Reprogramming cell fate: A changing story

Frontiers in Cell and Developmental Biology

Volumn 2, Issue AUG, 2014, Pages

  Chin, Michael T ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Cell fate; Direct reprogramming; Lineage determination; Regenerative medicine; Transdifferentiation

Indexed keywords

EID: 84956590269     PISSN: None     EISSN: 2296634X     Source Type: Journal    
DOI: 10.3389/fcell.2014.00046     Document Type: Short Survey

References (77)

1. Addis, R. C., and Epstein, J. A. (2013). Induced regeneration-the progress and promise of direct reprogramming for heart repair. Nat. Med. 19, 829-836. doi: 10.1038/nm.3225
2. Addis, R. C., Ifkovits, J. L., Pinto, F., Kellam, L. D., Esteso, P., Rentschler, S., et al. (2013). Optimization of direct fibroblast reprogramming to cardiomyocytes using calcium activity as a functional measure of success. J. Mol. Cell. Cardiol. 60, 97-106. doi: 10.1016/j.yjmcc.2013.04.004
3. Ambasudhan, R., Talantova, M., Coleman, R., Yuan, X., Zhu, S., Lipton, S. A., et al. (2011). Direct reprogramming of adult human fibroblasts to functional neurons under defined conditions. Cell Stem Cell 9, 113-118. doi: 10.1016/j.stem.2011.07.002
4. Beisel, C., and Paro, R. (2011). Silencing chromatin: comparing modes and mechanisms. Nat. Rev. Genet. 12, 123-135. doi: 10.1038/nrg2932
5. Blau, H. M., Chiu, C. P., and Webster, C. (1983). Cytoplasmic activation of human nuclear genes in stable heterocaryons. Cell 32, 1171-1180. doi: 10.1016/0092-8674(83)90300-8
6. Burridge, P. W., Matsa, E., Shukla, P., Lin, Z. C., Churko, J. M., Ebert, A. D., et al. (2014). Chemically defined generation of human cardiomyocytes. Nat. Methods 11, 855-860. doi: 10.1038/nmeth.2999
7. Caiazzo, M., Dell'Anno, M. T., Dvoretskova, E., Lazarevic, D., Taverna, S., Leo, D., et al. (2011). Direct generation of functional dopaminergic neurons from mouse and human fibroblasts. Nature 476, 224-227. doi: 10.1038/nature10284
8. Campbell, K. H., McWhir, J., Ritchie, W. A., and Wilmut, I. (1996). Sheep cloned by nuclear transfer from a cultured cell line. Nature 380, 64-66. doi: 10.1038/380064a0
9. Chen, J. X., Krane, M., Deutsch, M. A., Wang, L., Rav-Acha, M., Gregoire, S., et al. (2012). Inefficient reprogramming of fibroblasts into cardiomyocytes using Gata4, Mef2c, and Tbx5. Circ. Res. 111, 50-55. doi: 10.1161/CIRCRESAHA.112.270264
10. Christoforou, N., Chellappan, M., Adler, A. F., Kirkton, R. D., Wu, T., Addis, R. C., et al. (2013). Transcription factors MYOCD, SRF, Mesp1 and SMARCD3 enhance the cardio-inducing effect of GATA4, TBX5, and MEF2C during direct cellular reprogramming. PLoS ONE 8:e63577. doi: 10.1371/journal.pone.0063577
11. Cordes, K. R., Sheehy, N. T., White, M. P., Berry, E. C., Morton, S. U., Muth, A. N., et al. (2009). miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 460, 705-710. doi: 10.1038/nature08195
12. Crescini, E., Gualandi, L., Uberti, D., Prandelli, C., Presta, M., and Dell'Era, P. (2013). Ascorbic acid rescues cardiomyocyte development in Fgfr1(-/-) murine embryonic stem cells. Biochim. Biophys. Acta 1833, 140-147. doi: 10.1016/j.bbamcr.2012.06.024
13. Davis, R. L., Weintraub, H., and Lassar, A. B. (1987). Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51, 987-1000. doi: 10.1016/0092-8674(87)90585-X
14. Efe, J. A., Hilcove, S., Kim, J., Zhou, H., Ouyang, K., Wang, G., et al. (2011). Conversion of mouse fibroblasts into cardiomyocytes using a direct reprogramming strategy. Nat. Cell Biol. 13, 215-222. doi: 10.1038/ncb2164
