The importance of reendothelialization after arterial injury

Current Pharmaceutical Design

Volumn 13, Issue 17, 2007, Pages 1811-1824

  Versari, D ^a   Lerman, L O ^a   Lerman, Amir ^a  

^a Mayo Clinic   (United States)

Author keywords

Arterial injury; Atherosclerosis; Endothelialization; Endothelium; EPCs; Stent

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; ADRENOMEDULLIN; CD34 ANTIGEN; CERIVASTATIN; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ESTRADIOL; GELATIN; GELATINASE B; HEPARIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; NITRIC OXIDE; PACLITAXEL; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; RAPAMYCIN; TUMOR NECROSIS FACTOR RECEPTOR; VASCULOTROPIN; VASCULOTROPIN C; VASCULOTROPIN RECEPTOR 2;

AGING; ALLOTRANSPLANTATION; ANGIOGENESIS; ARTERY INJURY; ATHEROSCLEROSIS; AUTOTRANSPLANTATION; BONE MARROW CELL; CARDIOVASCULAR RISK; CAROTID ARTERY DISEASE; CELL ADHESION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STIMULATION; CHEMOTAXIS; CORONARY ARTERY DISEASE; DRUG DELIVERY SYSTEM; DRUG ELUTING STENT; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; EXERCISE; FAMILY HISTORY; GENE THERAPY; HEART FAILURE; HEMATOPOIETIC STEM CELL; HUMAN; HYPERCHOLESTEROLEMIA; HYPERTENSION; IN-STENT RESTENOSIS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PERIPHERAL VASCULAR DISEASE; PLASMID; PLEIOTROPY; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; SMOKING; SMOOTH MUSCLE FIBER; STABLE ANGINA PECTORIS; STEM CELL MOBILIZATION; STEM CELL TRANSPLANTATION; STENT; STROKE; TRANSLUMINAL CORONARY ANGIOPLASTY; UNSTABLE ANGINA PECTORIS; VASCULAR ENDOTHELIUM;

ANIMALS; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASES; CELL MOVEMENT; CELL PROLIFERATION; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; REGENERATION; RISK ASSESSMENT; RISK FACTORS; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 34250835029     PISSN: 13816128     EISSN: None     Source Type: Journal    
DOI: 10.2174/138161207780831239     Document Type: Review

References (191)

1. Braunwald E. Shattuck lecture-cardiovascular medicine at the turn of the millennium: Triumphs, concerns, and opportunities. N Engl J Med 1997; 337: 1360-9.
2. Murray CJ, Lopez AD. Global mortality, disability, and the contribution of risk factors: Global burden of disease study. Lancet 1997; 349: 1436-42.
3. Kannel WB, Schatzkin A. Sudden death: Lessons from subsets in population studies. J Am Coll Cardiol 1985; 5: 141B-9B.
4. Myerburg RJ, Interian A Jr, Mitrani RM, Kessler KM, Castellanos A. Frequency of sudden cardiac death and profiles of risk. Am J Cardiol 1997; 80: 10F-9F.
5. Ross R. The arterial wall and atherosclerosis. Annu Rev Med 1979; 30: 1-15.
6. Caplan BA, Schwartz CJ. Increased endothelial cell turnover in areas of in vivo Evans Blue uptake in the pig aorta. Atherosclerosis 1973; 17: 401-17.
7. Dimmeler S, Haendeler J, Zeiher AM. Regulation of endothelial cell apoptosis in atherothrombosis. Curr Opin Lipidol 2002; 13: 531-6.
8. Choy JC, Granville DJ, Hunt DW, McManus BM. Endothelial cell apoptosis: biochemical characteristics and potential implications for atherosclerosis. J Mol Cell Cardiol 2001; 33: 1673-90.
9. Schwartz SM, Benditt EP. Clustering of replicating cells in aortic endothelium. Proc Natl Acad Sci USA 1976; 73: 651-3.
10. Bonetti PO, Lerman LO, Lerman A. Endothelial dysfunction: A marker of atherosclerotic risk. Arterioscler Thromb Vasc Biol 2003; 23: 168-75
11. Furchgott RF, Zawadzki JV. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 1980; 288: 373-6.
12. Palmer RM, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987; 327: 524-6.
13. Taddei S, Virdis A, Ghiadoni L, Magagna A, Salvetti A. Vitamin C improves endothelium-dependent vasodilation by restoring nitric oxide activity in essential hypertension. Circulation 1998; 97: 2222-9.
14. Chade AR, Krier JD, Rodriguez-Porcel M, Breen JF, McKusick MA, Lerman A, et al. Comparison of acute and chronic antioxidant interventions in experimental renovascular disease. Am J Physiol Renal Physiol 2004; 286: F1079-86.
15. Rodriguez-Porcel M, Lerman LO, Holmes DR Jr, Richardson D, Napoli C, Lerman A. Chronic antioxidant supplementation attenuates nuclear factor-kappa B activation and preserves endothelial function in hypercholesterolemic pigs. Cardiovasc Res 2002; 53: 1010-8.
16. Stulak JM, Lerman A, Porcel MR, Caccitolo JA, Romero JC, Schaff HV, et al. Renal vascular function in hypercholesterolemia is preserved by chronic antioxidant supplementation. J Am Soc Nephrol 2001; 12: 1882-91.
17. Taddei S, Ghiadoni L, Virdis A, Versari D, Salvetti A. Mechanisms of endothelial dysfunction: Clinical significance and preventive non-pharmacological therapeutic strategies. Curr Pharm Des 2003; 9: 2385-402.
