Advanced glycation end products: A link between periodontitis and diabetes mellitus?

Current Diabetes Reviews

Volumn 9, Issue 5, 2013, Pages 355-361

  Gurav, Abhijit N ^a  

^a Tatyasaheb Kore Dental College and Research Centre   (India)

Author keywords

Advanced glycation end products; Diabetes mellitus; Inflammation; Oxidative stress; Periodontitis; Receptor for advanced glycation end products

Indexed keywords

ACETYLCYSTEINE; ADVANCED GLYCATION END PRODUCT; ALAGEBRIUM; AMINOGUANIDINE; ANTHOCYANIN; BENFOTIAMINE; CAPTOPRIL; CARNITINE; CARNOSINE; CATECHIN; COUMARIC ACID; CURCUMIN; EPICATECHIN; FERULIC ACID; FOSINOPRIL; GREEN TEA EXTRACT; ISOVITEXIN; METFORMIN; PIOGLITAZONE; PYRIDOXAMINE; QUERCITRIN; RESVERATROL; ROSIGLITAZONE; SINAPIC ACID; TAURINE; TENILSETAM; THIAMINE; VITEXIN;

ANTIOXIDANT ACTIVITY; BONE; CARBOHYDRATE METABOLISM; DIABETES MELLITUS; DISEASE ASSOCIATION; EXTRACELLULAR MATRIX; HUMAN; METABOLISM; NONHUMAN; PERIODONTITIS; PRIORITY JOURNAL; REVIEW;

ANIMALS; BONE AND BONES; DIABETES COMPLICATIONS; EXTRACELLULAR MATRIX; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; HYPOGLYCEMIC AGENTS; PERIODONTITIS; RECEPTORS, IMMUNOLOGIC; SOLUBILITY;

EID: 84882793768     PISSN: 15733998     EISSN: 18756417     Source Type: Journal    
DOI: 10.2174/15733998113099990066     Document Type: Review

References (97)

