Key features of the POU transcription factor Oct4 from an evolutionary perspective.
Animals
Cell Differentiation
/ physiology
Cellular Reprogramming
Dimerization
Embryonic Stem Cells
/ cytology
Female
Gene Expression Regulation
/ physiology
Humans
Mice
Neural Stem Cells
/ cytology
Octamer Transcription Factor-3
/ metabolism
Placenta
/ physiology
Pluripotent Stem Cells
/ cytology
Pregnancy
Transcriptional Activation
/ physiology
Zebrafish
ESCs
NSCs
Oct4
Pluripotency
Reprogramming
Zygotic genome activation
iPSCs
Journal
Cellular and molecular life sciences : CMLS
ISSN: 1420-9071
Titre abrégé: Cell Mol Life Sci
Pays: Switzerland
ID NLM: 9705402
Informations de publication
Date de publication:
Dec 2021
Dec 2021
Historique:
received:
07
08
2021
accepted:
12
10
2021
revised:
16
09
2021
pubmed:
27
10
2021
medline:
15
12
2021
entrez:
26
10
2021
Statut:
ppublish
Résumé
Oct4, a class V POU-domain protein that is encoded by the Pou5f1 gene, is thought to be a key transcription factor in the early development of mammals. This transcription factor plays indispensable roles in pluripotent stem cells as well as in the acquisition of pluripotency during somatic cell reprogramming. Oct4 has also been shown to play a role as a pioneer transcription factor during zygotic genome activation (ZGA) from zebrafish to human. However, during the past decade, several studies have brought these conclusions into question. It was clearly shown that the first steps in mouse development are not affected by the loss of Oct4. Subsequently, the role of Oct4 as a genome activator was brought into doubt. It was also found that the reprogramming of somatic cells into induced pluripotent stem cells (iPSCs) could proceed without Oct4. In this review, we summarize recent findings, reassess the role of Oct4 in reprogramming and ZGA, and point to structural features that may underlie this role. We speculate that pluripotent stem cells resemble neural stem cells more closely than previously thought. Oct4 orthologs within the POUV class hold key roles in genome activation during early development of species with late ZGA. However, in Placentalia, eutherian-specific proteins such as Dux overtake Oct4 in ZGA and endow them with the formation of an evolutionary new tissue-the placenta.
Identifiants
pubmed: 34698883
doi: 10.1007/s00018-021-03975-8
pii: 10.1007/s00018-021-03975-8
doi:
Substances chimiques
Octamer Transcription Factor-3
0
POU5F1 protein, human
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
7339-7353Subventions
Organisme : Russian Science Foundation
ID : 20-74-00072
Organisme : Ministry of Science and Higher Education of Russian Federation
ID : 075-15-2020-773
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Nature Switzerland AG.
Références
Schöler HR, Hatzopoulos AK, Balling R, Suzuki N, Gruss P (1989) A family of octamer-specific proteins present during mouse embryogenesis: evidence for germline-specific expression of an Oct factor. EMBO J 8:2543–2550. https://doi.org/10.1002/j.1460-2075.1989.tb08392.x
doi: 10.1002/j.1460-2075.1989.tb08392.x
pubmed: 2573523
pmcid: 401252
Rosner MH, Vigano MA, Ozato K, Timmons PM, Poirier F, Rigby PW, Staudt LM (1990) A POU-domain transcription factor in early stem cells and germ cells of the mammalian embryo. Nature 345:686–692. https://doi.org/10.1038/345686a0
doi: 10.1038/345686a0
pubmed: 1972777
Herr W, Sturm RA, Clerc RG, Corcoran LM, Baltimore D, Sharp PA, Ingraham HA et al (1988) The POU domain: a large conserved region in the mammalian pit-1, oct-1, oct-2, and Caenorhabditis elegans unc-86 gene products. Genes Dev. https://doi.org/10.1101/gad.2.12a.1513
doi: 10.1101/gad.2.12a.1513
pubmed: 3215510
Botquin V, Hess H, Fuhrmann G, Anastassiadis C, Gross MK, Vriend G, Schöler HR (1998) New POU dimer configuration mediates antagonistic control of an osteopontin preimplantation enhancer by Oct-4 and Sox-2. Genes Dev 12:2073–2090. https://doi.org/10.1101/gad.12.13.2073
doi: 10.1101/gad.12.13.2073
pubmed: 9649510
pmcid: 316977
Tomilin A, Remenyi A, Lins K, Bak H, Leidel S, Vriend G, Wilmanns M et al (2000) Synergism with the coactivator OBF-1 (OCA-B, BOB-1) is mediated by a specific POU dimer configuration. Cell. https://doi.org/10.1016/s0092-8674(00)00189-6
doi: 10.1016/s0092-8674(00)00189-6
pubmed: 11136971