18. Lerman A, Zeiher AM. Endothelial function: Cardiac events. Circulation 2005; 111: 363-8.
19. Szmitko PE, Wang CH, Weisel RD, Jeffries GA, Anderson TJ, Verma S. Biomarkers of vascular disease linking inflammation to endothelial activation: Part II. Circulation 2003; 108: 2041-8.
20. Szmitko PE, Wang CH, Weisel RD, de Almeida JR, Anderson TJ, Verma S. New markers of inflammation and endothelial cell activation: Part I. Circulation 2003; 108: 1917-23.
21. Gill M, Dias S, Hattori K, Rivera ML, Hicklin D, Witte L, et al. Vascular trauma induces rapid but transient mobilization of VEGFR2(+)AC133(+) endothelial precursor cells. Circ Res 2001; 88: 167-74.
22. Dimmeler S, Hermann C, Galle J, Zeiher AM. Upregulation of superoxide dismutase and nitric oxide synthase mediates the apoptosis- suppressive effects of shear stress on endothelial cells. Arterioscler Thromb Vasc Biol 1999; 19: 656-64.
23. Ballieux BE, Hiemstra PS, Klar-Mohamad N, Hagen EC, van Es LA, van der Woude FJ, et al. Detachment and cytolysis of human endothelial cells by proteinase 3. Eur J Immunol 1994; 24: 3211-5.
24. Re F, Zanetti A, Sironi M, Polentarutti N, Lanfrancone L, Dejana E, et al. Inhibition of anchorage-dependent cell spreading triggers apoptosis in cultured human endothelial cells. J Cell Biol 1994; 127: 537-46.
25. Rafii S, Meeus S, Dias S, Hattori K, Heissig B, Shmelkov S, et al. Contribution of marrow-derived progenitors to vascular and cardiac regeneration. Semin Cell Dev Biol 2002; 13: 61-7.
26. Park JB, Charbonneau F, Schiffrin EL. Correlation of endothelial function in large and small arteries in human essential hypertension. J Hypertens 2001; 19: 415-20.
27. Anderson TJ, Uehata A, Gerhard MD, Meredith IT, Knab S, Delagrange D, et al. Close relation of endothelial function in the human coronary and peripheral circulations. J Am Coll Cardiol 1995; 26: 1235-41.
28. Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 2003; 348: 593-600.
29. Blann AD, Woywodt A, Bertolini F, Bull TM, Buyon JP, Clancy RM, et al. Circulating endothelial cells. Biomarker of vascular disease. Thromb Haemost 2005; 93: 228-35.
30. Mutin M, Canavy I, Blann A, Bory M, Sampol J, Dignat-George F. Direct evidence of endothelial injury in acute myocardial infarction and unstable angina by demonstration of circulating endothelial cells. Blood 1999; 93: 2951-8.
31. Quilici J, Banzet N, Paule P, Meynard JB, Mutin M, Bonnet JL, et al. Circulating endothelial cell count as a diagnostic marker for non-ST-elevation acute coronary syndromes. Circulation 2004; 110: 1586-91.
32. McClung JA, Naseer N, Saleem M, Rossi GP, Weiss MB, Abraham NG, et al. Circulating endothelial cells are elevated in patients with type 2 diabetes mellitus independently of HbA(1)c. Diabetologia 2005; 48: 345-50.
33. Mutunga M, Fulton B, Bullock R, Batchelor A, Gascoigne A, Gillespie JI, et al. Circulating endothelial cells in patients with septic shock. Am J Respir Crit Care Med 2001; 163: 195-200.
34. Koc M, Richards HB, Bihorac A, Ross EA, Schold JD, Segal MS. Circulating endothelial cells are associated with future vascular events in hemodialysis patients. Kidney Int 2005; 67: 1078-83.
35. Lee KW, Lip GY, Tayebjee M, Foster W, Blann AD. Circulating endothelial cells, von Willebrand factor, interleukin-6, and prognosis in patients with acute coronary syndromes. Blood 2005; 105: 526-32.
36. Woywodt A, Streiber F, de Groot K, Regelsberger H, Haller H, Haubitz M. Circulating endothelial cells as markers for ANCA associated small-vessel vasculitis. Lancet 2003; 361: 206-10.
37. Bull TM, Golpon H, Hebbel RP, Solovey A, Cool CD, Tuder RM, et al. Circulating endothelial cells in pulmonary hypertension. Thromb Haemost 2003; 90: 698-703.
38. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997; 275: 964-7.
39. Lin Y, Weisdorf DJ, Solovey A, Hebbel RP. Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest 2000; 105: 71-7.
40. Rehman J, Li J, Orschell CM, March KL. Peripheral blood "endothelial progenitor cells" are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 2003; 107: 1164-9.
41. Peichev M, Naiyer AJ, Pereira D, Zhu Z, Lane WJ, Williams M, et al. Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 2000; 95: 952-8.
42. Harraz M, Jiao C, Hanlon HD, Hartley RS, Schatteman GC. CD34-blood-derived human endothelial cell progenitors. Stem Cells 2001; 19: 304-12.
43. Schmeisser A, Garlichs CD, Zhang H, Eskafi S, Graffy C, Ludwig J, et al. Monocytes coexpress endothelial and macrophagocytic lineage markers and form cord-like structures in Matrigel under angiogenic conditions. Cardiovasc Res 2001; 49: 671-80.
44. Romagnani P, Annunziato F, Liotta F, Lazzeri E, Mazzinghi B, Frosali F, et al. CD14+CD34low cells with stem cell phenotypic and functional features are the major source of circulating endothelial progenitors. Circ Res 2005; 97: 314-22.
45. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 2003; 114: 763-76.
46. Cheng T, Rodrigues N, Shen H, Yang Y, Dombkowski D, Sykes M, et al. Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science 2000; 287: 1804-8.
