The developmental potential of iPSCs is greatly influenced by reprogramming factor selection

Cell Stem Cell

Volumn 15, Issue 3, 2014, Pages 295-309

  Buganim, Yosef ^b   Markoulaki, Styliani ^a   Van Wietmarschen, Niek ^c   Hoke, Heather ^a,d   Wu, Tao ^e   Ganz, Kibibi ^a   Akhtar Zaidi, Batool ^a   He, Yupeng ^f   Abraham, Brian J ^a   Porubsky, David ^c   Kulenkampff, Elisabeth ^a   Faddah, Dina A ^a,d   Shi, Linyu ^a   Gao, Qing ^a   Sarkar, Sovan ^a   Cohen, Malkiel ^a   Goldmann, Johanna ^a   Nery, Joseph R ^f   Schultz, Matthew D ^f   Ecker, Joseph R ^f   Xiao, Andrew ^e   Young, Richard A ^a,d,g   Lansdorp, Peter M ^c,g   Jaenisch, Rudolf ^a,d,g   more..

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b HEBREW UNIVERSITY   (Israel)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^g SKOLKOVO INSTITUTE OF SCIENCE AND TECHNOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2AX; KRUPPEL LIKE FACTOR 4; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ESRRB; TRANSCRIPTION FACTOR LIN28; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SALL4; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; H2AX PROTEIN, MOUSE; HISTONE; MESSENGER RNA;

ADULT; ANEUPLOIDY; ANIMAL CELL; ARTICLE; CELL SELECTION; CHIMERA; CHROMOSOME 8; CONTROLLED STUDY; EMBRYO; ENHANCER REGION; FEMALE; FETUS; GENE EXPRESSION; GENETIC COMPLEMENTATION; METHYLATION; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; TETRAPLOIDY; TRISOMY; ANIMAL; C57BL MOUSE; CELL LINE; DBA MOUSE; DNA METHYLATION; EMBRYONIC STEM CELL; GENE EXPRESSION PROFILING; GENETICS; GENOME; HUMAN; INDUCED PLURIPOTENT STEM CELL; METABOLISM; NUCLEAR REPROGRAMMING;

MUS;

ANIMALS; CELL LINE; CELLULAR REPROGRAMMING; CHIMERA; CHROMOSOMES, HUMAN, PAIR 8; DNA METHYLATION; EMBRYONIC STEM CELLS; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION PROFILING; GENOME; HISTONES; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICE, INBRED C57BL; MICE, INBRED DBA; RNA, MESSENGER; TRANSCRIPTION FACTORS; TRISOMY;

EID: 84918548171     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2014.07.003     Document Type: Article

References (62)

