Role of asymmetrical dimethylarginine in the progression of renal disease

Nephrology

Volumn 18, Issue 1, 2013, Pages 11-21

  Raptis, Vasileios ^a   Kapoulas, Stergios ^a   Grekas, Dimitrios ^a  

^a AHEPA UNIVERSITY HOSPITAL   (Greece)

Author keywords

asymmetric dimethylarginine; chronic kidney disease progression; dimethylarginine dimethylamino hydrolase; endothelial dysfunction; nitric oxide deficiency; nitric oxide synthase inhibitors; proteinuria; renal fibrosis

Indexed keywords

COLLAGEN TYPE 1; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; N(G),N(G) DIMETHYLARGININE; NEURONAL NITRIC OXIDE SYNTHASE; REACTIVE OXYGEN METABOLITE; TRANSFORMING GROWTH FACTOR BETA1;

BLOOD VESSEL PERMEABILITY; BLOOD VESSEL TONE; CARDIOVASCULAR MORTALITY; CELL PROLIFERATION; CELLS; CHRONIC KIDNEY DISEASE; CORONARY ARTERY DISEASE; DIABETES MELLITUS; DISEASE COURSE; DNA POLYMORPHISM; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME ACTIVITY; GENE SILENCING; HUMAN; HYPERTENSION; INTERSTITIAL NEPHRITIS; NITROSYLATION; NONHUMAN; OXIDATIVE STRESS; PERIPHERAL VASCULAR DISEASE; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METHYLATION; PROTEINURIA; PULMONARY HYPERTENSION; REVIEW; RNA SYNTHESIS; SHEAR STRESS; VASODILATATION;

ARGININE; DISEASE PROGRESSION; HUMANS; KIDNEY DISEASES;

EID: 84872848363     PISSN: 13205358     EISSN: 14401797     Source Type: Journal    
DOI: 10.1111/j.1440-1797.2012.01659.x     Document Type: Review

References (113)

