Methylglyoxal administration induces diabetes-like microvascular changes and perturbs the healing process of cutaneous wounds

Clinical Science

Volumn 109, Issue 1, 2005, Pages 83-95

  Berlanga, Jorge ^a   Cibrian, Danay ^a   Guillén, Isabel ^a   Freyre, Freya ^a   Alba, José S ^a   Lopez Saura, Pedro ^a   Merino, Nelson ^b   Aldama, Alfredo ^c   Quintela, Ana M ^c   Triana, Maria E ^c   Montequin, Jose F ^c   Ajamieh, Hussam ^b   Urquiza, Dioslaida ^a   Ahmed, Naila ^d   Thornalley, Paul J ^d  

^a CENTER FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Cuba)

^b UNIVERSITY OF HAVANA   (Cuba)

^c National Institute of Angiology and Vascular Surgery   (Cuba)

^d UNIVERSITY OF ESSEX   (United Kingdom)

Author keywords

Diabetes; Diabetic complication; Glycation; Methylglyoxal; Wound healing

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCT RECEPTOR; CONNECTIVE TISSUE GROWTH FACTOR; CREATININE; GLYCERYL TRINITRATE; INTERLEUKIN 1BETA; METHYLGLYOXAL; PROTEIN; SODIUM CHLORIDE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANGIOGENESIS; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; BLOOD VESSEL OCCLUSION; CELL PROLIFERATION; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DIABETES MELLITUS; DIABETIC MICROANGIOPATHY; ENDOTHELIUM CELL; EPIDERMIS; FIBROSIS; GRANULATION TISSUE; HYPERCHOLESTEROLEMIA; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MICROANGIOPATHY; NERVE FIBER; NONHUMAN; PERIPHERAL NERVE; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; RAT; SKIN BLOOD VESSEL; SKIN INJURY; VASODILATATION; WOUND HEALING IMPAIRMENT;

ANIMALS; BLOOD GLUCOSE; CHOLESTEROL; DIABETIC ANGIOPATHIES; DISEASE MODELS, ANIMAL; FRUCTOSAMINE; INJECTIONS, INTRAPERITONEAL; INTERLEUKIN-1; MALE; MICROCIRCULATION; NEOVASCULARIZATION, PATHOLOGIC; PYRUVALDEHYDE; RANDOM ALLOCATION; RATS; RATS, WISTAR; SKIN; TRIGLYCERIDES; TUMOR NECROSIS FACTOR-ALPHA; VASODILATION; WOUND HEALING;

EID: 21744448064     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20050026     Document Type: Article

References (50)

