Novel Approaches to Profile Functional Long Noncoding RNAs Associated with Stem Cell Pluripotency

Author(s): Yanbo Zhu, Zi Yan, Ze Tang*, Wei Li*

Journal Name: Current Genomics

Volume 21 , Issue 1 , 2020

Become EABM
Become Reviewer

Graphical Abstract:


The pluripotent state of stem cells depends on the complicated network orchestrated by thousands of factors and genes. Long noncoding RNAs (lncRNAs) are a class of RNA longer than 200 nt without a protein-coding function. Single-cell sequencing studies have identified hundreds of lncRNAs with dynamic changes in somatic cell reprogramming. Accumulating evidence suggests that they participate in the initiation of reprogramming, maintenance of pluripotency, and developmental processes by cis and/or trans mechanisms. In particular, they may interact with proteins, RNAs, and chromatin modifier complexes to form an intricate pluripotency-associated network. In this review, we focus on recent progress in approaches to profiling functional lncRNAs in somatic cell reprogramming and cell differentiation.

Keywords: Pluripotency, stem cells, long noncoding RNA, reprogramming, epigenetics, RNA sequencing.

Djebali, S.; Davis, C.A.; Merkel, A.; Dobin, A.; Lassmann, T.; Mortazavi, A.; Tanzer, A.; Lagarde, J.; Lin, W.; Schlesinger, F.; Xue, C.; Marinov, G.K.; Khatun, J.; Williams, B.A.; Zaleski, C.; Rozowsky, J.; Röder, M.; Kokocinski, F.; Abdelhamid, R.F.; Alioto, T.; Antoshechkin, I.; Baer, M.T.; Bar, N.S.; Batut, P.; Bell, K.; Bell, I.; Chakrabortty, S.; Chen, X.; Chrast, J.; Curado, J.; Derrien, T.; Drenkow, J.; Dumais, E.; Dumais, J.; Duttagupta, R.; Falconnet, E.; Fastuca, M.; Fejes-Toth, K.; Ferreira, P.; Foissac, S.; Fullwood, M.J.; Gao, H.; Gonzalez, D.; Gordon, A.; Gunawardena, H.; Howald, C.; Jha, S.; Johnson, R.; Kapranov, P.; King, B.; Kingswood, C.; Luo, O.J.; Park, E.; Persaud, K.; Preall, J.B.; Ribeca, P.; Risk, B.; Robyr, D.; Sammeth, M.; Schaffer, L.; See, L.H.; Shahab, A.; Skancke, J.; Suzuki, A.M.; Takahashi, H.; Tilgner, H.; Trout, D.; Walters, N.; Wang, H.; Wrobel, J.; Yu, Y.; Ruan, X.; Hayashizaki, Y.; Harrow, J.; Gerstein, M.; Hubbard, T.; Reymond, A.; Antonarakis, S.E.; Hannon, G.; Giddings, M.C.; Ruan, Y.; Wold, B.; Carninci, P.; Guigó, R.; Gingeras, T.R. Landscape of transcription in human cells. Nature, 2012, 489(7414), 101-108.
[] [PMID: 22955620]
Consortium, E.P. ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature, 2012, 489(7414), 57-74.
[] [PMID: 22955616]
Marques-Rocha, J.L.; Samblas, M.; Milagro, F.I.; Bressan, J.; Martínez, J.A.; Marti, A. Noncoding RNAs, cytokines, and inflammation-related diseases. FASEB J., 2015, 29(9), 3595-3611.
[] [PMID: 26065857]
Clark, M.B.; Mercer, T.R.; Bussotti, G.; Leonardi, T.; Haynes, K.R.; Crawford, J.; Brunck, M.E.; Cao, K.A.; Thomas, G.P.; Chen, W.Y.; Taft, R.J.; Nielsen, L.K.; Enright, A.J.; Mattick, J.S.; Dinger, M.E. Quantitative gene profiling of long noncoding RNAs with targeted RNA sequencing. Nat. Methods, 2015, 12(4), 339-342.
[] [PMID: 25751143]
Guttman, M.; Rinn, J.L. Modular regulatory principles of large non-coding RNAs. Nature, 2012, 482(7385), 339-346.
[] [PMID: 22337053]
Cabili, M.N.; Trapnell, C.; Goff, L.; Koziol, M.; Tazon-Vega, B.; Regev, A.; Rinn, J.L. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev., 2011, 25(18), 1915-1927.
[] [PMID: 21890647]
Rinn, J.L.; Chang, H.Y. Genome regulation by long noncoding RNAs. Annu. Rev. Biochem., 2012, 81, 145-166.
[] [PMID: 22663078]
Wang, K.C.; Chang, H.Y. Molecular mechanisms of long noncoding RNAs. Mol. Cell, 2011, 43(6), 904-914.
[] [PMID: 21925379]
Wilusz, J.E.; Sunwoo, H.; Spector, D.L. Long noncoding RNAs: functional surprises from the RNA world. Genes Dev., 2009, 23(13), 1494-1504.
