Secretion of VEGF-165 has unique characteristics, including shedding from the plasma membrane

Molecular Biology of the Cell

Volumn 25, Issue 7, 2014, Pages 1061-1072

  Guzmán Hernández, Maria Luisa ^a   Potter, Gael ^b   Egervári, Kristòf ^b   Kiss, Jozsef Z ^b   Balla, Tamas ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; CALCIUM; EPITOPE; GREEN FLUORESCENT PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN KINASE C; PROTEIN SAR1; UNCLASSIFIED DRUG; VASCULOTROPIN 165; GUANOSINE TRIPHOSPHATASE; HYBRID PROTEIN; RAPAMYCIN; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ARTICLE; CELL MEMBRANE; CELL MIGRATION; CELL SURFACE; CELLULAR DISTRIBUTION; CELLULAR SECRETION; ENDOPLASMIC RETICULUM; GLYCOSYLATION; GOLGI COMPLEX; HUMAN; HUMAN CELL; MEMBRANE COMPONENT; PRIORITY JOURNAL; ANIMAL; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; DRUG EFFECTS; METABOLISM; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; SECRETION (PROCESS); ULTRASTRUCTURE; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOPLASMIC RETICULUM; GLYCOSYLATION; GOLGI APPARATUS; GREEN FLUORESCENT PROTEINS; GTP PHOSPHOHYDROLASES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SIROLIMUS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84898754872     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-07-0418     Document Type: Article

References (57)

