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Stem Cells International
Volume 2017, Article ID 3250624, 13 pages
https://doi.org/10.1155/2017/3250624
Review Article

When Long Noncoding RNAs Meet Genome Editing in Pluripotent Stem Cells

1State Key Laboratory of Medicinal Chemical Biology, Nankai University, Tianjin 300371, China
2College of Pharmacy, Nankai University, Tianjin 300350, China

Correspondence should be addressed to Xinyi Lu; nc.ude.iaknan@yxul

Received 30 August 2017; Accepted 25 October 2017; Published 23 November 2017

Academic Editor: Qiang Wu

Copyright © 2017 Fuquan Chen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Mandai, A. Watanabe, Y. Kurimoto et al., “Autologous induced stem-cell–derived retinal cells for macular degeneration,” The New England Journal of Medicine, vol. 376, no. 11, pp. 1038–1046, 2017. View at Publisher · View at Google Scholar
  2. A. Necsulea, M. Soumillon, M. Warnefors et al., “The evolution of lncRNA repertoires and expression patterns in tetrapods,” Nature, vol. 505, no. 7485, pp. 635–640, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Kapusta, Z. Kronenberg, V. J. Lynch et al., “Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs,” PLoS Genetics, vol. 9, no. 4, article e1003470, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. P. Bertone, V. Stolc, T. E. Royce et al., “Global identification of human transcribed sequences with genome tiling arrays,” Science, vol. 306, no. 5705, pp. 2242–2246, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. P. Kapranov, S. E. Cawley, J. Drenkow et al., “Large-scale transcriptional activity in chromosomes 21 and 22,” Science, vol. 296, no. 5569, pp. 916–919, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. P. Kapranov, J. Cheng, S. Dike et al., “RNA maps reveal new RNA classes and a possible function for pervasive transcription,” Science, vol. 316, no. 5830, pp. 1484–1488, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. P. Carninci, T. Kasukawa, S. Katayama et al., “The transcriptional landscape of the mammalian genome,” Science, vol. 309, no. 5740, pp. 1559–1563, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. E. Birney, J. A. Stamatoyannopoulos, A. Dutta et al., “Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project,” Nature, vol. 447, no. 7146, pp. 799–816, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. C. Liu, B. Bai, G. Skogerbø et al., “NONCODE: an integrated knowledge database of non-coding RNAs,” Nucleic Acids Research, vol. 33, Database issue, pp. D112–D115, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. C. C. Hon, J. A. Ramilowski, J. Harshbarger et al., “An atlas of human long non-coding RNAs with accurate 5 ends,” Nature, vol. 543, no. 7644, pp. 199–204, 2017. View at Publisher · View at Google Scholar
  11. G. Bussotti, T. Leonardi, M. B. Clark et al., “Improved definition of the mouse transcriptome via targeted RNA sequencing,” Genome Research, vol. 26, no. 5, pp. 705–716, 2016. View at Publisher · View at Google Scholar · View at Scopus
  12. G. Liang, J. C. Y. Lin, V. Wei et al., “Distinct localization of histone H3 acetylation and H3-K4 methylation to the transcription start sites in the human genome,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 19, pp. 7357–7362, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. M. G. Guenther, S. S. Levine, L. A. Boyer, R. Jaenisch, and R. A. Young, “A chromatin landmark and transcription initiation at most promoters in human cells,” Cell, vol. 130, no. 1, pp. 77–88, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. T. S. Mikkelsen, M. Ku, D. B. Jaffe et al., “Genome-wide maps of chromatin state in pluripotent and