Importance of the NCp7-like domain in the recognition of pre-let-7g by the pluripotency factor Lin28

Nucleic Acids Research

Volumn 40, Issue 4, 2012, Pages 1767-1777

  Desjardins, Alexandre ^a   Yang, Ao ^a   Bouvette, Jonathan ^a   Omichinski, James G ^a   Legault, Pascale ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DICER; MICRORNA; NCP7 PROTEIN; PLURIPOTENCY FACTOR LIN28; PRE LET 7G; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN UNFOLDING; RNA BINDING; RNA PROCESSING;

ANIMALS; BASE SEQUENCE; BINDING SITES; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; MICE; MICRORNAS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA PRECURSORS; RNA-BINDING PROTEINS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84855471182     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr808     Document Type: Article

References (73)

1. Bartel, D. P. (2009) MicroRNAs: target recognition and regulatory functions. Cell, 136, 215-233.
2. Winter, J., Jung, S., Keller, S., Gregory, R. I. and Diederichs, S. (2009) Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat. Cell. Biol., 11, 228-234.
3. Filipowicz, W., Bhattacharyya, S. N. and Sonenberg, N. (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat. Rev. Genet., 9, 102-114.
4. Kim, V. N., Han, J. and Siomi, M. C. (2009) Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol., 10, 126-139.
5. Zhao, Y., Ransom, J. F., Li, A., Vedantham, V., von Drehle, M., Muth, A. N., Tsuchihashi, T., McManus, M. T., Schwartz, R. J. and Srivastava, D. (2007) Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell, 129, 303-317. (Pubitemid 46574975)
6. Peter, M. E. (2009) Let-7 and miR-200 microRNAs: guardians against pluripotency and cancer progression. Cell Cycle, 8, 843-852.
7. Ambros, V. (2011) MicroRNAs and developmental timing. Curr. Opin. Genet. Dev., 21, 511-517.
8. Esquela-Kerscher, A. and Slack, F. J. (2006) Oncomirs-microRNAs with a role in cancer. Nat. Rev. Cancer, 6, 259-269.
9. Shi, X. B., Tepper, C. G. and deVere White, R. W. (2008) Cancerous miRNAs and their regulation. Cell Cycle, 7, 1529-1538. (Pubitemid 351881316)
10. Roush, S. and Slack, F. J. (2008) The let-7 family of microRNAs. Trends Cell Biol., 18, 505-516.
11. Bussing, I., Slack, F. J. and Grosshans, H. (2008) Let-7 microRNAs in development, stem cells and cancer. Trends Mol. Med., 14, 400-409.
12. Visone, R. and Croce, C. M. (2009) MiRNAs and cancer. Am. J. Pathol., 174, 1131-1138.
13. O'Day, E. and Lal, A. (2010) MicroRNAs and their target gene networks in breast cancer. Breast Cancer Res., 12, 201.
14. Thomson, J. M., Newman, M., Parker, J. S., Morin-Kensicki, E. M., Wright, T. and Hammond, S. M. (2006) Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev., 20, 2202-2207.
15. Wulczyn, F. G., 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. (Pubitemid 46213489)
16. Van Wynsberghe, P. M., Kai, Z. S., Massirer, K. B., Burton, V. H., Yeo, G. W. and Pasquinelli, A. E. (2011) LIN-28 co-transcriptionally binds primary let-7 to regulate miRNA maturation in Caenorhabditis elegans. Nat. Struct. Mol. Biol., 18, 302-308.
17. Michlewski, G. and Caceres, J. F. (2010) Antagonistic role of hnRNP A1 and KSRP in the regulation of let-7a biogenesis. Nat. Struct. Mol. Biol., 17, 1011-1018.
18. Trabucchi, M., Briata, P., Garcia-Mayoral, M., Haase, A. D., Filipowicz, W., Ramos, A., Gherzi, R. and Rosenfeld, M. G. (2009) The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature, 459, 1010-1014.
19. 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.
20. Piskounova, E., Viswanathan, S. R., Janas, M., LaPierre, 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.
21. Viswanathan, S. R., Daley, G. Q. and Gregory, R. I. (2008) Selective blockade of microRNA processing by Lin28. Science, 320, 97-100. (Pubitemid 351490762)
22. 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.