1. Audo, I., Bujakowska, K.M., Léveillard, T., Mohand-Saïd, S., Lancelot, M.E., Germain, A., Antonio, A., Michiels, C., Saraiva, J.P., Letexier, M., et al. (2012). Development and application of a next-generation-sequencing (NGS) approach to detect known and novel gene defects underlying retinal diseases. Orphanet J. Rare Dis. 7, 8.
2. Bar-Nur, O., Russ, H.A., Efrat, S., and Benvenisty, N. (2011). Epigenetic memory and preferential lineage-specific differentiation in induced pluripotent stem cells derived from human pancreatic islet beta cells. Cell Stem Cell 9, 17-23.
3. Barlow, J.H., Faryabi, R.B., Callén, E., Wong, N., Malhowski, A., Chen, H.T., Gutierrez-Cruz, G., Sun, H.W., McKinnon, P., Wright, G., et al. (2013). Identification of early replicating fragile sites that contribute to genome instability. Cell 152, 620-632.
4. Beard, C., Hochedlinger, K., Plath, K., Wutz, A., and Jaenisch, R. (2006). Efficient method to generate single-copy transgenic mice by site-specific integration in embryonic stem cells. Genesis 44, 23-28.
5. Boland, M.J., Hazen, J.L., Nazor, K.L., Rodriguez, A.R., Gifford, W., Martin, G., Kupriyanov, S., and Baldwin, K.K. (2009). Adult mice generated from induced pluripotent stem cells. Nature 461, 91-94.
6. Bonner, W.M., Redon, C.E., Dickey, J.S., Nakamura, A.J., Sedelnikova, O.A., Solier, S., and Pommier, Y. (2008). GammaH2AX and cancer. Nat. Rev. Cancer 8, 957-967.
7. Brambrink, T., Hochedlinger, K., Bell, G., and Jaenisch, R. (2006). ES cells derived from cloned and fertilized blastocysts are transcriptionally and functionally indistinguishable. Proc. Natl. Acad. Sci. USA 103, 933-938.
8. Buganim, Y., Faddah, D.A., Cheng, A.W., Itskovich, E., Markoulaki, S., Ganz, K., Klemm, S.L., van Oudenaarden, A., and Jaenisch, R. (2012). Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase. Cell 150, 1209-1222.
9. Buganim, Y., Faddah, D.A., and Jaenisch, R. (2013). Mechanisms and models of somatic cell reprogramming. Nat. Rev. Genet. 14, 427-439.
10. Carey, B.W., Markoulaki, S., Hanna, J.H., Faddah, D.A., Buganim, Y., Kim, J., Ganz, K., Steine, E.J., Cassady, J.P., Creyghton, M.P., et al. (2011). Reprogramming factor stoichiometry influences the epigenetic state and biological properties of induced pluripotent stem cells. Cell Stem Cell 9, 588-598.
11. Chen, J., Liu, J., Chen, Y., Yang, J., Chen, J., Liu, H., Zhao, X., Mo, K., Song, H., Guo, L., et al. (2011). Rational optimization of reprogramming culture conditions for the generation of induced pluripotent stem cells with ultra-high efficiency and fast kinetics. Cell Res. 21, 884-894.
12. Chin, M.H., Mason, M.J., Xie, W., Volinia, S., Singer, M., Peterson, C., Ambartsumyan, G., Aimiuwu, O., Richter, L., Zhang, J., et al. (2009). Induced pluripotent stem cells and embryonic stem cells are distinguished by gene expression signatures. Cell Stem Cell 5, 111-123.
13. Cho, J., Chang, H., Kwon, S.C., Kim, B., Kim, Y., Choe, J., Ha, M., Kim, Y.K., and Kim, V.N. (2012). LIN28A is a suppressor of ER-associated translation in embryonic stem cells. Cell 151, 765-777.
14. Doi, A., Park, I.H., Wen, B., Murakami, P., Aryee, M.J., Irizarry, R., Herb, B., Ladd-Acosta, C., Rho, J., Loewer, S., et al. (2009). Differential methylation of tissue-and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat. Genet. 41, 1350-1353.
15. Esteban, M.A., and Pei, D. (2012). Vitamin C improves the quality of somatic cell reprogramming. Nat. Genet. 44, 366-367.
