadeh, A.; Howell, G. J.; Walker, J. H.; Zachary, I. C.; Ponnambalam, S. Intrinsic tyrosine kinase activity is required for vascular endothelial growth factor receptor 2 ubiquitination, sorting and degradation in endothelial cells. Traffic 2006, 7, 1270-1282.
13. Lampugnani, M. G.; Orsenigo, F.; Gagliani, M. C.; Tacchetti, C.; Dejana, E. Vascular endothelial cadherin controls VEGFR-2 internalization and signaling from intracellular compartments. J. Cell Biol. 2006, 174, 593-604.
14. Bruns, A. F.; Herbert, S. P.; Odell, A. F.; Jopling, H. M.; Hooper, N. M.; Zachary, I. C.; Walker, J. H.; Ponnambalam, S. Ligand-stimulated VEGFR2 signaling is regulated by co-ordinated trafficking and proteolysis. Traffic 2010, 11, 161-174.
15. Jopling, H. M.; Howell, G. J.; Gamper, N.; Ponnambalam, S. The VEGFR2 receptor tyrosine kinase undergoes constitutive endosome-to-plasma membrane recycling. Biochem. Biophys. Res. Commun. 2011, 410, 170-176.
16. Howell, G. J.; Herbert, S. P.; Smith, J. M.; Mittar, S.; Ewan, L. C.; Mohammed, M.; Hunter, A. R.; Simpson, N.; Turner, A. J.; Zachary, I.; et al. Endothelial cell confluence regulates Weibel-Palade body formation. Mol. Membr. Biol. 2004, 21, 413-421.
17. Fearnley, G. W.; Smith, G. A.; Odell, A. F.; Latham, A. M.; Wheatcroft, S. B.; Harrison, M. A.; Tomlinson, D. C.; Ponnambalam, S. Vascular endothelial growth factor A-stimulated signaling from endosomes in primary endothelial cells. Meth. Enzymol. 2014, 535, 265-292.
18. Kankanala, J.; Latham, A.; Johnson, A.; Homer-Vanniasinkam, S.; Fishwick, C.; Ponnambalam, S. A combinatorial in silico and cellular approach to identify a new class of compounds that target VEGFR2 receptor tyrosine kinase activity and angiogenesis. Br. J. Pharmacol. 2012, 166, 737-748.
19. Latham, A. M.; Bruns, A. F.; Kankanala, J.; Johnson, A. P.; Fishwick, C. W.; Homer-Vanniasinkam, S.; Ponnambalam, S. Indolinones and anilinophthalazines differentially target VEGF-A-and basic fibroblast growth factor-mediated responses in primary human endothelial cells. Br. J. Pharmacol. 2012, 165, 245-259.
20. Bruns, A. F.; Yuldasheva, N.; Latham, A. M.; Bao, L.; Pellet-Many, C.; Frankel, P.; Stephen, S. L.; Howell, G. J.; Wheatcroft, S. B.; Kearney, M. T.; et al. A heat-shock protein axis regulates VEGFR2 proteolysis, blood vessel development and repair. PLoS One 2012, 7, e48539.
21. Ballmer-Hofer, K.; Andersson, A. E.; Ratcliffe, L. E.; Berger, P. Neuropilin-1 promotes VEGFR-2 trafficking through Rab11 vesicles thereby specifying signal output. Blood 2011, 118, 816-826.
22. Basu, S. K.; Goldstein, J. L.; Anderson, R. G.; Brown, M. S. Monensin interrupts the recycling of low density lipoprotein receptors in human fibroblasts. Cell 1981, 24, 493-502.
23. Stein, B. S.; Bensch, K. G.; Sussman, H. H. Complete inhibition of transferrin recycling by monensin in K562 cells. J. Biol. Chem. 1984, 259, 14762-14772.
24. Signoret, N.; Christophe, T.; Oppermann, M.; Marsh, M. pH-independent endocytic cycling of the chemokine receptor CCR5. Traffic 2004, 5, 529-543.
25. Eriksen, J.; Bjorn-Yoshimoto, W. E.; Jorgensen, T. N.; Newman, A. H.; Gether, U. Postendocytic sorting of constitutively internalized dopamine transporter in cell lines and dopaminergic neurons. J. Biol. Chem. 2010, 285, 27289-27301.
26. van der Sluijs, P.; Hull, M.; Webster, P.; Male, P.; Goud, B.; Mellman, I. The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway. Cell 1992, 70, 729-740.
