Vascular hypertrophy in experimental diabetes: Role of advanced glycation end products

Journal of Clinical Investigation

Volumn 99, Issue 5, 1997, Pages 1016-1027

  Rumble, Jonathan R ^a   Cooper, Mark E ^a   Soulis, Tina ^a   Cox, Alison ^a   Wu, Leonard ^a   Youssef, Sherif ^a   Jasik, Mariusz ^a   Jerums, George ^a   Gilbert, Richard E ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b AUSTIN HEALTH   (Australia)

Author keywords

diabetes mellitus; experimental; glycosylation end products, advanced; mesenteric arteries; transforming growth factor beta

Indexed keywords

AMINOGUANIDINE; COLLAGEN TYPE 4; GLYCOSYLATED HEMOGLOBIN; INSULIN ZINC SUSPENSION; MESSENGER RNA; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION; HISTOLOGY; HYPERTROPHY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MESENTERY BLOOD VESSEL; NONHUMAN; NORTHERN BLOTTING; ORAL DRUG ADMINISTRATION; PRIORITY JOURNAL; RAT; STREPTOZOCIN DIABETES; SUBCUTANEOUS DRUG ADMINISTRATION; VASCULAR DISEASE;

EID: 0030907178     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119229     Document Type: Article

References (72)

1. Williamson, J.R., R.G. Tilton, K. Chang, and C. Kilo. 1988. Basement membrane abnormalities in diabetes mellitus: relationship to clinical microangiopathv. Diabetes Metab. Rev. 4:339-370.
2. Brownlee, M.A., A. Cerami, and H. Vlassara. 1988. Advanced glycosylation end products in tissue and the biochemical basis of diabetic complications. N. Engl. J. Med. 318:131-138.
3. Soulis-Liparota, T., M. Cooper, D. Papazoglou, B. Clarke, and G. Jerums. 1991. Retardation by aminoguanidine of development of albuminuria, mesangial expansion, and tissue fluorescence in streptozocin-induced diabetic rat. Diabetes. 40:1328-1334.
4. Hammes, H-P., D. Strodter, A. Weiss, R.G. Bretzel, K. Federlin, and M. Brownlee. 1995. Secondary intervention with aminoguanidine retards the progression of diabetic retinopathy in the rat model. Diabetologia. 38:656-660.
5. Griffin, S.A., W.C. Brown, F. MacPherson, J.C. McGrath, V.O. Wilson, N. Korsgaard, M.J. Mulvanym and A.F. Lever. 1991. Angiotensin II causes vascular hypertrophy in part by a non-pressor mechanism. Hypertension. 17:626-635.
6. Simonsen, U., E. Ehrnrooth, L.U. Gerdes, O. Faergemann, J. Buch, F. Andreasen, and M.J. Mulvany. 1991. Functional properties in vitro of systematic small arteries from rabbits fed a cholesterol-rich diet for 12 weeks. Clin. Sci. (Lond.). 80:119-129.
7. Vranes, D., M.E. Cooper, and R.J. Dilley. 1995. Angiotensin converting enzyme inhibition reduces diabetes-induced vascular hypertrophy: Morphometric analysis. J. Vasc. Res. 32:183-189.
8. Cooper, M.E., J. Rumble, R. Komers, H-C. Du, K. Jandeleit, and S.T. Chou. 1994. Diabetes-associated mesenteric vascular hypertrophy is attenuated by angiotensin converting enzyme inhibition. Diabetes. 43:1221-1228.
9. Rumble, J.R., R. Komers, and M.E. Cooper. 1996. Kinins/nitric oxide are involved in the antihypertrophic effect of ACE inhibitors on diabetes-associated mesenteric vascular hypertrophy in the rat. J. Hypertens. 14:601-607.
10. Sarzani, R., P. Brecher, and A.V. Chobanian. 1989. Growth factor expression in aorta of normotensive and hypertensive rats. J. Clin. Invest. 83: 1404-1408.