lineage-committed cells,” Nature, vol. 448, no. 7153, pp. 553–560, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Guttman, I. Amit, M. Garber et al., “Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals,” Nature, vol. 458, no. 7235, pp. 223–227, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. C. Zhong, Q. Yin, Z. Xie et al., “CRISPR-Cas9-mediated genetic screening in mice with haploid embryonic stem cells carrying a guide RNA library,” Cell Stem Cell, vol. 17, no. 2, pp. 221–232, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. X. Lu, F. Sachs, L. A. Ramsay et al., “The retrovirus HERVH is a long noncoding RNA required for human embryonic stem cell identity,” Nature Structural & Molecular Biology, vol. 21, no. 4, pp. 423–425, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. V. Tripathi, J. D. Ellis, Z. Shen et al., “The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation,” Molecular Cell, vol. 39, no. 6, pp. 925–938, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. J. H. Yoon, K. Abdelmohsen, S. Srikantan et al., “LincRNA-p21 suppresses target mRNA translation,” Molecular Cell, vol. 47, no. 4, pp. 648–655, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. T. P. Zwaka and J. A. Thomson, “Homologous recombination in human embryonic stem cells,” Nature Biotechnology, vol. 21, no. 3, pp. 319–321, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Giudice and A. Trounson, “Genetic modification of human embryonic stem cells for derivation of target cells,” Cell Stem Cell, vol. 2, no. 5, pp. 422–433, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. D. Hockemeyer and R. Jaenisch, “Induced pluripotent stem cells meet genome editing,” Cell Stem Cell, vol. 18, no. 5, pp. 573–586, 2016. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Hotta and S. Yamanaka, “From genomics to gene therapy: induced pluripotent stem cells meet genome editing,” Annual Review of Genetics, vol. 49, no. 1, pp. 47–70, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Alwin, M. B. Gere, E. Guhl et al., “Custom zinc-finger nucleases for use in human cells,” Molecular Therapy, vol. 12, no. 4, pp. 610–617, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. J. C. Miller, S. Tan, G. Qiao et al., “A TALE nuclease architecture for efficient genome editing,” Nature Biotechnology, vol. 29, no. 2, pp. 143–148, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. F. Zhang, L. Cong, S. Lodato, S. Kosuri, G. M. Church, and P. Arlotta, “Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription,” Nature Biotechnology, vol. 29, no. 2, pp. 149–153, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Jinek, K. Chylinski, I. Fonfara, M. Hauer, J. A. Doudna, and E. Charpentier, “A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity,” Science, vol. 337, no. 6096, pp. 816–821, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. L. Cong, F. A. Ran, D. Cox et al., “Multiplex genome engineering using CRISPR/Cas systems,” Science, vol. 339, no. 6121, pp. 819–823, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. P. P. Amaral, M. B. Clark, D. K. Gascoigne, M. E. Dinger, and J. S. Mattick, “lncRNAdb: a reference database for long noncoding RNAs,” Nucleic Acids Research, vol. 39, Supplement 1, pp. D146–D151, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. D. Bhartiya, K. Pal, S. Ghosh et al., “lncRNome: a comprehensive knowledgebase of human long noncoding RNAs,” Database, vol. 2013, article bat034, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Park, N. Yu, I. Choi, W. Kim, and S. Lee, “lncRNAtor: a comprehensive resource for functional investigation of long non-coding RNAs,” Bioinformatics, vol. 30, no. 17, pp. 