Protein damage in diabetes and uremiaidentifying hotspots of proteome damage where minimal modification is amplified to marked pathophysiological effect

Free Radical Research

Volumn 45, Issue 1, 2011, Pages 89-100

  Thornalley, Paul J ^a   Rabbani, Naila ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

3 nitrotyrosine; Glycation; nitrosylation; oxidative stress; proteomics; systems biology

Indexed keywords

GELATINASE A; LOW DENSITY LIPOPROTEIN; PROTEOME;

ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; DIABETES MELLITUS; DISEASE COURSE; ENDOTHELIUM CELL; HUMAN; MASS FRAGMENTOGRAPHY; MATHEMATICAL MODEL; METABOLIC REGULATION; NITRATION; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN DEFECT; PROTEIN DOMAIN; PROTEIN GLYCOSYLATION; PROTEIN METABOLISM; PROTEIN MODIFICATION; REVIEW; STEADY STATE; UREMIA;

DIABETES MELLITUS; GLYCOSYLATION; HUMANS; NITRIC OXIDE; OXIDATIVE STRESS; PROTEOME; UREMIA;

EID: 78650117871     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2010.534162     Document Type: Review

References (105)

1. Ahmed N, Thornalley PJ. Advanced glycation endproducts: what is their relevance to diabetic complications? Diabetes Obes Metab 2007;9:233-245. (Pubitemid 46502041)
2. Thornalley PJ, Rabbani N. Highlights and hotspots of protein glycation in end-stage renal disease. Semin Dialysis 2009;22:400-404.
3. Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature 2000;408:239-247.
4. Ischiropoulos H. Protein tyrosine nitration-An update. Arch Biochem Biophys 2009;484:117-121.
5. Foster MW, Forrester MT, Stamler JS. A protein microarray-based analysis of S-nitrosylation. Proc Natl Acad Sci USA 2009;106:18948-18953.
6. Nishikawa T, Edelstein D, Liang Du X, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beede D, Oates PJ, Hammes H-P, Giardino I, Brownlee M. Normalizing mito-chondrial superoxide production blocks three pathways of hyperglycaemia damage. Nature 2000;404:787-790. (Pubitemid 30212409)
7. Karachalias N, Babaei-Jadidi R, Rabbani N, Thornalley P. Increased protein damage in renal glomeruli, retina, nerve, plasma and urine and its prevention by thiamine and ben-fotiamine therapy in a rat model of diabetes. Diabetologia 2010;53:1506-1516.
8. Rabbani N, Sebekova, Sebekova K, Jr, Heidland A, Thornalley PJ. Protein glycation, oxidation and nitration free adduct accumulation after bilateral nephrectomy and ureteral ligation. Kid Int 2007;72:1113-1121.
9. Ahmed N, Babaei-Jadidi R, Howell SK, Beisswenger PJ, Thornalley PJ. Degradation products of proteins damaged by glycation, oxidation and nitration in clinical type 1 diabetes. Diabetologia 2005;48:1590-1603. (Pubitemid 41175513)
10. Agalou S, Ahmed N, Babaei-Jadidi R, Dawnay A, Thornalley PJ. Profound mishandling of protein glycation degradation products in uremia and dialysis. J Am Soc Nephrol 2005; 16:1471-1485. (Pubitemid 41716533)
11. Duran-Jimenez B, Dobler D, Moffat S, Rabbani N, Streuli CH, Thornalley PJ, Tomlinson D, Gardiner NJ. Advanced glycation endproducts in extracellular matrix proteins contribute to the failure of sensory nerve regeneration in diabetes. Diabetes 2009;58:2893-2903.
12. Thornalley PJ, Battah S, Ahmed N, Karachalias N, Agalou S, Babaei-Jadidi R, Dawnay A. Quantitative screening of advanced glycation endproducts in cellular and extracellular proteins by tandem mass spectrometry. Biochem J 2003; 375:581-592. (Pubitemid 37433506)
13. e -carboxymethyllysine: a new Maillard reaction product, in rat urine. J Agric Food Chem 1987;35: 427-431.
