Endothelial progenitor thrombospondin-1 mediates diabetes-induced delay in reendothelialization following arterial injury

Circulation Research

Volumn 98, Issue 5, 2006, Pages 697-704

  Ii, Masaaki ^a,d   Takenaka, Hideya ^b   Asai, Jun ^a,b   Ibusuki, Kayoko ^a   Mizukami, Yusuke ^c   Maruyama, Kazuichi ^b   Yoon, Young Sup ^a   Wecker, Andrea ^a   Luedemann, Corinne ^a   Eaton, Elizabeth ^a   Silver, Marcy ^a   Thorne, Tina ^a   Losordo, Douglas W ^a,e  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^c ASAHIKAWA MEDICAL COLLEGE   (Japan)

^d RIKEN   (Japan)

^e ST ELIZABETH'S MEDICAL CENTER   (United States)

Author keywords

Carotid arteries; Diabetes mellitus; Endothelium; Restenosis

Indexed keywords

ANGIOPOIETIN RECEPTOR; BETA GALACTOSIDASE; CYTOKINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE; MESSENGER RNA; PLASMID DNA; THROMBOSPONDIN 1; VASCULOTROPIN; VASCULOTROPIN A;

ALLOGENIC BONE MARROW TRANSPLANTATION; ANGIOPLASTY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY ENDOTHELIUM; ARTICLE; BONE MARROW CELL; CAROTID ARTERY INJURY; CELL ADHESION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DIABETES MELLITUS; ENDOTHELIZATION; HISTOGENESIS; HISTOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RESTENOSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL; STENT; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; BONE MARROW TRANSPLANTATION; C57BL MOUSE; CELL CULTURE; CELL MOTION; ENDOTHELIUM CELL; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BONE MARROW TRANSPLANTATION; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; CYTOKINES; DIABETES MELLITUS; ENDOTHELIAL CELLS; MALE; MICE; MICE, INBRED C57BL; NITRIC OXIDE SYNTHASE TYPE III; STEM CELLS; THROMBOSPONDIN 1; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 33645303253     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000209948.50943.ea     Document Type: Article

References (31)