1. National Kidney Foundation. K/DOQI clinical practice guidelines for chronic kidney disease: Evaluation, classification, and stratification. Am. J. Kidney Dis. 2002; 39: S1-266.
2. Levey AS, Stevens LA, Coresh J,. Conceptual model of CKD: Applications and implications. Am. J. Kidney Dis. 2009; 53: S4-16.
3. Levey AS, Eckardt KU, Tsukamoto Y, et al. Definition and classification of chronic kidney disease: A position statement from Kidney Disease: Improving Global Outcomes (KDIGO). Kidney Int. 2005; 67: 2089-2100.
4. Levey AS, de Jong PE, Coresh J, et al. The definition, classification, and prognosis of chronic kidney disease: A KDIGO Controversies Conference report. Kidney Int. 2011; 80 (1): 17-28.
5. Coresh J, Selvin E, Stevens LA, et al. Prevalence of chronic kidney disease in the United States. JAMA 2007; 298: 2038-2047.
6. Hallan SI, Coresh J, Astor BC, et al. International comparison of the relationship of chronic kidney disease prevalence and ESRD risk. J. Am. Soc. Nephrol. 2006; 17: 2275-2284.
7. Chadban SJ, Briganti EM, Kerr PG, et al. Prevalence of kidney damage in Australian adults: The AusDiab kidney study. J. Am. Soc. Nephrol. 2003; 14: S131-138.
8. Imai E, Matsuo S,. Chronic kidney disease in Asia. Lancet 2008; 371: 2147-2214.
9. Kronenber F,. Emerging risk factors and markers of chronic kidney disease progression. Nat. Rev. Nephrol. 2009; 5: 677-689.
10. Kielstein JT, Boger RH, Bode-Boger SM, et al. Marked increase of asymmetric dimethylarginine in patients with incipient primary chronic renal disease. J. Am. Soc. Nephrol. 2002; 13: 170-176.
11. Caglar K, Yilmaz MI, Sonmez A, et al. ADMA, proteinuria, and insulin resistance in non-diabetic stage I chronic kidney disease. Kidney Int. 2006; 70: 781-787.
12. Kielstein JT, Martens-Lobenhoffer J, Vollmer S, Bode-Bger SM,. L-Arginine, ADMA, SDMA, creatinine, MDRD formula: Detour to renal function testing. J. Nephrol. 2008; 21: 959-961.
13. Panichi V, Mantuano E, Paoletti S, et al. Effect of simvastatin on plasma asymmetric dimethylarginine concentration in patients with chronic kidney disease. J. Nephrol. 2008; 21: 38-44.
14. Wang D, Strandgaard S, Borresen ML, et al. Asymmetric dimethylarginine and lipid peroxidation products in early autosomal dominant polycystic kidney disease. Am. J. Kidney Dis. 2008; 51 (2): 184-191.
15. Zoccali C, Benedetto FA, Maas R, et al. Asymmetric dimethylarginine, C-reactive protein, and carotid intima-media thickness in end-stage renal disease. J. Am. Soc. Nephrol. 2002; 13: 490-496.
16. Fliser D, Kronenberg F, Kielstein JT, et al. Asymmetric dimethylarginine and progression of chronic kidney disease: The mild to moderate kidney disease study. J. Am. Soc. Nephrol. 2005; 16: 2456-2461.
17. 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.
18. Schwedhelm E, Böger RH,. The role of asymmetric and symmetric dimethylarginines in renal disease. Nat. Rev. Nephrol. 2011; 7 (5): 275-278.
19. Davignon J, Ganz P,. Role of endothelial dysfunction in atherosclerosis. Circulation 2004; 109: III27-III32.
20. Deanfield JE, Halcox JP, Rabelink TJ,. Endothelial function and dysfunction: Testing and clinical relevance. Circulation 2007; 115: 1285-1295.
21. Mohler ER III,. Endothelialdysfunction. UpToDate[Internet] 2006; [updated 2012, cited 18 Jan 2012.] Available from URL: http://www.uptodate.com/contents/ endothelial-dysfunction
22. Gokce N,. L-Arginine and hypertension. J. Nutr. 2004; 134: 2807S-2811.
23. Landim MBP, Filho AC, Chagas ACP,. Asymmetric dimethylarginine (ADMA) and endothelial dysfunction: Implications for atherogenesis. Clinics 2009; 64 (5): 471-478.
24. Baylis C,. Arginine, arginine analogs and nitic oxide production in chronic kidney disease. Nat. Clin. Pract. Nephrol. 2006; 2 (4): 209-220.
25. Himmelfarb L,. Linking oxidative stress and inflammation in kidney disease: Which is the chicken and which is the egg? Semin. Dial. 2004; 17: 449-454.
26. Zatz R, Baylis C,. Chronic nitric oxide inhibitation model six years on. Hypertension 1998; 32: 958-964.
