Stimulation of endothelial progenitor cells: A new putative effect of several cardiovascular drugs

European Journal of Clinical Pharmacology

Volumn 66, Issue 3, 2010, Pages 219-230

  António, Natália ^a,b   Fernandes, Rosa ^b   Rodriguez Losada, Noela ^c   Jiménez Navarro, Manuel F ^c   Paiva, Artur ^d   De Teresa Galván, Eduardo ^c   Gonçalves, Lino ^a   Ribeiro, Carlos Fontes ^b   Providência, Luís A ^a  

^a CENTRO HOSPITALAR E UNIVERSITÁRIO DE COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c HOSPITAL UNIVERSITARIO VIRGEN DE LA VICTORIA   (Spain)

^d Centro de Histocompatibilidade do Centro Coimbra   (Portugal)

Author keywords

Cardiovascular disease; Drugs; Endothelial dysfunction; Endothelial progenitor cells; Neovascularization

Indexed keywords

ACETYLSALICYLIC ACID; ANGIOTENSIN RECEPTOR ANTAGONIST; ANTIANGINA PECTORIS AGENT; ANTITHROMBOCYTIC AGENT; BENIDIPINE; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CALCIUM ANTAGONIST; CANDESARTAN; CARDIOVASCULAR AGENT; CELIPROLOL; DIHYDROPYRIDINE DERIVATIVE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; ENALAPRIL; GLYCERYL TRINITRATE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; IRBESARTAN; ISOSORBIDE DINITRATE; LOSARTAN; NIFEDIPINE; NISOLDIPINE; NITRIC ACID DERIVATIVE; OLMESARTAN; PERINDOPRIL; PLACEBO; PRAVASTATIN; QUINAPRIL; RAMIPRIL; SPIRONOLACTONE; TELMISARTAN; UNINDEXED DRUG; ANGIOGENIC FACTOR;

ACUTE CORONARY SYNDROME; ANGIOGENESIS; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ATHEROSCLEROSIS; BLOOD VESSEL FUNCTION; BLOOD VESSEL INJURY; CARDIOVASCULAR RISK; CAROTID ARTERY INJURY; CELL COUNT; CELL DIFFERENTIATION; CELL FUNCTION; CELL HOMING; CELL MIGRATION; CELL PROLIFERATION; CELL STIMULATION; CLINICAL TRIAL; CORONARY ARTERY DISEASE; DRUG MECHANISM; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENDOTHELIUM INJURY; ESSENTIAL HYPERTENSION; HEART MUSCLE ISCHEMIA; HUMAN; HYPERCHOLESTEROLEMIA; HYPERTENSION; LIMB ISCHEMIA; LOW DRUG DOSE; METABOLIC SYNDROME X; NONHUMAN; PERINATAL PERIOD; PLEIOTROPY; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SENESCENCE; STEM CELL; VASCULAR DISEASE; VASCULAR ENDOTHELIUM; ANIMAL; CARDIOVASCULAR DISEASE; DRUG EFFECT; PATHOLOGY; PATHOPHYSIOLOGY; REGENERATION;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; CARDIOVASCULAR AGENTS; CARDIOVASCULAR DISEASES; CELL DIFFERENTIATION; CELL PROLIFERATION; ENDOTHELIAL CELLS; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; REGENERATION; STEM CELLS;

EID: 77951903806     PISSN: 00316970     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00228-009-0764-y     Document Type: Review

References (101)

