Skip to main content
Top
Published in: Heart Failure Reviews 2/2012

Open Access 01-03-2012

Advanced glycation end-products, a pathophysiological pathway in the cardiorenal syndrome

Authors: Suzan Willemsen, Jasper W. L. Hartog, M. Rebecca Heiner-Fokkema, Dirk J. van Veldhuisen, Adriaan A. Voors

Published in: Heart Failure Reviews | Issue 2/2012

Login to get access

Abstract

The prevalence of heart failure (HF) is increasing. A distinction is made between diastolic HF (preserved left ventricular ejection fraction (LVEF)) and systolic HF (reduced LVEF). Advanced glycation end-products (AGEs) are crystallized proteins that accumulate during ageing, but are particularly increased in patients with diabetes mellitus and in patients with renal failure. Through the formation of collagen crosslinks, and by interaction with the AGE-receptor, which impairs calcium handling and increases fibrosis, AGE-accumulation has pathophysiologically been associated with the development of diastolic and renal dysfunction. Interestingly, diastolic dysfunction is a frequent finding in elderly patients, diabetic patients and in patients with renal failure. Taken together, this suggests that AGEs are related to the development and progression of diastolic HF and renal failure. In this review, the role of AGEs as a possible pathophysiological factor that link the development and progression of heart and renal failure, is discussed. Finally, the role of AGE intervention as a possible treatment in HF patients will be discussed.
Literature
1.
go back to reference Dickstein K, Cohen-Solal A, Filippatos G, McMurray JJ, Ponikowski P, Poole-Wilson PA, Stromberg A, van Veldhuisen DJ, Atar D, Hoes AW, Keren A, Mebazaa A, Nieminen M, Priori SG, Swedberg K, Vahanian A, Camm J, De Caterina R, Dean V, Dickstein K, Filippatos G, Funck-Brentano C, Hellemans I, Kristensen SD, McGregor K, Sechtem U, Silber S, Tendera M, Widimsky P, Zamorano JL, Tendera M, Auricchio A, Bax J, Bohm M, Corra U, della Bella P, Elliott PM, Follath F, Gheorghiade M, Hasin Y, Hernborg A, Jaarsma T, Komajda M, Kornowski R, Piepoli M, Prendergast B, Tavazzi L, Vachiery JL, Verheugt FW, Zamorano JL, Zannad F (2008) ESC guidelines for the diagnosis and treatment of acute and chronic heart failure 2008: the Task Force for the diagnosis and treatment of acute and chronic heart failure 2008 of the European Society of Cardiology. Developed in collaboration with the Heart Failure Association of the ESC (HFA) and endorsed by the European Society of Intensive Care Medicine (ESICM). Eur J Heart Fail 10:933–989PubMedCrossRef Dickstein K, Cohen-Solal A, Filippatos G, McMurray JJ, Ponikowski P, Poole-Wilson PA, Stromberg A, van Veldhuisen DJ, Atar D, Hoes AW, Keren A, Mebazaa A, Nieminen M, Priori SG, Swedberg K, Vahanian A, Camm J, De Caterina R, Dean V, Dickstein K, Filippatos G, Funck-Brentano C, Hellemans I, Kristensen SD, McGregor K, Sechtem U, Silber S, Tendera M, Widimsky P, Zamorano JL, Tendera M, Auricchio A, Bax J, Bohm M, Corra U, della Bella P, Elliott PM, Follath F, Gheorghiade M, Hasin Y, Hernborg A, Jaarsma T, Komajda M, Kornowski R, Piepoli M, Prendergast B, Tavazzi L, Vachiery JL, Verheugt FW, Zamorano JL, Zannad F (2008) ESC guidelines for the diagnosis and treatment of acute and chronic heart failure 2008: the Task Force for the diagnosis and treatment of acute and chronic heart failure 2008 of the European Society of Cardiology. Developed in collaboration with the Heart Failure Association of the ESC (HFA) and endorsed by the European Society of Intensive Care Medicine (ESICM). Eur J Heart Fail 10:933–989PubMedCrossRef
2.
go back to reference Fox CS, Pencina MJ, Meigs JB, Vasan RS, Levitzky YS, D’Agostino RB Sr (2006) Trends in the incidence of type 2 diabetes mellitus from the 1970s to the 1990s: the Framingham Heart Study. Circulation 113:2914–2918PubMedCrossRef Fox CS, Pencina MJ, Meigs JB, Vasan RS, Levitzky YS, D’Agostino RB Sr (2006) Trends in the incidence of type 2 diabetes mellitus from the 1970s to the 1990s: the Framingham Heart Study. Circulation 113:2914–2918PubMedCrossRef
3.
go back to reference Bhatia RS, Tu JV, Lee DS, Austin PC, Fang J, Haouzi A, Gong Y, Liu PP (2006) Outcome of heart failure with preserved ejection fraction in a population-based study. N Engl J Med 355:260–269PubMedCrossRef Bhatia RS, Tu JV, Lee DS, Austin PC, Fang J, Haouzi A, Gong Y, Liu PP (2006) Outcome of heart failure with preserved ejection fraction in a population-based study. N Engl J Med 355:260–269PubMedCrossRef
4.
go back to reference Owan TE, Hodge DO, Herges RM, Jacobsen SJ, Roger VL, Redfield MM (2006) Trends in prevalence and outcome of heart failure with preserved ejection fraction. N Engl J Med 355:251–259PubMedCrossRef Owan TE, Hodge DO, Herges RM, Jacobsen SJ, Roger VL, Redfield MM (2006) Trends in prevalence and outcome of heart failure with preserved ejection fraction. N Engl J Med 355:251–259PubMedCrossRef
5.
go back to reference Zile MR, Baicu CF, Gaasch WH (2004) Diastolic heart failure–abnormalities in active relaxation and passive stiffness of the left ventricle. N Engl J Med 350:1953–1959PubMedCrossRef Zile MR, Baicu CF, Gaasch WH (2004) Diastolic heart failure–abnormalities in active relaxation and passive stiffness of the left ventricle. N Engl J Med 350:1953–1959PubMedCrossRef
6.
