Skip to main content
Top
Published in: Journal of Cardiovascular Translational Research 2/2016

01-04-2016 | Review

Endothelial Repair and Regeneration Following Intimal Injury

Author: Belay Tesfamariam

Published in: Journal of Cardiovascular Translational Research | Issue 2/2016

Login to get access

Abstract

Coronary artery intervention using device implants significantly reduce the risk of restenosis and the need for revascularization but are associated with endothelial denudation and impaired function. This may be due to incomplete endothelial recovery as a result of intimal injury, presence of polymer and/or high antiproliferative drug accumulation in the intima. The permanent presence of a metal prosthesis or polymer may impair the proliferation of resident endothelial cells to cover empty areas. Attention has focused on the robust replenishment of endothelial monolayer by recruitment of circulating endothelial progenitor cells derived from the bone marrow to areas of endothelial injury. The balance between endothelial damage and repair is critical for the maintenance of intimal integrity, function, and prevention of thrombotic complications. This review will discuss on the aftereffects of intravascular device implants on endothelial injury and the pathways involved in endothelial repair and regeneration with an emphasis on endothelial progenitor cells.
Literature
1.
go back to reference Massberg, S., Schulz, C., & Gawaz, M. (2003). Role of platelets in the pathophysiology of acute coronary syndrome. Seminars in Vascular Medicine, 3(2), 147–162.CrossRefPubMed Massberg, S., Schulz, C., & Gawaz, M. (2003). Role of platelets in the pathophysiology of acute coronary syndrome. Seminars in Vascular Medicine, 3(2), 147–162.CrossRefPubMed
2.
go back to reference Jackson, S. P., Nesbitt, W. S., & Kulkarni, S. (2003). Signaling events underlying thrombus formation. Journal of Thrombosis and Haemostasis, 1(7), 1602–1612.CrossRefPubMed Jackson, S. P., Nesbitt, W. S., & Kulkarni, S. (2003). Signaling events underlying thrombus formation. Journal of Thrombosis and Haemostasis, 1(7), 1602–1612.CrossRefPubMed
3.
go back to reference Konstantinides, S., Schäfer, K., Thinnes, T., & Loskutoff, D. J. (2001). Plasminogen activator inhibitor-1 and its cofactor vitronectin stabilize arterial thrombi after vascular injury in mice. Circulation, 103(4), 576–583.CrossRefPubMed Konstantinides, S., Schäfer, K., Thinnes, T., & Loskutoff, D. J. (2001). Plasminogen activator inhibitor-1 and its cofactor vitronectin stabilize arterial thrombi after vascular injury in mice. Circulation, 103(4), 576–583.CrossRefPubMed
4.
go back to reference Koppara, T., Cheng, Q., Yahagi, K., Mori, H., Sanchez, O. D., Feygin, J., et al. (2015). Thrombogenicity and early vascular healing response in metallic biodegradable polymer-based and fully bioabsorbable drug-eluting stents. Circulation. Cardiovascular Interventions, 8(6), e002427.CrossRefPubMed Koppara, T., Cheng, Q., Yahagi, K., Mori, H., Sanchez, O. D., Feygin, J., et al. (2015). Thrombogenicity and early vascular healing response in metallic biodegradable polymer-based and fully bioabsorbable drug-eluting stents. Circulation. Cardiovascular Interventions, 8(6), e002427.CrossRefPubMed
5.
go back to reference Tesfamariam, B. (2008). Platelet function in intravascular device implant-induced intimal injury. Cardiovascular Revascularization Medicine, 9(2), 78–87.CrossRefPubMed Tesfamariam, B. (2008). Platelet function in intravascular device implant-induced intimal injury. Cardiovascular Revascularization Medicine, 9(2), 78–87.CrossRefPubMed
6.
go back to reference Otsuka, F., Finn, A. V., Yazdani, S. K., Nakano, M., Kolodgie, F. D., & Virmani, R. (2012). The importance of the endothelium in atherothrombosis and coronary stenting. Nature Reviews Cardiology, 9(8), 439–453.CrossRefPubMed Otsuka, F., Finn, A. V., Yazdani, S. K., Nakano, M., Kolodgie, F. D., & Virmani, R. (2012). The importance of the endothelium in atherothrombosis and coronary stenting. Nature Reviews Cardiology, 9(8), 439–453.CrossRefPubMed
7.
