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Circulation. 2002;105:93-98
doi: 10.1161/hc0102.101442
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(Circulation. 2002;105:93.)
© 2002 American Heart Association, Inc.


Basic Science Reports

Human Mesenchymal Stem Cells Differentiate to a Cardiomyocyte Phenotype in the Adult Murine Heart

Catalin Toma, MD; Mark F. Pittenger, PhD; Kevin S. Cahill, BS; Barry J. Byrne, MD, PhD; Paul D. Kessler, MD

From the Department of Medicine, Division of Cardiology, Johns Hopkins School of Medicine (C.T., P.D.K.), and Osiris Therapeutics, Inc (M.F.P.), Baltimore, Md; and the Powell Gene Therapy Center, Departments of Pediatrics, Molecular Genetics, and Microbiology, University of Florida School of Medicine, Gainesville, Fla (K.S.C., B.J.B.).

Correspondence to Mark Pittenger, PhD, Osiris Therapeutics Inc, 2001 Aliceanna St, Baltimore, MD 21231. E-mail mpittenger{at}osiristx.com

Background Cellular cardiomyoplasty has been proposed as an alternative strategy for augmenting the function of diseased myocardium. We investigated the potential of human mesenchymal stem cells (hMSCs) from adult bone marrow to undergo myogenic differentiation once transplanted into the adult murine myocardium.

Methods and Results A small bone marrow aspirate was taken from the iliac crest of healthy human volunteers, and hMSCs were isolated as previously described. The stem cells, labeled with lacZ, were injected into the left ventricle of CB17 SCID/beige adult mice. At 4 days after injection, none of the engrafted hMSCs expressed myogenic markers. A limited number of cells survived past 1 week and over time morphologically resembled the surrounding host cardiomyocytes. Immunohistochemistry revealed de novo expression of desmin, ß-myosin heavy chain, {alpha}-actinin, cardiac troponin T, and phospholamban at levels comparable to those of the host cardiomyocytes; sarcomeric organization of the contractile proteins was observed. In comparison, neither cardiac troponin T nor phospholamban was detected in the myotubes formed in vitro by MyoD-transduced hMSCs.

Conclusions The purified hMSCs from adult bone marrow engrafted in the myocardium appeared to differentiate into cardiomyocytes. The persistence of the engrafted hMSCs and their in situ differentiation in the heart may represent the basis for using these adult stem cells for cellular cardiomyoplasty.


Key Words: stem cells • genes • myocytes • heart failure




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S. Y. Lim, Y. S. Kim, Y. Ahn, M. H. Jeong, M. H. Hong, S. Y. Joo, K. I. Nam, J. G. Cho, P. M. Kang, and J. C. Park
The effects of mesenchymal stem cells transduced with Akt in a porcine myocardial infarction model
Cardiovasc Res, June 1, 2006; 70(3): 530 - 542.
[Abstract] [Full Text] [PDF]


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Eur Heart JHome page
T. Freyman, G. Polin, H. Osman, J. Crary, M. Lu, L. Cheng, M. Palasis, and R. L. Wilensky
A quantitative, randomized study evaluating three methods of mesenchymal stem cell delivery following myocardial infarction
Eur. Heart J., May 1, 2006; 27(9): 1114 - 1122.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
C. A. Eisenberg, J. B.E. Burch, and L. M. Eisenberg
Bone Marrow Cells Transdifferentiate to Cardiomyocytes When Introduced into the Embryonic Heart
Stem Cells, May 1, 2006; 24(5): 1236 - 1245.
[Abstract] [Full Text] [PDF]


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CirculationHome page
M. G. Chang, L. Tung, R. B. Sekar, C. Y. Chang, J. Cysyk, P. Dong, E. Marban, and M. R. Abraham
Proarrhythmic Potential of Mesenchymal Stem Cell Transplantation Revealed in an In Vitro Coculture Model
Circulation, April 18, 2006; 113(15): 1832 - 1841.
[Abstract] [Full Text] [PDF]


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J. Thorac. Cardiovasc. Surg.Home page
J. J. Gavira, J. Herreros, A. Perez, M. J. Garcia-Velloso, J. Barba, F. Martin-Herrero, C. Canizo, A. Martin-Arnau, J. M. Marti-Climent, M. Hernandez, et al.
Autologous skeletal myoblast transplantation in patients with nonacute myocardial infarction: 1-year follow-up
J. Thorac. Cardiovasc. Surg., April 1, 2006; 131(4): 799 - 804.
[Abstract] [Full Text] [PDF]


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FASEB J.Home page
M. Gnecchi, H. He, N. Noiseux, O. D. Liang, L. Zhang, F. Morello, H. Mu, L. G. Melo, R. E. Pratt, J. S. Ingwall, et al.
Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement
FASEB J, April 1, 2006; 20(6): 661 - 669.
[Abstract] [Full Text] [PDF]


