Advanced Glycation End Products and Oxidative Stress in Type 2 Diabetes Mellitus
Abstract
:1. Introduction
2. AGEs in Diabetes: An Overview
3. Advanced Glycation End Products and Insulin Resistance
4. The Role of AGEs in β Cell Dysfunction and β Cell Death
5. The Role of AGEs in Diabetic Complications
5.1. Modified ECM Proteins and the Relevance for Diabetic Complications
5.2. Ischemic Heart Disease and Atherosclerosis
5.3. Diabetic Retinopathy
5.4. Diabetic Nephropathy
6. Conclusions
Abbreviations
AGEs | Advanced glycation end products |
AGER1 | Advanced glycation end product receptor 1 |
ATP | Adenosine triphosphate |
BSA | Bovine serum albumin |
CEL | Nε-(carboxyethyl) lysine |
CMA | Nω-(carboxymethyl) arginine |
CML | Nε-(carboxymethyl) lysine |
CTGF | Connective tissue growth factor |
ELISA | Enzyme-linked immunosorbent assay |
ECM | Extracellular matrix |
FoxO1 | Forkhead box protein O1 |
GOLD | Glyoxal-derived lysyl dimer |
GSH | Glutathione |
GSSG | Glutathione disulfide |
H2O2 | Hydrogen peroxide |
HPLC | High performance liquid chromatography |
iNOS | Inducible nitric oxide synthase |
IRS | Insulin receptor substrate |
MCP-1 | Monocyte chemoattractant peptide 1 |
MOLD | Methylglyoxal-derived lysyl dimer |
NAD+ | Oxidized nicotinamide adenine dinucleotide |
NADH | Reduced nicotinamide adenine dinucleotide |
NADPH | Reduced nicotinamide adenine dinucleotide phosphate |
NFκB | Nuclear factor kappa B |
•NO | Nitric oxide |
O2•− | Superoxide anion |
PDX-1 | Pancreatic and duodenal homeobox-1 |
PKC α | Protein kinase c alpha |
RAGE | Receptor of advanced glycation end products |
ROS | Reactive oxygen species |
SIRT1 | Sirtuin1 |
T1DM | Type 1 diabetes mellitus |
T2DM | Type 2 diabetes mellitus |
TCA | Tricarboxylic acid cycle |
TNFα | Tumor necrosis factor alpha |
UPLC-MS | Ultra pressure liquid chromatography with mass spectrometry detection |
VEGF | Vascular endothelial growth factor |
Conflicts of Interest
References
- International Diabetes Federation. IDF Diabetes Atlas Update Poster, 6th ed.; International Diabetes Federation: Brussels, Belgium, 2014. [Google Scholar]
- International Diabetes Federation. IDF Diabetes Atlas, 6th ed.; International Diabetes Federation: Brussels, Belgium, 2013. [Google Scholar]
- Morrish, N.; Wang, S.-L.; Stevens, L.; Fuller, J.; Keen, H. Mortality and causes of death in the who multinational study of vascular disease in diabetes. Diabetologia 2001, 44, S14–S21. [Google Scholar] [CrossRef] [PubMed]
- Sies, H. Oxidative stress: A concept in redox biology and medicine. Redox Biol. 2015, 4, 180–183. [Google Scholar] [CrossRef]
- Jung, T.; Catalgol, B.; Grune, T. The proteasomal system. Mol. Asp. Med. 2009, 30, 191–296. [Google Scholar] [CrossRef]
- Giacco, F.; Brownlee, M. Oxidative stress and diabetic complications. Circ. Res. 2010, 107, 1058–1070. [Google Scholar] [CrossRef] [PubMed]
- Abdul-Ghani, M.A.; DeFronzo, R.A. Oxidative stress in type 2 diabetes mellitus. In Oxidative stress in aging; Miwa, S., Beckman, K., Muller, F., Eds.; Humana Press: Totowa, NJ, USA, 2008; pp. 191–211. [Google Scholar]
- Henriksen, E.J.; Diamond-Stanic, M.K.; Marchionne, E.M. Oxidative stress and the etiology of insulin resistance and type 2 diabetes. Free Radic. Biol. Med. 2011, 51, 993–999. [Google Scholar] [CrossRef] [PubMed]
- Leahy, J.L. Pathogenesis of type 2 diabetes mellitus. Arch. Med. Res. 2005, 36, 197–209. [Google Scholar] [CrossRef] [PubMed]
- Vlassara, H.; Uribarri, J. Advanced glycation end products (AGE) and diabetes: Cause, effect, or both? Curr. Diab. Rep. 2014. [Google Scholar] [CrossRef]
- Rahbar, S. An abnormal hemoglobin in red cells of diabetics. Clin. Chim. Acta 1968, 22, 296–298. [Google Scholar] [CrossRef] [PubMed]
- Bunn, H.F.; Haney, D.N.; Gabbay, K.H.; Gallop, P.M. Further identification of the nature and linkage of the carbohydrate in hemoglobin A1c. Biochem. Biophys. Res. Commun. 1975, 67, 103–109. [Google Scholar] [CrossRef] [PubMed]
- Hodge, J.E. Dehydrated foods—Chemistry of browning reactions in model systems. J. Agric. Food Chem. 1953, 1, 928–943. [Google Scholar] [CrossRef]
- Fu, M.X.; Requena, J.R.; Jenkins, A.J.; Lyons, T.J.; Baynes, J.W.; Thorpe, S.R. The advanced glycation end product, nepsilon-(carboxymethyl)lysine, is a product of both lipid peroxidation and glycoxidation reactions. J. Biol. Chem. 1996, 271, 9982–9986. [Google Scholar] [CrossRef] [PubMed]
- Thornalley, P.J.; Langborg, A.; Minhas, H.S. Formation of glyoxal, methylglyoxal and 3-deoxyglucosone in the glycation of proteins by glucose. Biochem. J. 1999, 344, 109–116. [Google Scholar] [CrossRef] [PubMed]
- Wells-Knecht, K.J.; Zyzak, D.V.; Litchfield, J.E.; Thorpe, S.R.; Baynes, J.W. Mechanism of autoxidative glycosylation: Identification of glyoxal and arabinose as intermediates in the autoxidative modification of proteins by glucose. Biochemistry 1995, 34, 3702–3709. [Google Scholar] [CrossRef] [PubMed]
- Scheijen, J.L.; Schalkwijk, C.G. Quantification of glyoxal, methylglyoxal and 3-deoxyglucosone in blood and plasma by ultra performance liquid chromatography tandem mass spectrometry: Evaluation of blood specimen. Clin. Chem. Lab. Med. 2014, 52, 85–91. [Google Scholar] [CrossRef] [PubMed]
- Al-Abed, Y.; Bucala, R. Nε-carboxymethyllysine formation by direct addition of glyoxal to lysine during the maillard reaction. Bioorg. Med. Chem. Lett. 1995, 5, 2161–2162. [Google Scholar] [CrossRef]
- Wells-Knecht, K.J.; Brinkmann, E.; Baynes, J.W. Characterization of an imidazolium salt formed from glyoxal and N.alpha.-hippuryllysine: A model for maillard reaction crosslinks in proteins. J. Org. Chem. 1995, 60, 6246–6247. [Google Scholar] [CrossRef]
