Recent studies have demonstrated that aging or senescence constitutes a potential limitation to the ability of endothelial progenitor cells (EPCs) to sustain ischemic tissue repair. Excess amount of reactive oxygen species (ROS) is involved in senescence, causing defective neovascularization. Conversely, estrogens have been shown to accelerate recovery of the endothelium after vascular injury. Estrogen reduces EPC senescence through augmentation of telomerase activity. In addition, the inhibition of EPC senescence by estrogen in vitro may improve the functional activity of EPCs in a way that is important for potential cell therapy. This review describes current understanding of EPC senescence and the role of estrogen in preventing EPC senescence.
Ali, J., Liao, F., Martens, E. and Muller, W.A. ( 1997) Vascular endothelial cadherin (VE-cadherin): cloning and role in endothelial cell-cell adhesion. Microcirculation4: 267-277.
2.
Amrani, M., Goodwin, A.T., Gray, C.C. and Yacoub, M.H. ( 1996) Aging is associated with reduced basal and stimulated release of nitric oxide by the coronary endothelium. Acta Physiol Scand157: 79-84.
3.
Asahara, T., Murohara, T., Sullivan, A., Silver, M., van der Zee, R., Li, T. et al. (1997) Isolation of putative progenitor endothelial cells for angiogenesis . Science275: 964-967.
4.
Bahlmann, F.H., de Groot, K., Mueller, O.H., Hertel, B., Haller, H. and Fliser, D.(2005) Stimulation of endothelial progenitor cells - a new putative therapeutic effect of angiotensin II receptor antagonism. Hypertension45: 526-529.
5.
Ballard, V.L.T. and Edelberg, J.M. ( 2007) Stem cells and the regeneration of the aging cardiovascular system. Circ Res100: 1116-1127.
6.
Bauer, K.A., Weiss, L.M., Sparrow, D., Vokonas, P.S. and Rosenberg, R.D. ( 1987) Aging-associated changes in indices of thrombin generation and protein C activation in humans. Normative Aging Study. J Clin Invest80: 1527-1534.
7.
Benetos, A., Okuda, K., Lejemi, M., Kimura, M., Thomas, F., Skumick, J. et al. (2001) Telomere length as an indicator of biological aging: the gender effect and relation with pulse pressure and pulse wave velocity . Hypertension37: 381-385.
8.
Bernardini, D., Ballabio, E., Mariotti, M. and Maier, J.A. ( 2005) Differential expression of EDF-1 and endothelial nitric oxide synthase by proliferating, quiescent, and senescent microvascular endothelial cells. Biochim Biophys Acta1745: 265-272.
9.
Besler, C., Doerries, C., Giannotti, G., Luscher, T.F. and Landmesse, U. ( 2008) Pharmacological approaches to improve endothelial repair mechanisms. Expert Rev Cardiovasc Ther6: 1071-1082.
10.
Billon, A., Lehoux, S., Lam ShangLeen, L., Laurell, H., Filipe, C., Benouaich, V. et al. (2008) The estrogen effects on endothelial repair and mitogen-activated protein kinase activation are abolished in endothelial nitric-oxide (NO) synthase knockout mice, but not by NO synthase inhibition by N-nitro-L-arginine methyl ester. Am J Pathol172: 830-838.
11.
Blokhina, O., Virolainen, E. and Fagerstedt, K.Y. ( 2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot (Lond) 91: 179-194.
12.
Chang, E. and Harley, C.B. ( 1995) Telomere length and replicative aging in human vascular tissues. Proc Natl Acad Sci USA92: 11190-11194.
13.
Chen, J.Z., Zhang, F.R., Tao, Q.M., Wang, X.X. and Zhu, J.H. ( 2004) Number and activity of endothelial progenitor cells from peripheral blood in patients with hypercholesterolemia. Clin Sci Lond107: 273-280.
14.
