Methylglyoxal, glyoxalase 1 and the dicarbonyl proteome

Amino Acids

Volumn 42, Issue 4, 2012, Pages 1133-1142

  Rabbani, Naila ^a   Thornalley, Paul J ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Ageing; Diabetes; Glycation; Glyoxalase; Methylglyoxal; Oxidative stress; Proteomics; Renal failure

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ALBUMIN; CRYSTALLIN; DICARBONYL PROTEOME; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEMOGLOBIN; HYDROIMIDAZOLONE N DELTA (5 HYDRO 5 METHYL 4 IMIDAZOLON 2 YL)ORNITHINE; LACTOYLGLUTATHIONE LYASE; METHYLGLYOXAL; MITOCHONDRIAL PROTEIN; ORNITHINE DERIVATIVE; PROTEOME; SCLEROPROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; PROTEIN;

APOPTOSIS; AUTOPHAGY; BIOINFORMATICS; CATABOLISM; CHEMICAL ANALYSIS; CHEMICAL STRUCTURE; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DYSLIPIDEMIA; GLUCOSE INTAKE; GLYCATION; HUMAN; IMMUNOBLOTTING; MOLECULAR DYNAMICS; NEPHRECTOMY; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; PROTEIN MODIFICATION; PROTEOMICS; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; GLYCOSYLATION; METABOLISM;

ANIMALIA; FUNGI; PROTOCTISTA;

ANIMALS; GLYCOSYLATION; HUMANS; LACTOYLGLUTATHIONE LYASE; PROTEINS; PROTEOME; PYRUVALDEHYDE;

EID: 84862688640     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-010-0783-0     Document Type: Review

References (93)

1. Abordo EA, Minhas HS, Thornalley PJ (1999) Accumulation of a-oxoaldehydes during oxidative stress. A role in cytotoxicity. Biochem Pharmacol 58:641-648 (Pubitemid 29296884)
2. Agalou S, Ahmed N, Babaei-Jadidi R, Dawnay A, Thornalley PJ (2005) Profound mishandling of protein glycation degradation products in uremia and dialysis. J Am Soc Nephrol 16:1471-1485 (Pubitemid 41716533)
3. Ahmed N, Argirov OK, Minhas HS, Cordeiro CA, Thornalley PJ (2002) Assay of advanced glycation endproducts (AGEs): surveying AGEs by chromatographic assay with derivatisation by aminoquinolyl-N-hydroxysuccimidyl-carbamate and application to Ne-carboxymethyl-lysine- and Ne-(1-carboxyethyl)lysinemodified albumin. Biochem J 364:1-14 (Pubitemid 34538940)
4. Ahmed N, Thornalley PJ, Dawczynski J, Franke S, Strobel J, Stein G, Haik JRGM (2003) Methylglyoxal-derived hydroimidazolone advanced glycation endproducts of human lens proteins. Invest Ophthalmol Vis Sci 44:5287-5292 (Pubitemid 37475400)
5. Ahmed N, Ahmed U, Thornalley PJ, Hager K, Fleischer GA, Munch G (2004a) Protein glycation, oxidation and nitration marker residues and free adducts of cerebrospinal fluid in Alzheimer's disease and link to cognitive impairment. J Neurochem 92:255-263 (Pubitemid 40194017)
6. Ahmed N, Thornalley PJ, Luthen R, Haussinger D, Sebekova K, Schinzel R, Voelker W, Heidland A (2004b) Processing of protein glycation, oxidation and nitrosation adducts in the liver and the effect of cirrhosis. J Hepatol 41:913-919 (Pubitemid 39575657)
7. Ahmed N, Babaei-Jadidi R, Howell SK, Beisswenger PJ, Thornalley PJ (2005a) Degradation products of proteins damaged by glycation, oxidation and nitration in clinical type 1 diabetes. Diabetologia 48:1590-1603 (Pubitemid 41175513)
8. Ahmed N, Dobler D, Dean M, Thornalley PJ (2005b) Peptide mapping identifies hotspot site of modification in human serum albumin by methylglyoxal involved in ligand binding and esterase activity. J Biol Chem 280:5724-5732 (Pubitemid 40280052)
9. Ahmed N, Mirshekar-Syahkal B, Kennish L, Karachalias N, Babaei- Jadidi R, Thornalley PJ (2005c) Assay of advanced glycation endproducts in selected beverages and food by liquid chromatography with tandem mass spectrometric detection. Mol Nutr Food Res 49:691-699 (Pubitemid 41008207)
