Cardiac differentiation of cardiosphere-derived cells in scaffolds mimicking morphology of the cardiac extracellular matrix

Acta Biomaterialia

Volumn 10, Issue 8, 2014, Pages 3449-3462

  Xu, Yanyi ^a   Patnaik, Sourav ^b   Guo, Xiaolei ^a   Li, Zhenqing ^a   Lo, Wilson ^c   Butler, Ryan ^d   Claude, Andrew ^d   Liu, Zhenguo ^e   Zhang, Ge ^f   Liao, Jun ^b   Anderson, Peter M ^a   Guan, Jianjun ^a  

^a The Ohio State University   (United States)

^b MISSISSIPPI STATE UNIVERSITY   (United States)

^c OHIO STATE UNIVERSITY   (United States)

^d MISSISSIPPI STATE UNIVERSITY   (United States)

^e OHIO STATE UNIVERSITY   (United States)

^f University of Akron   (United States)

Author keywords

Cardiac differentiation; Cardiosphere derived cells; Matrix modulus; Stem cell therapy

Indexed keywords

ALIGNMENT; BLENDING; CELL ADHESION; ELECTROSPINNING; FIBERS; GENE EXPRESSION; HEART; SCAFFOLDS (BIOLOGY); TISSUE; VOLUME FRACTION;

CARDIAC DIFFERENTIATION; CARDIOSPHERE-DERIVED CELL; CELL DIFFERENTIATION; EXTRACELLULAR MATRICES; FIBRE ALIGNMENTS; MATRIX MODULUS; MYOCARDIAL INFARCTION; PROPERTY; STEM CELL THERAPY; STEM-CELL;

STEM CELLS;

CALCIUM CHANNEL; CONNEXIN 43; MYOSIN HEAVY CHAIN; MYOSIN HEAVY CHAIN 6; POLYURETHAN; TISSUE SCAFFOLD; TROPONIN I; TROPONIN T; UNCLASSIFIED DRUG; BIOMIMETIC MATERIAL; HYDROGEL;

ANIMAL CELL; ARTICLE; BIOMECHANICS; CARDIAC DIFFERENTIATION; CARDIOSPHERE DERIVED CELL; CELL ADHESION; CELL CULTURE; CELL DIFFERENTIATION; CELL GROWTH; CELL STRUCTURE; CELL SURVIVAL; CELLULAR PARAMETERS; CONTROLLED STUDY; ELECTROSPINNING; ELECTROSPRAY; EXTRACELLULAR MATRIX; FIBER DENSITY; GENE EXPRESSION; HEART MUSCLE CELL; HYDROGEL; IN VITRO STUDY; MOUSE; NANOFABRICATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; STRESS STRAIN RELATIONSHIP; TENSILE STRENGTH; YOUNG MODULUS; ANIMAL; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; MULTICELLULAR SPHEROID; PHYSIOLOGY; PROCEDURES; SYNTHESIS; TISSUE ENGINEERING;

ANIMALS; BIOMIMETIC MATERIALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EXTRACELLULAR MATRIX; HYDROGELS; MICE; MYOCYTES, CARDIAC; SPHEROIDS, CELLULAR; STEM CELLS; TISSUE ENGINEERING;

EID: 84903739720     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.04.018     Document Type: Article

References (64)

