The Role of E3s in Regulating Pluripotency of Embryonic Stem Cells and Induced Pluripotent Stem Cells
Abstract
:1. Pluripotent Cells
2. Ubiquitination
3. E3s-Mediated Regulation of Pluripotency Factors
3.1. Oct4
3.2. Sox2
3.3. Nanog
3.4. C-Myc
3.5. Krüppel-Like Factors (Klfs)
3.6. Epigenetic Regulators
4. Concluding Remarks and Perspectives
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
APC/C | Anaphase-promoting complex/cyclosome |
bHLH | basic Helix-loop-helix |
Cul7 | Culin 7 |
EC | Embryonal carcinoma |
ENK | Early embryo specific NK |
EpiSCs | Epiblast stem cells |
ESCs | Embryonic stem cells |
Fbxw8 | F-box and WD40 domain-containing protein 8 |
HECT | Homologous to E6-AP COOH terminus |
HERC | HECT and regulator of RCC1-like domains-containing |
HMG | High-mobility-group |
ICM | Inner cell mass |
iPSCs | induced Pluripotent Stem cells |
Klfs | Krüppel-like factors |
March5 | Membrane-associated ring finger (C3HC4) 5 |
MBs | Myc boxes |
MS | Mass spectrometry |
Nedd4 | Neuronal precursor cell-expressed developmentally downregulated 4 |
OCT4 | Octamer-binding transcription factor-4 |
PGCs | Primordial germ cells |
PHD/LAP | Plant homeodomain/leukemia-associated protein |
PKA | Protein kinase A |
POU | Pit-Oct-Unc |
POUh | POU homeodomain |
POUs | POU-specific domain |
Prkar1a | Protein kinase type I-alpha |
RA | Retinoid acid |
RBPs | RNA-binding proteins |
RBR | RING between RING |
Rbx1 | RING box protein-1 |
RCC1 | Regulator of chromosome condensation 1 |
RING | Really Interesting New Gene |
RLD | RCC1-like domains |
RNF20 | Ring Finger Protein 20 |
RNF40 | Ring Finger Protein 40 |
ROS | Reactive oxygen species |
Rpb1 | RNA polymerase II subunit B1 |
SCF | Skp1/Cul1/F-box |
shRNA | short-hairpin RNA |
Sox2 | SRY-related HMG Box 2 |
SRY | Sex-determining region Y |
TFs | Transcription factors |
TRIM32 | Tripartite motif containing 32 |
Uba/E1 | Ub-activating enzyme |
Ub-AMP | Ub-adenosine monophosphate |
UBC/E2 | Ub-conjugating enzyme |
Ube2s | Ubiquitin-conjugating enzyme E2s |
Ub-G76 | Glycine 76 of Ub |
WR | tryptophan repeat |
WW | two conserved tryptophans |
References
- Ivanova, N.; Dobrin, R.; Lu, R.; Kotenko, I.; Levorse, J.; Decoste, C.; Schafer, X.; Lun, Y.; Lemischka, I.R. Dissecting self-renewal in stem cells with RNA interference. Nat. Cell Biol. 2006, 442, 533–538. [Google Scholar] [CrossRef]
- Gökbuget, D.; Blelloch, R. Epigenetic control of transcriptional regulation in pluripotency and early differentiation. Development 2019, 146, dev164772. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, M.; Belmonte, J.C.I. Ground rules of the pluripotency gene regulatory network. Nat. Rev. Genet. 2017, 18, 180–191. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martello, G.; Smith, A. The Nature of Embryonic Stem Cells. Annu. Rev. Cell Dev. Biol. 2014, 30, 647–675. [Google Scholar] [CrossRef]
- De Los Angeles, A.; Ferrari, F.; Xi, R.; Fujiwara, Y.; Benvenisty, N.; Deng, H.; Hochedlinger, K.; Jaenisch, R.; Lee, S.; Leitch, H.G.; et al. Hallmarks of pluripotency. J. Nature 2015, 525, 469–478. [Google Scholar] [CrossRef] [PubMed]
- Boyer, L.A.; Lee, T.I.; Cole, M.F.; Johnstone, S.E.; Levine, S.S.; Zucker, J.P.; Guenther, M.G.; Kumar, R.M.; Murray, H.L.; Jenner, R.G.; et al. Core Transcriptional Regulatory Circuitry in Human Embryonic Stem Cells. Cell 2005, 122, 947–956. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ramalho-Santos, M.; Yoon, S.; Matsuzaki, Y.; Mulligan, R.C.; Melton, D.A. “Stemness”: Transcriptional Profiling of Embryonic and Adult Stem Cells. Science 2002, 298, 597–600. [Google Scholar] [CrossRef]
- Baharvand, H.; Hajheidari, M.; Ashtiani, S.K.; Salekdeh, G.H. Proteomic signature of human embryonic stem cells. Proteomics 2006, 6, 3544–3549. [Google Scholar] [CrossRef]
- Vilchez, D.; Boyer, L.; Morantte, I.; Lutz, M.; Merkwirth, C.; Joyce, D.; Spencer, B.; Page, L.; Masliah, E.; Berggren, W.T.; et al. Increased proteasome activity in human embryonic stem cells is regulated by PSMD11. Nat. Cell Biol. 2012, 489, 304–308. [Google Scholar] [CrossRef]
- Buckley, S.M.; Aranda-Orgilles, B.; Strikoudis, A.; Apostolou, E.; Loizou, E.; Moran-Crusio, K.; Farnsworth, C.L.; Koller, A.A.; Dasgupta, R.; Silva, J.C.; et al. Regulation of Pluripotency and Cellular Reprogramming by the Ubiquitin-Proteasome System. Cell Stem Cell 2012, 11, 783–798. [Google Scholar] [CrossRef] [Green Version]
- Selwood, L.; Johnson, M.H. Trophoblast and hypoblast in the monotreme, marsupial and eutherian mammal: Evolution and origins. BioEssays 2006, 28, 128–145. [Google Scholar] [CrossRef] [PubMed]
- Nichols, J.; Smith, A. Naive and Primed Pluripotent States. Cell Stem Cell 2009, 4, 487–492. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, J.; Yamauchi, T.; Belmonte, J.C.I. An overview of mammalian pluripotency. Development 2016, 143, 1644–1648. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martin, G.R.; Evans, M.J. The morphology and growth of a pluripotent teratocarcinoma cell line and its derivatives in tissue culture. Cell 1974, 2, 163–172. [Google Scholar] [CrossRef]
- Mintz, B.; Illmensee, K. Normal genetically mosaic mice produced from malignant teratocarcinoma cells. Proc. Natl. Acad. Sci. USA 1975, 72, 3585–3589. [Google Scholar] [CrossRef] [Green Version]
- Papaioannou, V.E.; McBurney, M.W.; Gardner, R.L.; Evans, M.J. Fate of teratocarcinoma cells injected into early mouse embryos. Nat. Cell Biol. 1975, 258, 70–73. [Google Scholar] [CrossRef]
- Illmensee, K.; Mintz, B. Totipotency and normal differentiation of single teratocarcinoma cells cloned by injection into blastocysts. Proc. Natl. Acad. Sci. USA 1976, 73, 549–553. [Google Scholar] [CrossRef] [Green Version]