8.
go back to reference Muldowney, J. A., 3rd, Stringham, J. R., Levy, S. E., Gleaves, L. A., Eren, M., Piana, R. N., et al. (2007). Antiproliferative agents alter vascular plasminogen activator inhibitor-1 expression: a potential prothrombotic mechanism of drug-eluting stents. Arteriosclerosis, Thrombosis, and Vascular Biology, 27(2), 400–406.CrossRefPubMed Muldowney, J. A., 3rd, Stringham, J. R., Levy, S. E., Gleaves, L. A., Eren, M., Piana, R. N., et al. (2007). Antiproliferative agents alter vascular plasminogen activator inhibitor-1 expression: a potential prothrombotic mechanism of drug-eluting stents. Arteriosclerosis, Thrombosis, and Vascular Biology, 27(2), 400–406.CrossRefPubMed
9.
go back to reference Ara, J., Mirapeix, E., Arrizabalaga, P., Rodriguez, R., Ascaso, C., Abellana, R., et al. (2001). Circulating soluble adhesion molecules in ANCA-associated vasculitis. Nephrology, Dialysis, Transplantation, 16, 276–285.CrossRefPubMed Ara, J., Mirapeix, E., Arrizabalaga, P., Rodriguez, R., Ascaso, C., Abellana, R., et al. (2001). Circulating soluble adhesion molecules in ANCA-associated vasculitis. Nephrology, Dialysis, Transplantation, 16, 276–285.CrossRefPubMed
10.
go back to reference Cai, H. (2005). NAD(P)H oxidase-dependent self-propagation of hydrogen peroxide and vascular disease. Circulation Research, 96(8), 818–822.CrossRefPubMed Cai, H. (2005). NAD(P)H oxidase-dependent self-propagation of hydrogen peroxide and vascular disease. Circulation Research, 96(8), 818–822.CrossRefPubMed
11.
go back to reference Blum, A., Schneider, D. J., Sobel, B. E., & Dauerman, H. L. (2004). Endothelial dysfunction and inflammation after percutaneous coronary intervention. American Journal of Cardiology, 94(11), 1420–1423.CrossRefPubMed Blum, A., Schneider, D. J., Sobel, B. E., & Dauerman, H. L. (2004). Endothelial dysfunction and inflammation after percutaneous coronary intervention. American Journal of Cardiology, 94(11), 1420–1423.CrossRefPubMed
12.
go back to reference Hofma, S. H., van der Giessen, W. J., van Dalen, B. M., Lemos, P. A., McFadden, E. P., Sianos, G., et al. (2006). Indication of long-term endothelial dysfunction after sirolimus-eluting stent implantation. European Heart Journal, 27(2), 166–170.CrossRefPubMed Hofma, S. H., van der Giessen, W. J., van Dalen, B. M., Lemos, P. A., McFadden, E. P., Sianos, G., et al. (2006). Indication of long-term endothelial dysfunction after sirolimus-eluting stent implantation. European Heart Journal, 27(2), 166–170.CrossRefPubMed
13.
go back to reference Togni, M., Windecker, S., Cocchia, R., Wenaweser, P., Cook, S., Billinger, M., et al. (2005). Sirolimus-eluting stents associated with paradoxic coronary vasoconstriction. Journal of the American College of Cardiology, 46(2), 231–236.CrossRefPubMed Togni, M., Windecker, S., Cocchia, R., Wenaweser, P., Cook, S., Billinger, M., et al. (2005). Sirolimus-eluting stents associated with paradoxic coronary vasoconstriction. Journal of the American College of Cardiology, 46(2), 231–236.CrossRefPubMed
14.
go back to reference Pendyala, L. K., Li, J., Shinke, T., Geva, S., Yin, X., Chen, J. P., et al. (2009). Endothelium-dependent vasomotor dysfunction in pig coronary arteries with paclitaxel-eluting stents is associated with inflammation and oxidative stress. JACC Cardiovascular Interventions, 2(3), 253–262.CrossRefPubMed Pendyala, L. K., Li, J., Shinke, T., Geva, S., Yin, X., Chen, J. P., et al. (2009). Endothelium-dependent vasomotor dysfunction in pig coronary arteries with paclitaxel-eluting stents is associated with inflammation and oxidative stress. JACC Cardiovascular Interventions, 2(3), 253–262.CrossRefPubMed
15.
go back to reference Tesfamariam, B. (2008). Drug release kinetics from stent device-based delivery systems. Journal of Cardiovascular Pharmacology, 51(2), 118–125.CrossRefPubMed Tesfamariam, B. (2008). Drug release kinetics from stent device-based delivery systems. Journal of Cardiovascular Pharmacology, 51(2), 118–125.CrossRefPubMed
16.
go back to reference Stähli, B. E., Camici, G. G., Steffel, J., Akhmedov, A., Shojaati, K., Graber, M., et al. (2006). Paclitaxel enhances thrombin-induced endothelial tissue factor expression via c-Jun terminal NH2 kinase activation. Circulation Research, 99(2), 149–155.CrossRefPubMed Stähli, B. E., Camici, G. G., Steffel, J., Akhmedov, A., Shojaati, K., Graber, M., et al. (2006). Paclitaxel enhances thrombin-induced endothelial tissue factor expression via c-Jun terminal NH2 kinase activation. Circulation Research, 99(2), 149–155.CrossRefPubMed
17.
