Adenosine mediates hypoxic induction of vascular endothelial growth factor in retinal pericytes and endothelial cells

Investigative Ophthalmology and Visual Science

Volumn 37, Issue 11, 1996, Pages 2165-2176

  Takagi, Hitoshi ^a   King, George L ^a,b,c   Robinson, Gregory S ^d   Ferrara, Napoleone ^e   Aiello, Lloyd Paul ^a,b  

^a JOSLIN DIABETES CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d HYBRIDON INC   (United States)

^e GENENTECH INC   (United States)

Author keywords

adenosine; adenosine receptor; cyclic adenosine monophosphate (cAMP) dependent protein kinase A; hypoxia; ischemia; neovascularization; vascular permeability factor (VPF)

Indexed keywords

2 [4 (2 CARBOXYETHYL)PHENETHYLAMINO]ADENOSINE 5' (N ETHYLCARBOXAMIDE); 6 N [2 (3,5 DIMETHOXYPHENYL) 2 (2 METHYLPHENYL)ETHYL]ADENOSINE; 6 N CYCLOPENTYLADENOSINE; 8 CYCLOPENTYL 1,3 DIPROPYLXANTHINE; ADENOSINE; ADENOSINE 5' (N ETHYLCARBOXAMIDE); ADENOSINE A1 RECEPTOR AGONIST; ADENOSINE A2 RECEPTOR AGONIST; ADENOSINE DEAMINASE; ADENOSINE RECEPTOR; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; VASCULOTROPIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; COW; ENDOTHELIUM CELL; GENE EXPRESSION; HYPOXIA; IMMUNOBLOTTING; NONHUMAN; NORTHERN BLOTTING; PERICYTE; PRIORITY JOURNAL; PROTEIN SECRETION; RADIOIMMUNOASSAY; RETINA BLOOD VESSEL; RETINA CAPILLARY; RETINA CELL;

ADENOSINE; ANIMALS; ANOXIA; BLOTTING, NORTHERN; BLOTTING, WESTERN; CATTLE; CELL HYPOXIA; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL GROWTH FACTORS; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; LYMPHOKINES; RECEPTORS, PURINERGIC P1; RETINAL VESSELS; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 0029840035     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (51)