2480–2485, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Ma, A. Li, D. Zou et al., “LncRNAWiki: harnessing community knowledge in collaborative curation of human long non-coding RNAs,” Nucleic Acids Research, vol. 43, no. D1, pp. D187–D192, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. P. J. Volders, K. Helsens, X. Wang et al., “LNCipedia: a database for annotated human lncRNA transcript sequences and structures,” Nucleic Acids Research, vol. 41, no. D1, pp. D246–D251, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. K. Liu, Z. Yan, Y. Li, and Z. Sun, “Linc2GO: a human LincRNA function annotation resource based on ceRNA hypothesis,” Bioinformatics, vol. 29, no. 17, pp. 2221-2222, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. J. H. Li, S. Liu, H. Zhou, L. H. Qu, and J. H. Yang, “starBase v2.0: decoding miRNA-ceRNA, miRNA-ncRNA and protein–RNA interaction networks from large-scale CLIP-Seq data,” Nucleic Acids Research, vol. 42, no. D1, pp. D92–D97, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Yuan, W. Wu, C. Xie, G. Zhao, Y. Zhao, and R. Chen, “NPInter v2.0: an updated database of ncRNA interactions,” Nucleic Acids Research, vol. 42, no. D1, pp. D104–D108, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Wang, S. Ning, Y. Zhang et al., “Identification of lncRNA-associated competing triplets reveals global patterns and prognostic markers for cancer,” Nucleic Acids Research, vol. 43, no. 7, pp. 3478–3489, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. J. H. Yang, J. H. Li, S. Jiang, H. Zhou, and L. H. Qu, “ChIPBase: a database for decoding the transcriptional regulation of long non-coding RNA and microRNA genes from ChIP-Seq data,” Nucleic Acids Research, vol. 41, no. D1, pp. D177–D187, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Ning, Z. Zhao, J. Ye et al., “SNP@lincTFBS: an integrated database of polymorphisms in human LincRNA transcription factor binding sites,” PLoS One, vol. 9, no. 7, article e103851, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. Q. Jiang, J. Wang, Y. Wang, R. Ma, X. Wu, and Y. Li, “TF2LncRNA: identifying common transcription factors for a list of lncRNA genes from ChIP-Seq data,” BioMed Research International, vol. 2014, Article ID 317642, 5 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. Z. Zhou, Y. Shen, M. R. Khan, and A. Li, “LncReg: a reference resource for lncRNA-associated regulatory networks,” Database, vol. 2015, article bav083, 2015. View at Publisher · View at Google Scholar · View at Scopus
  42. Z. Zhao, J. Bai, A. Wu et al., “Co-LncRNA: investigating the lncRNA combinatorial effects in GO annotations and KEGG pathways based on human RNA-Seq data,” Database, vol. 2015, article bav082, 2015. View at Publisher · View at Google Scholar · View at Scopus
  43. T. Weirick, D. John, S. Dimmeler, and S. Uchida, “C-It-Loci: a knowledge database for tissue-enriched loci,” Bioinformatics, vol. 31, no. 21, pp. 3537–3543, 2015. View at Publisher · View at Google Scholar · View at Scopus
  44. G. Chen, Z. Wang, D. Wang et al., “LncRNADisease: a database for long-non-coding RNA-associated diseases,” Nucleic Acids Research, vol. 41, no. D1, pp. D983–D986, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. Y. Liu and M. Zhao, “lnCaNet: pan-cancer co-expression network for human lncRNA and cancer genes,” Bioinformatics, vol. 32, no. 10, pp. 1595–1597, 2016. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Ning, J. Zhang, P. Wang et al., “Lnc2Cancer: a manually curated database of experimentally supported lncRNAs associated with various human cancers,” Nucleic Acids Research, vol. 44, no. D1, pp. D980–D985, 2016. View at Publisher · View at Google Scholar · View at Scopus