- Papaioannou, V.E.; Gardner, R.L.; McBurney, M.W.; Babinet, C.; Evans, M.J. Participation of cultured teratocarcinoma cells in mouse embryogenesis. J. Embryol. Exp. Morphol. 1978, 44, 93–104. [Google Scholar]
- Stewart, T.A.; Mintz, B. Successive generations of mice produced from an established culture line of euploid teratocarcinoma cells. Proc. Natl. Acad. Sci. USA 1981, 78, 6314–6318. [Google Scholar] [CrossRef] [Green Version]
- Stewart, T.A.; Mintz, B. Recurrent germ-line transmission of the teratocarcinoma genome from the METT-1 culture line to progeny in vivo. J. Exp. Zool. 1982, 224, 465–469. [Google Scholar] [CrossRef]
- Rossant, J.; McBurney, M.W. The developmental potential of a euploid male teratocarcinoma cell line after blastocyst injection. J. Embryol. Exp. Morphol. 1982, 70, 99–112. [Google Scholar] [PubMed]
- Smith, A. Embryo-Derived Stem Cells: Of Mice and Men. Annu. Rev. Cell Dev. Biol. 2001, 17, 435–462. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Evans, M.J.; Kaufman, M.H. Establishment in culture of pluripotential cells from mouse embryos. Nat. Cell Biol. 1981, 292, 154–156. [Google Scholar] [CrossRef]
- Martin, G.R. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. USA 1981, 78, 7634–7638. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brons, I.G.M.; Smithers, L.E.; Trotter, M.W.B.; Rugg-Gunn, P.; Sun, B.; Lopes, S.M.C.D.S.; Howlett, S.K.; Clarkson, A.; Ahrlund-Richter, L.; Pedersen, R.A.; et al. Derivation of pluripotent epiblast stem cells from mammalian embryos. Nat. Cell Biol. 2007, 448, 191–195. [Google Scholar] [CrossRef] [PubMed]
- Tesar, P.J.; Chenoweth, J.G.; Brook, F.A.; Davies, T.J.; Evans, E.P.; Mack, D.L.; Gardner, R.L.; McKay, R.D.G. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nat. Cell Biol. 2007, 448, 196–199. [Google Scholar] [CrossRef] [PubMed]
- Ying, Q.-L.; Wray, J.; Nichols, J.; Batlle-Morera, L.; Doble, B.; Woodgett, J.; Cohen, P.; Smith, G. The ground state of embryonic stem cell self-renewal. Nat. Cell Biol. 2008, 453, 519–523. [Google Scholar] [CrossRef] [Green Version]
- Yilmaz, A.; Benvenisty, N. Defining Human Pluripotency. Cell Stem Cell 2019, 25, 9–22. [Google Scholar] [CrossRef]
- Thomson, J.A.; Itskovitz-Eldor, J.; Shapiro, S.S.; Waknitz, M.A.; Swiergiel, J.J.; Marshall, V.S.; Jones, J.M. Embryonic Stem Cell Lines Derived from Human Blastocysts. Science 1998, 282, 1145–1147. [Google Scholar] [CrossRef] [Green Version]
- Reubinoff, B.E.; Pera, M.F.; Fong, C.-Y.; Trounson, A.; Bongso, A. Embryonic stem cell lines from human blastocysts: Somatic differentiation in vitro. Nat. Biotechnol. 2000, 18, 399–404. [Google Scholar] [CrossRef]
- Takahashi, K.; Yamanaka, S. Induction of Pluripotent Stem Cells from Mouse Embryonic and Adult Fibroblast Cultures by Defined Factors. Cell 2006, 126, 663–676. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Takahashi, K.; Tanabe, K.; Ohnuki, M.; Narita, M.; Ichisaka, T.; Tomoda, K.; Yamanaka, S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131, 861–872. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yu, J.; Vodyanik, M.A.; Smuga-Otto, K.; Antosiewicz-Bourget, J.; Frane, J.L.; Tian, S.; Nie, J.; Jonsdottir, G.A.; Ruotti, V.; Stewart, R.; et al. Induced Pluripotent Stem Cell Lines Derived from Human Somatic Cells. Science 2007, 318, 1917–1920. [Google Scholar] [CrossRef] [PubMed]
- Park, I.-H.; Zhao, R.; West, J.A.; Yabuuchi, A.; Huo, H.; Ince, T.A.; Lerou, P.H.; Lensch, M.W.; Daley, G.Q. Reprogramming of human somatic cells to pluripotency with defined factors. Nat. Cell Biol. 2007, 451, 141–146. [Google Scholar] [CrossRef] [PubMed]
- Hershko, A.; Ciechanover, A. The ubiquitin system. Annu. Rev. Biochem. 1998, 67, 425–479. [Google Scholar] [CrossRef]
- Wagner, S.A.; Beli, P.; Weinert, B.T.; Nielsen, M.L.; Cox, J.; Mann, M.; Choudhary, C. A Proteome-wide, Quantitative Survey of In Vivo Ubiquitylation Sites Reveals Widespread Regulatory Roles. Mol. Cell. Proteom. 2011, 10. [Google Scholar] [CrossRef] [Green Version]
- Pickart, C.M. Mechanisms Underlying Ubiquitination. Annu. Rev. Biochem. 2001, 70, 503–533. [Google Scholar] [CrossRef]
- Yau, R.; Rape, M. The increasing complexity of the ubiquitin code. Nat. Cell Biol. 2016, 18, 579–586. [Google Scholar] [CrossRef]
- Vijay-Kumar, S.; Bugg, C.; Wilkinson, K.; Vierstra, R.; Hatfield, P.; Cook, W. Comparison of the three-dimensional structures of human, yeast, and oat ubiquitin. J. Biol. Chem. 1987, 262, 6396–6399. [Google Scholar] [CrossRef]
- Aviel, S.; Winberg, G.; Massucci, M.; Ciechanover, A. Degradation of the Epstein-Barr Virus Latent Membrane Protein 1 (LMP1) by the Ubiquitin-Proteasome Pathway. J. Biol. Chem. 2000, 275, 23491–23499. [Google Scholar] [CrossRef] [Green Version]
- Ciechanover, A.; Ben-Saadon, R. N-terminal ubiquitination: More protein substrates join in. Trends Cell Biol. 2004, 14, 103–106. [Google Scholar] [CrossRef] [PubMed]
- Breitschopf, K.; Bengal, E.; Ziv, T.; Admon, A.; Ciechanover, A. A novel site for ubiquitination: The N-terminal residue, and not internal lysines of MyoD, is essential for conjugation and degradation of the protein. EMBO J. 1998, 17, 5964–5973. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cadwell, K.; Coscoy, L. Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science 2005, 309, 127–130. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bhogaraju, S.; Kalayil, S.; Liu, Y.; Bonn, F.; Colby, T.; Matic, I.; Dikic, I. Phosphoribosylation of Ubiquitin Promotes Serine Ubiquitination and Impairs Conventional Ubiquitination. Cell 2016, 167, 1636–1649.e13. [Google Scholar] [CrossRef] [PubMed]
- Komander, D.; Rape, M. The Ubiquitin Code. Annu. Rev. Biochem. 2012, 81, 203–229. [Google Scholar] [CrossRef] [Green Version]
- Wenzel, D.M.; Klevit, R.E. Following Ariadne’s thread: A new perspective on RBR ubiquitin ligases. BMC Biol. 2012, 10, 24. [Google Scholar] [CrossRef] [Green Version]
