Endothelial nitric oxide synthase gene polymorphisms and diabetic nephropathy: A HuGE review and meta-analysis

Genetics in Medicine

Volumn 11, Issue 10, 2009, Pages 695-706

  Zintzaras, Elias ^a,b   Papathanasiou, Afroditi A ^a   Stefanidis, Ioannis ^c  

^a UNIVERSITY OF THESSALY   (Greece)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY HOSPITAL OF LARISSA   (Greece)

Author keywords

4b a; Diabetes; Diabetic nephropathy; ENOS; G894T; Genetic epidemiology; Meta analysis; NOS3; Polymorphism; T786C

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE;

ASIAN; DIABETIC NEPHROPATHY; DISEASE SEVERITY; FAMILY; GENETIC ASSOCIATION; GENETIC HETEROGENEITY; GENETIC LINKAGE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOME; GENOTYPE; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; NON INSULIN DEPENDENT DIABETES MELLITUS; REVIEW; SYSTEMATIC REVIEW;

DIABETES MELLITUS, TYPE 2; DIABETIC NEPHROPATHIES; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; LINKAGE (GENETICS); NITRIC OXIDE SYNTHASE TYPE III; POLYMORPHISM, GENETIC;

EID: 70350222355     PISSN: 10983600     EISSN: None     Source Type: Journal    
DOI: 10.1097/GIM.0b013e3181b2046b     Document Type: Review

References (79)