27. Vallance P, Leiper J,. Cardiovascular biology of the asymmetric dimethylarginine: Dimethylarginine dimethylaminohydrolase pathway. Arterioscler. Thromb. Vasc. Biol. 2004; 24: 1023-1030.
28. Boger RH, Bode-Boger SM, Szuba A, et al. Asymmetric dimethylarginine (ADMA): A novel risk factor for endothelial dysfunction: Its role in hypercholesterolaemia. Circulation 1998; 98: 1842-1847.
29. Clarke S,. Protein methylation. Curr. Opin. Cell Biol. 1993; 5: 977-983.
30. McBride AE, Silver PA,. State of the Arg: Protein methylation at arginine comes of age. Cell 2001; 106: 5-8.
31. Devés R, Boyd CAR,. Transporters for cationic amino acids in animal cells: Discovery, structure, and function. Physiol. Rev. 1998; 78: 487-545.
32. Casellas P, Jeanteur P,. Protein methylation in animal cells. I. Purification and properties of Sadenosyl-L-methionine: Protein (arginine) N-methyltransferase from Krebs II ascites cells. Biochim. Biophys. Acta 1978; 519: 243-254.
33. Casellas P, Jeanteur P,. Protein methylation in animal cells. II. Inhibition of S-adenosyl-L-methionine: Protein (arginine) N-methyltransferase by analogs of S-adenosyl-L-homocysteine. Biochim. Biophys. Acta 1978; 519: 255-268.
34. Leiper J, Vallance P,. Biological significance of endogenous methylarginines that inhibit nitric oxide synthases. Cardiovasc. Res. 1999; 43: 542-548.
35. Closs E, Basha FZ, Habermeier A, Forstermann U,. Interference of L-arginine analogues with L-arginine transport mediated by the y+carrier hCAT-2B. Nitric. Oxide 1997; 1: 65-73.
36. Brunini T, Moss M, Siqueira M, et al. Inhibition of l-arginine transport in platelets by asymmetric dimethylarginine and Nmonomethyl- l-arginine: Effects of arterial hypertension. Clin. Exp. Pharmacol. Physiol. 2004; 31: 738-740.
37. Scalera F, Kielstein JT, Martens-Lobenhoffer J, Postel SC, Täger M, Bode-Böger SM,. Erythropoietin increases asymmetric dimethylarginine in endothelial cells: Role of Dimethylarginine dimethylaminohydrolase. J. Am. Soc. Nephrol. 2005; 16: 892-898.
38. Ueno S, Sano A, Kotani K, Kondoh K, Kakimoto Y,. Distribution of free methylarginines in rat tissues and in the bovine brain. J. Neurochem. 1992; 59: 2012-2016.
39. Osnai T, Saitoh M, Sasaki S, Tomita H, Matsunaga T, Okumura K,. Effect of shear stress on asymmetric dimethylardinine release from vascular endothelial cells. Hypertension 2003; 42: 985-990.
40. Böger RH, Sydow K, Borlak J, et al. LDL cholesterol upregulates synthesis of asymmetrical dimethylarginine in human endothelial cells: Involvement of S-adenosylmethionine-dependent methyltransferases. Circ. Res. 2000; 87: 99-105.
41. Vallance P, Leone A, Calver A, et al. Accumulation of an endogenous inhibitor of nitric oxide synthesis in chronic renal failure. Lancet 1992; 339: 572-576.
42. MacAllister R, Whitley G, Vallance P,. Effect of guanidine and uremic compounds on nitric oxide pathways. Kidney Int. 1994; 45: 737-742.
43. Osamu S, Masato T, Tsuyoshi M, et al. Asymmetric dimethylarginine produces vascular lesions in endothelial nitric oxide synthase-deficient mice. Involvement of renin-angiotensin system and oxidative stress. Arterioscler. Thromb. Vasc. Biol. 2004; 24: 1682-1688.
44. G-methyl-L-arginine functions as an alternative substance and mechanism-based inhibitor of nitric oxide synthase. Biochemistry 1993; 32: 9677-9685.
45. Pou S, Keaton L, Surichamom W, Rosen GM,. Mechanism of superoxide generation by neuronal nitric oxide synthase. J. Biol. Chem. 1999; 274: 9573-9580.
46. Wang D, Gill SP, Chabrashvili T, et al. Isoform-specific regulation by NG,NG-Dimethylarginine dimethylaminohydrolase of rat serum asymmetric dimethylarginine and vascular endothelium-derived relaxing factor/NO. Circ. Res. 2007; 101 (6): 627-635.
47. + ATPase activity. J. Neurochem. 1976; 27: 635-636.
48. Kajimoto H, Kai H, Aoki H, et al. Inhibition of eNOS phosphorylation mediates endothelial dysfunction in renal failure: New effect of asymmetric dimethylarginine. Kidney Int. 2012; 81 (8): 762-768.
49. Bogle RG, MacAllister RJ, Whitley GS, Vallance P,. Induction of NG-monomethyl-L-arginine uptake: A mechanism for differential inhibitor of NO synthases? Am. J. Physiol. 1995; 269: C750-756.