Remenyi A, Tomilin A, Pohl E, Lins K, Philippsen A, Reinbold R, Schöler HR et al (2001) Differential dimer activities of the transcription factor Oct-1 by DNA-induced interface swapping. Mol Cell 8:569–80. https://doi.org/10.1016/s1097-2765(01)00336-7
doi: 10.1016/s1097-2765(01)00336-7
pubmed: 11583619
Remenyi A, Lins K, Nissen LJ, Reinbold R, Scholer HR, Wilmanns M (2003) Crystal structure of a POU/HMG/DNA ternary complex suggests differential assembly of Oct4 and Sox2 on two enhancers. Genes Dev 17:2048–2059. https://doi.org/10.1101/gad.269303
doi: 10.1101/gad.269303
pubmed: 12923055
pmcid: 196258
Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, Schöler H et al (1998) Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95:379–391. https://doi.org/10.1016/s0092-8674(00)81769-9
doi: 10.1016/s0092-8674(00)81769-9
pubmed: 9814708
Wu G, Han D, Gong Y, Sebastiano V, Gentile L, Singhal N, Adachi K et al (2013) Establishment of totipotency does not depend on Oct4A. Nat Cell Biol 15:1089–1097. https://doi.org/10.1038/ncb2816
doi: 10.1038/ncb2816
pubmed: 23934214
pmcid: 3845671
Niwa H, Miyazaki J-I, Smith AG (2000) Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24:372–376. https://doi.org/10.1038/74199
doi: 10.1038/74199
pubmed: 10742100
Radzisheuskaya A, Chia Gle B, dos Santos RL, Theunissen TW, Castro LF, Nichols J, Silva JC (2013) A defined Oct4 level governs cell state transitions of pluripotency entry and differentiation into all embryonic lineages. Nat Cell Biol 15:579–590. https://doi.org/10.1038/ncb2742
doi: 10.1038/ncb2742
pubmed: 23629142
pmcid: 3671976
Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676. https://doi.org/10.1016/j.cell.2006.07.024
doi: 10.1016/j.cell.2006.07.024
pubmed: 16904174
An Z, Liu P, Zheng J, Si C, Li T, Chen Y, Ma T et al (2019) Sox2 and Klf4 as the functional core in pluripotency induction without exogenous Oct4. Cell Rep 29(1986–2000):e8. https://doi.org/10.1016/j.celrep.2019.10.026
doi: 10.1016/j.celrep.2019.10.026
Velychko S, Adachi K, Kim K-P, Hou Y, MacCarthy CM, Wu G, Schöler HR (2019) Excluding Oct4 from yamanaka cocktail unleashes the developmental potential of iPSCs. Cell Stem Cell. https://doi.org/10.1016/j.stem.2019.10.002
doi: 10.1016/j.stem.2019.10.002
pubmed: 31708402
pmcid: 6900749
Michael AK, Grand RS, Isbel L, Cavadini S, Kozicka Z, Kempf G, Bunker RD et al (2020) Mechanisms of OCT4-SOX2 motif readout on nucleosomes. Science. https://doi.org/10.1126/science.abb0074
doi: 10.1126/science.abb0074
pubmed: 32327602
Le Bin GC, Munoz-Descalzo S, Kurowski A, Leitch H, Lou X, Mansfield W, Etienne-Dumeau C et al (2014) Oct4 is required for lineage priming in the developing inner cell mass of the mouse blastocyst. Development 141:1001–1010. https://doi.org/10.1242/dev.096875
doi: 10.1242/dev.096875
pubmed: 24504341
pmcid: 3929414
Frum T, Halbisen MA, Wang C, Amiri H, Robson P, Ralston A (2013) Oct4 Cell-autonomously promotes primitive endoderm development in the mouse blastocyst. Dev Cell 25:610–622. https://doi.org/10.1016/j.devcel.2013.05.004
doi: 10.1016/j.devcel.2013.05.004
pubmed: 23747191
pmcid: 4076445
Verrijzer CP, Van der Vliet PC (1993) POU domain transcription factors. Biochim Biophys Acta 1173:1–21. https://doi.org/10.1016/0167-4781(93)90237-8
doi: 10.1016/0167-4781(93)90237-8
pubmed: 8485147
Klemm JD, Rould MA, Aurora R, Herr W, Pabo CO (1994) Crystal structure of the Oct-1 POU domain bound to an octamer site: DNA recognition with tethered DNA-binding modules. Cell 77:21–32. https://doi.org/10.1016/0092-8674(94)90231-3
doi: 10.1016/0092-8674(94)90231-3
pubmed: 8156594
Pan G, Qin B, Liu N, Scholer HR, Pei D (2004) Identification of a nuclear localization signal in OCT4 and generation of a dominant negative mutant by its ablation. J Biol Chem 279:37013–37020. https://doi.org/10.1074/jbc.M405117200
doi: 10.1074/jbc.M405117200
pubmed: 15218026
Kong X, Liu J, Li L, Yue L, Zhang L, Jiang H, Xie X et al (2015) Functional interplay between the RK motif and linker segment dictates Oct4-DNA recognition. Nucleic Acids Res 43:4381–4392. https://doi.org/10.1093/nar/gkv323
doi: 10.1093/nar/gkv323
pubmed: 25870414
pmcid: 4482079
Esch D, Vahokoski J, Groves MR, Pogenberg V, Cojocaru V, Vom Bruch H, Han D et al (2013) A unique Oct4 interface is crucial for reprogramming to pluripotency. Nat Cell Biol 15:295–301. https://doi.org/10.1038/ncb2680
doi: 10.1038/ncb2680
pubmed: 23376973