1. Zimmet, P., Alberti, K. G. and Shaw, J. (2002) Global and societal implications of the diabetes epidemic. Nature (London) 414, 782-787
2. Brownlee, M. (2001) Biochemistry and molecular cell biology of diabetic complications. Nature (London) 414, 813-820
3. Greenhalgh, D. G. (2003) Wound healing and diabetes mellitus. Clin. Plastic Surg. 30, 37-45
4. The Diabetes Control and Complications Trial Research Group (1993) The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. New Engl. J. Med. 327, 977-986
5. Stratton, I. M., Adler, I. A., Neil, H. A. W. et al. (2002) Association of glycaemic with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): prospective observational study. Br. Med. J. 321, 405-412
6. Ha, H., Yu, R. M., Choi, J. Y., Kitamura, M. and Lee, H. B. (2002) Role of high glucose induced nuclear factor-kB activation in monocyte chemoattractant protein-1 expression by mesangial cells. J. Am. Soc. Nephrol. 13, 894-902
7. Phillips, S. A. and Thornalley, P. J. (1993) The formation of methylglyoxal from triose phosphates. Investigation using a specific assay for methylglyoxal. Eur. J. Biochem. 212, 101-105
8. Thornalley, P. J. (1998) Glutathione-dependent detoxification of α-oxoaldehydes by the glyoxalase system: involvement in disease mechanisms and antiproliferative activity of glyoxalase I inhibitors. Chem. Biol. Interact. 111-112, 137-151
9. Thornalley, P. J. (1998) Modification of the glyoxalase system in human red blood cells by glucose in vitro. Biochem. J. 254, 751-755
10. Du, X., Matsumara, T., Edelsttein, D. et al. (2003) Inhibition of GAPDH activity by poly (ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells. J. Clin. Invest. 112, 1049-1057
11. McLellan, A. C., Thornalley, P. J., Benn, J. and Sonksen, P. H. (1994) The glyoxalase system in clinical diabetes mellitus and correlation with diabetic complications. Clin. Sci. 87, 21-29
12. Nishikawa, T., Edelstein, D., Liang, D. X. et al. (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemia damage. Nature (London) 404, 787-790
13. Abordo, E. A., Minhas, H. S. and Thornalley, P. J. (1999) Accumulation of α-oxoaldehydes during oxidative stress. A role in cytotoxicity. Biochem. Pharmacol. 58, 641-648
14. Thornalley, P. J. (2003) Glyoxalase I: structure, function and a critical role in the enzymatic defence against glycation. Biochem. Soc. Trans. 31, 1343-1348
15. Ahmed, N., Argirov, O. K., Minhas, H. S., Cordeiro, C. A. and Thornalley, P. J. (2002) Assay of advanced glycation endproducts (AGEs): surveying AGEs by chromatographic assay with derivatisation by aminoquinolyl-N-hydroxysuccimidyl- carbamate and application to Nε-carboxymethyl-lysine- and Nε-(1-carboxyethyl) lysine-modified albumin. Biochem. J. 364, 1-14
16. Thornalley, P. J., Battah, S., Ahmed, N. et al. (2003) Quantitative screening of advanced glycation endproducts in cellular and extracellular proteins by tandem mass spectrometry. Biochem. J. 375, 581-592
17. Thornalley, P. J. (2003) Use of aminoguanidine (Pimagedine) to prevent the formation of advanced glycation endproducts. Arch. Biochem. Biophys. 419, 31-40
18. Babaei-Jadidi, R., Karachalias, N., Ahmed, N., Battah, S. and Thornalley, P. J. (2003) Prevention of incipient diabetic nephropathy by high dose thiamine and Benfotiamine. Diabetes 52, 2110-2120
19. Golej, J., Hoeger, H., Radner, W., Unfried, G. and Lubec, G. (1998) Oral administration of methylglyoxal leads to kidney collagen accumulation in the mouse. Life Sci. 63, 801-807
20. Canapp, Jr, S. O., Farese, J. P., Schultz, G. S. et al. (2003) The effect of topical tripeptide-copper complex on healing of ischemic open wounds. Vet. Surg. 32, 515-523
21. Berlanga, J., Lodos, J., Labarta, V. P. et al. (1997) The effect of epidermal growth factor treatment schedule on the healing of full-thickness wounds in pigs. Biotecnología Aplicada 14, 163-168
22. Berlanga, J., Moreira, E., Pérez, L. C., Boix, E., González, T. and López-Saura, P. (1996) Wound healing promotion in rats is EGF dose dependent. Biotecnología Aplicada 13, 181-185
23. Donohue, K. and Falanga, V. (2003) Healing rate as a prognostic indicator of complete healing: a reappraisal. Wounds 15, 71-76
24. Aldama, A., Jhones, C., Riera, Y., Viada, C., Jiménez, G. and Rodríguez, J. (2001) Evaluación clínica del pletismógrafo digital Angiodin PD 3000: estudio fase II. Rev. Cub. Invest. Biomed. 20, 276-286
25. Westwood, M. E., Argirov, O. K., Abordo, E. A. and Thornalley, P. J. (1997) Methylglyoxal modified arginine residues: a signal for receptor-mediated endocytosis and degradation of proteins by monocytic THP-1 cells. Biochim. Biophys. Acta 1356, 84-94
26. Horiuchi, S., Araki, N. and Morin, Y. (1991) Immunochemical approach to characterize advanced glycation end products of the Maillard reaction. J. Biol. Chem. 266, 7329-7332
