The stimulation of the cardiac differentiation of mesenchymal stem cells in tissue constructs that mimic myocardium structure and biomechanics

Biomaterials

Volumn 32, Issue 24, 2011, Pages 5568-5580

  Guan, Jianjun ^a   Wang, Feng ^a   Li, Zhenqing ^a   Chen, Joseph ^b   Guo, Xiaolei ^a   Liao, Jun ^b   Moldovan, Nicanor I ^c  

^a Ohio State University   (United States)

^b MISSISSIPPI STATE UNIVERSITY   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

Electrospinning; Mesenchymal stem cell; Myocardium; Tissue specific constructs

Indexed keywords

ANISOTROPIC STRUCTURE; CALCIUM CHANNELS; CARDIAC DIFFERENTIATION; CARDIAC MARKERS; CARDIAC REGENERATION; CARDIOMYOCYTES; CELL ALIGNMENT; DEGREE OF ALIGNMENTS; DIFFERENTIATED CELLS; ELECTRICAL FIELD; IN-VIVO; MESENCHYMAL STEM CELL; MRNA EXPRESSION; MYOCARDIUM; PROCESSING PARAMETERS; REAL TIME RT-PCR; STRESS-STRAIN RESPONSE; STRUCTURAL AND MECHANICAL PROPERTIES; TISSUE CONSTRUCTS; TISSUE-SPECIFIC CONSTRUCTS;

ALIGNMENT; CELL CULTURE; ELECTROPHYSIOLOGY; FLOWCHARTING; HEART; MECHANICAL PROPERTIES; STEM CELLS; THREE DIMENSIONAL; TISSUE;

BIOMECHANICS;

CALCIUM CHANNEL; COLLAGEN TYPE 1; MESSENGER RNA; OSTEONECTIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR NKX2.5;

ANIMAL TISSUE; ANISOTROPY; ARTICLE; BIOMECHANICS; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION; HEART BEAT; HEART ELECTROPHYSIOLOGY; HEART INFARCTION; HEART MUSCLE; HEART MUSCLE CELL; IN VIVO STUDY; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SWINE;

ANIMALS; BIOMECHANICS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SHAPE; CELLS, CULTURED; ELECTROPHYSIOLOGY; HUMANS; MESENCHYMAL STEM CELLS; MYOCARDIUM; POLYMERS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SWINE; TISSUE SCAFFOLDS;

SUS;

EID: 79957895552     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.04.038     Document Type: Article

References (66)

