A three-dimensional gel bioreactor for assessment of cardiomyocyte induction in skeletal muscle-derived stem cells

Tissue Engineering - Part C: Methods

Volumn 16, Issue 3, 2010, Pages 375-385

  Clause, Kelly C ^a,b   Tinney, Joseph P ^a,c   Liu, Li J ^a,c   Gharaibeh, Burhan ^c   Huard, Johnny ^c   Kirk, Jonathan A ^b   Shroff, Sanjeev G ^b   Fujimoto, Kazuro L ^d   Wagner, William R ^b,d   Ralphe, John C ^a,c   Keller, Bradley B ^a,b,c   Tobita, Kimimasa ^a,b,c  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b University of Pittsburgh   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOREACTORS; CALCIUM; CELL CULTURE; COLLAGEN; GELS; HEART; STEM CELLS; THREE DIMENSIONAL;

3-D CULTURE SYSTEM; BEAT FREQUENCY; CARDIAC CELL; CARDIAC TISSUES; CARDIOMYOCYTES; COLLAGEN GELS; CONTRACTILE FORCE; IN-VITRO; INTRACELLULAR CALCIUM; LEG MUSCLES; MATRIX; PAPILLARY MUSCLE; RAT TAIL COLLAGEN; SKELETAL MUSCLE; TROPONIN;

MUSCLE;

RATTUS;

CALCIUM; COLLAGEN; PRIMER DNA;

ANIMAL; ARTICLE; BIOREACTOR; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; HEART MUSCLE; LEWIS RAT; METABOLISM; NEWBORN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; RAT; SKELETAL MUSCLE; STEM CELL; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; BASE SEQUENCE; BIOREACTORS; BLOTTING, WESTERN; CALCIUM; CELL DIFFERENTIATION; CELLS, CULTURED; COLLAGEN; DNA PRIMERS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MUSCLE, SKELETAL; MYOCARDIUM; POLYMERASE CHAIN REACTION; RATS; RATS, INBRED LEW; STEM CELLS;

EID: 77952923937     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2009.0098     Document Type: Article

References (48)

