Proatherogenic Importance of Carbamylation-induced Protein Damage and Type 2 Diabetes Mellitus: A Systematic Review

Author(s): Bahadir Simsek, Karolin Yanar, Ufuk Çakatay*

Journal Name: Current Diabetes Reviews

Volume 16 , Issue 6 , 2020

Become EABM
Become Reviewer
Call for Editor


Introduction & Background: Protein carbamylation is a non-enzymatic and irreversible posttranslational process. It affects functions of numerous enzymes, hormones and receptors playing several roles in diabetes pathogenesis by changing their native structures. Detrimental consequences of oxidative protein damage comprise, but are not limited to glyoxidation, lipoxidation and carbonylation reactions. Since the carbamylated plasma proteins are strongly related to the glycemic control parameters of diabetes, they may have an additive value and emerge as potential biomarkers for the follow up, prognosis and treatment of diabetes mellitus.

Methods & Results: To conduct our systematic review, we used PubMed and Semantic Scholar, and used ‘Protein carbamylation and diabetes’ and ‘Protein carbamylation and atherosclerosis’ as keywords and looked into about five hundred manuscripts. Manuscripts that are not in English were excluded as well as manuscripts that did not mention carbamylation to maintain the focus of the present article. Similar to glycation, carbamylation is able to alter functions of plasma proteins and their interactions with endothelial cells and has been shown to be involved in the development of atherosclerosis.

Conclusion: At this stage, it seems clear that protein carbamylation leads to worse clinical outcomes. To improve patient care, but maybe more importantly to improve healthcare-prevention, we believe the next stage involves understanding how exactly protein carbamylation leads to worse outcomes and when and in what group of people anti-carbamylation therapies must be employed.

Keywords: Carbamylation, carbamylated proteins, diabetes, myeloperoxidase, thiocyanates, atherosclerosis.

Chatterjee B, Thakur SS. Investigation of post-translational modifications in type 2 diabetes. Clin Proteomics 2018; 15: 32.
[] [PMID: 30258344]
Zheng H, Wu J, Jin Z, Yan L-J. Protein modifications as manifestations of hyperglycemic glucotoxicity in diabetes and its complications. Biochem Insights 2016; 9: 1-9.
[] [PMID: 27042090]
Duan G, Walther D. The roles of post-translational modifications in the context of protein interaction networks. PLoS Comput Biol 2015; 11(2) e1004049-e.
Schieber M, Chandel NS. ROS function in redox signaling and oxidative stress. Curr Biol 2014; 24(10): R453-62.
[] [PMID: 24845678]
Asmat U, Abad K, Ismail K. Diabetes mellitus and oxidative stress-A concise review. SPJ 2016; 24(5): 547-53.
Bryk AH, Konieczynska M, Rostoff P, et al. Plasma protein oxidation as a determinant of impaired fibrinolysis in type 2 diabetes. Thromb Haemost 2019; 119(2): 213-22.
[] [PMID: 30605917]
Colombo G, Reggiani F, Cucchiari D, et al. Plasma protein carbonylation in haemodialysed patients: focus on diabetes and gender. Oxid Med Cell Longev 2018; 2018 4149681
[] [PMID: 30057679]
Li X, Xu L, Hou X, et al. Advanced oxidation protein products aggravate tubulointerstitial fibrosis through protein kinase c-dependent mitochondrial injury in early diabetic nephropathy. Antioxid Redox Signal 2019; 30(9): 1162-85.
Hernández-Ramírez E, Sánchez-Chávez G, Estrella-Salazar LA, Salceda R. Nitrosative stress in the rat retina at the onset of streptozotocin-induced diabetes. Cell Physiol Biochem 2017; 42(6): 2353-63.
[] [PMID: 28848155]
Ates I, Kaplan M, Yuksel M, et al. Determination of thiol/disulphide homeostasis in type 1 diabetes mellitus and the factors associated with thiol oxidation. Endocrine 2016; 51(1): 47-51.
