Circulation Research. 2004;94:230-238
Published online before print December 4, 2003, doi: 10.1161/01.RES.0000110419.50982.1C
Published online before print December 4, 2003, doi: 10.1161/01.RES.0000110419.50982.1C
© 2004 American Heart Association, Inc.
Cellular Biology |
Bone Marrow-Derived Cells Do Not Incorporate Into the Adult Growing Vasculature
From Max-Planck-Institut for Clinical & Physiological Research (T.Z., B.F., S.K., M.H., A.H., W.S.), Bad Nauheim, Germany, and Department of Internal Medicine (R.V.), University Hospital Giessen, Giessen, Germany.
Correspondence to Tibor Ziegelhoeffer, MD, Max-Planck-Institute for Clinical & Physiological Research, Benekestrasse 2, 61231, Bad Nauheim, Germany. E-mail t.ziegelhoeffer{at}kerckhoff.mpg.de
Bone marrow-Derived cells have been proposed to form new vessels or at least incorporate into growing vessels in adult organisms under certain physiological and pathological conditions. We investigated whether bone marrow-Derived cells incorporate into vessels using mouse models of hindlimb ischemia (arteriogenesis and angiogenesis) and tumor growth. C57BL/6 wild-type mice were lethally irradiated and transplanted with bone marrow cells from littermates expressing enhanced green fluorescent protein (GFP). At least 6 weeks after bone marrow transplantation, the animals underwent unilateral femoral artery occlusions with or without pretreatment with vascular endothelial growth factor or were subcutaneously implanted with methylcholanthrene-induced fibrosarcoma (BFS-1) cells. Seven and 21 days after surgery, proximal hindlimb muscles with growing collateral arteries and ischemic gastrocnemius muscles as well as grown tumors and various organs were excised for histological analysis. We failed to colocalize GFP signals with endothelial or smooth muscle cell markers. Occasionally, the use of high-power laser scanning confocal microscopy uncovered false-positive results because of overlap of different fluorescent signals from adjacent cells. Nevertheless, we observed accumulations of GFP-positive cells around growing collateral arteries (3-fold increase versus nonoccluded side, P<0.001) and in ischemic distal hindlimbs. These cells were identified as fibroblasts, pericytes, and primarily leukocytes that stained positive for several growth factors and chemokines. Our findings suggest that in the adult organism, bone marrow-Derived cells do not promote vascular growth by incorporating into vessel walls but may function as supporting cells.
Key Words: arteriogenesis • angiogenesis • bone marrow-Derived cells
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E. Toyota, D. C. Warltier, T. Brock, E. Ritman, C. Kolz, P. O'Malley, P. Rocic, M. Focardi, and W. M. Chilian Vascular Endothelial Growth Factor Is Required for Coronary Collateral Growth in the Rat Circulation, October 4, 2005; 112(14): 2108 - 2113. [Abstract] [Full Text] [PDF]
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L. C. Amado, A. P. Saliaris, K. H. Schuleri, M. St. John, J.-S. Xie, S. Cattaneo, D. J. Durand, T. Fitton, J. Q. Kuang, G. Stewart, et al. Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction PNAS, August 9, 2005; 102(32): 11474 - 11479. [Abstract] [Full Text] [PDF]
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D. Chalothorn, H. Zhang, J. A. Clayton, S. A. Thomas, and J. E. Faber Catecholamines augment collateral vessel growth and angiogenesis in hindlimb ischemia Am J Physiol Heart Circ Physiol, August 1, 2005; 289(2): H947 - H959. [Abstract] [Full Text] [PDF]
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H. F.R. Dohmann, E. C. Perin, C. M. Takiya, G. V. Silva, S. A. Silva, A. L.S. Sousa, C. T. Mesquita, M.-I. D. Rossi, B. M.O. Pascarelli, I. M. Assis, et al. Transendocardial Autologous Bone Marrow Mononuclear Cell Injection in Ischemic Heart Failure: Postmortem Anatomicopathologic and Immunohistochemical Findings Circulation, July 26, 2005; 112(4): 521 - 526. [Abstract] [Full Text] [PDF]