- Ohtake, F.; Saeki, Y.; Ishido, S.; Kanno, J.; Tanaka, K. The K48-K63 Branched Ubiquitin Chain Regulates NF-κB Signaling. Mol. Cell 2016, 64, 251–266. [Google Scholar] [CrossRef] [Green Version]
- Emmerich, C.H.; Ordureau, A.; Strickson, S.; Arthur, J.S.; Pedrioli, P.G.; Komander, D.; Cohen, P. Activation of the canonical IKK complex by K63/M1-linked hybrid ubiquitin chains. Proc. Natl. Acad. Sci. USA 2013, 110, 15247–15252. [Google Scholar] [CrossRef] [Green Version]
- Boname, J.M.; Thomas, M.; Stagg, H.R.; Xu, P.; Peng, J.; Lehner, P.J. Efficient Internalization of MHC I Requires Lysine-11 and Lysine-63 Mixed Linkage Polyubiquitin Chains. Traffic 2010, 11, 210–220. [Google Scholar] [CrossRef]
- Hann, Z.S.; Ji, C.; Olsen, S.K.; Lu, X.; Lux, M.C.; Tan, D.S.; Lima, C.D. Structural basis for adenylation and thioester bond formation in the ubiquitin E1. Proc. Natl. Acad. Sci. USA 2019, 116, 15475–15484. [Google Scholar] [CrossRef] [Green Version]
- Passmore, L.A.; Barford, D. Getting into position: The catalytic mechanisms of protein ubiquitylation. Biochem. J. 2004, 379, 513–525. [Google Scholar] [CrossRef] [PubMed]
- Pickart, C.M.; Eddins, M.J. Ubiquitin: Structures, functions, mechanisms. Biochim. Biophys. Acta (BBA) Bioenerg. 2004, 1695, 55–72. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Morreale, F.E.; Walden, H. Types of Ubiquitin Ligases. Cell 2016, 165, 248–248.e1. [Google Scholar] [CrossRef] [PubMed]
- Dul, B.E.; Walworth, N.C. The Plant Homeodomain Fingers of Fission Yeast Msc1 Exhibit E3 Ubiquitin Ligase Activity. J. Biol. Chem. 2007, 282, 18397–18406. [Google Scholar] [CrossRef] [Green Version]
- Ivanov, A.V.; Peng, H.; Yurchenko, V.; Yap, K.L.; Negorev, D.G.; Schultz, D.C.; Psulkowski, E.; Fredericks, W.J.; White, D.E.; Maul, G.G.; et al. PHD Domain-Mediated E3 Ligase Activity Directs Intramolecular Sumoylation of an Adjacent Bromodomain Required for Gene Silencing. Mol. Cell 2007, 28, 823–837. [Google Scholar] [CrossRef] [Green Version]
- Metzger, M.B.; Pruneda, J.N.; Klevit, R.E.; Weissman, A.M. RING-type E3 ligases: Master manipulators of E2 ubiquitin-conjugating enzymes and ubiquitination. Biochim. Biophys. Acta (BBA) Bioenerg. 2014, 1843, 47–60. [Google Scholar] [CrossRef] [Green Version]
- Rotin, D.; Kumar, S. Physiological functions of the HECT family of ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 2009, 10, 398–409. [Google Scholar] [CrossRef]
- Wang, Y.; Argiles-Castillo, D.; Kane, E.I.; Zhou, A.; Spratt, D.E. HECT E3 ubiquitin ligases—Emerging insights into their biological roles and disease relevance. J. Cell Sci. 2020, 133, jcs228072. [Google Scholar] [CrossRef]
- Dunn, R.; Klos, D.A.; Adler, A.S.; Hicke, L. The C2 domain of the Rsp5 ubiquitin ligase binds membrane phosphoinositides and directs ubiquitination of endosomal cargo. J. Cell Biol. 2004, 165, 135–144. [Google Scholar] [CrossRef]
- Huibregtse, J.M.; Scheffner, M.; Beaudenon, S.; Howley, P.M. A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc. Natl. Acad. Sci. USA 1995, 92, 2563–2567. [Google Scholar] [CrossRef] [Green Version]
- Chen, H.I.; Sudol, M. The WW domain of Yes-associated protein binds a proline-rich ligand that differs from the consensus established for Src homology 3-binding modules. Proc. Natl. Acad. Sci. USA 1995, 92, 7819–7823. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lu, P.J.; Zhou, X.Z.; Shen, M.; Lu, K.P. Function of WW domains as phosphoserine- or phosphothreonine-binding modules. Science 1999, 283, 1325–1328. [Google Scholar] [CrossRef] [PubMed]
- Bork, P.; Sudol, M. The WW domain: A signalling site in dystrophin? Trends Biochem. Sci. 1994, 19, 531–533. [Google Scholar] [CrossRef]
- Scheffner, M.; Kumar, S. Mammalian HECT ubiquitin-protein ligases: Biological and pathophysiological aspects. Biochim. Biophys. Acta (BBA) Bioenerg. 2014, 1843, 61–74. [Google Scholar] [CrossRef] [PubMed]
- Eisenhaber, B.; Chumak, N.; Eisenhaber, F.; Hauser, M.-T. The ring between ring fingers (RBR) protein family. Genome Biol. 2007, 8, 209. [Google Scholar] [CrossRef] [Green Version]
- Dove, K.K.; Klevit, R.E. RING-Between-RING E3 Ligases: Emerging Themes amid the Variations. J. Mol. Biol. 2017, 429, 3363–3375. [Google Scholar] [CrossRef]
- Vigano, M.A.; Staudt, L.M. Transcriptional activation by Oct-3: Evidence for a specific role of the POU-specific domain in mediating functional interaction with Oct-1. Nucleic Acids Res. 1996, 24, 2112–2118. [Google Scholar] [CrossRef] [Green Version]
- Brehm, A.; Ohbo, K.; Schöler, H.R. The carboxy-terminal transactivation domain of Oct-4 acquires cell specificity through the POU domain. Mol. Cell. Biol. 1997, 17, 154–162. [Google Scholar] [CrossRef] [Green Version]
- Lim, H.-Y.; Do, H.-J.; Lee, W.-Y.; Kim, D.-K.; Seo, H.G.; Chung, H.-J.; Park, J.-K.; Chang, W.-K.; Kim, J.-H.; Kim, J. Implication of human OCT4 transactivation domains for self-regulatory transcription. Biochem. Biophys. Res. Commun. 2009, 385, 148–153. [Google Scholar] [CrossRef]
- Esch, D.; Vahokoski, J.; Groves, M.R.; Pogenberg, V.; Cojocaru, V.; Bruch, H.V.; Han, D.; Drexler, H.C.A.; Araúzo-Bravo, M.J.; Ng, C.K.L.; et al. A unique Oct4 interface is crucial for reprogramming to pluripotency. Nat. Cell Biol. 2013, 15, 295–301. [Google Scholar] [CrossRef]
- Schöler, H.R. Octamania: The POU factors in murine development. Trends Genet. 1991, 7, 323–329. [Google Scholar] [CrossRef]
- Okamoto, K.; Okazawa, H.; Okuda, A.; Sakai, M.; Muramatsu, M.; Hamada, H. A novel octamer binding transcription factor is differentially expressed in mouse embryonic cells. Cell 1990, 60, 461–472. [Google Scholar] [CrossRef]
