Altered circulating mitochondrial DNA and increased inflammation in patients with diabetic retinopathy

Diabetes Research and Clinical Practice

Volumn 110, Issue 3, 2015, Pages 257-265

  Malik, Afshan N ^a   Parsade, Chandani K ^a   Ajaz, Saima ^a   Crosby Nwaobi, Roxanne ^b   Gnudi, Luigi ^a   Czajka, Anna ^a   Sivaprasad, Sobha ^b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Diabetic retinopathy; Inflammation; Mitochondrial DNA

Indexed keywords

ALBUMIN; CREATININE; GLUCOSE; HEMOGLOBIN A1C; INSULIN; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; MITOCHONDRIAL DNA; ORAL ANTIDIABETIC AGENT; TUMOR NECROSIS FACTOR ALPHA; IL4 PROTEIN, HUMAN;

ADULT; AFRICAN; AGED; ARTICLE; ASIAN; CAUCASIAN; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DIABETIC DIET; DIABETIC RETINOPATHY; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE DURATION; DISEASE SEVERITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA CONTENT; DNA DAMAGE; FEMALE; GENE DOSAGE; GENOME; HUMAN; HYPERGLYCEMIA; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; MAJOR CLINICAL STUDY; MALE; MITOCHONDRIAL GENOME; NON INSULIN DEPENDENT DIABETES MELLITUS; NUCLEAR GENOME; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; VERY ELDERLY; BLOOD; COMPLICATION; COPY NUMBER VARIATION; MIDDLE AGED; RISK FACTOR;

ADULT; AGED; AGED, 80 AND OVER; CROSS-SECTIONAL STUDIES; DIABETES MELLITUS, TYPE 2; DIABETIC RETINOPATHY; DISEASE PROGRESSION; DNA COPY NUMBER VARIATIONS; DNA DAMAGE; DNA, MITOCHONDRIAL; FEMALE; HUMANS; HYPERGLYCEMIA; INFLAMMATION; INTERLEUKIN-4; MALE; MIDDLE AGED; RISK FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84955216075     PISSN: 01688227     EISSN: 18728227     Source Type: Journal    
DOI: 10.1016/j.diabres.2015.10.006     Document Type: Article

References (49)