15. Egli, D., Birkhoff, G., and Eggan, K. (2008). Mediators of reprogramming: transcription factors and transitions through mitosis. Nat. Rev. Mol. Cell Biol. 9, 505-516. doi: 10.1038/nrm2439
16. Feng, R., Desbordes, S. C., Xie, H., Tillo, E. S., Pixley, F., Stanley, E. R., et al. (2008). PU.1 and C/EBPalpha/beta convert fibroblasts into macrophage-like cells. Proc. Natl. Acad. Sci. U.S.A. 105, 6057-6062. doi: 10.1073/pnas.0711961105
17. Ferber, S., Halkin, A., Cohen, H., Ber, I., Einav, Y., Goldberg, I., et al. (2000). Pancreatic and duodenal homeobox gene 1 induces expression of insulin genes in liver and ameliorates streptozotocin-induced hyperglycemia. Nat. Med. 6, 568-572. doi: 10.1038/75050
18. Fu, J. D., Stone, N. R., Liu, L., Spencer, C. I., Qian, L., Hayashi, Y., et al. (2013). Direct reprogramming of human fibroblasts toward a cardiomyocyte-like state. Stem Cell Reports 1, 235-247. doi: 10.1016/j.stemcr.2013.07.005
19. Ginsberg, M., James, D., Ding, B. S., Nolan, D., Geng, F., Butler, J. M., et al. (2012). Efficient direct reprogramming of mature amniotic cells into endothelial cells by ETS factors and TGFbeta suppression. Cell 151, 559-575. doi: 10.1016/j.cell.2012.09.032
20. Guo, Z., Zhang, L., Wu, Z., Chen, Y., Wang, F., and Chen, G. (2014). In vivo direct reprogramming of reactive glial cells into functional neurons after brain injury and in an Alzheimer's disease model. Cell Stem Cell 14, 188-202. doi: 10.1016/j.stem.2013.12.001
21. Gurdon, J. B., Elsdale, T. R., and Fischberg, M. (1958). Sexually mature individuals of Xenopus laevis from the transplantation of single somatic nuclei. Nature 182, 64-65. doi: 10.1038/182064a0
22. Hanna, J., Saha, K., Pando, B., van Zon, J., Lengner, C. J., Creyghton, M. P., et al. (2009). Direct cell reprogramming is a stochastic process amenable to acceleration. Nature 462, 595-601. doi: 10.1038/nature08592
23. Hanna, J. H., Saha, K., and Jaenisch, R. (2010). Pluripotency and cellular reprogramming: facts, hypotheses, unresolved issues. Cell 143, 508-525. doi: 10.1016/j.cell.2010.10.008
24. Heinrich, C., Blum, R., Gascon, S., Masserdotti, G., Tripathi, P., Sanchez, R., et al. (2010). Directing astroglia from the cerebral cortex into subtype specific functional neurons. PLoS Biol. 8:e1000373. doi: 10.1371/journal.pbio.1000373
25. Heyworth, C., Pearson, S., May, G., and Enver, T. (2002). Transcription factor-mediated lineage switching reveals plasticity in primary committed progenitor cells. EMBO J. 21, 3770-3781. doi: 10.1093/emboj/cdf368
26. Hirai, H., Katoku-Kikyo, N., Keirstead, S. A., and Kikyo, N. (2013). Accelerated direct reprogramming of fibroblasts into cardiomyocyte-like cells with the MyoD transactivation domain. Cardiovasc. Res. 100, 105-113. doi: 10.1093/cvr/cvt167
27. Hirai, H., and Kikyo, N. (2014). Inhibitors of suppressive histone modification promote direct reprogramming of fibroblasts to cardiomyocyte-like cells. Cardiovasc. Res. 102, 188-190. doi: 10.1093/cvr/cvu023
28. Huang, P., He, Z., Ji, S., Sun, H., Xiang, D., Liu, C., et al. (2011). Induction of functional hepatocyte-like cells from mouse fibroblasts by defined factors. Nature 475, 386-389. doi: 10.1038/nature10116
29. Ieda, M., Fu, J. D., Delgado-Olguin, P., Vedantham, V., Hayashi, Y., Bruneau, B. G., et al. (2010). Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142, 375-386. doi: 10.1016/j.cell.2010.07.002
