Engineered fetal cardiac graft preserves its cardiomyocyte proliferation within postinfarcted myocardium and sustains cardiac function

Tissue Engineering - Part A

Volumn 17, Issue 5-6, 2011, Pages 585-596

  Fujimoto, Kazuro L ^a,b   Clause, Kelly C ^c,d   Liu, Li J ^b,d   Tinney, Joseph P ^e   Verma, Shivam ^d   Wagner, William R ^a,b,c   Keller, Bradley B ^b,e   Tobita, Kimimasa ^b,c,d  

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

^b MCGOWAN INSTITUTE FOR REGENERATIVE MEDICINE   (United States)

^c University of Pittsburgh   (United States)

^d CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^e University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL DEATH; REGRESSION ANALYSIS;

APOPTOSIS RATES; CARDIAC CELL; CARDIAC FUNCTIONS; CARDIAC TISSUES; CARDIOMYOCYTES; CELL TYPES; FUNCTIONAL RECOVERY; LEFT VENTRICLES; PROLIFERATION RATE;

HEART;

RATTUS;

ANGIOGENESIS; ANIMAL; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CYTOLOGY; ECHOGRAPHY; FEMALE; FETAL TISSUE TRANSPLANTATION; FETUS; GRAFT SURVIVAL; HEART; HEART CONTRACTION; HEART FUNCTION TEST; HEART INFARCTION; HEART MUSCLE CELL; HEART TRANSPLANTATION; HEART VENTRICLE; LEWIS RAT; METHODOLOGY; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; TISSUE CULTURE TECHNIQUE; TISSUE ENGINEERING;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; CELL PROLIFERATION; FEMALE; FETAL TISSUE TRANSPLANTATION; FETUS; GRAFT SURVIVAL; HEART; HEART FUNCTION TESTS; HEART TRANSPLANTATION; HEART VENTRICLES; MYOCARDIAL CONTRACTION; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; NEOVASCULARIZATION, PHYSIOLOGIC; RATS; RATS, INBRED LEW; TISSUE CULTURE TECHNIQUES; TISSUE ENGINEERING;

EID: 79952156803     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2010.0259     Document Type: Article

References (50)