Roberts GA, Ozkan B, Gachulincova I, O’Dwyer MR, Hall-Ponsele E, Saxena M, Robinson PJ et al (2021) Dissecting OCT4 defines the role of nucleosome binding in pluripotency. Nat Cell Biol 23:834–845. https://doi.org/10.1038/s41556-021-00727-5
doi: 10.1038/s41556-021-00727-5
pubmed: 34354236
Jerabek S, Ng CKL, Wu G, Arauzo-Bravo MJ, Kim KP, Esch D, Malik V et al (2016) Changing POU dimerization preferences converts Oct6 into a pluripotency inducer. EMBO Rep 18:319–333. https://doi.org/10.15252/embr.201642958
doi: 10.15252/embr.201642958
pubmed: 28007765
pmcid: 5286379
Jacobson EM, Li P, Leon-del-Rio A, Rosenfeld MG, Aggarwal AK (1997) Structure of Pit-1 POU domain bound to DNA as a dimer: unexpected arrangement and flexibility. Genes Dev 11:198–212. https://doi.org/10.1101/gad.11.2.198
doi: 10.1101/gad.11.2.198
pubmed: 9009203
Malik V, Glaser LV, Zimmer D, Velychko S, Weng M, Holzner M, Arend M et al (2019) Pluripotency reprogramming by competent and incompetent POU factors uncovers temporal dependency for Oct4 and Sox2. Nat Commun 10:3477. https://doi.org/10.1038/s41467-019-11054-7
doi: 10.1038/s41467-019-11054-7
pubmed: 31375664
pmcid: 6677745
Tan DS, Chen Y, Gao Y, Bednarz A, Wei Y, Malik V, Ho DH et al (2021) Directed evolution of an enhanced POU reprogramming factor for cell fate engineering. Mol Biol Evol. https://doi.org/10.1093/molbev/msab075
doi: 10.1093/molbev/msab075
pubmed: 34751376
pmcid: 8233511
Williams DC Jr, Cai M, Clore GM (2004) Molecular basis for synergistic transcriptional activation by Oct1 and Sox2 revealed from the solution structure of the 42-kDa Oct1.Sox2.Hoxb1-DNA ternary transcription factor complex. J Biol Chem 279:1449–1457. https://doi.org/10.1074/jbc.M309790200
doi: 10.1074/jbc.M309790200
pubmed: 14559893
Okumura-Nakanishi S, Saito M, Niwa H, Ishikawa F (2005) Oct-3/4 and Sox2 regulate Oct-3/4 gene in embryonic stem cells. J Biol Chem 280:5307–5317. https://doi.org/10.1074/jbc.M410015200
doi: 10.1074/jbc.M410015200
pubmed: 15557334
Yuan H, Corbi N, Basilico C, Dailey L (1995) Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3. Genes Dev 9:2635–2645. https://doi.org/10.1101/gad.9.21.2635
doi: 10.1101/gad.9.21.2635
pubmed: 7590241
Nishimoto M, Fukushima A, Okuda A, Muramatsu M (1999) The gene for the embryonic stem cell coactivator UTF1 carries a regulatory element which selectively interacts with a complex composed of Oct-3/4 and Sox-2. Mol Cell Biol 19:5453–5465. https://doi.org/10.1128/MCB.19.8.5453
doi: 10.1128/MCB.19.8.5453
pubmed: 10409735
pmcid: 84387
Tomioka M, Nishimoto M, Miyagi S, Katayanagi T, Fukui N, Niwa H, Muramatsu M et al (2002) Identification of Sox-2 regulatory region which is under the control of Oct-3/4-Sox-2 complex. Nucleic Acids Res 30:3202–3213. https://doi.org/10.1093/nar/gkf435
doi: 10.1093/nar/gkf435
pubmed: 12136102
pmcid: 135755
Rodda DJ, Chew JL, Lim LH, Loh YH, Wang B, Ng HH, Robson P (2005) Transcriptional regulation of nanog by OCT4 and SOX2. J Biol Chem 280:24731–24737. https://doi.org/10.1074/jbc.M502573200
doi: 10.1074/jbc.M502573200
pubmed: 15860457
Tapia N, MacCarthy C, Esch D, Gabriele Marthaler A, Tiemann U, Arauzo-Bravo MJ, Jauch R et al (2015) Dissecting the role of distinct OCT4-SOX2 heterodimer configurations in pluripotency. Sci Rep 5:13533. https://doi.org/10.1038/srep13533
doi: 10.1038/srep13533
pubmed: 26314899
pmcid: 4551974
Velychko S, Kang K, Kim SM, Kwak TH, Kim KP, Park C, Hong K et al (2019) Fusion of reprogramming factors alters the trajectory of somatic lineage conversion. Cell Rep 27(30–39):e4. https://doi.org/10.1016/j.celrep.2019.03.023
doi: 10.1016/j.celrep.2019.03.023
Leichsenring M, Maes J, Mossner R, Driever W, Onichtchouk D (2013) Pou5f1 transcription factor controls zygotic gene activation in vertebrates. Science 341:1005–1009. https://doi.org/10.1126/science.1242527
doi: 10.1126/science.1242527
pubmed: 23950494
Mistri TK, Devasia AG, Chu LT, Ng WP, Halbritter F, Colby D, Martynoga B et al (2015) Selective influence of Sox2 on POU transcription factor binding in embryonic and neural stem cells. EMBO Rep 16:1177–1191. https://doi.org/10.15252/embr.201540467
doi: 10.15252/embr.201540467
pubmed: 26265007
pmcid: 4576985
Chen J, Zhang Z, Li L, Chen BC, Revyakin A, Hajj B, Legant W et al (2014) Single-molecule dynamics of enhanceosome assembly in embryonic stem cells. Cell 156:1274–1285. https://doi.org/10.1016/j.cell.2014.01.062
