Structural basis of nucleic acid binding by Nicotiana tabacum glycine-rich RNA-binding protein: Implications for its RNA chaperone function

Nucleic Acids Research

Volumn 42, Issue 13, 2014, Pages 8705-8718

  Khan, Fariha ^a,b   Daniëls, Mark A ^a   Folkers, Gert E ^a   Boelens, Rolf ^a   Saqlan Naqvi, S M ^b   Van Ingen, Hugo ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b PMAS ARID AGRICULTURE UNIVERSITY   (Pakistan)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE RICH RNA BINDING PROTEIN; RNA BINDING PROTEIN; SINGLE STRANDED DNA; SINGLE STRANDED RNA; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BIOASSAY; COMPLEX FORMATION; CONTROLLED STUDY; DNA DENATURATION; DNA SEQUENCE; MOLECULAR MODEL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN RNA BINDING; RNA RECOGNITION MOTIF; STATIC ELECTRICITY; STRUCTURE ANALYSIS; TOBACCO;

AMINO ACID SEQUENCE; CONSERVED SEQUENCE; DNA, SINGLE-STRANDED; NUCLEIC ACID DENATURATION; PLANT PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA; RNA-BINDING PROTEINS; STATIC ELECTRICITY; TOBACCO;

EID: 84905570328     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku468     Document Type: Article

References (52)