1. Bose S, Mucke M, Freedman RB (1994). The characterization of a cyclophilin-type peptidyl prolyl cis-trans-isomerase from the endoplasmic-reticulum lumen. Biochem J 300, 871-875 (Pubitemid 24180606)
2. Brown FD, Rozelle AL, Yin HL, Balla T, Donaldson JG (2001). Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic. J Cell Biol 154, 1007-1017 (Pubitemid 34286180)
3. Carmeliet P, Collen D (1999). Role of vascular endothelial growth factor and vascular endothelial growth factor receptors in vascular development. Curr Top Microbiol Immunol 237, 133-158 (Pubitemid 28554862)
4. Carmeliet P, Ruiz de Almodovar C (2013). VEGF ligands and receptors: Implications in neurodevelopment and neurodegeneration. Cell Mol Life Sci 70, 1763-1778
5. Chen E, Hermanson S, Ekker SC (2004). Syndecan-2 is essential for angiogenic sprouting during zebrafish development. Blood 103, 1710-1719 (Pubitemid 38268963)
6. Chen S, Chakrabarti R, Keats EC, Chen M, Chakrabarti S, Khan ZA (2012). Regulation of vascular endothelial growth factor expression by extra domain B segment of fibronectin in endothelial cells. Invest Ophthalmol Vis Sci 53, 8333-8343
7. Chen TT, Luque A, Lee S, Anderson SM, Segura T, Iruela-Arispe ML (2010). Anchorage of VEGF to the extracellular matrix conveys differential signaling responses to endothelial cells. J Cell Biol 188, 595-609
8. Claesson-Welsh L, Welsh M (2013). VEGFA and tumour angiogenesis. J Intern Med 273, 114-127
9. Claffey KP, Senger DR, Spiegelman BM (1995). Structural requirements for dimerization, glycosylation, secretion, and biological function of VPF/VEGF. Biochim Biophys Acta 1246, 1-9
10. Claffey KP, Shih SC, Mullen A, Dziennis S, Cusick JL, Abrams KR, Lee SW, Detmar M (1998). Identification of a human VPF/VEGF 3' untranslated region mediating hypoxia-induced mRNA stability. Mol Biol Cell 9, 469-481 (Pubitemid 28084138)
11. Donaldson JG, Jackson CL (2011). ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat Rev Mol Cell Biol 12, 362-375
12. Eichmann A, Simons M (2012). VEGF signaling inside vascular endothelial cells and beyond. Curr Opin Cell Biol 24, 188-193
13. Esko JD, Stewart TE, Taylor WH (1985). Animal cell mutants defective in glycosaminoglycan biosynthesis. Proc Natl Acad Sci USA 82, 3197-3201 (Pubitemid 15029573)
14. Fearon P, Lonsdale-Eccles AA, Ross OK, Todd C, Sinha A, Allain F, Reynolds NJ (2011). Keratinocyte secretion of cyclophilin B via the constitutive pathway is regulated through its cyclosporin-binding site. J Invest Dermatol 131, 1085-1094
15. Ferrara N (2009). VEGF-A: A critical regulator of blood vessel growth. Eur Cytokine Netw 20, 158-163
16. Ferrara N, Gerber HP, LeCouter J (2003). The biology of VEGF and its receptors. Nat Med 9, 669-676 (Pubitemid 36749215)
17. Friedmann E, Hauben E, Maylandt K, Schleeger S, Vreugde S, Lichtenthaler SF, Kuhn PH, Stauffer D, Rovelli G, Martoglio B (2006). SPPL2a and SPPL2b promote intramembrane proteolysis of TNFalpha in activated dendritic cells to trigger IL-12 production. Nat Cell Biol 8, 843-848 (Pubitemid 44151587)
18. Gengrinovitch S, Berman B, David G, Witte L, Neufeld G, Ron D (1999). Glypican-1 is a VEGF165 binding proteoglycan that acts as an extracellular chaperone for VEGF165. J Biol Chem 274, 10816-10822
19. Grunewald FS, Prota AE, Giese A, Ballmer-Hofer K (2010). Structure-function analysis of VEGF receptor activation and the role of coreceptors in angiogenic signaling. Biochim Biophys Acta 1804, 567-580
20. Hammond GR, Fischer MJ, Anderson KE, Holdich J, Koteci A, Balla T, Irvine RF (2012). PI4P and PI(4,5)P2 are essential but independent lipid determinants of membrane identity. Science 337, 727-730
21. Hilmi C, Guyot M, Pages G (2012). VEGF spliced variants: possible role of anti-angiogenesis therapy. J Nucleic Acids 2012, 162692
22. Houck KA, Ferrara N, Winer J, Cachianes G, Li B, Leung DW (1991). The vascular endothelial growth factor family: Identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol Endocrinol 5, 1806-1814
23. Houck KA, Leung DW, Rowland AM, Winer J, Ferrara N (1992). Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J Biol Chem 267, 26031-26037 (Pubitemid 23014012)
24. Huez I, Bornes S, Bresson D, Creancier L, Prats H (2001). New vascular endothelial growth factor isoform generated by internal ribosome entry site-driven CUG translation initiation. Mol Endocrinol 15, 2197-2210 (Pubitemid 33141138)
25. Ikeda E, Achen MG, Breier G, Risau W (1995). Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells. J Biol Chem 270, 19761-19766
26. Inoue T, Heo WD, Grimley JS, Wandless TJ, Meyer T (2005). An inducible translocation strategy to rapidly activate and inhibit small GTPase signaling pathways. Nat Methods 2, 415-418 (Pubitemid 40916559)
27. Inoue H, Sakaue T, Ozawa T, Higashiyama S (2013). Spatiotemporal visualization of proHB-EGF ectodomain shedding in living cells. J Biochem 154, 67-76
28. James DJ, Khodthong C, Kowalchyk JA, Martin TF (2008). Phosphatidylinositol 4,5-bisphosphate regulates SNARE-dependent membrane fusion. J Cell Biol 182, 355-366
29. Keck RG, Berleau L, Harris R, Keyt BA (1997). Disulfide structure of the heparin binding domain in vascular endothelial growth factor: characterization of posttranslational modifications in VEGF. Arch Biochem Biophys 344, 103-113 (Pubitemid 27328102)
30. Kim YJ, Guzman-Hernandez ML, Balla T (2011). A highly dynamic ER-derived phosphatidylinositol-synthesizing organelle supplies phosphoinositides to cellular membranes. Dev Cell 21, 813-824