- Glomb, M.A.; Lang, G. Isolation and characterization of glyoxal-arginine modifications. J. Agric. Food Chem. 2001, 49, 1493–1501. [Google Scholar] [CrossRef] [PubMed]
- Thorpe, S.R.; Baynes, J.W. Maillard reaction products in tissue proteins: New products and new perspectives. Amino Acids 2003, 25, 275–281. [Google Scholar] [CrossRef] [PubMed]
- Ahmed, M.U.; Brinkmann Frye, E.; Degenhardt, T.P.; Thorpe, S.R.; Baynes, J.W. N-epsilon-(carboxyethyl)lysine, a product of the chemical modification of proteins by methylglyoxal, increases with AGE in human lens proteins. Biochem. J. 1997, 324, 565–570. [Google Scholar] [PubMed]
- Nagaraj, R.H.; Shipanova, I.N.; Faust, F.M. Protein cross-linking by the maillard reaction: Isolation, characterization, and in vivo detection of a lysine-lysine cross-link derived from methylglyoxal. J. Biol. Chem. 1996, 271, 19338–19345. [Google Scholar] [CrossRef] [PubMed]
- Shipanova, I.N.; Glomb, M.A.; Nagaraj, R.H. Protein modification by methylglyoxal: Chemical nature and synthetic mechanism of a major fluorescent adduct. Arch. Biochem. Biophys. 1997, 344, 29–36. [Google Scholar] [CrossRef] [PubMed]
- Henle, T.; Walter, A.; Haeßner, R.; Klostermeyer, H. Detection and identification of a protein-bound imidazolone resulting from the reaction of arginine residues and methylglyoxal. Z. Lebensm. Unters. Forsch. 1994, 199, 55–58. [Google Scholar] [CrossRef]
- Portero-Otin, M.; Nagaraj, R.H.; Monnier, V.M. Chromatographic evidence for pyrraline formation during protein glycation in vitro and in vivo. Biochim. Biophys. Acta 1995, 1247, 74–80. [Google Scholar] [CrossRef] [PubMed]
- Dyer, D.; Blackledge, J.; Thorpe, S.; Baynes, J. Formation of pentosidine during nonenzymatic browning of proteins by glucose. Identification of glucose and other carbohydrates as possible precursors of pentosidine in vivo. J. Biol. Chem. 1991, 266, 11654–11660. [Google Scholar] [PubMed]
- Jono, T.; Nagai, R.; Lin, X.; Ahmed, N.; Thornalley, P.J.; Takeya, M.; Horiuchi, S. Nε-(carboxymethyl) lysine and 3-DG-imidazolone are major AGE structures in protein modification by 3-deoxyglucosone. J. Biochem. 2004, 136, 351–358. [Google Scholar] [CrossRef] [PubMed]
- Singh, R.; Barden, A.; Mori, T.; Beilin, L. Advanced glycation end-products: A review. Diabetologia 2001, 44, 129–146. [Google Scholar] [CrossRef] [PubMed]
- Baynes, J.W. Role of oxidative stress in development of complications in diabetes. Diabetes 1991, 40, 405–412. [Google Scholar] [CrossRef] [PubMed]
- Nakamura, K.; Nakazawa, Y.; Ienaga, K. Acid-stable fluorescent advanced glycation end products: Vesperlysines A, B, and C are formed as crosslinked products in the maillard reaction between lysine or proteins with glucose. Biochem. Biophys. Res. Commun. 1997, 232, 227–230. [Google Scholar] [CrossRef] [PubMed]
- Pongor, S.; Ulrich, P.C.; Bencsath, F.A.; Cerami, A. Aging of proteins: Isolation and identification of a fluorescent chromophore from the reaction of polypeptides with glucose. Proc. Natl. Acad. Sci. USA 1984, 81, 2684–2688. [Google Scholar] [CrossRef] [PubMed]
- Sell, D.R.; Monnier, V.M. Structure elucidation of a senescence cross-link from human extracellular matrix. Implication of pentoses in the aging process. J. Biol. Chem. 1989, 264, 21597–21602. [Google Scholar] [PubMed]
- Poulsen, M.W.; Hedegaard, R.V.; Andersen, J.M.; de Courten, B.; Bügel, S.; Nielsen, J.; Skibsted, L.H.; Dragsted, L.O. Advanced glycation endproducts in food and their effects on health. Food Chem. Toxicol. 2013, 60, 10–37. [Google Scholar] [CrossRef] [PubMed]
- Kilhovd, B.K.; Berg, T.J.; Birkeland, K.I.; Thorsby, P.; Hanssen, K.F. Serum levels of advanced glycation end products are increased in patients with type 2 diabetes and coronary heart disease. Diabetes Care 1999, 22, 1543–1548. [Google Scholar] [CrossRef] [PubMed]
- Schleicher, E.D.; Wagner, E.; Nerlich, A.G. Increased accumulation of the glycoxidation product N(epsilon)-(carboxymethyl) lysine in human tissues in diabetes and aging. J. Clin. Investig. 1997, 99, 457–468. [Google Scholar] [CrossRef] [PubMed]
- Schalkwijk, C.G.; Baidoshvili, A.; Stehouwer, C.D.A.; van Hinsbergh, V.W.M.; Niessen, H.W.M. Increased accumulation of the glycoxidation product Nε-(carboxymethyl)lysine in hearts of diabetic patients: Generation and characterisation of a monoclonal anti-CML antibody. Biochim. Biophys. Acta 2004, 1636, 82–89. [Google Scholar] [CrossRef] [PubMed]
- Kilhovd, B.K.; Giardino, I.; Torjesen, P.A.; Birkeland, K.I.; Berg, T.J.; Thornalley, P.J.; Brownlee, M.; Hanssen, K.F. Increased serum levels of the specific AGE-compound methylglyoxal-derived hydroimidazolone in patients with type 2 diabetes. Metabolism 2003, 52, 163–167. [Google Scholar] [CrossRef] [PubMed]
- Sell, D.R.; Carlson, E.C.; Monnier, V.M. Differential effects of type 2 (non-insulin-dependent) diabetes mellitus on pentosidine formation in skin and glomerular basement membrane. Diabetologia 1993, 36, 936–941. [Google Scholar] [CrossRef] [PubMed]
- Biemel, K.M.; Friedl, D.A.; Lederer, M.O. 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. 2002, 277, 24907–24915. [Google Scholar] [CrossRef] [PubMed]
- Sell, D.R.; Biemel, K.M.; Reihl, O.; Lederer, M.O.; Strauch, C.M.; Monnier, V.M. Glucosepane is a major protein cross-link of the senescent human extracellular matrix. Relationship with diabetes. J. Biol. Chem. 2005, 280, 12310–12315. [Google Scholar] [CrossRef] [PubMed]
- Monnier, V.M.; Sell, D.R.; Genuth, S. Glycation products as markers and predictors of the progression of diabetic complications. Ann. NY Acad. Sci. 2005, 1043, 567–581. [Google Scholar] [CrossRef] [PubMed]
- Goldberg, T.; Cai, W.; Peppa, M.; Dardaine, V.; Baliga, B.S.; Uribarri, J.; Vlassara, H. Advanced glycoxidation end products in commonly consumed foods. J. Am. Diet. Assoc. 2004, 104, 1287–1291. [Google Scholar] [CrossRef] [PubMed]
