Bone marrow-derived human mesenchymal stem cells express cardiomyogenic proteins but do not exhibit functional cardiomyogenic differentiation potential

Stem Cells and Development

Volumn 21, Issue 13, 2012, Pages 2457-2470

  Siegel, Georg ^a   Krause, Petra ^a   Wöhrle, Stefanie ^a   Nowak, Patrick ^a   Ayturan, Miriam ^a   Kluba, Torsten ^a   Brehm, Bernhard R ^b   Neumeister, Birgid ^c   Köhler, David ^a   Rosenberger, Peter ^a   Just, Lothar ^d   Northoff, Hinnak ^a   Schäfer, Richard ^a,e  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b Katholisches Klinikum Koblenz   (Germany)

^c Laboratory Dr Gärtner   (Germany)

^d UNIVERSITY OF TÜBINGEN   (Germany)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; MESSENGER RNA; MYOSIN LIGHT CHAIN; STEM CELL ANTIGEN 1; TROPONIN I;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL SURVIVAL; COCULTURE; CONTROLLED STUDY; FEMALE; FETUS; GENE EXPRESSION; HEART INFARCTION; HEART MUSCLE CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NONHUMAN; NORMAL HUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGENERATION; UPREGULATION;

ACTINS; ADULT; ANIMALS; ANTIGENS, CD; BONE MARROW; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; COCULTURE TECHNIQUES; CULTURE MEDIA; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMANS; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; MIDDLE AGED; MODELS, ANIMAL; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; MYOSIN LIGHT CHAINS; PREGNANCY; RNA, MESSENGER; TROPONIN I; TUMOR CELLS, CULTURED;

MURINAE;

EID: 84865747523     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2011.0626     Document Type: Article

References (58)