go back to reference Kamalesh M, Subramanian U, Sawada S, Eckert G, Temkit M, Tierney W (2006) Decreased survival in diabetic patients with heart failure due to systolic dysfunction. Eur J Heart Fail 8:404–408PubMedCrossRef Kamalesh M, Subramanian U, Sawada S, Eckert G, Temkit M, Tierney W (2006) Decreased survival in diabetic patients with heart failure due to systolic dysfunction. Eur J Heart Fail 8:404–408PubMedCrossRef
7.
go back to reference Shindler DM, Kostis JB, Yusuf S, Quinones MA, Pitt B, Stewart D, Pinkett T, Ghali JK, Wilson AC (1996) Diabetes mellitus, a predictor of morbidity and mortality in the studies of left ventricular dysfunction (SOLVD) trials and registry. Am J Cardiol 77:1017–1020PubMedCrossRef Shindler DM, Kostis JB, Yusuf S, Quinones MA, Pitt B, Stewart D, Pinkett T, Ghali JK, Wilson AC (1996) Diabetes mellitus, a predictor of morbidity and mortality in the studies of left ventricular dysfunction (SOLVD) trials and registry. Am J Cardiol 77:1017–1020PubMedCrossRef
8.
go back to reference Ezekowitz JA, Lee DS, Tu JV, Newman AM, McAlister FA (2008) Comparison of one-year outcome (death and rehospitalization) in hospitalized heart failure patients with left ventricular ejection fraction >50% versus those with ejection fraction <50%. Am J Cardiol 102:79–83PubMedCrossRef Ezekowitz JA, Lee DS, Tu JV, Newman AM, McAlister FA (2008) Comparison of one-year outcome (death and rehospitalization) in hospitalized heart failure patients with left ventricular ejection fraction >50% versus those with ejection fraction <50%. Am J Cardiol 102:79–83PubMedCrossRef
9.
go back to reference Fonarow GC, Stough WG, Abraham WT, Albert NM, Gheorghiade M, Greenberg BH, O’Connor CM, Sun JL, Yancy CW, Young JB (2007) Characteristics, treatments, and outcomes of patients with preserved systolic function hospitalized for heart failure: a report from the OPTIMIZE-HF Registry. J Am Coll Cardiol 50:768–777PubMedCrossRef Fonarow GC, Stough WG, Abraham WT, Albert NM, Gheorghiade M, Greenberg BH, O’Connor CM, Sun JL, Yancy CW, Young JB (2007) Characteristics, treatments, and outcomes of patients with preserved systolic function hospitalized for heart failure: a report from the OPTIMIZE-HF Registry. J Am Coll Cardiol 50:768–777PubMedCrossRef
10.
go back to reference Philbin EF, Weil HF, Francis CA, Marx HJ, Jenkins PL, Pearson TA, Reed RG (2000) Race-related differences among patients with left ventricular dysfunction: observations from a biracial angiographic cohort. J Card Fail 6:187–193PubMedCrossRef Philbin EF, Weil HF, Francis CA, Marx HJ, Jenkins PL, Pearson TA, Reed RG (2000) Race-related differences among patients with left ventricular dysfunction: observations from a biracial angiographic cohort. J Card Fail 6:187–193PubMedCrossRef
11.
go back to reference Tribouilloy C, Rusinaru D, Mahjoub H, Tartiere JM, Kesri-Tartiere L, Godard S, Peltier M (2008) Prognostic impact of diabetes mellitus in patients with heart failure and preserved ejection fraction: a prospective five-year study. Heart 94:1450–1455PubMedCrossRef Tribouilloy C, Rusinaru D, Mahjoub H, Tartiere JM, Kesri-Tartiere L, Godard S, Peltier M (2008) Prognostic impact of diabetes mellitus in patients with heart failure and preserved ejection fraction: a prospective five-year study. Heart 94:1450–1455PubMedCrossRef
12.
go back to reference Hartog JW, Voors AA, Bakker SJ, Smit AJ, van Veldhuisen DJ (2007) Advanced glycation end-products (AGEs) and heart failure: pathophysiology and clinical implications. Eur J Heart Fail 9:1146–1155PubMedCrossRef Hartog JW, Voors AA, Bakker SJ, Smit AJ, van Veldhuisen DJ (2007) Advanced glycation end-products (AGEs) and heart failure: pathophysiology and clinical implications. Eur J Heart Fail 9:1146–1155PubMedCrossRef
13.
go back to reference Miyata T, Sugiyama S, Saito A, Kurokawa K (2001) Reactive carbonyl compounds related uremic toxicity (“carbonyl stress”). Kidney Int Suppl 78:S25–S31PubMedCrossRef Miyata T, Sugiyama S, Saito A, Kurokawa K (2001) Reactive carbonyl compounds related uremic toxicity (“carbonyl stress”). Kidney Int Suppl 78:S25–S31PubMedCrossRef
14.
go back to reference Willemsen S, Hartog JW, Hummel YM, van Ruijven MH, van der Horst IC, van Veldhuisen DJ, Voors AA (2011) Tissue advanced glycation end products are associated with diastolic function and aerobic exercise capacity in diabetic heart failure patients. Eur J Heart Fail 13:76–82PubMedCrossRef Willemsen S, Hartog JW, Hummel YM, van Ruijven MH, van der Horst IC, van Veldhuisen DJ, Voors AA (2011) Tissue advanced glycation end products are associated with diastolic function and aerobic exercise capacity in diabetic heart failure patients. Eur J Heart Fail 13:76–82PubMedCrossRef
15.
go back to reference Tonelli M, Wiebe N, Culleton B, House A, Rabbat C, Fok M, McAlister F, Garg AX (2006) Chronic kidney disease and mortality risk: a systematic review. J Am Soc Nephrol 17:2034–2047PubMedCrossRef Tonelli M, Wiebe N, Culleton B, House A, Rabbat C, Fok M, McAlister F, Garg AX (2006) Chronic kidney disease and mortality risk: a systematic review. J Am Soc Nephrol 17:2034–2047PubMedCrossRef
16.