[] [PMID: 26547218]
Badar A, Arif Z, Alam K. Role of carbamylated biomolecules in human diseases. IUBMB Life 2018; 70(4): 267-75.
[] [PMID: 29542227]
Apostolov EO, Ray D, Savenka AV, Shah SV, Basnakian AG. Chronic uremia stimulates LDL carbamylation and atherosclerosis. J Am Soc Nephrol 2010; 21(11): 1852-7.
[] [PMID: 20947625]
Carracedo J, Ramírez-Carracedo R, Martínez de Toda I, et al. Protein carbamylation: a marker reflecting increased age-related cell oxidation. Int J Mol Sci 2018; 19(5) E1495
[] [PMID: 29772765]
Gorisse L, Pietrement C, Vuiblet V, et al. Protein carbamylation is a hallmark of aging. Proc Natl Acad Sci USA 2016; 113(5): 1191-6.
[] [PMID: 26712018]
George R. Stark WHS, Stanford Moore. Reactions of the cyanate present in aqueous urea with amino acids and proteins. J Biol Chem 1960; 235(11)
Stark GR. Reactions of cyanate with functional groups of proteins. 3. Reactions with amino and carboxyl groups. Biochemistry 1965; 4(6): 1030-6.
[] [PMID: 5839993]
Odar-Cederlöf I, Lunde P, Sjöqvist F. Abnormal pharmacokinetics of phenytoin in a patient with uraemia. Lancet 1970; 2(7677): 831-2.
[] [PMID: 4196062]
Anton AH. The effect of disease, drugs, and dilution on the binding of sulfonamides in human plasma. Clin Pharmacol Ther 1968; 9(5): 561-7.
[] [PMID: 5676798]
Reidenberg MM, Odar-Cederlöf I, von Bahr C, Borgå O, Sjöqvist F. Protein binding of diphenylhydantoin and desmethylimipramine in plasma from patients with poor renal function. N Engl J Med 1971; 285(5): 264-7.
[] [PMID: 4378402]
Lindner A, Charra B, Sherrard DJ, Scribner BH. Accelerated atherosclerosis in prolonged maintenance hemodialysis. N Engl J Med 1974; 290(13): 697-701.
[] [PMID: 4813742]
Lazarus JM, Lowrie EG, Hampers CL, Merrill JP. Cardiovascular disease in uremic patients on hemodialysis. Kidney Int Suppl 1975; 2: 167-75.
[PMID: 1099301]
Goldstein JL, Ho YK, Basu SK, Brown MS. Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc Natl Acad Sci USA 1979; 76(1): 333-7.
[] [PMID: 218198]
Mahley RW, Weisgraber KH, Innerarity TL. Interaction of plasma lipoproteins containing apolipoproteins B and E with heparin and cell surface receptors. Biochim Biophys Acta 1979; 575(1): 81-91.
[] [PMID: 228738]
Steinbrecher UP, Fisher M, Witztum JL, Curtiss LK. Immunogenicity of homologous low density lipoprotein after methylation, ethylation, acetylation, or carbamylation: generation of antibodies specific for derivatized lysine. J Lipid Res 1984; 25(10): 1109-16.
[PMID: 6439810]
Curtiss LK, Witztum JL. A novel method for generating region-specific monoclonal antibodies to modified proteins. Application to the identification of human glucosylated low density lipoproteins. J Clin Invest 1983; 72(4): 1427-38.
[] [PMID: 6415110]
Gonen B, Goldberg AP, Harter HR, Schonfeld G. Abnormal cell-interactive properties of low-density lipoproteins isolated from patients with chronic renal failure. Metabolism 1985; 34(1): 10-4.
[] [PMID: 3965857]
Esterbauer H, Gebicki J, Puhl H, Jürgens G. The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Free Radic Biol Med 1992; 13(4): 341-90.