go back to reference Holy, E. W., Jakob, P., Eickner, T., Camici, G. G., Beer, J. H., Akhmedov, A., et al. (2014). PI3K/p110α inhibition selectively interferes with arterial thrombosis and neointima formation, but not re-endothelialization: potential implications for drug-eluting stent design. European Heart Journal, 35(12), 808–820.CrossRefPubMed Holy, E. W., Jakob, P., Eickner, T., Camici, G. G., Beer, J. H., Akhmedov, A., et al. (2014). PI3K/p110α inhibition selectively interferes with arterial thrombosis and neointima formation, but not re-endothelialization: potential implications for drug-eluting stent design. European Heart Journal, 35(12), 808–820.CrossRefPubMed
18.
go back to reference Ma, Q., Zhou, Y., Nie, X., Yu, M., Gao, F., Wang, Z., et al. (2012). Rapamycin affects tissue plasminogen activator and plasminogen activator inhibitor I expression: a potential prothrombotic mechanism of drug-eluting stents. Angiology, 63(5), 330–335.CrossRefPubMed Ma, Q., Zhou, Y., Nie, X., Yu, M., Gao, F., Wang, Z., et al. (2012). Rapamycin affects tissue plasminogen activator and plasminogen activator inhibitor I expression: a potential prothrombotic mechanism of drug-eluting stents. Angiology, 63(5), 330–335.CrossRefPubMed
19.
go back to reference Togni, M., Räber, L., Cocchia, R., Wenaweser, P., Cook, S., Windecker, S., et al. (2007). Local vascular dysfunction after coronary paclitaxel-eluting stent implantation. International Journal of Cardiology, 120(2), 212–220.CrossRefPubMed Togni, M., Räber, L., Cocchia, R., Wenaweser, P., Cook, S., Windecker, S., et al. (2007). Local vascular dysfunction after coronary paclitaxel-eluting stent implantation. International Journal of Cardiology, 120(2), 212–220.CrossRefPubMed
20.
go back to reference Jabs, A., Göbel, S., Wenzel, P., Kleschyov, A. L., Hortmann, M., Oelze, M., et al. (2008). Sirolimus-induced vascular dysfunction: increased mitochondrial and nicotinamide adenosine dinucleotide phosphate oxidase-dependent superoxide production and decreased vascular nitric oxide formation. Journal of the American College of Cardiology, 51(22), 2130–2138.CrossRefPubMed Jabs, A., Göbel, S., Wenzel, P., Kleschyov, A. L., Hortmann, M., Oelze, M., et al. (2008). Sirolimus-induced vascular dysfunction: increased mitochondrial and nicotinamide adenosine dinucleotide phosphate oxidase-dependent superoxide production and decreased vascular nitric oxide formation. Journal of the American College of Cardiology, 51(22), 2130–2138.CrossRefPubMed
21.
go back to reference Camici, G. G., Steffel, J., Amanovic, I., Breitenstein, A., Baldinger, J., Keller, S., et al. (2010). Rapamycin promotes arterial thrombosis in vivo: implications for everolimus and zotarolimus eluting stents. European Heart Journal, 31(2), 236–242.CrossRefPubMed Camici, G. G., Steffel, J., Amanovic, I., Breitenstein, A., Baldinger, J., Keller, S., et al. (2010). Rapamycin promotes arterial thrombosis in vivo: implications for everolimus and zotarolimus eluting stents. European Heart Journal, 31(2), 236–242.CrossRefPubMed
22.
go back to reference Liu, H. T., Li, F., Wang, W. Y., Li, X. J., Liu, Y. M., Wang, R. A., et al. (2010). Rapamycin inhibits re-endothelialization after percutaneous coronary intervention by impeding the proliferation and migration of endothelial cells and inducing apoptosis of endothelial progenitor cells. Texas Heart Institute Journal, 37(2), 194–201.PubMedPubMedCentral Liu, H. T., Li, F., Wang, W. Y., Li, X. J., Liu, Y. M., Wang, R. A., et al. (2010). Rapamycin inhibits re-endothelialization after percutaneous coronary intervention by impeding the proliferation and migration of endothelial cells and inducing apoptosis of endothelial progenitor cells. Texas Heart Institute Journal, 37(2), 194–201.PubMedPubMedCentral
23.
go back to reference Potnis, P. A., Tesfamariam, B., & Wood, S. C. (2011). Induction of nicotinamide-adenine dinucleotide phosphate oxidase and apoptosis by biodegradable polymers in macrophages: implications for stents. Journal of Cardiovascular Pharmacology, 57(6), 712–720.CrossRefPubMed Potnis, P. A., Tesfamariam, B., & Wood, S. C. (2011). Induction of nicotinamide-adenine dinucleotide phosphate oxidase and apoptosis by biodegradable polymers in macrophages: implications for stents. Journal of Cardiovascular Pharmacology, 57(6), 712–720.CrossRefPubMed
24.