31. Koch S, Tugues S, Li X, Gualandi L, Claesson-Welsh L (2011). Signal transduction by vascular endothelial growth factor receptors. Biochem J 437, 169-183
32. Krilleke D, DeErkenez A, Schubert W, Giri I, Robinson GS, Ng YS, Shima DT (2007). Molecular mapping and functional characterization of the VEGF164 heparin-binding domain. J Biol Chem 282, 28045-28056 (Pubitemid 47533565)
33. Lee S, Jilani SM, Nikolova GV, Carpizo D, Iruela-Arispe ML (2005). Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors. J Cell Biol 169, 681-691 (Pubitemid 41002860)
34. Levy AP, Levy NS, Goldberg MA (1996). Post-transcriptional regulation of vascular endothelial growth factor by hypoxia. J Biol Chem 271, 2746-2753 (Pubitemid 26047892)
35. Li W, Keller G (2000). VEGF nuclear accumulation correlates with phenotypical changes in endothelial cells. J Cell Sci 113, 1525-1534 (Pubitemid 30312501)
36. Liu Y, Berendsen AD, Jia S, Lotinun S, Baron R, Ferrara N, Olsen BR (2012). Intracellular VEGF regulates the balance between osteoblast and adipocyte differentiation. J Clin Invest 122, 3101-3113
37. Meiron M, Anunu R, Scheinman EJ, Hashmueli S, Levi BZ (2001). New isoforms of VEGF are translated from alternative initiation CUG codons located in its 5'UTR. Biochem Biophys Res Commun 282, 1053-1060 (Pubitemid 32924602)
38. Milosevic I, Sorensen JB, Lang T, Krauss M, Nagy G, Haucke V, Jahn R, Neher E (2005). Plasmalemmal phosphatidylinositol-4,5-bisphosphate level regulates the releasable vesicle pool size in chromaffin cells. J Neurosci 25, 2557-2565 (Pubitemid 40365167)
39. Mukdsi JH, De Paul AL, Gutierrez S, Roth FD, Aoki A, Torres AI (2005). Subcellular localisation of VEGF in different pituitary cells. Changes of its expression in oestrogen induced prolactinomas. J Mol Histol 36, 447-454 (Pubitemid 43829383)
40. Muller D, Wang C, Skibo G, Toni N, Cremer H, Calaora V, Rougon G, Kiss JZ (1996). PSA-NCAM is required for activity-induced synaptic plasticity. Neuron 17, 413-422 (Pubitemid 26322213)
41. Nowak DG et al. (2010). Regulation of vascular endothelial growth factor (VEGF) splicing from pro-angiogenic to anti-angiogenic isoforms: A novel therapeutic strategy for angiogenesis. J Biol Chem 285, 5532-5540
42. Park JE, Keller GA, Ferrara N (1993). The vascular endothelial growth factor (VEGF) isoforms: differential deposition into the subepithelial extracellular matrix and bioactivity of extracellular matrix-bound VEGF. Mol Biol Cell 4, 1317-1326 (Pubitemid 24045761)
43. Price ER, Jin M, Lim D, Pati S, Walsh CT, McKeon FD (1994). Cyclophilin B trafficking through the secretory pathway is altered by binding of cyclosporin A. Proc Natl Acad Sci USA 91, 3931-3935 (Pubitemid 24139546)
44. Pucadyil TJ, Schmid SL (2009). Conserved functions of membrane active GTPases in coated vesicle formation. Science 325, 1217-1220
45. Salmon P (2013). Generation of human cell lines using lentiviral-mediated genetic engineering. Methods Mol Biol 945, 417-448
46. Selleck SB (2006). Signaling from across the way: transactivation of VEGF receptors by HSPGs. Mol Cell 22, 431-432
47. Shah BH, Yesilkaya A, Olivares-Reyes JA, Chen HD, Hunyady L, Catt KJ (2004). Differential pathways of angiotensin II-induced extracellularly regulated kinase 1/2 phosphorylation in specific cell types: role of heparin-binding epidermal growth factor. Mol Endocrinol 18, 2035-2048 (Pubitemid 39006507)
48. Shibuya M (2013). Vascular endothelial growth factor and its receptor system: physiological functions in angiogenesis and pathological roles in various diseases. J Biochem 153, 13-19
49. Stein I, Neeman M, Shweiki D, Itin A, Keshet E (1995). Stabilization of vascular endothelial growth factor mRNA by hypoxia and hypoglycemia and coregulation with other ischemia-induced genes. Mol Cell Biol 15, 5363-5368
50. Tee MK, Jaffe RB (2001). A precursor form of vascular endothelial growth factor arises by initiation from an upstream in-frame CUG codon. Biochem J 359, 219-226 (Pubitemid 32939224)
51. Varnai P, Thyagarajan B, Rohacs T, Balla T (2006). Rapidly inducible changes in phosphatidylinositol 4,5-bisphosphate levels influence multiple regulatory functions of the lipid in intact living cells. J Cell Biol 175, 377-382 (Pubitemid 44708062)
52. Walter DH et al. (1996). The in vivo bioactivity of vascular endothelial growth factor/vascular permeability factor is independent of N-linked glycosylation. Lab Invest 74, 546-556 (Pubitemid 26072095)
53. Warren CM, Iruela-Arispe ML (2010). Signaling circuitry in vascular morphogenesis. Curr Opin Hematol 17, 213-218
54. Wijelath ES et al. (2002). Novel vascular endothelial growth factor binding domains of fibronectin enhance vascular endothelial growth factor biological activity. Circ Res 91, 25-31 (Pubitemid 34778938)
55. Wijelath ES, Rahman S, Namekata M, Murray J, Nishimura T, Mostafavi-Pour Z, Patel Y, Suda Y, Humphries MJ, Sobel M (2006). Heparin-II domain of fibronectin is a vascular endothelial growth factor-binding domain: enhancement of VEGF biological activity by a singular growth factor/matrix protein synergism. Circ Res 99, 853-860 (Pubitemid 44556384)
56. Woolard J, Bevan HS, Harper SJ, Bates DO (2009). Molecular diversity of VEGF-A as a regulator of its biological activity. Microcirculation 16, 572-592
57. Yeo TK, Senger DR, Dvorak HF, Freter L, Yeo KT (1991). Glycosylation is essential for efficient secretion but not for permeability-enhancing activity of vascular permeability factor (vascular endothelial growth factor). Biochem Biophys Res Commun 179, 1568-1575