1. Antman EM, M Hand, PW Armstrong, ER Bates, LA Green, LK Halasyamani, JS Hochman, HM Krumholz, GA Lamas, et al. (2008). 2007 focused update of the ACC/AHA 2004 guidelines for the management of patients with ST-elevation myocardial infarction: A report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol 51:210-247.
2. Cohen M, JE Diez, GN Levine, JJ Ferguson 3rd, DA Morrow, SV Rao and JP Zidar. (2007). Pharmacoinvasive management of acute coronary syndrome: Incorporating the 2007 ACC/AHA guidelines: The CATH (cardiac catheterization and antithrombotic therapy in the hospital) Clinical Consensus Panel Report -III. J Invasive Cardiol 19:525-538; quiz 539-540.
3. Fitchett D, K Rockwood, BT Chan, S Schultz, P Bogaty, A Gillis, M Arnold, F Miller, MM Graham, et al. (2004). Canadian Cardiovascular Society Consensus Conference 2002: Management of heart disease in the elderly patient. Can J Cardiol 20 (Suppl. A):7A-16A.
4. Anversa P, A Leri, M Rota, T Hosoda, C Bearzi, K Urbanek, J Kajstura and R Bolli. (2007). Concise review: stem cells, myocardial regeneration, and methodological artifacts. Stem Cells 25:589-601.
5. Anversa P, J Kajstura and A Leri. (2007). If I can stop one heart from breaking. Circulation 115:829-832.
6. Laugwitz KL, A Moretti, J Lam, P Gruber, Y Chen, S Woodard, LZ Lin, CL Cai, MM Lu, et al. (2005). Postnatal isl1 + cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433:647-653.
7. Qyang Y, S Martin-Puig, M Chiravuri, S Chen, H Xu, L Bu, X Jiang, L Lin, A Granger, et al. (2007). The renewal and differentiation of Isl1 + cardiovascular progenitors are controlled by a Wnt/beta-catenin pathway. Cell Stem Cell 1:165-179.
8. Bearzi C, M Rota, T Hosoda, J Tillmanns, A Nascimbene, A De Angelis, S Yasuzawa-Amano, I Trofimova, RW Siggins, et al. (2007). Human cardiac stem cells. Proc Natl Acad Sci U S A 104:14068-14073.
9. Tillmanns J, M Rota, T Hosoda, Y Misao, G Esposito, A Gonzalez, S Vitale, C Parolin, S Yasuzawa-Amano, et al. (2008). Formation of large coronary arteries by cardiac progenitor cells. Proc Natl Acad Sci U S A 105:1668-1673.
10. Casaclang-Verzosa G, BJ Gersh and TS Tsang. (2008). Structural and functional remodeling of the left atrium: Clinical and therapeutic implications for atrial fibrillation. J Am Coll Cardiol 51:1-11.
11. Schafer R and H Northoff. (2008). Cardioprotection and cardiac regeneration by mesenchymal stem cells. Panminerva Med 50:31-39.
12. Williams AR and JM Hare. (2011). Mesenchymal stem cells: biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease. Circ Res 109:923-940.
13. Shake JG, PJ Gruber, WA Baumgartner, G Senechal, J Meyers, JM Redmond, MF Pittenger and BJ Martin. (2002). Mesenchymal stem cell implantation in a swine myocardial infarct model: Engraftment and functional effects. Ann Thorac Surg 73:1919-1925; discussion 1926.
14. Kawada H, J Fujita, K Kinjo, Y Matsuzaki, M Tsuma, H Miyatake, Y Muguruma, K Tsuboi, Y Itabashi, et al. (2004). Nonhematopoietic mesenchymal stem cells can be mobilized and differentiate into cardiomyocytes after myocardial infarction. Blood 104:3581-3587.
15. Mangi AA, N Noiseux, D Kong, H He, M Rezvani, JS Ingwall and VJ Dzau. (2003). Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat Med 9:1195-1201.
16. Rose RA, H Jiang, X Wang, S Helke, JN Tsoporis, N Gong, SC Keating, TG Parker, PH Backx and A Keating. (2008). Bone marrow-derived mesenchymal stromal cells express cardiac-specific markers, retain the stromal phenotype, and do not become functional cardiomyocytes in vitro. Stem Cells 26:2884-2892.
17. Rose RA, A Keating and PH Backx. (2008). Do mesenchymal stromal cells transdifferentiate into functional cardiomyocytes? Circ Res 103:e120.
18. Colter DC, I Sekiya and DJ Prockop. (2001). Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc Natl Acad Sci U S A 98:7841-7845.
19. Pittenger MF, AM Mackay, SC Beck, RK Jaiswal, R Douglas, JD Mosca, MA Moorman, DW Simonetti, S Craig and DR Marshak. (1999). Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
20. Schafer R, R Kehlbach, M Muller, R Bantleon, T Kluba, M Ayturan, G Siegel, H Wolburg, H Northoff, et al. (2009). Labeling of human mesenchymal stromal cells with superparamagnetic iron oxide leads to a decrease in migration capacity and colony formation ability. Cytotherapy 11:68-78.
