Plausible diagnostic value of urinary isomeric dimethylarginine ratio for diabetic nephropathy.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
19 02 2020
Historique:
received: 14 06 2019
accepted: 23 01 2020
entrez: 21 2 2020
pubmed: 23 2 2020
medline: 21 11 2020
Statut: epublish

Résumé

Altered circulatory asymmetric and symmetric dimethylarginines have been independently reported in patients with end-stage renal failure suggesting their potential role as mediators and early biomarkers of nephropathy. These alterations can also be reflected in urine. Herein, we aimed to evaluate urinary asymmetric to symmetric dimethylarginine ratio (ASR) for early prediction of diabetic nephropathy (DN). In this cross-sectional study, individuals with impaired glucose tolerance (IGT), newly diagnosed diabetes (NDD), diabetic microalbuminuria (MIC), macroalbuminuria (MAC), and normal glucose tolerance (NGT) were recruited from Dr. Mohans' Diabetes Specialties centre, India. Urinary ASR was measured using a validated high-throughput MALDI-MS/MS method. Significantly lower ASR was observed in MIC (0.909) and MAC (0.741) in comparison to the NGT and NDD groups. On regression models, ASR was associated with MIC [OR: 0.256; 95% CI: 0.158-0.491] and MAC [OR 0.146; 95% CI: 0.071-0.292] controlled for all the available confounding factors. ROC analysis revealed ASR cut-point of 0.95 had C-statistic of 0.691 (95% CI: 0.627-0.755) to discriminate MIC from NDD with 72% sensitivity. Whereas, an ASR cut-point of 0.82 had C-statistic of 0.846 (95% CI: 0.800 - 0.893) had 91% sensitivity for identifying MAC. Our results suggest ASR as a potential early diagnostic biomarker for DN among the Asian Indians.

Identifiants

pubmed: 32076062
doi: 10.1038/s41598-020-59897-1
pii: 10.1038/s41598-020-59897-1
pmc: PMC7031402
doi:

Substances chimiques

dimethylarginine 0
symmetric dimethylarginine 49787G1ULV
Arginine 94ZLA3W45F

Types de publication

Journal Article Observational Study Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2970

