Enhanced efficiency of genetic programming toward cardiomyocyte creation through topographical cues

Biomaterials

Volumn 70, Issue , 2015, Pages 94-104

  Morez, Constant ^a,b,c   Noseda, Michela ^b,c   Paiva, Marta Abreu ^b,c   Belian, Elisa ^b,c   Schneider, Michael D ^b,c   Stevens, Molly M ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Cardiac tissue engineering; Cardiomyocyte; Micropatterning; Stem cell; Surface topography

Indexed keywords

ACETYLATION; CELLS; CYTOLOGY; GENETIC ALGORITHMS; GENETIC PROGRAMMING; PROTEINS; STEM CELLS; SURFACE TOPOGRAPHY; TISSUE; TISSUE ENGINEERING; TISSUE REGENERATION; WELL STIMULATION;

CARDIAC TISSUE ENGINEERING; CARDIOMYOCYTES; CHEMICAL-FREE TECHNIQUES; DIRECTED DIFFERENTIATIONS; HISTONE DEACETYLASE INHIBITOR; MICRO PATTERNING; POST-TRANSLATIONAL MODIFICATIONS; TRANSCRIPTIONAL FUNCTIONS;

CELL ENGINEERING;

HISTONE H3; MYOCARDIN; MYOCYTE ENHANCER FACTOR 2; MYOCYTE ENHANCER FACTOR 2A; MYOCYTE ENHANCER FACTOR 2C; PROSTAGLANDIN E2; T BOX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ACTC 1; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR GATA 6; TRANSCRIPTION FACTOR HAND 1; TRANSCRIPTION FACTOR HAND 2; TRANSCRIPTION FACTOR MYH6; TRANSCRIPTION FACTOR NKX2.5; TRANSCRIPTION FACTOR PLN; TRANSCRIPTION FACTOR RYR2; TRANSCRIPTION FACTOR TBX20; TRANSCRIPTION FACTOR TBX5; UNCLASSIFIED DRUG; VALPROIC ACID; DIMETICONE; HISTONE; NUCLEAR PROTEIN; TRANSACTIVATOR PROTEIN;

ANISOTROPY; ARTICLE; BIOCHEMICAL ANALYSIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STIMULATION; CELL STRUCTURE; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENETIC ENGINEERING; HEART MUSCLE CELL; HISTONE ACETYLATION; HUMAN; LENTIVIRINAE; MEMBRANE STRUCTURE; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; SARCOMERE; STEM CELL; SUMOYLATION; TISSUE REGENERATION; ACETYLATION; CARDIAC MUSCLE CELL; CELL CLONE; CELL LINEAGE; CELL NUCLEUS; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; SIDE POPULATION CELL;

ACETYLATION; CELL LINEAGE; CELL NUCLEUS; CELLULAR REPROGRAMMING; CLONE CELLS; DIMETHYLPOLYSILOXANES; HISTONES; MYOCYTES, CARDIAC; NUCLEAR PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; SARCOMERES; SIDE-POPULATION CELLS; SUMOYLATION; TRANS-ACTIVATORS; VALPROIC ACID;

EID: 84940852069     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.07.063     Document Type: Article

References (63)

