Involvement of lysosomal degradation in VEGF-C-induced down-regulation of VEGFR-3

FEBS Letters

Volumn 588, Issue 23, 2014, Pages 4357-4363

  Han, Kyu Yeon ^a   Chang, Jin Hong ^a   Dugas Ford, Jennifer ^a   Alexander, Jonathan S ^b   Azar, Dimitri T ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Lysosomal degradation; VEGF receptor 3; VEGF C

Indexed keywords

GAMMA SECRETASE INHIBITOR; LEUPEPTIN; MITOGEN ACTIVATED PROTEIN KINASE P38; N [N (3 CARBOXYOXIRANE 2 CARBONYL)LEUCYL]AGMATINE; NOTCH1 RECEPTOR; PEPSTATIN; PROTEIN TYROSINE KINASE INHIBITOR; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; VASCULOTROPIN C; VASCULOTROPIN C156S; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR 3; LIGAND; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE INHIBITOR;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPH VESSEL; LYSOSOME; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; CELL LINE; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; PHOSPHORYLATION; PROTEIN DEGRADATION; PROTEIN TRANSPORT;

CELL LINE; DOWN-REGULATION; ENDOTHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIGANDS; LYSOSOMES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN TRANSPORT; PROTEOLYSIS; RNA, MESSENGER; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR C; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 84910646473     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.09.034     Document Type: Article

References (41)

