Nuclear factor 90 uses an ADAR2-like binding mode to recognize specific bases in dsRNA

Nucleic Acids Research

Volumn 44, Issue 4, 2015, Pages 1924-1936

  Jayachandran, Uma ^a   Grey, Heather ^b   Cook, Atlanta G ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADAR2 PROTEIN; DEAMINASE; DIMER; DOUBLE STRANDED RNA; INTERLEUKIN ENHANCER BINDING FACTOR 2; INTERLEUKIN ENHANCER BINDING FACTOR 3; MONOMER; UNCLASSIFIED DRUG; ADARB1 PROTEIN, HUMAN; ADENOSINE DEAMINASE; MESSENGER RNA; MULTIPROTEIN COMPLEX; RNA BINDING PROTEIN;

ARTICLE; COMPLEX FORMATION; CRYSTAL STRUCTURE; DOUBLE STRANDED RNA BINDING DOMAIN; ENZYME SUBSTRATE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN RNA BINDING; STRUCTURAL HOMOLOGY; AMINO ACID SEQUENCE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE;

ADENOSINE DEAMINASE; AMINO ACID SEQUENCE; GENE EXPRESSION REGULATION; HUMANS; MULTIPROTEIN COMPLEXES; NUCLEAR FACTOR 90 PROTEINS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RNA, DOUBLE-STRANDED; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84960473068     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1508     Document Type: Article

References (51)