- Assar, S.; Moloney, C.; Lima, M.; Magee, R.; Ames, J. Determination of Nɛ-(carboxymethyl)lysine in food systems by ultra performance liquid chromatography-mass spectrometry. Amino Acids 2009, 36, 317–326. [Google Scholar] [CrossRef] [PubMed]
- Henle, T. AGEs in foods: Do they play a role in uremia? Kidney Int. Suppl. 2003, S145–S147. [Google Scholar] [CrossRef]
- Koschinsky, T.; He, C.J.; Mitsuhashi, T.; Bucala, R.; Liu, C.; Buenting, C.; Heitmann, 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. [Google Scholar] [CrossRef] [PubMed]
- Delgado-Andrade, C.; Tessier, F.J.; Niquet-Leridon, C.; Seiquer, I.; Pilar Navarro, M. Study of the urinary and faecal excretion of nepsilon-carboxymethyllysine in young human volunteers. Amino Acids 2012, 43, 595–602. [Google Scholar] [CrossRef] [PubMed]
- Vlassara, H.; Cai, W.; Crandall, J.; Goldberg, T.; Oberstein, R.; Dardaine, V.; Peppa, M.; Rayfield, E.J. Inflammatory mediators are induced by dietary glycotoxins, a major risk factor for diabetic angiopathy. Proc. Natl. Acad. Sci. USA 2002, 99, 15596–15601. [Google Scholar] [CrossRef] [PubMed]
- Uribarri, J.; Peppa, M.; Cai, W.; Goldberg, T.; Lu, M.; He, C.; Vlassara, H. Restriction of dietary glycotoxins reduces excessive advanced glycation end products in renal failure patients. J. Am. Soc. Nephrol. 2003, 14, 728–731. [Google Scholar] [CrossRef] [PubMed]
- Uribarri, J.; Cai, W.; Ramdas, M.; Goodman, S.; Pyzik, R.; Chen, X.; Zhu, L.; Striker, G.E.; Vlassara, H. Restriction of advanced glycation end products improves insulin resistance in human type 2 diabetes: Potential role of AGER1 and SIRT1. Diabetes Care 2011, 34, 1610–1616. [Google Scholar] [CrossRef] [PubMed]
- Uribarri, J.; Cai, W.; Peppa, M.; Goodman, S.; Ferrucci, L.; Striker, G.; Vlassara, H. Circulating glycotoxins and dietary advanced glycation endproducts: Two links to inflammatory response, oxidative stress, and aging. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 2007, 62, 427–433. [Google Scholar] [CrossRef]
- Cai, W.; Ramdas, M.; Zhu, L.; Chen, X.; Striker, G.E.; Vlassara, H. Oral advanced glycation endproducts (AGEs) promote insulin resistance and diabetes by depleting the antioxidant defenses AGE receptor-1 and Sirtuin 1. Proc. Natl. Acad. Sci. USA 2012, 109, 15888–15893. [Google Scholar] [CrossRef] [PubMed]
- Coughlan, M.T.; Yap, F.Y.; Tong, D.C.; Andrikopoulos, S.; Gasser, A.; Thallas-Bonke, V.; Webster, D.E.; Miyazaki, J.; Kay, T.W.; Slattery, R.M.; et al. Advanced glycation end products are direct modulators of beta-cell function. Diabetes 2011, 60, 2523–2532. [Google Scholar] [CrossRef] [PubMed]
- Hofmann, M.A.; Drury, S.; Fu, C.; Qu, W.; Taguchi, A.; Lu, Y.; Avila, C.; Kambham, N.; Bierhaus, A.; Nawroth, P.; et al. RAGE mediates a novel proinflammatory axis: A central cell surface receptor for S100/calgranulin polypeptides. Cell 1999, 97, 889–901. [Google Scholar] [CrossRef] [PubMed]
- Hori, O.; Brett, J.; Slattery, T.; Cao, R.; Zhang, J.; Chen, J.X.; Nagashima, M.; Lundh, E.R.; Vijay, S.; Nitecki, D.; et al. The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin. Mediation of neurite outgrowth and co-expression of RAGE and amphoterin in the developing nervous system. J. Biol. Chem. 1995, 270, 25752–25761. [Google Scholar] [CrossRef] [PubMed]
- Chavakis, T.; Bierhaus, A.; Al-Fakhri, N.; Schneider, D.; Witte, S.; Linn, T.; Nagashima, M.; Morser, J.; Arnold, B.; Preissner, K.T.; et al. The pattern recognition receptor (RAGE) is a counterreceptor for leukocyte integrins: A novel pathway for inflammatory cell recruitment. J. Exp. Med. 2003, 198, 1507–1515. [Google Scholar] [CrossRef] [PubMed]
- Grimm, S.; Ott, C.; Horlacher, M.; Weber, D.; Hohn, A.; Grune, T. Advanced-glycation-end-product-induced formation of immunoproteasomes: Involvement of RAGE and Jak2/Stat1. Biochem. J. 2012, 448, 127–139. [Google Scholar] [CrossRef] [PubMed]
- Hirose, A.; Tanikawa, T.; Mori, H.; Okada, Y.; Tanaka, Y. Advanced glycation end products increase endothelial permeability through the RAGE/Rho signaling pathway. FEBS Lett. 2010, 584, 61–66. [Google Scholar] [CrossRef] [PubMed]
- Tanikawa, T.; Okada, Y.; Tanikawa, R.; Tanaka, Y. Advanced glycation end products induce calcification of vascular smooth muscle cells through RAGE/p38 mapk. J. Vasc. Res. 2009, 46, 572–580. [Google Scholar] [CrossRef] [PubMed]
- Li, J.H.; Wang, W.; Huang, X.R.; Oldfield, M.; Schmidt, A.M.; Cooper, M.E.; Lan, H.Y. Advanced glycation end products induce tubular epithelial-myofibroblast transition through the RAGE-ERK1/2 MAP kinase signaling pathway. Am. J. Pathol. 2004, 164, 1389–1397. [Google Scholar] [CrossRef] [PubMed]
- Guimaraes, E.L.; Empsen, C.; Geerts, A.; van Grunsven, L.A. Advanced glycation end products induce production of reactive oxygen species via the activation of NADPH oxidase in murine hepatic stellate cells. J. Hepatol. 2010, 52, 389–397. [Google Scholar] [CrossRef] [PubMed]
- Zhang, M.; Kho, A.L.; Anilkumar, N.; Chibber, R.; Pagano, P.J.; Shah, A.M.; Cave, A.C. Glycated proteins stimulate reactive oxygen species production in cardiac myocytes: Involvement of Nox2 (gp91phox)-containing NADPH oxidase. Circulation 2006, 113, 1235–1243. [Google Scholar] [CrossRef] [PubMed]
- Bierhaus, A.; Schiekofer, S.; Schwaninger, M.; Andrassy, M.; Humpert, P.M.; Chen, J.; Hong, M.; Luther, T.; Henle, T.; Kloting, I.; et al. Diabetes-associated sustained activation of the transcription factor nuclear factor-κB. Diabetes 2001, 50, 2792–2808. [Google Scholar] [CrossRef] [PubMed]
- Libermann, T.A.; Baltimore, D. Activation of interleukin-6 gene expression through the NF-κB transcription factor. Mol. Cell. Biol. 1990, 10, 2327–2334. [Google Scholar] [PubMed]