50. Cardounel AJ, Zweier JL,. Endogenous methylarginines regulate neuronal nitric-oxide synthase and prevent excitotoxic injury. J. Biol. Chem. 2002; 277: 33995-34002.
51. MacAllister R, Parry H, Kimoto M, et al. Regulation of nitric oxide synthesis by Dimethylarginine dimethylaminohydrolase. Br. J. Pharmacol. 1996; 119: 1533-1540.
52. Teerlink T,. HPLC analysis of ADMA and other methylated L-arginine analogs in biological fluids. J. Chromatogr. B. Analyt Technol Biomed Life Sci. 2007; 851 (1-2): 21-29.
53. Schulze F, Wesemann R, Schwedhelm E, et al. Determination of asymmetric dimethylarginine (ADMA) using a novel ELISA assay. Clin. Chem. Lab. Med. 2004; 42 (12): 1377-1383.
54. Tong BC, Barbul A,. Cellular and physiological effects of arginine. Mini Rev. Med. Chem. 2004; 4: 823-832.
55. McDermott JR,. Studies on the catabolism of Ng-methylarginine, Ng, Ng-dimethylarginine and Ng, Ng-dimethylarginine in the rabbit. Biochem. J. 1976; 154: 179-184.
56. Ogawa T, Kimoto M, Watanabe H, Sasaoka K,. Metabolism of NG NG-dimethylarginine and NG NGdimethylarginine in rats. Arch. Biochem. Biophys. 1987; 252: 526-537.
57. Kimoto M, Whitley GS, Tsuji H, Ogawa T,. Detection of NG, NG-Dimethylarginine dimethylaminohydrolase in human tissues using a monoclonal antibody. J. Biochem. (Tokyo) 1995; 117: 237-238.
58. Leiper J, Murray-Rust J, McDonald N, Vallance P,. S-nitrosylation of dimethylarginine dimethylaminohydrolase regulates enzyme activity: Further interactions between nitric oxide synthase and dimethylarginine dimethylaminohydrolase. Proc. Natl Acad. Sci. U.S.A. 2002; 99: 13527-13532.
59. Murray-Rust J, Leiper J, McAlister M, et al. Structural insights into the hydrolysis of cellular nitric oxide synthase inhibitors by dimethylarginine dimethylaminohydrolase. Nat. Struct. Biol. 2001; 8: 679-683.
60. Tran CTL, Fox MF, Vallance P, Leiper J,. Chromosomal localization, gene structure and expression pattern of DDAH1: Comparison with DDAH2 and implications for evolutionary origins. Genomics 2000; 68: 101-105.
61. Leiper J, MacAllister R, Whitley G, et al. Identification of two human Dimethylarginine dimethylaminohydrolase s with distinct tissue distributions and homology to microbial arginine deiminases. Biochem. J. 1999; 343: 209-214.
62. Akbar F, Heinonen S, Pirskanen M, Uimari P, Tuomainen TP, Salonen JT,. Haplotypic association of DDAH1 with susceptibility to pre-eclampsia. Mol. Hum. Reprod. 2005; 11: 73-77.
63. Böger RH, Zoccali C,. ADMA: A novel risk factor that explains excess cardiovascular event rate in patients with end-stage renal disease. Atherosclerosis 2003; 4: (Suppl 4): S23-28.
64. Fleck C, Janz A, Schweitzer F, Karge E, Schwertfeger M, Stein G,. Serum concentrations of asymmetric (ADMA) and symmetric (SDMA) dimethylarginine in renal failure patients. Kidney Int. Suppl. 2001; 78: S14-18.
65. Nijveldt RJ, Van Leeuwen PA, Van Guldener C, Stehouwer CD, Rauwerda JA, Teerlink T,. Net renal extraction of asymmetrical (ADMA) and symmetrical (SDMA) dimethylarginine in fasting humans. Nephrol. Dial. Transplant. 2002; 17: 1999-2002.
66. Achan V, Broadhead M, Malaki M, et al. Asymmetric dimethylarginine causes hypertension and cardiac dysfunction in humans and is actively metabolized by dimethylarginine dimethylaminohydrolase. Arterioscler. Thromb. Vasc. Biol. 2003; 23: 1455-1459.
67. Pope AJ, Karuppiah K, Cardounel AJ,. Role of the PRMT-DDAH-ADMA axis in the regulation of endothelial nitric oxide production. Pharmacol. Res. 2009; 60 (6): 461-465.
68. Hu X, Atzler D, Xu X, et al. Dimethylarginine dimethylaminohydrolase-1 is the critical enzyme for degrading the cardiovascular risk factor asymmetrical dimethylarginine. Arterioscler. Thromb. Vasc. Biol. 2011; 31 (7): 1540-1546.
69. Ding H, Wu B, Wang H, et al. A novel loss-of-function DDAH1 promoter polymorphism is associated with increased susceptibility to thrombosis stroke and coronary heart disease. Circ. Res. 2010; 106 (6): 1145-1152.
70. Zoccali C, Kielstein JT,. Asymmetric dimethylarginine: A new player in the pathogenesis of renal disease? Curr. Opin. Nephrol. Hypertens. 2006; 15: 314-320.
