Preview

Problems of Endocrinology

Advanced search

The role of glycation end products in the development and progression of diabetic neuroarthropathy

https://doi.org/10.14341/probl12778

Abstract

Diabetic neuroarthropathy (DNOAP, Charcot’s foot) is a serious complication of diabetes mellitus, the genesis of which is not fully understood. In most cases, this pathology is diagnosed late, which leads to the development of severe deformities of the foot, up to the loss of support ability of the limb. There is no single hypothesis for the formation of Charcot’s foot, but there are factors predisposing to its development, as well as a few likely provoking events. Excessive formation and accumulation of end products of glycation may play an important role in the pathogenesis of this complication of diabetes. End products of glycation (AGE) are a variety of compounds formed as a result of a non-enzymatic reaction between carbohydrates and free amino groups of proteins, lipids and nucleic acids. There are various factors that lead to the accumulation of AGE in the human body. Allocate endogenous and exogenous factors. The former include certain diseases, such as diabetes mellitus, renal failure, which accelerate glycation processes. Exogenous factors leading to the formation of lipo-oxidation and glyco-oxidation products include tobacco smoke and prolonged heat treatment of food.

This review provides information on the role of glycation end products in the development and progression of complications in patients with diabetes mellitus.

About the Authors

M. M. Kalandiya
Endocrinology Research Centre
Russian Federation

Mariya M. Kalandiya - PhD student.

11 Dm. Ulyanova street, 117036 Moscow.

eLibrary SPIN: 5172-6651


Competing Interests:

No



A. Yu. Tokmakova
Endocrinology Research Centre
Russian Federation

Alla Yu. Tokmakova - MD, PhD.

11 Dm. Ulyanova street, 117036 Moscow.

eLibrary SPIN: 7479-7043


Competing Interests:

No



G. R. Galstyan
Endocrinology Research Centre
Russian Federation

Gagik R. Galstyan - MD, PhD, Professor.

11 Dm. Ulyanova street, 117036 Moscow.

eLibrary SPIN: 9815-7509


Competing Interests:

No



References

1. Cho NH, Shaw JE, Karuranga S, et al. IDF Diabetes Atlas: Global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract. 2018;138:271-281. doi: https://doi.org/10.1016/j.diabres.2018.02.023

2. Tokmakova AY, Doronina LP, Galstyan GR, Senyushkina ES, Mitish VA. The complex therapy long-term results for patients with the 2nd degree diabetes and the bilateral neuroosteoarthropathy. Wounds and Wound Infections. The Prof. B. M. Kostyuchenok Journal. 2018;5(1):39-49. (in Russ.). doi: https://doi.org/10.25199/2408-9613-2018-5-1-39–49

3. Tesfaye S, Selvarajah D, Gandhi R, et al. Diabetic peripheral neuropathy may not be as its name suggests: Evidence from magnetic resonance imaging. Pain. 2016;157: S72-S80. doi: https://doi.org/10.1097/j.pain.0000000000000465

4. Ziegler D, Rathmann W, Dickhaus T, et al. Prevalence of polyneuropathy in prediabetes and diabetes is associated with abdominal obesity and macroangiopathy: The Monica/Kora Augsburg surveys S2 and S3. Diabetes Care. 2008;31(3):464-469. doi: https://doi.org/10.2337/dc07-1796

5. Callaghan BC, Xia R, Banerjee M, et al. Metabolic syndrome components are associated with symptomatic polyneuropathy independent of glycemic status. Diabetes Care. 2016;39(5):801-807. doi: https://doi.org/10.2337/dc16-0081

6. Lin YC, Lin CSY, Chang TS, et al. Early sensory neurophysiological changes in prediabetes. J Diabetes Investig. 2020;11(2):458-465. doi: https://doi.org/10.1111/jdi.13151

7. Bongaerts BWC, Rathmann W, Heier M, et al. Older subjects with diabetes and prediabetes are frequently unaware of having distal sensorimotor polyneuropathy: the KORA F4 study. Diabetes Care. 2013;36(5):1141-6. doi: https://doi.org/10.2337/dc12-0744

8. Kurisu S, Sasaki H, Kishimoto S, et al. Clinical polyneuropathy does not increase with prediabetes or metabolic syndrome in the Japanese general population. J Diabetes Investig. 2019;10(6):1565-1575. doi: https://doi.org/10.1111/jdi.13058

9. Kloska A, Korzon-Burakowska A, Malinowska M, et al. The role of genetic factors and monocyte-to-osteoclast differentiation in the pathogenesis of Charcot neuroarthropathy. Diabetes Res Clin Pract. 2020;166. doi: https://doi.org/10.1016/j.diabres.2020.108337