10. Ahmed N, Ahmed U, Thornalley PJ, Watts R, Tarr J, Haigh R, Winyard P (2006) Profound increase in proteolytic products of glycated and oxidised proteins in synovial fluid and plasma in osteoarthritis and rheumatoid arthritis, corrected by TNF-a antibody therapy in rheumatoid arthritis. Rheumatology 45(Suppl 1):i53
11. Ahmed U, Dobler D, Larkin SJ, Rabbani N, Thornalley PJ (2008) Reversal of hyperglycemia-induced angiogenesis deficit of human endothelial cells by overexpression of glyoxalase 1 in vitro. Maillard reaction. Ann N Y Acad Sci 1126:262-264 (Pubitemid 351589297)
12. Baba SP, Barski OA, Ahmed Y, O'Toole TE, Conklin DJ, Bhatnagar A, Srivastava S (2009) Reductive metabolism of AGE precursors: a metabolic route for preventing AGE accumulation in cardiovascular tissue. Diabetes 58:2486-2497
13. Bechtold U, Rabbani N, Mullineaux PM, Thornalley PJ (2009) Quantitative measurement of specific biomarkers for protein oxidation, nitration and glycation in Arabidopsis leaves. Plant J 59:661-671
14. Beisswenger PJ, Howell S, Touchette A, Lal S, Szwergold BS (1999) Metformin reduces systemic methylglyoxal levels in type 2 diabetes. Diabetes 48:198-202 (Pubitemid 29019373)
15. Biemel KM, Friedl DA, Lederer MO (2002) Identification and quantification of major Maillard cross-links in human serum albumin and lens protein - evidence for glucosepane as the dominant compound. J Biol Chem 277:24907-24915 (Pubitemid 34951792)
16. Blom N, Sicheritz-Ponten T, Gupta R, Gammeltoft S, Brunak S (2004) Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4:1633-1649 (Pubitemid 38738322)
17. Bookchin RM, Gallop PM (1968) Structure of hemoglobin A1c: nature of the N-terminal b-chain blocking group. Biochem Biophys Res Commun 32:86-93
18. Brouwers O, Niessen P, Haenen G, Miyata T, Brownlee M, Stehouwer C, De Mey J, Schalkwijk C (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
19. Ceradini DJ, Yao D, Grogan RH, Callaghan MJ, Edelstein D, Brownlee M, Gurtner GC (2008) Decreasing intracellular superoxide corrects defective ischemia-induced new vessel formation in diabetic mice. J Biol Chem 283:10930-10938
20. Chan WH, Wu HJ, Shiao NH (2007) Apoptotic signaling in methylglyoxal-treated human osteoblasts involves oxidative stress, c-jun N-terminal kinase, caspase-3, and p21-activated kinase 2. J Cell Biochem 100:1056-1069
21. Chen Y, Ahmed N, Thornalley PJ (2005) Peptide mapping of human hemoglobin modified minimally by methylglyoxal in vitro. Ann N Y Acad Sci 1043:905
22. Delpierre G, Rider MH, Collard F, Stroobant V, Vanstapel F, Santos H, Van Schaftingen E (2000) Identification, cloning, and heterologous expression of a mammalian fructosamine-3-kinase. Diabetes 49:1627-1634
23. Dobler D, Ahmed N, Song LJ, Eboigbodin KE, Thornalley PJ (2006) Increased dicarbonyl metabolism in endothelial cells in hyperglycemia induces anoikis and impairs angiogenesis by RGD and GFOGER motif modification. Diabetes 55:1961-1969 (Pubitemid 44509968)
24. Dolhofer R, Wieland OH (1979) Glycosylation of serum-albumin - elevated glycosyl-albumin in diabetic-patients. FEBS Lett 103:282-286 (Pubitemid 9230516)
25. Dudek EJ, Shang F, Liu Q, Valverde P, Hobbs M, Taylor A (2005) Selectivity of the ubiquitin pathway for oxidatively modified proteins: relevance to protein precipitation diseases. FASEB J 19:1707-1709 (Pubitemid 41429537)
