Activation of Vascular Endothelial Growth Factor Receptor-1 Sustains Angiogenesis and Bcl-2 Expression Via the Phosphatidylinositol 3-Kinase Pathway in Endothelial Cells

Diabetes

Volumn 52, Issue 12, 2003, Pages 2959-2968

  Cai, Jun ^a   Ahmad, Shakil ^b   Jiang, Wen G ^a   Huang, Jianhua ^c   Kontos, Christopher D ^c   Boulton, Mike ^a   Ahmed, Asif ^b  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; DIMER; GROWTH FACTOR; LIGAND; LIPOCORTIN 5; MUTANT PROTEIN; PHOSPHATASE; PHOSPHATIDYLINOSITOL 3 KINASE; PLACENTA PROTEIN; PROPIDIUM IODIDE; PROTEIN BCL 2; PROTEIN KINASE B; VASCULOTROPIN RECEPTOR 1;

ADENOVIRUS; ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL GROWTH; CHROMOSOME 10; CONTROLLED STUDY; ENDOTHELIUM CELL; FLOW CYTOMETRY; GEL; GENE OVEREXPRESSION; MICROVASCULATURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SEQUENCE HOMOLOGY; SERUM; SIGNAL TRANSDUCTION; STAINING; STATISTICAL SIGNIFICANCE; UPREGULATION; WILD TYPE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; APOPTOSIS; CATTLE; CELL SURVIVAL; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; HUMANS; MICROCIRCULATION; NEOVASCULARIZATION, PATHOLOGIC; PREGNANCY PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RETINAL VESSELS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 0344844410     PISSN: 00121797     EISSN: None     Source Type: Journal    
DOI: 10.2337/diabetes.52.12.2959     Document Type: Article

References (48)