11. Yamamoto, T., T. Nakamura, N.A. Noble, E. Ruoslahti, and W.A. Border. 1993. Expression of transforming growth factor beta is elevated in human and experimental diabetic nephropathy. Proc. Natl. Acad. Sci. USA. 90:1814-1818.
12. Stouffer, G.A., and G.K. Owens. 1994. TGF-β promotes proliferation of cultured SMC via both PDGF-AA-dependent and PDGF-AA-independent mechanisms. J. Clin. Invest. 93:2048-2055.
13. Wolf, Y.G., L.M. Rasmussen, and E. Ruoslahti. 1994. Antibodies against transforming growth factor-β suppress intimai hyperplasia in a rat model. J. Clin. Invest. 93: 1172-1178.
14. Border, W.A., and N.A. Noble. 1994. Mechanisms of disease: Transforming growth factor-β in tissue fibrosis. N. Engl. J. Med. 331:1286-1292.
15. Throckmorton, D.C., A.P. Brogden, B. Min, H. Rasmussen, and M. Kashgarian. 1995. PDGF and TGF-β mediate collagen production by mesangial cells exposed to advanced glycosylation end products. Kidney Int. 48:111-117.
16. Yang, C.W., H. Vlassara, E.P. Peten, C.J. He, G.E. Striker, and L.J. Striker. 1994. Advanced glycation end products up-regulate gene expression found in diabetic glomerular disease. Proc. Natl. Acad. Sci. USA. 91:9436-9440.
17. Kiff, R.J., S.M. Gardiner, A.M. Compton, and T. Bennett. 1991. The effects of endothelin-1 and NG-nitro-L-arginine methyl ester on regional haemodynamics in conscious rats with streptozotocin-induced diabetes mellitus. Br. J. Pharmacol. 103:1321-1326.
18. Bunag, R.D. 1973. Validation in awake rats of a tail-cuff method for measuring systolic pressure. J. Appl. Physiol. 34:279-282.
19. Schmidt, F.H. 1961. Enzymatic determination of glucose and fructose simultaneously. Klin. Wochenschr. 39:1244-1247.
20. Allen, T.J., M.E. Cooper, R.C. O'Brien, L.A. Bach, B. Jackson, and G. Jerums. 1990. Glomerular filtration rate in the streptozocin diabetic rat: The role of exchangeable sodium, vasoactive hormones and insulin therapy. Diabetes. 38:1182-1190.
21. Chomczynski, P., and N. Sacchi. 1987. Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
22. Skonier, J., K. Bennett, V. Rothwell, S. Kosowski, G. Plowman, P. Wallace, S. Edelhoff, C. Disteche, M. Neubauer, H. Marquardt, J. Rougers, et al. 1994. Beta ig-h3: a transforming growth factor beta responsive gene encoding a secreted protein that inhibits cell attachment in vitro and suppresses the growth of CHO cells in nude mice. DNA Cell Biol. 13:571-574.
23. Duncan, M.K., T. Shimamura, and K. Chada. 1994. Expression of the helix-loop-helix protein, ID, during branching morphogenesis in the kidney. Kidney Int. 46:324-332.
24. Gilbert, R.E., P.G. McNally, A. Cox, M. Dziadek, J.R. Rumble, M.E. Cooper, and G. Jerums. 1995. Gene expression of the anti-adhesive extracellular matrix protein secreted protein acidic and rich in cysteine (SPARC) is reduced in early diabetes related kidney growth. Kidney Int. 48:1216-1225.
25. Elias, J.M. 1990. Immunohistopathology: A Practical Approach to Diagnosis. ASCP Press, Chicago. 21-29.
26. Kranzhofer, R., J. Schirmer, A. Schomig, E. von Hodenberg, E. Pestel, J. Metz, H.J. Lang, and W. Kubler. 1993. Suppression of neointimal thickening and smooth muscle cell proliferation after arterial injury in the rat by inhibitors of Na(+)-H+ exchange. Circ. Res. 73(2):264-268.
27. Kakinuma, Y., T. Kawamura, T. Bills, T. Yoshiola, I. Ichikawa, and A. Fogo. 1992. Blood pressure independent effect of angiotensin inhibition on vascular lesions in chronic renal failure. Kidney Int. 42:46-55.