go back to reference Ronco C, McCullough PA, Anker SD, Anand I, Aspromonte N, Bagshaw SM, Bellomo R, Berl T, Bobek I, Cruz DN, Daliento L, Davenport A, Haapio M, Hillege H, House A, Katz NM, Maisel A, Mankad S, Zanco P, Mebazaa A, Palazzuoli A, Ronco F, Shaw A, Sheinfeld G, Soni S, Vescovo G, Zamperetti N, Ponikowski P (2010) Cardiorenal syndromes: an executive summary from the consensus conference of the acute dialysis quality initiative (ADQI). Contrib Nephrol 165:54–67PubMedCrossRef Ronco C, McCullough PA, Anker SD, Anand I, Aspromonte N, Bagshaw SM, Bellomo R, Berl T, Bobek I, Cruz DN, Daliento L, Davenport A, Haapio M, Hillege H, House A, Katz NM, Maisel A, Mankad S, Zanco P, Mebazaa A, Palazzuoli A, Ronco F, Shaw A, Sheinfeld G, Soni S, Vescovo G, Zamperetti N, Ponikowski P (2010) Cardiorenal syndromes: an executive summary from the consensus conference of the acute dialysis quality initiative (ADQI). Contrib Nephrol 165:54–67PubMedCrossRef
17.
go back to reference Alpert MA (2003) Cardiac performance and morphology in end-stage renal disease. Am J Med Sci 325:168–178PubMedCrossRef Alpert MA (2003) Cardiac performance and morphology in end-stage renal disease. Am J Med Sci 325:168–178PubMedCrossRef
18.
go back to reference Hartog JW, Hummel YM, Voors AA, Schalkwijk CG, Miyata T, Huisman RM, Smit AJ, van Veldhuisen DJ (2008) Skin-autofluorescence, a measure of tissue advanced glycation end-products (AGEs), is related to diastolic function in dialysis patients. J Card Fail 14:596–602PubMedCrossRef Hartog JW, Hummel YM, Voors AA, Schalkwijk CG, Miyata T, Huisman RM, Smit AJ, van Veldhuisen DJ (2008) Skin-autofluorescence, a measure of tissue advanced glycation end-products (AGEs), is related to diastolic function in dialysis patients. J Card Fail 14:596–602PubMedCrossRef
19.
go back to reference Rakhit DJ, Zhang XH, Leano R, Armstrong KA, Isbel NM, Marwick TH (2007) Prognostic role of subclinical left ventricular abnormalities and impact of transplantation in chronic kidney disease. Am Heart J 153:656–664PubMedCrossRef Rakhit DJ, Zhang XH, Leano R, Armstrong KA, Isbel NM, Marwick TH (2007) Prognostic role of subclinical left ventricular abnormalities and impact of transplantation in chronic kidney disease. Am Heart J 153:656–664PubMedCrossRef
20.
go back to reference Virga G, Stomaci B, Munaro A, Mastrosimone S, Cara M, Artuso E, Piovesana P (2006) Systolic and diastolic function in renal replacement therapy: a cross-sectional study. J Nephrol 19:155–160PubMed Virga G, Stomaci B, Munaro A, Mastrosimone S, Cara M, Artuso E, Piovesana P (2006) Systolic and diastolic function in renal replacement therapy: a cross-sectional study. J Nephrol 19:155–160PubMed
21.
go back to reference Damman K, Navis G, Voors AA, Asselbergs FW, Smilde TD, Cleland JG, van Veldhuisen DJ, Hillege HL (2007) Worsening renal function and prognosis in heart failure: systematic review and meta-analysis. J Card Fail 13:599–608PubMedCrossRef Damman K, Navis G, Voors AA, Asselbergs FW, Smilde TD, Cleland JG, van Veldhuisen DJ, Hillege HL (2007) Worsening renal function and prognosis in heart failure: systematic review and meta-analysis. J Card Fail 13:599–608PubMedCrossRef
22.
go back to reference Damman K, Navis G, Voors AA, Asselbergs FW, Smilde TD, Cleland JG, van Veldhuisen DJ, Hillege HL (2007) Worsening renal function and prognosis in heart failure: systematic review and meta-analysis. J Card Fail 13:599–608PubMedCrossRef Damman K, Navis G, Voors AA, Asselbergs FW, Smilde TD, Cleland JG, van Veldhuisen DJ, Hillege HL (2007) Worsening renal function and prognosis in heart failure: systematic review and meta-analysis. J Card Fail 13:599–608PubMedCrossRef
23.
go back to reference Damman K, Navis G, Voors AA, Asselbergs FW, Smilde TD, Cleland JG, van Veldhuisen DJ, Hillege HL (2007) Worsening renal function and prognosis in heart failure: systematic review and meta-analysis. J Card Fail 13:599–608PubMedCrossRef Damman K, Navis G, Voors AA, Asselbergs FW, Smilde TD, Cleland JG, van Veldhuisen DJ, Hillege HL (2007) Worsening renal function and prognosis in heart failure: systematic review and meta-analysis. J Card Fail 13:599–608PubMedCrossRef
24.
go back to reference Damman K, van Deursen VM, Navis G, Voors AA, van Veldhuisen DJ, Hillege HL (2009) Increased central venous pressure is associated with impaired renal function and mortality in a broad spectrum of patients with cardiovascular disease. J Am Coll Cardiol 53:582–588PubMedCrossRef Damman K, van Deursen VM, Navis G, Voors AA, van Veldhuisen DJ, Hillege HL (2009) Increased central venous pressure is associated with impaired renal function and mortality in a broad spectrum of patients with cardiovascular disease. J Am Coll Cardiol 53:582–588PubMedCrossRef
25.
go back to reference Smit AJ, Gerrits EG (2010) Skin autofluorescence as a measure of advanced glycation endproduct deposition: a novel risk marker in chronic kidney disease. Curr Opin Nephrol Hypertens 19:527–533PubMedCrossRef Smit AJ, Gerrits EG (2010) Skin autofluorescence as a measure of advanced glycation endproduct deposition: a novel risk marker in chronic kidney disease. Curr Opin Nephrol Hypertens 19:527–533PubMedCrossRef
26.
go back to reference Schalkwijk CG, Baidoshvili A, Stehouwer CD, van HV, 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 1636:82–89PubMed Schalkwijk CG, Baidoshvili A, Stehouwer CD, van HV, 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 1636:82–89PubMed
27.
go back to reference Schleicher ED, Wagner E, Nerlich AG (1997) Increased accumulation of the glycoxidation product N(epsilon)-(carboxymethyl)lysine in human tissues in diabetes and aging. J Clin Invest 99:457–468PubMedCrossRef Schleicher ED, Wagner E, Nerlich AG (1997) Increased accumulation of the glycoxidation product N(epsilon)-(carboxymethyl)lysine in human tissues in diabetes and aging. J Clin Invest 99:457–468PubMedCrossRef
28.