  47. K. L. Yap, S. Li, A. M. Muñoz-Cabello et al., “Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a,” Molecular Cell, vol. 38, no. 5, pp. 662–674, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. J. L. Rinn, M. Kertesz, J. K. Wang et al., “Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs,” Cell, vol. 129, no. 7, pp. 1311–1323, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. S. L. Bumgarner, G. Neuert, B. F. Voight et al., “Single-cell analysis reveals that noncoding RNAs contribute to clonal heterogeneity by modulating transcription factor recruitment,” Molecular Cell, vol. 45, no. 4, pp. 470–482, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. N. Lin, K. Y. Chang, Z. Li et al., “An evolutionarily conserved long noncoding RNA TUNA controls pluripotency and neural lineage commitment,” Molecular Cell, vol. 53, no. 6, pp. 1005–1019, 2014. View at Publisher · View at Google Scholar · View at Scopus
  51. K. C. Wang, Y. W. Yang, B. Liu et al., “A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression,” Nature, vol. 472, no. 7341, pp. 120–124, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. S. J. Hainer, J. A. Pruneski, R. D. Mitchell, R. M. Monteverde, and J. A. Martens, “Intergenic transcription causes repression by directing nucleosome assembly,” Genes & Development, vol. 25, no. 1, pp. 29–40, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. K. Hirota, T. Miyoshi, K. Kugou, C. S. Hoffman, T. Shibata, and K. Ohta, “Stepwise chromatin remodelling by a cascade of transcription initiation of non-coding RNAs,” Nature, vol. 456, no. 7218, pp. 130–134, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. D. S. W. Tan, F. T. Chong, H. S. Leong et al., “Long noncoding RNA EGFR-AS1 mediates epidermal growth factor receptor addiction and modulates treatment response in squamous cell carcinoma,” Nature Medicine, vol. 23, no. 10, pp. 1167–1175, 2017. View at Publisher · View at Google Scholar
  55. S. Loewer, M. N. Cabili, M. Guttman et al., “Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells,” Nature Genetics, vol. 42, no. 12, pp. 1113–1117, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. X. Liu, D. Li, W. Zhang, M. Guo, and Q. Zhan, “Long non-coding RNA gadd7 interacts with TDP-43 and regulates Cdk6 mRNA decay,” The EMBO Journal, vol. 31, no. 23, pp. 4415–4427, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. L. Zhang, Z. Yang, J. Trottier, O. Barbier, and L. Wang, “Long noncoding RNA MEG3 induces cholestatic liver injury by interaction with PTBP1 to facilitate shp mRNA decay,” Hepatology, vol. 65, no. 2, pp. 604–615, 2017. View at Publisher · View at Google Scholar · View at Scopus
  58. C. Carrieri, L. Cimatti, M. Biagioli et al., “Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat,” Nature, vol. 491, no. 7424, pp. 454–457, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. J. Durruthy-Durruthy, V. Sebastiano, M. Wossidlo et al., “The primate-specific noncoding RNA HPAT5 regulates pluripotency during human preimplantation development and nuclear reprogramming,” Nature Genetics, vol. 48, no. 1, pp. 44–52, 2016. View at Publisher · View at Google Scholar · View at Scopus
  60. Y. Wang, F. Chen, M. Zhao et al., “The long noncoding RNA HULC promotes liver cancer by increasing the expression of the HMGA2 oncogene via sequestration of the microRNA-186,” The Journal of Biological Chemistry, vol. 292, no. 37, pp. 15395–15407, 2017. View at Publisher · View at Google Scholar
  61. A. Matsumoto, A. Pasut, M. Matsumoto et al., “mTORC1 and muscle regeneration are regulated by the LINC00961-encoded SPAR polypeptide,” Nature, vol. 541, no. 7636, pp. 228–232, 2017. View at Publisher · View at Google Scholar