[] [PMID: 1398217]
Chait A, Brazg RL, Tribble DL, Krauss RM. Susceptibility of small, dense, low-density lipoproteins to oxidative modification in subjects with the atherogenic lipoprotein phenotype, pattern B. Am J Med 1993; 94(4): 350-6.
[] [PMID: 8475928]
Orekhov AN, Tertov VV, Mukhin DN, Mikhailenko IA. Modification of low density lipoprotein by desialylation causes lipid accumulation in cultured cells: discovery of desialylated lipoprotein with altered cellular metabolism in the blood of atherosclerotic patients. Biochem Biophys Res Commun 1989; 162(1): 206-11.
[] [PMID: 2751649]
Zhang HF, Basra HJ, Steinbrecher UP. Effects of oxidatively modified LDL on cholesterol esterification in cultured macrophages. J Lipid Res 1990; 31(8): 1361-9.
[PMID: 2280179]
Stadtman ER. Covalent modification reactions are marking steps in protein turnover. Biochemistry 1990; 29(27): 6323-31.
[] [PMID: 2207077]
Levine RL, Oliver CN, Fulks RM, Stadtman ER. Turnover of bacterial glutamine synthetase: oxidative inactivation precedes proteolysis. Proc Natl Acad Sci USA 1981; 78(4): 2120-4.
[] [PMID: 6113590]
Rivett AJ. Regulation of intracellular protein turnover: covalent modification as a mechanism of marking proteins for degradation. Curr Top Cell Regul 1986; 28: 291-337.
[] [PMID: 2878793]
Wolff SP, Dean RT. Fragmentation of proteins by free radicals and its effect on their susceptibility to enzymic hydrolysis. Biochem J 1986; 234(2): 399-403.
[] [PMID: 3718475]
Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circ Res 2010; 107(9): 1058-70.
[] [PMID: 21030723]
Wright E Jr, Scism-Bacon JL, Glass LC. Oxidative stress in type 2 diabetes: the role of fasting and postprandial glycaemia. Int J Clin Pract 2006; 60(3): 308-14.
[] [PMID: 16494646]
Matough FA, Budin SB, Hamid ZA, Alwahaibi N, Mohamed J. The role of oxidative stress and antioxidants in diabetic complications. Sultan Qaboos Univ Med J 2012; 12(1): 5-18.
[] [PMID: 22375253]
Hörkkö S, Savolainen MJ, Kervinen K, Kesäniemi YA. Carbamylation-induced alterations in low-density lipoprotein metabolism. Kidney Int 1992; 41(5): 1175-81.
[] [PMID: 1319520]
Osborn L, Hession C, Tizard R, et al. Direct expression cloning of vascular cell adhesion molecule 1, a cytokine-induced endothelial protein that binds to lymphocytes. Cell 1989; 59(6): 1203-11.
[] [PMID: 2688898]
Rice GE, Bevilacqua MP. An inducible endothelial cell surface glycoprotein mediates melanoma adhesion. Science 1989; 246(4935): 1303-6.
[] [PMID: 2588007]
Kume N, Cybulsky MI, Gimbrone MA Jr. Lysophosphatidylcholine, a component of atherogenic lipoproteins, induces mononuclear leukocyte adhesion molecules in cultured human and rabbit arterial endothelial cells. J Clin Invest 1992; 90(3): 1138-44.
[] [PMID: 1381720]
Li H, Cybulsky MI, Gimbrone MA Jr, Libby P. An atherogenic diet rapidly induces VCAM-1, a cytokine-regulatable mononuclear leukocyte adhesion molecule, in rabbit aortic endothelium. Arterioscler Thromb 1993; 13(2): 197-204.
Cybulsky MI, Gimbrone MA Jr. Endothelial expression of a mononuclear leukocyte adhesion molecule during atherogenesis. Science 1991; 251(4995): 788-91.