26. Duran-Jimenez B, Dobler D, Moffat S, Rabbani N, Streuli CH, Thornalley PJ, Tomlinson D, Gardiner NJ (2009) Advanced glycation endproducts in extracellular matrix proteins contribute to the failure of sensory nerve regeneration in diabetes. Diabetes 58:2893-2903
27. Ellis KJ (2000) Human body composition: in vivo methods. Physiol Rev 80:649-680 (Pubitemid 30164946)
28. Emsley J, Knight CG, Farndale RW, Barnes MJ, Liddington RC (2000) Structural basis of collagen recognition by integrin alpha 2 beta 1. Cell 101:47-56
29. Franch HA, Sooparb S, Du J (2001) A mechanism regulating proteolysis of specific proteins during renal tubular cell growth. J Biol Chem 276:19126-19131
30. Gallet X, Charloteaux B, Thomas A, Braseur R (2000) A fast method to predict protein interaction sites from sequences. J Mol Biol 302:917-926
31. Gangadhariah MH, Wang BL, Linetsky M, Henning C, Spanneberg R, Glomb MA, Nagaraj RH (2010) Hydroimidazolone modification of human alpha A-crystallin: effect on the chaperone function and protein refolding ability. Biochim Biophy Acta Mol Basis Dis 1802:432-441
32. Gao Y, Wang YS (2006) Site-selective modifications of arginine residues in human hemoglobin induced by methylglyoxal. Biochemistry 45:15654-15660 (Pubitemid 46032486)
33. Goldberg AL, Akopian TN, Kisselev AF, Lee DH (1997) Protein degradation by the proteasome and dissection of its in vivo importance with synthetic inhibitors. Mol Biol Rep 24:69-75 (Pubitemid 27269429)
34. Gomes RA, Oliveira LMA, Silva M, Ascenso C, Quintas A, Costa G, Coelho AV, Silva MS, Ferreira AEN, Freire AP, Cordeiro C (2008) Protein glycation in vivo: functional and structural effects on yeast enolase. Biochem J 416:317-326
35. Gottschalk KE, Kessler H (2002) The structures of integrins and integrin-ligand complexes: implications for drug design and signal transduction. Angew Chem Int Ed 41:3767-3774 (Pubitemid 35277998)
36. Grune T, Reinheckel T, Davies KJA (1996) Degradation of oxidized proteins in K562 human hematopoietic cells by proteasome. J Biol Chem 271:15504-15509 (Pubitemid 26225322)
37. Henle T, Walter A, Haeßner R, Klostermeryer H (1994) Detection and identification of a protein-bound imidazolone resulting from the reaction of arginine residues and methylglyoxal. Z Lebensm Unters Forsch 199:55-58
38. Hernebring M, Brolen G, Aguilaniu H, Semb H, Nystrom T (2006) Elimination of damaged proteins during differentiation of embryonic stem cells. PNAS 103:7700-7705
39. Jerzykowski T, Matuszewski W, Tarnawski R, Winter R, Herman ZS, Sokola A (1975) Changes of certain pharmacological and biochemical indices in acute methylglyoxal poisoning. Arch Immunol Ther Exp 23:549-560
40. Kang Y, Edwards LG, Thornalley PJ (1996) Effect of methylglyoxal on human leukaemia 60 cell growth: modification of DNA, G1 growth arrest and induction of apoptosis. Leuk Res 20:397-405 (Pubitemid 26197249)
41. Karachalias N, Babaei-Jadidi R, Rabbani N, Thornalley P (2010) Increased protein damage in renal glomeruli, retina, nerve, plasma and urine and its prevention by thiamine and benfotiamine therapy in a rat model of diabetes. Diabetologia 53:1506-1516
42. Kim Y, Nakase H, Nagata K, Sakaki T, Maeda M, Yamamoto K (2004) Observation of arterial and venous thrombus formation by scanning and transmission electron microscopy. Acta Neurochir 146:45-51 (Pubitemid 38186206)
43. Knight CG, Morton LF, Peachey AR, Tuckwell DS, Farndale RW, Barnes MJ (2000) The collagen-binding A-domains of integrins alpha(1)beta(1) and alpha(2)beta(1) recognize the same specific amino acid sequence, GFOGER, in native (triple-helical) collagens. J Biol Chem 275:35-40 (Pubitemid 30038949)
