Substrates modified by advanced glycation end-products cause dysfunction and death in retinal pericytes by reducing survival signals mediated by platelet-derived growth factor

Diabetologia

Volumn 47, Issue 10, 2004, Pages 1735-1746

  Stitt, A W ^a   Hughes, S J ^a   Canning, P ^a   Lynch, O ^a   Cox, O ^a   Frizzell, N ^a   Thorpe, S R ^b   Cotter, T G ^c   Curtis, T M ^a   Gardiner, T A ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b UNIVERSITY OF SOUTH CAROLINA   (United States)

^c UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Advanced glycation; Apoptosis; Basement membrane; Diabetic retinopathy; Platelet derived growth factor; Retinal pericytes

Indexed keywords

ADVANCED GLYCATION END PRODUCT; MESSENGER RNA; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BASEMENT MEMBRANE; BIOASSAY; CATTLE; CELL DEATH; CELL GROWTH; CELL ISOLATION; CELL PROLIFERATION; CHEMICAL MODIFICATION; CONTROLLED STUDY; CYTOPATHOLOGY; DIABETIC RETINOPATHY; IN VITRO STUDY; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE; NICK END LABELING; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; RETINA CAPILLARY; RETINA CELL; SIGNAL TRANSDUCTION;

ANIMALS; BASEMENT MEMBRANE; CATTLE; CELL SURVIVAL; GLYCOSYLATION END PRODUCTS, ADVANCED; PERICYTES; PLATELET-DERIVED GROWTH FACTOR; RETINA; RETINAL VESSELS; SIGNAL TRANSDUCTION;

EID: 19944367877     PISSN: 0012186X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00125-004-1523-3     Document Type: Article

References (57)

