Endothelin receptor-a antagonist attenuates retinal vascular and neuroretinal pathology in diabetic mice

Investigative Ophthalmology and Visual Science

Volumn 55, Issue 4, 2014, Pages 2516-2525

  Chou, Jonathan C ^a   Rollins, Stuart D ^a   Ye, Minghao ^a   Batlle, Daniel ^a   Fawzi, Amani A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Diabetic mice; Diabetic retinopathy; Endothelins; Pericyte; Retinal vessels

Indexed keywords

ATRASENTAN; GLUCOSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DENSITY; CONTROLLED STUDY; DIABETIC RETINOPATHY; ENDOTHELIUM; FEMALE; IMMUNOHISTOCHEMISTRY; MOUSE; NICK END LABELING; NONHUMAN; PERICYTE; PRIORITY JOURNAL; RETINAL THICKNESS; VASCULAR DISEASE;

DIABETIC MICE; DIABETIC RETINOPATHY; ENDOTHELINS; PERICYTE; RETINAL VESSELS;

ANIMALS; APOPTOSIS; CELL COUNT; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; ENDOTHELIN-1; FEMALE; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; MICE; MICE, INBRED C57BL; PYRROLIDINES; RECEPTORS, ENDOTHELIN; RETINAL GANGLION CELLS; RETINAL VESSELS;

EID: 84898839636     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-13676     Document Type: Article

References (55)