1. Glisovic, T., Bachorik, J.L., Yong, J. and Dreyfuss, G. (2008) RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett., 582, 1977-1986.
2. Maris, C., Dominguez, C. and Allain, F.H.T. (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J., 272, 2118-2131.
3. Califice, S., Baurain, D., Hanikenne, M. and Motte, P. (2012) A single ancient origin for prototypical serine/arginine-rich splicing factors. Plant Physiol., 158, 546-560.
4. Gomez, J., Sanchez-Martinez, D., Stiefel, V., Rigau, J., Puigdomenech, P. and Pages, M. (1988) A gene induced by the plant hormone abscisic acid in response to water stress encodes a glycine-rich protein. Nature, 334, 262-264.
5. Maruyama, K., Sato, N. and Ohta, N. (1999) Conservation of structure and cold-regulation of RNA-binding proteins in cyanobacteria: Probable convergent evolution with eukaryotic glycine-rich RNA-binding proteins. Nucleic Acids Res., 27, 2029-2036.
6. Khan, F., Sultana, T., Deeba, F. and Naqvi, S.M. (2013) Dynamics of mRNA of glycine-rich rna-binding protein during wounding, cold and salt stresses in Nicotiana Tabacum. Pak. J. Bot., 45, 297-300.
7. Nicaise, V., Joe, A., Jeong, B.-R., Korneli, C., Boutrot, F., Westedt, I., Staiger, D., Alfano, J.R. and Zipfel, C. (2013) Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. EMBO J., 32, 701-712.
8. Mangeon, A., Junqueira, R.M. and Sachetto-Martins, G. (2010) Functional diversity of the plant glycine-rich proteins superfamily. Plant Signal. Behav., 5, 99-104.
9. Naqvi, S.M., Park, K.S., Yi, S.Y., Lee, H.W., Bok, S.H. and Choi, D. (1998) A glycine-rich RNA-binding protein gene is differentially expressed during acute hypersensitive response following Tobacco Mosaic Virus infection in tobacco. Plant Mol. Biol., 37, 571-576.
10. Lee, M.-O., Kim, K.P., Kim, B.-G., Hahn, J.-S. and Hong, C.B. (2009) Flooding Stress-Induced Glycine-Rich RNA-Binding Protein from Nicotiana tabacum. Mol. Cells 27, 47-54.
11. Lorković, Z.J. (2009) Role of plant RNA-binding proteins in development, stress response and genome organization. Trends Plant Sci., 14, 229-236.
12. Heintzen, C., Nater, M., Apel, K. and Staiger, D. (1997) AtGRP7, a nuclear RNA-binding protein as a component of a circadian-regulated negative feedback loop in Arabidopsis thaliana. Proc. Natl Acad. Sci. U.S.A., 94, 8515-8520.
13. Staiger, D., Zecca, L., Wieczorek Kirk, D.A., Apel, K. and Eckstein, L. (2003) The circadian clock regulated RNA-binding protein AtGRP7 autoregulates its expression by influencing alternative splicing of its own pre-mRNA. Plant J., 33, 361-371.
14. Schöning, J.C., Streitner, C., Meyer, I.M., Gao, Y. and Staiger, D. (2008) Reciprocal regulation of glycine-rich RNA-binding proteins via an interlocked feedback loop coupling alternative splicing to nonsense-mediated decay in Arabidopsis. Nucleic Acids Res., 36, 6977-6987.
15. Streitner, C., Köster, T., Simpson, C.G., Shaw, P., Danisman, S., Brown, J.W.S. and Staiger, D. (2012) An hnRNP-like RNA-binding protein affects alternative splicing by in vivo interaction with transcripts in Arabidopsis thaliana. Nucleic Acids Res., 40, 11240-11255.
16. Streitner, C., Danisman, S., Wehrle, F., Schöning, J.C., Alfano, J.R. and Staiger, D. (2008) The small glycine-rich RNA binding protein AtGRP7 promotes floral transition in Arabidopsis thaliana. Plant J., 56, 239-250.
17. Fu, Z.Q., Guo, M., Jeong, B.-R., Tian, F., Elthon, T.E., Cerny, R.L., Staiger, D. and Alfano, J.R. (2007) A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447, 284-288.
18. Kim, J.S., Park, S.J., Kwak, K.J., Kim, Y.O., Kim, J.Y., Song, J., Jang, B., Jung, C.-H. and Kang, H. (2007) Cold shock domain proteins and glycine-rich RNA-binding proteins from Arabidopsis thaliana can promote the cold adaptation process in Escherichia coli. Nucleic Acids Res., 35, 506-516.
19. Kim, J.Y., Kim, W.Y., Kwak, K.J., Oh, S.H., Han, Y.S. and Kang, H. (2010) Glycine-rich RNA-binding proteins are functionally conserved in Arabidopsis thaliana and Oryza sativa during cold adaptation process. J. Exp. Bot., 61, 2317-2325.
20. Nakaminami, K., Karlson, D.T. and Imai, R. (2006) Functional conservation of cold shock domains in bacteria and higher plants. Proc. Natl Acad. Sci. U.S.A., 103, 10122-10127.
21. Kim, M.K., Jung, H.J., Kim, D.H. and Kang, H. (2012) Characterization of glycine-rich RNA-binding proteins in Brassica napusunder stress conditions. Physiol. Plant., 146, 297-307.
22. Kwak, K.J., Park, S.J., Han, J.H., Kim, M.K., Oh, S.H., Han, Y.S. and Kang, H. (2011) Structural determinants crucial to the RNA chaperone activity of glycine-rich RNA-binding proteins 4 and 7 in Arabidopsis thaliana during the cold adaptation process. J. Exp. Bot., 62, 4003-4011.
23. de Jong, R.N., Daniëls, M.A., Kaptein, R. and Folkers, G.E. (2006) Enzyme free cloning for high throughput gene cloning and expression. J. Struct. Funct. Genomics, 7, 109-118.
24. Cavanagh, J., J Fairbrother, W., Palmer, A.G. III, J Skelton, N. and Rance, M. (2007) .Protein NMR spectroscopy: principles and practice. Academic Press, New York.
25. Zwahlen, C., Legault, P., Vincent, S., Greenblatt, J., Konrat, R. and Kay, L. (1997) Methods for measurement of intermolecular NOEs by multinuclear NMR spectroscopy: Application to a bacteriophage lambda N-peptide/boxB RNA complex. J. Am. Chem. Soc., 119, 6711-6721.
26. 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.
