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The role of advanced glycation end products in patogenesis of diabetic nephropathy

https://doi.org/10.14341/DM12784

Abstract

Diabetes mellitus (DM) and chronic kidney disease are the diseases that have exceeded epidemic thresholds in terms of prevalence all over the world. That made it possible to classify them as non-communicable epidemics of the XXI century. Diabetic nephropathy (DN) is implicated with high levels of disablement and mortality. Advanced glycation end products (AGE) play a key role in the progression of DN. Increased formation of AGE occurs due to hyperglycemia under the conditions of diabetes. Moreover, there are additional factors in DN that increase the elaboration of AGE, such as high levels of oxidative stress and decreased renal clearance which slows down the AGE excretion. Both immediate effects of AGE and interaction of AGE with its cell-bound receptor (RAGE) result in a сascade of events that lead to further progression of DN. Thus, the research of the new therapeutic approaches targeted on the AGE-RAGE system is of great interest to slow progression of DN and improve the prognosis.

About the Authors

A. O. Gavrilova
Endocrinology Research Centre
Russian Federation

Alina O. Gavrilova, PhD student; eLibrary SPIN: 8814-0121.

11 Dm. Ulyanova street, 117036 Moscow


Competing Interests:

no



A. S. Severina
Endocrinology Research Centre
Russian Federation

Anastasia S. Severina - MD, PhD, senior research associate; eLibrary SPIN: 3182-9510

Moscow


Competing Interests:

no



M. S. Shamhalova
Endocrinology Research Centre
Russian Federation

Minara S. Shamhalova - MD, PhD; eLibrary SPIN: 4942-5481

Moscow


Competing Interests:

no



M. V. Shestakova
Endocrinology Research Centre
Russian Federation

Marina V. Shestakova - MD, PhD, Professor; eLibrary SPIN: 7584-7015

Moscow


Competing Interests:

no



References

1. Kumar Pasupulati A, Chitra PS, Reddy GB. Advanced glycation end products mediated cellular and molecular events in the pathology of diabetic nephropathy. Biomol Concepts. 2016;7(5-6):293-309. doi: https://doi.org/10.1515/bmc-2016-0021

2. Bettiga A, Fiorio F, Di Marco F, et al. The Modern Western Diet Rich in Advanced Glycation End-Products (AGEs): An Overview of Its Impact on Obesity and Early Progression of Renal Pathology. Nutrients. 2019;11(8):1748. doi: https://doi.org/10.3390/nu11081748

3. Bucala R, Cerami A. Advanced glycosylation: chemistry, biology, and implications for diabetes and aging. Adv Pharmacol. 1992;23:1-34. doi: https://doi.org/10.1016/s1054-3589(08)60961-8

4. Miyata T, Ueda Y, Yamada Y, et al. Accumulation of carbonyls accelerates the formation of pentosidine, an advanced glycation end product: carbonyl stress in uremia. J Am Soc Nephrol. 1998;9(12):2349-56. doi: https://doi.org/10.1681/ASN.V9122349

5. Maillard L. Action of amino acids on sugars. Formation of melanoidins in a methodical way. Compt Rend. 1912;154:66-68.

6. Monnier VM, Nagaraj RH, Portero-Otin M, et al. Structure of advanced Maillard reaction products and their pathological role. Nephrol Dial Transplant. 1996;11 Suppl 5:20-6. doi: https://doi.org/10.1093/ndt/11.supp5.20

7. Wolff SP, Dean RT. Glucose autoxidation and protein modification. The potential role of ‘autoxidative glycosylation’ in diabetes. Biochem J. 1987;245(1):243-50. doi: https://doi.org/10.1042/bj2450243

8. Namiki M. Chemistry of Maillard reactions: recent studies on the browning reaction mechanism and the development of antioxidants and mutagens. Adv Food Res. 1988;32:115-84. doi: https://doi.org/10.1016/s0065-2628(08)60287-6

9. Hodge JE, Rist CE. The Amadori Rearrangement under New Conditions and its Significance for Non-enzymatic Browning Reactions2. J Am Chem Soc 1953; 75: 316-22. Nutrients. 2010;2:1247-1265. doi: https://doi.org/10.1021/ja01098a019