go back to reference Nakano, M., Yahagi, K., Otsuka, F., Sakakura, K., Finn, A. V., Kutys, R., et al. (2014). Causes of early stent thrombosis in patients presenting with acute coronary syndrome: an ex vivo human autopsy study. Journal of the American College of Cardiology, 63, 2510–2520.CrossRefPubMed Nakano, M., Yahagi, K., Otsuka, F., Sakakura, K., Finn, A. V., Kutys, R., et al. (2014). Causes of early stent thrombosis in patients presenting with acute coronary syndrome: an ex vivo human autopsy study. Journal of the American College of Cardiology, 63, 2510–2520.CrossRefPubMed
25.
go back to reference Wang, X., Zachman, A. L., Chun, Y. W., Shen, F. W., Hwang, Y. S., & Sung, H. J. (2014). Polymeric stent materials dysregulate macrophage and endothelial cell functions: implications for coronary artery stent. International Journal of Cardiology, 174(3), 688–695.CrossRefPubMedPubMedCentral Wang, X., Zachman, A. L., Chun, Y. W., Shen, F. W., Hwang, Y. S., & Sung, H. J. (2014). Polymeric stent materials dysregulate macrophage and endothelial cell functions: implications for coronary artery stent. International Journal of Cardiology, 174(3), 688–695.CrossRefPubMedPubMedCentral
26.
go back to reference Nührenberg, T. G., Voisard, R., Fahlisch, F., Rudelius, M., Braun, J., Gschwend, J., et al. (2005). Rapamycin attenuates vascular wall inflammation and progenitor cell promoters after angioplasty. FASEB Journal, 19(2), 246–248.PubMed Nührenberg, T. G., Voisard, R., Fahlisch, F., Rudelius, M., Braun, J., Gschwend, J., et al. (2005). Rapamycin attenuates vascular wall inflammation and progenitor cell promoters after angioplasty. FASEB Journal, 19(2), 246–248.PubMed
27.
go back to reference van Beusekom, H. M., Sorop, O., van den Heuvel, M., Onuma, Y., Duncker, D. J., Danser, A. H., et al. (2010). Endothelial function rather than endothelial restoration is altered in paclitaxel- as compared to bare metal-, sirolimus and tacrolimus-eluting stents. EuroIntervention, 6(1), 117–125.CrossRefPubMed van Beusekom, H. M., Sorop, O., van den Heuvel, M., Onuma, Y., Duncker, D. J., Danser, A. H., et al. (2010). Endothelial function rather than endothelial restoration is altered in paclitaxel- as compared to bare metal-, sirolimus and tacrolimus-eluting stents. EuroIntervention, 6(1), 117–125.CrossRefPubMed
28.
go back to reference Nakazawa, G., Nakano, M., Otsuka, F., Wilcox, J. N., Melder, R., Pruitt, S., et al. (2011). Evaluation of polymer-based comparator drug-eluting stents using a rabbit model of iliac artery atherosclerosis. Circulation. Cardiovascular Interventions, 4(1), 38–46.CrossRefPubMed Nakazawa, G., Nakano, M., Otsuka, F., Wilcox, J. N., Melder, R., Pruitt, S., et al. (2011). Evaluation of polymer-based comparator drug-eluting stents using a rabbit model of iliac artery atherosclerosis. Circulation. Cardiovascular Interventions, 4(1), 38–46.CrossRefPubMed
29.
go back to reference Otsuka, F., Byrne, R. A., Yahagi, K., Mori, H., Ladich, E., Fowler, D. R., et al. (2015). Neoatherosclerosis: overview of histopathologic findings and implications for intravascular imaging assessment. European Heart Journal, 36(32), 2147–2159.CrossRefPubMed Otsuka, F., Byrne, R. A., Yahagi, K., Mori, H., Ladich, E., Fowler, D. R., et al. (2015). Neoatherosclerosis: overview of histopathologic findings and implications for intravascular imaging assessment. European Heart Journal, 36(32), 2147–2159.CrossRefPubMed
30.
go back to reference Joner, M., Nakazawa, G., Finn, A. V., Quee, S. C., Coleman, L., Acampado, E., et al. (2008). Endothelial cell recovery between comparator polymer-based drug-eluting stents. Journal of the American College of Cardiology, 52(5), 333–342.CrossRefPubMed Joner, M., Nakazawa, G., Finn, A. V., Quee, S. C., Coleman, L., Acampado, E., et al. (2008). Endothelial cell recovery between comparator polymer-based drug-eluting stents. Journal of the American College of Cardiology, 52(5), 333–342.CrossRefPubMed
32.
go back to reference Torisu, T., Torisu, K., Lee, I. H., Liu, J., Malide, D., Combs, C. A., et al. (2013). Autophagy regulates endothelial cell processing, maturation and secretion of von Willebrand factor. Nature Medicine, 19(10), 1281–1287.CrossRefPubMedPubMedCentral Torisu, T., Torisu, K., Lee, I. H., Liu, J., Malide, D., Combs, C. A., et al. (2013). Autophagy regulates endothelial cell processing, maturation and secretion of von Willebrand factor. Nature Medicine, 19(10), 1281–1287.CrossRefPubMedPubMedCentral
34.