1. Landmesser U, Hornig B, Drexler H (2004) Endothelial function: a critical determinant in atherosclerosis? Circulation 109:II-27-33
2. Werner N, Kosiol S, Schiegl T, Ahlers P, Walenta K, Link A, Bohm M, Nickenig G (2005) Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med 353:999-1007 (Pubitemid 41262334)
3. Deanfield JE, Halcox JP, Rabelink TJ (2007) Endothelial function and dysfunction: testing and clinical relevance. Circulation 115:1285-1295
4. Hadi H, Suwaidi J (2007) Endothelial dysfunction in diabetes mellitus. Vasc Health Risk Manag 3:853-876
5. Endemann DH, Schiffrin EL (2004) Endothelial dysfunction. J Am Soc Nephrol 15:1983-1992
6. Félétou M, Vanhoutte P (2006) Endothelial dysfunction: a multifaceted disorder (The Wiggers Award Lecture). Am J Physiol Heart Circ Physiol 291:H985-H1002
7. Pola R, Gaetani E, Flex A, Aprahamian T, Bosch-Marcé M, Losordo D, Smith R, Pola P (2008) Comparative analysis of the in vivo angiogenic properties of stable prostacyclin analogs: a possible role for peroxisome proliferator-activated receptors. J Mol Cell Cardiol 36:363-370
8. Davignon J, Ganz P (2004) Role of endothelial dysfunction in atherosclerosis. Circulation 109: III-27-32
9. Yang Z, Ming X-F (2006) Recent advances in understanding endothelial dysfunction in atherosclerosis. Clin Med Res 4:53-65
10. Lerman A, Zeiher AM (2005) Endothelial function: cardiac events. Circulation 111:363-368
11. Schachinger V, Britten MB, Zeiher AM (2000) Prognostic impact of coronary vasodilator dysfunction on adverse longterm outcome of coronary heart disease. Circulation 101:1899-1906
12. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner J (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964-967
13. Umemura T, Higashi Y (2008) Endothelial progenitor cells: therapeutic target for cardiovascular diseases. J Pharmacol Sci 108:1-6
14. Wassmann S, Werner N, Czech T, Nickenig G (2006) Improvement of endothelial function by systemic transfusion of vascular progenitor cells. Circ Res 99:E74-E83
15. Kong D, Melo LG, Gnecchi M, Zhang L, Mostoslavsky G, Liew CC, Pratt RE, Dzau VJ (2004) Cytokine-induced mobilization ofcirculating endothelial progenitor cells enhances repair of injured arteries. Circulation 110:2039-2046
16. Werner N, Junk S, Laufs U, Link A, Walenta K, Bohm M, Nickenig G (2003) Intravenous transfusion of endothelial progenitor cells reduces neointima formation after vascular injury. Circ Res 93:e17-e24
17. Khoo C, Pozzilli P, Alison M (2008) Endothelial progenitor cells and their potential therapeutic applications. Regen Med 3:863-876
18. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, Magner M, Isner JM, Asahara T (1999) Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 5:434-438 (Pubitemid 29180584)
19. Semenza GL (2006) Development of novel therapeutic strategies that target HIF-1. Expert Opin Ther Targets 10:267-280
20. Real C, Caiado F, Dias S (2008) Endothelial progenitors in vascular repair and angiogenesis: how many are needed and what to do? Cardiovasc Hematol Disord Drug Targets 8:185-193
21. Geft D, Schwartzenberg S, George J (2008) Circulating endothelial progenitor cells in cardiovascular disorders. Expert Rev Cardiovasc Ther 6:1115-1121
22. Yamahara K, Itoh H (2009) Potential use of endothelial progenitor cells for regeneration of the vasculature. Ther Adv Cardiovasc Dis 3:17-27
23. Hristov M, Weber C (2008) Endothelial progenitor cells in vascular repair and remodeling. Pharmacol Res 58:148-151