21. Wakitani S, T Saito and AI Caplan. (1995). Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-Azacytidine. Muscle Nerve 18:1417-1426.
22. Xaymardan M, L Tang, L Zagreda, B Pallante, J Zheng, JL Chazen, A Chin, I Duignan, P Nahirney, et al. (2004). Platelet-derived growth factor-AB promotes the generation of adult bone marrow-derived cardiac myocytes. Circ Res 94:E39-E45.
23. Shim WS, S Jiang, P Wong, J Tan, YL Chua, YS Tan, YK Sin, CH Lim, T Chua, et al. (2004). Ex vivo differentiation of human adult bone marrow stem cells into cardiomyocytelike cells. Biochem Biophys Res Commun 324:481-488.
24. Kawai T, T Takahashi, M Esaki, H Ushikoshi, S Nagano, H Fujiwara and K Kosai. (2004). Efficient cardiomyogenic differentiation of embryonic stem cell by fibroblast growth factor 2 and bone morphogenetic protein 2. Circ J 68:691-702.
25. Yuasa S, Y Itabashi, U Koshimizu, T Tanaka, K Sugimura, M Kinoshita, F Hattori, S Fukami, T Shimazaki, S Ogawa, H Okano and K Fukuda. (2005). Transient inhibition of BMP signaling by Noggin induces cardiomyocyte differentiation of mouse embryonic stem cells. Nat Biotechnol 23:607-611.
26. Paquin J, BA Danalache, M Jankowski, SM McCann and J Gutkowska. (2002). Oxytocin induces differentiation of P19 embryonic stem cells to cardiomyocytes. Proc Natl Acad Sci U S A 99:9550-9555.
27. Just L, A Kursten, T Borth-Bruhns, W Lindenmaier, M Rohde, K Dittmar and A Bader. (2006). Formation of threedimensional fetal myocardial tissue cultures from rat for long-Term cultivation. Dev Dyn 235:2200-2209.
28. Cristofalo VJ, RG Allen, RJ Pignolo, BG Martin and JC Beck. (1998). Relationship between donor age and the replicative lifespan of human cells in culture: A reevaluation. Proc Natl Acad Sci U S A 95:10614-10619.
29. Pfaffl MW. (2001). A new mathematical model for relative quantification in real-Time RT-PCR. Nucleic Acids Res 29:e45.
30. Eckle T, A Grenz, D Kohler, A Redel, M Falk, B Rolauffs, H Osswald, F Kehl and HK Eltzschig. (2006). Systematic evaluation of a novel model for cardiac ischemic preconditioning in mice. Am J Physiol Heart Circ Physiol 291:H2533-H2540.
31. Schafer R, M Ayturan, R Bantleon, R Kehlbach, G Siegel, J Pintaske, S Conrad, H Wolburg, H Northoff, J Wiskirchen and R Weissert. (2008). The use of clinically approved small particles of iron oxide (SPIO) for labeling of mesenchymal stem cells aggravates clinical symptoms in experimental autoimmune encephalomyelitis and influences their in vivo distribution. Cell Transplant 17:923-941.
32. Hattan N, H Kawaguchi, K Ando, E Kuwabara, J Fujita, M Murata, M Suematsu, H Mori and K Fukuda. (2005). Purified cardiomyocytes from bone marrow mesenchymal stem cells produce stable intracardiac grafts in mice. Cardiovasc Res 65:334-344.
33. Fukuda K. (2001). Development of regenerative cardiomyocytes from mesenchymal stem cells for cardiovascular tissue engineering. Artif Organs 25:187-193.
34. Hakuno D, K Fukuda, S Makino, F Konishi, Y Tomita, T Manabe, Y Suzuki, A Umezawa and S Ogawa. (2002). Bone marrow-derived regenerated cardiomyocytes (CMG cells) express functional adrenergic and muscarinic receptors. Circulation 105:380-386.
35. Heng BC, H Haider, EK Sim, T Cao and SC Ng. (2004). Strategies for directing the differentiation of stem cells into the cardiomyogenic lineage in vitro. Cardiovasc Res 62:34-42.
36. Makino S, K Fukuda, S Miyoshi, F Konishi, H Kodama, J Pan, M Sano, T Takahashi, S Hori, et al. (1999). Cardiomyocytes can be generated from marrow stromal cells in vitro. J Clin Invest 103:697-705.
37. Mazhari R and JM Hare. (2007). Mechanisms of action of mesenchymal stem cells in cardiac repair: potential influences on the cardiac stem cell niche. Nat Clin Pract Cardiovasc Med 4 (Suppl. 1):S21-S26.
38. Toma C, MF Pittenger, KS Cahill, BJ Byrne and PD Kessler. (2002). Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 105:93-98.
39. Mohanty S, S Bose, KG Jain, B Bhargava and B Airan. (2011). TGFbeta1 contributes to cardiomyogenic-like differentiation of human bone marrow mesenchymal stem cells. Int J Cardiol [Epub ahead of print]; DOI: 10.1016/j.ijcardiol.2011 .08.003.