Cherif, H., Tary, J.I., Ozamne, S.E. and Hales, C.N. ( 2003) Ageing and telomeres: a study into organ- and gender-specific telomere shortening. Nucleic Acids Res31: 1576-1583.
15.
Colak, E., Majkic-Singh, N., Stankovic, S., Sreckovic-Dimitrijevie, V., Djordjevic, P.B., Lalik, K. et al. (2005) Parameters of antioxidative defence in type 2 diabetes patients with cardiovascular complications. Ann Med37: 613-620.
16.
Cooke, C.L. and Davidge, S.T. ( 2002) Peroxynitrite increases iNOS through NF-κB and decreases prostacyclin synthase in endothelial cells. Am J Physiol Cell Physiol282: C395-C402.
17.
Coviello-McLaughlin, G.M. and Prowse, K.R. ( 1997) Telomere length regulation during postnatal development and ageing in Mus spretus. Nucleic Acids Res25: 3051-3058.
18.
Dernbach, E., Urbich, C., Brandes, R.P., Hofmann, W.K., Zeiher, A.M. and Dimmeler, S. ( 2004) Antioxidative stress-associated genes in circulating progenitor cells: Evidence for enhanced resistance against oxidative stress. Blood104: 3591-3597.
19.
Doshida, M., Ohmichi, M., Tsutsumi, S., Kawagoe, J., Takahashi, T., Du, B. et al. (2006) Raloxifene increases proliferation and up-regulation of telomerase activity in human umbilical vein endothelial cells. J Biol Chem281: 24270-24278.
20.
Dubey, R.K. and Jackson, E.K. ( 2001) Estrogen-induced cardiorenal protection: potential cellular biochemical, and molecular mechanisms. Am J Physiol Renal Physio280: F365-F388.
21.
Edelberg, J.M., Tang, L., Hatton, K., Lyden, D. and Rafii, S. ( 2002) Young adult bone marrow-derived endothelial precursor cells restore aging-impaired cardiac angiogenic function. Circ Res90: E89-93.
22.
Egami, K., Murohara, T., Shimada, T., Sasaki, K., Shintani, S., Sugaya, T. et al. (2003) Role of host angiotensin II type 1 receptor in tumor angiogenesis and growth. J Clin Invest112: 67-75.
Fadini, G.P., Kreutzenberg, S., Albiero, M., Coracina, A., Pagnin, E., Baesso, I. et al. (2008) Gender differences in endothelial progenitor cells and cardiovascular risk profile: the role of female estrogens. Arterioscler Thromb Vasc Biol28: 997-1004.
25.
Fadini, G.P., Albiero, M., Cignarella, A., Bolego, C., Pinna, C., Boscaro, E. et al. (2009) Effects of androgens on endothelial progenitor cells in vitro and in vivo. Clin Sci (in press).
26.
Fadini, G.P., Coracina, A., Baesso, I., Agostini, C., Tiengo, A., Avogaro, A. et al. (2006) Peripheral blood CD34+KDR+ endothelial progenitor cells are determinants of subclinical atherosclerosis in a middle-aged general population. Stroke37: 2277-2282.
27.
Farhat, M.Y., Lavigne, M.C. and Ramwell, P.W. ( 1996) The vascular protective effects of estrogen. FASEB J10: 615-624.
28.
Feng, J., Funk, W.D., Wang, S.S., Weinrich, S.L., Avillon, A.A., Chiu, C.P. et al. (1995) The RNA component of human telomerase. Science269: 1236-1241.
29.
Fontaine, V., Filipe, C., Werner, N., Gourdy, P., Billon, A., Garmy-Suini, B. et al. (2006) Essential role of bone marrow fibroblast growth factor-2 in the effect of estradiol on re-endotheliazation and endothelial progenitor cell mobilization. Am J Pathol169: 1855-1862.
30.
Foresta, C., Caretta, N., Lana, A., De Toni, L., Biagioli, A., Ferlin, A. and Garolla, A. ( 2006) Reduced number of circulating endothelial cells in hypogonadal men. J Clin Endocrinol Metab91: 4599-4602.
