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PMID: 10856256 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Structure of tandem RNA recognition motifs from polypyrimidine tract binding protein reveals novel features of the RRM fold.

The EMBO journal ·Vol. 19 ·No. 12 ·2000-06-15 ·Pages 3132-41

Conte MR, Grüne T, Ghuman J, Kelly G, Ladas A, Matthews S, Curry S

Abstract

Polypyrimidine tract binding protein (PTB), an RNA binding protein containing four RNA recognition motifs (RRMs), is involved in both pre-mRNA splicing and translation initiation directed by picornaviral internal ribosome entry sites. Sequence comparisons previously indicated that PTB is a non-canonical RRM protein. The solution structure of a PTB fragment containing RRMs 3 and 4 shows that the protein consists of two domains connected by a long, flexible linker. The two domains tumble independently in solution, having no fixed relative orientation. In addition to the betaalphabetabetaalphabeta topology, which is characteristic of RRM domains, the C-terminal extension of PTB RRM-3 incorporates an unanticipated fifth beta-strand, which extends the RNA binding surface. The long, disordered polypeptide connecting beta4 and beta5 in RRM-3 is poised above the RNA binding surface and is likely to contribute to RNA recognition. Mutational analyses show that both RRM-3 and RRM-4 contribute to RNA binding specificity and that, despite its unusual sequence, PTB binds RNA in a manner akin to that of other RRM proteins.