1. Puddu A, Viviani GL. Advanced glycation end products and diabetes. Beyond vascular complications. EndocrMetab Immune Disord Drug Targets 2011; 11(2): 132-40.
2. Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet 2005; 366: 1809-20.
3. Mealey BL, Ocampo GL. Diabetes mellitus and periodontal disease. Periodontol 2000 2007; 44: 127-153.
4. Gurav A, Jadhav V. Periodontitis and risk of diabetes mellitus-A Review. J Diabetes 2011; 3: 21-8.
5. Preshaw PM, Alba AL, Herrera D, et al. Periodontitis and diabetes: a two-way relationship. Diabetologia 2012; 55: 21-31.
6. Graves DT, Liu R, Oates TW. Diabetes-enhanced inflammation and apoptosis: impact on periodontal pathosis. Periodontol 2000 2007; 45: 128-37.
7. Daroux M, Prévost G, Maillard-Lefebvre H, Gaxatte C, D'Agati VD, Schmidt AM, Boulanger E. Advanced glycation end-products: implications for diabetic and non-diabetic nephropathies. Diabetes Metab 2010; 36(1): 1-10.
8. Cho SJ, Roman G, Yeboah F, Konishi Y. The road to advanced glycation end products: a mechanistic perspective. Curr Med Chem 2007; 14: 1653-71.
9. Del Turco S, Basta G. An update on advanced glycation end products and atherosclerosis. Biofactors 2012; 38(4): 266-74.
10. Willemsen S, Hartog JWL, Heiner-Fokkema MR, van Veldhuisen DJ, Voors AA. Advanced glycation end-products, a pathophysiological pathway in the cardiorenal syndrome. Heart Fail Rev 2012; 17: 221-8.
11. Goldin A, Beckman JA, Schmidt AM, Creager MA. Advanced Glycation End Products: Sparking the Development of Diabetic Vascular injury. Circulation. 2006; 114: 597-605.
12. Thorpe SR, Baynes JW. Maillard reaction products in tissue proteins: new products and new perspectives. Amino Acids 2003; 25: 275-81.
13. Ahmed N. Advanced glycation end products-role in pathology of diabetic complications. Diabetes Res Clin Pract 2005; 67: 3-21.
14. Xue M, Rabbani N, Thornalley PJ. Glyoxalase in ageing. Semin Cell Dev Biol. 2011; 22(3): 293-301.
15. Wu X, Monnier VM. Enzymatic deglycation of proteins. Arch BiochemBiophys 2003; 419(1): 16-24.
16. Barlovic DP, Soro-Paavonen A, Jandeleit-Dahm KA. RAGE biology, atherosclerosis and diabetes. ClinSci (Lond) 2011; 121(2): 43-55.
17. Rojas A, Delgado-López F, González I, Pérez-Castro R, Romero J, Rojas I. The receptor for advanced glycation end-products: A complex signaling scenario for a promiscuous receptor. Cell Signal 2013; 25(3): 609-14.
18. Ramasamy R, Yan SF, Schmidt AM. Advanced glycationendproducts: from precursors to RAGE: round and round we go. Amino Acids 2012; 42(4): 1151-61.
19. Santilli F, Vazzana N, Bucciarelli LG, Davì G. Soluble forms of RAGE in human diseases: clinical and therapeutical implications. Curr Med Chem 2009; 16: 940-52.
20. Wang X, Shen X, Li X, Agrawal CM. Age-related changes in the collagen network and toughness of bone. Bone 2002; 31: 107.
21. Corthay A, Backlund J, Holmdahl R. Role of glycopeptide-specific T cells in collagen-induced arthritis: an example how posttranslational modification of proteins may be involved in autoimmune disease. Ann Med 2001; 33: 456-65.
22. Berbaum K, Shanmugam K, Stuchbury G, Wiede F, Körner H, Münch G. Induction of novel cytokines and chemokines by advanced glycation end products determined with a cytometric bead array. Cytokine 2008; 41(3): 198-203.
23. Yu S, Li H, Ma Y, Fu Y. Matrix metalloproteinase-1 of gingival fibroblasts influenced by advanced glycation end products (AGEs) and their association with receptor for AGEs and nuclear factor-κB in gingival connective tissue. J Periodontol 2012; 83(1): 119-26.
24. Lalla E, Lamster IB, Feit M, Huang L, et al. Blockade of RAGE suppresses periodontitis-associated bone loss in diabetic mice. J Clin Invest 2000; 105: 1117-24.
25. Chang PC, Chien LY, Yeo JF, Wang YP, et al. Progression of periodontal destruction and the roles of advanced glycation end products in experimental diabetes. J Periodontol 2013; 84(3): 379-88.
26. Kume S, Kato S, Yamagishi S, Inagaki Y, et al. Advancedglycation end-products attenuate human mesenchymal stem cells and prevent cognate differentiation into adipose tissue, cartilage, and bone. J Bone Miner Res 2005; 20(9): 1647-58.
27. Daley WP, Peters SB, Larsen M. Extracellular matrix dynamics in development and regenerative medicine. J Cell Sci 2008; 121(Pt 3): 255-64.
28. Furber JD. Extracellular glycation cross links: prospects for removal. Rejuvenation Res 2006; 9: 274-8.