28. Floege, J., C.E. Alpers, M.W. Burns, P. Pritzl, K. Gordon, W.G. Couser, and R.J. Johnson. 1992. Glomerular cells, extracellular matrix accumulation, and the development of glomerulosclerosis in the remnant kidney model. Lab. Invest. 66:485-197.
29. Gugliucci, A., and M. Bendayan. 1996. Renal fate of circulating advanced glycated end products (AGE): evidence for reabsorption and catabolism of AGE-peptides by renal proximal tubular cells. Diabetologia. 39:149-160.
30. Soulis, T., M.E. Cooper, D. Vranes, R. Bucala, and G. Jerums. 1996. The effects of aminoguanidine in preventing experimental diabetic nephropathy are related to the duration of treatment. Kidney Int. 50:627-634.
31. Monnier, V.M., V.J. Stevens, and A. Cerami. 1981. Maillard reactions involving proteins and carbohydrates in vivo: Relevance to diabetes mellitus and aging. Prog. Food Nutr. Sci. 5:315-327.
32. O'Brien, E.R., K.L. Bennett, M.R. Garvin, T.W. Zderic, T. Hinohara, J.B. Simpson, T. Kimura, M. Nobuyoshi, H. Mizgala, A. Purchio, et al. 1996. Beta ig-h3. transforming growth factor-beta-inducible gene, is overexpressed in atherosclerotic and restenotic human vascular lesions. Arterioscler. Thromb. Vasc. Biol. 16:576-584.
33. Masson, P. 1929. Trichrome stainings and their preliminary technique. J. Tech. Methods. 2:75-90.
34. Snedecor, G.W., and W.O. Cochran. 1980. Statistical Methods. 7th ed. Iowa State University Press, Ames, Iowa. 228-236.
35. Brenner, B.M. 1983. Hemodynamically mediated glomerular injury and the progressive nature of kidney disease. Kidney Int. 23:647-655.
36. Sever-Hansen, K. 1983. Renal hypertrophy in experimental diabetes mellitus. Kidney Inf. 23:643-646.
37. Rasch, R. 1980. Prevention of diabetic glomerulopathy in streptozotocin diabetic rats by insulin treatment; albumin excretion. Diabetologia. 18:413-416.
38. Wasty, F., M.Z. Alavi, and S. Moore. 1993. Distribution of glycosaminoglycans in the intima of human aortas: changes in atherosclerosis and diabetes. Diabetologia. 36:316-322.
39. Dybdahl, H., and T. Ledet. 1987. Diabetic macroangiopathy. Quantitative histopathological studies of the extramural coronary arteries from type 2 (non-insulin-dependent) diabetic patients. Diabetologia. 30:882-886.
40. Hulthen, U.L., Z. Cao, J.R. Rumble, M.E. Cooper, and C.I. Johnston. 1996. Vascular hypertrophy and albumin permeability in a rat model combining hypertension and diabetes mellitus. Effects of calcium antagonism, angiotensin converting enzyme inhibition and angiotensin II AT-1 receptor blockade. Am. J. Hypertens. 9:895-901.
41. Gonzalez, J., and J. Fevery. 1992. Spontaneously diabetic biobreeding rats and impairment of bile acid-independent bile flow and increased biliary bilirubin, calcium and lipid secretion. Hepatology. 16:426-432.
42. Koschinsky, T., C. He, T. Mitsuhashi, C. Liu, C. Buenting, K. Heitmann, and H. Vlassara. 1996. Impaired clearance of toxic food-derived advanced glycation endproducts as a risk for diabetic nephropathy. Diabetologia. 39:(Suppl 1):A70(Abstr).
43. Ziyadeh, F.N., and K. Sharma. 1995. Role of transforming growth factor-β in diabetic glomerulosclerosis and renal hypertrophy. Kidney Int. 48:S34-S36.
44. Yokoyama, H., and T. Deckert. 1996. Central role of TGF-β in the pathogenesis of diabetic nephropathy and macrovascular complications: a hypothesis. Diabetic Med. 13:313-320.