go back to reference Hayashi, S., Yamamoto, A., You, F., Yamashita, K., Ikegame, Y., Tawada, M., et al. (2009). The stent-eluting drugs sirolimus and paclitaxel suppress healing of the endothelium by induction of autophagy. American Journal of Pathology, 175(5), 2226–2234.CrossRefPubMedPubMedCentral Hayashi, S., Yamamoto, A., You, F., Yamashita, K., Ikegame, Y., Tawada, M., et al. (2009). The stent-eluting drugs sirolimus and paclitaxel suppress healing of the endothelium by induction of autophagy. American Journal of Pathology, 175(5), 2226–2234.CrossRefPubMedPubMedCentral
35.
go back to reference Barilli, A., Visigalli, R., Sala, R., Gazzola, G. C., Parolari, A., Tremoli, E., et al. (2008). In human endothelial cells rapamycin causes mTORC2 inhibition and impairs cell viability and function. Cardiovascular Research, 78, 563–571.CrossRefPubMed Barilli, A., Visigalli, R., Sala, R., Gazzola, G. C., Parolari, A., Tremoli, E., et al. (2008). In human endothelial cells rapamycin causes mTORC2 inhibition and impairs cell viability and function. Cardiovascular Research, 78, 563–571.CrossRefPubMed
36.
go back to reference Guo, F., Li, X., Peng, J., Tang, Y., Yang, Q., Liu, L., et al. (2014). Autophagy regulates vascular endothelial cell eNOS and ET-1 expression induced by laminar shear stress in an ex vivo perfused system. Annals of Biomedical Engineering, 42(9), 1978–1988.CrossRefPubMed Guo, F., Li, X., Peng, J., Tang, Y., Yang, Q., Liu, L., et al. (2014). Autophagy regulates vascular endothelial cell eNOS and ET-1 expression induced by laminar shear stress in an ex vivo perfused system. Annals of Biomedical Engineering, 42(9), 1978–1988.CrossRefPubMed
37.
go back to reference Perry, T. E., Song, M., Despres, D. J., Kim, S. M., San, H., Yu, Z. X., et al. (2009). Bone marrow-derived cells do not repair endothelium in a mouse model of chronic endothelial cell dysfunction. Cardiovascular Research, 84, 317–325.CrossRefPubMedPubMedCentral Perry, T. E., Song, M., Despres, D. J., Kim, S. M., San, H., Yu, Z. X., et al. (2009). Bone marrow-derived cells do not repair endothelium in a mouse model of chronic endothelial cell dysfunction. Cardiovascular Research, 84, 317–325.CrossRefPubMedPubMedCentral
38.
go back to reference Blann, A. D., Woywodt, A., Bertolini, F., Bull, T. M., Buyon, J. P., Clancy, R. M., et al. (2005). Circulating endothelial cells. Biomarker of vascular disease. Thrombosis and Haemostasis, 93(2), 228–235.PubMed Blann, A. D., Woywodt, A., Bertolini, F., Bull, T. M., Buyon, J. P., Clancy, R. M., et al. (2005). Circulating endothelial cells. Biomarker of vascular disease. Thrombosis and Haemostasis, 93(2), 228–235.PubMed
39.
go back to reference Quilici, J., Banzet, N., Paule, P., Meynard, J. B., Mutin, M., Bonnet, J. L., et al. (2004). Circulating endothelial cell count as a diagnostic marker for non-ST-elevation acute coronary syndromes. Circulation, 110(12), 1586–1591.CrossRefPubMed Quilici, J., Banzet, N., Paule, P., Meynard, J. B., Mutin, M., Bonnet, J. L., et al. (2004). Circulating endothelial cell count as a diagnostic marker for non-ST-elevation acute coronary syndromes. Circulation, 110(12), 1586–1591.CrossRefPubMed
40.
41.
go back to reference Szmitko, P. E., Fedak, P. W., Weisel, R. D., Stewart, D. J., Kutryk, M. J., & Verma, S. (2003). Endothelial progenitor cells: New hope for a broken heart. Circulation, 107(24), 3093–3100.CrossRefPubMed Szmitko, P. E., Fedak, P. W., Weisel, R. D., Stewart, D. J., Kutryk, M. J., & Verma, S. (2003). Endothelial progenitor cells: New hope for a broken heart. Circulation, 107(24), 3093–3100.CrossRefPubMed
42.
go back to reference Bonello, L., Harhouri, K., Baumstarck, K., Arnaud, L., Lesavre, N., Piot, C., et al. (2012). Mobilization of CD34+ KDR+ endothelial progenitor cells predicts target lesion revascularization. Journal of Thrombosis and Haemostasis, 10(9), 1906–1913.CrossRefPubMed Bonello, L., Harhouri, K., Baumstarck, K., Arnaud, L., Lesavre, N., Piot, C., et al. (2012). Mobilization of CD34+ KDR+ endothelial progenitor cells predicts target lesion revascularization. Journal of Thrombosis and Haemostasis, 10(9), 1906–1913.CrossRefPubMed
43.