44. Koenig RJ, Blobstein SH, Cerami A (1977) Structure of carbohydrate of hemoglobin A1c. J Biol Chem 252:2992-2997
45. Kumagai T, Nangaku M, Kojima I, Nagai R, Ingelfinger JR, Miyata T, Fujita T, Inagi R (2009) Glyoxalase I overexpression ameliorates renal ischemia-reperfusion injury in rats. Am J Physiol Renal Physiol 296:F912-F921
46. Kurz A, Rabbani N, Walter M, Bonin M, Thornalley PJ, Auburger G, Gispert S (2010) Alpha-synuclein deficiency leads to increased glyoxalase I expression and glycation stress. Cell Mol Life Sci (in press)
47. Langer T, Levy RI, Strober W (1972) Metabolism of low-density lipoprotein in familial type-H hyperlipoproteinemia. J Clin Invest 51:1528-1536
48. Lyles GA, Chalmers J (1992) The metabolism of aminoacetone to methylglyoxal by semicarbazide-sensitive amino oxidase in human umbilical artery. Biochem Pharmacol 43:1409-1414
49. Maillard LC (1912) Action des acides amines sur les sucres: formation des melanoidines par voie methodique. Compt Rend Acad Sci 154:66-68
50. Miyazawa N, Abe M, Souma T, Tanemoto M, Abe T, Nakayama M, Ito S (2010) Methylglyoxal augments intracellular oxidative stress in human aortic endothelial cells. Free Radic Res 44:101-107
51. Morcos M, Du X, Pfisterer F, Hutter H, Sayed AAR, Thornalley P, Ahmed N, Baynes J, Thorpe S, Kukudov G, Schlotterer A, Bozorgmehr F, El Baki RA, Stern D, Moehrlen F, Ibrahim Y, Oikonomou D, Hamann A, Becker C, Zeier M, Schwenger V, Miftari N, Humpert P, Hammes HP, Buechler M, Bierhaus A, Brownlee M, Nawroth PP (2008) Glyoxalase-1 prevents mitochondrial protein modification and enhances lifespan in Caenorhabditis elegans. Aging Cell 7:260-269 (Pubitemid 351359658)
52. Myint T, Hoshi S, Ookawara T, Miyazawa N, Keiichiro M, Suzuki K, Taniguchi N (1995) Immunological detection of glycated proteins in normal and streptozotocin-induced diabetic rats using anti hexitol-lysine IgG. Biochim Biophys Acta 1272:73-79
53. Nicolay JP, Schneider J, Niemoeller OM, Artunc F, Portero-Otin M, Haik G, Thornalley PJ, Schleicher E, Wieder T, Lang F (2006) Stimulation of suicidal erythrocyte death by methylglyoxal. Cell Physiol Biochem 18:223-232 (Pubitemid 44946977)
54. Pedchenko VK, Chetyrkin SV, Chuang P, Ham AJ, Saleem MA, Mathieson PW, Hudson BG, Voziyan PA (2005) Mechanism of perturbation of integrin-mediated cell-matrix interactions by reactive carbonyl compounds and its implication for pathogenesis of diabetic nephropathy. Diabetes 54:2952-2960 (Pubitemid 41401092)
55. Peters T (1996) All about albumin. Academic Press, New York
56. Phillips SA, Thornalley PJ (1993) The formation of methylglyoxal from triose phosphates. Investigation using a specific assay for methylglyoxal. Eur J Biochem 212:101-105 (Pubitemid 23064605)
57. Phillips SA, Mirrlees D, Thornalley PJ (1993) Modification of the glyoxalase system in streptozotocin-induced diabetic rats: effect of the aldose reductase inhibitor Statil. Biochem Pharmacol 46:805-811 (Pubitemid 23272760)
58. Pratt JM, Petty J, Riba-Garcia I, Robertson DHL, Gaskell SJ, Oliver SG, Beynon RJ (2002) Dynamics of protein turnover, a missing dimension in proteomics. Mol Cell Proteom 1:579-591
59. Queisser MA, Yao D, Geisler S, Hammes HP, Lochnit G, Schleicher ED, Brownlee M, Preissner KT (2010a) Hyperglycemia impairs proteasome function by methylglyoxal. Diabetes 59:670-678