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JNMHome page
S. L.M.A. Beeres, J. J. Bax, P. Dibbets, M. P.M. Stokkel, K. Zeppenfeld, W. E. Fibbe, E. E. van der Wall, M. J. Schalij, and D. E. Atsma
Effect of Intramyocardial Injection of Autologous Bone Marrow-Derived Mononuclear Cells on Perfusion, Function, and Viability in Patients with Drug-Refractory Chronic Ischemia
J. Nucl. Med., April 1, 2006; 47(4): 574 - 580.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
S. Francois, M. Bensidhoum, M. Mouiseddine, C. Mazurier, B. Allenet, A. Semont, J. Frick, A. Sache, S. Bouchet, D. Thierry, et al.
Local Irradiation Not Only Induces Homing of Human Mesenchymal Stem Cells at Exposed Sites but Promotes Their Widespread Engraftment to Multiple Organs: A Study of Their Quantitative Distribution After Irradiation Damage
Stem Cells, April 1, 2006; 24(4): 1020 - 1029.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Heart Circ. Physiol.Home page
X. Wang, Q. Hu, A. Mansoor, J. Lee, Z. Wang, T. Lee, A. H. L. From, and J. Zhang
Bioenergetic and functional consequences of stem cell-based VEGF delivery in pressure-overloaded swine hearts
Am J Physiol Heart Circ Physiol, April 1, 2006; 290(4): H1393 - H1405.
[Abstract] [Full Text] [PDF]


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BloodHome page
J. Stagg, S. Pommey, N. Eliopoulos, and J. Galipeau
Interferon-{gamma}-stimulated marrow stromal cells: a new type of nonhematopoietic antigen-presenting cell
Blood, March 15, 2006; 107(6): 2570 - 2577.
[Abstract] [Full Text] [PDF]


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BloodHome page
G. M. Spaggiari, A. Capobianco, S. Becchetti, M. C. Mingari, and L. Moretta
Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation
Blood, February 15, 2006; 107(4): 1484 - 1490.
[Abstract] [Full Text] [PDF]


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PhysiologyHome page
S. P. Raikwar, T. Mueller, and N. Zavazava
Strategies for Developing Therapeutic Application of Human Embryonic Stem Cells
Physiology, February 1, 2006; 21(1): 19 - 28.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
Y. Ma, Y. Xu, Z. Xiao, W. Yang, C. Zhang, E. Song, Y. Du, and L. Li
Reconstruction of Chemically Burned Rat Corneal Surface by Bone Marrow-Derived Human Mesenchymal Stem Cells
Stem Cells, February 1, 2006; 24(2): 315 - 321.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
M. Krampera, L. Cosmi, R. Angeli, A. Pasini, F. Liotta, A. Andreini, V. Santarlasci, B. Mazzinghi, G. Pizzolo, F. Vinante, et al.
Role for Interferon-{gamma} in the Immunomodulatory Activity of Human Bone Marrow Mesenchymal Stem Cells
Stem Cells, February 1, 2006; 24(2): 386 - 398.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
W. Zhu, J. Chen, X. Cong, S. Hu, and X. Chen
Hypoxia and Serum Deprivation-Induced Apoptosis in Mesenchymal Stem Cells
Stem Cells, February 1, 2006; 24(2): 416 - 425.
[Abstract] [Full Text] [PDF]


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Exp. Biol. Med.Home page
J. J. Minguell and A. Erices
Mesenchymal Stem Cells and the Treatment of Cardiac Disease
Experimental Biology and Medicine, January 1, 2006; 231(1): 39 - 49.
[Abstract] [Full Text] [PDF]


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J. Am. Soc. Nephrol.Home page
D. R. Abrahamson and B. M. Steenhard
Renal Therapy by Stem Cells: Outsource or In-House?
J. Am. Soc. Nephrol., January 1, 2006; 17(1): 12 - 14.
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Cardiovasc ResHome page
J. Andrade, J. T. Lam, M. Zamora, C. Huang, D. Franco, N. Sevilla, P. J. Gruber, J. T. Lu, and P. Ruiz-Lozano
Predominant fusion of bone marrow-derived cardiomyocytes
Cardiovasc Res, December 1, 2005; 68(3): 387 - 393.
[Abstract] [Full Text] [PDF]


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CirculationHome page
C. E. Murry, L. J. Field, and P. Menasche
Cell-Based Cardiac Repair: Reflections at the 10-Year Point
Circulation, November 15, 2005; 112(20): 3174 - 3183.
[Full Text] [PDF]


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J Am Coll CardiolHome page
Y. L. Tang, Y. Tang, Y. C. Zhang, K. Qian, L. Shen, and M. I. Phillips
Improved Graft Mesenchymal Stem Cell Survival in Ischemic Heart With a Hypoxia-Regulated Heme Oxygenase-1 Vector
J. Am. Coll. Cardiol., October 4, 2005; 46(7): 1339 - 1350.
[Abstract] [Full Text] [PDF]