1. Miller JW, Adamis AP, Aiello LP: Vascular endothelial growth factor in ocular neovascularization and proliferative diabetic retinopathy. Diabete Metab Rev 13:37-50, 1997
2. Aiello LP, Avery RL, Arrigg PG, Keyt BA, Jampel HD, Shah ST, Pasquale LR, Thieme H, Iwamoto MA, Park JE, et al: Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med 331:1480-1487, 1994
3. Tilton RG, Kawamura T, Chang KC, Ido Y, Bjercke RJ, Stephan CC, Brock TA, Williamson JR: Vascular dysfunction induced by elevated glucose levels in rats is mediated by vascular endothelial growth factor. J Clin Invest 99:2192-2202, 1997
4. Leinonen H, Matikainen E, Juntunen J: Permeability and morphology of skeletal muscle capillaries in type 1 (insulin-dependent) diabetes mellitus. Diabetologia 22:158-162, 1982
5. Maglione D, Guerriero V, Viglietto G, Delli-Bovi P, Persico MG: Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc Natl Acad Sci U S A 88:9267-9271, 1991
6. Maglione D, Guerriero V, Viglietto G, Ferraro MG, Aprelikova O, Alitalo K, Del Vecchio S, Lei KJ, Chou JY, Persico MG: Two alternative mRNAs coding for the angiogenic factor, placenta growth factor (PlGF), are transcribed from a single gene of chromosome 14. Oncogene 8:925-931, 1993
7. Cao Y, Ji WR, Qi P, Rosin A: Placenta growth factor: identification and characterization of a novel isoform generated by RNA alternative splicing. Biochem Biophys Res Commun 235:493-498, 1997
8. Cao Y, Chen H, Zhou L, Chiang MK, Anand-Apte B, Weatherbee JA, Wang Y, Fang F, Flanagan JG, Tsang ML: Heterodimers of placenta growth factor/vascular endothelial growth factor: endothelial activity, tumor cell expression, and high affinity binding to Flk-1/KDR. J Biol Chem 271:3154-3162, 1996
9. Khaliq A, Foreman D, Ahmed A, Weich H, Gregor Z, McLeod D, Boulton M: Increased expression of placenta growth factor in proliferative diabetic retinopathy. Lab Invest 78:109-116, 1998
10. Khaliq A, Dunk C, Jiang J, Shams M, Li XF, Acevedo C, Weich H, Whittle M, Ahmed A: Hypoxia down-regulates placenta growth factor, whereas fetal growth restriction up-regulates placenta growth factor expression: molecular evidence for "placental hyperoxia" in intrauterine growth restriction. Lab Invest 79:151-170, 1999
11. Yamashita H, Eguchi S, Watanabe K, Takeuchi S, Yamashita T, Miura M: Expression of placenta growth factor (PlGF) in ischaemic retinal diseases. Eye 13:372-374, 1999
12. Carmeliet P, Moons L, Luttun A, Vincenti V, Compernolle V, De Mol M, Wu Y, Bono F, Devy L, Beck H, Scholz D, Acker T, DiPalma T, Dewerchin M, Noel A, Stalmans I, Barra A, Blacher S, Vandendriessche T, Ponten A, Eriksson U, Plate KH, Foidart JM, Schaper W, Charnock-Jones DS, Hicklin DJ, Herbert JM, Collen D, Persico MG: Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med 7:575-583, 2001
13. Luttun A, Tjwa M, Moons L, Wu Y, Angelillo-Scherrer A, Liao F, Nagy JA, Hooper A, Priller J, De Klerck B, Compernolle V, Daci E, Bohlen P, Dewerchin M, Herbert JM, Fava R, Matthys P, Carmeliet G, Collen D, Dvorak HF, Hicklin DJ, Carmeliet P: Revascularization of ischemic tissues by PlGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1. Nat Med 8:831-840, 2002
14. Park JE, Chen HH, Winer J, Houck KA, Ferrara N: Placenta growth factor: potentiation of vascular endothelial growth factor bioactivity, in vitro and in vivo, and high affinity binding to Flt-1 but not to Flk-1/KDR. J Biol Chem 269:25646-25654, 1994
15. Bussolati B, Dunk C, Grohman M, Kontos CD, Mason J, Ahmed A: Vascular endothelial growth factor receptor-1 modulates vascular endothelial growth factor-mediated angiogenesis via nitric oxide. Am J Pathol 159: 993-1008, 2001.
16. Zeng H, Dvorak HF, Mukhopadhyay D: Vascular permeability factor (VPF)/vascular endothelial growth factor (VEGF) receptor-1 down-modulates VPF/VEGF receptor-2-mediated endothelial cell proliferation, but not migration, through phosphatidylinositol 3-kinase-dependent pathways. J Biol Chem 276:26969-26979, 2001
17. Carmeliet P, Lampugnani MG, Moons L, Breviario F, Compernolle V, Bono F, Balconi G, Spagnuolo R, Oostuyse B, Dewerchin M, Zanetti A, Angellilo A, Mattot V, Nuyens D, Lutgens E, Clotman F, de Ruiter MC, Gittenberger-de Groot A, Poelmann R, Lupu F, Herbert JM, Collen D, Dejana E: Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98:147-157, 1999
18. Adini A, Kornaga T, Firoozbakht F, Benjamin LE: Placental growth factor is a survival factor for tumor endothelial cells and macrophages. Cancer Res 62:2749-2752, 2002
19. Cal J, Jiang WG, Mansel RE: Inhibition of the expression of VE-cadherin/catenin complex by gamma linolenic acid in human vascular endothelial cells, and its impact on angiogenesis. Biochem Biophys Res Commun 258:113-118, 1999
20. Clauss M, Weich H, Breier G, Knies U, Rockl W, Waltenberger J, Risau W: The vascular endothelial growth factor receptor Flt-1 mediates biological activities: implications for a functional role of placenta growth factor in monocyte activation and chemotaxis. J Biol Chem 271:17629-17634, 1996
21. Huang J, Kontos CD: PTEN modulates vascular endothelial growth factor-mediated signaling and angiogenic effects. J Biol Chem 277:10760-10766, 2002
