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Review Article

Asymmetric Dimethylarginine: a Key Player in the Pathophysiology of Endothelial Dysfunction, Vascular Inflammation and Atherosclerosis in Rheumatoid Arthritis?

Author(s): Arduino A. Mangoni*, Sara Tommasi, Salvatore Sotgia, Angelo Zinellu, Panagiotis Paliogiannis, Matteo Piga, Alberto Cauli, Gianfranco Pintus, Ciriaco Carru and Gian L. Erre

Volume 27, Issue 18, 2021

Published on: 06 January, 2021

Page: [2131 - 2140] Pages: 10

DOI: 10.2174/1381612827666210106144247

Price: $65

Abstract

Patients with rheumatoid arthritis (RA), a chronic and disabling autoimmune condition that is characterized by articular and extra-articular manifestations and a pro-inflammatory and pro-oxidant state, suffer from premature atherosclerosis and excessive cardiovascular disease burden. A key step in the pathogenesis of atherosclerosis is impaired synthesis of the endogenous messenger nitric oxide (NO) by endothelial cells which, in turn, alters local homeostatic mechanisms and favors vascular damage and plaque deposition. While the exact mechanisms of endothelial dysfunction in RA remain to be established, there is good evidence that RA patients have relatively high circulating concentrations of the methylated arginine asymmetric dimethylarginine (ADMA), a potent endogenous inhibitor of endothelial NO synthase (eNOS). This review discusses the biological and pathophysiological role of ADMA, the interplay between ADMA, inflammation and oxidative stress, and the available evidence on the adverse impact of ADMA on endothelial function and atherosclerosis and potential ADMA-lowering therapies in RA patients.

Keywords: Asymmetric dimethylarginine, rheumatoid arthritis, endothelial function, arterial stiffness, cardiovascular risk, atherosclerosis, inflammation.

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[1]
Bäck M, Yurdagul A Jr, Tabas I, Öörni K, Kovanen PT. Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities. Nat Rev Cardiol 2019; 16(7): 389-406.
[http://dx.doi.org/10.1038/s41569-019-0169-2] [PMID: 30846875]
[2]
Tabas I, Williams KJ, Borén J. Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation 2007; 116(16): 1832-44.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.106.676890] [PMID: 17938300]
[3]
Savoia C, Schiffrin EL. Vascular inflammation in hypertension and diabetes: molecular mechanisms and therapeutic interventions. Clin Sci (Lond) 2007; 112(7): 375-84.
[http://dx.doi.org/10.1042/CS20060247] [PMID: 17324119]
[4]
Steinberg D. Hypercholesterolemia and inflammation in atherogenesis: two sides of the same coin. Mol Nutr Food Res 2005; 49(11): 995-8.
[http://dx.doi.org/10.1002/mnfr.200500081] [PMID: 16270285]
[5]
Ambrose JA, Barua RS. The pathophysiology of cigarette smoking and cardiovascular disease: an update. J Am Coll Cardiol 2004; 43(10): 1731-7.
[http://dx.doi.org/10.1016/j.jacc.2003.12.047] [PMID: 15145091]
[6]
Frostegård J. Atherosclerosis in patients with autoimmune disorders. Arterioscler Thromb Vasc Biol 2005; 25(9): 1776-85.
[http://dx.doi.org/10.1161/01.ATV.0000174800.78362.ec] [PMID: 15976324]
[7]
Skeoch S, Bruce IN. Atherosclerosis in rheumatoid arthritis: is it all about inflammation? Nat Rev Rheumatol 2015; 11(7): 390-400.
[http://dx.doi.org/10.1038/nrrheum.2015.40] [PMID: 25825281]
[8]
Full LE, Monaco C. Targeting inflammation as a therapeutic strategy in accelerated atherosclerosis in rheumatoid arthritis. Cardiovasc Ther 2011; 29(4): 231-42.
[http://dx.doi.org/10.1111/j.1755-5922.2010.00159.x] [PMID: 20553292]
[9]
Wållberg-Jonsson S, Caidahl K, Klintland N, Nyberg G, Rantapää-Dahlqvist S. Increased arterial stiffness and indication of endothelial dysfunction in long-standing rheumatoid arthritis. Scand J Rheumatol 2008; 37(1): 1-5.
[http://dx.doi.org/10.1080/03009740701633238] [PMID: 18189187]
[10]
Skeoch S, Cristinacce PLH, Williams H, et al. Imaging atherosclerosis in rheumatoid arthritis: evidence for increased prevalence, altered phenotype and a link between systemic and localised plaque inflammation. Sci Rep 2017; 7(1): 827.
