Intravitreal injection of erythropoietin protects both retinal vascular and neuronal cells in early diabetes

Investigative Ophthalmology and Visual Science

Volumn 49, Issue 2, 2008, Pages 732-742

  Zhang, Jingfa ^a,b,c   Wu, Yalan ^a,b   Jin, Ying ^b   Ji, Fei ^a,b   Sinclair, Stephen H ^d   Luo, Yan ^e   Xu, Guoxu ^f   Lu, Luo ^a   Dai, Wei ^a   Yanoff, Myron ^d   Li, Weiye ^a,b,d,e,g   Xu, Guo Tong ^a,b  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^d DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^e PEKING UNION MEDICAL COLLEGE   (China)

^f SUZHOU VOCATIONAL UNIVERSITY   (China)

^g NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROPOIETIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; RECOMBINANT ERYTHROPOIETIN; STAT5 PROTEIN; ERYTHROPOIETIN; EVANS BLUE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD RETINA BARRIER; CELL COUNT; CONTROLLED STUDY; DIABETIC RETINOPATHY; DISEASE COURSE; ELECTRON MICROSCOPY; ENZYME ACTIVATION; EYE PROTECTION; IMMUNOHISTOCHEMISTRY; MALE; NICK END LABELING; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; RAT; RETINA CELL; RETINA INJURY; RETINA NERVE CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; STREPTOZOCIN DIABETES; UPREGULATION; WESTERN BLOTTING; ANIMAL; CAPILLARY PERMEABILITY; DRUG EFFECT; ENZYME IMMUNOASSAY; EXPERIMENTAL DIABETES MELLITUS; INJECTION; METABOLISM; NERVE CELL; RETINA BLOOD VESSEL; VITREOUS BODY;

ANIMALS; APOPTOSIS; BLOOD-RETINAL BARRIER; BLOTTING, WESTERN; CAPILLARY PERMEABILITY; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; ERYTHROPOIETIN; EVANS BLUE; IMMUNOENZYME TECHNIQUES; IN SITU NICK-END LABELING; INJECTIONS; MALE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ERYTHROPOIETIN; RETINAL VESSELS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STAT5 TRANSCRIPTION FACTOR; VITREOUS BODY;

EID: 40649087674     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.07-0721     Document Type: Article

References (68)

