The methylglyoxal-derived AGE tetrahydropyrimidine is increased in plasma of individuals with type 1 diabetes mellitus and in atherosclerotic lesions and is associated with sVCAM-1

Diabetologia

Volumn 56, Issue 8, 2013, Pages 1845-1855

  Van Eupen, M G A ^a,b   Schram, M T ^a,b   Colhoun, H M ^c   Hanssen, N M J ^a,b   Niessen, H W M ^d   Tarnow, L ^e,f   Parving, H H ^f,g   Rossing, P ^e,f   Stehouwer, C D A ^a,b   Schalkwijk, C G ^a,b  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

^d VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^e STENO DIABETES CENTER   (Denmark)

^f AARHUS UNIVERSITY   (Denmark)

^g UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Advanced glycation end products; Atherosclerosis; Cardiovascular disease; Endothelial dysfunction; Macrovascular complications; Methylglyoxal; Microvascular complications; Soluble vascular cell adhesion molecule; Tetrahydropyrimidine; Type 1 diabetes mellitus

Indexed keywords

5 HYDRO 5 METHYLIMIDAZOLONE; 6 N CARBOXYETHYLLYSINE; 6 N CARBOXYMETHYLLYSINE; ADVANCED GLYCATION END PRODUCT; ARGPYRIMIDINE; CD68 ANTIGEN; DIAMINO ACID; METHYLGLYOXAL; MONOCLONAL ANTIBODY; PYRIMIDINE DERIVATIVE; SECRETORY PHOSPHOLIPASE A2; TETRAHYDROPYRIMIDINE; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ADULT; ARTICLE; BLOOD LEVEL; COHORT ANALYSIS; CONTROLLED STUDY; CORONARY ARTERY ATHEROSCLEROSIS; DIABETIC ANGIOPATHY; DISEASE ASSOCIATION; ENDOTHELIAL DYSFUNCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; MACROALBUMINURIA; MAJOR CLINICAL STUDY; MALE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS;

ADULT; ATHEROSCLEROSIS; DIABETES MELLITUS, TYPE 1; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; PYRIMIDINES; PYRUVALDEHYDE; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84879993701     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-013-2919-8     Document Type: Article

References (49)

1. Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414:813-820
2. Nin JW, Jorsal A, Ferreira I et al (2011) Higher plasma levels of advanced glycation end products are associated with incident cardiovascular disease and all-cause mortality in type 1 diabetes: a 12-year follow-up study. Diabetes Care 34:442-447
3. Shinohara M, Thornalley PJ, Giardino I et al (1998) Overexpression of glyoxalase-I in bovine endothelial cells inhibits intracellular advanced glycation endproduct formation and prevents hyperglycemia-induced increases in macromolecular endocytosis. J Clin Invest 101:1142-1147
4. Brouwers O, Niessen PM, Ferreira I et al (2011) Overexpression of glyoxalase-I reduces hyperglycemia-induced levels of advanced glycation end products and oxidative stress in diabetic rats. J Biol Chem 286:1374-1380
5. Thornalley PJ (1993) The glyoxalase system in health and disease. Mol Asp Med 14:287-371
6. Rabbani N, Thornalley PJ (2011) Glyoxalase in diabetes, obesity and related disorders. Semin Cell Dev Biol 22:309-317
7. Oya T, Hattori N, Mizuno Y et al (1999) Methylglyoxal modification of protein. Chemical and immunochemical characterization of methylglyoxal-arginine adducts. J Biol Chem 274:18492-18502
8. McLellan AC, Thornalley PJ, Benn J, Sonksen PH (1994) Glyoxalase system in clinical diabetes mellitus and correlation with diabetic complications. Clin Sci (Lond) 87:21-29
9. Kilhovd BK, Giardino I, Torjesen PA et al (2003) Increased serum levels of the specific AGE-compound methylglyoxal-derived hydroimidazolone in patients with type 2 diabetes. Metabolism 52:163-167
10. Wilker SC, Chellan P, Arnold BM, Nagaraj RH (2001) Chromatographic quantification of argpyrimidine, a methylglyoxal-derived product in tissue proteins: comparison with pentosidine. Anal Biochem 290:353-358
11. Ahmed N, Thornalley PJ, Dawczynski J et al (2003) Methylglyoxal-derived hydroimidazolone advanced glycation end-products of human lens proteins. Invest Ophthalmol Vis Sci 44:5287-5292
12. Brock JW, Cotham WE, Thorpe SR, Baynes JW, Ames JM (2007) Detection and identification of arginine modifications on methylglyoxal-modified ribonuclease by mass spectrometric analysis. J Mass Spectrom 42:89-100
13. Klopfer A, Spanneberg R, Glomb MA (2011) Formation of arginine modifications in a model system of Nalpha-tert-butoxycarbonyl (Boc)-arginine with methylglyoxal. J Agric Food Chem 59:394-401
14. Brouwers O, Niessen PM, Haenen G et al (2010) Hyperglycaemia-induced impairment of endothelium-dependent vasorelaxation in rat mesenteric arteries is mediated by intracellular methylglyoxal levels in a pathway dependent on oxidative stress. Diabetologia 53:989-1000
15. Wang H, Liu J, Wu L (2009) Methylglyoxal-induced mitochondrial dysfunction in vascular smooth muscle cells. Biochem Pharmacol 77:1709-1716
16. Rosca MG, Mustata TG, Kinter MT et al (2005) Glycation of mitochondrial proteins from diabetic rat kidney is associated with excess superoxide formation. Am J Physiol Ren Physiol 289:F420-F430
17. Rabbani N, Thornalley PJ (2008) Dicarbonyls linked to damage in the powerhouse: glycation of mitochondrial proteins and oxidative stress. Biochem Soc Trans 36:1045-1050
18. Yao D, Taguchi T, Matsumura T et al (2007) High glucose increases angiopoietin-2 transcription in microvascular endothelial cells through methylglyoxal modification of mSin3A. J Biol Chem 282:31038-31045
19. Ahmed N, Argirov OK, Minhas HS, Cordeiro CA, Thornalley PJ (2002) Assay of advanced glycation endproducts (AGEs): surveying AGEs by chromatographic assay with derivatization by 6-aminoquinolyl-N-hydroxysuccinimidyl-carbamate and application to Nepsilon-carboxymethyl-lysine- and Nepsilon-(1-carboxyethyl) lysine-modified albumin. Biochem J 364:1-14
20. Colhoun HM, Rubens MB, Underwood SR, Fuller JH (2000) The effect of type 1 diabetes mellitus on the gender difference in coronary artery calcification. J Am Coll Cardiol 36:2160-2167
21. Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D (1999) 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 130:461-470
22. Schalkwijk CG, Poland DC, van Dijk W et al (1999) Plasma concentration of C-reactive protein is increased in type I diabetic patients without clinical macroangiopathy and correlates with markers of endothelial dysfunction: evidence for chronic inflammation. Diabetologia 42:351-357
23. Tarnow L, Cambien F, Rossing P et al (1995) Insertion/deletion polymorphism in the angiotensin-I-converting enzyme gene is associated with coronary heart disease in IDDM patients with diabetic nephropathy. Diabetologia 38:798-803
24. De Jager J, Kooy A, Lehert P et al (2005) Effects of short-term treatment with metformin on markers of endothelial function and inflammatory activity in type 2 diabetes mellitus: a randomized, placebo-controlled trial. J Intern Med 257:100-109
25. Schalkwijk CG, Baidoshvili A, Stehouwer CD, van Hinsbergh VW, Niessen HW (2004) Increased accumulation of the glycoxidation product Nepsilon- (carboxymethyl)lysine in hearts of diabetic patients: generation and characterisation of a monoclonal anti-CML antibody. Biochim Biophys Acta 1636:82-89
26. Oya-Ito T, Kawakishi S, Shibata N, Kobayashi M, Osawa T, Uchida K (2002) A novel monoclonal antibody against methylglyoxal-arginine adduct. Int Congr Ser 1245:397-399