31.
Foresta, C., Zuccarello, D., De Toni, L., Garolla, A., Caretta, N. and Ferlin, A. ( 2007) Androgen stimulate endothelial progenitor cells through an androgen receptor-mediated pathway. Clin Endocrinol68: 284-289.
32.
Foresta, C., Toni, L., Di Mambro, A., Ferlin, A., Perilli, L., Bertuzzi, I. et al. (2008) Role of estrogen receptors in menstrual cycle-related neoangiogenesis and their influence on endothelial progenitor cell physiology . Fertil Steril (in press).
33.
Galasso, G., Schiekofer, S., Sato, K., Shibata, R., Hasndy, D.E., Ouchi, N. et al. (2006) Impaired angiogenesis in glutathione peroxidase-1-deficient mice is associated with endothelial progenitor cell dysfunction. Circ Res98: 254-261.
34.
Gargett, C.E., Zaitseva, M., Bucak, K., Chu, S., Fuller, P.J. and Rogers, P.A. ( 2002) 17Beta-estradiol up-regulates vascular endothelial growth factor-2 expression in human myometrial microvascular endothelial cells: role of estrogen receptor-alpha and -beta. J Clin Endocrinol Metab87: 4341-4349.
Goldschmidt-Clermont, P.J., Lam, G. and Dong, C. ( 2003) Progenitor cell dysfunction: a key trigger for atherosclerotic inflammation. Am Heart J146: S5-12.
37.
Gragasin, F.S., Xu, Y., Arenas, I.A., Kainth, N. and Davidge, S.T. ( 2003) Estrogen reduces angiotensin II-induced nitric oxide synthase and NAD(P)H oxidase expression in endothelial cells. Arterioscler Thromb Vasc Biol23: 38-44.
38.
Hager, K., Setzer, J., Vogl, T., Voit, J. and Platt, D. ( 1989) Blood coagulation factors in the elderly. Arch Gerontol Geriatr9: 277-282.
39.
Hamada, H., Kim, M.K., Iwakura, A., Ii, M., Throne, T., Qin, G. et al. (2006) Estrogen receptors alpha and beta mediate contribution of bone marrow-derived endothelial progenitor cells to functional recovery after myocardial infarction. Circulation114: 2261-2270.
40.
Hayflik, L. and Moorhead, P. ( 1961) The serial cultivation of human diploid strains. Exp Cell Res25: 585-621.
41.
He, T., Peterson, T.E., Holmuhamedov, E.L., Terzic, A., Caplice, N.M., Oberley, L.W. et al. (2004) Human endothelial progenitor cells tolerate oxidative stress due to intrinsically high expression of manganese superoxide dismutase. Arterioscler Thromb Vasc Biol24: 2021-2027.
42.
Heeschen, C., Lehmann, R., Honold, J., Assmus, B., Aicher, A., Walter, D.H. et al. (2004) Profoundly reduced neovascularization capacity of bone marrow mononuclear cells derived from patients with chronic ischemic heart disease. Circulation109: 1615-1622.
43.
Heiss, C., Keymel, S., Niesler, U., Ziemann, J., Kelm, M. and Kalka, C. ( 2005) Impaired progenitor cell activity in age-related endothelial dysfunction. J Am Coll Cardiol45: 1441-1448.
44.
Heitzer, T., Wenzel, U., Hink, U., Krollner, D., Skatchkov, M., Stahl, R.A. et al. (1999) Increased NAD(P)H oxidase-mediated superoxide production in renovascular hypertension: evidence for an involvement of protein kinase C. Kidney Int55: 252-260.
45.
Histov, M., Erl, W. and Weber, P.C. ( 2003) Endothelial progenitor cells: mobilization, differentiation, and homing. Arterioslcer Throm Basc Biol23: 1185-1189.
46.
