Chapter 3 The Emerging Role of Symmetric Dimethylarginine in Vascular Disease

Advances in Clinical Chemistry

Volumn 48, Issue , 2009, Pages 73-94

  Mangoni, Arduino A ^a  

^a FLINDERS UNIVERSITY   (Australia)

Author keywords

Asymmetric dimethylarginine; Cardiovascular disease; Cardiovascular system; Endothelium; Nitric oxide; Symmetric dimethylarginine

Indexed keywords

ARGININE; DRUG DERIVATIVE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; N,N DIMETHYLARGININE; N,N' DIMETHYLARGININE; N,N'-DIMETHYLARGININE; N,N-DIMETHYLARGININE; NITRIC OXIDE;

BLOOD; CARDIOVASCULAR DISEASE; CHEMISTRY; HOMEOSTASIS; HUMAN; KIDNEY FAILURE; METABOLISM; PHYSIOLOGY; REVIEW;

ARGININE; CARDIOVASCULAR DISEASES; HOMEOSTASIS; HUMANS; KIDNEY FAILURE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III;

EID: 69449095139     PISSN: 00652423     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0065-2423(09)48003-X     Document Type: Review

References (96)

1. Ignarro L.J. Nitric oxide as a unique signaling molecule in the vascular system: a historical overview. J. Physiol. Pharmacol. 53 (2002) 503-514
2. Ignarro L.J., and Napoli C. Novel features of nitric oxide, endothelial nitric oxide synthase, and atherosclerosis. Curr. Atheroscler. Rep. 6 (2004) 281-287
3. Wilkinson I.B., Franklin S.S., and Cockcroft J.R. Nitric oxide and the regulation of large artery stiffness: from physiology to pharmacology. Hypertension 44 (2004) 112-116
4. Lerman A., and Zeiher A.M. Endothelial function: cardiac events. Circulation 111 (2005) 363-368
5. Bonetti P.O., Lerman L.O., and Lerman A. Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler. Thromb. Vasc. Biol. 23 (2003) 168-175
6. Drexler H., and Hornig B. Endothelial dysfunction in human disease. J. Mol. Cell Cardiol. 31 (1999) 51-60
7. Hashimoto M., Kozaki K., Eto M., Akishita M., Ako J., Iijima K., et al. Association of coronary risk factors and endothelium-dependent flow-mediated dilatation of the brachial artery. Hypertens. Res. 23 (2000) 233-238
8. Moreno Jr. H., Chalon S., Urae A., Tangphao O., Abiose A.K., Hoffman B.B., et al. Endothelial dysfunction in human hand veins is rapidly reversible after smoking cessation. Am. J. Physiol. 275 (1998) H1040-H1045
9. Leung W.H., Lau C.P., and Wong C.K. Beneficial effect of cholesterol-lowering therapy on coronary endothelium-dependent relaxation in hypercholesterolaemic patients. Lancet 341 (1993) 1496-1500
10. Braam B., and Verhaar M.C. Understanding eNOS for pharmacological modulation of endothelial function: a translational view. Curr. Pharm. Des. 13 (2007) 1727-1740
11. Searles C.D. Transcriptional and posttranscriptional regulation of endothelial nitric oxide synthase expression. Am. J. Physiol. Cell Physiol. 291 (2006) C803-C816
12. Dudzinski D.M., Igarashi J., Greif D., and Michel T. The regulation and pharmacology of endothelial nitric oxide synthase. Annu. Rev. Pharmacol. Toxicol. 46 (2006) 235-276
13. Alp N.J., and Channon K.M. Regulation of endothelial nitric oxide synthase by tetrahydrobiopterin in vascular disease. Arterioscler. Thromb. Vasc. Biol. 24 (2004) 413-420
14. Minshall R.D., Sessa W.C., Stan R.V., Anderson R.G., and Malik A.B. Caveolin regulation of endothelial function. Am. J. Physiol. Lung Cell Mol. Physiol. 285 (2003) L1179-L1183
15. Boo Y.C., and Jo H. Flow-dependent regulation of endothelial nitric oxide synthase: role of protein kinases. Am. J. Physiol. Cell Physiol. 285 (2003) C499-C508