1. Hirschi KK, D'Amore PA (1996) Pericytes in the microvasculature. Cardiovasc Res 32:687-698
2. Wu DM, Kawamura H, Sakagami K, Kobayashi M, Puro DG (2003) Cholinergic regulation of pericyte-containing retinal microvessels. Am J Physiol Heart Circ Physiol 284:H2083-H2090
3. Kelley C, D'Amore P, Hechtman HB, Shepro D (1987) Microvascular pericyte contractility in vitro: comparison with other cells of the vascular wall. J Cell Biol 104:483-490
4. D'Amore PA, Smith SR (1993) Growth factor effects on cells of the vascular wall: a survey. Growth Factors 8:61-75
5. Garner A (1993) Histopathology of diabetic retinopathy in man. Eye 7:250-253
6. Li W, Yanoff M, Liu X, Ye X (1997) Retinal capillary pericyte apoptosis in early human diabetic retinopathy. Chin Med J (Engl) 110:659-663
7. Podesta F, Romeo G, Liu WH et al. (2000) Bax is increased in the retina of diabetic subjects and is associated with pericyte apoptosis in vivo and in vitro. Am J Pathol 156:1025-1032
8. Kern TS, Tang J, Mizutani M et al. (2000) Response of capillary cell death to aminoguanidine predicts the development of retinopathy: comparison of diabetes and galactosemia. Invest Ophthalmol Vis Sci 41:3972-3978
9. Murata M, Ohta N, Fujisawa S et al. (2002) Selective pericyte degeneration in the retinal capillaries of galactose-fed dogs results from apoptosis linked to aldose reductase-catalyzed galactitol accumulation. J Diabetes Complications 16:363-370
10. Miwa K, Nakamura J, Hamada Y et al. (2003) The role of polyol pathway in glucose-induced apoptosis of cultured retinal pericytes. Diabetes Res Clin Pract 60:1-9
11. Yamagishi S, Amano S, Inagaki Y et al. (2002) Advanced glycation end products-induced apoptosis and overexpression of vascular endothelial growth factor in bovine retinal pericytes. Biochem Biophys Res Commun 290:973-978
12. Stitt AW, Jenkins AJ, Cooper ME (2002) Advanced glycation end products and diabetic complications. Expert Opin Investig Drugs 11:1205-1223
13. Hammes HP (2003) Pathophysiological mechanisms of diabetic angiopathy. J Diabetes Complications 17:16-19
14. Baynes JW, Thorpe SR (2000) Glycoxidation and lipoxidation in atherogenesis. Free Radie Biol Med 28:1708-1716
15. Stitt AW, Li YM, Gardiner TA, Bucala R, Archer DB, Vlassara H (1997) Advanced glycation end products (AGEs) co-localize with AGE receptors in the retinal vasculature of diabetic and of AGE-infused rats. Am J Pathol 150:523-531
16. Stitt A, Gardiner TA, Alderson NL et al. (2002) The AGE inhibitor pyridoxamine inhibits development of retinopathy in experimental diabetes. Diabetes 51:2826-2832
17. Hammes HP, Alt A, Niwa T et al. (1999) Differential accumulation of advanced glycation end products in the course of diabetic retinopathy. Diabetologia 42:728-736
18. Frisch SM, Ruoslahti E (1997) Integrins and anoikis. Curr Opin Cell Biol 9:701-706
19. Cardone MH, Roy N, Stennicke HR et al. (1998) Regulation of cell death protease caspase-9 by phosphorylation. Science 282:1318-1321
20. Bailey AJ (2001) Molecular mechanisms of ageing in connective tissues. Mech Ageing Dev 122:735-755
21. Chakravarthy U, Gardiner TA (1999) Endothelium-derived agents in pericyte function/dysfunction. Prog Retin Eye Res 18:511-527
22. Hart CE, Forstrom JW, Kelly JD et al. (1988) Two classes of PDGF receptor recognize different isoforms of PDGF. Science 240:1529-1531
23. Matsui T, Pierce JH, Fleming TP et al. (1989) Independent expression of human alpha or beta platelet-derived growth factor receptor cDNAs in a naive hematopoietic cell leads to functional coupling with mitogenic and chemotactic signaling pathways. Proc Natl Acad Sci USA 86:8314-8318
24. Rosenkranz S, Kazlauskas A (1999) Evidence for distinct signaling properties and biological responses induced by the PDGF receptor alpha and beta subtypes. Growth Factors 16:201-216
25. Lindahl P, Johansson BR, Leveen P, Betsholtz C (1997) Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 277:242-245
26. Bostrom H, Willetts K, Pekny M et al. (1996) PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 85:863-873
27. Soriano P (1994) Abnormal kidney development and hematological disorders in PDGF beta-receptor mutant mice. Genes Dev 8:1888-1896
28. Hammes HP, Lin J, Renner O et al. (2002) Pericytes and the pathogenesis of diabetic retinopathy. Diabetes 51:3107-3112
29. Enge M, Bjarnegard M, Gerhardt H et al. (2002) Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy. EMBO J 21:4307-4316
30. Chakravarthy U, Stitt AW, McNally J, Bailie JR, Hoey EM, Duprex P (1995) Nitric oxide synthase activity and expression in retinal capillary endothelial cells and pericytes. Curr Eye Res 14:285-294
31. Yamagishi S, Yonekura H, Yamamoto Y et al. (1997) Advanced glycation end products-driven angiogenesis in vitro. Induction of the growth and tube formation of human microvascular endothelial cells through autocrine vascular endothelial growth factor. J Biol Chem 272:8723-8730
