Vascular dysfunction induced by elevated glucose levels in rats is mediated by vascular endothelial growth factor

Journal of Clinical Investigation

Volumn 99, Issue 9, 1997, Pages 2192-2202

  Tilton, Ronald G ^a   Kawamura, Takahiko ^c   Chang, Katherine C ^b   Ido, Yasuo ^b   Bjercke, Robert J ^a   Stephan, Clifford C ^a   Brock, Tommy A ^a   Williamson, Joseph R ^b  

^a TEXAS BIOTECHNOLOGY CORPORATION   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CHUBU ROSAI HOSPITAL   (Japan)

Author keywords

albumin permeation; blood flow; nitric oxide; polyol pathway; vascular endothelial growth factor

Indexed keywords

ALBUMIN; AMINOGUANIDINE; CALCIMYCIN; GLUCOSE; N(G) METHYLARGININE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; SUPEROXIDE; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD FLOW; BLOOD VESSEL PERMEABILITY; CONTROLLED STUDY; DIABETES MELLITUS; FEMALE; HYPERGLYCEMIA; HYPOXIA; MALE; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; VASCULAR DISEASE;

EID: 0031000258     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119392     Document Type: Article

References (58)

1. Greene, D.A., S. Lattimer, J. Ulbrecht, and P. Carroll. 1985. Glucose-induced alterations in nerve metabolism: current perspective on the pathogenesis of diabetic neuropathy and future directions for research and therapy. Diabetes Care. 8:290-299.
2. Winegrad, A.E. 1987. Does a common mechanism induce the diverse complications of diabetes? Diabetes. 36:396-406.
3. Kinoshita, J.H., and C. Nishimura. 1988. The involvement of aldose reductase in diabetic complications. Diabetes Metab. Rev. 4:323-337.
4. Pugliese, G., R.G. Tilton, and J.R. Williamson. 1991. Glucose-induced metabolic imbalances in the pathogenesis of diabetic vascular disease. Diabetes Metab. Rev. 7:35-59.
5. Ruderman, N.B., J.R. Williamson, and M. Brownlee. 1992. Glucose and diabetic vascular disease. FASEB J. 6:2905-2914.
6. Tilton, R.G., K. Chang, G. Pugliese, D.M. Eades, M.A. Province, W.R. Sherman, C. Kilo, and J.R. Williamson. 1989. Prevention of hemodynamic and vascular albumin filtration changes in diabetic rats by aldose reductase inhibitors. Diabetes. 38:1258-1270.
7. Pugliese, G., R.G. Tilton, A. Speedy, K. Chang, M.A. Province, C. Kilo, and J.R. Williamson. 1990. Vascular filtration function in galactose-fed versus diabetic rats: the role of polyol pathway activity. Metab. Clin. Exp. 39:690-697.
8. Tilton, R.G., K. Chang, J.R. Nyengaard, M. Van den Enden, Y. Ido, and J.R. Williamson. 1995. Inhibition of sorbitol dehydrogenase: effects on vascular and neural dysfunction in streptozocin-induced diabetic rats. Diabetes. 44:234-242.
9. Williamson, J.R., E. Ostrow, D.M. Eades, K. Chang, W. Allison, C. Kilo, and W.R. Sherman. 1990. Glucose-induced microvascular functional changes in nondiabetic rats are stereospecific and are prevented by an aldose reductase inhibitor. J. Clin. Invest. 85:1167-1172.
10. Williamson, J.R., K. Chang, E. Ostrow, W. Allison, J. Harlow, and C. Kilo. 1989. Sorbitol-induced increases in vascular albumin clearance are prevented by pyruvate but not myo-inositol. Diabetes. 38:94a. (Abstr.)
