Estrogen-Mediated, Endothelial Nitric Oxide Synthase-Dependent Mobilization of Bone Marrow-Derived Endothelial Progenitor Cells Contributes to Reendothelialization after Arterial Injury

Circulation

Volumn 108, Issue 25, 2003, Pages 3115-3121

  Iwakura, Atsushi ^a   Luedemann, Corinne ^a   Shastry, Shubha ^a   Hanley, Allison ^a   Kearney, Marianne ^a   Aikawa, Ryuichi ^a   Isner, Jeffrey M ^a   Asahara, Takayuki ^a   Losordo, Douglas W ^a,b  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

Author keywords

Arteries; Endothelium; Estrogen; Nitric oxide synthase

Indexed keywords

ANGIOPOIETIN RECEPTOR; BETA GALACTOSIDASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ESTRADIOL; ESTROGEN; NITRIC OXIDE SYNTHASE; PLACEBO; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTERY DIAMETER; ARTICLE; BONE MARROW; CAROTID ARTERY INJURY; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ESTROGEN THERAPY; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MITOGENESIS; MOUSE; NONHUMAN; OVARIECTOMY; PERIPHERAL CIRCULATION; PRIORITY JOURNAL; STEM CELL; STEM CELL TRANSPLANTATION; TISSUE REPAIR; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS; ARTERIAL OCCLUSIVE DISEASES; BONE MARROW CELLS; CAROTID ARTERIES; CAROTID STENOSIS; CELL DIVISION; CELL MOVEMENT; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; ESTRADIOL; FEMALE; KINETICS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; REGENERATION; STEM CELLS;

EID: 0346157997     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.CIR.0000106906.56972.83     Document Type: Article

References (35)

1. Ross R. Atherosclerosis: a defense mechanism gone awry. Am J Pathol. 1993;143:985-1002.
2. Morales DE, McGowan KA, Grant DS, et al. Estrogen promotes angiogenic activity in human umbilical vein endothelial cells in vitro and in a murine model. Circulation. 1995;91:755-763.
3. Venkov CD, Rankin AB, Vaughan DE. Identification of authentic estrogen receptor in cultured endothelial cells. Circulation. 1996;94:727-733.
4. Kim-Schulze S, McGowan KA, Hubchak SC, et al. Expression of an estrogen receptor by human coronary artery and umbilical vein endothelial cells. Circulation. 1996;94:1402-1407.
5. Clowes AW, Collazzo RE, Karnovsky MJ. A morphologic and permeability study of luminal smooth muscle cells after arterial injury in the rat. Lab Invest. 1978;39:141-150.
6. Clowes AW, Reidy MA, Clowes MM. Kinetics of cellular proliferation after arterial injury, I: smooth muscle growth in the absence of endothelium. Lab Invest. 1983;49:327-333.
7. Asahara T, Bauters C, Pastore CJ, et al. Local delivery of vascular endothelial growth factor accelerates reendothelialization and attenuates intimal hyperplasia in balloon-injured rat carotid artery. Circulation. 1995;91:2793-2801.
8. Krasinski K, Asahara T, Spyridopoulos I, et al. Estradiol accelerates endothelial recovery after arterial injury. Circulation. 1997;95:1768-1772.
9. Asahara T, Murohara T, Sullivan A, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:964-967.
10. Takahashi T, Kalka C, Masuda H, et al. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med. 1999;5:434-438.
11. Shi Q, Rafii S, Wu MH-D, et al. Evidence for circulating bone marrow-derived endothelial cells. Blood. 1998;92:362-367.
12. Reyes M, Dudek A, Jahagirdar B, et al. Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest. 2002;109:337-346.
13. Edelberg JM, Tang L, Hattori K, et al. Young adult bone marrow-derived endothelial precursor cells restore aging-impaired cardiac angiogenic function. Circ Res. 2002;90:E89-E93.
14. Lyden D, Hattori K, Dias S, et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med. 2001;7:1194-1201.
15. Otani A, Kinder K, Ewalt K, et al. Bone marrow-derived stem cells target retinal astrocytes and can promote or inhibit retinal angiogenesis. Nat Med. 2002;8:1004-1010.
16. Masuda H, Kalka C, Takahashi T, et al. Regulatory role of estrogen on endothelial progenitor cell kinetics for cyclic endometrial neovascularization. Circulation. 1999;100(suppl I):I-2503.
17. Burger HG, Loriaux DL, Marshall JC, et al. Endocrinology. 4th ed. Philadelphia, Pa: WB Saunders Co; 2001.
18. Asahara T, Masuda H, Takahashi T, et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res. 1999;85:221-228.
19. Lindner V, Fingerle J, Reidy MA. Mouse model of arterial injury. Circ Res. 1993;73:792-796.
20. Goukassian D, Kishore R, Dolan C, et al. Engineering the response to vascular injury: divergent effects of deregulated E2F1 expression on vascular smooth muscle cells and endothelial cells result in endothelial recovery and inhibition of neointimal growth. Circ Res. 2003;93:162-169.
21. Asahara T, Takahashi T, Masuda H, et al. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J. 1999;18:3964-3972.
22. Werner N, Priller J, Laufs U, et al. 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.
23. Walter DH, Rittig K, Bahlmann FH, et al. Statin therapy accelerates reendothelialization: a novel effect involving mobilization and incorporation of bone marrow-derived endothelial progenitor cells. Circulation. 2002;105:3017-3024.
24. Yamaguchi J, Kusano KF, Masuo O, et al. Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation. 2003;107:1322-1328.
25. Aikawa R, Nawano M, Gu Y, et al. Insulin prevents cardiomyocytes from oxidative stress-induced apoptosis through activation of PI3 kinase/Akt. Circulation. 2001;102:2873-2879.
26. Brouchet L, Krust A, Dupont S, et al. Estradiol accelerates reendothelialization in mouse carotid artery through estrogen receptor-alpha but not estrogen receptor-beta. Circulation. 2001;103:423-428.
27. Strehlow K, Werner N, Berweiler J, et al. Estrogen increases bone marrow-derived endothelial progenitor cell production and diminishes neointima formation. Circulation. 2003;107:3059-3065.
28. Sullivan TR, Karas RH, Aronovitz M, et al. Estrogen inhibits the response-to-injury in a mouse carotid artery model. J Clin Invest. 1995;95:2482-2488.
29. Spyridopoulos I, Sullivan AB, Kearney M, et al. Estrogen-receptor-mediated inhibition of human endothelial cell apoptosis: estradiol as a survival factor. Circulation. 1997;95:1505-1514.
30. Asahara T, Masuda H, Takahashi T, et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res. 1999;85:221-228.
31. Kureishi Y, Luo Z, Shiojima I. The HMG-CoA reductase inhibitor simvastatin activates the protein kinase Akt and promotes angiogenesis in normocholesterotemic animals. Nat Med. 2000;6:1004-1010.
32. Dimmeler S, Aicher A, Vasa M, et al. HMG-CoA-reductase inhibitors (statins) increase endothelial progenitor cells via the PI3 kinase/Akt pathway. J Clin Invest. 2001;108:391-397.
33. Simoncini T, Hafezi-Moghadam A, Brazil DP, et al. Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature. 2000;407:538-541.
34. Hishikawa K, Nakaki T, Marumo T, et al. Up-regulation of nitric oxide synthase by estradiol in human aortic endothelial cells. FEBS Lett. 1995;360:291-293.
35. MacRitchie AN, Jun SS, Chen Z, et al. Estrogen upregulates endothelial nitric oxide synthase gene expression in fetal pulmonary artery endothelium. Circ Res. 1997;81:355-362.