24. Peichev M, Naiyer AJ, Pereira D, Zhu Z, Lane WJ, Williams M, Oz MC, Hicklin DJ, Witte L, Moore MAS, Rafii S (2000) Expression of VEGFR-2 and AC133 by circulating human CD34 + cells identifies a population of functional endothelial precursors. Blood 95:952-958
25. Vasa M, Fichtlscherer S, Adler K, Aicher A, Martin H, Zeiher AM, Dimmeler S (2001) Increase in circulating endothelial progenitor cells by statin therapy in patients with stable coronary artery disease. Circulation 103:2885-2890
26. Bahlmann FH, de Groot K, Mueller O, Hertel B, Haller H, Fliser D (2005) Stimulation of endothelial progenitor cells: a new putative therapeutic effect of angiotensin II receptor antagonists. Hypertension 45:526-529
27. Chen J, Zhang F, Tao Q, Wang X, Zhu J, Zhu J (2004) Number and activity of endothelial progenitor cells from peripheral blood in patients with hypercholesterolaemia. Clin Sci (Lond) 107:273-280 (Pubitemid 39243886)
28. Badimon L, Martínez-González J, Llorente-Cortés V, Rodríguez C, Padró T (2006) Cell biology and lipoproteins in atherosclerosis. Curr Mol Med 6:439-456
29. Rodríguez C, Slevin M, Rodríguez-Calvo R, Kumar S, Krupinski J, Tejerina T, Martínez-González J (2009) Modulation of endothelium and endothelial progenitor cell function by lowdensity lipoproteins: implication for vascular repair, angiogenesis and vasculogenesis. Pathobiology 76:11-22
30. Dimmeler S, Haendeler J, Galle J, Zeiher AM (1997) Oxidized low-density lipoprotein induces apoptosis of human endothelial cells by activation of CPP32-like proteases: a mechanistic clue to the 'Response to Injury' hypothesis. Circulation 95:1760-1763
31. Kume N, Kita T (2004) Apoptosis of vascular cells by oxidized LDL: involvement of caspases and LOX-1 and its implication in atherosclerotic plaque rupture. Circ Res 94:269-270
32. Ii M, Losordo D (2007) Statins and the endothelium. Vascul Pharmacol 46:1-9
33. Bustos C, Hernández-Presa M, Ortego M, Tuñón J, Ortega L, Pérez F, Díaz C, Hernández G, Egido J (1998) HMG-CoA reductase inhibition by atorvastatin reduces neointimal inflammation in a rabbit model of atherosclerosis. J Am Coll Cardiol 32:2057-2064
34. Lacoste L, Lam JYT, Hung J, Letchacovski G, Solymoss CB, Waters D (1995) Hyperlipidemia and coronary disease: correc-tion of the increased thrombogenic potential with cholesterol reduction. Circulation 92:3172-3177
35. Laufs U, Liao JK (1998) Post-transcriptional regulation of endothelial nitric oxide synthase mRNA stability by Rho GTPase. J Biol Chem 273:24266-24271
36. Treasure CB, Klein JL, Weintraub WS, Talley JD, Stillabower ME, Kosinski AS, Zhang J, Boccuzzi SJ, Cedarholm JC, Alexander RW (1995) Beneficial effects of cholesterol-lowering therapy on the coronary endothelium in patients with coronary artery disease. N Engl J Med 332:481-487
37. Laufs U, La Fata V, Plutzky J, Liao JK (1998) Upregulation of endothelial nitric oxide synthase by HMG CoA reductase inhibitors. Circulation 97:1129-1135
38. Laufs U, Marra D, Node K, Liao JK (1999) 3-Hydroxy-3-methylglutaryl-CoA reductase inhibitors attenuate vascular smooth muscle proliferation by preventing Rho GTPaseinduced down-regulation of p27Kip1. J Biol Chem 274:21926-21931
39. Martinez-Gonzalez J, Raposo B, Rodriguez C, Badimon L (2001) 3-hydroxy-3-methylglutaryl coenzyme a reductase inhibition prevents endothelial NO synthase downregulation by atherogenic levels of native LDLs: balance between transcriptional and posttranscriptional regulation. Arterioscler Thromb Vasc Biol 21:804-809
