Increased oxidative and nitrative stress accelerates aging of the retinal vasculature in the diabetic retina

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Lamoke, Folami ^a   Shaw, Sean ^a   Yuan, Jianghe ^a   Ananth, Sudha ^a   Duncan, Michael ^a   Martin, Pamela ^a   Bartoli, Manuela ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; MESSENGER RNA; SIRTUIN 1; 4-HYDROXY-2-NONENAL; ALDEHYDE; LIPID; MICRORNA; NITROGEN; SIRT1 PROTEIN, RAT; STREPTOZOCIN;

ADULT; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC RETINOPATHY; DISEASE COURSE; ENZYME ACTIVITY; EPIGENETICS; EPITHELIUM; HYPERGLYCEMIA; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; LIPID PEROXIDATION; MALE; MORPHOLOGY; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PIGMENT EPITHELIUM; PRIMARY CELL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RETINA BLOOD VESSEL; SENESCENCE; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CELL AGING; CHEMISTRY; EXPERIMENTAL DIABETES MELLITUS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RETINA; SPRAGUE DAWLEY RAT;

AGING; ALDEHYDES; ANIMALS; CELL AGING; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; IMMUNOHISTOCHEMISTRY; LIPIDS; MALE; MICRORNAS; NITROGEN; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; RETINA; RETINAL VESSELS; RNA, MESSENGER; SIRTUIN 1; STREPTOZOCIN;

EID: 84949035142     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0139664     Document Type: Article

References (65)

1. Sivaprasad S, Gupta B, Crosby-Nwaobi R, Evans J. Prevalence of diabetic retinopathy in various ethnic groups: a worldwide perspective. Survey of ophthalmology. 2012; 57(4):347-70. doi: 10.1016/j. survophthal.2012.01.004 PMID: 22542913.
2. Caldwell RB, Bartoli M, Behzadian MA, El-Remessy AE, Al-Shabrawey M, Platt DH, et al. Vascular endothelial growth factor and diabetic retinopathy: pathophysiological mechanisms and treatment perspectives. Diabetes/metabolism research and reviews. 2003; 19(6):442-55. doi: 10.1002/dmrr.415 PMID: 14648803.
3. Stitt AW, Gardiner TA, Archer DB. Histological and ultrastructural investigation of retinal microaneurysm development in diabetic patients. The British journal of ophthalmology. 1995; 79(4):362-7. PMID: 7742285; PubMed Central PMCID: PMC505103.
4. Simo R, Hernandez C, European Consortium for the Early Treatment of Diabetic R. Neurodegeneration in the diabetic eye: new insights and therapeutic perspectives. Trends in endocrinology and metabolism: TEM. 2014; 25(1):23-33. doi: 10.1016/j.tem.2013.09.005 PMID: 24183659.
5. 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. The Journal of clinical investigation. 1998; 102(4):783-91. doi: 10.1172/JCI2425 PMID: 9710447; PubMed Central PMCID: PMC508941.
6. Park HY, Kim IT, Park CK. Early diabetic changes in the nerve fibre layer at the macula detected by spectral domain optical coherence tomography. The British journal of ophthalmology. 2011; 95 (9):1223-8. doi: 10.1136/bjo.2010.191841 PMID: 21216799.
7. Lasta M, Pemp B, Schmidl D, Boltz A, Kaya S, Palkovits S, et al. Neurovascular dysfunction precedes neural dysfunction in the retina of patients with type 1 diabetes. Investigative ophthalmology & visual science. 2013; 54(1):842-7. doi: 10.1167/iovs.12-10873 PMID: 23307962.
8. Tremolada G, Del Turco C, Lattanzio R, Maestroni S, Maestroni A, Bandello F, et al. The role of angiogenesis in the development of proliferative diabetic retinopathy: impact of intravitreal anti-VEGF treatment. Experimental diabetes research. 2012; 2012:728325. doi: 10.1155/2012/728325 PMID: 22566995; PubMed Central PMCID: PMC3332167.
9. Wang S, Park JK, Duh EJ. Novel targets against retinal angiogenesis in diabetic retinopathy. Current diabetes reports. 2012; 12(4):355-63. doi: 10.1007/s11892-012-0289-0 PMID: 22638940.
10. Al-Shabrawey M, Rojas M, Sanders T, Behzadian A, El-Remessy A, Bartoli M, et al. Role of NADPH oxidase in retinal vascular inflammation. Investigative ophthalmology & visual science. 2008; 49 (7):3239-44. doi: 10.1167/iovs.08-1755 PMID: 18378574.