30. Ifkovits, J. L., Addis, R. C., Epstein, J. A., and Gearhart, J. D. (2014). Inhibition of TGFbeta signaling increases direct conversion of fibroblasts to induced cardiomyocytes. PLoS ONE 9:e89678. doi: 10.1371/journal.pone.0089678
31. Inagawa, K., Miyamoto, K., Yamakawa, H., Muraoka, N., Sadahiro, T., Umei, T., et al. (2012). Induction of cardiomyocyte-like cells in infarct hearts by gene transfer of Gata4, Mef2c, and Tbx5. Circ. Res. 111, 1147-1156. doi: 10.1161/CIRCRESAHA.112.271148
32. Islas, J. F., Liu, Y., Weng, K. C., Robertson, M. J., Zhang, S., Prejusa, A., et al. (2012). Transcription factors ETS2 and MESP1 transdifferentiate human dermal fibroblasts into cardiac progenitors. Proc. Natl. Acad. Sci. U.S.A. 109, 13016-13021. doi: 10.1073/pnas.1120299109
33. Jayawardena, T. M., Egemnazarov, B., Finch, E. A., Zhang, L., Payne, J. A., Pandya, K., et al. (2012). MicroRNA-mediated in vitro and in vivo direct reprogramming of cardiac fibroblasts to cardiomyocytes. Circ. Res. 110, 1465-1473. doi: 10.1161/CIRCRESAHA.112.269035
34. Karamariti, E., Margariti, A., Winkler, B., Wang, X., Hong, X., Baban, D., et al. (2013). Smooth muscle cells differentiated from reprogrammed embryonic lung fibroblasts through DKK3 signaling are potent for tissue engineering of vascular grafts. Circ. Res. 112, 1433-1443. doi: 10.1161/CIRCRESAHA.111.300415
35. Kim, K., Doi, A., Wen, B., Ng, K., Zhao, R., Cahan, P., et al. (2010). Epigenetic memory in induced pluripotent stem cells. Nature 467, 285-290. doi: 10.1038/nature09342
36. Kim, K., Zhao, R., Doi, A., Ng, K., Unternaehrer, J., Cahan, P., et al. (2011). Donor cell type can influence the epigenome and differentiation potential of human induced pluripotent stem cells. Nat. Biotechnol. 29, 1117-1119. doi: 10.1038/nbt.2052
37. Kulessa, H., Frampton, J., and Graf, T. (1995). GATA-1 reprograms avian myelomonocytic cell lines into eosinophils, thromboblasts, and erythroblasts. Genes Dev. 9, 1250-1262. doi: 10.1101/gad.9.10.1250
38. Lassar, A. B., Paterson, B. M., and Weintraub, H. (1986). Transfection of a DNA locus that mediates the conversion of 10T1/2 fibroblasts to myoblasts. Cell 47, 649-656. doi: 10.1016/0092-8674(86)90507-6
39. Lin, C., Yu, C., and Ding, S. (2013). Toward directed reprogramming through exogenous factors. Curr. Opin. Genet. Dev. 23, 519-525. doi: 10.1016/j.gde.2013.06.002
40. Liu, M. L., Zang, T., Zou, Y., Chang, J. C., Gibson, J. R., Huber, K. M., et al. (2013). Small molecules enable neurogenin 2 to efficiently convert human fibroblasts into cholinergic neurons. Nat. Commun. 4, 2183. doi: 10.1038/ncomms3183
41. Lujan, E., Chanda, S., Ahlenius, H., Sudhof, T. C., and Wernig, M. (2012). Direct conversion of mouse fibroblasts to self-renewing, tripotent neural precursor cells. Proc. Natl. Acad. Sci. U.S.A. 109, 2527-2532. doi: 10.1073/pnas.1121003109
42. Lumelsky, N. (2014). Small molecules convert fibroblasts into islet-like cells avoiding pluripotent state. Cell Metab. 19, 551-552. doi: 10.1016/j.cmet.2014.03.019
43. Marro, S., Pang, Z. P., Yang, N., Tsai, M. C., Qu, K., Chang, H. Y., et al. (2011). Direct lineage conversion of terminally differentiated hepatocytes to functional neurons. Cell Stem Cell 9, 374-382. doi: 10.1016/j.stem.2011.09.002
44. Mitchell, R., Szabo, E., Shapovalova, Z., Aslostovar, L., Makondo, K., and Bhatia, M. (2014a). Molecular evidence for OCT4 induced plasticity in adult human fibroblasts required for direct cell fate conversion to lineage specific progenitors. Stem Cells. 32, 2178-2187. doi: 10.1002/stem.1721