22. Gille H, Kowalski J, Yu L, Chen H, Pisabarro MT, Davis-Smyth T, Ferrara N: A repressor sequence in the juxtamembrane domain of Flt-1 (VEGFR-1) constitutively inhibits vascular endothelial growth factor-dependent phosphatidylinositol 3′-kinase activation and endothelial cell migration. Embo J 19:4064-4073, 2000
23. Narayan P, Mentzer RM Jr, Lasley RD: Annexin V staining during reperfusion detects cardiomyocytes with unique properties. Am J Physiol Heart Circ Physiol 281:H1931-H1937, 2001
24. Nor JE, Christensen J, Mooney DJ, Polverini PJ: Vascular endothelial growth factor (VEGF)-mediated angiogenesis is associated with enhanced endothelial cell survival and induction of Bcl-2 expression. Am J Pathol 154:375-384, 1999
25. Birkenhager R, Schneppe B, Roeld W, Wilting J, Weich HA, McCarthy JE: Synthesis and physiological activity of heterodimers comprising different splice forms of vascular endothelial growth factor and placenta growth factor. Biochem J 316:703-707, 1996
26. Takahashi A, Sasaki H, Kim SJ, Kakizoe, T, Miyao N, Sugimura, T, Terada M, Tsukamoto T: Identification of receptor genes in renal cell carcinoma associated with angiogenesis by differential hybridization technique. Biochem Biophys Res Commun 257:855-859, 1999
27. Shi J, Miller RA: Differential tyrosine-specific protein phosphorylation in mouse T lymphocyte subsets: effect of age. J Immunol 151:730-739, 1993
28. Seffert RA, Hart CE, Phillips PE, Forstrom JW, Ross R, Murray MJ, Bowen-Pope DF: Two different subunits associate to create isoform-specific platelet-derived growth factor receptors. J Biol Chem 264:8771-8778, 1989.
29. Sato Y, Karmo S, Oda N, Abe M, Ito M, Shitara K, Shibuya M: Properties of two VEGF receptors, Flt-1 and KDR, in signal transduction (Review). Ann N YAcad Sci 902:201-207, 2000
30. Heidaran MA, Pierce JH, Yu JC, Lombardi D, Artrip JE, Fleming TP, Thomason A, Aaronson SA: Role of alpha beta receptor heterodimer formation in beta platelet-derived growth factor (PDGF) receptor activation by PDGF-AB. J Biol Chem 266:20232-20237, 1991
31. Reed JC: Bcl-2 family proteins. Oncogene 17:3225-3236, 1998
32. Chao DT, Korsmeyer SJ: BCL-2 family regulators of cell death. Annu Rev Immunol 16:395-419, 1998
33. Xiang J, Chao DT, Korsmeyer SJ: BAX-induced cell death may not require interleukin 1 beta-converting enzyme-like proteases. Proc Natl Acad Sci U S A 93:14559-14563, 1996
34. Inohara N, Ekhterae D, Garcia I, Carrio R, Merino J, Merry A, Chen S, Nunez G: Mtd, a novel Bcl-2 family member activates apoptosis in the absence of heterodimerization with Bcl-2 and Bcl-XL. J Biol Chem 273:8705-8710, 1998
35. Stambolic V, Suzuki A, de la Pompa JL, Brothers GM, Mirtsos C, Sasaki T, Ruland J, Penninger JM, Siderovski DP, Mak TW: Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell 95:29-39, 1998
36. Li J, Simpson L, Takahashi M, Miliaresis C, Myers MP, Tonks N, Parsons R: The PTEN/MMAC1 tumor suppressor induces cell death that is rescued by the AKT/protein kinase B oncogene. Cancer Res 58:5667-5672, 1998
37. Kurose K, Zhou XP, Araki T, Cannistra SA, Maher ER, Eng C: Frequent loss of PTEN expression is linked to elevated phosphorylated Akt levels, but not associated with p27 and cyclin D1 expression, in primary epithelial ovarian carcinomas. Am J Pathol 158:2097-2106, 2001
38. Di Cristofano A, Pandolfi PP: The multiple roles of PTEN in tumor suppression. Cell 100:387-390, 2000
39. Bonni A, Brunet A, West AE, Datta SR, Takasu MA, Greenberg ME: Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286:1358-1362, 1999
40. Du K, Montminy M: CREB is a regulatory target for the protein kinase Akt/PKB. J Biol Chem 273:32377-32379, 1998
41. Pugazhenthi S, Nesterova A, Sable C, Heidenreich KA, Boxer LM, Heasley LE, Reusch JE: Akt/protein kinase B up-regulates Bcl-2 expression through cAMP-response element-binding protein. J Biol Chem 275:10761-10766, 2000
42. Pugazhenthi S, Miller E, Sable C, Young P, Heidenreich KA, Boxer LM, Reusch JE: Insulin-like growth factor-I induces bcl-2 promoter through the transcription factor cAMP-response element-binding protein. J Biol Chem 274:27529-27535, 1999
43. Riccio A, Ahn S, Davenport CM, Blendy JA, Ginty DD: Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons. Science 286:2358-2361, 1999
44. Odorisio T, Schietroma C, Zaccaria ML, Cianfarani F, Tiveron C, Tatangelo L, Failla CM, Zambruno G: Mice overexpressing placenta growth factor exhibit increased vascularization and vessel permeability. J Cell Sci 115:2559-2567, 2002
45. Nomura M, Yamagishi S, Harada S, Hayashi Y, Yamashima T, Yamashita J, Yamamoto H: Possible participation of autocrine and paracrine vascular endothelial growth factors in hypoxia-induced proliferation of endothelial cells and pericytes. J Biol Chem 270:28316-28324, 1995
46. Boulton M, Foreman D, Williams G, McLeod D: VEGF localisation in diabetic retinopathy. Br J Ophthalmol 82:561-568, 1998
47. Alon T, Hemo I, Itin A, Pe'er J, Stone J, Keshet E: Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat Med 1:1024-1028, 1995
48. Spyridopoulos I, Brogi E, Kearney M, Sullivan AB, Cetrulo C, Isner JM, Losordo DW: Vascular endothelial growth factor inhibits endothelial cell apoptosis induced by tumor necrosis factor-alpha: balance between growth and death signals. J Mol Cell Cardiol 29:1321-1330, 1997