Références

Brancati, F. L. et al. Risk of end-stage renal disease in diabetes mellitus: a prospective cohort study of men screened for MRFIT. JAMA 278, 2069–2074 (1997).
pubmed: 9403420 doi: 10.1001/jama.1997.03550230045035 pmcid: 9403420
Gregg, E. W. et al. Trends in cause-specific mortality among adults with and without diagnosed diabetes in the USA: an epidemiological analysis of linked national survey and vital statistics data. Lancet 391, 2430–2440 (2018).
pubmed: 29784146 doi: 10.1016/S0140-6736(18)30314-3 pmcid: 29784146
Perkins, B. A. et al. Microalbuminuria and the risk for early progressive renal function decline in type 1 diabetes. J. Am. Soc. Nephrol. 18, 1353–1361 (2007).
pubmed: 17329575 doi: 10.1681/ASN.2006080872 pmcid: 17329575
Paik, W. K. & Kim, S. N(G)-Methylarginines: Biosynthesis, biochemical function and metabolism. Amino Acids 4, 267–86 (1993).
pubmed: 24190608 pmcid: 24190608
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. 245, 5751–8 (1970).
pubmed: 5472370 pmcid: 5472370
Markiw, R. T. Isolation of N-methylated basic amino acids from physiological fluids and protein hydrolysates. Biochem. Med. 13, 23–27 (1975).
pubmed: 1167163 doi: 10.1016/0006-2944(75)90136-2 pmcid: 1167163
Zakrzewicz, D. & Eickelberg, O. From arginine methylation to ADMA: A novel mechanism with therapeutic potential in chronic lung diseases. BMC Pulm. Med. 9, 1–7 (2009).
doi: 10.1186/1471-2466-9-5
Tran, C. T. L., Leiper, J. M. & Vallance, P. The DDAH/ADMA/NOS pathway. Atheroscler. Suppl. 4, 33–40 (2003).
pubmed: 14664901 doi: 10.1016/S1567-5688(03)00032-1 pmcid: 14664901
Davids, M. et al. Role of dimethylarginine dimethylaminohydrolase activity in regulation of tissue and plasma concentrations of asymmetric dimethylarginine in an animal model of prolonged critical illness. Metabolism. 61, 482–90 (2012).
pubmed: 22000584 doi: 10.1016/j.metabol.2011.08.007 pmcid: 22000584
Shibata, R. et al. Involvement of asymmetric dimethylarginine (ADMA) in tubulointerstitial ischaemia in the early phase of diabetic nephropathy. Nephrol. Dial. Transplant. 24, 1162–1169 (2009).
pubmed: 19015171 doi: 10.1093/ndt/gfn630 pmcid: 19015171
Bode-Böger, S. M. et al. Symmetrical dimethylarginine: a new combined parameter for renal function and extent of coronary artery disease. J. Am. Soc. Nephrol. 17, 1128–34 (2006).
pubmed: 16481412 doi: 10.1681/ASN.2005101119 pmcid: 16481412
Schlesinger, S., Sonntag, S. R., 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 11, 1–26 (2016).
doi: 10.1371/journal.pone.0165811
Willeit, P. et al. Asymmetric dimethylarginine and cardiovascular risk: systematic review and meta-analysis of 22 prospective studies. J. Am. Heart Assoc. 4, e001833 (2015).
pubmed: 26021436 pmcid: 4599532 doi: 10.1161/JAHA.115.001833
Jayachandran, I. et al. Association of circulatory asymmetric dimethylarginine (ADMA) with diabetic nephropathy in Asian Indians and its causative role in renal cell injury. Clin. Biochem. 50, 835–842 (2017).
pubmed: 28495185 doi: 10.1016/j.clinbiochem.2017.05.007 pmcid: 28495185
Iapichino, G. et al. Time course of endogenous nitric oxide inhibitors in severe sepsis in humans. Minerva Anestesiol. 76, 325–33 (2010).
pubmed: 20395894 pmcid: 20395894
Cupisti, A. et al. Dimethylarginine levels and nutritional status in hemodialysis patients. J. Nephrol 22, 623–629 (2009).
pubmed: 19809995 pmcid: 19809995
Hsu, C. N., Huang, L. T., Lau, Y. T., Lin, C. Y. & Tain, Y. L. The combined ratios of L-arginine and asymmetric and symmetric dimethylarginine as biomarkers in spontaneously hypertensive rats. Transl. Res. 159, 90–98 (2012).
pubmed: 22243793 doi: 10.1016/j.trsl.2011.09.002 pmcid: 22243793
Zobel, E. H. et al. Symmetric and asymmetric dimethylarginine as risk markers of cardiovascular disease, all-cause mortality and deterioration in kidney function in persons with type 2 diabetes and microalbuminuria. Cardiovasc. Diabetol. 16, 1–9 (2017).
