The genetics of vascular complications in diabetes mellitus

Cardiology Clinics

Volumn 28, Issue 3, 2010, Pages 477-496

  Farbstein, Dan ^a   Levy, Andrew P ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Cardiovascular disease; Diabetes; Genetic variance; Genotype; Phenotype; Polymorphism

Indexed keywords

5 METHYLTETRAHYDROFOLATE HOMOCYSTEINE METHYLTRANSFERASE; ALPHA TOCOPHEROL; ARYLDIALKYLPHOSPHATASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HAPTOGLOBIN; HOMOCYSTEINE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; DIABETES MELLITUS; DNA MODIFICATION; DRUG TARGETING; GENE FUNCTION; GENE LOCUS; GENETIC DISORDER; GENETIC IDENTIFICATION; GENETIC VARIABILITY; GENETICS; HUMAN; HYPERHOMOCYSTEINEMIA; NONHUMAN; OXIDATIVE STRESS; PHARMACOGENOMICS; PRIORITY JOURNAL; PROTEIN FAMILY; RESOURCE ALLOCATION; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; VASCULAR DISEASE; BLOOD VESSEL; CARDIOVASCULAR DISEASES; DIABETIC ANGIOPATHIES; GENETIC POLYMORPHISM; METABOLISM; PATHOPHYSIOLOGY; RETROSPECTIVE STUDY;

ARYLDIALKYLPHOSPHATASE; BLOOD VESSELS; CARDIOVASCULAR DISEASES; DIABETIC ANGIOPATHIES; HAPTOGLOBINS; HOMOCYSTEINE; HUMANS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXIDATIVE STRESS; POLYMORPHISM, GENETIC; RETROSPECTIVE STUDIES;

EID: 77954513315     PISSN: 07338651     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccl.2010.04.005     Document Type: Review

References (207)

1. American Diabetes Association Economic costs of diabetes in the U.S. in 2007. Diabetes Care 2008, 31(3):596-615.
2. Levy A.P. Application of pharmacogenomics in the prevention of diabetic cardiovascular disease: mechanistic basis and clinical evidence for utilization of the haptoglobin genotype in determining benefit from antioxidant therapy. Pharmacol Ther 2006, 112(2):501-512.
3. Bowden D.W., Lehtinen A.B., Ziegler J.T., et al. Genetic epidemiology of subclinical cardiovascular disease in the diabetes heart study. Ann Hum Genet 2008, 72(Pt 5):598-610.
4. Doria A., Wojcik J., Xu R., et al. Interaction between poor glycemic control and 9p21 locus on risk of coronary artery disease in type 2 diabetes. JAMA 2008, 300(20):2389-2397.
5. Grammer T.B., Renner W., von Karger S., et al. The angiotensin-I converting enzyme I/D polymorphism is not associated with type 2 diabetes in individuals undergoing coronary angiography. (The Ludwigshafen Risk and Cardiovascular Health Study). Mol Genet Metab 2006, 88(4):378-383.
6. Burdon K.P., Langefeld C.D., Wagenknecht L.E., et al. Association analysis of genes in the renin-angiotensin system with subclinical cardiovascular disease in families with Type 2 diabetes mellitus: the Diabetes Heart Study. Diabet Med 2006, 23(3):228-234.
7. Gable D.R., Matin J., Whittall R., et al. Common adiponectin gene variants show different effects on risk of cardiovascular disease and type 2 diabetes in European subjects. Ann Hum Genet 2007, 71(Pt 4):453-466.
8. Prior S.L., Gable D.R., Cooper J.A., et al. Association between the adiponectin promoter rs266729 gene variant and oxidative stress in patients with diabetes mellitus. Eur Heart J 2009, 30(10):1263-1269.
9. Lacquemant C., Froguel P., Lobbens S., et al. The adiponectin gene SNP+45 is associated with coronary artery disease in Type 2 (non-insulin-dependent) diabetes mellitus. Diabet Med 2004, 21(7):776-781.
10. Qi L., Doria A., Manson J.E., et al. Adiponectin genetic variability, plasma adiponectin, and cardiovascular risk in patients with type 2 diabetes. Diabetes 2006, 55(5):1512-1516.
11. Vendramini M.F., Pereira A.C., Ferreira S.R., et al. Association of genetic variants in the adiponectin encoding gene (ADIPOQ) with type 2 diabetes in Japanese Brazilians. J Diabetes Complications 2010, 24(2):115-120.
12. Kim S.H., Kang E.S., Hur K.Y., et al. Adiponectin gene polymorphism 45T>G is associated with carotid artery plaques in patients with type 2 diabetes mellitus. Metabolism 2008, 57(2):274-279.
13. Bacci S., Menzaghi C., Ercolino T., et al. The +276 G/T single nucleotide polymorphism of the adiponectin gene is associated with coronary artery disease in type 2 diabetic patients. Diabetes Care 2004, 27(8):2015-2020.
14. Soccio T., Zhang Y.Y., Bacci S., et al. Common haplotypes at the adiponectin receptor 1 (ADIPOR1) locus are associated with increased risk of coronary artery disease in type 2 diabetes. Diabetes 2006, 55(10):2763-2770.
15. Lin J., Hu F.B., Qi L., et al. Genetic polymorphisms of angiotensin-2 type 1 receptor and angiotensinogen and risk of renal dysfunction and coronary heart disease in type 2 diabetes mellitus. BMC Nephrol 2009, 10:9.
16. Tuncman G., Erbay E., Hom X., et al. A genetic variant at the fatty acid-binding protein aP2 locus reduces the risk for hypertriglyceridemia, type 2 diabetes, and cardiovascular disease. Proc Natl Acad Sci U S A 2006, 103(18):6970-6975.
17. Kretowski A., Hokanson J.E., McFann K., et al. The apolipoprotein A-IV Gln360His polymorphism predicts progression of coronary artery calcification in patients with type 1 diabetes. Diabetologia 2006, 49(8):1946-1954.
18. Winkler K., Hoffmann M.M., Krane V., et al. Apolipoprotein E genotype predicts cardiovascular endpoints in dialysis patients with type 2 diabetes mellitus. Atherosclerosis 2009, 208(1):197-202.