[] [PMID: 19571179]
Huang, Y.; Liu, N.; Wang, J.P.; Wang, Y.Q.; Yu, X.L.; Wang, Z.B.; Cheng, X.C.; Zou, Q. Regulatory long non-coding RNA and its functions. J. Physiol. Biochem., 2012, 68(4), 611-618.
[] [PMID: 22535282]
López-León, M.; Outeiro, T.F.; Goya, R.G. Cell reprogramming: Therapeutic potential and the promise of rejuvenation for the aging brain. Ageing Res. Rev., 2017, 40, 168-181.
[] [PMID: 28903069]
Di Baldassarre, A.; Cimetta, E.; Bollini, S.; Gaggi, G.; Ghinassi, B. Human-induced pluripotent stem cell technology and cardiomyocyte generation: progress and clinical applications. Cells, 2018, 7(6)E48
[] [PMID: 29799480]
Dinger, M.E.; Amaral, P.P.; Mercer, T.R.; Pang, K.C.; Bruce, S.J.; Gardiner, B.B.; Askarian-Amiri, M.E.; Ru, K.; Soldà, G.; Simons, C.; Sunkin, S.M.; Crowe, M.L.; Grimmond, S.M.; Perkins, A.C.; Mattick, J.S. Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res., 2008, 18(9), 1433-1445.
[] [PMID: 18562676]
Guttman, M.; Donaghey, J.; Carey, B.W.; Garber, M.; Grenier, J.K.; Munson, G.; Young, G.; Lucas, A.B.; Ach, R.; Bruhn, L.; Yang, X.; Amit, I.; Meissner, A.; Regev, A.; Rinn, J.L.; Root, D.E.; Lander, E.S. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature, 2011, 477(7364), 295-300.
[] [PMID: 21874018]
Zheng, G.X.; Do, B.T.; Webster, D.E.; Khavari, P.A.; Chang, H.Y. Dicer-microRNA-Myc circuit promotes transcription of hundreds of long noncoding RNAs. Nat. Struct. Mol. Biol., 2014, 21(7), 585-590.
[] [PMID: 24929436]
Lin, N.; Chang, K.Y.; Li, Z.; Gates, K.; Rana, Z.A.; Dang, J.; Zhang, D.; Han, T.; Yang, C.S.; Cunningham, T.J.; Head, S.R.; Duester, G.; Dong, P.D.; Rana, T.M. An evolutionarily conserved long noncoding RNA TUNA controls pluripotency and neural lineage commitment. Mol. Cell, 2014, 53(6), 1005-1019.
[] [PMID: 24530304]
Ng, S.Y.; Johnson, R.; Stanton, L.W. Human long non-coding RNAs promote pluripotency and neuronal differentiation by association with chromatin modifiers and transcription factors. EMBO J., 2012, 31(3), 522-533.
[] [PMID: 22193719]
Perry, R.B.; Ulitsky, I. The functions of long noncoding RNAs in development and stem cells. Development, 2016, 143(21), 3882-3894.
[] [PMID: 27803057 ]
Cloonan, N.; Forrest, A.R.; Kolle, G.; Gardiner, B.B.; Faulkner, G.J.; Brown, M.K.; Taylor, D.F.; Steptoe, A.L.; Wani, S.; Bethel, G.; Robertson, A.J.; Perkins, A.C.; Bruce, S.J.; Lee, C.C.; Ranade, S.S.; Peckham, H.E.; Manning, J.M.; McKernan, K.J.; Grimmond, S.M. Stem cell transcriptome profiling via massive-scale mRNA sequencing. Nat. Methods, 2008, 5(7), 613-619.
[] [PMID: 18516046]
Wang, E.T.; Sandberg, R.; Luo, S.; Khrebtukova, I.; Zhang, L.; Mayr, C.; Kingsmore, S.F.; Schroth, G.P.; Burge, C.B. Alternative isoform regulation in human tissue transcriptomes. Nature, 2008, 456(7221), 470-476.
[] [PMID: 18978772]
Mortazavi, A.; Williams, B.A.; McCue, K.; Schaeffer, L.; Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods, 2008, 5(7), 621-628.
[] [PMID: 18516045]
Guttman, M.; Garber, M.; Levin, J.Z.; Donaghey, J.; Robinson, J.; Adiconis, X.; Fan, L.; Koziol, M.J.; Gnirke, A.; Nusbaum, C.; Rinn, J.L.; Lander, E.S.; Regev, A. Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat. Biotechnol., 2010, 28(5), 503-510.
[] [PMID: 20436462]
Pan, Q.; Shai, O.; Lee, L.J.; Frey, B.J.; Blencowe, B.J. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat. Genet., 2008, 40(12), 1413-1415.
[] [PMID: 18978789]
Maher, C.A.; Kumar-Sinha, C.; Cao, X.; Kalyana-Sundaram, S.; Han, B.; Jing, X.; Sam, L.; Barrette, T.; Palanisamy, N.; Chinnaiyan, A.M. Transcriptome sequencing to detect gene fusions in cancer. Nature, 2009, 458(7234), 97-101.