1. Rubin R., Strayer D.S., Rubin E. Rubin's pathology: clinicopathologic foundations of medicine 2008, Lippincott Williams & Wilkins. 4th ed.
2. Flynn A., O'Brien T. Stem cell therapy for cardiac disease. Expert Opin Biol Ther 2011, 11:177-187.
3. Forrester J.S., Makkar R.R., Marbán E. Long-term outcome of stem cell therapy for acute myocardial infarction: right results, wrong reasons. J Am Coll Cardiol 2009, 53:2270-2272.
4. Miyahara Y., Nagaya N., Kataoka M., Yanagawa B., Tanaka K., Hao H., et al. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med 2006, 12:459-465.
5. Quevedo H.C., Hatzistergos K.E., Oskouei B.N., Feigenbaum G.S., Rodriguez J.E., Valdes D., et al. Allogeneic mesenchymal stem cells restore cardiac function in chronic ischemic cardiomyopathy via trilineage differentiating capacity. Proc Natl Acad Sci U S A 2009, 106:14022-14027.
6. Toma C., Pittenger M.F., Cahill K.S., Byrne B.J., Kessler P.D. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 2002, 105:93-98.
7. Cho J., Zhai P., Maejima Y., Sadoshima J. Myocardial injection with GSK-3β-overexpressing bone marrow-derived mesenchymal stem cells attenuates cardiac dysfunction after myocardial infarction. Circ Res 2011, 108(4):478-489.
8. Nagaya N., Kangawa K., Itoh T., Iwase T., Murakami S., Miyahara Y., et al. Transplantation of mesenchymal stem cells improves cardiac function in a rat model of dilated cardiomyopathy. Circulation 2005, 112(8):1128-1135.
9. Song H., Hwang H.J., Chang W., Song B.W., Cha M.J., Kim I.K., et al. Cardiomyocytes from phorbol myristate acetate-activated mesenchymal stem cells restore electromechanical function in infarcted rat hearts. Proc Natl Acad Sci U S A 2011, 108(1):296-301.
10. Bel A., Planat-Bernard V., Saito A., Bonnevie L., Bellamy V., Sabbah L., et al. Composite cell sheets: a further step toward safe and effective myocardial regeneration by cardiac progenitors derived from embryonic stem cells. Circulation 2010, 122:S118-S123.
11. Nelson T.J., Martinez-Fernandez A., Yamada S., Perez-Terzic C., Ikeda Y., Terzic A. Repair of acute myocardial infarction by human stemness factors induced pluripotent stem cells. Circulation 2009, 120:408-416.
12. Bailey B., Izarra A., Alvarez R., Fischer K.M., Cottage C.T., Quijada P., et al. Cardiac stem cell genetic engineering using the αMHC promoter. Regen Med 2009, 4:823-833.
13. Davis D.R., Zhang Y., Smith R.R., Cheng K., Terrovitis J., Malliaras K., et al. Validation of the cardiosphere method to culture cardiac progenitor cells from myocardial tissue. PloS One 2009, 4:e7195.
14. Smith R.R., Barile L., Cho H.C., Leppo M.K., Hare J.M., Messina E., et al. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 2007, 115:896-908.
15. Hare J.M. Translational development of mesenchymal stem cell therapy for cardiovascular diseases. Tex Heart Inst J 2009, 36(2):145-147.
16. Ripa R.S., Haack-Sørensen M., Wang Y., Jørgensen E., Mortensen S., Bindslev L., et al. Bone marrow derived mesenchymal cell mobilization by granulocyte-colony stimulating factor after acute myocardial infarction: results from the stem cells in myocardial infarction (STEMMI) trial. Circulation 2007, 116:I24-I30.
17. Chen S., Liu Z., Tian N., Zhang J., Yei F., Duan B., et al. Intracoronary transplantation of autologous bone marrow mesenchymal stem cells for ischemic cardiomyopathy due to isolated chronic occluded left anterior descending artery. J Invasive Cardiol 2006, 18:552-556.
18. Feng C., Zhu J., Zhao L., Lu T., Zhang W., Liu Z., et al. Suberoylanilide hydroxamic acid promotes cardiomyocyte differentiation of rat mesenchymal stem cells. Exp Cell Res 2009, 315:3044-3051.
19. Hakuno D., Fukuda K., Makino S., Konishi F., Tomita Y., Manabe T., et al. Bone marrow-derived regenerated cardiomyocytes (CMG Cells) express functional adrenergic and muscarinic receptors. Circulation 2002, 105(3):380-386.
20. Yang M.C., Wang S.S., Chou N.K., Chi N.H., Huang Y.Y., Chang Y.L., et al. The cardiomyogenic differentiation of rat mesenchymal stem cells on silk fibroin-polysaccharide cardiac patches in vitro. Biomaterials 2009, 30(22):3757-3765.
21. Cho J., Rameshwar P., Sadoshima J. Distinct roles of glycogen synthase kinase (GSK)-3alpha and GSK-3beta in mediating cardiomyocyte differentiation in murine bone marrow-derived mesenchymal stem cells. J Biol Chem 2009, 284(52):36647-36658.