40. Kim MH, M Kino-oka, N Maruyama, A Saito, Y Sawa and M Taya. (2010). Cardiomyogenic induction of human mesenchymal stem cells by altered Rho family GTPase expression on dendrimer-immobilized surface with D-glucose display. Biomaterials 31:7666-7677.
41. Labovsky V, EL Hofer, L Feldman, V Fernandez Vallone, H Garcia Rivello, A Bayes-Genis, A Hernando Insua, MJ Levin and NA Chasseing. (2010). Cardiomyogenic differentiation of human bone marrow mesenchymal cells: Role of cardiac extract from neonatal rat cardiomyocytes. Differentiation 79:93-101.
42. Schittini AV, PF Celedon, MA Stimamiglio, M Krieger, P Hansen, FD da Costa, S Goldenberg, B Dallagiovanna and A Correa. (2010). Human cardiac explant-conditioned medium: soluble factors and cardiomyogenic effect on mesenchymal stem cells. Exp Biol Med (Maywood) 235:1015-1024.
43. Koninckx R, K Hensen, A Daniels, M Moreels, I Lambrichts, H Jongen, C Clijsters, U Mees, P Steels, M Hendrikx and JL Rummens. (2009). Human bone marrow stem cells cocultured with neonatal rat cardiomyocytes display limited cardiomyogenic plasticity. Cytotherapy 11:778-792.
44. Balana B, C Nicoletti, I Zahanich, EM Graf, T Christ, S Boxberger and U Ravens. (2006). 5-Azacytidine induces changes in electrophysiological properties of human mesenchymal stem cells. Cell Res 16:949-960.
45. Yoon J, WJ Shim, YM Ro and DS Lim. (2005). Transdifferentiation of mesenchymal stem cells into cardiomyocytes by direct cell-To-cell contact with neonatal cardiomyocyte but not adult cardiomyocytes. Ann Hematol 84:715-721.
46. Bayes-Genis A, S Roura, C Soler-Botija, J Farre, L Hove-Madsen, A Llach and J Cinca. (2005). Identification of cardiomyogenic lineage markers in untreated human bone marrow-derived mesenchymal stem cells. Transplant Proc 37:4077-4079.
47. Seib FP, M Franke, D Jing, C Werner and M Bornhauser. (2009). Endogenous bone morphogenetic proteins in human bone marrow-derived multipotent mesenchymal stromal cells. Eur J Cell Biol 88:257-271.
48. Behfar A, S Yamada, R Crespo-Diaz, JJ Nesbitt, LA Rowe, C Perez-Terzic, V Gaussin, C Homsy, J Bartunek and A Terzic. (2010). Guided cardiopoiesis enhances therapeutic benefit of bone marrow human mesenchymal stem cells in chronic myocardial infarction. J Am Coll Cardiol 56:721-734.
49. Yoon YS, JS Park, T Tkebuchava, C Luedeman and DW Losordo. (2004). Unexpected severe calcification after transplantation of bone marrow cells in acute myocardial infarction. Circulation 109:3154-3157.
50. Brand T. (2003). Heart development: Molecular insights into cardiac specification and early morphogenesis. Dev Biol 258:1-19.
51. Ladd AN, TA Yatskievych and PB Antin. (1998). Regulation of avian cardiac myogenesis by activin/TGFbeta and bone morphogenetic proteins. Dev Biol 204:407-419.
52. Valenzuela DM, AN Economides, E Rojas, TM Lamb, L Nunez, P Jones, NY Lp, R Espinosa 3rd, CI Brannan and DJ Gilbert. (1995). Identification of mammalian noggin and its expression in the adult nervous system. J Neurosci 15:6077-6084.
53. Rifas L. (2007). The role of noggin in human mesenchymal stem cell differentiation. J Cell Biochem 100:824-834.
54. Rota M, J Kajstura, T Hosoda, C Bearzi, S Vitale, G Esposito, G Iaffaldano, ME Padin-Iruegas, A Gonzalez, et al. (2007). Bone marrow cells adopt the cardiomyogenic fate in vivo. Proc Natl Acad Sci U S A 104:17783-17788.
55. Psaltis PJ, AC Zannettino, SG Worthley and S Gronthos. (2008). Concise review: Mesenchymal stromal cells: potential for cardiovascular repair. Stem Cells 26:2201-2210.
56. Schafer R, M Dominici, I Muller, F Dazzi, K Bieback, K Godthardt, KL Blanc, R Meisel, R Pochampally, et al. (2007). Progress in characterization, preparation and clinical applications of non-hematopoietic stem cells, 29-30 September 2006, Tubingen, Germany. Cytotherapy 9:397-405.
57. Pittenger MF and BJ Martin. (2004). Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res 95:9-20.
58. Ulloa-Montoya F, BL Kidder, KA Pauwelyn, LG Chase, A Luttun, A Crabbe, M Geraerts, AA Sharov, Y Piao, MS Ko, WS Hu and CM Verfaillie. (2007). Comparative transcriptome analysis of embryonic and adult stem cells with extended and limited differentiation capacity. Genome Biol 8:R163.