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(Circulation Research. 2000;87:728.)
© 2000 American Heart Association, Inc.


Reports

Endothelial Cells of Hematopoietic Origin Make a Significant Contribution to Adult Blood Vessel Formation

Jeffrey R. Crosby, Wolfgang E. Kaminski, Gina Schatteman, Paul J. Martin, Elaine W. Raines, Ron A. Seifert, Daniel F. Bowen-Pope

From the Department of Pathology (J.R.C., W.E.K., E.W.R., R.A.S., D.F.B.-P.), University of Washington, Seattle, Wash; and Division of Clinical Research (P.J.M.), Fred Hutchinson Cancer Research Center, Seattle, Wash. Current affiliations: J.R.C., S.C. Johnson Research Center, Mayo Clinic Scottsdale, Scottsdale, Ariz; W.E.K., Department of Clinical Chemistry and Laboratory Medicine, University of Regensburg Medical School, Regensburg, Germany; and G.S., Department of Anatomy and Cell Biology, University of Iowa, Iowa City, Iowa.

Correspondence to Daniel F. Bowen-Pope, University of Washington, Department of Pathology, Box 357470, Health Sciences Center, Room D525, Seattle, WA 98195-7470. E-mail bp{at}u.washington.edu

Granulation tissue formation is an example of new tissue development in an adult. Its rich vascular network has been thought to derive via angiogenic sprouting and extension of preexisting vessels from the surrounding tissue. The possibility that circulating cells of hematopoietic origin can differentiate into vascular endothelial cells (ECs) in areas of vascular remodeling has recently gained credibility. However, no quantitative data have placed the magnitude of this contribution into a physiological perspective. We have used hematopoietic chimeras to determine that 0.2% to 1.4% of ECs in vessels in control tissues derived from hematopoietic progenitors during the 4 months after irradiation and hematopoietic recovery. By contrast, 8.3% to 11.2% of ECs in vessels that developed in sponge-induced granulation tissue during 1 month derived from circulating hematopoietic progenitors. This recruitment of circulating progenitors to newly forming vessels would be difficult to observe in standard histological studies, but it is large enough to be encouraging for attempts to manipulate this contribution for therapeutic gain.