47. Asahara T, Takahashi T, Masuda H, Kalka C, Chen D, Iwaguro H, et al. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. Embo J 1999; 18: 3964-72
48. Kalka C, Masuda H, Takahashi T, Gordon R, Tepper O, Gravereaux E, et al. Vascular endothelial growth factor(165) gene transfer augments circulating endothelial progenitor cells in human subjects. Circ Res 2000; 86: 1198-202.
49. Anagnostou A, Lee ES, Kessimian N, Levinson R, Steiner M. Erythropoietin has a mitogenic and positive chemotactic effect on endothelial cells. Proc Natl Acad Sci USA 1990; 87: 5978-82.
50. Heeschen C, Aicher A, Lehmann R, Fichtlscherer S, Vasa M, Urbich C, et al. Erythropoietin is a potent physiologic stimulus for endothelial progenitor cell mobilization. Blood 2003; 102: 1340-6.
51. Bahlmann FH, De Groot K, Spandau JM, Landry AL, Hertel B, Duckert T, et al. Erythropoietin regulates endothelial progenitor cells. Blood 2004; 103: 921-6.
52. Bahlmann FH, DeGroot K, Duckert T, Niemczyk E, Bahlmann E, Boehm SM, et al. Endothelial progenitor cell proliferation and differentiation is regulated by erythropoietin. Kidney Int 2003; 64: 1648-52.
53. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, et al. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 1999; 5: 434-8.
54. Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 2002; 109: 625-37.
55. Hattori K, Heissig B, Wu Y, Dias S, Tejada R, Ferris B, et al. Placental growth factor reconstitutes hematopoiesis by recruiting VEGFR1(+) stem cells from bone-marrow microenvironment. Nat Med 2002;8:841-9.
56. Li X, Tjwa M, Moons L, Fons P, Noel A, Ny A, et al. Revascularization of ischemic tissues by PDGF-CC via effects on endothelial cells and their progenitors. J Clin Invest 2005; 115: 118-27.
57. Hattori K, Dias S, Heissig B, Hackett NR, Lyden D, Tateno M, et al. Vascular endothelial growth factor and angiopoietin-1 stimulate postnatal hematopoiesis by recruitment of vasculogenic and hematopoietic stem cells. J Exp Med 2001; 193: 1005-14.
58. Llevadot J, Murasawa S, Kureishi Y, Uchida S, Masuda H, Kawamoto A, et al. HMG-CoA reductase inhibitor mobilizes bone marrow-derived endothelial progenitor cells. J Clin Invest 2001; 108: 399-405.
59. Vasa M, Fichtlscherer S, Adler K, Aicher A, Martin H, Zeiher AM, et al. Increase in circulating endothelial progenitor cells by statin therapy in patients with stable coronary artery disease. Circulation 2001; 103: 2885-90.
60. Pistrosch F, Herbrig K, Oelschlaegel U, Richter S, Passauer J, Fischer S, et al. PPARgamma-agonist rosiglitazone increases number and migratory activity of cultured endothelial progenitor cells. Atherosclerosis 2005; 183: 163-7.
61. Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, Martin H, et al. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 2001; 89: E1-7.
62. Eizawa T, Ikeda U, Murakami Y, Matsui K, Yoshioka T, Suzuki C, et al. Increase in circulating endothelial progenitor cells after aortic aneurysm repair. Heart Vessels 2004; 19: 107-10.
63. Concina P, Sordello S, Barbacanne MA, Elhage R, Pieraggi MT, Fournial G, et al. The mitogenic effect of 17beta-estradiol on in vitro endothelial cell proliferation and on in vivo reendothelialization are both dependent on vascular endothelial growth factor. J Vasc Res 2000; 37: 202-8.
64. Krasinski K, Spyridopoulos I, Asahara T, van der Zee R, Isner JM, Losordo DW. Estradiol accelerates functional endothelial recovery after arterial injury. Circulation 1997; 95: 1768-72.
65. Iwakura A, Luedemann C, Shastry S, Hanley A, Kearney M, Aikawa R, et al. Estrogen-mediated, endothelial nitric oxide synthase dependent mobilization of bone marrow-derived endothelial progenitor cells contributes to reendothelialization after arterial injury. Circulation 2003; 108: 3115-21.
66. Levesque JP, Liu F, Simmons PJ, Betsuyaku T, Senior RM, Pham C, et al. Characterization of hematopoietic progenitor mobilization in protease-deficient mice. Blood 2004; 104: 65-72.
67. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 1999; 399: 601-5.
68. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, et al. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 1999; 399: 597-601.
69. Aicher A, Heeschen C, Mildner-Rihm C, Urbich C, Ihling C, Technau-Ihling K, et al. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 2003; 9: 1370-6.
70. Rauscher FM, Goldschmidt-Clermont PJ, Davis BH, Wang T, Gregg D, Ramaswami P, et al. Aging, progenitor cell exhaustion, and atherosclerosis. Circulation 2003; 108: 457-63.
71. Heiss C, Keymel S, Niesler U, Ziemann J, Kelm M, Kalka C. Impaired progenitor cell activity in age-related endothelial dysfunction. J Am Coll Cardiol 2005; 45: 1441-8.
72. Scheubel RJ, Zorn H, Silber RE, Kuss O, Morawietz H, Holtz J, et al. Age-dependent depression in circulating endothelial progenitor cells in patients undergoing coronary artery bypass grafting. J Am Coll Cardiol 2003; 42: 2073-80.
73. Schmidt-Lucke C, Rossig L, Fichtlscherer S, Vasa M, Britten M, Kamper U, et al. Reduced number of circulating endothelial progenitor cells predicts future cardiovascular events: Proof of concept for the clinical importance of endogenous vascular repair. Circulation 2005; 111: 2981-7.
