Advertisement

Cell and Tissue Research

, Volume 353, Issue 3, pp 443–456 | Cite as

Enhanced cardiomyogenic lineage differentiation of adult bone-marrow-derived stem cells grown on cardiogel

  • P. Sreejit
  • R. S. VermaEmail author
Regular Article

Abstract

The extracellular matrix (ECM) and its components are known to promote growth and cellular differentiation in vitro. Cardiogel, a three-dimensional extracellular matrix derived from cardiac fibroblasts, is evaluated for its cardiomyogenic-differentiation-inducing potential on bone-marrow-derived stem cells (BMSC). BMSC from adult mice were grown on cardiogel and induced to differentiate into specific lineages that were validated by morphological, phenotypic and molecular assays. The data revealed that the cardiogel enhanced cardiomyogenic and adipogenic differentiation and relegated osteogenic differentiation following specific induction. More importantly, increased cardiomyogenic differentiation was also observed following BMSC growth on cardiogel without specific chemical (5-azacytidine) induction. This is the first report of an attempt to use cardiogel as a biomaterial on which to achieve cardiomyogenic differentiation of BMSC without chemical induction. Our study suggests that cardiogel is an efficient extracellular matrix that enhances the cardiomyogenic differentiation of BMSC and that it can therefore be used as a scaffold for cardiac tissue regeneration.

Keywords

Stem cells Differentiation Cardiogel Cardiomyogenic induction Mouse 

Supplementary material

441_2013_1661_Fig5_ESM.jpg (33 kb)
Fig. S1

(JPEG 32 kb)

441_2013_1661_MOESM1_ESM.tiff (7.1 mb)
High Resolution Image (TIFF 7221 kb)
441_2013_1661_Fig6_ESM.jpg (84 kb)
Fig. S2

(JPEG 84 kb)

441_2013_1661_MOESM2_ESM.tiff (6.9 mb)
High Resolution Image (TIFF 7112 kb)
441_2013_1661_Fig7_ESM.jpg (76 kb)
Fig. S3

(JPEG 75 kb)

441_2013_1661_MOESM3_ESM.tif (5.4 mb)
High Resolution Image (TIFF 5556 kb)
441_2013_1661_Fig8_ESM.jpg (17 kb)
Fig. S4

(JPEG 16 kb)

441_2013_1661_MOESM4_ESM.tif (1.5 mb)
High Resolution Image (TIFF 1497 kb)
441_2013_1661_Fig9_ESM.jpg (47 kb)
Fig. S5

(JPEG 47 kb)

441_2013_1661_MOESM5_ESM.tif (2.3 mb)
High Resolution Image (TIFF 2357 kb)
441_2013_1661_Fig10_ESM.jpg (78 kb)
Fig. S6

(JPEG 77 kb)

441_2013_1661_MOESM6_ESM.tif (4.4 mb)
High Resolution Image (TIFF 4539 kb)
441_2013_1661_Fig11_ESM.jpg (21 kb)
Fig. S7

(JPEG 21 kb)

441_2013_1661_MOESM7_ESM.tif (1.4 mb)
High Resolution Image (TIFF 1407 kb)
441_2013_1661_Fig12_ESM.jpg (54 kb)
Fig. S8

(JPEG 53 kb)

441_2013_1661_MOESM8_ESM.tif (3.2 mb)
High Resolution Image (TIFF 3231 kb)
441_2013_1661_MOESM9_ESM.pdf (61 kb)
Table S1 (PDF 61 kb)
441_2013_1661_MOESM10_ESM.pdf (78 kb)
Table S2 (PDF 77 kb)
441_2013_1661_MOESM11_ESM.pdf (59 kb)
Table S3 (PDF 58 kb)
441_2013_1661_MOESM12_ESM.doc (128 kb)
ESM (DOC 127 kb)