10. Piperi C, Adamopoulos C, Dalagiorgou G, et al. Crosstalk between advanced glycation and endoplasmic reticulum stress: emerging therapeutic targeting for metabolic diseases. J Clin Endocrinol Metab. 2012;97(7):2231-42. doi: https://doi.org/10.1210/jc.2011-3408

11. Dedov II, Shestakova MV. The metabolic memory phenomenon in predicting a risk for vascular complications in diabetes mellitus. Terapevticheskii Arkhiv (Ter. Arkh.). (In Russ.). doi: https://doi.org/10.17116/terarkh201587104-10

12. Bohlender JM, Franke S, Stein G, et al. Advanced glycation end products and the kidney. Am J Physiol Renal Physiol. 2005;289(4):F645-59. doi: https://doi.org/10.1152/ajprenal.00398.2004

13. Arsov S, Graaff R, van Oeveren W, et al. Advanced glycation end-products and skin autofluorescence in end-stage renal disease: a review. Clin Chem Lab Med. 2014;52(1):11-20. doi: https://doi.org/10.1515/cclm-2012-0832

14. Kandarakis SA, Piperi C, Topouzis F, et al. Emerging role of advanced glycation-end products (AGEs) in the pathobiology of eye diseases. Prog Retin Eye Res. 2014;42:85-102. doi: https://doi.org/10.1016/j.preteyeres.2014.05.002

15. Forbes JM, Yee LT, Thallas V, et al. Advanced glycation end product interventions reduce diabetes-accelerated atherosclerosis. Diabetes. 2004;53(7):1813-23. doi: https://doi.org/10.2337/diabetes.53.7.1813

16. Yamamoto Y, Doi T, Kato I, et al. Receptor for advanced glycation end products is a promising target of diabetic nephropathy. Ann N Y Acad Sci. 2005;1043:562-6. doi: https://doi.org/10.1196/annals.1333.064

17. Yamagishi S, Nakamura K, Inoue H, et al. Serum or cerebrospinal fluid levels of glyceraldehyde-derived advanced glycation end products (AGEs) may be a promising biomarker for early detection of Alzheimer’s disease. Med Hypotheses. 2005;64(6):1205-7. doi: https://doi.org/10.1016/j.mehy.2005.01.016

18. Angeloni C, Zambonin L, Hrelia S. Role of methylglyoxal in Alzheimer’s disease. Biomed Res Int. 2014;2014:238485. doi: https://doi.org/10.1155/2014/238485

19. Chilelli NC, Burlina S, Lapolla A. AGEs, rather than hyperglycemia, are responsible for microvascular complications in diabetes: a «glycoxidation-centric» point of view. Nutr Metab Cardiovasc Dis. 2013;23(10):913-9. doi: https://doi.org/10.1016/j.numecd.2013.04.004

20. Makita Z, Radoff S, Rayfield EJ, et al. Advanced glycosylation end products in patients with diabetic nephropathy. N Engl J Med. 1991;325(12):836-42. doi: https://doi.org/10.1056/NEJM199109193251202

21. Loughrey CM, Young IS, Lightbody JH, et al. Oxidative stress in haemodialysis. QJM. 1994;87(11):679-83. PMID: 7820542

22. Witko-Sarsat V, Friedlander M, Capeillère-Blandin C, et al. Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney Int. 1996;49(5):1304-13. doi: https://doi.org/10.1038/ki.1996.186

23. Dozio E, Vettoretti S, Caldiroli L, et al. Advanced Glycation End Products (AGE) and Soluble Forms of AGE Receptor: Emerging Role as Mortality Risk Factors in CKD. Biomedicines. 2020;8(12):638. doi: https://doi.org/10.3390/biomedicines8120638

24. Vlassara H, Striker LJ, Teichberg S, et al. Advanced glycation end products induce glomerular sclerosis and albuminuria in normal rats. Proc Natl Acad Sci U S A. 1994;91(24):11704-8. doi: https://doi.org/10.1073/pnas.91.24.11704

25. Yang CW, Vlassara H, Peten EP, et al. Advanced glycation end products up-regulate gene expression found in diabetic glomerular disease. Proc Natl Acad Sci U S A. 1994;91(20):9436-40. doi: https://doi.org/10.1073/pnas.91.20.9436

26. Tsilibary EC, Charonis AS, Reger LA, et al. The effect of nonenzymatic glucosylation on the binding of the main noncollagenous NC1 domain to type IV collagen. J Biol Chem. 1988;263(9):4302-8. PMID: 3346249

27. Charonis AS, Reger LA, Dege JE, et al. Laminin alterations after in vitro nonenzymatic glycosylation. Diabetes. 1990;39(7):807-14. doi: https://doi.org/10.2337/diab.39.7.807. PMID: 2113013.

