Identification of LIN28B-bound mRNAs reveals features of target recognition and regulation

RNA Biology

Volumn 10, Issue 7, 2013, Pages 1146-1159

  Graf, Robin ^a   Munschauer, Mathias ^a   Mastrobuoni, Guido ^a   Mayr, Florian ^a   Heinemann, Udo ^a   Kempa, Stefan ^a   Rajewsky, Nikolaus ^a   Landthaler, Markus ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Clip; Post transcriptional regulation; RNA binding protein; Stem cell

Indexed keywords

LIN28B PROTEIN; MESSENGER RNA; MICRORNA; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL CYCLE; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEOMICS; QUANTITATIVE ANALYSIS;

CLIP; POST-TRANSCRIPTIONAL REGULATION; RNA-BINDING PROTEIN; STEM CELL;

BASE SEQUENCE; BINDING SITES; CELL CYCLE; CELL CYCLE PROTEINS; CELL LINE; CONSENSUS SEQUENCE; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HUMANS; MICRORNAS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; NUCLEOTIDE MOTIFS; POSITION-SPECIFIC SCORING MATRICES; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; REPRODUCIBILITY OF RESULTS; RNA PRECURSORS; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84880915075     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.25194     Document Type: Article

References (70)

1. Dreyfuss G, Kim VN, Kataoka N. Messenger-RNAbinding proteins and the messages they carry. Nat Rev Mol Cell Biol 2002; 3:195-205; PMID:11994740; http://dx.doi.org/10.1038/nrm760.
2. Keene JD. RNA regulons: coordination of post-transcriptional events. Nat Rev Genet 2007; 8:533-43; PMID:17572691; http://dx.doi.org/10.1038/nrg2111.
3. Martin KC, Ephrussi A. mRNA localization: gene expression in the spatial dimension. Cell 2009; 136:719-30; PMID:19239891; http://dx.doi.org/10.1016/j. cell.2009.01.044.
4. Sonenberg N, Hinnebusch AG. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 2009; 136:731-45; PMID:19239892; http://dx.doi.org/10.1016/j.cell.2009.01.042.
5. Moore MJ, Proudfoot NJ. Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 2009; 136:688-700; PMID:19239889; http://dx.doi.org/10.1016/j.cell.2009.02.001.
6. Lukong KE, Chang KW, Khandjian EW, Richard S. RNA-binding proteins in human genetic disease. Trends Genet 2008; 24:416-25; PMID:18597886; http://dx.doi.org/10.1016/j.tig.2008.05.004.
7. Baltz AG, Munschauer M, Schwanhäusser B, Vasile A, Murakawa Y, Schueler M, et al. The mRNAbound proteome and its global occupancy profile on protein-coding transcripts. Mol Cell 2012; 46:674-90; PMID:22681889; http://dx.doi.org/10.1016/j.molcel.2012.05.021.
8. Castello A, Fischer B, Eichelbaum K, Horos R, Beckmann BM, Strein C, et al. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 2012; 149:1393-406; PMID:22658674; http://dx.doi.org/10.1016/j.cell.2012. 04.031.
9. Ambros V, Horvitz HR. Heterochronic mutants of the nematode Caenorhabditis elegans. Science 1984; 226:409-16; PMID:6494891; http://dx.doi.org/10.1126/science.6494891.
10. Guo Y, Chen Y, Ito H, Watanabe A, Ge X, Kodama T, et al. Identification and characterization of lin-28 homolog B (LIN28B) in human hepatocellular carcinoma. Gene 2006; 384:51-61; PMID:16971064; http://dx.doi.org/10.1016/j. gene.2006.07.011.
11. Zhou J, Ng SB, Chng WJ. LIN28/LIN28B: An emerging oncogenic driver in cancer stem cells. Int J Biochem Cell Biol 2013; 45:973-8; PMID:23420006; http://dx.doi.org/10.1016/j.biocel.2013.02.006.
12. Piskounova E, Polytarchou C, Thornton JE, LaPierre RJ, Pothoulakis C, Hagan JP, et al. Lin28A and Lin28B inhibit let-7 microRNA biogenesis by distinct mechanisms. Cell 2011; 147:1066-79; PMID:22118463; http://dx.doi.org/10.1016/j. cell.2011.10.039.
13. Rybak A, Fuchs H, Smirnova L, Brandt C, Pohl EE, Nitsch R, et al. A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat Cell Biol 2008; 10:987-93; PMID:18604195http:// dx.doi.org/10.1038/ncb1759.