[] [PMID: 1990440]
Libby P, Li H. Vascular cell adhesion molecule-1 and smooth muscle cell activation during atherogenesis. J Clin Invest 1993; 92(2): 538-9.
[] [PMID: 7688759]
Witztum JL, Steinberg D. Role of oxidized low density lipoprotein in atherogenesis. J Clin Invest 1991; 88(6): 1785-92.
[] [PMID: 1752940]
Kraus LM, Elberger AJ, Handorf CR, Pabst MJ, Kraus AP Jr. Urea-derived cyanate forms epsilon-amino-carbamoyl-lysine (homocitrulline) in leukocyte proteins in patients with end-stage renal disease on peritoneal dialysis. J Lab Clin Med 1994; 123(6): 882-91.
[PMID: 8201267]
Roxborough HE, Young IS. Carbamylation of proteins and atherogenesis in renal failure. Med Hypotheses 1995; 45(2): 125-8.
[] [PMID: 8531833]
Roxborough HE, Millar CA, McEneny J, Young IS. Carbamylation inhibits the ferroxidase activity of caeruloplasmin. Biochem Biophys Res Commun 1995; 214(3): 1073-8.
[] [PMID: 7575512]
Stim J, Shaykh M, Anwar F, Ansari A, Arruda JA, Dunea G. Factors determining hemoglobin carbamylation in renal failure. Kidney Int 1995; 48(5): 1605-10.
[] [PMID: 8544421]
Parsy D, Dracon M, Cachera C, et al. Lipoprotein abnormalities in chronic haemodialysis patients. Nephrol Dial Transplant 1988; 3(1): 51-6.
[PMID: 3132640]
Drüeke TB. Genesis of atherosclerosis in uremic patients. Miner Electrolyte Metab 1999; 25(4-6): 251-7.
[] [PMID: 10681648]
Shaykh M, Pegoraro AA, Mo W, Arruda JA, Dunea G, Singh AK. Carbamylated proteins activate glomerular mesangial cells and stimulate collagen deposition. J Lab Clin Med 1999; 133(3): 302-8.
[] [PMID: 10072262]
Kraus LM, Kraus AP Jr. Carbamoylation of amino acids and proteins in uremia. Kidney Int Suppl 2001; 78: S102-7.
[] [PMID: 11168993]
Kraus LM, Kraus AP Jr. The search for the uremic toxin: the case for carbamoylation of amino acids and proteins. Wien Klin Wochenschr 1998; 110(15): 521-30.
[PMID: 9782570]
Hasuike Y, Nakanishi T, Maeda K, Tanaka T, Inoue T, Takamitsu Y. Carbamylated hemoglobin as a therapeutic marker in hemodialysis. Nephron 2002; 91(2): 228-34.
[] [PMID: 12053058]
Pecoits-Filho R, Lindholm B, Stenvinkel P. The malnutrition, inflammation, and atherosclerosis (MIA) syndrome -- the heart of the matter. Nephrol Dial Transplant 2002; 17(Suppl. 11): 28-31.
[] [PMID: 12386254]
Himmelfarb J, Stenvinkel P, Ikizler TA, Hakim RM. The elephant in uremia: oxidant stress as a unifying concept of cardiovascular disease in uremia. Kidney Int 2002; 62(5): 1524-38.
[] [PMID: 12371953]
Kayali R, Cakatay U, Telci A, Akçay T, Sivas A, Altug T. Decrease in mitochondrial oxidative protein damage parameters in the streptozotocin-diabetic rat. Diabetes Metab Res Rev 2004; 20(4): 315-21.
[] [PMID: 15250034]
Kayali R, Telci A, Cakatay U, et al. Oxidative protein damage parameters in plasma in chronic experimental diabetes in rats. Eur J Med Res 2003; 8(7): 307-12.
[PMID: 12911868]
Telci A, Çakatay U, Salman S, Satman I, Sivas A. Oxidative protein damage in early stage Type 1 diabetic patients. Diabetes Res Clin Pract 2000; 50(3): 213-23.
