Human stem cell-based three-dimensional microtissues for advanced cardiac cell therapies

Biomaterials

Volumn 34, Issue 27, 2013, Pages 6339-6354

  Emmert, Maximilian Y ^a,b   Wolint, Petra ^a   Wickboldt, Nadine ^c   Gemayel, Gino ^c   Weber, Benedikt ^a   Brokopp, Chad E ^a   Boni, Alessandro ^c   Falk, Volkmar ^b   Bosman, Alexis ^c   Jaconi, Marisa E ^c   Hoerstrup, Simon P ^a,b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

Cardiac stem cell therapy; Embryonic stem cells; Induced pluripotent stem cells; Mesenchymal stem cells; Three dimensional microtissues

Indexed keywords

ADIPOSE TISSUE-DERIVED MESENCHYMAL STEM CELLS; CARDIAC STEM CELLS; EMBRYONIC STEM CELLS; EXTRACELLULAR MATRIX PRODUCTION; FORMATION CHARACTERISTICS; HUMAN EMBRYONIC STEM CELLS; INDUCED PLURIPOTENT STEM CELLS; MESENCHYMAL STEM CELL;

CELL CULTURE; CELLULAR MANUFACTURING; DROPS; FLOW CYTOMETRY; HEART; STEM CELLS; THREE DIMENSIONAL; THREE DIMENSIONAL COMPUTER GRAPHICS; TISSUE;

SCAFFOLDS (BIOLOGY);

ALPHA ACTININ; ENDOGLIN; HERMES ANTIGEN; STEM CELL FACTOR RECEPTOR; THY 1 ANTIGEN;

ADIPOSE DERIVED STEM CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYONIC STEM CELL; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELL; HISTOCHEMISTRY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; MALE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; THREE DIMENSIONAL MICROTISSUE; TISSUE AND ORGAN PREPARATION AND CULTURE;

CELL DIFFERENTIATION; CELL PROLIFERATION; CELL- AND TISSUE-BASED THERAPY; CELLS, CULTURED; EMBRYONIC STEM CELLS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MESENCHYMAL STROMAL CELLS; MYOCARDIUM; TISSUE ENGINEERING;

EID: 84879104901     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.04.034     Document Type: Article

References (56)