16. Li H., Wallerath T., Munzel T., and Forstermann U. Regulation of endothelial-type NO synthase expression in pathophysiology and in response to drugs. Nitric Oxide 7 (2002) 149-164
17. Li H., Wallerath T., and Forstermann U. Physiological mechanisms regulating the expression of endothelial-type NO synthase. Nitric Oxide 7 (2002) 132-147
18. Wallerath T., Deckert G., Ternes T., Anderson H., Li H., Witte K., et al. Resveratrol, a polyphenolic phytoalexin present in red wine, enhances expression and activity of endothelial nitric oxide synthase. Circulation 106 (2002) 1652-1658
19. Govers R., and Rabelink T.J. Cellular regulation of endothelial nitric oxide synthase. Am. J. Physiol. Renal. Physiol. 280 (2001) F193-F206
20. Vallance P., and Leiper J. Cardiovascular biology of the asymmetric dimethylarginine:dimethylarginine dimethylaminohydrolase pathway. Arterioscler. Thromb. Vasc. Biol. 24 (2004) 1023-1030
21. Cooke J.P. ADMA: its role in vascular disease. Vasc. Med. 10 Suppl. 1 (2005) S11-S17
22. Kielstein J.T., Donnerstag F., Gasper S., Menne J., Kielstein A., Martens-Lobenhoffer J., et al. ADMA increases arterial stiffness and decreases cerebral blood flow in humans. Stroke 37 (2006) 2024-2029
23. Zhang G.G., Bai Y.P., Chen M.F., Shi R.Z., Jiang D.J., Fu Q.M., et al. Asymmetric dimethylarginine induces TNF-alpha production via ROS/NF-kappaB dependent pathway in human monocytic cells and the inhibitory effect of reinioside C. Vascul. Pharmacol. 48 (2008) 115-121
24. Schnabel R., Blankenberg S., Lubos E., Lackner K.J., Rupprecht H.J., Espinola-Klein C., et al. Asymmetric dimethylarginine and the risk of cardiovascular events and death in patients with coronary artery disease: results from the AtheroGene Study. Circ. Res. 97 (2005) e53-e59
25. Zoccali C., Bode-Boger S., Mallamaci F., Benedetto F., Tripepi G., Malatino L., et al. Plasma concentration of asymmetrical dimethylarginine and mortality in patients with end-stage renal disease: a prospective study. Lancet 358 (2001) 2113-2117
26. Mittermayer F., Krzyzanowska K., Exner M., Mlekusch W., Amighi J., Sabeti S., et al. Asymmetric dimethylarginine predicts major adverse cardiovascular events in patients with advanced peripheral artery disease. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 2536-2540
27. Meinitzer A., Seelhorst U., Wellnitz B., Halwachs-Baumann G., Boehm B.O., Winkelmann B.R., et al. Asymmetrical dimethylarginine independently predicts total and cardiovascular mortality in individuals with angiographic coronary artery disease (the Ludwigshafen Risk and Cardiovascular Health study). Clin. Chem. 53 (2007) 273-283
28. Duckelmann C., Mittermayer F., Haider D.G., Altenberger J., Eichinger J., and Wolzt M. Asymmetric dimethylarginine enhances cardiovascular risk prediction in patients with chronic heart failure. Arterioscler. Thromb. Vasc. Biol. 27 (2007) 2037-2042
29. Krzyzanowska K., Mittermayer F., Wolzt M., and Schernthaner G. Asymmetric dimethylarginine predicts cardiovascular events in patients with type 2 diabetes. Diabetes Care 30 (2007) 1834-1839
30. Zeller M., Korandji C., Guilland J.C., Sicard P., Vergely C., Lorgis L., et al. Impact of asymmetric dimethylarginine on mortality after acute myocardial infarction. Arterioscler. Thromb. Vasc. Biol. 28 (2008) 954-960
31. Nicholls S.J., Wang Z., Koeth R., Levison B., DelFraino B., Dzavik V., et al. Metabolic profiling of arginine and nitric oxide pathways predicts hemodynamic abnormalities and mortality in patients with cardiogenic shock after acute myocardial infarction. Circulation 116 (2007) 2315-2324
