Constitutive endocytosis of VEGFR2 protects the receptor against shedding

Journal of Biological Chemistry

Volumn 291, Issue 32, 2016, Pages 16892-16903

  Basagiannis, Dimitris ^a,b   Christoforidis, Savvas ^a,b  

^a INSTITUTE OF COMPUTER SCIENCE   (Greece)

^b UNIVERSITY OF IOANNINA   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; BLOOD VESSELS; CELL MEMBRANES;

ANGIOGENESIS; BINDING DOMAIN; EXTRACELLULAR SPACE; FUNCTIONAL STATE; GROWTH FACTOR RECEPTORS; IMMUNOPRECIPITATES; TRANSPORT CYCLE; VESSEL FORMATION;

MOLECULAR BIOLOGY;

CELL PROTEIN; CLATHRIN; DYNAMIN; PROTEASOME; PROTEIN P130; PROTEIN RAB5; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; KDR PROTEIN, HUMAN; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING DOMAIN; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CLATHRIN MEDIATED ENDOCYTOSIS; COMPARATIVE STUDY; CONSTITUTIVE ENDOCYTOSIS; CONTROLLED STUDY; ENDOCYTOSIS; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INTERNALIZATION; INTRACELLULAR SIGNALING; LIGAND BINDING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PROCESSING; PROTEIN SHEDDING; PROTEIN SYNTHESIS; UMBILICAL VEIN ENDOTHELIAL CELL; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

ENDOCYTOSIS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; PROTEIN DOMAINS; PROTEIN TRANSPORT; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84982851954     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.730309     Document Type: Article

References (70)