14. Yang DH, Moss EG. Temporally regulated expression of Lin-28 in diverse tissues of the developing mouse. Gene Expr Patterns 2003; 3:719-26; PMID:14643679; http://dx.doi.org/10.1016/S1567-133X(03)00140-6.
15. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318:1917-20; PMID:18029452; http://dx.doi.org/10.1126/science. 1151526.
16. Zhu H, Shah S, Shyh-Chang N, Shinoda G, Einhorn WS, Viswanathan SR, et al. Lin28a transgenic mice manifest size and puberty phenotypes identified in human genetic association studies. Nat Genet 2010; 42:626-30; PMID:20512147; http://dx.doi.org/10.1038/ng.593.
17. Thornton JE, Gregory RI. How does Lin28 let-7 control development and disease? Trends Cell Biol 2012; 22:474-82; PMID:22784697; http://dx.doi.org/10. 1016/j.tcb.2012.06.001.
18. Viswanathan SR, Powers JT, Einhorn W, Hoshida Y, Ng TL, Toffanin S, et al. Lin28 promotes transformation and is associated with advanced human malignancies. Nat Genet 2009; 41:843-8; PMID:19483683; http://dx.doi.org/10. 1038/ng.392.
19. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000; 403:901-6; PMID:10706289; http://dx.doi.org/10.1038/35002607.
20. Martinez NJ, Gregory RI. MicroRNA gene regulatory pathways in the establishment and maintenance of ESC identity. Cell Stem Cell 2010; 7:31-5; PMID:20621047; http://dx.doi.org/10.1016/j.stem.2010.06.011.
21. Lehrbach NJ, Armisen J, Lightfoot HL, Murfitt KJ, Bugaut A, Balasubramanian S, et al. LIN-28 and the poly(U) polymerase PUP-2 regulate let-7 microRNA processing in Caenorhabditis elegans. Nat Struct Mol Biol 2009; 16:1016-20; PMID:19713957; http://dx.doi.org/10.1038/nsmb.1675.
22. Hagan JP, Piskounova E, Gregory RI. Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nat Struct Mol Biol 2009; 16:1021-5; PMID:19713958; http://dx.doi.org/10.1038/nsmb.1676.
23. Heo I, Joo C, Kim YK, Ha M, Yoon MJ, Cho J, et al. TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 2009; 138:696-708; PMID:19703396; http://dx.doi.org/10.1016/j.cell.2009.08.002.
24. Mayr F, Schütz A, Döge N, Heinemann U. The Lin28 cold-shock domain remodels pre-let-7 microRNA. Nucleic Acids Res 2012; 40:7492-506; PMID:22570413; http://dx.doi.org/10.1093/nar/gks355.
25. 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; PMID:22078496; http://dx.doi.org/10.1016/j.cell.2011.10.020.
26. Loughlin FE, Gebert LF, Towbin H, Brunschweiger A, Hall J, Allain FH. Structural basis of pre-let-7 miRNA recognition by the zinc knuckles of pluripotency factor Lin28. Nat Struct Mol Biol 2012; 19:84-9; PMID:22157959; http://dx.doi.org/10.1038/nsmb.2202.
27. Desjardins A, Yang A, Bouvette J, Omichinski JG, Legault P. Importance of the NCp7-like domain in the recognition of pre-let-7g by the pluripotency factor Lin28. Nucleic Acids Res 2012; 40:1767-77; PMID:22013165; http://dx.doi.org/10.1093/nar/gkr808.
28. Mihailovich M, Militti C, Gabaldón T, Gebauer F. Eukaryotic cold shock domain proteins: highly versatile regulators of gene expression. Bioessays 2010; 32:109-18; PMID:20091748; http://dx.doi.org/10.1002/bies.200900122.
29. Max KE, Zeeb M, Bienert R, Balbach J, Heinemann U. T-rich DNA single strands bind to a preformed site on the bacterial cold shock protein Bs-CspB. J Mol Biol 2006; 360:702-14; PMID:16780871; http://dx.doi.org/10.1016/j.jmb.2006. 05.044.
30. Zeeb M, Balbach J. Single-stranded DNA binding of the cold-shock protein CspB from Bacillus subtilis: NMR mapping and mutational characterization. Protein Sci 2003; 12:112-23; PMID:12493834; http://dx.doi.org/10.1110/ps. 0219703.
31. Balzer E, Moss EG. Localization of the developmental timing regulator Lin28 to mRNP complexes, P-bodies and stress granules. RNA Biol 2007; 4:16-25; PMID:17617744; http://dx.doi.org/10.4161/rna.4.1.4364.
32. 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 Dev 2007; 21:1125-38; PMID:17473174; http://dx.doi.org/10.1101/gad.415007.