go back to reference Shantsila, E., Watson, T., & Lip, G. Y. (2007). Endothelial progenitor cells in cardiovascular disorders. Journal of the American College of Cardiology, 49(7), 741–752.CrossRefPubMed Shantsila, E., Watson, T., & Lip, G. Y. (2007). Endothelial progenitor cells in cardiovascular disorders. Journal of the American College of Cardiology, 49(7), 741–752.CrossRefPubMed
44.
go back to reference Ben Shoshan, J., & George, J. (2007). Endothelial progenitor cells as therapeutic vectors in cardiovascular disorders: from experimental models to human trials. Pharmacology and Therapeutics, 115(1), 25–36.CrossRefPubMed Ben Shoshan, J., & George, J. (2007). Endothelial progenitor cells as therapeutic vectors in cardiovascular disorders: from experimental models to human trials. Pharmacology and Therapeutics, 115(1), 25–36.CrossRefPubMed
45.
go back to reference Rafii, S., & Lyden, D. (2003). Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nature Medicine, 9(6), 702–712.CrossRefPubMed Rafii, S., & Lyden, D. (2003). Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nature Medicine, 9(6), 702–712.CrossRefPubMed
46.
go back to reference Werner, N., Kosiol, S., Schiegl, T., Ahlers, P., Walenta, K., Link, A., et al. (2005). Circulating endothelial progenitor cells and cardiovascular outcomes. New England Journal of Medicine, 353(10), 999–1007.CrossRefPubMed Werner, N., Kosiol, S., Schiegl, T., Ahlers, P., Walenta, K., Link, A., et al. (2005). Circulating endothelial progenitor cells and cardiovascular outcomes. New England Journal of Medicine, 353(10), 999–1007.CrossRefPubMed
47.
go back to reference Hill, J. M., Zalos, G., Halcox, J. P., Schenke, W. H., Waclawiw, M. A., Quyyumi, A. A., et al. (2003). Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. New England Journal of Medicine, 348(7), 593–600.CrossRefPubMed Hill, J. M., Zalos, G., Halcox, J. P., Schenke, W. H., Waclawiw, M. A., Quyyumi, A. A., et al. (2003). Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. New England Journal of Medicine, 348(7), 593–600.CrossRefPubMed
48.
go back to reference Urbich, C., & Dimmeler, S. (2004). Endothelial progenitor cells: characterization and role in vascular biology. Circulation Research, 95(4), 343–353.CrossRefPubMed Urbich, C., & Dimmeler, S. (2004). Endothelial progenitor cells: characterization and role in vascular biology. Circulation Research, 95(4), 343–353.CrossRefPubMed
49.
go back to reference Sata, M., Saiura, A., Kunisato, A., Tojo, A., Okada, S., Tokuhisa, T., et al. (2002). Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nature Medicine, 8(4), 403–409.CrossRefPubMed Sata, M., Saiura, A., Kunisato, A., Tojo, A., Okada, S., Tokuhisa, T., et al. (2002). Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nature Medicine, 8(4), 403–409.CrossRefPubMed
50.
go back to reference Larsen, K., Cheng, C., Tempel, D., Parker, S., Yazdani, S., den Dekker, W. K., et al. (2012). Capture of circulatory endothelial progenitor cells and accelerated re-endothelialization of a bio-engineered stent in human ex vivo shunt and rabbit denudation model. European Heart Journal, 33(1), 120–128.CrossRefPubMedPubMedCentral Larsen, K., Cheng, C., Tempel, D., Parker, S., Yazdani, S., den Dekker, W. K., et al. (2012). Capture of circulatory endothelial progenitor cells and accelerated re-endothelialization of a bio-engineered stent in human ex vivo shunt and rabbit denudation model. European Heart Journal, 33(1), 120–128.CrossRefPubMedPubMedCentral
51.
go back to reference Takabatake, S., Hayashi, K., Nakanishi, C., Hao, H., Sakata, K., Kawashiri, M. A., et al. (2014). Vascular endothelial growth factor bound stents: application of in situ capture technology of circulating endothelial progenitor cells in porcine coronary model. Journal of Interventional Cardiology, 27(1), 63–72.CrossRefPubMed Takabatake, S., Hayashi, K., Nakanishi, C., Hao, H., Sakata, K., Kawashiri, M. A., et al. (2014). Vascular endothelial growth factor bound stents: application of in situ capture technology of circulating endothelial progenitor cells in porcine coronary model. Journal of Interventional Cardiology, 27(1), 63–72.CrossRefPubMed
52.
go back to reference Pernagallo, S., Tura, O., Wu, M., Samuel, K., Diaz-Mochon, J. J., Hansen, A., et al. (2012). Novel biopolymers to enhance endothelialization of intra-vascular devices. Adv Healthc Mater, 1(5), 646–656.CrossRefPubMed Pernagallo, S., Tura, O., Wu, M., Samuel, K., Diaz-Mochon, J. J., Hansen, A., et al. (2012). Novel biopolymers to enhance endothelialization of intra-vascular devices. Adv Healthc Mater, 1(5), 646–656.CrossRefPubMed
53.