1. Hopkins, C. R., Miller, K., and Beardmore, J. M. (1985) Receptor-mediated endocytosis of transferrin and epidermal growth factor receptors: a comparison of constitutive and ligand-induced uptake. J. Cell Sci. Suppl. 3, 173-186
2. McMahon, H. T., and Boucrot, E. (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 12, 517-533
3. Goh, L. K., and Sorkin, A. (2013) Endocytosis of receptor tyrosine kinases. Cold Spring Harb. Perspect. Biol. 5, a017459
4. Sorkin, A., and von Zastrow, M. (2009) Endocytosis and signalling: intertwining molecular networks. Nat. Rev. Mol. Cell Biol. 10, 609-622
5. Miaczynska, M., Pelkmans, L., and Zerial, M. (2004) Not just a sink: endosomes in control of signal transduction. Curr. Opin. Cell Biol. 16, 400-406
6. Sigismund, S., Confalonieri, S., Ciliberto, A., Polo, S., Scita, G., and Di Fiore, P. P. (2012) Endocytosis and signaling: cell logistics shape the eukaryotic cell plan. Physiol. Rev. 92, 273-366
7. Ivanov, A. I. (2008) Exocytosis and endocytosis. Preface. Methods Mol. Biol. 440, v-vi
8. Di Fiore, P. P., and Gill, G. N. (1999) Endocytosis and mitogenic signaling. Curr. Opin. Cell Biol. 11, 483-488
9. Marmor, M. D., and Yarden, Y. (2004) Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases. Oncogene 23, 2057-2070
10. 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
11. Herbert, S. P., and Stainier, D. Y. (2011) Molecular control of endothelial cell behaviour during blood vessel morphogenesis. Nat. Rev. Mol. Cell Biol. 12, 551-564
12. Bhattacharya, R., Kang-Decker, N., Hughes, D. A., Mukherjee, P., Shah, V., McNiven, M. A., and Mukhopadhyay, D. (2005) Regulatory role of dynamin-2 in VEGFR-2/KDR-mediated endothelial signaling. FASEB J. 19, 1692-1694
13. Ewan, L. C., Jopling, H. M., Jia, H., Mittar, S., Bagherzadeh, A., Howell, G. J., Walker, J. H., Zachary, I. C., and Ponnambalam, S. (2006) Intrinsic tyrosine kinase activity is required for vascular endothelial growth factor receptor 2 ubiquitination, sorting and degradation in endothelial cells. Traffic 7, 1270-1282
14. 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
15. Bruns, A. F., Herbert, S. P., Odell, A. F., Jopling, H. M., Hooper, N. M., Zachary, I. C., Walker, J. H., and Ponnambalam, S. (2010) Ligand-stimulated VEGFR2 signaling is regulated by co-ordinated trafficking and proteolysis. Traffic 11, 161-174
16. Sawamiphak, S., Seidel, S., Essmann, C. L., Wilkinson, G. A., Pitulescu, M. E., Acker, T., and Acker-Palmer, A. (2010) Ephrin-B2 regulates VEGFR2 function in developmental and tumour angiogenesis. Nature 465, 487-491
17. Ballmer-Hofer, K., Andersson, A. E., Ratcliffe, L. E., and Berger, P. (2011) Neuropilin-1 promotes VEGFR-2 trafficking through Rab11 vesicles thereby specifying signal output. Blood 118, 816-826
18. Pasula, S., Cai, X., Dong, Y., Messa, M., McManus, J., Chang, B., Liu, X., Zhu, H., Mansat, R. S., Yoon, S. J., Hahn, S., Keeling, J., Saunders, D., Ko, G., Knight, J., et al. (2012) Endothelial epsin deficiency decreases tumor growth by enhancing VEGF signaling. J. Clin. Invest. 122, 4424-4438
19. 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., Zachary, I. C., and Ponnambalam, S. (2012) A heat-shock protein axis regulates VEGFR2 proteolysis, blood vessel development and repair. PLoS ONE 7, e48539
20. Gourlaouen, M., Welti, J. C., Vasudev, N. S., and Reynolds, A. R. (2013) Essential role for endocytosis in the growth factor-stimulated activation of ERK1/2 in endothelial cells. J. Biol. Chem. 288, 7467-7480
21. Nakayama, M., Nakayama, A., van Lessen, M., Yamamoto, H., Hoffmann, S., Drexler, H. C., Itoh, N., Hirose, T., Breier, G., Vestweber, D., Cooper, J. A., Ohno, S., Kaibuchi, K., and Adams, R. H. (2013) Spatial regulation of VEGF receptor endocytosis in angiogenesis. Nat. Cell Biol. 15, 249-260
22. Tessneer, K. L., Pasula, S., Cai, X., Dong, Y., McManus, J., Liu, X., Yu, L., Hahn, S., Chang, B., Chen, Y., Griffin, C., Xia, L., Adams, R. H., and Chen, H. (2014) Genetic reduction of vascular endothelial growth factor receptor 2 rescues aberrant angiogenesis caused by epsin deficiency. Arterioscler. Thromb. Vasc. Biol. 34, 331-337
23. Lee, M. Y., Skoura, A., Park, E. J., Landskroner-Eiger, S., Jozsef, L., Luciano, A. K., Murata, T., Pasula, S., Dong, Y., Bouaouina, M., Calderwood, D. A., Ferguson, S. M., De Camilli, P., and Sessa, W. C. (2014) Dynamin 2 regulation of integrin endocytosis, but not VEGF signaling, is crucial for developmental angiogenesis. Development 141, 1465-1472
24. Koch, S., van Meeteren, L. A., Morin, E., Testini, C., Weström, S., Björkelund, H., Le Jan, S., Adler, J., Berger, P., and Claesson-Welsh, L. (2014) NRP1 presented in trans to the endothelium arrests VEGFR2 endocytosis, preventing angiogenic signaling and tumor initiation. Dev. Cell 28, 633-646