60. Queisser MA, Yao DC, Geisler S, Hammes HP, Lochnit G, Schleicher ED, Brownlee M, Preissner KT (2010b) Hyperglycemia impairs proteasome function by methylglyoxal. Diabetes 59:670-678
61. Rabbani N, Thornalley PJ (2008a) Dicarbonyls linked to damage in the powerhouse: glycation of mitochondrial proteins and oxidative stress. Biochem Soc Trans 036:1045-1050
62. Rabbani N, Thornalley PJ (2008b) The dicarbonyl proteome: proteins susceptible to dicarbonyl glycation at functional sites in health, aging, and disease. Ann N Y Acad Sci 1126:124-127 (Pubitemid 351589305)
63. Rabbani N, Sebekova K, Sebekova K Jr, Heidland A, Thornalley PJ (2007) Protein glycation, oxidation and nitration free adduct accumulation after bilateral nephrectomy and ureteral ligation. Kidney Int 72:1113-1121
64. Rabbani N, Chittari MV, Zehnder D, Ceriello A, Thornalley PJ (2009) High dose metformin therapy reduces glycation and oxidative damage to apolipoprotein B100 and may decelerate atherosclerosis in patients with type 2 diabetes. Diabetologia 52:1293
65. Rabbani N, Varma Chittari M, Bodmer CW, Zehnder D, Ceriello A, Thornalley PJ (2010) Increased glycation and oxidative damage to apolipoprotein B100 of LDL in patients with type 2 diabetes and effect of metformin. Diabetes 59:1038-1045
66. Reichard GA, Skutches CL, Hoeldtke RD, Owen OE (1986) Acetone metabolism in humans during diabetic ketoacidosis. Diabetes 35:668-674 (Pubitemid 16088344)
67. Rosca MG, Mustata TG, Kinter MT, Ozdemir AM, Kern TS, Szweda LI, Brownlee M, Monnier VM, Weiss MF (2005) Glycation of mitochondrial proteins from diabetic rat kidney is associated with excess superoxide formation. Am J Physiol Renal Physiol 289:F420-F430 (Pubitemid 41003672)
68. Ruoslahti E (1996) RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol 12:697-715 (Pubitemid 26422728)
69. Santarius T, Bignell GR, Greenan CD, Widaa S, Chen L, Mahoney CL, Butler A, Edkins S, Waris S, Thornalley PJ, Futreal PA, Stratton MR (2010) GLO1 - a novel amplified gene in human cancer. Genes Chromosom Cancer 49:711-725
70. Shinohara M, Thornalley PJ, Giardino I, Beisswenger PJ, Thorpe SR, Onorato J, Brownlee M (1998) Overexpression of glyoxalase I in bovine endothelial cells inhibits intracellular advanced glycation endproduct formation and prevents hyperglycaemia-induced increases in macromolecular endocytosis. J Clin Invest 101: 1142-1147 (Pubitemid 28125293)
71. Stevens VJ, Monnier VM, Cerami A (1980) Hemoglobin glycosylation as a model for modification of other proteins. Texas Rep Biol Med 40:387-396 (Pubitemid 12214031)
72. Stupack DG, Cheresh DA (2002) Get a ligand, get a life: integrins, signaling and cell survival. J Cell Sci 115:3729-3738 (Pubitemid 35203599)
73. Tajika T, Bando I, Furuta T, Moriya N, Koshino H, Uramoto M (1997) Novel amino acid metabolite produced by Streptomyces sp.: taxonomy, isolation and structural elucidation. Biosci Biotechnol Biochem 61:1007-1010 (Pubitemid 27369483)
74. Thangarajah H, Yao DC, Chang EI, Shi YB, Jazayeri L, Vial IN, Galiano RD, Du XL, Grogan R, Galvez MG, Januszyk M, Brownlee M, Gurtner GC (2009) The molecular basis for impaired hypoxia-induced VEGF expression in diabetic tissues. Proc Natl Acad Sci USA 106:13505-13510
75. Thornalley PJ (1988) Modification of the glyoxalase system in human red blood cells by glucose in vitro. Biochem J 254:751-755
76. Thornalley PJ (1993) The glyoxalase system in health and disease. Mol Aspects Med 14:287-371
77. Thornalley PJ (1998) Glutathione-dependent detoxification of a-oxoaldehydes by the glyoxalase system: involvement in disease mechanisms and antiproliferative activity of glyoxalase I inhibitors. Chem Biol Interact 111-112:137-151 (Pubitemid 28271940)
