New Muscle for Old Hearts: Engineering Tissue from Pluripotent Stem Cells

Human Gene Therapy

Volumn 26, Issue 5, 2015, Pages 305-311

  Martin, Ulrich ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT STEM CELL; ARTICLE; AUTOLOGOUS STEM CELL TRANSPLANTATION; CARDIOMYOPLASTY; CELL DIFFERENTIATION; CELL EXPANSION; CELL PROLIFERATION; CELL SUBPOPULATION; CELL SURVIVAL; CELL THERAPY; EMBRYONIC STEM CELL; FIBROBLAST; HEART INFARCTION; HEART MUSCLE; HEART MUSCLE CELL; HUMAN; MESENCHYMAL STEM CELL; MYOFIBROBLAST; NONHUMAN; PERICYTE; PLURIPOTENT STEM CELL; SMOOTH MUSCLE FIBER; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING; ANIMAL; BIOLOGICAL THERAPY; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CYTOLOGY; INDUCED PLURIPOTENT STEM CELL; PROCEDURES; TISSUE REGENERATION;

ANIMALS; CELL DIFFERENTIATION; CELL- AND TISSUE-BASED THERAPY; GUIDED TISSUE REGENERATION; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MYOCARDIUM; MYOCYTES, CARDIAC; PLURIPOTENT STEM CELLS; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING;

EID: 84929743979     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2015.022     Document Type: Article

References (68)