1. Vision Problems in the U.S.: Facts and Figures. Chicago: National Society to Prevent Blindness (now Prevent Blindness America): 1980.
2. Abu-El-Asrar AM, Dralands L, Missotten L, Al-Jadaan IA, Geboes K. Expression of apoptosis markers in the retinas of human subjects with diabetes. Invest Ophthalmol Vis Sci. 2004;45:2760-2766.
3. Lieth E, Gardner TW, Barber AJ, Antonetti DA. Retinal neurodegeneration: early pathology in diabetes. Clin Exp Ophthalmol. 2000:28:3-8.
4. Gardner TW, Antonetti DA, Barber AJ, LaNoue KF, Levison SW. Diabetic retinopathy: more than meets the eye. Surv Ophthalmol. 2002:47(suppl 2):S253-S262.
5. Cunha-Vaz JG, Gray JR, Zeimer RC, Mota MC, Ishimoto BM, Leite E. Characterization of the early stages of diabetic retinopathy by vitreous fluorophotometry. Diabetes. 1985;34:53-59.
6. Coupland SG. A comparison of oscillatory potential and pattern electroretinogram measures in diabetic retinopathy. Doc Ophthalmol. 1987;66:207-218.
7. Roy MS, Gunkel RD, Podgor MJ. Color vision defects in early diabetic retinopathy. Arch Ophthalmol. 1986;104:225-228.
8. Sokol S, Moskowitz A, Skarf B, Evans R, Molitch M, Senior B. Contrast sensitivity in diabetics with and without background retinopathy. Arch Ophthalmol. 1985;103:51-54.
9. Ferris F. Early photocoagulation in patients with either type I or type II diabetes. Trans Am Ophthalmol Soc. 1996;94:505-537.
10. Early Treatment Diabetic Retinopathy Study Research Group. Early photocoagulation for diabetic retinopathy. ETDRS report number 9. Ophthalmology. 1991;98:766-785.
11. Chong ZZ, Kang JQ, Maiese K. Erythropoietin is a novel vascular protectant through activation of Akt1 and mitochondrial modulation of cysteine proteases. Circulation. 2002;106:2973-2979.
12. Ghezzi P, Brines M. Erythropoietin as an antiapoptotic, tissue-protective cytokine. Cell Death Differ. 2004;11(suppl 1):S37-S44.
13. Buemi M, Cavallaro E, Floccari F, et al. The pleiotropic effects of erythropoietin in the central nervous system. J Neuropathol Exp Neurol. 2003;62:228-236.
14. Zhong L, Bradley J, Schubert W, et al. Erythropoietin promotes survival of retinal ganglion cells in DBA/2J glaucoma mice. Invest Ophthalmol Vis Sci. 2007;48:1212-1218.
15. Juul SE, Yachnis AT, Christensen RD. Tissue distribution of erythropoietin and erythropoietin receptor in the developing human fetus. Early Hum Dev. 1998;52:235-249.
16. Bocker-Meffert S, Rosenstiel P, Rohl C, et al. Erythropoietin and VEGF promote neural outgrowth from retinal explants in postnatal rats. Invest Ophthalmol Vis Sci. 2002;43:2021-2026.
17. Weishaupt JH, Rohde G, Polking E, Siren AL, Ehrenreich H, Bahr M. Effect of erythropoietin axotomy-induced apoptosis in rat retinal ganglion cells. Invest Ophthalmol Vis Sci. 2004;45:1514-1522.
18. King CE, Rodger J, Bartlett C, Esmaili T, Dunlop SA, Beazley LD. Erythropoietin is both neuroprotective and neuroregenerative following optic nerve transection. Exp Neurol. 2007;205:48-55.
19. Junk AK, Mammis A, Savitz SI, et al. Erythropoietin administration protects retinal neurons from acute ischemia-reperfusion injury. Proc Natl Acad Sci USA. 2002;99:10659-10664.
20. Becerra SP, Amaral J. Erythropoietin-an endogenous retinal survival factor. N Engl J Med. 2002;347:1968-1970.
21. Grimm C, Wenzel A, Groszer M, et al. HIF-1-induced erythropoietin in the hypoxic retina protects against light-induced retinal degeneration. Nat Med. 2002;8:718-724.
22. Cotroneo P, Maria Ricerca B, Todaro L, et al. Blunted erythropoietin response to anemia in patients with type 1 diabetes. Diabetes Metab Res Rev. 2000;16:172-176.
23. Winkler AS, Marsden J, Chaudhuri KR, Hambley H, Watkins PJ. Erythropoietin depletion and anaemia in diabetes mellitus. Diabet Med. 1999;16:813-819.
