A protein-RNA specificity code enables targeted activation of an endogenous human transcript

Nature Structural and Molecular Biology

Volumn 21, Issue 8, 2014, Pages 732-738

  Campbell, Zachary T ^a   Valley, Cary T ^a   Wickens, Marvin ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASE SEQUENCE; BINDING SITES; CELL LINE, TUMOR; CONSENSUS SEQUENCE; CYCLIN B1; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN ENGINEERING; RNA, MESSENGER; RNA-BINDING PROTEINS; TRANSCRIPTIONAL ACTIVATION;

EID: 84905593100     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2847     Document Type: Article

References (37)

1. Proudfoot, C., McPherson, A.L., Kolb, A.F. & Stark, W.M. Zinc finger recombinases with adaptable DNA sequence specificity. PLoS ONE 6, e19537 (2011
2. Wood, A.J. et al. Targeted genome editing across species using ZFNs and TALENs. Science 333, 307 (2011
3. Wickens, M., Bernstein, D.S., Kimble, J. & Parker, R. A PUF family portrait: 3'UTR regulation as a way of life. Trends Genet. 18, 150-157 (2002
4. Campbell, Z.T. et al. Cooperativity in RNA-protein interactions: Global analysis of RNA binding specificity. Cell Reports 1, 570-581 (2012
5. Galgano, A. et al. Comparative analysis of mRNA targets for human PUF-family proteins suggests extensive interaction with the miRNA regulatory system. PLoS ONE 3, e3164 (2008
6. Gerber, A.P., Herschlag, D. & Brown, P.O. Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast. PLoS Biol. 2, E79 (2004
7. Kershner, A.M. & Kimble, J. Genome-wide analysis of mRNA targets for Caenorhabditis elegans FBF, a conserved stem cell regulator. Proc. Natl. Acad. Sci. USA 107, 3936-3941 (2010
8. Hafner, M. et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141, 129-141 (2010
9. Wang, Y., Opperman, L., Wickens, M. & Hall, T.M. Structural basis for specific recognition of multiple mRNA targets by a PUF regulatory protein. Proc. Natl. Acad. Sci. USA 106, 20186-20191 (2009
10. Wang, X., McLachlan, J., Zamore, P.D. & Hall, T.M. Modular recognition of RNA by a human pumilio-homology domain. Cell 110, 501-512 (2002
11. Wang, X., Zamore, P.D. & Hall, T.M. Crystal structure of a Pumilio homology domain. Mol. Cell 7, 855-865 (2001
12. Zhu, D., Stumpf, C.R., Krahn, J.M., Wickens, M. & Hall, T.M. A 5' cytosine binding pocket in Puf3p specifies regulation of mitochondrial mRNAs. Proc. Natl. Acad. Sci. USA 106, 20192-20197 (2009
13. Koh, Y.Y. et al. Stacking interactions in PUF-RNA complexes. RNA 17, 718-727 (2011
14. Wang, Y., Wang, Z. & Tanaka Hall, T.M. Engineered proteins with Pumilio/fem-3 mRNA binding factor scaffold to manipulate RNA metabolism. FEBS J. 280, 3755-3767 (2013
15. Opperman, L., Hook, B., DeFino, M., Bernstein, D.S. & Wickens, M. A single spacer nucleotide determines the specificities of two mRNA regulatory proteins. Nat. Struct. Mol. Biol. 12, 945-951 (2005
16. Dong, S. et al. Specific and modular binding code for cytosine recognition in Pumilio/FBF (PUF) RNA-binding domains. J. Biol. Chem. 286, 26732-26742 (2011
17. Filipovska, A., Razif, M.F., Nygard, K.K. & Rackham, O. A universal code for RNA recognition by PUF proteins. Nat. Chem. Biol. 7, 425-427 (2011
18. Bernstein, D., Hook, B., Hajarnavis, A., Opperman, L. & Wickens, M. Binding specificity and mRNA targets of a C. elegans PUF protein, FBF-1. RNA 11, 447-458 (2005
19. Valley, C.T. et al. Patterns and plasticity in RNA-protein interactions enable recruitment of multiple proteins through a single site. Proc. Natl. Acad. Sci. USA 109, 6054-6059 (2012
20. Qiu, C. et al. Divergence of Pumilio/fem-3 mRNA binding factor (PUF) protein specificity through variations in an RNA-binding pocket. J. Biol. Chem. 287, 6949-6957 (2012
21. Stumpf, C.R., Kimble, J. & Wickens, M. A Caenorhabditis elegans PUF protein family with distinct RNA binding specificity. RNA 14, 1550-1557 (2008
22. Tuerk, C. & Gold, L. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249, 505-510 (1990
23. Ellington, A.D. & Szostak, J.W. In vitro selection of RNA molecules that bind specific ligands. Nature 346, 818-822 (1990
24. Carlson, C.D. et al. Specificity landscapes of DNA binding molecules elucidate biological function. Proc. Natl. Acad. Sci. USA 107, 4544-4549 (2010
25. Miller, M.T., Higgin, J.J. & Hall, T.M. Basis of altered RNA-binding specificity by PUF proteins revealed by crystal structures of yeast Puf4p. Nat. Struct. Mol. Biol. 15, 397-402 (2008
26. Brito, D.A. & Rieder, C.L. The ability to survive mitosis in the presence of microtubule poisons differs significantly between human nontransformed (RPE-1) and cancer (U2OS, HeLa) cells. Cell Motil. Cytoskeleton 66, 437-447 (2009
27. Russo, A.J. et al. E2F-1 overexpression in U2OS cells increases cyclin B1 levels and cdc2 kinase activity and sensitizes cells to antimitotic agents. Cancer Res. 66, 7253-7260 (2006
28. Valencia-Sanchez, M.A., Liu, J., Hannon, G.J. & Parker, R. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev. 20, 515-524 (2006
29. Gray, N.K., Collar, J.M., Dickson, K.S. & Wickens, M. Multiple portions of poly(A)-binding protein stimulate translation in vivo. EMBO J. 19, 4723-4733 (2000
30. Lam, K.N., van Bakel, H., Cote, A.G., Van Der Ven, A. & Hughes, T.R. Sequence specificity is obtained from the majority of modular C2H2 zinc-finger arrays. Nucleic Acids Res. 39, 4680-4690 (2011
31. Enuameh, M.S. et al. Global analysis of Drosophila Cys2-His2 zinc finger proteins reveals a multitude of novel recognition motifs and binding determinants. Genome Res. 23, 928-940 (2013
32. Lu, G. & Hall, T.M. Alternate modes of cognate RNA recognition by human PUMILIO proteins. Structure 19, 361-367 (2011
33. Campbell, Z.T. & Baldwin, T.O. Two lysine residues in the bacterial luciferase mobile loop stabilize reaction intermediates. J. Biol. Chem. 284, 32827-32834 (2009
34. Campbell, Z.T. & Baldwin, T.O. Fre is the major flavin reductase supporting bioluminescence from Vibrio harveyi luciferase in Escherichia coli. J. Biol. Chem. 284, 8322-8328 (2009
35. LeGendre, J.B. et al. RNA targets and specificity of Staufen, a double-stranded RNA-binding protein in Caenorhabditis elegans. J. Biol. Chem. 288, 2532-2545 (2013
36. Li, L. et al. GLIPR1 suppresses prostate cancer development through targeted oncoprotein destruction. Cancer Res. 71, 7694-7704 (2011
37. Gibson, D.G. et al. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6, 343-345 (2009