1. Yau J.W., Rogers S.L., Kawasaki R., Lamoureux E.L., Kowalski J.W., Bek T., et al. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care 2012, 35(March (3)):556-564.
2. Klein R., Klein B.E., Moss S.E., Davis M.D., DeMets D.L. The Wisconsin epidemiologic study of diabetic retinopathy III. Prevalence and risk of diabetic retinopathy when age at diagnosis is 30 or more years. Arch Ophthalmol 1984, 102(April (4)):527-532.
3. Guariguata L., Whiting D.R., Hambleton I., Beagley J., Linnenkamp U., Shaw J.E. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract 2014, 103(2):137-149.
4. Antonetti D.A., Barber A.J., Bronson S.K., Freeman W.M., Gardner T.W., Jefferson L.S., et al. Diabetic retinopathy: seeing beyond glucose-induced microvascular disease. Diabetes 2006, 55(September (9)):2401-2411.
5. Giacco F., Brownlee M. Oxidative stress and diabetic complications. Circ Res 2010, 107(October (9)):1058-1070.
6. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N Engl J Med 1993, 329(September (14)):977-986.
7. Kowluru R.A., Chan P.S. Oxidative stress and diabetic retinopathy. Exp Diabetes Res 2007, 2007:43603.
8. Madsen-Bouterse S.A., Zhong Q., Mohammad G., Ho Y.S., Kowluru R.A. Oxidative damage of mitochondrial DNA in diabetes and its protection by manganese superoxide dismutase. Free Radic Res 2010, 44(March (3)):313-321.
9. Chan P.S.1, Kanwar M., Kowluru R.A. Resistance of retinal inflammatory mediators to suppress after reinstitution of good glycemic control: novel mechanism for metabolic memory. J Diabetes Complicat 2010, 24(January-February (1)):55-63.
10. Xie L., Zhu X., Hu Y., Li T., Gao Y., Shi Y., et al. Mitochondrial DNA oxidative damage triggering mitochondrial dysfunction and apoptosis in high glucose-induced HRECs. Investig Ophthalmol Vis Sci 2008, 49(September (9)):4203-4209.
11. Madsen-Bouterse S.A., Mohammad G., Kanwar M., Kowluru R.A. Role of mitochondrial DNA damage in the development of diabetic retinopathy, and the metabolic memory phenomenon associated with its progression. Antioxid Redox Signal 2010, 13(September (6)):797-805.
12. Kanwar M., Chan P.S., Kern T.S., Kowluru R.A. Oxidative damage in the retinal mitochondria of diabetic mice: possible protection by superoxide dismutase. Investig Ophthalmol Vis Sci 2007, 48(August (8)):3805-3811.
13. Czajka A., Ajaz S., Gnudi L., Parsade C.K., Jones P., Reid F., et al. Altered mitochondrial function, mitochondrial DNA and reduced metabolic flexibility in patients with diabetic nephropathy. EBioMedicine 2015.
14. Malik A.N., Czajka A. Is mitochondrial DNA content a potential biomarker of mitochondrial dysfunction?. Mitochondrion 2012.
15. Jawa A., Kcomt J., Fonseca V.A. Diabetic nephropathy and retinopathy. Med Clin North Am 2004, 88(July (4)):1001-1036.
16. Collins L.V., Hajizadeh S., Holme E., Jonsson I.M., Tarkowski A. Endogenously oxidized mitochondrial DNA induces in vivo and in vitro inflammatory responses. J Leukoc Biol 2004, 75(June (6)):995-1000.
17. Oka T., Hikoso S., Yamaguchi O., Taneike M., Takeda T., Tamai T., et al. Mitochondrial DNA that escapes from autophagy causes inflammation and heart failure. Nature 2012, 485(May (7397)):251-255.
18. Adamis A.P. Is diabetic retinopathy an inflammatory disease?. Br J Ophthalmol 2002, 86(April (4)):363-365.
19. Tang J., Kern T.S. Inflammation in diabetic retinopathy. Prog Retin Eye Res 2011, 30(September (5)):343-358.
20. Grading diabetic retinopathy from stereoscopic color fundus photographs - an extension of the modified Airlie House classification. ETDRS report number 10. Early Treatment Diabetic Retinopathy Study Research Group. Ophthalmology 1991, 98(May (5 Suppl)):786-806.
21. Stoves J., Lindley E.J., Barnfield M.C., Burniston M.T., Newstead C.G. MDRD equation estimates of glomerular filtration rate in potential living kidney donors and renal transplant recipients with impaired graft function. Nephrol Dial Transplant 2002, 17(November (11)):2036-2037.
22. Malik A.N., Shahni R., Rodriguez-de-Ledesma A., Laftah A., Cunningham P. Mitochondrial DNA as a non-invasive biomarker: accurate quantification using real time quantitative PCR without co-amplification of pseudogenes and dilution bias. Biochem Biophys Res Commun 2011, 412(August (1)):1-7.
23. Ajaz S., Czajka A., Malik A.N. Accurate measurement of circulating mitochondrial DNA content from human blood samples using real-time quantitative PCR. Methods Mol Biol 2014, 1264.
24. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 2009, 55(April (4)):611-622.
25. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25(December (4)):402-408.
26. Furda A., Santos J.H., Meyer J.N., Van Houten B. Quantitative PCR-based measurement of nuclear and mitochondrial DNA damage and repair in mammalian cells. Methods Mol Biol 2014, 1105:419-437.