doi: 10.1016/j.cell.2014.01.062
pubmed: 24630727
pmcid: 4040518
Nishimoto M, Miyagi S, Yamagishi T, Sakaguchi T, Niwa H, Muramatsu M, Okuda A (2005) Oct-3/4 maintains the proliferative embryonic stem cell state via specific binding to a variant octamer sequence in the regulatory region of the UTF1 locus. Mol Cell Biol 25:5084–5094. https://doi.org/10.1128/MCB.25.12.5084-5094.2005
doi: 10.1128/MCB.25.12.5084-5094.2005
pubmed: 15923625
pmcid: 1140574
Pan X, Cang X, Dan S, Li J, Cheng J, Kang B, Duan X et al (2016) Site-specific disruption of the Oct4/Sox2 protein interaction reveals coordinated mesendodermal differentiation and the epithelial-mesenchymal transition. J Biol Chem 291:18353–18369. https://doi.org/10.1074/jbc.M116.745414
doi: 10.1074/jbc.M116.745414
pubmed: 27369080
pmcid: 5000082
Aksoy I, Jauch R, Chen J, Dyla M, Divakar U, Bogu GK, Teo R et al (2013) Oct4 switches partnering from Sox2 to Sox17 to reinterpret the enhancer code and specify endoderm. EMBO J 32:938–953. https://doi.org/10.1038/emboj.2013.31
doi: 10.1038/emboj.2013.31
pubmed: 23474895
pmcid: 3616284
Jauch R, Aksoy I, Hutchins AP, Ng CK, Tian XF, Chen J, Palasingam P et al (2011) Conversion of Sox17 into a pluripotency reprogramming factor by reengineering its association with Oct4 on DNA. Stem Cells 29:940–951. https://doi.org/10.1002/stem.639
doi: 10.1002/stem.639
pubmed: 21472822
Merino F, Ng CKL, Veerapandian V, Scholer HR, Jauch R, Cojocaru V (2014) Structural basis for the SOX-dependent genomic redistribution of OCT4 in stem cell differentiation. Structure 22:1274–1286. https://doi.org/10.1016/j.str.2014.06.014
doi: 10.1016/j.str.2014.06.014
pubmed: 25126959
Niwa H, Sekita Y, Trend-Ayush E, Grützner F (2008) Platypus Pou5f1 reveals the first steps in the evolution of trophectoderm differentiation and pluripotency in mammals. Evol Dev 10:671–682. https://doi.org/10.1111/j.1525-142X.2008.00280.x
doi: 10.1111/j.1525-142X.2008.00280.x
pubmed: 19021737
Lavial F, Acloque H, Bertocchini F, Macleod DJ, Boast S, Bachelard E, Montillet G et al (2007) The Oct4 homologue PouV and Nanog regulate pluripotency in chicken embryonic stem cells. Development 134:3549–3563. https://doi.org/10.1242/dev.006569
doi: 10.1242/dev.006569
pubmed: 17827181
Morrison GM, Brickman JM (2006) Conserved roles for Oct4 homologues in maintaining multipotency during early vertebrate development. Development 133:2011–2022. https://doi.org/10.1242/dev.02362
doi: 10.1242/dev.02362
pubmed: 16651543
Onichtchouk D, Geier F, Polok B, Messerschmidt DM, Mossner R, Wendik B, Song S et al (2010) Zebrafish Pou5f1-dependent transcriptional networks in temporal control of early development. Mol Syst Biol 6:354. https://doi.org/10.1038/msb.2010.9
doi: 10.1038/msb.2010.9
pubmed: 20212526
pmcid: 2858445
Tapia N, Reinhardt P, Duemmler A, Wu G, Arauzo-Bravo MJ, Esch D, Greber B et al (2012) Reprogramming to pluripotency is an ancient trait of vertebrate Oct4 and Pou2 proteins. Nat Commun 3:1279. https://doi.org/10.1038/ncomms2229
doi: 10.1038/ncomms2229
pubmed: 23232409
Niwa H, Nakamura A, Urata M, Shirae-Kurabayashi M, Kuraku S, Russell S, Ohtsuka S (2016) The evolutionally-conserved function of group B1 Sox family members confers the unique role of Sox2 in mouse ES cells. BMC Evol Biol 16:173. https://doi.org/10.1186/s12862-016-0755-4
doi: 10.1186/s12862-016-0755-4
pubmed: 27582319
pmcid: 5007870
Gentsch GE, Spruce T, Owens NDL, Smith JC (2019) Maternal pluripotency factors initiate extensive chromatin remodelling to predefine first response to inductive signals. Nat Commun 10:4269. https://doi.org/10.1038/s41467-019-12263-w
doi: 10.1038/s41467-019-12263-w
pubmed: 31537794
pmcid: 6753111
Onichtchouk D, Driever W (2016) Zygotic genome activators, developmental timing, and pluripotency. Curr Top Dev Biol 116:273–297. https://doi.org/10.1016/bs.ctdb.2015.12.004
doi: 10.1016/bs.ctdb.2015.12.004
pubmed: 26970624
Okuda Y, Ogura E, Kondoh H, Kamachi Y (2010) B1 SOX coordinate cell specification with patterning and morphogenesis in the early zebrafish embryo. PLoS Genet 6:e1000936. https://doi.org/10.1371/journal.pgen.1000936
doi: 10.1371/journal.pgen.1000936
pubmed: 20463883
pmcid: 2865518
