The Lin28 cold-shock domain remodels pre-let-7 microRNA

Nucleic Acids Research

Volumn 40, Issue 15, 2012, Pages 7492-7506

  Mayr, Florian ^a,b   Schütz, Anja ^a   Döge, Nadine ^a   Heinemann, Udo ^a,b  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DICER; LET 7 MICRORNA PRECURSOR; MICRORNA; NUCLEIC ACID; PROTEIN LIN28; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; COLD SHOCK DOMAIN; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; GEL MOBILITY SHIFT ASSAY; ISOTHERMAL TITRATION CALORIMETRY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RNA BINDING DOMAIN; XENOPUS TROPICALIS; ZINC KNUCKLE DOMAIN;

ANIMALS; BINDING SITES; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; HUMANS; MICRORNAS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; NUCLEOTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA; RNA PRECURSORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA-BINDING PROTEINS; XENOPUS;

EID: 84867304012     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks355     Document Type: Article

References (70)

1. Landthaler, M., Yalcin, A. and Tuschl, T. (2004) The human DiGeorge syndrome critical region gene 8 and its D. melanogaster homolog are required for miRNA biogenesis. Curr. Biol., 14, 2162.2167.
2. Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Rådmark, O., Kim, S. et al. (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature, 425, 415.419.
3. Bohnsack, M. T., Czaplinski, K. and Gorlich, D. (2004) Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA, 10, 185.191.
4. Yi, R., Qin, Y., Macara, I. G. and Cullen, B. R. (2003) Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev., 17, 3011.3016.
5. Hutvágner, G., McLachlan, J., Pasquinelli, A. E., Bálint, E., Tuschl, T. and Zamore, P. D. (2001) A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science, 293, 834.838.
6. Ketting, R. F., Fischer, S. E., Bernstein, E., Sijen, T., Hannon, G. J. and Plasterk, R. H. (2001) Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev., 15, 2654.2659.
7. Knight, S. W. and Bass, B. L. (2001) A role for the RNase III enzyme DCR-1 in RNA interference and germ line development in Caenorhabditis elegans. Science, 293, 2269.2271.
8. Grosshans, H., Johnson, T., Reinert, K. L., Gerstein, M. and Slack, F. J. (2005) The temporal patterning microRNA let-7 regulates several transcription factors at the larval to adult transition in C. elegans. Dev. Cell, 8, 321.330.
9. Pasquinelli, A. E., Reinhart, B. J., Slack, F., Martindale, M. Q., Kuroda, M. I., Maller, B., Hayward, D. C., Ball, E. E., Degnan, B., Müller, P. et al. (2000) Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature, 408, 86.89.
10. Reinhart, B. J., Slack, F. J., Basson, M., Pasquinelli, A. E., Bettinger, J. C., Rougvie, A. E., Horvitz, H. R. and Ruvkun, G. (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature, 403, 901.906.
11. Büssing, I., Slack, F. J. and Grosshans, H. (2008) let-7 microRNAs in development, stem cells and cancer. Trends Mol. Med., 14, 400.409.
12. Johnson, S., Grosshans, H., Shingara, J., Byrom, M., Jarvis, R., Cheng, A., Labourier, E., Reinert, K., Brown, D. and Slack, F. (2005) RAS is regulated by the let-7 microRNA family. Cell, 120, 635.647.
13. Mayr, C., Hemann, M. T. and Bartel, D. P. (2007) Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science, 315, 1576.1579.
14. Wulczyn, F., Smirnova, L., Rybak, A., Brandt, C., Kwidzinski, E., Ninnemann, O., Strehle, M., Seiler, A., Schumacher, S. and Nitsch, R. (2007) Post-transcriptional regulation of the let-7 microRNA during neural cell specification. FASEB J., 21, 415.426.