27. Hunter S.E., Jung D., Di Giulio R.T., Meyer J.N. The QPCR assay for analysis of mitochondrial DNA damage, repair, and relative copy number. Methods 2010, 51(August (4)):444-451.
28. Effect of intensive diabetes treatment on the development and progression of long-term complications in adolescents with insulin-dependent diabetes mellitus: Diabetes Control and Complications Trial. Diabetes Control and Complications Trial Research Group. J Pediatr 1994, 125(August (2)):177-188.
29. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes F (UKPDS. 33). UK Prospective Diabetes Study (UKPDS) Group. Lancet 1998, 352(September (9131)):837-853.
30. Chen Y.H., Chen H.S., Tarng D.C. More impact of microalbuminuria on retinopathy than moderately reduced GFR among type 2 diabetic patients. Diabetes Care 2012, 35(April (4)):803-808.
31. Tewari S., Santos J.M., Kowluru R.A. Damaged mitochondrial DNA replication system and the development of diabetic retinopathy. Antioxid Redox Signal 2012, 17(August (3)):492-504.
32. Santos J.M., Mishra M., Kowluru R.A. Posttranslational modification of mitochondrial transcription factor A in impaired mitochondria biogenesis: implications in diabetic retinopathy and metabolic memory phenomenon. Exp Eye Res 2014, 121:168-177.
33. Santos J.M., Tewari S., Lin J.Y., Kowluru R.A. Interrelationship between activation of matrix metalloproteinases and mitochondrial dysfunction in the development of diabetic retinopathy. Biochem Biophys Res Commun 2013, 438(September (4)):760-764.
34. Scheffler I.E. Drug-Induced mitochondria dysfunction. Basic molecular biology of mitochondrial replication 2008, John Willey & Sons Inc., New Jersey. J.A. Dykens, Y. Will (Eds.).
35. Falkenberg M., Larsson N.G., Gustafsson C.M. DNA replication and transcription in mammalian mitochondria. Annu Rev Biochem 2007, 76:679-699.
36. Bannwarth S., Procaccio V., Paquis-Flucklinger V. Rapid identification of unknown heteroplasmic mutations across the entire human mitochondrial genome with mismatch-specific Surveyor Nuclease. Nat Protoc 2006, 1(4):2037-2047.
37. Wong-Riley M T.T. Energy metabolism of the visual system. Eye Brain 2010, 2:99-116.
38. West A.P., Khoury-Hanold W., Staron M., Tal M.C., Pineda C.M., Lang S.M., et al. Mitochondrial DNA stress primes the antiviral innate immune response. Nature 2015.
39. Mohr S., Liew C.C. The peripheral-blood transcriptome: new insights into disease and risk assessment. Trends Mol Med 2007, 13(October (10)):422-432.
40. Lunnon K., Ibrahim Z., Proitsi P., Lourdusamy A., Newhouse S., Sattlecker M., et al. Mitochondrial dysfunction and immune activation are detectable in early Alzheimer's disease blood. J Alzheimers Dis 2012, 30(3):685-710.
41. Rudkowska I., Raymond C., Ponton A., Jacques H., Lavigne C., Holub B.J., et al. Validation of the use of peripheral blood mononuclear cells as surrogate model for skeletal muscle tissue in nutrigenomic studies. Omics 2011, 15(January-February (1-2)):1-7.
42. Choudhuri S., Mandal L.K., Paine S.K., Sen A., Dutta D., Chowdhury I.H., et al. Role of hyperglycemia-mediated erythrocyte redox state alteration in the development of diabetic retinopathy. Retina 2013, 33(January (1)):207-216.
43. Holmstrom M.H., Iglesias-Gutierrez E., Zierath J.R., Garcia-Roves P.M. Tissue-specific control of mitochondrial respiration in obesity-related insulin resistance and diabetes. Am J Physiol Endocrinol Metab 2012, 302(March (6)):E731-E739.
44. Khurana R.N., Parikh J.G., Saraswathy S., Wu G.S., Rao N.A. Mitochondrial oxidative DNA damage in experimental autoimmune uveitis. Investig Ophthalmol Vis Sci 2008, 49(August (8)):3299-3304.
45. Romeo G., Liu W.H., Asnaghi V., Kern T.S., Lorenzi M. Activation of nuclear factor-kappaB induced by diabetes and high glucose regulates a proapoptotic program in retinal pericytes. Diabetes 2002, 51(July (7)):2241-2248.
46. Kowluru R.A., Koppolu P., Chakrabarti S., Chen S. Diabetes-induced activation of nuclear transcriptional factor in the retina, and its inhibition by antioxidants. Free Radic Res 2003, 37(November (11)):1169-1180.
47. Preciado-Puga M.C., Malacara J.M., Fajardo-Araujo M.E., Wröbel K., Wröbel K., Kornhauser-Araujo C., et al. Markers of the progression of complications in patients with type 2 diabetes: a one-year longitudinal study. Exp Clin Endocrinol Diabetes 2014, 122(September (8)):484-490.
48. Cunha-Vaz J.G. Studies on the pathophysiology of diabetic retinopathy. The blood-retinal barrier in diabetes. Diabetes 1983, 32(May (Suppl. 2)):20-27.
49. Sakon S., Xue X., Takekawa M., Sasazuki T., Okazaki T., Kojima Y., et al. NF-kappaB inhibits TNF-induced accumulation of ROS that mediate prolonged MAPK activation and necrotic cell death. Embo J 2003, 22(August (15)):3898-3909.