1. Soonpaa, M. H., and Field, L. J. Survey of studies examining mammalian cardiomyocyte DNA synthesis. Circ Res 83, 15, 1998.
2. Buja, L. M., and Vela, D. Cardiomyocyte death and renewal in the normal and diseased heart. Cardiovasc Pathol 17, 349, 2008.
3. Keck, B. M., Bennett, L. E., Rosendale, J., Daily, O. P., Novick, R. J., and Hosenpud, J. D. Worldwide thoracic organ transplantation: a report from the UNOS/ISHLT International Registry for Thoracic Organ Transplantation. Clin Transpl 35, 1999.
4. Ailawadi, G., and Kron, I. L. New strategies for surgical management of ischemic cardiomyopathy. Expert Rev Cardiovasc Ther 6, 521, 2008.
5. Dimmeler, S., Zeiher, A. M., and Schneider, M. D. Unchain my heart: the scientific foundations of cardiac repair. J Clin Invest 115, 572, 2005.
6. Al Kindi, A., Ge, Y., Shum-Tim, D., and Chiu, R. C. Cellular cardiomyoplasty: routes of cell delivery and retention. Front Biosci 13, 2421, 2008.
7. Segers, V. F., and Lee, R. T. Stem-cell therapy for cardiac disease. Nature 451, 937, 2008.
8. Laflamme, M. A., and Murry, C. E. Regenerating the heart. Nat Biotechnol 23, 845, 2005.
9. Laflamme, M. A., Chen, K. Y., Naumova, A. V., Muskheli, V., Fugate, J. A., Dupras, S. K., et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25, 1015, 2007.
10. Fujimoto, K. L., Miki, T., Liu, L. J., Hashizume, R., Strom, S. C., Wagner, W. R., et al. Naive rat amnion-derived cell transplantation improved left ventricular function and reduced myocardial scar of postinfarcted heart. Cell Transplant 18, 477, 2009.
11. Fujimoto, K. L., Tobita, K., Merryman, W. D., Guan, J., Momoi, N., Stolz, D. B., et al. An elastic, biodegradable cardiac patch induces contractile smooth muscle and improves cardiac remodeling and function in subacute myocardial infarction. J Am Coll Cardiol 49, 2292, 2007.
12. *). Tissue Eng Part A 16, 3099, 2010.
13. Hamdi, H., Furuta, A., Bellamy, V., Bel, A., Puymirat, E., Peyrard, S., et al. Cell delivery: intramyocardial injections or epicardial deposition? A head-to-head comparison. Ann Thorac Surg 87, 1196, 2009.
14. Huang, C. C., Liao, C. K., Yang, M. J., Chen, C. H., Hwang, S. M., Hung, Y. W., et al. A strategy for fabrication of a threedimensional tissue construct containing uniformly distributed embryoid body-derived cells as a cardiac patch. Biomaterials 31, 6218, 2010.
15. Fedak, P. W. Cardiac progenitor cell sheet regenerates myocardium and renews hope for translation. Cardiovasc Res 87, 8, 2010.
16. Hata, H., Bar, A., Dorfman, S., Vukadinovic, Z., Sawa, Y., Haverich, A., et al. Engineering a novel three-dimensional contractile myocardial patch with cell sheets and decellularised matrix. Eur J Cardiothorac Surg 38, 450, 2010.
17. Wang, F., and Guan, J. Cellular cardiomyoplasty and cardiac tissue engineering for myocardial therapy. Adv Drug Deliv Rev 62, 784, 2010.
18. Shimizu, T., Sekine, H., Yamato, M., and Okano, T. Cell sheet-based myocardial tissue engineering: new hope for damaged heart rescue. Curr Pharm Des 15, 2807, 2009.
19. Hoashi, T., Matsumiya, G., Miyagawa, S., Ichikawa, H., Ueno, T., Ono, M., et al. Skeletal myoblast sheet transplantation improves the diastolic function of a pressure-overloaded right heart. J Thorac Cardiovasc Surg 138, 460, 2009.
20. Stevens, K. R., Pabon, L., Muskheli, V., and Murry, C. E. Scaffold-free human cardiac tissue patch created from embryonic stem cells. Tissue Eng Part A 15, 1211, 2009.
21. Jawad, H., Ali, N. N., Lyon, A. R., Chen, Q. Z., Harding, S. E., and Boccaccini, A. R. Myocardial tissue engineering: a review. J Tissue Eng Regen Med 1, 327, 2007.
22. Zimmermann, W. H., Didie, M., Doker, S., Melnychenko, I., Naito, H., Rogge, C., et al. Heart muscle engineering: an update on cardiac muscle replacement therapy. Cardiovasc Res 71, 419, 2006.
23. Zimmermann, W. H., Melnychenko, I., Wasmeier, G., Didie, M., Naito, H., Nixdorff, U., et al. Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med 12, 452, 2006.
24. Li, R. K., Jia, Z. Q., Weisel, R. D., Mickle, D. A., Choi, A., and Yau, T. M. Survival and function of bioengineered cardiac grafts. Circulation 100, II63, 1999.
25. Lee, E. J., Kim do, E., Azeloglu, E. U., and Costa, K. D. Engineered cardiac organoid chambers: toward a functional biological model ventricle. Tissue Eng Part A 14, 215, 2008.
26. Eschenhagen, T., Fink, C., Remmers, U., Scholz, H., Wattchow, J., Weil, J., et al. Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system. FASEB J 11, 683, 1997.
27. Fink, C., Ergun, S., Kralisch, D., Remmers, U., Weil, J., and Eschenhagen, T. Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement. FASEB J 14, 669, 2000.
