The 4a/4a genotype of the VNTR polymorphism for endothelial nitric oxide synthase (eNOS) gene predicts risk for proliferative diabetic retinopathy in Slovenian patients (Caucasians) with type 2 diabetes mellitus

Molecular Biology Reports

Volumn 39, Issue 6, 2012, Pages 7061-7067

  Cilenšek, Ines ^a   Mankoč, Sara ^a   Petrovič, Mojca Globočnik ^b   Petrovič, Daniel ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b UNIVERSITY MEDICAL CENTRE LJUBLJANA   (Slovenia)

Author keywords

Endothelial nitric oxide synthase; Polymorphism; Proliferative diabetic retinopathy; Type 2 diabetes

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE;

AGED; ARTICLE; CASE CONTROL STUDY; CAUCASIAN; CLINICAL FEATURE; CONTROLLED STUDY; DIABETIC RETINOPATHY; DISEASE ACTIVITY; DISEASE ASSOCIATION; ENDOTHELIAL NITRIC OXIDE SYNTHASE GENE; FEMALE; GENE; GENE FREQUENCY; GENETIC POLYMORPHISM; GENETIC RISK; GENOTYPE PHENOTYPE CORRELATION; GENOTYPING TECHNIQUE; HUMAN; MAJOR CLINICAL STUDY; MALE; MOLECULAR PATHOLOGY; NON INSULIN DEPENDENT DIABETES MELLITUS; PREDICTION; REAL TIME POLYMERASE CHAIN REACTION; RISK ASSESSMENT; RISK FACTOR; VARIABLE NUMBER OF TANDEM REPEAT;

AGED; CASE-CONTROL STUDIES; DIABETES MELLITUS, TYPE 2; DIABETIC RETINOPATHY; EUROPEAN CONTINENTAL ANCESTRY GROUP; FEMALE; GENE FREQUENCY; GENES, RECESSIVE; GENETIC ASSOCIATION STUDIES; GENOTYPE; HUMANS; LOGISTIC MODELS; MALE; MIDDLE AGED; MINISATELLITE REPEATS; MODELS, GENETIC; NITRIC OXIDE SYNTHASE TYPE III; ODDS RATIO; RISK FACTORS; SLOVENIA;

EID: 84864280375     PISSN: 03014851     EISSN: 15734978     Source Type: Journal    
DOI: 10.1007/s11033-012-1537-8     Document Type: Article

References (49)