[] [PMID: 19136943]
Guttman, M.; Amit, I.; Garber, M.; French, C.; Lin, M.F.; Feldser, D.; Huarte, M.; Zuk, O.; Carey, B.W.; Cassady, J.P.; Cabili, M.N.; Jaenisch, R.; Mikkelsen, T.S.; Jacks, T.; Hacohen, N.; Bernstein, B.E.; Kellis, M.; Regev, A.; Rinn, J.L.; Lander, E.S. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature, 2009, 458(7235), 223-227.
[] [PMID: 19182780]
Yan, L.; Yang, M.; Guo, H.; Yang, L.; Wu, J.; Li, R.; Liu, P.; Lian, Y.; Zheng, X.; Yan, J.; Huang, J.; Li, M.; Wu, X.; Wen, L.; Lao, K.; Li, R.; Qiao, J.; Tang, F. Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat. Struct. Mol. Biol., 2013, 20(9), 1131-1139.
[] [PMID: 23934149]
Du, Z.; Jia, L.; Wang, Y.; Wang, C.; Wen, X.; Chen, J.; Zhu, Y.; Yu, D.; Zhou, L.; Chen, N.; Zhang, S.; Celik, I.; Ay, F.; Gao, S.; Zhang, S.; Li, W.; Hoffman, A.R.; Cui, J.; Hu, J.F. Combined RNA-seq and RAT-seq mapping of long noncoding RNAs in pluripotent reprogramming. Sci. Data, 2018, 5180255
Kim, D.H.; Marinov, G.K.; Pepke, S.; Singer, Z.S.; He, P.; Williams, B.; Schroth, G.P.; Elowitz, M.B.; Wold, B.J. Single-cell transcriptome analysis reveals dynamic changes in lncRNA expression during reprogramming. Cell Stem Cell, 2015, 16(1), 88-101.
[] [PMID: 25575081]
Chakraborty, D.; Kappei, D.; Theis, M.; Nitzsche, A.; Ding, L.; Paszkowski-Rogacz, M.; Surendranath, V.; Berger, N.; Schulz, H.; Saar, K.; Hubner, N.; Buchholz, F. Combined RNAi and localization for functionally dissecting long noncoding RNAs. Nat. Methods, 2012, 9(4), 360-362.
[] [PMID: 22327834]
Sheik Mohamed, J.; Gaughwin, P.M.; Lim, B.; Robson, P.; Lipovich, L. Conserved long noncoding RNAs transcriptionally regulated by Oct4 and Nanog modulate pluripotency in mouse embryonic stem cells. RNA, 2010, 16(2), 324-337.
[] [PMID: 20026622 ]
Bassett, A.R.; Akhtar, A.; Barlow, D.P.; Bird, A.P.; Brockdorff, N.; Duboule, D.; Ephrussi, A.; Ferguson-Smith, A.C.; Gingeras, T.R.; Haerty, W.; Higgs, D.R.; Miska, E.A.; Ponting, C.P. Considerations when investigating lncRNA function in vivo. eLife, 2014, 3e03058
[] [PMID: 25124674 ]
Sauvageau, M.; Goff, L.A.; Lodato, S.; Bonev, B.; Groff, A.F.; Gerhardinger, C.; Sanchez-Gomez, D.B.; Hacisuleyman, E.; Li, E.; Spence, M.; Liapis, S.C.; Mallard, W.; Morse, M.; Swerdel, M.R.; D’Ecclessis, M.F.; Moore, J.C.; Lai, V.; Gong, G.; Yancopoulos, G.D.; Frendewey, D.; Kellis, M.; Hart, R.P.; Valenzuela, D.M.; Arlotta, P.; Rinn, J.L. Multiple knockout mouse models reveal lincRNAs are required for life and brain development. eLife, 2013, 2e01749
[] [PMID: 24381249]
Liu, S.J.; Horlbeck, M.A.; Cho, S.W.; Birk, H.S.; Malatesta, M.; He, D.; Attenello, F.J.; Villalta, J.E.; Cho, M.Y.; Chen, Y.; Mandegar, M.A.; Olvera, M.P.; Gilbert, L.A.; Conklin, B.R.; Chang, H.Y.; Weissman, J.S.; Lim, D.A. CRISPRi-based genome-scale identification of functional long noncoding RNA loci in human cells. Science, 2017, 355(6320)aah7111
[] [PMID: 27980086]
Fulco, C.P.; Munschauer, M.; Anyoha, R.; Munson, G.; Grossman, S.R.; Perez, E.M.; Kane, M.; Cleary, B.; Lander, E.S.; Engreitz, J.M. Systematic mapping of functional enhancer-promoter connections with CRISPR interference. Science, 2016, 354(6313), 769-773.
