Journal of the American Society of Hypertension
Volume 1, Issue 5 , Pages 362-368 , September 2007

Influence of nitric oxide synthase gene polymorphism (G894T) on carotid artery intima-media thickness in adults: the Bogalusa Heart Study

  • Azad R. Bhuiyan, MD, PhD

      Affiliations

    • Tulane Center for Cardiovascular Health and Department of Epidemiology, New Orleans, Louisiana, USA
  • ,
  • Wei Chen, MD, PhD

      Affiliations

    • Tulane Center for Cardiovascular Health and Department of Epidemiology, New Orleans, Louisiana, USA
  • ,
  • Sathanur R. Srinivasan, PhD

      Affiliations

    • Tulane Center for Cardiovascular Health and Department of Epidemiology, New Orleans, Louisiana, USA
  • ,
  • Janet Rice, PhD

      Affiliations

    • Tulane University School of Public Health and Tropical Medicine, New Orleans, Louisiana, USA
  • ,
  • Nancy Mock, DrPH

      Affiliations

    • Tulane University School of Public Health and Tropical Medicine, New Orleans, Louisiana, USA
  • ,
  • Rong Tang, MD, MS

      Affiliations

    • Division of Vascular Ultrasound Research, Wake Forest University School of Medicine, Winston-Salem, North Carolina, USA
  • ,
  • M. Gene Bond, PhD

      Affiliations

    • Division of Vascular Ultrasound Research, Wake Forest University School of Medicine, Winston-Salem, North Carolina, USA
  • ,
  • Eric Boerwinkle, PhD

      Affiliations

    • Human Genetics Center and Institute of Molecular Medicine, Houston, Health Sciences Center, University of Texas, Houston, Texas, USA
  • ,
  • Gerald S. Berenson, MD

      Affiliations

    • Tulane Center for Cardiovascular Health and Department of Epidemiology, New Orleans, Louisiana, USA
    • Corresponding Author InformationCorresponding author: Gerald S. Berenson, MD, Tulane Center for Cardiovascular Health, 1440 Canal Street, Suite 1829, New Orleans, Louisiana 70112. Tel: 504-988-7182; fax: 504-988-7194.

Received 6 May 2007 ,Accepted 13 June 2007.