29. Brownlee M, Vlassara H, Cerami A. Non-enzymatic glycosylation products on collagen covalently trap low-density lipoprotein. Diabetes 1985; 34: 938-41.
30. Chang PC, Chien LY, Chong LY, Kuo YP, Hsiao JK. Glycated matrix up-regulates inflammatory signaling similarly to Porphyromonas gingivalis lipopolysaccharide. J Periodontal Res 2013; 48(2): 184-93.
31. Ren L, Fu Y, Deng Y, Qi L, Jin L. Advanced glycation end products inhibit the expression of collagens type I and III by human gingival fibroblasts. J Periodontol 2009; 80(7): 1166-73.
32. Fukada SY, Silva TA, Saconato IF, Garlet GP, Avila-Campos MJ, Silva JS, Cunha FQ. iNOS-derived nitric oxide modulates infectionstimulated bone loss. J Dent Res 2008; 87(12): 1155-9.
33. Liao H, Zakhaleva J, Chen W. Cells and tissue interactions with glycated collagen and their relevance to delayed diabetic wound healing. Biomaterials 2009; 30(9): 1689-96.
34. Saito M, Marumo K. Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. OsteoporosInt 2010; 21: 195-214.
35. Garnero P, Borel O, Gineyts E, Duboeuf F, Solberg H, Bouxsein ML, Christiansen C, Delmas PD. Extracellular post-translational modifications of collagen are major determinants of biomechanical properties of fetal bovine cortical bone. Bone 2006; 38: 300-9.
36. Sanguineti R, Storace D, Monacelli F, Federici A, Odetti P. Pentosidine effects on human osteoblasts in vitro. Ann N Y AcadSci 2008; 1126: 166-72.
37. Hernandez CJ, Tang SY, Baumbach BM, et al. Trabecular micro fracture and the influence of pyridinium and non-enzymatic glycation mediated collagen cross-links. Bone 2005; 37: 825-32.
38. Viguet-Carrin S, Roux JP, Arlot ME, et al. Contribution of the advanced glycation end product pentosidine and of maturation of type I collagen to compressive biomechanical properties of human lumbar vertebrae. Bone 2006; 39: 1073-9.
39. Yamamoto T, Ozono K, Miyauchi A, Kasayama S, Kojima Y, Shima M, Okada S. Role of advanced glycation end products in a dynamic bone disease in patients with diabetic nephropathy. Am J Kidney Dis 2001; 38: S161-S164.
40. Franke S, Rüster C, Pester J, Hofmann G, Oelzner P, Wolf G. Advanced glycation end products affect growth and function of osteoblasts. Clin ExpRheumatol 2011; 29(4): 650-60.
41. Chang PC, Chung MC, Wang YP, et al. Patterns of diabetic periodontal wound repair: a study using micro-computed tomography and immunohistochemistry. J Periodontol 2012; 83(5): 644-52.
42. Karim L, Vashishth D. Heterogeneous Glycation of Cancellous Bone and Its Association with Bone Quality and Fragility. PLoS ONE 2012; 7(4): e35047.
43. Ogawa N, Yamaguchi T, Yano S, Yamauchi M, Yamamoto M, Sugimoto T. The combination of high glucose and advanced glycation end-products (AGEs) inhibits the mineralization of osteoblastic MC3T3-E1 cells through glucose-induced increase in the receptor for AGEs. HormMetab Res 2007; 39: 871-5.
44. Ding KH, Wang ZZ, Hamrick MW, et al. Disordered osteoclast formation in RAGE deficient mouse establishes an essential role for RAGE in diabetes related bone loss. BiochemBiophys Res Commun 2006; 340: 1091-7.
45. Alikhani M, Alikhani Z, Boyd C, et al. Advanced glycation end products stimulate osteoblast apoptosis via the MAP kinase and cytosolic apoptotic pathways. Bone 2007; 40(2): 345-53.
46. Okazaki K, Yamaguchi T, Tanaka K, et al. Advanced glycation end products (AGEs), but not high glucose, inhibit the osteoblastic differentiation of mouse stromal ST2 cells through the suppression of osterix expression, and inhibit cell growth and increasing cell apoptosis. Calcif Tissue Int 2012; 91(4): 286-96.
47. García-Hernández A, Arzate H, Gil-Chavarría I, Rojo R, Moreno-Fierros L. High glucose concentrations alter the biomineralization process in human osteoblastic cells. Bone 2012; 50: 276-88.
48. Miyata T, Notoya K, Yoshida K, et al. Advanced glycation end products enhance osteoclast-induced bone resorption in cultured mouse unfractionated bone cells and in rats implanted subcutaneously with devitalized bone particles. J Am SocNephrol 1997; 8: 260-70.
49. Dong XN, Qin A, Xu J, Wang X. In situ accumulation of advanced glycation end products (AGEs) in bone matrix and its correlation with osteoclastic bone resorption. Bone 2011; 49(2): 174-83.
