Receptor for advanced glycation end products is involved in impaired angiogenic response in diabetes

Diabetes

Volumn 55, Issue 8, 2006, Pages 2245-2255

  Shoji, Takuhito ^a   Koyama, Hidenori ^a   Morioka, Tomoaki ^a   Tanaka, Shinji ^a   Kizu, Akane ^a   Motoyama, Kohka ^a   Mori, Katsuhito ^a   Fukumoto, Shinya ^a   Shioi, Atsushi ^a   Shimogaito, Noriko ^b   Takeuchi, Masayoshi ^b   Yamamoto, Yasuhiko ^c   Yonekura, Hideto ^c   Yamamoto, Hiroshi ^c   Nishizawa, Yoshiki ^a  

^a OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b HOKURIKU UNIVERSITY   (Japan)

^c KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

Author keywords

SM actin, smooth muscle actin; Ad esRAGE, pAdHM15 esRAGE; AGE, advanced glycation end product; CML, N carboxymethyllysine; esRAGE, endogenous secretory RAGE; MMP, matrix metalloproteinase; NF B, nuclear factor B

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; MATRIGEL; MESSENGER RNA; ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCOSYLATION END PRODUCT RECEPTOR; ADVANCED GLYCOSYLATION END-PRODUCT RECEPTOR; ANGIOPOIETIN 1; ANGIOPOIETIN 2; COLLAGEN; CYCLINE; GELATINASE A; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN RECEPTOR; LAMININ; PROTEOGLYCAN; THROMBOSPONDIN 1; VASCULOTROPIN A;

ADENOVIRUS VECTOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; DIABETES MELLITUS; DIABETOGENESIS; ENDOTHELIUM CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN SECRETION; SMOOTH MUSCLE FIBER; ADENOVIRUS; ANGIOGENESIS; ANIMAL; APOPTOSIS; BLOOD; C57BL MOUSE; CELL COUNT; CELL DIVISION; CYTOLOGY; DRUG COMBINATION; DRUG IMPLANT; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; PATHOPHYSIOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VASCULAR SMOOTH MUSCLE;

ADENOVIRIDAE; ANGIOPOIETIN-1; ANGIOPOIETIN-2; ANIMALS; APOPTOSIS; CELL COUNT; CELL DIVISION; COLLAGEN; DIABETES MELLITUS, EXPERIMENTAL; DRUG COMBINATIONS; DRUG IMPLANTS; ENDOTHELIAL CELLS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GLYCOSYLATION END PRODUCTS, ADVANCED; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; LAMININ; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; MUSCLE, SMOOTH, VASCULAR; NEOVASCULARIZATION, PHYSIOLOGIC; NF-KAPPA B; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEOGLYCANS; RECEPTORS, IMMUNOLOGIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THROMBOSPONDIN 1; TRANSFECTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 33749327828     PISSN: 00121797     EISSN: 00121797     Source Type: Journal    
DOI: 10.2337/db05-1375     Document Type: Article

References (45)