1. Dimmeler, S., Zeiher, A.M., and Schneider, M.D. Unchain my heart: the scientific foundations of cardiac repair. J Clin Investig 115, 572, 2005.
2. Dowell, J.D., Rubart, M., Pasumarthi, K.B., Soonpaa, M.H., and Field, L.J. Myocyte and myogenic stem cell transplantation in the heart. Cardiovasc Res 58, 336, 2003.
3. Roell, W., Lu, Z.J., Bloch, W., Siedner, S., Tiemann, K., Xia, Y., Stoecker, E., Fleischmann, M., Bohlen, H., Stehle, R., Kolossov, E., Brem, G., Addicks, K., Pfitzer, G., Welz, A., Hescheler, J., and Fleischmann, B.K. Cellular cardiomyo-plasty improves survival after myocardial injury. Circulation 105, 2435, 2002.
4. Christoforou, N., and Gearhart, J.D. Stem cells and their potential in cell-based cardiac therapies. Prog Cardiovasc Dis 49, 396, 2007.
5. Rota, M., Kajstura, J., Hosoda, T., Bearzi, C., Vitale, S., Esposito, G., Iaffaldano, G., Padin-Iruegas, M.E., Gonzalex, A., Rizzi, R., Small, N., Muraski, J., Alvarez, R., Chen, X., Urbanek, K., Bolli, R., Houser, S.R., Leri, A., Sussman, M.A., and Anversa, P. Bone marrow cells adopt the cardiomyo-genic fate in vivo. PNAS 104, 17783, 2007.
6. Ott, H.C., Davis, B.H., and Taylor, D.A. Cell therapy for heart failure\muscle, bone marrow, blood, and cardiac-derived stem cells. Semin Thorac Cardiovasc Surg 17, 348, 2005.
7. Tossios, P., Muller-Ehmsen, J., Schmidt, M., Scheid, C., Unal, N., Moka, D., Schwinger, R.H., and Mehlhorn, U. No evidence of myocardial restoration following transplantation of mononuclear bone marrow cells in coronary bypass grafting surgery patients based upon cardiac SPECT and 18F-PET. BMC Med Imaging 6, 7, 2006.
8. Okada, M., Payne, T.R., Bo, Z., Oshima, H., Momoi, N., To-bita, K., Keller, B.B., Peault, B., and Huard, J. Identification of a novel progenitor cell population in human skeletal muscle with a superior ability for myocardial repair in comparison to commited skeletal myoblast. JACC 52, 1869, 2008.
9. Kolossov, E., Bostani, T., Roell, W., Breitbach, M., Pillekamp, F., Nygren, J.M., Sasse, P., Rubenchik, O., Fries, J.W., Wenzel, D., Geisen, C., Xia, Y., Lu, Z., Duan, Y., Kettenho-fen, R., Jovinge, S., Bloch, W., Bohlen, H., Welz, A., He-scheler, J., Jacobsen, S.E., and Fleischmann, B.K. Engraftment of engineered ES cell-derived cardiomyocytes but not BM cells restores contractile function to the infarcted myocardium. J Exp Med 203, 2315, 2006.
10. Peng, H., and Huard, J. Muscle-derived stem cells for mus-culoskeletal tissue regeneration and repair. Transplant Immunol 12, 311, 2004.
11. Lee, J.Y., Qu-Petersen, Z., Cao, B., Kimura, S., Jankowski, R., Cummins, J., Usas, A., Gates, C., Robbins, P., Wernig, A., and Huard, J. Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing. J Cell Biol 150, 1085, 2000.
12. Jankowski, R.J., Haluszczak, C., Trucco, M., and Huard, J. Flow cytometric characterization of myogenic cell populations obtained via the preplate technique: potential for rapid isolation of muscle-derived stem cells. Hum Gene Ther 12, 619, 2001.
13. Zheng, B., Cao, B., Crisan, M., Sun, B., Li, G., Logar, A., Yap, S., Pollett, J.B., Drowley, L., Cassino, T., Gharaibeh, B., Deasy, B.M., Huard, J., and Péault, B. Prospective identification of myogenic endothelial cells in human skeletal muscle. Nat Biotechnol 25, 1025, 2007.
14. Oshima, H., Payne, T.R., Urish, K.L., Sakai, T., Ling, Y., Gharaibeh, B., Tobita, K., Keller, B.B., Cummins, J.H., and Huard, J. Differential myocardial infarct repair with muscle stem cells compared to myoblasts. Mol Ther 12, 1130, 2005.