Key Words: hematopoietic stem cell • angiogenesis • endothelial cell




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SEMIN CARDIOTHORAC VASC ANESTHHome page
V. Chhokar and A. L. Tucker
Angiogenesis: Basic Mechanisms and Clinical Applications
Seminars in Cardiothoracic and Vascular Anesthesia, September 1, 2003; 7(3): 253 - 280.
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Am. J. Pathol.Home page
B. S. Buetow, K. A. Tappan, J. R. Crosby, R. A. Seifert, and D. F. Bowen-Pope
Chimera Analysis Supports a Predominant Role of PDGFR{beta} in Promoting Smooth-Muscle Cell Chemotaxis after Arterial Injury
Am. J. Pathol., September 1, 2003; 163(3): 979 - 984.
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Am. J. Pathol.Home page
M. B. Rookmaaker, A. M. Smits, H. Tolboom, K. van 't Wout, A. C. Martens, R. Goldschmeding, J. A. Joles, A. J. van Zonneveld, H.-J. Grone, T. J. Rabelink, et al.
Bone-Marrow-Derived Cells Contribute to Glomerular Endothelial Repair in Experimental Glomerulonephritis
Am. J. Pathol., August 1, 2003; 163(2): 553 - 562.
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Circ. Res.Home page
B. Assmus, C. Urbich, A. Aicher, W. K. Hofmann, J. Haendeler, L. Rossig, I. Spyridopoulos, A. M. Zeiher, and S. Dimmeler
HMG-CoA Reductase Inhibitors Reduce Senescence and Increase Proliferation of Endothelial Progenitor Cells via Regulation of Cell Cycle Regulatory Genes
Circ. Res., May 16, 2003; 92(9): 1049 - 1055.
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Cardiovasc ResHome page
H. Masuda and T. Asahara
Post-natal endothelial progenitor cells for neovascularization in tissue regeneration
Cardiovasc Res, May 1, 2003; 58(2): 390 - 398.
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Am. J. Pathol.Home page
A. Solowiej, P. Biswas, D. Graesser, and J. A. Madri
Lack of Platelet Endothelial Cell Adhesion Molecule-1 Attenuates Foreign Body Inflammation because of Decreased Angiogenesis
Am. J. Pathol., March 1, 2003; 162(3): 953 - 962.
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Arterioscler. Thromb. Vasc. Bio.Home page
N. Werner, J. Priller, U. Laufs, M. Endres, M. Bohm, U. Dirnagl, and G. Nickenig
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., October 1, 2002; 22(10): 1567 - 1572.
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Am. J. Physiol. Renal Physiol.Home page
M. S. Segal, A. Bihorac, and M. Koc
Circulating endothelial cells: tea leaves for renal disease
Am J Physiol Renal Physiol, July 1, 2002; 283(1): F11 - F19.
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Circ. Res.Home page
M. G. Frid, V. A. Kale, and K. R. Stenmark
Mature Vascular Endothelium Can Give Rise to Smooth Muscle Cells via Endothelial-Mesenchymal Transdifferentiation: In Vitro Analysis
Circ. Res., June 14, 2002; 90(11): 1189 - 1196.
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StrokeHome page
D. C. Hess, W. D. Hill, A. Martin-Studdard, J. Carroll, J. Brailer, and J. Carothers
Bone Marrow as a Source of Endothelial Cells and NeuN-Expressing Cells After Stroke
Stroke, May 1, 2002; 33(5): 1362 - 1368.
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Circ. Res.Home page
C. Urbich, E. Dernbach, A. M. Zeiher, and S. Dimmeler
Double-Edged Role of Statins in Angiogenesis Signaling
Circ. Res., April 5, 2002; 90(6): 737 - 744.
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Am. J. Pathol.Home page
B. S. Buetow, J. R. Crosby, W. E. Kaminski, R. K. Ramachandran, P. Lindahl, P. Martin, C. Betsholtz, R. A. Seifert, E. W. Raines, and D. F. Bowen-Pope
Platelet-Derived Growth Factor B-Chain of Hematopoietic Origin Is Not Necessary for Granulation Tissue Formation and Its Absence Enhances Vascularization
Am. J. Pathol., November 1, 2001; 159(5): 1869 - 1876.
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Clin. Cancer Res.Home page
A. M. Davidoff, C. Y. C. Ng, P. Brown, M. A. Leary, W. W. Spurbeck, J. Zhou, E. Horwitz, E. F. Vanin, and A. W. Nienhuis
Bone Marrow-derived Cells Contribute to Tumor Neovasculature and, When Modified to Express an Angiogenesis Inhibitor, Can Restrict Tumor Growth in Mice
Clin. Cancer Res., September 1, 2001; 7(9): 2870 - 2879.
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Stem CellsHome page
M. Harraz, C. Jiao, H. D. Hanlon, R. S. Hartley, and G. C. Schatteman
CD34- Blood-Derived Human Endothelial Cell Progenitors
Stem Cells, July 1, 2001; 19(4): 304 - 312.
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Circ. Res.Home page
Editorial Policy Changes at Circulation Research
Circ. Res., January 19, 2001; 88(1): 1 - 1.
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Am. J. Physiol. Renal Physiol.Home page
S. V. Brodsky, T. Yamamoto, T. Tada, B. Kim, J. Chen, F. Kajiya, and M. S. Goligorsky
Endothelial dysfunction in ischemic acute renal failure: rescue by transplanted endothelial cells
Am J Physiol Renal Physiol, June 1, 2002; 282(6): F1140 - F1149.
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CirculationHome page
H. Iwaguro, J.-i. Yamaguchi, C. Kalka, S. Murasawa, H. Masuda, S.-i. Hayashi, M. Silver, T. Li, J. M. Isner, and T. Asahara
Endothelial Progenitor Cell Vascular Endothelial Growth Factor Gene Transfer for Vascular Regeneration
Circulation, February 12, 2002; 105(6): 732 - 738.
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Circ. Res.Home page
C. Urbich, E. Dernbach, A. M. Zeiher, and S. Dimmeler
Double-Edged Role of Statins in Angiogenesis Signaling
Circ. Res., April 5, 2002; 90(6): 737 - 744.
[Abstract] [Full Text] [PDF]