10. Rogers LC, Frykberg RG, Armstrong DG, et al. The Charcot foot in diabetes. Diabetes Care. 2011;34(9):2123-2129. doi: https://doi.org/10.2337/dc11-0844

11. Armstrong DG, Peters EJG. Charcot’s arthropathy of the foot. J Am Podiatr Med Assoc. 2002;92(7):390-394. doi: https://doi.org/10.7547/87507315-92-7-390

12. Frykberg RG, Belczyk R. Epidemiology of the Charcot Foot. Clin Podiatr Med Surg. 2008;25(1):17-28. doi: https://doi.org/10.1016/j.cpm.2007.10.001

13. Salini D, Harish K, Minnie P, et al. Prevalence of Charcot arthropathy in Type 2 diabetes patients aged over 50 years with severe peripheral neuropathy: A retrospective study in a Tertiary Care South Indian Hospital. Indian J Endocrinol Metab. 2018;22(1):107-111. doi: https://doi.org/10.4103/ijem.IJEM_257_17

14. Miller DS, William Miller WF. Lichtman,Diabetic neuropathic arthropathy of feet. Published online 1965: 530.

15. McEwen LN, Ylitalo KR, Herman WH, Wrobel JS. Prevalence and risk factors for diabetes-related foot complications in Translating Research into Action for Diabetes (TRIAD). J.Diabetes. Complications.2013;27(6):588-592. doi: https://doi.org/10.1016/j.jdiacomp.2013.08.003

16. Younis B Bin, Shahid A, Arshad R, et al. Charcot osteoarthropathy in type 2 diabetes persons presenting to specialist diabetes clinic at a tertiary care hospital. BMC Endocr Disord. 2015;15(1):1-5. doi: https://doi.org/10.1186/s12902-015-0023-4

17. Jeffcoate WJ, Game F, Cavanagh PR. The role of proinflammatory cytokines in the cause of neuropathic osteoarthropathy (acute Charcot foot) in diabetes. Lancet. 2005;366(9502):2058-2061. doi: https://doi.org/10.1016/S0140-6736(05)67029-8

18. Baker N, Green A, Krishnan S, et al. Microvascular and C-fiber function in diabetic charcot neuroarthropathy and diabetic peripheral neuropathy. Diabetes Care. 2007;30(12):3077-3079. doi: https://doi.org/10.2337/dc07-1063

19. Trieb K. The Charcot foot: Pathophysiology, diagnosis and classification. Bone Jt J. 2016;98-B(9):1155-1159. doi: https://doi.org/10.1302/0301-620X.98B9.37038

20. Jansen RB, Christensen TM, Bülow J, et al. Markers of Local Inflammation and Bone Resorption in the Acute Diabetic Charcot Foot. J Diabetes Res. 2018;2018. doi: https://doi.org/10.1155/2018/5647981

21. Dinarello CA. Proinflammatory cytokines. Chest. 2000;118(2):503-508. doi: https://doi.org/10.1378/chest.118.2.503

22. GROSE SWAR. Regulation of wound healing by growth factors and cytokines. Wound Heal Process Phases Promot. Published online 2003:73-93.

23. Boyce BF, Xing L. Functions of RANKL/RANK/OPG in bone modeling and remodeling. Arch Biochem Biophys. 2008;473(2):139-146. doi: https://doi.org/10.1016/j.abb.2008.03.018

24. Mountzios G, Dimopoulos MA, Bamias A, et al. Abnormal bone remodeling process is due to an imbalance in the receptor activator of nuclear factor-κB ligand (RANKL)/osteoprotegerin (OPG) axis in patients with solid tumors metastatic to the skeleton. Acta Oncol (Madr). 2007;46(2):221-229. doi: https://doi.org/10.1080/02841860600635870

25. Silva I, Branco JC. Rank/RANKL/OPG: Literature review. Acta Reumatol Port. 2011;36(3):209-218.

26. Mascarenhas JV, Jude EB. The Charcot Foot as a Complication of Diabetic Neuropathy. Curr Diab Rep. 2014;14(12):1-9. doi: https://doi.org/10.1007/s11892-014-0561-6

27. Wautier JL, Schmidt AM. Protein glycation: A firm link to endothelial cell dysfunction. Circ Res. 2004;95(3):233-238. doi: https://doi.org/10.1161/01.RES.0000137876.28454.64

28. Zieman SJ, Kass DA. Advanced glycation endproduct crosslinking in the cardiovascular system: Potential therapeutic target for cardiovascular disease. Drugs. 2004;64(5):459-470. doi: https://doi.org/10.2165/00003495-200464050-00001

