The morphological features and mitochondrial oxidative stress mechanism of the retinal neurons apoptosis in early diabetic rats

Journal of Diabetes Research

Volumn 2014, Issue , 2014, Pages

  Li, Xiaoyan ^a   Zhang, Maonian ^a   Zhou, Huanfen ^a  

^a CHINESE PLA GENERAL HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BODY WEIGHT; CELL STRUCTURE; CELL ULTRASTRUCTURE; CELL VACUOLE; CHROMATIN; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC RETINOPATHY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; GLUCOSE BLOOD LEVEL; HISTOPATHOLOGY; MALE; NICK END LABELING; NONHUMAN; OXIDATIVE STRESS; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETINA GANGLION CELL; RETINA NERVE CELL; ANIMAL; CELL COUNT; CELL NUCLEUS; COMPARATIVE STUDY; ECHOGRAPHY; ENZYMOLOGY; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MITOCHONDRION; NUCLEAR SHAPE; NUCLEAR SIZE; PATHOLOGY; PATHOPHYSIOLOGY; SEVERITY OF ILLNESS INDEX; SPRAGUE DAWLEY RAT; ULTRASTRUCTURE;

ANIMALS; APOPTOSIS; CELL COUNT; CELL NUCLEUS; CELL NUCLEUS SHAPE; CELL NUCLEUS SIZE; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MALE; MITOCHONDRIA; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; RETINAL GANGLION CELLS; RETINAL NEURONS; RNA, MESSENGER; SEVERITY OF ILLNESS INDEX; SUPEROXIDE DISMUTASE;

EID: 84893350154     PISSN: 23146745     EISSN: 23146753     Source Type: Journal    
DOI: 10.1155/2014/678123     Document Type: Article

References (52)

