Serum asymmetric dimethylarginine and arginine levels predict microvascular and macrovascular complications in type 2 diabetes mellitus

Diabetes/Metabolism Research and Reviews

Volumn 33, Issue 2, 2017, Pages

  Ganz, Tali ^a,b   Wainstein, Julio ^a,b   Gilad, Suzan ^c   Limor, Rona ^c   Boaz, Mona ^a,d   Stern, Naftali ^b,c  

^a WOLFSON MEDICAL CENTER   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

^c TEL AVIV SOURASKY MEDICAL CENTER   (Israel)

^d ARIEL UNIVERSITY   (Israel)

Author keywords

diabetes complications; metabolic syndrome; obesity

Indexed keywords

ARGININE; HEMOGLOBIN A1C; N(G),N(G) DIMETHYLARGININE; BIOLOGICAL MARKER; N,N-DIMETHYLARGININE;

ADULT; AMINO ACID BLOOD LEVEL; ARTICLE; CEREBROVASCULAR ACCIDENT; CEREBROVASCULAR DISEASE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; DIABETIC RETINOPATHY; FEMALE; FOLLOW UP; HUMAN; MAJOR CLINICAL STUDY; MALE; MICROANGIOPATHY; NON INSULIN DEPENDENT DIABETES MELLITUS; OXIDATIVE STRESS; PERIPHERAL NEUROPATHY; PERIPHERAL VASCULAR DISEASE; PRIORITY JOURNAL; PROSPECTIVE STUDY; RISK ASSESSMENT; ADOLESCENT; AGED; ANALOGS AND DERIVATIVES; BLOOD; CARDIOVASCULAR DISEASES; CASE CONTROL STUDY; COMPARATIVE STUDY; COMPLICATION; CROSS-SECTIONAL STUDY; DIABETES COMPLICATIONS; MIDDLE AGED; PROGNOSIS; RISK FACTOR; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; ARGININE; BIOMARKERS; CARDIOVASCULAR DISEASES; CASE-CONTROL STUDIES; CROSS-SECTIONAL STUDIES; DIABETES COMPLICATIONS; DIABETES MELLITUS, TYPE 2; FEMALE; FOLLOW-UP STUDIES; HUMANS; MALE; MIDDLE AGED; OXIDATIVE STRESS; PROGNOSIS; PROSPECTIVE STUDIES; RISK FACTORS; YOUNG ADULT;

EID: 84994885657     PISSN: 15207552     EISSN: 15207560     Source Type: Journal    
DOI: 10.1002/dmrr.2836     Document Type: Article

References (68)