[http://dx.doi.org/10.1038/s41598-017-00989-w] [PMID: 28400572]
[11]
Baghdadi LR, Woodman RJ, Shanahan EM, Mangoni AA. The impact of traditional cardiovascular risk factors on cardiovascular outcomes in patients with rheumatoid arthritis: a systematic review and meta-analysis. PLoS One 2015; 10(2): e0117952.
[http://dx.doi.org/10.1371/journal.pone.0117952] [PMID: 25689371]
[12]
Liao KP. Cardiovascular disease in patients with rheumatoid arthritis. Trends Cardiovasc Med 2017; 27(2): 136-40.
[http://dx.doi.org/10.1016/j.tcm.2016.07.006] [PMID: 27612551]
[13]
Ramji DP, Davies TS. Cytokines in atherosclerosis: Key players in all stages of disease and promising therapeutic targets. Cytokine Growth Factor Rev 2015; 26(6): 673-85.
[http://dx.doi.org/10.1016/j.cytogfr.2015.04.003] [PMID: 26005197]
[14]
Vallance P, Leiper J. Cardiovascular biology of the asymmetric dimethylarginine:dimethylarginine dimethylaminohydrolase pathway. Arterioscler Thromb Vasc Biol 2004; 24(6): 1023-30.
[http://dx.doi.org/10.1161/01.ATV.0000128897.54893.26] [PMID: 15105281]
[15]
Cross M, Smith E, Hoy D, et al. The global burden of rheumatoid arthritis: estimates from the global burden of disease 2010 study. Ann Rheum Dis 2014; 73(7): 1316-22.
[http://dx.doi.org/10.1136/annrheumdis-2013-204627] [PMID: 24550173]
[16]
Hunter TM, Boytsov NN, Zhang X, Schroeder K, Michaud K, Araujo AB. Prevalence of rheumatoid arthritis in the United States adult population in healthcare claims databases, 2004-2014. Rheumatol Int 2017; 37(9): 1551-7.
[http://dx.doi.org/10.1007/s00296-017-3726-1] [PMID: 28455559]
[17]
Smolen JS, Aletaha D, McInnes IB. Rheumatoid arthritis. Lancet 2016; 388(10055): 2023-38.
[http://dx.doi.org/10.1016/S0140-6736(16)30173-8] [PMID: 27156434]
[18]
Dadoun S, Zeboulon-Ktorza N, Combescure C, et al. Mortality in rheumatoid arthritis over the last fifty years: systematic review and meta-analysis. Joint Bone Spine 2013; 80(1): 29-33.
[http://dx.doi.org/10.1016/j.jbspin.2012.02.005] [PMID: 22459416]
[19]
Sokka T, Abelson B, Pincus T. Mortality in rheumatoid arthritis: 2008 update. Clin Exp Rheumatol 2008; 26(5)(Suppl. 51): S35-61.
[PMID: 19026144]
[20]
van den Hoek J, Boshuizen HC, Roorda LD, et al. Mortality in patients with rheumatoid arthritis: a 15-year prospective cohort study. Rheumatol Int 2017; 37(4): 487-93.
[http://dx.doi.org/10.1007/s00296-016-3638-5] [PMID: 28032180]
[21]
van Riel PL, Renskers L. The Disease Activity Score (DAS) and the Disease Activity Score using 28 joint counts (DAS28) in the management of rheumatoid arthritis. Clin Exp Rheumatol 2016; 34(5)(Suppl. 101): S40-4.
[PMID: 27762189]
[22]
Pradhan A, Bagchi A, De S, et al. Role of redox imbalance and cytokines in mediating oxidative damage and disease progression of patients with rheumatoid arthritis. Free Radic Res 2019; 53(7): 768-79.
[http://dx.doi.org/10.1080/10715762.2019.1629586] [PMID: 31284792]
[23]
Mantel Ä, Holmqvist M, Nyberg F, et al. Risk factors for the rapid increase in risk of acute coronary events in patients with new-onset rheumatoid arthritis: a nested case-control study. Arthritis Rheumatol 2015; 67(11): 2845-54.
[http://dx.doi.org/10.1002/art.39267] [PMID: 26138387]
[24]
Erre GL, Piga M, Fedele AL, et al. Prevalence and Determinants of Peripheral Microvascular Endothelial Dysfunction in Rheumatoid Arthritis Patients: A Multicenter Cross-Sectional Study. Mediators Inflamm 2018; 2018: 6548715.