29. Bastien P. Aged Human Skin is More Susceptible than Young Skin to Accumulate Advanced Glycoxidation Products Induced by Sun Exposure. J Aging Sci. 2013;01(03):1-5. doi: https://doi.org/10.4172/2329-8847.1000112

30. Fishman SL, Sonmez H, Basman C, et al. The role of advanced glycation end-products in the development of coronary artery disease in patients with and without diabetes mellitus: A review. Mol Med. 2018;24(1):1-12. doi: https://doi.org/10.1186/s10020-018-0060-3

31. Koyama Y, Takeishi Y, Arimoto T, et al. High Serum Level of Pentosidine, an Advanced Glycation End Product (AGE), is a Risk Factor of Patients with Heart Failure. J Card Fail. 2007;13(3):199-206. doi: https://doi.org/10.1016/j.cardfail.2006.11.009

32. Bidasee KR, Zhang Y, Shao CH, et al. Diabetes Increases Formation of Advanced Glycation End Products on Sarco(endo)plasmic Reticulum Ca2+-ATPase. Diabetes. 2004;53(2):463-473. doi: https://doi.org/10.2337/diabetes.53.2.463

33. Yan SF, Ramasamy R, Schmidt AM. The receptor for advanced glycation endproducts (RAGE) and cardiovascular disease. Expert Rev Mol Med. 2009;11(March):1-13. doi: https://doi.org/10.1017/S146239940900101X

34. Potekhina Y. Collagen Structure and Function. Russ Osteopath J. 2016;(1-2):87-99. doi: https://doi.org/10.32885/2220-0975-2016-1-2-87-99

35. Bishop JE, Rhodes S, Laurent GJ, Low RB. Increased collagen synthesis and decreased collagen degradation in right ventricular hypertrophy induced by pressure overload. Published online 1994:1581-1585.

36. Saito M, Soshi S, Fujii K. Effect of hyper- and microgravity on collagen post-translational controls of MC3T3-E1 osteoblasts. J Bone Miner Res. 2003;18(9):1695-1705. doi: https://doi.org/10.1359/jbmr.2003.18.9.1695

37. Shiraki M, Urano T, Kuroda T, et al. The synergistic effect of bone mineral density and methylenetetrahydrofolate reductase (MTHFR) polymorphism (C677T) on fractures. J Bone Miner Metab. 2008;26(6):595-602. doi: https://doi.org/10.1007/s00774-008-0878-9

38. Kanazawa I. Interaction between bone and glucose metabolism. Endocr J. 2017;64(11):1043-1053. doi: https://doi.org/10.1507/endocrj.EJ17-0323

39. Portero-otín M, Pamplona R, Ruiz MC, Cabiscol E, Prat J, Bellmunt MJ. Diabetes Induces an Impairment in the Proteolytic Activity Against Oxidized Proteins and a Heterogeneous Effect in Nonenzymatic Protein Modifications in the Cytosol of Rat Liver and Kidney. :2215-2220.

40. Karim L, Tang SY, Sroga GE, et al. Differences in non-enzymatic glycation and collagen cross-links between human cortical and cancellous bone. Osteoporos Int. 2013;24(9):2441-2447. doi: https://doi.org/10.1007/s00198-013-2319-4

41. Saito M, Fujii K, Mori Y, et al. Role of collagen enzymatic and glycation induced cross-links as a determinant of bone quality in spontaneously diabetic WBN/Kob rats. Osteoporos Int. 2006;17(10):1514-1523. doi: https://doi.org/10.1007/s00198-006-0155-5

42. Schwartz A V., Garnero P, Hillier TA, et al. Pentosidine and increased fracture risk in older adults with type 2 diabetes. J Clin Endocrinol Metab. 2009;94(7):2380-2386. doi: https://doi.org/10.1210/jc.2008-2498

43. Shiraki M, Kuroda T, Tanaka S, et al. Nonenzymatic collagen cross-links induced by glycoxidation (pentosidine) predicts vertebral fractures. J Bone Miner Metab. 2008;26(1):93-100. doi: https://doi.org/10.1007/s00774-007-0784-6

44. Yamamoto M, Yamaguchi T, Yamauchi M, et al. Serum pentosidine levels are positively associated with the presence of vertebral fractures in postmenopausal women with type 2 diabetes. J Clin Endocrinol Metab. 2008;93(3):1013-1019. doi: https://doi.org/10.1210/jc.2007-1270