1. Moncada S, Higgs EA. The discovery of nitric oxide and its role in vascular biology. Br J Pharmacol 2006;147(suppl 1):S193-S201.
2. Wang Y, Kikuchi S, Suzuki H, Nagase S, Koyama A. Endothelial nitric oxide synthase gene polymorphism in intron 4 affects the progression of renal failure in non-diabetic renal diseases. Nephrol Dial Transplant 1999; 14:2898-2902.
3. Noiri E, Satoh H, Taguchi J, et al. Association of eNOS Glu298Asp polymorphism with end-stage renal disease. Hypertension 2002;40:535-540.
4. Zanchi A, Moczulski DK, Hanna LS, Wantman M, Warram JH, Krolewski AS. Risk of advanced diabetic nephropathy in type 1 diabetes is associated with endothelial nitric oxide synthase gene polymorphism. Kidney Int 2000; 57:405-413.
5. Ezzidi I, Mtiraoui N, Mohamed MB, Mahjoub T, Kacem M, Almawi WY. Association of endothelial nitric oxide synthase Glu298Asp, 4b/a, and-786T<C gene variants with diabetic nephropathy. J Diabetes Complications 2008;22:331-338.
6. Ahluwalia TS, Ahuja M, Rai TS, et al. Endothelial nitric oxide synthase gene haplotypes and diabetic nephropathy among Asian Indians. Mol Cell Bio-chem 2008;314:9-17.
7. Yoshimura M, Yasue H, Nakayama M, et al. A missense Glu298Asp variant in the endothelial nitric oxide synthase gene is associated with coronary spasm in the Japanese. Hum Genet 1998;103:65-69. (Pubitemid 28398388)
8. Nakayama M, Yasue H, Yoshimura M, et al. T-786->C mutation in the 5'-flanking region of the endothelial nitric oxide synthase gene is associated with coronary spasm. Circulation 1999;99:2864-2870.
9. Wang XL, Wang J. Endothelial nitric oxide synthase gene sequence variations and vascular disease. Mol Genet Metab 2000;70:241-251.
10. Zintzaras E, Kitsios G, Stefanidis I. Endothelial NO synthase gene polymorphisms and hypertension: a meta-analysis. Hypertension 2006;48:700-710.
11. Thomas GD, Zhang W, Victor RG. Nitric oxide deficiency as a cause of clinical hypertension: promising new drug targets for refractory hypertension. JAMA 2001;285:2055-2057.
12. Wang XL, Sim AS, Badenhop RF, McCredie RM, WilckenDE. A smoking-dependent risk of coronary artery disease associated with a polymorphism of the endothelial nitric oxide synthase gene. Nat Med 1996;2:41-45.
13. Asakimori Y, Yorioka N, Taniguchi Y, et al. T(-786)-C polymorphism of the endothelial nitric oxide synthase gene influences the progression of renal disease. Nephron 2002;91:747-751.
14. Gross JL, de Azevedo MJ, Silveiro SP, Canani LH, Caramori ML, Zelmano-vitz T. Diabetic nephropathy: diagnosis, prevention, and treatment. Diabetes Care 2005;28:164-176.
15. Adler AI, Stevens RJ, Manley SE, Bilous RW, Cull CA, Holman RR. Development and progression of nephropathy in type 2 diabetes: the United Kingdom Prospective Diabetes Study (UKPDS 64). Kidney Int 2003;63: 225-232.
16. Newman DJ, Mattock MB, Dawnay AB, et al. Systematic review on urine albumin testing for early detection of diabetic complications. Health Technol Assess 2005;9:iii-vi,
17. Krolewski AS, Warram JH, Christlieb AR, Busick EJ, Kahn CR. The changing natural history of nephropathy in type I diabetes. Am J Med 1985;78:785-794.
18. Shpichinetsky V, Raz I, Friedlander Y, et al. The association between two common mutations C677T and A1298C in human methylenetetrahydrofo-late reductase gene and the risk for diabetic nephropathy in type II diabetic patients. J Nutr 2000;130:2493-2497.
19. Borch-Johnsen K, Norgaard K, Hommel E, et al. Is diabetic nephropathy an inherited complication? Kidney Int 1992;41:719-722.
20. Quinn M, Angelico MC, Warram JH, Krolewski AS. Familial factors determine the development of diabetic nephropathy in patients with IDDM. Diabetologia 1996;39:940-945.
21. Strojek K, Grzeszczak W, Morawin E, et al. Nephropathy of type II diabetes: evidence for hereditary factors? Kidney Int 1997;51:1602-1607.
22. Zintzaras E, Stefanidis I. Association between the GLUT1 gene polymorphism and the risk of diabetic nephropathy: a meta-analysis. J Hum Genet 2005;50:84-91.
23. Zintzaras E, Uhlig K, Koukoulis GN, Papathanasiou AA, Stefanidis I. Methylenetetrahydrofolate reductase gene polymorphism as a risk factor for diabetic nephropathy: a meta-analysis. J Hum Genet 2007;52:881-890.
24. Freedman BI, Bostrom M, Daeihagh P, Bowden DW. Genetic factors in diabetic nephropathy. Clin J Am Soc Nephrol 2007;2:1306-1316.
25. Zintzaras E, Lau J. Synthesis of genetic association studies for pertinent gene-disease associations requires appropriate methodological and statistical approaches. J Clin Epidemiol 2008;61:634-645.
26. Zintzaras E, Lau J. Trends in meta-analysis of genetic association studies. J Hum Genet 2008;53:1-9.
27. Trikalinos TA, Salanti G, Zintzaras E, Ioannidis JP. Meta-analysis methods. Adv Genet 2008;60:311-334.