11. El-Remessy AB, Al-Shabrawey M, Platt DH, Bartoli M, Behzadian MA, Ghaly N, et al. Peroxynitrite mediates VEGF's angiogenic signal and function via a nitration-independent mechanism in endothelial cells. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2007; 21(10):2528-39. doi: 10.1096/fj.06-7854com PMID: 17384142.
12. Zhong Q, Mishra M, Kowluru RA. Transcription factor Nrf2-mediated antioxidant defense system in the development of diabetic retinopathy. Investigative ophthalmology & visual science. 2013; 54(6):3941-8 doi: 10.1167/iovs.13-11598 PMID: 23633659; PubMed Central PMCID: PMC3676188.
13. Donato AJ, Morgan RG, Walker AE, Lesniewski LA. Cellular and molecular biology of aging endothelial cells. J Mol Cell Cardiol. 2015. doi: 10.1016/j.yjmcc.2015.01.021 PMID: 25655936.
14. El Assar M, Angulo J, Vallejo S, Peiro C, Sanchez-Ferrer CF, Rodriguez-Manas L. Mechanisms involved in the aging-induced vascular dysfunction. Front Physiol. 2012; 3:132. doi: 10.3389/fphys. 2012.00132 PMID: 22783194; PubMed Central PMCID: PMC3361078.
15. Rodriguez-Manas L, El-Assar M, Vallejo S, Lopez-Doriga P, Solis J, Petidier R, et al. Endothelial dysfunction in aged humans is related with oxidative stress and vascular inflammation. Aging Cell. 2009; 8 (3):226-38. doi: 10.1111/j.1474-9726.2009.00466.x PMID: 19245678.
16. Sun S, Cheng B, Sun PG, Wu XH, Wu QQ, He P. RTEF-1 protects against oxidative damage induced by H2O2 in human umbilical vein endothelial cells through Klotho activation. Exp Biol Med (Maywood). 2015. doi: 10.1177/1535370215587914 PMID: 26041389.
17. Servillo L, D'Onofrio N, Longobardi L, Sirangelo I, Giovane A, Cautela D, et al. Stachydrine ameliorates high-glucose induced endothelial cell senescence and SIRT1 downregulation. Journal of cellular biochemistry. 2013. doi: 10.1002/jcb.24598 PMID: 23744621.
18. Mortuza R, Chen S, Feng B, Sen S, Chakrabarti S. High glucose induced alteration of SIRTs in endothelial cells causes rapid aging in a p300 and FOXO regulated pathway. PloS one. 2013; 8(1):e54514. doi: 10.1371/journal.pone.0054514 PMID: 23342163; PubMed Central PMCID: PMC3546959.
19. Austad SN. Comparative biology of aging. The journals of gerontology Series A, Biological sciences and medical sciences. 2009; 64(2):199-201. doi: 10.1093/gerona/gln060 PMID: 19223603; PubMed Central PMCID: PMC2655036.
20. Suzuki E, Takahashi M, Oba S, Nishimatsu H. Oncogene-and oxidative stress-induced cellular senescence shows distinct expression patterns of proinflammatory cytokines in vascular endothelial cells. TheScientificWorldJournal. 2013; 2013:754735. doi: 10.1155/2013/754735 PMID: 24198727; PubMed Central PMCID: PMC3806413.
21. Steinle JJ, Sharma S, Smith CP, McFayden-Ketchum LS. Normal aging involves modulation of specific inflammatory markers in the rat retina and choroid. The journals of gerontology Series A, Biological sciences and medical sciences. 2009; 64(3):325-31. doi: 10.1093/gerona/gln052 PMID: 19181710; PubMed Central PMCID: PMC2655001.
22. Zhong W, Zou G, Gu J, Zhang J. L-arginine attenuates high glucose-accelerated senescence in human umbilical vein endothelial cells. Diabetes research and clinical practice. 2010; 89(1):38-45. doi:10. 1016/j.diabres.2010.03.013 PMID: 20398956.
23. Zhu Y, Armstrong JL, Tchkonia T, Kirkland JL. Cellular senescence and the senescent secretory phenotype in age-related chronic diseases. Current opinion in clinical nutrition and metabolic care. 2014; 17(4):324-8. doi: 10.1097/MCO.0000000000000065 PMID: 24848532.
24. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature. 2001; 414 (6865):813-20. doi: 10.1038/414813a PMID: 11742414.