19. Burdon K.P., Langefeld C.D., Beck S.R., et al. Variants of the CD40 gene but not of the CD40L gene are associated with coronary artery calcification in the Diabetes Heart Study (DHS). Am Heart J 2006, 151(3):706-711.
20. Burdon K.P., Langefeld C.D., Beck S.R., et al. Association of genes of lipid metabolism with measures of subclinical cardiovascular disease in the Diabetes Heart Study. J Med Genet 2005, 42(9):720-724.
21. Rudock M.E., Liu Y., Ziegler J.T., et al. Association of polymorphisms in cyclooxygenase (COX)-2 with coronary and carotid calcium in the Diabetes Heart Study. Atherosclerosis 2009, 203(2):459-465.
22. Boger C.A., Fischereder M., Deinzer M., et al. RANTES gene polymorphisms predict all-cause and cardiac mortality in type 2 diabetes mellitus hemodialysis patients. Atherosclerosis 2005, 183(1):121-129.
23. Chen M.P., Chung F.M., Chang D.M., et al. ENPP1 K121Q polymorphism is not related to type 2 diabetes mellitus, features of metabolic syndrome, and diabetic cardiovascular complications in a Chinese population. Rev Diabet Stud 2006, 3(1):21-30.
24. Burdon K.P., Lehtinen A.B., Langefeld C.D., et al. Genetic analysis of the soluble epoxide hydrolase gene, EPHX2, in subclinical cardiovascular disease in the Diabetes Heart Study. Diab Vasc Dis Res 2008, 5(2):128-134.
25. Giacconi R., Caruso C., Lio D., et al. 1267 HSP70-2 polymorphism as a risk factor for carotid plaque rupture and cerebral ischaemia in old type 2 diabetes-atherosclerotic patients. Mech Ageing Dev 2005, 126(8):866-873.
26. Liao Y.F., Zeng T.S., Chen L.L., et al. Association of a functional polymorphism (C59038T) in GTP cyclohydrolase 1 gene and Type 2 diabetic macrovascular disease in the Chinese population. J Diabetes Complications Jun 8 2009, [Online].
27. Hayek T., Stephens J.W., Hubbart C.S., et al. A common variant in the glutathione S transferase gene is associated with elevated markers of inflammation and lipid peroxidation in subjects with diabetes mellitus. Atherosclerosis 2006, 184(2):404-412.
28. Doney A.S., Lee S., Leese G.P., et al. Increased cardiovascular morbidity and mortality in type 2 diabetes is associated with the glutathione S transferase theta-null genotype: a Go-DARTS study. Circulation 2005, 111(22):2927-2934.
29. Danielsson P., Truedsson L., Eriksson K.F., et al. Inflammatory markers and IL-6 polymorphism in peripheral arterial disease with and without diabetes mellitus. Vasc Med 2005, 10(3):191-198.
30. Giacconi R., Bonfigli A.R., Testa R., et al. +647 A/C and +1245 MT1A polymorphisms in the susceptibility of diabetes mellitus and cardiovascular complications. Mol Genet Metab 2008, 94(1):98-104.
31. Romzova M., Hohenadel D., Kolostova K., et al. NFkappaB and its inhibitor IkappaB in relation to type 2 diabetes and its microvascular and atherosclerotic complications. Hum Immunol 2006, 67(9):706-713.
32. Han S.J., Kang E.S., Kim H.J., et al. The C609T variant of NQO1 is associated with carotid artery plaques in patients with type 2 diabetes. Mol Genet Metab 2009, 97(1):85-90.
33. Saely C.H., Muendlein A., Vonbank A., et al. Type 2 diabetes significantly modulates the cardiovascular risk conferred by the PAI-1 -675 4G/5G polymorphism in angiographied coronary patients. Clin Chim Acta 2008, 396(1-2):18-22.
34. Tai E.S., Collins D., Robins S.J., et al. The L162V polymorphism at the peroxisome proliferator activated receptor alpha locus modulates the risk of cardiovascular events associated with insulin resistance and diabetes mellitus: the Veterans Affairs HDL Intervention Trial (VA-HIT). Atherosclerosis 2006, 187(1):153-160.
35. Doney A.S., Fischer B., Lee S.P., et al. Association of common variation in the PPARA gene with incident myocardial infarction in individuals with type 2 diabetes: a Go-DARTS study. Nucl Recept 2005, 3:4.
36. Zalewski G., Ciccarone E., Di Castelnuovo A., et al. P-selectin gene genotypes or haplotypes and cardiovascular complications in type 2 diabetes mellitus. Nutr Metab Cardiovasc Dis 2006, 16(6):418-425.
37. Burdon K.P., Bento J.L., Langefeld C.D., et al. Association of protein tyrosine phosphatase-N1 polymorphisms with coronary calcified plaque in the Diabetes Heart Study. Diabetes 2006, 55(3):651-658.
38. Buraczynska M., Ksiazek P., Baranowicz-Gaszczyk I., et al. Association of the VEGF gene polymorphism with diabetic retinopathy in type 2 diabetes patients. Nephrol Dial Transplant 2007, 22(3):827-832.
39. Suganthalakshmi B., Anand R., Kim R., et al. Association of VEGF and eNOS gene polymorphisms in type 2 diabetic retinopathy. Mol Vis 2006, 12:336-341.
40. Primo-Parmo S.L., Sorenson R.C., Teiber J., et al. The human serum paraoxonase/arylesterase gene (PON1) is one member of a multigene family. Genomics 1996, 33(3):498-507.
41. Blatter M.C., James R.W., Messmer S., et al. Identification of a distinct human high-density lipoprotein subspecies defined by a lipoprotein-associated protein, K-45. Identity of K-45 with paraoxonase. Eur J Biochem 1993, 211(3):871-879.
42. Reddy S.T., Wadleigh D.J., Grijalva V., et al. Human paraoxonase-3 is an HDL-associated enzyme with biological activity similar to paraoxonase-1 protein but is not regulated by oxidized lipids. Arterioscler Thromb Vasc Biol 2001, 21(4):542-547.