[] [PMID: 11106836]
Telci A, Cakatay U, Kayali R, Erdogan C, Orhan Y, Sivas A, et al. Oxidative protein damage in plasma of type 2 diabetic patients.Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme 2000; 32(1): 40-3.
Gelisgen R, Genc H, Kayali R, et al. Protein oxidation markers in women with and without gestational diabetes mellitus: a possible relation with paraoxonase activity. Diabetes Res Clin Pract 2011; 94(3): 404-9.
[] [PMID: 21885148]
Cakatay U, Kayali R. The evaluation of altered redox status in plasma and mitochondria of acute and chronic diabetic rats. Clin Biochem 2006; 39(9): 907-12.
[] [PMID: 16806143]
Çakatay U. Protein oxidation parameters in type 2 diabetic patients with good and poor glycaemic control. Diabetes Metab 2005; 31(6): 551-7.
[] [PMID: 16357803]
Cakatay U, Telci A, Kayali R, Sivas A, Akçay T. Effect of alpha-lipoic acid supplementation on oxidative protein damage in the streptozotocin-diabetic rat. Res Exp Med (Berl) 2000; 199(4): 243-51.
[] [PMID: 10743682]
Cakatay U, Telci A, Salman S, Satman L, Sivas A. Oxidative protein damage in type I diabetic patients with and without complications. Endocr Res 2000; 26(3): 365-79.
[] [PMID: 11019902]
Abell SK, De Courten B, Boyle JA, Teede HJ. inflammatory and other biomarkers: role in pathophysiology and prediction of gestational diabetes mellitus. Int J Mol Sci 2015; 16(6): 13442-73.
[] [PMID: 26110385]
Meigs JB, Hu FB, Rifai N, Manson JE. Biomarkers of endothelial dysfunction and risk of type 2 diabetes mellitus. JAMA 2004; 291(16): 1978-86.
[] [PMID: 15113816]
van der Leeuw J, Beulens JW, van Dieren S, et al. Novel biomarkers to improve the prediction of cardiovascular event risk in type 2 diabetes mellitus. J Am Heart Assoc 2016; 5(6) e003048
[] [PMID: 27247335]
Ritz E. Atherosclerosis in dialyzed patients. Blood Purif 2004; 22(1): 28-37.
[] [PMID: 14732809]
Zhang R, Brennan ML, Shen Z, et al. Myeloperoxidase functions as a major enzymatic catalyst for initiation of lipid peroxidation at sites of inflammation. J Biol Chem 2002; 277(48): 46116-22.
[] [PMID: 12359714]
Hazen SL. Myeloperoxidase and plaque vulnerability. Arterioscler Thromb Vasc Biol 2004; 24(7): 1143-6.
[] [PMID: 15237089]
Garnotel R, Sabbah N, Jaisson S, Gillery P. Enhanced activation of and increased production of matrix metalloproteinase-9 by human blood monocytes upon adhering to carbamylated collagen. FEBS Lett 2004; 563(1-3): 13-6.
[] [PMID: 15063715]
Koro C, Bielecka E, Dahl-Knudsen A, et al. Carbamylation of immunoglobulin abrogates activation of the classical complement pathway. Eur J Immunol 2014; 44(11): 3403-12.
[] [PMID: 25130613]
Drechsler C, Kalim S, Wenger JB, et al. Protein carbamylation is associated with heart failure and mortality in diabetic patients with end-stage renal disease. Kidney Int 2015; 87(6): 1201-8.
[] [PMID: 25671766]
Wanner C, Krane V, März W, et al. Deutsche diabetes-dialyse-studie (4d) study group. randomized controlled trial on the efficacy and safety of atorvastatin in patients with type 2 diabetes on hemodialysis (4d study): demographic and baseline characteristics. Kidney Blood Press Res 2004; 27(4): 259-66.