1. Doganay S, Everklioglu C, Er H et al (2002) Comparison of serum NO, TNF-a, IL-1b, sil-2R, IL-6 and IL-8 levels with grades of retinopathy in patients with diabetes mellitus. Eye 16:163-170 (Pubitemid 34537693)
2. El-Asrar AM, Struyf S, Opdenakker G, Van Damme J, Geboes K (2010) Expression of stem cell factor/c-kit signalling pathway components in diabetic fibrovascular epiretinal membranes. Mol Vis 16:1098-1107
3. Hallman DM, Huber JC, Gonzalez VH, Klein BE, Klein R, Hanis CL (2005) Familial aggregation of severity of diabetic retinopa-thy in Mexican Americans from Starr county, Texas. Diabetes Care 28:1163-1168 (Pubitemid 40616629)
4. Rema M, Saravanan G, Deepa R, Mohan V (2002) Familial clustering of diabetic retinopathy in south Indian type 2 diabetic patients. Diabetes Med 19:910-916 (Pubitemid 35356916)
5. Warpeha KM, Charkravarthy U (2003) Molecular genetics of diabetic retinopathy. Eye 17:305-311
6. Balasubbu S, Rajendran A, Ramasamy K, Namperumalsamy P, Sundaresan P (2006) Emerging patterns of possible potential candidate gene polymorphisms associated with diabetic retinop-athy-a. Asian J Exp Sci 20:15-28
7. Ng DPK (2010) Human genetics of diabetic retinopathy: current perspectives. J Ophthalmol 2010:1-6
8. Patel S, Chen H, Tinkham NH, Zhankg K (2008) Genetic susceptibility of diabetic retinopathy. Curr Diabetes Rep 8:257-262
9. McVeigh GE, Brennan GM, Johnston GD et al (1992) Impaired endothelial-dependent and independent vasodilatation in patients with type 2 (non-insulin dependent) diabetes mellitus. Diabeto-logia 35:771-776
10. Moncada S, Higgs EA (2006) The discovery of nitric oxide and its role in vascular biology. Br J Pharmacol 147:S193-S201 (Pubitemid 43077277)
11. Yang Y, Hayden MR, Sowers S, Bagree SV, Sowers JR (2010) Retinal redox stress and remodeling in cardiometabolic syndrome and diabetes. Oxid Med Cell Longev 3:392-403
12. Toda N, Nakanishi-Toda M (2007) Nitric oxide: ocular blood flow, glaucoma, and diabetic retinopathy. Prog Retin Eye Res 26:205-238 (Pubitemid 46498800)
13. Alderton WK, Cooper CE, Knowles RG (2001) Nitric oxide synthases: structure, function and inhibition. Biochem J 357: 593-615 (Pubitemid 32735142)
14. Miyamoto Y, Saito Y, Nakayama M et al (2000) Replication protein A1 reduces transcription of the endothelial nitric oxide synthase gene containing a-786T ? C mutation associated with coronary spastic angina. Hum Mol Genet 9:2629-2637
15. Asif AR, Oellerich M, Armstrong VW, Hecker M, Cattaruzza M (2009) T-786C polymorphism of the NOS-3 gene and the endo-thelial cell response to fluid shear stress-a proteome analysis. J Proteome Res 8:3161-3168
16. Farbstein D, Levy AP (2010) The genetics of vascular complications in diabetes mellitus. Cardiol Clin 28:477-496
17. Bank N, Aynedijan HS (1993) Role of EDRF (nitric oxide) in diabetic renal hyperfiltration. Kidney Int 43:1306-1312 (Pubitemid 23161417)
18. Fairchild TA, Fulton D, Fontana JT, Gratton JP, McCabe TJ, Sessa WC (2001) Acidic hydrolysis as a mechanism for the cleavage of the Glu298Asp variant of human endothelial nitric oxide synthase. J Biol Chem 276:26674-26679
19. Tesauro M, Thompson WC, Rogliani P, Qi L, Chaudhary PP, Moss J (2000) Intracellular processing of endothelial nitric oxide synthase isoforms associated with differences in severity of car-diopulmonary diseases: cleavage of proteins with aspartate vs. glutamate at position 298. Proc Natl Acad Sci USA 97:2832-2835 (Pubitemid 30159257)
20. Pulkkinen A, Viitanen L, Kareinen A, Lehto S, Vauhkonen I, Laakso M (2000) Intron 4 polymorphism of the endothelial nitric oxide synthase gene is associated with elevated blood pressure in type 2 diabetic patients with coronary heart disease. J Mol Med 78:372-379
21. Casas JP, Bautista LE, Humphries SE, Hingorani AD (2004) Endothelial nitric oxide synthase genotype and ischemic heart disease: meta-analysis of 26 studies involving 23, 028 subjects. Circulation 109:1359-1365 (Pubitemid 38387821)
22. Rao S, Austin H, Davidoff MN, Zafari AM (2005) Endothelial nitric oxide synthase intron 4 polymorphism is a marker for coronary artery disease in African-American and Caucasian men. Ethn Dis 15:191-197 (Pubitemid 40561636)
23. Neugebauer S, Baba T, Watanabe T (2000) Association of the nitric oxide synthase gene polymorphism with an increased risk for progression to diabetic nephropathy in type 2 diabetes. Diabetes 49:500-503 (Pubitemid 30131798)
24. Taverna MJ, Sola A, Guyot-Argenton C et al (2002) eNOS4 polymorphism of the endothelial nitric oxide synthase predicts risk for severe diabetic retinopathy. Diabetes Med 19:240-245 (Pubitemid 34429656)
25. Awata T, Neda T, Iizuka H et al (2004) Endothelial nitric oxide synthase gene is associated with diabetic macular edema in type two diabetes. Diabetes Care 27:2184-2190 (Pubitemid 39167183)
