Advanced glycation endproducts (AGEs) induce oxidant stress in the gingiva: A potential mechanism underlying accelerated periodontal disease associated with diabetes

Journal of Periodontal Research

Volumn 31, Issue 7, 1996, Pages 508-515

  Schmidt, Ann Marie ^a   Weidman, Elliott ^a   Lalla, Evanthia ^a   Yan, Shi Du ^a   Hori, Osamu ^a   Cao, Rong ^a   Brett, Jerold G ^a   Lamster, Ira B ^a  

^a The New York Presbyterian Hospital   (United States)

Author keywords

Diabetes; Glycation; Oxidation; Periodontum

Indexed keywords

ADVANCED GLYCATION END PRODUCT; HEME OXYGENASE; STREPTOZOCIN; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ADULT; ANIMAL; ARTICLE; BIOSYNTHESIS; BLOOD; CHEMICALLY INDUCED DISORDER; DIABETES MELLITUS; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL DIABETES MELLITUS; GINGIVA; HUMAN; METABOLISM; MOUSE; OXIDATIVE STRESS; PERIODONTITIS; PHYSIOLOGY;

ADULT; ANIMALS; DIABETES COMPLICATIONS; DIABETES MELLITUS; DIABETES MELLITUS, EXPERIMENTAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; GINGIVA; GLYCOSYLATION END PRODUCTS, ADVANCED; HEME OXYGENASE (DECYCLIZING); HUMANS; MICE; OXIDATIVE STRESS; PERIODONTITIS; STREPTOZOCIN; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

EID: 0030254624     PISSN: 00223484     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0765.1996.tb01417.x     Document Type: Article

References (55)