25. Gampel, A., Moss, L., Jones, M. C., Brunton, V., Norman, J. C., and Mellor, H. (2006) VEGF regulates the mobilization of VEGFR2/KDR from an intracellular endothelial storage compartment. Blood 108, 2624-2631
26. Jopling, H. M., Howell, G. J., Gamper, N., and Ponnambalam, S. (2011) The VEGFR2 receptor tyrosine kinase undergoes constitutive endosome-to-plasma membrane recycling. Biochem. Biophys. Res. Commun. 410, 170-176
27. 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., Jones, D. T., Saunders, G., Kostourou, V., Perron-Sierra, F., Norman, J. C., Tucker, G. C., and Hodivala-Dilke, K. M. (2009) Stimulation of tumor growth and angiogenesis by low concentrations of RGD-mimetic integrin inhibitors. Nat. Med. 15, 392-400
28. Schmid, S. L., and Frolov, V. A. (2011) Dynamin: functional design of a membrane fission catalyst. Annu. Rev. Cell Dev. Biol. 27, 79-105
29. Ferguson, S. M., and De Camilli, P. (2012) Dynamin, a membrane-remodelling GTPase. Nat. Rev. Mol. Cell Biol. 13, 75-88
30. Macia, E., Ehrlich, M., Massol, R., Boucrot, E., Brunner, C., and Kirchhausen, T. (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 10, 839-850
31. Ivanov, A. I. (2014) Pharmacological inhibitors of exocytosis and endocytosis: novel bullets for old targets. Methods Mol. Biol. 1174, 3-18
32. Damke, H., Baba, T., van der Bliek, A. M., and Schmid, S. L. (1995) Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J. Cell Biol. 131, 69-80
33. Pelkmans, L., Bürli, T., Zerial, M., and Helenius, A. (2004) Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 118, 767-780
34. Mayor, S., and Pagano, R. E. (2007) Pathways of clathrin-independent endocytosis. Nat. Rev. Mol. Cell Biol. 8, 603-612
35. Shvets, E., Ludwig, A., and Nichols, B. J. (2014) News from the caves: update on the structure and function of caveolae. Curr. Opin. Cell Biol. 29, 99-106
36. Parton, R. G., and del Pozo, M. A. (2013) Caveolae as plasma membrane sensors, protectors and organizers. Nat. Rev. Mol. Cell Biol. 14, 98-112
37. Lajoie, P., and Nabi, I. R. (2010) Lipid rafts, caveolae, and their endocytosis. Int. Rev. Cell Mol. Biol. 282, 135-163
38. Mukherjee, S., Tessema, M., and Wandinger-Ness, A. (2006) Vesicular trafficking of tyrosine kinase receptors and associated proteins in the regulation of signaling and vascular function. Circ. Res. 98, 743-756
39. McLauchlan, H., Newell, J., Morrice, N., Osborne, A., West, M., and Smythe, E. (1998) A novel role for Rab5-GDI in ligand sequestration into clathrin-coated pits. Curr. Biol. 8, 34-45
40. Christoforidis, S., McBride, H. M., Burgoyne, R. D., and Zerial, M. (1999) The Rab5 effector EEA1 is a core component of endosome docking. Nature 397, 621-625
41. Somsel Rodman, J., and Wandinger-Ness, A. (2000) Rab GTPases coordinate endocytosis. J. Cell Sci. 113, 183-192
42. Numrich, J., and Ungermann, C. (2014) Endocytic Rabs in membrane trafficking and signaling. Biol. Chem. 395, 327-333
43. Park, S. Y., Shi, X., Pang, J., Yan, C., and Berk, B. C. (2013) Thioredoxin-interacting protein mediates sustained VEGFR2 signaling in endothelial cells required for angiogenesis. Arterioscler. Thromb. Vasc. Biol. 33, 737-743
44. Stenmark, H., Parton, R. G., Steele-Mortimer, O., Lütcke, A., Gruenberg, J., and Zerial, M. (1994) Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 13, 1287-1296
45. Hunker, C. M., Kruk, I., Hall, J., Giambini, H., Veisaga, M. L., and Barbieri, M. A. (2006) Role of Rab5 in insulin receptor-mediated endocytosis and signaling. Arch. Biochem. Biophys. 449, 130-142
46. Takahashi, T., and Shibuya, M. (1997) The 230 kDa mature form of KDR/Flk-1 (VEGF receptor-2) activates the PLC-γ pathway and partially induces mitotic signals in NIH3T3 fibroblasts. Oncogene 14, 2079-2089
47. McNiven, M. A., Cao, H., Pitts, K. R., and Yoon, Y. (2000) The dynamin family of mechanoenzymes: pinching in new places. Trends Biochem. Sci. 25, 115-120
48. Praefcke, G. J., and McMahon, H. T. (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nat. Rev. Mol. Cell Biol. 5, 133-147
49. González-Jamett, A. M., Momboisse, F., Haro-Acuna, V., Bevilacqua, J. A., Caviedes, P., and Cardenas, A. M. (2013) Dynamin-2 function and dysfunction along the secretory pathway. Front. Endocrinol. (Lausanne) 4, 126
50. Robinson, D. G., and Pimpl, P. (2014) Clathrin and post-Golgi trafficking: a very complicated issue. Trends Plant Sci. 19, 134-139
51. Lodish, H. F., Kong, N., Snider, M., and Strous, G. J. (1983) Hepatoma secretory proteins migrate from rough endoplasmic reticulum to Golgi at characteristic rates. Nature 304, 80-83