45. MacKay, K., L.J. Striker, J.W. Stauffer, T. Doi, L.Y. Agoda, and G.E. Striker. 1989. Transforming growth factor-β. Murine glomerular receptors and responses of isolated glomerular cells. J. Clin. Invest. 83:1160-1167.
46. Sharma, K., Y. Jin, J. Guo, and F.N. Ziyadeh. 1996. Neutralization of TGF-beta by anti-TGF-beta antibody attenuates kidney hypertrophy and the enhanced extracellular matrix gene expression in STZ-induced diabetic mice. Diabetes. 45:522-530.
47. Koh, G.Y., S.-J. Kim, M.G. Klug, K. Park, M.H. Soonpaa, and L.J. Field. 1995. Targeted expression of transforming growth factor-β1 in intracardiac grafts promotes vascular endothelial cell DNA synthesis. J. Clin. Invest. 95: 114-121.
48. Vranes, D., R.J. Dilley, and M.E. Cooper. 1995. Diabetes asspciated vascular hypertrophy is associated with endothelial proliferation. Diabetologia. 38(Suppl 1):A255(Abstr).
49. Wysocki, S.J., M.-H. Zheng, Y. Fan, M.D. Lamawansa, A.K. House, and P.E. Norman. 1996. Expression of transforming growth factor-β1 (TGF-β1) and urokinase-type plasminogen activator (u-PA) genes during arterial repair in the pig. Cardiovasc. Res. 31:28-36.
50. Gibbons, G.H., R.E. Pratt, and V.J. Dzau. 1992. Vascular smooth muscle cell hypertrophy vs. hyperplasia. J. Clin. Invest. 90:456-461.
51. Ralph, D., M. McClelland, and J. Welsh. 1993. RNA fingerprinting using arbitrarily primed PCR identifies differentially regulated RNAs in mink lung (Mv1Lu) cells growth arrested by transforming growth factor beta 1. Proc. Natl. Acad. Sci. USA. 90:10710-10714.
52. Kagami, S., W.A. Border, D.E. Miller, and N.A. Noble. 1994. Angiotensin II stimulates extracellular matrix protein synthesis through induction of transforming growth factor-β expression in rat glomerular mesangial cells. J. Clin. Invest. 93:2431-2437.
53. Kim, S.-J., F. Denhez, K.-Y. Kim, T.J. Holt, M.B. Sporn, and A.B. Roberts. 1989. Activation of the second promoter of the transforming growth factor-β1 gene and phorbol ester occurs through the same target sequences. J. Biol. Chem. 264:19373-19378.
54. Wilson, E., K. Sudhir, and H.E. Ives. 1995. Mechanical strain of rat vascular smooth muscle cells is sensed by specific extracellular matrix/integrin interactions. J. Clin. Invest. 96:2364-2372.
55. Cohen, M.P., and F.N. Ziyadeh. 1996. Role of amadori-modified nonenzymatically glycated serum proteins in the pathogenesis of diabetic nephropathy. J. Am. Soc. Nephrol. 7:183-190.
56. Brownlee, M., H. Vlassara, and A. Cerami. 1985. Non-enzymatic glycosylation products on collagen covalently trap low-density lipoprotein. Diabetes. 34:938-941.
57. Hill, M.A., and E.A. Ege. 1994. Active and passive mechanical properties of isolated arterioles from STZ-induced diabetic rats: effect of aminoguanidine treatment. Diabetes. 43:1450-1456.
58. Bucala, R., K.J. Tracey, and A. Cerami. 1991. Advanced glyeosylation products quench nitric oxide and mediate defective endothelium-dependent vasodilatation in experimental diabetes. J. Clin. Invest. 87:432-438.
59. Vlassara, H., H. Fuh, Z. Makita, S. Krungkrai, A. Cerami, and R. Bucala. 1992. Exogenous advanced glycation end products induce complex vascular dysfunction in normal animals. Proc. Natl. Acad. Sci. USA. 89:12043-12047.