1. Flammer AJ, Lüscher TF. Human endothelial dysfunction: EDRFs. Pflugers Arch. 2010;459:1005–1013.
2. Manrique C, Lastra G, Sowers JR. New insights into insulin action and resistance in the vasculature. Ann N Y Acad Sci. 2014;1311:138–150.
3. Luiking YC, Ten Have GA, Wolfe RR, Deutz NE. Arginine de novo and nitric oxide production in disease states. Am J Physiol Endocrinol Metab. 2012;303:E1177–E1189.
4. Chin-Dusting JFP, Willems L, Kaye DM. l-Arginine transporters in cardiovascular disease: a novel therapeutic target. Pharmacol Ther. 2007;116:428–436.
5. Rochette L, Lorin J, Zeller M, et al. Nitrix oxide inhibition and oxidative stress in cardiovascular disease: possible therapeutic targets? Pharmacol Ther. 2013;140:239–257.
6. Clarke S. Protein methylation. Curr Opin Cell Biol. 1993;5:977–983.
7. Kielstein JT, Impraim B, Simmel S, et al. Cardiovascular effects of systemic nitric oxide synthase inhibition with asymmetrical dimethylarginine in humans. Circulation. 2004;109:172–177.
8. Laakso M, Edelman SV, Brechtel G, Baron AD. Decreased effect of insulin to stimulate skeletal muscle flow in obese men. J Clin Invest. 1990;85:1844–1852.
9. Cook S, Scherrer U. Insulin resistance, a new target for nitric oxide delivery drugs. Fundam Clin Pharmacol. 2002;16:441–453.
10. Kapur S, Bedard S, Marcotte B, Cote CH, Marette A. Expression of nitric oxide synthase I skeletal muscle: a novel role for nitric oxide as a modulator of insulin action. Diabetes. 1997;46:1691–1700.
11. Perticone F, Sciacqua A, Maio R, et al. Endothelial dysfunction, ADMA and insulin resistance in essential hypertension. Int J Cardiol. 2010;142:236–241.
12. Kielstein JT, Donnerstag F, Gasper S, et al. ADMA increases arterial stiffness and decreases cerebral blood flow in humans. Stroke. 2006;37:2024–2029.
13. Xia Y, Dawson V, Dawson T, Snyder S, Zweier J. Nitric oxide synthase generates superoxide and nitric oxide in arginine-depleted cells leading to peroxynitrite-mediated cellular injury. Proc Natl Acad Sci U S A. 1996;93:6770–6774.
14. Noris M, Todeschini M, Cassis P, et al. l-Arginine depletion in preeclampsia orients nitric oxide synthase toward oxidant species. Hypertension. 2004;43:614–622.
15. Förstermann U, Münzel T. Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation. 2006;113:1708–1714.
16. Schuhmacher S, Oelze M, Bollmann F, et al. Vascular dysfunction in experimental diabetes is improved by pentaerithrityl tetranitrate but not isosorbide-5-mononitrate therapy. Diabetes. 2011;60:2608–2616.
17. Schmidt K, Kolesnik B, Gorren AC, Werner ER, Mayer B. Cell type-specific recycling of tetrahydrobiopterin by dihydrofolate reductase explains differential effects of 7,8-dihydrobiopterin on endothelial nitric oxide synthase uncoupling. Biochem Pharmacol. 2014;90:246–253.
18. Sharma M, Zhou Z, Miura H, et al. ADMA injures the glomerular filtration barrier: role of nitric oxide and superoxide. Am J Physiol Renal Physiol. 2009;296:F1386–F1395.
19. Chan NN, Chan JCN. Asymetric dimethylarginine (ADMA): a potential link between endothelial dysfunction and cardiovascular disease in insulin resistence syndrome? Diabetologia. 2002;45:1609–1616.
20. Abbasi F, Asagmi T, Cooke P, et al. Plasma concentrations of asymmetric dimethylarginine are increased in patients with Type 2 diabetes mellitus. Am J Cardiol. 2001;88:1201–1203.
21. Altinova AE, Arslan M, Sepici-Dincel A, Akturk M, Altan N, Toruner FB. Uncomplicated type 1 diabetes is associated with increased asymmetric dimethylarginine concentrations. J Clin Endocrinol Metab. 2007;92:1881–1885.
22. Pereira EC, Ferderbar S, Bertolami MC, et al. Biomarkers of oxidative stress and endothelial dysfunction in glucose intolerance and diabetes mellitus. Clin Biochem. 2008;41:1454–1460.
23. Sugai M, Ohta A, Ogata Y, et al. Asymmetric dimethylarginine (ADMA) in the aqueous humor of diabetic patients. Endocr J. 2007;54:303–309.
24. Paiva H, Lehtimaki T, Laakso J, et al. Plasma concentrations of asymmetric dimethylarginine in type 2 diabetes associate with glycemic control and glomerular filtration rate but not with risk factors of vasculopathy. Metabolism. 2003;52:303–307.
25. Sibal L, Agarwal SC, Schwedhelm E, Luneburg N, Boger RH, Home PD. A study of endothelial function and circulating asymmetric dimethylarginine levels in people with type 1 diabetes without macrovascular disease or microalbuminuria. Cardiovasc Diabetol. 2009;8:27