32. Wilson Tang W.H., Tong W., Shrestha K., Wang Z., Levison B.S., DelFraino B., et al. Differential effects of arginine methylation on diastolic dysfunction and disease progression in patients with chronic systolic heart failure. Eur. Heart J. 29 (2008) 2506-2513
33. Kielstein J.T., Bode-Boger S.M., Hesse G., Martens-Lobenhoffer J., Takacs A., Fliser D., et al. Asymmetrical dimethylarginine in idiopathic pulmonary arterial hypertension. Arterioscler. Thromb. Vasc. Biol. 25 (2005) 1414-1418
34. Clarke S. Protein methylation. Curr. Opin. Cell Biol. 5 (1993) 977-983
35. Wang Y., Wysocka J., Sayegh J., Lee Y.H., Perlin J.R., Leonelli L., et al. Human PAD4 regulates histone arginine methylation levels via demethylimination. Science 306 (2004) 279-283
36. Cuthbert G.L., Daujat S., Snowden A.W., Erdjument-Bromage H., Hagiwara T., Yamada M., et al. Histone deimination antagonizes arginine methylation. Cell 118 (2004) 545-553
37. Duerre J.A., Miller C.H., and Reams G.G. Metabolism of S-adenosyl-l-homocysteine in vivo by the rat. J. Biol. Chem. 244 (1969) 107-111
38. Kakimoto Y., and Akazawa S. Isolation and identification of N-G, N-G- and N-G, N′-G-dimethyl-arginine, N-epsilon-mono-, di-, and trimethyllysine, and glucosylgalactosyl- and galactosyl-delta-hydroxylysine from human urine. J. Biol. Chem. 245 (1970) 5751-5758
39. Boger R.H., Sydow K., Borlak J., Thum T., Lenzen H., Schubert B., et al. LDL cholesterol upregulates synthesis of asymmetrical dimethylarginine in human endothelial cells: involvement of S-adenosylmethionine-dependent methyltransferases. Circ. Res. 87 (2000) 99-105
40. Teerlink T. ADMA metabolism and clearance. Vasc. Med. 10 Suppl. 1 (2005) S73-S81
41. Mehlhase J., and Grune T. Proteolytic response to oxidative stress in mammalian cells. Biol. Chem. 383 (2002) 559-567
42. Ogawa T., Kimoto M., and Sasaoka K. Purification and properties of a new enzyme, NG, NG-dimethylarginine dimethylaminohydrolase, from rat kidney. J. Biol. Chem. 264 (1989) 10205-10209
43. Leiper J.M., Santa M.J., Chubb A., MacAllister R.J., Charles I.G., Whitley G.S., et al. Identification of two human dimethylarginine dimethylaminohydrolases with distinct tissue distributions and homology with microbial arginine deiminases. Biochem. J. 343 Pt 1 (1999) 209-214
44. Nijveldt R.J., Teerlink T., van Guldener C., Prins H.A., van Lambalgen A.A., Stehouwer C.D., et al. Handling of asymmetrical dimethylarginine and symmetrical dimethylarginine by the rat kidney under basal conditions and during endotoxaemia. Nephrol. Dial. Transplant 18 (2003) 2542-2550
45. Nijveldt R.J., Teerlink T., Siroen M.P., van Lambalgen A.A., Rauwerda J.A., and van Leeuwen P.A. The liver is an important organ in the metabolism of asymmetrical dimethylarginine (ADMA). Clin. Nutr. 22 (2003) 17-22
46. Kimoto M., Tsuji H., Ogawa T., and Sasaoka K. Detection of NG, NG-dimethylarginine dimethylaminohydrolase in the nitric oxide-generating systems of rats using monoclonal antibody. Arch. Biochem. Biophys. 300 (1993) 657-662
47. Tran C.T., Fox M.F., Vallance P., and Leiper J.M. Chromosomal localization, gene structure, and expression pattern of DDAH1: comparison with DDAH2 and implications for evolutionary origins. Genomics 68 (2000) 101-105
48. Dayoub H., Achan V., Adimoolam S., Jacobi J., Stuehlinger M.C., Wang B.Y., et al. Dimethylarginine dimethylaminohydrolase regulates nitric oxide synthesis: genetic and physiological evidence. Circulation 108 (2003) 3042-3047