60. Huijberts, M.S.P., B.H.R. Wolffenbuttel, H.A.J. Struijker Boudier, F.R.L. Crijns, A.C. Nieuwenhuijzen Kruseman, P. Poitevin, and B.I. Levy. 1993. Aminoguanidine treatment increases elasticity and decreases fluid filtration of large arteries from diabetic rats. J. Clin. Invest. 92:1407-1411.
61. Schmidt, A.M., M. Vianna, M. Gerlach, J. Brett, J. Ryan, J. Kao, C. Esposito, H. Hegarty, W. Hurley, M. Clauss, et al. 1992. Isolation and characterisation of two binding proteins for advanced glycation end products from bovine lung which are present on the endothelial cell surface. J. Biol. Chem. 267: 14987-14997.
62. Vlassara, H. 1995. Receptors for advanced glycation endproducts: In vivo role and human studies. In Diabetes 1994. S. Baba and T. Kaneko, editors. Elsevier Science Publishing Co. Inc., New York. 286-291.
63. Schmidt, A.M., M. Hasu, D. Popov, J.H. Zhang, J. Chen, S.D. Van, J. Brett, R. Cao, K. Kuwabara, G. Costache, et al. 1994. Receptor for advanced glycation end products (AGEs) has a central role in vessel wall interactions and gene activation in response to circulating AGE proteins. Proc. Natl. Acad. Sci. USA. 91:8807-8811.
64. Corbett, J.A., R.G. Tilton, K. Chang, K.S. Hasan, Y. Ido, J.L. Wang, M.A. Sweetland, J.R. Lancaster Jr., J.R. Williamson, and M.L. McDaniel. 1992. Aminoguanidine, a novel inhibitor of nitric oxide formation, prevents diabetic vascular dysfunction. Diabetes. 41:552-556.
65. Tilton, R.G., K. Chang, K.S. Hasan, S.R. Smith, J.M. Petrash, T.P. Misko, W.M. Moore, M.G. Currie, J.A. Corbett, M.L. McDaniel, et al. 1993. Prevention of diabetic vascular dysfunction by guanidines: Inhibition of nitric oxide synthase versus advanced glycation end-product formation. Diabetes. 42: 221-232.
66. Komers, R., T.J. Allen, and M.E. Cooper. 1994. Role of endothelium-derived nitric oxide in the pathogenesis of the renal hemodynamic changes of experimental diabetes. Diabetes. 43:1190-1197.
67. Cooper, M.E., T.J. Allen, R.C. O'Brien, D. Papazoglou, B. Clarke, G. Jerums, and A.E. Doyle. 1990. Nephropathy in a model combining genetic hypertension with experimental diabetes: Enalapril versus hydralazine and metoprolol therapy. Diabetes. 39:1575-1579.
68. Rumble, J.R., A.E. Doyle, and M.E. Cooper. 1995. Comparison of effects of ACE inhibition with calcium channel blockade on renal disease in a model combining genetic hypertension with diabetes. Am. J. Hypertens. 8:53-57.
69. Fukui, M., T. Nakamura, I Ebihara, Y. Makita, S. Osada, Y. Tomino, and H. Koide. 1994. Effects of enalapril on endothelin-1 and growth factor gene expression in diabetic rat glomeruli. J. Lab. Clin. Med. 123:763-768.
70. Nakamura, T., T. Takahashi, M. Fukui, I. Ebihara, S. Osada, Y. Tomino, and H. Koide. 1995. Enalapril attenuates increased gene expression of extracellular matrix components in diabetic rats. J. Am. Soc. Nephrol. 5:1492-1497.
71. Li, Y.M., Steffes T. Donnelly, C. Liu, H. Fuh, J. Basgen, R. Bucala, and H. Vlassara. 1996. Prevention of cardiovascular and renal pathology of aging by the advanced glycation inhibitor aminoguanidine. Proc. Natl. Acad. Sci. USA. 93:3902-3907.
72. Jerums, G., T. Soulis, S. Panagiotopoulos, and M.E. Cooper. 1995. In vivo effects of aminoguanidine in experimental diabetes and atherosclerosis. In Diabetes 1994. S. Baba and T. Kaneko, editors. Elsevier Science Publishing Co. Inc., New York. 299-305.