11. Wolf, B.A., J.R. Williamson, R.A. Easom, K. Chang, W.R. Sherman, and J. Turk. 1990. Diacylglycerol accumulation and microvascular abnormalities induced by elevated glucose levels. J. Clin. Invest. 87:31-38.
12. Williamson, J.R., K. Chang, M. Frangos, K.S. Hasan, Y. Ido, T. Kawamura, J.R. Nyengaard, M. Van den Enden, C. Kilo and R.G. Tilton. 1993. Hyperglycemic pseudohypoxia and diabetic complications. Diabetes. 42:801-813.
13. Bunger, R., R.T. Mallet, and D.A. Hartman. 1989. Pyruvate-enhanced phosphorylation potential and inotropism in normoxic and postischemic isolated working heart: near-complete prevention of reperfusion contractile failure. Eur. J. Biochem. 180:221-233.
14. Cavallini, L., M. Valente, and M.P. Rigobello. 1990. The protective action of pyruvate on recovery of ischemic rat heart: comparison with other oxidizable substrates. J. Mol. Cell. Cardiol. 22:143-154.
15. Ferrara, N. 1993. Vascular endothelial growth factor. Trends Cardiovasc. Med. 3:244-250.
16. Dvorak, H.F., L.F. Brown, M. Detmar, and A.M. Dvorak. 1995. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am. J. Pathol. 146:1029-1039.
17. Ku, D.D., J.K. Zaleski, S. Liu, and T.A. Brock. 1993. Vascular endothelial growth factor induces EDRF-dependent relaxation in coronary arteries. Am. J. Physiol. 265:H586-H592.
18. Minchenko, A., T. Bauer, S. Salceda, and J. Caro. 1994. Hypoxic stimulation of vascular endothelial growth factor expression in vitro and in vivo. Lab. Invest. 71:374-379.
19. Namiki, A., E. Brogi, M. Kearney, E.A. Kim, T. Wu, T. Couffinhal, L. Varticovski, and J.M. Isner. 1995. Hypoxia induces vascular endothelial growth factor in cultured human endothelial cells. J. Biol. Chem. 270:31189-31195.
20. Aiello, L.P., J.M. Northrup, B.A. Keyt, H. Takagi, and M.A. Iwamoto. 1995. Hypoxic regulation of vascular endothelial growth factor in retinal cells. Arch. Ophthalmol. 113:1538-1544.
21. Fiebich, B.L., B. Jäger, C. Schöllmann, K. Weindel, J. Wilting, G. Kochs, D. Marmé, H. Hug, and H.A. Weich. 1993. Synthesis and assembly of functionally active human vascular endothelial growth factor homodimers in insect cells. Eur. J. Biochem. 211:19-26.
22. Bjercke, R.J., G. Cook, N. Rychlik, H.B. Gjika, H.V. Vunakis, and J.J. Langone. 1986. Stereospecific monoclonal antibodies to nicotine and cotinine and their use in enzyme-linked immunosorbent assays. J. Immunol. Methods. 90:203-213.
23. Koehler, G., and C. Milstein. 1976. Derivation of specific antibody-producing tissue culture and tumor lines by cell fusion. Eur. J. Immunol. 6:511-519.
24. Brock, T.A., and E. L. Capasso. 1988. Thrombin and histamine activate phospholipase C in human endothelial cells via a phorbol ester-sensitive pathway. J. Cell. Physiol. 136:54-62.
25. 2+ and von Willebrand factor release in human endothelial cells. Am. J. Pathol. 138:213-221.
26. Lundberg, C., and B. Gerdin. 1984. The inflammatory reaction in an experimental model of open wounds in the rat. The effect of arachidonic acid metabolites. Eur. J. Pharmacol. 97:229-238.
27. Tilton, R.G., K. Chang, K.S. Hasan, J.M. Petrash, T.P. Misko, W.M. Moore, M.G. Currie, J.A. Corbett, M.L. McDaniel, and J.R. Williamson. 1993. Prevention of diabetic vascular dysfunction by guanidines: inhibition of nitric oxide synthase versus advanced glycation end product formation. Diabetes. 42:221-232.