1. Castella, S., Bernard, R., Corno, M., Fradin, A. and Larcher, J.C. (2014) Ilf3 and NF90 functions in RNA biology. Wiley Interdiscip. Rev. RNA
2. Masuda, K., Kuwano, Y., Nishida, K., Rokutan, K. and Imoto, I. (2013) NF90 in posttranscriptional gene regulation and microRNA biogenesis. Int. J. Mol. Sci., 14, 17111-17121.
3. Patino, C., Haenni, A.L. and Urcuqui-Inchima, S. (2014) NF90 isoforms, a new family of cellular proteins involved in viral replication? Biochimie, 108C, 20-24.
4. Gwizdek, C., Ossareh-Nazari, B., Brownawell, A.M., Evers, S., Macara, I.G. and Dargemont, C. (2004) Minihelix-containing RNAs mediate exportin-5-dependent nuclear export of the double-stranded RNA-binding protein ILF3. J. Biol. Chem., 279, 884-891.
5. Hoque, M., Shamanna, R.A., Guan, D., Pe'ery, T. and Mathews, M.B. (2011) HIV-1 replication and latency are regulated by translational control of cyclin T1. J. Mol. Biol., 410, 917-932.
6. Kuwano, Y., Kim, H.H., Abdelmohsen, K., Pullmann, R. Jr, Martindale, J.L., Yang, X. and Gorospe, M. (2008) MKP-1 mRNA stabilization and translational control by RNA-binding proteins HuR and NF90. Mol. Cell. Biol., 28, 4562-4575.
7. Shi, L., Zhao, G., Qiu, D., Godfrey, W.R., Vogel, H., Rando, T.A., Hu, H. and Kao, P.N. (2005) NF90 regulates cell cycle exit and terminal myogenic differentiation by direct binding to the 3'-untranslated region of MyoD and p21WAF1/CIP1 mRNAs. J. Biol. Chem., 280, 18981-18989.
8. Shim, J., Lim, H., J, R.Y. and Karin, M. (2002) Nuclear export of NF90 is required for interleukin-2 mRNA stabilization. Mol. Cell, 10, 1331-1344.
9. Gomila, R.C., Martin, G.W. and Gehrke, L. (2011) NF90 binds the dengue virus RNA 3' terminus and is a positive regulator of dengue virus replication. PLoS One, 6, e16687.
10. Isken, O., Baroth, M., Grassmann, C.W., Weinlich, S., Ostareck, D.H., Ostareck-Lederer, A. and Behrens, S.E. (2007) Nuclear factors are involved in hepatitis C virus RNA replication. RNA, 13, 1675-1692.
11. Li, Y., Masaki, T., Shimakami, T. and Lemon, S.M. (2014) hnRNP L and NF90 interact with hepatitis C virus 5'-terminal untranslated RNA and promote efficient replication. J. Virol., 88, 7199-7209.
12. Schumacher, J.M., Lee, K., Edelhoff, S. and Braun, R.E. (1995) Spnr, a murine RNA-binding protein that is localized to cytoplasmic microtubules. J. Cell Biol., 129, 1023-1032.
13. Wolkowicz, U.M. and Cook, A.G. (2012) NF45 dimerizes with NF90, Zfr and SPNR via a conserved domain that has a nucleotidyltransferase fold. Nucleic Acids Res., 40, 9356-9368.
14. Tian, B., Bevilacqua, P.C., Diegelman-Parente, A. and Mathews, M.B. (2004) The double-stranded-RNA-binding motif: interference and much more. Nat. Rev. Mol. Cell Biol., 5, 1013-1023.
15. Masliah, G., Barraud, P. and Allain, F.H. (2013) RNA recognition by double-stranded RNA binding domains: a matter of shape and sequence. Cell Mol. Life Sci., 70, 1875-1895.
16. Slotkin, W. and Nishikura, K. (2013) Adenosine-to-inosine RNA editing and human disease. Genome Med., 5, 105.
17. Nishikura, K. (2010) Functions and regulation of RNA editing by ADAR deaminases. Annu. Rev. Biochem., 79, 321-349.
18. Barbon, A. and Barlati, S. (2011) Glutamate receptor RNA editing in health and disease. Biochemistry (Mosc), 76, 882-889.
19. Bass, B.L. (2002) RNA editing by adenosine deaminases that act on RNA. Annu. Rev. Biochem., 71, 817-846.
20. Sommer, B., Kohler, M., Sprengel, R. and Seeburg, P.H. (1991) RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell, 67, 11-19.
21. Higuchi, M., Single, F.N., Kohler, M., Sommer, B., Sprengel, R. and Seeburg, P.H. (1993) RNA editing of AMPA receptor subunit GluR-B: a base-paired intron-exon structure determines position and efficiency. Cell, 75, 1361-1370.
22. Stefl, R., Oberstrass, F.C., Hood, J.L., Jourdan, M., Zimmermann, M., Skrisovska, L., Maris, C., Peng, L., Hofr, C., Emeson, R.B. et al. (2010) The solution structure of the ADAR2 dsRBM-RNA complex reveals a sequence-specific readout of the minor groove. Cell, 143, 225-237.
23. Rigo, F., Hua, Y., Chun, S.J., Prakash, T.P., Krainer, A.R. and Bennett, C.F. (2012) Synthetic oligonucleotides recruit ILF2/3 to RNA transcripts to modulate splicing. Nat. Chem. Biol., 8, 555-561.
24. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr., 62, 72-82.
25. Kabsch, W. (2010) Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr. D Biol. Crystallogr., 66, 133-144.
26. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132.
27. Seetharaman, J., Neely, H., Wang, D., Janjua, H., Cunningham, K., Owens, L., Xiao, R., Liu, J., Baran, M.C., Acton, T.B. et al. (2010) Crystal structure of DRBM 2 domain of Interleukin enhancer-binding factor 3 from Homo sapiens, Northeast Structural Genomics Consortium Target HR4527E. PDB ID: 3P1X.
28. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C. and Read, R.J. (2007) Phaser crystallographic software. J. Appl. Crystallogr., 40, 658-674.
29. Pallan, P.S., Greene, E.M., Jicman, P.A., Pandey, R.K., Manoharan, M., Rozners, E. and Egli, M. (2011) Unexpected origins of the enhanced pairing affinity of 2'-fluoro-modified RNA. Nucleic Acids Res., 39, 3482-3495.
30. Kadirvel, S., He, F., Muto, Y., Inoue, M., Kigawa, T., Shirouzu, M., Terada, T., Yokoyama, S. and (RSGI), R.S.G.P.I. (2006) Solution structure of DSRM domain in Spermatid perinuclear RNA-bind protein. PDB ID: 2DMY.
31. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W. et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr., 66, 213-221.
32. Roehrl, M.H., Wang, J.Y. and Wagner, G. (2004) A general framework for development and data analysis of competitive high-throughput screens for small-molecule inhibitors of protein-protein interactions by fluorescence polarization. Biochemistry, 43, 16056-16066.
33. Brownawell, A.M. and Macara, I.G. (2002) Exportin-5, a novel karyopherin, mediates nuclear export of double-stranded RNA binding proteins. J. Cell Biol., 156, 53-64.
34. Kuwano, Y., Pullmann, R. Jr, Marasa, B.S., Abdelmohsen, K., Lee, E.K., Yang, X., Martindale, J.L., Zhan, M. and Gorospe, M. (2010) NF90 selectively represses the translation of target mRNAs bearing an AU-rich signature motif. Nucleic Acids Res., 38, 225-238.
35. Liao, H.J., Kobayashi, R. and Mathews, M.B. (1998) Activities of adenovirus virus-associated RNAs: purification and characterization of RNA binding proteins. Proc. Natl. Acad. Sci. U.S.A., 95, 8514-8519.
36. Yao, P., Potdar, A.A., Ray, P.S., Eswarappa, S.M., Flagg, A.C., Willard, B. and Fox, P.L. (2013) The HILDA complex coordinates a conditional switch in the 3'-untranslated region of the VEGFA mRNA. PLoS Biol., 11, e1001635.
37. Parrott, A.M. and Mathews, M.B. (2007) Novel rapidly evolving hominid RNAs bind nuclear factor 90 and display tissue-restricted distribution. Nucleic Acids Res., 35, 6249-6258.
38. Layzer, J.M., McCaffrey, A.P., Tanner, A.K., Huang, Z., Kay, M.A. and Sullenger, B.A. (2004) In vivo activity of nuclease-resistant siRNAs. RNA, 10, 766-771.
39. Fu, Q. and Yuan, Y.A. (2013) Structural insights into RISC assembly facilitated by dsRNA-binding domains of human RNA helicase A (DHX9). Nucleic Acids Res., 41, 3457-3470.
40. Gan, J., Tropea, J.E., Austin, B.P., Court, D.L., Waugh, D.S. and Ji, X. (2005) Intermediate states of ribonuclease III in complex with double-stranded RNA. Structure, 13, 1435-1442.
41. Ryter, J.M. and Schultz, S.C. (1998) Molecular basis of double-stranded RNA-protein interactions: structure of a dsRNA-binding domain complexed with dsRNA. EMBO J., 17, 7505-7513.
42. Ohman, M., Kallman, A.M. and Bass, B.L. (2000) In vitro analysis of the binding of ADAR2 to the pre-mRNA encoding the GluR-B R/G site. RNA, 6, 687-697.
43. Steitz, T.A. (1990) Structural studies of protein-nucleic acid interaction: the sources of sequence-specific binding. Q. Rev. Biophys., 23, 205-280.
44. Olsen, J.V., Vermeulen, M., Santamaria, A., Kumar, C., Miller, M.L., Jensen, L.J., Gnad, F., Cox, J., Jensen, T.S., Nigg, E.A. et al. (2010) Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal., 3, ra3.
45. Rigbolt, K.T., Prokhorova, T.A., Akimov, V., Henningsen, J., Johansen, P.T., Kratchmarova, I., Kassem, M., Mann, M., Olsen, J.V. and Blagoev, B. (2011) System-wide temporal characterization of the proteome and phosphoproteome of human embryonic stem cell differentiation. Sci Signal, 4, rs3.
46. Duchange, N., Pidoux, J., Camus, E. and Sauvaget, D. (2000) Alternative splicing in the human interleukin enhancer binding factor 3 (ILF3) gene. Gene, 261, 345-353.
47. Chilibeck, K.A., Wu, T., Liang, C., Schellenberg, M.J., Gesner, E.M., Lynch, J.M. and MacMillan, A.M. (2006) FRET analysis of in vivo dimerization by RNA-editing enzymes. J. Biol. Chem., 281, 16530-16535.
48. Cho, D.S., Yang, W., Lee, J.T., Shiekhattar, R., Murray, J.M. and Nishikura, K. (2003) Requirement of dimerization for RNA editing activity of adenosine deaminases acting on RNA. J. Biol. Chem., 278, 17093-17102.
49. Gallo, A., Keegan, L.P., Ring, G.M. and O'Connell, M.A. (2003) An ADAR that edits transcripts encoding ion channel subunits functions as a dimer. EMBO J., 22, 3421-3430.
50. Poulsen, H., Jorgensen, R., Heding, A., Nielsen, F.C., Bonven, B. and Egebjerg, J. (2006) Dimerization of ADAR2 is mediated by the double-stranded RNA binding domain. RNA, 12, 1350-1360.
51. Nie, Y., Ding, L., Kao, P.N., Braun, R. and Yang, J.H. (2005) ADAR1 interacts with NF90 through double-stranded RNA and regulates NF90-mediated gene expression independently of RNA editing. Mol. Cell. Biol., 25, 6956-6963.