Circulation. 2001;104:1046-1052
doi: 10.1161/hc3501.093817
doi: 10.1161/hc3501.093817
(Circulation. 2001;104:1046.)
© 2001 American Heart Association, Inc.
Basic Science Reports |
Implantation of Bone Marrow Mononuclear Cells Into Ischemic Myocardium Enhances Collateral Perfusion and Regional Function via Side Supply of Angioblasts, Angiogenic Ligands, and Cytokines
From the Department of Medicine II and Cardiovascular Center, Kansai Medical University, Moriguchi, Osaka (H.K., H. Matsubara, T.N., S.F., Y.T., H. Masaki, Y.M., O.I., E.T., A.K., T. Iwasaka); the Department of Laboratory Medicine, Hiroshima University School of Medicine, Hiroshima (R.O.); and the Cardiovascular Research Institute and Department of Medicine III, Kurume University School of Medicine, Kurume (S.S., T.M., T. Imaizumi), Japan. The first 4 authors contributed equally to this article, and the order of authorship is arbitrary.
Correspondence to Hiroaki Matsubara, MD, Department of Medicine II, Kansai Medical University, Moriguchi, Osaka 570-8507, Japan. E-mail matsubah{at}takii.kmu.ac.jp
Background— Bone marrow implantation (BMI) was shown to enhance angiogenesis in a rat ischemic heart model. This preclinical study using a swine model was designed to test the safety and therapeutic effectiveness of BMI.
Methods and Results— BM-derived mononuclear cells (BM-MNCs) were injected into a zone made ischemic by coronary artery ligation. Three weeks after BMI, regional blood flow and capillary densities were significantly higher (4.6- and 2.8-fold, respectively), and cardiac function was improved. Angiography revealed that there was a marked increase (5.7-fold) in number of visible collateral vessels. Implantation of porcine coronary microvascular endothelial cells (CMECs) did not cause any significant increase in capillary densities. Labeled BM-MNCs were incorporated into 
31% of neocapillaries and corresponded to 8.7% of macrophages but did not actively survive as myoblasts or fibroblasts. There was no bone formation by osteoblasts or malignant ventricular arrhythmia. Time-dependent changes in plasma levels for cardiac enzymes (troponin I and creatine kinase-MB) did not differ between the BMI, CMEC, and medium-alone implantation groups. BM-MNCs contained 16% of endothelial-lineage cells and expressed basic fibroblast growth factor>>vascular endothelial growth factor>angiopoietin 1 mRNAs, and their cardiac levels were significantly upregulated by BMI. Cardiac interleukin-1ß and tumor necrosis factor-
mRNA expression were also induced by BMI but not by CMEC implantation. BM-MNCs were actively differentiated to endothelial cells in vitro and formed network structure with human umbilical vein endothelial cells.
Conclusions— BMI may constitute a novel safety strategy for achieving optimal therapeutic angiogenesis by the natural ability of the BM cells to secrete potent angiogenic ligands and cytokines as well as to be incorporated into foci of neovascularization.
Key Words: angiogenesis • blood cells • transplantation • ischemia
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G. V. Silva, S. Litovsky, J. A.R. Assad, A. L.S. Sousa, B. J. Martin, D. Vela, S. C. Coulter, J. Lin, J. Ober, W. K. Vaughn, et al. Mesenchymal Stem Cells Differentiate into an Endothelial Phenotype, Enhance Vascular Density, and Improve Heart Function in a Canine Chronic Ischemia Model Circulation, January 18, 2005; 111(2): 150 - 156. [Abstract] [Full Text] [PDF]
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J. Song, P. S. Cottler, A. L. Klibanov, S. Kaul, and R. J. Price Microvascular remodeling and accelerated hyperemia blood flow restoration in arterially occluded skeletal muscle exposed to ultrasonic microbubble destruction Am J Physiol Heart Circ Physiol, December 1, 2004; 287(6): H2754 - H2761. [Abstract] [Full Text] [PDF]
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L. G. Melo, M. Gnecchi, A. S. Pachori, D. Kong, K. Wang, X. Liu, R. E. Pratt, and V. J. Dzau Endothelium-Targeted Gene and Cell-Based Therapies for Cardiovascular Disease Arterioscler Thromb Vasc Biol, October 1, 2004; 24(10): 1761 - 1774. [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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Y.-S. Yoon, J.-S. Park, T. Tkebuchava, C. Luedeman, and D. W. Losordo Unexpected Severe Calcification After Transplantation of Bone Marrow Cells in Acute Myocardial Infarction Circulation, June 29, 2004; 109(25): 3154 - 3157. [Abstract] [Full Text] [PDF]
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D. W. Losordo and S. Dimmeler Therapeutic Angiogenesis and Vasculogenesis for Ischemic Disease: Part II: Cell-Based Therapies Circulation, June 8, 2004; 109(22): 2692 - 2697. [Full Text] [PDF]
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T. J. Rabelink, H. C. de Boer, E. J.P. de Koning, and A.-J. van Zonneveld Endothelial Progenitor Cells: More Than an Inflammatory Response? Arterioscler Thromb Vasc Biol, May 1, 2004; 24(5): 834 - 838. [Abstract] [Full Text]
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H. Fujii, S. Tomita, T. Nakatani, S. Fukuhara, A. Hanatani, Y. Ohtsu, M. Ishida, C. Yutani, K. Miyatake, and S. Kitamura A novel application of myocardial contrast echocardiography to evaluate angiogenesis by autologous bone marrow cell transplantation in chronic ischemic pig model J. Am. Coll. Cardiol., April 7, 2004; 43(7): 1299 - 1305. [Abstract] [Full Text] [PDF]