23. Rybak, A., Fuchs, H., Smirnova, L., Brandt, C., Pohl, E. E., Nitsch, R. and Wulczyn, F. G. (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.
24. 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.
25. Hagan, J. P., Piskounova, E. and Gregory, R. I. (2009) Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nat. Struct. Mol. Biol., 16, 1021-1025.
26. 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.
27. Newman, M. A. and Hammond, S. M. (2010) Lin-28: an early embryonic sentinel that blocks Let-7 biogenesis. Int. J. Biochem. Cell Biol., 42, 1330-1333.
28. Yu, J., Vodyanik, M. A., Smuga-Otto, K., Antosiewicz-Bourget, J., Frane, J. L., Tian, S., Nie, J., Jonsdottir, G. A., Ruotti, V., Stewart, R. et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science, 318, 1917-1920.
29. Viswanathan, S. R. and Daley, G. Q. (2010) Lin28: a microRNA regulator with a macro role. Cell, 140, 445-449.
30. 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. (Pubitemid 27152406)
31. Balzer, E. and Moss, E. G. (2007) Localization of the developmental timing regulator Lin28 to mRNP complexes, P-bodies and stress granules. RNA Biol., 4, 16-25. (Pubitemid 47328289)
32. Landsman, D. (1992) RNP-1, an RNA-binding motif is conserved in the DNA-binding cold shock domain. Nucleic Acids Res., 20, 2861-2864.
33. 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. (Pubitemid 28063374)
34. Polesskaya, A., Cuvellier, S., Naguibneva, I., Duquet, A., Moss, E. G. and Harel-Bellan, A. (2007) Lin-28 binds IGF-2 mRNA and participates in skeletal myogenesis by increasing translation efficiency. Genes Dev., 21, 1125-1138. (Pubitemid 46686480)
35. 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.
36. 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.
37. 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.
38. 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.
39. Di Tomasso, G., Lampron, P., Dagenais, P., Omichinski, J. G. and Legault, P. (2011) The ARiBo tag: a reliable tool for affinity purification of RNAs under native conditions. Nucleic Acids Res., 39, e18.
40. Di Tomasso, G., Dagenais, P., Desjardins, A., Rompré-Brodeur, A., Delfosse, V. and Legault, P. (2012) Affinity purification of RNA using an ARiBo tag. Methods Mol. Biol., In Press.
41. Delfosse, V., Bouchard, P., Bonneau, E., Dagenais, P., Lemay, J. F., Lafontaine, D. A. and Legault, P. (2010) Riboswitch structure: an internal residue mimicking the purine ligand. Nucleic Acids Res., 38, 2057-2068.
42. Bouchard, P., Lacroix-Labonté, J., Desjardins, G., Lampron, P., Lisi, V., Lemieux, S., Major, F. and Legault, P. (2008) Role of SLV in SLI substrate recognition by the Neurospora VS ribozyme. RNA, 14, 736-748. (Pubitemid 351480885)
43. Jenkins, L. M., Byrd, J. C., Hara, T., Srivastava, P., Mazur, S. J., Stahl, S. J., Inman, J. K., Appella, E., Omichinski, J. G. and Legault, P. (2005) Studies on the mechanism of inactivation of the HIV-1 nucleocapsid protein NCp7 with 2-mercaptobenzamide thioesters. J. Med. Chem., 48, 2847-2858. (Pubitemid 40548099)
44. Omichinski, J. G., Clore, G. M., Schaad, O., Felsenfeld, G., Trainor, C., Appella, E., Stahl, S. J. and Gronenborn, A. M. (1993) NMR structure of a specific DNA complex of Zn-containing DNA binding domain of GATA-1. Science, 261, 438-446. (Pubitemid 23276551)
45. Regulski, E. E. and Breaker, R. R. (2008) In-line probing analysis of riboswitches. Methods Mol. Biol., 419, 53-67.
46. Kay, L., Keifer, P. and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc., 114, 10663-10665.
47. Wittekind, M. and Mueller, L. (1993) HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha-and beta-carbon resonances in proteins. J. Magn. Reson. Series B, 101, 201-205.
48. Grzesiek, S., Dobeli, H., Gentz, R., Garotta, G., Labhardt, A. M. and Bax, A. (1992) 1H, 13C, and 15N NMR backbone assignments and secondary structure of human interferon-gamma. Biochemistry, 31, 8180-8190.