40. Dimmeler S, Aicher A, Vasa M, Mildner-Rihm C, Adler K, Tiemann M, Rütten H, Fichtlscherer S, Martin H, Zeiher A (2001) HMG-CoA reductase inhibitors (statins) increase endothelial progenitor cells via the PI 3-kinase/Akt pathway. J Clin Invest 108:391-397
41. Llevadot J, Murasawa S, Kureishi Y, Uchida S, Masuda H, Kawamoto A, Walsh K, Isner J, Asahara T (2001) HMG-CoA reductase inhibitor mobilizes bone marrow-derived endothelial progenitor cells. J Clin Invest 108:399-405
42. Landmesser U, Bahlmann F, Mueller M, Spiekermann S, Kirchhoff N, Schulz S, Manes C, Fischer D, de Groot K, Fliser D, Fauler G, Marz W, Drexler H (2005) Simvastatin versus ezetimibe: pleiotropic and lipid-lowering effects on endothelial function in humans. Circulation 111:2356-2363
43. Pirro M, Schillaci G, Romagno PF, Mannarino MR, Bagaglia F, Razzi R, Pasqualini L, Vaudo G, Mannarino E (2009) Influence of short-term rosuvastatin therapy on endothelial progenitor cells and endothelial function. J Cardiovasc Pharmacol Ther 14:14-21
44. Kureishi Y, Luo Z, Shiojima I, Bialik A, Fulton D, Lefer DJ, Sessa WC, Walsh K (2000) The HMG-CoA reductase inhibitor simvastatin activates the protein kinase Akt and promotes angiogenesis in normocholesterolemic animals. Nat Med 6:1004-1010
45. Walter DH, Rittig K, Bahlmann FH, Kirchmair R, Silver M, Murayama T, Nishimura H, Losordo DW, Asahara T, Isner JM (2002) Statin therapy accelerates reendothelialization: a novel effect involving mobilization and incorporation of bone marrowderived endothelial progenitor cells. Circulation 105:3017-3024
46. Minami Y, Satoh M, Maesawa C, Takahashi Y, Tabuchi T, Itoh T, Nakamura M (2009) Effect of atorvastatin on microRNA 221 / 222 expression in endothelial progenitor cells obtained from patients with coronary artery disease. Eur J Clin Invest 39:359-367
47. Landmesser U, Engberding N, Bahlmann FH, Schaefer A, Wiencke A, Heineke A, Spiekermann S, Hilfiker-Kleiner D, Templin C, Kotlarz D, Mueller M, Fuchs M, Hornig B, Haller H, Drexler H (2004) Statin-induced improvement of endothelial progenitor cell mobilization, myocardial neovascularization, left ventricular function, and survival after experimental myocardial infarction requires endothelial nitric oxide synthase. Circulation 110:1933-1939
48. Spyridopoulos I, Haendeler J, Urbich C, Brummendorf TH, Oh H, Schneider MD, Zeiher AM, Dimmeler S (2004) Statinsenhance migratory capacity by upregulation of the telomere repeat-binding factor TRF2 in endothelial progenitor cells. Circulation 110:3136-3142
49. Corsini A, Pazzucconi F, Pfister P, Paoletti R, Sirtori C (1996) Inhibitor of proliferation of arterial smooth-muscle cells by fluvastatin Lancet 348:1584
50. Sata M, Nishimatsu H, Suzuki E, Sugiura S, Yoshizumi M, Ouchi Y, Hirata Y, Nagai R (2001) Endothelial nitric oxide synthase is essential for the HMG-CoA reductase inhibitor cerivastatin to promote collateral growth in response to ischemia. FASEB J 15:2530-2532
51. Satoh M, Minami Y, Takahashi Y, Tabuchi T, Itoh T, Nakamura M (2009) Effect of intensive lipid-lowering therapy on telomere erosion in endothelial progenitor cells obtained from patients with coronary artery disease. Clin Sci (Lond) 116:827-835
52. Walter D, Zeiher A, Dimmeler S (2004) Effects of statins on endothelium and their contribution to neovascularization by mobilization of endothelial progenitor cells. Coron Artery Dis 15:235-242
53. Brouet A, Sonveaux P, Dessy C, Balligand J-L, Feron O (2001) Hsp90 ensures the transition from the early Ca2+-dependent to the late phosphorylation-dependent activation of the endothelial nitric-oxide synthase in vascular endothelial growth factorexposed endothelial cells. J Biol Chem 276:32663-32669