28. Naito, H., Melnychenko, I., Didie, M., Schneiderbanger, K., Schubert, P., Rosenkranz, S., et al. Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation 114, I72, 2006.
29. Roell, W., Lu, Z. J., Bloch, W., Siedner, S., Tiemann, K., Xia, Y., et al. Cellular cardiomyoplasty improves survival after myocardial injury. Circulation 105, 2435, 2002.
30. Roell, W., Lewalter, T., Sasse, P., Tallini, Y. N., Choi, B. R., Breitbach, M., et al. Engraftment of connexin 43-expressing cells prevents post-infarct arrhythmia. Nature 450, 819, 2007.
31. 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.
32. Rubart, M., Pasumarthi, K. B., Nakajima, H., Soonpaa, M. H., Nakajima, H. O., and Field, L. J. Physiological coupling of donor and host cardiomyocytes after cellular transplantation. Circ Res 92, 1217, 2003.
33. Koh, G. Y., Soonpaa, M. H., Klug, M. G., Pride, H. P., Cooper, B. J., Zipes, D. P., et al. Stable fetal cardiomyocyte grafts in the hearts of dystrophic mice and dogs. J Clin Invest 96, 2034, 1995.
34. Scorsin, M., Hagege, A., Vilquin, J. T., Fiszman, M., Marotte, F., Samuel, J. L., et al. Comparison of the effects of fetal cardiomyocyte and skeletal myoblast transplantation on postinfarction left ventricular function. J Thorac Cardiovasc Surg 119, 1169, 2000.
35. Leor, J., Patterson, M., Quinones, M. J., Kedes, L. H., and Kloner, R. A. Transplantation of fetal myocardial tissue into the infarcted myocardium of rat. A potential method for repair of infarcted myocardium? Circulation 94, II332, 1996.
36. Leor, J., Aboulafia-Etzion, S., Dar, A., Shapiro, L., Barbash, I. M., Battler, A., et al. Bioengineered cardiac grafts: a new approach to repair the infarcted myocardium? Circulation 102, III56, 2000.
37. Tobita, K., Liu, L. J., Janczewski, A. M., Tinney, J. P., Nonemaker, J. M., Augustine, S., et al. Engineered early embryonic cardiac tissue retains proliferative and contractile properties of developing embryonic myocardium. Am J Physiol Heart Circ Physiol 291, H1829, 2006.
38. Clause, K. C., Tinney, J. P., Liu, L. J., Keller, B. B., and Tobita, K. Engineered early embryonic cardiac tissue increases cardiomyocyte proliferation by cyclic mechanical stretch via p38-MAP kinase phosphorylation. Tissue Eng Part A 15, 1373, 2009.
39. Toyokawa, H., Nakao, A., Stolz, D. B., Romanosky, A. J., Nalesnik, M. A., Neto, J. S., et al. 3D-confocal structural analysis of bone marrow-derived renal tubular cells during renal ischemia/reperfusion injury. Lab Invest 86, 72, 2006.
40. Evans, H. J., Sweet, J. K., Price, R. L., Yost, M., and Goodwin, R. L. Novel 3D culture system for study of cardiac myocyte development. Am J Physiol Heart Circ Physiol 285, H570, 2003.
41. Sedmera, D., Hu, N., Weiss, K. M., Keller, B. B., Denslow, S., and Thompson, R. P. Cellular changes in experimental left heart hypoplasia. Anat Rec 267, 137, 2002.
42. Zimmermann, W. H., Didie, M., Wasmeier, G. H., Nixdorff, U., Hess, A., Melnychenko, I., et al. Cardiac grafting of engineered heart tissue in syngenic rats. Circulation 106, I151, 2002.
43. Saiki, Y., Konig, A., Waddell, J., and Rebeyka, I. M. Hemodynamic alteration by fetal surgery accelerates myocyte proliferation in fetal guinea pig hearts. Surgery 122, 412, 1997.
44. Clark, E. B., Hu, N., Frommelt, P., Vandekieft, G. K., Dummett, J. L., and Tomanek, R. J. Effect of increased pressure on ventricular growth in stage 21 chick embryos. Am J Physiol 257, H55, 1989.
45. Coles, J. G., Boscarino, C., Takahashi, M., Grant, D., Chang, A., Ritter, J., et al. Cardioprotective stress response in the human fetal heart. J Thorac Cardiovasc Surg 129, 1128, 2005.
46. Kleinman, H. K., McGarvey, M. L., Liotta, L. A., Robey, P. G., Tryggvason, K., and Martin, G. R. Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry 21, 6188, 1982.
47. Cheng, M., Moretti, M., Engelmayr, G. C., and Freed, L. E. Insulin-like growth factor-I and slow, bi-directional perfusion enhance the formation of tissue-engineered cardiac grafts. Tissue Eng Part A 15, 645, 2009.
48. Baharvand, H., Azarnia, M., Parivar, K., and Ashtiani, S. K. The effect of extracellular matrix on embryonic stem cellderived cardiomyocytes. J Mol Cell Cardiol 38, 495, 2005.
49. Radisic, M., Marsano, A., Maidhof, R., Wang, Y., and Vunjak-Novakovic, G. Cardiac tissue engineering using perfusion bioreactor systems. Nat Protoc 3, 719, 2008.
50. Clause, K. C., Tinney, J. P., Liu, L. J., Gharaibeh, B., Huard, J., Kirk, J. A., et al. A three-dimensional gel bioreactor for assessment of cardiomyocyte induction in skeletal muscle derived stem cells. Tissue Eng Part C Methods 16, 375, 2009.