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B. Modarai, K.G. Burnand, B. Sawyer, and A. Smith Endothelial Progenitor Cells Are Recruited Into Resolving Venous Thrombi Circulation, May 24, 2005; 111(20): 2645 - 2653. [Abstract] [Full Text] [PDF]
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N. Ma, C. Stamm, A. Kaminski, W. Li, H.-D. Kleine, B. Muller-Hilke, L. Zhang, Y. Ladilov, D. Egger, and G. Steinhoff Human cord blood cells induce angiogenesis following myocardial infarction in NOD/scid-mice Cardiovasc Res, April 1, 2005; 66(1): 45 - 54. [Abstract] [Full Text] [PDF]
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M. Simons Angiogenesis: Where Do We Stand Now? Circulation, March 29, 2005; 111(12): 1556 - 1566. [Full Text] [PDF]
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D. Fukuda, M. Sata, K. Tanaka, and R. Nagai Potent Inhibitory Effect of Sirolimus on Circulating Vascular Progenitor Cells Circulation, February 22, 2005; 111(7): 926 - 931. [Abstract] [Full Text] [PDF]
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T. Tammela, B. Enholm, K. Alitalo, and K. Paavonen The biology of vascular endothelial growth factors Cardiovasc Res, February 15, 2005; 65(3): 550 - 563. [Abstract] [Full Text] [PDF]
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B. H. Annex and M. Simons Growth factor-induced therapeutic angiogenesis in the heart: protein therapy Cardiovasc Res, February 15, 2005; 65(3): 649 - 655. [Abstract] [Full Text] [PDF]
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M. Abedin, Y. Tintut, and L. L. Demer Mesenchymal Stem Cells and the Artery Wall Circ. Res., October 1, 2004; 95(7): 671 - 676. [Abstract] [Full Text] [PDF]
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I. Rajantie, M. Ilmonen, A. Alminaite, U. Ozerdem, K. Alitalo, and P. Salven Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells Blood, October 1, 2004; 104(7): 2084 - 2086. [Abstract] [Full Text] [PDF]
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E. Khmelewski, A. Becker, T. Meinertz, and W. D. Ito Tissue Resident Cells Play a Dominant Role in Arteriogenesis and Concomitant Macrophage Accumulation Circ. Res., September 17, 2004; 95(6): e56 - e64. [Abstract] [Full Text] [PDF]
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M. Heil and W. Schaper Influence of Mechanical, Cellular, and Molecular Factors on Collateral Artery Growth (Arteriogenesis) Circ. Res., September 3, 2004; 95(5): 449 - 458. [Abstract] [Full Text] [PDF]
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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]
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T. Kinnaird, E. Stabile, M. S. Burnett, and S. E. Epstein Bone Marrow-Derived Cells for Enhancing Collateral Development: Mechanisms, Animal Data, and Initial Clinical Experiences Circ. Res., August 20, 2004; 95(4): 354 - 363. [Abstract] [Full Text] [PDF]
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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]
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D. Skowasch, A. Jabs, B. Luderitz, and G. Bauriedel Bone Marrow-Derived Cells and Vascular Growth Circ. Res., April 30, 2004; 94(8): e71 - e71. [Full Text] [PDF]
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M. Heil, T. Ziegelhoeffer, B. Mees, and W. Schaper A Different Outlook on the Role of Bone Marrow Stem Cells in Vascular Growth: Bone Marrow Delivers Software not Hardware Circ. Res., March 19, 2004; 94(5): 573 - 574. [Full Text] [PDF]
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M. Heil, T. Ziegelhoeffer, S. Wagner, B. Fernandez, A. Helisch, S. Martin, S. Tribulova, W. A. Kuziel, G. Bachmann, and W. Schaper Collateral Artery Growth (Arteriogenesis) After Experimental Arterial Occlusion Is Impaired in Mice Lacking CC-Chemokine Receptor-2 Circ. Res., March 19, 2004; 94(5): 671 - 677. [Abstract] [Full Text] [PDF]
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