Enalapril Alters Expression of Key Growth Factors in Experimental Diabetic Retinopathy

REFERENCES

• Aiello LP, Gardner TW, King GL, et al. Diabetic retinopathy. Diabetes Care. 1998;21:143–156.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Aiello LP, Avery RL, Arrigg PG, et al. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med. 1994;331:1480–1487.
   PubMed Web of Science ®Google Scholar
• Aiello LP, Pierce EA, Foley ED, et al. Suppression of retinal neovascularization in vivo by inhibition of vascular endothelial growth factor (VEGF) using soluble VEGF-receptor chimeric proteins. Proc Natl Acad Sci USA. 1995;92:10457–10461.
   PubMed Web of Science ®Google Scholar
• Chikuma M, Masuda S, Kobayashi T, Nagao M, Sasaki R. Tissue-specific regulation of erythropoietin production in the murine kidney, brain, and uterus. Am J Physiol Endocrinol Metab. 2000;279:E1242–1248.
   Web of Science ®Google Scholar
• Hernandez C, Fonollosa A, Garcia-Ramirez M, et al. Erythropoietin is expressed in the human retina and it is highly elevated in the vitreous fluid of patients with diabetic macular edema. Diabetes Care. 2006;29:2028–2033.
   PubMed Web of Science ®Google Scholar
• Ribatti D, Vacca A, Roccaro AM, Crivellato E, Presta M. Erythropoietin as an angiogenic factor. Eur J Clin Invest. 2003;33:891–896.
   PubMed Web of Science ®Google Scholar
• Genc S, Koroglu TF, Genc K. Erythropoietin and the nervous system. Brain Res. 2004;1000:19–31.
   PubMed Web of Science ®Google Scholar
• Jelkmann W. Effects of erythropoietin on brain function. Curr Pharm Biotechnol. 2005;6:65–79.
   PubMed Web of Science ®Google Scholar
• Becerra SP, Amaral J. Erythropoietin―an endogenous retinal survival factor. N Engl J Med. 2002;347:1968–1970.
   PubMed Web of Science ®Google Scholar
• Joussen AM, Poulaki V, Tsujikawa A, et al. Suppression of diabetic retinopathy with angiopoietin-1. Am J Pathol. 2002;160:1683–1693.
   PubMed Web of Science ®Google Scholar
• Koblizek TI, Weiss C, Yancopoulos GD, Deutsch U, Risau W. Angiopoietin-1 induces sprouting angiogenesis in vitro. Curr Biol. 1998;8:529–532.
   PubMed Web of Science ®Google Scholar
• Papapetropoulos A, Garcia-Cardena G, Dengler TJ, Maisonpierre PC, Yancopoulos GD, Sessa WC. Direct actions of angiopoietin-1 on human endothelium: Evidence for network stabilization, cell survival, and interaction with other angiogenic growth factors. Lab Invest. 1999;79:213–223.
   PubMed Web of Science ®Google Scholar
• Pizurki L, Zhou Z, Glynos K, Roussos C, Papapetropoulos A. Angiopoietin-1 inhibits endothelial permeability, neutrophil adherence, and IL-8 production. Br J Pharmacol. 2003;139:329–336.
   PubMed Web of Science ®Google Scholar
• Witzenbichler B, Maisonpierre PC, Jones P, Yancopoulos GD, Isner JM. Chemotactic properties of angiopoietin-1 and -2, ligands for the endothelial-specific receptor tyrosine kinase Tie2. J Biol Chem. 1998;273:18514–18521.
   PubMed Web of Science ®Google Scholar
• Patel JI, Hykin PG, Gregor ZJ, Boulton M, Cree IA. Angiopoietin concentrations in diabetic retinopathy. Br J Ophthalmol. 2005;89:480–483.
   PubMed Web of Science ®Google Scholar
• Lobov IB, Brooks PC, Lang RA. Angiopoietin-2 displays VEGF-dependent modulation of capillary structure and endothelial cell survival in vivo. Proc Natl Acad Sci USA. 2002;99:11205–11210.
   PubMed Web of Science ®Google Scholar
• Maisonpierre PC, Suri C, Jones PF, et al. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science. 1997;277:55–60.
   PubMed Web of Science ®Google Scholar
• Otani A, Takagi H, Oh H, et al. Angiotensin II-stimulated vascular endothelial growth factor expression in bovine retinal pericytes. Invest Ophthalmol Vis Sci. 2000;41:1192–1199.
   PubMed Web of Science ®Google Scholar
• Anderson S, Jung FF, Ingelfinger JR. Renal renin-angiotensin system in diabetes: Functional, immunohistochemical, and molecular biological correlations. Am J Physiol. 1993;265:F477–486.
   Google Scholar
• Bilous R. Renin angiotensin system (RAS) blockade and diabetic microvascular complications in the eye and kidney. Prim Care Diabetes. 2008;2:201–202.
   PubMedGoogle Scholar
• Wolf G, Ziyadeh FN. The role of angiotensin II in diabetic nephropathy: Emphasis on nonhemodynamic mechanisms. Am J Kidney Dis. 1997;29:153–163.
   PubMed Web of Science ®Google Scholar
• Wolf G, Butzmann U, Wenzel UO. The renin-angiotensin system and progression of renal disease: From hemodynamics to cell biology. Nephron Physiol. 2003;93:P3–13.
   PubMedGoogle Scholar
• Funatsu H, Yamashita H. Pathogenesis of diabetic retinopathy and the renin-angiotensin system. Ophthalmic Physiol Opt. 2003;23:495–501.