[] [PMID: 15316128]
Kalim S, Trottier CA, Wenger JB, et al. Longitudinal changes in protein carbamylation and mortality risk after initiation of hemodialysis. Clin J Am Soc Nephrol 2016; 11(10): 1809-16.
[] [PMID: 27445162]
Holy EW, Akhmedov A, Speer T, et al. Carbamylated low-density lipoproteins induce a prothrombotic state via lox-1: impact on arterial thrombus formation in vivo. J Am Coll Cardiol 2016; 68(15): 1664-76.
[] [PMID: 27712780]
Tang WH, Hazen SL. Carbamylated low-density lipoprotein and thrombotic risk in chronic kidney disease. J Am Coll Cardiol 2016; 68(15): 1677-9.
[] [PMID: 27712781]
Terman A. Garbage catastrophe theory of aging: imperfect removal of oxidative damage? Redox report: communications in free radical research 2001; 6(1): 15-26.
Terman A, Brunk UT. Oxidative stress, accumulation of biological'garbage', and aging. Antioxidants redox signaling 2006; 8(1-2): 197-204.
Bhattacharya D, Mukhopadhyay M, Bhattacharyya M, Karmakar P. Is autophagy associated with diabetes mellitus and its complications? A review. EXCLI J 2018; 17: 709-20.
[PMID: 30190661]
Hayes HL, Peterson BS, Haldeman JM, Newgard CB, Hohmeier HE, Stephens SB. Delayed apoptosis allows islet β-cells to implement an autophagic mechanism to promote cell survival. PLoS One 2017; 12(2) e0172567
[] [PMID: 28212395]
Shiu SW, Xiao SM, Wong Y, Chow WS, Lam KS, Tan KC. Carbamylation of LDL and its relationship with myeloperoxidase in type 2 diabetes mellitus. Clinical science (London, England : 1979) 2014; 126(2): 175-81.
Nicolas C, Jaisson S, Gorisse L, et al. Carbamylation is a competitor of glycation for protein modification in vivo. Diabetes Metab 2018; 44(2): 160-7.
[] [PMID: 28690125]
Desmons A, Jaisson S, Leroy N, Gillery P, Guillard E. Labile glycated haemoglobin and carbamylated haemoglobin are still critical points for HbA1c measurement. Biochem Med (Zagreb) 2017; 27(2): 378-86.
[] [PMID: 28694727]
Simsek B, Çakatay U. Could ornithine supplementation be beneficial to prevent the formation of pro-atherogenic carbamylated low-density lipoprotein (c-LDL) particles? Med Hypotheses 2019; 126: 20-2.
[] [PMID: 31010493]
Jaisson S, Pietrement C, Gillery P. Protein carbamylation: chemistry, pathophysiological involvement, and biomarkers. Adv Clin Chem 2018; 84: 1-38.
[] [PMID: 29478512]
Koro C, Hellvard A, Delaleu N, et al. Carbamylated LL-37 as a modulator of the immune response. Innate Immun 2016; 22(3): 218-29.
[] [PMID: 26878866]
Jaisson S, Pietrement C, Gillery P. Carbamylation-derived products: bioactive compounds and potential biomarkers in chronic renal failure and atherosclerosis. Clin Chem 2011; 57(11): 1499-505.
[] [PMID: 21768218]
Iannuzzi C, Irace G, Sirangelo I. Differential effects of glycation on protein aggregation and amyloid formation. Front Mol Biosci 2014; 1: 9.
[] [PMID: 25988150]
Oimomi M, Hatanaka H, Yoshimura Y, Yokono K, Baba S, Taketomi Y. Carbamylation of insulin and its biological activity. Nephron 1987; 46(1): 63-6.
[] [PMID: 3299118]
Tsou CL, Tian WX, Zhao KY. Kinetics of irreversible modification of enzyme activity Molecular Architecture of Proteins and Enzymes. Academic Press 1985; pp. 15-30.