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H.C. Ott, N. Bonaros, R. Marksteiner, D. Wolf, E. Margreiter, T. Schachner, G. Laufer, and S. Hering Combined transplantation of skeletal myoblasts and bone marrow stem cells for myocardial repair in rats Eur. J. Cardiothorac. Surg., April 1, 2004; 25(4): 627 - 634. [Abstract] [Full Text] [PDF]
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M. A. Retuerto, P. Schalch, G. Patejunas, J. Carbray, N. Liu, K. Esser, R. G. Crystal, and T. K. Rosengart Angiogenic pretreatment improves the efficacy of cellular cardiomyoplasty performed with fetal cardiomyocyte implantation J. Thorac. Cardiovasc. Surg., April 1, 2004; 127(4): 1041 - 1050. [Abstract] [Full Text] [PDF]
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T.-S. Li, M. Hayashi, Z.-L. Liu, H. Ito, A. Mikamo, A. Furutani, M. Matsuzaki, and K. Hamano Low angiogenic potency induced by the implantation of ex vivo expanded CD117+ stem cells Am J Physiol Heart Circ Physiol, April 1, 2004; 286(4): H1236 - H1241. [Abstract] [Full Text] [PDF]
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T. Kinnaird, E. Stabile, M.S. Burnett, M. Shou, C.W. Lee, S. Barr, S. Fuchs, and S.E. Epstein Local Delivery of Marrow-Derived Stromal Cells Augments Collateral Perfusion Through Paracrine Mechanisms Circulation, March 30, 2004; 109(12): 1543 - 1549. [Abstract] [Full Text] [PDF]
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T. Kinnaird, E. Stabile, M.S. Burnett, C.W. Lee, S. Barr, S. Fuchs, and S.E. Epstein Marrow-Derived Stromal Cells Express Genes Encoding a Broad Spectrum of Arteriogenic Cytokines and Promote In Vitro and In Vivo Arteriogenesis Through Paracrine Mechanisms Circ. Res., March 19, 2004; 94(5): 678 - 685. [Abstract] [Full Text] [PDF]
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M Fujita and K Tambara Recent insights into human coronary collateral development Heart, March 1, 2004; 90(3): 246 - 250. [Abstract] [Full Text] [PDF]
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S. Zhang, P. Zhang, J. Guo, Z. Jia, K. Ma, Y. Liu, C. Zhou, and L. Li Enhanced cytoprotection and angiogenesis by bone marrow cell transplantation may contribute to improved ischemic myocardial function Eur. J. Cardiothorac. Surg., February 1, 2004; 25(2): 188 - 195. [Abstract] [Full Text] [PDF]
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J. G.F. Cleland, N. Freemantle, G. Kaye, M. Nasir, P. Velavan, K. Lalukota, T. Mudawi, R. Shelton, A. L. Clark, and A. P. Coletta Clinical trials update from the American Heart Association meeting: {Omega}-3 fatty acids and arrhythmia risk in patients with an implantable defibrillator, ACTIV in CHF, VALIANT, the Hanover autologous bone marrow transplantation study, SPORTIF V, ORBIT and PAD and DEFINITE Eur J Heart Fail, January 1, 2004; 6(1): 109 - 115. [Abstract] [Full Text] [PDF]
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S. Fujiyama, K. Amano, K. Uehira, M. Yoshida, Y. Nishiwaki, Y. Nozawa, D. Jin, S. Takai, M. Miyazaki, K. Egashira, et al. Bone Marrow Monocyte Lineage Cells Adhere on Injured Endothelium in a Monocyte Chemoattractant Protein-1-Dependent Manner and Accelerate Reendothelialization as Endothelial Progenitor Cells Circ. Res., November 14, 2003; 93(10): 980 - 989. [Abstract] [Full Text] [PDF]
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R. Gulati, D. Jevremovic, T. E. Peterson, T. A. Witt, L. S. Kleppe, C. S. Mueske, A. Lerman, R. G. Vile, and R. D. Simari Autologous Culture-Modified Mononuclear Cells Confer Vascular Protection After Arterial Injury Circulation, September 23, 2003; 108(12): 1520 - 1526. [Abstract] [Full Text] [PDF]
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A. Bel, E. Messas, O. Agbulut, P. Richard, J. L. Samuel, P. Bruneval, A. A. Hagege, and P. Menasche Transplantation of Autologous Fresh Bone Marrow Into Infarcted Myocardium: A Word of Caution Circulation, September 9, 2003; 108(90101): II-247 - 252. [Abstract] [Full Text] [PDF]
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S. Davani, A. Marandin, N. Mersin, B. Royer, B. Kantelip, P. Herve, J.-P. Etievent, and J.-P. Kantelip Mesenchymal Progenitor Cells Differentiate into an Endothelial Phenotype, Enhance Vascular Density, and Improve Heart Function in a Rat Cellular Cardiomyoplasty Model Circulation, September 9, 2003; 108(90101): II-253 - 258. [Abstract] [Full Text] [PDF]
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N. Werner, S. Junk, U. Laufs, A. Link, K. Walenta, M. Bohm, and G. Nickenig Intravenous Transfusion of Endothelial Progenitor Cells Reduces Neointima Formation After Vascular Injury Circ. Res., July 25, 2003; 93 (2): e17 - e24. [Abstract] [Full Text] [PDF]
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M. Hristov, W. Erl, and P. C. Weber Endothelial Progenitor Cells: Mobilization, Differentiation, and Homing Arterioscler Thromb Vasc Biol, July 1, 2003; 23(7): 1185 - 1189. [Abstract] [Full Text] [PDF]
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