References 

  1. Grobbee DE, Bots ML. Carotid artery intima-media thickness as an indicator of generalized atherosclerosis. J Intern Med. 1994;236:567–573
  2. Sarzynska-Dlugosz I, Nowaczenko M. Common carotid artery intima-media thickness: the role in evaluation of atherosclerosis progression. Neurol Neurochir Pol. 2001;35:1093–1102
  3. Burke GL, Evans GW, Riley WA, Sharrett AR, Howard G, Barnes RW, et al. Arterial wall thickness is associated with prevalent cardiovascular disease in middle-aged adults: the Atherosclerosis Risk in Communities (ARIC) Study. Stroke. 1995;26:386–391
  4. Hodis HN, Mack WJ, LaBree L, Selzer RH, Liu CR, Liu CH, et al. The role of carotid arterial intima-media thickness in predicting clinical coronary events. Ann Intern Med. 1998;128:262–269
  5. Heiss G, Sharrett AR, Barnes R, Chambless LE, Szklo M, Alzola C. Carotid atherosclerosis measured by B-mode ultrasound in populations: associations with cardiovascular risk factors in the ARIC Study. Am J Epidemiol. 1991;134:250–256
  6. Urbina EM, Srinivasan SR, Tang R, Bond MG, Kieltyka L, Berenson GS Bogalusa Heart Study. Impact of multiple coronary risk factors on the intima-media thickness of different segments of carotid artery in healthy young adults (the Bogalusa Heart Study). Am J Cardiol. 2002;90:953–958
  7. Bhuiyan AR, Srinivasan SR, Chen W, Paul TK, Berenson GS. Correlates of vascular structure and function measures in asymptomatic young adults: the Bogalusa Heart Study. Atherosclerosis. 2006;189:1–7
  8. Scuteri A, Najjar SS, Muller DC, Andres R, Hougaku H, Metter EJ, et al. Metabolic syndrome amplifies the age-associated increases in vascular thickness and stiffness. J Am Coll Cardiol. 2004;43:1388–1395
  9. Duggirala R, Gonzalez Villalpando C, O’Leary DH, Stern MP, Blangero L. Genetic basis of variation in carotid artery wall thickness. Stroke. 1996;27:833–837
  10. Zannad F, Visvikis S, Gueguen R, Sass C, Chapet O, Herbeth B, et al. Genetics strongly determines the wall thickness of the left and right carotid arteries. Hum Genet. 1998;103:183–188
  11. Arnett DK, Borecki IB, Ludwig EH, Pankow JS, Myers R, Evans G, et al. Angiotensinogen and angiotensin converting enzyme genotypes and carotid atherosclerosis: the Atherosclerosis Risk in Communities and the NHLBI Family Heart Studies. Atherosclerosis. 1998;138:111–116
  12. Bhuiyan AR, Chen W, Srinivasan SR, Rice J, Mock N, Tang R, et al. G-6A polymorphism of angiotensinogen gene modulates the effect of blood pressure on carotid intima–media thickness: the Bogalusa Heart Study. In press.
  13. Bozec E, Fassot C, Tropeano AI, Boutouyrie P, Jeunemaitre X, Lacolley P, et al. Angiotensinogen gene M235T polymorphism and reduction in wall thickness in response to antihypertensive treatment. Clin Sci. 2003;105:637–644
  14. Palmer RM, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 1987;327:524–526
  15. Wilkinson IB, MacCallum H, Cockcroft JR, Webb DJ. Inhibition of basal nitric oxide synthesis increases aortic augmentation index and pulse wave velocity in vivo. Br J Clin Pharmacol. 2002;53:189–192
  16. Chen W, Srinivasan SR, Bond MG, Tang R, Urbina EM, Li S, et al. Nitric oxide synthase gene polymorphism (G894T) influences arterial stiffness in adults: the Bogalusa Heart Study. Am J Hypertens. 2004;17:553–559
  17. Rees DD, Palmer RM, Moncada S. Role of endothelium-derived nitric oxide in the regulation of blood pressure. Proc Natl Acad Sci U S A. 1989;86:3375–3378
  18. Chen W, Srinivasan SR, Li S, Boerwinkle E, Berenson GS. Gender specific influence of NO synthase gene on blood pressure since childhood: the Bogalusa Heart Study. Hypertension. 2004;44:668–673
  19. Chen W, Srinivasan SR, Elkasabany A, Ellsworth DL, Boerwinkle E, Berenson GS. Combined effects of endothelial nitric oxide synthase gene polymorphism (G894T) and insulin resistance status on blood pressure and familial risk of hypertension in young adults: the Bogalusa Heart Study. Am J Hypertens. 2001;14:1046–1052
  20. Marsden PA, Heng HH, Scherer SW, Stewart RJ, Hall AV, Shi XM, et al. Structure and chromosomal localization of the human constitutive endothelial nitric oxide synthase gene. J Biol Chem. 1993;268:17478–17488
  21. Paradossi U, Ciofini E, Clerico A, Botto N, Biagini A, Colombo MG. 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;35:1305–1309
  22. Czarnecka D, Kawecka-Jaszcz K, Stolarz K, Olszanecka A, Dembinska-Kiec A, Kiec-Wilk B. Ambulatory blood pressure, left ventricular mass and vascular phenotypes in relation to the endothelial nitric oxide synthase gene Glu298Asp and intron 4 polymorphisms in a population-based family study. J Hum Hypertens. 2005;19:413–420
  23. Lembo G, De Luca N, Battagli C, Iovino G, Aretini A, Musicco M, et al. A common variant of endothelial nitric oxide synthase (Glu298Asp) is an independent risk factor for carotid atherosclerosis. Stroke. 2001;32:735–740