Hoetzer, G.L., MacEneaney, O.J., Irmiger, H.M., Keith, R., Van Guilder, G.P., Stauffer, B.L. et al. (2007) Gender differences in circulating endothelial progenitor cell colony-forming capacity and migratory activity in middle-aged adults. Am J Cardiol99: 46-48.
47.
Hulley, S., Furberg, C., Barrett-Connor, E., Cauley, J., Grady, D., Haskell, W. et al.; HERS Research Group (2002) Noncardiovascular disease outcomes during 6.8 years of hormone therapy: Heart and Estrogen/progestin Replacement Study follow-up (HERS II). JAMA288: 58-66.
48.
Hulley, S., Grady, D., Bush, T., Furberg, C., Herrington, D., Riggs, B. et al. (1998) Randomized trial of estrogen plus progestin for secondary prevention of coronary heart disease in postmenopausal women. Heart and Estrogen/progestin Replacement Study (HERS) Research Group. JAMA280: 605-613.
49.
Hur, J., Yoon, C.H., Kim, H.S., Choi, J.H., Kang, H.J., Hwang, K.K. et al. (2004) Characterization of two types of endothelial progenitor cells and their different contribution to neovasculogenesis. Arterioscler Thromb Vasc Biol24: 288-293.
50.
Ichiki, T., Usui, M., Kato, M., Funakoshi, Y., Ito, K., Egashira, K. et al. (1998) Downregulation of angiotensin II type 1 receptor gene transcription by nitric oxide. Hypertension31: 342-348.
Imanishi, T., Hano, T. and Nishio, I. ( 2005a) Estrogen reduces endothelial progenitor cell senescence through augmentation of telomerase activity. J Hypertens23: 1699-1706.
53.
Imanishi, T., Tsujioka, H. and Akasaka, T. ( 2008) Endothelial progenitor cells and senescence: contribution to oxidative stress. Curr Cardiol Rev4: 275-286.
54.
Imanishi, T., Moriwaki, C., Hano, T. and Nishio, I. ( 2005b) Endothelial progenitor cell senescence is accelerated in both experimental hypertensive rats and patients with hypertension. J Hypertens23: 1831-1837.
55.
Imanishi, T., Hano, T. and Nishio, I. ( 2005c) Angiotensin II accelerates endothelial progenitor cell senescence through induction of oxidative stress. J Hypertens23: 97-104.
56.
Imanishi, T., Hano, T. and Nishio, I. ( 2005d) Estrogen reduces angiotensin II-induced acceleration of senescence in endothelial progenitor cells. Hypertes Res28: 263-271.
57.
Ingram, D.A., Krier, T.R., Mead, L.E., McGuire, C., Prater, D.N., Bhavsar, J. et al. (2007) Clonogenic endothelial progenitor cells are sensitive to oxidative stress. Stem Cells25: 297-304.
58.
Iwakura, A., Luedemann, C., Shastry, S., Hanley, A., Kearney, M., Aikawa, R. et al. (2003) Estrogen-mediated, endothelial nitiric oxide synthase-dependent mobilization of bone marrow-derived endothelial progenitor cells contributes to re-endotheliazation after arterial injury. Circulation108: 3115-3121.
59.
Iwakura, A., Shubha, S., Luedemann, C., Hamada, H., Kawamoto, A., Kishore, R. et al. (2006) Estradiol enhances recovery after myocardial infarction by augmenting incorporation of bone marrow-derived endothelial progenitor cells into sites of ischemia-induced neovascularization via endothelial nitric oxide synthase-mediated activation of matrix metalloproteinase-9. Circulation113: 1605-1614.
60.
Jeanclos, E., Schork, N.J., Kyvik, K.O., Kimura, M., Skumick, J.H. and Aviv, A. ( 2000) Telomere length inversely correlates with pulse pressure and is highly familial. Hypertension36: 195-200.
61.
Kang, S.S., Kwon, T., Kwon, D.Y. and Do, S.I. ( 1999) Akt protein kinase enhances human telomerase activity through phosphorylation of telomerase reverse transcriptase subunit. J Biol Chem274: 13085-13090.