[] [PMID: 27708057]
Yin, Y.; Yan, P.; Lu, J.; Song, G.; Zhu, Y.; Li, Z.; Zhao, Y.; Shen, B.; Huang, X.; Zhu, H.; Orkin, S.H.; Shen, X. Opposing roles for the lncRNA haunt and its genomic locus in regulating HOXA gene activation during embryonic stem cell differentiation. Cell Stem Cell, 2015, 16(5), 504-516.
[] [PMID: 25891907]
Zhu, S.; Li, W.; Liu, J.; Chen, C.H.; Liao, Q.; Xu, P.; Xu, H.; Xiao, T.; Cao, Z.; Peng, J.; Yuan, P.; Brown, M.; Liu, X.S.; Wei, W. Genome-scale deletion screening of human long non-coding RNAs using a paired-guide RNA CRISPR-Cas9 library. Nat. Biotechnol., 2016, 34(12), 1279-1286.
[] [PMID: 27798563]
Adamson, B.; Smogorzewska, A.; Sigoillot, F.D.; King, R.W.; Elledge, S.J. A genome-wide homologous recombination screen identifies the RNA-binding protein RBMX as a component of the DNA-damage response. Nat. Cell Biol., 2012, 14(3), 318-328.
[] [PMID: 22344029]
Zeng, Y.; Cullen, B.R. RNA interference in human cells is restricted to the cytoplasm. RNA, 2002, 8(7), 855-860.
[] [PMID: 12166640 ]
Krueger, U.; Bergauer, T.; Kaufmann, B.; Wolter, I.; Pilk, S.; Heider-Fabian, M.; Kirch, S.; Artz-Oppitz, C.; Isselhorst, M.; Konrad, J. Insights into effective RNAi gained from large-scale siRNA validation screening. Oligonucleotides, 2007, 17(2), 237-250.
[] [PMID: 17638527]
Kim, H.; Kim, J.S. A guide to genome engineering with programmable nucleases. Nat. Rev. Genet., 2014, 15(5), 321-334.
[] [PMID: 24690881]
Gaj, T.; Gersbach, C.A.; Barbas, C.F. III ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol., 2013, 31(7), 397-405.
[] [PMID: 23664777]
Mandegar, M.A.; Huebsch, N.; Frolov, E.B.; Shin, E.; Truong, A.; Olvera, M.P.; Chan, A.H.; Miyaoka, Y.; Holmes, K.; Spencer, C.I.; Judge, L.M.; Gordon, D.E.; Eskildsen, T.V.; Villalta, J.E.; Horlbeck, M.A.; Gilbert, L.A.; Krogan, N.J.; Sheikh, S.P.; Weissman, J.S.; Qi, L.S.; So, P.L.; Conklin, B.R. CRISPR interference efficiently induces specific and reversible gene silencing in human iPSCs. Cell Stem Cell, 2016, 18(4), 541-553.
[] [PMID: 26971820]
Gilbert, L.A.; Larson, M.H.; Morsut, L.; Liu, Z.; Brar, G.A.; Torres, S.E.; Stern-Ginossar, N.; Brandman, O.; Whitehead, E.H.; Doudna, J.A.; Lim, W.A.; Weissman, J.S.; Qi, L.S. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell, 2013, 154(2), 442-451.
[] [PMID: 23849981]
Shalem, O.; Sanjana, N.E.; Hartenian, E.; Shi, X.; Scott, D.A.; Mikkelson, T.; Heckl, D.; Ebert, B.L.; Root, D.E.; Doench, J.G.; Zhang, F. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science, 2014, 343(6166), 84-87.
[] [PMID: 24336571]
Wang, T.; Wei, J.J.; Sabatini, D.M.; Lander, E.S. Genetic screens in human cells using the CRISPR-Cas9 system. Science, 2014, 343(6166), 80-84.
[] [PMID: 24336569]
González, F.; Zhu, Z.; Shi, Z.D.; Lelli, K.; Verma, N.; Li, Q.V.; Huangfu, D. An iCRISPR platform for rapid, multiplexable, and inducible genome editing in human pluripotent stem cells. Cell Stem Cell, 2014, 15(2), 215-226.
[] [PMID: 24931489]
Gilbert, L.A.; Horlbeck, M.A.; Adamson, B.; Villalta, J.E.; Chen, Y.; Whitehead, E.H.; Guimaraes, C.; Panning, B.; Ploegh, H.L.; Bassik, M.C.; Qi, L.S.; Kampmann, M.; Weissman, J.S. Genome-scale CRISPR-mediated control of gene repression and activation. Cell, 2014, 159(3), 647-661.
[] [PMID: 25307932]
Qi, L.S.; Larson, M.H.; Gilbert, L.A.; Doudna, J.A.; Weissman, J.S.; Arkin, A.P.; Lim, W.A. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell, 2013, 152(5), 1173-1183.
[] [PMID: 23452860]
Liu, Z.; Hui, Y.; Shi, L.; Chen, Z.; Xu, X.; Chi, L.; Fan, B.; Fang, Y.; Liu, Y.; Ma, L.; Wang, Y.; Xiao, L.; Zhang, Q.; Jin, G.; Liu, L.; Zhang, X. Efficient CRISPR/Cas9-mediated versatile, predictable, and donor-free gene knockout in human pluripotent stem cells. Stem Cell Reports, 2016, 7(3), 496-507.