- Ueda, A.; Ishigatsubo, Y.; Okubo, T.; Yoshimura, T. Transcriptional regulation of the human monocyte chemoattractant protein-1 gene: Cooperation of two NF-κB sites and NF-κB/Rel subunit specificity. J. Biol. Chem. 1997, 272, 31092–31099. [Google Scholar] [CrossRef] [PubMed]
- Li, J.; Schmidt, A.M. Characterization and functional analysis of the promoter of RAGE, the receptor for advanced glycation end products. J. Biol. Chem. 1997, 272, 16498–16506. [Google Scholar] [CrossRef] [PubMed]
- Ott, C.; Jacobs, K.; Haucke, E.; Navarrete Santos, A.; Grune, T.; Simm, A. Role of advanced glycation end products in cellular signaling. Redox Biol. 2014, 2, 411–429. [Google Scholar] [CrossRef] [PubMed]
- Grimm, S.; Ernst, L.; Grotzinger, N.; Hohn, A.; Breusing, N.; Reinheckel, T.; Grune, T. Cathepsin D is one of the major enzymes involved in intracellular degradation of AGE-modified proteins. Free Radic. Res. 2010, 44, 1013–1026. [Google Scholar] [CrossRef] [PubMed]
- Grimm, S.; Horlacher, M.; Catalgol, B.; Hoehn, A.; Reinheckel, T.; Grune, T. Cathepsins D and L reduce the toxicity of advanced glycation end products. Free Radic. Biol. Med. 2012, 52, 1011–1023. [Google Scholar] [CrossRef] [PubMed]
- Cai, W.; Torreggiani, M.; Zhu, L.; Chen, X.; He, J.C.; Striker, G.E.; Vlassara, H. AGER1 regulates endothelial cell NADPH oxidase-dependent oxidant stress via PKC-delta: Implications for vascular disease. Am. J. Physiol. Cell Physiol. 2010, 298, C624–C634. [Google Scholar] [CrossRef] [PubMed]
- Lu, C.; He, J.C.; Cai, W.; Liu, H.; Zhu, L.; Vlassara, H. Advanced glycation endproduct (AGE) receptor 1 is a negative regulator of the inflammatory response to AGE in mesangial cells. Proc. Natl. Acad. Sci. USA 2004, 101, 11767–11772. [Google Scholar] [CrossRef] [PubMed]
- Vlassara, H.; Cai, W.; Goodman, S.; Pyzik, R.; Yong, A.; Chen, X.; Zhu, L.; Neade, T.; Beeri, M.; Silverman, J.M.; et al. Protection against loss of innate defenses in adulthood by low advanced glycation end products (AGE) intake: Role of the antiinflammatory AGE receptor-1. J. Clin. Endocrinol. Metab. 2009, 94, 4483–4491. [Google Scholar] [CrossRef] [PubMed]
- Torreggiani, M.; Liu, H.; Wu, J.; Zheng, F.; Cai, W.; Striker, G.; Vlassara, H. Advanced glycation end product receptor-1 transgenic mice are resistant to inflammation, oxidative stress, and post-injury intimal hyperplasia. Am. J. Pathol. 2009, 175, 1722–1732. [Google Scholar] [CrossRef] [PubMed]
- Zimmet, P.; Alberti, K.G.M.M.; Shaw, J. Global and societal implications of the diabetes epidemic. Nature 2001, 414, 782–787. [Google Scholar] [CrossRef] [PubMed]
- Tan, K.C.; Shiu, S.W.; Wong, Y.; Tam, X. Serum advanced glycation end products (AGEs) are associated with insulin resistance. Diabetes Metab. Res. Rev. 2011, 27, 488–492. [Google Scholar] [CrossRef] [PubMed]
- Matthews, D.; Hosker, J.; Rudenski, A.; Naylor, B.; Treacher, D.; Turner, R. Homeostasis model assessment: Insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985, 28, 412–419. [Google Scholar] [CrossRef] [PubMed]
- Tahara, N.; Yamagishi, S.; Matsui, T.; Takeuchi, M.; Nitta, Y.; Kodama, N.; Mizoguchi, M.; Imaizumi, T. Serum levels of advanced glycation end products (AGEs) are independent correlates of insulin resistance in nondiabetic subjects. Cardiovasc. Ther. 2012, 30, 42–48. [Google Scholar] [CrossRef] [PubMed]
- Naitoh, T.; Kitahara, M.; Tsuruzoe, N. Tumor necrosis factor-alpha is induced through phorbol ester—And glycated human albumin-dependent pathway in Thp-1 cells. Cell Signal. 2001, 13, 331–334. [Google Scholar] [CrossRef] [PubMed]
- Miele, C.; Riboulet, A.; Maitan, M.A.; Oriente, F.; Romano, C.; Formisano, P.; Giudicelli, J.; Beguinot, F.; van Obberghen, E. Human glycated albumin affects glucose metabolism in l6 skeletal muscle cells by impairing insulin-induced insulin receptor substrate (IRS) signaling through a protein kinase C alpha-mediated mechanism. J. Biol. Chem. 2003, 278, 47376–47387. [Google Scholar] [CrossRef] [PubMed]
- Cassese, A.; Esposito, I.; Fiory, F.; Barbagallo, A.P.; Paturzo, F.; Mirra, P.; Ulianich, L.; Giacco, F.; Iadicicco, C.; Lombardi, A.; et al. In skeletal muscle advanced glycation end products (AGEs) inhibit insulin action and induce the formation of multimolecular complexes including the receptor for AGEs. J. Biol. Chem. 2008, 283, 36088–36099. [Google Scholar] [CrossRef] [PubMed]
- Borst, S. The role of TNF-α in insulin resistance. Endocrine 2004, 23, 177–182. [Google Scholar] [CrossRef] [PubMed]
- Nakajima, K.; Yamauchi, K.; Shigematsu, S.; Ikeo, S.; Komatsu, M.; Aizawa, T.; Hashizume, K. Selective attenuation of metabolic branch of insulin receptor down-signaling by high glucose in a hepatoma cell line, Hepg2 cells. J. Biol. Chem. 2000, 275, 20880–20886. [Google Scholar] [CrossRef] [PubMed]
- Ravichandran, L.V.; Esposito, D.L.; Chen, J.; Quon, M.J. Protein kinase c-ζ phosphorylates insulin receptor substrate-1 and impairs its ability to activate phosphatidylinositol 3-kinase in response to insulin. J. Biol. Chem. 2001, 276, 3543–3549. [Google Scholar] [CrossRef] [PubMed]
- Boyd, A.C.; Abdel-Wahab, Y.H.; McKillop, A.M.; McNulty, H.; Barnett, C.R.; O’Harte, F.P.; Flatt, P.R. Impaired ability of glycated insulin to regulate plasma glucose and stimulate glucose transport and metabolism in mouse abdominal muscle. Biochim. Biophys. Acta 2000, 1523, 128–134. [Google Scholar] [CrossRef] [PubMed]
- Hunter, S.J.; Boyd, A.C.; O’Harte, F.P.; McKillop, A.M.; Wiggam, M.I.; Mooney, M.H.; McCluskey, J.T.; Lindsay, J.R.; Ennis, C.N.; Gamble, R.; et al. Demonstration of glycated insulin in human diabetic plasma and decreased biological activity assessed by euglycemic-hyperinsulinemic clamp technique in humans. Diabetes 2003, 52, 492–498. [Google Scholar] [CrossRef] [PubMed]
