Comparative analysis of LIN28-RNA binding sites identified at single nucleotide resolution

References

• Ambros V, Horvitz HR. Heterochronic mutants of the nematode Caenorhabditis elegans. Science. 1984;226:409–16. doi:10.1126/science.6494891.
   PubMed Web of Science ®Google Scholar
• Ambros V. A hierarchy of regulatory genes controls a larva-to-adult developmental switch in C. elegans. Cell. 1989;57:49–57. doi:10.1016/0092-8674(89)90171-2.
   PubMed Web of Science ®Google Scholar
• Liu ZC, Ambros V. Heterochronic genes control the stage-specific initiation and expression of the dauer larva developmental program in Caenorhabditis elegans. Genes & development. 1989;3:2039–49. doi:10.1101/gad.3.12b.2039
   PubMed Web of Science ®Google Scholar
• Xu B, Zhang K, Huang Y. Lin28 modulates cell growth and associates with a subset of cell cycle regulator mRNAs in mouse embryonic stem cells. Rna. 2009;15:357–61. doi:10.1261/rna.1368009.
   PubMed Web of Science ®Google Scholar
• Viswanathan SR, Daley GQ, Gregory RI. Selective blockade of microRNA processing by Lin28. Science. 2008;320:97–100. doi:10.1126/science.1154040.
   PubMed Web of Science ®Google Scholar
• Qiu C, Ma Y, Wang J, Peng S, Huang Y. Lin28-mediated post-transcriptional regulation of Oct4 expression in human embryonic stem cells. Nucleic acids research. 2010;38:1240–8. doi:10.1093/nar/gkp1071.
   PubMed Web of Science ®Google Scholar
• Polesskaya A, Cuvellier S, Naguibneva I, Duquet A, Moss EG, Harel-Bellan A. Lin-28 binds IGF-2 mRNA and participates in skeletal myogenesis by increasing translation efficiency. Genes & development. 2007;21:1125–38. doi:10.1101/gad.415007
   PubMed Web of Science ®Google Scholar
• Zhu H, Shyh-Chang N, Segre AV, Shinoda G, Shah SP, Einhorn WS, Takeuchi A, Engreitz JM, Hagan JP, Kharas MG, et al. The Lin28/let-7 axis regulates glucose metabolism. Cell. 2011;147:81–94. doi:10.1016/j.cell.2011.08.033.
   PubMed Web of Science ®Google Scholar
• Shyh-Chang N, Zhu H, Yvanka de Soysa T, Shinoda G, Seligson MT, Tsanov KM, Nguyen L, Asara JM, Cantley LC, Daley GQ. Lin28 enhances tissue repair by reprogramming cellular metabolism. Cell. 2013;155:778–92. doi:10.1016/j.cell.2013.09.059.
   PubMed Web of Science ®Google Scholar
• Viswanathan SR, Powers JT, Einhorn W, Hoshida Y, Ng TL, Toffanin S, O'Sullivan M, Lu J, Phillips LA, Lockhart VL, et al. Lin28 promotes transformation and is associated with advanced human malignancies. Nature genetics. 2009;41:843–8. doi:10.1038/ng.392.
   PubMed Web of Science ®Google Scholar
• King CE, Cuatrecasas M, Castells A, Sepulveda AR, Lee JS, Rustgi AK. LIN28B promotes colon cancer progression and metastasis. Cancer research. 2011;71:4260–8. doi:10.1158/0008-5472.CAN-10-4637.
   PubMed Web of Science ®Google Scholar
• Tu HC, Schwitalla S, Qian Z, LaPier GS, Yermalovich A, Ku YC, Chen SC, Viswanathan SR, Zhu H, Nishihara R, et al. LIN28 cooperates with WNT signaling to drive invasive intestinal and colorectal adenocarcinoma in mice and humans. Genes & development. 2015;29:1074–86. doi:10.1101/gad.256693.114
   PubMed Web of Science ®Google Scholar
• Madison BB, Liu Q, Zhong X, Hahn CM, Lin N, Emmett MJ, Stanger BZ, Lee JS, Rustgi AK. LIN28B promotes growth and tumorigenesis of the intestinal epithelium via Let-7. Genes & development. 2013;27:2233–45. doi:10.1101/gad.224659.113
   PubMed Web of Science ®Google Scholar
• Newman MA, Hammond SM. Emerging paradigms of regulated microRNA processing. Genes & development. 2010;24:1086–92. doi:10.1101/gad.1919710
   PubMed Web of Science ®Google Scholar
• Rybak A, Fuchs H, Smirnova L, Brandt C, Pohl EE, Nitsch R, Wulczyn FG. A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nature cell biology. 2008;10:987–93. doi:10.1038/ncb1759.