1. Brownlee M: Biochemistry and molecular cell biology of diabetic complications. Nature 414:813-820, 2001
2. Mizutani M, Kern TS, Lorenzi M: Accelerated death of retinal microvascular cells in human and experimental diabetic retinopathy. J Clin Invest 97:2883-2890, 1996
3. Stitt A, Gardiner TA, Anderson NL, Canning P, Frizzell N, Duffy N, Boyle C, Januszewski AS, Chachich M, Baynes JW, Thorpe SR: The AGE inhibitor pyridoxamine inhibits development of retinopathy in experimental diabetes. Diabetes 51:2826-2832, 2002
4. Hammes HP, Du X, Edelstein D, Taguchi T, Matsumura T, Ju Q, Lin J, Bierhaus A, Nawroth P, Hannak D, Neumaier M, Bergfeld R, Giardino I, Brownlee M: Benfotiamine blocks three major pathways of hyperglycemic damage and prevents experimental diabetic retinopathy. Nat Med 9:294-299, 2003
5. Abaci A, Oguzhan A, Kahraman S, Eryol NK, Unal S, Arinc H, Ergin A: Effect of diabetes mellitus on formation of coronary collateral vessels. Circulation 99:2239-2242, 1999
6. Rivard A, Silver M, Chen D, Kearney M, Magner M, Annex B, Peters K, Isner JM: Rescue of diabetes-related impairment of angiogenesis by intramuscular gene therapy with adeno-VEGF. Am J Pathol 154:355-363, 1999
7. Waltenberger J: Impaired collateral vessel development in diabetes: potential cellular mechanisms and therapeutic implications. Cardiovasc Res 49:554-560, 2001
8. Stitt AW, McGoldrick C, Rice-McCaldin A, McCance DR, Glenn JV, Hsu DK, Liu F-T, Thorpe SR, Gardiner TA: Impaired retinal angiogenesis in diabetes: role of advanced glycation end products and galectin-3. Diabetes 54:785-794, 2005
9. Neeper M, Schmidt AM, Brett J, Yan SD, Wang F, Pan YC, Elliston K, Stern D, Shaw A: Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J Biol Chem 267:14998-15004, 1992
10. Schmidt AM, Yan SD, Yan SF, Stern DM: The biology of the receptor for advanced glycation end products and its ligands. Biochim Biophys Acta 1498:99-111, 2000
11. Schmidt AM, Hori O, Chen JX, Li JF, Crandall J, Zhang J, Cao R, Yan SD, Brett J, Stern D: Advanced glycation endproducts interacting with their endothelial receptor induce expression of vascular cell adhesion molecule-1 (VCAM-1) in cultured human endothelial cells and in mice: a potential mechanism for the accelerated vasculopathy of diabetes. J Clin Invest 96:1395-1403, 1995
12. Basta G, Lazzerini G, Massaro M, Simoncini T, Tanganelli P, Fu C, Kislinger T, Stern DM, Schmidt AM, De Caterina R: Advanced glycation end products activate endothelium through signal-transduction receptor RAGE: a mechanism for amplification of inflammatory responses. Circulation 105:816-822, 2002
13. Yamamoto Y, Kato I, Doi T, Yonekura H, Ohashi S, Takeuchi M, Watanabe T, Yamagishi S, Sakurai S, Takasawa S, Okamoto H, Yamamoto H: Development and prevention of advanced diabetic nephropathy in RAGE-overexpressing mice. J Clin Invest 108:261-268, 2001
14. Yan SF, Ramasamy R, Naka Y, Schmidt AM: Glycation, inflammation, and RAGE: a scaffold for the macrovascular complications of diabetes and beyond. Circ Res 93:1159-1169, 2003
15. Nawroth P, Bierhaus A, Marrero M, Yamamoto H, Stern DM: Atherosclerosis and restenosis: is there a role for RAGE? Curr Diab Rep 5:11-16, 2005
16. Kuzuya M, Satake S, Ai S, Asai T, Kanda S, Ramos MA, Miura H, Ueda M, Iguchi A: Inhibition of angiogenesis on glycated collagen lattices. Diabetologia 41:491-499, 1998
17. Yamagishi S, Yonekura H, Yamamoto Y, Katsuno K, Sato F, Mita I, Ooka H, Satozawa N, Kawakami T, Nomura M, Yamamoto H: 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, 1997
18. Tamarat R, Silvestre JS, Huijberts M, Benessiano J, Ebrahimian TG, Duriez M, Wautier MP, Wautier JL, Levy BI: Blockade of advanced glycation end-product formation restores ischemia-induced angiogenesis in diabetic mice. Proc Natl Acad Sci U S A 100:8555-8560, 2003
19. Goova MT, Li J, Kislinger T, Qu W, Lu Y, Bucciarelli LG, Nowygrod S, Wolf BM, Caliste X, Yan SF, Stern DM, Schmidt AM: Blockade of receptor for advanced glycation end-products restores effective wound healing in diabetic mice. Am J Pathol 159:513-525, 2001
20. Yamamoto Y, Doi T, Kato I, Shinohara H, Sakurai S, Yonekura H, Watanabe T, Myint KM, Harashima A, Takeuchi M, Takasawa S, Okamoto H, Hashimoto N, Asano M, Yamamoto H: Receptor for advanced glycation end products is a promising target of diabetic nephropathy. Ann N Y Acad Sci 1043:562-566, 2005
21. Kunjathoor VV, Wilson DL, LeBoeuf RC: Increased atherosclerosis in streptozotocin-induced diabetic mice. J Clin Invest 97:1767-1773, 1996
22. Takeuchi M, Makita Z, Yanagisawa K, Kameda Y, Koike T: Detection of noncarboxymethyllysine and carboxymethyllysine advanced glycation end products (AGE) in serum of diabetic patients. Mol Med 5:393-405, 1999
23. Tamarat R, Silvestre JS, Durie M, Levy BI: Angiotensin II angiogenic effect in vivo involves vascular endothelial growth factor- and inflammation-related pathways. Lab Invest 82:747-756, 2002