26. Chen Y, Huang H, Zhou J et al (2007) Polymorphism of the endothelial nitric oxide synthase gene is associated with diabetic retinopathy in a cohort of west Africans. Mol Vis 13:2142-2147 (Pubitemid 350200388)
27. Ezzidi I, Mtiraoui N, Mohamed MBH, Mahjoub T, Kacem M, Almawi WY (2007) Endothelial nitric oxide synthase Glu298Asp, 4b/a, and T-786C polymorphisms in type 2 diabetic retinopathy. Clin Endocrinol 68:542-546
28. Frost D, Chitu J, Meyer M, Beischer W, Pfohl M (2003) Endo-thelial nitric oxide synthase (ecNOS) 4 a/b gene polymorphism and carotid artery intima-media thickness in type-1 diabetic patients. Exp Clin Endocrinol Diabetes 111:12-15 (Pubitemid 36336810)
29. de Syllos RWC, Sandrim VC, Lisboa HRK, Tres GS, Tanus-Santos JE (2006) Endothelial nitric oxide synthase genotype and haplotype are not associated with diabetic retinopathy in diabetes type 2 patients. Nitric Oxide 15:417-422 (Pubitemid 44649283)
30. Suganthalakshmi B, Anand R, Kim R et al (2006) Association of VEGF and eNOS gene polymorphisms in type 2 diabetic reti-nopathy. Mol Vis 12:336-341
31. Abhary S, Hewitt AW, Burdon KP, Craig JE (2009) A systemic meta-analysis of genetic association studies for diabetic retinop-athy. Diabetes 58:2137-2147
32. Li H, Louey JWC, Choy KW et al (2008) EDN1 Lys198Asn is associated with diabetic retinopathy in type 2 diabetes. Mol Vis 14:1698-1704
33. Uthra S, Raman R, Mukesh BN et al (2007) Intron 4 VNTR of endothelial nitric oxide synthase (eNOS) gene and diabetic reti-nopathy in type 2 patients in southern India. Ophthalmic Genet 28:77-81 (Pubitemid 46904764)
34. The expert committee on the diagnosis and classification of diabetes mellitus (2003). Reportofthe expert committeeonthe diagnosis and classification of diabetes mellitus. Diabetes Care 26:S5-S20
35. Early treatment diabetic retinopathy study research group (1991) Grading diabetic retinopathy from stereoscopic colour fundus photographs-an extension of the modified Airlie house classification ETDRS report number 10. Ophthalmology 98:786-806
36. Wang XL, Sim AS, Badenhop RF, McCredie RM, Wilcken DE (1996) A smoking-dependent risk of coronary artery disease associated with a polymorphism of the endothelial nitric oxide synthase gene. Nature Med 2:41-45 (Pubitemid 26028071)
37. Elston RC, Forthofer R (1977) Testing for Hardy-Weinberg equilibrium in small samples. Biometrics 33:536-542 (Pubitemid 8194085)
38. Kalinowski ST (2006) Hw-QuickCheck: an easy-to-use computer program for checking genotypes for agreement with Hardy-Weinberg expectations. Mol Ecol Notes 6:974-979 (Pubitemid 44807918)
39. Purcell S, Neale B, Todd-Brown K et al (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559-575 (Pubitemid 47330214)
40. Dupont WD, Plummer WD (1997) PS power and sample size program available for free on the Internet. Control Clin Trials 18:274
41. Ahluwalia TS, Ahuja M, Rai TS et al (2008) Endothelial nitric oxide synthase gene haplotypes and diabetic nephropathy among Asian Indians. Mol Cell Biochem 314:9-17
42. Asakimori Y, Yorioka N, Yamamoto I et al (2001) Endothelial nitric oxide synthase intron 4 polymorphism influences the progression of renal disease. Nephron 89:219-223 (Pubitemid 32830613)
43. Zanchi A, Moczulski DK, Hanna LS, Wantman M, Warram JH, Krolewski AS (2000) Risk of advanced diabetic nephropathy in type 1 diabetes is associated with endothelial nitric oxide syn-thase gene polymorphism. Kidney Int 57:405-413 (Pubitemid 30430632)
44. White NH, Sun W, Cleary PA et al (2009) Prolonged effect of intensive therapy on the risk of retinopathy complications in patients with type 1 diabetes mellitus: 10 years after the diabetes control and complications trial. Arch Ophthalmol 126:1707-1715
45. Nakamura S, Iwasaki N, Funatsu H, Kitano S, Iwamoto Y (2009) Impact of variants in the VEGF gene on progression of prolif-erative diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 247:21-26
46. Stratton IM, Kohner EM, Aldington SJ et al (2001) UKPDS 50: risk factors for incidence and progression of retinopathy in type II diabetes over 6 years from diagnosis. Diabetologia 44:156
47. Esser C, Tomiuk J (2005) Reporting Hardy-Weinberg tests in case-control studies: reasons for caution but not for panic reactions. J Invest Dermatol 124:1082-1083 (Pubitemid 40629116)
48. Wang J, Dudley D, Wang XL (2002) Haplotype-specific effects on endothelial NO synthase promoter efficiency: modifiable by cigarette smoking. Arterioscler Thromb Vasc Biol 22:e1-e4
49. Nakayama M, Yasue H, Yoshimura M et al (1999) T-786-C mutation in the 5′-flanking region of the endothelial nitric oxide synthase gene is associated with coronary spasm. Circulation 99:2864-2870 (Pubitemid 29258973)