1. D. Ellenberg, D.T. Azar, J.A. Hallak, F. Tobaigy, K.Y. Han, S. Jain, Z. Zhou, and J.H. Chang Novel aspects of corneal angiogenic and lymphangiogenic privilege Prog. Retin. Eye Res. 29 2010 208 248
2. V. Joukov 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 1996 1751
3. Y. Cao Opinion: emerging mechanisms of tumour lymphangiogenesis and lymphatic metastasis Nat. Rev. Cancer 5 2005 735 743
4. R.J. Albuquerque Alternatively spliced vascular endothelial growth factor receptor-2 is an essential endogenous inhibitor of lymphatic vessel growth Nat. Med. 15 2009 1023 1030
5. S. Coso, E. Bovay, and T.V. Petrova Pressing the right buttons: signaling in lymphangiogenesis Blood 123 2014 2614 2624
6. C. Cursiefen VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment J. Clin. Invest. 113 2004 1040 1050
7. F. Galvagni 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 2010 1839 1848
8. A. Salameh, F. Galvagni, M. Bardelli, F. Bussolino, and S. Oliviero Direct recruitment of CRK and GRB2 to VEGFR-3 induces proliferation, migration, and survival of endothelial cells through the activation of ERK, AKT, and JNK pathways Blood 106 2005 3423 3431
9. M. Graupera, and M. Potente Regulation of angiogenesis by PI3K signaling networks Exp. Cell Res. 319 2013 1348 1355
10. R. Roskoski Jr. ERK1/2 MAP kinases: structure, function, and regulation Pharmacol. Res. 66 2012 105 143
11. P. Emami-Naeini, T.H. Dohlman, M. Omoto, T. Hattori, Y. Chen, H.S. Lee, S.K. Chauhan, and R. Dana Soluble vascular endothelial growth factor receptor-3 suppresses allosensitization and promotes corneal allograft survival Graefes Arch. Clin. Exp. Ophthalmol 2014
12. I. Omoto Expression of vascular endothelial growth factor-C and vascular endothelial growth factor receptor-3 in esophageal squamous cell carcinoma Oncol. Lett. 7 2014 1027 1032
13. D. Hos, F. Bock, T. Dietrich, J. Onderka, F.E. Kruse, K.H. Thierauch, and C. Cursiefen Inflammatory corneal (lymph)angiogenesis is blocked by VEGFR-tyrosine kinase inhibitor ZK 261991, resulting in improved graft survival after corneal transplantation Invest. Ophthalmol. Vis. Sci. 49 2008 1836 1842
14. H. Zhang, S. Grimaldo, D. Yuen, and L. Chen Combined blockade of VEGFR-3 and VLA-1 markedly promotes high-risk corneal transplant survival Invest. Ophthalmol. Vis. Sci. 52 2011 6529 6535
15. Y.W. Chang Novel peptides suppress VEGFR-3 activity and antagonize VEGFR-3-mediated oncogenic effects Oncotarget 5 2014 3823 3835
16. N. Singh Soluble vascular endothelial growth factor receptor 3 is essential for corneal alymphaticity Blood 121 2013 4242 4249
17. K. Hamada, Y. Oike, N. Takakura, Y. Ito, L. Jussila, D.J. Dumont, K. Alitalo, and T. Suda VEGF-C signaling pathways through VEGFR-2 and VEGFR-3 in vasculoangiogenesis and hematopoiesis Blood 96 2000 3793 3800
18. T. Tammela VEGFR-3 controls tip to stalk conversion at vessel fusion sites by reinforcing Notch signalling Nat. Cell Biol. 13 2011 1202 1213
19. T. Tammela Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation Nature 454 2008 656 660
20. T. Li, G.D. Wang, Y.Z. Tan, and H.J. Wang Inhibition of lymphangiogenesis of endothelial progenitor cells with VEGFR-3 siRNA delivered with PEI-alginate nanoparticles Int. J. Biol. Sci. 10 2014 160 170
21. C.A. Heckman The tyrosine kinase inhibitor cediranib blocks ligand-induced vascular endothelial growth factor receptor-3 activity and lymphangiogenesis Cancer Res. 68 2008 4754 4762
22. T. Kojima, D.T. Azar, and J.H. Chang Neostatin-7 regulates bFGF-induced corneal lymphangiogenesis FEBS Lett. 582 2008 2515 2520
23. C.J. Shawber Notch alters VEGF responsiveness in human and murine endothelial cells by direct regulation of VEGFR-3 expression J. Clin. Invest. 117 2007 3369 3382
24. P.A. Eisenach, C. Roghi, M. Fogarasi, G. Murphy, and W.R. English MT1-MMP regulates VEGF-A expression through a complex with VEGFR-2 and Src J. Cell Sci. 123 2010 4182 4193
25. K.Y. Han, D.C. Fahd, M. Tshionyi, N. Allemann, S. Jain, J.H. Chang, and D.T. Azar MT1-MMP modulates bFGF-induced VEGF-A expression in corneal fibroblasts Protein Pept. Lett. 19 2012 1334 1339
26. A. Karroum, P. Mirshahi, A.M. Faussat, A. Therwath, M. Mirshahi, and M. Hatmi Tubular network formation by adriamycin-resistant MCF-7 breast cancer cells is closely linked to MMP-9 and VEGFR-2/VEGFR-3 over-expressions Eur. J. Pharmacol. 685 2012 1 7
27. L.K. Goh, F. Huang, W. Kim, S. Gygi, and A. Sorkin Multiple mechanisms collectively regulate clathrin-mediated endocytosis of the epidermal growth factor receptor J. Cell Biol. 189 2010 871 883
28. L.C. Ewan Intrinsic tyrosine kinase activity is required for vascular endothelial growth factor receptor 2 ubiquitination, sorting and degradation in endothelial cells Traffic 7 2006 1270 1282
29. M.G. Lampugnani, F. Orsenigo, M.C. Gagliani, C. Tacchetti, and E. Dejana Vascular endothelial cadherin controls VEGFR-2 internalization and signaling from intracellular compartments J. Cell Biol. 174 2006 593 604
30. F. Galvagni, F. Anselmi, A. Salameh, M. Orlandini, M. Rocchigiani, and S. Oliviero Vascular endothelial growth factor receptor-3 activity is modulated by its association with caveolin-1 on endothelial membrane Biochemistry 46 2007 3998 4005
31. A. Garouniatis, A. Zizi-Sermpetzoglou, S. Rizos, A. Kostakis, N. Nikiteas, and A.G. Papavassiliou Vascular endothelial growth factor receptors 1,3 and caveolin-1 are implicated in colorectal cancer aggressiveness and prognosis-correlations with epidermal growth factor receptor, CD44v6, focal adhesion kinase, and c-Met Tumour Biol. 34 2013 2109 2117
32. T. Ando, P. Jordan, T. Joh, Y. Wang, M.H. Jennings, J. Houghton, and J.S. Alexander Isolation and characterization of a novel mouse lymphatic endothelial cell line: SV-LEC Lymphat. Res. Biol. 3 2005 105 115
33. M. Freitas-Andrade, P. Carmeliet, D.B. Stanimirovic, and M. Moreno VEGFR-2-mediated increased proliferation and survival in response to oxygen and glucose deprivation in PlGF knockout astrocytes J. Neurochem. 107 2008 756 767
34. N. Rahimi, T.E. Golde, and R.D. Meyer Identification of ligand-induced proteolytic cleavage and ectodomain shedding of VEGFR-1/FLT1 in leukemic cancer cells Cancer Res. 69 2009 2607 2614
35. T. Veikkola Signalling via vascular endothelial growth factor receptor-3 is sufficient for lymphangiogenesis in transgenic mice EMBO J. 20 2001 1223 1231
36. H.A. Weich Quantification of vascular endothelial growth factor-C (VEGF-C) by a novel ELISA J. Immunol. Methods 285 2004 145 155
37. M.G. Achen, and S.A. Stacker The vascular endothelial growth factor family; proteins which guide the development of the vasculature Int. J. Exp. Pathol. 79 1998 255 265
38. M. Koch VEGF-D deficiency in mice does not affect embryonic or postnatal lymphangiogenesis but reduces lymphatic metastasis J. Pathol. 219 2009 356 364
39. E.S. Chung Contribution of macrophages to angiogenesis induced by vascular endothelial growth factor receptor-3-specific ligands Am. J. Pathol. 175 2009 1984 1992
40. E. Mizuno, T. Iura, A. Mukai, T. Yoshimori, N. Kitamura, and M. Komada Regulation of epidermal growth factor receptor down-regulation by UBPY-mediated deubiquitination at endosomes Mol. Biol. Cell 16 2005 5163 5174
41. A.F. Bruns, S.P. Herbert, A.F. Odell, H.M. Jopling, N.M. Hooper, I.C. Zachary, J.H. Walker, and S. Ponnambalam Ligand-stimulated VEGFR2 signaling is regulated by co-ordinated trafficking and proteolysis Traffic 11 2010 161 174