References

  1. Abbate A, Biondi-Zoccai GGL, Van Tassell BW, Baldi A (2009) Cellular preservation therapy in acute myocardial infarction. Am J Physiol Heart Circ Physiol 296:H563–H565PubMedCrossRefGoogle Scholar
  2. Adler ED, Chen VC, Bystrup A, Kaplan AD, Giovannone S, Briley-Saebo K, Young W, Kattman S, Mani V, Laflamme M, Zhu W-Z, Fayad Z, Keller G (2010) The cardiomyocyte lineage is critical for optimization of stem cell therapy in a mouse model of myocardial infarction. FASEB J 24:1073–1081PubMedCrossRefGoogle Scholar
  3. Baharvand H, Azarnia M, Parivar K, Ashtiani SK (2005) The effect of extracellular matrix on embryonic stem cell-derived cardiomyocytes. J Mol Cell Cardiol 38:495–503PubMedCrossRefGoogle Scholar
  4. Bettiol E, Clement S, Krause KH, Jaconi ME (2007) Embryonic and adult stem cell-derived cardiomyocytes: lessons from in vitro models. Rev Physiol Biochem Pharmacol 157:1–30Google Scholar
  5. Bick RJ, Snuggs MB, Poindexter BJ, Buja LM, Van Winkle WB (1998) Physical, contractile and calcium handling properties of neonatal cardiac myocytes cultured on different matrices. Cell Commun Adhes 6:301–310CrossRefGoogle Scholar
  6. Burdick JA, Vunjak-Novakovic G (2009) Engineered microenvironments for controlled stem cell differentiation. Tissue Eng A 15:205–219CrossRefGoogle Scholar
  7. Castells-Sala C, Semino CE (2012) Biomaterials for stem cell culture and seeding for the generation and delivery of cardiac myocytes. Curr Opin Organ Transplant 17:681–687PubMedCrossRefGoogle Scholar
  8. Chang W, Lim S, Song H, Lee S, Song B-W, Jang Y, Chung N, Hwang K-C (2007) In vitro expansion of mesenchymal stem cells using 3-D matrix derived from cardiac fibroblast. Tissue Eng Regen Med 4:370–375Google Scholar
  9. Chen Q-Z, Harding SE, Ali NN, Lyon AR, Boccaccini AR (2008) Biomaterials in cardiac tissue engineering: ten years of research survey. Mater Sci Eng R-Rep 59:1–37CrossRefGoogle Scholar
  10. Choi S-C, Shim W-J, Lim D-S (2008) Specific monitoring of cardiomyogenic and endothelial differentiation by dual promoter-driven reporter systems in bone marrow mesenchymal stem cells. Biotechnol Lett 30:835–843PubMedCrossRefGoogle Scholar
  11. Chomczynski P, Sacchi N (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat Protoc 1:581–585PubMedCrossRefGoogle Scholar
  12. Christman KL, Lee RJ (2006) Biomaterials for the treatment of myocardial infarction. J Am Coll Cardiol 48:907–913PubMedCrossRefGoogle Scholar
  13. Condorelli G, Borello U, De Angelis L, Latronico M, Sirabella D, Coletta M, Galli R, Balconi G, Follenzi A, Frati G, De Angelis MGC, Gioglio L, Amuchastegui S, Adorini L, Naldini L, Vescovi A, Dejana E, Cossu G (2001) Cardiomyocytes induce endothelial cells to trans-differentiate into cardiac muscle: implications for myocardium regeneration. Proc Natl Acad Sci USA 98:10733–10738PubMedCrossRefGoogle Scholar
  14. Costanzo MR, Augustine S, Bourge R, Bristow M, O’Connell JB, Driscoll D, Rose E (1995) Selection and treatment of candidates for heart transplantation: a statement for health professionals from the Committee on Heart Failure and Cardiac Transplantation of the Council on Clinical Cardiology, American Heart association. Circulation 92:3593–3612PubMedCrossRefGoogle Scholar