28. Yamagishi S, Matsui T. Advanced glycation end products, oxidative stress and diabetic nephropathy. Oxid Med Cell Longev. 2010;3(2):101-8. doi: https://doi.org/10.4161/oxim.3.2.11148

29. Ziyadeh FN, Hoffman BB, Han DC, et al. Long-term prevention of renal insufficiency, excess matrix gene expression, and glomerular mesangial matrix expansion by treatment with monoclonal antitransforming growth factor-beta antibody in db/db diabetic mice. Proc Natl Acad Sci U S A. 2000;97(14):8015-20. doi: https://doi.org/10.1073/pnas.120055097

30. Silbiger S, Crowley S, Shan Z, et al. Nonenzymatic glycation of mesangial matrix and prolonged exposure of mesangial matrix to elevated glucose reduces collagen synthesis and proteoglycan charge. Kidney Int. 1993;43(4):853-64. doi: https://doi.org/10.1038/ki.1993.120

31. Kushwaha K, Sharma S, Gupta J. Metabolic memory and diabetic nephropathy: Beneficial effects of natural epigenetic modifiers. Biochimie. 2020;170:140-151. doi: https://doi.org/10.1016/j.biochi.2020.01.007

32. Genuth S, Sun W, Cleary P, et al. DCCT Skin Collagen Ancillary Study Group. Glycation and carboxymethyllysine levels in skin collagen predict the risk of future 10-year progression of diabetic retinopathy and nephropathy in the diabetes control and complications trial and epidemiology of diabetes interventions and complications participants with type 1 diabetes. Diabetes. 2005;54(11):3103-11. doi: https://doi.org/10.2337/diabetes.54.11.3103

33. Ramasamy R, Yan SF, Schmidt AM. Receptor for AGE (RAGE): signaling mechanisms in the pathogenesis of diabetes and its complications. Ann N Y Acad Sci. 2011;1243:88-102. doi: https://doi.org/10.1111/j.1749-6632.2011.06320.x

34. Fukami K, Taguchi K, Yamagishi S, et al. Receptor for advanced glycation endproducts and progressive kidney disease. Curr Opin Nephrol Hypertens. 2015;24(1):54-60. doi: https://doi.org/10.1097/MNH.0000000000000091

35. Wautier MP, Chappey O, Corda S, et al. Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am J Physiol Endocrinol Metab. 2001;280(5):E685-94. doi: https://doi.org/10.1152/ajpendo.2001.280.5.E685

36. Hofmann MA, Drury S, Fu C, et al. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell. 1999;97(7):889-901. doi: https://doi.org/10.1016/s0092-8674(00)80801-6

37. Yamamoto Y, Kato I, Doi T, et al. Development and prevention of advanced diabetic nephropathy in RAGE-overexpressing mice. J Clin Invest. 2001;108(2):261-8. doi: https://doi.org/10.1172/JCI11771

38. Shankland SJ. The podocyte’s response to injury: role in proteinuria and glomerulosclerosis. Kidney Int. 2006;69(12):2131-47. doi: https://doi.org/10.1038/sj.ki.5000410

39. Busch M, Franke S, Rüster C, et al. Advanced glycation end-products and the kidney. Eur J Clin Invest. 2010;40(8):742-55. doi: https://doi.org/10.1111/j.1365-2362.2010.02317.x

40. Striker LJ, Striker GE. Administration of AGEs in vivo induces extracellular matrix gene expression. Nephrol Dial Transplant. 1996;11 Suppl 5:62-5. doi: https://doi.org/10.1093/ndt/11.supp5.62