go back to reference Cerami C, Founds H, Nicholl I, Mitsuhashi T, Giordano D, Vanpatten S, Lee A, Al Abed Y, Vlassara H, Bucala R, Cerami A (1997) Tobacco smoke is a source of toxic reactive glycation products. Proc Natl Acad Sci USA 94:13915–13920PubMedCrossRef Cerami C, Founds H, Nicholl I, Mitsuhashi T, Giordano D, Vanpatten S, Lee A, Al Abed Y, Vlassara H, Bucala R, Cerami A (1997) Tobacco smoke is a source of toxic reactive glycation products. Proc Natl Acad Sci USA 94:13915–13920PubMedCrossRef
29.
go back to reference Uribarri J, Peppa M, Cai W, Goldberg T, Lu M, He C, Vlassara H (2003) Restriction of dietary glycotoxins reduces excessive advanced glycation end products in renal failure patients. J Am Soc Nephrol 14:728–731PubMedCrossRef Uribarri J, Peppa M, Cai W, Goldberg T, Lu M, He C, Vlassara H (2003) Restriction of dietary glycotoxins reduces excessive advanced glycation end products in renal failure patients. J Am Soc Nephrol 14:728–731PubMedCrossRef
30.
go back to reference Teerlink T, Barto R, Ten Brink HJ, Schalkwijk CG (2004) Measurement of Nepsilon-(carboxymethyl)lysine and Nepsilon-(carboxyethyl)lysine in human plasma protein by stable-isotope-dilution tandem mass spectrometry. Clin Chem 50:1222–1228PubMedCrossRef Teerlink T, Barto R, Ten Brink HJ, Schalkwijk CG (2004) Measurement of Nepsilon-(carboxymethyl)lysine and Nepsilon-(carboxyethyl)lysine in human plasma protein by stable-isotope-dilution tandem mass spectrometry. Clin Chem 50:1222–1228PubMedCrossRef
31.
go back to reference Scheijen JL, van de Waarenburg MP, Stehouwer CD, Schalkwijk CG (2009) Measurement of pentosidine in human plasma protein by a single-column high-performance liquid chromatography method with fluorescence detection. J Chromatogr B Analyt Technol Biomed Life Sci 877:610–614PubMedCrossRef Scheijen JL, van de Waarenburg MP, Stehouwer CD, Schalkwijk CG (2009) Measurement of pentosidine in human plasma protein by a single-column high-performance liquid chromatography method with fluorescence detection. J Chromatogr B Analyt Technol Biomed Life Sci 877:610–614PubMedCrossRef
32.
go back to reference Meerwaldt R, Graaff R, Oomen PH, Links TP, Jager JJ, Alderson NL, Thorpe SR, Baynes JW, Gans RO, Smit AJ (2004) Simple non-invasive assessment of advanced glycation endproduct accumulation. Diabetologia 47:1324–1330PubMedCrossRef Meerwaldt R, Graaff R, Oomen PH, Links TP, Jager JJ, Alderson NL, Thorpe SR, Baynes JW, Gans RO, Smit AJ (2004) Simple non-invasive assessment of advanced glycation endproduct accumulation. Diabetologia 47:1324–1330PubMedCrossRef
33.
34.
go back to reference Loimaala A, Groundstroem K, Rinne M, Nenonen A, Huhtala H, Vuori I (2007) Exercise training does not improve myocardial diastolic tissue velocities in Type 2 diabetes. Cardiovasc Ultrasound 5:32–40PubMedCrossRef Loimaala A, Groundstroem K, Rinne M, Nenonen A, Huhtala H, Vuori I (2007) Exercise training does not improve myocardial diastolic tissue velocities in Type 2 diabetes. Cardiovasc Ultrasound 5:32–40PubMedCrossRef
35.
go back to reference Smit AJ, Hartog JW, Voors AA, van Veldhuisen DJ (2008) Advanced glycation endproducts in chronic heart failure. Ann N Y Acad Sci 1126:225–230PubMedCrossRef Smit AJ, Hartog JW, Voors AA, van Veldhuisen DJ (2008) Advanced glycation endproducts in chronic heart failure. Ann N Y Acad Sci 1126:225–230PubMedCrossRef
36.
go back to reference Wu YW, Hsu CL, Wang SS, Tsai MW, Chu SH, Chen YS, Yang WS, Wu YT (2008) Impaired exercise capacity in diabetic patients after coronary bypass surgery: effects of diastolic and endothelial function. Cardiology 110:191–198PubMedCrossRef Wu YW, Hsu CL, Wang SS, Tsai MW, Chu SH, Chen YS, Yang WS, Wu YT (2008) Impaired exercise capacity in diabetic patients after coronary bypass surgery: effects of diastolic and endothelial function. Cardiology 110:191–198PubMedCrossRef
37.
go back to reference Nichols GA, Gullion CM, Koro CE, Ephross SA, Brown JB (2004) The incidence of congestive heart failure in type 2 diabetes: an update. Diabetes Care 27:1879–1884PubMedCrossRef Nichols GA, Gullion CM, Koro CE, Ephross SA, Brown JB (2004) The incidence of congestive heart failure in type 2 diabetes: an update. Diabetes Care 27:1879–1884PubMedCrossRef
38.
go back to reference Lindsey JB, Cipollone F, Abdullah SM, McGuire DK (2009) Receptor for advanced glycation end-products (RAGE) and soluble RAGE (sRAGE): cardiovascular implications. Diab Vasc Dis Res 6:7–14PubMedCrossRef Lindsey JB, Cipollone F, Abdullah SM, McGuire DK (2009) Receptor for advanced glycation end-products (RAGE) and soluble RAGE (sRAGE): cardiovascular implications. Diab Vasc Dis Res 6:7–14PubMedCrossRef
39.