43. Ng C.J., Wadleigh D.J., Gangopadhyay A., et al. Paraoxonase-2 is a ubiquitously expressed protein with antioxidant properties and is capable of preventing cell-mediated oxidative modification of low density lipoprotein. J Biol Chem 2001, 276(48):44444-44449.
44. Draganov D.I., Teiber J.F., Speelman A., et al. Human paraoxonases (PON1, PON2, and PON3) are lactonases with overlapping and distinct substrate specificities. J Lipid Res 2005, 46(6):1239-1247.
45. Shih D.M., Lusis A.J. The roles of PON1 and PON2 in cardiovascular disease and innate immunity. Curr Opin Lipidol 2009, 20(4):288-292.
46. Durrington P.N., Mackness B., Mackness M.I. Paraoxonase and atherosclerosis. Arterioscler Thromb Vasc Biol 2001, 21(4):473-480.
47. Yang F., Wang L.H., Wang J., et al. Quorum quenching enzyme activity is widely conserved in the sera of mammalian species. FEBS Lett 2005, 579(17):3713-3717.
48. Mackness M.I., Arrol S., Durrington P.N. Paraoxonase prevents accumulation of lipoperoxides in low-density lipoprotein. FEBS Lett 1991, 286(1-2):152-154.
49. Watson A.D., Berliner J.A., Hama S.Y., et al. Protective effect of high density lipoprotein associated paraoxonase. Inhibition of the biological activity of minimally oxidized low density lipoprotein. J Clin Invest 1995, 96(6):2882-2891.
50. Aviram M., Rosenblat M., Bisgaier C.L., et al. Paraoxonase inhibits high-density lipoprotein oxidation and preserves its functions. A possible peroxidative role for paraoxonase. J Clin Invest 1998, 101(8):1581-1590.
51. Shih D.M., Gu L., Xia Y.R., et al. Mice lacking serum paraoxonase are susceptible to organophosphate toxicity and atherosclerosis. Nature 1998, 394(6690):284-287.
52. Shih D.M., Xia Y.R., Wang X.P., et al. Combined serum paraoxonase knockout/apolipoprotein E knockout mice exhibit increased lipoprotein oxidation and atherosclerosis. J Biol Chem 2000, 275(23):17527-17535.
53. Tward A., Xia Y.R., Wang X.P., et al. Decreased atherosclerotic lesion formation in human serum paraoxonase transgenic mice. Circulation 2002, 106(4):484-490.
54. Deakin S., Leviev I., Brulhart-Meynet M.C., et al. Paraoxonase-1 promoter haplotypes and serum paraoxonase: a predominant role for polymorphic position - 107, implicating the Sp1 transcription factor. Biochem J 2003, 372(Pt 2):643-649.
55. Leviev I., James R.W. Promoter polymorphisms of human paraoxonase PON1 gene and serum paraoxonase activities and concentrations. Arterioscler Thromb Vasc Biol 2000, 20(2):516-521.
56. Leviev I., Righetti A., James R.W. Paraoxonase promoter polymorphism T(-107)C and relative paraoxonase deficiency as determinants of risk of coronary artery disease. J Mol Med 2001, 79(8):457-463.
57. Wang X., Fan Z., Huang J., et al. Extensive association analysis between polymorphisms of PON gene cluster with coronary heart disease in Chinese Han population. Arterioscler Thromb Vasc Biol 2003, 23(2):328-334.
58. Najafi M., Gohari L.H., Firoozrai M. Paraoxonase 1 gene promoter polymorphisms are associated with the extent of stenosis in coronary arteries. Thromb Res 2009, 123(3):503-510.
59. Yamada Y., Izawa H., Ichihara S., et al. Prediction of the risk of myocardial infarction from polymorphisms in candidate genes. N Engl J Med 2002, 347(24):1916-1923.
60. Adkins S., Gan K.N., Mody M., et al. Molecular basis for the polymorphic forms of human serum paraoxonase/arylesterase: glutamine or arginine at position 191, for the respective A or B allozymes. Am J Hum Genet 1993, 52(3):598-608.
61. Bhattacharyya T., Nicholls S.J., Topol E.J., et al. Relationship of paraoxonase 1 (PON1) gene polymorphisms and functional activity with systemic oxidative stress and cardiovascular risk. JAMA 2008, 299(11):1265-1276.
62. Gaidukov L., Rosenblat M., Aviram M., et al. The 192R/Q polymorphs of serum paraoxonase PON1 differ in HDL binding, lipolactonase stimulation, and cholesterol efflux. J Lipid Res 2006, 47(11):2492-2502.
63. Wheeler J.G., Keavney B.D., Watkins H., et al. Four paraoxonase gene polymorphisms in 11212 cases of coronary heart disease and 12786 controls: meta-analysis of 43 studies. Lancet 2004, 363(9410):689-695.
64. Jarvik G.P., Hatsukami T.S., Carlson C., et al. Paraoxonase activity, but not haplotype utilizing the linkage disequilibrium structure, predicts vascular disease. Arterioscler Thromb Vasc Biol 2003, 23(8):1465-1471.
65. Mackness B., Davies G.K., Turkie W., et al. Paraoxonase status in coronary heart disease: are activity and concentration more important than genotype?. Arterioscler Thromb Vasc Biol 2001, 21(9):1451-1457.
66. Mackness B., Mackness M.I., Arrol S., et al. Serum paraoxonase (PON1) 55 and 192 polymorphism and paraoxonase activity and concentration in non-insulin dependent diabetes mellitus. Atherosclerosis 1998, 139(2):341-349.
67. Inoue M., Suehiro T., Nakamura T., et al. Serum arylesterase/diazoxonase activity and genetic polymorphisms in patients with type 2 diabetes. Metabolism 2000, 49(11):1400-1405.
68. Flekac M., Skrha J., Zidkova K., et al. Paraoxonase 1 gene polymorphisms and enzyme activities in diabetes mellitus. Physiol Res 2008, 57(5):717-726.
69. Mastorikou M., Mackness M., Mackness B. Defective metabolism of oxidized phospholipid by HDL from people with type 2 diabetes. Diabetes 2006, 55(11):3099-3103.