15. Heo, I., Joo, C., Cho, J., Ha, M., Han, J. and Kim, V. N. (2008) Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA. Mol. Cell, 32, 276.284.
16. Newman, M. A., Thomson, J. M. and Hammond, S. M. (2008) Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing. RNA, 14, 1539.1549.
17. Rybak, A., Fuchs, H., Smirnova, L., Brandt, C., Pohl, E., Nitsch, R. and Wulczyn, F. (2008) A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat. Cell Biol., 10, 987.993.
18. Viswanathan, S. R., Daley, G. Q. and Gregory, R. I. (2008) Selective blockade of microRNA processing by Lin28. Science, 320, 97.100.
19. Ambros, V. and Horvitz, H. (1984) Heterochronic mutants of the nematode Caenorhabditis elegans. Science, 226, 409.416.
20. Moss, E. G., Lee, R. C. and Ambros, V. (1997) The cold shock domain protein LIN-28 controls developmental timing in C. elegans and is regulated by the lin-4 RNA. Cell, 88, 637.646.
21. Seggerson, K., Tang, L. and Moss, E. G. (2002) Two genetic circuits repress the Caenorhabditis elegans heterochronic gene lin-28 after translation initiation. Dev. Biol., 243, 215.225.
22. Reinhart, B., Slack, F., Basson, M., Pasquinelli, A., Bettinger, J., Rougvie, A., Horvitz, H. and Ruvkun, G. (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature, 403, 901.906.
23. Richards, M., Tan, S.-P., Tan, J.-H., Chan, W.-K. and Bongso, A. (2004) The transcriptome profile of human embryonic stem cells as defined by SAGE. Stem Cells, 22, 51.64.
24. Yang, D. H. and Moss, E. G. (2003) Temporally regulated expression of Lin-28 in diverse tissues of the developing mouse. Gene Expr. Patterns, 3, 719.726.
25. Yang, X., Lin, X., Zhong, X., Kaur, S., Li, N., Liang, S., Lassus, H., Wang, L., Katsaros, D., Montone, K. et al. (2010) Double-negative feedback loop between reprogramming factor LIN28 and microRNA let-7 regulates aldehyde dehydrogenase 1-positive cancer stem cells. Cancer Res., 70, 9463.9472.
26. Yu, J., Vodyanik, M., Smuga-Otto, K., Antosiewicz-Bourget, J., Frane, J., Tian, S., Nie, J., Jonsdottir, G., Ruotti, V., Stewart, R. et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science, 318, 1917.1920.
27. Viswanathan, S., Powers, J., Einhorn, W., Hoshida, Y., Ng, T., Toffanin, S., O'Sullivan, M., Lu, J., Phillips, L., Lockhart, V. et al. (2009) Lin28 promotes transformation and is associated with advanced human malignancies. Nat. Genet., 41, 843.848.
28. Piskounova, E., Viswanathan, S. R., Janas, M., La Pierre, R. J., Daley, G. Q., Sliz, P. and Gregory, R. I. (2008) Determinants of microRNA processing inhibition by the developmentally regulated RNA-binding protein Lin28. J. Biol. Chem., 283, 21310.21314.
29. Hagan, J., Piskounova, E. and Gregory, R. (2009) Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nat. Struct. Mol. Biol., 16, 1021.1025.
30. Lehrbach, N. J., Armisen, J., Lightfoot, H. L., Murfitt, K. J., Bugaut, A., Balasubramanian, S. and Miska, E. A. (2009) LIN-28 and the poly (U) polymerase PUP-2 regulate let-7 microRNA processing in Caenorhabditis elegans. Nat. Struct. Mol. Biol., 16, 1016.1020.
31. Heo, I., Joo, C., Kim, Y.-K., Ha, M., Yoon, M.-J., Cho, J., Yeom, K.-H., Han, J. and Kim, V. N. (2009) TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell, 138, 696.708.
32. Nam, Y., Chen, C., Gregory, R. I., Chou, J. J. and Sliz, P. (2011) Molecular basis for interaction of let-7 microRNAs with Lin28. Cell, 147, 1080.1091.