41. Li Y, Kang YS, Dai C, et al. Epithelial-to-mesenchymal transition is a potential pathway leading to podocyte dysfunction and proteinuria. Am J Pathol. 2008;172(2):299-308. doi: https://doi.org/10.2353/ajpath.2008.070057

42. Kumar PA, Welsh GI, Raghu G, et al. Carboxymethyl lysine induces EMT in podocytes through transcription factor ZEB2: Implications for podocyte depletion and proteinuria in diabetes mellitus. Arch Biochem Biophys. 2016;590:10-19. doi: https://doi.org/10.1016/j.abb.2015.11.003

43. Schiffer M, Bitzer M, Roberts IS, et al. Apoptosis in podocytes induced by TGF-beta and Smad7. J Clin Invest. 2001;108(6):807-16. doi: https://doi.org/10.1172/JCI12367

44. Bondeva T, Rüster C, Franke S, et al. Advanced glycation end-products suppress neuropilin-1 expression in podocytes. Kidney Int. 2009;75(6):605-16. doi: https://doi.org/10.1038/ki.2008.603

45. López-Díez R, Rastrojo A, Villate O, et al. Complex tissue-specific patterns and distribution of multiple RAGE splice variants in different mammals. Genome Biol Evol. 2013;5(12):2420-35. doi: https://doi.org/10.1093/gbe/evt188

46. Tam XH, Shiu SW, Leng L, et al. Enhanced expression of receptor for advanced glycation end-products is associated with low circulating soluble isoforms of the receptor in Type 2 diabetes. Clin Sci (Lond). 2011;120(2):81-9. doi: https://doi.org/10.1042/CS20100256

47. Geroldi D, Falcone C, Emanuele E, et al. Decreased plasma levels of soluble receptor for advanced glycation end-products in patients with essential hypertension. J Hypertens. 2005;23(9):1725-9. doi: https://doi.org/10.1097/01.hjh.0000177535.45785.64

48. Prasad K, Mishra M. Do Advanced Glycation End Products and Its Receptor Play a Role in Pathophysiology of Hypertension? Int J Angiol. 2017;26(1):1-11. doi: https://doi.org/10.1055/s-0037-1598183

49. McNair ED, Wells CR, Qureshi AM, et al. Low levels of soluble receptor for advanced glycation end products in non-ST elevation myocardial infarction patients. Int J Angiol. 2009;18(4):187-92. doi: https://doi.org/10.1055/s-0031-1278352

50. Basta G, Leonardis D, Mallamaci F, et al. Circulating soluble receptor of advanced glycation end product inversely correlates with atherosclerosis in patients with chronic kidney disease. Kidney Int. 2010;77(3):225-31. doi: https://doi.org/10.1038/ki.2009.419

51. Kalousová M, Hodková M, Kazderová M, et al. Soluble receptor for advanced glycation end products in patients with decreased renal function. Am J Kidney Dis. 2006;47(3):406-11. doi: https://doi.org/10.1053/j.ajkd.2005.12.028

52. Kim JK, Park S, Lee MJ, et al. Plasma levels of soluble receptor for advanced glycation end products (sRAGE) and proinflammatory ligand for RAGE (EN-RAGE) are associated with carotid atherosclerosis in patients with peritoneal dialysis. Atherosclerosis. 2012;220(1):208-14. doi: https://doi.org/10.1016/j.atherosclerosis.2011.07.115

53. Hartog JW, de Vries AP, Lutgers HL, et al. Accumulation of advanced glycation end products, measured as skin autofluorescence, in renal disease. Ann N Y Acad Sci. 2005;1043:299-307. doi: https://doi.org/10.1196/annals.1333.037

54. Renard C, Chappey O, Wautier MP, et al. Recombinant advanced glycation end product receptor pharmacokinetics in normal and diabetic rats. Mol Pharmacol. 1997;52(1):54-62. doi: https://doi.org/10.1124/mol.52.1.54

55. Linden E, Cai W, He JC, et al. Endothelial dysfunction in patients with chronic kidney disease results from advanced glycation end products (AGE)-mediated inhibition of endothelial nitric oxide synthase through RAGE activation. Clin J Am Soc Nephrol. 2008;3(3):691-8. doi: https://doi.org/10.2215/CJN.04291007