- Schöler, H.; Hatzopoulos, A.; Balling, R.; Suzuki, N.; Gruss, P. A family of octamer-specific proteins present during mouse embryogenesis: Evidence for germline-specific expression of an Oct factor. EMBO J. 1989, 8, 2543–25500. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rosner, M.H.; Vigano, M.A.; Ozato, K.; Timmons, P.M.; Poirie, F.; Rigby, P.W.J.; Staudt, L.M. A POU-domain transcription factor in early stem cells and germ cells of the mammalian embryo. Nat. Cell Biol. 1990, 345, 686–692. [Google Scholar] [CrossRef] [PubMed]
- Palmieri, S.L.; Peter, W.; Hess, H.; Schöler, H.R. 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. 1994, 166, 259–267. [Google Scholar] [CrossRef]
- Nichols, J.; Zevnik, B.; Anastassiadis, K.; Niwa, H.; Klewe-Nebenius, D.; Chambers, I.; Schöler, H.; Smith, A. Formation of Pluripotent Stem Cells in the Mammalian Embryo Depends on the POU Transcription Factor Oct4. Cell 1998, 95, 379–391. [Google Scholar] [CrossRef] [Green Version]
- Le Bin, G.C.; Muñoz-Descalzo, S.; Kurowski, A.; Leitch, H.; Lou, X.; Mansfield, W.; Etienne-Dumeau, C.; Grabole, N.; Mulas, C.; Niwa, H.; et al. Oct4 is required for lineage priming in the developing inner cell mass of the mouse blastocyst. Development 2014, 141, 1001–1010. [Google Scholar] [CrossRef] [Green Version]
- Niwa, H.; Miyazaki, J.; Smith, A.G. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 2000, 24, 372–376. [Google Scholar] [CrossRef]
- Wu, T.; Wang, H.; He, J.; Kang, L.; Jiang, Y.; Liu, J.; Zhang, Y.; Kou, Z.; Liu, L.; Zhang, X.; et al. Reprogramming of Trophoblast Stem Cells into Pluripotent Stem Cells by Oct4. Stem Cells 2011, 29, 755–763. [Google Scholar] [CrossRef]
- Tsai, S.-Y.; Bouwman, B.A.; Ang, Y.-S.; Kim, S.J.; Lee, D.-F.; Lemischka, I.R.; Rendl, M. Single Transcription Factor Reprogramming of Hair Follicle Dermal Papilla Cells to Induced Pluripotent Stem Cells. Stem Cells 2011, 29, 964–971. [Google Scholar] [CrossRef] [Green Version]
- Li, H.; Zhang, Z.; Wang, B.; Zhang, J.; Zhao, Y.; Jin, Y. Wwp2-Mediated Ubiquitination of the RNA Polymerase II Large Subunit in Mouse Embryonic Pluripotent Stem Cells. Mol. Cell. Biol. 2007, 27, 5296–5305. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xu, H.M.; Liao, B.; Zhang, Q.J.; Wang, B.B.; Li, H.; Zhong, X.-M.; Sheng, H.Z.; Zhao, Y.M.; Jin, Y. Wwp2, an E3 Ubiquitin Ligase That Targets Transcription Factor Oct-4 for Ubiquitination. J. Biol. Chem. 2004, 279, 23495–23503. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liao, B.; Jin, Y. Wwp2 mediates Oct4 ubiquitination and its own auto-ubiquitination in a dosage-dependent manner. Cell Res. 2009, 20, 332–344. [Google Scholar] [CrossRef] [PubMed]
- Xu, H.; Wang, W.; Li, C.; Yu, H.; Yang, A.; Wang, B.; Jin, Y. WWP2 promotes degradation of transcription factor OCT4 in human embryonic stem cells. Cell Res. 2009, 19, 561–573. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, S.; Xiao, F.; Zhang, J.; Sun, X.; Wang, H.; Zeng, Y.; Hu, J.; Tang, F.; Gu, J.; Zhao, Y.; et al. Disruption of OCT4 Ubiquitination Increases OCT4 Protein Stability and ASH2L-B-Mediated H3K4 Methylation Promoting Pluripotency Acquisition. Stem Cell Rep. 2018, 11, 973–987. [Google Scholar] [CrossRef] [Green Version]
- Liao, B.; Zhong, X.; Xu, H.; Xiao, F.; Fang, Z.; Gu, J.; Chen, Y.; Zhao, Y.; Jin, Y. Itch, an E3 ligase of Oct4, is required for embryonic stem cell self-renewal and pluripotency induction. J. Cell. Physiol. 2013, 228, 1443–1451. [Google Scholar] [CrossRef]
- Aki, D.; Li, Q.; Li, H.; Liu, Y.-C.; Lee, J.H. Immune regulation by protein ubiquitination: Roles of the E3 ligases VHL and Itch. Protein Cell 2019, 10, 395–404. [Google Scholar] [CrossRef]
- Aki, D.; Zhang, W.; Liu, Y.-C. The E3 ligase Itch in immune regulation and beyond. Immunol. Rev. 2015, 266, 6–26. [Google Scholar] [CrossRef]
- Napolitano, L.M.; Jaffray, E.G.; Hay, R.T.; Meroni, G. Functional interactions between ubiquitin E2 enzymes and TRIM proteins. Biochem. J. 2011, 434, 309–319. [Google Scholar] [CrossRef] [Green Version]
- Meroni, G.; Diez-Roux, G. TRIM/RBCC, a novel class of ‘single protein RING finger’ E3 ubiquitin ligases. BioEssays 2005, 27, 1147–1157. [Google Scholar] [CrossRef]
- Lazzari, E.; Meroni, G. TRIM32 ubiquitin E3 ligase, one enzyme for several pathologies: From muscular dystrophy to tumours. Int. J. Biochem. Cell Biol. 2016, 79, 469–477. [Google Scholar] [CrossRef] [PubMed]
- Schwamborn, J.C.; Berezikov, E.; Knoblich, J.A. The TRIM-NHL Protein TRIM32 Activates MicroRNAs and Prevents Self-Renewal in Mouse Neural Progenitors. Cell 2009, 136, 913–925. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bahnassawy, L.; Perumal, T.; Gonzalez-Cano, L.; Hillje, A.-L.; Taher, L.; Makałowski, W.; Suzuki, Y.; Fuellen, G.; Del Sol, A.; Schwamborn, J.C. TRIM32 modulates pluripotency entry and exit by directly regulating Oct4 stability. Sci. Rep. 2015, 5, 13456. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pardo, M.; Lang, B.; Yu, L.; Prosser, H.; Bradley, A.; Babu, M.M.; Choudhary, J.S. An Expanded Oct4 Interaction Network: Implications for Stem Cell Biology, Development, and Disease. Cell Stem Cell 2010, 6, 382–395. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, J.; Rao, S.; Chu, J.; Shen, X.; Levasseur, D.N.; Theunissen, T.W.; Orkin, S.H. A protein interaction network for pluripotency of embryonic stem cells. Nature 2006, 444, 364–368. [Google Scholar] [CrossRef] [PubMed]
- Van den Berg, D.L.; Snoek, T.; Mullin, N.P.; Yates, A.; Bezstarosti, K.; Demmers, J.; Chambers, I.; Poot, R.A. An Oct4-centered protein interaction network in embryonic stem cells. Cell Stem Cell 2010, 6, 369–381. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, C.; Zhang, D.; Shen, Y.; Tao, X.; Liu, L.; Zhong, Y.; Fang, S. DPF2 regulates OCT4 protein level and nuclear distribution. Biochim. Biophys. Acta 2015, 1853, 3279–3293. [Google Scholar] [CrossRef] [Green Version]