28. Lau J, Antman EM, Jimenez-Silva J, Kupelnick B, Mosteller F, Chalmers TC. Cumulative meta-analysis of therapeutic trials for myocardial infarction. N Engl J Med 1992;327:248-254.
29. Frosst P, Blom HJ, Milos R, et al. A candidate genetic risk factor for vascular disease: a common mutation in methylenetetrahydrofolate reductase. Nat Genet 1995;10:111-113.
30. Minelli C, Thompson JR, Abrams KR, Thakkinstian A, Attia J. The choice of a genetic model in the meta-analysis of molecular association studies. Int J Epidemiol 2005;34:1319-1328.
31. Falconer DS. Introduction to quantitative genetics. 3rd ed. New York, NY: Longman Scientific & Technical, 1989.
32. Cochran W. The combination of estimates from different experiments. Biometrics 1954;10:101-129.
33. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002;21:1539-1558.
34. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986;7:177-188.
35. Harbord RM, Egger M, Sterne JA. A modified test for small-study effects in meta-analyses of controlled trials with binary endpoints. Stat Med 2006;25: 3443-3457.
36. Weir B. Genetic data analysis ii: methods for discrete population genetic data. Sunderland, MA: Sinauer Associates, 1996.
37. Zintzaras E, Hadjigeorgiou GM. The role of G196A polymorphism in the brain-derived neurotrophic factor gene in the cause of Parkinson's disease: a meta-analysis. J Hum Genet 2005;50:560-566.
38. Thaha M, Pranawa, Yogiantoro M, et al. Association of endothelial nitric oxide synthase Glu298Asp polymorphism with end-stage renal disease. Clin Nephrol 2008;70:144-154.
39. Bellini MH, Figueira MN, Piccoli MF, et al. Association of endothelial nitric oxide synthase gene intron 4 polymorphism with end-stage renal disease. Nephrology (Carlton) 2007;12:289-293.
40. Mollsten A, Wessman M, Svensson M, et al. Glu298Asp and NOS4ab polymorphisms in diabetic nephropathy. Ann Med 2006;38:522-528.
41. Lamnissou K, Zirogiannis P, Trygonis S, et al. Evidence for association of endothelial cell nitric oxide synthase gene polymorphism with earlier progression to end-stage renal disease in a cohort of Hellens from Greece and Cyprus. Genet Test 2004;8:319-324.
42. Shin Shin Y, Baek SH, Chang KY, et al. Relations between eNOS Glu298Asp polymorphism and progression of diabetic nephropathy. Diabetes Res Clin Pract 2004;65:257-265.
43. Buraczynska M, Ksiazek P, Zaluska W, Nowicka T, Ksiazek A. Endothelial nitric oxide synthase gene intron 4 polymorphism in patients with end-stage renal disease. Nephrol Dial Transplant 2004;19:2302-2306.
44. Nagase S, Suzuki H, Wang Y, et al. Association of ecNOS gene polymorphisms with end stage renal diseases. Mol Cell Biochem 2003;244:113-118.
45. Rippin JD, Patel A, Belyaev ND, Gill GV, Barnett AH, Bain SC. Nitric oxide synthase gene polymorphisms and diabetic nephropathy. Diabetologia 2003;46:426-428.
46. Shimizu T, Onuma T, Kawamori R, Makita Y, Tomino Y. Endothelial nitric oxide synthase gene and the development of diabetic nephropathy. Diabetes Res Clin Pract 2002;58:179-185.
47. Lin S, Qu H, Qiu M. Allele A in intron 4 of ecNOS gene will not increase the risk of diabetic nephropathy in type 2 diabetes of Chinese population. Nephron 2002;91:768.
48. Asakimori Y, Yorioka N, Yamamoto I, et al. Endothelial nitric oxide synthase intron 4 polymorphism influences the progression of renal disease. Nephron 2001;89:219-223.
49. Taniwaki H, Ishimura E, Matsumoto N, Emoto M, Inaba M, Nishizawa Y. Relations between ACE gene and ecNOS gene polymorphisms and resistive index in type 2 diabetic patients with nephropathy. Diabetes Care 2001;24: 1653-1660.
50. Neugebauer S, Baba T, Watanabe T. Association of the nitric oxide synthase gene polymorphism with an increased risk for progression to diabetic nephropathy in type 2 diabetes. Diabetes 2000;49:500-503.
51. Fujita H, Narita T, Meguro H, et al. Lack of association between an ecNOS gene polymorphism and diabetic nephropathy in type 2 diabetic patients with proliferative diabetic retinopathy. Horm Metab Res 2000;32:80-83. (Pubitemid 30143614)
52. Degen B, Schmidt S, Ritz E. A polymorphism in the gene for the endothelial nitric oxide synthase and diabetic nephropathy. Nephrol Dial Transplant 2001;16:185.
53. Cai H, Wang X, Colagiuri S, Wilcken DE. A common Glu298-Asp (894G-T) mutation at exon 7 of the endothelial nitric oxide synthase gene and vascular complications in type 2 diabetes. Diabetes Care 1998;21:2195-2196.
54. Suzuki H, Nagase S, Kikuchi S, Wang Y, Koyama A. Association of a missense Glu298Asp mutation of the endothelial nitric oxide synthase gene with end stage renal disease. Clin Chem 2000;46:1858-1860.
55. Ksiazek P, Wojewoda P, Muc K, Buraczynska M. Endothelial nitric oxide synthase gene intron 4 polymorphism in type 2 diabetes mellitus. Mol Diagn 2003;7:119-123.