56. Isoyama N, Leurs P, Qureshi AR, et al. Plasma S100A12 and soluble receptor of advanced glycation end product levels and mortality in chronic kidney disease Stage 5 patients. Nephrol Dial Transplant. 2015;30(1):84-91. doi: https://doi.org/10.1093/ndt/gfu259

57. Wadén JM, Dahlström EH, Elonen N, et al. Soluble receptor for AGE in diabetic nephropathy and its progression in Finnish individuals with type 1 diabetes. Diabetologia. 2019;62(7):1268-1274. doi: https://doi.org/10.1007/s00125-019-4883-4

58. Prasad K. Is there any evidence that AGE/sRAGE is a universal biomarker/risk marker for diseases? Mol Cell Biochem. 2019;451(1-2):139-144. doi: https://doi.org/10.1007/s11010-018-3400-2

59. Chiang KH, Chen JW, Huang SS, et al. The ratio of AGE to sRAGE independently associated with albuminuria in hypertensive patients. BMC Endocr Disord. 2018;18(1):84. doi: https://doi.org/10.1186/s12902-018-0306-7

60. Dozio E, Ambrogi F, de Cal M, et al. Role of the Soluble Receptor for Advanced Glycation End Products (sRAGE) as a Prognostic Factor for Mortality in Hemodialysis and Peritoneal Dialysis Patients. Mediators Inflamm. 2018;2018:1347432. doi: https://doi.org/10.1155/2018/1347432

61. Baragetti I, Norata GD, Sarcina C, et al. -374 T/A RAGE polymorphism is associated with chronic kidney disease progression in subjects affected by nephrocardiovascular disease. PLoS One. 2013;8(4):e60089. doi: https://doi.org/10.1371/journal.pone.0060089

62. Tan AL, Forbes JM, Cooper ME. AGE, RAGE, and ROS in diabetic nephropathy. Semin Nephrol. 2007;27(2):130-43. doi: https://doi.org/10.1016/j.semnephrol.2007.01.006

63. Ott C, Jacobs K, Haucke E, et al. Role of advanced glycation end products in cellular signaling. Redox Biol. 2014;2:411-29. doi: https://doi.org/10.1016/j.redox.2013.12.016

64. Nakashima A, Carrero JJ, Qureshi AR, et al. Effect of circulating soluble receptor for advanced glycation end products (sRAGE) and the proinflammatory RAGE ligand (EN-RAGE, S100A12) on mortality in hemodialysis patients. Clin J Am Soc Nephrol. 2010;5(12):2213-9. doi: https://doi.org/10.2215/CJN.03360410

65. Choi BH, Ro H, Jung ES, et al. Circulating S100A12 Levels Are Associated with Progression of Abdominal Aortic Calcification in Hemodialysis Patients. PLoS One. 2016;11(2):e0150145. doi: https://doi.org/10.1371/journal.pone.0150145

66. Yan L, Bjork P, Butuc R, et al. Beneficial effects of quinoline-3-carboxamide (ABR-215757) on atherosclerotic plaque morphology in S100A12 transgenic ApoE null mice. Atherosclerosis. 2013;228(1):69-79. doi: https://doi.org/10.1016/j.atherosclerosis.2013.02.023

67. Rahbar S, Natarajan R, Yerneni K, et al. Evidence that pioglitazone, metformin and pentoxifylline are inhibitors of glycation. Clin Chim Acta. 2000;301(1-2):65-77. doi: https://doi.org/10.1016/s0009-8981(00)00327-2

68. Kanazawa I, Yamamoto M, Yamaguchi T, et al. Effects of metformin and pioglitazone on serum pentosidine levels in type 2 diabetes mellitus. Exp Clin Endocrinol Diabetes. 2011;119(6):362-5. doi: https://doi.org/10.1055/s-0030-1267953

69. Zhang SS, Wu Z, Zhang Z, Xiong ZY, Chen H, Huang QB. Glucagon-like peptide-1 inhibits the receptor for advanced glycation endproducts to prevent podocyte apoptosis induced by advanced oxidative protein products. Biochem Biophys Res Commun. 2017;482(4):1413-1419. doi: https://doi.org/10.1016/j.bbrc.2016.12.050