74. Geiger H, Van Zant G. The aging of lympho-hematopoietic stem cells. Nat Immunol 2002; 3: 329-33.
75. Chen JZ, Zhang FR, Tao QM, Wang XX, Zhu JH, Zhu JH. Number and activity of endothelial progenitor cells from peripheral blood in patients with hypercholesterolaemia. Clin Sci (Lond) 2004; 107: 273-80.
76. Wang X, Chen J, Tao Q, Zhu J, Shang Y. Effects of ox-LDL on number and activity of circulating endothelial progenitor cells. Drug Chem Toxicol 2004; 27: 243-55.
77. Tan H, Jiang X, Yang F, Li Z, Liao D, Trial J, et al. Hyperhomocysteinemia inhibits post-injury reendothelialization in mice. Cardiovasc Res 2006; 69: 253-62
78. Virdis A, Ghiadoni L, Versari D, Salvetti G, Pinto S, Favilla S, et al. Is Hyperhomocyst(e)inemia a humoral predictor of coronary heart disease? Curr Pharm Des 2005; 11: 2187-97.
79. Dimmeler S, Vasa-Nicotera M. Aging of progenitor cells: Limitation for regenerative capacity? J Am Coll Cardiol 2003; 42: 2081-2.
80. Kalka C, Tehrani H, Laudenberg B, Vale PR, Isner JM, Asahara T, et al. VEGF gene transfer mobilizes endothelial progenitor cells in patients with inoperable coronary disease. Ann Thorac Surg 2000; 70: 829-34.
81. George J, Goldstein E, Abashidze S, Deutsch V, Shmilovich H, Finkelstein A, et al. Circulating endothelial progenitor cells in patients with unstable angina: Association with systemic inflammation. Eur Heart J 2004; 25: 1003-8.
82. Massa M, Rosti V, Ferrario M, Campanelli R, Ramajoli I, Rosso R, et al. Increased circulating hematopoietic and endothelial progenitor cells in the early phase of acute myocardial infarction. Blood 2005; 105: 199-206.
83. Shintani S, Murohara T, Ikeda H, Ueno T, Honma T, Katoh A, et al. Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation 2001; 103: 2776-9.
84. Seko Y, Imai Y, Suzuki S, Kamijukkoku S, Hayasaki K, Sakomura Y, et al. Serum levels of vascular endothelial growth factor in patients with acute myocardial infarction undergoing reperfusion therapy. Clin Sci (Lond) 1997; 92: 453-4.
85. Seko Y, Fukuda S, Nagai R. Serum levels of endostatin, vascular endothelial growth factor (VEGF) and hepatocyte growth factor (HGF) in patients with acute myocardial infarction undergoing early reperfusion therapy. Clin Sci (Lond) 2004; 106: 439-42.
86. Ogawa H, Suefuji H, Soejima H, Nishiyama K, Misumi K, Takazoe K, et al. Increased blood vascular endothelial growth factor levels in patients with acute myocardial infarction. Cardiology 2000; 93: 93-9
87. Hojo Y, Ikeda U, Zhu Y, Okada M, Ueno S, Arakawa H, et al. Expression of vascular endothelial growth factor in patients with acute myocardial infarction. J Am Coll Cardiol 2000; 35: 968-73.
88. Taguchi A, Matsuyama T, Moriwaki H, Hayashi T, Hayashida K, Nagatsuka K, et al. Circulating CD34-positive cells provide an index of cerebrovascular function. Circulation 2004; 109: 2972-5.
89. Ghani U, Shuaib A, Salam A, Nasir A, Shuaib U, Jeerakathil T, et al. Endothelial progenitor cells during cerebrovascular disease. Stroke 2005; 36: 151-3.
90. Lindner V, Majack RA, Reidy MA. Basic fibroblast growth factor stimulates endothelial regrowth and proliferation in denuded arteries. J Clin Invest 1990; 85: 2004-8.
91. Meurice T, Bauters C, Auffray JL, Vallet B, Hamon M, Valero F, et al. Basic fibroblast growth factor restores endothelium-dependent responses after balloon injury of rabbit arteries. Circulation 1996; 93: 18-22.
92. Asahara T, Bauters C, Pastore C, Kearney M, Rossow S, Bunting S, et al. Local delivery of vascular endothelial growth factor accelerates reendothelialization and attenuates intimal hyperplasia in balloon-injured rat carotid artery. Circulation 1995; 91: 2793-801.
93. Asahara T, Chen D, Tsurumi Y, Kearney M, Rossow S, Passeri J, et al. Accelerated restitution of endothelial integrity and endothelium- dependent function after phVEGF165 gene transfer. Circulation 1996; 94: 3291-302.
94. Hayashi K, Nakamura S, Morishita R, Moriguchi A, Aoki M, Matsumoto K, et al. in vivo transfer of human hepatocyte growth factor gene accelerates re-endothelialization and inhibits neointimal formation after balloon injury in rat model. Gene Ther 2000; 7: 1664-71.
95. Numaguchi Y, Naruse K, Harada M, Osanai H, Mokuno S, Murase K, et al. Prostacyclin synthase gene transfer accelerates reendothelialization and inhibits neointimal formation in rat carotid arteries after balloon injury. Arterioscler Thromb Vasc Biol 1999; 19: 727-33.
96. Weidinger FF, McLenachan JM, Cybulsky MI, Gordon JB, Rennke HG, Hollenberg NK, et al. Persistent dysfunction of regenerated endothelium after balloon angioplasty of rabbit iliac artery. Circulation 1990; 81: 1667-79.
97. Oberhoff M, Novak S, Herdeg C, Baumbach A, Kranzhofer A, Bohnet A, et al. Local and systemic delivery of low molecular weight heparin stimulates the reendothelialization after balloon angioplasty. Cardiovasc Res 1998; 38: 751-62.