27. Ullrich, O.; Reinsch, S.; Urbe, S.; Zerial, M.; Parton, R. G. Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 1996, 135, 913-924.
28. Ren, M.; Xu, G.; Zeng, J.; De Lemos-Chiarandini, C.; Adesnik, M.; Sabatini, D. D. Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc. Natl. Acad. Sci. USA 1998, 95, 6187-6192.
29. Sonnichsen, B.; De Renzis, S.; Nielsen, E.; Rietdorf, J.; Zerial, M. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol. 2000, 149, 901-914.
30. de Renzis, S.; Sonnichsen, B.; Zerial, M. Divalent Rab effectors regulate the sub-compartmental organization and sorting of early endosomes. Nat. Cell Biol. 2002, 4, 124-133.
31. Mohrmann, K.; Gerez, L.; Oorschot, V.; Klumperman, J.; van der Sluijs, P. Rab4 function in membrane recycling from early endosomes depends on a membrane to cytoplasm cycle. J. Biol. Chem. 2002, 277, 32029-32035.
32. Moore, R. H.; Millman, E. E.; Alpizar-Foster, E.; Dai, W.; Knoll, B. J. Rab11 regulates the recycling and lysosome targeting of b2-adrenergic receptors. J. Cell Sci. 2004, 117, 3107-3117.
33. Jones, M. C.; Caswell, P. T.; Moran-Jones, K.; Roberts, M.; Barry, S. T.; Gampel, A.; Mellor, H.; Norman, J. C. VEGFR1 (Flt1) regulates Rab4 recycling to control fibronectin polymerization and endothelial vessel branching. Traffic 2009, 10, 754-766.
34. Smith, R. M.; Jarett, L. Ultrastructural basis for chloroquine-induced increase in intracellular insulin in adipocytes: alteration of lysosomal function. Proc. Natl. Acad. Sci. USA 1982, 79, 7302-7306.
35. Kamei, M.; Weinstein, B. M. Long-term time-lapse fluorescence imaging of developing zebrafish. Zebrafish 2005, 2, 113-123.
36. Jopling, H. M.; Odell, A.; Hooper, N. M.; Zachary, I. C.; Walker, J. H.; Ponnambalam, S. Rab GTPase regulation of VEGFR2 trafficking and signaling in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 2009, 29, 1119-1124.
37. Bruns, A. F.; Bao, L.; Walker, J. H.; Ponnambalam, S. VEGF-A-stimulated signalling in endothelial cells via a dual receptor tyrosine kinase system is dependent on co-ordinated trafficking and proteolysis. Biochem. Soc. Trans. 2009, 37, 1193-1197.
38. Reynolds, A. R.; Hart, I. R.; Watson, A. R.; Welti, J. C.; Silva, R. G.; Robinson, S. D.; Da Violante, G.; Gourlaouen, M.; Salih, M.; Jones, M. C.; et al. Stimulation of tumor growth and angiogenesis by low concentrations of RGD-mimetic integrin inhibitors. Nat. Med. 2009, 15, 392-400.
39. McCaffrey, M. W.; Bielli, A.; Cantalupo, G.; Mora, S.; Roberti, V.; Santillo, M.; Drummond, F.; Bucci, C. Rab4 affects both recycling and degradative endosomal trafficking. FEBS Lett. 2001, 495, 21-30.
40. Gonzalez, E.; Nagiel, A.; Lin, A. J.; Golan, D. E.; Michel, T. Small interfering RNA-mediated down-regulation of caveolin-1 differentially modulates signaling pathways in endothelial cells. J. Biol. Chem. 2004, 279, 40659-40669.
41. Ikeda, S.; Ushio-Fukai, M.; Zuo, L.; Tojo, T.; Dikalov, S.; Patrushev, N. A.; Alexander, R. W. Novel role of ARF6 in vascular endothelial growth factor-induced signaling and angiogenesis. Circ. Res. 2005, 96, 467-475.
42. Bernatchez, P. N.; Acevedo, L.; Fernandez-Hernando, C.; Murata, T.; Chalouni, C.; Kim, J.; Erdjument-Bromage, H.; Shah, V.; Gratton, J. P.; McNally, E. M.; et al. Myoferlin regulates vascular endothelial growth factor receptor-2 stability and function. J. Biol. Chem. 2007, 282, 30745-30753.
43. Salikhova, A.; Wang, L.; Lanahan, A. A.; Liu, M.; Simons, M.; Leenders, W. P.; Mukhopadhyay, D.; Horowitz, A. Vascular endothelial growth factor and semaphorin induce neuropilin-1 endocytosis via separate pathways. Circ. Res. 2008, 103, e71-e79.