1. Kertes PJJT. Evidence Based Eye Care. 1st ed. Philadelphia: Lippincott Williams & Wilkins; 2006.
2. Centers for Disease Control and Prevention. Blindness caused by diabetes-Massachusetts, 1987-1994. MMWR Morbid Mortal Wkly Rep. 1996;45:937-941.
3. World Health Organization. Prevention of Blindness and Visual Impairment. Causes of blindness and visual impairment. Available at: http://www.who.int/blindness/causes/en/. Accessed November 25, 2013.
4. Mizutani M, Kern TS, Lorenzi M. Accelerated death of retinal microvascular cells in human and experimental diabetic retinopathy. J Clin Invest. 1996;97:2883-2890.
5. Armulik A, Abramsson A, Betsholtz C. Endothelial/pericyte interactions. Circ Res. 2005;97:512-523.
6. Balabanov R, Dore-Duffy P. Role of the CNS microvascular pericyte in the blood-brain barrier. J Neurosci Res. 1998;53: 637-644.
7. Dore-Duffy P, Balabanov R, Beaumont T, Katar M. The CNS pericyte response to low oxygen: early synthesis of cyclopentenone prostaglandins of the J-series. Microvasc Res. 2005; 69:79-88.
8. Geraldes P, Hiraoka-Yamamoto J, Matsumoto M, et al. Activation of PKC-delta and SHP-1 by hyperglycemia causes vascular cell apoptosis and diabetic retinopathy. Nat Med. 2009;15:1298-1306.
9. Kalani M. The importance of endothelin-1 for microvascular dysfunction in diabetes. Vasc Health Risk Manag. 2008;4: 1061-1068.
10. Chakrabarti S, Gan XT, Merry A, Karmazyn M, Sima AA. Augmented retinal endothelin-1, endothelin-3, endothelinA and endothelinB gene expression in chronic diabetes. Curr Eye Res. 1998;17:301-307.
11. Yanagisawa M, Kurihara H, Kimura S, et al. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature. 1988;332:411-415.
12. Warner BB, Stuart LA, Papes RA, Wispe JR. Functional and pathological effects of prolonged hyperoxia in neonatal mice. Am J Physiol. 1998;275:L110-L117.
13. Syed H, Safa R, Chidlow G, Osborne NN. Sulfisoxazole, an endothelin receptor antagonist, protects retinal neurones from insults of ischemia/reperfusion or lipopolysaccharide. Neurochem Int. 2006;48:708-717.
14. Wang Z, Yadav AS, Leskova W, Harris NR. Attenuation of streptozotocin-induced microvascular changes in the mouse retina with the endothelin receptor A antagonist atrasentan. Exp Eye Res. 2010;91:670-675.
15. Bursell SE, Clermont AC, Oren B, King GL. The in vivo effect of endothelins on retinal circulation in nondiabetic and diabetic rats. Invest Ophthalmol Vis Sci. 1995;36:596-607.
16. Wenzel RR, Littke T, Kuranoff S, et al. Avosentan reduces albumin excretion in diabetics with macroalbuminuria. J Am Soc Nephrol. 2009;20:655-664.
17. Mann JF, Green D, Jamerson K, et al. Avosentan for overt diabetic nephropathy. J Am Soc Nephrol. 2010;21:527-535.
18. Kohan DE, Pritchett Y, Molitch M, et al. Addition of atrasentan to renin-angiotensin system blockade reduces albuminuria in diabetic nephropathy. J Am Soc Nephrol. 2011;22:763-772.
19. Barton M, Tharaux PT. Endothelin and the podocyte. Clin Kidney J. 2012;5:17-27.
20. Shankland SJ. The podocyte's response to injury: role in proteinuria and glomerulosclerosis. Kidney Int. 2006;69: 2131-2147.
21. Ramachandran E, Frank RN, Kennedy A. Effects of endothelin on cultured bovine retinal microvascular pericytes. Invest Ophthalmol Vis Sci. 1993;34:586-595.
22. Kuwabara T, Cogan DG. Studies of retinal vascular patterns. I. Normal architecture. Arch Ophthalmol. 1960;64:904-911.
23. Chou JC, Rollins SD, Fawzi AA. Trypsin digest protocol to analyze the retinal vasculature of a mouse model. J Vis Exp. 2013;76:e50489.
24. Cuthbertson RA, Mandel TE. Anatomy of the mouse retina. Endothelial cell-pericyte ratio and capillary distribution. Invest Ophthalmol Vis Sci. 1986;27:1659-1664.
25. Midena E, Segato T, Radin S, et al. Studies on the retina of the diabetic db/db mouse. I. Endothelial cell-pericyte ratio. Ophthalmic Res. 1989;21:106-111.
26. Zheng L, Szabo C, Kern TS. Poly(ADP-ribose) polymerase is involved in the development of diabetic retinopathy via regulation of nuclear factor-kappaB. Diabetes. 2004;53:2960-2967. Accessed September 1, 2012.
27. Olaisen BR. Distance between lines, a plugin for ImageJ. NIH ImageJ Archives. 2006. Available at: https://list.nih.gov/cgi-bin/wa.exe?A2=IMAGEJ;7ff36be1.0608.
28. Krueger M, Bechmann I. CNS pericytes: concepts, misconceptions, and a way out. Glia. 2010;58:1-10.
29. Barton M. Endothelin antagonism and reversal of proteinuric renal disease in humans. Contrib Nephrol. 2011;172:210-222.