70. Forbes JM, Cooper ME, Thallas V, et al. Reduction of the accumulation of advanced glycation end products by ACE inhibition in experimental diabetic nephropathy. Diabetes. 2002;51(11):3274-82. doi: https://doi.org/10.2337/diabetes.51.11.3274

71. Ishibashi Y, Yamagishi S, Matsui T, et al. Pravastatin inhibits advanced glycation end products (AGEs)-induced proximal tubular cell apoptosis and injury by reducing receptor for AGEs (RAGE) level. Metabolism. 2012;61(8):1067-72. doi: https://doi.org/10.1016/j.metabol.2012.01.006

72. Xu L, Zang P, Feng B, et al. Atorvastatin inhibits the expression of RAGE induced by advanced glycation end products on aortas in healthy Sprague-Dawley rats. Diabetol Metab Syndr. 2014;6(1):102. doi: https://doi.org/10.1186/1758-5996-6-102

73. Okamoto T, Yamagishi S, Inagaki Y, et al. Angiogenesis induced by advanced glycation end products and its prevention by cerivastatin. FASEB J. 2002;16(14):1928-30. doi: https://doi.org/10.1096/fj.02-0030fje

74. Sung JY, Chung W, Kim AJ, et al. Calcitriol treatment increases serum levels of the soluble receptor of advanced glycation end products in hemodialysis patients with secondary hyperparathyroidism. Tohoku J Exp Med. 2013;230(1):59-66. doi: https://doi.org/10.1620/tjem.230.59

75. Vlassara H, Uribarri J, Cai W, et al. Effects of sevelamer on HbA1c, inflammation, and advanced glycation end products in diabetic kidney disease. Clin J Am Soc Nephrol. 2012;7(6):934-42. doi: https://doi.org/10.2215/CJN.12891211

76. Huang K, Huang J, Xie X, et al. Sirt1 resists advanced glycation end products-induced expressions of fibronectin and TGF-β1 by activating the Nrf2/ARE pathway in glomerular mesangial cells. Free Radic Biol Med. 2013;65:528-540. doi: https://doi.org/10.1016/j.freeradbiomed.2013.07.029

77. Hong Q, Zhang L, Das B, et al. Increased podocyte Sirtuin-1 function attenuates diabetic kidney injury. Kidney Int. 2018;93(6):1330-1343. doi: https://doi.org/10.1016/j.kint.2017.12.008

78. Matsui T, Higashimoto Y, Nishino Y, et al. RAGE-Aptamer Blocks the Development and Progression of Experimental Diabetic Nephropathy. Diabetes. 2017;66(6):1683-1695. doi: https://doi.org/10.2337/db16-1281

79. Candido R, Forbes JM, Thomas MC, et al. A breaker of advanced glycation end products attenuates diabetes-induced myocardial structural changes. Circ Res. 2003;92(7):785-92. doi: https://doi.org/10.1161/01.RES.0000065620.39919.20


Supplementary files

1. Figure 1. Mechanism of formation of advanced glycation end products (AGE). A - classic reaction of AGE formation (Maillard reaction); B - AGE formation reactions due to the transformation of intermediate compounds formed during the Maillard reaction. Adapted from [1].
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2. Figure 2. Different interactions between AGE and RAGE and their associated effects on diabetic nephropathy (DN): AGE - glycation end products; RAGE - AGE receptor; sRAGE, soluble RAGE; other AGE receptors: AGE-R1 - oligosaccharyltransferase-48; AGE-R2 - 80 K-H phosphoprotein; AGE-R3 - galectin-3; EN-RAGE, also known as S100A12, RAGE ligand; TGF-β1 - transforming growth factor-β1; ZEB2 (zinc finger E-box binding homeobox 2) is a transcription factor of the zinc finger family that controls the epithelial-mesenchymal transition; NF-kB - nuclear factor-kappa B.
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Gavrilova A.O., Severina A.S., Shamhalova M.S., Shestakova M.V. The role of advanced glycation end products in patogenesis of diabetic nephropathy. Diabetes mellitus. 2021;24(5):461-469. (In Russ.) https://doi.org/10.14341/DM12784

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