28. Lowry. O.H., and J.V. Passoneau. 1972. A Flexible System of Enzymatic Analysis. Academic Press. Inc., Orlando, FL. 174.
29. Passonneau, J.V., and O.H. Lowry. 1993. Enzymatic Analysis. A Practical Guide. The Humana Press, Totowa, NJ.
30. Chi, M.M.-Y., M.E. Pusateri, J.G. Carter, B.J. Norris, D.B. McDougal, Jr., and O.H. Lowry. 1987. Enzymatic assays for 2-deoxyglucose and 2-deoxyglucose 6-phosphate. Anal. Biochem. 161:508-513.
31. Williamson, D.H., P. Lund, and H.A. Krebs. 1967. The redox state of free nicotinamide-adenine dinucleotide in the cytoplasm and mitochondria of rat liver. Biochem. J. 103:514-527.
32. Lehman, E.L. 1975. Nonparametrics: Statistical Methods Based on Ranks. Holden-Day, San Francisco.
33. Anderson, T.W. 1958. An Introduction to Multivariate Statistical Analysis. John Wiley & Sons, Inc., New York.
34. Blom, G. 1958. Statistical Estimates and Transformed Beta Variables. John Wiley & Sons. Inc., New York.
35. Phillips, H.S., M. Armanini, D. Stavrou, N. Ferrara, and M. Westphal. 1993. Intense focal expression of vascular endothelial growth factor mRNA in human intracranial neoplasms: association with regions of necrosis. Int. J. Oncol. 2:913-919.
36. Shweiki, D., A. Itin, D. Soffer, and E. Keshet. 1992. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature (Lond.). 359:843-845.
37. Ladoux, A., and C. Frelin. 1993. Hypoxia is a strong inducer of vascular endothelial growth factor mRNA expression in the heart. Biochem. Biophys. Res. Commun. 195:1005-1010.
38. Plate, K.H., G. Breier, H.A. Weich, and W. Risau. 1992. Vascular endothelial growth factor is a potential tumour angiogenesis factor in vivo. Nature (Lond.). 359:845-847.
39. Koos, R.D., and C.E. Olson. 1991. Hypoxia stimulates expression of the gene for vascular endothelial growth factor (VEGF), a putative angiogenic factor, by granulosa cells of the ovarian follicle, a site of angiogenesis. J. Cell biol. 115:421a. (Abstr.)
40. Goldberg, M., and T. Schneider. 1994. Similarities between the oxygen sensing mechanisms regulating the expression of vascular endothelial growth factor and erythropoietin. J. Biol. Chem. 269:4355-4359.
41. Tilton, R.G., L.M. Baier, J.E. Harlow, S.R. Smith, E. Ostrow, and J.R. Williamson. 1992. Diabetes-induced glomerular dysfunction: links to a more reduced cytosolic redox state. Kidney Int. 41:778-788.
42. Van den Enden, M.K., J.R. Nyengaard, E. Ostrow, J.H. Burgan, and J.R. Williamson. 1995. Elevated glucose levels increase retinal glycolysis and sorbitol pathway metabolism. Invest. Ophthalmol. & Visual Sci. 36:1675-1685.
43. Obrosova, I., J. Marvel, A.M. Faller, and J.R. Williamson. 1995. Reductive stress is a very early metabolic imbalance in sciatic nerve in diabetic and galactose-fed rats. Diabetologia. 38:8a. (Abstr.)
44. Kuroki, M., E.E. Voest, S. Amano, L.V. Beerepoot, S. Takashima, M. Tolentino, R.Y. Kim, R.M. Rohan, K.A. Colby, K.-T. Yeo, and A.P. Adamis. 1996. Reactive oxygen intermediates increase vascular endothelial growth factor expression in vitro and in vivo. J. Clin. Invest. 98:1167-1175.