1. Senyo S.E., et al. Mammalian heart renewal by pre-existing cardiomyocytes. Nature 2013, 493(7432):433-436.
2. Mercola M., Ruiz-Lozano P., Schneider M.D. Cardiac muscle regeneration: lessons from development. Genes Dev. 2011, 25(4):299-309.
3. Murry C.E., Reinecke H., Pabon L.M. Regeneration gaps: observations on stem cells and cardiac repair. J. Am. Coll. Cardiol. 2006, 47(9):1777-1785.
4. Laflamme M.A., Murry C.E. Heart regeneration. Nature 2011, 473(7347):326-335.
5. Behfar A., Crespo-Diaz R., Terzic A., Gersh B.J. Cell therapy for cardiac repair-lessons from clinical trials. Nat. Rev. Cardiol. 2014, 11(4):232-246.
6. Oh H., et al. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc. Natl. Acad. Sci. U. S. A. 2003, 100(21):12313-12318.
7. Uchida S., et al. Sca1-derived cells are a source of myocardial renewal in the murine adult heart. Stem Cell Rep. 2013, 1(5):397-410.
8. Matsuura K., et al. Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J. Biol. Chem. 2004, 279(12):11384-11391.
9. Beltrami A.P., et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 2003, 114(6):763-776.
10. Dey D., et al. Dissecting the molecular relationship among various cardiogenic progenitor cells. Circ. Res. 2013, 112(9):1253-1262.
11. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126(4):663-676.
12. Addis R.C., Epstein J.A. Induced regeneration-the progress and promise of direct reprogramming for heart repair. Nat. Med. 2013, 19(7):829-836.
13. Ieda M., et al. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 2010, 142(3):375-386.
14. Inagawa K., et al. Induction of cardiomyocyte-like cells in infarct hearts by gene transfer of Gata4, Mef2c, and Tbx5. Circ. Res. 2012, 111(9):1147-1156.
15. Wada R., et al. Induction of human cardiomyocyte-like cells from fibroblasts by defined factors. Proc. Natl. Acad. Sci. U. S. A. 2013, 110(31):12667-12672.
16. Efe J.A., et al. Conversion of mouse fibroblasts into cardiomyocytes using a direct reprogramming strategy. Nat. Cell Biol. 2011, 13(3):215-222.
17. Wang H., et al. Small molecules enable cardiac reprogramming of mouse fibroblasts with a single factor, Oct4. Cell Rep. 2014, 6(5):951-960.
18. Christoforou N., et al. Transcription factors MYOCD, SRF, Mesp1 and SMARCD3 enhance the cardio-inducing effect of GATA4, TBX5, and MEF2C during direct cellular reprogramming. PLoS One 2013, 8(5):e63577.
19. Song K., et al. Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature 2012, 485(7400):599-604.
20. Qian L., et al. In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 2012, 485(7400):593-598.
21. Fu J.D., et al. Direct reprogramming of human fibroblasts toward a cardiomyocyte-like state. Stem Cell Rep. 2013, 1(3):235-247.
22. Hirai H., Katoku-Kikyo N., Keirstead S.A., Kikyo N. Accelerated direct reprogramming of fibroblasts into cardiomyocyte-like cells with the MyoD transactivation domain. Cardiovasc Res. 2013, 100(1):105-113.
23. Muraoka N., et al. MiR-133 promotes cardiac reprogramming by directly repressing snai1 and silencing fibroblast signatures. EMBO J. 2014, 33(14):1565-1581.
24. Protze S., et al. A new approach to transcription factor screening for reprogramming of fibroblasts to cardiomyocyte-like cells. J. Mol. Cell Cardiol. 2012, 53(3):323-332.
25. Mathison M., et al. In vivo cardiac cellular reprogramming efficacy is enhanced by angiogenic preconditioning of the infarcted myocardium with vascular endothelial growth factor. J. Am. Heart Assoc. 2012, 1(6):e005652.
26. Wang L., et al. Stoichiometry of gata4, mef2c, and tbx5 influences the efficiency and quality of induced cardiac myocyte reprogramming. Circ. Res. 2015, 116(2):237-244.
27. Nam Y., et al. Reprogramming of human fibroblasts toward a cardiac fate. Proc. Natl. Acad. Sci. 2013, 110(14):5588-5593.
28. Chen J.X., et al. Inefficient reprogramming of fibroblasts into cardiomyocytes using Gata4, Mef2c, and Tbx5. Circ. Res. 2012, 111(1):50-55.
29. Pasque V., Jullien J., Miyamoto K., Halley-Stott R.P., Gurdon J.B. Epigenetic factors influencing resistance to nuclear reprogramming. Trends Genet. 2011, 27(12):516-525.
30. Plath K., Lowry W.E. Progress in understanding reprogramming to the induced pluripotent state. Nat. Rev. Genet. 2011, 12(4):253-265.
31. Onder T.T., et al. Chromatin-modifying enzymes as modulators of reprogramming. Nature 2012, 483(7391):598-602.
32. Hirai H., Kikyo N. Inhibitors of suppressive histone modification promote direct reprogramming of fibroblasts to cardiomyocyte-like cells. Cardiovasc Res. 2014, 102(1):188-190.