1. Brown A. F., Jiang L., Fong D. S., Need for eye care among older adults with diabetes mellitus in free-for-service and managed medicare. Archives of Ophthalmology 2005 123 5 669 675 10.1001/archopht.123.5.669 (Pubitemid 40695516)
2. Kowluru R. A., Mitochondria damage in the pathogenesis of diabetic retinopathy and in the metabolic memory associated with its continued progression. Current Medicinal Chemistry 2013 20 26 3226 3233
3. Klein B. E. K., Overview of epidemiologic studies of diabetic retinopathy. Ophthalmic Epidemiology 2007 14 4 179 183 2-s2.0-34848907420 10.1080/09286580701396720 (Pubitemid 47493723)
4. Kempen J. H., O'Colmain B. J., Leske M. C., The prevalence of diabetic retinopathy among adults in the United States. Archives of Ophthalmology 2004 122 4 552 563 (Pubitemid 38456292)
5. Abu El-Asrar A. M., Dralands L., Missotten L., Al-Jadaan I. A., Geboes K., Expression of apoptosis markers in the retinas of human subjects with diabetes. Investigative Ophthalmology and Visual Science 2004 45 8 2760 2766 2-s2.0-3242884227 10.1167/iovs.03-1392 (Pubitemid 38998875)
6. Lieth E., Gardner T. W., Barber A. J., Antonetti D. A., Retinal neurodegeneration: early pathology in diabetes. Clinical and Experimental Ophthalmology 2000 28 1 3 8 2-s2.0-0033917515 10.1046/j.1442-9071.2000.00222.x (Pubitemid 30433242)
7. Gardner T. W., Antonetti D. A., Barber A. J., LaNoue K. F., Levison S. W., Diabetic retinopathy: more than meets the eye. Survey of Ophthalmology 2002 47 supplement 2 S253 S262 2-s2.0-0036943831 10.1016/S0039-6257(02)00387-9 (Pubitemid 36351245)
8. Tam J., Dhamdhere K. P., Tiruveedhula P., Lujan B. J., Johnson R. N., Bearse M. A. Jr., Adams A. J., Roorda A., Subclinical capillary changes in non-proliferative diabetic retinopathy. Optometry and Vision Science 2012 89 5 E692 E703 2-s2.0-84859910812 10.1097/OPX.0b013e3182548b07
9. Costa G. N., Vindeirinho J., Cavadas C., Ambrósio A. F., Santos P. F., Contribution of TNF receptor 1 to retinal neural cell death induced by elevated glucose. Molecular and Cellular Neuroscience 2012 50 1 113 123 2-s2.0-84860624256 10.1016/j.mcn.2012.04.003
10. Roy M. S., Gunkel R. D., Podgor M. J., Color vision defects in early diabetic retinopathy. Archives of Ophthalmology 1986 104 2 225 228 2-s2.0-0022580197 (Pubitemid 16119619)
11. Cunha-Vaz J. G., Gray J. R., Zeimer R. C., Mota M. C., Ishimoto B. M., Leite E., Characterization of the early stages of diabetic retinopathy by vitreous fluorophotometry. Diabetes 1985 34 1 53 59 2-s2.0-0021969094 (Pubitemid 15192852)
12. Coupland S. G., A comparison of oscillatory potential and pattern electroretinogram measures in diabetic retinopathy. Documenta Ophthalmologica 1987 66 3 207 218 2-s2.0-0023629156 (Pubitemid 17164947)
13. Sokol S., Moskowitz A., Skarf B., Evans R., Molitch M., Senior B., Contrast sensitivity in diabetics with and without background retinopathy. Archives of Ophthalmology 1985 103 1 51 54 2-s2.0-0021920233 (Pubitemid 15152624)
14. Bucolo C., Leggio G. M., Drago F., Salomone S., Eriodictyol prevents early retinal and plasma abnormalities in streptozotocin-induced diabetic rats. Biochemical Pharmacology 2012 84 1 88 92 2-s2.0-84859702164 10.1016/j.bcp.2012. 03.019
15. 2 in diabetic retinopathy: in vitro and in vivo studies. Biochemical Pharmacology 2013 86 11 1603 1613 10.1016/j.bcp.2013.09.008
16. Brownlee M., The pathobiology of diabetic complications: a unifying mechanism. Diabetes 2005 54 6 1615 1625 2-s2.0-20044376702 10.2337/diabetes.54. 6.1615 (Pubitemid 40770750)
17. Rolo A. P., Palmeira C. M., Diabetes and mitochondrial function: role of hyperglycemia and oxidative stress. Toxicology and Applied Pharmacology 2006 212 2 167 178 2-s2.0-33645765312 10.1016/j.taap.2006.01.003
18. Russell J. W., Golovoy D., Vincent A. M., Mahendru P., Olzmann J. A., Mentzer A., Feldman E. L., High glucose-induced oxidative stress and mitochondrial dysfunction in nuerons. The FASEB Journal 2002 16 13 1738 1748 2-s2.0-0036845661 10.1096/fj.01-1027com (Pubitemid 35340354)
19. Schmeichel A. M., Schmelzer J. D., Low P. A., Oxidative injury and apoptosis of dorsal root ganglion neurons in chronic experimental diabetic neuropathy. Diabetes 2003 52 1 165 171 2-s2.0-0037222391 10.2337/diabetes.52.1. 165 (Pubitemid 36042122)