15. Zuba-Surma, E.K., Abdel-Latif, A., Case, J., Tiwari, S., Hunt, G., Kucia, M., Vincent, R.J., Ranjan, S., Ratajszak, M.Z., Srour, E.F., Bolli, R., and Dawn, B. Sac-1 expression is associated with decreased cardiomyogenic differentiation potential of skeletal muscle-derived adult primitive cells. JMCC 41, 650, 2006.
16. Winitsky, S.O., Gopal, T.V., Hassanzadeh, S., Takahashi, H., Gryder, D., Rogawski, M.A., Takeda, K., Yu, Z.X., Xu, Y.H., and Epstein, N.D. Adult murine skeletal muscle contains cells that can differentiate into beating cardiomyocytes in vitro. PLoS Biol 3, e87, 2005.
17. Invernici, G., Cristini, S., Madeddu, P., Brock, S., Spillmann, F., Bernasconi, P., Cappelletti, C., Calatozzolo, C., Fascio, U., Bisleri, G., Muneretto, C., Alessandri, G., and Parati, E.A. Human adult skeletal muscle stem cells differentiate into cardiomyocyte phenotype in vitro. Exp Cell Res 314, 366, 2008.
18. Tamaki, T., Akatsuka, A., Okada, Y., Uchiyama, Y., Tono, K., Wada, M., Hoshi, A., Iwaguro, H., Iwasaki, H., Oyamada, A., and Asahara, T. Cardiomyocyte formation by skeletal muscle-derived multi-myogenic stem cells after transplantation into infarcted myocardium. PLoS ONE 3, e1789, 2008.
19. Arsic, N., Mamaeva, D., Lamb, N.J., and Fernandez, A. Muscle-derived stem cells isolated as non-adherent population give rise to cardiac, skeletal muscle and neural lineages. Exp Cell Res 314, 1266, 2008.
20. Payne, T.R., Oshima, H., Okada, M., Momoi, N., Tobita, K., Keller, B.B., Peng, H., and Huard, J. A relationship between VEGF, angiogenesis, and cardiac repair after muscle stem cell transplantation into ischemic hearts. JACC 23, 1677, 2007.
21. Steinberg, M.S. Reconstruction of tissues by dissociated cells. Science 141, 401, 1963.
22. Akins, R.E., Gratton, K., Quezada, E., Rutter, H., Tsuda, T., and Soteropoulos, P. Gene expression profile of bioreactor-cultured cardiac cells: activation of morphogenetic pathways for tissue engineering. DNA Cell Biol 26, 425, 2007.
23. Anderson, P.A., Muller-Borer, B.J., Esch, G.L., Coleman, W.B., Grisham, J.W., and Malouf, N.N. Calcium signals induce liver stem cells to acquire a cardiac phenotype. Cell Cycle 6, 1565, 2007.
24. Dertinger, H., and Hulser, D.F. Intercellular communication in spheroids. In: Acker, H., Carlsson, J., Durand, R., and Sutherland, R.M., eds. Spheroids in Cancer Research: Methods and Perspectives. Berlin: Springer-Verlag, 1984, pp. 67-83.
25. Carpenedo, R.L., Sargent, C.Y., and McDevitt, T.C. Rotary suspension culture enhances the efficiency, yield, and homogeneity of embryoid body differentiation. Stem Cells 25, 2224, 2007.
26. Watzka, S.B., Lucien, J., Shimada, M., Edwards, V., Yeger, H., Hannigan, G., and Coles, J.G. Selection of viable cardi-omyocytes for cell transplantation using three-dimensional tissue culture. Transplantation 70, 1310, 2000.
27. Zimmermann, W.H., Didie, M., Doker, S., Melnychenko, I., Naito, H., Rogge, C., Tiburcy, M., and Eschenhagen, T. Heart muscle engineering: an update on cardiac muscle replacement therapy. Cardiovasc Res 71, 419, 2006.
28. Zimmermann, W.H., Melnychenko, I., Wasmeier, G., Didié, M., Naito, H., Nixdorff, U., Hess, A., Budinsky, L., Brune, K., Michaelis, B., Dhein, S., Schwoerer, A., Ehmke, H., and Eschenhagen, T. Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med 12, 452, 2006.
29. Jankowski, R.J., Deasy, B.M., and Huard, J. Muscle-derived stem cells. Gene Ther 9, 642, 2002.
30. Deasy, B.M., Gharaibeh, B., Pollett, J.B., Jones, M.M., Lucas, M.A., Kanda, Y., and Huard, J. Long-term self-renewal of postnatal muscle-derived Stem cells. Mol Bio Cell 16, 3323, 2005.
31. Gharaibeh, B., Lu, A., Tebbets, J., Zheng, B., Feduska, J., Crisan, M., Peault, B., Cummins, J., and Huard, J. Isolation of a slowly adhering cell fraction containing stem cells from murine skeletal muscle by the preplate technique. Nat Prot 3, 1501, 2008.