   PubMed Web of Science ®Google Scholar
• Heo I, Joo C, Kim YK, Ha M, Yoon MJ, Cho J, Yeom KH, Han J, Kim VN. TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell. 2009;138:696–708. doi:10.1016/j.cell.2009.08.002.
   PubMed Web of Science ®Google Scholar
• Lehrbach NJ, Armisen J, Lightfoot HL, Murfitt KJ, Bugaut A, Balasubramanian S, Miska EA. LIN-28 and the poly(U) polymerase PUP-2 regulate let-7 microRNA processing in Caenorhabditis elegans. Nature structural & molecular biology. 2009;16:1016–20. doi:10.1038/nsmb.1675
   PubMed Web of Science ®Google Scholar
• Nam Y, Chen C, Gregory RI, Chou JJ, Sliz P. Molecular basis for interaction of let-7 microRNAs with Lin28. Cell. 2011;147:1080–91. doi:10.1016/j.cell.2011.10.020.
   PubMed Web of Science ®Google Scholar
• Mayr F, Schutz A, Doge N, Heinemann U. The Lin28 cold-shock domain remodels pre-let-7 microRNA. Nucleic acids research. 2012;40:7492–506. doi:10.1093/nar/gks355.
   PubMed Web of Science ®Google Scholar
• Heo I, Joo C, Cho J, Ha M, Han J, Kim VN. Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA. Molecular cell. 2008;32:276–84. doi:10.1016/j.molcel.2008.09.014.
   PubMed Web of Science ®Google Scholar
• Heo I, Ha M, Lim J, Yoon MJ, Park JE, Kwon SC, Chang H, Kim VN. Mono-uridylation of pre-microRNA as a key step in the biogenesis of group II let-7 microRNAs. Cell. 2012;151:521–32. doi:10.1016/j.cell.2012.09.022.
   PubMed Web of Science ®Google Scholar
• Chang HM, Triboulet R, Thornton JE, Gregory RI. A role for the Perlman syndrome exonuclease Dis3l2 in the Lin28-let-7 pathway. Nature. 2013;497:244–8. doi:10.1038/nature12119.
   PubMed Web of Science ®Google Scholar
• Wilbert ML, Huelga SC, Kapeli K, Stark TJ, Liang TY, Chen SX, Yan BY, Nathanson JL, Hutt KR, Lovci MT, et al. LIN28 binds messenger RNAs at GGAGA motifs and regulates splicing factor abundance. Molecular cell. 2012;48:195–206. doi:10.1016/j.molcel.2012.08.004.
   PubMed Web of Science ®Google Scholar
• Cho J, Chang H, Kwon SC, Kim B, Kim Y, Choe J, Ha M, Kim YK, Kim VN. LIN28A is a suppressor of ER-associated translation in embryonic stem cells. Cell. 2012;151:765–77. doi:10.1016/j.cell.2012.10.019.
   PubMed Web of Science ®Google Scholar
• Hafner M, Max KE, Bandaru P, Morozov P, Gerstberger S, Brown M, Molina H, Tuschl T. Identification of mRNAs bound and regulated by human LIN28 proteins and molecular requirements for RNA recognition. Rna. 2013;19:613–26. doi:10.1261/rna.036491.112.
   PubMed Web of Science ®Google Scholar
• Graf R, Munschauer M, Mastrobuoni G, Mayr F, Heinemann U, Kempa S, Rajewsky N, Landthaler M. Identification of LIN28B-bound mRNAs reveals features of target recognition and regulation. RNA biology. 2013;10:1146–59. doi:10.4161/rna.25194.
   PubMed Web of Science ®Google Scholar
• Stefani G, Chen X, Zhao H, Slack FJ. A novel mechanism of LIN-28 regulation of let-7 microRNA expression revealed by in vivo HITS-CLIP in C. elegans. Rna. 2015;21:985–96
   PubMed Web of Science ®Google Scholar
• Mili S, Steitz JA. Evidence for reassociation of RNA-binding proteins after cell lysis: implications for the interpretation of immunoprecipitation analyses. Rna. 2004;10:1692–4. doi:10.1261/rna.7151404.
   PubMed Web of Science ®Google Scholar
• Ule J, Jensen K, Mele A, Darnell RB. CLIP: a method for identifying protein-RNA interaction sites in living cells. Methods. 2005;37:376–86. doi:10.1016/j.ymeth.2005.07.018.