54. Assmus B, Urbich C, Aicher A, Hofmann WK, Haendeler J, Rossig L, Spyridopoulos I, Zeiher AM, Dimmeler S (2003) HMG-CoA reductase inhibitors reduce senescence and increase proliferation of endothelial progenitor cells via regulation of cell cycle regulatory genes. Circ Res 92:1049-1055
55. Karlseder J, Broccoli D, Dai Y, Hardy S, de Lange T (1999) p53-and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science 283:1321-1325
56. Spyridopoulos I, Isner J, Losordo D (2002) Oncogenic ras induces premature senescence in endothelial cells: role of p21 (Cip1/Waf1). Basic Res Cardiol 97:117-124
57. Ben-Porath I, Weinberg R (2004) When cells get stressed: an integrative view of cellular senescence. J Clin Invest 113:8-13
58. Ferreira M, Miller K, Cooper J (2004) Indecent exposure: when telomeres become uncapped. Mol Cell 13:7-18
59. Karlseder J, Smogorzewska A, de Lange T (2002) Senescence induced by altered telomere state, not telomere loss. Science 295:2446-2449
60. Gerber H-P, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, Ferrara N (1998) Vascular endothelial growth factor regulates endothelial cell survival through the Phosphatidylinositol 3'-Kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem 273:30336-30343
61. Morales-Ruiz M, Fulton D, Sowa G, Languino LR, Fujio Y, Walsh K, Sessa WC (2000) Vascular endothelial growth factorstimulated actin reorganization and migration of endothelial cells is regulated via the serine/threonine kinase Akt. Circ Res 86:892-896
62. Wassmann S, Nickenig G (2006) Pathophysiological regulation of the AT1-receptor and implications for vascular disease. J Hypertens Suppl 24:S15-S21
63. Nickenig G, Harrison DG (2002) The AT1-type angiotensin receptor in oxidative stress and atherogenesis: part I: oxidative stress and atherogenesis. Circulation 105:393-396 (Pubitemid 34106191)
64. Werner C, Baumhäkel M, Teo K, Schmieder R, Mann J, Unger T, Yusuf S, Böhm M (2008) RAS blockade with ARB and ACE inhibitors: current perspective on rationale and patient selection. Clin Res Cardiol 97: 418-431
65. Okunishi H, Miyazaki M, Toda N (1984) Evidence for a putatively new angiotensin II-generating enzyme in the vascular wall. J Hypertens 2:277-284 228.
66. Vinh A, Widdop RE, Drummond GR, Gaspari TA (2008) Chronic angiotensin IV treatment reverses endothelial dysfunction in ApoE-deficient mice. Cardiovasc Res 77:178-187
67. Ferrario C (2006) Role of angiotensin II in cardiovascular disease therapeutic implications of more than a century of research. J Renin Angiotensin Aldosterone Syst 7:3-14
68. Sasaki K, Murohara T, Ikeda H, Sugaya T, Shimada T, Shintani S, Imaizumi T (2002) Evidence for the importance of angiotensin II type 1 receptor in ischemia-induced angiogenesis. J Clin Invest 109:603-611
69. Egami K, Murohara T, Shimada T, Sasaki K, Shintani S, Sugaya T, Ishii M, Akagi T, Ikeda H, Matsuishi T, Imaizumi T (2003) Role of host angiotensin II type 1 receptor in tumor angiogenesis and growth. J Clin Invest 112:67-75
70. Imanishi T, Hano T, Nishio I (2005) Angiotensin II accelerates endothelial progenitor cell senescence through induction of oxidative stress. J Hypertens 23:97-104
71. Oberleithner H, Ludwig T, Riethmuller C, Hillebrand U, Albermann L, Schafer C, Shahin V, Schillers H (2004) Human endothelium: target for aldosterone. Hypertension 43:952-956
72. Schiffrin EL (2006) Effects of aldosterone on the vasculature. Hypertension 47:312-318
