1hd1 Citations

Structure and interactions with RNA of the N-terminal UUAG-specific RNA-binding domain of hnRNP D0.

Abstract

Heterogeneous nuclear ribonucleoprotein (hnRNP) D0 has two ribonucleoprotein (RNP)-type RNA-binding domains (RBDs), each of which can bind solely to the UUAG sequence specifically. The structure of the N-terminal RBD (RBD1) determined by NMR is presented here. It folds into a compact alphabeta structure comprising a four-stranded antiparallel beta-sheet packed against two alpha-helices, which is characteristic of the RNP-type RBDs. Special structural features of RBD1 include N-capping boxes for both alpha-helices, a beta-bulge in the second beta-strand, and an additional short antiparallel beta-sheet coupled with a beta-turn-like structure in a loop. Two hydrogen bonds which restrict the positions of loops were identified. Backbone resonance assignments for RBD1 complexed with r(UUAGGG) revealed that the overall folding is maintained in the complex. The candidate residues involved in the interactions with RNA were identified by chemical shift perturbation analysis. They are located in the central and peripheral regions of the RNA-binding surface composed of the four-stranded beta-sheet, loops, and the C-terminal region. It is suggested that non-specific interactions with RNA are performed by the residues in the central region of the RNA-binding surface, while specific interactions are performed by those in the peripheral regions. It was also found that RBD1 has the ability to inhibit the formation of the quadruplex structure.

Articles - 1hd1 mentioned but not cited (1)

  1. RNA-Induced Conformational Switching and Clustering of G3BP Drive Stress Granule Assembly by Condensation. Guillén-Boixet J, Kopach A, Holehouse AS, Wittmann S, Jahnel M, Schlüßler R, Kim K, Trussina IREA, Wang J, Mateju D, Poser I, Maharana S, Ruer-Gruß M, Richter D, Zhang X, Chang YT, Guck J, Honigmann A, Mahamid J, Hyman AA, Pappu RV, Alberti S, Franzmann TM. Cell 181 346-361.e17 (2020)


Reviews citing this publication (7)

  1. G-quadruplexes in RNA biology. Millevoi S, Moine H, Vagner S. Wiley Interdiscip Rev RNA 3 495-507 (2012)
  2. Musashi RNA-Binding Proteins as Cancer Drivers and Novel Therapeutic Targets. Kudinov AE, Karanicolas J, Golemis EA, Boumber Y. Clin Cancer Res 23 2143-2153 (2017)
  3. The role of AUF1 in regulated mRNA decay. Gratacós FM, Brewer G. Wiley Interdiscip Rev RNA 1 457-473 (2010)
  4. MRNA stability and the control of gene expression: implications for human disease. Hollams EM, Giles KM, Thomson AM, Leedman PJ. Neurochem Res 27 957-980 (2002)
  5. Modulation of neoplastic gene regulatory pathways by the RNA-binding factor AUF1. Zucconi BE, Wilson GM. Front Biosci (Landmark Ed) 16 2307-2325 (2011)
  6. microRNA-binding proteins: specificity and function. Zealy RW, Wrenn SP, Davila S, Min KW, Yoon JH. Wiley Interdiscip Rev RNA 8 (2017)
  7. Control of protein expression through mRNA stability in calcium signalling. Misquitta CM, Chen T, Grover AK. Cell Calcium 40 329-346 (2006)