1. Berse B, Brown LF, Van dWL, Dvorak HF, Senger DR. Vascular permeability factor (vascular endothelial growth factor) gene is expressed differentially in normal tissues, macrophages, and tumors. Mol Biol Cell. 1992;3:211-220.
2. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 1989;246:1306-1309.
3. Senger DR, Perruzzi CA, Feder J, Dvorak HF. A highly conserved vascular permeability factor secreted by a variety of human and rodent tumor cell lines. Cancer Res. 1986;46:5629-5632.
4. Aiello LP, Northrup JM, Keyt BA, Takagi H, Iwamoto MA. Hypoxic regulation of vascular endothelial growth factor in retinal cells. Arch Ophthalmol. 1995; 113:1538-1544.
5. Pierce EA, Avery RL, Foley ED, Aiello LP, Smith LEH. Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc Natl Acad Sci USA. 1995; 92:905-909.
6. Aiello LP, Avery RL, Arrigg PG, et al. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders [see comments]. N Engl J Med. 1994;331:1480-1487.
7. Shweiki D, Itin A, Soffer D, Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature. 1992;359:843-845.
8. Ferrara N, Houck KA, Jakeman LB, Leung DW. Molecular and biological properties of the vascular endothelial growth factor family of proteins. Endocr Rev. 1992;13:18-32.
9. Thieme H, Aiello LP, Takagi H, Ferrara N, King GL. Comparative analysis of vascular endothelial growth factor receptors on retinal and aortic vascular endothelial cells. Diabetes. 199544:98-103.
10. Millauer B, Wizigmann VS, Schnurch H, Martinez R, Moller NP, Risau W, Ullrich A. High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell. 1993;72:835-846.
11. Adamis AP, Miller JW, Bernal MT, et al. Increased vascular endothelial growth factor levels in the vitreous of eyes with proliferative diabetic retinopathy. Am J Ophthalmol. 1994;118:445-450.
12. Minchenko A, Salceda S, Bauer T, Caro J. Hypoxia regulatory elements of the human vascular endothelial growth factor gene. Cell Mol Biol Res. 1994; 40:35-39.
13. Levy AP, Levy NS, Wegner S, Goldberg MA. Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J Biol Chem. 1995; 270:13333-13340.
14. Ikeda E, Achen MG, Breier G, Risau W. Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells. J Biol Chem. 1995;270:19761-19766.
15. Stein I, Neeman M. Stabilization of vascular endothelial growth factor mRNA by hypoxia and hypoglycemia and coregulation with other ischemia-induced genes. Mol Cell Biol. 1995;15:5363-5368.
16. Claffey KP, Wilkison WO, Spiegelman BM. Vascular endothelial growth factor: Regulation by cell differentiation and activated second messenger pathways. J Biol Chem. 1992;267:16317-16322.
17. Levy AP, Levy NS, Loscalzo J, et al. Regulation of vascular endothelial growth factor in cardiac myocytes. Circ Res. 1995;76:758-766.
18. Mukhopadhyay D, Tsiokas L, Zhou XM, Foster D, Brugge JS, Sukhatme W. Hypoxic induction of human vascular endothelial growth factor expression through c-Src activation. Nature. 1995;375:577-581.
19. Bontemps F, Vincent MF, Van den Berghe G. Mechanisms of elevation of adenosine levels in anoxic hepatocytes. J Biochem. 1993;290:671-677.
20. Rathbone MP, Middlemiss PJ, Kim JK, et al. Adenosine and its nucleotides stimulate proliferation of chick astrocytes and human astrocytoma cells. Nucleosci Res. 1992;13:1-17.
21. Ethier MF, Chander V, Dobson JG. Adenosine stimulates proliferation of human endothelial cells in culture. Am J Physiol. 1993;265:H131-H138.
22. Beru N, McDonald J, Lacombe C, Goldwasser E. Expression of the erythropoietin gene. Mol Cell Biol. 1986;6:2571-2575.
23. Bondurant MC, Koury MJ. Anemia induces accumulation of erythropoietin mRNA in the kidney and liver. Mol Cell Biol. 1986;6:2731-2733.
24. Goldberg MA, Schneider TJ. Similarities between the oxygen-sensing mechanisms regulating the expression of vascular endothelial growth factor and erythropoietin. J Biol Chem. 1994;269:4355-4359.
25. Nakashima J, Ohigashi T, Brookins JW, Beckman BS, Agrawal KC, Fisher JW. Effects of 5′-N-ethylcarboxamideadenosine (NEGA) on erythropoietin production. Kidney Int. 1993;44:734-740.
26. Tucker AL, Linden J. Cloned receptors and cardiovascular responses to adenosine. Cardiovasc Res. 1993; 27:62-67.
27. Collis MG, Hourani SMO. Adenosine receptor subtypes. Trends Pharmacol Sci Rev. 1993;14:360-366.
28. Linden J. Structure and function of A1 adenosine receptors. FASEB J. 1991;5:2668-2676.
29. Libert F, Parmentier M, Lefort A. Selective amplification and cloning of four new members of the G-protein coupled receptor family. Science. 1989;244:569-572.
