Circulation Research. 2003;93:1023-1025
Published online before print November 6, 2003, doi: 10.1161/01.RES.0000105569.77539.21
Published online before print November 6, 2003, doi: 10.1161/01.RES.0000105569.77539.21
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
© 2003 American Heart Association, Inc.
Reports |
Diverse Origin and Function of Cells With Endothelial Phenotype Obtained From Adult Human Blood
From the Division of Cardiovascular Diseases and Internal Medicine (R.G., T.E.P., R.D.S.), Molecular Medicine Program (R.G., D.J., T.E.P., R.G.V., R.D.S.), Department of Pathology (D.J.), Department of Biochemistry and Molecular Biology (S.C., V.S., R.D.S), GI Research Unit and Tumor Biology Program (S.C., V.S.), Mayo Clinic College of Medicine, Rochester, Minn.
Correspondence to Robert D. Simari, MD, Mayo Clinic College of Medicine, 200 First St SW, Rochester, MN 55905. E-mail simari.robert{at}mayo.edu
Abstract
Cells with endothelial phenotype generated from adult peripheral blood have emerging diagnostic and therapeutic potential. This study examined the lineage relationship between, and angiogenic function of, early endothelial progenitor cells (EPCs) and late outgrowth endothelial cells (OECs) in culture. Culture conditions were established to support the generation of both EPCs and OECs from the same starting population of peripheral blood mononuclear cells (PBMCs). Utilizing differences in expression of the surface endotoxin receptor CD14, it was determined that the vast majority of EPCs arose from a CD14+ subpopulation of PBMCs but OECs developed exclusively from the CD14- fraction. Human OECs, but not EPCs, expressed key regulatory proteins endothelial nitric oxide synthase (eNOS) and caveolin-1. Moreover, OECs exhibited a markedly greater capacity for capillary morphogenesis in in vitro and in vivo matrigel models, tube formation by OECs being in part dependent on eNOS function. Collectively, these data indicate lineage and functional heterogeneity in the population of circulating cells capable of assuming an endothelial phenotype and provide rationale for the investigation of new cell-therapeutic approaches to ischemic cardiovascular disease.
Key Words: angiogenesis • endothelial progenitor cells • endothelial nitric oxide synthase
This article has been cited by other articles:
 |
|
 |
|
  H. Fujinaga, C. D. Baker, S. L. Ryan, N. E. Markham, G. J. Seedorf, V. Balasubramaniam, and S. H. Abman Hyperoxia disrupts vascular endothelial growth factor-nitric oxide signaling and decreases growth of endothelial colony-forming cells from preterm infants Am J Physiol Lung Cell Mol Physiol, December 1, 2009; 297(6): L1160 - L1169. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Zhang, B.-S. Herbert, G. Rajashekhar, D. A. Ingram, M. C. Yoder, M. Clauss, and J. Rehman Premature senescence of highly proliferative endothelial progenitor cells is induced by tumor necrosis factor-{alpha} via the p38 mitogen-activated protein kinase pathway FASEB J, May 1, 2009; 23(5): 1358 - 1365. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Froehlich, R. Gulati, B. Boilson, T. Witt, A. Harbuzariu, L. Kleppe, A. B. Dietz, A. Lerman, and R. D. Simari Carotid Repair Using Autologous Adipose-Derived Endothelial Cells Stroke, May 1, 2009; 40(5): 1886 - 1891. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Zhang, D. A. Ingram, M. P. Murphy, M. R. Saadatzadeh, L. E. Mead, D. N. Prater, and J. Rehman Release of proinflammatory mediators and expression of proinflammatory adhesion molecules by endothelial progenitor cells Am J Physiol Heart Circ Physiol, May 1, 2009; 296(5): H1675 - H1682. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. M. Leone, M. Valgimigli, M. B. Giannico, V. Zaccone, M. Perfetti, D. D'Amario, A. G. Rebuzzi, and F. Crea From bone marrow to the arterial wall: the ongoing tale of endothelial progenitor cells Eur. Heart J., April 2, 2009; 30(8): 890 - 899. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Gulati and R. D. Simari Defining the potential for cell therapy for vascular disease using animal models Dis. Model. Mech., March 1, 2009; 2(3-4): 130 - 137. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. R. Chade, X. Zhu, R. Lavi, J. D. Krier, S. Pislaru, R. D. Simari, C. Napoli, A. Lerman, and L. O. Lerman Endothelial Progenitor Cells Restore Renal Function in Chronic Experimental Renovascular Disease Circulation, February 3, 2009; 119(4): 547 - 557. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Yamahara and H. Itoh Potential use of endothelial progenitor cells for regeneration of the vasculature Therapeutic Advances in Cardiovascular Disease, February 1, 2009; 3(1): 17 - 27. [Abstract] [PDF]
|
|
|
|
 |
|
 J. Grisar, C. W. Steiner, M. Bonelli, T. Karonitsch, I. Schwarzinger, G. Weigel, G. Steiner, and J. S. Smolen Systemic lupus erythematosus patients exhibit functional deficiencies of endothelial progenitor cells Rheumatology, October 1, 2008; 47(10): 1476 - 1483. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. K. Hirschi, D. A. Ingram, and M. C. Yoder Assessing Identity, Phenotype, and Fate of Endothelial Progenitor Cells Arterioscler Thromb Vasc Biol, September 1, 2008; 28(9): 1584 - 1595. [Full Text] [PDF]
|
|
|
|
|
|
T. J. Povsic and P. J. Goldschmidt-Clermont Review: Endothelial progenitor cells: markers of vascular reparative capacity Therapeutic Advances in Cardiovascular Disease, June 1, 2008; 2(3): 199 - 213. [Abstract] [PDF]
|
|
|
|
 |
|
 M. Thill, N. V. Strunnikova, M. J. Berna, N. Gordiyenko, K. Schmid, S. W. Cousins, D. J. S. Thompson, and K. G. Csaky Late Outgrowth Endothelial Progenitor Cells in Patients with Age-Related Macular Degeneration Invest. Ophthalmol. Vis. Sci., June 1, 2008; 49(6): 2696 - 2708. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Zampetaki, J. P. Kirton, and Q. Xu Vascular repair by endothelial progenitor cells Cardiovasc Res, June 1, 2008; 78(3): 413 - 421. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Chu, K.-H. Jung, S.-T. Lee, H.-K. Park, D.-I. Sinn, J.-M. Kim, D.-H. Kim, J.-H. Kim, S.-J. Kim, E.-C. Song, et al. Circulating Endothelial Progenitor Cells as a New Marker of Endothelial Dysfunction or Repair in Acute Stroke * Supplemental Methods Stroke, May 1, 2008; 39(5): 1441 - 1447. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Chen, J. M. Abrahams, L. M. Smith, J. H. McVey, R. I. Lechler, and A. Dorling Regenerative repair after endoluminal injury in mice with specific antagonism of protease activated receptors on CD34+ vascular progenitors Blood, April 15, 2008; 111(8): 4155 - 4164. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Tang, J. Lu, J. P. Walterscheid, H.-H. Chen, D. A. Engler, T. Sawamura, P.-Y. Chang, H. J. Safi, C.-Y. Yang, and C.-H. Chen Electronegative LDL circulating in smokers impairs endothelial progenitor cell differentiation by inhibiting Akt phosphorylation via LOX-1 J. Lipid Res., January 1, 2008; 49(1): 33 - 47. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C.-H. Wang, W.-J. Cherng, N.-I Yang, L.-T. Kuo, C.-M. Hsu, H.-I Yeh, Y.-J. Lan, C.-H. Yeh, and W. L. Stanford Late-Outgrowth Endothelial Cells Attenuate Intimal Hyperplasia Contributed by Mesenchymal Stem Cells After Vascular Injury Arterioscler Thromb Vasc Biol, January 1, 2008; 28(1): 54 - 60. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Suarez, B. R. Shepherd, D. A. Rao, and J. S. Pober Alloimmunity to Human Endothelial Cells Derived from Cord Blood Progenitors J. Immunol., December 1, 2007; 179(11): 7488 - 7496. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. F. Denny, S. Thacker, H. Mehta, E. C. Somers, T. Dodick, F. J. Barrat, W. J. McCune, and M. J. Kaplan Interferon-{alpha} promotes abnormal vasculogenesis in lupus: a potential pathway for premature atherosclerosis Blood, October 15, 2007; 110(8): 2907 - 2915. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Hur, H.-M. Yang, C.-H. Yoon, C.-S. Lee, K.-W. Park, J.-H. Kim, T.-Y. Kim, J.-Y. Kim, H.-J. Kang, I.-H. Chae, et al. Identification of a Novel Role of T Cells in Postnatal Vasculogenesis: Characterization of Endothelial Progenitor Cell Colonies Circulation, October 9, 2007; 116(15): 1671 - 1682. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. K Y Goon and G. Y H Lip Endothelial progenitor cells, endothelial cell dysfunction and much more: observations from cardiac syndrome X Heart, September 1, 2007; 93(9): 1020 - 1021. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. M. Melero-Martin, Z. A. Khan, A. Picard, X. Wu, S. Paruchuri, and J. Bischoff In vivo vasculogenic potential of human blood-derived endothelial progenitor cells Blood, June 1, 2007; 109(11): 4761 - 4768. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Casamassimi, M. L. Balestrieri, C. Fiorito, C. Schiano, C. Maione, R. Rossiello, V. Grimaldi, V. Del Giudice, C. Balestrieri, B. Farzati, et al. Comparison Between Total Endothelial Progenitor Cell Isolation Versus Enriched Cd133+ Culture J. Biochem., April 1, 2007; 141(4): 503 - 511. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. Kang-Decker, S. Cao, S. Chatterjee, J. Yao, L. J. Egan, D. Semela, D. Mukhopadhyay, and V. Shah Nitric oxide promotes endothelial cell survival signaling through S-nitrosylation and activation of dynamin-2 J. Cell Sci., February 1, 2007; 120(3): 492 - 501. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. M. Shepherd, B. J. Capoccia, S. M. Devine, J. DiPersio, K. M. Trinkaus, D. Ingram, and D. C. Link Angiogenic cells can be rapidly mobilized and efficiently harvested from the blood following treatment with AMD3100 Blood, December 1, 2006; 108(12): 3662 - 3667. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. V. Pislaru, A. Harbuzariu, R. Gulati, T. Witt, N. P. Sandhu, R. D. Simari, and G. S. Sandhu Magnetically Targeted Endothelial Cell Localization in Stented Vessels J. Am. Coll. Cardiol., November 7, 2006; 48(9): 1839 - 1845. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. J. Boos, G. Y.H. Lip, and A. D. Blann Circulating Endothelial Cells in Cardiovascular Disease J. Am. Coll. Cardiol., October 17, 2006; 48(8): 1538 - 1547. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. V. Pislaru, A. Harbuzariu, G. Agarwal, T. Witt AAS CVT LATG, R. Gulati, N. P. Sandhu, C. Mueske AA, M. Kalra, R. D. Simari, and G. S. Sandhu Magnetic Forces Enable Rapid Endothelialization of Synthetic Vascular Grafts Circulation, July 4, 2006; 114(1_suppl): I-314 - I-318. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. X. Ma, B. Zhou, Z. Chen, Q. Ren, S. H. Lu, T. Sawamura, and Z. C. Han Oxidized low density lipoprotein impairs endothelial progenitor cells by regulation of endothelial nitric oxide synthase J. Lipid Res., June 1, 2006; 47(6): 1227 - 1237. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. E. Sharpe III, A. A. Teleron, B. Li, J. Price, M. S. Sands, K. Alford, and P. P. Young The Origin and in Vivo Significance of Murine and Human Culture-Expanded Endothelial Progenitor Cells Am. J. Pathol., May 1, 2006; 168(5): 1710 - 1721. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Yamada and N. Takakura Physiological pathway of differentiation of hematopoietic stem cell population into mural cells J. Exp. Med., April 17, 2006; 203(4): 1055 - 1065. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Glod, D. Kobiler, M. Noel, R. Koneru, S. Lehrer, D. Medina, D. Maric, and H. A. Fine Monocytes form a vascular barrier and participate in vessel repair after brain injury Blood, February 1, 2006; 107(3): 940 - 946. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Emmerich Current State and Perspective on Medical Treatment of Critical Leg Ischemia: Gene and Cell Therapy International Journal of Lower Extremity Wounds, December 1, 2005; 4(4): 234 - 241. [Abstract] [PDF]
|
|
|
|
|
|
R. Gulati and R. D. Simari Cell Therapy for Angiogenesis: Embracing Diversity Circulation, September 13, 2005; 112(11): 1522 - 1524. [Full Text] [PDF]
|
|
|
|
|
|
