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Front. Biol.    2014, Vol. 9 Issue (5) : 389-409    https://doi.org/10.1007/s11515-014-1326-y
REVIEW
RNA-binding proteins in pluripotency, differentiation, and reprogramming
Diana GUALLAR1,2,Jianlong WANG1,2,3,*()
1. The Black Family Stem Cell Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
2. Department of Developmental and Regenerative Biology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
3. The Graduate School of Biomedical Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
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Abstract

Embryonic stem cell maintenance, differentiation, and somatic cell reprogramming require the interplay of multiple pluripotency factors, epigenetic remodelers, and extracellular signaling pathways. RNA-binding proteins (RBPs) are involved in a wide range of regulatory pathways, from RNA metabolism to epigenetic modifications. In recent years we have witnessed more and more studies on the discovery of new RBPs and the assessment of their functions in a variety of biological systems, including stem cells. We review the current studies on RBPs and focus on those that have functional implications in pluripotency, differentiation, and/or reprogramming in both the human and mouse systems.
Keywords RNA-binding protein      embryonic stem cell      pluripotency      differentiation      somatic cell reprogramming      lncRNA     
Corresponding Author(s): Jianlong WANG   
Just Accepted Date: 24 July 2014   Issue Date: 11 October 2014
 Cite this article:   
Diana GUALLAR,Jianlong WANG. RNA-binding proteins in pluripotency, differentiation, and reprogramming[J]. Front. Biol., 2014, 9(5): 389-409.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-014-1326-y
https://academic.hep.com.cn/fib/EN/Y2014/V9/I5/389
RNA binding domainExampleFunctionReference
RRMRbfox2Regulation of alternative splicing of reprogramming and differentiationYeo et al., 2009; Venables et al., 2013b
SRSonRegulation of alternative splicing of pluripotency genes in hESCLu et al; 2013
KHhnRNP K and hnRNP E1/E2Translational control in erythroid differentiationOstareck et al., 1997
RGGhnRNPURNA/DNA binding, activation of OCT4 gene expressionChoi et al., 2011
PAZAgo2Regulation of miRNA and siRNA pathways for proper ESC maintenanceShekar et al., 2011
dsRBDDroshamicroRNA maturationKanellopoulou et al., 2005; Wang et al., 2007; Doyle et al., 2013
DEAD boxDDX5Regulation of splicing and transcription in cell differentiation and proliferationCaretti et al., 2006
ZnFLin28Inhibition of pri-miR-let7 processingPiskounova et al., 2011
PuFPum1Transcriptional repression and activation by binding to 3′UTR of target mRNAGalgano et al., 2008
Non canonicalEzh2Chromatin silencing through H3 K27 trimetylationZhao et al., 2010
Tab.1  RNA binding domains and representative proteins with functions in development, differentiation, and reprogramming
ProteinCell lineTechniqueReference
Rbfox2hESCsCLIP-seqYeo et al., 2009
mESCsCLIPJangi et al., 2014
Mouse brainHITS-CLIPWeyn-Vanhentenryck et al., 2014
Mbnl1/ Rbfox2hESCs/human fibroblastsHigh-throughput PCR for ASVenables et al., 2013b
SonhESCsRIP-qPCRLu et al., 2013
Srsf3P19CLIP-seq?nk? et al., 2012
Fip1mESCsCLIP-seqLackford et al., 2014
UnrDrosophilaRIP-seqMihailovic et al., 2012
Esrp1mESCsRIPFagoonee et al., 2013
DazlMouse testisOligo dT capturedTsui et al., 2000
Mouse testisUV-RIPReynolds et al., 2005
Pum1DrosophilaRIP-ChipGerber et al., 2006
Tagged-AGO2/Tagged-PUM2HEK293PAR-CLIPHafner et al., 2010a
Ago2mESCsRIPHanina et al., 2010
mESCsHITS-CLIPLeung et al., 2011
Mouse brain/HeLaHITS-CLIPChi et al., 2009
Dgcr8/DroshaHEK293HITS-CLIPMacias et al., 2012
Lin28hESCsCLIP-seqWilbert et al., 2012
mESCsCLIP-seqCho et al., 2012
Lsd1/Ezh2Foreskin fibroblasts (CRL-2091), lung fibroblasts (FL2), and HeLa (CCL-2)RIP-qPCRTsai et al., 2010
Ezh2mESCsRIP-seqZhao et al., 2010
mESCsPAR-CLIPKaneko et al., 2013
Suz12CEM cellsRIP-qPCRKanhere et al., 2010
Human foreskin and foot fibroblastsRIPRinn et al., 2007