70. Mackness B., Durrington P.N., Boulton A.J., et al. Serum paraoxonase activity in patients with type 1 diabetes compared to healthy controls. Eur J Clin Invest 2002, 32(4):259-264.
71. van den Berg S.W., Jansen E.H., Kruijshoop M., et al. Paraoxonase 1 phenotype distribution and activity differs in subjects with newly diagnosed Type 2 diabetes (the CODAM Study). Diabet Med 2008, 25(2):186-193.
72. Rozenberg O., Shiner M., Aviram M., et al. Paraoxonase 1 (PON1) attenuates diabetes development in mice through its antioxidative properties. Free Radic Biol Med 2008, 44(11):1951-1959.
73. Ikeda Y., Inoue M., Suehiro T., et al. Low human paraoxonase predicts cardiovascular events in Japanese patients with type 2 diabetes. Acta Diabetol 2009, 46(3):239-242.
74. Mackness B., Durrington P.N., Abuashia B., et al. Low paraoxonase activity in type II diabetes mellitus complicated by retinopathy. Clin Sci (Lond) 2000, 98(3):355-363.
75. Kosaka T., Yamaguchi M., Motomura T., et al. Investigation of the relationship between atherosclerosis and paraoxonase or homocysteine thiolactonase activity in patients with type 2 diabetes mellitus using a commercially available assay. Clin Chim Acta 2005, 359(1-2):156-162.
76. Ikeda Y., Suehiro T., Inoue M., et al. Serum paraoxonase activity and its relationship to diabetic complications in patients with non-insulin-dependent diabetes mellitus. Metabolism 1998, 47(5):598-602.
77. James R.W., Leviev I., Ruiz J., et al. Promoter polymorphism T(-107)C of the paraoxonase PON1 gene is a risk factor for coronary heart disease in type 2 diabetic patients. Diabetes 2000, 49(8):1390-1393.
78. Tsuzura S., Ikeda Y., Suehiro T., et al. Correlation of plasma oxidized low-density lipoprotein levels to vascular complications and human serum paraoxonase in patients with type 2 diabetes. Metabolism 2004, 53(3):297-302.
79. Sampson M.J., Braschi S., Willis G., et al. Paraoxonase-1 (PON-1) genotype and activity and in vivo oxidized plasma low-density lipoprotein in type II diabetes. Clin Sci (Lond) 2005, 109(2):189-197.
80. Agachan B., Yilmaz H., Ergen H.A., et al. Paraoxonase (PON1) 55 and 192 polymorphism and its effects to oxidant-antioxidant system in Turkish patients with type 2 diabetes mellitus. Physiol Res 2005, 54(3):287-293.
81. Pfohl M., Koch M., Enderle M.D., et al. Paraoxonase 192 Gln/Arg gene polymorphism, coronary artery disease, and myocardial infarction in type 2 diabetes. Diabetes 1999, 48(3):623-627.
82. Murata M., Maruyama T., Suzuki Y., et al. Paraoxonase 1 Gln/Arg polymorphism is associated with the risk of microangiopathy in type 2 diabetes mellitus. Diabet Med 2004, 21(8):837-844.
83. Odawara M., Tachi Y., Yamashita K. Paraoxonase polymorphism (Gln192-Arg) is associated with coronary heart disease in Japanese noninsulin-dependent diabetes mellitus. J Clin Endocrinol Metab 1997, 82(7):2257-2260.
84. Ruiz J., Blanche H., James R.W., et al. Gln-Arg192 polymorphism of paraoxonase and coronary heart disease in type 2 diabetes. Lancet 1995, 346(8979):869-872.
85. Aubo C., Senti M., Marrugat J., et al. Risk of myocardial infarction associated with Gln/Arg 192 polymorphism in the human paraoxonase gene and diabetes mellitus. The REGICOR Investigators. Eur Heart J 2000, 21(1):33-38.
86. Li J., Wang X., Huo Y., et al. PON1 polymorphism, diabetes mellitus, obesity, and risk of myocardial infarction: modifying effect of diabetes mellitus and obesity on the association between PON1 polymorphism and myocardial infarction. Genet Med 2005, 7(1):58-63.
87. Finkelstein J.D. Methionine metabolism in mammals. J Nutr Biochem 1990, 1(5):228-237.
88. Jakubowski H. The pathophysiological hypothesis of homocysteine thiolactone-mediated vascular disease. J Physiol Pharmacol 2008, 59(Suppl 9):155-167.
89. Obeid R., Herrmann W. Homocysteine and lipids: S-adenosyl methionine as a key intermediate. FEBS Lett 2009, 583(8):1215-1225.
90. Refsum H., Ueland P.M., Nygard O., et al. Homocysteine and cardiovascular disease. Annu Rev Med 1998, 49:31-62.
91. Nygard O., Vollset S.E., Refsum H., et al. Total homocysteine and cardiovascular disease. J Intern Med 1999, 246(5):425-454.
92. Kerkeni M., Tnani M., Chuniaud L., et al. Comparative study on in vitro effects of homocysteine thiolactone and homocysteine on HUVEC cells: evidence for a stronger proapoptotic and proinflammative homocysteine thiolactone. Mol Cell Biochem 2006, 291(1-2):119-126.
93. Chang P.Y., Lu S.C., Lee C.M., et al. Homocysteine inhibits arterial endothelial cell growth through transcriptional downregulation of fibroblast growth factor-2 involving G protein and DNA methylation. Circ Res 2008, 102(8):933-941.
94. Jamaluddin M.D., Chen I., Yang F., et al. Homocysteine inhibits endothelial cell growth via DNA hypomethylation of the cyclin A gene. Blood 2007, 110(10):3648-3655.
95. Wang H., Yoshizumi M., Lai K., et al. Inhibition of growth and p21ras methylation in vascular endothelial cells by homocysteine but not cysteine. J Biol Chem 1997, 272(40):25380-25385.
96. Tsai J.C., Wang H., Perrella M.A., et al. Induction of cyclin A gene expression by homocysteine in vascular smooth muscle cells. J Clin Invest 1996, 97(1):146-153.