30. Chakravarthy U, Gardiner TA, Anderson P, Archer DB, Trimble ER. The effect of endothelin 1 on the retinal microvascular pericyte. Microvasc Res. 1992;43:241-254.
31. Romeo G, Liu WH, Asnaghi V, Kern TS, Lorenzi M. Activation of nuclear factor-kappaB induced by diabetes and high glucose regulates a proapoptotic program in retinal pericytes. Diabetes. 2002;51:2241-2248.
32. Williams FM, Dosso AA, Kohner EM, Porta M. Pericyte mitogenic activity is reduced in the blood of type 1 diabetic patients with and without retinopathy. Acta Diabetol. 1993; 30:123-127.
33. Geraldes P, Hiraoka-Yamamoto J, Matsumoto M, et al. Activation of PKC-delta and SHP-1 by hyperglycemia causes vascular cell apoptosis and diabetic retinopathy. Nat Med. 2009;15:1298-1306.
34. Park JY, Takahara N, Gabriele A, et al. Induction of endothelin-1 expression by glucose: an effect of protein kinase C activation. Diabetes. 2000;49:1239-1248.
35. Ramzy D, Rao V, Tumiati LC, et al. Elevated endothelin-1 levels impair nitric oxide homeostasis through a PKC-dependent pathway. Circulation. 2006;114:I319-I326.
36. Wedgwood S, Black SM. Endothelin-1 decreases endothelial NOS expression and activity through ETA receptor-mediated generation of hydrogen peroxide. Am J Physiol Lung Cell Mol Physiol. 2005;288:L480-L487.
37. Walshe TE, Connell P, Cryan L, Ferguson G, O'Brien C, Cahill PA. The role of pulsatile flow in controlling microvascular retinal endothelial and pericyte cell apoptosis and proliferation. Cardiovasc Res. 2011;89:661-670.
38. Barber AJ, Antonetti DA, Kern TS, et al. The Ins2(Akita) mouse as a model of early retinal complications in diabetes. Invest Ophthalmol Vis Sci. 2005;46:2210-2218.
39. Martin PM, Roon P, Van Ells TK, Ganapathy V, Smith SB. Death of retinal neurons in streptozotocin-induced diabetic mice. Invest Ophthalmol Vis Sci. 2004;45:3330-3336.
40. Park SH, Park JW, Park SJ, et al. Apoptotic death of photoreceptors in the streptozotocin-induced diabetic rat retina. Diabetologia. 2003;46:1260-1268.
41. Barber AJ, Lieth E, Khin SA, Antonetti DA, Buchanan AG, Gardner TW. Neural apoptosis in the retina during experimental and human diabetes. Early onset and effect of insulin. J Clin Invest. 1998;102:783-791.
42. van Dijk HW, Verbraak FD, Kok PH, et al. Early neurodegeneration in the retina of type 2 diabetic patients. Invest Ophthalmol Vis Sci. 2012;53:2715-2719.
43. Antonetti DA, Barber AJ, Bronson SK, et al. Diabetic retinopathy: seeing beyond glucose-induced microvascular disease. Diabetes. 2006;55:2401-2411.
44. Gardner TW, Antonetti DA, Barber AJ, LaNoue KF, Levison SW. Diabetic retinopathy: more than meets the eye. Surv Ophthalmol. 2002;47:S253-S262.
45. Chakrabarti S, Sima AA. Endothelin-1 and endothelin-3-like immunoreactivity in the eyes of diabetic and non-diabetic BB/ W rats. Diabetes Res Clin Pract. 1997;37:109-120.
46. Tacconi MT. Neuronal death: is there a role for astrocytes? Neurochem Res. 1998;23:759-765.
47. Salvatore S, Vingolo EM. Endothelin-1 role in human eye: a review. J Ophthalmol. 2010;2010:354645.
48. Kobayashi T, Oku H, Fukuhara M, et al. Endothelin-1 enhances glutamate-induced retinal cell death, possibly through ETA receptors. Invest Ophthalmol Vis Sci. 2005;46:4684-4690.
49. Chou YC, Perng JC, Juan CC, et al. Endothelin-1 inhibits insulin-stimulated glucose uptake in isolated rat adipocytes. Biochem Biophys Res Commun. 1994;202:688-693.
50. Berthiaume N, Wessale JL, Opgenorth TJ, Zinker BA. Metabolic responses with endothelin antagonism in a model of insulin resistance. Metabolism. 2005;54:735-740.
51. Ortmann J, Nett PC, Celeiro J, et al. Endothelin inhibition delays onset of hyperglycemia and associated vascular injury in type I diabetes: evidence for endothelin release by pancreatic islet beta-cells. Biochem Biophys Res Commun. 2005;334:689-695.
52. Zoja C, Cattaneo S, Fiordaliso F, et al. Distinct cardiac and renal effects of ETA receptor antagonist and ACE inhibitor in experimental type 2 diabetes. Am J Physiol Renal Physiol. 2011;301:F1114-F1123.
53. Wenzel R, Ritz E, Wenzel M. Endothelin receptor antagonists in diabetic nephropathy. European Nephrology. 2012;6:38-41.
54. Polak K, Luksch A, Frank B, Jandrasits K, Polska E, Schmetterer L. Regulation of human retinal blood flow by endothelin-1. Exp Eye Res. 2003;76:633-640.
55. Sen S, Chen S, Feng B, Iglarz M, Chakrabarti S. Renal, retinal and cardiac changes in type 2 diabetes are attenuated by macitentan, a dual endothelin receptor antagonist. Life Sci. 2012;91:658-668.