45. Mitchell, R. R., Szabo, E., Benoit, Y. D., Case, D. T., Mechael, R., Alamilla, J., et al. (2014b). Activation of neural cell fate programs toward direct conversion of adult human fibroblasts into Tri-potent neural progenitors using OCT-4. Stem Cells Dev. 23, 1937-1946. doi: 10.1089/scd.2014.0023
46. Morris, S. A., and Daley, G. Q. (2013). A blueprint for engineering cell fate: current technologies to reprogram cell identity. Cell Res. 23, 33-48. doi: 10.1038/cr.2013.1
47. Muraoka, N., Yamakawa, H., Miyamoto, K., Sadahiro, T., Umei, T., Isomi, M., et al. (2014). MiR-133 promotes cardiac reprogramming by directly repressing Snai1 and silencing fibroblast signatures. EMBO J. 33, 1565-1581. doi: 10.15252/embj.201387605
48. Nam, Y. J., Song, K., Luo, X., Daniel, E., Lambeth, K., West, K., et al. (2013). Reprogramming of human fibroblasts toward a cardiac fate. Proc. Natl. Acad. Sci. U.S.A. 110, 5588-5593. doi: 10.1073/pnas.1301019110
49. Nerlov, C., and Graf, T. (1998). PU.1 induces myeloid lineage commitment in multipotent hematopoietic progenitors. Genes Dev. 12, 2403-2412. doi: 10.1101/gad.12.15.2403
50. Ng, R. K., and Gurdon, J. B. (2005). Epigenetic memory of active gene transcription is inherited through somatic cell nuclear transfer. Proc. Natl. Acad. Sci. U.S.A. 102, 1957-1962. doi: 10.1073/pnas.0409813102
51. Palii, C. G., Perez-Iratxeta, C., Yao, Z., Cao, Y., Dai, F., Davison, J., et al. (2011). Differential genomic targeting of the transcription factor TAL1 in alternate haematopoietic lineages. EMBO J. 30, 494-509. doi: 10.1038/emboj.2010.342
52. Pang, Z. P., Yang, N., Vierbuchen, T., Ostermeier, A., Fuentes, D. R., Yang, T. Q., et al. (2011). Induction of human neuronal cells by defined transcription factors. Nature 476, 220-223. doi: 10.1038/nature10202
53. Pfisterer, U., Kirkeby, A., Torper, O., Wood, J., Nelander, J., Dufour, A., et al. (2011). Direct conversion of human fibroblasts to dopaminergic neurons. Proc. Natl. Acad. Sci. U.S.A. 108, 10343-10348. doi: 10.1073/pnas.1105135108
54. Polo, J. M., Liu, S., Figueroa, M. E., Kulalert, W., Eminli, S., Tan, K. Y., et al. (2010). Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat. Biotechnol. 28, 848-855. doi: 10.1038/nbt.1667
55. Protze, S., Khattak, S., Poulet, C., Lindemann, D., Tanaka, E. M., and Ravens, U. (2012). A new approach to transcription factor screening for reprogramming of fibroblasts to cardiomyocyte-like cells. J. Mol. Cell. Cardiol. 53, 323-332. doi: 10.1016/j.yjmcc.2012.04.010
56. Qian, L., Huang, Y., Spencer, C. I., Foley, A., Vedantham, V., Liu, L., et al. (2012). In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 485, 593-598. doi: 10.1038/nature11044
57. Qiang, L., Fujita, R., Yamashita, T., Angulo, S., Rhinn, H., Rhee, D., et al. (2011). Directed conversion of Alzheimer's disease patient skin fibroblasts into functional neurons. Cell 146, 359-371. doi: 10.1016/j.cell.2011.07.007
58. Robinton, D. A., and Daley, G. Q. (2012). The promise of induced pluripotent stem cells in research and therapy. Nature 481, 295-305. doi: 10.1038/nature10761
59. Sekiya, S., and Suzuki, A. (2011). Direct conversion of mouse fibroblasts to hepatocyte-like cells by defined factors. Nature 475, 390-393. doi: 10.1038/nature10263