1. Segers V.F., Lee R.T. Stem-cell therapy for cardiac disease. Nature 2008, 451:937-942.
2. Assmus B., Honold J., Schachinger V., Britten M.B., Fischer-Rasokat U., Lehmann R., et al. Transcoronary transplantation of progenitor cells after myocardial infarction. NEngl J Med 2006, 355:1222-1232.
3. Bolli R., Chugh A.R., D'Amario D., Loughran J.H., Stoddard M.F., Ikram S., et al. Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet 2011, 378:1847-1857.
4. Hare J.M., Traverse J.H., Henry T.D., Dib N., Strumpf R.K., Schulman S.P., et al. Arandomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. JAm Coll Cardiol 2009, 54:2277-2286.
5. Makkar R.R., Smith R.R., Cheng K., Malliaras K., Thomson L.E., Berman D., et al. Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 2012, 379:895-904.
6. Williams A.R., Trachtenberg B., Velazquez D.L., McNiece I., Altman P., Rouy D., et al. Intramyocardial stem cell injection in patients with ischemic cardiomyopathy: functional recovery and reverse remodeling. Circ Res 2011, 108:792-796.
7. Wollert K.C., Meyer G.P., Lotz J., Ringes-Lichtenberg S., Lippolt P., Breidenbach C., et al. Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet 2004, 364:141-148.
8. Asahara T., Kawamoto A. Endothelial progenitor cells for postnatal vasculogenesis. Am J Physiol, Cell Physiol 2004, 287:C572-C579.
9. Balsam L.B., Wagers A.J., Christensen J.L., Kofidis T., Weissman I.L., Robbins R.C. Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 2004, 428:668-673.
10. Emmert M.Y., Emmert L.S., Martens A., Ismail I., Schmidt-Richter I., Gawol A., et al. Higher frequencies of BCRP+ cardiac resident cells in ischaemic human myocardium. Eur Heart J 2012 Jun 26, [Epub ahead of print].
11. Haase A., Olmer R., Schwanke K., Wunderlich S., Merkert S., Hess C., et al. Generation of induced pluripotent stem cells from human cord blood. Cell Stem Cell 2009, 5:434-441.
12. Menasche P. Skeletal myoblasts for cardiac repair: Act II?. JAm Coll Cardiol 2008, 52:1881-1883.
13. Oyama T., Nagai T., Wada H., Naito A.T., Matsuura K., Iwanaga K., et al. Cardiac side population cells have a potential to migrate and differentiate into cardiomyocytes invitro and invivo. JCell Biol 2007, 176:329-341.
14. Pfister O., Mouquet F., Jain M., Summer R., Helmes M., Fine A., et al. CD31- but Not CD31+ cardiac side population cells exhibit functional cardiomyogenic differentiation. Circ Res 2005, 97:52-61.
15. Schuleri K.H., Feigenbaum G.S., Centola M., Weiss E.S., Zimmet J.M., Turney J., et al. Autologous mesenchymal stem cells produce reverse remodelling in chronic ischaemic cardiomyopathy. Eur Heart J 2009, 30:2722-2732.
16. Williams A.R., Hare J.M. Mesenchymal stem cells: biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease. Circ Res 2011, 109:923-940.
17. Emmert M.Y., Wolint P., Winklhofer S., Stolzmann P., Cesarovic N., Fleischmann T., et al. Transcatheter based electromechanical mapping guided intramyocardial transplantation and invivo tracking of human stem cell based three dimensional microtissues in the porcine heart. Biomaterials 2013, 34:2428-2441.
18. Kang W.J., Kang H.J., Kim H.S., Chung J.K., Lee M.C., Lee D.S. Tissue distribution of 18F-FDG-labeled peripheral hematopoietic stem cells after intracoronary administration in patients with myocardial infarction. JNucl Med 2006, 47:1295-1301.
19. van der Bogt K.E., Schrepfer S., Yu J., Sheikh A.Y., Hoyt G., Govaert J.A., et al. Comparison of transplantation of adipose tissue- and bone marrow-derived mesenchymal stem cells in the infarcted heart. Transplantation 2009, 87:642-652.
20. Bartosh T.J., Ylostalo J.H., Mohammadipoor A., Bazhanov N., Coble K., Claypool K., et al. Aggregation of human mesenchymal stromal cells (MSCs) into 3D spheroids enhances their antiinflammatory properties. Proc Natl Acad Sci U S A 2010, 107:13724-13729.
21. Frith J.E., Thomson B., Genever P.G. Dynamic three-dimensional culture methods enhance mesenchymal stem cell properties and increase therapeutic potential. Tissue Eng Part C Methods 2010, 16:735-749.
22. Garzoni L.R., Rossi M.I., de Barros A.P., Guarani V., Keramidas M., Balottin L.B., et al. Dissecting coronary angiogenesis: 3D co-culture of cardiomyocytes with endothelial or mesenchymal cells. Exp Cell Res 2009, 315:3406-3418.
23. Kelm J.M., Diaz Sanchez-Bustamante C., Ehler E., Hoerstrup S.P., Djonov V., Ittner L., et al. VEGF profiling and angiogenesis in human microtissues. JBiotechnol 2005, 118:213-229.
24. Kelm J.M., Djonov V., Hoerstrup S.P., Guenter C.I., Ittner L.M., Greve F., et al. Tissue-transplant fusion and vascularization of myocardial microtissues and macrotissues implanted into chicken embryos and rats. Tissue Eng 2006, 12:2541-2553.
25. Kelm J.M., Djonov V., Ittner L.M., Fluri D., Born W., Hoerstrup S.P., et al. Design of custom-shaped vascularized tissues using microtissue spheroids as minimal building units. Tissue Eng 2006, 12:2151-2160.
26. Kelm J.M., Fussenegger M. Microscale tissue engineering using gravity-enforced cell assembly. Trends Biotechnol 2004, 22:195-202.
27. Wang W., Itaka K., Ohba S., Nishiyama N., Chung U.I., Yamasaki Y., et al. 3D spheroid culture system on micropatterned substrates for improved differentiation efficiency of multipotent mesenchymal stem cells. Biomaterials 2009, 30:2705-2715.