98. Tanaka T, Fukunaga Y, Itoh H, Doi K, Yamashita J, Chun TH, et al. Therapeutic potential of thiazolidinediones in activation of peroxisome proliferator-activated receptor gamma for monocyte recruitment and endothelial regeneration. Eur J Pharmacol 2005; 508: 255-65.
99. Van Belle E, Meurice T, Tio FO, Corseaux D, Dupuis B, McFadden EP, et al. ACE inhibition accelerates endothelial regrowth in vivo: A possible explanation for the benefit observed with ACE inhibitors following arterial injury. Biochem Biophys Res Commun 1997; 231: 577-81.
100. Agata J, Zhang JJ, Chao J, Chao L. Adrenomedullin gene delivery inhibits neointima formation in rat artery after balloon angioplasty. Regul Pept 2003; 112: 115-20.
101. Krasinski K, Spyridopoulos I, Kearney M, Losordo DW. in vivo blockade of tumor necrosis factor-alpha accelerates functional endothelial recovery after balloon angioplasty. Circulation 2001; 104: 1754-6.
102. Herring M, Gardner A, Glover J. A single-staged technique for seeding vascular grafts with autogenous endothelium. Surgery 1978; 84: 498-504.
103. Van Belle E, Bauters C, Asahara T, Isner JM. Endothelial regrowth after arterial injury: From vascular repair to therapeutics. Cardiovasc Res 1998; 38: 54-68.
104. Gangadharan SP, Eslami MH, Weiss IP, Sui X, Conte MS. Monocyte adhesion to balloon-injured arteries: The influence of endothelial cell seeding. J Vasc Surg 2001; 33: 1247-54.
105. Werner N, Junk S, Laufs U, Link A, Walenta K, Bohm M, et al. Intravenous transfusion of endothelial progenitor cells reduces neointima formation after vascular injury. Circ Res 2003; 93: E17-24.
106. Fujiyama S, Amano K, Uehira K, Yoshida M, Nishiwaki Y, Nozawa Y, et al. Bone marrow monocyte lineage cells adhere on injured endothelium in a monocyte chemoattractant protein-1- dependent manner and accelerate reendothelialization as endothelial progenitor cells. Circ Res 2003; 93: 980-9.
107. He T, Smith LA, Harrington S, Nath KA, Caplice NM, Katusic ZS. Transplantation of circulating endothelial progenitor cells restores endothelial function of denuded rabbit carotid arteries. Stroke 2004; 35: 2378-84.
108. Gulati R, Jevremovic D, Peterson TE, Witt TA, Kleppe LS, Mueske CS, et al. Autologous culture-modified mononuclear cells confer vascular protection after arterial injury. Circulation 2003; 108: 1520-6.
109. Griese DP, Ehsan A, Melo LG, Kong D, Zhang L, Mann MJ, et al. Isolation and transplantation of autologous circulating endothelial cells into denuded vessels and prosthetic grafts: Implications for cell-based vascular therapy. Circulation 2003; 108: 2710-5.
110. Gulati R, Jevremovic D, Witt TA, Kleppe LS, Vile RG, Lerman A, et al. Modulation of the vascular response to injury by autologous blood-derived outgrowth endothelial cells. Am J Physiol Heart Circ Physiol 2004; 287: H512-7.
111. Urbich C, Dimmeler S. Endothelial progenitor cells: Characterization and role in vascular biology. Circ Res 2004; 95: 343-53.
112. Hristov M, Weber C. Endothelial progenitor cells: Characterization, pathophysiology, and possible clinical relevance. J Cell Mol Med 2004; 8: 498-508.
113. Kipshidze N, Dangas G, Tsapenko M, Moses J, Leon MB, Kutryk M, et al. Role of the endothelium in modulating neointimal formation: vasculoprotective approaches to attenuate restenosis after percutaneous coronary interventions. J Am Coll Cardiol 2004; 44: 733-9.
114. Werner N, Kosiol S, Schiegl T, Ahlers P, Walenta K, Link A, et al. Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med 2005; 353: 999-1007.
115. Adams V, Lenk K, Linke A, Lenz D, Erbs S, Sandri M, et al. Increase of circulating endothelial progenitor cells in patients with coronary artery disease after exercise-induced ischemia. Arterioscler Thromb Vasc Biol 2004; 24: 684-90.
116. Laufs U, Werner N, Link A, Endres M, Wassmann S, Jurgens K, et al. Physical training increases endothelial progenitor cells, inhibits neointima formation, and enhances angiogenesis. Circulation 2004; 109: 220-6.
117. Lyden D, Hattori K, Dias S, Costa C, Blaikie P, Butros L, et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 2001; 7: 1194-201.
118. Zhang H, Vakil V, Braunstein M, Smith EL, Maroney J, Chen L, et al. Circulating endothelial progenitor cells in multiple myeloma: implications and significance. Blood 2005; 105: 3286-94.
119. Kwon HM, Sangiorgi G, Ritman EL, McKenna C, Holmes DR Jr, Schwartz RS, et al. Enhanced coronary vasa vasorum neovascularization in experimental hypercholesterolemia. J Clin Invest 1998; 101: 1551-6.
120. Herrmann J, Lerman LO, Rodriguez-Porcel M, Holmes DR, Jr., Richardson DM, Ritman EL, et al. Coronary vasa vasorum neovascularization precedes epicardial endothelial dysfunction in experimental hypercholesterolemia. Cardiovasc Res 2001; 51: 762-6.