  15. Dalby MJ, Gadegaard N, Tare R, Andar A, Riehle MO, Herzyk P, Wilkinson CDW, Oreffo ROC (2007) The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater 6:997–1003PubMedCrossRefGoogle Scholar
  16. DeQuach JA, Mezzano V, Miglani A, Lange S, Keller GM, Sheikh F, Christman KL (2010) Simple and high yielding method for preparing tissue specific extracellular matrix coatings for cell culture. PLoS One 5:e13039PubMedCrossRefGoogle Scholar
  17. Dimarakis I, Habib NA, Gordon MYA (2005) Adult bone marrow-derived stem cells and the injured heart: just the beginning? Eur J Cardiothorac Surg 28:665–676PubMedCrossRefGoogle Scholar
  18. Dimarakis I, Levicar N, Nihoyannopoulos P, Gordon MY, Habib NA (2006a) In vitro stem cell differentiation into cardiomyocytes. Part 2. Chemicals, extracellular matrix, physical stimuli and coculture assays. J Cardiothorac Renal Res 1:115–121CrossRefGoogle Scholar
  19. Dimarakis I, Levicar N, Nihoyannopoulos P, Habib NA, Gordon MY (2006b) In vitro stem cell differentiation into cardiomyocytes. Part 1. Culture medium and growth factors. J Cardiothorac Renal Res 1:107–114CrossRefGoogle Scholar
  20. Donald GP, Darwin JP (2007) Concise review. Mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair—current views. Stem Cells 25:2896–2902CrossRefGoogle Scholar
  21. Engel FB, Schebesta M, Keating MT (2006) Anillin localization defect in cardiomyocyte binucleation. J Mol Cell Cardiol 41:601–612PubMedCrossRefGoogle Scholar
  22. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677–689PubMedCrossRefGoogle Scholar
  23. Eshghi S, Schaffer DV (2008) Engineering microenvironments to control stem cell fate and function. In: Sangeeta B, Polak J (eds) StemBook. Harvard Stem Cell Institute, CambridgeGoogle Scholar
  24. Even-Ram S, Artym V, Yamada KM (2006) Matrix control of stem cell fate. Cell 126:645–647PubMedCrossRefGoogle Scholar
  25. Fukuda K (2001) Development of regenerative cardiomyocytes from mesenchymal stem cells for cardiovascular tissue engineering. Artif Organs 25:187–193PubMedCrossRefGoogle Scholar
  26. Fukuda K (2003) Use of adult marrow mesenchymal stem cells for regeneration of cardiomyocytes. Bone Marrow Transplant 32:S25–S27PubMedCrossRefGoogle Scholar
  27. Grepin C, Nemer G, Nemer M (1997) Enhanced cardiogenesis in embryonic stem cells overexpressing the GATA-4 transcription factor. Development 124:2387–2395PubMedGoogle Scholar
  28. Guilak F, Cohen DM, Estes BT, Gimble JM, Liedtke W, Chen CS (2009) Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 5:17–26PubMedCrossRefGoogle Scholar
  29. Hattan N, Kawaguchi H, Ando K, Kuwabara E, Fujita J, Murata M, Suematsu M, Mori H, Fukuda K (2005) Purified cardiomyocytes from bone marrow mesenchymal stem cells produce stable intracardiac grafts in mice. Cardiovasc Res 65:334–344PubMedCrossRefGoogle Scholar
  30. Heng BC, Haider HK, Sim EK-W, Cao T, Ng SC (2004) Strategies for directing the differentiation of stem cells into the cardiomyogenic lineage in vitro. Cardiovasc Res 62:34–42PubMedCrossRefGoogle Scholar