Kobayashi K, Khan A, Ikeda M, Nakamoto A, Maekawa M, Yamasu K (2018) In vitro analysis of the transcriptional regulatory mechanism of zebrafish pou5f3. Exp Cell Res 364:28–41. https://doi.org/10.1016/j.yexcr.2018.01.023
doi: 10.1016/j.yexcr.2018.01.023
pubmed: 29366809
Fernandez-Tresguerres B, Canon S, Rayon T, Pernaute B, Crespo M, Torroja C, Manzanares M (2010) Evolution of the mammalian embryonic pluripotency gene regulatory network. Proc Natl Acad Sci USA 107:19955–19960. https://doi.org/10.1073/pnas.1010708107
doi: 10.1073/pnas.1010708107
pubmed: 21048080
pmcid: 2993340
Han JY, Lee HG, Park YH, Hwang YS, Kim SK, Rengaraj D, Cho BW et al (2018) Acquisition of pluripotency in the chick embryo occurs during intrauterine embryonic development via a unique transcriptional network. J Anim Sci Biotechnol 9:31. https://doi.org/10.1186/s40104-018-0246-0
doi: 10.1186/s40104-018-0246-0
pubmed: 29644074
pmcid: 5891889
Brumbaugh J, Hou Z, Russell JD, Howden SE, Yu P, Ledvina AR, Coon JJ et al (2012) Phosphorylation regulates human OCT4. Proc Natl Acad Sci USA 109:7162–7168. https://doi.org/10.1073/pnas.1203874109
doi: 10.1073/pnas.1203874109
pubmed: 22474382
pmcid: 3358887
Saxe JP, Tomilin A, Scholer HR, Plath K, Huang J (2009) Post-translational regulation of Oct4 transcriptional activity. PLoS One 4:e4467. https://doi.org/10.1371/journal.pone.0004467
doi: 10.1371/journal.pone.0004467
pubmed: 19221599
pmcid: 2637973
Abulaiti X, Zhang H, Wang A, Li N, Li Y, Wang C, Du X et al (2017) Phosphorylation of threonine(343) Is crucial for OCT4 interaction with SOX2 in the maintenance of mouse embryonic stem cell pluripotency. Stem Cell Rep 9:1630–1641. https://doi.org/10.1016/j.stemcr.2017.09.001
doi: 10.1016/j.stemcr.2017.09.001
Bae KB, Yu DH, Lee KY, Yao K, Ryu J, Lim DY, Zykova TA et al (2017) Serine 347 phosphorylation by JNKs negatively regulates OCT4 protein stability in mouse embryonic stem cells. Stem Cell Rep 9:2050–2064. https://doi.org/10.1016/j.stemcr.2017.10.017
doi: 10.1016/j.stemcr.2017.10.017
Lin Y, Yang Y, Li W, Chen Q, Li J, Pan X, Zhou L et al (2012) Reciprocal regulation of Akt and Oct4 promotes the self-renewal and survival of embryonal carcinoma cells. Mol Cell 48:627–640. https://doi.org/10.1016/j.molcel.2012.08.030
doi: 10.1016/j.molcel.2012.08.030
pubmed: 23041284
pmcid: 3601782
Spelat R, Ferro F, Curcio F (2012) Serine 111 phosphorylation regulates OCT4A protein subcellular distribution and degradation. J Biol Chem 287:38279–38288. https://doi.org/10.1074/jbc.M112.386755
doi: 10.1074/jbc.M112.386755
pubmed: 23024368
pmcid: 3488096
Wei F, Scholer HR, Atchison ML (2007) Sumoylation of Oct4 enhances its stability, DNA binding, and transactivation. J Biol Chem 282:21551–21560. https://doi.org/10.1074/jbc.M611041200
doi: 10.1074/jbc.M611041200
pubmed: 17525163
Liao B, Jin Y (2010) Wwp2 mediates Oct4 ubiquitination and its own auto-ubiquitination in a dosage-dependent manner. Cell Res 20:332–344. https://doi.org/10.1038/cr.2009.136
doi: 10.1038/cr.2009.136
pubmed: 19997087
Swaney DL, Wenger CD, Thomson JA, Coon JJ (2009) Human embryonic stem cell phosphoproteome revealed by electron transfer dissociation tandem mass spectrometry. Proc Natl Acad Sci USA 106:995–1000. https://doi.org/10.1073/pnas.0811964106
doi: 10.1073/pnas.0811964106
pubmed: 19144917
pmcid: 2633571
Tolkunova E, Malashicheva A, Parfenov VN, Sustmann C, Grosschedl R, Tomilin A (2007) PIAS proteins as repressors of Oct4 function. J Mol Biol 374:1200–1212. https://doi.org/10.1016/j.jmb.2007.09.081
doi: 10.1016/j.jmb.2007.09.081
pubmed: 17991485
Jukam D, Shariati SAM, Skotheim JM (2017) Zygotic genome activation in vertebrates. Dev Cell 42:316–332. https://doi.org/10.1016/j.devcel.2017.07.026
doi: 10.1016/j.devcel.2017.07.026
pubmed: 28829942
pmcid: 5714289
Schulz KN, Harrison MM (2019) Mechanisms regulating zygotic genome activation. Nat Rev Genet 20:221–234. https://doi.org/10.1038/s41576-018-0087-x
doi: 10.1038/s41576-018-0087-x
pubmed: 30573849
pmcid: 6558659
Zaret KS, Carroll JS (2011) Pioneer transcription factors: establishing competence for gene expression. Genes Dev 25:2227–2241. https://doi.org/10.1101/gad.176826.111
doi: 10.1101/gad.176826.111
pubmed: 22056668
pmcid: 3219227
Soufi A, Garcia MF, Jaroszewicz A, Osman N, Pellegrini M, Zaret KS (2015) Pioneer transcription factors target partial DNA motifs on nucleosomes to initiate reprogramming. Cell 161:555–568. https://doi.org/10.1016/j.cell.2015.03.017