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J Am Coll CardiolHome page
V. J. Dzau, M. Gnecchi, and A. S. Pachori
Enhancing Stem Cell Therapy Through Genetic Modification
J. Am. Coll. Cardiol., October 4, 2005; 46(7): 1351 - 1353.
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J CARDIOVASC PHARMACOL THERHome page
R. R. Makkar, M. J. Price, M. Lill, M. Frantzen, K. Takizawa, T. Kleisli, J. Zheng, S. Kar, R. McClelan, T. Miyamota, et al.
Intramyocardial Injection of Allogenic Bone Marrow-Derived Mesenchymal Stem Cells Without Immunosuppression Preserves Cardiac Function in a Porcine Model of Myocardial Infarction
Journal of Cardiovascular Pharmacology and Therapeutics, October 1, 2005; 10(4): 225 - 233.
[Abstract] [PDF]


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CirculationHome page
D. L. Kraitchman, M. Tatsumi, W. D. Gilson, T. Ishimori, D. Kedziorek, P. Walczak, W. P. Segars, H. H. Chen, D. Fritzges, I. Izbudak, et al.
Dynamic Imaging of Allogeneic Mesenchymal Stem Cells Trafficking to Myocardial Infarction
Circulation, September 6, 2005; 112(10): 1451 - 1461.
[Abstract] [Full Text] [PDF]


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Am. J. Pathol.Home page
M. A. Laflamme, J. Gold, C. Xu, M. Hassanipour, E. Rosler, S. Police, V. Muskheli, and C. E. Murry
Formation of Human Myocardium in the Rat Heart from Human Embryonic Stem Cells
Am. J. Pathol., September 1, 2005; 167(3): 663 - 671.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
T. Tondreau, N. Meuleman, A. Delforge, M. Dejeneffe, R. Leroy, M. Massy, C. Mortier, D. Bron, and L. Lagneaux
Mesenchymal Stem Cells Derived from CD133-Positive Cells in Mobilized Peripheral Blood and Cord Blood: Proliferation, Oct4 Expression, and Plasticity
Stem Cells, September 1, 2005; 23(8): 1105 - 1112.
[Abstract] [Full Text] [PDF]


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CirculationHome page
N. Nagaya, K. Kangawa, T. Itoh, T. Iwase, S. Murakami, Y. Miyahara, T. Fujii, M. Uematsu, H. Ohgushi, M. Yamagishi, et al.
Transplantation of Mesenchymal Stem Cells Improves Cardiac Function in a Rat Model of Dilated Cardiomyopathy
Circulation, August 23, 2005; 112(8): 1128 - 1135.
[Abstract] [Full Text] [PDF]


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Eur. J. Cardiothorac. Surg.Home page
M. Siepe, C. Heilmann, P. von Samson, P. Menasche, and F. Beyersdorf
Stem cell research and cell transplantation for myocardial regeneration
Eur. J. Cardiothorac. Surg., August 1, 2005; 28(2): 318 - 324.
[Abstract] [Full Text] [PDF]


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Am. J. Respir. Cell Mol. Bio.Home page
M. Rojas, J. Xu, C. R. Woods, A. L. Mora, W. Spears, J. Roman, and K. L. Brigham
Bone Marrow-Derived Mesenchymal Stem Cells in Repair of the Injured Lung
Am. J. Respir. Cell Mol. Biol., August 1, 2005; 33(2): 145 - 152.
[Abstract] [Full Text] [PDF]


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Stem CellsHome page
C. Muscari, F. Bonafe, I. Stanic, F. Flamigni, C. Stefanelli, G. Farruggia, C. Guarnieri, and C. M. Caldarera
Polyamine Depletion Reduces TNF{alpha}/MG132-Induced Apoptosis in Bone Marrow Stromal Cells
Stem Cells, August 1, 2005; 23(7): 983 - 991.
[Abstract] [Full Text] [PDF]


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Cardiovasc ResHome page
C. Ventura
Forced myocardin expression primes cardiac and smooth muscle transcription patterning in human mesenchymal stem cells
Cardiovasc Res, August 1, 2005; 67(2): 182 - 183.
[Full Text] [PDF]


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CirculationHome page
K. C. Wollert and H. Drexler
Mesenchymal Stem Cells for Myocardial Infarction: Promises and Pitfalls
Circulation, July 12, 2005; 112(2): 151 - 153.
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Stem CellsHome page
O. Pelz, M. Wu, T. Nikolova, M. Kamprad, M. Ackermann, D. Egger, F. Emmrich, A. M. Wobus, and M. Cross
Duplex Polymerase Chain Reaction Quantification of Human Cells in a Murine Background
Stem Cells, June 1, 2005; 23(6): 828 - 833.
[Abstract] [Full Text] [PDF]