33. Peng S, Chen LL, Lei XX, Yang L, Lin H, Carmichael GG, et al. Genome-wide studies reveal that Lin28 enhances the translation of genes important for growth and survival of human embryonic stem cells. Stem Cells 2011; 29:496-504; PMID:21425412; http://dx.doi.org/10.1002/stem.591.
34. 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; PMID:19147696; http://dx.doi.org/10.1261/rna.1368009.
35. Wang YC, Chen YL, Yuan RH, Pan HW, Yang WC, Hsu HC, et al. Lin-28B expression promotes transformation and invasion in human hepatocellular carcinoma. Carcinogenesis 2010; 31:1516-22; PMID:20525879; http://dx.doi.org/10. 1093/carcin/bgq107.
36. Xu B, Huang Y. Histone H2a mRNA interacts with Lin28 and contains a Lin28-dependent posttranscriptional regulatory element. Nucleic Acids Res 2009; 37:4256-63; PMID:19443445; http://dx.doi.org/10.1093/nar/gkp372.
37. 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 Res 2010; 38:1240-8; PMID:19966271; http://dx.doi.org/10.1093/nar/gkp1071.
38. Cho J, Chang H, Kwon SC, Kim B, Kim Y, Choe J, et al. LIN28A is a suppressor of ER-Associated translation in embryonic stem cells. Cell 2012; 151:765-77; PMID:23102813; http://dx.doi.org/10.1016/j.cell.2012.10.019.
39. Wilbert ML, Huelga SC, Kapeli K, Stark TJ, Liang TY, Chen SX, et al. LIN28 binds messenger RNAs at GGAGA motifs and regulates splicing factor abundance. Mol Cell 2012; 48:195-206; PMID:22959275; http://dx.doi.org/10.1016/ j.molcel.2012.08.004.
40. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 2010; 141:129-41; PMID:20371350; http://dx.doi.org/10. 1016/j.cell.2010.03.009.
41. Hafner M, Max KE, Bandaru P, Morozov P, Gerstberger S, Brown M, et al. Identification of mRNAs bound and regulated by human LIN28 proteins and molecular requirements for RNA recognition. RNA 2013; 19:613-26; PMID:23481595; http://dx.doi.org/10.1261/rna.036491.112.
42. Lebedeva S, Jens M, Theil K, Schwanhäusser B, Selbach M, Landthaler M, et al. Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein HuR. Mol Cell 2011; 43:340-52; PMID:21723171; http://dx.doi.org/10.1016/j.molcel.2011.06.008.
43. Selbach M, Schwanhäusser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature 2008; 455:58-63; PMID:18668040; http://dx.doi.org/10.1038/nature07228.
44. Schwanhäusser B, Gossen M, Dittmar G, Selbach M. Global analysis of cellular protein translation by pulsed SILAC. Proteomics 2009; 9:205-9; PMID:19053139; http://dx.doi.org/10.1002/pmic.200800275.
45. 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. Nat Methods 2011; 8:559-64; PMID:21572407; http://dx.doi.org/10.1038/nmeth.1608.
46. Zhang C, Darnell RB. Mapping in vivo protein-RNA interactions at single-nucleotide resolution from HITS-CLIP data. Nat Biotechnol 2011; 29:607-14; PMID:21633356; http://dx.doi.org/10.1038/nbt.1873.
47. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, et al. MEME SUITE: Tools for motif discovery and searching. Nucleic Acids Res 2009; 37(Web Server issue):W202-8; PMID:19458158; http://dx.doi.org/10.1093/nar/gkp335.
48. Lei XX, Xu J, Ma W, Qiao C, Newman MA, Hammond SM, et al. Determinants of mRNA recognition and translation regulation by Lin28. Nucleic Acids Res 2012; 40:3574-84; PMID:22210884; http://dx.doi.org/10.1093/nar/gkr1279.
49. Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, et al. Combinatorial microRNA target predictions. Nat Genet 2005; 37:495-500;PMID: 15806104; http://dx.doi.org/10.1038/ng1536.
50. Anders G, Mackowiak SD, Jens M, Maaskola J, Kuntzagk A, Rajewsky N, et al. doRiNA: A database of RNA interactions in post-transcriptional regulation. Nucleic Acids Res 2012; 40(Database issue):D180-6; PMID:22086949; http://dx.doi.org/10.1093/nar/gkr1007.
51. Mukherjee N, Lager PJ, Friedersdorf MB, Thompson MA, Keene JD. Coordinated posttranscriptional mRNA population dynamics during T-cell activation. Mol Syst Biol 2009; 5:288; PMID:19638969; http://dx.doi.org/10.1038/ msb.2009.44.