Nilsson L, Lundquist P, Kågedal B, Larsson R. Plasma cyanate concentrations in chronic renal failure. Clin Chem 1996; 42(3): 482-3.
[PMID: 8598126]
Tarif N, Shaykh M, Stim J, Arruda JA, Dunea G. Carbamylated hemoglobin in hemodialysis patients. Am J Kidney Dis 1997; 30(3): 361-5.
[] [PMID: 9292564]
Chang CT, Lim YP, Lee CW, et al. PON-1 carbamylation is enhanced in HDL of uremia patients. Yao Wu Shi Pin Fen Xi 2019; 27(2): 542-50.
[] [PMID: 30987726]
Crow JA, Meek EC, Wills RW, Chambers JE. A case-control study: The association of serum paraoxonase 1 activity and concentration with the development of type 2 diabetes mellitus. Diabetes Metab Res Rev 2018; 34(3)
[] [PMID: 29156090]
Kalim S. Protein carbamylation in end stage renal disease: is there a mortality effect? Curr Opin Nephrol Hypertens 2018; 27(6): 454-62.
[] [PMID: 30148723]
Velasquez MT, Ramezani A, Raj DS. Urea and protein carbamylation in ESRD: surrogate markers or partners in crime? Kidney Int 2015; 87(6): 1092-4.
[] [PMID: 26024026]
Pietrement C, Gorisse L, Jaisson S, Gillery P. Chronic increase of urea leads to carbamylated proteins accumulation in tissues in a mouse model of CKD. PLoS One 2013; 8(12) e82506
[] [PMID: 24324801]
Di Iorio BR, Marzocco S, Bellasi A, et al. Nutritional therapy reduces protein carbamylation through urea lowering in chronic kidney disease. Nephrol Dial Transplant 2018; 33(5): 804-13.
[] [PMID: 28992314]
Delporte C, Zouaoui Boudjeltia K, Furtmüller PG, et al. Myeloperoxidase-catalyzed oxidation of cyanide to cyanate: A potential carbamylation route involved in the formation of atherosclerotic plaques? J Biol Chem 2018; 293(17): 6374-86.
[] [PMID: 29496995]
Kato Y. Neutrophil myeloperoxidase and its substrates: formation of specific markers and reactive compounds during inflammation. J Clin Biochem Nutr 2016; 58(2): 99-104.
[] [PMID: 27013775]
Khan AA, Alsahli MA, Rahmani AH. Myeloperoxidase as an active disease biomarker: recent biochemical and pathological perspectives. Med Sci (Basel) 2018; 6(2): 33.
Simsek B, Çakatay U. Could cyanogenic glycoside rich diet cause increased risk for carbamylation-induced protein damage in individuals with chronic inflammatory diseases? Med Hypotheses 2019; 130 109275
[] [PMID: 31383327]
WHO Ambient Air Pollution: A Global Assessment of Exposure and Burden of Disease World Health Organization. 2016.
Landrigan PJ, Fuller R, Hu H, et al. Pollution and Global Health – An Agenda for Prevention. Environ Health Perspect 2018; 126(8) 084501
[] [PMID: 30118434]
Landrigan PJ, Fuller R, Acosta NJR, et al. The Lancet Commission on pollution and health. Lancet 2018; 391(10119): 462-512.
[] [PMID: 29056410]
Rajagopalan S, Brook RD. Air pollution and type 2 diabetes: mechanistic insights. Diabetes 2012; 61(12): 3037-45.
[] [PMID: 23172950]
Li H, Duan D, Xu J, et al. Ambient air pollution and risk of type 2 diabetes in the Chinese. Environ Sci Pollut Res Int 2019; 26(16): 16261-73.
[] [PMID: 30977004]
Yang BY, Guo Y, Markevych I, et al. Association of long-term exposure to ambient air pollutants with risk factors for cardiovascular disease in China. JAMA Netw Open 2019; 2(3) e190318
[] [PMID: 30848806]
Thiering E, Heinrich J. Epidemiology of air pollution and diabetes. Trends Endocrinol Metab 2015; 26(7): 384-94.