  62. M. Eissmann, T. Gutschner, M. Hämmerle et al., “Loss of the abundant nuclear non-coding RNA MALAT1 is compatible with life and development,” RNA Biology, vol. 9, no. 8, pp. 1076–1087, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. Y. Yin, P. Yan, J. Lu et al., “Opposing roles for the lncRNA Haunt and its genomic locus in regulating HOXA gene activation during embryonic stem cell differentiation,” Cell Stem Cell, vol. 16, no. 5, pp. 504–516, 2015. View at Publisher · View at Google Scholar · View at Scopus
  64. M. R. Capecchi, “Gene targeting in mice: functional analysis of the mammalian genome for the twenty-first century,” Nature Reviews Genetics, vol. 6, no. 6, pp. 507–512, 2005. View at Publisher · View at Google Scholar · View at Scopus
  65. P. A. Latos, S. H. Stricker, L. Steenpass et al., “An in vitro ES cell imprinting model shows that imprinted expression of the Igf2r gene arises from an allele-specific expression bias,” Development, vol. 136, no. 3, pp. 437–448, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. P. A. Leighton, R. S. Ingram, J. Eggenschwiler, A. Efstratiadis, and S. M. Tilghman, “Disruption of imprinting caused by deletion of the H19 gene region in mice,” Nature, vol. 375, no. 6526, pp. 34–39, 1995. View at Publisher · View at Google Scholar
  67. M. Blasco, W. Funk, B. Villeponteau, and C. Greider, “Functional characterization and developmental regulation of mouse telomerase RNA,” Science, vol. 269, no. 5228, pp. 1267–1270, 1995. View at Publisher · View at Google Scholar
  68. J. Feng, W. Funk, S. Wang et al., “The RNA component of human telomerase,” Science, vol. 269, no. 5228, pp. 1236–1241, 1995. View at Publisher · View at Google Scholar
  69. H. Niida, T. Matsumoto, H. Satoh et al., “Severe growth defect in mouse cells lacking the telomerase RNA component,” Nature Genetics, vol. 19, no. 2, pp. 203–206, 1998. View at Publisher · View at Google Scholar · View at Scopus
  70. J. Huang, F. Wang, M. Okuka et al., “Association of telomere length with authentic pluripotency of ES/iPS cells,” Cell Research, vol. 21, no. 5, pp. 779–792, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. E. Herrera, E. Samper, J. Martín-Caballero, J. M. Flores, H. W. Lee, and M. A. Blasco, “Disease states associated with telomerase deficiency appear earlier in mice with short telomeres,” The EMBO Journal, vol. 18, no. 11, pp. 2950–2960, 1999. View at Publisher · View at Google Scholar · View at Scopus
  72. Y. Liu, D. Luo, H. Zhao, Z. Zhu, W. Hu, and C. H. K. Cheng, “Inheritable and precise large genomic deletions of non-coding RNA genes in zebrafish using TALENs,” PLoS One, vol. 8, no. 10, article e76387, 2013. View at Publisher · View at Google Scholar · View at Scopus
  73. T. T. Ho, N. Zhou, J. Huang et al., “Targeting non-coding RNAs with the CRISPR/Cas9 system in human cell lines,” Nucleic Acids Research, vol. 43, no. 3, article e17, 2015. View at Publisher · View at Google Scholar · View at Scopus
  74. M. Zhang, Y. Liu, G. Liu et al., “Rapidly generating knockout mice from H19-Igf2 engineered androgenetic haploid embryonic stem cells,” Cell Discovery, vol. 1, article 15031, 2015. View at Publisher · View at Google Scholar
  75. C. Zhong, Z. Xie, Q. Yin et al., “Parthenogenetic haploid embryonic stem cells efficiently support mouse generation by oocyte injection,” Cell Research, vol. 26, no. 1, pp. 131–134, 2016. View at Publisher · View at Google Scholar · View at Scopus
  76. A. Minkovsky, S. Patel, and K. Plath, “Concise review: pluripotency and the transcriptional inactivation of the female mammalian X chromosome,” Stem Cells, vol. 30, no. 1, pp. 48–54, 2012. View at Publisher · View at Google Scholar · View at Scopus