Ezh2/Suz12/CoRESTHeLa, human fetal lung fibroblast, andforeskin fibroblastsRIP-Chip (native IP)Khalil et al., 2009
Jarid2mESCsPAR-CLIP/CLIP-qPCRKaneko et al., 2014
Wdr5mESCsRIPiTYang et al., 2014
Thoc2mESCsRIP-seqWang et al., 2013
Thoc5mESCsRIP-qPCRWang et al., 2013
Tagged-Rbm47mESCsRIP-PCRYeganeh et al., 2013
Tab.2  High-throughput studies of RBPs with roles in ESC maintenance, differentiation, and/or reprogramming discussed in this review
Fig.1  RBPs with important roles in ESC maintenance and/or differentiation are depicted according to the RNA metabolism step in which they are implicated. Ezh2, Suz12 and Lsd1 repress transcription whereas Wdr5 activates it, binding to chromatin through lncRNAs. Rbfox2 is implicated both in AS and AS-NMD, whereas Mbnl1, Son, Rbm47, U2af1, Srsf3 and Fus have only been reported to regulate AS. Fip1 mediates APA. Once processed, transcripts can either be retained in paraspeckles by PSPs or exported to the cytoplasm. Thoc2 and Thoc5 regulate the transport of important pluripotency-related transcripts in ESC. In the cytoplasm, transcripts are stabilized and transcribed to proteins or targeted for destabilization and/or miRNA silencing by Unr and Pum1 or Ago2 and PTB, respectively. Translation efficiency can be also subjected to regulation, through proteins such as Larp7 (stabilizer) or Esrp1 and Dazl (reduce ribosomal loading). Processing of pri-miRNAs by Drosha and pre-miRNA by Dicer gives rise to mature miRNAs available in the cytoplasm for transcript silencing. Lin28 affects its targets through targeting pre-miRNAs for degradation, therefore reducing the steady-state levels of miRNAs. From top to bottom: AS-NMD: alternative splicing-coupled nonsense-mediated decay, AS: alternative splicing; APA: alternative polyadenylation; PSPs: paraspeckle proteins; pri-miRNA: primary microRNA transcript; pre-miRNA: precursor microRNA transcript; miRNA: microRNA.
ProteinFunctional processReference
UnrEmbryonic developmentESC maintenanceBoussadia et al., 1997Elatmani et al., 2011
Paraspeckle proteinsESC differentiationPrasanth et al., 2005; Chen and Carmichael, 2009
Thoc2/Thoc5Embryonic developmentESC maintenance and somatic cell reprogrammingWang et al., 2006Ivanova et al., 2006; Ding et al., 2009; Subramanian et al., 2009; Chia et al., 2010
DicerEmbryonic developmentESC proliferation and differentiationBernstein et al., 2003Kanellopoulou et al., 2005; Murchison et al., 2005; Wang et al., 2007
Lin28Pluripotency maintenanceSomatic cell reprogrammingSchulman et al., 2005; Melton et al., 2010Yu et al., 2007
Ago2Post-implantation embryonic developmentESC proliferation and differentiationMorita et al., 2007Shekar et al., 2011
Ezh2X-inactivationESC differentiationZhao et al., 2008;Kaneko et al., 2010; Kanhere et al., 2010Zhao et al., 2010
Suz12ESC differentiationX-inactivationPasini et al., 2007Zhao et al., 2008;Kaneko et al., 2010; Kanhere et al., 2010
Jarid2ESC differentiationX-inactivationPeng et al. 2009; Pasini et al. 2010da Rocha et al., 2014; Kaneko et al. 2014
Rbfox2ESC viabilityESC differentiationYeo et al., 2009Venables et al., 2013b
Lsd1ESC differentiationAdamo et al., 2011; Whyte et al., 2012
Wdr5ESC maintenance and iPSC generationRamakrishna et al., 2011; Li et al., 2012; Yang et al., 2014
Fip1ESC self-renewal and differentiationDing et al., 2009; Hu et al., 2009; Lackford et al., 2014
SonESC maintenanceSomatic cell reprogrammingChia et al., 2010Lu et al., 2013
Tip110ESC maintenanceLiu et al., 2012; Liu et al., 2013
PTBRepression of a neural phenotype in non-neural cellsYuanchao Xue et al. 2013
U2af1Somatic cell reprogrammingOhta et al., 2013b
Srsf3Somatic cell reprogrammingOhta et al., 2013b
Mbnl1ESC differentiationVenables et al., 2013b
Esrp1ESC maintenance-differentiation balanceFagoonee et al., 2013
DazlESC maintenance-differentiation balanceXu et al., 2013
Larp7ESC maintenanceDai et al., 2014
Pum1ESC differentiationLeeb et al., 2014
Tab.3  Summary of the main RBPs with functions in ESC maintenance, differentiation or somatic cell reprogramming
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