97. Tsai J.C., Perrella M.A., Yoshizumi M., et al. Promotion of vascular smooth muscle cell growth by homocysteine: a link to atherosclerosis. Proc Natl Acad Sci U S A 1994, 91(14):6369-6373.
98. McCully K.S. Vascular pathology of homocysteinemia: implications for the pathogenesis of arteriosclerosis. Am J Pathol 1969, 56(1):111-128.
99. Khandanpour N., Loke Y.K., Meyer F.J., et al. Homocysteine and peripheral arterial disease: systematic review and meta-analysis. Eur J Vasc Endovasc Surg 2009, 38(3):316-322.
100. Humphrey L.L., Fu R., Rogers K., et al. Homocysteine level and coronary heart disease incidence: a systematic review and meta-analysis. Mayo Clin Proc 2008, 83(11):1203-1212.
101. Homocysteine and risk of ischemic heart disease and stroke: a meta-analysis. JAMA 2002, 288(16):2015-2022. Homocysteine Studies Collaboration.
102. Mager A., Orvin K., Koren-Morag N., et al. Impact of homocysteine-lowering vitamin therapy on long-term outcome of patients with coronary artery disease. Am J Cardiol 2009, 104(6):745-749.
103. Van Guelpen B., Hultdin J., Johansson I., et al. Plasma folate and total homocysteine levels are associated with the risk of myocardial infarction, independently of each other and of renal function. J Intern Med 2009, 266(2):182-195.
104. Albert C.M., Cook N.R., Gaziano J.M., et al. Effect of folic acid and B vitamins on risk of cardiovascular events and total mortality among women at high risk for cardiovascular disease: a randomized trial. JAMA 2008, 299(17):2027-2036.
105. Bazzano L.A., Reynolds K., Holder K.N., et al. Effect of folic acid supplementation on risk of cardiovascular diseases: a meta-analysis of randomized controlled trials. JAMA 2006, 296(22):2720-2726.
106. Ebbing M., Bleie O., Ueland P.M., et al. Mortality and cardiovascular events in patients treated with homocysteine-lowering B vitamins after coronary angiography: a randomized controlled trial. JAMA 2008, 300(7):795-804.
107. Bonaa K.H., Njolstad I., Ueland P.M., et al. Homocysteine lowering and cardiovascular events after acute myocardial infarction. N Engl J Med 2006, 354(15):1578-1588.
108. Lonn E., Yusuf S., Arnold M.J., et al. Homocysteine lowering with folic acid and B vitamins in vascular disease. N Engl J Med 2006, 354(15):1567-1577.
109. Wang X., Qin X., Demirtas H., et al. Efficacy of folic acid supplementation in stroke prevention: a meta-analysis. Lancet 2007, 369(9576):1876-1882.
110. Carlsson C.M. Lowering homocysteine for stroke prevention. Lancet 2007, 369(9576):1841-1842.
111. Kark J.D., Selhub J., Bostom A., et al. Plasma homocysteine and all-cause mortality in diabetes. Lancet 1999, 353(9168):1936-1937.
112. Hoogeveen E.K., Kostense P.J., Beks P.J., et al. Hyperhomocysteinemia is associated with an increased risk of cardiovascular disease, especially in non-insulin-dependent diabetes mellitus: a population-based study. Arterioscler Thromb Vasc Biol 1998, 18(1):133-138.
113. Brazionis L., Rowley K., Itsiopoulos C., et al. Homocysteine and diabetic retinopathy. Diabetes Care 2008, 31(1):50-56.
114. Becker A., Kostense P.J., Bos G., et al. Hyperhomocysteinaemia is associated with coronary events in type 2 diabetes. J Intern Med 2003, 253(3):293-300.
115. Buysschaert M., Dramais A.S., Wallemacq P.E., et al. Hyperhomocysteinemia in type 2 diabetes: relationship to macroangiopathy, nephropathy, and insulin resistance. Diabetes Care 2000, 23(12):1816-1822.
116. Mazza A., Bossone E., Mazza F., et al. Reduced serum homocysteine levels in type 2 diabetes. Nutr Metab Cardiovasc Dis 2005, 15(2):118-124.
117. Ndrepepa G., Kastrati A., Braun S., et al. Circulating homocysteine levels in patients with type 2 diabetes mellitus. Nutr Metab Cardiovasc Dis 2008, 18(1):66-73.
118. Emoto M., Kanda H., Shoji T., et al. Impact of insulin resistance and nephropathy on homocysteine in type 2 diabetes. Diabetes Care 2001, 24(3):533-538.
119. Kluijtmans L.A., van den Heuvel L.P., Boers G.H., et al. Molecular genetic analysis in mild hyperhomocysteinemia: a common mutation in the methylenetetrahydrofolate reductase gene is a genetic risk factor for cardiovascular disease. Am J Hum Genet 1996, 58(1):35-41.
120. Deloughery T.G., Evans A., Sadeghi A., et al. Common mutation in methylenetetrahydrofolate reductase. Correlation with homocysteine metabolism and late-onset vascular disease. Circulation 1996, 94(12):3074-3078.
121. Lewis S.J., Ebrahim S., Davey Smith G. Meta-analysis of MTHFR 677C->T polymorphism and coronary heart disease: does totality of evidence support causal role for homocysteine and preventive potential of folate?. BMJ 2005, 331(7524):1053.
122. Khandanpour N., Willis G., Meyer F.J., et al. Peripheral arterial disease and methylenetetrahydrofolate reductase (MTHFR) C677T mutations: a case-control study and meta-analysis. J Vasc Surg 2009, 49(3):711-718.
123. Sun J., Xu Y., Zhu Y., et al. The relationship between MTHFR gene polymorphisms, plasma homocysteine levels and diabetic retinopathy in type 2 diabetes mellitus. Chin Med J (Engl) 2003, 116(1):145-147.
124. Maeda M., Yamamoto I., Fukuda M., et al. MTHFR gene polymorphism is susceptible to diabetic retinopathy but not to diabetic nephropathy in Japanese type 2 diabetic patients. J Diabetes Complications 2008, 22(2):119-125.
125. Maeda M., Yamamoto I., Fukuda M., et al. MTHFR gene polymorphism as a risk factor for diabetic retinopathy in type 2 diabetic patients without serum creatinine elevation. Diabetes Care 2003, 26(2):547-548.