121. Hayden MR, Tyagi SC. Vasa vasorum in plaque angiogenesis, metabolic syndrome, type 2 diabetes mellitus, and atheroscleropathy: A malignant transformation. Cardiovasc Diabetol 2004; 3: 1.
122. George J, Afek A, Abashidze A, Shmilovich H, Deutsch V, Kopolovich J, et al. Transfer of endothelial progenitor and bone marrow cells influences atherosclerotic plaque size and composition in apolipoprotein e knockout mice. Arterioscler Thromb Vasc Biol 2005; 25: 2636-41.
123. Hoffmann R, Mintz GS. Coronary in-stent restenosis - predictors, treatment and prevention. Eur Heart J 2000; 21: 1739-49.
124. Teirstein PS, Massullo V, Jani S, Popma JJ, Mintz GS, Russo RJ, et al. Catheter-based radiotherapy to inhibit restenosis after coronary stenting. N Engl J Med 1997; 336: 1697-703.
125. Costa MA, Simon DI. Molecular basis of restenosis and drug-eluting stents. Circulation 2005; 111: 2257-73.
126. Lerman A, Eeckhout E. Coronary endothelial dysfunction following sirolimus-eluting stent placement: Should we worry about it? Eur Heart J 2006; 27: 125-6.
127. Shirotani M, Yui Y, Kawai C. Restenosis after coronary angioplasty: pathogenesis of neointimal thickening initiated by endothelial loss. Endothelium 1993; 1: 5-22.
128. Haudenschild CC, Schwartz SM. Endothelial regeneration. II. Restitution of endothelial continuity. Lab Invest 1979; 41: 407-18.
129. Edelman ER, Rogers C. Pathobiologic responses to stenting. Am J Cardiol 1998; 81: 4E-6E.
130. Blum A, Schneider DJ, Sobel BE, Dauerman HL. Endothelial dysfunction and inflammation after percutaneous coronary intervention. Am J Cardiol 2004; 94: 1420-3.
131. McLenachan JM, Vita J, Fish DR, Treasure CB, Cox DA, Ganz P, et al. Early evidence of endothelial vasodilator dysfunction at coronary branch points. Circulation 1990; 82: 1169-73.
132. Shimokawa H, Flavahan NA, Shepherd JT, Vanhoutte PM. Endothelium- dependent inhibition of ergonovine-induced contraction is impaired in porcine coronary arteries with regenerated endothelium. Circulation 1989; 80: 643-50.
133. Patti G, Pasceri V, Melfi R, Goffredo C, Chello M, D'Ambrosio A, et al. Impaired flow-mediated dilation and risk of restenosis in patients undergoing coronary stent implantation. Circulation 2005; 111: 70-5.
134. Kitta Y, Nakamura T, Kodama Y, Takano H, Umetani K, Fujioka D, et al. Endothelial vasomotor dysfunction in the brachial artery is associated with late in-stent coronary restenosis. J Am Coll Cardiol 2005; 46: 648-55.
135. Hehrlein C, Gollan C, Donges K, Metz J, Riessen R, Fehsenfeld P, et al. Low-dose radioactive endovascular stents prevent smooth muscle cell proliferation and neointimal hyperplasia in rabbits. Circulation 1995; 92: 1570-5.
136. Van Belle E, Tio FO, Couffinhal T, Maillard L, Passeri J, Isner JM. Stent endothelialization. Time course, impact of local catheter delivery, feasibility of recombinant protein administration, and response to cytokine expedition. Circulation 1997; 95: 438-48.
137. Palmaz JC, Windeler SA, Garcia F, Tio FO, Sibbitt RR, Reuter SR. Atherosclerotic rabbit aortas: Expandable intraluminal grafting. Radiology 1986; 160: 723-6.
138. Waksman R, Robinson KA, Crocker IR, Gravanis MB, Palmer SJ, Wang C, et al. Intracoronary radiation before stent implantation inhibits neointima formation in stented porcine coronary arteries. Circulation 1995; 92: 1383-6.
139. Karas SP, Gravanis MB, Santoian EC, Robinson KA, Anderberg KA, King SB, 3rd. Coronary intimal proliferation after balloon injury and stenting in swine: An animal model of restenosis. J Am Coll Cardiol 1992; 20: 467-74.
140. Anderson PG, Bajaj RK, Baxley WA, Roubin GS. Vascular pathology of balloon-expandable flexible coil stents in humans. J Am Coll Cardiol 1992; 19: 372-81.
141. Liuzzo JP, Ambrose JA, Coppola JT. Sirolimus- and taxol-eluting stents differ towards intimal hyperplasia and re-endothelialization. J Invasive Cardiol 2005; 17: 497-502.
142. Suzuki T, Kopia G, Hayashi S, Bailey LR, Llanos G, Wilensky R, et al. Stent-based delivery of sirolimus reduces neointimal formation in a porcine coronary model. Circulation 2001; 104: 1188-93.
143. Windecker S, Remondino A, Eberli FR, Juni P, Raber L, Wenaweser P, et al. Sirolimus-eluting and paclitaxel-eluting stents for coronary revascularization. N Engl J Med 2005; 353: 653-62.
144. Fukuda D, Sata M, Tanaka K, Nagai R. Potent inhibitory effect of sirolimus on circulating vascular progenitor cells. Circulation 2005; 111: 926-31.
145. Hofma SH, van der Giessen WJ, van Dalen BM, Lemos PA, McFadden EP, Sianos G, et al. Indication of long-term endothelial dysfunction after sirolimus-eluting stent implantation. Eur Heart J 2005; 27: 166-70.
146. Togni M, Windecker S, Cocchia R, Wenaweser P, Cook S, Billinger M, et al. Sirolimus-eluting stents associated with paradoxic coronary vasoconstriction. J Am Coll Cardiol 2005; 46: 231-6.