1. Belting C, Hinker J, Dummett C. Influence of diabetes mellitus on the severity of periodontal disease. J Periodontol 1964; 35: 476-480.
2. Cohen D, Friedman L, Shapiro J, Kyle GC, Franklin S. Diabetes mellitus and periodontal disease: two year longitudinal observations. Part I. J Periodontol 1970; 41: 709-712.
3. Bernick C, Cohen D, Baker L, Laster L. Dental disease in children with diabetes mellitus. J Periodontol 1975; 46: 241-245.
4. Sznajder R, Carraro J, Rugna S, Sereday M. Periodontal findings in diabetic and nondiabetic patients. J Periodontol 1978; 49: 445-448.
5. Bartolucci E, Parks R. Accelerated periodontal breakdown in uncontrolled diabetes; pathogenesis and treatment. Oral Surg Oral Med Oral Path 1981; 52: 387-390.
6. Schlossman M, Knowler W, Pettit D, Genco R. Type II diabetes mellitus and periodontal disease. J Am Dent Assoc 1990; 121: 532-536.
7. Ureles S. Case report: a patient with severe periodontitis in conjunction with adult-onset diabetes. Compend Contin Educ Dent 1983; 4: 522-528.
8. Cianciola L, Park B, Bruck E, Mosorich L, Genco RJ. Prevalence of periodontal disease in insulin-dependent diabetes mellitus. J Am Dent Assoc 1982; 104: 653-660.
9. Safkan-Seppala B, Ainamo J. Periodontal conditions in insulin dependent diabetes mellitus. J Clin Periodontol 1992; 19: 628-632.
10. McNamara T, Ramamurthy N, Mulvihill J, Golub L. The development of an altered gingival crevicular microflora in the alloxan-diabetic rat. Arch Oral Biol 1982; 27: 217-223.
11. Mowat A, Baum J. Chemotaxis of PMNs from patients with diabetes. New Engl J Med 1971; 284: 621-627.
12. Biassada N, Manouchehr-Pour M. Haddow M, Spagnuolo P. Neutrophil functional activity in juvenile and adult onset diabetic patients with mild and severe periodontitis. J Periodont Res 1982; 17: 500-502.
13. Ruderman N, Williamson J, Brownlee M. Glucose and diabetic vascular disease. FASEB J 1992; 6: 2905-2914.
14. Sell D, Monnier V. Structure elucidation of a senescence cross-link from human extracellular matrix: implication of pentoses in the aging process. J Biol Chem 1989; 264: 21597-21602.
15. Brownlee M, Cerami A, Vlassara H. Advanced glycosylation endproducts in tissue and the biochemical basis of diabetic complications. N Engl J Med 1988; 318: 1315-1320.
16. Bucala R, Makita Z, Koschinsky T, Cerami A, Vlassara H. Lipid advanced glycosylation: pathway for lipid oxidation in vivo. PNAS (USA) 1993; 90: 6434-6438.
17. Baynes J. Role of oxidative stress in the development of complications in diabetes. Diabetes 1991; 40: 405-412.
18. Yan SD, Schmidt AM, Anderson G, et al. Enhanced cellular oxidant stress by the interaction of advanced glycation endproducts with their receptors/binding proteins. J Biol Chem 1994; 269: 9889-9897.
19. Godin D, Wohaieb S, Garnett M, Goumeniouk A. Antioxidant enzyme alterations in experimental clinical diabetes. Mol Cell Biochem 1988; 84: 223-231.
20. Wohaieb S, Godin D Alterations in free radical tissue-defense mechanisms in streptozotocin-induced diabetes in rat. Diabetes 1987; 36: 1014-1018.
21. Jain S, Levine S, Duett J, Hollier B. Reduced vitamin E and increased lipofuscin products in erythrocytes of diabetic rats. Diabetes 1991; 40: 1241-1244.
22. Stehouwer CDA, Nauta JJP, Zeldentust GC, Hackeng WHL, Donke AJM, Den Ottolander GJH. Urinary albumin excretion, cardiovascular disease, and endothelial dysfunction in non-insulin dependent diabetes mellitus. Lancet 1992; 340: 319-323.
23. Wautier JL, Zoukounan C, Chappey O, et al. Receptor-mediated endothelial cell dysfunction in diabetic vasculopathy: soluble receptor for advanced glycation endproducts blocks hyperpermeability. Clin Res 1995; 215A.
24. Schmidt AM, Yan SD, Brett J, Mora R, Nowygrod R, Stern D. Regulation of human mononuclear phagocyte migration by cell surface-binding proteins for advanced glycation endproducts. J Clin Invest 1993; 267: 5133-5138.
25. Schmidt AM, Vianna M, Gerlach M, et al. Isolation and characterization of binding proteins for advanced glycation endproducts from lung tissue which are present on the endothelial cell surface. J Biol Chem 1992; 267: 14987-14997.
26. Vaitukaitis, J. Production of antisera with small doses of immunogen: multiple intradermal injections. Meth Enzymol 1981; 73: 46-52.
27. Schmidt AM, Hasu M, Popov D, et al. The receptor for advanced glycation endproducts (AGEs) has a central role in vessel wall interactions and gene activatioin in response to circulating AGE-proteins. PNAS (USA) 1994; 91: 8807-8811.
28. Yan SD, Chen X, Schmidt AM, et al. Glycated tau protein in Alzheimer disease: a mechanism for induction of oxidant stress. PNAS (USA) 1994; 91: 7787-7791.
29. Neeper M, Schmidt AM, Brett J, et al. Cloning and expression of RAGE:a cell surface receptor for advanced glycation endproducts of proteins. J Biol Chem 1992; 267: 14998-15004.