  77. A. Wutz, “Xist function: bridging chromatin and stem cells,” Trends in Genetics, vol. 23, no. 9, pp. 457–464, 2007. View at Publisher · View at Google Scholar · View at Scopus
  78. G. D. Penny, G. F. Kay, S. A. Sheardown, S. Rastan, and N. Brockdorff, “Requirement for Xist in X chromosome inactivation,” Nature, vol. 379, no. 6561, pp. 131–137, 1996. View at Publisher · View at Google Scholar · View at Scopus
  79. Y. Marahrens, B. Panning, J. Dausman, W. Strauss, and R. Jaenisch, “Xist-deficient mice are defective in dosage compensation but not spermatogenesis,” Genes & Development, vol. 11, no. 2, pp. 156–166, 1997. View at Publisher · View at Google Scholar
  80. F. Mohammad, T. Mondal, N. Guseva, G. K. Pandey, and C. Kanduri, “Kcnq1ot1 noncoding RNA mediates transcriptional gene silencing by interacting with Dnmt1,” Development, vol. 137, no. 15, pp. 2493–2499, 2010. View at Publisher · View at Google Scholar · View at Scopus
  81. F. Mohammad, R. R. Pandey, T. Nagano et al., “Kcnq1ot1/Lit1 noncoding RNA mediates transcriptional silencing by targeting to the perinucleolar region,” Molecular and Cellular Biology, vol. 28, no. 11, pp. 3713–3728, 2008. View at Publisher · View at Google Scholar · View at Scopus
  82. H. J. Lee, J. Kweon, E. Kim, S. Kim, and J. S. Kim, “Targeted chromosomal duplications and inversions in the human genome using zinc finger nucleases,” Genome Research, vol. 22, no. 3, pp. 539–548, 2012. View at Publisher · View at Google Scholar · View at Scopus
  83. A. Gupta, V. L. Hall, F. O. Kok et al., “Targeted chromosomal deletions and inversions in zebrafish,” Genome Research, vol. 23, no. 6, pp. 1008–1017, 2013. View at Publisher · View at Google Scholar · View at Scopus
  84. Y. Kim, J. Kweon, A. Kim et al., “A library of TAL effector nucleases spanning the human genome,” Nature Biotechnology, vol. 31, no. 3, pp. 251–258, 2013. View at Publisher · View at Google Scholar · View at Scopus
  85. P. Essletzbichler, T. Konopka, F. Santoro et al., “Megabase-scale deletion using CRISPR/Cas9 to generate a fully haploid human cell line,” Genome Research, vol. 24, no. 12, pp. 2059–2065, 2014. View at Publisher · View at Google Scholar · View at Scopus
  86. J. Han, J. Zhang, L. Chen et al., “Efficient in vivo deletion of a large imprinted lncRNA by CRISPR/Cas9,” RNA Biology, vol. 11, no. 7, pp. 829–835, 2014. View at Publisher · View at Google Scholar · View at Scopus
  87. M. Sauvageau, L. A. Goff, S. Lodato et al., “Multiple knockout mouse models reveal lincRNAs are required for life and brain development,” eLife, vol. 2, article e01749, 2013. View at Publisher · View at Google Scholar · View at Scopus
  88. K. M. V. Lai, G. Gong, A. Atanasio et al., “Diverse phenotypes and specific transcription patterns in twenty mouse lines with ablated LincRNAs,” PLoS One, vol. 10, no. 4, article e0125522, 2015. View at Publisher · View at Google Scholar · View at Scopus
  89. T. Gutschner, M. Baas, and S. Diederichs, “Noncoding RNA gene silencing through genomic integration of RNA destabilizing elements using zinc finger nucleases,” Genome Research, vol. 21, no. 11, pp. 1944–1954, 2011. View at Publisher · View at Google Scholar · View at Scopus
  90. P. Grote and B. G. Herrmann, “The long non-coding RNA Fendrr links epigenetic control mechanisms to gene regulatory networks in mammalian embryogenesis,” RNA Biology, vol. 10, no. 10, pp. 1579–1585, 2013. View at Publisher · View at Google Scholar · View at Scopus
  91. P. Grote, L. Wittler, D. Hendrix et al., “The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse,” Developmental Cell, vol. 24, no. 2, pp. 206–214, 2013. View at Publisher · View at Google Scholar · View at Scopus