- Jia, X.; Olson, D.J.; Ross, A.R.; Wu, L. Structural and functional changes in human insulin induced by methylglyoxal. FASEB J. 2006, 20, 1555–1557. [Google Scholar] [CrossRef] [PubMed]
- Abdel-Wahab, Y.H.A.; O’Harte, F.P.; Ratcliff, H.; McClenaghan, N.H.; Barnett, C.R.; Flatt, P.R. Glycation of insulin in the islets of langerhans of normal and diabetic animals. Diabetes 1996, 45, 1489–1496. [Google Scholar] [CrossRef] [PubMed]
- Abdel-Wahab, Y.H.A.; O’Harte, F.P.M.; Barnett, C.R.; Flatt, P.R. Characterization of insulin glycation in insulin-secreting cells maintained in tissue culture. J. Endocrinol. 1997, 152, 59–67. [Google Scholar] [CrossRef] [PubMed]
- O’Harte, F.P.; Hojrup, P.; Barnett, C.R.; Flatt, P.R. Identification of the site of glycation of human insulin. Peptides 1996, 17, 1323–1330. [Google Scholar] [CrossRef] [PubMed]
- Krause, R.; Kühn, J.; Penndorf, I.; Knoll, K.; Henle, T. N-terminal pyrazinones: A new class of peptide-bound advanced glycation end-products. Amino Acids 2004, 27, 9–18. [Google Scholar] [CrossRef] [PubMed]
- Unoki-Kubota, H.; Yamagishi, S.; Takeuchi, M.; Bujo, H.; Saito, Y. Pyridoxamine, an inhibitor of advanced glycation end product (AGE) formation ameliorates insulin resistance in obese, type 2 diabetic mice. Protein Pept. Lett. 2010, 17, 1177–1181. [Google Scholar] [CrossRef] [PubMed]
- Guo, Q.; Mori, T.; Jiang, Y.; Hu, C.; Osaki, Y.; Yoneki, Y.; Sun, Y.; Hosoya, T.; Kawamata, A.; Ogawa, S.; et al. Methylglyoxal contributes to the development of insulin resistance and salt sensitivity in sprague-dawley rats. J. Hypertens. 2009, 27, 1664–1671. [Google Scholar] [CrossRef] [PubMed]
- Liang, F.; Kume, S.; Koya, D. Sirt1 and insulin resistance. Nat. Rev. Endocrinol. 2009, 5, 367–373. [Google Scholar] [CrossRef] [PubMed]
- Lim, M.; Park, L.; Shin, G.; Hong, H.; Kang, I.; Park, Y. Induction of apoptosis of beta cells of the pancreas by advanced glycation end-products, important mediators of chronic complications of diabetes mellitus. Ann. NY Acad. Sci. 2008, 1150, 311–315. [Google Scholar] [CrossRef] [PubMed]
- Luciano Viviani, G.; Puddu, A.; Sacchi, G.; Garuti, A.; Storace, D.; Durante, A.; Monacelli, F.; Odetti, P. Glycated fetal calf serum affects the viability of an insulin-secreting cell line in vitro. Metabolism 2008, 57, 163–169. [Google Scholar] [CrossRef] [PubMed]
- Zhu, Y.; Shu, T.; Lin, Y.; Wang, H.; Yang, J.; Shi, Y.; Han, X. Inhibition of the receptor for advanced glycation endproducts (RAGE) protects pancreatic beta-cells. Biochem. Biophys. Res. Commun. 2011, 404, 159–165. [Google Scholar] [CrossRef] [PubMed]
- Lin, N.; Zhang, H.; Su, Q. Advanced glycation end-products induce injury to pancreatic beta cells through oxidative stress. Diabetes Metab. 2012, 38, 250–257. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Z.; Zhao, C.; Zhang, X.H.; Zheng, F.; Cai, W.; Vlassara, H.; Ma, Z.A. Advanced glycation end products inhibit glucose-stimulated insulin secretion through nitric oxide-dependent inhibition of cytochrome C oxidase and adenosine triphosphate synthesis. Endocrinology 2009, 150, 2569–2576. [Google Scholar] [CrossRef] [PubMed]
- Jitrapakdee, S.; Wutthisathapornchai, A.; Wallace, J.C.; MacDonald, M.J. Regulation of insulin secretion: Role of mitochondrial signalling. Diabetologia 2010, 53, 1019–1032. [Google Scholar] [CrossRef] [PubMed]
- Hachiya, H.; Miura, Y.; Inoue, K.; Park, K.H.; Takeuchi, M.; Kubota, K. Advanced glycation end products impair glucose-induced insulin secretion from rat pancreatic beta-cells. J. Hepatobiliary Pancreat. Sci. 2014, 21, 134–141. [Google Scholar] [CrossRef] [PubMed]
- Eto, K.; Tsubamoto, Y.; Terauchi, Y.; Sugiyama, T.; Kishimoto, T.; Takahashi, N.; Yamauchi, N.; Kubota, N.; Murayama, S.; Aizawa, T.; et al. Role of NADH shuttle system in glucose-induced activation of mitochondrial metabolism and insulin secretion. Science 1999, 283, 981–985. [Google Scholar] [CrossRef] [PubMed]
- Shu, T.; Zhu, Y.; Wang, H.; Lin, Y.; Ma, Z.; Han, X. AGEs decrease insulin synthesis in pancreatic beta-cell by repressing Pdx-1 protein expression at the post-translational level. PLOS ONE 2011, 6, e18782. [Google Scholar] [CrossRef] [PubMed]
- Puddu, A.; Storace, D.; Odetti, P.; Viviani, G.L. Advanced glycation end-products affect transcription factors regulating insulin gene expression. Biochem. Biophys. Res. Commun. 2010, 395, 122–125. [Google Scholar] [CrossRef] [PubMed]
- Wautier, M.; Massin, P.; Guillausseau, P.; Huijberts, M.; Levy, B.; Boulanger, E.; Laloi-Michelin, M.; Wautier, J. N(carboxymethyl) lysine as a biomarker for microvascular complications in type 2 diabetic patients. Diabetes Metab. 2003, 29, 44–52. [Google Scholar] [CrossRef] [PubMed]
- Boehm, B.; Schilling, S.; Rosinger, S.; Lang, G.; Lang, G.; Kientsch-Engel, R.; Stahl, P. Elevated serum levels of Nε-carboxymethyl-lysine, an advanced glycation end product, are associated with proliferative diabetic retinopathy and macular oedema. Diabetologia 2004, 47, 1376–1379. [Google Scholar] [CrossRef] [PubMed]
- Fosmark, D.S.; Torjesen, P.A.; Kilhovd, B.K.; Berg, T.J.; Sandvik, L.; Hanssen, K.F.; Agardh, C.-D.; Agardh, E. 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 2006, 55, 232–236. [Google Scholar] [CrossRef] [PubMed]
- Aso, Y.; Inukai, T.; Tayama, K.; Takemura, Y. Serum concentrations of advanced glycation endproducts are associated with the development of atherosclerosis as well as diabetic microangiopathy in patients with type 2 diabetes. Acta Diabetol. 2000, 37, 87–92. [Google Scholar] [CrossRef] [PubMed]