50. Valcourt U, Merle B, Gineyts E, Viguet-Carrin S, Delmas PD, Garnero P. Non-enzymatic glycation of bone collagen modifies osteoclastic activity and differentiation. J BiolChem 2007; 282(8): 5691-703.
51. Santana RB, Xu L, Chase HB, Amar S, Graves DT, Trackman PC. A role for advanced glycation end products in diminished bone healing in type 1 diabetes. Diabetes 2003; 52(6): 1502-10.
52. Brownlee M, Vlassara H, Kooney A, Ulrich P, Cerami A. Aminoguanidine prevents diabetes-induced arterial wall protein crosslinking. Science 1986; 232: 1629-32.
53. Desai K, Wu L. Methylglyoxal and advanced glycation end products: new therapeutic horizons? Recent Pat Cardiovasc Drug Discov 2007; 2: 89-99.
54. Thomas MC, Baynes JW, Thorpe SR, Cooper ME. The role of AGEs and AGE inhibitors in diabetic cardiovascular disease. Curr Drug Targets 2005; 6(4): 453-74.
55. Voziyan PA, Hudson BG. Pyridoxamine as a multifunctional pharmaceutical: targeting pathogenic glycation and oxidative damage. Cell Mol Life Sci 2005; 62(15): 1671-81.
56. Balakumar P, Rohilla A, Krishan P, Solairaj P, Thangathirupathi A. The multifaceted therapeutic potential of benfotiamine. Pharmacol Res 2010; 61(6): 482-8.
57. Guiotto A, Calderan A, Ruzza P, Borin G. Carnosine and carnosine-related antioxidants: a review. Curr Med Chem 2005; 12: 2293-315.
58. Tang SC, Arumugam TV, Cutler RG J et al. Neuroprotective actions of a histidine analogue in models of ischemic stroke. J Neurochem 2007; 101: 729-36.
59. Arakawa M, Ishimura A, Arai Y, et al. Acetylcysteine and ebselen but not nifedipine protected cerebellar granule neurons against 4-hydroxynonenal-induced neuronal death. Neurosci Res 2006; 57: 220-9.
60. Valentovic M, Terneus M, Harmon RC, Carpenter AB. SAdenosylmethionine (SAMe) attenuates acetaminophen hepatotoxicity in C57BL/6 mice. ToxicolLett 2004; 154: 165-74.
61. Ito T, Schaffer SW, Azuma J. The potential usefulness of taurine on diabetes mellitus and its complications. Amino Acids 2012; 42: 1529-39.
62. Rajasekar P, Anuradha CV. L-Carnitine inhibits protein glycation in vitro and in vivo: evidence for a role in diabetic management. ActaDiabetol 2007; 44(2): 83-90.
63. Hayek T, Attias J, Coleman R, et al. The angiotensin-converting enzyme inhibitor, fosinopril, and the angiotensin II receptor antagonist, losartan, inhibit LDL oxidation and attenuate atherosclerosis independent of lowering blood pressure in apolipoprotein E deficient mice. Cardiovasc Res 1999; 44: 579-87.
64. Beisswenger P, Ruggiero-Lopez D. Metformin inhibition of glycation processes. Diabetes Metab 2003; 29(4 Pt 2): 6S95-103.
65. Marx N, Walcher D, Ivanova N, et al. Thiazolidinediones reduce endothelial expression of receptors for advanced glycation end products. Diabetes 2004; 53(10): 2662-8.
66. Ishibashi Y, Matsui T, Takeuchi M, Yamagishi S. Sitagliptin augments protective effects of GLP-1 against advanced glycation end product receptor axis in endothelial cells. HormMetab Res 2011; 43(10): 731-4.
67. Figarola JL, Scott S, Loera S, Xi B, Synold T, Weiss L, Rahbar S. Prevention of early renal disease, dyslipidaemia and lipid peroxidation in STZ-diabetic rats by LR-9 and LR-74,novel AGE inhibitors. Diabetes Metab Res Rev 2005; 21: 533-44.
68. Figarola JL, Loera S, Weng Y, Shanmugam N, Natarajan R, Rahbar S. LR-90 prevents dyslipidemia and diabetic nephropathy in the Zucker diabetic fatty rat. Diabetologia 2008; 51: 882-891.
69. Münch G, Mayer S, Michaelis J, et al. Influence of advanced glycation end-products and AGE-inhibitors on nucleation-dependent polymerization of beta-amyloid peptide. BiochimBiophysActa 1997; 1360(1): 17-29.
70. Babu PV, Sabitha KE, Shyamaladevi CS. Therapeutic effect of green tea extract on advanced glycation and cross-linking of collagen in the aorta of streptozotocin diabetic rats. Clin Exp Pharmacol Physiol 2006; 33(4): 351-7.
71. Bengmark S, Mesa MD, Gil A. Plant-derived health: the effects of turmeric and curcuminoids. NutrHosp 2009; 24(3): 273-81.
72. Yao Y, Cheng X, Wang L, Wang S, Ren G. Major Phenolic Compounds, Antioxidant Capacity and Antidiabetic Potential of Rice Bean (Vignaumbellata L.) in China. Int J MolSci 2012; 13: 2707-16.
73. Cervantes-Laurean D, Schramm DD, Jacobson EL, Halaweish I, Bruckner GG, Boissonneault GA. Inhibition of advanced glycation end product formation on collagen by rutin and its metabolites. J NutrBiochem 2006; 17: 531-40.