[http://dx.doi.org/10.1155/2018/6548715] [PMID: 29483841]
[25]
Erre GL, Buscetta G, Paliogiannis P, et al. Coronary flow reserve in systemic rheumatic diseases: a systematic review and meta-analysis. Rheumatol Int 2018; 38(7): 1179-90.
[http://dx.doi.org/10.1007/s00296-018-4039-8] [PMID: 29732488]
[26]
Ambrosino P, Tasso M, Lupoli R, et al. Non-invasive assessment of arterial stiffness in patients with rheumatoid arthritis: a systematic review and meta-analysis of literature studies. Ann Med 2015; 47(6): 457-67.
[http://dx.doi.org/10.3109/07853890.2015.1068950] [PMID: 26340234]
[27]
Wilkinson IB, Franklin SS, Cockcroft JR. Nitric oxide and the regulation of large artery stiffness: from physiology to pharmacology. Hypertension 2004; 44(2): 112-6.
[http://dx.doi.org/10.1161/01.HYP.0000138068.03893.40] [PMID: 15262901]
[28]
Gunter S, Robinson C, Norton GR, et al. Cardiovascular Risk Factors and Disease Characteristics Are Consistently Associated with Arterial Function in Rheumatoid Arthritis. J Rheumatol 2017; 44(8): 1125-33.
[http://dx.doi.org/10.3899/jrheum.170029] [PMID: 28572463]
[29]
Botta E, Meroño T, Saucedo C, et al. Associations between disease activity, markers of HDL functionality and arterial stiffness in patients with rheumatoid arthritis. Atherosclerosis 2016; 251: 438-44.
[http://dx.doi.org/10.1016/j.atherosclerosis.2016.06.009] [PMID: 27344073]
[30]
Kaur R, Kaur M, Singh J. Endothelial dysfunction and platelet hyperactivity in type 2 diabetes mellitus: molecular insights and therapeutic strategies. Cardiovasc Diabetol 2018; 17(1): 121.
[http://dx.doi.org/10.1186/s12933-018-0763-3] [PMID: 30170601]
[31]
Schäfer A, Bauersachs J. Endothelial dysfunction, impaired endogenous platelet inhibition and platelet activation in diabetes and atherosclerosis. Curr Vasc Pharmacol 2008; 6(1): 52-60.
[http://dx.doi.org/10.2174/157016108783331295] [PMID: 18220940]
[32]
Safar ME, Levy BI, Struijker-Boudier H. Current perspectives on arterial stiffness and pulse pressure in hypertension and cardiovascular diseases. Circulation 2003; 107(22): 2864-9.
[http://dx.doi.org/10.1161/01.CIR.0000069826.36125.B4] [PMID: 12796414]
[33]
London GM, Marchais SJ, Guerin AP, Pannier B. Arterial stiffness: pathophysiology and clinical impact. Clin Exp Hypertens 2004; 26(7-8): 689-99.
[http://dx.doi.org/10.1081/CEH-200031982] [PMID: 15702623]
[34]
Hansen PR, Feineis M, Abdulla J. Rheumatoid arthritis patients have higher prevalence and burden of asymptomatic coronary artery disease assessed by coronary computed tomography: A systematic literature review and meta-analysis. Eur J Intern Med 2019; 62: 72-9.
[http://dx.doi.org/10.1016/j.ejim.2019.02.018] [PMID: 30826172]
[35]
Karpouzas GA, Ormseth SR, Hernandez E, Budoff MJ. Impact of Cumulative Inflammation, Cardiac Risk Factors, and Medication Exposure on Coronary Atherosclerosis Progression in Rheumatoid Arthritis. Arthritis Rheumatol 2020; 72(3): 400-8.
[http://dx.doi.org/10.1002/art.41122] [PMID: 31532064]
[36]
Napoli C, de Nigris F, Williams-Ignarro S, Pignalosa O, Sica V, Ignarro LJ. Nitric oxide and atherosclerosis: an update. Nitric Oxide 2006; 15(4): 265-79.
[http://dx.doi.org/10.1016/j.niox.2006.03.011] [PMID: 16684613]
[37]
Jarzebska N, Mangoni AA, Martens-Lobenhoffer J, Bode-Böger SM, Rodionov RN. The Second Life of Methylarginines as Cardiovascular Targets. Int J Mol Sci 2019; 20(18): E4592.