- Ono, Y.; Aoki, S.; Ohnishi, K.; Yasuda, T.; Kawano, K.; Tsukada, Y. Increased serum levels of advanced glycation end-products and diabetic complications. Diabetes Res. Clin. Pract. 1998, 41, 131–137. [Google Scholar] [CrossRef] [PubMed]
- Kiuchi, K.; Nejima, J.; Takano, T.; Ohta, M.; Hashimoto, H. Increased serum concentrations of advanced glycation end products: A marker of coronary artery disease activity in type 2 diabetic patients. Heart 2001, 85, 87–91. [Google Scholar] [CrossRef] [PubMed]
- Busch, M.; Franke, S.; Wolf, G.; Brandstädt, A.; Ott, U.; Gerth, J.; Hunsicker, L.G.; Stein, G. The advanced glycation end product Nε-carboxymethyllysine is not a predictor of cardiovascular events and renal outcomes in patients with type 2 diabetic kidney disease and hypertension. Am. J. Kidney Dis. 2006, 48, 571–579. [Google Scholar] [CrossRef] [PubMed]
- Hanssen, N.M.; Engelen, L.; Ferreira, I.; Scheijen, J.L.; Huijberts, M.S.; van Greevenbroek, M.M.; van der Kallen, C.J.; Dekker, J.M.; Nijpels, G.; Stehouwer, C.D. Plasma levels of advanced glycation endproducts Nε-(carboxymethyl) lysine, Nε-(carboxyethyl) lysine, and pentosidine are not independently associated with cardiovascular disease in individuals with or without type 2 diabetes: The hoorn and codam studies. J. Clin. Endocrinol. Metab. 2013, 98, E1369–E1373. [Google Scholar] [CrossRef] [PubMed]
- Hanssen, N.M.; Beulens, J.W.; van Dieren, S.; Scheijen, J.L.; Spijkerman, A.M.; van der Schouw, Y.T.; Stehouwer, C.D.; Schalkwijk, C.G. Plasma advanced glycation endproducts are associated with incident cardiovascular events in individuals with type 2 diabetes: A case-cohort study with a median follow-up of 10 years (EPIC-NL). Diabetes 2014, 64, 257–265. [Google Scholar] [CrossRef] [PubMed]
- Dobler, D.; Ahmed, N.; Song, L.; Eboigbodin, K.E.; Thornalley, P.J. Increased dicarbonyl metabolism in endothelial cells in hyperglycemia induces anoikis and impairs angiogenesis by RGD and GFOGER motif modification. Diabetes 2006, 55, 1961–1969. [Google Scholar] [CrossRef] [PubMed]
- Chong, S.A.; Lee, W.; Arora, P.D.; Laschinger, C.; Young, E.W.; Simmons, C.A.; Manolson, M.; Sodek, J.; McCulloch, C.A. Methylglyoxal inhibits the binding step of collagen phagocytosis. J. Biol. Chem. 2007, 282, 8510–8520. [Google Scholar] [CrossRef] [PubMed]
- Nowotny, K.; Grune, T. Degradation of oxidized and glycoxidized collagen: Role of collagen cross-linking. Arch. Biochem. Biophys. 2014, 542, 56–64. [Google Scholar] [CrossRef] [PubMed]
- Yuen, A.; Laschinger, C.; Talior, I.; Lee, W.; Chan, M.; Birek, J.; Young, E.W.; Sivagurunathan, K.; Won, E.; Simmons, C.A.; et al. Methylglyoxal-modified collagen promotes myofibroblast differentiation. Matrix Biol. 2010, 29, 537–548. [Google Scholar] [CrossRef] [PubMed]
- Talior-Volodarsky, I.; Arora, P.D.; Wang, Y.; Zeltz, C.; Connelly, K.A.; Gullberg, D.; McCulloch, C.A. Glycated collagen induces alpha11 integrin expression through TGF-beta2 and Smad3. J. Cell. Physiol. 2015, in press. [Google Scholar]
- Talior-Volodarsky, I.; Connelly, K.A.; Arora, P.D.; Gullberg, D.; McCulloch, C.A. Alpha11 integrin stimulates myofibroblast differentiation in diabetic cardiomyopathy. Cardiovasc. Res. 2012, 96, 265–275. [Google Scholar] [CrossRef] [PubMed]
- Pozzi, A.; Zent, R.; Chetyrkin, S.; Borza, C.; Bulus, N.; Chuang, P.; Chen, D.; Hudson, B.; Voziyan, P. Modification of collagen IV by glucose or methylglyoxal alters distinct mesangial cell functions. J. Am. Soc. Nephrol. 2009, 20, 2119–2125. [Google Scholar] [CrossRef] [PubMed]
- Sassi-Gaha, S.; Loughlin, D.T.; Kappler, F.; Schwartz, M.L.; Su, B.; Tobia, A.M.; Artlett, C.M. Two dicarbonyl compounds, 3-deoxyglucosone and methylglyoxal, differentially modulate dermal fibroblasts. Matrix Biol. 2010, 29, 127–134. [Google Scholar] [CrossRef] [PubMed]
- Charonis, A.S.; Tsilibary, E.C.; Saku, T.; Furthmayr, H. Inhibition of laminin self-assembly and interaction with type IV collagen by antibodies to the terminal domain of the long arm. J. Cell Biol. 1986, 103, 1689–1697. [Google Scholar] [CrossRef] [PubMed]
- Haitoglou, C.S.; Tsilibary, E.C.; Brownlee, M.; Charonis, A.S. Altered cellular interactions between endothelial cells and nonenzymatically glucosylated laminin/type IV collagen. J. Biol. Chem. 1992, 267, 12404–12407. [Google Scholar] [PubMed]
- Cohen, M.P.; Ku, L. Inhibition of fibronectin binding to matrix components by nonenzymatic glycosylation. Diabetes 1984, 33, 970–974. [Google Scholar] [CrossRef] [PubMed]
- Liu, B.; Bhat, M.; Padival, A.K.; Smith, D.G.; Nagaraj, R.H. Effect of dicarbonyl modification of fibronectin on retinal capillary pericytes. Investig. Ophthalmol. Vis. Sci. 2004, 45, 1983–1995. [Google Scholar] [CrossRef]
- Duran-Jimenez, B.; Dobler, D.; Moffatt, S.; Rabbani, N.; Streuli, C.H.; Thornalley, P.J.; Tomlinson, D.R.; Gardiner, N.J. Advanced glycation end products in extracellular matrix proteins contribute to the failure of sensory nerve regeneration in diabetes. Diabetes 2009, 58, 2893–2903. [Google Scholar] [CrossRef] [PubMed]
- Collaboration, E.R.F. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: A collaborative meta-analysis of 102 prospective studies. Lancet 2010, 375, 2215–2222. [Google Scholar] [CrossRef] [PubMed]
- Kilhovd, B.K.; Juutilainen, A.; Lehto, S.; Rönnemaa, T.; Torjesen, P.A.; Hanssen, K.F.; Laakso, M. 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 2007, 50, 1409–1417. [Google Scholar] [CrossRef] [PubMed]
- Meerwaldt, R.; Lutgers, H.L.; Links, T.P.; Graaff, R.; Baynes, J.W.; Gans, R.O.B.; Smit, A.J. Skin autofluorescence is a strong predictor of cardiac mortality in diabetes. Diabetes Care 2007, 30, 107–112. [Google Scholar] [CrossRef] [PubMed]