22. Pijnappels D.A., Schalij M.J., Ramkisoensing A.A., van Tuyn J., de Vries A.A., van der Laarse A., et al. Forced alignment of mesenchymal stem cells undergoing cardiomyogenic differentiation affects functional integration with cardiomyocyte cultures. Circ Res 2008, 103(2):167-176.
23. Radisic M., Park H., Chen F., Salazar-Lazzaro J.E., Wang Y., Dennis R., et al. Biomimetic approach to cardiac tissue engineering: oxygen carriers and channeled scaffolds. Tissue Eng 2006, 12:2077-2091.
24. Engelmayr G.C., Cheng M., Bettinger C.J., Borenstein J.T., Langer R., Freed L.E. Accordion-like honeycombs for tissue engineering of cardiac anisotropy. Nat Mater 2008, 7:1003-1010.
25. Radisic M., Park H., Shing H., Consi T., Schoen F.J., Langer R., et al. Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc Natl Acad Sci U S A 2004, 101:18129-18134.
26. Zimmermann W.H., Melnychenko I., Wasmeier G., Didié M., Naito H., Nixdorff U., et al. Engineered heart tissue grafts improve systolic and diastolic function in infarct rat hearts. Nat Med 2006, 12:452-458.
27. Simpson D., Liu H., Fan T.H., Nerem R., Dudley S.C. A tissue engineering approach to progenitor cell delivery results in significant cell engraftment and improved myocardial remodeling. Stem Cells 2007, 25:2350-2357.
28. Dvir T., Kedem A., Ruvinov E., Levy O., Freeman I., Landa N., et al. Prevascularization of cardiac patch on the omentum improves its therapeutic outcome. Proc Natl Acad Sci U S A 2009, 106:14990-14995.
29. Yang M.C., Chi N.H., Chou N.K., Huang Y.Y., Chung T.W., Chang Y.L., et al. The influence of rat mesenchymal stem cell CD44 surface markers on cell growth, fibronectin expression, and cardiomyogenic differentiation on silk fibroin - Hyaluronic acid cardiac patches. Biomaterials 2010, 31(5):854-862.
30. 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 2007, 49:2292-2300.
31. Rockwood D.N., Akins R.E., Parrag I.C., Woodhouse K.A., Rabolt J.F. Culture on electrospun polyurethane scaffolds decreases atrial natriuretic peptide expression by cardiomyocytes in vitro. Biomaterials 2008, 29:4783-4791.
32. Wang F., Guan J. Cellular cardiomyoplasty and cardiac tissue engineering for myocardial therapy. Adv Drug Deliv Rev 2010, 62:784-797.
33. Wang F., Li Z., Lannutti J.L., Wagner W.R., Guan J. Synthesis, characterization and surface modification of low moduli poly(ether carbonate urethane)ureas for soft tissue engineering. Acta Biomater 2009, 5:2901-2912.
34. Guan J., Sacks M.S., Beckman E.J., Wagner W.R. Biodegradable poly(ether ester urethane)urea elastomers based on poly(ether ester) triblock copolymers and putrescine: synthesis, characterization and cytocompatibility. Biomaterials 2004, 25:85-96.
35. Guan J., Sacks M.S., Beckman E.J., Wagner W.R. Synthesis, characterization, and cytocompatibility of elastomeric, biodegradable poly(ester urethane)ureas based on polycaprolactone and putrescine. J Biomed Mater Res 2002, 61:493-503.
36. Wang F., Li Z., Khan M., Tamama K., Kuppusamy P., Wagner W.R., et al. Injectable, rapid gelling and highly flexible hydrogel composites as growth factor and cell carriers. Acta Biomater 2010, 6:1978-1991.
37. Song L., Tuan R.S. Transdifferentiation potential of human mesenchymal stem cells derived from bone marrow. FASEB J 2004, 18:980-982.
38. Wang F., Li Z., Tamama K., Sen C.K., Guan J. Fabrication and characterization of prosurvival growth factor releasing, anisotropic scaffolds for enhanced mesenchymal stem cell survival/growth and orientation. Biomacromolecules 2009, 10:2609-2618.
39. Cohen J., Zaleski K.L., Nourissat G., Julien T.P., Randolph M.A., Yaremchuk M.J. Survival of porcine mesenchymal stem cells over the alginate recovered cellular method. J Biomed Mater Res A 2011, 96:93-99.
40. Yow S.Z., Quek C.H., Yim K.F., Lim C.T., Leong K.W. Collagen-based fibrous scaffold for spatial organization of encapsulated and seeded human mesenchymal stem cells. Biomaterials 2009, 30:1133-1142.
41. Song L., Webb N.E., Song Y., Tuan R.S. Identification and functional analysis of candidate genes regulating mesenchymal stem cell self-renewal and multipotency. Stem Cells 2006, 24:1707-1718.
42. Stankus J.J., Guan J., Fujimoto K., Wagner W.R. Microintegrating smooth muscle cells into a biodegradable, elastomeric fiber matrix. Biomaterials 2006, 27:735-744.
43. Li W.J., Mauck R.L., Cooper J.A., Yuan X., Tuan R.S. Engineering controllable anisotropy in electrospun biodegradable nanofibrous scaffolds for musculoskeletal tissue engineering. J Biomech 2007, 40:1686-1693.