- Gubbay, J.; Collignon, J.; Koopman, P.; Capel, B.; Economou, A.; Münsterberg, A.; Vivian, N.; Goodfellow, P.; Lovell-Badge, R. A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nat. Cell Biol. 1990, 346, 245–250. [Google Scholar] [CrossRef]
- Novak, D.; Hüser, L.; Elton, J.J.; Umansky, V.; Altevogt, P.; Utikal, J. SOX2 in development and cancer biology. Semin. Cancer Biol. 2020, 67, 74–82. [Google Scholar] [CrossRef]
- Avilion, A.A.; Nicolis, S.K.; Pevny, L.H.; Perez, L.; Vivian, N.; Lovell-Badge, R. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 2003, 17, 126–140. [Google Scholar] [CrossRef] [Green Version]
- Wood, H.B.; Episkopou, V. Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages. Mech. Dev. 1999, 86, 197–201. [Google Scholar] [CrossRef]
- Yabuta, Y.; Kurimoto, K.; Ohinata, Y.; Seki, Y.; Saitou, M. Gene Expression Dynamics During Germline Specification in Mice Identified by Quantitative Single-Cell Gene Expression Profiling1. Biol. Reprod. 2006, 75, 705–716. [Google Scholar] [CrossRef] [PubMed]
- Cavallaro, M.; Mariani, J.; Lancini, C.; Latorre, E.; Caccia, R.; Gullo, F.; Valotta, M.; DeBiasi, S.; Spinardi, L.; Ronchi, A.; et al. Impaired generation of mature neurons by neural stem cells from hypomorphic Sox2 mutants. Development 2008, 135, 541–557. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cimadamore, F.; Fishwick, K.; Giusto, E.; Gnedeva, K.; Cattarossi, G.; Miller, A.; Pluchino, S.; Brill, L.M.; Bronner, M.; Terskikh, A.V. Human ESC-derived neural crest model reveals a key role for SOX2 in sensory neurogenesis. Cell Stem Cell 2011, 8, 538–551. [Google Scholar] [CrossRef] [Green Version]
- Fauquier, T.; Rizzoti, K.; Dattani, M.; Lovell-Badge, R.; Robinson, I.C.A.F. SOX2-expressing progenitor cells generate all of the major cell types in the adult mouse pituitary gland. Proc. Natl. Acad. Sci. USA 2008, 105, 2907–2912. [Google Scholar] [CrossRef] [Green Version]
- Chew, J.-L.; Loh, Y.-H.; Zhang, W.; Chen, X.; Tam, W.-L.; Yeap, L.-S.; Li, P.; Ang, Y.-S.; Lim, B.; Robson, P.; et al. Reciprocal Transcriptional Regulation of Pou5f1 and Sox2 via the Oct4/Sox2 Complex in Embryonic Stem Cells. Mol. Cell. Biol. 2005, 25, 6031–6046. [Google Scholar] [CrossRef] [Green Version]
- Li, J.; Pan, G.; Cui, K.; Liu, Y.; Xu, S.; Pei, D. A Dominant-negative Form of Mouse SOX2 Induces Trophectoderm Differentiation and Progressive Polyploidy in Mouse Embryonic Stem Cells. J. Biol. Chem. 2007, 282, 19481–19492. [Google Scholar] [CrossRef] [Green Version]
- Kopp, J.L.; Ormsbee, B.D.; Desler, M.; Rizzino, A. Small Increases in the Level of Sox2 Trigger the Differentiation of Mouse Embryonic Stem Cells. Stem Cells 2008, 26, 903–911. [Google Scholar] [CrossRef]
- Chen, X.; Xu, H.; Yuan, P.; Fang, F.; Huss, M.; Vega, V.B.; Wong, E.; Orlov, Y.L.; Zhang, W.; Jiang, J.; et al. Integration of External Signaling Pathways with the Core Transcriptional Network in Embryonic Stem Cells. Cell 2008, 133, 1106–1117. [Google Scholar] [CrossRef] [Green Version]
- Fang, L.; Zhang, L.; Wei, W.; Jin, X.; Wang, P.; Tong, Y.; Li, J.; Du, J.X.; Wong, J. A Methylation-Phosphorylation Switch Determines Sox2 Stability and Function in ESC Maintenance or Differentiation. Mol. Cell 2014, 55, 537–551. [Google Scholar] [CrossRef] [Green Version]
- Zhang, C.; Leng, F.; Saxena, L.; Hoang, N.; Yu, J.; Alejo, S.; Lee, L.; Qi, D.; Lu, F.; Sun, H.; et al. Proteolysis of methylated SOX2 protein is regulated by L3MBTL3 and CRL4DCAF5 ubiquitin ligase. J. Biol. Chem. 2019, 294, 476–489. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, J.; Zhang, Y.; Hou, J.; Qian, X.; Zhang, H.; Zhang, Z.; Li, M.; Wang, R.; Liao, K.; Wang, Y.; et al. Ube2s regulates Sox2 stability and mouse ES cell maintenance. Cell Death Differ. 2015, 23, 393–404. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Peters, J.-M. The anaphase promoting complex/cyclosome: A machine designed to destroy. Nat. Rev. Mol. Cell Biol. 2006, 7, 644–656. [Google Scholar] [CrossRef] [PubMed]
- Chang, L.-F.; Zhang, Z.; Yang, J.; McLaughlin, S.H.; Barford, D. Molecular architecture and mechanism of the anaphase-promoting complex. Nat. Cell Biol. 2014, 513, 388–393. [Google Scholar] [CrossRef] [Green Version]
- Buganim, Y.; Faddah, D.A.; Cheng, A.W.; Itskovich, E.; Markoulaki, S.; Ganz, K.; Klemm, S.L.; Van Oudenaarden, A.; Jaenisch, R. Single-Cell Expression Analyses during Cellular Reprogramming Reveal an Early Stochastic and a Late Hierarchic Phase. Cell 2012, 150, 1209–1222. [Google Scholar] [CrossRef] [Green Version]
- Chambers, I.; Colby, D.; Robertson, M.; Nichols, J.; Lee, S.; Tweedie, S.; Smith, A. Functional Expression Cloning of Nanog, a Pluripotency Sustaining Factor in Embryonic Stem Cells. Cell 2003, 113, 643–655. [Google Scholar] [CrossRef] [Green Version]
- Mitsui, K.; Tokuzawa, Y.; Itoh, H.; Segawa, K.; Murakami, M.; Takahashi, K.; Maruyama, M.; Maeda, M.; Yamanaka, S. The Homeoprotein Nanog Is Required for Maintenance of Pluripotency in Mouse Epiblast and ES Cells. Cell 2003, 113, 631–642. [Google Scholar] [CrossRef] [Green Version]
- Silva, J.C.R.; Nichols, J.; Theunissen, T.W.; Guo, G.; Van Oosten, A.L.; Barrandon, O.; Wray, J.; Yamanaka, S.; Chambers, I.; Smith, A. Nanog Is the Gateway to the Pluripotent Ground State. Cell 2009, 138, 722–737. [Google Scholar] [CrossRef] [Green Version]
- Pan, G.J.; Pei, D.Q. Identification of two distinct transactivation domains in the pluripotency sustaining factor nanog. Cell Res. 2003, 13, 499–502. [Google Scholar] [CrossRef] [Green Version]
- Hart, A.H.; Hartley, L.; Ibrahim, M.; Robb, L. Identification, cloning and expression analysis of the pluripotency promoting Nanog genes in mouse and human. Dev. Dyn. 2004, 230, 187–198. [Google Scholar] [CrossRef]