- Meerwaldt, R.; Graaff, R.; Oomen, P.; Links, T.; Jager, J.; Alderson, N.; Thorpe, S.; Baynes, J.; Gans, R.; Smit, A. Simple non-invasive assessment of advanced glycation endproduct accumulation. Diabetologia 2004, 47, 1324–1330. [Google Scholar] [CrossRef] [PubMed]
- Del Turco, S.; Basta, G. An update on advanced glycation endproducts and atherosclerosis. BioFactors 2012, 38, 266–274. [Google Scholar] [CrossRef] [PubMed]
- Kume, S.; Takeya, M.; Mori, T.; Araki, N.; Suzuki, H.; Horiuchi, S.; Kodama, T.; Miyauchi, Y.; Takahashi, K. Immunohistochemical and ultrastructural detection of advanced glycation end products in atherosclerotic lesions of human aorta with a novel specific monoclonal antibody. Am. J. Pathol. 1995, 147, 654–667. [Google Scholar] [PubMed]
- Nerlich, A.G.; Schleicher, E.D. Nε-(carboxymethyl)lysine in atherosclerotic vascular lesions as a marker for local oxidative stress. Atherosclerosis 1999, 144, 41–47. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Y.J.; Wang, J.H.; Zhang, J. Hepatocyte growth factor protects human endothelial cells against advanced glycation end products-induced apoposis. Biochem. Biophys. Res. Communi. 2006, 344, 658–666. [Google Scholar] [CrossRef]
- Li, Y.; Li, J.; Cui, L.; Lai, Y.; Yao, Y.; Zhang, Y.; Pang, X.; Wang, J.; Liu, X. Inhibitory effect of atorvastatin on AGE-induced HCAEC apoptosis by upregulating HSF-1 protein. Int. J. Biol. Macromol. 2013, 57, 259–264. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Song, M.; Yu, S.; Gao, P.; Yu, Y.; Wang, H.; Huang, L. Advanced glycation endproducts alter functions and promote apoptosis in endothelial progenitor cells through receptor for advanced glycation endproducts mediate overpression of cell oxidant stress. Mol. Cell. Biochem. 2010, 335, 137–146. [Google Scholar] [CrossRef] [PubMed]
- Inagaki, Y.; Yamagishi, S.; Okamoto, T.; Takeuchi, M.; Amano, S. Pigment epithelium-derived factor prevents advanced glycation end products-induced monocyte chemoattractant protein-1 production in microvascular endothelial cells by suppressing intracellular reactive oxygen species generation. Diabetologia 2003, 46, 284–287. [Google Scholar] [PubMed]
- Vlassara, H.; Fuh, H.; Donnelly, T.; Cybulsky, M. Advanced glycation endproducts promote adhesion molecule (VCAM-1, ICAM-1) expression and atheroma formation in normal rabbits. Mol. Med. 1995, 1, 447–456. [Google Scholar] [PubMed]
- Schmidt, A.M.; Hori, O.; Chen, J.X.; Li, J.F.; Crandall, J.; Zhang, J.; Cao, R.; Yan, S.D.; Brett, J.; Stern, D. 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. Investig. 1995, 96, 1395–1403. [Google Scholar] [CrossRef] [PubMed]
- Ishibashi, Y.; Matsui, T.; Takeuchi, M.; Yamagishi, S.-I. Glucagon-like peptide-1 (GLP-1) inhibits advanced glycation end product (AGE)-induced up-regulation of VCAM-1 mRNA levels in endothelial cells by suppressing AGE receptor (RAGE) expression. Biochem. Biophys. Res. Commun. 2010, 391, 1405–1408. [Google Scholar] [CrossRef] [PubMed]
- Ishibashi, Y.; Matsui, T.; Maeda, S.; Higashimoto, Y.; Yamagishi, S.-I. Advanced glycation end products evoke endothelial cell damage by stimulating soluble dipeptidyl peptidase-4 production and its interaction with mannose 6-phosphate/insulin-like growth factor II receptor. Cardiovasc. Diabetol. 2013, 12, 125–125. [Google Scholar] [CrossRef] [PubMed]
- Yamagishi, S.; Fujimori, H.; Yonekura, H.; Yamamoto, Y.; Yamamoto, H. Advanced glycation endproducts inhibit prostacyclin production and induce plasminogen activator inhibitor-1 in human microvascular endothelial cells. Diabetologia 1998, 41, 1435–1441. [Google Scholar] [CrossRef] [PubMed]
- Quehenberger, P.; Bierhaus, A.; Fasching, P.; Muellner, C.; Klevesath, M.; Hong, M.; Stier, G.; Sattler, M.; Schleicher, E.; Speiser, W.; et al. Endothelin 1 transcription is controlled by nuclear factor-κB in AGE-stimulated cultured endothelial cells. Diabetes 2000, 49, 1561–1570. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Zalewski, A.; Liu, Y.; Mazurek, T.; Cowan, S.; Martin, J.L.; Hofmann, S.M.; Vlassara, H.; Shi, Y. Diabetes-induced oxidative stress and low-grade inflammation in porcine coronary arteries. Circulation 2003, 108, 472–478. [Google Scholar] [CrossRef] [PubMed]
- Bucala, R.; Tracey, K.J.; Cerami, A. Advanced glycosylation products quench nitric oxide and mediate defective endothelium-dependent vasodilatation in experimental diabetes. J. Clin. Investig. 1991, 87, 432–438. [Google Scholar] [CrossRef] [PubMed]
- Xu, B.; Chibber, R.; Ruggiero, D.; Kohner, E.; Ritter, J.; Ferro, A. Impairment of vascular endothelial nitric oxide synthase activity by advanced glycation end products. FASEB J. 2003, 17, 1289–1291. [Google Scholar] [CrossRef] [PubMed]
- Chakravarthy, U.; Hayes, R.G.; Stitt, A.W.; McAuley, E.; Archer, D.B. Constitutive nitric oxide synthase expression in retinal vascular endothelial cells is suppressed by high glucose and advanced glycation end products. Diabetes 1998, 47, 945–952. [Google Scholar] [CrossRef] [PubMed]
- Barbato, J.E.; Tzeng, E. Nitric oxide and arterial disease. J. Vasc. Surg. 2004, 40, 187–193. [Google Scholar] [CrossRef] [PubMed]
- Yamagishi, S.; Amano, S.; Inagaki, Y.; Okamoto, T.; Koga, K.; Sasaki, N.; Yamamoto, H.; Takeuchi, M.; Makita, Z. Advanced glycation end products-induced apoptosis and overexpression of vascular endothelial growth factor in bovine retinal pericytes. Biochem. Biophys. Res. Commun. 2002, 290, 973–978. [Google Scholar] [CrossRef] [PubMed]
- Stitt, A.W.; Hughes, S.J.; Canning, P.; Lynch, O.; Cox, O.; Frizzell, N.; Thorpe, S.R.; Cotter, T.G.; Curtis, T.M.; Gardiner, T.A. Substrates modified by advanced glycation end-products cause dysfunction and death in retinal pericytes by reducing survival signals mediated by platelet-derived growth factor. Diabetologia 2004, 47, 1735–1746. [Google Scholar] [CrossRef] [PubMed]