26. Baylis C. Nitric oxide deficiency in chronic kidney disease. Am J Physiol Renal Physiol. 2008;294:F1–F9.
27. Yildirim AO, Bulau P, Zakrzewicz D, et al. Increased protein arginine methylation in chronic hypoxia: role of protein arginine methyltransferases. Am J Respir Cell Mol Biol. 2006;35:436–443.
28. Wang Z, Tang WH, Cho L, Brennan DM, Hazen SL. Targeted metabolomic evaluation of arginine methylation and cardiovascular risks: potential mechanisms beyond nitric oxide synthase inhibition. Arterioscler Thromb Vasc Biol. 2009;29:1383–1391.
29. Perticone F, Sciacqua A, Maio R, et al. Asymmetric dimethylarginine, l-arginine, and endothelial dysfunction in essential hypertension. J Am Coll Cardiol. 2005;46:518–523.
30. Kielstein JT, Bode-Böger SM, Frölich JC, Ritz E, Haller H, Fliser D. Asymmetric dimethylarginine, blood pressure, and renal perfusion in elderly subjects. Circulation. 2003;107:1891–1895.
31. Kanazawa I, Yano S, Notsu Y, Yamaguchi T, Nabika T, Sugimoto T. Asymmetric dimethylarginine as a risk factor for cardiovascular disease in Japanese patients with type 2 diabetes mellitus. Clin Endocrinol (Oxf). 2011;74:467–472.
32. Steinberg HO, Brechtel G, Johnson A, Fineberg N, Baron AD. Insulin-mediated skeletal muscle vasodilation is nitric oxide dependent. A novel action of insulin to increase nitric oxide release. J Clin Invest. 1994;94:1172–1179.
33. Lin KY, Ito A, Asagami T, et al. Impaired nitric oxide synthase pathway in diabetes mellitus. Circulation. 2002;106:987–992.
34. Teerlink T. Determination of the endogenous nitric oxide synthase inhibitor asymmetric dimethylarginine in biological samples by HPLC. Methods Mol Med. 2005;108:263–274.
35. Böger RH, Bode-Böger SM, Thiele W, Creutzig A, Alexander K, Frölich JC. Restoring vascular nitric oxide formation by l-arginine improves the symptoms of intermittent claudication in patients with peripheral arterial occlusive disease. J Am Coll Cardiol. 1998;32:1336–1344.
36. Bergström A, Staalsø JM, Romner B, Olsen NV. Impaired endothelial function after aneurysmal subarachnoid hemorrhage correlates with arginine: asymmetric dimethylarginine ratio. Br J Anaesth. 2014;112:311–318.
37. Bariş N, Erdoğan M, Sezer E, et al. Alterations in l-arginine and inflammatory markers in type 2 diabetic patients with and without microalbuminuria. Acta Diabetol. 2009;46:309–316.
38. Menge BA, Schrader H, Ritter PR, et al. Selective amino acid deficiency in patients with impaired glucose tolerance and type 2 diabetes. Regul Pept. 2010;160:75–80.
39. Mihalik SJ, Michaliszyn SF, de las Heras J, et al. Metabolomic profiling of fatty acid and amino acid metabolism in youth with obesity and type 2 diabetes: evidence for enhanced mitochondrial oxidation. Diabetes Care. 2012;35:605–611.
40. Malecki MT, Undas A, Cyganek K, et al. Plasma asymmetric dimethylarginine (ADMA) is associated with retinopathy in type 2 diabetes. Diabetes Care. 2007;30:2899–2901.
41. Adams MR, McCredie R, Jessup W, Robinson J, Sullivan D, Celermajer DS. Oral l-arginine improves endothelium-dependent dilatation and reduces monocyte adhesion to endothelial cells in young men with coronary artery disease. Atherosclerosis. 1997;129:261–269.
42. Hambrecht R, Hilbrich L, Erbs S, et al. Correction of endothelial dysfunction in chronic heart failure: additional effects of exercise training and oral l-arginine supplementation. J Am Coll Cardiol. 2000;35:706–713.
43. Clarkson P, Adams MR, Powe AJ, et al. Oral l-arginine improves endothelium-dependent dilation in hypercholesterolemic young adults. J Clin Invest. 1996;97:1989–1994.
44. Theilmeier G, Chan JR, Zalpour C, et al. Adhesiveness of mononuclear cells in hypercholesterolemic humans is normalized by dietary l-arginine. Arterioscler Thromb Vasc Biol. 1997;17:3557–3564.
45. Lerman A, Burnett JC, Higano ST, McKinley LJ, Holmes DR. Long-term l-arginine supplementation improves small vessel coronary endothelial function in humans. Circulation. 1998;97:2123–2128.
46. Lucotti P, Setola E, Monti LD, et al. Beneficial effects of a long-term oral l-arginine treatment added to a hypocaloric diet and exercise training program in obese, insulin-resistant type 2 diabetic patients. Am J Physiol Endocrinol Metab. 2006;291:E906–E912.