  92. F. Sleutels, R. Zwart, and D. P. Barlow, “The non-coding Air RNA is required for silencing autosomal imprinted genes,” Nature, vol. 415, no. 6873, pp. 810–813, 2002. View at Publisher · View at Google Scholar
  93. F. Santoro, D. Mayer, R. M. Klement et al., “Imprinted Igf2r silencing depends on continuous Airn lncRNA expression and is not restricted to a developmental window,” Development, vol. 140, no. 6, pp. 1184–1195, 2013. View at Publisher · View at Google Scholar · View at Scopus
  94. P. A. Latos, F. M. Pauler, M. V. Koerner et al., “Airn transcriptional overlap, but not its lncRNA products, induces imprinted Igf2r silencing,” Science, vol. 338, no. 6113, pp. 1469–1472, 2012. View at Publisher · View at Google Scholar · View at Scopus
  95. E. Aparicio-Prat, C. Arnan, I. Sala, N. Bosch, R. Guigó, and R. Johnson, “DECKO: single-oligo, dual-CRISPR deletion of genomic elements including long non-coding RNAs,” BMC Genomics, vol. 16, no. 1, p. 846, 2015. View at Publisher · View at Google Scholar · View at Scopus
  96. T. Kono, Y. Obata, Q. Wu et al., “Birth of parthenogenetic mice that can develop to adulthood,” Nature, vol. 428, no. 6985, pp. 860–864, 2004. View at Publisher · View at Google Scholar · View at Scopus
  97. M. Kawahara, Q. Wu, N. Takahashi et al., “High-frequency generation of viable mice from engineered bi-maternal embryos,” Nature Biotechnology, vol. 25, no. 9, pp. 1045–1050, 2007. View at Publisher · View at Google Scholar · View at Scopus
  98. G. Friedrich and P. Soriano, “Promoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mice,” Genes & Development, vol. 5, no. 9, pp. 1513–1523, 1991. View at Publisher · View at Google Scholar
  99. B. P. Zambrowicz, A. Imamoto, S. Fiering, L. A. Herzenberg, W. G. Kerr, and P. Soriano, “Disruption of overlapping transcripts in the ROSA βgeo 26 gene trap strain leads to widespread expression of β-galactosidase in mouse embryos and hematopoietic cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 8, pp. 3789–3794, 1997. View at Publisher · View at Google Scholar · View at Scopus
  100. P. Soriano, “Generalized lacZ expression with the ROSA26 Cre reporter strain,” Nature Genetics, vol. 21, no. 1, pp. 70–1, 1999. View at Publisher · View at Google Scholar · View at Scopus
  101. M. Sadelain, E. P. Papapetrou, and F. D. Bushman, “Safe harbours for the integration of new DNA in the human genome,” Nature Reviews Cancer, vol. 12, no. 1, pp. 51–58, 2011. View at Publisher · View at Google Scholar · View at Scopus
  102. S. Irion, H. Luche, P. Gadue, H. J. Fehling, M. Kennedy, and G. Keller, “Identification and targeting of the ROSA26 locus in human embryonic stem cells,” Nature Biotechnology, vol. 25, no. 12, pp. 1477–1482, 2007. View at Publisher · View at Google Scholar · View at Scopus
  103. J. D. Brenton, R. A. Drewell, S. Viville et al., “A silencer element identified in Drosophila is required for imprinting of H19 reporter transgenes in mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 16, pp. 9242–9247, 1999. View at Publisher · View at Google Scholar · View at Scopus
  104. J. Goke, X. Lu, Y. S. Chan et al., “Dynamic transcription of distinct classes of endogenous retroviral elements marks specific populations of early human embryonic cells,” Cell Stem Cell, vol. 16, no. 2, pp. 135–141, 2015. View at Publisher · View at Google Scholar · View at Scopus
  105. J. Wang, G. Xie, M. Singh et al., “Primate-specific endogenous retrovirus-driven transcription defines naive-like stem cells,” Nature, vol. 516, no. 7531, pp. 405–409, 2014. View at Publisher · View at Google Scholar · View at Scopus