1. Van Belle E, Bauters C, Hubert E, Bodart JC, Abolmaali K, Meurice T, McFadden EP, Lablanche JM, Bertrand ME. Restenosis rates in diabetic patients: a comparison of coronary stenting and balloon angioplasty in native coronary vessels. Circulation. 1997;96:1454-1460.
2. Elezi S, Kastrati A, Pache J, Wehinger A, Hadamitzky M, Dirschinger J, Neumann FJ, Schomig A. Diabetes mellitus and the clinical and angiographic outcome after coronary stent placement. J Am Coll Cardiol. 1998;32:1866-1873.
3. Schofer J, Schluter M, Rau T, Hammer F, Haag N, Mathey DG. Influence of treatment modality on angiographic outcome after coronary stenting in diabetic patients: a controlled study. J Am Coll Cardiol. 2000;35:1554-1559.
4. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362:801-805.
5. Aronson D, Bloomgarden Z, Rayfield EJ. Potential mechanisms promoting restenosis in diabetic patients. J Am Coll Cardiol. 1996;27:528-535.
6. Kubota T, Kubota N, Moroi M, Terauchi Y, Kobayashi T, Kamata K, Suzuki R, Tobe K, Namiki A, Aizawa S, Nagai R, Kadowaki T, Yamaguchi T. Lack of insulin receptor substrate-2 causes progressive neointima formation in response to vessel injury. Circulation. 2003;107:3073-3080.
7. Shelton J, Wang D, Gupta H, Wyss JM, Oparil S, White CR. The neointimal response to endovascular injury is increased in obese Zucker rats. Diabetes Obes Metab. 2003;5:415-423.
8. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:964-967.
9. Shi Q, Rafii S, Wu MH, Wijelath ES, Yu C, Ishida A, Fujita Y, Kothari S, Mohle R, Sauvage LR, Moore MA, Storb RF, Hammond WP. Evidence for circulating bone marrow-derived endothelial cells. Blood. 1998;92:362-367.
10. Laufs U, Werner N, Link A, Endres M, Wassmann S, Jurgens K, Miche E, Bohm M, Nickenig G. Physical training increases endothelial progenitor cells, inhibits neointima formation, and enhances angiogenesis. Circulation. 2004;109:220-226.
11. Walter DH, Rittig K, Bahlmann FH, Kirchmair R, Silver M, Murayama T, Nishimura H, Losordo DW, Asahara T, Isner JM. Statin therapy accelerates reendothelialization: a novel effect involving mobilization and incorporation of bone marrow-derived endothelial progenitor cells. Circulation. 2002;105:3017-3024.
12. Werner N, Priller J, Laufs U, Endres M, Bohm M, Dirnagl U, Nickenig G. Bone marrow-derived progenitor cells modulate vascular reendothelialization and neointimal formation: effect of 3-hydroxy-3-methylglutaryl coenzyme a reductase inhibition. Arterioscler Thromb Vasc Biol. 2002;22:1567-1572.
13. Iwakura A, Luedemann C, Shastry S, Hanley A, Kearney M, Aikawa R, Isner JM, Asahara T, Losordo DW. Estrogen-mediated, endothelial nitric oxide synthase-dependent mobilization of bone marrow-derived endothelial progenitor cells contributes to reendothelialization after arterial injury. Circulation. 2003;108:3115-3121.
14. Strehlow K, Werner N, Berweiler J, Link A, Dirnagl U, Priller J, Laufs K, Ghaeni L, Milosevic M, Bohm M, Nickenig G. Estrogen increases bone marrow-derived endothelial progenitor cell production and diminishes neointima formation. Circulation. 2003;107:3059-3065.
15. Cho HJ, Kim HS, Lee MM, Kim DH, Yang HJ, Hur J, Hwang KK, Oh S, Choi YJ, Chae TH, Oh BH, Choi YS, Walsh K, Park YB. Mobilized endothelial progenitor cells by granulocyte-macrophage colony-stimulating factor accelerate reendothelialization and reduce vascular inflammation after intravascular radiation. Circulation. 2003;108:2918-2925.
16. Kong D, Melo LG, Gnecchi M, Zhang L, Mostoslavsky G, Liew CC, Pratt RE, Dzau VJ. Cytokine-induced mobilization of circulating endothelial progenitor cells enhances repair of injured arteries. Circulation. 2004;110:2039-2046.
17. Werner N, Junk S, Laufs U, Link A, Walenta K, Bohm M, Nickenig G. Intravenous transfusion of endothelial progenitor cells reduces neointima formation after vascular injury. Circ Res. 2003;93:e17-e24.
18. Griese DP, Ehsan A, Melo LG, Kong D, Zhang L, Mann MJ, Pratt RE, Mulligan RC, Dzau VJ. Isolation and transplantation of autologous circulating endothelial cells into denuded vessels and prosthetic grafts: implications for cell-based vascular therapy. Circulation. 2003;108:2710-2715.
19. Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, Martin H, Zeiher AM, Dimmeler S. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res. 2001;89:e1-e7.
20. Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, Finkel T. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med. 2003;348:593-600.
21. Tepper OM, Galiano RD, Capla JM, Kalka C, Gagne PJ, Jacobowitz GR, Levine JP, Gurtner GC. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation. 2002;106:2781-2786.
22. Loomans CJ, de Koning EJ, Staal FJ, Rookmaaker MB, Verseyden C, de Boer HC, Verhaar MC, Braam B, Rabelink TJ, van Zonneveld AJ. Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes. 2004;53:195-199.
23. Asahara T, Takahashi T, Masuda H, Kalka C, Chen D, Iwaguro H, Inai Y, Silver M, Isner JM. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J. 1999;18:3964-3972.
24. Ii M, Nishimura H, Iwakura A, Wecker A, Eaton E, Asahara T, Losordo DW. Endothelial progenitor cells are rapidly recruited to myocardium and mediate protective effect of ischemic preconditioning via "imported" nitric oxide synthase activity. Circulation. 2005;111:1114-1120.
25. Ii M, Hoshiga M, Fukui R, Negoro N, Nakakoji T, Nishiguchi F, Kohbayashi E, Ishihara T, Hanafusa T. Beraprost sodium regulates cell cycle in vascular smooth muscle cells through cAMP signaling by preventing down-regulation of p27(Kip1). Cardiovasc Res. 2001;52:500-508.
26. Duh E, Aiello LP. Vascular endothelial growth factor and diabetes: the agonist versus antagonist paradox. Diabetes. 1999;48:1899-1906.
27. Stenina OI, Krukovets I, Wang K, Zhou Z, Forudi F, Penn MS, Topol EJ, Plow EF. Increased expression of thrombospondin-1 in vessel wall of diabetic Zucker rat. Circulation. 2003;107:3209-3215.
28. Bayraktar M, Dundar S, Kirazli S, Teletar F. Platelet factor 4, beta-thromboglobulin and thrombospondin levels in type I diabetes mellitus patients. J Int Med Res. 1994;22:90-94.
29. Stouffer GA, Hu Z, Sajid M, Li H, Jin G, Nakada MT, Hanson SR, Runge MS. Beta3 integrins are upregulated after vascular injury and modulate thrombospondin- and thrombin-induced proliferation of cultured smooth muscle cells. Circulation. 1998;97:907-915.
30. Chen D, Asahara T, Krasinski K, Witzenbichler B, Yang J, Magner M, Keamey M, Frazier WA, Isner JM, Andres V. Antibody blockade of thrombospondin accelerates reendothelialization and reduces neointima formation in balloon-injured rat carotid artery. Circulation. 1999;100:849-854.
31. Rodrigues RG, Guo N, Zhou L, Sipes JM, Williams SB, Templeton NS, Gralnick HR, Roberts DD. Conformational regulation of the fibronectin binding and alpha 3beta 1 integrin-mediated adhesive activities of thrombospondin-1. J Biol Chem. 2001;276:27913-27922.