16. Falconer, E., Hills, M., Naumann, U., Poon, S.S., Chavez, E.A., Sanders, A.D., Zhao, Y., Hirst, M., and Lansdorp, P.M. (2012). DNA template strand sequencing of single-cells maps genomic rearrangements at high resolution. Nat. Methods 9, 1107-1112.
17. Festuccia, N., Osorno, R., Halbritter, F., Karwacki-Neisius, V., Navarro, P., Colby, D., Wong, F., Yates, A., Tomlinson, S.R., and Chambers, I. (2012). Esrrb is a direct Nanog target gene that can substitute for Nanog function in pluripotent cells. Cell Stem Cell 11, 477-490.
18. González, F., Georgieva, D., Vanoli, F., Shi, Z.D., Stadtfeld, M., Ludwig, T., Jasin, M., and Huangfu, D. (2013). Homologous recombination DNA repair genes play a critical role in reprogramming to a pluripotent state. Cell Reports 3, 651-660.
19. Gore, A., Li, Z., Fung, H.L., Young, J.E., Agarwal, S., Antosiewicz-Bourget, J., Canto, I., Giorgetti, A., Israel, M.A., Kiskinis, E., et al. (2011). Somatic coding mutations in human induced pluripotent stem cells. Nature 471, 63-67.
20. Graf, T., and Enver, T. (2009). Forcing cells to change lineages. Nature 462, 587-594.
21. Hanna, L.A., Foreman, R.K., Tarasenko, I.A., Kessler, D.S., and Labosky, P.A. (2002). Requirement for Foxd3 in maintaining pluripotent cells of the early mouse embryo. Genes Dev. 16, 2650-2661.
22. Hills, M., O'Neill, K., Falconer, E., Brinkman, R., and Lansdorp, P.M. (2013). BAIT: organizing genomes and mapping rearrangements in single cells. Genome Med. 5, 82.
23. Hnisz, D., Abraham, B.J., Lee, T.I., Lau, A., Saint-André, V., Sigova, A.A., Hoke, H.A., and Young, R.A. (2013). Super-enhancers in the control of cell identity and disease. Cell 155, 934-947.
24. Hussein, S.M., Batada, N.N., Vuoristo, S., Ching, R.W., Autio, R., Närvä, E., Ng, S., Sourour, M., Hämäläinen, R., Olsson, C., et al. (2011). Copy number variation and selection during reprogramming to pluripotency. Nature 471, 58-62.
25. Jiang, J., Ding, G., Lin, J., Zhang, M., Shi, L., Lv, W., Yang, H., Xiao, H., Pei, G., Li, Y., et al. (2011). Different developmental potential of pluripotent stem cells generated by different reprogramming strategies. J. Mol. Cell Biol. 3, 197-199.
26. Jiang, J., Lv, W., Ye, X., Wang, L., Zhang, M., Yang, H., Okuka, M., Zhou, C., Zhang, X., Liu, L., et al. (2013). Zscan4 promotes genomic stability during reprogramming and dramatically improves the quality of iPS cells as demonstrated by tetraploid complementation. Cell Res. 23 (1), 92-106.
27. Kang, L., Wang, J., Zhang, Y., Kou, Z., and Gao, S. (2009). iPS cells can support full-term development of tetraploid blastocyst-complemented embryos. Cell Stem Cell 5, 135-138.
28. Kim, K., Doi, A., Wen, B., Ng, K., Zhao, R., Cahan, P., Kim, J., Aryee, M.J., Ji, H., Ehrlich, L.I., et al. (2010). Epigenetic memory in induced pluripotent stem cells. Nature 467, 285-290.
29. Kim, K., Zhao, R., Doi, A., Ng, K., Unternaehrer, J., Cahan, P., Huo, H., Loh, Y.H., Aryee, M.J., Lensch, M.W., et al. (2011). Donor cell type can influence the epigenome and differentiation potential of human induced pluripotent stem cells. Nat. Biotechnol. 29, 1117-1119.
30. Klemm, S., Semrau, S., Wiebrands, K., Mooijman, D., Faddah, D.A., Jaenisch, R., and van Oudenaarden, A. (2014). Transcriptional profiling of cells sorted by RNA abundance. Nat. Methods 11, 549-551.
31. Langmead, B., and Salzberg, S.L. (2012). Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359.
32. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S.L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25.
33. Laurent, L.C., Ulitsky, I., Slavin, I., Tran, H., Schork, A., Morey, R., Lynch, C., Harness, J.V., Lee, S., Barrero, M.J., et al. (2011). Dynamic changes in the copy number of pluripotency and cell proliferation genes in human ESCs and iPSCs during reprogramming and time in culture. Cell Stem Cell 8, 106-118.
34. Lin, C.Y., Lovén, J., Rahl, P.B., Paranal, R.M., Burge, C.B., Bradner, J.E., Lee, T.I., and Young, R.A. (2012). Transcriptional amplification in tumor cells with elevated c-Myc. Cell 151, 56-67.
35. Lister, R., Pelizzola, M., Kida, Y.S., Hawkins, R.D., Nery, J.R., Hon, G., Antosiewicz-Bourget, J., O'Malley, R., Castanon, R., Klugman, S., et al. (2011). Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 471, 68-73.
36. Liu, Y., and Labosky, P.A. (2008). Regulation of embryonic stem cell selfrenewal and pluripotency by Foxd3. Stem Cells 26, 2475-2484.
37. Liu, X., Wu, H., Loring, J., Hormuzdi, S., Disteche, C.M., Bornstein, P., and Jaenisch, R. (1997). Trisomy eight in ES cells is a common potential problem in gene targeting and interferes with germ line transmission. Dev. Dyn. 209, 85-91.
38. Marión, R.M., Strati, K., Li, H., Murga, M., Blanco, R., Ortega, S., Fernandez-Capetillo, O., Serrano, M., and Blasco, M.A. (2009). A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 460, 1149-1153.
39. Mayshar, Y., Ben-David, U., Lavon, N., Biancotti, J.C., Yakir, B., Clark, A.T., Plath, K., Lowry, W.E., and Benvenisty, N. (2010). Identification and classification of chromosomal aberrations in human induced pluripotent stem cells. Cell Stem Cell 7, 521-531.
40. Müller, L.U., Milsom, M.D., Harris, C.E., Vyas, R., Brumme, K.M., Parmar, K., Moreau, L.A., Schambach, A., Park, I.H., London, W.B., et al. (2012). Overcoming reprogramming resistance of Fanconi anemia cells. Blood 119, 5449-5457.
41. Nie, Z., Hu, G., Wei, G., Cui, K., Yamane, A., Resch, W., Wang, R., Green, D.R., Tessarollo, L., Casellas, R., et al. (2012). c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 151, 68-79.
42. Ohi, Y., Qin, H., Hong, C., Blouin, L., Polo, J.M., Guo, T., Qi, Z., Downey, S.L., Manos, P.D., Rossi, D.J., et al. (2011). Incomplete DNA methylation underlies a transcriptional memory of somatic cells in human iPS cells. Nat. Cell Biol. 13, 541-549.
43. Pan, G., and Pei, D. (2012). Order from chaos: single cell reprogramming in two phases. Cell Stem Cell 11, 445-447.
44. Pera, M.F. (2011). Stem cells: The dark side of induced pluripotency. Nature 471, 46-47.
45. Phanstiel, D.H., Brumbaugh, J., Wenger, C.D., Tian, S., Probasco, M.D., Bailey, D.J., Swaney, D.L., Tervo, M.A., Bolin, J.M., Ruotti, V., et al. (2011). Proteomic and phosphoproteomic comparison of human ES and iPS cells. Nat. Methods 8, 821-827.
46. Polo, J.M., Liu, S., Figueroa, M.E., Kulalert, W., Eminli, S., Tan, K.Y., Apostolou, E., Stadtfeld, M., Li, Y., Shioda, T., et al. (2010). Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat. Biotechnol. 28, 848-855.
47. Raj, A., Rifkin, S.A., Andersen, E., and van Oudenaarden, A. (2010). Variability in gene expression underlies incomplete penetrance. Nature 463, 913-918.
48. Shah, S.N., Kerr, C., Cope, L., Zambidis, E., Liu, C., Hillion, J., Belton, A., Huso, D.L., and Resar, L.M. (2012). HMGA1 reprograms somatic cells into pluripotent stem cells by inducing stem cell transcriptional networks. PLoS ONE 7, e48533.