[] [PMID: 27594587]
Papp, B.; Plath, K. Epigenetics of reprogramming to induced pluripotency. Cell, 2013, 152(6), 1324-1343.
[] [PMID: 23498940]
Rodríguez-Ubreva, J.; Ballestar, E. Chromatin immunoprecipitation. Methods Mol. Biol., 2014, 1094, 309-318.
[] [PMID: 24162998 ]
Loh, Y.H.; Wu, Q.; Chew, J.L.; Vega, V.B.; Zhang, W.; Chen, X.; Bourque, G.; George, J.; Leong, B.; Liu, J.; Wong, K.Y.; Sung, K.W.; Lee, C.W.; Zhao, X.D.; Chiu, K.P.; Lipovich, L.; Kuznetsov, V.A.; Robson, P.; Stanton, L.W.; Wei, C.L.; Ruan, Y.; Lim, B.; Ng, H.H. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat. Genet., 2006, 38(4), 431-440.
[] [PMID: 16518401 ]
Zheng, L.; Zhai, Y.; Li, N.; Ma, F.; Zhu, H.; Du, X.; Li, G.; Hua, J. The modification of Tet1 in male germline stem cells and interact with PCNA, HDAC1 to promote their self-renewal and proliferation. Sci. Rep., 2016, 6, 37414.
[] [PMID: 27857213]
Cakouros, D.; Hemming, S.; Gronthos, K.; Liu, R.; Zannettino, A.; Shi, S.; Gronthos, S. Specific functions of TET1 and TET2 in regulating mesenchymal cell lineage determination. Epigenetics Chromatin, 2019, 12(1), 3.
[] [PMID: 30606231 ]
Fidalgo, M.; Huang, X.; Guallar, D.; Sanchez-Priego, C.; Valdes, V.J.; Saunders, A.; Ding, J.; Wu, W.S.; Clavel, C.; Wang, J. Zfp281 coordinates opposing functions of Tet1 and Tet2 in pluripotent states. Cell Stem Cell, 2016, 19(3), 355-369.
[] [PMID: 27345836]
Zhao, J.; Sun, B.K.; Erwin, J.A.; Song, J.J.; Lee, J.T. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science, 2008, 322(5902), 750-756.
[] [PMID: 18974356]
Dawlaty, M.M.; Breiling, A.; Le, T.; Barrasa, M.I.; Raddatz, G.; Gao, Q.; Powell, B.E.; Cheng, A.W.; Faull, K.F.; Lyko, F.; Jaenisch, R. Loss of Tet enzymes compromises proper differentiation of embryonic stem cells. Dev. Cell, 2014, 29(1), 102-111.
[] [PMID: 24735881 ]
Williams, K.; Christensen, J.; Pedersen, M.T.; Johansen, J.V.; Cloos, P.A.; Rappsilber, J.; Helin, K. TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature, 2011, 473(7347), 343-348.
[] [PMID: 21490601 ]
Gu, T.P.; Guo, F.; Yang, H.; Wu, H.P.; Xu, G.F.; Liu, W.; Xie, Z.G.; Shi, L.; He, X.; Jin, S.G.; Iqbal, K.; Shi, Y.G.; Deng, Z.; Szabó, P.E.; Pfeifer, G.P.; Li, J.; Xu, G.L. The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature, 2011, 477(7366), 606-610.
[] [PMID: 21892189]
Li, Z.; Cai, X.; Cai, C.L.; Wang, J.; Zhang, W.; Petersen, B.E.; Yang, F.C.; Xu, M. Deletion of Tet2 in mice leads to dysregulated hematopoietic stem cells and subsequent development of myeloid malignancies. Blood, 2011, 118(17), 4509-4518.
[] [PMID: 21803851]
Zelentsova, K.; Talmi, Z.; Abboud-Jarrous, G.; Sapir, T.; Capucha, T.; Nassar, M.; Burstyn-Cohen, T.; Protein, S. Protein S regulates neural stem cell quiescence and neurogenesis. Stem Cells, 2017, 35(3), 679-693.
[] [PMID: 27753164]
Muñoz Descalzo, S.; Rué, P.; Faunes, F.; Hayward, P.; Jakt, L.M.; Balayo, T.; Garcia-Ojalvo, J.; Martinez Arias, A. A competitive protein interaction network buffers Oct4-mediated differentiation to promote pluripotency in embryonic stem cells. Mol. Syst. Biol., 2013, 9, 694.
[] [PMID: 24104477]
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(7117), 364-368.
[] [PMID: 17093407]
Neri, F.; Incarnato, D.; Krepelova, A.; Rapelli, S.; Pagnani, A.; Zecchina, R.; Parlato, C.; Oliviero, S. Genome-wide analysis identifies a functional association of Tet1 and Polycomb repressive complex 2 in mouse embryonic stem cells. Genome Biol., 2013, 14(8), R91.