49. Dayoub H., Rodionov R., Lynch C., Cooke J.P., Arning E., Bottiglieri T., et al. Overexpression of dimethylarginine dimethylaminohydrolase inhibits asymmetric dimethylarginine-induced endothelial dysfunction in the cerebral circulation. Stroke 39 (2008) 180-184
50. Murray-Rust J., Leiper J., McAlister M., Phelan J., Tilley S., Santa M.J., et al. Structural insights into the hydrolysis of cellular nitric oxide synthase inhibitors by dimethylarginine dimethylaminohydrolase. Nat. Struct. Biol. 8 (2001) 679-683
51. Leiper J., Murray-Rust J., McDonald N., and Vallance P. S-nitrosylation of dimethylarginine dimethylaminohydrolase regulates enzyme activity: further interactions between nitric oxide synthase and dimethylarginine dimethylaminohydrolase. Proc. Natl. Acad. Sci. USA 99 (2002) 13527-13532
52. Closs E.I., Basha F.Z., Habermeier A., and Forstermann U. Interference of l-arginine analogues with l-arginine transport mediated by the y+ carrier hCAT-2B. Nitric Oxide 1 (1997) 65-73
53. Meinitzer A., Puchinger M., Winklhofer-Roob B.M., Rock E., Ribalta J., Roob J.M., et al. Reference values for plasma concentrations of asymmetrical dimethylarginine (ADMA) and other arginine metabolites in men after validation of a chromatographic method. Clin. Chim. Acta 384 (2007) 141-148
54. Hov G.G., Sagen E., Bigonah A., and Asberg A. Health-associated reference values for arginine, asymmetric dimethylarginine (ADMA) and symmetric dimethylarginine (SDMA) measured with high-performance liquid chromatography. Scand. J. Clin. Lab. Invest. 67 (2007) 868-876
55. Schulze F., Maas R., Freese R., Schwedhelm E., Silberhorn E., and Boger R.H. Determination of a reference value for N(G), N(G)-dimethyl-l-arginine in 500 subjects. Eur. J. Clin. Invest. 35 (2005) 622-626
56. Schwedhelm E. Quantification of ADMA: analytical approaches. Vasc. Med. 10 Suppl 1 (2005) S89-S95
57. Nijveldt R.J., van Leeuwen P.A., van Guldener C., Stehouwer C.D., Rauwerda J.A., and Teerlink T. Net renal extraction of asymmetrical (ADMA) and symmetrical (SDMA) dimethylarginine in fasting humans. Nephrol. Dial. Transplant 17 (2002) 1999-2002
58. Vallance P., Leone A., Calver A., Collier J., and Moncada S. Accumulation of an endogenous inhibitor of nitric oxide synthesis in chronic renal failure. Lancet 339 (1992) 572-575
59. Siroen M.P., van der Sijp J.R., Teerlink T., van Schaik C., and van Leeuwen P.A. The human liver clears both asymmetric and symmetric dimethylarginine. Hepatology 41 (2005) 559-565
60. Hattori Y., Kasai K., and Gross S.S. Cationic amino acid transporter gene expression in cultured vascular smooth muscle cells and in rats. Am. J. Physiol. 276 (1999) H2020-H2028
61. MacAllister R., and Vallance P. Nitric oxide in essential and renal hypertension. J. Am. Soc. Nephrol. 5 (1994) 1057-1065
62. MacAllister R.J., Whitley G.S., and Vallance P. Effects of guanidino and uremic compounds on nitric oxide pathways. Kidney Int. 45 (1994) 737-742
63. Gardiner S.M., Kemp P.A., Bennett T., Palmer R.M., and Moncada S. Regional and cardiac haemodynamic effects of NG, NG, dimethyl-l-arginine and their reversibility by vasodilators in conscious rats. Br. J. Pharmacol. 110 (1993) 1457-1464
64. Jin J.S., and D'Alecy L.G. Central and peripheral effects of asymmetric dimethylarginine, an endogenous nitric oxide synthetase inhibitor. J. Cardiovasc. Pharmacol. 28 (1996) 439-446
65. Kielstein J.T., Impraim B., Simmel S., Bode-Boger S.M., Tsikas D., Frolich J.C., et al. Cardiovascular effects of systemic nitric oxide synthase inhibition with asymmetrical dimethylarginine in humans. Circulation 109 (2004) 172-177