126. Moczulski D., Fojcik H., Zukowska-Szczechowska E., et al. Effects of the C677T and A1298C polymorphisms of the MTHFR gene on the genetic predisposition for diabetic nephropathy. Nephrol Dial Transplant 2003, 18(8):1535-1540.
127. Ukinc K., Ersoz H.O., Karahan C., et al. Methyltetrahydrofolate reductase C677T gene mutation and hyperhomocysteinemia as a novel risk factor for diabetic nephropathy. Endocrine 2009, 36(2):255-261.
128. Sun J., Xu Y., Zhu Y., et al. Genetic polymorphism of methylenetetrahydrofolate reductase as a risk factor for diabetic nephropathy in Chinese type 2 diabetic patients. Diabetes Res Clin Pract 2004, 64(3):185-190.
129. Mazza A., Motti C., Nulli A., et al. Lack of association between carotid intima-media thickness and methylenetetrahydrofolate reductase gene polymorphism or serum homocysteine in non-insulin-dependent diabetes mellitus. Metabolism 2000, 49(6):718-723.
130. Hermans M.P., Gala J.L., Buysschaert M. The MTHFR CT polymorphism confers a high risk for stroke in both homozygous and heterozygous T allele carriers with Type 2 diabetes. Diabet Med 2006, 23(5):529-536.
131. Szabo G.V., Kunstar A., Acsady G. Methylentetrahydrofolate Reductase and Nitric Oxide Synthase Polymorphism in Patients with Atherosclerosis and Diabetes. Pathol Oncol Res 2009, 15(4):631-637.
132. Mazza A., Motti C., Nulli A., et al. Serum homocysteine, MTHFR gene polymorphism, and carotid intimal-medial thickness in NIDDM subjects. J Thromb Thrombolysis 1999, 8(3):207-212.
133. Kaye J.M., Stanton K.G., McCann V.J., et al. Homocysteine, folate, methylene tetrahydrofolate reductase genotype and vascular morbidity in diabetic subjects. Clin Sci (Lond) 2002, 102(6):631-637.
134. Pollex R.L., Mamakeesick M., Zinman B., et al. Methylenetetrahydrofolate reductase polymorphism 677C>T is associated with peripheral arterial disease in type 2 diabetes. Cardiovasc Diabetol 2005, 4:17.
135. Sun J., Xu Y., Xue J., et al. Methylenetetrahydrofolate reductase polymorphism associated with susceptibility to coronary heart disease in Chinese type 2 diabetic patients. Mol Cell Endocrinol 2005, 229(1-2):95-101.
136. Russo G.T., Di Benedetto A., Magazzu D., et al. Mild hyperhomocysteinemia, C677T polymorphism on methylenetetrahydrofolate reductase gene and the risk of macroangiopathy in type 2 diabetes: a prospective study. Acta Diabetol 2009, [Online].
137. Dudzinski D.M., Michel T. Life history of eNOS: partners and pathways. Cardiovasc Res 2007, 75(2):247-260.
138. Li H., Forstermann U. Nitric oxide in the pathogenesis of vascular disease. J Pathol 2000, 190(3):244-254.
139. Napoli C., Ignarro L.J. Nitric oxide and pathogenic mechanisms involved in the development of vascular diseases. Arch Pharm Res 2009, 32(8):1103-1108.
140. Kagan V.E., Laskin J.D. Direct and indirect antioxidant effects of nitric oxide: radically unsettled issues. Antioxid Redox Signal 2001, 3(2):173-175.
141. Marsden P.A., Heng H.H., Scherer S.W., et al. Structure and chromosomal localization of the human constitutive endothelial nitric oxide synthase gene. J Biol Chem 1993, 268(23):17478-17488.
142. Andrew P.J., Mayer B. Enzymatic function of nitric oxide synthases. Cardiovasc Res 1999, 43(3):521-531.
143. Napoli C., Ignarro L.J. Polymorphisms in endothelial nitric oxide synthase and carotid artery atherosclerosis. J Clin Pathol 2007, 60(4):341-344.
144. Tesauro M., Thompson W.C., Rogliani P., et al. Intracellular processing of endothelial nitric oxide synthase isoforms associated with differences in severity of cardiopulmonary diseases: cleavage of proteins with aspartate vs. glutamate at position 298. Proc Natl Acad Sci U S A 2000, 97(6):2832-2835.
145. Persu A., Stoenoiu M.S., Messiaen T., et al. Modifier effect of ENOS in autosomal dominant polycystic kidney disease. Hum Mol Genet 2002, 11(3):229-241.
146. Fairchild T.A., Fulton D., Fontana J.T., et al. Acidic hydrolysis as a mechanism for the cleavage of the Glu(298)->Asp variant of human endothelial nitric-oxide synthase. J Biol Chem 2001, 276(28):26674-26679.
147. McDonald D.M., Alp N.J., Channon K.M. Functional comparison of the endothelial nitric oxide synthase Glu298Asp polymorphic variants in human endothelial cells. Pharmacogenetics 2004, 14(12):831-839.
148. Golser R., Gorren A.C., Mayer B., et al. Functional characterization of Glu298Asp mutant human endothelial nitric oxide synthase purified from a yeast expression system. Nitric Oxide 2003, 8(1):7-14.
149. Paradossi U., Ciofini E., Clerico A., et al. Endothelial function and carotid intima-media thickness in young healthy subjects among endothelial nitric oxide synthase Glu298->Asp and T-786->C polymorphisms. Stroke 2004, 35(6):1305-1309.
150. Naber C.K., Baumgart D., Altmann C., et al. eNOS 894T allele and coronary blood flow at rest and during adenosine-induced hyperemia. Am J Physiol Heart Circ Physiol 2001, 281(5):H1908-H1912.
151. Philip I., Plantefeve G., Vuillaumier-Barrot S., et al. G894T polymorphism in the endothelial nitric oxide synthase gene is associated with an enhanced vascular responsiveness to phenylephrine. Circulation 1999, 99(24):3096-3098.