1. World Health Organization. The top 10 causes of death. Available from: www.who.int/mediacentre/factsheets/fs310/en/
2. Fisher SA, Brunskill SJ, Doree C, et al. Stem cell therapy for chronic ischaemic heart disease and congestive heart failure. Cochrane Database Syst Rev 2014;4:CD007888.
3. Nowbar AN, Mielewczik M, Karavassilis M, et al. Discrepancies in autologous bone marrow stem cell trials and enhancement of ejection fraction (damascene): weighted regression and meta-analysis. BMJ 2014;348:g2688.
4. Gruh I, Martin U. Transdifferentiation of stem cells: a critical view. Adv Biochem Eng Biotechnol 2009;114:73-106.
5. Davis RL, Weintraub H, Lassar AB. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 1987;51:987-1000.
6. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126:663-676.
7. Ieda M, Fu JD, Delgado-Olguin P, et al. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 2010;142:375-386.
8. Song K, Nam YJ, Luo X, et al. Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature 2012;485:599-604.
9. Protze S, Khattak S, Poulet C, et al. A new approach to transcription factor screening for reprogramming of fibroblasts to cardiomyocyte-like cells. J Mol Cell Cardiol 2012;53:323-332.
10. Chen JX, Krane M, Deutsch MA, et al. Inefficient reprogramming of fibroblasts into cardiomyocytes using Gata4, Mef2c, and Tbx5. Circ Res 2012;111:50-55.
11. Yi BA, Mummery CL, Chien KR. Direct cardiomyocyte reprogramming: a new direction for cardiovascular regenerative medicine. Cold Spring Harb Perspect Med 2013;3:a014050.
12. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131:861-872.
13. Haase A, Olmer R, Schwanke K, et al. Generation of induced pluripotent stem cells from human cord blood. Cell Stem Cell 2009;5:434-441.
14. Lachmann N, Happle C, Ackermann M, et al. Gene correction of human induced pluripotent stem cells repairs the cellular phenotype in pulmonary alveolar proteinosis. Am J Respir Crit Care Med 2014;189:167-182.
15. Schlaeger TM, Daheron L, Brickler TR, et al. A comparison of non-integrating reprogramming methods. Nat Biotechnol 2015;33:58-63.
16. Gaj T, Gersbach CA, Barbas CF III. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 2013;31:397-405.
17. Merkert S, Wunderlich S, Bednarski C, et al. Efficient designer nuclease-based homologous recombination enables direct pcr screening for footprintless targeted human pluripotent stem cells. Stem Cell Reports 2014;2:107-118.
18. Templin C, Zweigerdt R, Schwanke K, et al. Transplantation and tracking of human-induced pluripotent stem cells in a pig model of myocardial infarction: assessment of cell survival, engraftment, and distribution by hybrid single photon emission computed tomography/computed tomography of sodium iodide symporter transgene expression. Circulation 2012;126:430-439.
19. Klug MG, Soonpaa MH, Koh GY, et al. Genetically selected cardiomyocytes from differentiating embryonic stem cells form stable intracardiac grafts. J Clin Invest 1996;98:216-224.
20. Kensah G, Roa Lara A, Dahlmann J, et al. Murine and human pluripotent stem cell-derived cardiac bodies form contractile myocardial tissue in vitro. Eur Heart J 2013;34:1134-1146.
21. Di Stasi A, Tey SK, Dotti G, et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N Engl J Med 2011;365:1673-1683.
22. Olmer R, Haase A, Merkert S, et al. Long term expansion of undifferentiated human iPS and ES cells in suspension culture using a defined medium. Stem Cell Res 2010;5:51-64.
23. Olmer R, Lange A, Selzer S, et al. Suspension culture of human pluripotent stem cells in controlled, stirred bioreactors. Tissue Eng Part C Methods 2012;18:772-784.
24. Burridge PW, Thompson S, Millrod MA, et al. A universal system for highly efficient cardiac differentiation of human induced pluripotent stem cells that eliminates interline variability. PLoS One 2011;6:e18293.
25. Murry CE, Keller G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 2008;132:661-680.
26. Lian X, Zhang J, Azarin SM, et al. Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/β-catenin signaling under fully defined conditions. Nat Protoc 2013;8:162-175.
27. Kempf H, Olmer R, Kropp C, et al. Controlling expansion and cardiomyogenic differentiation of human pluripotent stem cells in scalable suspension culture. Stem Cell Reports 2014;3:1132-1146.
28. Hattori F, Chen H, Yamashita H, et al. Nongenetic method for purifying stem cell-derived cardiomyocytes. Nat Methods 2010;7:61-66.
29. Dubois NC, Craft AM, Sharma P, et al. Sirpa is a specific cell-surface marker for isolating cardiomyocytes derived from human pluripotent stem cells. Nat Biotechnol 2011;29:1011-1018.
30. Tohyama S, Hattori F, Sano M, et al. Distinct metabolic flow enables large-scale purification of mouse and human pluripotent stem cell-derived cardiomyocytes. Cell Stem Cell 2013;12:127-137.
31. Yang X, Pabon L, Murry CE. Engineering adolescence: maturation of human pluripotent stem cell-derived cardiomyocytes. Circ Res 2014;114:511-523.
32. Jung JJ, Husse B, Rimmbach C, et al. Programming and isolation of highly pure physiologically and pharmacologically functional sinus-nodal bodies from pluripotent stem cells. Stem Cell Reports 2014;2:592-605.
33. Dorn T, Goedel A, Lam JT, et al. Direct Nkx2-5 transcriptional repression of Isl1 controls cardiomyocyte subtype identity. Stem Cells 2015;33:1113-1129.
34. Kleger A, Seufferlein T, Malan D, et al. Modulation of calcium-activated potassium channels induces cardiogenesis of pluripotent stem cells and enrichment of pacemakerlike cells. Circulation 2010;122:1823-1836.
