Direct reprogramming of fibroblasts into cardiomyocytes

Stem Cell Research and Therapy

Volumn 8, Issue 1, 2017, Pages

  Chen, Yueqiu ^a   Yang, Ziying ^a   Zhao, Zhen Ao ^a   Shen, Zhenya ^a  

^a SOOCHOW UNIVERSITY   (China)

Author keywords

Cardiomyocyte; Direct reprogramming; Fibroblast; MicroRNA; Small molecule; Transcription factor

Indexed keywords

ALPHA ACTININ; FIBROBLAST GROWTH FACTOR 10; HOMEOBOX PROTEIN NKX-2.5; MICRORNA; MICRORNA 1; MICRORNA 133; MICRORNA 208; MICRORNA 499; MYOCARDIN; MYOCYTE ENHANCER FACTOR 2; MYOD PROTEIN; MYOSIN HEAVY CHAIN ALPHA; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN V MAF; TESTIS DETERMINING FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR MAFA; TRANSCRIPTION FACTOR PDX 1; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR TBX5; TRANSFORMING GROWTH FACTOR BETA; TROPONIN; UNCLASSIFIED DRUG; VASCULOTROPIN;

APOPTOSIS; CANCER RECURRENCE; CARDIAC MUSCLE CELL; CARDIOVASCULAR DISEASE; CAUSE OF DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; FIBROBLAST; HEART INFARCTION; HUMAN; MYOFIBROBLAST; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PURKINJE FIBER; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CYTOLOGY; METABOLISM;

ANIMALS; CELLULAR REPROGRAMMING; FIBROBLASTS; HUMANS; MICRORNAS; MYOCYTES, CARDIAC; TRANSCRIPTION FACTORS;

EID: 85019926277     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/s13287-017-0569-3     Document Type: Review

References (49)