74. Bousová I, Martin J, Jahodár L, Dusek J, Palicka V, Drsata J. Evaluation of in vitro effects of natural substances of plant origin using a model of protein glycoxidation. J Pharm Biomed Anal 2005; 37: 957-62.
75. Wu CH, Yen GC. Inhibitory effect of naturally occurring flavonoids on the formation of advanced glycation end products. J Agric Food Chem 2005; 53(8): 3167-73.
76. Wu CH, Huang SM, Yen GC. Silymarin: a novel antioxidant with anti glycation and anti inflammatory properties in vitro and in vivo. Antioxid Redox Signal 2011; 14(3): 353-66.
77. Rout S, Banerjee R. Free radical scavenging, anti-glycation and tyrosinase inhibition properties of a polysaccharide fraction isolated from the rind from Punicagranatum. BioresourTechnol 2007; 98(16): 3159-63.
78. Prasad K. Resveratrol, wine, and atherosclerosis. Int J Angiol 2012; 21(1): 7-18.
79. Soman S, Rauf AA, Indira M, Rajamanickam C. Antioxidant and antiglycative potential of ethyl acetate fraction of Psidiumguajava leaf extract in streptozotocin-induced diabetic rats. Plant Foods Hum Nutr 2010; 65(4): 386-91.
80. Kiho T, Usui S, Hirano K, Aizawa K, Inakuma T. Tomato paste fraction inhibiting the formation of advanced glycation endproducts. BiosciBiotechnolBiochem 2004; 68(1): 200-5.
81. Hanamura T, Hagiwara T, Kawagishi H. Structural and functional characterization of polyphenols isolated from acerola (Malpighiaemarginata DC.) fruit. BiosciBiotechnolBiochem 2005; 69(2): 280-6.
82. Ahmad MS, Pischetsrieder M, Ahmed N. Aged garlic extract and S-allyl cysteine prevent formation of advanced glycation end products. Eur J Pharmacol. 2007; 561(1-3): 32-8.
83. Vasan S, Foiles P, Founds H. Therapeutic potential of breakers of advanced glycation end product-protein cross links. Arch Biochem Biophysics 2003; 419: 89-96.
84. Joshi D, Gupta R, Dubey A, et al. TRC4186, a novel AGE-breaker, improves diabetic cardiomyopathy and nephropathy in Ob-ZSF1 model of type 2 diabetes. J CardiovascPharmacol 2009; 54: 72-81.
85. Pathak P, Gupta R, Chaudhari A, et al. TRC4149 a novel advanced glycation end product breaker improves hemodynamic status in diabetic spontaneously hypertensive rats. Eur J Med Res 2008; 13(8): 388-98.
86. Wilkinson-Berka JL, Kelly DJ, Koerner SM, Jaworski K, Davis B, Thallas V, Cooper ME. ALT-946 and aminoguanidine, inhibitors of advanced glycation, improve severe nephropathy in the diabetic transgenic (mREN-2)27 rat. Diabetes 2002; 51(11): 3283-9.
87. Susic D. Cross-link breakers as a new therapeutic approach to cardiovascular disease. BiochemSoc Trans 2007; 35: 853-856.
88. Vazzana N, Santilli F, Cuccurullo C, Davi G. Soluble forms of RAGE in internal medicine 1. Intern Emerg Med 2009; 4: 389-401.
89. Maillard-Lefebvre H, Boulanger E, Daroux M, Gaxatte C, Hudson BI, Lambert M. Soluble receptor for advanced glycation end products: a new biomarker in diagnosis and prognosis of chronic inflammatory diseases. Rheumatology (Oxford) 2009; 48(10): 1190-6.
90. Forbes JM, Thorpe SR, Thallas-Bonke V, et al. Modulation of soluble receptor for advanced glycation end products by angiotensin-converting enzyme-1 inhibition in diabetic nephropathy. J Am SocNephrol 2005; 16: 2363-72.
91. Tan KC, Chow WS, Tso AW, et al. Thiazolidinedione increases serum soluble receptor for advanced glycation end-products in type 2 diabetes. Diabetologia 2007; 50: 1819-25.
92. Santilli F, Bucciarelli L, Noto D, et al. Decreased plasma soluble RAGE in patients with hypercholesterolemia: effects of statins. Free RadicBiol Med 2007; 43: 1255-62.
93. Nishimura F, Takahashi K, Kurihara M, Takashiba S, Murayama Y. Periodontal disease as a complication of diabetes mellitus. Ann Periodontol 1998; 3(1): 20-9.
94. Nass N, Vogel K, Hofmann B, Presek P, Silber RE, Simm A. Glycation of PDGF results in decreased biological activity. Int J Biochem Cell Biol 2010; 42(5): 749-54.
95. Schmidt AM, Weidman E, Lalla E, et al. Advanced glycationendproducts (AGEs) induce oxidant stress in the gingiva: a potential mechanism underlying accelerated periodontal disease associated with diabetes. J Periodontal Res 1996; 31(7): 508-15.
96. Lalla E, Lamster IB, Feit M, Huang L, Schmidt AM. A murine model of accelerated periodontal disease in diabetes. J Periodontal Res 1998; 33(7): 387-99.
97. Peng X, Ma J, Chenab F, Wang M. Naturally occurring inhibitors against the formation of advanced glycation end-products. Food Funct 2011; 2: 289-301.