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  1. Human, Drosophila, and C.elegans TDP43: nucleic acid binding properties and splicing regulatory function. Ayala YM, Pantano S, D'Ambrogio A, Buratti E, Brindisi A, Marchetti C, Romano M, Baralle FE. J Mol Biol 348 575-588 (2005)
  2. RNA G-quadruplexes are globally unfolded in eukaryotic cells and depleted in bacteria. Guo JU, Bartel DP. Science 353 aaf5371 (2016)
  3. A circular RNA circ-DNMT1 enhances breast cancer progression by activating autophagy. Du WW, Yang W, Li X, Awan FM, Yang Z, Fang L, Lyu J, Li F, Peng C, Krylov SN, Xie Y, Zhang Y, He C, Wu N, Zhang C, Sdiri M, Dong J, Ma J, Gao C, Hibberd S, Yang BB. Oncogene 37 5829-5842 (2018)
  4. Recognition of GU-rich polyadenylation regulatory elements by human CstF-64 protein. Pérez Cañadillas JM, Varani G. EMBO J 22 2821-2830 (2003)
  5. Structural analysis of cooperative RNA binding by the La motif and central RRM domain of human La protein. Alfano C, Sanfelice D, Babon J, Kelly G, Jacks A, Curry S, Conte MR. Nat Struct Mol Biol 11 323-329 (2004)
  6. Quantitative proteomics analysis integrated with microarray data reveals that extracellular matrix proteins, catenins, and p53 binding protein 1 are important for chemotherapy response in ovarian cancers. Pan S, Cheng L, White JT, Lu W, Utleg AG, Yan X, Urban ND, Drescher CW, Hood L, Lin B. OMICS 13 345-354 (2009)
  7. Solution structure of the two N-terminal RNA-binding domains of nucleolin and NMR study of the interaction with its RNA target. Allain FH, Gilbert DE, Bouvet P, Feigon J. J Mol Biol 303 227-241 (2000)
  8. Structural characterization of Set1 RNA recognition motifs and their role in histone H3 lysine 4 methylation. Trésaugues L, Dehé PM, Guérois R, Rodriguez-Gil A, Varlet I, Salah P, Pamblanco M, Luciano P, Quevillon-Cheruel S, Sollier J, Leulliot N, Couprie J, Tordera V, Zinn-Justin S, Chàvez S, van Tilbeurgh H, Géli V. J Mol Biol 359 1170-1181 (2006)
  9. Vertebrate 2xRBD hnRNP proteins: a comparative analysis of genome, mRNA and protein sequences. Akindahunsi AA, Bandiera A, Manzini G. Comput Biol Chem 29 13-23 (2005)
  10. The RRM domain of poly(A)-specific ribonuclease has a noncanonical binding site for mRNA cap analog recognition. Nagata T, Suzuki S, Endo R, Shirouzu M, Terada T, Inoue M, Kigawa T, Kobayashi N, Güntert P, Tanaka A, Hayashizaki Y, Muto Y, Yokoyama S. Nucleic Acids Res 36 4754-4767 (2008)
  11. The high kinetic stability of a G-quadruplex limits hnRNP F qRRM3 binding to G-tract RNA. Samatanga B, Dominguez C, Jelesarov I, Allain FH. Nucleic Acids Res 41 2505-2516 (2013)
  12. Heterogeneous nuclear ribonucleoprotein D0 contains transactivator and DNA-binding domains. Tolnay M, Baranyi L, Tsokos GC. Biochem J 348 Pt 1 151-158 (2000)
  13. High precision NMR structure of YhhP, a novel Escherichia coli protein implicated in cell division. Katoh E, Hatta T, Shindo H, Ishii Y, Yamada H, Mizuno T, Yamazaki T. J Mol Biol 304 219-229 (2000)
  14. Structure of the C-terminal RNA-binding domain of hnRNP D0 (AUF1), its interactions with RNA and DNA, and change in backbone dynamics upon complex formation with DNA. Katahira M, Miyanoiri Y, Enokizono Y, Matsuda G, Nagata T, Ishikawa F, Uesugi S. J Mol Biol 311 973-988 (2001)
  15. Protein kinase A enhances, whereas glycogen synthase kinase-3 beta inhibits, the activity of the exon 2-encoded transactivator domain of heterogeneous nuclear ribonucleoprotein D in a hierarchical fashion. Tolnay M, Juang YT, Tsokos GC. Biochem J 363 127-136 (2002)
  16. Origin of higher affinity to RNA of the N-terminal RNA-binding domain than that of the C-terminal one of a mouse neural protein, musashi1, as revealed by comparison of their structures, modes of interaction, surface electrostatic potentials, and backbone dynamics. Miyanoiri Y, Kobayashi H, Imai T, Watanabe M, Nagata T, Uesugi S, Okano H, Katahira M. J Biol Chem 278 41309-41315 (2003)
  17. Elucidation of the mode of interaction in the UP1-telomerase RNA-telomeric DNA ternary complex which serves to recruit telomerase to telomeric DNA and to enhance the telomerase activity. Nagata T, Takada Y, Ono A, Nagata K, Konishi Y, Nukina T, Ono M, Matsugami A, Furukawa A, Fujimoto N, Fukuda H, Nakagama H, Katahira M. Nucleic Acids Res 36 6816-6824 (2008)
  18. Interactions of heterogeneous nuclear ribonucleoprotein D-like protein JKTBP and its domains with high-affinity binding sites. Kamei D, Yamada M. Gene 298 49-57 (2002)
  19. The RGG/RG motif of AUF1 isoform p45 is a key modulator of the protein's RNA chaperone and RNA annealing activities. Meyer A, Golbik RP, Sänger L, Schmidt T, Behrens SE, Friedrich S. RNA Biol 16 960-971 (2019)
  20. Crystal Structure of the N-Terminal RNA Recognition Motif of mRNA Decay Regulator AUF1. Choi YJ, Yoon JH, Chang JH. Biomed Res Int 2016 3286191 (2016)
  21. Structural basis for the recognition of transiently structured AU-rich elements by Roquin. Binas O, Tants JN, Peter SA, Janowski R, Davydova E, Braun J, Niessing D, Schwalbe H, Weigand JE, Schlundt A. Nucleic Acids Res 48 7385-7403 (2020)
  22. Analysis of the structural determinants for RNA binding of the human protein AUF1/hnRNP D. Moraes KC, Lee WH, Kobarg J. Biol Chem 383 831-837 (2002)
  23. In-vitro dual binding activity of a evolutionarily related subgroup of hnRNP proteins. Bandiera A, Medic N, Akindahunsi AA, Manzini G. Mol Cell Biochem 268 121-127 (2005)
  24. The Complete Chloroplast Genome of Plukenetia volubilis Provides Insights Into the Organelle Inheritance. Villanueva-Corrales S, García-Botero C, Garcés-Cardona F, Ramírez-Ríos V, Villanueva-Mejía DF, Álvarez JC. Front Plant Sci 12 667060 (2021)