78. Thornalley PJ (2003a) Glyoxalase I - structure, function and a critical role in the enzymatic defence against glycation. Biochem Soc Trans 31:1343-1348 (Pubitemid 38030973)
79. Thornalley PJ (2003b) The enzymatic defence against glycation in health, disease and therapeutics: a symposium to examine the concept. Biochem Soc Trans 31:1343-1348
80. Thornalley PJ (2005) Dicarbonyl intermediates in the Maillard reaction. Ann N Y Acad Sci 1043:111-117 (Pubitemid 41123896)
81. Thornalley PJ (2008) Protein and nucleotide damage by methylglyoxal in physiological systems - role in ageing and disease. Drug Metab Drug Interact 23:125-150 (Pubitemid 351669568)
82. Thornalley PJ, Strath M, Wilson RJM (1994) Anti-malarial activity in vitro of the glyoxalase I inhibitor diester, S-p-bromobenzylglutathione diethyl ester. Biochem Pharmacol 268:14189-14825
83. Thornalley PJ, Edwards LG, Kang Y, Wyatt C, Davies N, Ladan MJ, Double J (1996) Antitumour activity of S-p-bromobenzylglutathione cyclopentyl diester in vitro and in vivo. Inhibition of glyoxalase I and induction of apoptosis. Biochem Pharmacol 51:1365-1372 (Pubitemid 26142860)
84. Thornalley PJ, Langborg A, Minhas HS (1999) Formation of glyoxal, methylglyoxal and 3-deoxyglucosone in the glycation of proteins by glucose. Biochem J 344:109-116
85. Thornalley PJ, Battah S, Ahmed N, Karachalias N, Agalou S, Babaei- Jadidi R, Dawnay A (2003) Quantitative screening of advanced glycation endproducts in cellular and extracellular proteins by tandem mass spectrometry. Biochem J 375:581-592 (Pubitemid 37433506)
86. Tsikas D, Mitschke A, Suchy MT, Gutzki FM, Stichtenoth DO (2005) Determination of 3-nitrotyrosine in human urine at the basal state by gas chromatography-tandem mass spectrometry and evaluation of the excretion after oral intake. J Chromatogr B 827:146-156 (Pubitemid 41551608)
87. Vander Jagt DL, Robinson B, Taylor KK, Hunsaker LA (1992) Reduction of trioses by NADPH-dependent aldo-keto reductases (aldose reductase, methylglyoxal, and diabetic complications). J Biol Chem 267:4364-4369
88. Venkatraman J, Aggarwal K, Balaram P (2001) Helical peptide models for protein glycation: proximity effects in catalysis of the Amadori rearrangement. Chem Biol 8:611-625 (Pubitemid 32632529)
89. Wendler A, Irsch T, Rabbani N, Thornalley PJ, Krauth-Siegel RL (2009) Glyoxalase II does not support methylglyoxal detoxification but serves as a general trypanothione thioesterase in African trypanosomes. Mol Biochem Parasitol 163:19-27
90. Xiong JP, Stehle T, Zhang RG, Joachimiak A, Frech M, Goodman SL, Aranout MA (2002) Crystal structure of the extracellular segment of integrin alpha V beta 3 in complex with an Arg-Gly- Asp ligand. Science 296:151-155 (Pubitemid 34280076)
91. Yao D, Brownlee M (2009) Hyperglycemia-induced reactive oxygen species increase expression of RAGE and RAGE ligands. Diabetes 59:249-255
92. Yao DC, Brownlee M (2010) Hyperglycemia-induced reactive oxygen species increase expression of the receptor for advanced glycation end products (RAGE) and RAGE ligands. Diabetes 59:249-255
93. Yao D, Taguchi T, Matsumura T, Pestell R, Edelstein D, Giardino I, Suske G, Rabbani N, Thornalley PJ, Sarthy VP, Hammes HP, Brownlee M (2007) High glucose increases angiopoietin-2 transcription in microvascular endothelial cells through methylglyoxal modification of mSin3A. J Biol Chem 282:31038-31045 (Pubitemid 350035169)