33. Loughlin, F. E., Gebert, L. F., Towbin, H., Brunschweiger, A., Hall, J. and Allain, F. H. (2012) Structural basis of pre-let-7 miRNA recognition by the zinc knuckles of pluripotency factor Lin28. Nat. Struct. Mol. Biol., 19, 84.89.
34. Max, K. E. A., Zeeb, M., Bienert, R., Balbach, J. and Heinemann, U. (2006) T-rich DNA single strands bind to a preformed site on the bacterial cold shock protein Bs-CspB. J. Mol. Biol., 360, 702.714.
35. Max, K. E. A., Zeeb, M., Bienert, R., Balbach, J. and Heinemann, U. (2007) Common mode of DNA binding to cold shock domains. Crystal structure of hexathymidine bound to the domain-swapped form of a major cold shock protein from Bacillus caldolyticus. FEBS J., 274, 1265.1279.
36. Zeeb, M. and Balbach, J. (2003) Single-stranded DNA binding of the cold-shock protein CspB from Bacillus subtilis: NMR mapping and mutational characterization. Protein Sci., 12, 112.123.
37. Zeeb, M., Max, K. E. A., Weininger, U., Löw, C., Sticht, H. and Balbach, J. (2006) Recognition of T-rich single-stranded DNA by the cold shock protein Bs-CspB in solution. Nucleic Acids Res., 34, 4561.4571.
38. Scheich, C., Kümmel, D., Soumailakakis, D., Heinemann, U. and Büssow, K. (2007) Vectors for co-expression of an unrestricted number of proteins. Nucleic Acids Res., 35, e43.
39. Heinemann, U., Büssow, K., Mueller, U. and Umbach, P. (2003) Facilities and methods for the high-throughput crystal structural analysis of human proteins. Acc. Chem. Res., 36, 157.163.
40. Leslie, A. (1992) Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 + ESFEAMCB Newsletter on Protein Crystallography, No. 26.
41. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr., 66, 125-132.
42. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Method Enzymol., 276, 307-326.
43. Perrakis, A., Langer, G., Cohen, S. X. and Lamzin, V. S. (2008) Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protoc., 3, 1171-1179.
44. Murshudov, G. N., Vagin, A. A. and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr., 53, 240-255.
45. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132.
46. Ferrin, T. E., Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M. and Meng, E. C. (2004) UCSF chimera-a visualization system for exploratory research and analysis. J. Comput. Chem., 25, 1605-1612.
47. Eftink, M. R. (1997) Fluorescence methods for studying equilibrium macromolecule-ligand interactions. Methods Enzymol., 278, 221-257.
48. Lohman, T. M. and Bujalowski, W. (1991) Thermodynamic methods for model-independent determination of equilibrium binding isotherms for protein-DNA interactions-spectroscopic approaches to monitor binding. Methods Enzymol., 208, 258-290.
49. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
50. Amarasinghe, G. K., De Guzman, R. N., Turner, R. B., Chancellor, K. J., Wu, Z. R. and Summers, M. F. (2000) NMR structure of the HIV-1 nucleocapsid protein bound to stem-loop SL2 of the psi-RNA packaging signal. Implications for genome recognition. J. Mol. Biol., 301, 491-511.
51. De Guzman, R. N., Wu, Z. R., Stalling, C. C., Pappalardo, L., Borer, P. N. and Summers, M. F. (1998) Structure of the HIV-1 nucleocapsid protein bound to the SL3 psi-RNA recognition element. Science, 279, 384-388.
52. Rajkowitsch, L., Chen, D., Stampfl, S., Semrad, K., Waldsich, C., Mayer, O., Jantsch, M. F., Konrat, R., Bläsi, U. and Schroeder, R. (2007) RNA chaperones, RNA annealers and RNA helicases. RNA Biol., 4, 118-130.