25. Farris W, Mansourian S, Chang Y, Lindsley L, Eckman EA, Frosch MP, et al. Insulin-degrading enzyme regulates the levels of insulin, amyloid beta-protein, and the beta-amyloid precursor protein intracellular domain in vivo. Proceedings of the National Academy of Sciences of the United States of America. 2003; 100(7):4162-7. doi: 10.1073/pnas.0230450100 PMID: 12634421; PubMed Central PMCID: PMC153065.
26. Chen S, Khan ZA, Cukiernik M, Chakrabarti S. Differential activation of NF-kappa B and AP-1 in increased fibronectin synthesis in target organs of diabetic complications. American journal of physiology Endocrinology and metabolism. 2003; 284(6):E1089-97. doi: 10.1152/ajpendo.00540.2002 PMID: 12582013.
27. Hanna ME, Taylor CR, Chen B, La HS, Maraj JJ, Kilar CR, et al. Structural Remodeling of Coronary Resistance Arteries: Effects of Age and Exercise Training. Journal of applied physiology. 2014. doi:10. 1152/japplphysiol.01296.2013 PMID: 25059239.
28. Donato AJ, Henson GD, Hart CR, Layec G, Trinity JD, Bramwell RC, et al. The impact of aging on adipose structure, function, and vasculature in the B6D2F1 mouse: Evidence of significant multisystem dysfunction. The Journal of physiology. 2014. doi: 10.1113/jphysiol.2014.274175 PMID: 25038241.
29. Avogaro A, de Kreutzenberg SV, Federici M, Fadini GP. The endothelium abridges insulin resistance to premature aging. Journal of the American Heart Association. 2013; 2(3):e000262. doi: 10.1161/JAHA. 113.000262 PMID: 23917532; PubMed Central PMCID: PMC3698793.
30. Chen J, Brodsky SV, Goligorsky DM, Hampel DJ, Li H, Gross SS, et al. Glycated collagen I induces premature senescence-like phenotypic changes in endothelial cells. Circ Res. 2002; 90(12):1290-8. PMID: 12089067.
31. Badi I, Burba I, Ruggeri C, Zeni F, Bertolotti M, Scopece A, et al. MicroRNA-34a Induces Vascular Smooth Muscle Cells Senescence by SIRT1 Downregulation and Promotes the Expression of Age-Associated Pro-inflammatory Secretory Factors. J Gerontol A Biol Sci Med Sci. 2014. doi: 10.1093/gerona/glu180 PMID: 25352462.
32. Salminen A, Kauppinen A, Kaarniranta K. Emerging role of NF-kappaB signaling in the induction of senescence-associated secretory phenotype (SASP). Cell Signal. 2012; 24(4):835-45. doi: 10.1016/j. cellsig.2011.12.006 PMID: 22182507.
33. Obrosova IG, Drel VR, Oltman CL, Mashtalir N, Tibrewala J, Groves JT, et al. Role of nitrosative stress in early neuropathy and vascular dysfunction in streptozotocin-diabetic rats. American journal of physiology Endocrinology and metabolism. 2007; 293(6):E1645-55. doi: 10.1152/ajpendo.00479.2007 PMID: 17911342.
34. Arora M, Kumar A, Kaundal RK, Sharma SS. Amelioration of neurological and biochemical deficits by peroxynitrite decomposition catalysts in experimental diabetic neuropathy. European journal of pharmacology. 2008; 596(1-3):77-83. doi: 10.1016/j.ejphar.2008.08.003 PMID: 18768138.
35. Pacher P, Obrosova IG, Mabley JG, Szabo C. Role of nitrosative stress and peroxynitrite in the pathogenesis of diabetic complications. Emerging new therapeutical strategies. Current medicinal chemistry. 2005; 12(3):267-75. PMID: 15723618; PubMed Central PMCID: PMC2225483.
36. Lamoke F, Labazi M, Montemari A, Parisi G, Varano M, Bartoli M. Trans-Chalcone prevents VEGF expression and retinal neovascularization in the ischemic retina. Experimental eye research. 2011; 93 (4):350-4. doi: 10.1016/j.exer.2011.02.007 PMID: 21354136.
37. Calabrese V, Cornelius C, Leso V, Trovato-Salinaro A, Ventimiglia B, Cavallaro M, et al. Oxidative stress, glutathione status, sirtuin and cellular stress response in type 2 diabetes. Biochimica et biophysica acta. 2012; 1822(5):729-36. doi: 10.1016/j.bbadis.2011.12.003 PMID: 22186191.