  31. Higuchi S, Lin Q, Wang J, Lim TK, Joshi SB, Anand GS, Chung MCM, Sheetz MP, Fujita H (2013) Heart extracellular matrix supports cardiomyocyte differentiation of mouse embryonic stem cells. J Biosci Bioeng 115:320–325PubMedCrossRefGoogle Scholar
  32. Inaba K, Inaba M, Romani N, Aya H, Deguchi M, Ikehara S, Muramatsu S, Steinman RM (1992) Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 176:1693–1702PubMedCrossRefGoogle Scholar
  33. Ishii O, Shin M, Sueda T, Vacanti JP (2005) In vitro tissue engineering of a cardiac graft using a degradable scaffold with an extracellular matrix-like topography. J Thorac Cardiovasc Surg 130:1358–1363PubMedCrossRefGoogle Scholar
  34. Jansen JA, van Veen TAB, de Bakker JMT, van Rijen HVM (2010) Cardiac connexins and impulse propagation. J Mol Cell Cardiol 48:76–82PubMedCrossRefGoogle Scholar
  35. Ji YR, Kim MO, Kim SH, Yu DH, Shin MJ, Kim HJ, Yuh HS, Bae KB, Kim JY, Park HD, Lee SG, Hyun BH, Ryoo ZY (2010) Effects of regulator of G protein signaling 19 (RGS19) on heart development and function. J Biol Chem 285:28627–28634PubMedCrossRefGoogle Scholar
  36. Kajstura J, Rota M, Whang B, Cascapera S, Hosoda T, Bearzi C, Nurzynska D, Kasahara H, Zias E, Bonafe M, Nadal-Ginard B, Torella D, Nascimbene A, Quaini F, Urbanek K, Leri A, Anversa P (2005) Bone marrow cells differentiate in cardiac cell lineages after infarction independently of cell fusion. Circ Res 96:127–137PubMedCrossRefGoogle Scholar
  37. Kehat I, Khimovich L, Caspi O, Gepstein A, Shofti R, Arbel G, Huber I, Satin J, Itskovitz-Eldor J, Gepstein L (2004) Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat Biotech 22:1282–1289CrossRefGoogle Scholar
  38. Kolf C, Cho E, Tuan R (2007) Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: regulation of niche, self-renewal and differentiation. Arthritis Res Ther 9:204–214PubMedCrossRefGoogle Scholar
  39. Kraehenbuehl TP, Zammaretti P, Van der Vlies AJ, Schoenmakers RG, Lutolf MP, Jaconi ME, Hubbell JA (2008) Three-dimensional extracellular matrix-directed cardioprogenitor differentiation: systematic modulation of a synthetic cell-responsive PEG-hydrogel. Biomaterials 29:2757–2766PubMedCrossRefGoogle Scholar
  40. Kretlow J, Jin Y-Q, Liu W, Zhang W, Hong T-H, Zhou G, Baggett LS, Mikos A, Cao Y (2008) Donor age and cell passage affects differentiation potential of murine bone marrow-derived stem cells. BMC Cell Biol 9:60PubMedCrossRefGoogle Scholar
  41. Kurdi M, Chidiac R, Hoemann C, Zouein F, Zgheib C, Booz GW (2010) Hydrogels as a platform for stem cell delivery to the heart. Congest Heart Fail 16:132–135PubMedCrossRefGoogle Scholar
  42. Li W-J, Tuli R, Huang X, Laquerriere P, Tuan RS (2005) Multilineage differentiation of human mesenchymal stem cells in a three-dimensional nanofibrous scaffold. Biomaterials 26:5158–5166PubMedCrossRefGoogle Scholar
  43. Lu G, Haider HK, Jiang S, Ashraf M (2009) Sca-1+ stem cell survival and engraftment in the infarcted heart: dual role for preconditioning induced connexin-43. Circulation 119:2587–2596PubMedCrossRefGoogle Scholar