24. Yonekura H, Yamamoto Y, Sakurai S, Petrova RG, Abedin MJ, Li H, Yasui K, Takeuchi M, Makita Z, Takasawa S, Okamoto H, Watanabe T, Yamamoto H: Novel splice variants of the receptor for advanced glycation end-products expressed in human vascular endothelial cells and pericytes, and their putative roles in diabetes-induced vascular injury. Biochem J 370:1097-1109, 2003
25. Mizuguchi H, Koizumi N, Hosono T, Utoguchi N, Watanabe Y, Kay MA, Hayakawa T: A simplified system for constructing recombinant adenoviral vectors containing heterologous peptides in the HI loop of their fiber knob. Gene Ther 8:730-735, 2001
26. Morioka T, Koyama H, Yamamura H, Tanaka S, Fukumoto S, Emoto M, Mizuguchi H, Hayakawa T, Kojima I, Takahashi K, Nishizawa Y: Role of H1-calponin in pancreatic AR42J cell differentiation into insulin-producing cells. Diabetes 52:760-766, 2003
27. Armulik A, Abramsson A, Betsholtz C: Endothelial/pericyte interactions. Circ Res 97:512-523, 2005
28. Mackman N: Role of tissue factor in hemostasis, thrombosis, and vascular development arterioscler. Arterioscler Thromb Vasc Biol 24:1015-1022, 2004
29. Lindahl P, Johansson BR, Leveen P, Betsholtz C: Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 277:242-245, 1997
30. Koyama H, Shoji T, Yokoyama H, Motoyama K, Mori K, Fukumoto S, Emoto M, Shoji T, Tamei H, Matsuki H, Sakurai S, Yamamoto Y, Yonekura H, Watanabe T, Yamamoto H, Nishizawa Y: Plasma level of endogenous secretory RAGE is associated with components of the metabolic syndrome and atherosclerosis. Arterioscler Thromb Vasc Biol 25:2587-2593, 2005
31. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N: Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 6:41-48, 2000
32. Sargiannidou I, Zhou J, Tuszynski GP: The role of thrombospondin-1 in tumor progression. Exp Biol Med (Maywood) 226:726-733, 2001
33. Yamagishi S, Kobayashi K, Yamamoto H: Vascular pericytes not only regulate growth, but also preserve prostacyclin-producing ability and protect against lipid peroxide-induced injury of co-cultured endothelial cells. Biochem Biophys Res Commun 190:418-425, 1993
34. Yamagishi S, Hsu CC, Taniguchi M, Harada S, Yamamoto Y, Ohsawa K, Kobayashi K, Yamamoto H: Receptor-mediated toxicity to pericytes of advanced glycosylation end products: a possible mechanism of pericyte loss in diabetic microangiopathy. Biochem Biophys Res Commun 213:681-687, 1995
35. Yamagishi S, Inagaki Y, Amano S, Okamoto T, Takeuchi M, Makita Z: 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, 2002
36. Alikhani Z, Alikhani M, Boyd CM, Nagao K, Trackman PC, Graves DT: Advanced glycation end products enhance expression of pro-apoptotic genes and stimulate fibroblast apoptosis through cytoplasmic and mitochondrial pathways. J Biol Chem 280:12087-12095, 2005
37. Larger E, Marre M, Corvol P, Gasc JM: Hyperglycemia-induced defects in angiogenesis in the chicken chorioallantoic membrane model. Diabetes 53:752-761, 2004
38. Sakaguchi T, Yan SF, Yan SD, Belov D, Rong LL, Sousa M, Andrassy M, Marso SP, Duda S, Arnold B, Liliensiek B, Nawroth PP, Stern DM, Schmidt AM, Naka Y: Central role of RAGE-dependent neointimal expansion in arterial restenosis. J Clin Invest 111:959-972, 2003
39. Zhou Z, Wang K, Penn MS, Marso SP, Lauer MA, Forudi F, Zhou X, Qu W, Lu Y, Stern DM, Schmidt AM, Lincoff AM, Topol EJ: Receptor for AGE (RAGE) mediates neointimal formation in response to arterial injury. Circulation 107:2238-2243, 2003
40. Cogan D, Toussaint D, Kuwabara T: Retinal vascular pattern. IV. Diabetic retinopathy. Arch Ophthalmol 66:366-378, 1961
41. Hammes HP, Lin J, Renner O, Shani M, Lundqvist A, Betsholtz C, Brownlee M, Deutsch U: Pericytes and the pathogenesis of diabetic retinopathy. Diabetes 51:3107-3112, 2002
42. Bierhaus A, Schiekofer S, Schwaninger M, Andrassy M, Humpert PM, Chen J, Hong M, Luther T, Henle T, Kloting I, Morcos M, Hofmann M, Tritschler H, Weigle B, Kasper M, Smith M, Perry G, Schmidt AM, Stern DM, Haring HU, Schleicher E, Nawroth PP: Diabetes-associated sustained activation of the transcription factor nuclear factor-κB. Diabetes 50:2792-2808, 2001
43. Alves M, Calegari VC, Cunha DA, Saad MJ, Velloso LA, Rocha EM: Increased expression of advanced glycation end-products and their receptor, and activation of nuclear factor kappa-B in lacrimal glands of diabetic rats. Diabetologia 48:2675-2681, 2005
44. Falcone C, Emanuele E, D'Angelo A, Buzzi MP, Belvito C, Cuccia M, Geroldi D: Plasma levels of soluble receptor for advanced glycation end products and coronary artery disease in nondiabetic men. Arterioscler Thromb Vasc Biol 25:1032-1037, 2005
45. Katakami N, Matsuhisa M, Kaneto H, Matsuoka TA, Sakamoto K, Nakatani Y, Ohtoshi K, Hayaishi-Okano R, Kosugi K, Hori M, Yamasaki Y: Decreased endogenous secretory advanced glycation end product receptor in type 1 diabetic patients: its possible association with diabetic vascular complications. Diabetes Care 28:2716-2721, 2005