27. Nagai, R., Thornalley, P. J., Jono, T. and Horiuchi, S. (1999) Detection of Nε-(carboxyethyl) lysine in glucose-modified age-proteins: implication of an important role of methylglyoxal as an active intermediate in AGE formation. Diabetes. 48 (Suppl. 1), A32
28. Jerzykowski, T., Matuszeski, W, Tarnawski, R., Winter, R., Herman, Z. S. and Sokola, A. (1975) Changes of certain pharmacological and biochemical indices in acute methylglyoxal poisoning. Arch. Immunol. Ther. Exp. 23, 549-560
29. Conroy, P. J. (1979) Carcinostatic activity of methylglyoxal and related substances in tumour-bearing mice. In Submolecular Biology and Cancer, vol. 67, pp. 271-298, Ciba Foundation Symposium, Excerpta Medica, Amsterdam
30. Sheader, E. A., Benson, R. S. and Best, L. (2001) Cytotoxic action of methylglyoxal on insulin-secreting cells. Biochem. Pharmacol. 61, 1381-1386
31. Cook, L. J., Davies, J., Yates, A. P. et al. (1998) Effects of methylglyoxal on rat pancreatic β-cells. Biochem. Pharmacol. 55, 1361-1367
32. Ahmed, N. and Thornalley, P. J. (2002) Chromatographic assay of glycation adducts in human serum albumin glycated in vitro by derivatisation with aminoquinolyl-N-hydroxysuccimidyl-carbamate and intrinsic fluorescence. Biochem. J. 364, 15-24
33. Schalkwijk, C. G., Vermeer, M. A., Stehouwer, C. D. A., te Koppele, J., Princen, H. M. G. and van Hinsbergh, V. W. M. (1998) Effect of methylglyoxal on the physicochemical and biological properties of low-density lipoprotein. Biochim. Biophys. Acta 1394, 187-198
34. Rashid, G., Benchetrit, S., Fishman, D. and Bernheim, J. (2004) Effect of advanced glycation end-products on gene expression and synthesis of TNF-α and endothelial nitric oxide synthase by endothelial cells. Kidney Int. 66, 1099-1106
35. El-seweidy, M. M., El-Swefy, S. E., Ameen, R. S. and Hazme, R. M. (2002) Effect of age receptor blocker and/or anti-inflammatory coadministration in relation to glycation, oxidative stress and cytokine production in STZ diabetic rats. Pharmacol. Res. 45, 391-398
36. Kislinger, T., Tanji, N., Wendt, T. et al. (2001) Receptor for advanced glycation end products mediates inflammation and enhanced expression of tissue factor in vasculature of diabetic apolipoprotem E-null mice. Arteriosler., Thromb., Vasc. Biol. 21, 905-910
37. Hofmann, M. A., Drury, S., Fu, C. F. et al. (1999) RAGE mediates a novel pro-inflammatory axis: A central cell surface receptor for S100/calgranulin polypeptides. Cell 97, 889-901
38. Treutiger, C. J., Mullins, G. E., Johansson, A. S. M. et al. (2003) High mobility group 1 B-box mediates activation of human endothelium. J. Intern. Med. 254, 375-385
39. Goova, M. T., Li, J., Kislinger, T., Qu, W. et al. (2001) Blockade of receptor for advanced glycation end-products restores effective wound healing in diabetic mice. Am. J. Pathol. 159, 513-525
40. Lalla, E., Lamster, I. B., Feit, M. et al. (2000) Blockade of RAGE suppresses periodontitis associated bone loss in diabetic mice. J. Clin. Invest. 105, 1117-1124
41. Chen, C., Schultz, G. S., Bloch, M., Edwards, P. D., Tebes, S. and Mast, B. A. (1997) Molecular and mechanistic validation of delayed healing rat wounds as a model for chronic human wounds. Wound Rep. Reg. 7, 486-494
42. Maish, G. O., Shumate, M. L., Ehrlich, H. P., Vary, T. C. and Cooney, R. N. (1999) Interleukin-1 receptor antagonist attenuates tumor necrosis factor-induced alterations in wound breaking strength. J. Trauma: Inj. Infect. Crit. Care 47, 533-537
43. Portero-Otin, M., Pamplona, R., Bellmunt, M. J. A. et al. (2002) Advanced glycation end product precursors impair epidermal growth factor receptor signaling. Diabetes 51, 1535-1542
44. Twigg, S. M., Joly, A. H., Chen, M. M. et al. (2002) Connective tissue growth factor/IGF-binding protein-related protein-2 is a mediator in the induction of fibronectin by advanced glycosylation end-products in human dermal fibroblasts. Endocrinology 143, 1260-1269
45. Bucala, R., Tracey, K. and Cerami, A. (1991) Advanced glycosylation products quench nitric oxide and mediate defective endothelium-dependent vasodilation in experimental diabetes. J. Clin. Invest. 87, 432-438
46. Wang, S. N. and Hirschberg, R. (2003) BMP7 antagonizes TGF-β-dependent fibrogenesis in mesangial cells. Am. J. Physiol. Renal Physiol. 284, F1006-F1013
47. Weston, B. S., Wahab, N. A. and Mason, R. M. (2003) CTGF mediates TGF-β-induced fibronectin matrix deposition by upregulating active α5β1 integrin in human mesangial cells. J. Am. Soc. Nephrol. 14, 601-610
48. Uesugi, N., Sakata, N., Nagai, R., Jono, T., Horiuchi, S. and Takebayashi, S. (2000) Glycoxidative modification of AA amyloid deposits in renal tissue. Nephrol., Dialysis Transplant. 15, 355-365
49. Rocken, C., Kientsch-Engel, R., Mansfeld, S. et al. (2003) Advanced glycation end products and receptor for advanced glycation end products in AA amyloidosis. Am. J. Pathol. 162, 1213-1220
50. Yan, S. D., Zhu, H. J., Zhu, A. P. et al. (2000) Receptor-dependent cell stress and amyloid accumulation in systemic amyloidosis. Nat. Med. 6, 643-651