- Hatano, S.-Y.; Tada, M.; Kimura, H.; Yamaguchi, S.; Kono, T.; Nakano, T.; Suemori, H.; Nakatsuji, N.; Tada, T. Pluripotential competence of cells associated with Nanog activity. Mech. Dev. 2005, 122, 67–79. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chambers, I.; Silva, J.; Colby, D.; Nichols, J.; Nijmeijer, B.; Robertson, M.; Vrana, J.; Jones, K.L.; Grotewold, L.; Smith, A. Nanog safeguards pluripotency and mediates germline development. Nat. Cell Biol. 2007, 450, 1230–1234. [Google Scholar] [CrossRef] [PubMed]
- Chickarmane, V.; Olariu, V.; Peterson, C. Probing the role of stochasticity in a model of the embryonic stem cell—Heterogeneous gene expression and reprogramming efficiency. BMC Syst. Biol. 2012, 6, 98. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ramakrishna, S.; Suresh, R.; Lim, K.-H.; Cha, B.-H.; Lee, S.-H.; Kim, K.-S.; Baek, K.-H. PEST Motif Sequence Regulating Human NANOG for Proteasomal Degradation. Stem Cells Dev. 2011, 20, 1511–1519. [Google Scholar] [CrossRef] [PubMed]
- Kim, S.-H.; Kim, M.O.; Cho, Y.-Y.; Yao, K.; Kim, D.J.; Jeong, C.-H.; Yu, D.H.; Bae, K.B.; Cho, E.J.; Jung, S.K.; et al. ERK1 phosphorylates Nanog to regulate protein stability and stem cell self-renewal. Stem Cell Res. 2014, 13, 1–11. [Google Scholar] [CrossRef] [Green Version]
- Elledge, S.J.; Harper, J.W. The role of protein stability in the cell cycle and cancer. Biochim. Biophys. Acta (BBA) Bioenerg. 1998, 1377, M61–M70. [Google Scholar] [CrossRef]
- Kamura, T.; Koepp, D.M.; Conrad, M.N.; Skowyra, D.; Moreland, R.J.; Iliopoulos, O.; Lane, W.S.; Kaelin, W.G., Jr.; Elledge, S.J.; Conaway, R.C.; et al. Rbx1, a Component of the VHL Tumor Suppressor Complex and SCF Ubiquitin Ligase. Sci. 1999, 284, 657–661. [Google Scholar] [CrossRef]
- Ohta, T.; Michel, J.J.; Schottelius, A.J.; Xiong, Y. ROC1, a Homolog of APC11, Represents a Family of Cullin Partners with an Associated Ubiquitin Ligase Activity. Mol. Cell 1999, 3, 535–541. [Google Scholar] [CrossRef]
- Seol, J.H.; Feldman, R.R.; Zachariae, W.; Shevchenko, A.; Correll, C.C.; Lyapina, S.; Chi, Y.; Galova, M.; Claypool, J.; Sandmeyer, S.; et al. Cdc53/cullin and the essential Hrt1 RING-H2 subunit of SCF define a ubiquitin ligase module that activates the E2 enzyme Cdc34. Genes Dev. 1999, 13, 1614–1626. [Google Scholar] [CrossRef]
- Arai, T.; Kasper, J.S.; Skaar, J.R.; Ali, S.H.; Takahashi, C.; DeCaprio, J.A. Targeted disruption of p185/Cul7 gene results in abnormal vascular morphogenesis. Proc. Natl. Acad. Sci. USA 2003, 100, 9855–9860. [Google Scholar] [CrossRef] [Green Version]
- Lin, P.; Fu, J.; Zhao, B.; Lin, F.; Zou, H.; Liu, L.; Zhu, C.; Wang, H.; Yu, X. Fbxw8 is involved in the proliferation of human choriocarcinoma JEG-3 cells. Mol. Biol. Rep. 2011, 38, 1741–1747. [Google Scholar] [CrossRef] [PubMed]
- Tsunematsu, R.; Nishiyama, M.; Kotoshiba, S.; Saiga, T.; Kamura, T.; Nakayama, K.I. Fbxw8 Is Essential for Cul1-Cul7 Complex Formation and for Placental Development. Mol. Cell. Biol. 2006, 26, 6157–6169. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dang, C.V. MYC, Metabolism, Cell Growth, and Tumorigenesis. Cold Spring Harb. Perspect. Med. 2013, 3, a014217. [Google Scholar] [CrossRef] [PubMed]
- Bretones, G.; Delgado, M.D.; León, J. Myc and cell cycle control. Biochim. Biophys. Acta (BBA) Bioenerg. 2015, 1849, 506–516. [Google Scholar] [CrossRef] [PubMed]
- Cartwright, P.; McLean, C.; Sheppard, A.; Rivett, D.; Jones, K.; Dalton, S. LIF/STAT3 controls ES cell self-renewal and pluripotency by a Myc-dependent mechanism. Development 2005, 132, 885–896. [Google Scholar] [CrossRef] [Green Version]
- Nie, Z.; Hu, G.; Wei, G.; Cui, K.; Yamane, A.; Resch, W.; Wang, R.; Green, D.R.; Tessarollo, L.; Casellas, R.; et al. c-Myc Is a Universal Amplifier of Expressed Genes in Lymphocytes and Embryonic Stem Cells. Cell 2012, 151, 68–79. [Google Scholar] [CrossRef] [Green Version]
- Young, R.A. Control of the Embryonic Stem Cell State. Cell 2011, 144, 940–954. [Google Scholar] [CrossRef] [Green Version]
- Sumi, T.; Tsuneyoshi, N.; Nakatsuji, N.; Suemori, H. Apoptosis and differentiation of human embryonic stem cells induced by sustained activation of c-Myc. Oncogene 2007, 26, 5564–5576. [Google Scholar] [CrossRef] [Green Version]
- Farrell, A.S.; Sears, R.C. MYC Degradation. Cold Spring Harb. Perspect. Med. 2014, 4, a014365. [Google Scholar] [CrossRef]
- Hann, S.R.; Eisenman, R.N. Proteins encoded by the human c-myc oncogene: Differential expression in neoplastic cells. Mol. Cell. Biol. 1984, 4, 2486–2497. [Google Scholar] [CrossRef]
- Sun, X.X.; He, X.; Yin, L.; Komada, M.; Sears, R.C.; Dai, M.S. The nucleolar ubiquitin-specific protease USP36 deubiquitinates and stabilizes c-Myc. Proc. Natl. Acad. Sci. USA 2015, 112, 3734–3739. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Flinn, E.M.; Busch, C.M.C.; Wright, A.P.H. myc Boxes, Which Are Conserved in myc Family Proteins, Are Signals for Protein Degradation via the Proteasome. Mol. Cell. Biol. 1998, 18, 5961–5969. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sears, R.; Leone, G.; DeGregori, J.; Nevins, J.R. Ras Enhances Myc Protein Stability. Mol. Cell 1999, 3, 169–179. [Google Scholar] [CrossRef]
- Sears, R.; Nuckolls, F.; Haura, E.; Taya, Y.; Tamai, K.; Nevins, J.R. Multiple Ras-dependent phosphorylation pathways regulate Myc protein stability. Genes Dev. 2000, 14, 2501–2514. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, S.Y.; Herbst, A.; Tworkowski, K.A.; Salghetti, S.E.; Tansey, W.P. Skp2 Regulates Myc Protein Stability and Activity. Mol. Cell 2003, 11, 1177–1188. [Google Scholar] [CrossRef]