45. + )-ATPase in the slowing of nerve conduction in the streptozotocin diabetic rat. J. Clin. Invest. 94:853-859.
46. Lou, M.F., J.R. Dickerson, Jr., R. Garadi, and B.M. York, Jr. 1988. Glutathione depletion in the lens of galactosemic and diabetic rats. Exp. Eye Res. 46:517-530.
47. Morbidelli, L., C.-H. Chang, J.G. Douglas, H.J. Granger, F. Ledda, and M. Ziehe. 1996. Nitric oxide mediates mitogenic effect of VEGF on coronary venular endothelium. Am. J. Physiol. 270:H411-H415.
48. Leibovich, S.J., P.J. Polverini, T.W. Fong, L.A. Harlow, and A.E. Koch. 1994. Production of angiogenic activity by human monocytes requires an L-arginine/nitric oxide-synthase-dependent effector mechanism. Proc. Natl. Acad. Sci. USA. 91:4190-4194.
49. Ziehe, M., L. Morbidelli, E. Masini, S. Amerini, H.J. Granger, C.A. Maggi, P. Geppetti, and F. Ledda. 1994. Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J. Clin. Invest. 94:2036-2044.
50. Yang, R., G.R. Thomas, S. Bunting, A. Ko, N. Ferrara, B. Keyt, J. Ross, and H. Jin. 1996. Effects of vascular endothelial growth factor on hemodynamics and cardiac performance. J. Cardiovasc. Pharmacol. 27:838-844.
51. Hasan, K.S., K. Chang, W. Allison, A. Faller, J.V. Santiago, R.G. Tilton, and J.R. Williamson. 1993. Glucose-induced increases in regional blood flow are prevented by aminoguanidine and L-NMMA, inhibitors of nitric oxide synthase. FASEB J. 7:105a. (Abstr.)
52. Sone, S., Y. Kawakami, Y. Okuda, S. Kondo, M. Hanatani, H. Suzuki, and K. Yamashita. 1996. Vascular endothelial growth factor is induced by long-term high glucose concentration and up-regulated by acute glucose deprivation in cultured bovine retinal pigmented epithelial cells. Biochem. Biophys. Res. Commun. 221:193-198.
53. Inabe,T., S. Ishibashi, T. Gotoda, M. Kawamura, N. Morino, Y. Nojima, M. Kawakami, Y. Yazaki, and N. Yamada. 1996. Enhanced expression of platelet-derived growth factor-β receptor by high glucose. Involvement of platelet-derived growth factor in diabetic angiopathy. Diabetes. 45:507-512.
54. Shweiki, D., M. Neeman, A. Itin, and E. Keshet. 1995. Induction of vascular endothelial growth factor expression by hypoxia and by glucose deficiency in multicell spheroids: implications for tumor angiogenesis. Proc. Natl, Acad. Sci. USA. 92:768-772.
55. Corbett, J.A., R.G. Tilton, K. Chang, K.S. Hasan, Y. Ido, J.L. Wang, M.A. Sweetland, J.R. Lancaster, J.R. Williamson, and M.L. McDaniel. 1992. Aminoguanidine, a novel inhibitor of nitric oxide formation, prevents diabetic vascular dysfunction. Diabetes. 41:552-556.
56. Xu, X.-P., J.S. Pollock, M.A. Tanner, and P.R. Myers. 1995. Hypoxia activates nitric oxide synthase and stimulates nitric oxide production in porcine coronary resistance arteriolar endothelial cells. Cardiovasc. Res. 30:841-847.
57. Arnet, U.A., A. McMillan, J.L. Dinerman, B. Ballermann, and C.J. Lowenstein. 1996. Regulation of endothelial nitric-oxide synthase during hypoxia. J. Biol. Chem. 271:15069-15073.
58. Wolff, D.J., and A. Lubeskie. 1995. Aminoguanidine is an isoform-selective, mechanism-based inactivator of nitric oxide synthase. Arch. Biochem. Biophys. 316:290-301.