152. Li R., Lyn D., Lapu-Bula R., et al. Relation of endothelial nitric oxide synthase gene to plasma nitric oxide level, endothelial function, and blood pressure in African Americans. Am J Hypertens 2004, 17(7):560-567.
153. Rossi G.P., Taddei S., Virdis A., et al. The T-786C and Glu298Asp polymorphisms of the endothelial nitric oxide gene affect the forearm blood flow responses of Caucasian hypertensive patients. J Am Coll Cardiol 2003, 41(6):938-945.
154. Schmoelzer I., Renner W., Paulweber B., et al. Lack of association of the Glu298Asp polymorphism of endothelial nitric oxide synthase with manifest coronary artery disease, carotid atherosclerosis and forearm vascular reactivity in two Austrian populations. Eur J Clin Invest 2003, 33(3):191-198.
155. Lamblin N., Cuilleret F.J., Helbecque N., et al. A common variant of endothelial nitric oxide synthase (Glu298Asp) is associated with collateral development in patients with chronic coronary occlusions. BMC Cardiovasc Disord 2005, 5:27.
156. Gulec S., Karabulut H., Ozdemir A.O., et al. Glu298Asp polymorphism of the eNOS gene is associated with coronary collateral development. Atherosclerosis 2008, 198(2):354-359.
157. Miyamoto Y., Saito Y., Nakayama M., et al. 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 2000, 9(18):2629-2637.
158. Cattaruzza M., Guzik T.J., Slodowski W., et al. Shear stress insensitivity of endothelial nitric oxide synthase expression as a genetic risk factor for coronary heart disease. Circ Res 2004, 95(8):841-847.
159. Asif A.R., Oellerich M., Armstrong V.W., et al. T-786C polymorphism of the NOS-3 gene and the endothelial cell response to fluid shear stress-a proteome analysis. J Proteome Res 2009, 8(6):3161-3168.
160. Wang X.L., Sim A.S., Wang M.X., et al. Genotype dependent and cigarette specific effects on endothelial nitric oxide synthase gene expression and enzyme activity. FEBS Lett 2000, 471(1):45-50.
161. Tsukada T., Yokoyama K., Arai T., et al. Evidence of association of the ecNOS gene polymorphism with plasma NO metabolite levels in humans. Biochem Biophys Res Commun 1998, 245(1):190-193.
162. Jeerooburkhan N., Jones L.C., Bujac S., et al. Genetic and environmental determinants of plasma nitrogen oxides and risk of ischemic heart disease. Hypertension 2001, 38(5):1054-1061.
163. Yoon Y., Song J., Hong S.H., et al. Plasma nitric oxide concentrations and nitric oxide synthase gene polymorphisms in coronary artery disease. Clin Chem 2000, 46(10):1626-1630.
164. Salimi S., Firoozrai M., Nourmohammadi I., et al. Lack of evidence for contribution of intron4a/b polymorphism of endothelial nitric oxide synthase (NOS3) gene to plasma nitric oxide levels. Acta Cardiol 2008, 63(2):229-234.
165. Casas J.P., Cavalleri G.L., Bautista L.E., et al. Endothelial nitric oxide synthase gene polymorphisms and cardiovascular disease: a HuGE review. Am J Epidemiol 2006, 164(10):921-935.
166. Vallance P., Chan N. Endothelial function and nitric oxide: clinical relevance. Heart 2001, 85(3):342-350.
167. Huang P.L. eNOS, metabolic syndrome and cardiovascular disease. Trends Endocrinol Metab 2009, 20(6):295-302.
168. Guang-da X., Qiong-shu W., Wen J. A T-786C polymorphism in 5'-flanking region of the endothelial nitric oxide synthase gene and endothelium-dependent arterial dilation in Type 2 diabetes. Diabet Med 2005, 22(12):1663-1669.
169. Rittig K., Holder K., Stock J., et al. Endothelial NO-synthase intron 4 polymorphism is associated with disturbed in vivo nitric oxide production in individuals prone to type 2 diabetes. Horm Metab Res 2008, 40(1):13-17.
170. Sandrim V.C., de Syllos R.W., Lisboa H.R., et al. Influence of eNOS haplotypes on the plasma nitric oxide products concentrations in hypertensive and type 2 diabetes mellitus patients. Nitric Oxide 2007, 16(3):348-355.
171. Zintzaras E., Papathanasiou A.A., Stefanidis I. Endothelial nitric oxide synthase gene polymorphisms and diabetic nephropathy: a HuGE review and meta-analysis. Genet Med 2009, 11(10):695-706.
172. Abhary S., Hewitt A.W., Burdon K.P., et al. A systematic meta-analysis of genetic association studies for diabetic retinopathy. Diabetes 2009, 58(9):2137-2147.
173. Odeberg J., Larsson C.A., Rastam L., et al. The Asp298 allele of endothelial nitric oxide synthase is a risk factor for myocardial infarction among patients with type 2 diabetes mellitus. BMC Cardiovasc Disord 2008, 8:36.
174. Zhang C., Lopez-Ridaura R., Hunter D.J., et al. Common variants of the endothelial nitric oxide synthase gene and the risk of coronary heart disease among U.S. diabetic men. Diabetes 2006, 55(7):2140-2147.
175. Cai H., Wang X., Colagiuri S., et al. 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(12):2195-2196.
176. Mollsten A., Lajer M., Jorsal A., et al. The endothelial nitric oxide synthase gene and risk of diabetic nephropathy and development of cardiovascular disease in type 1 diabetes. Mol Genet Metab 2009, 97(1):80-84.
177. Bowman B.H., Kurosky A. Haptoglobin: the evolutionary product of duplication, unequal crossing over, and point mutation. Adv Hum Genet 1982, 12:189-261. 453-4.
178. Garby L., Noyes W.D. Studies on hemoglobin metabolism. I. The kinetic properties of the plasma hemoglobin pool in normal man. J Clin Invest 1959, 38:1479-1483.
179. Fagoonee S., Gburek J., Hirsch E., et al. Plasma protein haptoglobin modulates renal iron loading. Am J Pathol 2005, 166(4):973-983.
180. Lim S.K., Kim H., Lim S.K., et al. Increased susceptibility in Hp knockout mice during acute hemolysis. Blood 1998, 92(6):1870-1877.