45. Farlay D, Armas LAG, Gineyts E, et al. Nonenzymatic Glycation and Degree of Mineralization Are Higher in Bone from Fractured Patients with Type 1 Diabetes Mellitus. J Bone Miner Res. 2016;31(1):190-195. doi: https://doi.org/10.1002/jbmr.2607

46. Schmidt AM, Yan S Du, Yan SF, et al. The biology of the receptor for advanced glycation end products and its ligands. Biochim Biophys Acta - Mol Cell Res. 2000;1498(2-3):99-111. doi: https://doi.org/10.1016/S0167-4889(00)00087-2

47. Lee EJ, Park JH. Receptor for Advanced Glycation Endproducts (RAGE), Its Ligands, and Soluble RAGE: Potential Biomarkers for Diagnosis and Therapeutic Targets for Human Renal Diseases. Genomics Inform. 2013;11(4):224. doi: https://doi.org/10.5808/gi.2013.11.4.224

48. Ott C, Jacobs K, Haucke E, et al. Role of advanced glycation end products in cellular signaling. Redox Biol. 2014;2(1):411-429. doi: https://doi.org/10.1016/j.redox.2013.12.016

49. Xue J, Manigrasso M, Scalabrin M, et al. Change in the Molecular Dimension of a RAGE-Ligand Complex Triggers RAGE Signaling. Structure. 2016;24(9):1509-1522. doi: https://doi.org/10.1016/j.str.2016.06.021

50. Goldin A, Beckman JA, Schmidt AM, et al. Advanced glycation end products: Sparking the development of diabetic vascular injury. Circulation. 2006;114(6):597-605. doi: https://doi.org/10.1161/CIRCULATIONAHA.106.621854

51. Wautier JL, Wautier MP, Schmidt AM, et al. Advanced glycation end products (AGEs) on the surface of diabetic erythrocytes bind to the vessel wall via a specific receptor inducing oxidant stress in the vasculature: A link between surface-associated AGEs and diabetic complications. Proc Natl Acad Sci U S A. 1994;91(16):7742-7746. doi: https://doi.org/10.1073/pnas.91.16.7742

52. Nilforoushan D, Gramoun A, Glogauer M, et al. Nitric oxide enhances osteoclastogenesis possibly by mediating cell fusion. Nitric Oxide - Biol Chem. 2009;21(1):27-36. doi: https://doi.org/10.1016/j.niox.2009.04.002

53. Nowak WN, Borys S, Kusińska K, et al. Number of circulating pro-angiogenic cells, growth factor and anti-oxidative gene profiles might be altered in type 2 diabetes with and without diabetic foot syndrome. J Diabetes Investig. 2014;5(1):99-107. doi: https://doi.org/10.1111/jdi.12131

54. Hegab Z. Role of advanced glycation end products in cardiovascular disease. World J Cardiol. 2012;4(4):90. doi: https://doi.org/10.4330/wjc.v4.i4.90

55. Stirban A, Gawlowski T, Roden M. Vascular effects of advanced glycation endproducts: Clinical effects and molecular mechanisms. Mol Metab. 2014;3(2):94-108. doi: https://doi.org/10.1016/j.molmet.2013.11.006

56. Saremi A, Howell S, Schwenke DC, et al. Advanced glycation end products, oxidation products, and the extent of atherosclerosis during the VA diabetes trial and follow-up study. Diabetes Care. 2017;40(4):591-598. doi: https://doi.org/10.2337/dc16-1875

57. Oldfield MD, Bach LA, Forbes JM, et al. Advanced glycation end products cause epithelial-myofibroblast transdifferentiation via the receptor for advanced glycation end products (RAGE). J Clin Invest. 2001;108(12):1853-1863. doi: https://doi.org/10.1172/JCI11951

58. Rabbani N, Thornalley PJ. Glyoxalase 1 modulation in obesity and diabetes. Antioxidants Redox Signal. 2019;30(3):354-374. doi: https://doi.org/10.1089/ars.2017.7424

59. Giacco F, Du X, D’Agati VD, et al. Knockdown of glyoxalase 1 mimics diabetic nephropathy in nondiabetic mice. Diabetes. 2014;63(1):291-299. doi: https://doi.org/10.2337/db13-0316


Supplementary files

Review

For citations:


Kalandiya M.M., Tokmakova A.Yu., Galstyan G.R. The role of glycation end products in the development and progression of diabetic neuroarthropathy. Problems of Endocrinology. 2021;67(3):4-9. (In Russ.) https://doi.org/10.14341/probl12778

Views: 6260


ISSN 0375-9660 (Print)
ISSN 2308-1430 (Online)