go back to reference Blindt, R., Vogt, F., Astafieva, I., Fach, C., Hristov, M., Krott, N., et al. (2006). A novel drug-eluting stent coated with an integrin-binding cyclic Arg-Gly-Asp peptide inhibits neointimal hyperplasia by recruiting endothelial progenitor cells. Journal of the American College of Cardiology, 47(9), 1786–1795.CrossRefPubMed Blindt, R., Vogt, F., Astafieva, I., Fach, C., Hristov, M., Krott, N., et al. (2006). A novel drug-eluting stent coated with an integrin-binding cyclic Arg-Gly-Asp peptide inhibits neointimal hyperplasia by recruiting endothelial progenitor cells. Journal of the American College of Cardiology, 47(9), 1786–1795.CrossRefPubMed
54.
go back to reference Heissig, B., Hattori, K., Dias, S., Friedrich, M., Ferris, B., Hackett, N. R., et al. (2002). Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell, 109(5), 625–637.CrossRefPubMedPubMedCentral Heissig, B., Hattori, K., Dias, S., Friedrich, M., Ferris, B., Hackett, N. R., et al. (2002). Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell, 109(5), 625–637.CrossRefPubMedPubMedCentral
55.
go back to reference Paradisi, G., Bracaglia, M., Basile, F., Di'Ipolito, S., Di Nicuolo, F., Ianniello, F., et al. (2012). Effect of pravastatin on endothelial function and endothelial progenitor cells in healthy postmenopausal women. Clinical and Experimental Obstetrics and Gynecology, 39(2), 153–159.PubMed Paradisi, G., Bracaglia, M., Basile, F., Di'Ipolito, S., Di Nicuolo, F., Ianniello, F., et al. (2012). Effect of pravastatin on endothelial function and endothelial progenitor cells in healthy postmenopausal women. Clinical and Experimental Obstetrics and Gynecology, 39(2), 153–159.PubMed
56.
go back to reference Baran, Ç., Durdu, S., Dalva, K., Zaim, Ç., Dogan, A., Ocakoglu, G., et al. (2012). Effects of preoperative short term use of atorvastatin on endothelial progenitor cells after coronary surgery: a randomized, controlled trial. Stem Cell Reviews, 8(3), 963–971.CrossRefPubMed Baran, Ç., Durdu, S., Dalva, K., Zaim, Ç., Dogan, A., Ocakoglu, G., et al. (2012). Effects of preoperative short term use of atorvastatin on endothelial progenitor cells after coronary surgery: a randomized, controlled trial. Stem Cell Reviews, 8(3), 963–971.CrossRefPubMed
57.
go back to reference Walter, D. H., Zeiher, A. M., & Dimmeler, S. (2004). Effects of statins on endothelium and their contribution to neovascularization by mobilization of endothelial progenitor cells. Coronary Artery Disease, 15(5), 235–242.CrossRefPubMed Walter, D. H., Zeiher, A. M., & Dimmeler, S. (2004). Effects of statins on endothelium and their contribution to neovascularization by mobilization of endothelial progenitor cells. Coronary Artery Disease, 15(5), 235–242.CrossRefPubMed
58.
go back to reference Sugiura, T., Kondo, T., Kureishi-Bando, Y., Numaguchi, Y., Yoshida, O., Dohi, Y., et al. (2008). Nifedipine improves endothelial function: role of endothelial progenitor cells. Hypertension, 52(3), 491–498.CrossRefPubMed Sugiura, T., Kondo, T., Kureishi-Bando, Y., Numaguchi, Y., Yoshida, O., Dohi, Y., et al. (2008). Nifedipine improves endothelial function: role of endothelial progenitor cells. Hypertension, 52(3), 491–498.CrossRefPubMed
59.
go back to reference de Ciuceis, C., Pilu, A., Rizzoni, D., Porteri, E., Muiesan, M. L., Salvetti, M., et al. (2011). Effect of antihypertensive treatment on circulating endothelial progenitor cells in patients with mild essential hypertension. Blood Pressure, 20(2), 77–83.CrossRefPubMed de Ciuceis, C., Pilu, A., Rizzoni, D., Porteri, E., Muiesan, M. L., Salvetti, M., et al. (2011). Effect of antihypertensive treatment on circulating endothelial progenitor cells in patients with mild essential hypertension. Blood Pressure, 20(2), 77–83.CrossRefPubMed
60.
go back to reference Yao, E. H., Fukuda, N., Matsumoto, T., Katakawa, M., Yamamoto, C., Han, Y., et al. (2008). Effects of the antioxidative blocker celiprolol on endothelial progenitor cells in hypertensive rats. American Journal of Hypertension, 21(9), 1062–1068.CrossRefPubMed Yao, E. H., Fukuda, N., Matsumoto, T., Katakawa, M., Yamamoto, C., Han, Y., et al. (2008). Effects of the antioxidative blocker celiprolol on endothelial progenitor cells in hypertensive rats. American Journal of Hypertension, 21(9), 1062–1068.CrossRefPubMed
61.