[] [PMID: 23987249]
Shen, X.; Kim, W.; Fujiwara, Y.; Simon, M.D.; Liu, Y.; Mysliwiec, M.R.; Yuan, G.C.; Lee, Y.; Orkin, S.H. Jumonji modulates polycomb activity and self-renewal versus differentiation of stem cells. Cell, 2009, 139(7), 1303-1314.
[] [PMID: 20064376]
Hadjimichael, C.; Chanoumidou, K.; Nikolaou, C.; Klonizakis, A.; Theodosi, G.I.; Makatounakis, T.; Papamatheakis, J.; Kretsovali, A. Promyelocytic leukemia protein is an essential regulator of stem cell pluripotency and somatic cell reprogramming. Stem Cell Reports, 2017, 8(5), 1366-1378.
[] [PMID: 28392218]
Wu, C.S.; Yu, C.Y.; Chuang, C.Y.; Hsiao, M.; Kao, C.F.; Kuo, H.C.; Chuang, T.J. Integrative transcriptome sequencing identifies trans-splicing events with important roles in human embryonic stem cell pluripotency. Genome Res., 2014, 24(1), 25-36.
[] [PMID: 24131564]
Yu, C.Y.; Kuo, H.C. The trans-spliced long noncoding RNA tsRMST impedes human embryonic stem cell differentiation through WNT5A-mediated inhibition of the epithelial-to-mesenchymal transition. Stem Cells, 2016, 34(8), 2052-2062.
[] [PMID: 27090862]
Yang, Y.W.; Flynn, R.A.; Chen, Y.; Qu, K.; Wan, B.; Wang, K.C.; Lei, M.; Chang, H.Y. Essential role of lncRNA binding for WDR5 maintenance of active chromatin and embryonic stem cell pluripotency. eLife, 2014, 3e02046
[] [PMID: 24521543]
Zhao, J.; Ohsumi, T.K.; Kung, J.T.; Ogawa, Y.; Grau, D.J.; Sarma, K.; Song, J.J.; Kingston, R.E.; Borowsky, M.; Lee, J.T. Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol. Cell, 2010, 40(6), 939-953.
[] [PMID: 21172659]
Morey, L.; Santanach, A.; Di Croce, L. Pluripotency and epigenetic factors in mouse embryonic stem cell fate regulation. Mol. Cell. Biol., 2015, 35(16), 2716-2728.
[] [PMID: 26031336]
Mohammad, F.; Pandey, G.K.; Mondal, T.; Enroth, S.; Redrup, L.; Gyllensten, U.; Kanduri, C. Long noncoding RNA-mediated maintenance of DNA methylation and transcriptional gene silencing. Development, 2012, 139(15), 2792-2803.
[] [PMID: 22721776 ]
Mondal, T.; Subhash, S.; Vaid, R.; Enroth, S.; Uday, S.; Reinius, B.; Mitra, S.; Mohammed, A.; James, A.R.; Hoberg, E.; Moustakas, A.; Gyllensten, U.; Jones, S.J.; Gustafsson, C.M.; Sims, A.H.; Westerlund, F.; Gorab, E.; Kanduri, C. MEG3 long noncoding RNA regulates the TGF-β pathway genes through formation of RNA-DNA triplex structures. Nat. Commun., 2015, 6, 7743.
[] [PMID: 26205790]
Chu, C.; Qu, K.; Zhong, F.L.; Artandi, S.E.; Chang, H.Y. Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol. Cell, 2011, 44(4), 667-678.
[] [PMID: 21963238]
Chu, C.; Chang, H.Y. Understanding RNA-chromatin interactions using chromatin isolation by RNA purification (ChIRP). Methods Mol. Biol., 2016, 1480, 115-123.
[] [PMID: 27659979]
Mondal, T.; Subhash, S.; Kanduri, C.; Chromatin, R.N.A. Immunoprecipitation (ChRIP). Methods Mol. Biol., 2018, 1689, 65-76.
[] [PMID: 29027165]
Pandey, R.R.; Mondal, T.; Mohammad, F.; Enroth, S.; Redrup, L.; Komorowski, J.; Nagano, T.; Mancini-Dinardo, D.; Kanduri, C. Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol. Cell, 2008, 32(2), 232-246.
[] [PMID: 18951091]
Engreitz, J.M.; Pandya-Jones, A.; McDonel, P.; Shishkin, A.; Sirokman, K.; Surka, C.; Kadri, S.; Xing, J.; Goren, A.; Lander, E.S.; Plath, K.; Guttman, M. The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science, 2013, 341(6147)1237973
[] [PMID: 23828888]
Chu, C.; Quinn, J.; Chang, H.Y. Chromatin isolation by RNA purification (ChIRP). J. Vis. Exp., 2012, 61, 3912.
Simon, M.D.; Wang, C.I.; Kharchenko, P.V.; West, J.A.; Chapman, B.A.; Alekseyenko, A.A.; Borowsky, M.L.; Kuroda, M.I.; Kingston, R.E. The genomic binding sites of a noncoding RNA. Proc. Natl. Acad. Sci. USA, 2011, 108(51), 20497-20502.