49. Song, Q., and Smith, A.D. (2011). Identifying dispersed epigenomic domains from ChIP-Seq data. Bioinformatics 27, 870-871.
50. Stadtfeld, M., Apostolou, E., Akutsu, H., Fukuda, A., Follett, P., Natesan, S., Kono, T., Shioda, T., and Hochedlinger, K. (2010). Aberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells. Nature 465, 175-181.
51. Stadtfeld, M., Apostolou, E., Ferrari, F., Choi, J., Walsh, R.M., Chen, T., Ooi, S.S., Kim, S.Y., Bestor, T.H., Shioda, T., et al. (2012). Ascorbic acid prevents loss of Dlk1-Dio3 imprinting and facilitates generation of all-iPS cell mice from terminally differentiated B cells. Nat. Genet. 44, 398-405, S1-S2.
52. Stelzer, G., Inger, A., Olender, T., Iny-Stein, T., Dalah, I., Harel, A., Safran, M., and Lancet, D. (2009). GeneDecks: paralog hunting and gene-set distillation with GeneCards annotation. OMICS 13, 477-487.
53. Vafa, O., Wade, M., Kern, S., Beeche, M., Pandita, T.K., Hampton, G.M., and Wahl, G.M. (2002). c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: a mechanism for oncogene-induced genetic instability. Mol. Cell 9, 1031-1044.
54. Viswanathan, S.R., Powers, J.T., Einhorn, W., Hoshida, Y., Ng, T.L., Toffanin, S., O'Sullivan, M., Lu, J., Phillips, L.A., Lockhart, V.L., et al. (2009). Lin28 promotes transformation and is associated with advanced human malignancies. Nat. Genet. 41, 843-848.
55. Wang, Z., and Jaenisch, R. (2004). At most three ES cells contribute to the somatic lineages of chimeric mice and of mice produced by ES-tetraploid complementation. Dev. Biol. 275, 192-201.
56. Weinhold, B., Schratt, G., Arsenian, S., Berger, J., Kamino, K., Schwarz, H., Rüther, U., and Nordheim, A. (2000). Srf(-/-) ES cells display non-cell-autonomous impairment in mesodermal differentiation. EMBO J. 19, 5835-5844.
57. West, J.A., Viswanathan, S.R., Yabuuchi, A., Cunniff, K., Takeuchi, A., Park, I.H., Sero, J.E., Zhu, H., Perez-Atayde, A., Frazier, A.L., et al. (2009). A role for Lin28 in primordial germ-cell development and germ-cell malignancy. Nature 460, 909-913.
58. Whyte, W.A., Orlando, D.A., Hnisz, D., Abraham, B.J., Lin, C.Y., Kagey, M.H., Rahl, P.B., Lee, T.I., and Young, R.A. (2013). Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153, 307-319.
59. Wu, T., Liu, Y., Wen, D., Tseng, Z., Tahmasian, M., Zhong, M., Rafii, S., Stadtfeld, M., Hochedlinger, K., and Xiao, A. (2014). Histone Variant H2A.X Deposition Pattern Serves as a Functional Epigenetic Mark for Distinguishing the Developmental Potentials of iPSCs. Cell Stem Cell 15, this issue, 281-294.
60. Zhao, X.Y., Li, W., Lv, Z., Liu, L., Tong, M., Hai, T., Hao, J., Guo, C.L., Ma, Q.W., Wang, L., et al. (2009). iPS cells produce viable mice through tetraploid complementation. Nature 461, 86-90.
61. Zhu, H., Shah, S., Shyh-Chang, N., Shinoda, G., Einhorn, W.S., Viswanathan, S.R., Takeuchi, A., Grasemann, C., Rinn, J.L., Lopez, M.F., et al. (2010). Lin28a transgenic mice manifest size and puberty phenotypes identified in human genetic association studies. Nat. Genet. 42, 626-630.
62. Zhu, H., Shyh-Chang, N., Segrè, A.V., Shinoda, G., Shah, S.P., Einhorn, W.S., Takeuchi, A., Engreitz, J.M., Hagan, J.P., Kharas, M.G., et al.; DIAGRAM Consortium; MAGIC Investigators (2011). The Lin28/let-7 axis regulates glucose metabolism. Cell 147, 81-94.