24. Friedman EA, L'Esperance FA, Brown CD, Berman DH. Treating azotemia-induced anemia with erythropoietin improves diabetic eye disease. Kidney Int Suppl. 2003;S57-S63.
25. Inomata Y, Hirata A, Takahashi E, Kawaji T, Fukushima M, Tanihara H. Elevated erythropoietin in vitreous with ischemic retinal diseases. Neuroreport. 2004;15:877-879.
26. 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.
27. 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.
28. Xu Q, Qaum T, Adamis AP. Sensitive blood-retinal barrier breakdown quantitation using Evans blue. Invest Ophthalmol Vis Sci. 2001;42:789-794.
29. Krishnamoorthy RR, Agarwal P, Prasanna G, et al. Characterization of a transformed rat retinal ganglion cell line. Brain Res Mol Brain Res. 2001;86:1-12.
30. Seigel GM. Establishment of an E1A-immortalized retinal cell culture. In Vitro Cell Dev Biol Anim. 1996;32:66-68.
31. LeVeen HH, Fishman WH. Combination of Evans blue with plasma protein: its significance in capillary permeability studies, blood dye disappearance curves, and its use as a protein tag. Am J Physiol. 1947;151:26-33.
32. Charriaut-Marlangue C, Ben-Ari Y. A cautionary note on the use of the TUNEL stain to determine apoptosis. Neuroreport. 1995;7:61-64.
33. De La Cruz JP, Gonzalez-Correa JA, Guerrero A, de la Cuesta FS. Pharmacological approach to diabetic retinopathy. Diabetes Metab Res Rev. 2004;20:91-113.
34. Donnelly R, Emslie-Smith AM, Gardner ID, Morris AD. ABC of arterial and venous disease: vascular complications of diabetes. BMJ. 2000;320:1062-1066.
35. Yu DY, Cringle SJ, Su EN, Yu PK, Jerums G, Cooper ME. Pathogenesis and intervention strategies in diabetic retinopathy. Clin Experiment Ophthalmol. 2001;29:164-166.
36. Li W, Yanoff M, Jian B, He Z. Altered mRNA levels of antioxidant enzymes in pre-apoptotic pericytes from human diabetic retinas. Cell Mol Biol (Noisy-le-grand). 1999;45:59-66.
37. 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.
38. Joussen AM, Poulaki V, Mitsiades N, et al. Suppression of Fas-FasL-induced endothelial cell apoptosis prevents diabetic blood-retinal barrier breakdown in a model of streptozotocin-induced diabetes. FASEB J. 2003;17:76-78.
39. Joussen AM, Murata T, Tsujikawa A, Kirchhof B, Bursell SE, Adamis AP. Leukocyte-mediated endothelial cell injury and death in the diabetic retina. Am J Pathol. 2001;158:147-152.
40. Sorbinil Retinopathy Trial Research Group. A randomized trial of sorbinil, an aldose reductase inhibitor, in diabetic retinopathy. Arch Ophthalmol. 1990;108:1234-1244.
41. Milton R, Aiello L, Davis M, et al. Initial results of the Protein Kinase C b Inhibitor Diabetic Retinopathy Study (PKC-DRS) (Abstract). Diabetes. 2003;52:(suppl 1):A-127.
42. Hammes HP, Du X, Edelstein D, et al. Benfotiamine blocks three major pathways of hyperglycemic damage and prevents experimental diabetic retinopathy. Nat Med. 2003;9:294-299.
43. 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.
44. Li W, Yanoff M, Liu X, Ye X. Retinal capillary pericyte apoptosis in early human diabetic retinopathy. Chin Med J(Engl). 1997;110:659-663.
45. 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.
46. Zhang SX, Ma JX, Sima J, et al. Genetic difference in susceptibility to the blood-retina barrier breakdown in diabetes and oxygen-induced retinopathy. Am J Pathol. 2005;166:313-321.
47. Kirber WM, Nichols CW, Grimes PA, Winegrad AI, Laties AM. A permeability defect of the retinal pigment epithelium: occurrence in early streptozocin diabetes. Arch Ophthalmol. 1980;98:725-728.
48. Aizu Y, Oyanagi K, Hu J, Nakagawa H. Degeneration of retinal neuronal processes and pigment epithelium in the early stage of the streptozotocin- diabetic rats. Neuropathology. 2002;22:161-170.