66. Kielstein J.T., Simmel S., Bode-Boger S.M., Roth H.J., Schmidt-Gayk H., Haller H., et al. Subpressor dose asymmetric dimethylarginine modulates renal function in humans through nitric oxide synthase inhibition. Kidney Blood Press. Res. 27 (2004) 143-147
67. Pullamsetti S., Kiss L., Ghofrani H.A., Voswinckel R., Haredza P., Klepetko W., et al. Increased levels and reduced catabolism of asymmetric and symmetric dimethylarginines in pulmonary hypertension. FASEB J. 19 (2005) 1175-1177
68. Carlstrom M., Brown R.D., Edlund J., Sallstrom J., Larsson E., Teerlink T., et al. Role of nitric oxide deficiency in the development of hypertension in hydronephrotic animals. Am. J. Physiol. Renal. Physiol. 294 (2008) F362-F370
69. Kielstein J.T., Bode-Boger S.M., Frolich J.C., Ritz E., Haller H., and Fliser D. Asymmetric dimethylarginine, blood pressure, and renal perfusion in elderly subjects. Circulation 107 (2003) 1891-1895
70. Safar M.E., Levy B.I., and Struijker-Boudier H. Current perspectives on arterial stiffness and pulse pressure in hypertension and cardiovascular diseases. Circulation 107 (2003) 2864-2869
71. Chen M., Li Y., Yang T., Wang Y., Bai Y., and Xie X. ADMA induces monocyte adhesion via activation of chemokine receptors in cultured THP-1 cells. Cytokine 43 (2008) 149-159
72. Xiao H.B., Yang Z.C., Jia S.J., Li N.S., Jiang D.J., Zhang X.H., et al. Effect of asymmetric dimethylarginine on atherogenesis and erythrocyte deformability in apolipoprotein E deficient mice. Life Sci. 81 (2007) 1-7
73. Leong T., Zylberstein D., Graham I., Lissner L., Ward D., Fogarty J., et al. Asymmetric dimethylarginine independently predicts fatal and nonfatal myocardial infarction and stroke in women: 24-year follow-up of the population study of women in Gothenburg. Arterioscler. Thromb. Vasc. Biol. 28 (2008) 961-967
74. Kiechl S., Lee T., Santer P., Thompson G., Tsimikas S., Egger G., et al. Asymmetric and symmetric dimethylarginines are of similar predictive value for cardiovascular risk in the general population. Atherosclerosis (2009) in press
75. Lajer M., Tarnow L., Jorsal A., Teerlink T., Parving H.H., and Rossing P. Plasma concentration of asymmetric dimethylarginine (ADMA) predicts cardiovascular morbidity and mortality in type 1 diabetic patients with diabetic nephropathy. Diabetes Care 31 (2008) 747-752
76. Bode-Boger S.M., Scalera F., Kielstein J.T., Martens-Lobenhoffer J., Breithardt G., Fobker M., et al. Symmetrical dimethylarginine: a new combined parameter for renal function and extent of coronary artery disease. J. Am. Soc. Nephrol. 17 (2006) 1128-1134
77. Mangoni A.A., Hewitson C.L., Woodman R.J., Whiting M.J., McAteer-Carr B., and Barbara J.A. Symmetric dimethylarginine is an independent predictor of intradialytic hypotension. Am. J. Hypertens. 21 (2008) 955-959
78. Schepers E., Glorieux G., Dhondt A., Leybaert L., and Vanholder R. Role of symmetric dimethylarginine in vascular damage by increasing ROS via store-operated calcium influx in monocytes. Nephrol. Dial. Transplant 24 (2009) 1429-1435
79. Kielstein J.T., Salpeter S.R., Bode-Boeger S.M., Cooke J.P., and Fliser D. Symmetric dimethylarginine (SDMA) as endogenous marker of renal function-a meta-analysis. Nephrol. Dial. Transplant 21 (2006) 2446-2451
80. Brooks E.R., Langman C.B., Wang S., Price H.E., Hodges A.L., Darling L., et al. Methylated arginine derivatives in children and adolescents with chronic kidney disease. Pediatr. Nephrol. 24 (2009) 129-134