71. Young JM, Terrin N, Wang X, et al. Asymmetric dimethylarginine and mortality in stages 3 to 4 chronic kidney disease. Clin. J. Am. Soc. Nephrol. 2009; 4 (6): 1115-1120.
72. Miyazaki H, Matsuoka H, Cooke JP, et al. Endogenous nitric oxide synthase inhibitor: A novel marker of atherosclerosis. Circulation 1999; 99: 1141-1146.
73. Zoccali C, Bode-Boger S, Mallamci 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.
74. Vallance P, Leiper J,. ADMA and kidney disease-marker or mediator. J. Am. Soc. Nephrol. 2005; 16: 2254-2256.
75. Pecchini P, Malberti F, Mieth M, et al. Measuring asymmetric dimethylarginine (ADMA) in CKD: A comparison between enzyme-linked immunosorbent assay and liquid chromatography-electrospray tandem mass spectrometry. J. Nephrol. 2012; doi: 10.5301/jn.5000085
76. Arnal J-F, Michel J-B, Harrison DG,. Nitric oxide in the pathogenesis of hypertension. Curr. Opin. Nephrol. Hypertens. 1995; 4: 182-188.
77. Matsuoka H, Itoh S, Kimoto M, et al. Asymmetrical dimethylarginine, an endogenous nitric oxide synthase inhibitor, in experimental hypertension. Hypertension 1997; 29: 242-247.
78. Mihout F, Shweke N, Bigé N, et al. Asymmetric dimethylarginine (ADMA) induces chronic kidney disease through a mechanism involving collagen and TGF-β1 synthesis. J. Pathol. 2011; 223: 37-45.
79. Caplin B, Leiper J,. Endogenous nitric oxide synthase inhibitors in the biology of disease: Markers, mediators, and regulators? Arterioscler. Thromb. Vasc. Biol. 2012; 32 (6): 1343-1353.
80. Perticone F, Sciacqua A, Maio R, et al. Endothelial dysfunction, ADMA and insulin resistance in essential hypertension. Int. J. Cardiol. 2010; 142 (3): 236-241.
81. 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.
82. Curgunlu A, Uzun H, Bavunoǧlu I, Karter Y, Genç H, Vehid S,. Increased circulating concentrations of asymmetric dimethylarginine (ADMA) in white coat hypertension. J. Hum. Hypertens. 2005; 19 (8): 629-633.
83. Kielstein JT, Simmel S, Bode-Böger SM, et al. Suppressor dose asymmetric dimethylarginine modulates renal function in humans through nitric oxide synthase inhibition. Kidney Blood Press. Res. 2004; 27 (3): 143-147.
84. Cabral PD, Garvin JL,. Luminal flow regulates NO and O2(-) along the nephron. Am. J. Physiol. Renal Physiol. 2011; 300 (5): F1047-1053.
85. Böger RH, Bode-Böger SM, Tsao PS, Lin PS, Chan JR, Cooke JP,. An endogenous inhibitor of nitric oxide synthase regulates endothelial adhesiveness for monocytes. J. Am. Coll. Cardiol. 2000; 36: 2287-2295.
86. Mount PF, Power DA,. Nitric oxide in the kidney: Functions and regulation of synthesis. Acta Physiol. (Oxf.) 2006; 187 (4): 433-446.
87. Fujiwara N, Osanai T, Kamada T, Katoh T, Takahashi K, Okumura K,. Study on the relationship between plasma nitrite and nitrate level and salt sensitivity in human hypertension: Modulation of nitric oxide synthesis by salt intake. Circulation 2000; 101 (8): 856-861.
88. Arcos MI, Fujihara CK, Sesso A, et al. Mechanisms of albuminuria in the chronic nitric oxide inhibition model. Am. J. Physiol. Renal Physiol. 2000; 279: F1060-1066.
89. Sharma M, McCarthy ET, Savin VJ, Lianos EA,. Nitric oxide preserves the glomerular protein permeability barrier by antagonizing superoxide. Kidney Int. 2005; 68: 2735-2744.
90. 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: 1386-1395.
91. Shibata R, Ueda S, Yamagishi S, et al. Involvement of asymmetric dimethylarginine (ADMA) in tubulointerstitialischaemia in the early phase of diabetic nephropathy. Nephrol. Dial. Transplant. 2009; 24 (4): 1162-1169.
92. Matsumoto Y, Ueda S, Yamagishi S, et al. Dimethylarginine dimethylaminohydrolase prevents progression of renal dysfunction by inhibiting loss of peritubular capillaries and tubulointerstitial fibrosis in a rat model of chronic kidney disease. J. Am. Soc. Nephrol. 2007; 18: 1525-1533.
93. Yilmaz MI, Sonmez A, Saglam M, et al. ADMA levels correlate with proteinuria, secondary amyloidosis, and endothelial dysfunction. J. Am. Soc. Nephrol. 2008; 19: 388-395.