doi: 10.1016/j.cell.2015.03.017
pubmed: 25892221
pmcid: 4409934
Zhu F, Farnung L, Kaasinen E, Sahu B, Yin Y, Wei B, Dodonova SO et al (2018) The interaction landscape between transcription factors and the nucleosome. Nature 562:76–81. https://doi.org/10.1038/s41586-018-0549-5
doi: 10.1038/s41586-018-0549-5
pubmed: 30250250
pmcid: 6173309
Veil M, Yampolsky LY, Gruning B, Onichtchouk D (2019) Pou5f3, SoxB1, and Nanog remodel chromatin on high nucleosome affinity regions at zygotic genome activation. Genome Res 29:383–395. https://doi.org/10.1101/gr.240572.118
doi: 10.1101/gr.240572.118
pubmed: 30674556
pmcid: 6396415
Lee MT, Bonneau AR, Takacs CM, Bazzini AA, DiVito KR, Fleming ES, Giraldez AJ (2013) Nanog, Pou5f1 and SoxB1 activate zygotic gene expression during the maternal-to-zygotic transition. Nature 503:360–364. https://doi.org/10.1038/nature12632
doi: 10.1038/nature12632
pubmed: 24056933
pmcid: 3925760
Mirny LA (2010) Nucleosome-mediated cooperativity between transcription factors. Proc Natl Acad Sci USA 107:22534–22539. https://doi.org/10.1073/pnas.0913805107
doi: 10.1073/pnas.0913805107
pubmed: 21149679
pmcid: 3012490
Meers MP, Janssens DH, Henikoff S (2019) Pioneer factor-nucleosome binding events during differentiation are motif encoded. Mol Cell. https://doi.org/10.1016/j.molcel.2019.05.025
doi: 10.1016/j.molcel.2019.05.025
pubmed: 31253573
pmcid: 6697550
Chronis C, Fiziev P, Papp B, Butz S, Bonora G, Sabri S, Ernst J et al (2017) Cooperative binding of transcription factors orchestrates reprogramming. Cell. https://doi.org/10.1016/j.cell.2016.12.016
doi: 10.1016/j.cell.2016.12.016
pubmed: 28111071
pmcid: 5302508
Liu G, Wang W, Hu S, Wang X, Zhang Y (2018) Inherited DNA methylation primes the establishment of accessible chromatin during genome activation. Genome Res 28:998–1007. https://doi.org/10.1101/gr.228833.117
doi: 10.1101/gr.228833.117
pubmed: 29844026
pmcid: 6028135
King HW, Klose RJ (2017) The pioneer factor OCT4 requires the chromatin remodeller BRG1 to support gene regulatory element function in mouse embryonic stem cells. Elife. https://doi.org/10.7554/eLife.22631
doi: 10.7554/eLife.22631
pubmed: 29083302
pmcid: 5662283
Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E et al (2008) Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133:1106–1117. https://doi.org/10.1016/j.cell.2008.04.043
doi: 10.1016/j.cell.2008.04.043
pubmed: 18555785
Stadhouders R, Vidal E, Serra F, Di Stefano B, Le Dily F, Quilez J, Gomez A et al (2018) Transcription factors orchestrate dynamic interplay between genome topology and gene regulation during cell reprogramming. Nat Genet 50:238–249. https://doi.org/10.1038/s41588-017-0030-7
doi: 10.1038/s41588-017-0030-7
pubmed: 29335546
pmcid: 5810905
Di Stefano B, Sardina JL, van Oevelen C, Collombet S, Kallin EM, Vicent GP, Lu J et al (2014) C/EBPalpha poises B cells for rapid reprogramming into induced pluripotent stem cells. Nature 506:235–239. https://doi.org/10.1038/nature12885
doi: 10.1038/nature12885
pubmed: 24336202
Palfy M, Schulze G, Valen E, Vastenhouw NL (2020) Chromatin accessibility established by Pou5f3, Sox19b and Nanog primes genes for activity during zebrafish genome activation. PLoS Genet 16:e1008546. https://doi.org/10.1371/journal.pgen.1008546
doi: 10.1371/journal.pgen.1008546
pubmed: 31940339
pmcid: 6986763
Wu J, Xu J, Liu B, Yao G, Wang P, Lin Z, Huang B et al (2018) Chromatin analysis in human early development reveals epigenetic transition during ZGA. Nature 557:256–260. https://doi.org/10.1038/s41586-018-0080-8
doi: 10.1038/s41586-018-0080-8
pubmed: 29720659
Lu F, Liu Y, Inoue A, Suzuki T, Zhao K, Zhang Y (2016) Establishing chromatin regulatory landscape during mouse preimplantation development. Cell 165:1375–1388. https://doi.org/10.1016/j.cell.2016.05.050
doi: 10.1016/j.cell.2016.05.050
pubmed: 27259149
pmcid: 6625655
Simandi Z, Horvath A, Wright LC, Cuaranta-Monroy I, De Luca I, Karolyi K, Sauer S et al (2016) OCT4 acts as an integrator of pluripotency and signal-induced differentiation. Mol Cell 63:647–661. https://doi.org/10.1016/j.molcel.2016.06.039
doi: 10.1016/j.molcel.2016.06.039
pubmed: 27499297
Flach G, Johnson MH, Braude PR, Taylor RA, Bolton VN (1982) The transition from maternal to embryonic control in the 2-cell mouse embryo. EMBO J 1:681–686. https://doi.org/10.1002/j.1460-2075.1982.tb01230.x