[] [PMID: 22143764]
Chu, C.; Spitale, R.C.; Chang, H.Y. Technologies to probe functions and mechanisms of long noncoding RNAs. Nat. Struct. Mol. Biol., 2015, 22(1), 29-35.
[] [PMID: 25565030]
Rando, O.J.; Chang, H.Y. Genome-wide views of chromatin structure. Annu. Rev. Biochem., 2009, 78, 245-271.
[] [PMID: 19317649]
Bhattacharya, D.; Talwar, S.; Mazumder, A.; Shivashankar, G.V. Spatio-temporal plasticity in chromatin organization in mouse cell differentiation and during Drosophila embryogenesis. Biophys. J., 2009, 96(9), 3832-3839.
[] [PMID: 19413989]
Thorpe, S.D.; Lee, D.A. Dynamic regulation of nuclear architecture and mechanics-a rheostatic role for the nucleus in tailoring cellular mechanosensitivity. Nucleus, 2017, 8(3), 287-300.
[] [PMID: 28152338]
Phillips-Cremins, J.E.; Sauria, M.E.; Sanyal, A.; Gerasimova, T.I.; Lajoie, B.R.; Bell, J.S.; Ong, C.T.; Hookway, T.A.; Guo, C.; Sun, Y.; Bland, M.J.; Wagstaff, W.; Dalton, S.; McDevitt, T.C.; Sen, R.; Dekker, J.; Taylor, J.; Corces, V.G. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell, 2013, 153(6), 1281-1295.
[] [PMID: 23706625]
Zhang, H.; Jiao, W.; Sun, L.; Fan, J.; Chen, M.; Wang, H.; Xu, X.; Shen, A.; Li, T.; Niu, B.; Ge, S.; Li, W.; Cui, J.; Wang, G.; Sun, J.; Fan, X.; Hu, X.; Mrsny, R.J.; Hoffman, A.R.; Hu, J.F. Intrachromosomal looping is required for activation of endogenous pluripotency genes during reprogramming. Cell Stem Cell, 2013, 13(1), 30-35.
[] [PMID: 23747202]
Lodato, M.A.; Ng, C.W.; Wamstad, J.A.; Cheng, A.W.; Thai, K.K.; Fraenkel, E.; Jaenisch, R.; Boyer, L.A. SOX2 co-occupies distal enhancer elements with distinct POU factors in ESCs and NPCs to specify cell state. PLoS Genet., 2013, 9(2)e1003288
[] [PMID: 23437007]
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(5), 631-642.
[] [PMID: 12787504]
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(4), 372-376.
[] [PMID: 10742100]
Takahashi, K.; Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 2006, 126(4), 663-676.
[] [PMID: 16904174]
Tang, F.; Barbacioru, C.; Bao, S.; Lee, C.; Nordman, E.; Wang, X.; Lao, K.; Surani, M.A. Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNA-Seq analysis. Cell Stem Cell, 2010, 6(5), 468-478.
[] [PMID: 20452321]
Zhang, S.; Wang, Y.; Jia, L.; Wen, X.; Du, Z.; Wang, C.; Hao, Y.; Yu, D.; Zhou, L.; Chen, N.; Chen, J.; Chen, H.; Zhang, H.; Celik, I.; Gülsoy, G.; Luo, J.; Qin, B.; Cui, X.; Liu, Z.; Zhang, S.; Esteban, M.A.; Ay, F.; Xu, W.; Chen, R.; Li, W.; Hoffman, A.R.; Hu, J.F.; Cui, J. Profiling the long noncoding RNA interaction network in the regulatory elements of target genes by chromatin in situ reverse transcription sequencing. Genome Res., 2019, 29(9), 1521-1532.
[] [PMID: 31315906]
Bergmann, J.H.; Li, J.; Eckersley-Maslin, M.A.; Rigo, F.; Freier, S.M.; Spector, D.L. Regulation of the ESC transcriptome by nuclear long noncoding RNAs. Genome Res., 2015, 25(9), 1336-1346.
[] [PMID: 26048247]
Sherstyuk, V.V.; Medvedev, S.P.; Zakian, S.M. Noncoding RNAs in the regulation of pluripotency and reprogramming. Stem Cell Rev Rep, 2018, 14(1), 58-70.
[] [PMID: 29143182]
Wang, X.; Arai, S.; Song, X.; Reichart, D.; Du, K.; Pascual, G.; Tempst, P.; Rosenfeld, M.G.; Glass, C.K.; Kurokawa, R. Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature, 2008, 454(7200), 126-130.
[] [PMID: 18509338]
Sigova, A.A.; Abraham, B.J.; Ji, X.; Molinie, B.; Hannett, N.M.; Guo, Y.E.; Jangi, M.; Giallourakis, C.C.; Sharp, P.A.; Young, R.A. Transcription factor trapping by RNA in gene regulatory elements. Science, 2015, 350(6263), 978-981.