35. Prasain N, Lee MR, Vemula S, et al. Differentiation of human pluripotent stem cells to cells similar to cord-blood endothelial colony-forming cells. Nat Biotechnol 2014;32:1151-1157.
36. Wilson HK, Canfield SG, Shusta EV, et al. Concise review: tissue-specific microvascular endothelial cells derived from human pluripotent stem cells. Stem Cells 2014;32:3037-3045.
37. Orlova VV, Van Den Hil FE, Petrus-Reurer S, et al. Generation, expansion and functional analysis of endothelial cells and pericytes derived from human pluripotent stem cells. Nat Protoc 2014;9:1514-1531.
38. Marchand M, Anderson EK, Phadnis SM, et al. Concurrent generation of functional smooth muscle and endothelial cells via a vascular progenitor. Stem Cells Transl Med 2014;3:91-97.
39. Lian X, Bao X, Al-Ahmad A, et al. Efficient differentiation of human pluripotent stem cells to endothelial progenitors via small-molecule activation of Wnt signaling. Stem Cell Reports 2014;3:804-816.
40. Goldsmith EC, Bradshaw AD, Zile MR, et al. Myocardial fibroblast-matrix interactions and potential therapeutic targets. J Mol Cell Cardiol 2014;70:92-99.
41. Jung Y, Bauer G, Nolta JA. Concise review: induced pluripotent stem cell-derived mesenchymal stem cells: progress toward safe clinical products. Stem Cells 2012;30:42-47.
42. Ronen D, Benvenisty N. Genomic stability in reprogramming. Curr Opin Genet Dev 2012;22:444-449.
43. Abyzov A, Mariani J, Palejev D, et al. Somatic copy number mosaicism in human skin revealed by induced pluripotent stem cells. Nature 2012;492:438-442.
44. Travis WD, Brambilla E, Müller-Hermelink K, et al. Pathology and Genetics of Tumours of the Lung, Pleura, Thymus and Heart. IARC Press, Lyon, France. 2004.
45. Reardon S, Cyranoski D. Japan stem-cell trial stirs envy. Nature 2014;513:287-288.
46. Mauritz C, Martens A, Rojas SV, et al. Induced pluripotent stem cell (iPSC)-derived Flk-1 progenitor cells engraft, differentiate, and improve heart function in a mouse model of acute myocardial infarction. Eur Heart J 2011;32:2634-2641.
47. Blin G, Nury D, Stefanovic S, et al. A purified population of multipotent cardiovascular progenitors derived from primate pluripotent stem cells engrafts in postmyocardial infarcted nonhuman primates. J Clin Invest 2010;120:1125-1139.
48. Nunes SS, Song H, Chiang CK, et al. Stem cell-based cardiac tissue engineering. J Cardiovasc Transl Res 2011;4:592-602.
49. Martens A, Rojas SV, Baraki H, et al. Substantial early loss of induced pluripotent stem cells following transplantation in myocardial infarction. Artif Organs 2014;38:978-984.
50. Didie M, Christalla P, Rubart M, et al. Parthenogenetic stem cells for tissue-engineered heart repair. J Clin Invest 2013;123:1285-1298.
51. Van Laake LW, Passier R, Doevendans PA, et al. Human embryonic stem cell-derived cardiomyocytes and cardiac repair in rodents. Circ Res 2008;102:1008-1010.
52. Shiba Y, Fernandes S, Zhu WZ, et al. Human ES-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts. Nature 2012;489:322-325.
53. Gandolfi F, Pennarossa G, Maffei S, et al. Why is it so difficult to derive pluripotent stem cells in domestic ungulates? Reprod Domest Anim 2012;47(Suppl 5):11-17.
54. Ye L, Chang YH, Xiong Q, et al. Cardiac repair in a porcine model of acute myocardial infarction with human induced pluripotent stem cell-derived cardiovascular cells. Cell Stem Cell 2014;15:750-761.
55. Institut National de la Santé et de la Recherche Médicale. Press release (2015): stem cell therapy for heart failure: first implant of cardiac cells derived from human embryonic stem cells. Available from: http://presse-inserm.Fr/en/stemcell-therapy-for-heart-failure-first-implant-of-cardiac-cellsderived-from-human-embryonic-stem-cells/17502/
56. Chong JJ, Yang X, Don CW, et al. Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 2014;510:273-277.
57. Ott HC, Matthiesen TS, Goh SK, et al. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat Med 2008;14:213-221.
58. Andrée B, Bela K, Horvath T, et al. Successful reendothelialization of a perfusable biological vascularized matrix (BioVaM) for the generation of 3D artificial cardiac tissue. Basic Res Cardiol 2014;109:441.
59. Shimizu T, Yamato M, Isoi Y, et al. Fabrication of pulsatile cardiac tissue grafts using a novel 3-dimensional cell sheet manipulation technique and temperature-responsive cell culture surfaces. Circ Res 2002;90:e40.
60. Eschenhagen T, Fink C, Remmers U, et al. Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system. FASEB J 1997;11:683-694.
61. Zimmermann WH, Melnychenko I, Wasmeier G, et al. Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med 2006;12:452-458.
62. Liau B, Christoforou N, Leong KW, et al. Pluripotent stem cell-derived cardiac tissue patch with advanced structure and function. Biomaterials 2011;32:9180-9187.
63. Lian X, Hsiao C, Wilson G, et al. Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling. Proc Natl Acad Sci U S A 2012;109:E1848-E1857.
64. Schaaf S, Shibamiya A, Mewe M, et al. Human engineered heart tissue as a versatile tool in basic research and preclinical toxicology. PLoS One 2011;6:e26397.
65. Zweigerdt R, Gruh I, Martin U. Your heart on a chip: iPSC-based modeling of Barth-syndrome-associated cardiomyopathy. Cell Stem Cell 2014;15:9-11.
66. Tulloch NL, Muskheli V, Razumova MV, et al. Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ Res 2011;109:47-59.
67. Kawamura M, Miyagawa S, Miki K, 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.
68. Dahlmann J, Krause A, Moller L, et al. Fully defined in situ cross-linkable alginate and hyaluronic acid hydrogels for myocardial tissue engineering. Biomaterials 2013;34:940-951.