14. Koschinsky T, He C-J, Mitsuhashi T, Bucala R, Liu C, Buenting C, Heitman K, Vlassara H. Orally absorbed reactive glycation products (glycotoxins): an environmental risk factor in diabetic nephropathy. Proc Natl Acad Sci USA 1997;94:6474-6479. (Pubitemid 27270709)
15. Ahmed N, Thornalley PJ, Luthen R, Haussinger D, Sebekova K, Schinzel R, Voelker W, Heidland A. Processing of protein glycation, oxidation and nitrosation adducts in the liver and the effect of cirrhosis. J Hepatol 2004;41: 913-919. (Pubitemid 39575657)
16. Pannala AS, Mani AR, Rice-Evans CA, Moore KP. pH-dependent nitration of para-hydroxyphenylacetic acid in the stomach. Free Radic Biol Med 2006;41:896-901. (Pubitemid 44247542)
17. Thornalley PJ, Waris S, Fleming T, Santarius T, Larkin SJ, Winklhofer-Roob BM, Stratton MR, Rabbani N. Imidazopuri-nones are markers of physiological genomic damage linked to DNA instability and glyoxalase 1-associated tumour multidrug resistance. Nucl Acids Res 2010; Volume 38: 5432-5442.
18. Kilhovd BK, Juutilainen A, Lehto S, Ronnemaa T, Torjesen PA, Hanssen KF, Laakso M. Increased serum levels of methylglyoxal-derived hydroimidazolone-AGE are associated with increased cardiovascular disease mortality in nondia-betic women. Atherosclerosis 2009;205:590-594.
19. Rabbani N, Varma Chittari M, Bodmer CW, Zehnder D, Ceriello A, Thornalley PJ. Increased glycation and oxidative damage to apolipoprotein B100 of LDL in patients with type 2 diabetes and effect of metformin. Diabetes 2010;59: 1038-1045.
20. Ahmed N, Ahmed U, Thornalley PJ, Hager K, Fleischer GA, Munch G. Protein glycation, oxidation and nitration marker residues and free adducts of cerebrospinal fluid in Alzheimer's disease and link to cognitive impairment. J Neuro-chem 2004;92:255-263. (Pubitemid 40194017)
21. Kurz A, Rabbani N, Walter M, Bonin M, Thornalley PJ, Auburger G, Gispert S. Alpha-synuclein deficiency leads to increased glyoxalase I expression and glycation stress. Cell Mol Life Sci 2010; in press.
22. Xue M, AntonySunil A, Rabbani N, Thornalley PJ. Protein damage by glycation, oxidation and nitration in the ageing process. Advances in quantitation of protein damage and the emerging importance of decline in enzymatic defences as the ageing phenotype develops. In: Foyer CH, Faraghar R, Thornalley PJ, editors. Redox metabolism and longevity relationships in animals and plants. London: Garland Science; 2008. p 227-265.
23. Hambsch B, Chen BG, Brenndorfer J, Meyer M, Avrabos C, Maccarrone G, Liu RH, Eder M, Turck CW, Landgraf R. Methylglyoxal-mediated anxiolysis involves increased protein modification and elevated expression of glyoxalase 1 in the brain. J Neurochem 2010;113:1240-1251.
24. Arai M, Yuzawa H, Nohara I, Ohnishi T, Obata N, Iwayama Y, Haga S, Toyota T, Ujike H, Arai M, Ichikawa T, Nishida A, Tanaka Y, Furukawa A, Aikawa Y, Kuroda O, Niizato K, Izawa R, Nakamura K, Mori N, Matsuzawa D, Hashimoto K, Iyo M, Sora I, Matsushita M, Okazaki Y, Yoshikawa T, Miyata T, Itokawa M. Enhanced carbonyl stress in a sub-population of schizophrenia. Arch Gen Psychiatry 2010; 67:589-597.