52. Pullmann R Jr., Kim HH, Abdelmohsen K, Lal A, Martindale JL, Yang X, et al. Analysis of turnover and translation regulatory RNA-binding protein expression through binding to cognate mRNAs. Mol Cell Biol 2007; 27:6265-78; PMID:17620417; http://dx.doi.org/10.1128/MCB.00500-07.
53. Saltzman AL, Kim YK, Pan Q, Fagnani MM, Maquat LE, Blencowe BJ. Regulation of multiple core spliceosomal proteins by alternative splicing-coupled nonsense-mediated mRNA decay. Mol Cell Biol 2008; 28:4320-30; PMID:18443041; http://dx.doi.org/10.1128/MCB.00361-08.
54. Rossbach O, Hung LH, Schreiner S, Grishina I, Heiner M, Hui J, et al. Auto-And cross-regulation of the hnRNP L proteins by alternative splicing. Mol Cell Biol 2009; 29:1442-51; PMID:19124611http://dx.doi.org/10.1128/MCB.01689-08.
55. Ni JZ, Grate L, Donohue JP, Preston C, Nobida N, O'Brien G, et al. Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay. Genes Dev 2007; 21:708-18; PMID:17369403; http://dx.doi.org/10.1101/gad.1525507.
56. Sureau A, Gattoni R, Dooghe Y, Stévenin J, Soret J. SC35 autoregulates its expression by promoting splicing events that destabilize its mRNAs. EMBO J 2001; 20:1785-96; PMID:11285241; http://dx.doi.org/10.1093/emboj/ 20.7.1785.
57. Wollerton MC, Gooding C, Robinson F, Brown EC, Jackson RJ, Smith CW. Differential alternative splicing activity of isoforms of polypyrimidine tract binding protein (PTB). RNA 2001; 7:819-32; PMID:11421360; http://dx.doi.org/10. 1017/S1355838201010214.
58. Lareau LF, Inada M, Green RE, Wengrod JC, Brenner SE. Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements. Nature 2007; 446:926-9; PMID:17361132; http://dx.doi.org/10.1038/ nature05676.
59. Ayala YM, De Conti L, Avendaño-Vázquez SE, Dhir A, Romano M, D'Ambrogio A, et al. TDP-43 regulates its mRNA levels through a negative feedback loop. EMBO J 2011; 30:277-88; PMID:21131904; http://dx.doi.org/10.1038/ emboj.2010.310.
60. Avendaño-Vázquez SE, Dhir A, Bembich S, Buratti E, Proudfoot N, Baralle FE. Autoregulation of TDP-43 mRNA levels involves interplay between transcription, splicing, and alternative polyA site selection. Genes Dev 2012; 26:1679-84; PMID:22855830; http://dx.doi.org/10.1101/gad.194829.112.
61. Sun S, Zhang Z, Sinha R, Karni R, Krainer AR. SF2/ASF autoregulation involves multiple layers of posttranscriptional and translational control. Nat Struct Mol Biol 2010; 17:306-12; PMID:20139984; http://dx.doi.org/10.1038/nsmb. 1750.
62. Ali PS, Ghoshdastider U, Hoffmann J, Brutschy B, Filipek S. Recognition of the let-7g miRNA precursor by human Lin28B. FEBS Lett 2012; 586:3986-90; PMID:23063642; http://dx.doi.org/10.1016/j.febslet.2012.09.034.
63. Jin J, Jing W, Lei XX, Feng C, Peng S, Boris-Lawrie K, et al. Evidence that Lin28 stimulates translation by recruiting RNA helicase A to polysomes. Nucleic Acids Res 2011; 39:3724-34; PMID:21247876; http://dx.doi.org/10.1093/ nar/gkq1350.
64. Subramaniam S, Unsicker K. ERK and cell death: ERK1/2 in neuronal death. FEBS J 2010; 277:22-9; PMID:19843173; http://dx.doi.org/10.1111/j.1742-4658. 2009.07367.x.
65. Zhu H, Shyh-Chang N, Segrè AV, Shinoda G, Shah SP, Einhorn WS, et al.; DIAGRAM Consortium; MAGIC Investigators. The Lin28/let-7 axis regulates glucose metabolism. Cell 2011; 147:81-94; PMID:21962509; http://dx.doi.org/10. 1016/j.cell.2011.08.033.
66. Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 2002; 1:376-86; PMID:12118079; http://dx.doi.org/10.1074/mcp.M200025-MCP200.
67. Rappsilber J, Ishihama Y, Mann M. Stop and go extraction tips for matrix-Assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal Chem 2003; 75:663-70; PMID:12585499; http://dx.doi.org/10.1021/ac026117i.
68. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754-60; PMID:19451168; http://dx.doi.org/10.1093/bioinformatics/btp324.
69. Bailey TL, Elkan C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 1994; 2:28-36; PMID:7584402.
70. Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 2008; 26:1367-72; PMID:19029910; http://dx.doi.org/10.1038/nbt.1511.