go back to reference Raposeiras-Roubin S, Rodino-Janeiro BK, Grigorian-Shamagian L, Moure-Gonzalez M, Seoane-Blanco A, Varela-Roman A, Alvarez E, Gonzalez-Juanatey JR (2010) Soluble receptor of advanced glycation end products levels are related to ischaemic aetiology and extent of coronary disease in chronic heart failure patients, independent of advanced glycation end products levels: new roles for soluble RAGE. Eur J Heart Fail 12:1092–1100PubMedCrossRef Raposeiras-Roubin S, Rodino-Janeiro BK, Grigorian-Shamagian L, Moure-Gonzalez M, Seoane-Blanco A, Varela-Roman A, Alvarez E, Gonzalez-Juanatey JR (2010) Soluble receptor of advanced glycation end products levels are related to ischaemic aetiology and extent of coronary disease in chronic heart failure patients, independent of advanced glycation end products levels: new roles for soluble RAGE. Eur J Heart Fail 12:1092–1100PubMedCrossRef
40.
go back to reference Lindsey JB, de Lemos JA, Cipollone F, Ayers CR, Rohatgi A, Morrow DA, Khera A, McGuire DK (2009) Association between circulating soluble receptor for advanced glycation end products and atherosclerosis: observations from the dallas heart study. Diabetes Care 32:1218–1220PubMedCrossRef Lindsey JB, de Lemos JA, Cipollone F, Ayers CR, Rohatgi A, Morrow DA, Khera A, McGuire DK (2009) Association between circulating soluble receptor for advanced glycation end products and atherosclerosis: observations from the dallas heart study. Diabetes Care 32:1218–1220PubMedCrossRef
41.
go back to reference Falcone C, Emanuele E, D’Angelo A, Buzzi MP, Belvito C, Cuccia M, Geroldi D (2005) Plasma levels of soluble receptor for advanced glycation end products and coronary artery disease in nondiabetic men. Arterioscler Thromb Vasc Biol 25:1032–1037PubMedCrossRef Falcone C, Emanuele E, D’Angelo A, Buzzi MP, Belvito C, Cuccia M, Geroldi D (2005) Plasma levels of soluble receptor for advanced glycation end products and coronary artery disease in nondiabetic men. Arterioscler Thromb Vasc Biol 25:1032–1037PubMedCrossRef
42.
go back to reference Ramasamy R, Yan SF, Schmidt AM. Advanced glycation endproducts: from precursors to RAGE: round and round we go. Amino Acids 2010;PMID:20957395 Ramasamy R, Yan SF, Schmidt AM. Advanced glycation endproducts: from precursors to RAGE: round and round we go. Amino Acids 2010;PMID:20957395
44.
go back to reference Zile MR, Brutsaert DL (2002) New concepts in diastolic dysfunction and diastolic heart failure: Part I: diagnosis, prognosis, and measurements of diastolic function. Circulation 105:1387–1393PubMedCrossRef Zile MR, Brutsaert DL (2002) New concepts in diastolic dysfunction and diastolic heart failure: Part I: diagnosis, prognosis, and measurements of diastolic function. Circulation 105:1387–1393PubMedCrossRef
45.
go back to reference Moreo A, Ambrosio G, De Chiara B, Pu M, Tran T, Mauri F, Raman SV (2009) Influence of myocardial fibrosis on left ventricular diastolic function: noninvasive assessment by cardiac magnetic resonance and echo. Circ Cardiovasc Imaging 2:437–443PubMedCrossRef Moreo A, Ambrosio G, De Chiara B, Pu M, Tran T, Mauri F, Raman SV (2009) Influence of myocardial fibrosis on left ventricular diastolic function: noninvasive assessment by cardiac magnetic resonance and echo. Circ Cardiovasc Imaging 2:437–443PubMedCrossRef
46.
go back to reference Hartog JW, Voors AA, Schalkwijk CG, Scheijen J, Smilde TD, Damman K, Bakker SJ, Smit AJ, van Veldhuisen DJ (2007) Clinical and prognostic value of advanced glycationend-products in chronic heart failure. Eur Heart J 28:2879–2885PubMedCrossRef Hartog JW, Voors AA, Schalkwijk CG, Scheijen J, Smilde TD, Damman K, Bakker SJ, Smit AJ, van Veldhuisen DJ (2007) Clinical and prognostic value of advanced glycationend-products in chronic heart failure. Eur Heart J 28:2879–2885PubMedCrossRef
47.
go back to reference Kass DA, Bronzwaer JG, Paulus WJ (2004) What mechanisms underlie diastolic dysfunction in heart failure? Circ Res 94:1533–1542PubMedCrossRef Kass DA, Bronzwaer JG, Paulus WJ (2004) What mechanisms underlie diastolic dysfunction in heart failure? Circ Res 94:1533–1542PubMedCrossRef
48.
go back to reference Zieman SJ, Kass DA (2004) Advanced glycation endproduct crosslinking in the cardiovascular system: potential therapeutic target for cardiovascular disease. Drugs 64:459–470PubMedCrossRef Zieman SJ, Kass DA (2004) Advanced glycation endproduct crosslinking in the cardiovascular system: potential therapeutic target for cardiovascular disease. Drugs 64:459–470PubMedCrossRef
49.
go back to reference Zile MR, Brutsaert DL (2002) New concepts in diastolic dysfunction and diastolic heart failure: part II: causal mechanisms and treatment. Circulation 105:1503–1508PubMedCrossRef Zile MR, Brutsaert DL (2002) New concepts in diastolic dysfunction and diastolic heart failure: part II: causal mechanisms and treatment. Circulation 105:1503–1508PubMedCrossRef
50.
go back to reference Schafer S, Huber J, Wihler C, Rutten H, Busch AE, Linz W (2006) Impaired left ventricular relaxation in type 2 diabetic rats is related to myocardial accumulation of N(epsilon)-(carboxymethyl) lysine. Eur J Heart Fail 8:2–6PubMedCrossRef Schafer S, Huber J, Wihler C, Rutten H, Busch AE, Linz W (2006) Impaired left ventricular relaxation in type 2 diabetic rats is related to myocardial accumulation of N(epsilon)-(carboxymethyl) lysine. Eur J Heart Fail 8:2–6PubMedCrossRef
51.
go back to reference Petrova R, Yamamoto Y, Muraki K, Yonekura H, Sakurai S, Watanabe T, Li H, Takeuchi M, Makita Z, Kato I, Takasawa S, Okamoto H, Imaizumi Y, Yamamoto H (2002) Advanced glycation endproduct-induced calcium handling impairment in mouse cardiac myocytes. J Mol Cell Cardiol 34:1425–1431PubMedCrossRef Petrova R, Yamamoto Y, Muraki K, Yonekura H, Sakurai S, Watanabe T, Li H, Takeuchi M, Makita Z, Kato I, Takasawa S, Okamoto H, Imaizumi Y, Yamamoto H (2002) Advanced glycation endproduct-induced calcium handling impairment in mouse cardiac myocytes. J Mol Cell Cardiol 34:1425–1431PubMedCrossRef
52.