1. American Heart Association Heart Disease and Stroke Statistics - 2012 Update 2012 American Heart Association Dallas, TX
2. M.A. Laflamme, and C.E. Murry Heart regeneration Nature 473 2011 326 335
3. F. Wang, and J. Guan Cellular cardiomyoplasty and cardiac tissue engineering for myocardial therapy Adv Drug Deliv Rev 62 2010 784 797
4. J.L. Herrmann, A.M. Abarbanell, B.R. Weil, Y. Wang, M. Wang, and J. Tan et al. Cell-based therapy for ischemic heart disease: a clinical update Ann Thorac Surg 88 5 2009 1714 1722
5. J.S. Forrester, R.R. Makkar, and E. Marbán Long-term outcome of stem cell therapy for acute myocardial infarction: right results, wrong reasons J Am Coll Cardiol 53 2009 2270 2272
6. M.N. Jameel, and J. Zhang Heart failure management: the present and the future Antioxid Redox Signal 11 8 2009 1989 2010
7. H.C. Quevedo, K.E. Hatzistergos, B.N. Oskouei, G.S. Feigenbaum, J.E. Rodriguez, and D. Valdes et al. Allogeneic mesenchymal stem cells restore cardiac function in chronic ischemic cardiomyopathy via trilineage differentiating capacity Proc Natl Acad Sci U S A 106 2009 14022 14027
8. K. Malliaras, and E. Marbán Cardiac cell therapy: where we've been, where we are, and where we should be headed Br Med Bull 98 2011 161 185
9. P.K. Nguyen, D. Nag, and J.C. Wu Methods to assess stem cell lineage, fate and function Adv Drug Deliv Rev 62 12 2010 1175 1186
10. N. Bursac Cardiac tissue engineering using stem cells IEEE Eng Med Biol Mag 28 2009 88 89
11. G. Vunjak-Novakovic, N. Tandon, A. Godier, R. Maidhof, A. Marsano, and T.P. Martens et al. Challenges in cardiac tissue engineering Tissue Eng Part B Rev 16 2 2010 169 187
12. G.M. Fomovsky, J.R. Macadangdang, G. Ailawadi, and J.W. Holmes Model-based design of mechanical therapies for myocardial infarction J Cardiovasc Transl Res 4 1 2011 82 91
13. G.M. Fomovsky, and J.W. Holmes Evolution of scar structure, mechanics, and ventricular function after myocardial infarction in the rat Am J Physiol Heart Circ Physiol 298 1 2010 H221 H228
14. Campbell PH, Hunt DL, Jones Y, Harwood F, Amiel D, Omens JH, McCulloch AD. Effects of biglycan deficiency on myocardial infarct structure and mechanics. Mol Cell Biomech 2008;5(1):27-35.
15. K.L. Herrmann, A.D. McCulloch, and J.H. Omens Glycated collagen cross-linking alters cardiac mechanics in volume-overload hypertrophy Am J Physiol Heart Circ Physiol 284 4 2003 H1277 H1284
16. S.M. Weis, J.L. Emery, K.D. Becker, D.J. McBride Jr, J.H. Omens, and A.D. McCulloch Myocardial mechanics and collagen structure in the osteogenesis imperfecta murine (oim) Circ Res 87 8 2000 663 669
17. J.W. Holmes, T.K. Borg, and J.W. Covell Structure and mechanics of healing myocardial infarcts Annu Rev Biomed Eng 7 2005 223 253
18. K.B. Gupta, M.B. Ratcliffe, M.A. Fallert, L.H. Edmunds Jr, and D.K. Bogen Changes in passive mechanical stiffness of myocardial tissue with aneurysm formation Circulation 89 1994 2315 2326
19. J.W. Holmes, and J.W. Covell Collagen fiber orientation in myocardial scar tissue Cardiovasc Pathobiol 1 1996 15 22
20. J.W. Holmes, J.A. Nunez, and J.W. Covell Functional implications of myocardial scar structure Am J Physiol Heart Circ Physiol 272 1997 H2123 H2130
21. C.M. Connelly, W.M. Vogel, A.W. Wiegner, E.L. Osmers, O.H. Bing, and R.A. Kloner et al. Effects of reperfusion after coronary artery occlusion on post-infarction scar tissue Circ Res 57 1985 562 577
22. P. Whittaker, D.R. Boughner, and R.A. Kloner Analysis of healing after myocardial infarction using polarized light microscopy Am J Pathol 134 1989 879 893
23. P. Whittaker, R.A. Kloner, D.R. Boughner, and J.G. Pickering Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light Basic Res Cardiol 89 1994 397 410
24. M.F. Berry, A.J. Engler, Y.J. Woo, T.J. Pirolli, and L.T. Bish et al. Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance Am J Physiol Heart Circ Physiol 290 2006 H2196 H2203