  106. S. Zhu, W. Li, J. Liu et al., “Genome-scale deletion screening of human long non-coding RNAs using a paired-guide RNA CRISPR–Cas9 library,” Nature Biotechnology, vol. 34, no. 12, pp. 1279–1286, 2016. View at Publisher · View at Google Scholar · View at Scopus
  107. L. S. Qi, M. H. Larson, L. A. Gilbert et al., “Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression,” Cell, vol. 152, no. 5, pp. 1173–1183, 2013. View at Publisher · View at Google Scholar · View at Scopus
  108. L. A. Gilbert, M. A. Horlbeck, B. Adamson et al., “Genome-scale CRISPR-mediated control of gene repression and activation,” Cell, vol. 159, no. 3, pp. 647–661, 2014. View at Publisher · View at Google Scholar · View at Scopus
  109. M. S. Werner, M. A. Sullivan, R. N. Shah et al., “Chromatin-enriched lncRNAs can act as cell-type specific activators of proximal gene transcription,” Nature Structural & Molecular Biology, vol. 24, no. 7, pp. 596–603, 2017. View at Publisher · View at Google Scholar
  110. S. J. Liu, M. A. Horlbeck, S. W. Cho et al., “CRISPRi-based genome-scale identification of functional long noncoding RNA loci in human cells,” Science, vol. 355, no. 6320, article eaah7111, 2017. View at Publisher · View at Google Scholar · View at Scopus
  111. X. Chen, M. Rinsma, J. M. Janssen, J. Liu, I. Maggio, and M. A. F. V. Gonçalves, “Probing the impact of chromatin conformation on genome editing tools,” Nucleic Acids Research, vol. 44, no. 13, pp. 6482–6492, 2016. View at Publisher · View at Google Scholar · View at Scopus
  112. J. Hu, Y. Lei, W. K. Wong et al., “Direct activation of human and mouse Oct4 genes using engineered TALE and Cas9 transcription factors,” Nucleic Acids Research, vol. 42, no. 7, pp. 4375–4390, 2014. View at Publisher · View at Google Scholar · View at Scopus
  113. H. Wu, L. Yang, and L. L. Chen, “The diversity of long noncoding RNAs and their generation,” Trends in Genetics, vol. 33, no. 8, pp. 540–552, 2017. View at Publisher · View at Google Scholar
  114. J. Joung, J. M. Engreitz, S. Konermann et al., “Genome-scale activation screen identifies a lncRNA locus regulating a gene neighbourhood,” Nature, vol. 548, no. 7667, pp. 343–346, 2017. View at Publisher · View at Google Scholar
  115. A. M. Khalil, M. Guttman, M. Huarte et al., “Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 28, pp. 11667–11672, 2009. View at Publisher · View at Google Scholar · View at Scopus
  116. M. Guttman, J. Donaghey, B. W. Carey et al., “lincRNAs act in the circuitry controlling pluripotency and differentiation,” Nature, vol. 477, no. 7364, pp. 295–300, 2011. View at Publisher · View at Google Scholar · View at Scopus
  117. J. M. Engreitz, J. E. Haines, E. M. Perez et al., “Local regulation of gene expression by lncRNA promoters, transcription and splicing,” Nature, vol. 539, no. 7629, pp. 452–455, 2016. View at Publisher · View at Google Scholar · View at Scopus
  118. D. M. Shechner, E. Hacisuleyman, S. T. Younger, and J. L. Rinn, “Multiplexable, locus-specific targeting of long RNAs with CRISPR-Display,” Nature Methods, vol. 12, no. 7, pp. 664–670, 2015. View at Publisher · View at Google Scholar · View at Scopus
  119. M. R. O'Connell, B. L. Oakes, S. H. Sternberg, A. East-Seletsky, M. Kaplan, and J. A. Doudna, “Programmable RNA recognition and cleavage by CRISPR/Cas9,” Nature, vol. 516, no. 7530, pp. 263–266, 2014. View at Publisher · View at Google Scholar · View at Scopus
  120. D. A. Nelles, M. Y. Fang, M. R. O’Connell et al., “Programmable RNA tracking in live cells with CRISPR/Cas9,” Cell, vol. 165, no. 2, pp. 488–496, 2016. View at Publisher · View at Google Scholar · View at Scopus