[http://dx.doi.org/10.3390/ijms20184592] [PMID: 31533264]
[38]
Ghosh SK, Paik WK, Kim S. Purification and molecular identification of two protein methylases I from calf brain. Myelin basic protein- and histone-specific enzyme. J Biol Chem 1988; 263(35): 19024-33.
[PMID: 2461933]
[39]
Rawal N, Rajpurohit R, Paik WK, Kim S. Purification and characterization of S-adenosylmethionine-protein-arginine N-methyltransferase from rat liver. Biochem J 1994; 300(Pt 2): 483-9.
[http://dx.doi.org/10.1042/bj3000483] [PMID: 8002954]
[40]
Closs EI, Basha FZ, Habermeier A, Förstermann U. Interference of L-arginine analogues with L-arginine transport mediated by the y+ carrier hCAT-2B. Nitric Oxide 1997; 1(1): 65-73.
[http://dx.doi.org/10.1006/niox.1996.0106] [PMID: 9701046]
[41]
Strobel J, Müller F, Zolk O, et al. Transport of asymmetric dimethylarginine (ADMA) by cationic amino acid transporter 2 (CAT2), organic cation transporter 2 (OCT2) and multidrug and toxin extrusion protein 1 (MATE1). Amino Acids 2013; 45(4): 989-1002.
[http://dx.doi.org/10.1007/s00726-013-1556-3] [PMID: 23864433]
[42]
Porcelli V, Longo A, Palmieri L, Closs EI, Palmieri F. Asymmetric dimethylarginine is transported by the mitochondrial carrier SLC25A2. Amino Acids 2016; 48(2): 427-36.
[http://dx.doi.org/10.1007/s00726-015-2096-9] [PMID: 26403849]
[43]
Ogawa T, Kimoto M, Sasaoka K. Dimethylarginine:pyruvate aminotransferase in rats. Purification, properties, and identity with alanine:glyoxylate aminotransferase 2. J Biol Chem 1990; 265(34): 20938-45.
[PMID: 2123486]
[44]
Martens-Lobenhoffer J, Rodionov RN, Bode-Böger SM. Determination of asymmetric Nα-acetyldimethylarginine in humans: a phase II metabolite of asymmetric dimethylarginine. Anal Biochem 2014; 452: 25-30.
[http://dx.doi.org/10.1016/j.ab.2014.02.016] [PMID: 24560726]
[45]
Kakimoto Y, 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 1970; 245(21): 5751-8.
[PMID: 5472370]
[46]
Kielstein JT, Böger RH, Bode-Böger SM, et al. Marked increase of asymmetric dimethylarginine in patients with incipient primary chronic renal disease. J Am Soc Nephrol 2002; 13(1): 170-6.
[PMID: 11752034]
[47]
Hewitson CL, Whiting MJ, Barbara JA, Mangoni AA. Acute effects of haemodialysis on biochemical modulators of endothelial function. J Intern Med 2007; 262(5): 571-80.
[http://dx.doi.org/10.1111/j.1365-2796.2007.01848.x] [PMID: 17949366]
[48]
Németh B, Ajtay Z, Hejjel L, et al. The issue of plasma asymmetric dimethylarginine reference range - A systematic review and meta-analysis. PLoS One 2017; 12(5): e0177493.
[http://dx.doi.org/10.1371/journal.pone.0177493] [PMID: 28494019]
[49]
Mangoni AA, Zinellu A, Sotgia S, Rowland A, Carru C. Methylated arginines as biomarkers in renal disease.Biomarkers in kidney disease. Patel, VB, Preedy, VR, Eds. Spinger Science+Business Media Dordrecht 2016; 1: pp. 397-426.
[http://dx.doi.org/10.1007/978-94-007-7699-9_19]
[50]
Radi R. Oxygen radicals, nitric oxide, and peroxynitrite: Redox pathways in molecular medicine. Proc Natl Acad Sci USA 2018; 115(23): 5839-48.
[http://dx.doi.org/10.1073/pnas.1804932115] [PMID: 29802228]
[51]
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 USA 2002; 99(21): 13527-32.
[http://dx.doi.org/10.1073/pnas.212269799] [PMID: 12370443]
[52]
Rees DD, Palmer RM, Schulz R, Hodson HF, Moncada S. Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Br J Pharmacol 1990; 101(3): 746-52.
[http://dx.doi.org/10.1111/j.1476-5381.1990.tb14151.x] [PMID: 1706208]
[53]
Vallance P, Leone A, Calver A, Collier J, Moncada S. Accumulation of an endogenous inhibitor of nitric oxide synthesis in chronic renal failure. Lancet 1992; 339(8793): 572-5.