56. Ewens KG, George RA, Sharma K, Ziyadeh FN, Spielman RS. Assessment of 115 candidate genes for diabetic nephropathy by transmission/disequilibrium test. Diabetes 2005;54:3305-3318.
57. Rogus JJ, Poznik GD, Pezzolesi MG, et al. High-density single nucleotide polymorphism genome-wide linkage scan for susceptibility genes for diabetic nephropathy in type 1 diabetes: discordant sibpair approach. Diabetes 2008;57:2519-2526.
58. Freedman BI, Bowden DW, Rich SS, et al. A genome scan for all-cause end-stage renal disease in African Americans. Nephrol Dial Transplant 2005;20:712-718.
59. Freedman BI, Bowden DW, Rich SS, et al. Genome-wide linkage scans for renal function and albuminuria in type 2 diabetes mellitus: the Diabetes Heart Study. Diabet Med 2008;25:268-276.
60. Krolewski AS, Poznik GD, Placha G, et al. A genome-wide linkage scan for genes controlling variation in urinary albumin excretion in type II diabetes. Kidney Int 2006;69:129-136.
61. Osterholm AM, He B, Pitkaniemi J, et al. Genome-wide scan for type 1 diabetic nephropathy in the Finnish population reveals suggestive linkage to a single locus on chromosome 3q. Kidney Int 2007;71:140-145.
62. Chen G, Adeyemo AA, Zhou J, et al. A genome-wide search for linkage to renal function phenotypes in West Africans with type 2 diabetes. Am J Kidney Dis 2007;49:394-400. (Pubitemid 46320765)
63. Bowden DW, Colicigno CJ, Langefeld CD, et al. A genome scan for diabetic nephropathy in African Americans. Kidney Int 2004;66:1517-1526.
64. Imperatore G, Hanson RL, Pettitt DJ, Kobes S, Bennett PH, Knowler WC. Sib-pair linkage analysis for susceptibility genes for microvascular complications among Pima Indians with type 2 diabetes. Pima Diabetes Genes Group. Diabetes 1998;47:821-830.
65. Iyengar SK, Abboud HE, Goddard KA, et al. Genome-wide scans for diabetic nephropathy and albuminuria in multiethnic populations: the Family Investigation of Nephropathy and Diabetes (FIND). Diabetes 2007;56:1577-1585.
66. Moczulski DK, Rogus JJ, Antonellis A, Warram JH, Krolewski AS. Major susceptibility locus for nephropathy in type 1 diabetes on chromosome 3q: results of novel discordant sib-pair analysis. Diabetes 1998;47:1164-1169.
67. Vardarli I, Baier LJ, Hanson RL, et al. Gene for susceptibility to diabetic nephropathy in type 2 diabetes maps to 18q22.3-23. Kidney Int 2002;62: 2176-2183.
68. Placha G, Poznik GD, Dunn J, et al. A genome-wide linkage scan for genes controlling variation in renal function estimated by serum cystatin C levels in extended families with type 2 diabetes. Diabetes 2006;55:3358-3365.
69. Pezzolesi MG, Poznik GD, Mychaleckyj JC, et al. Genome-wide association scan for diabetic nephropathy susceptibility genes in type 1 diabetes. Diabetes 2009;58:1403-1410.
70. Maeda S, Osawa N, Hayashi T, Tsukada S, Kobayashi M, Kikkawa R. Genetic variations associated with diabetic nephropathy and type II diabetes in a Japanese population. Kidney Int Suppl 2007:S43-S48.
71. Tanaka N, Babazono T, Saito S, et al. Association of solute carrier family 12 (sodium/chloride) member 3 with diabetic nephropathy, identified by genome-wide analyses of single nucleotide polymorphisms. Diabetes 2003;52: 2848-2853.
72. Egger M, Zellweger-Zahner T, Schneider M, Junker C, Lengeler C, Antes G. Language bias in randomised controlled trials published in English and German. Lancet 1997;350:326-329.
73. Zintzaras E, Kaditis AG. Sleep-disordered breathing and blood pressure in children: a meta-analysis. Arch Pediatr Adolesc Med 2007;161:172-178.
74. Zintzaras E, Koufakis T, Ziakas PD, Rodopoulou P, Giannouli S, Voulgar-elis M. A meta-analysis of genotypes and haplotypes of methylenetetrahy-drofolate reductase gene polymorphisms in acute lymphoblastic leukemia. Eur J Epidemiol 2006;21:501-510.
75. Monti LD, Barlassina C, Citterio L, et al. Endothelial nitric oxide synthase polymorphisms are associated with type 2 diabetes and the insulin resistance syndrome. Diabetes 2003;52:1270-1275.
76. Ohtoshi K, Yamasaki Y, Gorogawa S, et al. Association of (-)786T-C mutation of endothelial nitric oxide synthase gene with insulin resistance. Diabetologia 2002;45:1594-1601.
77. Passaro A, Calzoni F, Volpato S, et al. Effect of metabolic control on homocysteine levels in type 2 diabetic patients: a 3-year follow-up. J Intern Med 2003;254:264-271.
78. Ma J, Stampfer MJ, Giovannucci E, et al. Methylenetetrahydrofolate reductase polymorphism, dietary interactions, and risk of colorectal cancer. Cancer Res 1997;57:1098-1102.
79. Clayton D, McKeigue PM. Epidemiological methods for studying genes and environmental factors in complex diseases. Lancet 2001;358:1356-1360.