25. A.J. Engler, S. Sen, H.L. Sweeney, and D.E. Discher Matrix elasticity directs stem cell lineage specification Cell 126 4 2006 677 689
26. J.A. Burdick, and G. Vunjak-Novakovic Engineered microenvironments for controlled stem cell differentiation Tissue Eng Part A 15 2009 205 219
27. D.E. Discher, D.J. Mooney, and P.W. Zandstra Growth factors, matrices, and forces combine and control stem cells Science 324 2009 1673 1677
28. J.P. Winer, P.A. Janmey, M.E. McCormick, and M. Funaki Bone marrow-derived human mesenchymal stem cells become quiescent on soft substrates but remain responsive to chemical or mechanical stimuli Tissue Eng Part A 15 2009 147 154
29. N. Huebsch, P.R. Arany, A.S. Mao, D. Shvartsman, O.A. Ali, and S.A. Bencherif et al. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate Nat Mater 9 2010 518 526
30. J. Guan, F. Wang, Z. Li, J. Chen, X. Guo, and J. Liao et al. The stimulation of the cardiac differentiation of mesenchymal stem cells in tissue constructs that mimic myocardium structure and biomechanics Biomaterials 32 24 2011 5568 5580
31. Z. Li, X. Guo, S. Matsushita, and J. Guan Differentiation of cardiosphere-derived cells into a mature cardiac lineage using biodegradable poly(N-isopropylacrylamide) hydrogels Biomaterials 32 12 2011 3220 3232
32. Z. Li, X. Guo, A.F. Palmer, H. Das, and J. Guan High-efficiency matrix modulus-induced cardiac differentiation of human mesenchymal stem cells inside a thermosensitive hydrogel Acta Biomater 8 10 2012 3586 3595
33. T.P. Kraehenbuehl, P. Zammaretti, A.J.V. der Vlies, R.G. Schoenmakers, M.P. Lutolf, and J.A. Hubbell Three-dimensional extracellular matrix directed cardioprogenitor differentiation: systematic modulation of asynthetic cell-responsive PEG-hydrogel Biomaterials 29 2008 2757 2766
34. G.C. Reilly, and A.J. Engler Intrinsic extracellular matrix properties regulate stem cell differentiation J Biomech 43 1 2010 55 62
35. C. Conrad, H. Niess, R. Huss, S. Huber, I. von Luettichau, and P.J. Nelson et al. Multipotent mesenchymal stem cells acquire a lymphendothelial phenotype and enhance lymphatic regeneration in vivo Circulation 119 2 2009 281 289
36. J.C. Friedland, M.H. Lee, and D. Boettiger Mechanically activated integrin switch controls alpha5beta1 function Science 323 2009 642 644
37. M.M. Martino, M. Mochizuki, D.A. Rothenfluh, S.A. Rempel, J.A. Hubbell, and T.H. Barker Controlling integrin specificity and stem cell differentiation in 2D and 3D environments through regulation of fibronectin domain stability Biomaterials 30 2009 1089 1097
38. A.S. Rowlands, P.A. George, and J.J. Cooper-White Directing osteogenic and myogenic differentiation of MSCs: interplay of stiffness and adhesive ligand presentation Am J Physiol Cell Physiol 295 2008 C1037 C1044
39. M. Yasunaga, S. Tada, S. Torikai-Nishikawa, Y. Nakano, M. Okada, and L.M. Jakt et al. Induction and monitoring of definitive and visceral endoderm differentiation of mouse ES cells Nat Biotechnol 23 2005 1542 1550
40. S.A. Ruiz, and C.S. Chen Emergence of patterned stem cell differentiation within multicellular structures Stem Cells 26 2008 2921 2927
41. M.M. Stevens, and J.H. George Exploring and engineering the cell surface interface Science 310 2005 1135 1138
42. J. Guan, M.S. Sacks, E.J. Beckman, and W.R. Wagner Synthesis, characterization, and cytocompatibility of elastomeric, biodegradable poly(ester-urethane)ureas based on poly(caprolactone) and putrescine J Biomed Mater 61 2002 493 503
43. F. Wang, Z. Li, M. Khan, K. Tamama, P. Kuppusamy, and W.R. Wagner et al. Injectable, rapid gelling and highly flexible hydrogel composites as growth factor and cell carriers Acta Biomater 6 2010 1978 1991