[http://dx.doi.org/10.1016/0140-6736(92)90865-Z] [PMID: 1347093]
[54]
Kielstein JT, Impraim B, Simmel S, et al. Cardiovascular effects of systemic nitric oxide synthase inhibition with asymmetrical dimethylarginine in humans. Circulation 2004; 109(2): 172-7.
[http://dx.doi.org/10.1161/01.CIR.0000105764.22626.B1] [PMID: 14662708]
[55]
Kielstein JT, Donnerstag F, Gasper S, et al. ADMA increases arterial stiffness and decreases cerebral blood flow in humans. Stroke 2006; 37(8): 2024-9.
[http://dx.doi.org/10.1161/01.STR.0000231640.32543.11] [PMID: 16809568]
[56]
Chan JR, Böger RH, Bode-Böger SM, et al. Asymmetric dimethylarginine increases mononuclear cell adhesiveness in hypercholesterolemic humans. Arterioscler Thromb Vasc Biol 2000; 20(4): 1040-6.
[http://dx.doi.org/10.1161/01.ATV.20.4.1040] [PMID: 10764670]
[57]
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): 1540-6.
[http://dx.doi.org/10.1161/ATVBAHA.110.222638] [PMID: 21493890]
[58]
Hu X, Xu X, Zhu G, et al. Vascular endothelial-specific dimethylarginine dimethylaminohydrolase-1-deficient mice reveal that vascular endothelium plays an important role in removing asymmetric dimethylarginine. Circulation 2009; 120(22): 2222-9.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.108.819912] [PMID: 19917889]
[59]
Leiper J, Nandi M, Torondel B, et al. Disruption of methylarginine metabolism impairs vascular homeostasis. Nat Med 2007; 13(2): 198-203.
[http://dx.doi.org/10.1038/nm1543] [PMID: 17273169]
[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(9299): 2113-7.
[http://dx.doi.org/10.1016/S0140-6736(01)07217-8] [PMID: 11784625]
[61]
Dückelmann C, Mittermayer F, Haider DG, Altenberger J, Eichinger J, Wolzt M. Asymmetric dimethylarginine enhances cardiovascular risk prediction in patients with chronic heart failure. Arterioscler Thromb Vasc Biol 2007; 27(9): 2037-42.
[http://dx.doi.org/10.1161/ATVBAHA.107.147595] [PMID: 17569878]
[62]
Schnabel R, Blankenberg S, Lubos E, 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 2005; 97(5): e53-9.
[http://dx.doi.org/10.1161/01.RES.0000181286.44222.61] [PMID: 16100045]
[63]
Horowitz JD, De Caterina R, Heresztyn T, et al. ARISTOTLE Investigators. Asymmetric and Symmetric Dimethylarginine Predict Outcomes in Patients With Atrial Fibrillation: An ARISTOTLE Substudy. J Am Coll Cardiol 2018; 72(7): 721-33.
[http://dx.doi.org/10.1016/j.jacc.2018.05.058] [PMID: 30092948]
[64]
Krzyzanowska K, Mittermayer F, Wolzt M, Schernthaner G. Asymmetric dimethylarginine predicts cardiovascular events in patients with type 2 diabetes. Diabetes Care 2007; 30(7): 1834-9.
[http://dx.doi.org/10.2337/dc07-0019] [PMID: 17456842]
[65]
Erre GL, Mangoni AA, Castagna F, et al. Meta-Analysis of Asymmetric Dimethylarginine Concentrations in Rheumatic Diseases. Sci Rep 2019; 9(1): 5426.
[http://dx.doi.org/10.1038/s41598-019-41994-5] [PMID: 30932011]
[66]
Zhao CN, Wu Q, Mao YM, et al. Elevated circulating asymmetric dimethylarginine levels in rheumatoid arthritis: a systematic review and meta-analysis. Amino Acids 2019; 51(5): 773-82.
[http://dx.doi.org/10.1007/s00726-019-02714-5] [PMID: 30830311]
[67]
Zafari P, Zarifian A, Alizadeh-Navaei R, et al. Asymmetric and symmetric dimethylarginine concentration as an indicator of cardiovascular diseases in rheumatoid arthritis patients: a systematic review and meta-analysis of case-control studies. Clin Rheumatol 2020; 39(1): 127-34.