52. Mohler, K. M., Sleath, P. R., Fitzner, J. N., Cerretti, D. P., Alderson, M., Kerwar, S. S., Torrance, D. S., Otten-Evans, C., Greenstreet, T., and Weerawarna, K. (1994) Protection against a lethal dose of endotoxin by an inhibitor of tumour necrosis factor processing. Nature 370, 218-220
53. Ebos, J. M., Bocci, G., Man, S., Thorpe, P. E., Hicklin, D. J., Zhou, D., Jia, X., and Kerbel, R. S. (2004) A naturally occurring soluble form of vascular endothelial growth factor receptor 2 detected in mouse and human plasma. Mol. Cancer Res. 2, 315-326
54. Albuquerque, R. J., Hayashi, T., Cho, W. G., Kleinman, M. E., Dridi, S., Takeda, A., Baffi, J. Z., Yamada, K., Kaneko, H., Green, M. G., Chappell, J., Wilting, J., Weich, H. A., Yamagami, S., Amano, S., et al. (2009) Alternatively spliced vascular endothelial growth factor receptor-2 is an essential endogenous inhibitor of lymphatic vessel growth. Nat. Med. 15, 1023-1030
55. Domigan, C. K., and Iruela-Arispe, M. L. (2014) Stealing VEGF from thy neighbor. Cell 159, 473-474
56. Smith, G. A., Fearnley, G. W., Abdul-Zani, I., Wheatcroft, S. B., Tomlinson, D. C., Harrison, M. A., and Ponnambalam, S. (2016) VEGFR2 trafficking, signaling and proteolysis is regulated by the ubiquitin isopeptidase USP8. Traffic 17, 53-65
57. Swendeman, S., Mendelson, K., Weskamp, G., Horiuchi, K., Deutsch, U., Scherle, P., Hooper, A., Rafii, S., and Blobel, C. P. (2008) VEGF-A stimulates ADAM17-dependent shedding of VEGFR2 and crosstalk between VEGFR2 and ERK signaling. Circ. Res. 103, 916-918
58. Donners, M. M., Wolfs, I. M., Olieslagers, S., Mohammadi-Motahhari, Z., Tchaikovski, V., Heeneman, S., van Buul, J. D., Caolo, V., Molin, D. G., Post, M. J., and Waltenberger, J. (2010) A disintegrin and metalloprotease 10 is a novel mediator of vascular endothelial growth factor-induced endothelial cell function in angiogenesis and is associated with atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 30, 2188-2195
59. Jin, Y., Liu, Y., Lin, Q., Li, J., Druso, J. E., Antonyak, M. A., Meininger, C. J., Zhang, S. L., Dostal, D. E., Guan, J. L., Cerione, R. A., and Peng, X. (2013) Deletion of Cdc42 enhances ADAM17-mediated vascular endothelial growth factor receptor 2 shedding and impairs vascular endothelial cell survival and vasculogenesis. Mol. Cell Biol. 33, 4181-4197
60. Gupta-Rossi, N., Six, E., LeBail, O., Logeat, F., Chastagner, P., Olry, A., Israël, A., and Brou, C. (2004) Monoubiquitination and endocytosis direct γ-secretase cleavage of activated Notch receptor. J. Cell Biol. 166, 73-83
61. Buchanan, S. M., Schalm, S. S., and Maniatis, T. (2010) Proteolytic processing of protocadherin proteins requires endocytosis. Proc. Natl. Acad. Sci. U.S.A. 107, 17774-17779
62. Huang, Y.-W., Su, P., Liu, G. Y., Crow, M. R., Chaukos, D., Yan, H., and Robinson, L. A. (2009) Constitutive endocytosis of the chemokine CX3CL1 prevents its degradation by cell surface metalloproteases. J. Biol. Chem. 284, 29644-29653
63. Chyung, J. H., and Selkoe, D. J. (2003) Inhibition of receptor-mediated endocytosis demonstrates generation of amyloid β-protein at the cell surface. J. Biol. Chem. 278, 51035-51043
64. Fukuda, S., Nishida-Fukuda, H., Nakayama, H., Inoue, H., and Higashiyama, S. (2012) Monoubiquitination of pro-amphiregulin regulates its endocytosis and ectodomain shedding. Biochem. Biophys. Res. Commun. 420, 315-320
65. Carey, R. M., Balcz, B. A., Lopez-Coviella, I., and Slack, B. E. (2005) Inhibition of dynamin-dependent endocytosis increases shedding of the amyloid precursor protein ectodomain and reduces generation of amyloid beta protein. BMC Cell Biol. 6, 30
66. Zografou, S., Basagiannis, D., Papafotika, A., Shirakawa, R., Horiuchi, H., Auerbach, D., Fukuda, M., and Christoforidis, S. (2012) A complete Rab screening reveals novel insights in Weibel-Palade body exocytosis. J. Cell Sci. 125, 4780-4790
67. Panopoulou, E., Gillooly, D. J., Wrana, J. L., Zerial, M., Stenmark, H., Murphy, C., and Fotsis, T. (2002) Early endosomal regulation of Smad-dependent signaling in endothelial cells. J. Biol. Chem. 277, 18046-18052
68. Tiscornia, G., Singer, O., and Verma, I. M. (2006) Production and purification of lentiviral vectors. Nat. Protoc. 1, 241-245
69. Papanikolaou, A., Papafotika, A., and Christoforidis, S. (2011) CD39 reveals novel insights into the role of transmembrane domains in protein processing, apical targeting and activity. Traffic 12, 1148-1165
70. Roberts, M., Barry, S., Woods, A., van der Sluijs, P., and Norman, J. (2001) PDGF-regulated rab4-dependent recycling of αvβ3 integrin from early endosomes is necessary for cell adhesion and spreading. Curr. Biol. 11, 1392-1402