49. Marti HH, Bernaudin M, Petit E, Bauer C. Neuroprotection and angiogenesis: dual role of erythropoietin in brain ischemia. News Physiol Sci. 2000;15:225-229.
50. Foster DJ, Moe OW, Hsia CC. Upregulation of erythropoietin receptor during postnatal and postpneumonectomy lung growth. Am J Physiol. 2004;287:L1107-L1115.
51. Brines M, Cerami A. Emerging biological roles for erythropoietin in the nervous system. Nat Rev Neurosci. 2005;6:484-494.
52. Villa P, Bigini P, Mennini T, et al. Erythropoietin selectively attenuates cytokine production and inflammation in cerebral ischemia by targeting neuronal apoptosis. J Exp Med. 2003;198:971-975.
53. Agnello D, Bigini P, Villa P, et al. Erythropoietin exerts an anti-inflammatory effect on the CNS in a model of experimental autoimmune encephalomyelitis. Brain Res. 2002;952:128-134.
54. Wang L, Zhang Z, Wang Y, Zhang R, Chopp M. Treatment ofstroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke. 2004;35:1732-1737.
55. Beleslin-Cokic BB, Cokic VP, Yu X, Weksler BB, Schechter AN, Noguchi CT. Erythropoietin and hypoxia stimulate erythropoietin receptor and nitric oxide production by endothelial cells. Blood. 2004;104:2073-2080.
56. Morishita E, Masuda S, Nagao M, Yasuda Y, Sasaki R. Erythropoietin receptor is expressed in rat hippocampal and cerebral cortical neurons, and erythropoietin prevents in vitro glutamate-induced neuronal death. Neuroscience. 1997;76:105-116.
57. Gorio A, Gokmen N, Erbayraktar S, et al. Recombinant human erythropoietin counteracts secondary injury and markedly enhances neurological recovery from experimental spinal cord trauma. Proc Natl Acad Sci USA. 2002;99:9450-9455.
58. Brines M, Grasso G, Fiordaliso F, et al. Erythropoietin mediates tissue protection through an erythropoietin and common beta-subunit heteroreceptor. Proc Natl Acad Sci USA. 2004;101:14907-14912.
59. Um M, Lodish HF. Antiapoptotic effects of erythropoietin in differentiated neuroblastoma SH-SY5Y cells require activation of both the STAT5 and AKT signaling pathways. J Biol Chem. 2006;281: 5648-5656.
60. Bartesaghi S, Marinovich M, Corsini E, Galli CL, Viviani B. Erythropoietin: a novel neuroprotective cytokine. Neurotoxicology. 2005;26:923-928.
61. Kilic U, Kilic E, Soliz J, Bassetti CI, Gassmann M, Hermann DM. Erythropoietin protects from axotomy-induced degeneration of retinal ganglion cells by activating ERK-1/-2. FASEB J. 2005;19:249-251.
62. Kretz A, Happold CJ, Marticke JK, Isenmann S. Erythropoietin promotes regeneration of adult CNS neurons via Jak2/Stat3 and PI3K/AKT pathway activation. Mol Cell Neurosci. 2005;29:569- 579.
63. Lee SM, Nguyen TH, Park MH, et al. EPO receptor-mediated ERK kinase and NF-kappaB activation in erythropoietin-promoted differentiation of astrocytes. Biochem Biophys Res Commun. 2004; 320:1087-1095.
64. Jacobs-Helber SM, Ryan JJ, Sawyer ST. JNK and p38 are activated by erythropoietin (EPO) but are not induced in apoptosis following EPO withdrawal in EPO-dependent HCD57 cells. Blood. 2000; 96:933-940.
65. Ammarguellat F, Llovera M, Kelly PA, Goffin V. Low doses of EPO activate MAP kinases but not JAK2-STAT5 in rat vascular smooth muscle cells. Biochem Biophys Res Commun. 2001;284:1031-1038.
66. Tsuji-Takayama K, Otani T, Inoue T, et al. Erythropoietin induces sustained phosphorylation of STAT5 in primitive but not definitive erythrocytes generated from mouse embryonic stem cells. Exp Hematol. 2006;34:1323-1332.
67. Manzoni P, Maestri A, Gomirato G, Takagi H, Watanabe D, Matsui S. Erythropoietin as a retinal angiogenic factor (letter). N Engl J Med. 2005;353:2190-2191; reply 2005:2191.
68. Gewirtz DA, Di X, Walker TD, Sawyer ST. Erythropoietin fails to interfere with the antiproliferative and cytotoxic effects of antitumor drugs. Clin Cancer Res. 2006;12:2232-2238.