go back to reference Cowburn PJ, Cleland JG, Coats AJ, Komajda M (1998) Risk stratification in chronic heart failure. Eur Heart J 19:696–710PubMedCrossRef Cowburn PJ, Cleland JG, Coats AJ, Komajda M (1998) Risk stratification in chronic heart failure. Eur Heart J 19:696–710PubMedCrossRef
53.
go back to reference Groenveld HF, Januzzi JL, Damman K, van Wijngaarden J, Hillege HL, van Veldhuisen DJ, van der Meer P (2008) Anemia and mortality in heart failure patients a systematic review and meta-analysis. J Am Coll Cardiol 52:818–827PubMedCrossRef Groenveld HF, Januzzi JL, Damman K, van Wijngaarden J, Hillege HL, van Veldhuisen DJ, van der Meer P (2008) Anemia and mortality in heart failure patients a systematic review and meta-analysis. J Am Coll Cardiol 52:818–827PubMedCrossRef
54.
go back to reference Hillege HL, Nitsch D, Pfeffer MA, Swedberg K, McMurray JJ, Yusuf S, Granger CB, Michelson EL, Ostergren J, Cornel JH, de ZD, Pocock S, van Veldhuisen DJ (2006) Renal function as a predictor of outcome in a broad spectrum of patients with heart failure. Circulation 113:671–678PubMedCrossRef Hillege HL, Nitsch D, Pfeffer MA, Swedberg K, McMurray JJ, Yusuf S, Granger CB, Michelson EL, Ostergren J, Cornel JH, de ZD, Pocock S, van Veldhuisen DJ (2006) Renal function as a predictor of outcome in a broad spectrum of patients with heart failure. Circulation 113:671–678PubMedCrossRef
55.
go back to reference Koyama Y, Takeishi Y, Arimoto T, Niizeki T, Shishido T, Takahashi H, Nozaki N, Hirono O, Tsunoda Y, Nitobe J, Watanabe T, Kubota I (2007) High serum level of pentosidine, an advanced glycation end product (AGE), is a risk factor of patients with heart failure. J Card Fail 13:199–206PubMedCrossRef Koyama Y, Takeishi Y, Arimoto T, Niizeki T, Shishido T, Takahashi H, Nozaki N, Hirono O, Tsunoda Y, Nitobe J, Watanabe T, Kubota I (2007) High serum level of pentosidine, an advanced glycation end product (AGE), is a risk factor of patients with heart failure. J Card Fail 13:199–206PubMedCrossRef
56.
go back to reference Koyama Y, Takeishi Y, Niizeki T, Suzuki S, Kitahara T, Sasaki T, Kubota I (2008) Soluble Receptor for advanced glycation end products (RAGE) is a prognostic factor for heart failure. J Card Fail 14:133–139PubMedCrossRef Koyama Y, Takeishi Y, Niizeki T, Suzuki S, Kitahara T, Sasaki T, Kubota I (2008) Soluble Receptor for advanced glycation end products (RAGE) is a prognostic factor for heart failure. J Card Fail 14:133–139PubMedCrossRef
57.
go back to reference Ljungman S, Laragh JH, Cody RJ (1990) Role of the kidney in congestive heart failure. Relationship of cardiac index to kidney function. Drugs 39(Suppl 4):10–21PubMedCrossRef Ljungman S, Laragh JH, Cody RJ (1990) Role of the kidney in congestive heart failure. Relationship of cardiac index to kidney function. Drugs 39(Suppl 4):10–21PubMedCrossRef
58.
go back to reference Stam F, van Guldener C, Schalkwijk CG, ter Wee PM, Donker AJ, Stehouwer CD (2003) Impaired renal function is associated with markers of endothelial dysfunction and increased inflammatory activity. Nephrol Dial Transplant 18:892–898PubMedCrossRef Stam F, van Guldener C, Schalkwijk CG, ter Wee PM, Donker AJ, Stehouwer CD (2003) Impaired renal function is associated with markers of endothelial dysfunction and increased inflammatory activity. Nephrol Dial Transplant 18:892–898PubMedCrossRef
59.
go back to reference Zoccali C, Mallamaci F, Tripepi G (2003) Inflammation and atherosclerosis in end-stage renal disease. Blood Purif 21:29–36PubMedCrossRef Zoccali C, Mallamaci F, Tripepi G (2003) Inflammation and atherosclerosis in end-stage renal disease. Blood Purif 21:29–36PubMedCrossRef
60.
go back to reference Gugliucci A, Bendayan M (1996) Renal fate of circulating advanced glycated end products (AGE): evidence for reabsorption and catabolism of AGE-peptides by renal proximal tubular cells. Diabetologia 39:149–160PubMedCrossRef Gugliucci A, Bendayan M (1996) Renal fate of circulating advanced glycated end products (AGE): evidence for reabsorption and catabolism of AGE-peptides by renal proximal tubular cells. Diabetologia 39:149–160PubMedCrossRef
61.
go back to reference Hartog JW, Smit AJ, van Son WJ, Navis G, Gans RO, Wolffenbuttel BH, de Jong PE (2004) Advanced glycation end products in kidney transplant patients: a putative role in the development of chronic renal transplant dysfunction. Am J Kidney Dis 43:966–975PubMedCrossRef Hartog JW, Smit AJ, van Son WJ, Navis G, Gans RO, Wolffenbuttel BH, de Jong PE (2004) Advanced glycation end products in kidney transplant patients: a putative role in the development of chronic renal transplant dysfunction. Am J Kidney Dis 43:966–975PubMedCrossRef
62.
go back to reference Miyata T, Ueda Y, Horie K, Nangaku M, Tanaka S, Ypersele de Strihou C, Kurokawa K (1998) Renal catabolism of advanced glycation end products: the fate of pentosidine. Kidney Int 53:416–422PubMedCrossRef Miyata T, Ueda Y, Horie K, Nangaku M, Tanaka S, Ypersele de Strihou C, Kurokawa K (1998) Renal catabolism of advanced glycation end products: the fate of pentosidine. Kidney Int 53:416–422PubMedCrossRef
63.