47. Mullen MJ, Wright D, Donald AE, Thorne S, Thomson H, Deanfield JE. Atorvastatin but not l-arginine improves endothelial function in type I diabetes mellitus: a double-blind study. J Am Coll Cardiol. 2000;36:410–416.
48. Patel C, Rojas M, Narayanan SP, et al. Arginase as a mediator of diabetic retinopathy. Front Immunol. 2013;4:173–183.
49. Ramírez-Zamora S, Méndez-Rodríguez ML, Olguín-Martínez M, et al. Increased erythrocytes by-products of arginine catabolism are associated with hyperglycemia and could be involved in the pathogenesis of type 2 diabetes mellitus. PLoS One. 2013;8(6):e66823
50. Morris SM Jr, Gao T, Cooper TK, Kepka-Lenhart D, Awad AS. Arginase-2 mediates diabetic renal injury. Diabetes. 2011;60:3015–3022.
51. Romero MJ, Platt DH, Tawfik HE, et al. Diabetes-induced coronary vascular dysfunction involves increased arginase activity. Circ Res. 2008;102:95–102.
52. You H, Gao T, Cooper TK, Morris SM Jr, Awad AS. Arginase inhibition mediates renal tissue protection in diabetic nephropathy by a nitric oxide synthase 3-dependent mechanism. Kidney Int. 2013;84:1189–1197.
53. Ogier de Baulny H, Schiff M, Dionisi-Vici C. Lysinuric protein intolerance (LPI): a multi organ disease by far more complex than a classic urea cycle disorder. Mol Genet Metab. 2012;106:12–17.
54. Lukkarinen M, Näntö-Salonen K, Pulkki K, Aalto M, Simell O. Oral supplementation corrects plasma lysine concentrations in lysinuric protein intolerance. Metabolism. 2003;52:935–938.
55. Kamada Y, Nagaretani H, Tamura S, et al. Vascular endothelial dysfunction resulting from l-arginine deficiency in a patient with lysinuric protein intolerance. J Clin Invest. 2001;108:717–724.
56. Donnini D, Zambito AM, Perrella G, Ambesi-Impiombato FS, Curcio F. Glucose may induce cell death through a free radical-mediated mechanism. Biochem Biophys Res Commun. 1996;219:412–417.
57. Pieper GM, Langenstroer P, Siebeneich W. Diabetic-induced endothelial dysfunction in rat aorta: role of hydroxyl radicals. Cardiovasc Res. 1997;34:145–156.
58. Krzyzanowska K, Mittermayer F, Wolzt M, Schernthaner G. Asymmetric dimethylarginine predicts cardiovascular events in patients with type 2 diabetes. Diabetes Care. 2007;30:1834–1839.
59. Cavusoglu E, Ruwende C, Chopra V, et al. Relation of baseline plasma ADMA levels to cardiovascular morbidity and mortality at two years in men with diabetes mellitus referred for coronary angiography. Atherosclerosis. 2010;210:226–231.
60. Zoccali C, Bode-Böger S, Mallamaci F, et al. Plasma concentration of asymmetrical dimethylarginine and mortality in patients with end-stage renal disease: a prospective study. Lancet. 2001;358:2113–2117.
61. Aucella F, Maas R, Vigilante M, et al. Methyl-arginines and mortality in patients with end stage renal disease: a prospective cohort study. Atherosclerosis. 2009;207:541–545.
62. Shi B, Ni Z, Zhou W, et al. Circulating levels of asymmetric dimethylarginine are an independent risk factor for left ventricular hypertrophy and predict cardiovascular events in pre-dialysis patients with chronic kidney disease. Eur J Intern Med. 2010;21:444–448.
63. Ravani P, Tripepi G, Malberti F, Testa S, Mallamaci F, Zoccali C. Asymmetrical dimethylarginine predicts progression to dialysis and death in patients with chronic kidney disease: a competing risks modeling approach. J Am Soc Nephrol. 2005;16:2449–2455.
64. Wilson AM, Shin DS, Weatherby C, et al. Asymmetric dimethylarginine correlates with measures of disease severity, major adverse cardiovascular events and all-cause mortality in patients with peripheral arterial disease. Vasc Med. 2010;15:267–274.
65. Kiechl S, Lee T, Santer P, et al. Asymmetric and symmetric dimethylarginines are of similar predictive value for cardiovascular risk in the general population. Atherosclerosis. 2009;205:261–265.
66. Böger RH, Sullivan LM, Schwedhelm E, et al. Plasma asymmetric dimethylarginine and incidence of cardiovascular disease and death in the community. Circulation. 2009;119:1592–1600.
67. Adams MR, McCredie R, Jessup W, Robinson J, Sullivan D, Celermajer DS. Oral l-arginine improves endothelium-dependent dilatation and reduces monocyte adhesion to endothelial cells in young men with coronary artery disease. Atherosclerosis. 1997;129:261–269.
68. Hambrecht R, Hilbrich L, Erbs S, et al. Correction of endothelial dysfunction in chronic heart failure: additional effects of exercise training and oral l-arginine supplementation. J Am Coll Cardiol. 2000;35:706–713.