147. Gomma AH, Elrayess MA, Knight CJ, Hawe E, Fox KM, Humphries SE. The endothelial nitric oxide synthase (Glu298Asp and - 786T≥C) gene polymorphisms are associated with coronary instent restenosis. Eur Heart J 2002; 23: 1955-62.
148. Suzuki T, Okumura K, Sone T, Kosokabe T, Tsuboi H, Kondo J, et al. The Glu298Asp polymorphism in endothelial nitric oxide synthase gene is associated with coronary in-stent restenosis. Int J Cardiol 2002; 86: 71-6.
149. Vermeersch P, Nong Z, Stabile E, Varenne O, Gillijns H, Pellens M, et al. L-arginine administration reduces neointima formation after stent injury in rats by a nitric oxide-mediated mechanism. Arterioscler Thromb Vasc Biol 2001; 21: 1604-9.
150. Kaul S, Makkar RR, Nakamura M, Litvack FI, Shah PK, Forrester JS, et al. Inhibition of acute stent thrombosis under high-shear flow conditions by a nitric oxide donor, DMHD/NO. An ex vivo porcine arteriovenous shunt study. Circulation 1996; 94: 2228-34.
151. Buergler JM, Tio FO, Schulz DG, Khan MM, Mazur W, French BA, et al. Use of nitric-oxide-eluting polymer-coated coronary stents for prevention of restenosis in pigs. Coron Artery Dis 2000; 11: 351-7.
152. Do YS, Kao EY, Ganaha F, Minamiguchi H, Sugimoto K, Lee J, et al. In-stent restenosis limitation with stent-based controlled-release nitric oxide: Initial results in rabbits. Radiology 2004; 230: 377-82
153. Muhs A, Heublein B, Schletter J, Herrmann A, Rudiger M, Sturm M, et al. Preclinical evaluation of inducible nitric oxide synthase lipoplex gene therapy for inhibition of stent-induced vascular neointimal lesion formation. Hum Gene Ther 2003; 14: 375-83.
154. Wang K, Kessler PD, Zhou Z, Penn MS, Forudi F, Zhou X, et al. Local adenoviral-mediated inducible nitric oxide synthase gene transfer inhibits neointimal formation in the porcine coronary stented model. Mol Ther 2003; 7: 597-603.
155. Lincoff AM, Topol EJ, Ellis SG. Local drug delivery for the prevention of restenosis. Fact, fancy, and future. Circulation 1994; 90: 2070-84.
156. Saia F, Marzocchi A, Serruys PW. Drug-eluting stents. The third revolution in percutaneous coronary intervention. Ital Heart J 2005; 6: 289-303.
157. Walter DH, Cejna M, Diaz-Sandoval L, Willis S, Kirkwood L, Stratford PW, et al. Local gene transfer of phVEGF-2 plasmid by gene-eluting stents: An alternative strategy for inhibition of restenosis. Circulation 2004; 110: 36-45.
158. Hedman M, Hartikainen J, Syvanne M, Stjernvall J, Hedman A, Kivela A, et al. Safety and feasibility of catheter-based local intracoronary vascular endothelial growth factor gene transfer in the prevention of postangioplasty and in-stent restenosis and in the treatment of chronic myocardial ischemia: Phase II results of the Kuopio Angiogenesis Trial (KAT). Circulation 2003; 107: 2677-83.
159. Swanson N, Hogrefe K, Javed Q, Malik N, Gershlick AH. Vascular endothelial growth factor (VEGF)-eluting stents: in vivo effects on thrombosis, endothelialization and intimal hyperplasia. J Invasive Cardiol 2003; 15: 688-92.
160. Barleon B, Sozzani S, Zhou D, Weich HA, Mantovani A, Marme D. Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood 1996; 87: 3336-43.
161. Marumo T, Schini-Kerth VB, Busse R. Vascular endothelial growth factor activates nuclear factor-kappaB and induces monocyte chemoattractant protein-1 in bovine retinal endothelial cells. Diabetes 1999; 48: 1131-7.
162. Yonemitsu Y, Kaneda Y, Morishita R, Nakagawa K, Nakashima Y, Sueishi K. Characterization of in vivo gene transfer into the arterial wall mediated by the Sendai virus (hemagglutinating virus of Japan) liposomes: An effective tool for the in vivo study of arterial diseases. Lab Invest 1996; 75: 313-23.
163. Halligan SC, Murtagh B, Lennon RJ, Pumper GM, Mathew V, Higano ST, et al. Effect of long-term hormone replacement therapy on coronary endothelial function in postmenopausal women. Mayo Clin Proc 2004; 79: 1514-20.
164. Taddei S, Virdis A, Ghiadoni L, Mattei P, Sudano I, Bernini G, et al. Menopause is associated with endothelial dysfunction in women. Hypertension 1996; 28: 576-82.
165. Pinto S, Virdis A, Ghiadoni L, Bernini G, Lombardo M, Petraglia F, et al. Endogenous estrogen and acetylcholine-induced vasodilation in normotensive women. Hypertension 1997; 29: 268-73.
166. Virdis A, Pinto S, Versari D, Salvetti G, Bernini G, Fruzzetti F, et al. Effect of oral contraceptives on endothelial function in the peripheral microcirculation of healthy women. J Hypertens 2003; 21: 2275-80.
167. Abizaid A, Albertal M, Costa MA, Abizaid AS, Staico R, Feres F, et al. First human experience with the 17-beta-estradiol-eluting stent: the Estrogen And Stents To Eliminate Restenosis (EASTER) trial. J Am Coll Cardiol 2004; 43: 1118-21.
