NEUROD1 Intrinsically Initiates Differentiation of Induced Pluripotent Stem Cells into Neural Progenitor Cells |
Choi, Won-Young
(Interdisciplinary Program of Integrated OMICS for Biomedical Science, The Graduate School, Yonsei University)
Hwang, Ji-Hyun (Interdisciplinary Program of Integrated OMICS for Biomedical Science, The Graduate School, Yonsei University) Cho, Ann-Na (Department of Biotechnology, College of Life Science and Biotechnology, Yonsei University) Lee, Andrew J. (Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST)) Jung, Inkyung (Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST)) Cho, Seung-Woo (Department of Biotechnology, College of Life Science and Biotechnology, Yonsei University) Kim, Lark Kyun (Severance Biomedical Science Institute and BK21 PLUS Project for Medical Sciences, Gangnam Severance Hospital, Yonsei University College of Medicine) Kim, Young-Joon (Department of Biochemistry, College of Life Science and Biotechnology, Yonsei University) |
1 | Chen, G., Gulbranson, D.R., Hou, Z., Bolin, J.M., Ruotti, V., Probasco, M.D., Smuga-Otto, K., Howden, S.E., Diol, N.R., Propson, N.E., et al. (2011). Chemically defined conditions for human iPSC derivation and culture. Nat. Methods 8, 424-429. DOI |
2 | Forrest, M.P., Zhang, H., Moy, W., McGowan, H., Leites, C., Dionisio, L.E., Xu, Z., Shi, J., Sanders, A.R., Greenleaf, W.J., et al. (2017). Open chromatin profiling in hiPSC-derived neurons prioritizes functional noncoding psychiatric risk variants and highlights neurodevelopmental loci. Cell Stem Cell 21, 305-318.e8. DOI |
3 | Frank, C.L., Liu, F., Wijayatunge, R., Song, L.Y., Biegler, M.T., Yang, M.G., Vockley, C.M., Safi, A., Gersbach, C.A., Crawford, G.E., et al. (2015). Regulation of chromatin accessibility and Zic binding at enhancers in the developing cerebellum. Nat. Neurosci. 18, 647-656. DOI |
4 | Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y.C., Laslo, P., Cheng, J.X., Murre, C., Singh, H., and Glass, C.K. (2010). Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576-589. DOI |
5 | Higuchi, A., Kao, S.H., Ling, Q.D., Chen, Y.M., Li, H.F., Alarfaj, A.A., Munusamy, M.A., Murugan, K., Chang, S.C., Lee, H.C., et al. (2015). Longterm xeno-free culture of human pluripotent stem cells on hydrogels with optimal elasticity. Sci. Rep. 5, 18136. DOI |
6 | Honkaniemi, J. and Sharp, F.R. (1999). Prolonged expression of zinc finger immediate-early gene mRNAs and decreased protein synthesis following kainic acid induced seizures. Eur. J. Neurosci. 11, 10-17. DOI |
7 | Jin, Y., Lee, J.U., Chung, E., Yang, K., Kim, J., Kim, J.W., Lee, J.S., Cho, A.N., Oh, T., Lee, J.H., et al. (2019). Magnetic Control of axon navigation in reprogrammed neurons. Nano Lett. 19, 6517-6523. DOI |
8 | Kang, S., Chen, X., Gong, S., Yu, P., Yau, S., Su, Z., Zhou, L., Yu, J., Pan, G., and Shi, L. (2017). Characteristic analyses of a neural differentiation model from iPSC-derived neuron according to morphology, physiology, and global gene expression pattern. Sci. Rep. 7, 12233. DOI |
9 | Pataskar, A., Jung, J., Smialowski, P., Noack, F., Calegari, F., Straub, T., and Tiwari, V.K. (2016). NeuroD1 reprograms chromatin and transcription factor landscapes to induce the neuronal program. EMBO J. 35, 24-45. DOI |
10 | Philippidou, P. and Dasen, J.S. (2013). Hox genes: choreographers in neural development, architects of circuit organization. Neuron 80, 12-34. DOI |