[] [PMID: 26068457]
Roberts JM, Veres PR, Cochran AK, et al. Isocyanic acid in the atmosphere and its possible link to smoke-related health effects. Proc Natl Acad Sci USA 2011; 108(22): 8966-71.
[] [PMID: 21576489]
Lee D, Wexler AS. Atmospheric amines – Part III: Photochemistry and toxicity. Atmos Environ 2013; 71: 95-103.
Kalim S, Ortiz G, Trottier CA. Deferio JJ, Karumanchi SA, Thadhani RI, et al. The effects of parenteral amino acid therapy on protein carbamylation in maintenance hemodialysis patients. J Ren Nutr 2015; 25(4): 388-92.
Holzer M, Zangger K, El-Gamal D, et al. Myeloperoxidase-derived chlorinating species induce protein carbamylation through decomposition of thiocyanate and urea: novel pathways generating dysfunctional high-density lipoprotein. Antioxid Redox Signal 2012; 17(8): 1043-52.
Jaisson S, Desmons A, Doué M, Gorisse L, Pietrement C, Gillery P. Measurement of homocitrulline, a carbamylation-derived product, in serum and tissues by lc-ms/ms. Curr Protoc Protein Sci 2018; 92(1) e56
[] [PMID: 30040196]
Shah SV, Apostolov EO, Ok E, Basnakian AG. Novel mechanisms in accelerated atherosclerosis in kidney disease. J Ren Nutr 2008; 18(1): 65-9.
Carracedo J, Merino A, Briceño C, et al. Carbamylated low-density lipoprotein induces oxidative stress and accelerated senescence in human endothelial progenitor cells. FASEB J 2011; 25(4): 1314-22.
[] [PMID: 21228221]
Asci G, Basci A, Shah SV, et al. Carbamylated low-density lipoprotein induces proliferation and increases adhesion molecule expression of human coronary artery smooth muscle cells. Nephrology (Carlton) 2008; 13(6): 480-6.
[] [PMID: 18518940]
Ghaffari MA, Shanaki M. Evalution of in vitro effect of flavonoids on human low-density lipoprotein carbamylation. Iran J Pharm Res 2010; 9(1): 67-74.
[PMID: 24363709]
Mydel P, Wang Z, Brisslert M, et al. Carbamylation-dependentactivation of T cells: a novel mechanism in the pathogenesis of autoimmune arthritis. Journal of immunology (Baltimore, Md :1950) 2010; 184(12): 6882-90.
Kummu O, Turunen SP, Wang C, et al. Carbamyl adducts on lowdensity lipoprotein induce IgG response in LDLR-/- mice and bind plasma autoantibodies in humans under enhanced carbamylation.Antioxidants redox signaling 2013; 19(10): 1047-62.
El-Gamal D, Rao SP, Holzer M, et al. The urea decomposition product cyanate promotes endothelial dysfunction. Kidney Int 2014; 86(5): 923-31.
[] [PMID: 24940796]
Verbrugge FH, Tang WH, Hazen SL. Protein carbamylation and cardiovascular disease. Kidney Int 2015; 88(3): 474-8.
[] [PMID: 26061545]
Koeth RA, Kalantar-Zadeh K, Wang Z, Fu X, Tang WH, Hazen SL. Protein carbamylation predicts mortality in ESRD. J Am Soc Nephrol 2013; 24(5): 853-61.
[] [PMID: 23431074]
Berg AH, Drechsler C, Wenger J, et al. Carbamylation of serum albumin as a risk factor for mortality in patients with kidney failure. Sci Transl Med 2013; 5(175) 175ra29

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2020
Page: [608 - 618]
Pages: 11
DOI: 10.2174/1573399816666200107102918
Price: $65

Article Metrics

PDF: 21