doi: 10.1186/s12933-017-0569-8
Matsuguma, K. et al. Molecular mechanism for elevation of asymmetric dimethylarginine and its role for hypertension in chronic kidney disease. J. Am. Soc. Nephrol. 17, 2176–2183 (2006).
pubmed: 16807406 doi: 10.1681/ASN.2005121379 pmcid: 16807406
Jaźwińska-Kozuba, A. et al. Associations between endogenous dimethylarginines and renal function in healthy children and adolescents. Int. J. Mol. Sci. 13, 15464–15474 (2012).
pubmed: 23203136 doi: 10.3390/ijms131115464 pmcid: 23203136
Busch, M., Fleck, C., Wolf, G. & Stein, G. Asymmetrical (ADMA) and symmetrical dimethylarginine (SDMA) as potential risk factors for cardiovascular and renal outcome in chronic kidney disease - Possible candidates for paradoxical epidemiology? Amino Acids 30, 225–232 (2006).
pubmed: 16680555 doi: 10.1007/s00726-005-0268-8 pmcid: 16680555
Oner-Iyidogan, Y. et al. Dimethylarginines and inflammation markers in patients with chronic kidney disease undergoing dialysis. Clin. Exp. Med. 9, 235–241 (2009).
pubmed: 19238516 doi: 10.1007/s10238-009-0035-3 pmcid: 19238516
Shafi, T. et al. Serum Asymmetric and Symmetric Dimethylarginine and Morbidity and Mortality in Hemodialysis Patients. Am. J. Kidney Dis. 70, 48–58 (2017).
pubmed: 28089476 pmcid: 5483385 doi: 10.1053/j.ajkd.2016.10.033
Kielstein, J. T., Salpeter, S. R., Bode-Boeger, S. M., Cooke, J. P. & Fliser, D. Symmetric dimethylarginine (SDMA) as endogenous marker of renal function–a meta-analysis. Nephrol. Dial. Transplant 21, 2446–51 (2006).
pubmed: 16766542 doi: 10.1093/ndt/gfl292 pmcid: 16766542
Anjana, R. M. et al. Prevalence of diabetes and prediabetes (impaired fasting glucose and/or impaired glucose tolerance) in urban and rural India: Phase I results of the Indian Council of Medical Research-INdia DIABetes (ICMR-INDIAB) study. Diabetologia 54, 3022–3027 (2011).
pubmed: 21959957 doi: 10.1007/s00125-011-2291-5 pmcid: 21959957
Unnikrishnan, R., Anjana, R. M. & Mohan, V. Diabetes mellitus and its complications in India. Nat. Rev. Endocrinol 12, 357–70 (2016).
pubmed: 27080137 doi: 10.1038/nrendo.2016.53 pmcid: 27080137
Anand, S. et al. Prevalence of chronic kidney disease in two major Indian cities and projections for associated cardiovascular disease. Kidney Int. 88, 178–85 (2015).
pubmed: 25786102 pmcid: 4490055 doi: 10.1038/ki.2015.58
Unnikrishnan, R. I. et al. Prevalence and risk factors of diabetic nephropathy in an urban South Indian population: the Chennai Urban Rural Epidemiology Study (CURES 45). Diabetes Care 30, 2019–24 (2007).
pubmed: 17488949 doi: 10.2337/dc06-2554 pmcid: 17488949
Brown, C. M., Becker, J. O., Wise, P. M. & Hoofnagle, A. N. Simultaneous determination of 6 L-arginine metabolites in human and mouse plasma by using hydrophilic-interaction chromatography and electrospray tandem mass spectrometry. Clin. Chem 57, 701–709 (2011).
pubmed: 21406573 pmcid: 3199374 doi: 10.1373/clinchem.2010.155895
Paglia, G., D’Apolito, O., Tricarico, F., Garofalo, D. & Corso, G. Evaluation of mobile phase, ion pairing, and temperature influence on an HILIC-MS/MS method for L-arginine and its dimethylated derivatives detection. J. Sep. Sci. 31, 2424–2429 (2008).
pubmed: 18646270 doi: 10.1002/jssc.200800142 pmcid: 18646270
Bhattacharya, N. et al. Matrix-assisted laser desorption/ionization mass spectrometry analysis of dimethyl arginine isomers from urine. Anal. Methods 6, 4602–4609 (2014).
doi: 10.1039/C4AY00309H
Arnold, A. et al. Fast quantitative determination of methylphenidate levels in rat plasma and brain ex vivo by MALDI-MS/MS. J. Mass Spectrom. 50, 963–971 (2015).
pubmed: 28338275 doi: 10.1002/jms.3605 pmcid: 28338275
Chowdhury, T. A., Barnett, A. H. & Bain, S. C. Pathogenesis of diabetic nephropathy. Trends Endocrinol. Metab. 7, 320–3 (1996).
pubmed: 18406765 doi: 10.1016/S1043-2760(96)00152-X pmcid: 18406765
Risk, N., Caramori, M. L., Fioretto, P. & Mauer, M. The Need for Early Predictors of Diabetic Nephropathy Risk. Diabetes 49, 1399–1408 (2000).