1. Kattman SJ, Witty AD, Gagliardi M, Dubois NC, Niapour M, Hotta A, et al. Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell. 2011;8:228-40.
2. Cao N, Liu Z, Chen Z, Wang J, Chen T, Zhao X, et al. Ascorbic acid enhances the cardiac differentiation of induced pluripotent stem cells through promoting the proliferation of cardiac progenitor cells. Cell Res. 2012;22:219-36.
3. Wang X, From AH, Zhang J. Myocardial regeneration: the role of progenitor cells derived from bone marrow and heart. Prog Mol Biol Transl Sci. 2012;111:195-215.
4. Tane S, Kubota M, Okayama H, Ikenishi A, Yoshitome S, Iwamoto N, et al. Repression of cyclin D1 expression is necessary for the maintenance of cell cycle exit in adult mammalian cardiomyocytes. J Biol Chem. 2014;289:18033-44.
5. Gnecchi M, Pisano F, Bariani R. microRNA and cardiac regeneration. Adv Exp Med Biol. 2015;887:119-41.
6. Fu JD, Stone NR, Liu L, Spencer CI, Qian L, Hayashi Y, Delgado-Olguin P, Ding S, Bruneau BG, Srivastava D. Direct reprogramming of human fibroblasts toward a cardiomyocyte-like state. Stem Cell Rep. 2013;1:235-47.
7. Palazzolo G, Quattrocelli M, Toelen J, Dominici R, Anastasia L, Tettamenti G et al. Cardiac niche influences the direct reprogramming of canine fibroblasts into cardiomyocyte-like cells. Stem Cells International. 2016. doi: 10.1155/2016/4969430.
8. van den Borne SW, Diez J, Blankesteijn WM, Verjans J, Hofstra L, Narula J. Myocardial remodeling after infarction: the role of myofibroblasts. Nat Rev Cardiol. 2010;7:30-7.
9. Talman V, Ruskoaho H. Cardiac fibrosis in myocardial infarction - from repair and remodeling to regeneration. Cell Tissue Res. 2016;365:563-81.
10. Choi J, Costa ML, Mermelstein CS, Chagas C, Holtzer S, Holtzer H. MyoD converts primary dermal fibroblasts, chondroblasts, smooth muscle, and retinal pigmented epithelial cells into striated mononucleated myoblasts and multinucleated myotubes. Proc Natl Acad Sci U S A. 1990;87:7988-92.
11. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663-76.
12. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131:861-72.
13. Zhou Q, Brown J, Kanarek A, Rajagopal J, Melton DA. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature. 2008;455:627-32.
14. Song K, Nam YJ, Luo X, Qi X, Tan W, Huang GN, Acharya A, Smith CL, Tallquist MD, Neilson EG, Hill JA, Bassel-Duby R, Olson EN. Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature. 2012;485:599-604.
15. Ieda M, Fu JD, Delgado-Olguin P, Vedantham V, Hayashi Y, Bruneau BG, Srivastava D. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell. 2010;142:375-86.
16. Qian L, Huang Y, Spencer CI, Foley A, Vedantham V, Liu L, Conway SJ, Fu JD, Srivastava D. In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature. 2012;485:593-8.
17. Lee K, Yu P, Lingampalli N, Kim HJ, Tang R, Murthy N. Peptide-enhanced mRNA transfection in cultured mouse cardiac fibroblasts and direct reprogramming towards cardiomyocyte-like cells. Int J Nanomedicine. 2015;10:1841-54.
18. Li XH, Li Q, Jiang L, Deng C, Liu Z, Fu Y, et al. Generation of functional human cardiac progenitor cells by high-efficiency protein transduction. Stem Cells Transl Med. 2015;4:1415-24.
19. Ifkovits JL, Addis RC, Epstein JA, Gearhart JD. Inhibition of TGFbeta signaling increases direct conversion of fibroblasts to induced cardiomyocytes. PLoS One. 2014;9:e89678.
20. Zhao Y, Londono P, Cao Y, Sharpe EJ, Proenza C, O'Rourke R, et al. High-efficiency reprogramming of fibroblasts into cardiomyocytes requires suppression of pro-fibrotic signalling. Nat Commun. 2015;6:8243.
21. Yamakawa H, Muraoka N, Miyamoto K, Sadahiro T, Isomi M, Haginiwa S, et al. FFV promote cardiac reprogramming under defined conditions. Stem Cell Rep. 2015;5:1128-42.
22. Rao PK, Toyama Y, Chiang HR, Gupta S, Bauer M, Medvid R, et al. Loss of cardiac microRNA-mediated regulation leads to dilated cardiomyopathy and heart failure. Circ Res. 2009;105:585-94.
23. Jayawardena TM, Egemnazarov B, Finch EA, Zhang L, Payne JA, Pandya K, et al. MicroRNA-mediated in vitro and in vivo direct reprogramming of cardiac fibroblasts to cardiomyocytes. Circ Res. 2012;110:1465-73.
24. Jayawardena TM, Finch EA, Zhang L, Zhang H, Hodgkinson CP, Pratt RE, et al. MicroRNA induced cardiac reprogramming in vivo: evidence for mature cardiac myocytes and improved cardiac function. Circ Res. 2015;116:418-24.
25. Vaseghi H, Liu J, Qian L. Molecular barriers to direct cardiac reprogramming. Protein Cell. 2017. doi: 10.1007/s13238-017-0402-x.