- Yada, M.; Hatakeyama, S.; Kamura, T.; Nishiyama, M.; Tsunematsu, R.; Imaki, H.; Ishida, N.; Okumura, F.; Nakayama, K.; Nakayama, K.I. Phosphorylation-dependent degradation of c-Myc is mediated by the F-box protein Fbw7. EMBO J. 2004, 23, 2116–2125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Welcker, M.; Orian, A.; Jin, J.; Grim, J.A.; Harper, J.W.; Eisenman, R.N.; Clurman, B.E. The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation-dependent c-Myc protein degradation. Proc. Natl. Acad. Sci. USA 2004, 101, 9085–9090. [Google Scholar] [CrossRef] [Green Version]
- Sato, T.; Okumura, F.; Ariga, T.; Hatakeyama, S. TRIM6 interacts with Myc and maintains the pluripotency of mouse embryonic stem cells. J. Cell Sci. 2012, 125, 1544–1555. [Google Scholar] [CrossRef] [Green Version]
- Von der Lehr, N.; Johansson, S.; Wu, S.; Bahram, F.; Castell, A.; Cetinkaya, C.; Hydbring, P.; Weidung, I.; Nakayama, K.; Nakayama, K.I.; et al. The F-box protein Skp2 participates in c-Myc proteosomal degradation and acts as a cofactor for c-Myc-regulated transcription. Mol. Cell 2003, 11, 1189–1200. [Google Scholar] [CrossRef]
- Egozi, D.; Shapira, M.; Paor, G.; Ben-Izhak, O.; Skorecki, K.; Hershko, D.D. Regulation of the cell cycle inhibitor p27 and its ubiquitin ligase Skp2 in differentiation of human embryonic stem cells. FASEB J. 2007, 21, 2807–2817. [Google Scholar] [CrossRef]
- Hillje, A.L.; Worlitzer, M.M.; Palm, T.; Schwamborn, J.C. Neural stem cells maintain their stemness through protein kinase C ζ-mediated inhibition of TRIM32. Stem Cells 2011, 29, 1437–1447. [Google Scholar] [PubMed]
- Fults, D.; Pedone, C.; Dai, C.; Holland, E.C. MYC Expression Promotes the Proliferation of Neural Progenitor Cells in Culture and In Vivo. Neoplasia 2002, 4, 32–39. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ke, Y.; Zhang, E.E.; Hagihara, K.; Wu, D.; Pang, Y.; Klein, R.; Curran, T.; Ranscht, B.; Feng, G.-S. Deletion of Shp2 in the Brain Leads to Defective Proliferation and Differentiation in Neural Stem Cells and Early Postnatal Lethality. Mol. Cell. Biol. 2007, 27, 6706–6717. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oishi, Y.; Manabe, I. Krüppel-Like Factors in Metabolic Homeostasis and Cardiometabolic Disease. Front. Cardiovasc. Med. 2018, 5, 69. [Google Scholar] [CrossRef]
- Pearson, R.; Fleetwood, J.; Eaton, S.; Crossley, M.; Bao, S. Krüppel-like transcription factors: A functional family. Int. J. Biochem. Cell Biol. 2008, 40, 1996–2001. [Google Scholar] [CrossRef]
- Jiang, J.; Chan, Y.-S.; Loh, Y.-H.; Cai, J.; Tong, G.-Q.; Lim, C.-A.; Robson, P.R.H.; Zhong, S.; Ng, H.-H. A core Klf circuitry regulates self-renewal of embryonic stem cells. Nat. Cell Biol. 2008, 10, 353–360. [Google Scholar] [CrossRef]
- Zhang, P.; Andrianakos, R.; Yang, Y.; Liu, C.; Lu, W. Kruppel-like Factor 4 (Klf4) Prevents Embryonic Stem (ES) Cell Differentiation by Regulating Nanog Gene Expression*. J. Biol. Chem. 2010, 285, 9180–9189. [Google Scholar] [CrossRef] [Green Version]
- Aksoy, I.; Giudice, V.; Delahaye, E.; Wianny, F.; Aubry, M.; Mure, M.; Chen, J.; Jauch, R.; Bogu, G.K.; Nolden, T.; et al. Klf4 and Klf5 differentially inhibit mesoderm and endoderm differentiation in embryonic stem cells. Nat. Commun. 2014, 5, 3719. [Google Scholar] [CrossRef] [Green Version]
- Yeo, J.-C.; Jiang, J.; Tan, Z.-Y.; Yim, G.-R.; Göke, J.; Kraus, P.; Liang, H.; Gonzales, K.A.U.; Chong, H.-C.; Tan, C.-P.; et al. Klf2 Is an Essential Factor that Sustains Ground State Pluripotency. Cell Stem Cell 2014, 14, 864–872. [Google Scholar] [CrossRef] [Green Version]
- Guo, G.; Yang, J.; Nichols, J.; Hall, J.S.; Eyres, I.; Mansfield, W.; Smith, A. Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 2009, 136, 1063–1069. [Google Scholar] [CrossRef] [Green Version]
- Hanna, J.H.; Cheng, A.W.; Saha, K.; Kim, J.; Lengner, C.J.; Soldner, F.; Cassady, J.P.; Muffat, J.; Carey, B.W.; Jaenisch, R. Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. Proc. Natl. Acad. Sci. USA 2010, 107, 9222–9227. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dunn, S.-J.; Martello, G.; Yordanov, B.; Emmott, S.; Smith, A. Defining an essential transcription factor program for naive pluripotency. Science 2014, 344, 1156–1160. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dhaliwal, N.K.; Abatti, L.E.; Mitchell, J.A. KLF4 protein stability regulated by interaction with pluripotency transcription factors overrides transcriptional control. Genes Dev. 2019, 33, 1069–1082. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, M.O.; Kim, S.-H.; Cho, Y.-Y.; Nadas, J.; Jeong, C.-H.; Yao, K.; Kim, D.J.; Yu, D.-H.; Keum, Y.-S.; Lee, K.-Y.; et al. ERK1 and ERK2 regulate embryonic stem cell self-renewal through phosphorylation of Klf4. Nat. Struct. Mol. Biol. 2012, 19, 283–290. [Google Scholar] [CrossRef]
- Gu, H.; Li, Q.; Huang, S.; Lu, W.; Cheng, F.; Gao, P.; Wang, C.; Miao, L.; Mei, Y.; Wu, M. Mitochondrial E3 ligase March5 maintains stemness of mouse ES cells via suppression of ERK signalling. Nat. Commun. 2015, 6, 7112. [Google Scholar] [CrossRef] [Green Version]
- Yonashiro, R.; Sugiura, A.; Miyachi, M.; Fukuda, T.; Matsushita, N.; Inatome, R.; Ogata, Y.; Suzuki, T.; Dohmae, N.; Yanagi, S. Mitochondrial Ubiquitin Ligase MITOL Ubiquitinates Mutant SOD1 and Attenuates Mutant SOD1-induced Reactive Oxygen Species Generation. Mol. Biol. Cell 2009, 20, 4524–4530. [Google Scholar] [CrossRef] [Green Version]
- Karbowski, M.; Neutzner, A.; Youle, R.J. The mitochondrial E3 ubiquitin ligase MARCH5 is required for Drp1 dependent mitochondrial division. J. Cell Biol. 2007, 178, 71–84. [Google Scholar] [CrossRef]
- Park, Y.-Y.; Lee, S.; Karbowski, M.; Neutzner, A.; Youle, R.J.; Cho, H. Loss of MARCH5 mitochondrial E3 ubiquitin ligase induces cellular senescence through dynamin-related protein 1 and mitofusin 1. J. Cell Sci. 2010, 123, 619–626. [Google Scholar] [CrossRef] [Green Version]
- Shi, H.-X.; Liu, X.; Wang, Q.; Tang, P.; Liu, X.-Y.; Shan, Y.-F.; Wang, C. Mitochondrial Ubiquitin Ligase MARCH5 Promotes TLR7 Signaling by Attenuating TANK Action. PLoS Pathog. 2011, 7, e1002057. [Google Scholar] [CrossRef]