44. Courtney T., Sacks M.S., Stankus J., Guan J., Wagner W.R. Design and analysis of tissue engineering scaffolds that mimic soft tissue mechanical anisotropy. Biomaterials 2006, 27:3631-3638.
45. Grashow J.S., Yoganathan A.P., Sacks M.S. Biaixal stress-stretch behavior of the mitral valve anterior leaflet at physiologic strain rates. Ann Biomed Eng 2006, 34:315-325.
46. Wang B., Borazjani A., Tahai M., Curry A.L., Simionescu D.T., Guan J., et al. Fabrication of cardiac patch with decellularized porcine myocardial scaffold and bone marrow mononuclear cells. J Biomed Mater Res A 2010, 94:1100-1110.
47. Li Z., Wang F., Roy S., Sen C.K., Guan J. Injectable, highly flexible, and thermosensitive hydrogels capable of delivering superoxide dismutase. Biomacromolecules 2009, 10:3306-3316.
48. Ng C.P., Hinz B., Swartz M.A. Interstitial fluid flow induces myofibroblast differentiation and collagen alignment in vitro. J Cell Sci 2005, 118:4731-4739.
49. Li Z., Guo X., Matsushita S., Guan J. Differentiation of cardiosphere-derived cells into a mature cardiac lineage using biodegradable poly(N-isopropylacrylamide) hydrogels. Biomaterials 2011, 32:3220-3232.
50. Kraehenbuehl T.P., Ferreira L.S., Hayward A.M., Nahrendorf M., van der Vlies AJ., Vasile E., et al. Human embryonic stem cell-derived microvascular grafts for cardiac tissue preservation after myocardial infarction. Biomaterials 2011, 32:1102-1109.
51. Ryu J.H., Kim I.K., Cho S.W. Implantation of bone marrow mononuclear cells using injectable fibrin matrix enhances neovascularization in infarcted myocardium. Biomaterials 2005, 26:319-326.
52. Zhang G., Hu Q., Braunlin E.A., Suggs L.J., Zhang J. Enhancing efficacy of stem cell transplantation to the heart with a PEGylated fibrin biomatrix. Tissue Eng Part A 2008, 14:1025-1036.
53. 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 three-dimensional tissue construct containing uniformly distributed embryoid body-derived cells as a cardiac patch. Biomaterials 2010, 31:6218-6227.
54. Sahoo S., Lee W.C., Goh J.C., Toh S.L. Bio-electrospraying: a potentially safe technique for delivering progenitor cells. Biotechnol Bioeng 2010, 106(4):690-698.
55. Weis S.M., Emery J.L., Becker K.D., McBride D.J., Omens J.H., McCulloch A.D. Myocardial mechanics and collagen structure in the osteogenesis imperfecta murine (oim). Circ Res 2000, 87:663-669.
56. Tse J.R., Engler A.J. Stiffness gradients mimicking in vivo tissue variation regulate mesenchymal stem cell fate. PLoS One 2011, 6(1):e15978.
57. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
58. Wall S.T., Walker J.C., Healy K.E., Ratcliffe M.B., Guccione J.M. Theoretical impact of the injection of material into the myocardium - a finite element model simulation. Circulation 2006, 114:2627-2635.
59. Amoroso N.J., D'Amore A., Hong Y., Wagner W.R., Sacks M.S. Elastomeric electrospun polyurethane scaffolds: the interrelationship between fabrication conditions, fiber topology, and mechanical properties. Adv Mater 2011, 23:106-111.
60. Greiner A., Wendorff J.H. Electrospinning: a fascinating method for the preparation of ultrathin fibres. Angew Chem-Int Edit 2007, 46:5670-5703.
61. Nam J., Huang Y., Agarwal S., Lannutti J.J. Improved cellular infiltration in electrospun fiber via engineered porosity. Tissue Eng 2007, 13:2249-2257.
62. Baker B.M., Gee A.O., Metter R.B., Nathan A.S., Marklein R.A., Burdick J.A., et al. The potential to improve cell infiltration in composite fiber-aligned electrospun scaffolds by the selective removal of sacrificial fibers. Biomaterials 2008, 29:2348-2358.
63. Blakeney B.A., Tambralli A., Anderson J.M., Andukuri A., Lim D.J., Dean D.R., et al. Cell infiltration and growth in a low density, uncompressed three-dimensional electrospun nanofibrous scaffold. Biomaterials 2011, 32:1583-1590.
64. Yang X., Shah J.D., Wang H. Nanofiber enabled layer-by-layer approach toward three-dimensional tissue formation. Tissue Eng Part A 2009, 15:945-956.
65. Lim S.H., Liu X.Y., Song H., Yarema K.J., Mao H.Q. The effect of nanofiber-guided cell alignment on the preferential differentiation of neural stem cells. Biomaterials 2010, 31(34):9031-9039.
66. Bashur C.A., Shaffer R.D., Dahlgren L.A., Guelcher S.A., Goldstein A.S. Effect of fiber diameter and alignment of electrospun polyurethane meshes on mesenchymal progenitor cells. Tissue Eng Part A 2009, 15(9):2435-2445.