32. Tobita, K., Liu, L.J., Janczewski, A.M., Tinney, J.P., None-maker, J.M., Augustine, S., Stolz, D.B., Shroff, S.G., and Keller, B.B. Engineered early embryonic cardiac tissue (EEECT) retains proliferative and contractile properties of developing embryonic myocardium. Am J Physiol Heart Circ Physiol 291, H1829, 2006.
33. Penefsky, Z.J., Wolfe, J., Greengard, O., and Bernstein, J. Mechanical responses of developing Fisher rat heart. Effects of steroid hormone. J Dev Physiol 8, 333, 1986.
34. Liu, J., Fu, J.D., Siu, C.W., and Li, R.A. Functional sarco-plasmic reticulum for calcium handling of human embryonic stem cell-derived cardiomyocytes: insights for driven maturation. Stem Cells 25, 3038, 2007.
35. Iijima, Y., Nagai, T., Mizukami, M., Matsuura, K., Ogura, T., Wada, H., Toko, H., Akazawa, H., Takano, H., Nakaya, H., and Komuro, I. Beating is necessary for transdifferentiation of skeletal muscle-derived cells into cardiomyocytes. FASEB J 17, 1361, 2003.
36. Rudy-Reil, D., and Lough, J. Avian precardiac endoderm= mesoderm induces cardiac myocyte differentiation in mu-rine embryonic stem cells. Circ Res 94, e107, 2004.
37. Hansen, L.K., Hsiao, C., Friend, J.R., Wu, F.J., Bridge, G.A., Remmel, R.P., Cerra, F.B., and Hu, W. Enhanced morphology and function in hepatocyte spheroids: a model of tissue self-assembly. Tissue Eng 4, 65, 1998.
38. Albrecht, D.R., Underhill, G.H., Wassermann, T.B., Sah, R.L., and Bhatia, S.N. Probing the role of multicellular organization in three-dimensional microenvironments. Nat Methods 3, 369, 2006.
39. Suenaga, H., Furukawa, K.S., Ushida, T., Takato, T., and Tateishi, T. Aggregate formation of bone marrow stromal cells by rotation culture. Mat Sci Eng C24, 421, 2004.
40. Kehat, I., Kenyagin-Karsenti, D., Snir, M., Segev, H., Amit, M., Gepstein, A., Livne, E., Binah, O., Itskovitz-Eldor, J., and Gepstein, L. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest 108, 407, 2001.
41. Zimmermann, W.H., Schneiderbanger, K., Schubert, P., Di-die, M., Munzel, F., Heubach, J.F., Kostin, S., Neuhuber, W.L., and Eschenhagen, T. Tissue engineering of a differentiated cardiac muscle construct. Circ Res 8, 223, 2002.
42. Bursac, N., Papadaki, M., White, J.A., Eisenberg, S.R., Vunjak-Novakovic, G., and Freed, L.E. Cultivation in rotating bioreactors promotes maintenance of cardiac myocyte electrophysiology and molecular properties. Tissue Eng 9, 1243, 2003.
43. Panorchan, P., Lee, J.S.H., Kole, T.P., Tseng, Y., and Wirtz, D. Microrheology and ROCK signaling of human endothelial cells embedded in a 3D matrix. Biophys J 91, 3499, 2006.
44. 2\+ handling and the role of sarcoplasmic reticulum in the contraction. Stem Cells 24, 236, 2006.
45. Frangogiannis, N.G. The mechanistic basis of infarct healing. Antioxid Redox Signal 8, 1907, 2006.
46. Kastrup, J., Ripa, R.S., Wang, Y., and Jorgensen, E. Myocardial regeneration induced by granulocyte-colony-stimulating factor mobilization of stem cells in patients with acute or chronic ischaemic heart disease: a non-invasive alternative for clinical stem cell therapy? Eur Heart J 27, 2748, 2006.
47. Cognard, C., Rivet-Bastide, M., Constantin, B., and Raymond, G. Progressive predominance of "skeletal'' versus "cardiac'' types of excitation-contraction coupling during in vitro skeletal myogenesis. Eur J Phys 422, 207, 1992.
48. Rose, R.A., Juang, H., Wang, X., Helke, S., Tsoporis, J.N., Gong, N., Keating, S.C.J., Parker, T.G., Backx, P.H., and Keating, A. 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, 2008.