  44. Madden LR, Mortisen DJ, Sussman EM, Dupras SK, Fugate JA, Cuy JL, Hauch KD, Laflamme MA, Murry CE, Ratner BD (2010) Proangiogenic scaffolds as functional templates for cardiac tissue engineering. Proc Natl Acad Sci USA 107:15211–15216PubMedCrossRefGoogle Scholar
  45. Makino S, Fukuda K, Miyoshi S, Konishi F, Kodama H, Pan J, Sano M, Takahashi T, Hori S, Abe H, J-i H, Umezawa A, Ogawa S (1999) Cardiomyocytes can be generated from marrow stromal cells in vitro. J Clin Invest 103:697–705PubMedCrossRefGoogle Scholar
  46. Maulik N, Thirunavukkarasu M (2008) Growth factor/s and cell therapy in myocardial regeneration. J Mol Cell Cardiol 44:219–227PubMedCrossRefGoogle Scholar
  47. McNamara LE, McMurray RJ, Biggs MJP, Kantawong F, Oreffo ROC, Dalby MJ (2010) Nanotopographical control of stem cell differentiation. J Tissue Eng 2010:1206233Google Scholar
  48. Memon IA, Sawa Y, Fukushima N, Matsumiya G, Miyagawa S, Taketani S, Sakakida SK, Kondoh H, Aleshin AN, Shimizu T, Okano T, Matsuda H (2005) Repair of impaired myocardium by means of implantation of engineered autologous myoblast sheets. J Thorac Cardiovasc Surg 130:1333–1341PubMedCrossRefGoogle Scholar
  49. Menasche P (2009) Stem cell therapy for heart failure: are arrhythmias a real safety concern? Circulation 119:2735–2740PubMedCrossRefGoogle Scholar
  50. Miner EC, Miller WL (2006) A look between the cardiomyocytes: the extracellular matrix in heart failure. Mayo Clin Proc 81:71–76PubMedCrossRefGoogle Scholar
  51. Mummery CL, Davis RP, Krieger JE (2010) Challenges in using stem cells for cardiac repair. Sci Transl Med 2:17CrossRefGoogle Scholar
  52. Nesselmann C, Ma N, Bieback K, Wagner W, Ho A, Konttinen YT, Zhang H, Hinescu ME, Steinhoff G (2008) Mesenchymal stem cells and cardiac repair. J Cell Mol Med 12:1795–1810PubMedCrossRefGoogle Scholar
  53. Odorico JS, Kaufman DS, Thomson JA (2001) Multilineage differentiation from human embryonic stem cell lines. Stem Cells 19:193–204PubMedCrossRefGoogle Scholar
  54. Orlic D, Hill JM, Arai AE (2002) Stem cells for myocardial regeneration. Circ Res 91:1092–1102PubMedCrossRefGoogle Scholar
  55. Pasumarthi KBS, Kardami E, Cattini PA (1996) High and low molecular weight fibroblast growth factor-2 increase proliferation of neonatal rat cardiac myocytes but have differential effects on binucleation and nuclear morphology: evidence for both paracrine and intracrine actions of fibroblast growth factor-2. Circ Res 78:126–136PubMedCrossRefGoogle Scholar
  56. Peister A, Mellad JA, Larson BL, Hall BM, Gibson LF, Prockop DJ (2004) Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 103:1662–1668PubMedCrossRefGoogle Scholar
  57. Perin EC (2006) Stem cell therapy for cardiovascular disease. Tex Heart Inst J 33:204–208PubMedGoogle Scholar
  58. Perin EC, Lopez J (2006) Methods of stem cell delivery in cardiac diseases. Nat Clin Pract Cardiovasc Med 3:S110–S113PubMedCrossRefGoogle Scholar
  59. Piao H, Kwon J-S, Piao S, Sohn J-H, Lee Y-S, Bae J-W, Hwang K-K, Kim D-W, Jeon O, Kim B-S, Park Y-B, Cho M-C (2007) Effects of cardiac patches engineered with bone marrow-derived mononuclear cells and PGCL scaffolds in a rat myocardial infarction model. Biomaterials 28:641–649PubMedCrossRefGoogle Scholar