- Antonetti, D. Eye vessels saved by rescuing their pericyte partners. Nat. Med. 2009, 15, 1248–1249. [Google Scholar] [CrossRef] [PubMed]
- Moore, T.C.; Moore, J.E.; Kaji, Y.; Frizzell, N.; Usui, T.; Poulaki, V.; Campbell, I.L.; Stitt, A.W.; Gardiner, T.A.; Archer, D.B.; et al. The role of advanced glycation end products in retinal microvascular leukostasis. Investig. Ophthalmol. Vis. Sci. 2003, 44, 4457–4464. [Google Scholar] [CrossRef]
- Lu, M.; Kuroki, M.; Amano, S.; Tolentino, M.; Keough, K.; Kim, I.; Bucala, R.; Adamis, A.P. Advanced glycation end products increase retinal vascular endothelial growth factor expression. J. Clin. Investig. 1998, 101, 1219–1224. [Google Scholar] [CrossRef] [PubMed]
- Stitt, A.W.; Bhaduri, T.; McMullen, C.B.; Gardiner, T.A.; Archer, D.B. Advanced glycation end products induce blood-retinal barrier dysfunction in normoglycemic rats. Mol. Cell Biol. Res. Commun. 2000, 3, 380–388. [Google Scholar] [CrossRef] [PubMed]
- Mamputu, J.C.; Renier, G. Advanced glycation end products increase, through a protein kinase C-dependent pathway, vascular endothelial growth factor expression in retinal endothelial cells. Inhibitory effect of gliclazide. J. Diabetes Complicat. 2002, 16, 284–293. [Google Scholar] [CrossRef] [PubMed]
- Yamagishi, S.; Inagaki, Y.; Okamoto, T.; Amano, S.; Koga, K.; Takeuchi, M.; Makita, Z. Advanced glycation end product-induced apoptosis and overexpression of vascular endothelial growth factor and monocyte chemoattractant protein-1 in human-cultured mesangial cells. J. Biol. Chem. 2002, 277, 20309–20315. [Google Scholar] [CrossRef] [PubMed]
- Ghayur, M.N.; Krepinsky, J.C.; Janssen, L.J. Contractility of the renal glomerulus and mesangial cells: Lingering doubts and strategies for the future. Med. Hypotheses Res. 2008, 4, 1–9. [Google Scholar] [PubMed]
- Yamagishi, S.; Inagaki, Y.; Okamoto, T.; Amano, S.; Koga, K.; Takeuchi, M. Advanced glycation end products inhibit de novo protein synthesis and induce TGF-beta overexpression in proximal tubular cells. Kidney Int. 2003, 63, 464–473. [Google Scholar] [CrossRef] [PubMed]
- Throckmorton, D.C.; Brogden, A.P.; Min, B.; Rasmussen, H.; Kashgarian, M. PDGF and TGF-bold beta mediate collagen production by mesangial cells exposed to advanced glycosylation end products. Kidney Int. 1995, 48, 111–117. [Google Scholar] [CrossRef] [PubMed]
- Yang, C.W.; Vlassara, H.; Peten, E.P.; He, C.J.; Striker, G.E.; Striker, L.J. Advanced glycation end products up-regulate gene expression found in diabetic glomerular disease. Proc. Natl. Acad. Sci. USA 1994, 91, 9436–9440. [Google Scholar] [CrossRef] [PubMed]
- Fukami, K.; Ueda, S.; Yamagishi, S.; Kato, S.; Inagaki, Y.; Takeuchi, M.; Motomiya, Y.; Bucala, R.; Iida, S.; Tamaki, K.; et al. AGEs activate mesangial TGF-beta-Smad signaling via an angiotensin II type I receptor interaction. Kidney Int. 2004, 66, 2137–2147. [Google Scholar] [CrossRef] [PubMed]
- Oldfield, M.D.; Bach, L.A.; Forbes, J.M.; Nikolic-Paterson, D.; McRobert, A.; Thallas, V.; Atkins, R.C.; Osicka, T.; Jerums, G.; Cooper, M.E. Advanced glycation end products cause epithelial-myofibroblast transdifferentiation via the receptor for advanced glycation end products (RAGE). J. Clin. Investig. 2001, 108, 1853–1863. [Google Scholar] [CrossRef] [PubMed]
- Burns, W.C.; Twigg, S.M.; Forbes, J.M.; Pete, J.; Tikellis, C.; Thallas-Bonke, V.; Thomas, M.C.; Cooper, M.E.; Kantharidis, P. Connective tissue growth factor plays an important role in advanced glycation end product-induced tubular epithelial-to-mesenchymal transition: Implications for diabetic renal disease. J. Am. Soc. Nephrol. 2006, 17, 2484–2494. [Google Scholar] [CrossRef] [PubMed]
- Roestenberg, P.; van Nieuwenhoven, F.A.; Wieten, L.; Boer, P.; Diekman, T.; Tiller, A.M.; Wiersinga, W.M.; Oliver, N.; Usinger, W.; Weitz, S.; et al. Connective tissue growth factor is increased in plasma of type 1 diabetic patients with nephropathy. Diabetes Care 2004, 27, 1164–1170. [Google Scholar] [CrossRef] [PubMed]
- Chung, A.C.K.; Zhang, H.; Kong, Y.-Z.; Tan, J.-J.; Huang, X.R.; Kopp, J.B.; Lan, H.Y. Advanced glycation end-products induce tubular CTGF via TGF-β-independent Smad3 signaling. J. Am. Soc. Nephrol. 2010, 21, 249–260. [Google Scholar] [CrossRef] [PubMed]
- Thornalley, P.J. Dietary AGEs and ALEs and risk to human health by their interaction with the receptor for advanced glycation endproducts (RAGE)—An introduction. Mol. Nutr. Food Res. 2007, 51, 1107–1110. [Google Scholar] [CrossRef] [PubMed]
- Ramasamy, R.; Yan, S.F.; Schmidt, A.M. Arguing for the motion: Yes, rage is a receptor for advanced glycation endproducts. Mol. Nutr. Food Res. 2007, 51, 1111–1115. [Google Scholar] [CrossRef] [PubMed]
- Heizmann, C.W. The mechanism by which dietary AGEs are a risk to human health is via their interaction with RAGE: Arguing against the motion. Mol. Nutr. Food Res. 2007, 51, 1116–1119. [Google Scholar] [CrossRef] [PubMed]
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Nowotny, K.; Jung, T.; Höhn, A.; Weber, D.; Grune, T. Advanced Glycation End Products and Oxidative Stress in Type 2 Diabetes Mellitus. Biomolecules 2015, 5, 194-222. https://doi.org/10.3390/biom5010194
Nowotny K, Jung T, Höhn A, Weber D, Grune T. Advanced Glycation End Products and Oxidative Stress in Type 2 Diabetes Mellitus. Biomolecules. 2015; 5(1):194-222. https://doi.org/10.3390/biom5010194
Chicago/Turabian StyleNowotny, Kerstin, Tobias Jung, Annika Höhn, Daniela Weber, and Tilman Grune. 2015. "Advanced Glycation End Products and Oxidative Stress in Type 2 Diabetes Mellitus" Biomolecules 5, no. 1: 194-222. https://doi.org/10.3390/biom5010194