30. Hashimoto E, Kage K, Ogita T, Nakaoka T, Matsuoka R, Kira Y. Adenosine as an endogenous mediator of hypoxia for induction of vascular endothelial growth factor mRNA in U-937 cells. Biochem Biophys Res Commun. 1994;204:318-324.
31. Fischer S, Sharma HS, Karliczek GF, Schaper W. Expression of vascular permeability factor/vascular endothelial growth factor in pig cerebral microvascular endothelial cells and its upregulation by adenosine. Brain Res Mol Brain Res. 1995;28:141-148.
32. Nayak RC, Berman AB, George KL, Eisenbarth GS, King GL. A monoclonal antibody (3G5)-defined ganglioside antigen is expressed on the cell surface of microvascular pericytes. J Exp Med. 1988;167:1003-1015.
33. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-PhOH-chloroform extraction. Anal Biochem. 1987;162:156-159.
34. Masiakowski P, Breathnach R, Bloch J, Gannon F, Krust A, Chambon P. Cloning of cDNA sequences of hormone-regulated genes from the MCF-7 human breast cancer cell lines. Nucl Acids Res. 1982;10:7895-7903.
35. Sanders SP, Zweier JL, Kuppusamy SL, et al. Hyperoxic sheep pulmonary microvascular endothelial cells generate free radicals via mitochondrial electron transport. J Clin Invest. 1993;91:46-52.
36. Bruns RF, Lu GH, Pugsley TA. Characterization of the A2 adenosine receptor labeled by [3H]NECA in rat striatal membranes. Mol Pharmacol. 1986;29:331-346.
37. Research Biochemicals International 1995 Handbook. Available from RBI, Strathmore Road, Natick, MA 01760-2447.
38. Adamis AP, Shima DT, Yeo KT, et al. Synthesis and secretion of vascular permeability factor/vascular endothelial growth factor by human retinal pigment epithelial cells. Biochem Biophys Res Commun. 1993; 193:631-638.
39. Miller JW, Adamis AP, Shima DT, et al. Vascular endothelial growth factor/vascular permeability factor is temporally and spatially correlated with ocular angiogenesis in a primate model. Am J Pathol. 1994; 145:574-584.
40. Aiello LP, Pierce EA, Foley ED, et al. Inhibition of vascular endothelial growth factor suppresses retinal neovascularization in vivo. Proc Natl Acad Sci USA. 1995;92:10457-10461.
41. Adamis AP, Shima DT, Tolentino MJ, et al. Inhibition of vascular endothelial growth factor prevents retinal ischemia-associated iris neovascularization in a non-human primate. Arch Ophthalmol. 1996;114:66-71.
42. Bridges AJ, Bruns RF, Ortwine DF, Priebe SR, Szotek DL, Trivedi BK. N6-[2-(3,5-dimethoxyphenyl)-2-(2-methylphenyl)ethyl]adenosine and its uronamide derivatives: Novel adenosine agonists with both high affinity and high selectivity for the adenosine A2 receptor. J Med Chem. 1988;31:1282-1285.
43. Jarvis MF, Schulz R, Hutchison AJ, Do UH, Sills MA, Williams M. [3H]CGS 21680, a selective A2 adenosine receptor agonist directly labels A2 receptors in rat brain. J Pharmacol Exp Ther. 1989;251:888-893.
44. Kroll K, Schrader J. Myocardial adenosine stimulates release of cyclic adenosine monophosphate from capillary endothelial cells in guinea pig heart. Pflugers Arch. 1993;423:330-337.
45. Ogawa S, Koga S, Kuwabara K, et al. Hypoxia-induced increased permeability of endothelial monolayers occurs through lowering of cellular cAMP levels. Am J Physiol. 1992;262:C546-C554.
46. Tischer E, Mitchell R, Hartman T, et al. The human gene for vascular endothelial growth factor: Multiple protein forms are encoded through alternative exon splicing. J Biol Chem. 1991;266:11947-11954.
47. Wieloch T, Cardell M, Bingren H, Zivin J, Saitoh T. Changes in the activity of protein kinase C and the differential subcellular redistribution of its isozymes in the rat striatum during and following transient forebrain ischemia. J Neurochem. 1991;56:1227-1235.
48. Webster KA, Discher DJ, Bishopric NH. Induction and nuclear accumulation of fos and jun proto-oncogenes in hypoxic cardiac myocytes. J Biol Chem. 1993; 268:16852-16858.
49. Simorre PV, Guerrin M, Chollet P, et al. Vasculotropin-VEGF stimulates retinal capillary endothelial cells through an autocrine pathway. Invest Ophthalmol Vis Sci. 1994;35:3393-3400.
50. Jacobson KA, Nikodijevic C, Padgett WL, Gallo-Rodriguez C, Maillard M. 8-(3-chlorostyryl) caffeine (CSC) is a selective A2-adenosine antagonist in vitro and in vivo. FEBS Lett. 1993;323:141-144.
51. Houck KA, Leung DW, Rowland AM, Winer J, Ferrara N. Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J Biol Chem. 1992;267:26031-26037.