  60. Reffelmann T, Kloner RA (2003) Cellular cardiomyoplasty—cardiomyocytes, skeletal myoblasts, or stem cells for regenerating myocardium and treatment of heart failure? Cardiovasc Res 58:358–368PubMedCrossRefGoogle Scholar
  61. Rosca AM, Burlacu A (2011) The effect of 5-azacytidine: evidence for alteration of the multipotent ability of mesenchymal stem cells. Stem Cells Dev 20:1213–1221PubMedCrossRefGoogle Scholar
  62. Rota M, Kajstura J, Hosoda T, Bearzi C, Vitale S, Esposito G, Iaffaldano G, Padin-Iruegas ME, Gonzalez A, Rizzi R, Small N, Muraski J, Alvarez R, Chen X, Urbanek K, Bolli R, Houser SR, Leri A, Sussman MA, Anversa P (2007) Bone marrow cells adopt the cardiomyogenic fate in vivo. Proc Natl Acad Sci USA 104:17783–17788PubMedCrossRefGoogle Scholar
  63. Scadden DT (2006) The stem-cell niche as an entity of action. Nature 441:1075–1079PubMedCrossRefGoogle Scholar
  64. Segers VFM, Lee RT (2008) Stem-cell therapy for cardiac disease. Nature 451:937–942PubMedCrossRefGoogle Scholar
  65. Siegel G, Krause P, Wöhrle S, Nowak P, Ayturan M, Kluba T, Brehm BR, Neumeister B, Köhler D, Rosenberger P, Just L, Northoff H, Schäfer R (2012) Bone marrow-derived human mesenchymal stem cells express cardiomyogenic proteins but do not exhibit functional cardiomyogenic differentiation potential. Stem Cells Dev 21:2457–2470PubMedCrossRefGoogle Scholar
  66. Singelyn JM, DeQuach JA, Seif-Naraghia SB, Littlefield RB, Schup-Magoffina PJ, Christman KL (2009) Naturally derived myocardial matrix as an injectable scaffold for cardiac tissue engineering. Biomaterials 30:5409–5416PubMedCrossRefGoogle Scholar
  67. Song H, Chang W, Lim S, Seo H-S, Shim CY, Park S, Yoo K-J, Kim B-S, Min B-H, Lee H, Jang Y, Chung N, Hwang K-C (2007) Tissue transglutaminase is essential for integrin-mediated survival of bone marrow-derived mesenchymal stem cells. Stem Cells 25:1431–1438PubMedCrossRefGoogle Scholar
  68. Song H, Cha M-J, Song B-W, Kim I-K, Chang W, Lim S, Choi E, Ham O, Lee S-Y, Chung N, Jang Y, Hwang K-C (2010) Reactive oxygen species inhibit adhesion of mesenchymal stem cells implanted into ischemic myocardium via interference of focal adhesion complex. Stem Cells 28:555–563PubMedGoogle Scholar
  69. Sreejit P, Verma RS (2011a) Cardiogel supports adhesion, proliferation and differentiation of stem cells with increased oxidative stress protection. Cells Mater 21:107–121Google Scholar
  70. Sreejit P, Verma RS (2011b) Scanning electron microscopy preparation protocol for differentiated stem cells. Anal Biochem 416:186–190CrossRefGoogle Scholar
  71. Sreejit P, Verma RS (2013) Natural ECM as biomaterial for scaffold based cardiac regeneration using adult bone marrow derived stem cells. Stem Cell Rev Rep 9:158–171CrossRefGoogle Scholar
  72. Sreejit P, Kumar S, Verma RS (2008) An improved protocol for primary culture of cardiomyocyte from neonatal mice. In Vitro Cell Dev Biol Anim 44:45–50PubMedCrossRefGoogle Scholar
  73. Sreejit P, Dilip K, Verma R (2012) Generation of mesenchymal stem cell lines from murine bone marrow. Cell Tissue Res 350:55–68PubMedCrossRefGoogle Scholar