26. Bondue A, Lapouge G, Paulissen C, Semeraro C, Iacovino M, Kyba M, et al. Mesp1 acts as a master regulator of multipotent cardiovascular progenitor specification. Cell Stem Cell. 2008;3:69-84.
27. Liu L, Yuan Y, He X, Xia X, Mo X. MicroRNA-1 upregulation promotes myocardiocyte proliferation and suppresses apoptosis during heart development. Mol Med Rep. 2017;15:2837-42.
28. Muraoka N, Yamakawa H, Miyamoto K, Sadahiro T, Umei T, Isomi M, et al. MiR-133 promotes cardiac reprogramming by directly repressing Snai1 and silencing fibroblast signatures. EMBO J. 2014;33:1565-81.
29. Efe JA, Hilcove S, Kim J, Zhou H, Ouyang K, Wang G, et al. Conversion of mouse fibroblasts into cardiomyocytes using a direct reprogramming strategy. Nat Cell Biol. 2011;13:215-22.
30. Fu Y, Huang C, Xu X, Gu H, Ye Y, Jiang C, et al. Direct reprogramming of mouse fibroblasts into cardiomyocytes with chemical cocktails. Cell Res. 2015;25:1013-24.
31. Nam YJ, Song KH, Luo X, Daniel E, Lambeth K, West K, et al. Reprogramming of human fibroblasts toward a cardiac fate. Proc Natl Acad Sci U S A. 2013;110:5588-93.
32. Wada R, Muraoka N, Inagawa K, Yamakawa H, Miyamoto K, Sadahiro T, et al. Induction of human cardiomyocyte-like cells from fibroblasts by defined factors. Proc Natl Acad Sci U S A. 2013;110:12667-72.
33. Li K, Zhu S, Russ HA, Xu S, Xu T, Zhang Y, et al. Small molecules facilitate the reprogramming of mouse fibroblasts into pancreatic lineages. Cell Stem Cell. 2014;14:228-36.
34. Zhu S, Ambasudhan R, Sun W, Kim HJ, Talantova M, Wang X, et al. Small molecules enable OCT4-mediated direct reprogramming into expandable human neural stem cells. Cell Res. 2014;24:126-9.
35. Wang H, Cao N, Spencer CI, Nie B, Ma T, Xu T, Zhang Y, Wang X, Srivastava D, Ding S. Small molecules enable cardiac reprogramming of mouse fibroblasts with a single factor, Oct4. Cell Rep. 2014;6:951-60.
36. Cao N, Huang Y, Zheng J, Spencer CI, Zhang Y, Fu JD, Nie B, Xie M, Zhang M, Wang H, Ma T, Xu T, Shi G, Srivastava D, Ding S. Conversion of human fibroblasts into functional cardiomyocytes by small molecules. Science. 2016;352:1216-20.
37. Palazzolo G, Quattrocelli M, Toelen J, Dominici R, Anastasia L, Tettamenti G, et al. Cardiac niche influences the direct reprogramming of canine fibroblasts into cardiomyocyte-like cells. Stem Cells Int. 2016;2016:4969430.
38. Yang X, Pabon L, Murry CE. Engineering adolescence: maturation of human pluripotent stem cell-derived cardiomyocytes. Circ Res. 2014;114:511-23.
39. Kong CW, Chen S, Geng L, Shum AM, Sun D, Li RA. Increasing the physical size and nucleation status of human pluripotent stem cell-derived ventricular cardiomyocytes by cell fusion. Stem Cell Res. 2017;19:76-81.
40. Passier R, Mummery C. Getting to the heart of the matter: direct reprogramming to cardiomyocytes. Cell Stem Cell. 2010;7:139-41.
41. Fu JD, Srivastava D. Direct reprogramming of fibroblasts into cardiomyocytes for cardiac regenerative medicine. Circ J. 2015;79:245-54.
42. Christoforou N, Chellappan M, Adler AF, Kirkton RD, Wu T, Addis RC, 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:e63577.
43. Addis RC, Ifkovits JL, Pinto F, Kellam LD, Esteso P, Rentschler S, et al. Optimization of direct fibroblast reprogramming to cardiomyocytes using calcium activity as a functional measure of success. J Mol Cell Cardiol. 2013;60:97-106.
44. Smith AW, Hoyne JD, Nguyen PK, McCreedy DA, Aly H, Efimov IR, et al. Direct reprogramming of mouse fibroblasts to cardiomyocyte-like cells using Yamanaka factors on engineered poly(ethylene glycol) (PEG) hydrogels. Biomaterials. 2013;34:6559-71.
45. Hirai H, Katoku-Kikyo N, Keirstead SA, Kikyo N. Accelerated direct reprogramming of fibroblasts into cardiomyocyte-like cells with the MyoD transactivation domain. Cardiovasc Res. 2013;100:105-13.
46. Hirai H, Kikyo N. Inhibitors of suppressive histone modification promote direct reprogramming of fibroblasts to cardiomyocyte-like cells. Cardiovasc Res. 2014;102:188-90.
47. Nam YJ, Lubczyk C, Bhakta M, Zang T, Fernandez-Perez A, McAnally J, et al. Induction of diverse cardiac cell types by reprogramming fibroblasts with cardiac transcription factors. Development. 2014;141:4267-78.
48. Talkhabi M, Pahlavan S, Aghdami N, Baharvand H. Ascorbic acid promotes the direct conversion of mouse fibroblasts into beating cardiomyocytes. Biochem Biophys Res Commun. 2015;463:699-705.
49. Islas JF, Liu Y, Weng KC, Robertson MJ, Zhang S, Prejusa A, et al. Transcription factors ETS2 and MESP1 transdifferentiate human dermal fibroblasts into cardiac progenitors. Proc Natl Acad Sci U S A. 2012;109:13016-21.