62.
Khan, M.A., Liu, M.W., Singh, D., Pal, A., Chio, F.L., Lawson, D. et al. (2000) Long-term (three years) effect of estrogen replacement therapy on major adverse cardiac events in postmenopausal women after intracoronary stenting. Am J Cardiol86: 330-333.
63.
Kushner, E.J., Van Guilder, G.P., MacEneaney, O.J., Cech, J.N., Stauffer, B.L. and DeSouza, C.A.(2009) Aging and endothelial progenitor cell telomere length in healthy men . Clin Chem Lab Med47: 47-50.
64.
Kyo, S., Takakura, M., Kanaya, T., Zhuo, W., Fujimoto, K., Nishio, Y. et al. (1999) Estrogen activates telomerase. Cancer Res59: 5917-5921.
65.
Lan ShangLeen, L., Filipe, C., Billon, A., Garmy-Susini, B., Jalvy, S., Robbesyn, F. et al. (2008) Estrogen-stimulated endothelial repair requires osteopontin. Arterioscler Thromb Vasc Biol28: 2131-2136.
66.
Lantin-Hermoso, R.L., Rosenfield, C.R., Yuhanna, I.S., German, Z., Chen, Z. and Shaul, P.W. ( 1997) Estrogen acutely stimulates nitric oxide synthase activity in fetal pulmonary artery endothelium. Am J Physiol273: L119-L126.
67.
Lassegue, B. and Clempus, R.E. ( 2003) Vascular NAD(P)H oxidases: specific features, expression, and regulation. Am J Physiol285: R277-R297.
68.
Leri, A., Malhotra, A., Liew, C.C., Kajstura, J. and Anversa, P. ( 2000) Telomerase activity in rat cardiac myocytes is age- and gender-dependent. J Moll Cell Cardiol32: 385-390.
69.
Li, D., Saldeen, T., Romeo, F. and Mehta, J.L. ( 2000) Oxidized LDL upregulates angiotensin II type 1 receptor expression in cultured human coronary artery endothelial cells: the potential role of transcription factor NF-κB. Circulation102: 1970-1976.
70.
Lin, Y., Weisdorf, D.J., Solovey, A. and Hebbel, R.P. ( 2000) Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest105: 71-77.
71.
Linke, A., Adams, V., Schulze, P.C., Erbs, S., Gielen, S., Fiehn, E. et al. (2005) Antioxidative effects of exercise training in patients with chronic heart failure: increase in radical scavenger enzyme activity in skeletal muscle. Circulation111: 1763-1770.
72.
Ma, F.X., Zhou, B., Chen, Z., Ren, Q., Lu, S.H., Sawamura, T. and Han, Z.C. ( 2006) Oxidized low density lipoprotein impairs endothelial progenitor cells by regulation of endothelial nitric oxide synthase. J Lipid Res47: 1227-1237.
73.
Masuda, H., Kalka, C., Takahashi, T., Yoshida, M., Wada, M., Kobori, M. et al. (2007) Estrogen-mediated endothelial progenitor cell biology and kinetics for physiological postnatal vasculogenesis. Circ Res101: 598-606.
74.
Matsumori, K., Yu, E.Y., Khurts, S., Ben-Porath, I., Currier, J.L., Metz, G.B. et al. (2003) Telomerase maintains telomere structure in normal human cells. Cell114: 241-253.
75.
Matsushita, H., Chang, E., Glassford, A.J., Cooke, J.P., Chiu, C.P. and Tsao, P.S. ( 2001) eNOS activity is reduced in senescent human endothelial cells: preservation by hTERT immortalization. Circ Res89: 793-798.
76.
Mendelsohn, M.E. and Karas, R.H. ( 1999) The protective effects of estrogen on the cardiovascular system. N Engl J Med10: 615-624.
77.