go back to reference Santulli, G., Wronska, A., Uryu, K., Diacovo, T. G., Gao, M., Marx, S. O., et al. (2014). A selective microRNA-based strategy inhibits restenosis while preserving endothelial function. Journal of Clinical Investigation, 124(9), 4102–4114.CrossRefPubMedPubMedCentral Santulli, G., Wronska, A., Uryu, K., Diacovo, T. G., Gao, M., Marx, S. O., et al. (2014). A selective microRNA-based strategy inhibits restenosis while preserving endothelial function. Journal of Clinical Investigation, 124(9), 4102–4114.CrossRefPubMedPubMedCentral
62.
go back to reference Szmitko, P. E., Wang, C. H., Weisel, R. D., de Almeida, J. R., Anderson, T. J., & Verma, S. (2003). New markers of inflammation and endothelial cell activation: part I. Circulation, 108(16), 1917–1923.CrossRefPubMed Szmitko, P. E., Wang, C. H., Weisel, R. D., de Almeida, J. R., Anderson, T. J., & Verma, S. (2003). New markers of inflammation and endothelial cell activation: part I. Circulation, 108(16), 1917–1923.CrossRefPubMed
63.
go back to reference Kozuka, K., Kohriyama, T., Nomura, E., Ikeda, J., Kajikawa, H., & Nakamura, S. (2002). Endothelial markers and adhesion molecules in acute ischemic stroke-sequential change and differences in stroke subtype. Atherosclerosis, 161, 161–168.CrossRefPubMed Kozuka, K., Kohriyama, T., Nomura, E., Ikeda, J., Kajikawa, H., & Nakamura, S. (2002). Endothelial markers and adhesion molecules in acute ischemic stroke-sequential change and differences in stroke subtype. Atherosclerosis, 161, 161–168.CrossRefPubMed
64.
go back to reference Sabatier, F., Camoin-Jau, L., Anfosso, F., Sampol, J., & Dignat-George, F. (2009). Circulating endothelial cells, microparticles and progenitors: key players towards the definition of vascular competence. Journal of Cellular and Molecular Medicine, 13(3), 454–471.CrossRefPubMedPubMedCentral Sabatier, F., Camoin-Jau, L., Anfosso, F., Sampol, J., & Dignat-George, F. (2009). Circulating endothelial cells, microparticles and progenitors: key players towards the definition of vascular competence. Journal of Cellular and Molecular Medicine, 13(3), 454–471.CrossRefPubMedPubMedCentral
65.
go back to reference Kümpers, P., Hellpap, J., David, S., Horn, R., Leitolf, H., Haller, H., et al. (2009). Circulating angiopoietin-2 is a marker and potential mediator of endothelial cell detachment in ANCA-associated vasculitis with renal involvement. Nephrology, Dialysis, Transplantation, 24(6), 1845–1850.CrossRefPubMed Kümpers, P., Hellpap, J., David, S., Horn, R., Leitolf, H., Haller, H., et al. (2009). Circulating angiopoietin-2 is a marker and potential mediator of endothelial cell detachment in ANCA-associated vasculitis with renal involvement. Nephrology, Dialysis, Transplantation, 24(6), 1845–1850.CrossRefPubMed
66.
go back to reference Vowinkel, T., Wood, K. C., Stokes, K. Y., Russell, J., Krieglstein, C. F., & Granger, D. N. (2006). Differential expression and regulation of murine CD40 in regional vascular beds. American Journal of Physiology Heart and Circulatory Physiology, 290(2), H631–639.CrossRefPubMed Vowinkel, T., Wood, K. C., Stokes, K. Y., Russell, J., Krieglstein, C. F., & Granger, D. N. (2006). Differential expression and regulation of murine CD40 in regional vascular beds. American Journal of Physiology Heart and Circulatory Physiology, 290(2), H631–639.CrossRefPubMed
67.
go back to reference Burger, D., & Touyz, R. M. (2012). Cellular biomarkers of endothelial health: microparticles, endothelial progenitor cells, and circulating endothelial cells. Journal of the American Society of Hypertension, 6(2), 85–99.CrossRefPubMed Burger, D., & Touyz, R. M. (2012). Cellular biomarkers of endothelial health: microparticles, endothelial progenitor cells, and circulating endothelial cells. Journal of the American Society of Hypertension, 6(2), 85–99.CrossRefPubMed
Metadata
Title
Endothelial Repair and Regeneration Following Intimal Injury
Author
Belay Tesfamariam
Publication date
01-04-2016
Publisher
Springer US
Published in
Journal of Cardiovascular Translational Research / Issue 2/2016
Print ISSN: 1937-5387
Electronic ISSN: 1937-5395
DOI
https://doi.org/10.1007/s12265-016-9677-1

Other articles of this Issue 2/2016

Journal of Cardiovascular Translational Research 2/2016 Go to the issue