27. Vranken, W.F., Boucher, W., Stevens, T.J., Fogh, R.H., Pajon, A., Llinás, M., Ulrich, E.L., Markley, J.L., Ionides, J. and Laue, E.D. (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins, 59, 687-696.
28. Shen, Y., Delaglio, F., Cornilescu, G. and Bax, A. (2009) TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR, 44, 213-223.
29. Güntert, P., Mumenthaler, C. and Wüthrich, K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol., 273, 283-298.
30. Herrmann, T., Güntert, P. and Wüthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol., 319, 209-227.
31. Brünger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S. et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr., 54, 905-921.
32. Nederveen, A.J., Doreleijers, J.F., Vranken, W., Miller, Z., Spronk, C.A.E.M., Nabuurs, S.B., Güntert, P., Livny, M., Markley, J.L., Nilges, M. et al. (2005) RECOORD: a recalculated coordinate database of 500+ proteins from the PDB using restraints from the BioMagResBank. Proteins, 59, 662-672.
33. Doreleijers, J.F., Sousa da Silva, A.W., Krieger, E., Nabuurs, S.B., Spronk, C.A.E.M., Stevens, T.J., Vranken, W.F., Vriend, G. and Vuister, G.W. (2012) CING: an integrated residue-based structure validation program suite. J. Biomol. NMR, 54, 267-283.
34. Schüttpelz, M., Schöning, J.C., Doose, S., Neuweiler, H., Peters, E., Staiger, D. and Sauer, M. (2008) Changes in conformational dynamics of mRNA upon AtGRP7 binding studied by fluorescence correlation spectroscopy. J. Am. Chem. Soc., 130, 9507-9513.
35. Kato, H., van Ingen, H., Zhou, B.-R., Feng, H., Bustin, M., Kay, L.E. and Bai, Y. (2011) Architecture of the high mobility group nucleosomal protein 2-nucleosome complex as revealed by methyl-based NMR. Proc. Natl Acad. Sci. U.S.A., 108, 12283-12288.
36. Dominguez, C., Boelens, R. and Bonvin, A.M.J.J. (2003) HADDOCK: A protein?protein docking approach based on biochemical or biophysical information. J. Am. Chem. Soc., 125, 1731-1737.
37. de Vries, S.J., van Dijk, A.D.J., Krzeminski, M., van Dijk, M., Thureau, A., Hsu, V., Wassenaar, T. and Bonvin, A.M.J.J. (2007) HADDOCK versus HADDOCK: new features and performance of HADDOCK2.0 on the CAPRI targets. Proteins, 69, 726-733.
38. Leeper, T.C., Qu, X., Lu, C., Moore, C. and Varani, G. (2010) Novel protein-protein contacts facilitate mRNA 3′-processing signal recognition by Rna15 and Hrp1. J. Mol. Biol., 401, 334-349.
39. Cléry, A., Jayne, S., Benderska, N., Dominguez, C., Stamm, S. and Allain, F.H.T. (2011) Molecular basis of purine-rich RNA recognition by the human SR-like protein Tra2-β1. Nat. Struct. Mol. Biol., 18, 443-450.
40. Ohyama, T., Nagata, T., Tsuda, K., Kobayashi, N., Imai, T., Okano, H., Yamazaki, T. and Katahira, M. (2012) Structure of Musashi1 in a complex with target RNA: the role of aromatic stacking interactions. Nucleic Acids Res., 40, 3218-3231.
41. Daubner, G.M., Cléry, A., Jayne, S., Stevenin, J. and Allain, F.H.T. (2012) A syn-anti conformational difference allows SRSF2 to recognize guanines and cytosines equally well. EMBO J., 31, 162-174.
42. Safaee, N., Kozlov, G., Noronha, A.M., Xie, J., Wilds, C.J. and Gehring, K. (2012) Interdomain allostery promotes assembly of the poly(A) mRNA complex with PABP and eIF4G. Mol. Cell, 48, 375-386.
43. Berjanskii, M.V. and Wishart, D.S. (2005) A simple method to predict protein flexibility using secondary chemical shifts. J. Am. Chem. Soc., 127, 14970-14971.
44. Schoening, J.C., Streitner, C., Page, D.R., Hennig, S., Uchida, K., Wolf, E., Furuya, M. and Staiger, D. (2007) Auto-regulation of the circadian slave oscillator component AtGRP7 and regulation of its targets is impaired by a single RNA recognition motif point mutation. Plant J., 52, 1119-1130.
45. Jeong, B.-R., Lin, Y., Joe, A., Guo, M., Korneli, C., Yang, H., Wang, P., Yu, M., Cerny, R.L., Staiger, D. et al. (2011) Structure function analysis of an ADP-ribosyltransferase type III effector and its RNA-binding target in plant immunity. J. Biol. Chem., 286, 43272-43281.
46. Abdul-Manan, N. and Williams, K.R. (1996) hnRNP A1 binds promiscuously to oligoribonucleotides: utilization of random and homo-oligonucleotides to discriminate sequence from base-specific binding. Nucleic Acids Res., 24, 4063-4070.
47. Tavanez, J.P., Madl, T., Kooshapur, H., Sattler, M. and Valcárcel, J. (2012) hnRNP A1 proofreads 3′ splice site recognition by U2AF. Mol. Cell, 45, 314-329.
48. Mason, K.E., Tripet, B.P., Parrott, D., Fischer, A.M. and Copié, V. (2014) (1)H, (13)C, (15)N backbone and side chain NMR resonance assignments for the N-terminal RNA recognition motif of the HvGR-RBP1 protein involved in the regulation of barley (Hordeum vulgare L) senescence. Biomol. NMR Assign., 8, 149-153.
49. Van Dusen, C.M., Yee, L., McNally, L.M. and McNally, M.T. (2010) A glycine-rich domain of hnRNP H/F promotes nucleocytoplasmic shuttling and nuclear import through an interaction with transportin 1. Mol. Cell. Biol., 30, 2552-2562.
50. Ziemienowicz, A., Haasen, D., Staiger, D. and Merkle, T. (2003) Arabidopsis transportin1 is the nuclear import receptor for the circadian clock-regulated RNA-binding protein AtGRP7. Plant Mol. Biol., 53, 201-212.
51. Bhatt, P., d'Avout, C., Kane, N.S., Borowiec, J.A. and Saxena, A. (2011) Specific domains of nucleolin interact with Hdm2 and antagonize Hdm2-mediated p53 ubiquitination. FEBS J., 279, 370-383.
52. Zu, K., Sikes, M.L. and Beyer, A.L. (1998) Separable roles in vivo for the two RNA binding domains of Drosophila A1-hnRNP homolog. RNA, 4, 1585-1598.