53. Schindelin, H., Jiang, W., Inouye, M. and Heinemann, U. (1994) Crystal structure of CspA, the major cold shock protein of Escherichia coli. Proc. Natl. Acad. Sci. USA., 91, 5119-5123.
54. Chaikam, V. and Karlson, D. T. (2010) Comparison of structure, function and regulation of plant cold shock domain proteins to bacterial and animal cold shock domain proteins. BMB Rep., 43, 1-8.
55. Horn, G., Hofweber, R., Kremer, W. and Kalbitzer, H. R. (2007) Structure and function of bacterial cold shock proteins. Cell. Mol. Life Sci., 64, 1457-1470.
56. Mihailovich, M., Militti, C., Gabaldón, T. and Gebauer, F. (2010) Eukaryotic cold shock domain proteins: highly versatile regulators of gene expression. Bioessays, 32, 109-118.
57. Max, K. E. A., Wunderlich, M., Roske, Y., Schmid, F. X. and Heinemann, U. (2007) Optimized variants of the cold shock protein from in vitro selection: structural basis of their high thermostability. J. Mol. Biol., 369, 1087-1097.
58. Bienert, R., Zeeb, M., Dostál, L., Feske, A., Magg, C., Max, K., Welfle, H., Balbach, J. and Heinemann, U. (2004) Single-stranded DNA bound to bacterial cold-shock proteins: preliminary crystallographic and Raman analysis. Acta Crystallogr. D Biol. Crystallogr., 60, 755-757.
59. Lopez, M. M. and Makhatadze, G. I. (2000) Major cold shock proteins, CspA from Escherichia coli and CspB from Bacillus subtilis, interact differently with single-stranded DNA templates. Biochim. Biophys. Acta, 1479, 196-202.
60. Lopez, M. M., Yutani, K. and Makhatadze, G. I. (2001) Interactions of the cold shock protein CspB from Bacillus subtilis with single-stranded DNA. Importance of the T base content and position within the template. J. Biol. Chem., 276, 15511-15518.
61. Lightfoot, H. L., Bugaut, A., Armisen, J., Lehrbach, N. J., Miska, E. A. and Balasubramanian, S. (2011) A LIN28-dependent structural change in pre-let-7g directly inhibits dicer processing. Biochemistry, 50, 7514-7521.
62. Phadtare, S., Inouye, M. and Severinov, K. (2004) The mechanism of nucleic acid melting by a CspA family protein. J. Mol. Biol., 337, 147-155.
63. Phadtare, S. (2011) Unwinding activity of cold shock proteins and RNA metabolism. RNA Biol., 8, 394-397.
64. Phadtare, S. and Severinov, K. (2005) Nucleic acid melting by Escherichia coli CspE. Nucleic Acids Res., 33, 5583-5590.
65. Desjardins, A., Yang, A., Bouvette, J., Omichinski, J. G. and Legault, P. (2012) Importance of the NCp7-like domain in the recognition of pre-let-7g by the pluripotency factor Lin28. Nucleic Acids Res., 40, 1767-1777.
66. Balzer, E., Heine, C., Jiang, Q., Lee, V. and Moss, E. (2010) LIN28 alters cell fate succession and acts independently of the let-7 microRNA during neurogliogenesis in vitro. Development, 137, 891-900.
67. Peng, S., Chen, L.-L., Lei, X.-X., Yang, L., Lin, H., Carmichael, G. G. and Huang, Y. (2011) Genome-wide studies reveal that Lin28 enhances the translation of genes important for growth and survival of human embryonic stem cells. Stem Cells, 29, 496-504.
68. Qiu, C., Ma, Y., Wang, J., Peng, S. and Huang, Y. (2010) Lin28-mediated post-transcriptional regulation of Oct4 expression in human embryonic stem cells. Nucleic Acids Res., 38, 1240-1248.
69. Xu, B. and Huang, Y. (2009) Histone H2a mRNA interacts with Lin28 and contains a Lin28-dependent posttranscriptional regulatory element. Nucleic Acids Res., 37, 4256-4263.
70. Xu, B., Zhang, K. and Huang, Y. (2009) Lin28 modulates cell growth and associates with a subset of cell cycle regulator mRNAs in mouse embryonic stem cells. RNA, 15, 357-361.