49. Muhandiram, D. R. and Kay, L. E. (1994) Gradient-enhanced triple-resonance three-dimensional NMR experiments with improved sensitivity. J. Magn. Reson. Series B, 103, 203-216.
50. Wishart, D. S., Bigam, C. G., Yao, J., Dyson, H. J., Oldfield, E., Markley, J. L. and Sykes, B. D. (1995) 1H, 13C, 15N chemical shift referencing in biomolecular NMR. J. Biomol. NMR, 6, 135-140.
51. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J. and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR, 6, 277-293.
52. Johnson, B. A. and Blevins, R. A. (1994) NMR view: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR, 4, 603-614.
53. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402. (Pubitemid 27359211)
54. 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.
55. Steyaert, J. (1997) A decade of protein engineering on ribonuclease T1-atomic dissection of the enzyme-substrate interactions. Eur. J. Biochem., 247, 1-11. (Pubitemid 27319479)
56. Weiss, J. N. (1997) The Hill equation revisited: uses and misuses. FASEB J., 11, 835-841. (Pubitemid 27371892)
57. Ermolenko, D. N. and Makhatadze, G. I. (2002) Bacterial cold-shock proteins. Cell Mol. Life Sci., 59, 1902-1913. (Pubitemid 36015863)
58. Jiang, W., Hou, Y. and Inouye, M. (1997) CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J. Biol. Chem., 272, 196-202. (Pubitemid 27021144)
59. Dannull, J., Surovoy, A., Jung, G. and Moelling, K. (1994) Specific binding of HIV-1 nucleocapsid protein to PSI RNA in vitro requires N-terminal zinc finger and flanking basic amino acid residues. EMBO J., 13, 1525-1533. (Pubitemid 24114702)
60. Shubsda, M. F., Paoletti, A. C., Hudson, B. S. and Borer, P. N. (2002) Affinities of packaging domain loops in HIV-1 RNA for the nucleocapsid protein. Biochemistry, 41, 5276-5282. (Pubitemid 34411683)
61. Paoletti, A. C., Shubsda, M. F., Hudson, B. S. and Borer, P. N. (2002) Affinities of the nucleocapsid protein for variants of SL3 RNA in HIV-1. Biochemistry, 41, 15423-15428. (Pubitemid 36008154)
62. Fisher, R. J., Rein, A., Fivash, M., Urbaneja, M. A., Casas-Finet, J. R., Medaglia, M. and Henderson, L. E. (1998) Sequence-specific binding of human immunodeficiency virus type 1 nucleocapsid protein to short oligonucleotides. J. Virol., 72, 1902-1909. (Pubitemid 28100742)
63. Yuan, Y., Kerwood, D. J., Paoletti, A. C., Shubsda, M. F. and Borer, P. N. (2003) Stem of SL1 RNA in HIV-1: structure and nucleocapsid protein binding for a 1,3 internal loop. Biochemistry, 42, 5259-5269. (Pubitemid 36560422)
64. Jin, J., Jing, W., Lei, X. X., Feng, C., Peng, S., Boris-Lawrie, K. and Huang, Y. (2011) Evidence that Lin28 stimulates translation by recruiting RNA helicase A to polysomes. Nucleic Acids Res., 39, 3724-3734.
65. 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.
66. Claverie, J. M. (2006) Viruses take center stage in cellular evolution. Genome Biol., 7, 110.
67. Bandea, C. I. (2009) The origin and evolution of viruses as molecular organisms. Nat. Precedings, npre. 2009. 3886. 2001.
68. Guo, Y., Chen, Y., Ito, H., Watanabe, A., Ge, X., Kodama, T. and Aburatani, H. (2006) Identification and characterization of lin-28 homolog B (LIN28B) in human hepatocellular carcinoma. Gene, 384, 51-61. (Pubitemid 44755336)
69. Tsuchihashi, Z., Khosla, M. and Herschlag, D. (1993) Protein enhancement of hammerhead ribozyme catalysis. Science, 262, 99-102.
70. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R. et al. (2007) Clustal W and Clustal X version 2.0 Bioinformatics, 23, 2947-2948.
71. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415. (Pubitemid 37442169)
72. Parisien, M. and Major, F. (2008) The MC-Fold and MC-Sym pipeline infers RNA structure from sequence data. Nature, 452, 51-55. (Pubitemid 351355097)
73. Notredame, C., Higgins, D. G. and Heringa, J. (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol., 302, 205-217.