doi: 10.2337/diabetes.49.9.1399
Forsblom, C. M., Groop, P. H., Ekstrand, A. & Groop, L. C. Predictive value of microalbuminuria in patients with insulin-dependent diabetes of long duration. Br. Med. J 305, 1051–1053 (1992).
doi: 10.1136/bmj.305.6861.1051
Perkins, B. A. et al. Regression of Microalbuminuria in Type 1 Diabetes. N. Engl. J. Med. 348, 2285–2293 (2003).
pubmed: 12788992 doi: 10.1056/NEJMoa021835 pmcid: 12788992
Bakris, G. L. & Molitch, M. Microalbuminuria as a risk predictor in diabetes: The continuing saga. Diabetes Care 37, 867–875 (2014).
pubmed: 24558077 doi: 10.2337/dc13-1870 pmcid: 24558077
Persson, F. & Rossing, P. Diagnosis of diabetic kidney disease: state of the art and future perspective. Kidney Int. Suppl. 8, 2–7 (2018).
doi: 10.1016/j.kisu.2017.10.003
Surdacki, A., Kruszelnicka, O., Rakowski, T., Jaźwińska-Kozuba, A. & Dubiel, J. S. Asymmetric dimethylarginine predicts decline of glucose tolerance in men with stable coronary artery disease: a 4.5-year follow-up study. Cardiovasc. Diabetol. 12, 64 (2013).
pubmed: 23578341 pmcid: 3642017 doi: 10.1186/1475-2840-12-64
Wolf, C. et al. Urinary asymmetric dimethylarginine (ADMA) is a predictor of mortality risk in patients with coronary artery disease. Int. J. Cardiol. 156, 289–94 (2012).
pubmed: 21159392 doi: 10.1016/j.ijcard.2010.11.003 pmcid: 21159392
Ueda, S., Yamagishi, S., Kaida, Y. & Okuda, S. Asymmetric dimethylarginine may be a missing link between cardiovascular disease and chronic kidney disease. Nephrology (Carlton) 12, 582–90 (2007).
doi: 10.1111/j.1440-1797.2007.00840.x
Gorenflo, M., Zheng, C., Werle, E., Fiehn, W. & Ulmer, H. E. Plasma levels of asymmetrical dimethyl-L-arginine in patients with congenital heart disease and pulmonary hypertension. J. Cardiovasc. Pharmacol. 37, 489–92 (2001).
pubmed: 11300662 doi: 10.1097/00005344-200104000-00016 pmcid: 11300662
Fleck, C., Schweitzer, F., Karge, E., Busch, M. & Stein, G. Serum concentrations of asymmetric (ADMA) and symmetric (SDMA) dimethylarginine in patients with chronic kidney diseases. Clin. Chim. Acta. 336, 1–12 (2003).
pubmed: 14500028 doi: 10.1016/S0009-8981(03)00338-3 pmcid: 14500028
Meinitzer, A. et al. Symmetrical and asymmetrical dimethylarginine as predictors for mortality in patients referred for coronary angiography: The ludwigshafen risk and cardiovascular health study. Clin. Chem 57, 112–121 (2011).
pubmed: 21036946 doi: 10.1373/clinchem.2010.150854 pmcid: 21036946
Schepers, E., Speer, T., Bode-Böger, S. M., Fliser, D. & Kielstein, J. T. Dimethylarginines ADMA and SDMA: the real water-soluble small toxins? Semin. Nephrol. 34, 97–105 (2014).
pubmed: 24780466 doi: 10.1016/j.semnephrol.2014.02.003 pmcid: 24780466
Bouatra, S. et al. The human urine metabolome. Plos One 8, e73076 (2013).
pubmed: 24023812 pmcid: 3762851 doi: 10.1371/journal.pone.0073076
Tarnow, L., Hovind, P., Teerlink, T., Stehouwer, C. D. A. & Parving, H. H. Elevated plasma asymmetric dimethylarginine as a marker of cardiovascular morbidity in early diabetic nephropathy in type 1 diabetes. Diabetes Care 27, 765–9 (2004).
pubmed: 14988299 doi: 10.2337/diacare.27.3.765 pmcid: 14988299
Fliser, D. et al. Asymmetric dimethylarginine and progression of chronic kidney disease: the mild to moderate kidney disease study. J. Am. Soc. Nephrol. 16, 2456–61 (2005).
pubmed: 15930091 doi: 10.1681/ASN.2005020179 pmcid: 15930091
Ravani, P. et al. Asymmetrical dimethylarginine predicts progression to dialysis and death in patients with chronic kidney disease: a competing risks modeling approach. J. Am. Soc. Nephrol. 16, 2449–55 (2005).
pubmed: 15944335 doi: 10.1681/ASN.2005010076 pmcid: 15944335
Duranton, F. et al. Plasma and urinary amino acid metabolomic profiling in patients with different levels of kidney function. Clin. J. Am. Soc. Nephrol. 9, 37–45 (2014).
pubmed: 24235289 doi: 10.2215/CJN.06000613 pmcid: 24235289