go back to reference Stenvinkel P, Alvestrand A (2002) Inflammation in end-stage renal disease: sources, consequences, and therapy. Semin Dial 15:329–337PubMedCrossRef Stenvinkel P, Alvestrand A (2002) Inflammation in end-stage renal disease: sources, consequences, and therapy. Semin Dial 15:329–337PubMedCrossRef
64.
go back to reference Basta G, Lazzerini G, Massaro M, Simoncini T, Tanganelli P, Fu C, Kislinger T, Stern DM, Schmidt AM, De Caterina R (2002) Advanced glycation end products activate endothelium through signal- transduction receptor RAGE: a mechanism for amplification of inflammatory responses. Circulation 105:816–822PubMedCrossRef Basta G, Lazzerini G, Massaro M, Simoncini T, Tanganelli P, Fu C, Kislinger T, Stern DM, Schmidt AM, De Caterina R (2002) Advanced glycation end products activate endothelium through signal- transduction receptor RAGE: a mechanism for amplification of inflammatory responses. Circulation 105:816–822PubMedCrossRef
66.
go back to reference Vlassara H, Striker LJ, Teichberg S, Fuh H, Li YM, Steffes M (1994) Advanced glycation end products induce glomerular sclerosis and albuminuria in normal rats. Proc Natl Acad Sci USA 91:11704–11708PubMedCrossRef Vlassara H, Striker LJ, Teichberg S, Fuh H, Li YM, Steffes M (1994) Advanced glycation end products induce glomerular sclerosis and albuminuria in normal rats. Proc Natl Acad Sci USA 91:11704–11708PubMedCrossRef
67.
go back to reference Yamada K, Miyahara Y, Hamaguchi K, Nakayama M, Nakano H, Nozaki O, Miura Y, Suzuki S, Tuchida H, Mimura N (1994) Immunohistochemical study of human advanced glycosylation end-products (AGE) in chronic renal failure. Clin Nephrol 42:354–361PubMed Yamada K, Miyahara Y, Hamaguchi K, Nakayama M, Nakano H, Nozaki O, Miura Y, Suzuki S, Tuchida H, Mimura N (1994) Immunohistochemical study of human advanced glycosylation end-products (AGE) in chronic renal failure. Clin Nephrol 42:354–361PubMed
68.
go back to reference Zoccali C, Mallamaci F, Tripepi G (2000) AGEs and carbonyl stress: potential pathogenetic factors of long-term uraemic complications. Nephrol Dial Transplant 15(Suppl 2):7–11PubMedCrossRef Zoccali C, Mallamaci F, Tripepi G (2000) AGEs and carbonyl stress: potential pathogenetic factors of long-term uraemic complications. Nephrol Dial Transplant 15(Suppl 2):7–11PubMedCrossRef
69.
go back to reference Hartog JW, de Vries AP, Lutgers HL, Meerwaldt R, Huisman RM, van Son WJ, de Jong PE, Smit AJ (2005) Accumulation of advanced glycation end products, measured as skin autofluorescence, in renal disease. Ann N Y Acad Sci 1043:299–307PubMedCrossRef Hartog JW, de Vries AP, Lutgers HL, Meerwaldt R, Huisman RM, van Son WJ, de Jong PE, Smit AJ (2005) Accumulation of advanced glycation end products, measured as skin autofluorescence, in renal disease. Ann N Y Acad Sci 1043:299–307PubMedCrossRef
70.
go back to reference Al Ahmad A, Rand WM, Manjunath G, Konstam MA, Salem DN, Levey AS, Sarnak MJ (2001) Reduced kidney function and anemia as risk factors for mortality in patients with left ventricular dysfunction. J Am Coll Cardiol 38:955–962PubMedCrossRef Al Ahmad A, Rand WM, Manjunath G, Konstam MA, Salem DN, Levey AS, Sarnak MJ (2001) Reduced kidney function and anemia as risk factors for mortality in patients with left ventricular dysfunction. J Am Coll Cardiol 38:955–962PubMedCrossRef
71.
go back to reference Damman K, Navis G, Smilde TD, Voors AA, van der Bij W, van Veldhuisen DJ, Hillege HL (2007) Decreased cardiac output, venous congestion and the association with renal impairment in patients with cardiac dysfunction. Eur J Heart Fail 9:872–878PubMedCrossRef Damman K, Navis G, Smilde TD, Voors AA, van der Bij W, van Veldhuisen DJ, Hillege HL (2007) Decreased cardiac output, venous congestion and the association with renal impairment in patients with cardiac dysfunction. Eur J Heart Fail 9:872–878PubMedCrossRef
72.
go back to reference Dries DL, Exner DV, Domanski MJ, Greenberg B, Stevenson LW (2000) The prognostic implications of renal insufficiency in asymptomatic and symptomatic patients with left ventricular systolic dysfunction. J Am Coll Cardiol 35:681–689PubMedCrossRef Dries DL, Exner DV, Domanski MJ, Greenberg B, Stevenson LW (2000) The prognostic implications of renal insufficiency in asymptomatic and symptomatic patients with left ventricular systolic dysfunction. J Am Coll Cardiol 35:681–689PubMedCrossRef
73.
go back to reference Hartog JW, Gross S, Oterdoom LH, van Ree RM, de Vries AP, Smit AJ, Schouten JP, Nawroth PP, Gans RO, van Son WJ, Bierhaus A, Bakker SJ (2009) Skin-autofluorescence is an independent predictor of graft loss in renal transplant recipients. Transplantation 87:1069–1077PubMedCrossRef Hartog JW, Gross S, Oterdoom LH, van Ree RM, de Vries AP, Smit AJ, Schouten JP, Nawroth PP, Gans RO, van Son WJ, Bierhaus A, Bakker SJ (2009) Skin-autofluorescence is an independent predictor of graft loss in renal transplant recipients. Transplantation 87:1069–1077PubMedCrossRef
74.