25. Delpierre G, Rider MH, Collard F, Stroobant V, Vanstapel F, Santos H, Van Schaftingen E. Identification, cloning, and heterologous expression of a mammalian fructosamine-3-kinase. Diabetes 2000;49:1627-1634.
26. Leonard SE, Reddie KG, Carroll KS. Mining the thiol proteome for sulfenic acid modifications reveals new targets for oxidation in cells. ACS Chem Biol 2009;4:783-799.
27. Woo HA, Jeong W, Chang TS, Park KJ, Park SJ, Yang JS, Rhee SG. Reduction of cysteine sulfi nic acid by sulfi redoxin is specific to 2-cys peroxiredoxins. J Biol Chem 2005;280: 3125-3128. (Pubitemid 40223772)
28. Weissbach H, Resnick L, Brot N. Methionine sulfoxide reductases: history and cellular role in protecting against oxidative damage. Biochim Biophys Acta 2005;1703: 203-212. (Pubitemid 40170443)
29. Pabarcus MK, Casida JE. Cloning, expression, and catalytic triad of recombinant arylformamidase. Prot ExpR Purif 2005;44:39-44. (Pubitemid 41405933)
30. Smallwood HS, Lourette NM, Boschek CB, Bigelow DJ, Smith RD, Pasa-Tolic L, Squier TC. Identification of a denitrase activity against calmodulin in activated macro-phages using high-field liquid chromatography-FTICR mass spectrometry. Biochemistry 2007;46:10498-10505. (Pubitemid 47417245)
31. Ohshima H, Friesen M, Brouet I, Bartsch H. Nitrotyrosine as a new marker for endogenous nitrosation and nitration of proteins. Food Chem Toxicol 1990;28:647-652.
32. Grune T, Reinheckel T, Davies KJA. Degradation of oxidized proteins in K562 human hematopoietic cells by pro-teasome. J Biol Chem 1996;271:15504-15509. (Pubitemid 26225322)
33. Hernebring M, Brolen G, Aguilaniu H, Semb H, Nystrom T. Elimination of damaged proteins during differentiation of embryonic stem cells. Proc Natl Acad Sci USA 2006;103: 7700-7705.
34. Dudek EJ, Shang F, Liu Q, Valverde P, Hobbs M, Taylor A. Selectivity of the ubiquitin pathway for oxidatively modified proteins: relevance to protein precipitation diseases. Faseb J 2005;19:1707-1709. (Pubitemid 41429537)
35. Goldberg AL, Akopian TN, Kisselev AF, Lee DH. Protein degradation by the proteasome and dissection of its in vivo importance with synthetic inhibitors. Mol Biol Rep 1997; 24:69-75. (Pubitemid 27269429)
36. Franch HA, Sooparb S, Du J. A mechanism regulating pro-teolysis of specific proteins during renal tubular cell growth. J Biol Chem 2001;276:19126-19131.
37. Sooparb S, Price SR, Shaoguang J, Franch HA. Suppression of chaperone-mediated autophagy in the renal cortex during acute diabetes mellitus. Kid Int 2004;65:2135-2144. (Pubitemid 38669999)
38. Bassi AM, Ledda S, De Pascale MC, Penco S, Rossi S, Odetti P, Cottalasso D. Antioxidant status in J774A.1 mac-rophage cell line during chronic exposure to glycated serum. Biochem Cell Biol Biochim Biol Cell 2005;83:176-187. (Pubitemid 41113544)
39. Whittier JE, Xiong Y, Rechsteiner MC, Squier TC. Hsp90 enhances degradation of oxidized calmodulin by the 20 S proteasome. J Biol Chem 2004;279:46135-46142. (Pubitemid 39491608)
40. Bulteau A-L, Verbeke P, Petropoulos I, Chaffotte A-F, Friguet B. Proteasome inhibition in glyoxal-treated fibrob-lasts and resistance of glycated glucose-6-phosphate dehy-drogenase to 20 S proteasome degradation in vitro . J Biol Chem 2001;276:45662-45668.