44. Z. Li, F. Wang, S. Roy, C.K. Sen, and J. Guan Injectable, highly flexible, and thermosensitive hydrogels capable of delivering superoxide dismutase Biomacromolecules 10 2009 3306 3316
45. J. Guan, Y. Hong, Z. Ma, and W.R. Wagner Protein-reactive, thermoresponsive copolymers with high flexibility and biodegradability Biomacromolecules 9 2008 1283 1292
46. D.R. Davis, Y. Zhang, R.R. Smith, K. Cheng, J. Terrovitis, and K. Malliaras et al. Validation of the cardiosphere method to culture cardiac progenitor cells from myocardial tissue PLoS One 4 2009 e7195
47. J. Ye, A. Boyle, H. Shih, R.E. Sievers, Y. Zhang, and M. Prasad et al. Sca-1+ cardiosphere-derived cells are enriched for Isl1-expressing cardiac precursors and improve cardiac function after myocardial injury PLoS One 7 2012 e30329
48. L.B. De Souza, S.G. de Aquino, P.P. de Souza, J. Hebling, and C.A. Costa Cytotoxic effects of different concentrations of chlorhexidine Am J Dent 20 2007 400 404
49. O. Ziv-Polat, H. Skaat, and S. Margel Novel magnetic fibrin hydrogel scaffolds containing thrombin and growth factors conjugated iron oxide nanoparticles for tissue engineering Int J Nanomedicine 7 2012 1259 1274
50. J.E. McBane, B. Vulesevic, and E.J. Suuronen Evalustion of collagen-chitosan hydrogel for potential use as a pro-angiogenic site for islet transplantation PLoS One 8 10 2013 e77538
51. H. Huang, Y. Ding, and T.A. Nguyen Peptide hydragelation and cell encapsulation for 3D culture of MCF-7 breast cancer cells PLoS One 8 3 2013 e59482
52. M.S. Sacks Incorporation of experimentally-derived fiber orientation into a structural constitutive model for planar collagenous tissues J Biomed Eng 125 2003 280 287
53. M.S. Sacks A structural constitutive model for chemically treated planar tissues under biaxial loading Comput Mech 26 2000 243 249
54. T.W. Gilbert, F.B. Badylack, M.B. Chancellor, and M.S. Sacks et al. Fiber kinematics of small intestinal submucosa under biaxial and uniaxial stretch J Biomech Eng 128 6 2006 890 898
55. D.R. Davis, Y. Zhang, R.R. Smith, K. Cheng, J. Terrovitis, and K. Malliaras et al. Validation of the cardiosphere method to culture cardiac progenitor cells from myocardial tissue PloS One 4 2009 e7195
56. Real-time Quantitative RT-PCR Design, calculations, and statistics The Plant Cell 21 2009 1031 1033
57. A.S. Badami, M.R. Kreke, M.S. Thompson, J.S. Riffle, and A.S. Goldstein Effect of fiber diameter on spreading, proliferation, and differentiation of osteoblastic cells on electrospun poly(lactic acid) substrates Biomaterials 27 2006 596
58. J. Holst, S. Watson, M.S. Lord, S.S. Eamegdool, D.V. Bax, and L.B. Nivison-Smith et al. Substrate elasticity provides mechanical signals for the expansion of hemopoietic stem and progenitor cells Nat Biotech 28 2010 1123 1128
59. G.C. Engelmayr, M. Cheng, C.J. Bettinger, J.T. Borenstein, R. Langer, and L.E. Freed Accordion-like honeycombs for tissue engineering of cardiac anisotropy Nature Mater. 7 12 2008 1003 1010
60. L.E. McNamara, R.J. McMurray, M.J.P. Biggs, F. Kantawong, R.O.C. Oreffo, and M.J. Dalby Nanotopographical control of stem cell differentiation J Tissue Eng 2010 2010 120623
61. K.A. Beningo, M. Dembo, I. Kaverina, J.V. Small, and Y.L. Wang Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts J. Cell Biol 153 2001 881 888
62. J.R. Venugopal, M.P. Prabhakaran, S. Mukherjee, R. Ravichandran, K. Dan, and S. Ramakrishna Biomaterial strategies for alleviation of myocardial infarction J R Soc Interface 9 2012 1 19
63. Z. Li, X. Guo, and J. Guan An oxygen release system to augment cardiac progenitor cell survival and differentiation under hypoxic condition Biomaterials 33 25 2012 5914 5923
64. F. Guilak, D.M. Cohen, B.T. Estes, J.M. Gimble, W. Liedtke, and C.S. Chen Control of stem cell fate by physical interactions with the extracellular matrix Cell Stem Cell 5 1 2009 17 26