94. Lücke T, Kanzelmeyer N, Chobanyan K, et al. Elevated asymmetric dimethylarginine (ADMA) and inverse correlation between circulating ADMA and glomerular filtration rate in children with sporadic focal segmental glomerulosclerosis (FSGS). Nephrol. Dial. Transplant. 2008; 23: 734-740.
95. Hanai K, Babazono T, Nyumura I, et al. Asymmetric dimethylarginine is closely associated with the development and progression of nephropathy in patients with type 2 diabetes. Nephrol. Dial. Transplan 2009; 24 (6): 1884-1888.
96. Yilmaz MI, Sonmez A, Saglam M, et al. Reduced proteinuria using ramipril in diabetic CKD stage 1 decreases circulating cell death receptor activators concurrently with ADMA. A novel pathophysiological pathway? Nephrol. Dial. Transplant. 2010; 25 (10): 3250-3256.
97. Kielstein JT, Fliser D,. Lowering asymmetric dimethylarginine: A new mechanism mediating the renoprotective effects of reninangiotensin system inhibitors in proteinuric patients? Blood Purif. 2007; 25: 324-326.
98. Yilmaz MI, Saglam M, Sonmez A, et al. Improving proteinuria, endothelial functions and asymmetric dimethylarginine levels in chronic kidney disease: Ramipril versus valsartan. Blood Purif. 2007; 25: 327-335.
99. Ueda S, Yamagishi S, Okuda S,. New pathways to renal damage: Role of ADMA in retarding renal disease progression. J. Nephrol. 2010; 23 (4): 377-386.
100. Nangaku M,. Chronic hypoxia and tubulointerstitial injury: A final common pathway to end-stage renal failure. J. Am. Soc. Nephrol. 2006; 17: 17-25.
101. Fine LG, Orphanides C, Norman JT,. Progressive renal disease: The chronic hypoxia hypothesis. Kidney Int. Suppl. 1998; 65: S74-78.
102. Kielstein JT, Zoccali C,. A new perspective for the treatment of renal diseases? J. Am. Soc. Nephrol. 2007; 18 (5): 1365-1367.
103. Yamada SS, Sassaki AL, Fujihara CK, Malheiros DM, De Nucci G, Zatz R,. Effect of salt intake and inhibitor dose on arterial hypertension and renal injury induced by chronic nitric oxide blockade. Hypertension 1996; 27 (5): 1165-1172.
104. Lajer M, Tarnow L, Jorsal A, Teerlink T, Parving HH, Rossing P,. Plasma concentration of asymmetric dimethylarginine (ADMA) predicts cardiovascular morbidity and mortality in type 1 diabetic patients with diabetic nephropathy. Diabetes Care 2008; 31 (4): 747-752.
105. Abedini S, Meinitzer A, Holme I, et al. Asymmetrical dimethylarginine is associated with renal and cardiovascular outcomes and all-cause mortality in renal transplant recipients. Kidney Int. 2010; 77: 44-50.
106. Caplin B, Nitsch D, Gill H, et al. Circulating methylarginine levels and the decline in renal function in patients with chronic kidney disease are modulated by DDAH1 polymorphisms. Kidney Int. 2010; 77 (5): 459-467.
107. Al Banchaabouchi M, Marescau B, Possemiers I, D'Hooge R, Levillain O, De Deyn PP,. NG, NG-dimethylarginine and NG, NG-dimethylarginine in renal insufficiency. Pflugers Arch. 2000; 439 (5): 524-531.
108. Teerlink T, Luo Z, Palm F, Wilcox CS,. Cellular ADMA: Regulation and action. Pharmacol. Res. 2009; 60 (6): 448-460.
109. Davids M, Teerlink T,. Asymmetric dimethylarginine (ADMA) and cardiovascular disease. Ned. Tijdschr. Klin. Chem. Labgeneesk 2012; 37: 10-14.
110. Delles C, Schneider MP, John S, Gekle M, Schmieder RE,. Angiotensin converting enzyme inhibition and angiotensin II AT1-receptor blockade reduce the levels of asymmetrical N(G), N(G)-dimethylarginine in human essential hypertension. Am. J. Hypertens. 2002; 15 (7 Pt 1): 590-593.
111. Ito A, Egashira K, Narishige T, Muramatsu K, Takeshita A,. Renin-angiotensin system is involved in the mechanism of increased serum asymmetric dimethylarginine in essential hypertension. Jpn Circ. J. 2001; 65 (9): 775-778.
112. Napoli C, Sica V, de, Nigris F, et al. Sulfhydryl angiotensin-converting enzyme inhibition induces sustained reduction of systemic oxidative stress and improves the nitric oxide pathway in patients with essential hypertension. Am. Heart J. 2004; 148 (1): e5.
113. Dayoub H, Achan V, Adimoolam S, et al. Dimethylarginine dimethylaminohydrolase regulates nitric oxide synthesis: Genetic and physiological evidence. Circulation 2003; 108 (24): 3042-3047.