   PubMed Web of Science ®Google Scholar
• Tikellis C, Johnston CI, Forbes JM, et al. Identification of angiotensin-converting enzyme 2 in the rodent retina. Curr Eye Res. 2004;29:419–427.
   PubMed Web of Science ®Google Scholar
• Chaturvedi N, Sjolie AK, Stephenson JM, et al. Effect of lisinopril on progression of retinopathy in normotensive people with type 1 diabetes. The EUCLID Study Group. EURODIAB Controlled Trial of Lisinopril in Insulin-Dependent Diabetes Mellitus. Lancet. 1998;351:28–31.
   PubMed Web of Science ®Google Scholar
• Danser AH, Derkx FH, Admiraal PJ, Deinum J, de Jong PT, Schalekamp MA. Angiotensin levels in the eye. Invest Ophthalmol Vis Sci. 1994;35:1008–1018.
   PubMed Web of Science ®Google Scholar
• Danser AH, van den Dorpel MA, Deinum J, et al. Renin, prorenin, and immunoreactive renin in vitreous fluid from eyes with and without diabetic retinopathy. J Clin Endocrinol Metab. 1989;68:160–167.
   PubMed Web of Science ®Google Scholar
• Williams B, Baker AQ, Gallacher B, Lodwick D. Angiotensin II increases vascular permeability factor gene expression by human vascular smooth muscle cells. Hypertension. 1995;25:913–917.
   PubMed Web of Science ®Google Scholar
• Ottlecz A, Bensaoula T. Captopril ameliorates the decreased Na+,K(+)-ATPase activity in the retina of streptozotocin-induced diabetic rats. Invest Ophthalmol Vis Sci. 1996;37:1633–1641.
   PubMed Web of Science ®Google Scholar
• Bensaoula T, Ottlecz A. Biochemical and ultrastructural studies in the neural retina and retinal pigment epithelium of STZ-diabetic rats: Effect of captopril. J Ocul Pharmacol Ther. 2001;17:573–586.
   PubMed Web of Science ®Google Scholar
• Folkman J. Angiogenesis in cancer, vascular, rheumatoid, and other disease. Nat Med. 1995;1:27–31.
   PubMed Web of Science ®Google Scholar
• Ferrara N, Henzel WJ. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem Biophys Res Commun. 1989;161:851–858.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Jaquet K, Krause K, Tawakol-Khodai M, Geidel S, Kuck KH. Erythropoietin and VEGF exhibit equal angiogenic potential. Microvasc Res. 2002;64:326–333.
   PubMed Web of Science ®Google Scholar
• Watanabe D, Suzuma K, Matsui S, et al. Erythropoietin as a retinal angiogenic factor in proliferative diabetic retinopathy. N Engl J Med. 2005;353:782–792.
   PubMed Web of Science ®Google Scholar
• Garcia-Ramirez M, Hernandez C, Simo R. Expression of erythropoietin and its receptor in the human retina: A comparative study of diabetic and nondiabetic subjects. Diabetes Care. 2008;31:1189–1194.
   PubMed Web of Science ®Google Scholar
• Darnell JE Jr. The JAK-STAT pathway: Summary of initial studies and recent advances. Recent Prog Horm Res. 1996;51:391–403; discussion 403–394.
   PubMedGoogle Scholar
• Jung JE, Lee HG, Cho IH, et al. STAT3 is a potential modulator of HIF-1-mediated VEGF expression in human renal carcinoma cells. FASEB J. 2005;19:1296–1298.
   PubMedGoogle Scholar
• Wojchowski DM, Gregory RC, Miller CP, Pandit AK, Pircher TJ. Signal transduction in the erythropoietin receptor system. Exp Cell Res. 1999;253:143–156.
   PubMed Web of Science ®Google Scholar
• Nomura S, Kanazawa H, Hirata K, Iwao H, Yoshikawa J. Relationship between vascular endothelial growth factor and angiopoietin-2 in asthmatics before and after inhaled beclomethasone therapy. J Asthma. 2005;42:141–146.
   PubMed Web of Science ®Google Scholar
• Berka JL, Stubbs AJ, Wang DZ, et al. Renin-containing Muller cells of the retina display endocrine features. Invest Ophthalmol Vis Sci. 1995;36:1450–1458.
   PubMed Web of Science ®Google Scholar
• Gilbert RE, Kelly DJ, Cox AJ, et al. Angiotensin-converting enzyme inhibition reduces retinal overexpression of vascular endothelial growth factor and hyperpermeability in experimental diabetes. Diabetologia. 2000;43:1360–1367.
   PubMed Web of Science ®Google Scholar
• Hogeboom van Buggenum IM, Polak BC, Reichert-Thoen JW, de Vries-Knoppert WA, van Hinsbergh VW, Tangelder GJ. Angiotensin-converting enzyme-inhibiting therapy is associated with lower vitreous vascular endothelial growth factor concentrations in patients with proliferative diabetic retinopathy. Diabetologia. 2002;45:203–209.
   PubMed Web of Science ®Google Scholar
• Zheng Z, Chen H, Xu X, Li C, Gu Q. Effects of angiotensin-converting enzyme inhibitors and beta-adrenergic blockers on retinal vascular endothelial growth factor expression in rat diabetic retinopathy. Exp Eye Res. 2007;84:745–752.
   PubMed Web of Science ®Google Scholar