[http://dx.doi.org/10.1007/s10067-019-04713-z] [PMID: 31376089]
[68]
Schlesinger S, Sonntag SR, Lieb W, Maas R. Asymmetric and Symmetric Dimethylarginine as Risk Markers for Total Mortality and Cardiovascular Outcomes: A Systematic Review and Meta-Analysis of Prospective Studies. PLoS One 2016; 11(11): e0165811.
[http://dx.doi.org/10.1371/journal.pone.0165811] [PMID: 27812151]
[69]
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(2): 99-105.
[http://dx.doi.org/10.1161/01.RES.87.2.99] [PMID: 10903992]
[70]
Erre GL, Mangoni AA, Passiu G, et al. Comprehensive arginine metabolomics and peripheral vasodilatory capacity in rheumatoid arthritis: A monocentric cross-sectional study. Microvasc Res 2020; 131: 104038.
[http://dx.doi.org/10.1016/j.mvr.2020.104038] [PMID: 32622695]
[71]
Ito A, Tsao PS, Adimoolam S, Kimoto M, Ogawa T, Cooke JP. Novel mechanism for endothelial dysfunction: dysregulation of dimethylarginine dimethylaminohydrolase. Circulation 1999; 99(24): 3092-5.
[http://dx.doi.org/10.1161/01.CIR.99.24.3092] [PMID: 10377069]
[72]
Frombaum M, Therond P, Djelidi R, Beaudeux JL, Bonnefont-Rousselot D, Borderie D. Piceatannol is more effective than resveratrol in restoring endothelial cell dimethylarginine dimethylaminohydrolase expression and activity after high-glucose oxidative stress. Free Radic Res 2011; 45(3): 293-302.
[http://dx.doi.org/10.3109/10715762.2010.527337] [PMID: 21235286]
[73]
Millatt LJ, Whitley GS, Li D, et al. Evidence for dysregulation of dimethylarginine dimethylaminohydrolase I in chronic hypoxia-induced pulmonary hypertension. Circulation 2003; 108(12): 1493-8.
[http://dx.doi.org/10.1161/01.CIR.0000089087.25930.FF] [PMID: 12952847]
[74]
Fearon U, Canavan M, Biniecka M, Veale DJ. Hypoxia, mitochondrial dysfunction and synovial invasiveness in rheumatoid arthritis. Nat Rev Rheumatol 2016; 12(7): 385-97.
[http://dx.doi.org/10.1038/nrrheum.2016.69] [PMID: 27225300]
[75]
Quiñonez-Flores CM, González-Chávez SA, Del Río Nájera D, Pacheco-Tena C. Oxidative Stress Relevance in the Pathogenesis of the Rheumatoid Arthritis: A Systematic Review. BioMed Res Int 2016; 2016: 6097417.
[http://dx.doi.org/10.1155/2016/6097417] [PMID: 27340664]
[76]
Matsuno H, Yudoh K, Katayama R, et al. The role of TNF-alpha in the pathogenesis of inflammation and joint destruction in rheumatoid arthritis (RA): a study using a human RA/SCID mouse chimera. Rheumatology (Oxford) 2002; 41(3): 329-37.
[http://dx.doi.org/10.1093/rheumatology/41.3.329] [PMID: 11934972]
[77]
Surdacki A, Martens-Lobenhoffer J, Wloch A, et al. Plasma asymmetric dimethylarginine is related to anticitrullinated protein antibodies in rheumatoid arthritis of short duration. Metabolism 2009; 58(3): 316-8.
[http://dx.doi.org/10.1016/j.metabol.2008.10.002] [PMID: 19217445]
[78]
Mangoni AA, Jackson SH. Homocysteine and cardiovascular disease: current evidence and future prospects. Am J Med 2002; 112(7): 556-65.
[http://dx.doi.org/10.1016/S0002-9343(02)01021-5] [PMID: 12015248]
[79]
Roubenoff R, Dellaripa P, Nadeau MR, et al. Abnormal homocysteine metabolism in rheumatoid arthritis. Arthritis Rheum 1997; 40(4): 718-22.
[http://dx.doi.org/10.1002/art.1780400418] [PMID: 9125255]
[80]
Dayal S, Rodionov RN, Arning E, et al. Tissue-specific downregulation of dimethylarginine dimethylaminohydrolase in hyperhomocysteinemia. Am J Physiol Heart Circ Physiol 2008; 295(2): H816-25.