  74. Swain SM, Parameswaran S, Sahu G, Verma RS, Bera AK (2012) Proton-gated ion channels in mouse bone marrow stromal cells. Stem Cell Res 9:59–68PubMedCrossRefGoogle Scholar
  75. Tang YL, Phillips MI (2007) Invited commentary. Ann Thorac Surg 83:1499–1500PubMedCrossRefGoogle Scholar
  76. Tong M, Yang XJ, Geng BY, Han LH, Zhou YF, Zhao X, Li HX (2010) Overexpression of connexin 45 in rat mesenchymal stem cells improves the function as cardiac biological pacemakers. Chin Med J 123:1571–1576PubMedGoogle Scholar
  77. Uriel S, Labay E, Francis-Sedlak M, Moya ML, Weichselbaum RR, Ervin N, Cankova Z, Brey EM (2009) Extraction and assembly of tissue-derived gels for cell culture and tissue engineering. Tissue Eng Part C Methods 15:309–321PubMedCrossRefGoogle Scholar
  78. van der Heyden MAG, Defize LHK (2003) Twenty one years of P19 cells: what an embryonal carcinoma cell line taught us about cardiomyocyte differentiation. Cardiovasc Res 58:292–302PubMedCrossRefGoogle Scholar
  79. van Laake L, van Donselaar E, Monshouwer-Kloots J, Schreurs C, Passier R, Humbel B, Doevendans P, Sonnenberg A, Verkleij A, Mummery C (2010) Extracellular matrix formation after transplantation of human embryonic stem cell-derived cardiomyocytes. Cell Mol Life Sci 67:277–290PubMedCrossRefGoogle Scholar
  80. VanWinkle WB, Snuggs MB, Buja LM (1996) Cardiogel: a biosynthetic extracellular matrix for cardiomyocyte culture. In Vitro Cell Dev Biol Anim 32:478–485PubMedCrossRefGoogle Scholar
  81. Wang J-S, Shum-Tim D, Chedrawy E, Chiu RCJ (2001) The coronary delivery of marrow stromal cells for myocardial regeneration: pathophysiologic and therapeutic implications. J Thorac Cardiovasc Surg 122:699–705PubMedCrossRefGoogle Scholar
  82. Wei-xin L, Jian S, Yu W, Guo-dong P, Yu L, Bang-chang C, Xi-chang C (2004) A microenvironment, rather than chemical, initiates the cardiomyogenic differentiation of marrow stromal cells. Wuhan Univ J Nat Sci 9:513–521CrossRefGoogle Scholar
  83. Wollert KC, Drexler H (2010) Cell therapy for the treatment of coronary heart disease: a critical appraisal. Nat Rev Cardiol 7:204–215PubMedCrossRefGoogle Scholar
  84. Wu KH, Liu YL, Zhou B, Han ZC (2006) Cellular therapy and myocardial tissue engineering: the role of adult stem and progenitor cells. Eur J Cardiothorac Surg 30:770–781PubMedCrossRefGoogle Scholar
  85. Zhang FB, Li L, Fang B, Zhu DL, Yang HT, Gao PJ (2005) Passage-restricted differentiation potential of mesenchymal stem cells into cardiomyocyte-like cells. Biochem Biophys Res Commun 336:784–792PubMedCrossRefGoogle Scholar
  86. Zimmermann W-H, Melnychenko I, Wasmeier G, Didie M, Naito H, Nixdorff U, Hess A, Budinsky L, Brune K, Michaelis B, Dhein S, Schwoerer A, Ehmke H, Eschenhagen T (2006) Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med 12:452–458PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Stem Cell & Molecular Biology Laboratory, Bhupat and Jyoti Mehta School of Biosciences, Department of BiotechnologyIndian Institute of Technology MadrasChennaiIndia

Personalised recommendations