go back to reference Roberts MA, Thomas MC, Fernando D, Macmillan N, Power DA, Ierino FL (2006) Low molecular weight advanced glycation end products predict mortality in asymptomatic patients receiving chronic haemodialysis. Nephrol Dial Transplant 21:1611–1617PubMedCrossRef Roberts MA, Thomas MC, Fernando D, Macmillan N, Power DA, Ierino FL (2006) Low molecular weight advanced glycation end products predict mortality in asymptomatic patients receiving chronic haemodialysis. Nephrol Dial Transplant 21:1611–1617PubMedCrossRef
75.
go back to reference Schwedler SB, Metzger T, Schinzel R, Wanner C (2002) Advanced glycation end products and mortality in hemodialysis patients. Kidney Int 62:301–310PubMedCrossRef Schwedler SB, Metzger T, Schinzel R, Wanner C (2002) Advanced glycation end products and mortality in hemodialysis patients. Kidney Int 62:301–310PubMedCrossRef
76.
go back to reference Wagner Z, Molnar M, Molnar GA, Tamasko M, Laczy B, Wagner L, Csiky B, Heidland A, Nagy J, Wittmann I (2006) Serum carboxymethyllysine predicts mortality in hemodialysis patients. Am J Kidney Dis 47:294–300PubMedCrossRef Wagner Z, Molnar M, Molnar GA, Tamasko M, Laczy B, Wagner L, Csiky B, Heidland A, Nagy J, Wittmann I (2006) Serum carboxymethyllysine predicts mortality in hemodialysis patients. Am J Kidney Dis 47:294–300PubMedCrossRef
77.
go back to reference Meerwaldt R, Hartog JW, Graaff R, Huisman RJ, Links TP, den Hollander NC, Thorpe SR, Baynes JW, Navis G, Gans RO, Smit AJ (2005) Skin autofluorescence, a measure of cumulative metabolic stress and advanced glycation end products, predicts mortality in hemodialysis patients. J Am Soc Nephrol 16:3687–3693PubMedCrossRef Meerwaldt R, Hartog JW, Graaff R, Huisman RJ, Links TP, den Hollander NC, Thorpe SR, Baynes JW, Navis G, Gans RO, Smit AJ (2005) Skin autofluorescence, a measure of cumulative metabolic stress and advanced glycation end products, predicts mortality in hemodialysis patients. J Am Soc Nephrol 16:3687–3693PubMedCrossRef
78.
go back to reference Miyata T, van Ypersele dS (2003) Angiotensin II receptor blockers and angiotensin converting enzyme inhibitors: implication of radical scavenging and transition metal chelation in inhibition of advanced glycation end product formation. Arch Biochem Biophys 419:50–54PubMedCrossRef Miyata T, van Ypersele dS (2003) Angiotensin II receptor blockers and angiotensin converting enzyme inhibitors: implication of radical scavenging and transition metal chelation in inhibition of advanced glycation end product formation. Arch Biochem Biophys 419:50–54PubMedCrossRef
79.
go back to reference Monacelli F, Poggi A, Storace D, Durante A, Traverso N, Viviani GL, Odetti P (2006) Effects of valsartan therapy on protein glycoxidation. Metabolism 55:1619–1624PubMedCrossRef Monacelli F, Poggi A, Storace D, Durante A, Traverso N, Viviani GL, Odetti P (2006) Effects of valsartan therapy on protein glycoxidation. Metabolism 55:1619–1624PubMedCrossRef
80.
go back to reference Saisho Y, Komiya N, Hirose H (2006) Effect of valsartan, an angiotensin II receptor blocker, on markers of oxidation and glycation in Japanese type 2 diabetic subjects: Blood pressure-independent effect of valsartan. Diabetes Res Clin Pract 74:201–203PubMedCrossRef Saisho Y, Komiya N, Hirose H (2006) Effect of valsartan, an angiotensin II receptor blocker, on markers of oxidation and glycation in Japanese type 2 diabetic subjects: Blood pressure-independent effect of valsartan. Diabetes Res Clin Pract 74:201–203PubMedCrossRef
81.
go back to reference Wagenaar LJ, Voors AA, Buikema H, van Gilst WH (2002) Angiotensin receptors in the cardiovascular system. Can J Cardiol 18:1331–1339PubMed Wagenaar LJ, Voors AA, Buikema H, van Gilst WH (2002) Angiotensin receptors in the cardiovascular system. Can J Cardiol 18:1331–1339PubMed
82.
go back to reference Hartog JW, van de Wal RM, Schalkwijk CG, Miyata T, Jaarsma W, Plokker HW, van Wijk LM, Smit AJ, van Veldhuisen DJ, Voors AA (2010) Advanced glycation end-products, anti-hypertensive treatment and diastolic function in patients with hypertension and diastolic dysfunction. Eur J Heart Fail 12:397–403PubMedCrossRef Hartog JW, van de Wal RM, Schalkwijk CG, Miyata T, Jaarsma W, Plokker HW, van Wijk LM, Smit AJ, van Veldhuisen DJ, Voors AA (2010) Advanced glycation end-products, anti-hypertensive treatment and diastolic function in patients with hypertension and diastolic dysfunction. Eur J Heart Fail 12:397–403PubMedCrossRef
83.
go back to reference Willemsen S, Hartog JW, Hummel YM, Posma JL, van Wijk LM, van Veldhuisen DJ, Voors AA (2010) Effects of alagebrium, an advanced glycation end-product breaker, in patients with chronic heart failure: study design and baseline characteristics of the BENEFICIAL trial. Eur J Heart Fail 12:294–300PubMedCrossRef Willemsen S, Hartog JW, Hummel YM, Posma JL, van Wijk LM, van Veldhuisen DJ, Voors AA (2010) Effects of alagebrium, an advanced glycation end-product breaker, in patients with chronic heart failure: study design and baseline characteristics of the BENEFICIAL trial. Eur J Heart Fail 12:294–300PubMedCrossRef
Metadata
Title
Advanced glycation end-products, a pathophysiological pathway in the cardiorenal syndrome
Authors
Suzan Willemsen
Jasper W. L. Hartog
M. Rebecca Heiner-Fokkema
Dirk J. van Veldhuisen
Adriaan A. Voors
Publication date
01-03-2012
Publisher
Springer US
Published in
Heart Failure Reviews / Issue 2/2012
Print ISSN: 1382-4147
Electronic ISSN: 1573-7322
DOI
https://doi.org/10.1007/s10741-010-9225-z

Other articles of this Issue 2/2012

Heart Failure Reviews 2/2012 Go to the issue