60. Son, E. Y., Ichida, J. K., Wainger, B. J., Toma, J. S., Rafuse, V. F., Woolf, C. J., et al. (2011). Conversion of mouse and human fibroblasts into functional spinal motor neurons. Cell Stem Cell 9, 205-218. doi: 10.1016/j.stem.2011.07.014
61. Song, K., Nam, Y. J., Luo, X., Qi, X., Tan, W., Huang, G. N., et al. (2012). Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature 485, 599-604. doi: 10.1038/nature11139
62. Taberlay, P. C., Kelly, T. K., Liu, C. C., You, J. S., De Carvalho, D. D., Miranda, T. B., et al. (2011). Polycomb-repressed genes have permissive enhancers that initiate reprogramming. Cell 147, 1283-1294. doi: 10.1016/j.cell.2011.10.040
63. Takahashi, K., and Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676. doi: 10.1016/j.cell.2006.07.024
64. Taylor, S. M., and Jones, P. A. (1979). Multiple new phenotypes induced in 10T1/2 and 3T3 cells treated with 5-azacytidine. Cell 17, 771-779. doi: 10.1016/0092-8674(79)90317-9
65. Torper, O., Pfisterer, U., Wolf, D. A., Pereira, M., Lau, S., Jakobsson, J., et al. (2013). Generation of induced neurons via direct conversion in vivo. Proc. Natl. Acad. Sci. U.S.A. 110, 7038-7043. doi: 10.1073/pnas.1303829110
66. Vierbuchen, T., Ostermeier, A., Pang, Z. P., Kokubu, Y., Sudhof, T. C., and Wernig, M. (2010). Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463, 1035-1041. doi: 10.1038/nature08797
67. Vierbuchen, T., and Wernig, M. (2012). Molecular roadblocks for cellular reprogramming. Mol. Cell 47, 827-838. doi: 10.1016/j.molcel.2012.09.008
68. Visvader, J. E., Elefanty, A. G., Strasser, A., and Adams, J. M. (1992). GATA-1 but not SCL induces megakaryocytic differentiation in an early myeloid line. EMBO J. 11, 4557-4564.
69. Wada, R., Muraoka, N., Inagawa, K., Yamakawa, H., Miyamoto, K., Sadahiro, T., et al. (2013). Induction of human cardiomyocyte-like cells from fibroblasts by defined factors. Proc. Natl. Acad. Sci. U.S.A. 110, 12667-12672. doi: 10.1073/pnas.1304053110
70. Wakayama, T., Perry, A. C., Zuccotti, M., Johnson, K. R., and Yanagimachi, R. (1998). Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 394, 369-374. doi: 10.1038/28615
71. Weintraub, H., Tapscott, S. J., Davis, R. L., Thayer, M. J., Adam, M. A., Lassar, A. B., et al. (1989). Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD. Proc. Natl. Acad. Sci. U.S.A. 86, 5434-5438. doi: 10.1073/pnas.86.14.5434
72. Wilson, N. K., Foster, S. D., Wang, X., Knezevic, K., Schutte, J., Kaimakis, P., et al. (2010). Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell 7, 532-544. doi: 10.1016/j.stem.2010.07.016
73. Xie, H., Ye, M., Feng, R., and Graf, T. (2004). Stepwise reprogramming of B cells into macrophages. Cell 117, 663-676. doi: 10.1016/S0092-8674(04)00419-2
74. Yoo, A. S., Sun, A. X., Li, L., Shcheglovitov, A., Portmann, T., Li, Y., et al. (2011). MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 476, 228-231. doi: 10.1038/nature10323
75. Zaret, K. S., and Carroll, J. S. (2011). Pioneer transcription factors: establishing competence for gene expression. Genes Dev. 25, 2227-2241. doi: 10.1101/gad.176826.111
76. Zhou, Q., Brown, J., Kanarek, A., Rajagopal, J., and Melton, D. A. (2008). In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 455, 627-632. doi: 10.1038/nature07314
77. Zhu, S., Ambasudhan, R., Sun, W., Kim, H. J., Talantova, M., Wang, X., et al. (2014). Small molecules enable OCT4-mediated direct reprogramming into expandable human neural stem cells. Cell Res. 24, 126-129. doi: 10.1038/cr.2013.156