41. Tatsuta T, Langer T. Quality control of mitochondria: protection against neurodegeneration and ageing. Embo Journal 2008;27:306-314. (Pubitemid 351161660)
42. Matsumoto K, Sano K, Nagai R, Suzuki H, Kodama T, Yoshida M, Ueda S, Smedsrod B, Horiuchi S. Endocytic uptake of advanced glycation end products by mouse liver sinusoidal endothelial cells is mediated by a scavenger receptor distinct from the macrophage scavenger receptor class A. Biochem J 2000;352:233-240.
43. Westwood ME, Thornalley PJ. Molecular characteristics of methylglyoxal-modified bovine and human serum albumins. Comparison with glucose-derived advanced glycation endproduct-modified serum albumins. J Prot Chem 1995;14:359-372.
44. Johnson RN, Easdale RW, Tatnell M, Baker JR. Significance of variation in turnover of glycated albumin on indexes of diabetic control. Clin Chim Acta 1991;198:229-238.
45. Ahmed N, Thornalley PJ. Chromatographic assay of glyca-tion adducts in human serum albumin glycated in vitro by derivatisation with aminoquinolyl-N-hydroxysuccimidyl-carbamate and intrinsic fluorescence. Biochem J 2002;364: 15-24. (Pubitemid 34538941)
46. Nagai R, Mera K, Fujiwara Y, Nagai M, Otagiri M. Comparison of pharmacokinetics between highly and mildly modified AGE proteins in mice. Ann N Y Acad Sci 2008; 1126:325-327. (Pubitemid 351589265)
47. Dobler D, Ahmed N, Song LJ, Eboigbodin KE, Thornalley PJ. Increased dicarbonyl metabolism in endothelial cells in hyperglycemia induces anoikis and impairs angiogenesis by RGD and GFOGER motif modification. Diabetes 2006;55:1961-1969. (Pubitemid 44509968)
48. Doherty MK, Hammond DE, Clagule MJ, Gaskell SJ, Beynon RJ. Turnover of the Human Proteome: determination of protein intracellular stability by Dynamic SILAC. J Proteome Res 2009;8:104-112.
49. Alderson NL, Wang Y, Blatnik M, Frizzell N, Walla MD, Lyons TJ, Alt N, Carson JA, Nagai R, Thorpe SR, Baynes J W. S-(2-Succinyl)cysteine: a novel chemical modification of tissue proteins by a Krebs cycle intermediate. Arch Biochem Biophys 2006;450:1-8. (Pubitemid 43782733)
50. Gaut JP, Byun J, Tran HD, Heinecke J W. Artifact-free quan-titation of free 3-chlorotyrosine, 3-bromotyrosine, and 3-nitrotyrosine in human plasma by electron capture-negative chemical ionization gas chromatography mass spectrometry and liquid chromatography-electrospray ionization tandem mass spectrometry. Anal Biochem 2002;300:252-259. (Pubitemid 34093701)
51. Koito W, Araki T, Horiuchi S, Nagai R. Conventional antibody against Ne-(carboxymethyl)lysine (CML) shows cross-reaction to Ne-(carboxyethyl)lysine (CEL): immuno-chemical Quantification of CML with a specific antibody. J Biochem 2004;136:831-837. (Pubitemid 40364174)
52. Safi nowski M, Wilhelm B, Reimer T, Weise A, Thome N, Hanel H, Forst T, Pfutzner A. Determination of nitrotyro-sine concentrations in plasma samples of diabetes mellitus patients by four different immunoassays leads to contradic-tive results and disqualifiles the majority of the tests. Clin Chem Lab Med 2009;47:483-488.
53. Choudhary C, Mann M. Decoding signalling networks by mass spectrometry-based proteomics. Nat Rev Mol Cell Biol 2010;11:427-439.
54. Rabbani N, Thornalley PJ. Assay of 3-Nitrotyrosine in tissues and body fluids by liquid chromatography with tandem mass spectrometric detection. Meth Enzymol 2008; 440:337-359.