20. Bucolo C., Ward K. W., Mazzon E., Cuzzocrea S., Drago F., Protective effects of a coumarin derivative in diabetic rats. Investigative Ophthalmology and Visual Science 2009 50 8 3846 3852 2-s2.0-68349104279 10.1167/iovs.08-3328
21. Phaneuf S., Leeuwenburgh C., Cytochrome c release from mitochondria in the aging heart: a possible mechanism for apoptosis with age. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 2002 282 2 R423 R430 2-s2.0-0036081753 (Pubitemid 34664592)
22. Anuradha C. D., Kanno S., Hirano S., Oxidative damage to mitochondria is a preliminary step to caspase-3 activation in fluoride-induced apoptosis in HL-60 cells. Free Radical Biology and Medicine 2001 31 3 367 373 2-s2.0-0035426001 10.1016/S0891-5849(01)00591-3 (Pubitemid 32675342)
23. Lin C.-H., Chen P.-S., Kuo S.-C., Huang L.-J., Gean P.-W., Chiu T.-H., The role of mitochondria-mediated intrinsic death pathway in gingerdione derivative I6-induced neuronal apoptosis. Food and Chemical Toxicology 2012 50 3-4 1073 1081 2-s2.0-84856415585 10.1016/j.fct.2011.11.053
24. Haskins K., Bradley B., Powers K., Fadok V., Flores S., Ling X., Pugazhenthi S., Reusch J., Kench J., Oxidative stress in type 1 diabetes. Annals of the New York Academy of Sciences 2003 1005 43 54 2-s2.0-1942443115 10.1196/annals.1288.006 (Pubitemid 38507733)
25. Umasuthan N., Bathige S. D. N. K., Revathy K. S., Lee Y., Whang I., Choi C. Y., Park H. C., Lee J., A manganese superoxide dismutase (MnSOD) from Ruditapes philippinarum: comparative structural- and expressional-analysis with copper/zinc superoxide dismutase (Cu/ZnSOD) and biochemical analysis of its antioxidant activities. Fish Shellfish Immunol 2012 33 4 753 765 10.1016/j.fsi.2012.06.024
26. Kim J., Yokoyama K., Araki S., The effects of Ginkgo biloba extract (GBe) on axonal transport, microvasculature and morphology of sciatic nerve in streptozotocin-induced diabetic rats. Environmental Health and Preventive Medicine 2000 5 2 53 59 2-s2.0-0033863943 10.1265/ehpm.2000.53
27. Kowluru R. A., Atasi L., Ho Y.-S., Role of mitochondrial superoxide dismutase in the development of diabetic retinopathy. Investigative Ophthalmology and Visual Science 2006 47 4 1594 1599 2-s2.0-33645964980 10.1167/iovs.05-1276 (Pubitemid 46780770)
28. Colombrita C., Calabrese V., Stella A. M. G., Mattei F., Alkon D. L., Scapagnini G., Regional rat brain distribution of heme oxygenase-1 and manganese superoxide dismutase mRNA: relevance of redox homeostasis in the aging processes. Experimental Biology and Medicine 2003 228 5 517 524 2-s2.0-0038206468 (Pubitemid 37203670)
29. Limaye P. V., Raghuram N., Sivakami S., Oxidative stress and gene expression of antioxidant enzymes in the renal cortex of streptozotocin-induced diabetic rats. Molecular and Cellular Biochemistry 2003 243 1-2 147 152 2-s2.0-0037281169 10.1023/A:1021620414979 (Pubitemid 36240562)
30. Li X., Zhang M., Tang W., Effects of melatonin on streptozotocin-induced retina neuronal apoptosis in high blood glucose rat. Neurochemical Research 2013 38 3 669 676 10.1007/s11064-012-0966-z
31. Levkovitch-Verbin H., Sadan O., Vander S., Rosner M., Barhum Y., Melamed E., Offen D., Melamed S., Intravitreal injections of neurotrophic factors secreting mesenchymal stem cells are neuroprotective in rat eyes following optic nerve transaction. Investigative Ophthalmology and Visual Science 2010 51 12 6394 6400 2-s2.0-79955063380 10.1167/iovs.09-4310
32. Li S., Fang J. H., Jiang F. G., Histological observation of RGCs and optic nerve injury in acute ocular hypertension rats. International Journal of Ophthalmology 2010 3 4 311 315 10.3980/j.issn.2222-3959.2010.04.08
33. Shima C., Adachi Y., Minamino K., Okigaki M., Shi M., Imai Y., Yanai S., Takahashi K., Ikehara S., Neuroprotective effects of granulocyte colony-stimulating factor on ischemia-reperfusion injury of the retina. Ophthalmic Research 2012 48 4 199 207 10.1159/000340059
34. Barber A. J., Lieth E., Khin S. A., Antonetti D. A., Buchanan A. G., Gardner T. W., Neural apoptosis in the retina during experimental and human diabetes. Early onset and effect of insulin. Journal of Clinical Investigation 1998 102 4 783 791 2-s2.0-0032529103 (Pubitemid 28399611)