doi: 10.1002/j.1460-2075.1982.tb01230.x
pubmed: 7188357
pmcid: 553268
Dobson AT, Raja R, Abeyta MJ, Taylor T, Shen S, Haqq C, Pera RA (2004) The unique transcriptome through day 3 of human preimplantation development. Hum Mol Genet 13:1461–1470. https://doi.org/10.1093/hmg/ddh157
doi: 10.1093/hmg/ddh157
pubmed: 15150160
Palmieri SL, Peter W, Hess H, Scholer HR (1994) Oct-4 transcription factor is differentially expressed in the mouse embryo during establishment of the first two extraembryonic cell lineages involved in implantation. Dev Biol 166:259–267. https://doi.org/10.1006/dbio.1994.1312
doi: 10.1006/dbio.1994.1312
pubmed: 7958450
Khan DR, Dube D, Gall L, Peynot N, Ruffini S, Laffont L, Le Bourhis D et al (2012) Expression of pluripotency master regulators during two key developmental transitions: EGA and early lineage specification in the bovine embryo. PLoS One 7:e34110. https://doi.org/10.1371/journal.pone.0034110
doi: 10.1371/journal.pone.0034110
pubmed: 22479535
pmcid: 3315523
Niakan KK, Eggan K (2013) Analysis of human embryos from zygote to blastocyst reveals distinct gene expression patterns relative to the mouse. Dev Biol 375:54–64. https://doi.org/10.1016/j.ydbio.2012.12.008
doi: 10.1016/j.ydbio.2012.12.008
pubmed: 23261930
Blakeley P, Fogarty NM, Del Valle I, Wamaitha SE, Hu TX, Elder K, Snell P et al (2015) Defining the three cell lineages of the human blastocyst by single-cell RNA-seq. Development 142:3613. https://doi.org/10.1242/dev.131235
doi: 10.1242/dev.131235
pubmed: 26487783
pmcid: 4631772
Gao L, Wu K, Liu Z, Yao X, Yuan S, Tao W, Yi L et al (2018) Chromatin accessibility landscape in human early embryos and its association with evolution. Cell 173(248–259):e15. https://doi.org/10.1016/j.cell.2018.02.028
doi: 10.1016/j.cell.2018.02.028
Hendrickson PG, Dorais JA, Grow EJ, Whiddon JL, Lim JW, Wike CL, Weaver BD et al (2017) Conserved roles of mouse DUX and human DUX4 in activating cleavage-stage genes and MERVL/HERVL retrotransposons. Nat Genet 49:925–934. https://doi.org/10.1038/ng.3844
doi: 10.1038/ng.3844
pubmed: 28459457
pmcid: 5703070
De Iaco A, Planet E, Coluccio A, Verp S, Duc J, Trono D (2017) DUX-family transcription factors regulate zygotic genome activation in placental mammals. Nat Genet 49:941–945. https://doi.org/10.1038/ng.3858
doi: 10.1038/ng.3858
pubmed: 28459456
pmcid: 5446900
Yang F, Huang X, Zang R, Chen J, Fidalgo M, Sanchez-Priego C, Yang J et al (2020) DUX-miR-344-ZMYM2-mediated activation of MERVL LTRs induces a totipotent 2C-like state. Cell Stem Cell 26(234–250):e7. https://doi.org/10.1016/j.stem.2020.01.004
doi: 10.1016/j.stem.2020.01.004
Macfarlan TS, Gifford WD, Driscoll S, Lettieri K, Rowe HM, Bonanomi D, Firth A et al (2012) Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 487:57–63. https://doi.org/10.1038/nature11244
doi: 10.1038/nature11244
pubmed: 22722858
pmcid: 3395470
Eckersley-Maslin M, Alda-Catalinas C, Blotenburg M, Kreibich E, Krueger C, Reik W (2019) Dppa2 and Dppa4 directly regulate the Dux-driven zygotic transcriptional program. Genes Dev 33:194–208. https://doi.org/10.1101/gad.321174.118
doi: 10.1101/gad.321174.118
pubmed: 30692203
pmcid: 6362816
Stirparo GG, Kurowski A, Yanagida A, Bates LE, Strawbridge SE, Hladkou S, Stuart HT et al (2021) OCT4 induces embryonic pluripotency via STAT3 signaling and metabolic mechanisms. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.2008890118
doi: 10.1073/pnas.2008890118
pubmed: 33452132
pmcid: 7826362
Fogarty NME, McCarthy A, Snijders KE, Powell BE, Kubikova N, Blakeley P, Lea R et al (2017) Genome editing reveals a role for OCT4 in human embryogenesis. Nature 550:67–73. https://doi.org/10.1038/nature24033
doi: 10.1038/nature24033
pubmed: 28953884
pmcid: 5815497
Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–872. https://doi.org/10.1016/j.cell.2007.11.019
doi: 10.1016/j.cell.2007.11.019
pubmed: 18035408
Heng JC, Feng B, Han J, Jiang J, Kraus P, Ng JH, Orlov YL et al (2010) The nuclear receptor Nr5a2 can replace Oct4 in the reprogramming of murine somatic cells to pluripotent cells. Cell Stem Cell 6:167–174. https://doi.org/10.1016/j.stem.2009.12.009
doi: 10.1016/j.stem.2009.12.009
pubmed: 20096661
Buganim Y, Markoulaki S, van Wietmarschen N, Hoke H, Wu T, Ganz K, Akhtar-Zaidi B et al (2014) The developmental potential of iPSCs is greatly influenced by reprogramming factor selection. Cell Stem Cell 15:295–309. https://doi.org/10.1016/j.stem.2014.07.003