[] [PMID: 26516199]
Xiang, J.F.; Yin, Q.F.; Chen, T.; Zhang, Y.; Zhang, X.O.; Wu, Z.; Zhang, S.; Wang, H.B.; Ge, J.; Lu, X.; Yang, L.; Chen, L.L. Human colorectal cancer-specific CCAT1-L lncRNA regulates long-range chromatin interactions at the MYC locus. Cell Res., 2014, 24(5), 513-531.
[] [PMID: 24662484]
Sun, J.; Li, W.; Sun, Y.; Yu, D.; Wen, X.; Wang, H.; Cui, J.; Wang, G.; Hoffman, A.R.; Hu, J.F. A novel antisense long noncoding RNA within the IGF1R gene locus is imprinted in hematopoietic malignancies. Nucleic Acids Res., 2014, 42(15), 9588-9601.
[] [PMID: 25092925]
Wang, H.; Li, W.; Guo, R.; Sun, J.; Cui, J.; Wang, G.; Hoffman, A.R.; Hu, J.F. An intragenic long noncoding RNA interacts epigenetically with the RUNX1 promoter and enhancer chromatin DNA in hematopoietic malignancies. Int. J. Cancer, 2014, 135(12), 2783-2794.
[] [PMID: 24752773]
Li, X.; Chen, N.; Zhou, L.; Wang, C.; Wen, X.; Jia, L.; Cui, J.; Hoffman, A.R.; Hu, J.F.; Li, W. Genome-wide target interactome profiling reveals a novel EEF1A1 epigenetic pathway for oncogenic lncRNA MALAT1 in breast cancer. Am. J. Cancer Res., 2019, 9(4), 714-729.
[PMID: 31105998]
Rudkin, G.T.; Stollar, B.D. High resolution detection of DNA-RNA hybrids in situ by indirect immunofluorescence. Nature, 1977, 265(5593), 472-473.
[] [PMID: 401954]
Cui, C.; Shu, W.; Li, P. Fluorescence in situ hybridization: cell-based genetic diagnostic and research applications. Front. Cell Dev. Biol., 2016, 4, 89.
[] [PMID: 27656642 ]
Kwon, S. Single-molecule fluorescence in situ hybridization: quantitative imaging of single RNA molecules. BMB Rep., 2013, 46(2), 65-72.
[] [PMID: 23433107]
Pollex, T.; Piolot, T.; Heard, E. Live-cell imaging combined with immunofluorescence, RNA, or DNA FISH to study the nuclear dynamics and expression of the X-inactivation center. Methods Mol. Biol., 2013, 1042, 13-31.
[] [PMID: 23979997]
Ross, F.M.; Avet-Loiseau, H.; Ameye, G.; Gutiérrez, N.C.; Liebisch, P.; O’Connor, S.; Dalva, K.; Fabris, S.; Testi, A.M.; Jarosova, M.; Hodkinson, C.; Collin, A.; Kerndrup, G.; Kuglik, P.; Ladon, D.; Bernasconi, P.; Maes, B.; Zemanova, Z.; Michalova, K.; Michau, L.; Neben, K.; Hermansen, N.E.; Rack, K.; Rocci, A.; Protheroe, R.; Chiecchio, L.; Poirel, H.A.; Sonneveld, P.; Nyegaard, M.; Johnsen, H.E. European Myeloma Network. Report from the European Myeloma Network on interphase FISH in multiple myeloma and related disorders. Haematologica, 2012, 97(8), 1272-1277.
[] [PMID: 22371180]
Imataka, G.; Arisaka, O. Chromosome analysis using spectral karyotyping (SKY). Cell Biochem. Biophys., 2012, 62(1), 13-17.
[] [PMID: 21948110 ]
Takizawa, T.; Meaburn, K.J.; Misteli, T. The meaning of gene positioning. Cell, 2008, 135(1), 9-13.
[] [PMID: 18854147]
Chaumeil, J.; Augui, S.; Chow, J.C.; Heard, E. Combined immunofluorescence, RNA fluorescent in situ hybridization, and DNA fluorescent in situ hybridization to study chromatin changes, transcriptional activity, nuclear organization, and X-chromosome inactivation. Methods Mol. Biol., 2008, 463, 297-308.
[] [PMID: 18951174]
Namekawa, S.H.; Lee, J.T. Detection of nascent RNA, single-copy DNA and protein localization by immunoFISH in mouse germ cells and preimplantation embryos. Nat. Protoc., 2011, 6(3), 270-284.
[] [PMID: 21372809]
Barakat, T.S.; Gribnau, J. Combined DNA-RNA fluorescent in situ hybridization (FISH) to study X chromosome inactivation in differentiated female mouse embryonic stem cells. J. Vis. Exp., 2014, 88e51628
[] [PMID: 24961515]

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2020
Page: [37 - 45]
Pages: 9
DOI: 10.2174/1389202921666200210142840
Price: $65

Article Metrics

PDF: 21
PRC: 1