55. Tsikas D. Measurement of nitrotyrosine in plasma by immu-noassays is fraught with danger: commercial availability is no guarantee of analytical reliability. Clin Chem Lab Med 2010;48:141-143.
56. Dickins M, van de Waterbeemd H. Simulation models for drug disposition and drug interactions. Drug Disc Today: BIOSILICO 2004;2:38-45. (Pubitemid 40542943)
57. Kell DB. Metabolomics, modelling and machine learning in systems biology-towards an understanding of the languages of cells. FEBS J 2006;273:873-894.
58. Harman D. Aging: a theory based on free radical and radiation chemistry. J Gerontol 1956;11:298-300.
59. Rabbani N, Thornalley PJ. The dicarbonyl proteome: proteins susceptible to dicarbonyl glycation at functional sites in health, aging, and disease. Ann N Y Acad Sci 2008;1126: 124-127. (Pubitemid 351589305)
60. Yoo YS, Regnier FE. Proteomic analysis of carbonylated proteins in two-dimensional gel electrophoresis using avidin-fluorescein affinity staining. Electrophoresis 2004;25: 1334-1341. (Pubitemid 38801652)
61. Hill BG, Reily C, Oh JY, Johnson MS, Landar A. Methods for the determination and Quantification of the reactive thiol proteome. Free Radic Biol Med 2009;47:675-683.
62. Bigelow DJ, Qian WJ. Quantitative proteome mapping of nitrotyrosines. Meth Enzymol 2008;440:191-205.
63. Sheehan D. Detection of redox-based modification in two-dimensional electrophoresis proteomic separations. Biochem Biophys Res Comm 2006;349:455-462. (Pubitemid 44363063)
64. Venkatraman J, Aggarwal K, Balaram P. Helical peptide models for protein glycation: proximity effects in catalysis of the Amadori rearrangement. Chem Biol 2001;8:611-625. (Pubitemid 32632529)
65. Brandes N, Schmitt S, Jakob U. Thiol-based redox switches in eukaryotic proteins. Antioxid Redox Signal 2009;11: 997-1014.
66. Hess DT, Matsumoto A, Kim SO, HMarshall HE, Stamler JS. Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 2005;6:150-166. (Pubitemid 40215810)
67. Spickett CM, Pitt AR, Morrice N, Kolch W. Proteomic analysis of phosphorylation, oxidation and nitrosylation in signal transduction. Biochim Biophys Acta-Prot Proteom 2006;1764:1823-1841. (Pubitemid 44914060)
68. Souza JM, Peluffo G, Radi R. Protein tyrosine nitration-Functional alteration or just a biomarker? Free Radic Biol Med 2008;45:357-366.
69. Hong F, Freeman ML, Liebler DC. Identification of sensor cysteines in human keap1 modified by the cancer chemo-preventive agent sulforaphane. Chem Res Toxicol 2005;18: 1917-1926. (Pubitemid 43023050)
70. Niture SK, Kaspar JW, Shen J, Jaiswal AK. Nrf2 signaling and cell survival. Toxicol Appl Pharmacol 2010;244: 37-42.
71. Doherty MK, Beynon RJ. Protein turnover on the scale of the proteome. Exp Rev Proteom 2006;3:97-110. (Pubitemid 43979395)
72. Riboulet-Chavey A, Pierron A, Durand I, Murdaca J, Giudicelli J, Van Obberghen E. Methylglyoxal impairs the insulin signaling pathways independently of the formation of intracellular reactive oxygen species. Diabetes 2006;55: 1289-1299. (Pubitemid 44195367)
73. Tatsunami R, Oba T, Takahashi K, Tampo Y. Methylglyoxal causes dysfunction of thioredoxin and thioredoxin reductase in endothelial cells. J Pharmacology Sci 2009;111:426-432.