doi: 10.1016/j.stem.2014.07.003
pubmed: 25192464
pmcid: 4170792
Gao Y, Chen J, Li K, Wu T, Huang B, Liu W, Kou X et al (2013) Replacement of Oct4 by Tet1 during iPSC induction reveals an important role of DNA methylation and hydroxymethylation in reprogramming. Cell Stem Cell 12:453–469. https://doi.org/10.1016/j.stem.2013.02.005
doi: 10.1016/j.stem.2013.02.005
pubmed: 23499384
Han DW, Tapia N, Hermann A, Hemmer K, Hoing S, Arauzo-Bravo MJ, Zaehres H et al (2012) Direct reprogramming of fibroblasts into neural stem cells by defined factors. Cell Stem Cell 10:465–472. https://doi.org/10.1016/j.stem.2012.02.021
doi: 10.1016/j.stem.2012.02.021
pubmed: 22445517
Kim KP, Wu Y, Yoon J, Adachi K, Wu G, Velychko S, MacCarthy CM et al (2020) Reprogramming competence of OCT factors is determined by transactivation domains. Sci Adv. https://doi.org/10.1126/sciadv.aaz7364
doi: 10.1126/sciadv.aaz7364
pubmed: 33355138
pmcid: 7732195
Kim KP, Choi J, Yoon J, Bruder JM, Shin B, Kim J, Arauzo-Bravo MJ et al (2021) Permissive epigenomes endow reprogramming competence to transcriptional regulators. Nat Chem Biol 17:47–56. https://doi.org/10.1038/s41589-020-0618-6
doi: 10.1038/s41589-020-0618-6
pubmed: 32807969
Theunissen TW, Powell BE, Wang H, Mitalipova M, Faddah DA, Reddy J, Fan ZP et al (2014) Systematic identification of culture conditions for induction and maintenance of naive human pluripotency. Cell Stem Cell 15:471–487. https://doi.org/10.1016/j.stem.2014.07.002
doi: 10.1016/j.stem.2014.07.002
pubmed: 25090446
pmcid: 4184977
Takashima Y, Guo G, Loos R, Nichols J, Ficz G, Krueger F, Oxley D et al (2014) Resetting transcription factor control circuitry toward ground-state pluripotency in human. Cell 158:1254–1269. https://doi.org/10.1016/j.cell.2014.08.029
doi: 10.1016/j.cell.2014.08.029
pubmed: 25215486
pmcid: 4162745
Thier M, Worsdorfer P, Lakes YB, Gorris R, Herms S, Opitz T, Seiferling D et al (2012) Direct conversion of fibroblasts into stably expandable neural stem cells. Cell Stem Cell 10:473–479. https://doi.org/10.1016/j.stem.2012.03.003
doi: 10.1016/j.stem.2012.03.003
pubmed: 22445518
Kim JB, Sebastiano V, Wu G, Arauzo-Bravo MJ, Sasse P, Gentile L, Ko K et al (2009) Oct4-induced pluripotency in adult neural stem cells. Cell 136:411–419. https://doi.org/10.1016/j.cell.2009.01.023
doi: 10.1016/j.cell.2009.01.023
pubmed: 19203577
Choi HW, Kim JS, Choi S, Hong YJ, Kim MJ, Seo HG, Do JT (2014) Neural stem cells differentiated from iPS cells spontaneously regain pluripotency. Stem Cells 32:2596–2604. https://doi.org/10.1002/stem.1757
doi: 10.1002/stem.1757
pubmed: 24898298
Wurmser AE, Nakashima K, Summers RG, Toni N, D’Amour KA, Lie DC, Gage FH (2004) Cell fusion-independent differentiation of neural stem cells to the endothelial lineage. Nature 430:350–356. https://doi.org/10.1038/nature02604
doi: 10.1038/nature02604
pubmed: 15254537
Clarke DL, Johansson CB, Wilbertz J, Veress B, Nilsson E, Karlström H, Lendahl U et al (2000) Generalized potential of adult neural stem cells. Science 288:1660–1663. https://doi.org/10.1126/science.288.5471.1660
doi: 10.1126/science.288.5471.1660
pubmed: 10834848
Galli R, Borello U, Gritti A, Minasi MG, Bjornson CR, Coletta M, Mora M et al (2000) Skeletal myogenic potential of human and mouse neural stem cells. Nat Neurosci 3:986–991. https://doi.org/10.1038/79924
doi: 10.1038/79924
pubmed: 11017170
Bjornson CR, Rietze RL, Reynolds BA, Magli MC, Vescovi AL (1999) Turning brain into blood: a hematopoietic fate adopted by adult neural stem cells in vivo. Science 283:534–537. https://doi.org/10.1126/science.283.5401.534
doi: 10.1126/science.283.5401.534
pubmed: 9915700
Zalc A, Sinha R, Gulati GS, Wesche DJ, Daszczuk P, Swigut T, Weissman IL et al (2021) Reactivation of the pluripotency program precedes formation of the cranial neural crest. Science. https://doi.org/10.1126/science.abb4776
doi: 10.1126/science.abb4776
pubmed: 33542111
pmcid: 8557957
Cherepanova OA, Gomez D, Shankman LS, Swiatlowska P, Williams J, Sarmento OF, Alencar GF et al (2016) Activation of the pluripotency factor OCT4 in smooth muscle cells is atheroprotective. Nat Med 22:657–665. https://doi.org/10.1038/nm.4109
doi: 10.1038/nm.4109
pubmed: 27183216
pmcid: 4899256