73. Marumo T, Uchimura H, Hayashi M, Hishikawa K, Fujita T (2006) Aldosterone impairs bone marrow-derived progenitor cell formation. Hypertension 48:490-496
74. The OI (2008) Telmisartan, ramipril, or both in patients at high risk for vascular events. N Engl J Med 358:1547-1559
75. Wang C, Verma S, Hsieh I, Chen Y, Kuo L, Yang N, Wang S, Wu M, Hsu C, Cheng C, Cherng W (2006) Enalapril increases ischemia-induced endothelial progenitor cell mobilization through manipulation of the CD26 system. J Mol Cell Cardiol 41:34-43
76. Min TQ, Zhu CJ, Xiang WX, Hui ZJ, Peng SY (2004) Improvement in endothelial progenitor cells from peripheral blood by ramipril therapy in patients with stable coronary artery disease. Cardiovasc Drugs Ther 18:203-209
77. Boyle AJ, Schuster M, Witkowski P, Guosheng X, Seki T, Way K, Itescu S (2005) Additive effects of endothelial progenitor cells combined with ACE inhibition and {beta}-blockade on left ventricular function following acute myocardial infarction. J Renin Angiotensin Aldosterone Syst 6:33-37
78. You D, Cochain C, Loinard C, Vilar J, Mees B, Duriez M, Levy BI, Silvestre J-S (2008) Combination of the angiotensin-converting enzyme inhibitor perindopril and the diuretic indapamide activate postnatal vasculogenesis in spontaneously hypertensive rats. J Pharmacol Exp Ther 325:766-773
79. Chen M, Ichiki T, Ohtsubo H, Imayama I, Inanaga K, Miyazaki R, Sunagawa K (2007) Inhibition of balloon injury-induced neointimal formation by olmesartan and pravastatin in rats with insulin resistance. Hypertens Res 30:971-978
80. Porto I, Di Vito L, De Maria G, Dato I, Tritarelli A, Leone A, Niccoli G, Capogrossi M, Biasucci L, Crea F (2009) Comparison of the effects of ramipril versus telmisartan on high-sensitivity Creactive protein and endothelial progenitor cells after acute coronary syndrome. Am J Cardiol 103:1500-1505
81. Yao E-H, Fukuda N, Matsumoto T, Kobayashi N, Katakawa M, Yamamoto C, Tsunemi A, Suzuki R, Ueno T, Matsumoto K (2007) Losartan improves the impaired function of endothelial progenitor cells in hypertension via an antioxidant effect. Hypertens Res 30:1119-1128
82. Yu Y, Fukuda N, Yao E-H, Matsumoto T, Kobayashi N, Suzuki R, Tahira Y, Ueno T, Matsumoto K (2008) Effects of an ARB on endothelial progenitor cell function and cardiovascular oxidation in hypertension. Am J Hypertens 21:72-77
83. Dahlöf B, Devereux R, Kjeldsen S, Julius S, Beevers G, de Faire U, Fyhrquist F, Ibsen H, Kristiansson K, Lederballe-Pedersen O, Lindholm L, Nieminen M, Omvik P, Oparil S, Wedel H, Group LS (2002) Cardiovascular morbidity and mortality in the Losartan Intervention For Endpoint reduction in hypertension study (LIFE): a randomised trial against atenolol. Lancet 359:995-1003 (Pubitemid 34286536)
84. Fliser D, Buchholz K, Haller H, for the EToO, Pravastatin in I, Atherosclerosis I (2004) Antiinflammatory effects of angiotensin II subtype 1 receptor blockade in hypertensive patients with microinflammation. Circulation 110:1103-1107
85. Schupp M, Clemenz M, Gineste R, Witt H, Jr J, Helleboid S, Hennuyer N, Ruiz P, Unger T, Staels B, Kintscher U (2005) Molecular characterization of new selective peroxisome proliferator-activated receptor gamma modulators with angiotensin receptor blocking activity. Diabetes 54:3442-3452
86. Beattie MS, Shlipak MG, Liu H, Browner WS, Schiller NB, Whooley MA (2003) C-reactive protein and ischemia in users and nonusers of {beta}-blockers and statins: data from the heart and soul study. Circulation 107:245-250