38. Bhayadia R, Schmidt BM, Melk A, Homme M. Senescence-Induced Oxidative Stress Causes Endothelial Dysfunction. J Gerontol A Biol Sci Med Sci. 2015. doi: 10.1093/gerona/glv008 PMID: 25735595.
39. Ben-Porath I, Weinberg RA. The signals and pathways activating cellular senescence. The international journal of biochemistry & cell biology. 2005; 37(5):961-76. doi: 10.1016/j.biocel.2004.10.013 PMID: 15743671.
40. Kokkinopoulos I, Shahabi G, Colman A, Jeffery G. Mature peripheral RPE cells have an intrinsic capacity to proliferate; a potential regulatory mechanism for age-related cell loss. PLoS One. 2011; 6(4): e18921. doi: 10.1371/journal.pone.0018921 PMID: 21526120; PubMed Central PMCID: PMC3081302.
41. Tabuchi T, Satoh M, Itoh T, Nakamura M. MicroRNA-34a regulates the longevity-associated protein SIRT1 in coronary artery disease: effect of statins on SIRT1 and microRNA-34a expression. Clinical science. 2012; 123(3):161-71. doi: 10.1042/CS20110563 PMID: 22364258.
42. Squier TC. Oxidative stress and protein aggregation during biological aging. Experimental gerontology. 2001; 36(9):1539-50. PMID: 11525876.
43. Chen Q, Ames BN. Senescence-like growth arrest induced by hydrogen peroxide in human diploid fibroblast F65 cells. Proceedings of the National Academy of Sciences of the United States of America. 1994; 91(10):4130-4. PMID: 8183882; PubMed Central PMCID: PMC43738.
44. Chen QM, Tu VC, Liu J. Measurements of hydrogen peroxide induced premature senescence: senescence-associated beta-galactosidase and DNA synthesis index in human diploid fibroblasts with downregulated p53 or Rb. Biogerontology. 2000; 1(4):335-9. PMID: 11708215.
45. Zhu K, Kakehi T, Matsumoto M, Iwata K, Ibi M, Ohshima Y, et al. NADPH oxidase NOX1 is involved in activation of protein kinase C and premature senescence in early stage diabetic kidney. Free radical biology & medicine. 2015; 83:21-30. doi: 10.1016/j.freeradbiomed.2015.02.009 PMID: 25701431.
46. Zou H, Stoppani E, Volonte D, Galbiati F. Caveolin-1, cellular senescence and age-related diseases. Mechanisms of ageing and development. 2011; 132(11-12):533-42. doi: 10.1016/j.mad.2011.11.001 PMID: 22100852; PubMed Central PMCID: PMC3243775.
47. Herbert KE, Mistry Y, Hastings R, Poolman T, Niklason L, Williams B. Angiotensin II-mediated oxidative DNA damage accelerates cellular senescence in cultured human vascular smooth muscle cells via telomere-dependent and independent pathways. Circulation research. 2008; 102(2):201-8. doi:10. 1161/CIRCRESAHA.107.158626 PMID: 17991883; PubMed Central PMCID: PMC2861985.
48. Chen Q, Fischer A, Reagan JD, Yan LJ, Ames BN. Oxidative DNA damage and senescence of human diploid fibroblast cells. Proceedings of the National Academy of Sciences of the United States of America. 1995; 92(10):4337-41. PMID: 7753808; PubMed Central PMCID: PMC41939.
49. Frippiat C, Chen QM, Zdanov S, Magalhaes JP, Remacle J, Toussaint O. Subcytotoxic H2O2 stress triggers a release of transforming growth factor-beta 1, which induces biomarkers of cellular senescence of human diploid fibroblasts. The Journal of biological chemistry. 2001; 276(4):2531-7. doi:10. 1074/jbc.M006809200 PMID: 11060295.
50. Robles SJ, Adami GR. Agents that cause DNA double strand breaks lead to p16INK4a enrichment and the premature senescence of normal fibroblasts. Oncogene. 1998; 16(9):1113-23. doi: 10.1038/sj.onc. 1201862 PMID: 9528853.
51. Arend N, Wertheimer C, Laubichler P, Wolf A, Kampik A, Kernt M. Idebenone Prevents Oxidative Stress, Cell Death and Senescence of Retinal Pigment Epithelium Cells by Stabilizing BAX/Bcl-2 Ratio. Ophthalmologica. 2015. doi: 10.1159/000381726 PMID: 26044821.
52. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proceedings of the National Academy of Sciences of the United States of America. 1995; 92(20):9363-7. PMID: 7568133; PubMed Central PMCID: PMC40985.