   PubMed Web of Science ®Google Scholar
• Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M Jr, Jungkamp AC, Munschauer M, et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell. 2010;141:129–41. doi:10.1016/j.cell.2010.03.009.
   PubMed Web of Science ®Google Scholar
• Kishore S, Jaskiewicz L, Burger L, Hausser J, Khorshid M, Zavolan M. A quantitative analysis of CLIP methods for identifying binding sites of RNA-binding proteins. Nature methods. 2011;8:559–64. doi:10.1038/nmeth.1608.
   PubMed Web of Science ®Google Scholar
• Sauliere J, Murigneux V, Wang Z, Marquenet E, Barbosa I, Le Tonqueze O, Audic Y, Paillard L, Roest Crollius H, Le Hir H. CLIP-seq of eIF4AIII reveals transcriptome-wide mapping of the human exon junction complex. Nature structural & molecular biology. 2012;19:1124–31. doi:10.1038/nsmb.2420
   PubMed Web of Science ®Google Scholar
• Moy RH, Cole BS, Yasunaga A, Gold B, Shankarling G, Varble A, Molleston JM, tenOever BR, Lynch KW, Cherry S. Stem-loop recognition by DDX17 facilitates miRNA processing and antiviral defense. Cell. 2014;158:764–77. doi:10.1016/j.cell.2014.06.023.
   PubMed Web of Science ®Google Scholar
• Granneman S, Kudla G, Petfalski E, Tollervey D. Identification of protein binding sites on U3 snoRNA and pre-rRNA by UV cross-linking and high-throughput analysis of cDNAs. Proceedings of the National Academy of Sciences of the United States of America. 2009;106:9613–8. doi:10.1073/pnas.0901997106.
   PubMed Web of Science ®Google Scholar
• Li YI, Sanchez-Pulido L, Haerty W, Ponting CP. RBFOX and PTBP1 proteins regulate the alternative splicing of micro-exons in human brain transcripts. Genome research. 2015;25:1–13. doi:10.1101/gr.181990.114.
   PubMed Web of Science ®Google Scholar
• Zhang C, Darnell RB. Mapping in vivo protein-RNA interactions at single-nucleotide resolution from HITS-CLIP data. Nature biotechnology. 2011;29:607–14. doi:10.1038/nbt.1873.
   PubMed Web of Science ®Google Scholar
• Moore MJ, Zhang C, Gantman EC, Mele A, Darnell JC, Darnell RB. Mapping Argonaute and conventional RNA-binding protein interactions with RNA at single-nucleotide resolution using HITS-CLIP and CIMS analysis. Nature protocols. 2014;9:263–93. doi:10.1038/nprot.2014.012.
   PubMed Web of Science ®Google Scholar
• Lelyveld VS, Bjorkbom A, Ransey EM, Sliz P, Szostak JW. Pinpointing RNA-Protein Cross-Links with Site-Specific Stable Isotope-Labeled Oligonucleotides. Journal of the American Chemical Society. 2015. doi:10.1021/jacs.5b10596
   Web of Science ®Google Scholar
• Wang L, Nam Y, Lee AK, Yu C, Roth K, Chen C, Ransey EM, Sliz P. LIN28 Zinc Knuckle Domain Is Required and Sufficient to Induce let-7 Oligouridylation. Cell Reports. 2017;18:2664–75. doi.org/10.1016/j.celrep.2017.02.044.
   Google Scholar
• Piskounova E, Viswanathan SR, Janas M, LaPierre RJ, Daley GQ, Sliz P, Gregory RI. Determinants of microRNA processing inhibition by the developmentally regulated RNA-binding protein Lin28. The Journal of biological chemistry. 2008;283:21310–4. doi:10.1074/jbc.C800108200.
   PubMed Web of Science ®Google Scholar
• Kramer K, Sachsenberg T, Beckmann BM, Qamar S, Boon KL, Hentze MW, Kohlbacher O, Urlaub H. Photo-cross-linking and high-resolution mass spectrometry for assignment of RNA-binding sites in RNA-binding proteins. Nature methods. 2014;11:1064–70. doi:10.1038/nmeth.3092.
   Google Scholar
• Apffel A, Chakel JA, Fischer S, Lichtenwalter K, Hancock WS. Analysis of Oligonucleotides by HPLC-Electrospray Ionization Mass Spectrometry. Analytical chemistry. 1997;69:1320–5. doi:10.1021/ac960916h.
   PubMed Web of Science ®Google Scholar