30. Yang Z, Makita J, Horii Y, et al. Two novel rat liver membrane proteins that bind advanced glycosylation endproducts: relationship to macrophage receptor for glucosemodified proteins. J Exp Med 1991; 174: 515-524.
31. El-Khoury J, Thomas CA, Loike J, Cao L, Silverstein SC. Macrophages adhere to glucose-modified basement membrane collagen IV via their scavenger receptors. J Biol Chem 1994; 269: 10197-10200.
32. Balla G, Jacob H, Balla J, et al. Ferritin: a cytoprotective antioxidant stratagem of endothelium. J Biol Chem 1992; 267: 18148-18153.
33. Keyse A, Applegate L, Tromvoukis Y, Tyrrell R. Oxidant stress leads to transcriptional activation of the human heme oxygenase gene in cultured human skin fibroblasts. Mol Cell Biol 1990; 10: 4967-4969
34. Wasowicz W, Neve J, Peretz A. Optimized steps in fluorometric determination of thiobarbituric acid-reactive substances in serum: importance of extraction pH and influence of sample preservation and storage. Clin Chem 1993; 39: 2522-2526.
35. Knight JA, Pieper RK, McClellan L. Specific of the Thiobarbituric Acid Reaction: its use in studies of lipid peroxidation. Clin Chem 1988; 34: 2433-2438.
36. Gutteridge JMC, Halliwell B The measurement and mechanism of lipid peroxidation in biological systems. Trends Biochem Sci 1990; 15: 129-135.
37. Schmidt AM, Mora R, Cao R, et al. The endothelial cell binding site for advanced glycation endproducts consists of a complex: an integral membrane protein and a lactoferrinlike polypeptide. J Biol Chem 1994; 269: 9882-9888.
38. Brett J, Schmidt AM, Yan SD, et al. Survey of the distribution of a newly characterized receptor for advanced glycation end products in tissues. Am J Pathol 1993; 143: 1699-1712.
39. Moughal N, Adonogianaki E, Thornhill M, Kinanc D. Endothelial cell leukocyte adhesion molecule-I and intercellular adhesion molecule-I expression in gingival tissue during health and experimentally-induced gingivitis. J Periodent Res 1992; 27: 623-630.
40. Baeuerle P. The inducible transcription activator NF-kappa B: regulation by distinct protein subunits. Biochim Biophys Acta 1991; 1072: 63-80.
41. Schreck R, Rieber P, Baeuerle P. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappaB transcription factor and HIV. EMBO J 1991; 10: 2247-2258.
42. Collins T. Endothelia nuclear factor kB and the initiation of the atherosclerotic lesion. Lab Invest 1993; 68: 499-508.
43. Takahasi K,Takashiba S, Nagai A, et al. Assessment of IL-6 in the pathogenesis of periodontal disease. J Periodontol 1994; 65: 147-153.
44. Schmidt AM, Hori O, Chen JX, et al. Advanced glycation Endproducts interacting with their endothelial receptor induce expression of vascular cell adhesion molecule-1 (VCAM-I) in cultured human umbilical vein endothelial cells and in mice: a potential mechanism for the accelerated vasculopathy of diabetes. J Clin Invest 1995; 96: 1395-1403.
45. Osborn L, Hession C, Tizard R, et al. Direct expression cloning of vascular cell adhesion molecule 1, a cytokine-induced endothelial protein that binds to lymphocytes. Cell 1989; 59: 1203-1211.
46. Cybulsky M, Gimbrone M. Endothelial expression of a mononuclear leukocyte adhesion molecule during atherogenesis. Science 1991; 251: 788-791.
47. Richardson M, Hadcock S, DeReske M, Cybulsky M. Increased expression in vivo of VCAM-1 and E-selectin by the aortic endothelium of normolipemic and hyperlipemic diabetic rabbits. Arterioscler Thromb 1994; 14: 760-769.
48. Jandinski J, Stashenko P, Feder L, et al. Localization of Interleukin-1 beta in human periodontal disease. J Periodontol 1991; 62: 36-43.
49. Page R. The role of inflammatory mediators in the pathogenesis of periodontal disease. J Periodont Res 1991; 26: 230-242.
50. Ranney R. Immunologic mechanisms of pathogenesis in periodontal diseases: an assessment. J Periodont Res 1991; 26: 243-254.
51. Mundy G. Inflammatory mediators and the destruction of bone. J Periodont Res 1991; 26: 213-217.
52. Richards D, Rutherford R. IL-1 regulation of procollagenase mRNA and protein in periodontal fibroblasts in vitro. J Periodont Res 1990; 25: 222-229.
53. Lefebvre V, Peeteers-Joris C, Vaes G. Production of gelatin-degrading matrix metalloproteinases and inhibitors by articular chondrocytes during their dedifferentiation by serial subcultures and under stimulation by IL-1 and TNF. Biochem Biophys Acta 1991; 1094: 8-18.
54. Unemori E, Hibbs M, Amento E. Constitutive expression of a 92 kD gelatinase by rheumatoid synovial fibroblasts and its induction in normal human fibroblasts by inflammatory cytokines. J Clin Invest 1991; 88: 1656-1662.
55. Meikle M, Hembry R, Holley J, Horton C, McFarlane C, Reynolds J. Immunolocalization of matrix metalloproteinases and TIMP-1 in human gingival tissues from periodontitis patients. J Periodont Res 1994; 29: 118-126