11 | Qian, L., Berry, E.C., Fu, J.D., Ieda, M., and Srivastava, D. (2013). Reprogramming of mouse fibroblasts into cardiomyocyte-like cells in vitro. Nat. Protoc. 8, 1204-1215. DOI |
12 | Qin, Z., Ren, F., Xu, X., Ren, Y., Li, H., Wang, Y., Zhai, Y., and Chang, Z. (2009). ZNF536, a novel zinc finger protein specifically expressed in the brain, negatively regulates neuron differentiation by repressing retinoic acid-induced gene transcription. Mol. Cell. Biol. 29, 3633-3643. DOI |
13 | Rao, S.S.P., Huntley, M.H., Durand, N.C., Stamenova, E.K., Bochkov, I.D., Robinson, J.T., Sanborn, A.L., Machol, I., Omer, A.D., Lander, E.S., et al. (2014). A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665-1680. DOI |
14 | Rhee, J.W., Arata, A., Selleri, L., Jacobs, Y., Arata, S., Onimaru, H., and Cleary, M.L. (2004). Pbx3 deficiency results in central hypoventilation. Am. J. Pathol. 165, 1343-1350. DOI |
15 | Ross, S.E., Greenberg, M.E., and Stiles, C.D. (2003). Basic helix-loop-helix factors in cortical development. Neuron 39, 13-25. DOI |
16 | Cimadamore, F., Fishwick, K., Giusto, E., Gnedeva, K., Cattarossi, G., Miller, A., Pluchino, S., Brill, L.M., Bronner-Fraser, M., and Terskikh, A.V. (2011). Human ESC-derived neural crest model reveals a key role for SOX2 in sensory neurogenesis. Cell Stem Cell 8, 538-551. DOI |
17 | Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W., et al. (2008). Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137. DOI |
18 | Zhang, Y., Pak, C., Han, Y., Ahlenius, H., Zhang, Z., Chanda, S., Marro, S., Patzke, C., Acuna, C., Covy, J., et al. (2013). Rapid single-step induction of functional neurons from human pluripotent stem cells. Neuron 78, 785-798. DOI |
19 | Krumlauf, R. (1994). Hox genes in vertebrate development. Cell 78, 191-201. DOI |
20 | Chen, Y.M., Chen, L.H., Li, M.P., Li, H.F., Higuchi, A., Kumar, S.S., Ling, Q.D., Alarfaj, A.A., Munusamy, M.A., Chang, Y., et al. (2017). Xeno-free culture of human pluripotent stem cells on oligopeptide-grafted hydrogels with various molecular designs. Sci. Rep. 7, 45146. DOI |
21 | Cotovio, J.P. and Fernandes, T.G. (2020). Production of human pluripotent stem cell-derived hepatic cell lineages and liver organoids: current status and potential applications. Bioengineering (Basel) 7, 36. DOI |
22 | Dixon, J.R., Jung, I., Selvaraj, S., Shen, Y., Antosiewicz-Bourget, J.E., Lee, A.Y., Ye, Z., Kim, A., Rajagopal, N., Xie, W., et al. (2015). Chromatin architecture reorganization during stem cell differentiation. Nature 518, 331-336. DOI |
23 | Dubreuil, W., Hirsch, M.R., Jouve, C., Brunet, J.F., and Goridis, C. (2002). The role of Phox2b in synchronizing pan-neuronal and type-specific aspects of neurogenesis. Development 129, 5241-5253. DOI |
24 | Episkopou, V. (2005). SOX2 functions in adult neural stem cells. Trends Neurosci. 28, 219-221. DOI |
25 | Ferretti, E., Villaescusa, J.C., Di Rosa, P., Fernandez-Diaz, L.C., Longobardi, E., Mazzieri, R., Miccio, A., Micali, N., Selleri, L., Ferrari, G., et al. (2006). Hypomorphic mutation of the TALE gene Prep1 (pKnox1) causes a major reduction of Pbx and Meis proteins and a pleiotropic embryonic phenotype. Mol. Cell. Biol. 26, 5650-5662. DOI |
26 | Lupien, M., Eeckhoute, J., Meyer, C.A., Wang, Q., Zhang, Y., Li, W., Carroll, J.S., Liu, X.S., and Brown, M. (2008). FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 132, 958-970. DOI |