74. Thornalley PJ, Rabbani N. Dicarbonyls in cola drinks sweetened with sucrose or high fructose corn syrup. In: Thomas MC, Forbes J, editors. Maillard reaction: interface between aging, nutrition and metabolism. London: RSC Publishing; 2010. p. 158-163.
75. Fenaille F, Campos-Gimenez E, Guy PA, Schmitt C, Morgan F. Monitoring of beta-lactoglobulin dry-state glyca-tion using various analytical techniques. Anal Biochem 2003;320:144-148. (Pubitemid 36937077)
76. Gallet X, Charloteaux B, Thomas A, Braseur R. A fast method to predict protein interaction sites from sequences. J Mol Biol 2000;302:917-926.
77. Emsley J, Knight CG, Farndale RW, Barnes MJ, Liddington RC. Structural basis of collagen recognition by integrin alpha 2 beta 1. Cell 2000;101:47-56.
78. Knight CG, Morton LF, Peachey AR, Tuckwell DS, Farndale RW, Barnes MJ. 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 2000;275:35-40. (Pubitemid 30038949)
79. Stupack DG, Cheresh DA. Get a ligand, get a life: integrins, signaling and cell survival. J Cell Sci 2002;115:3729-3738. (Pubitemid 35203599)
80. Ruoslahti E. RGD and other recognition sequences for integrins. Ann Rev Cell Dev Biol 1996;12:697-715. (Pubitemid 26422728)
81. Xiong JP, Stehle T, Zhang RG, Joachimiak A, Frech M, Goodman SL, Aranout MA. Crystal structure of the extracellular segment of integrin alpha V beta 3 in complex with an Arg-Gly-Asp ligand. Science 2002;296:151-155. (Pubitemid 34280076)
82. Gottschalk KE, Kessler H. The structures of integrins and integrin-ligand complexes: implications for drug design and signal transduction. Angew Chem Int Ed 2002;41: 3767-3774. (Pubitemid 35277998)
83. Kim Y, Nakase H, Nagata K, Sakaki T, Maeda M, Yamamoto K. Observation of arterial and venous thrombus formation by scanning and transmission electron microscopy. Acta Neurochir 2004;146:45-51. (Pubitemid 38186206)
84. McClung JA, Naseer N, Saleem M, Rossi GP, Meiss MB, Abraham NG, Kappas A. Circulating endothelial cells are elevated in patients with type 2 diabetes mellitus independently of HbA(1)c. Diabetologia 2005;48:345-350. (Pubitemid 40543308)
85. Koc M, Richards HB, Bihorac A, Ross EA, Schold JD, Segal MS. Circulating endothelial cells are associated with future vascular events in hemodialysis patients. Kid Int 2005;67: 1078-1083. (Pubitemid 41623333)
86. Sarwar N, Gao P, Seshasai SRK, Gobin R, Kaptoge S, Di Angelantonio E, Ingelsson E, Lawlor DA, Selvin E, Stampfer M, Stehouwer CDA, Lewington S, Pennells L, Thompson A, Sattar N, White IR, Ray KK, Danesh J. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet 2010;375:2215-2222.
87. Williams ME. Diabetic CKD/ESRD 2010: a progress report? Semin Dialysis 2010;23:129-133.
88. Rabbani N, Thornalley PJ. Quantitation of markers of protein damage by glycation, oxidation, and nitration in peritoneal dialysis. Perit Dial Int 2009;29:S51-S56.
89. Rosca MG, Mustata TG, Kinter MT, Ozdemir AM, Kern TS, Szweda LI, Brownlee M, Monnier VM, Weiss MF. Glycation of mitochondrial proteins from diabetic rat kidney is associated with excess superoxide formation. AJP-Renal Physio 2005;289:F420-F430. (Pubitemid 41003672)
90. Hurd TR, Prime TA, Harbour ME, Lilley KS, Murphy MP. Detection of reactive oxygen species-sensitive thiol proteins by redox difference gel electrophoresis: implication for mito-chondrial redox. J Biol Chem 2007;282:22040-22051. (Pubitemid 47195755)
91. Turko IV, Li L, Aulak KS, Stuehr DJ, Chang JY, Murad F. Protein tyrosine nitration in the mitochondria from diabetic mouse heart-Implications to dysfunctional mitochondria in diabetes. J Biol Chem 2003;278:33972-33977. (Pubitemid 37553232)