Min, T.Q., Zhu, C.J., Xiang, W.X., Hui, Z.J. and Peng, S.Y. ( 2004) Improvement in endothelial progenitor cells from peripheral blood by ramipril therapy in patients with stable coronary artery disease . Cardiovasc Drugs Ther18: 203-209.
78.
Miller, V.M. and Duckles, S.P. ( 2008) Vascular actions of estrogens: functional implications . Pharmacol Rev60: 210-241.
79.
Mooradian, A.D. ( 1993) Antioxidant properties of steroids. J Steroid Biochem Mol Biol45: 509-511.
80.
Murasawa, S., Llevadot, J., Silver, M., Isner, M., Losordo, D.W. and Asahara, T. ( 2002) Constitutive human telomerase reverse transcriptase expression enhances regenerative properties of endothelial progenitor cells. Circulation106: 1133-1139.
81.
Nakamura, T.M., Morin, G.B., Chapman, K.B., Weinrich, S.L., Andrews, W.H., Linger, J. et al. (1997) Telomerase catalytic subunit homologs from fission yeast and human. Science277: 955-959.
82.
Nathan, L. and Chaudhuri, G. ( 1997) Estrogen and atherosclerosis. Ann Rev Pharmacol Toxicol37: 477-515.
83.
Nawrot, T.S., Staessen, J.A., Gardner, J.P. and Aviv, A. ( 2004) Telomere length and possible link to X chromosome. Lancet363: 507-510.
84.
Noble, M., Smith, J., Power, J. and Mayer-Proschel, M. ( 2003) Redox state as a central modulator of precursor cell function . Ann NY Acad Sci991: 251-271.
85.
Papapetropoulos, A., Garcia-Cardena, G., Madri, J.A. and Sessa, W.C. ( 1997) Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells . J Clin Invest100: 3131-3139.
86.
Rauscher, F.M., Goldschmidt-Clermont, P.J., Davis, B.H., Wang, T., Gregg, D., Ramaswami, P. et al. (2003) Aging, progenitor cell exhaustion, and atherosclerosis . Circulation108: 457-463.
87.
Robb, A.O., Mills, N.L., Smith, I.B., Short, A., Tura-Ceide, O., Barclay, G.R. et al. (2009) Influence of menstrual cycle on circulating endothelial progenitor cells. Hum Reprod24: 619-625.
88.
Rodgers, K.E., Xiong, S., Steer, R. and diZerega, G.S. ( 2000) Effect of angiotensin II on hematopoietic progenitor cell proliferation. Stem Cells18: 287-294.
89.
Ruiz-Ortega, M., Lorenzo, O., Ruperez, M., Konig, S., Wittig, B. and Egido, J. ( 2000) Angiotensin II activates nuclear transcription factor κB through AT1 and AT2 in vascular smooth muscle cells: molecular mechanism . Circ Res86: 1266-1272.
90.
Sanada, F., Taniyama, Y., Azuma, J., Ikeuchi, K., Dosaka, N., Yokoi, T. et al. (2009) Hepatocyte growth factor, but not vascular endothelial growth factor, attenuates angiotensin II-induced endothelial progenitor cell senescence . Hypertension53: 77-82.
91.
Sasaki, K., Murohara, T., Ikeda, H., Sugaya, T., Shimada, T., Shintani, S. et al. (2002) Evidence for the importance of angiotensin II type 1 receptor in ischemia-induced angiogenesis. J Clin Inves109: 603-611.
92.
Scheubel, R.J., Zorn, H., Silber, R.E., Kuss, O., Morawierz, H., Holtz, J. et al. (2003) Age-dependent depression in circulating endothelial progenitor cells in patients undergoing coronary artery bypass grafting. J Am Coll Cardiol42: 2073-2080.
93.
Serrano, A.L. and Andres, V. ( 2004) Telomeres and cardiovascular disease: does size matter ? Circ Res94: 575-584.
94.