33. Ifkovits J.L., Addis R.C., Epstein J.A., Gearhart J.D. Inhibition of TGFbeta signaling increases direct conversion of fibroblasts to induced cardiomyocytes. PLoS One 2014, 9(2):e89678.
34. Murphy W.L., McDevitt T.C., Engler A.J. Materials as stem cell regulators. Nat. Mater 2014, 13(6):547-557.
35. Dalby M.J., Gadegaard N., Oreffo R.O.C. Harnessing nanotopography and integrin-matrix interactions to influence stem cell fate. Nat. Mater 2014, 13(6):558-569.
36. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126(4):677-689.
37. McBeath R., Pirone D.M., Nelson C.M., Bhadriraju K., Chen C.S. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 2004, 6(4):483-495.
38. Engler A.J., et al. Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J. Cell Biol. 2004, 166(6):877-887.
39. Kshitiz, et al. Matrix rigidity controls endothelial differentiation and morphogenesis of cardiac precursors. Sci. Signal 2012, 5(227):ra41.
40. Rao C., et al. The effect of microgrooved culture substrates on calcium cycling of cardiac myocytes derived from human induced pluripotent stem cells. Biomaterials 2013, 34(10):2399-2411.
41. Tay C.Y., et al. Micropatterned matrix directs differentiation of human mesenchymal stem cells towards myocardial lineage. Exp. Cell Res. 2010, 316(7):1159-1168.
42. Sordella R., Jiang W., Chen G.-C., Curto M., Settleman J. Modulation of Rho GTPase signaling regulates a switch between adipogenesis and myogenesis. Cell 2003, 113(2):147-158.
43. Downing T.L., et al. Biophysical regulation of epigenetic state and cell reprogramming. Nat. Mater 2013, 12(12):1154-1162.
44. Kulangara K., et al. The effect of substrate topography on direct reprogramming of fibroblasts to induced neurons. Biomaterials 2014, 35(20):5327-5336.
45. Yoo J., et al. Cell reprogramming into the pluripotent state using graphene based substrates. Biomaterials 2014, 35(29):8321-8329.
46. Belian E., et al. Forward programming of cardiac stem cells by homogeneous transduction with MYOCD plus TBX5. PLoS One 2015, 10(6):e0125384.
47. Noseda M., et al. PDGFRalpha demarcates the cardiogenic clonogenic Sca1+ stem/progenitor cell in adult murine myocardium. Nat. Commun. 2015, 6:6930.
48. Zhou L., Liu Y., Lu L., Lu X., Dixon R.A. Cardiac gene activation analysis in mammalian non-myoblasic cells by Nkx2-5, Tbx5, Gata4 and Myocd. PLoS One 2012, 7(10):e48028.
49. Hsueh Y.C., Wu J.M.F., Yu C.K., Wu K.K., Hsieh P.C.H. Prostaglandin E2 Promotes Post-Infarction Cardiomyocyte Replenishment by Endogenous Stem Cells 2014, 496-503.
50. Pfister O., et al. CD31- but Not CD31+ cardiac side population cells exhibit functional cardiomyogenic differentiation. Circ. Res. 2005, 97(1):52-61.
51. Noseda M., et al. PDGFRa demarcates the cardiogenic clonogenic Sca1+ stem/progenitor cell in adult murine myocardium. Nat. Commun. 2015, 6.
52. McNamara L.E., et al. The role of microtopography in cellular mechanotransduction. Biomaterials 2012, 33(10):2835-2847.
53. Li Y., et al. Biophysical regulation of histone acetylation in mesenchymal stem cells. Biophys. J. 2011, 100(8):1902-1909.
54. Li J., Wu M., Chu J., Sochol R., Patel S. Engineering micropatterned surfaces to modulate the function of vascular stem cells. Biochem. Biophys. Res. Commun. 2014, 444(4):562-567.
55. Roca-Cusachs P., et al. Micropatterning of single endothelial cell shape reveals a tight coupling between nuclear volume in G1 and proliferation. Biophys. J. 2008, 94(12):4984-4995.
56. Le Beyec J., et al. Cell shape regulates global histone acetylation in human mammary epithelial cells. Exp. Cell Res. 2007, 313(14):3066-3075.
57. Feng B., Ng J.H., Heng J.C., Ng H.H. Molecules that promote or enhance reprogramming of somatic cells to induced pluripotent stem cells. Cell Stem Cell 2009, 4(4):301-312.
58. Blakeslee W.W., et al. Class I HDAC inhibition stimulates cardiac protein SUMOylation through a post-translational mechanism. Cell Signal 2014, 26(12):2912-2920.
59. Wang J., et al. Myocardin sumoylation transactivates cardiogenic genes in pluripotent 10T1/2 fibroblasts. Mol. Cell Biol. 2007, 27(2):622-632.
60. Gaspar-Maia A., Alajem A., Meshorer E., Ramalho-Santos M. Open chromatin in pluripotency and reprogramming. Nat. Rev. Mol. Cell Biol. 2011, 12(1):36-47.
61. Huangfu D., et al. Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds. Nat. Biotechnol. 2008, 26(7):795-797.
62. Iwafuchi-Doi M., Zaret K.S. Pioneer transcription factors in cell reprogramming. Genes Dev. 2014, 28(24):2679-2692.
63. McCain M.L., Agarwal A., Nesmith H.W., Nesmith A.P., Parker K.K. Micromolded gelatin hydrogels for extended culture of engineered cardiac tissues. Biomaterials 2014, 35(21):5462-5471.