27 | Klemm, S.L., Shipony, Z., and Greenleaf, W.J. (2019). Chromatin accessibility and the regulatory epigenome. Nat. Rev. Genet. 20, 207-220. DOI |
28 | Lamar, E., Kintner, C., and Goulding, M. (2001). Identification of NKL, a novel Gli-Kruppel zinc-finger protein that promotes neuronal differentiation. Development 128, 1335-1346. DOI |
29 | Li, D., Liu, J., Yang, X., Zhou, C., Guo, J., Wu, C., Qin, Y., Guo, L., He, J., Yu, S., et al. (2017). Chromatin accessibility dynamics during iPSC reprogramming. Cell Stem Cell 21, 819-833.e6. DOI |
30 | Matsuda, T., Irie, T., Katsurabayashi, S., Hayashi, Y., Nagai, T., Hamazaki, N., Adefuin, A.M.D., Miura, F., Ito, T., Kimura, H., et al. (2019). Pioneer factor NeuroD1 rearranges transcriptional and epigenetic profiles to execute microglia-neuron conversion. Neuron 101, 472-485.e7. DOI |
31 | McLean, C.Y., Bristor, D., Hiller, M., Clarke, S.L., Schaar, B.T., Lowe, C.B., Wenger, A.M., and Bejerano, G. (2010). GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495-501. DOI |
32 | Mitchell, R.R., Szabo, E., Benoit, Y.D., Case, D.T., Mechael, R., Alamilla, J., Lee, J.H., Fiebig-Comyn, A., Gillespie, D.C., and Bhatia, M. (2014). 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 |
33 | Buenrostro, J.D., Wu, B., Chang, H.Y., and Greenleaf, W.J. (2015). ATAC-seq: a method for assaying chromatin accessibility genome-wide. Curr. Protoc. Mol. Biol. 109, 21.29.1-21.29.9. |
34 | Akiyama, K., Ishikawa, M., and Saito, A. (2008). mRNA expression of activity-regulated cytoskeleton-associated protein (arc) in the amygdala-kindled rats. Brain Res. 1189, 236-246. DOI |
35 | Baker, N.E. and Brown, N.L. (2018). All in the family: proneural bHLH genes and neuronal diversity. Development 145, dev159426. DOI |
36 | Bel-Vialar, S., Medevielle, F., and Pituello, F. (2007). The on/off of Pax6 controls the tempo of neuronal differentiation in the developing spinal cord. Dev. Biol. 305, 659-673. DOI |
37 | Bertrand, N., Castro, D.S., and Guillemot, F. (2002). Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 3, 517-530. DOI |
38 | Brunet, J.F. and Pattyn, A. (2002). Phox2 genes - from patterning to connectivity. Curr. Opin. Genet. Dev. 12, 435-440. DOI |
39 | Cedar, H. and Bergman, Y. (2009). Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 10, 295-304. DOI |
40 | Chang, C.Y., Ting, H.C., Liu, C.A., Su, H.L., Chiou, T.W., Lin, S.Z., Harn, H.J., and Ho, T.J. (2020). Induced pluripotent stem cell (iPSC)-based neurodegenerative disease models for phenotype recapitulation and drug screening. Molecules 25, 2000. DOI |
41 | Shimizu, T., Nakazawa, M., Kani, S., Bae, Y.K., Shimizu, T., Kageyama, R., and Hibi, M. (2010). Zinc finger genes Fezf1 and Fezf2 control neuronal differentiation by repressing Hes5 expression in the forebrain. Development 137, 1875-1885. DOI |
42 | Pang, Z.P., Yang, N., Vierbuchen, T., Ostermeier, A., Fuentes, D.R., Yang, T.Q., Citri, A., Sebastiano, V., Marro, S., Sudhof, T.C., et al. (2011). Induction of human neuronal cells by defined transcription factors. Nature 476, 220-223. DOI |
43 | Rowe, R.G. and Daley, G.Q. (2019). Induced pluripotent stem cells in disease modelling and drug discovery. Nat. Rev. Genet. 20, 377-388. DOI |
44 | Rue, P. and Martinez Arias, A. (2015). Cell dynamics and gene expression control in tissue homeostasis and development. Mol. Syst. Biol. 11, 792. DOI |