32. Nagai R, Matsumoto K, Ling X, Suzuki H, Araki T, Horiuchi S (2000) Glycolaldehyde, a reactive intermediate for advanced glycation end products, plays an important role in the generation of an active ligand for the macrophage scavenger receptor. Diabetes 49:1714-1723
33. Shaw JN, Baynes JW, Thorpe SR (2002) N epsilon-(carboxymethyl)lysine (CML) as a biomarker of oxidative stress in long-lived tissue proteins. Methods Mol Biol 186:129-137
34. Stegemann H, Stalder K (1967) Determination of hydroxyproline. Clin Chim Acta 18:267-273
35. Simpson DA, Feeney S, Boyle C, Stitt AW (2000) Retinal VEGF mRNA measured by SYBR green I fluorescence: a versatile approach to quantitative PCR. Mol Vis 6:178-183
36. Diaz G, Setzu MD, Zucca A et al. (1999) Subcellular heterogeneity of mitochondrial membrane potential: relationship with organelle distribution and intercellular contacts in normal, hypoxic and apoptotic cells. J Cell Sci 112:1077-1084
37. Hammes HP, Wellensiek B, Kloting I, Sickel E, Bretzel RG, Brownlee M (1998) The relationship of glycaemic level to advanced glycation end-product (AGE) accumulation and retinal pathology in the spontaneous diabetic hamster. Diabetologia 41:165-170
38. Gardiner TA, Anderson HR, Stitt AW (2003) AGE-inhibition protects against retinal capillary basement membrane thickening during long-term diabetes. J Pathol 201:328-333
39. Cox O, Stitt AW, Simpson DA, Gardiner TA (2003) Sources of PDGF expression in murine retina and the effect of short-term diabetes. Mol Vis 10:665-672
40. Degenhardt TP, Alderson NL, Arlington DD et al. (2002) Pyridoxamine inhibits early renal disease and dyslipidemia in the streptozotocin-diabetic rat. Kidney Int 61:939-950
41. Chibber R, Molinatti PA, Wong JS, Mirlees D, Kohner EM (1994) The effect of aminoguanidine and tolrestat on glucose toxicity in bovine retinal capillary pericytes. Diabetes 43:758-763
42. Ruggiero-Lopez D, Rellier N, Lecomte M, Lagarde M, Wiemsperger N (1997) Growth modulation of retinal microvascular cells by early and advanced glycation products. Diabetes Res Clin Pract 34:135-142
43. Sharma NK, Gardiner TA, Archer DB (1985) A morphologic and autoradiographic study of cell death and regeneration in the retinal microvasculature of normal and diabetic rats. Am J Ophthalmol 100:51-60
44. Denis U, Lecomte M, Paget C, Ruggiero D, Wiernsperger N, Lagarde M (2002) Advanced glycation end-products induce apoptosis of bovine retinal pericytes in culture: involvement of diacylglycerol/ceramide production and oxidative stress induction. Free Rad Biol Med 33:236-247
45. Yamagishi S, Okamoto T, Amano S et al. (2002) Palmitate-induced apoptosis of microvascular endothelial cells and pericytes. Mol Med 8:179-184
46. Yamagishi S, Amano S, Inagaki Y, Okamoto T, Takeuchi M, Makita Z (2002) Beraprost sodium, a prostaglandin 12 analogue, protects against advanced gycation end products-induced injury in cultured retinal pericytes. Mol Med 8:546-550
47. Yamagishi S, Inagaki Y, Amano S, Okamoto T, Takeuchi M, Makita Z (2002) Pigment epithelium-derived factor protects cultured retinal pericytes from advanced glycation end product-induced injury through its antioxidative properties. Biochem Biophys Res Commun 296:877-882
48. Iozzo RV, San Antonio JD (2001) Heparan sulfate proteoglycans: heavy hitters in the angiogenesis arena. J Clin Invest 108:349-355
49. Vlodavsky I, Miao HQ, Medalion B, Danagher P, Ron D (1996) Involvement of heparan sulfate and related molecules in sequestration and growth promoting activity of fibroblast growth factor. Cancer Metastasis Rev 15:177-186
50. Boyd-White J, Williams JC Jr (1996) Effect of cross-linking on matrix permeability. A model for AGE-modified basement membranes. Diabetes 45:348-353
51. Mott JD, Khalifah RG, Nagase H, Shield CF 3rd, Hudson JK, Hudson BG (1997) Nonenzymatic glycation of type IV collagen and matrix metalloproteinase susceptibility. Kidney Int 52:1302-1312
52. Sensi M, Tanzi P, Bruno MR et al. (1989) Nonenzymic glycation of isolated human glomerular basement membrane changes its physicochemical characteristics and binding properties. Nephron 52:222-226
53. Kuzuya M, Satake S, Ai S et al. (1998) Inhibition of angiogenesis on glycated collagen lattices. Diabetologia 41:491-499
54. Beltramo E, Pomero F, Allione A, D'Alu F, Ponte E, Porta M (2002) Pericyte adhesion is impaired on extracellular matrix produced by endothelial cells in high hexose concentrations. Diabetologia 45:416-419
55. Beltramo E, Buttiglieri S, Pomero F et al. (2003) A study of capillary pericyte viability on extracellular matrix produced by endothelial cells in high glucose. Diabetologia 46:409-415
56. Giardino I, Edelstein D, Brownlee M (1994) Nonenzymatic glycosylation in vitro and in bovine endothelial cells alters basic fibroblast growth factor activity. A model for intracellular glycosylation in diabetes. J Clin Invest 94:110-117
57. Taylor CC (2000) Platelet-derived growth factor activates porcine thecal cell phosphatidylinositol-3-kinase-Akt/PKB and ras-extracellular signal-regulated kinase-1/2 kinase signaling pathways via the platelet-derived growth factor-beta receptor. Endocrinology 141:1545-1553