44. Le Saux, G.; Magenau, A.; Gunaratnam, K.; Kilian, K. A.; Bocking, T.; Gooding, J. J.; Gaus, K. Spacing of integrin ligands influences signal transduction in endothelial cells. Biophys. J. 2011, 101, 764-773.
45. Mitchell, H.; Choudhury, A.; Pagano, R. E.; Leof, E. B. Ligand-dependent and-independent transforming growth factor-b receptor recycling regulated by clathrin-mediated endocytosis and Rab11. Mol. Biol. Cell 2004, 15, 4166-4178.
46. Murphy, S. J.; Dore, J. J.; Edens, M.; Coffey, R. J.; Barnard, J. A.; Mitchell, H.; Wilkes, M.; Leof, E. B. Differential trafficking of transforming growth factor-b receptors and ligand in polarized epithelial cells. Mol. Biol. Cell 2004, 15, 2853-2862.
47. Gallant, M. A.; Slipetz, D.; Hamelin, E.; Rochdi, M. D.; Talbot, S.; de Brum-Fernandes, A. J.; Parent, J. L. Differential regulation of the signaling and trafficking of the two prostaglandin D2 receptors, prostanoid DP receptor and CRTH2. Eur. J. Pharmacol. 2007, 557, 115-123.
48. Mohrmann, K.; van der Sluijs, P. Regulation of membrane transport through the endocytic pathway by rabGTPases. Mol. Membr. Biol. 1999, 16, 81-87.
49. Ward, E. S.; Martinez, C.; Vaccaro, C.; Zhou, J.; Tang, Q.; Ober, R. J. From sorting endosomes to exocytosis: Association of Rab4 and Rab11 GTPases with the Fc receptor, FcRn, during recycling. Mol. Biol. Cell 2005, 16, 2028-2038.
50. Cormont, M.; Bortoluzzi, M. N.; Gautier, N.; Mari, M.; van Obberghen, E.; Le Marchand-Brustel, Y. Potential role of Rab4 in the regulation of subcellular localization of Glut4 in adipocytes. Mol. Cell Biol. 1996, 16, 6879-6886.
51. Mora, S.; Monden, I.; Zorzano, A.; Keller, K. Heterologous expression of rab4 reduces glucose transport and GLUT4 abundance at the cell surface in oocytes. Biochem. J. 1997, 324, 455-459.
52. Hashiramoto, M.; James, D. E. Characterization of insulin-responsive GLUT4 storage vesicles isolated from 3T3-L1 adipocytes. Mol. Cell Biol. 2000, 20, 416-427.
53. Cormont, M.; Gautier, N.; Ilc, K.; le Marchand-Brustel, Y. Expression of a prenylation-deficient Rab4 inhibits the GLUT4 translocation induced by active phosphatidylinositol 3-kinase and protein kinase B. Biochem. J. 2001, 356, 143-149.
54. Imamura, T.; Huang, J.; Usui, I.; Satoh, H.; Bever, J.; Olefsky, J. M. Insulin-induced GLUT4 translocation involves protein kinase C-lambda-mediated functional coupling between Rab4 and the motor protein kinesin. Mol. Cell Biol. 2003, 23, 4892-4900.
55. Sheff, D. R.; Daro, E. A.; Hull, M.; Mellman, I. The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. J. Cell Biol. 1999, 145, 123-139.
56. Leterrier, C.; Bonnard, D.; Carrel, D.; Rossier, J.; Lenkei, Z. Constitutive endocytic cycle of the CB1 cannabinoid receptor. J. Biol. Chem. 2004, 279, 36013-36021.
57. Roosterman, D.; Schmidlin, F.; Bunnett, N. W. Rab5a and rab11a mediate agonist-induced trafficking of protease-activated receptor 2. Am. J. Physiol. Cell Physiol. 2003, 284, C1319-C1329.
58. Dale, L. B.; Seachrist, J. L.; Babwah, A. V.; Ferguson, S. S. Regulation of angiotensin II type 1A receptor intracellular retention, degradation, and recycling by Rab5, Rab7, and Rab11 GTPases. J. Biol. Chem. 2004, 279, 13110-13118.
59. Roosterman, D.; Cottrell, G. S.; Schmidlin, F.; Steinhoff, M.; Bunnett, N. W. Recycling and resensitization of the neurokinin 1 receptor. Influence of agonist concentration and Rab GTPases. J. Biol. Chem. 2004, 279, 30670-30679.