  24. Fatini C, Sofi F, Gensini F, Sticchi E, Lari B, Pratesi G, et al. Influence of eNOS gene polymorphisms on carotid atherosclerosis. Eur J Vasc Endovasc Surg. 2004;27:540–544
  25. Spoto B, Benedetto FA, Testa A, Tripepi G, Mallamaci F, Maas R, et al. Atherosclerosis and the Glu298Asp polymorphism of the eNOS gene in white patients with end–stage renal disease. Am J Hypertens. 2005;18:1549–1555
  26. Wolff B, Braun C, Schluter C, Grabe HJ, Popowski K, Volzke H, et al. Endothelial nitric oxide synthase Glu(298)––>Asp polymorphism, carotid atherosclerosis and intima-media thickness in a general population sample. Clin Sci (Lond). 2005;109:475–481
  27. Takaoka M. NOS gene polymorphism. Nippon Rinsho. 2004;62:103–109
  28. Karvonen J, Kauma H, Kervinen K, Rantala M, Ikaheimo M, Paivansalo M, et al. Endothelial nitric oxide synthase gene Glu298Asp polymorphism and blood pressure, left ventricular mass and carotid artery atherosclerosis in a population-based cohort. J Intern Med. 2002;251:102–110
  29. Asakimori Y, Yorioka N, Tanaka J, Kohno N. Effect of polymorphism of the endothelial nitric oxide synthase and apolipoprotein E genes on carotid atherosclerosis in hemodialysis patients. Am J Kidney Dis. 2003;41:822–832
  30. The Bogalusa Heart Study 20th anniversary symposium. Am J Med Symposium. 1995;310(suppl 1):S1–S138
  31. Srinivasan SR, Berenson GS. Serum lipoproteins in children and methods for study. In:  Lewis LA editors. CRC handbook of electrophoresis (v. III. Lipoprotein methodology and human studies). Boca Raton, Florida: CRC Press; 1983;p. 185–204
  32. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412–419
  33. Bond MG, Barnes RW, Riley WA, Wilmoth SK, Chambless LE, Howard G, et al. ARIC Study Group high resolution B-mode ultrasound scanning methods in the Atherosclerosis Risk in Communities Study (ARIC). J Neuroimaging. 1991;1:68–73
  34. Tang R, Hennig M, Thomasson B, Scherz R, Ravinetto R, Catalini R, et al. Baseline reproducibility of B–mode ultrasonic measurement of carotid artery intima–media thickness: the European Lacidipine Study on Atherosclerosis (ELSA). J Hypertens. 2000;18:197–201
  35. Neter J, Wasserman W, Kutner MH. Applied linear statistical models: regression, analysis of variance and experimental designs. In: 3rd ed.. Homewood, Illinois and Boston, Massachusetts: IRWIN; 1990;p. 225–236730–50
  36. Wang XL, Mahaney MC, Sim AS, Wang J, Wang J, Blangero J, et al. Genetic contribution of the endothelial constitutive nitric oxide synthase gene to plasma nitric oxide levels. Arterioscler Thromb Vasc Biol. 1997;17:3147–3153
  37. Miyazaki H, Matsuoka H, Cooke JP, Usui M, Ueda S, Okuda S, et al. Endogenous nitric oxide synthase inhibitor: a novel marker of atherosclerosis. Circulation. 1999;99:1141–1146
  38. Garg UC, Hassid A. Nitric oxide–generating vasodilators and 8–bromo–cyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J Clin Invest. 1989;83:1774–1777
  39. Jeremy JY, Rowe D, Emsley AM, Newby AC. Nitric oxide and the proliferation of vascular smooth muscle cells. Cardiovasc Res. 1999;43:580–594
  40. McDonald DM, Alp NJ, Channon KM. Functional comparison of the endothelial nitric oxide synthase Glu298Asp polymorphic variants in human endothelial cells. Pharmacogenetics. 2004;14:831–839
  41. Lander ES, Schork NJ. Genetic dissection of complex traits. Science. 1994;265:2037–2048
  42. Burt VL, Whelton P, Roccella EJ, Brown C, Cutler JA, Higgins M, et al. Prevalence of hypertension in the United States adult population (Results from the Third National Health and Nutrition Examination Survey, 1988–1991). Hypertension. 1995;25:305–313
  43. Cornoni–Huntley J, LaCroix AZ, Havlik RJ. Race and sex differentials in the impact of hypertension in the United States (The National Health and Nutrition Examination Survey I: Epidemiologic follow-up study). Arch Intern Med. 1989;149:780–788
  44. Kalinowski L, Dobrucki IT, Malinski T. Race–specific differences in endothelial function: predisposition of African-Americans to vascular diseases. Circulation. 2004;109:2511–2517
  45. Gibbons GH, Liew CC, Goodarzi MO, Rotter JI, Hsueh WA, Siragy HM, et al. Genetic markers: progress and potential for cardiovascular disease. Circulation. 2004;109(25 suppl 1):IV47–IV58
  46. Tabor HK, Risch NJ, Myers RM. Candidate-gene approaches for studying complex genetic traits: practical considerations. Nat Rev Genet. 2002;3:391–397

 This study was supported by Grants HD-047247 from the National Institute of Child Health and Human Development, 0555168B from the American Heart Association, AG-16592 from the National Institute on Aging and HL-38844 from the National Heart, Lung, and Blood Institute.

 Conflict of interest: none.

PII: S1933-1711(07)00131-3

doi: 10.1016/j.jash.2007.06.006

Journal of the American Society of Hypertension
Volume 1, Issue 5 , Pages 362-368 , September 2007