81. Fliser D., Kronenberg F., Kielstein J.T., Morath C., Bode-Boger S.M., Haller H., et al. Asymmetric dimethylarginine and progression of chronic kidney disease: the mild to moderate kidney disease study. J. Am. Soc. Nephrol. 16 (2005) 2456-2461
82. Wang J., Sim A.S., Wang X.L., Salonikas C., Naidoo D., and Wilcken D.E. Relations between plasma asymmetric dimethylarginine (ADMA) and risk factors for coronary disease. Atherosclerosis 184 (2006) 383-388
83. Al Banchaabouchi M., Marescau B., Possemiers I., D'Hooge R., Levillain O., and De Deyn P.P. NG,NG-dimethylarginine and NG,NG-dimethylarginine in renal insufficiency. Pflugers Arch. 439 (2000) 524-531
84. Marescau B., Nagels G., Possemiers I., De Broe M.E., Becaus I., Billiouw J.M., et al. Guanidino compounds in serum and urine of nondialyzed patients with chronic renal insufficiency. Metabolism 46 (1997) 1024-1031
85. Nanayakkara P.W., Teerlink T., Stehouwer C.D., Allajar D., Spijkerman A., Schalkwijk C., et al. Plasma asymmetric dimethylarginine (ADMA) concentration is independently associated with carotid intima-media thickness and plasma soluble vascular cell adhesion molecule-1 (sVCAM-1) concentration in patients with mild-to-moderate renal failure. Kidney Int. 68 (2005) 2230-2236
86. Kielstein J.T., Boger R.H., Bode-Boger S.M., Frolich J.C., Haller H., Ritz E., et al. Marked increase of asymmetric dimethylarginine in patients with incipient primary chronic renal disease. J. Am. Soc. Nephrol. 13 (2002) 170-176
87. Goonasekera C.D., Rees D.D., Woolard P., Frend A., Shah V., and Dillon M.J. Nitric oxide synthase inhibitors and hypertension in children and adolescents. J. Hypertens. 15 (1997) 901-909
88. Levey A.S., Bosch J.P., Lewis J.B., Greene T., Rogers N., and Roth D. A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of Diet in Renal Disease Study Group. Ann. Intern. Med. 130 (1999) 461-470
89. Herget-Rosenthal S., Bokenkamp A., and Hofmann W. How to estimate GFR-serum creatinine, serum cystatin C or equations?. Clin. Biochem. 40 (2007) 153-161
90. Almquist T., Forslund L., Rehnqvist N., and Hjemdahl P. Prognostic implications of renal dysfunction in patients with stable angina pectoris. J. Intern. Med. 260 (2006) 537-544
91. Anavekar N.S., McMurray J.J., Velazquez E.J., Solomon S.D., Kober L., Rouleau J.L., et al. Relation between renal dysfunction and cardiovascular outcomes after myocardial infarction. N. Engl. J. Med. 351 (2004) 1285-1295
92. Mann J.F., Gerstein H.C., Pogue J., Bosch J., and Yusuf S. Renal insufficiency as a predictor of cardiovascular outcomes and the impact of ramipril: the HOPE randomized trial. Ann. Intern. Med. 134 (2001) 629-636
93. Raj D.S., Vincent B., Simpson K., Sato E., Jones K.L., Welbourne T.C., et al. Hemodynamic changes during hemodialysis: role of nitric oxide and endothelin. Kidney Int. 61 (2002) 697-704
94. Hewitson C.L., Whiting M.J., Barbara J.A., and Mangoni A.A. Acute effects of haemodialysis on biochemical modulators of endothelial function. J. Intern. Med. 262 (2007) 571-580
95. Chapleau M.W., Cunningham J.T., Sullivan M.J., Wachtel R.E., and Abboud F.M. Structural versus functional modulation of the arterial baroreflex. Hypertension 26 (1995) 341-347
96. Aslam S., Santha T., Leone A., and Wilcox C. Effects of amlodipine and valsartan on oxidative stress and plasma methylarginines in end-stage renal disease patients on hemodialysis. Kidney Int. 70 (2006) 2109-2115