[http://dx.doi.org/10.1152/ajpheart.01348.2007] [PMID: 18567702]
[81]
Stühlinger MC, Tsao PS, Her JH, Kimoto M, Balint RF, Cooke JP. Homocysteine impairs the nitric oxide synthase pathway: role of asymmetric dimethylarginine. Circulation 2001; 104(21): 2569-75.
[http://dx.doi.org/10.1161/hc4601.098514] [PMID: 11714652]
[82]
Surdacki A, Martens-Lobenhoffer J, Wloch A, et al. Elevated plasma asymmetric dimethyl-L-arginine levels are linked to endothelial progenitor cell depletion and carotid atherosclerosis in rheumatoid arthritis. Arthritis Rheum 2007; 56(3): 809-19.
[http://dx.doi.org/10.1002/art.22424] [PMID: 17328055]
[83]
Turiel M, Atzeni F, Tomasoni L, et al. Non-invasive assessment of coronary flow reserve and ADMA levels: a case-control study of early rheumatoid arthritis patients. Rheumatology (Oxford) 2009; 48(7): 834-9.
[http://dx.doi.org/10.1093/rheumatology/kep082] [PMID: 19465588]
[84]
Sandoo A, Dimitroulas T, Veldhuijzen van Zanten JJ, et al. Lack of association between asymmetric dimethylarginine and in vivo microvascular and macrovascular endothelial function in patients with rheumatoid arthritis. Clin Exp Rheumatol 2012; 30(3): 388-96.
[PMID: 22410121]
[85]
Erre GL, Piras A, Mura S, et al. Asymmetric dimethylarginine and arterial stiffness in patients with rheumatoid arthritis: A case-control study. J Int Med Res 2016; 44(1)(Suppl.): 76-80.
[http://dx.doi.org/10.1177/0300060515593255] [PMID: 27683145]
[86]
Şentürk T, Yılmaz N, Sargın G, Köseoğlu K, Yenisey Ç. Relationship between asymmetric dimethylarginine and endothelial dysfunction in patients with rheumatoid arthritis. Eur J Rheumatol 2016; 3(3): 106-8.
[http://dx.doi.org/10.5152/eurjrheum.2016.15096] [PMID: 27733940]
[87]
Turiel M, Tomasoni L, Sitia S, et al. Effects of long-term disease-modifying antirheumatic drugs on endothelial function in patients with early rheumatoid arthritis. Cardiovasc Ther 2010; 28(5): e53-64.
[http://dx.doi.org/10.1111/j.1755-5922.2009.00119.x] [PMID: 20337633]
[88]
Sandoo A, Dimitroulas T, Toms TE, et al. Clinical remission following treatment with tumour necrosis factor-alpha antagonists is not accompanied by changes in asymmetric dimethylarginine in patients with rheumatoid arthritis. Clin Biochem 2012; 45(16-17): 1399-403.
[http://dx.doi.org/10.1016/j.clinbiochem.2012.07.092] [PMID: 22820438]
[89]
Angel K, Provan SA, Mowinckel P, Seljeflot I, Kvien TK, Atar D. The L-arginine/asymmetric dimethylarginine ratio is improved by anti-tumor necrosis factor-α therapy in inflammatory arthropathies. Associations with aortic stiffness. Atherosclerosis 2012; 225(1): 160-5.
[http://dx.doi.org/10.1016/j.atherosclerosis.2012.08.033] [PMID: 23014354]
[90]
Di Franco M, Spinelli FR, Metere A, et al. Serum levels of asymmetric dimethylarginine and apelin as potential markers of vascular endothelial dysfunction in early rheumatoid arthritis. Mediators Inflamm 2012; 2012: 347268.
[http://dx.doi.org/10.1155/2012/347268] [PMID: 22927708]
[91]
Spinelli FR, Metere A, Barbati C, et al. Effect of therapeutic inhibition of TNF on circulating endothelial progenitor cells in patients with rheumatoid arthritis. Mediators Inflamm 2013; 2013: 537539.
[http://dx.doi.org/10.1155/2013/537539] [PMID: 24222719]
[92]
Spinelli FR, Di Franco M, Metere A, et al. Decrease of asymmetric dimethyl arginine after anti-TNF therapy in patients with rheumatoid arthritis. Drug Dev Res 2014; 75(Suppl. 1): S67-9.
[http://dx.doi.org/10.1002/ddr.21200] [PMID: 25381982]
[93]
Radhakutty A, Mangelsdorf BL, Drake SM, et al. Opposing effects of rheumatoid arthritis and low dose prednisolone on arginine metabolomics. Atherosclerosis 2017; 266: 190-5.