92. Brand MD. The sites and topology of mitochondrial super-oxide production. Exp Gerontol 2010;45:466-472.
93. Schlotterer A, Kukudov G, Bozorgmehr F, Hutter H, Du XL, Oikonomou D, Ibrahim Y, Pfisterer F, Rabbani N, Thornalley P, Sayed A, Fleming T, Humpert P, Schwenger V, Zeier M, Hamann A, Stern D, Brownlee M, Bierhaus A, Nawroth P, Morcos M. C-elegans as model for the study of high glucose-mediated life span reduction. Diabetes 2009;58:2450-2456.
94. Oorni K, Pentikainen MO, Ala-Korpela M, Kovanen P T. Aggregation, fusion, and vesicle formation of modified low density lipoprotein particles: molecular mechanisms and effects on matrix interactions. J Lipid Res 2000;41:1703-1714.
95. Pentikainen MO, Lehtonen EM, Kovanen PT. Aggregation and fusion of modified low density lipoprotein. J Lipid Res 1996;37:2638-2649. (Pubitemid 27051510)
96. MacArthur JM, Bishop JR, Stanford KI, Wang LC, Bensadoun A, Witztum JL, Esko JD. Liver heparan sulfate proteoglycans mediate clearance of triglyceride-rich lipoproteins independently of LDL receptor family members. J Clin Invest 2007;117:153-164. (Pubitemid 46048462)
97. Stanford KI, Bishop JR, Foley EM, Gonzales JC, Niesman IR, Witztum JL, Esko JD. Syndecan-1 is the primary heparan sul-fate proteoglycan mediating hepatic clearance of triglyceride-rich lipoproteins in mice. J Clin Invest 2009;119:3236-3245.
98. Evanko SP, Raines EW, Ross R, Gold LI, Wight TN. Prote-oglycan distribution in lesions of atherosclerosis depends on lesion severity, structural characteristics, and the proximity of platelet-derived growth factor and transforming growth factor-beta. Am J Pathol 1998;152:533-546. (Pubitemid 28106400)
99. Talusan P, Bedri S, Yang S, Kattapuram T, Silva N, Roughley PJ, Stone JR. Analysis of intimal proteoglycans in atherosclerosis-prone and atherosclerosis-resistant human arteries by mass spectrometry. Mol Cell Proteom 2005;4: 1350-1357. (Pubitemid 41460274)
100. Skalen K, Gustafsson M, Rydberg EK, Hulten LM, Wiklund O, Innerarity TL, Boren J. Subendothelial retention of atherogenic lipoproteins in early atherosclerosis. Nature 2002;417:750-754. (Pubitemid 34640629)
101. Xue M, Thornalley PJ, Rabbani N. LDL glycated by meth-ylglyoxal to physiological extent in vitro has increased binding of proteoglycan without impairment of LDL receptor binding. Diabetologia 2008;51:S299.
102. Bailey CJ. Metformin: effects on micro and macrovascular complications in type 2 diabetes. Cardiovasc Drug Ther 2008;22:215-224.
103. Baynes JW, Thorpe SR, Murtiashaw MH. Nonenzymatic glucosylation of lysine residues in albumin. Meth Enzymol 1984;106:88-98. (Pubitemid 14079122)
104. Thornalley PJ. Dicarbonyl intermediates in the Maillard reaction. Ann N Y Acad Sci 2005;1043:111-117. (Pubitemid 41123896)
105. Ahmed N, Dobler D, Dean M, Thornalley PJ. Peptide mapping identifiles hotspot site of modification in human serum albumin by methylglyoxal involved in ligand binding and esterase activity. J Biol Chem 2005;280:5724-5732. (Pubitemid 40280052)