87. Zanchetti A, Bond MG, Hennig M, Neiss A, Mancia G, Dal Palu C, Hansson L, Magnani B, Rahn K-H, Reid JL, Rodicio J, Safar M, Eckes L, Rizzini P, on behalf of the Ei (2002) Calcium antagonist lacidipine slows down progression of asymptomatic carotid atherosclerosis: principal results of the European Lacidipine Study on Atherosclerosis (ELSA), a randomized, doubleblind, long-term trial. Circulation 106:2422-2427
88. Ando H, Nakanishi K, Shibata M, Hasegawa K, Yao K, Miyaji H (2006) Benidipine, a dihydropyridine-Ca2+ channel blocker, increases the endothelial differentiation of endothelial progenitor cells in vitro. Hypertens Res 29:1047-1054
89. Benndorf RA, Gehling UM, Appel D, Maas R, Schwedhelm E, Schlagner K, Silberhorn E, Hossfeld DK, Rogiers X, Böger R (2007) Mobilization of putative high-proliferative-potential endothelial colony-forming cells during antihypertensive treatment in patients with essential hypertension. Stem Cells Dev 16: 329-338
90. Passacquale G, Desideri G, Croce G, Murgo S, Mancarelli MM, Zazzeroni F, Alesse E, Ferri C (2008) Nifedipine improves the migratory ability of circulating endothelial progenitor cells depending on manganese superoxide dismutase upregulation. J Hypertens 26:737-746
91. Yao E-H, Fukuda N, Matsumoto T, Katakawa M, Yamamoto C, Han Y, Ueno T, Kobayashi N, Matsumoto K (2008) Effects of the antioxidative [beta]-blocker celiprolol on endothelial progenitor cells in hypertensive rats. Am J Hypertens 21:1062-1068
92. Aicher A, Heeschen C, Mildner-Rihm C, Urbich C, Ihling C, Technau-Ihling K, Zeiher AM, Dimmeler S (2003) Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 9:1370-1376
93. Jung O, Marklund SL, Geiger H, Pedrazzini T, Busse R, Brandes RP (2003) Extracellular superoxide dismutase is a major determinant of nitric oxide bioavailability: in vivo and ex vivo evidence from ecSOD-deficient mice. Circ Res 93:622-629
94. DiFabio JM, Thomas GR, Zucco L, Kuliszewski MA, Bennett BM, Kutryk MJ, Parker JD (2006) Nitroglycerin attenuates human endothelial progenitor cell differentiation, function, and survival. J Pharmacol Exp Ther 318:117-123
95. Thum T, Fraccarollo D, Thum S, Schultheiss M, Daiber A, Wenzel P, Munzel T, Ertl G, Bauersachs J (2007) Differential effects of organic nitrates on endothelial progenitor cells are determined by oxidative stress. Arterioscler Thromb Vasc Biol 27:748-754
96. Jurt U, Gori T, Ravandi A, Babaei S, Zeman P, Parker JD (2001) Differential effects of pentaerythritol tetranitrate and nitroglycerin on the development of tolerance and evidence of lipid peroxidation: a human in vivo study. J Am Coll Cardiol 38:854-859
97. Antithrombotic Trialists' Collaboration (2002) Collaborative meta-analysis of randomised trials of antiplatelet therapy for prevention of death, myocardial infarction, and stroke in high risk patients. Br Med J 324:71-86
98. Mehta J (1998) Salutary effects of aspirin in coronary artery disease are not limited to its platelet inhibitory effects. Clin Cardiol 21:879-884
99. Kharbanda RK, Walton B, Allen M, Klein N, Hingorani AD, MacAllister RJ, Vallance P (2002) Prevention of inflammationinduced endothelial dysfunction: a novel vasculo-protective action of aspirin. Circulation 105:2600-2604
100. Chen T, Chen J, Xie X (2006) Effects of aspirin on number, activity and inducible nitric oxide synthase of endothelial progenitor cells from peripheral blood. Acta Pharmacol Sin 27:430-436
101. Hu Z, Zhang F, Yang Z, Zhang J, Zhang D, Yang N, Zhang Y, Cao K (2008) Low-dose aspirin promotes endothelial progenitor cell migration and adhesion and prevents senescence. Cell Biol Int 32:761-768