168. New G, Moses JW, Roubin GS, Leon MB, Colombo A, Iyer SS, et al. Estrogen-eluting, phosphorylcholine-coated stent implantation is associated with reduced neointimal formation but no delay in vascular repair in a porcine coronary model. Catheter Cardiovasc Interv 2002; 57: 266-71.
169. Jaschke B, Michaelis C, Milz S, Vogeser M, Mund T, Hengst L, et al. Local statin therapy differentially interferes with smooth muscle and endothelial cell proliferation and reduces neointima on a drug-eluting stent platform. Cardiovasc Res 2005; 68: 483-92.
170. Rotmans JI, Heyligers JM, Verhagen HJ, Velema E, Nagtegaal MM, de Kleijn DP, et al. in vivo cell seeding with anti-CD34 antibodies successfully accelerates endothelialization but stimulates intimal hyperplasia in porcine arteriovenous expanded polytetrafluoroethylene grafts. Circulation 2005; 112: 12-8.
171. Kutryk MJ, Kuliszewski MA. in vivo endothelial progenitor cell seeding for the accelerated endothelialization of endovascular devices. Am J Cardiol 2003; 92: 94L.
172. Aoki J, Serruys PW, van Beusekom H, Ong AT, McFadden EP, Sianos G, et al. Endothelial progenitor cell capture by stents coated with antibody against CD34: The HEALING-FIM (Healthy Endothelial Accelerated Lining Inhibits Neointimal Growth-First In Man) Registry. J Am Coll Cardiol 2005; 45: 1574-9.
173. Sandhu GS, Gulati R, Pislaru SV, Sandhu NP, Witt TA, Simari RD. Magnetic Targeting and Localization of Endothelial Cells on Implanted Stents. Circulation 2005; 111: 1722.
174. Van der Giessen WJ, Serruys P, Visser WJ, Verdouw PD, Van Schalkwijk WP, Jonkind JF. Endothelialization of intravascular stents. J Interven Cardiology 1988; 1: 109-20.
175. Dichek DA, Neville RF, Zwiebel JA, Freeman SM, Leon MB, Anderson WF. Seeding of intravascular stents with genetically engineered endothelial cells. Circulation 1989; 80: 1347-53.
176. Flugelman MY, Virmani R, Leon MB, Bowman RL, Dichek DA. Genetically engineered endothelial cells remain adherent and viable after stent deployment and exposure to flow in vitro. Circ Res 1992; 70: 348-54.
177. Scott NA, Candal FJ, Robinson KA, Ades EW. Seeding of intracoronary stents with immortalized human microvascular endothelial cells. Am Heart J 1995; 129: 860-6.
178. Shirota T, Yasui H, Shimokawa H, Matsuda T. Fabrication of endothelial progenitor cell (EPC)-seeded intravascular stent devices and in vitro endothelialization on hybrid vascular tissue. Biomaterials 2003; 24: 2295-302.
179. Shirota T, Yasui H, Matsuda T. Intralumenal tissue-engineered therapeutic stent using endothelial progenitor cell-inoculated hybrid tissue and in vitro performance. Tissue Eng 2003; 9: 473-85.
180. Rehman J, Li J, Parvathaneni L, Karlsson G, Panchal VR, Temm CJ, et al. Exercise acutely increases circulating endothelial progenitor cells and monocyte-/macrophage-derived angiogenic cells. J Am Coll Cardiol 2004; 43: 2314-8.
181. Michaud SE, Dussault S, Haddad P, Groleau J, Rivard A. Circulating endothelial progenitor cells from healthy smokers exhibit impaired functional activities. Atherosclerosis 2006: 187(2): 423-32.
182. Kondo T, Hayashi M, Takeshita K, Numaguchi Y, Kobayashi K, Iino S, et al. Smoking cessation rapidly increases circulating progenitor cells in peripheral blood in chronic smokers. Arterioscler Thromb Vasc Biol 2004; 24: 1442-7.
183. Loomans CJ, de Koning EJ, Staal FJ, Rookmaaker MB, Verseyden C, de Boer HC, et al. Endothelial progenitor cell dysfunction: A novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes 2004; 53: 195-9.
184. Fadini GP, Miorin M, Facco M, Bonamico S, Baesso I, Grego F, et al. Circulating endothelial progenitor cells are reduced in peripheral vascular complications of type 2 diabetes mellitus. J Am Coll Cardiol 2005; 45: 1449-57.
185. Tepper OM, Galiano RD, Capla JM, Kalka C, Gagne PJ, Jacobowitz GR, et al. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 2002; 106: 2781-6.
186. George J, Herz I, Goldstein E, Abashidze S, Deutch V, Finkelstein A, et al. Number and adhesive properties of circulating endothelial progenitor cells in patients with in-stent restenosis. Arterioscler Thromb Vasc Biol 2003; 23: E57-60.
187. Valgimigli M, Rigolin GM, Fucili A, Porta MD, Soukhomovskaia O, Malagutti P, et al. CD34+ and endothelial progenitor cells in patients with various degrees of congestive heart failure. Circulation 2004; 110: 1209-12.
188. Kong D, Melo LG, Mangi AA, Zhang L, Lopez-Ilasaca M, Perrella MA, et al. Enhanced inhibition of neointimal hyperplasia by genetically engineered endothelial progenitor cells. Circulation 2004; 109: 1769-75.
189. Desideri G, Ferri C. Endothelial activation. Sliding door to atherosclerosis. Curr Pharm Des 2005; 11(17): 2163-75.
190. Dinh T, Veves A. Microcirculation of the diabetic foot. Curr Pharm Des 2005; 11(18): 2301-9.
191. Muro S, Muzykantov V. R. Targeting of antioxidant and antithrombotic drugs to endothelial cell adhesion molecules. Curr Pharm Des 2005; 11(18): 2383-401.