35. Cai L., Li W., Wang G., Guo L., Jiang Y., Kang Y. J., Hyperglycemia-induced apoptosis in mouse myocardium: mitochondrial cytochrome C-mediated caspase-3 activation pathway. Diabetes 2002 51 6 1938 1948 2-s2.0-0036267006 (Pubitemid 34564309)
36. Perdomo J., Cabrera J., Estévez F., Loro J., Reiter R. J., Quintana J., Melatonin induces apoptosis through a caspase-dependent but reactive oxygen species-independent mechanism in human leukemia Molt-3 cells. Journal of Pineal Research 2013 55 2 195 206 10.1111/jpi.12062
37. Li J.-M., Shah A. M., Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 2004 287 5 R1014 R1030 2-s2.0-6344285417 10.1152/ajpregu.00124.2004 (Pubitemid 39391043)
38. Li N., Ragheb K., Lawler G., Sturgis J., Rajwa B., Melendez J. A., Robinson J. P., DPI induces mitochondrial superoxide-mediated apoptosis. Free Radical Biology and Medicine 2003 34 4 465 477 2-s2.0-0037441348 10.1016/S0891-5849(02)01325-4 (Pubitemid 36140171)
39. Scatena R., Mitochondria and cancer: a growing role in apoptosis, cancer cell metabolism and dedifferentiation. Advances in Experimental Medicine and Biology 2012 942 287 308 2-s2.0-84859898559 10.1007/978-94-007-2869-1-13
40. Allen R. G., Balin A. K., Oxidative influence on development and differentiation: an overview of a free radical theory of development. Free Radical Biology and Medicine 1989 6 6 631 661 2-s2.0-0024382255 (Pubitemid 19147814)
41. Kowluru R. A., Tang J., Kern T. S., Abnormalities of retinal metabolism in diabetes and experimental galactosemia. VII. Effect of long-term administration of antioxidants on the development of retinopathy. Diabetes 2001 50 8 1938 1942 2-s2.0-0035434119 (Pubitemid 33641616)
42. Kowluru R. A., Koppolu P., Diabetes-induced activation of caspase-3 in retina: effect of antioxidant therapy. Free Radical Research 2002 36 9 993 999 2-s2.0-0036023314 10.1080/1071576021000006572 (Pubitemid 34863646)
43. Evans J. R., Lawrenson J. G., Antioxidant vitamin and mineral supplements for slowing the progression of age-related macular degeneration. The Cochrane Database of Systematic Reviews 2012 11 CD000254 10.1002/14651858 2-s2.0-33745023856
44. Kowluru R. A., Kern T. S., Engerman R. L., Abnormalities of retinal metabolism in diabetes or experimental galactosemia. IV. Antioxidant defense system. Free Radical Biology and Medicine 1996 22 4 587 592 2-s2.0-0031026597 10.1016/S0891-5849(96)00347-4
45. Li W., Yanoff M., Jian B., He Z., Altered mRNA levels of antioxidant enzymes in pre-apoptotic pericytes from human diabetic retinas. Cellular and Molecular Biology 1999 45 1 59 66 2-s2.0-0033071239
46. Sugawara T., Lewén A., Gasche Y., Yu F., Chan P. H., Overexpression of SOD1 protects vulnerable motor neurons after spinal cord injury by attenuating mitochondrial cytochrome c release. The FASEB Journal 2002 16 14 1997 1999 2-s2.0-0036883891
47. 2+ superoxide dismutase protects against early diabetic glomerular injury in transgenic mice. Diabetes 2001 50 9 2114 2125 2-s2.0-0035461381 10.2337/diabetes.50.9.2114 (Pubitemid 33643680)
48. Craven P. A., Phillips S. L., Melhem M. F., Liachenko J., DeRubertis F. R., Overexpression of manganese superoxide dismutase suppresses increases in collagen accumulation induced by culture of mesangial cells in high-media glucose. Metabolism 2001 50 9 1043 1048 2-s2.0-0034789374 10.1053/meta.2001. 25802 (Pubitemid 32904162)
49. Mohammadzadeh M., Halabian R., Gharehbaghian A., Amirizadeh N., Jahanian-Najafabadi A., Roushandeh A. M., Roudkenar M. H., Nrf-2 overexpression in mesenchymal stem cells reduces oxidative stress-induced apoptosis and cytotoxicity. Cell Stress and Chaperones 2012 17 5 553 565 2-s2.0-84857223245 10.1007/s12192-012-0331-9
50. Santos J. M., Tewari S., Kowluru R. A., A compensatory mechanism protects retinal mitochondria from initial insult in diabetic retinopathy. Free Radical Biology 2012 53 9 1729 1737 10.1016/j.freeradbiomed.2012.08.588
51. Fukai T., Ushio-Fukai M., Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxidants and Redox Signaling 2011 15 6 1583 1606 2-s2.0-79961193678 10.1089/ars.2011.3999
52. Yuki K., Yoshida T., Miyake S., Tsubota K., Ozawa Y., Neuroprotective role of superoxide dismutase 1 in retinal ganglion cells and inner nuclear layer cells against N-methyl-d-aspartate-induced cytotoxicity. Experimental Eye Research 2013 115 230 238 10.1016/j.exer.2013.07.002