C.-H. Yoon, J. Hur, K.-W. Park, J.-H. Kim, C.-S. Lee, I.-Y. Oh, T.-Y. Kim, H.-J. Cho, H.-J. Kang, I.-H. Chae, et al. Synergistic Neovascularization by Mixed Transplantation of Early Endothelial Progenitor Cells and Late Outgrowth Endothelial Cells: The Role of Angiogenic Cytokines and Matrix Metalloproteinases Circulation, September 13, 2005; 112(11): 1618 - 1627. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. B. Rookmaaker, M. C. Verhaar, C. J.M. Loomans, R. Verloop, E. Peters, P. E. Westerweel, T. Murohara, F. J.T. Staal, A. J. van Zonneveld, P. Koolwijk, et al. CD34+ Cells Home, Proliferate, and Participate in Capillary Formation, and in Combination With CD34- Cells Enhance Tube Formation in a 3-Dimensional Matrix Arterioscler Thromb Vasc Biol, September 1, 2005; 25(9): 1843 - 1850. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. A. Ingram, N. M. Caplice, and M. C. Yoder Unresolved questions, changing definitions, and novel paradigms for defining endothelial progenitor cells Blood, September 1, 2005; 106(5): 1525 - 1531. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. P. Fadini, C. Agostini, A. Avogaro, U. Ghani, A. Shuaib, A. Salam, A. Nasir, U. Shuaib, T. Jeerakathil, F. Sher, et al. Endothelial Progenitor Cells in Cerebrovascular Disease * Response: Stroke, June 1, 2005; 36(6): 1112 - 1113. [Full Text] [PDF]
|
|
|
|
|
|
E. O. Weinberg, M. Scherrer-Crosbie, M. H. Picard, B. A. Nasseri, C. MacGillivray, J. Gannon, Q. Lian, K. D. Bloch, and R. T. Lee Rosuvastatin reduces experimental left ventricular infarct size after ischemia-reperfusion injury but not total coronary occlusion Am J Physiol Heart Circ Physiol, April 1, 2005; 288(4): H1802 - H1809. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. A. Ingram, L. E. Mead, D. B. Moore, W. Woodard, A. Fenoglio, and M. C. Yoder Vessel wall-derived endothelial cells rapidly proliferate because they contain a complete hierarchy of endothelial progenitor cells Blood, April 1, 2005; 105(7): 2783 - 2786. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Grisar, D. Aletaha, C. W. Steiner, T. Kapral, S. Steiner, D. Seidinger, G. Weigel, I. Schwarzinger, W. Wolozcszuk, G. Steiner, et al. Depletion of Endothelial Progenitor Cells in the Peripheral Blood of Patients With Rheumatoid Arthritis Circulation, January 18, 2005; 111(2): 204 - 211. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T.-S. Li, H. Ito, M. Hayashi, A. Furutani, M. Matsuzaki, and K. Hamano Cellular expression of integrin-{beta}1 is of critical importance for inducing therapeutic angiogenesis by cell implantation Cardiovasc Res, January 1, 2005; 65(1): 64 - 72. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. A. Ingram, L. E. Mead, H. Tanaka, V. Meade, A. Fenoglio, K. Mortell, K. Pollok, M. J. Ferkowicz, D. Gilley, and M. C. Yoder Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood Blood, November 1, 2004; 104(9): 2752 - 2760. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Biancone, V. Cantaluppi, D. Duo, M. C. Deregibus, C. Torre, and G. Camussi Role of L-Selectin in the Vascular Homing of Peripheral Blood-Derived Endothelial Progenitor Cells J. Immunol., October 15, 2004; 173(8): 5268 - 5274. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Urbich and S. Dimmeler Endothelial Progenitor Cells: Characterization and Role in Vascular Biology Circ. Res., August 20, 2004; 95(4): 343 - 353. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. L. March and B. H. Johnstone Cellular approaches to tissue repair in cardiovascular disease: the more we know, the more there is to learn Am J Physiol Heart Circ Physiol, August 1, 2004; 287(2): H458 - H463. [Full Text] [PDF]
|
|
|
|
|
|
D. Jevremovic, R. Gulati, I. Hennig, R. M. Diaz, C. Cole, L. Kleppe, F. L. Cosset, R. D. Simari, and R. G. Vile Use of blood outgrowth endothelial cells as virus-producing vectors for gene delivery to tumors Am J Physiol Heart Circ Physiol, August 1, 2004; 287(2): H494 - H500. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Gulati, D. Jevremovic, T. A. Witt, L. S. Kleppe, R. G. Vile, A. Lerman, and R. D. Simari Modulation of the vascular response to injury by autologous blood-derived outgrowth endothelial cells Am J Physiol Heart Circ Physiol, August 1, 2004; 287(2): H512 - H517. [Abstract] [Full Text] [PDF]
|
|