- Mattout, A.; Meshorer, E. Chromatin plasticity and genome organization in pluripotent embryonic stem cells. Curr. Opin. Cell Biol. 2010, 22, 334–341. [Google Scholar] [CrossRef]
- Bernstein, B.E.; Mikkelsen, T.S.; Xie, X.; Kamal, M.; Huebert, D.J.; Cuff, J.; Fry, B.; Meissner, A.; Wernig, M.; Plath, K.; et al. A Bivalent Chromatin Structure Marks Key Developmental Genes in Embryonic Stem Cells. Cell 2006, 125, 315–326. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhu, B.; Zheng, Y.; Pham, A.-D.; Mandal, S.S.; Erdjument-Bromage, H.; Tempst, P.; Reinberg, D. Monoubiquitination of Human Histone H2B: The Factors Involved and Their Roles in HOX Gene Regulation. Mol. Cell 2005, 20, 601–611. [Google Scholar] [CrossRef] [PubMed]
- Henry, K.W.; Wyce, A.; Lo, W.-S.; Duggan, L.J.; Emre, N.T.; Kao, C.-F.; Pillus, L.; Shilatifard, A.; Osley, M.A.; Berger, S.L. Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGA-associated Ubp8. Genes Dev. 2003, 17, 2648–2663. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kao, C.-F.; Hillyer, C.; Tsukuda, T.; Henry, K.; Berger, S.L.; Osley, M.A. Rad6 plays a role in transcriptional activation through ubiquitylation of histone H2B. Genes Dev. 2004, 18, 184–195. [Google Scholar] [CrossRef] [Green Version]
- Fuchs, G.; Shema, E.; Vesterman, R.; Kotler, E.; Wolchinsky, Z.; Wilder, S.; Golomb, L.; Pribluda, A.; Zhang, F.; Haj-Yahya, M.; et al. RNF20 and USP44 regulate stem cell differentiation by modulating H2B monoubiquitylation. Mol. Cell 2012, 46, 662–673. [Google Scholar] [CrossRef] [Green Version]
- Xie, W.; Miehe, M.; Laufer, S.; Johnsen, S.A. The H2B ubiquitin-protein ligase RNF40 is required for somatic cell reprogramming. Cell Death Dis. 2020, 11, 287. [Google Scholar] [CrossRef]
- Zhou, W.; Zhu, P.; Wang, J.; Pascual, G.; Ohgi, K.A.; Lozach, J.; Glass, C.K.; Rosenfeld, M.G. Histone H2A Monoubiquitination Represses Transcription by Inhibiting RNA Polymerase II Transcriptional Elongation. Mol. Cell 2008, 29, 69–80. [Google Scholar] [CrossRef] [Green Version]
- Nakagawa, T.; Kajitani, T.; Togo, S.; Masuko, N.; Ohdan, H.; Hishikawa, Y.; Koji, T.; Matsuyama, T.; Ikura, T.; Muramatsu, M.; et al. Deubiquitylation of histone H2A activates transcriptional initiation via trans-histone cross-talk with H3K4 di- and trimethylation. Genes Dev. 2008, 22, 37–49. [Google Scholar] [CrossRef] [Green Version]
- Endoh, M.; Endo, T.A.; Endoh, T.; Fujimura, Y.-I.; Ohara, O.; Toyoda, T.; Otte, A.P.; Okano, M.; Brockdorff, N.; Vidal, M.; et al. Polycomb group proteins Ring1A/B are functionally linked to the core transcriptional regulatory circuitry to maintain ES cell identity. Development 2008, 135, 1513–1524. [Google Scholar] [CrossRef] [Green Version]
- Wang, H.; Wang, L.; Erdjument-Bromage, H.; Vidal, M.; Tempst, P.; Jones, R.S.; Zhang, Y. Role of histone H2A ubiquitination in Polycomb silencing. Nat. Cell Biol. 2004, 431, 873–878. [Google Scholar] [CrossRef]
- De Napoles, M.; Mermoud, J.E.; Wakao, R.; Tang, Y.A.; Endoh, M.; Appanah, R.; Nesterova, T.B.; Silva, J.; Otte, A.P.; Vidal, M.; et al. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev. Cell 2004, 7, 663–676. [Google Scholar] [CrossRef] [PubMed]
- Stock, J.K.; Giadrossi, S.; Casanova, M.; Brookes, E.; Vidal, M.; Koseki, H.; Brockdorff, N.; Fisher, A.G.; Pombo, A. Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat. Cell Biol. 2007, 9, 1428–1435. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Van der Stoop, P.; Boutsma, E.A.; Hulsman, D.; Noback, S.; Heimerikx, M.; Kerkhoven, R.M.; Voncken, J.W.; Wessels, L.F.; van Lohuizen, M. Ubiquitin E3 ligase Ring1b/Rnf2 of polycomb repressive complex 1 contributes to stable maintenance of mouse embryonic stem cells. PLoS ONE 2008, 3, e2235. [Google Scholar] [CrossRef] [Green Version]
- Inoue, D.; Aihara, H.; Sato, T.; Mizusaki, H.; Doiguchi, M.; Higashi, M.; Imamura, Y.; Yoneda, M.; Miyanishi, T.; Fujii, S.; et al. Dzip3 regulates developmental genes in mouse embryonic stem cells by reorganizing 3D chromatin conformation. Sci. Rep. 2015, 5, 16567. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Okita, Y.; Nakayama, K.I. UPS delivers pluripotency. Cell Stem Cell 2012, 11, 728–730. [Google Scholar] [CrossRef] [Green Version]
- Gontan, C.; Achame, E.M.; Demmers, J.; Barakat, T.S.; Rentmeester, E.; Van Ijcken, W.; Grootegoed, J.A.; Gribnau, J. RNF12 initiates X-chromosome inactivation by targeting REX1 for degradation. Nat. Cell Biol. 2012, 485, 386–390. [Google Scholar] [CrossRef]
- Bustos, F.; Segarra-Fas, A.; Chaugule, V.K.; Brandenburg, L.; Branigan, E.; Toth, R.; Macartney, T.; Knebel, A.; Hay, R.T.; Walden, H.; et al. RNF12 X-Linked Intellectual Disability Mutations Disrupt E3 Ligase Activity and Neural Differentiation. Cell Rep. 2018, 23, 1599–1611. [Google Scholar] [CrossRef]
- Sui, X.; Wang, Y.; Du, Y.-X.; Liang, L.-J.; Zheng, Q.; Li, Y.-M.; Liu, L. Development and application of ubiquitin-based chemical probes. Chem. Sci. 2020, 11, 12633–12646. [Google Scholar] [CrossRef]
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Wu, Y.; Zhang, W. The Role of E3s in Regulating Pluripotency of Embryonic Stem Cells and Induced Pluripotent Stem Cells. Int. J. Mol. Sci. 2021, 22, 1168. https://doi.org/10.3390/ijms22031168
Wu Y, Zhang W. The Role of E3s in Regulating Pluripotency of Embryonic Stem Cells and Induced Pluripotent Stem Cells. International Journal of Molecular Sciences. 2021; 22(3):1168. https://doi.org/10.3390/ijms22031168
Chicago/Turabian StyleWu, Yahong, and Weiwei Zhang. 2021. "The Role of E3s in Regulating Pluripotency of Embryonic Stem Cells and Induced Pluripotent Stem Cells" International Journal of Molecular Sciences 22, no. 3: 1168. https://doi.org/10.3390/ijms22031168