Shearman, A.M., Cupples, L.A., Demissie, S., Peter, I., Schmid, C.H., Karasa, R.H. et al. (2003) Association between estrogen receptor alpha gene variation and cardiovascular disease. JAMA290: 2263-2270.
95.
Simoncini, T., Hafezi-Moghadam, A., Brazil, D.P., Ley, K., Chin, W.W. and Liao, J.K. ( 2000) Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature407: 538-541.
96.
Sowers, J.R. ( 2002) Hypertension, angiotensin ii, and oxidative stress. N Engl J Med346: 1999-2001.
97.
Splipak, M.G., Angela, B.G., Go, A.S., Fredrick, P.D., Canto, J.G. and Grady, D. ( 2001) Hormone therapy and in-hospital survival after myocardial infarction in postmenopausal women. Circulation104: 2300-2304.
98.
Stehlow, K., Werner, N., Berweiler, J., Link, A., Dirnagl, U., Priller, J. et al. (2003) Estrogen increases bone marrow-derived endothelia progenitor cell production and diminishes neointima formation. Circulation107: 3059-3065.
99.
Sugihara, S., Yamamoto, Y., Matsuura, T., Narazaki, G., Yamasaki, A., Igawa, G. et al. (2007) Age-related BM-MNC dysfunction hampers neovascularization . Mech Ageing Dev128: 511-516.
100.
Tanaka, M., Kyo, S., Takakura, M., Kanaya, T., Segawa, T., Yamashita, K. et al. (1998) Expression of telomerase activity in human endometrium is localized to epithelial glandular cells and regulated in a menstrual phase-dependent manner correlated 1with cell proliferation. Am J Pathol153: 1985-1991.
101.
Touyz, R.M. ( 2004) Reactive oxygen species, vascular oxidative stress, and redox signaling in hypertension: what is the clinical significance?Hypertension44: 248-252.
102.
Touyz, R.M., Endemann, D., He, G., Li, J.S. and Schiffrin, E.L. ( 1999) Role of AT2 receptors in angiotensin II-stimulated contraction of small mesenteric arteries in young SHR. Hypertension33: 366-372.
103.
Urbich, C., Heeschen, C., Aisher, A., Dernbach, E., Zeiher, A.M. and Dimmeler, S. ( 2003) Relevance of monocyte features for neovascularization capacity of circulating endothelial progenitor cells. Circulation108: 2511-2516.
104.
Urbich, C. and Dimmeler, S. ( 2004) Endothelial progenitor cells: characterization and role in vascular biology. Circ Res95: 343-353.
105.
Valgimigli, M., Rigolin, G.M., Fucili, A., Porta, M.D., Soukhomovskaia, O., Malaguti, P. et al. (2004) CD34+ and endothelial progenitor cells in patients with various degree of congestive heart failure. Circulation110: 1209-1212.
106.
Vasa, M., Breitschopf, K., Zeiher, A.M. and Dimmeler, S. ( 2000) Nitric oxide activates telomerase and delays endothelial cell senescence. Circ Res87: 540-542.
107.
Vasa, M., Fichtlscherer, S., Adler, K., Aicher, A., Martin, H., Zeiher, A.M. et al. (2001a) Increase in circulating endothelial progenitor cells by statin therapy in patients with stable coronary artery disease. Circulation103: 2885-2890.
108.
Vasa, M., Fichtlscherer, S., Aicher, A., Adler, K., Urbich, C., Martin, H. et al. (2001b) Numbers and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res89: e1-e7.
109.
Ward, M.R., Stewart, D.J. and Kutryk, M.J. ( 2007) Endothelial progenitor cell therapy for the treatment of coronary disease, acute MI, and pulmonary arterial hypertension: current perspectives. Catheter Cardiovasc Interv70: 983-998.
110.
Wassmann, S., Werner, N., Czech, T. and Nickenig, G. ( 2006) Improvement of endothelial function by systemic transfusion of vascular progenitor cells. Circ Res99: e74-e83.