53. Venkatesh D, Fredette N, Rostama B, Tang Y, Vary CP, Liaw L, et al. RhoA-mediated signaling in Notch-induced senescence-like growth arrest and endothelial barrier dysfunction. Arterioscler Thromb Vasc Biol. 2011; 31(4):876-82. doi: 10.1161/ATVBAHA.110.221945 PMID: 21273559; PubMed Central PMCID: PMC3252819.
54. Hyland P, Barnett C, Pawelec G, Barnett Y. Age-related accumulation of oxidative DNA damage and alterations in levels of p16(INK4a/CDKN2a), p21(WAF1/CIP1/SDI1) and p27(KIP1) in human CD4+ T cell clones in vitro. Mech Ageing Dev. 2001; 122(11):1151-67. PMID: 11389930.
55. Yoshida Y, Hayashi Y, Suda M, Tateno K, Okada S, Moriya J, et al. Notch signaling regulates the lifespan of vascular endothelial cells via a p16-dependent pathway. PloS one. 2014; 9(6):e100359. doi: 10.1371/journal.pone.0100359 PMID: 24950189; PubMed Central PMCID: PMC4065107.
56. Kauppinen A, Suuronen T, Ojala J, Kaarniranta K, Salminen A. Antagonistic crosstalk between NF-kappaB and SIRT1 in the regulation of inflammation and metabolic disorders. Cell Signal. 2013; 25 (10):1939-48. doi: 10.1016/j.cellsig.2013.06.007 PMID: 23770291.
57. Gano LB, Donato AJ, Pasha HM, Hearon CM Jr., Sindler AL, Seals DR. The SIRT1 activator SRT1720 reverses vascular endothelial dysfunction, excessive superoxide production, and inflammation with aging in mice. Am J Physiol Heart Circ Physiol. 2014; 307(12):H1754-63. doi: 10.1152/ajpheart.00377. 2014 PMID: 25326534; PubMed Central PMCID: PMC4269699.
58. Yang H, Zhang W, Pan H, Feldser HG, Lainez E, Miller C, et al. SIRT1 activators suppress inflammatory responses through promotion of p65 deacetylation and inhibition of NF-kappaB activity. PloS one. 2012; 7(9):e46364. doi: 10.1371/journal.pone.0046364 PMID: 23029496; PubMed Central PMCID: PMC3460821.
59. Kubota S, Ozawa Y, Kurihara T, Sasaki M, Yuki K, Miyake S, et al. Roles of AMP-activated protein kinase in diabetes-induced retinal inflammation. Investigative ophthalmology & visual science. 2011; 52(12):9142-8. doi: 10.1167/iovs.11-8041 PMID: 22058332.
60. Rippo MR, Olivieri F, Monsurro V, Prattichizzo F, Albertini MC, Procopio AD. MitomiRs in human inflamm-aging: a hypothesis involving miR-181a, miR-34a and miR-146a. Experimental gerontology. 2014; 56:154-63. doi: 10.1016/j.exger.2014.03.002 PMID: 24607549.
61. Russo F, Di Bella S, Nigita G, Macca V, Lagana A, Giugno R, et al. miRandola: extracellular circulating microRNAs database. PloS one. 2012; 7(10):e47786. doi: 10.1371/journal.pone.0047786 PMID: 23094086; PubMed Central PMCID: PMC3477145.
62. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, Lindenberg JL, et al. Functional delivery of viral miRNAs via exosomes. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107(14):6328-33. doi: 10.1073/pnas.0914843107 PMID: 20304794; PubMed Central PMCID: PMC2851954.
63. Hunten S, Kaller M, Drepper F, Oeljeklaus S, Bonfert T, Erhard F, et al. p53-regulated networks of protein, mRNA, miRNA and lncRNA expression revealed by integrated pSILAC and NGS analyses. Mol Cell Proteomics. 2015. doi: 10.1074/mcp.M115.050237 PMID: 26183718.
64. Adams T, Shahabi G, Hoh-Kam J, Jeffery G. Held under arrest: Many mature albino RPE cells display polyploidal features consistent with abnormal cell cycle retention. Exp Eye Res. 2010; 90(2):368-72. doi: 10.1016/j.exer.2009.10.002 PMID: 19833124.
65. Al-Hussaini H, Kam JH, Vugler A, Semo M, Jeffery G. Mature retinal pigment epithelium cells are retained in the cell cycle and proliferate in vivo. Mol Vis. 2008; 14:1784-91. PMID: 18843376; PubMed Central PMCID: PMC2562424.