181. Kristiansen M., Graversen J.H., Jacobsen C., et al. Identification of the haemoglobin scavenger receptor. Nature 2001, 409(6817):198-201.
182. Graversen J.H., Madsen M., Moestrup S.K. CD163: a signal receptor scavenging haptoglobin-hemoglobin complexes from plasma. Int J Biochem Cell Biol 2002, 34(4):309-314.
183. Sadrzadeh S.M., Graf E., Panter S.S., et al. A biologic fenton reagent. J Biol Chem 1984, 259(23):14354-14356.
184. Melamed-Frank M., Lache O., Enav B.I., et al. Structure-function analysis of the antioxidant properties of haptoglobin. Blood 2001, 98(13):3693-3698.
185. Miller Y.I., Altamentova S.M., Shaklai N. Oxidation of low-density lipoprotein by hemoglobin stems from a heme-initiated globin radical: antioxidant role of haptoglobin. Biochemistry 1997, 36(40):12189-12198.
186. Buehler P.W., Abraham B., Vallelian F., et al. Haptoglobin preserves the CD163 hemoglobin scavenger pathway by shielding hemoglobin from peroxidative modification. Blood 2009, 113(11):2578-2586.
187. Langlois M.R., Delanghe J.R. Biological and clinical significance of haptoglobin polymorphism in humans. Clin Chem 1996, 42(10):1589-1600.
188. Levy A.P., Hochberg I., Jablonski K., et al. Haptoglobin phenotype is an independent risk factor for cardiovascular disease in individuals with diabetes: the Strong Heart Study. J Am Coll Cardiol 2002, 40(11):1984-1990.
189. Suleiman M., Aronson D., Asleh R., et al. Haptoglobin polymorphism predicts 30-day mortality and heart failure in patients with diabetes and acute myocardial infarction. Diabetes 2005, 54(9):2802-2806.
190. Roguin A., Koch W., Kastrati A., et al. Haptoglobin genotype is predictive of major adverse cardiac events in the 1-year period after percutaneous transluminal coronary angioplasty in individuals with diabetes. Diabetes Care 2003, 26(9):2628-2631.
191. Costacou T., Ferrell R.E., Orchard T.J. Haptoglobin genotype: a determinant of cardiovascular complication risk in type 1 diabetes. Diabetes 2008, 57(6):1702-1706.
192. Milman U., Blum S., Shapira C., et al. Vitamin E supplementation reduces cardiovascular events in a subgroup of middle-aged individuals with both type 2 diabetes mellitus and the haptoglobin 2-2 genotype: a prospective double-blinded clinical trial. Arterioscler Thromb Vasc Biol 2008, 28(2):341-347.
193. Miller-Lotan R., Miller B., Nakhoul F., et al. Retinal capillary basement membrane thickness in diabetic mice genetically modified at the haptoglobin locus. Diabetes Metab Res Rev 2007, 23(2):152-156.
194. Miller-Lotan R., Herskowitz Y., Kalet-Litman S., et al. Increased renal hypertrophy in diabetic mice genetically modified at the haptoglobin locus. Diabetes Metab Res Rev 2005, 21(4):332-337.
195. Asleh R., Miller-Lotan R., Aviram M., et al. Haptoglobin genotype is a regulator of reverse cholesterol transport in diabetes in vitro and in vivo. Circ Res 2006, 99(12):1419-1425.
196. Levy A.P., Levy J.E., Kalet-Litman S., et al. Haptoglobin genotype is a determinant of iron, lipid peroxidation, and macrophage accumulation in the atherosclerotic plaque. Arterioscler Thromb Vasc Biol 2007, 27(1):134-140.
197. De Bacquer D., De Backer G., Langlois M., et al. Haptoglobin polymorphism as a risk factor for coronary heart disease mortality. Atherosclerosis 2001, 157(1):161-166.
198. Holme I., Aastveit A.H., Hammar N., et al. Haptoglobin and risk of myocardial infarction, stroke, and congestive heart failure in 342,125 men and women in the Apolipoprotein MOrtality RISk study (AMORIS). Ann Med 2009, 1-11. [Online].
199. Asleh R., Marsh S., Shilkrut M., et al. Genetically determined heterogeneity in hemoglobin scavenging and susceptibility to diabetic cardiovascular disease. Circ Res 2003, 92(11):1193-1200.
200. Asleh R., Guetta J., Kalet-Litman S., et al. Haptoglobin genotype- and diabetes-dependent differences in iron-mediated oxidative stress in vitro and in vivo. Circ Res 2005, 96(4):435-441.
201. Kalet-Litman S., Moreno P.R., Levy A.P. The haptoglobin 2-2 genotype is associated with increased redox active hemoglobin derived iron in the atherosclerotic plaque. Atherosclerosis 2010, 209(1):28-31.
202. Levy A.P., Purushothaman K.R., Levy N.S., et al. Downregulation of the hemoglobin scavenger receptor in individuals with diabetes and the Hp 2-2 genotype: implications for the response to intraplaque hemorrhage and plaque vulnerability. Circ Res 2007, 101(1):106-110.
203. Timmermann M., Hogger P. Oxidative stress and 8-iso-prostaglandin F(2alpha) induce ectodomain shedding of CD163 and release of tumor necrosis factor-alpha from human monocytes. Free Radic Biol Med 2005, 39(1):98-107.
204. Boyle J.J., Harrington H.A., Piper E., et al. Coronary intraplaque hemorrhage evokes a novel atheroprotective macrophage phenotype. Am J Pathol 2009, 174(3):1097-1108.
205. Asleh R., Blum S., Kalet-Litman S., et al. Correction of HDL dysfunction in individuals with diabetes and the haptoglobin 2-2 genotype. Diabetes 2008, 57(10):2794-2800.
206. Farbstein D., Levy A.P. Pharmacogenomics and the prevention of vascular complications in diabetes mellitus. Therapy 2009, 6(4):531-538.
207. Levy A.P., Asleh R., Blum S., et al. Haptoglobin: basic and clinical aspects. Antioxid Redox Signal 2010, 12(2):293-304.