Auteurs

Dharmeshkumar Parmar (D)

Biochemical Engineering, CSIR-National Chemical Laboratory, Dr. Homi Bhabha Road, Pune, 411008, India.
Academy of Scientific and Innovative Research, CSIR-NCL Campus, Dr. Homi Bhabha Road, Pune, 411008, India.

Nivedita Bhattacharya (N)

Biochemical Engineering, CSIR-National Chemical Laboratory, Dr. Homi Bhabha Road, Pune, 411008, India.
Academy of Scientific and Innovative Research, CSIR-NCL Campus, Dr. Homi Bhabha Road, Pune, 411008, India.

Shanthini Kannan (S)

Biochemical Engineering, CSIR-National Chemical Laboratory, Dr. Homi Bhabha Road, Pune, 411008, India.
Department of Research Biochemistry, Madras Diabetes Research Foundation, No. 4, Conran Smith Road, Gopalapuram, Chennai, 600086, India.

Sangeetha Vadivel (S)

Biochemical Engineering, CSIR-National Chemical Laboratory, Dr. Homi Bhabha Road, Pune, 411008, India.
Department of Research Biochemistry, Madras Diabetes Research Foundation, No. 4, Conran Smith Road, Gopalapuram, Chennai, 600086, India.

Gautam Kumar Pandey (GK)

Department of Research Biochemistry, Madras Diabetes Research Foundation, No. 4, Conran Smith Road, Gopalapuram, Chennai, 600086, India.

Avinash Ghanate (A)

Biochemical Engineering, CSIR-National Chemical Laboratory, Dr. Homi Bhabha Road, Pune, 411008, India.
Academy of Scientific and Innovative Research, CSIR-NCL Campus, Dr. Homi Bhabha Road, Pune, 411008, India.

Nagarjuna Chary Ragi (NC)

CSIR-Indian Institute of Chemical Technology, Uppal Road, Hyderabad, 500007, India.

Paramasivam Prabu (P)

Department of Research Biochemistry, Madras Diabetes Research Foundation, No. 4, Conran Smith Road, Gopalapuram, Chennai, 600086, India.

Thyparambil Aravindakshan Pramodkumar (TA)

Department of Research Biochemistry, Madras Diabetes Research Foundation, No. 4, Conran Smith Road, Gopalapuram, Chennai, 600086, India.

Nagaraj Manickam (N)

Department of Vascular Biology, Madras Diabetes Research Foundation, No. 4, Conran Smith Road, Gopalapuram, Chennai, 600086, India.

Viswanathan Mohan (V)

Department of Research Biochemistry, Madras Diabetes Research Foundation, No. 4, Conran Smith Road, Gopalapuram, Chennai, 600086, India.

Prabhakar Sripadi (P)

Academy of Scientific and Innovative Research, CSIR-NCL Campus, Dr. Homi Bhabha Road, Pune, 411008, India.
CSIR-Indian Institute of Chemical Technology, Uppal Road, Hyderabad, 500007, India.

Gokulakrishnan Kuppan (G)

Department of Research Biochemistry, Madras Diabetes Research Foundation, No. 4, Conran Smith Road, Gopalapuram, Chennai, 600086, India. gokul@nimhans.ac.in.
Department of Neurochemistry, National Institute of Mental Health and Neurosciences, Hosur Road, Bengaluru, 560029, India. gokul@nimhans.ac.in.

Venkateswarlu Panchagnula (V)

Biochemical Engineering, CSIR-National Chemical Laboratory, Dr. Homi Bhabha Road, Pune, 411008, India. v.panchagnula@ncl.res.in.
Academy of Scientific and Innovative Research, CSIR-NCL Campus, Dr. Homi Bhabha Road, Pune, 411008, India. v.panchagnula@ncl.res.in.

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