[http://dx.doi.org/10.1016/j.atherosclerosis.2017.10.004] [PMID: 29035782]
[94]
Di Franco M, Lucchino B, Conti F, Valesini G, Spinelli FR. Asymmetric Dimethyl Arginine as a Biomarker of Atherosclerosis in Rheumatoid Arthritis. Mediators Inflamm 2018; 2018: 3897295.
[http://dx.doi.org/10.1155/2018/3897295] [PMID: 29576746]
[95]
van Dyk M, Mangoni AA, McEvoy M, Attia JR, Sorich MJ, Rowland A. Targeted arginine metabolomics: A rapid, simple UPLC-QToF-MS(E) based approach for assessing the involvement of arginine metabolism in human disease. Clin Chim Acta 2015; 447: 59-65.
[http://dx.doi.org/10.1016/j.cca.2015.05.014] [PMID: 26026257]
[96]
Sotgia S, Zinellu A, Paliogiannis P, et al. A diethylpyrocarbonate-based derivatization method for the LC-MS/MS measurement of plasma arginine and its chemically related metabolites and analogs. Clin Chim Acta 2019; 492: 29-36.
[http://dx.doi.org/10.1016/j.cca.2019.02.004] [PMID: 30731087]
[97]
Agca R, Heslinga SC, Rollefstad S, et al. EULAR recommendations for cardiovascular disease risk management in patients with rheumatoid arthritis and other forms of inflammatory joint disorders: 2015/2016 update. Ann Rheum Dis 2017; 76(1): 17-28.
[http://dx.doi.org/10.1136/annrheumdis-2016-209775] [PMID: 27697765]
[98]
Wei T, Yang B, Liu H, Xin F, Fu L. Development and validation of a nomogram to predict coronary heart disease in patients with rheumatoid arthritis in northern China. Aging (Albany NY) 2020; 12(4): 3190-204.
[http://dx.doi.org/10.18632/aging.102823] [PMID: 32112552]
[99]
Wadham C, Mangoni AA. Dimethylarginine dimethylaminohydrolase regulation: a novel therapeutic target in cardiovascular disease. Expert Opin Drug Metab Toxicol 2009; 5(3): 303-19.
[http://dx.doi.org/10.1517/17425250902785172] [PMID: 19331593]
[100]
Nishiyama Y, Ueda M, Otsuka T, et al. Statin treatment decreased serum asymmetric dimethylarginine (ADMA) levels in ischemic stroke patients. J Atheroscler Thromb 2011; 18(2): 131-7.
[http://dx.doi.org/10.5551/jat.5553] [PMID: 21081834]
[101]
Wu CJ, Wang L, Li X, Wang CX, Ma JP, Xia XS. Impact of adding folic acid, vitamin B(12) and probucol to standard antihypertensive medication on plasma homocysteine and asymmetric dimethylarginine levels of essential hypertension patients. Zhonghua Xin Xue Guan Bing Za Zhi 2012; 40(12): 1003-8.
[PMID: 23363713]
[102]
Xia XS, Li X, Wang L, Wang JZ, Ma JP, Wu CJ. Supplementation of folic acid and vitamin B12; reduces plasma levels of asymmetric dimethylarginine in patients with acute ischemic stroke. J Clin Neurosci 2014; 21(9): 1586-90.
[http://dx.doi.org/10.1016/j.jocn.2013.11.043] [PMID: 24814858]
[103]
Paul B, Whiting MJ, De Pasquale CG, Mangoni AA. Acute effects of 5-methyltetrahydrofolate on endothelial function and asymmetric dimethylarginine in patients with chronic heart failure. Nutr Metab Cardiovasc Dis 2010; 20(5): 341-9.
[http://dx.doi.org/10.1016/j.numecd.2009.04.008] [PMID: 19748251]
[104]
Holven KB, Haugstad TS, Holm T, Aukrust P, Ose L, Nenseter MS. Folic acid treatment reduces elevated plasma levels of asymmetric dimethylarginine in hyperhomocysteinaemic subjects. Br J Nutr 2003; 89(3): 359-63.
[http://dx.doi.org/10.1079/BJN2002779] [PMID: 12628031]
[105]
Tousoulis D, Oikonomou E, Economou EK, Crea F, Kaski JC. Inflammatory cytokines in atherosclerosis: current therapeutic approaches. Eur Heart J 2016; 37(22): 1723-32.
[http://dx.doi.org/10.1093/eurheartj/ehv759] [PMID: 26843277]

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