45 | Schmitt, A.D., Hu, M., Jung, I., Xu, Z., Qiu, Y., Tan, C.L., Li, Y., Lin, S., Lin, Y., Barr, C.L., et al. (2016). A compendium of chromatin contact maps reveals spatially active regions in the human genome. Cell Rep. 17, 2042-2059. DOI |
46 | Schwartzentruber, J., Foskolou, S., Kilpinen, H., Rodrigues, J., Alasoo, K., Knights, A.J., Patel, M., Goncalves, A., Ferreira, R., Benn, C.L., et al. (2018). Molecular and functional variation in iPSC-derived sensory neurons. Nat. Genet. 50, 54-61. DOI |
47 | Scott-Browne, J.P., Lopez-Moyado, I.F., Trifari, S., Wong, V., Chavez, L., Rao, A., and Pereira, R.M. (2016). Dynamic changes in chromatin accessibility occur in CD8(+) T cells responding to viral infection. Immunity 45, 1327-1340. DOI |
48 | Seo, H.I., Cho, A.N., Jang, J., Kim, D.W., Cho, S.W., and Chung, B.G. (2015). Thermo-responsive polymeric nanoparticles for enhancing neuronal differentiation of human induced pluripotent stem cells. Nanomedicine 11, 1861-1869. DOI |
49 | Shum, C., Macedo, S.C., Warre-Cornish, K., Cocks, G., Price, J., and Srivastava, D.P. (2015). Utilizing induced pluripotent stem cells (iPSCs) to understand the actions of estrogens in human neurons. Horm. Behav. 74, 228-242. DOI |
50 | Shin, J., Choi, E.J., Cho, J.H., Cho, A.N., Jin, Y., Yang, K., Song, C., and Cho, S.W. (2017). Three-dimensional electroconductive hyaluronic acid hydrogels incorporated with carbon nanotubes and polypyrrole by catechol-mediated dispersion enhance neurogenesis of human neural stem cells. Biomacromolecules 18, 3060-3072. DOI |
51 | Schaffner, W. (2015). Enhancers, enhancers - from their discovery to today's universe of transcription enhancers. Biol. Chem. 396, 311-327. DOI |
52 | Wapinski, O.L., Vierbuchen, T., Qu, K., Lee, Q.Y., Chanda, S., Fuentes, D.R., Giresi, P.G., Ng, Y.H., Marro, S., Neff, N.F., et al. (2013). Hierarchical mechanisms for direct reprogramming of fibroblasts to neurons. Cell 155, 621-635. DOI |
53 | Soufi, A., Donahue, G., and Zaret, K.S. (2012). Facilitators and impediments of the pluripotency reprogramming factors' initial engagement with the genome. Cell 151, 994-1004. DOI |
54 | 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 |
55 | Terzic, J. and Saraga-Babic, M. (1999). Expression pattern of PAX3 and PAX6 genes during human embryogenesis. Int. J. Dev. Biol. 43, 501-508. |
56 | Yu, G., Wang, L.G., and He, Q.Y. (2015). ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization. Bioinformatics 31, 2382-2383. DOI |
57 | Wu, F., Sapkota, D., Li, R., and Mu, X. (2012). Onecut 1 and Onecut 2 are potential regulators of mouse retinal development. J. Comp. Neurol. 520, 952-969. DOI |
58 | Wu, Y.Y., Chiu, F.L., Yeh, C.S., and Kuo, H.C. (2019). Opportunities and challenges for the use of induced pluripotent stem cells in modelling neurodegenerative disease. Open Biol. 9, 180177. DOI |
59 | Yang, D., Jang, I., Choi, J., Kim, M.S., Lee, A.J., Kim, H., Eom, J., Kim, D., Jung, I., and Lee, B. (2018). 3DIV: a 3D-genome Interaction Viewer and database. Nucleic Acids Res. 46, D52-D57. DOI |
60 | Zhang, S.W., Zhang, H.W., Zhou, Y.F., Qiao, M., Zhao, S.M., Kozlova, A., Shi, J.X., Sanders, A.R., Wang, G., Luo, K.X., et al. (2020). Allele-specific open chromatin in human iPSC neurons elucidates functional disease variants. Science 369, 561-565. DOI |