28. Kensah G., Roa Lara A., Dahlmann J., Zweigerdt R., Schwanke K., Hegermann J., et al. Murine and human pluripotent stem cell-derived cardiac bodies form contractile myocardial tissue invitro. Eur Heart J 2013, 34(15):1134-1146.
29. Testa U., Pannitteri G., Condorelli G.L. Vascular endothelial growth factors in cardiovascular medicine. JCardiovasc Med (Hagerstown) 2008, 9:1190-1221.
30. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
31. Zuk P.A., Zhu M., Mizuno H., Huang J., Futrell J.W., Katz A.J., et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001, 7:211-228.
32. Bu L., Jiang X., Martin-Puig S., Caron L., Zhu S., Shao Y., et al. Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature 2009, 460:113-117.
33. Unger C., Gao S., Cohen M., Jaconi M., Bergstrom R., Holm F., et al. Immortalized human skin fibroblast feeder cells support growth and maintenance of both human embryonic and induced pluripotent stem cells. Humanit Rep 2009, 24:2567-2581.
34. Chicha L., Feki A., Boni A., Irion O., Hovatta O., Jaconi M. Human pluripotent stem cells differentiated in fully defined medium generate hematopoietic CD34- and CD34+ progenitors with distinct characteristics. PLoS One 2011, 6:e14733.
35. Sommer C.A., Stadtfeld M., Murphy G.J., Hochedlinger K., Kotton D.N., Mostoslavsky G. Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Stem Cells 2009, 27:543-549.
36. Birraux J., Wildhaber B.E., Jond C., Belli D.C., Menzel O. Exvivo hepatocyte gene therapy: increased biosafety protocol for transduction in suspension with lentiviral vectors and immediate transplantation (SLIT). Transplantation 2010, 89:127-129.
37. Bettiol E., Sartiani L., Chicha L., Krause K.H., Cerbai E., Jaconi M.E. Fetal bovine serum enables cardiac differentiation of human embryonic stem cells. Differentiation 2007, 75:669-681.
38. Kelm J.M., Timmins N.E., Brown C.J., Fussenegger M., Nielsen L.K. Method for generation of homogeneous multicellular tumor spheroids applicable to a wide variety of cell types. Biotechnol Bioeng 2003, 83:173-180.
39. Laugwitz K.L., Moretti A., Caron L., Nakano A., Chien K.R. Islet1 cardiovascular progenitors: a single source for heart lineages?. Development 2008, 135:193-205.
40. Moretti A., Caron L., Nakano A., Lam J.T., Bernshausen A., Chen Y., et al. Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 2006, 127:1151-1165.
41. Schachinger V., Erbs S., Elsasser A., Haberbosch W., Hambrecht R., Holschermann H., et al. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. NEngl J Med 2006, 355:1210-1221.
42. Jeevanantham V, Butler M, Saad A, Abdel-Latif A, Zuba-Surma EK, Dawn B. Adult bone marrow cell therapy improves survival and induces long-term improvement in cardiac parameters: a systematic review and meta-analysis. Circulation 126:551-68.
43. Strauer B.E., Steinhoff G. 10 years of intracoronary and intramyocardial bone marrow stem cell therapy of the heart: from the methodological origin to clinical practice. JAm Coll Cardiol 2011, 58:1095-1104.
44. Valina C., Pinkernell K., Song Y.H., Bai X., Sadat S., Campeau R.J., et al. Intracoronary administration of autologous adipose tissue-derived stem cells improves left ventricular function, perfusion, and remodelling after acute myocardial infarction. Eur Heart J 2007, 28:2667-2677.
45. Frantz S. Embryonic stem cell pioneer geron exits field, cuts losses. Nat Biotechnol 2012, 30:12-13.
46. Schwartz S.D., Hubschman J.P., Heilwell G., Franco-Cardenas V., Pan C.K., Ostrick R.M., et al. Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet 2012, 379:713-720.
47. Nakagawa M., Koyanagi M., Tanabe K., Takahashi K., Ichisaka T., Aoi T., et al. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 2008, 26:101-106.
48. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
49. Okita K., Ichisaka T., Yamanaka S. Generation of germline-competent induced pluripotent stem cells. Nature 2007, 448:313-317.
50. Sartiani L., Bettiol E., Stillitano F., Mugelli A., Cerbai E., Jaconi M.E. Developmental changes in cardiomyocytes differentiated from human embryonic stem cells: a molecular and electrophysiological approach. Stem Cells 2007, 25:1136-1144.
51. Bellin M., Marchetto M.C., Gage F.H., Mummery C.L. Induced pluripotent stem cells: the new patient?. Nat Rev Mol Cell Biol 2012, 13:713-726.
52. Mauritz C., Schwanke K., Reppel M., Neef S., Katsirntaki K., Maier L.S., et al. Generation of functional murine cardiac myocytes from induced pluripotent stem cells. Circulation 2008, 118:507-517.
53. Kawamura M., Miyagawa S., Miki K., Saito A., Fukushima S., Higuchi T., et al. Feasibility, safety, and therapeutic efficacy of human induced pluripotent stem cell-derived cardiomyocyte sheets in a porcine ischemic cardiomyopathy model. Circulation 2012, 126:S29-S37.
54. Lister R., Pelizzola M., Kida Y.S., Hawkins R.D., Nery J.R., Hon G., et al. Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 2011, 471:68-73.
55. Ye J., Boyle A., Shih H., Sievers R.E., Zhang Y., Prasad M., et al. Sca-1+ cardiosphere-derived cells are enriched for Isl1-expressing cardiac precursors and improve cardiac function after myocardial injury. PLoS One 2012, 7:e30329.
56. Rust W., Balakrishnan T., Zweigerdt R. Cardiomyocyte enrichment from human embryonic stem cell cultures by selection of ALCAM surface expression. Regen Med 2009, 4:225-237.