27. Hegele J, Buetler T, Delatour T (2008) Comparative LC-MS/MS profiling of free and protein-bound early and advanced glycation-induced lysine modifications in dairy products. Anal Chim Acta 617:85-96
28. Schmidt AM, Hori O, Chen JX et al (1995) Advanced glycation endproducts interacting with their endothelial receptor induce expression of vascular cell adhesion molecule-1 (VCAM-1) in cultured human endothelial cells and in mice. A potential mechanism for the accelerated vasculopathy of diabetes. J Clin Invest 96:1395-1403
29. Vlassara H, Fuh H, Donnelly T, Cybulsky M (1995) Advanced glycation endproducts promote adhesion molecule (VCAM-1, ICAM-1) expression and atheroma formation in normal rabbits. Mol Med 1:447-456
30. Salman AG, Mansour DE, Swelem AH, Al-Zawahary WM, Radwan AA (2009) Pentosidine: a new biochemical marker in diabetic retinopathy. Ophthalmic Res 42:96-98
31. Han Y, Randell E, Vasdev S et al (2009) Plasma advanced glycation endproduct, methylglyoxal-derived hydroimidazolone is elevated in young, complication-free patients with type 1 diabetes. Clin Biochem 42:562-569
32. Ahmed N, Babaei-Jadidi R, Howell SK, Beisswenger PJ, Thornalley PJ (2005) Degradation products of proteins damaged by glycation, oxidation and nitration in clinical type 1 diabetes. Diabetologia 48:1590-1603
33. Smulders RA, Stehouwer CD, Schalkwijk CG, Donker AJ, van Hinsbergh VW, TeKoppele JM (1998) Distinct associations of HbA1c and the urinary excretion of pentosidine, an advanced glycosylation end-product, with markers of endothelial function in insulin-dependent diabetes mellitus. Thromb Haemost 80:52-57
34. Hope SA, Meredith IT (2003) Cellular adhesion molecules and cardiovascular disease. Part II. Their association with conventional and emerging risk factors, acute coronary events and cardiovascular risk prediction. Intern Med J 33:450-462
35. Glowinska B, Urban M, Peczynska J, Florys B (2005) Soluble adhesion molecules (sICAM-1, sVCAM-1) and selectins (sE selectin, sP selectin, sL selectin) levels in children and adolescents with obesity, hypertension, and diabetes. Metabolism 54:1020-1026
36. Richardson M, Hadcock SJ, DeReske M, Cybulsky MI (1994) Increased expression in vivo of VCAM-1 and E-selectin by the aortic endothelium of normolipemic and hyperlipemic diabetic rabbits. Arterioscler Thromb 14:760-769
37. O'Brien KD, Allen MD, McDonald TO et al (1993) Vascular cell adhesion molecule-1 is expressed in human coronary atherosclerotic plaques. Implications for the mode of progression of advanced coronary atherosclerosis. J Clin Invest 92:945-951
38. Peter K, Weirich U, Nordt TK, Ruef J, Bode C (1999) Soluble vascular cell adhesion molecule-1 (VCAM-1) as potential marker of atherosclerosis. Thromb Haemost 82(Suppl 1):38-43
39. Soedamah-Muthu SS, Chaturvedi N, Schalkwijk CG, Stehouwer CD, Ebeling P, Fuller JH (2006) Soluble vascular cell adhesion molecule-1 and soluble E-selectin are associated with micro- and macrovascular complications in type 1 diabetic patients. J Diabetes Complications 20:188-195
40. Clausen P, Jacobsen P, Rossing K, Jensen JS, Parving HH, Feldt-Rasmussen B (2000) Plasma concentrations of VCAM-1 and ICAM-1 are elevated in patients with type 1 diabetes mellitus with microalbuminuria and overt nephropathy. Diabet Med J Br Diabet Assoc 17:644-649
41. Lieuw-a-Fa ML, Schalkwijk CG, Engelse M, van Hinsbergh VW (2006) Interaction of Nepsilon(carboxymethyl)lysine- and methylglyoxal-modified albumin with endothelial cells and macrophages. Splice variants of RAGE may limit the responsiveness of human endothelial cells to AGEs. Thromb Haemost 95:320-328
42. Abordo EA, Thornalley PJ (1997) Synthesis and secretion of tumour necrosis factor-alpha by human monocytic THP-1 cells and chemotaxis induced by human serum albumin derivatives modified with methylglyoxal and glucose-derived advanced glycation endproducts. Immunol Lett 58:139-147
43. Westwood ME, Thornalley PJ (1996) Induction of synthesis and secretion of interleukin 1 beta in the human monocytic THP-1 cells by human serum albumins modified with methylglyoxal and advanced glycation endproducts. Immunol Lett 50:17-21
44. Hurt-Camejo E, Camejo G, Peilot H, Oorni K, Kovanen P (2001) Phospholipase A(2) in vascular disease. Circ Res 89:298-304
45. Piek JJ, de Winter RJ (2003) Type II secretory phospholipase A2: the emerging role of biochemical markers of plaque inflammation. Eur Heart J 24:1804-1806
46. Hirata K, Kubo K (2004) Relationship between blood levels of N-carboxymethyl-lysine and pentosidine and the severity of microangiopathy in type 2 diabetes. Endocr J 51:537-544
47. Fosmark DS, Torjesen PA, Kilhovd BK et al (2006) Increased serum levels of the specific advanced glycation end product methylglyoxal-derived hydroimidazolone are associated with retinopathy in patients with type 2 diabetes mellitus. Metabolism 55:232-236
48. Shimoike T, Inoguchi T, Umeda F, Nawata H, Kawano K, Ochi H (2000) The meaning of serum levels of advanced glycosylation end products in diabetic nephropathy. Metabolism 49:1030-1035
49. Kilhovd BK, Juutilainen A, Lehto S et al (2007) Increased serum levels of advanced glycation endproducts predict total, cardiovascular and coronary mortality in women with type 2 diabetes: a population-based 18 year follow-up study. Diabetologia 50:1409-1417