MeSH Terms
Amino Acid Motifs Amino Acid Sequence Binding Sites DNA-Binding Proteins/chemistry Models, Molecular Molecular Sequence Data Motion Nuclear Magnetic Resonance, Biomolecular Peptide Chain Initiation, Translational Polypyrimidine Tract-Binding Protein Protein Binding Protein Structure, Tertiary RNA Splicing RNA-Binding Proteins/chemistry
Chemicals
DNA-Binding Proteins RNA-Binding Proteins Polypyrimidine Tract-Binding Protein
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Conte M R
Department of Biochemistry, Imperial College of Science, Technology and Medicine, Exhibition Road, London, UK.
Grüne T
Ghuman J
Kelly G
Ladas A
Matthews S
Curry S
References (54)
54 references, click to expand
  1. Recognition of polyadenylate RNA by the poly(A)-binding protein.
    Cell. 1999 Sep 17;98(6):835-45 PMID: 10499800
  2. Protein backbone angle restraints from searching a database for chemical shift and sequence homology.
    J Biomol NMR. 1999 Mar;13(3):289-302 PMID: 10212987
  3. RNA-protein interactions in regulation of picornavirus RNA translation.
    Microbiol Rev. 1996 Sep;60(3):499-511 PMID: 8840784
  4. Identification of the RNA binding segment of human U1 A protein and definition of its binding site on U1 snRNA.
    EMBO J. 1989 Dec 20;8(13):4163-70 PMID: 2531658
  5. hnRNP I, the polypyrimidine tract-binding protein: distinct nuclear localization and association with hnRNAs.
    Nucleic Acids Res. 1992 Jul 25;20(14):3671-8 PMID: 1641332
  6. Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation.
    Biochemistry. 1994 May 17;33(19):5984-6003 PMID: 7514039
  7. Structural analysis of the interaction of the pyrimidine tract-binding protein with the internal ribosomal entry site of encephalomyocarditis virus and foot-and-mouth disease virus RNAs.
    RNA. 1996 Dec;2(12):1199-212 PMID: 8972770
  8. Polypyrimidine tract-binding protein positively regulates inclusion of an alternative 3'-terminal exon.
    Mol Cell Biol. 1999 Jan;19(1):78-85 PMID: 9858533
  9. Absence of interdomain contacts in the crystal structure of the RNA recognition motifs of Sex-lethal.
    Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):4892-7 PMID: 10220389
  10. Structural basis for recognition of the tra mRNA precursor by the Sex-lethal protein.
    Nature. 1999 Apr 15;398(6728):579-85 PMID: 10217141
  11. Polypyrimidine-tract binding protein (PTB) is necessary, but not sufficient, for efficient internal initiation of translation of human rhinovirus-2 RNA.
    RNA. 1999 Mar;5(3):344-59 PMID: 10094304
  12. Mutation of PTB binding sites causes misregulation of alternative 3' splice site selection in vivo.
    RNA. 1997 Jul;3(7):764-78 PMID: 9214659
  13. Interaction of polypyrimidine tract binding protein with the encephalomyocarditis virus mRNA internal ribosomal entry site.
    Biochemistry. 1993 Aug 17;32(32):8268-75 PMID: 8394133
  14. Solution structures of the first and second RNA-binding domains of human U2 small nuclear ribonucleoprotein particle auxiliary factor (U2AF(65)).
    EMBO J. 1999 Aug 16;18(16):4523-34 PMID: 10449418
  15. Characterization of cDNAs encoding the polypyrimidine tract-binding protein.
    Genes Dev. 1991 Jul;5(7):1224-36 PMID: 1906035
  16. A common RNA recognition motif identified within a defined U1 RNA binding domain of the 70K U1 snRNP protein.
    Cell. 1989 Apr 7;57(1):89-101 PMID: 2467746
  17. Crystal structure of the RNA-binding domain of the U1 small nuclear ribonucleoprotein A.
    Nature. 1990 Dec 6;348(6301):515-20 PMID: 2147232
  18. The cellular polypeptide p57 (pyrimidine tract-binding protein) binds to multiple sites in the poliovirus 5' nontranslated region.
    J Virol. 1994 Feb;68(2):941-50 PMID: 8289396
  19. Interaction of a cellular 57-kilodalton protein with the internal translation initiation site of foot-and-mouth disease virus.
    J Virol. 1991 Dec;65(12):6486-94 PMID: 1658355
  20. Post-transcriptional regulation: the dawn of PTB.
    Curr Biol. 1997 Nov 1;7(11):R705-8 PMID: 9382788
  21. Crystal structure of human UP1, the domain of hnRNP A1 that contains two RNA-recognition motifs.
    Structure. 1997 Apr 15;5(4):559-70 PMID: 9115444
  22. Determination of functional domains in polypyrimidine-tract-binding protein.
    Biochem J. 1998 Apr 1;331 ( Pt 1):169-75 PMID: 9512476
  23. A Xenopus protein related to hnRNP I has a role in cytoplasmic RNA localization.
    Mol Cell. 1999 Sep;4(3):431-7 PMID: 10518224
  24. Quantitative determination that one of two potential RNA-binding domains of the A protein component of the U1 small nuclear ribonucleoprotein complex binds with high affinity to stem-loop II of U1 RNA.
    Proc Natl Acad Sci U S A. 1990 Aug;87(16):6393-7 PMID: 1696729
  25. RNA recognition: towards identifying determinants of specificity.
    Trends Biochem Sci. 1991 Jun;16(6):214-20 PMID: 1716386
  26. A neuron-specific splicing switch mediated by an array of pre-mRNA repressor sites: evidence of a regulatory role for the polypyrimidine tract binding protein and a brain-specific PTB counterpart.
    RNA. 1997 Sep;3(9):996-1015 PMID: 9292499
  27. The determinants of RNA-binding specificity of the heterogeneous nuclear ribonucleoprotein C proteins.
    J Biol Chem. 1994 Sep 16;269(37):23074-8 PMID: 8083209
  28. Characterization and molecular cloning of polypyrimidine tract-binding protein: a component of a complex necessary for pre-mRNA splicing.
    Genes Dev. 1991 Jul;5(7):1237-51 PMID: 1906036
  29. The polypyrimidine tract binding protein binds upstream of neural cell-specific c-src exon N1 to repress the splicing of the intron downstream.
    Mol Cell Biol. 1997 Aug;17(8):4667-76 PMID: 9234723
  30. The upstream sequence element of the C2 complement poly(A) signal activates mRNA 3' end formation by two distinct mechanisms.
    Genes Dev. 1998 Aug 15;12(16):2522-34 PMID: 9716405
  31. Direct evidence that polypyrimidine tract binding protein (PTB) is essential for internal initiation of translation of encephalomyocarditis virus RNA.
    RNA. 1995 Nov;1(9):924-38 PMID: 8548657
  32. Protein structure comparison by alignment of distance matrices.
    J Mol Biol. 1993 Sep 5;233(1):123-38 PMID: 8377180
  33. Multiple RNA binding domains (RBDs) just don't add up.
    Nucleic Acids Res. 1995 Mar 11;23(5):725-8 PMID: 7535921
  34. Solution structure of the N-terminal RNP domain of U1A protein: the role of C-terminal residues in structure stability and RNA binding.
    J Mol Biol. 1996 Mar 29;257(2):398-411 PMID: 8609632
  35. Role of an inhibitory pyrimidine element and polypyrimidine tract binding protein in repression of a regulated alpha-tropomyosin exon.
    RNA. 1998 Jan;4(1):85-100 PMID: 9436911
  36. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR.
    J Biomol NMR. 1996 Dec;8(4):477-86 PMID: 9008363
  37. Multiple RRMs contribute to RNA binding specificity and affinity for polypyrimidine tract binding protein.
    Biochemistry. 1997 Sep 30;36(39):11881-90 PMID: 9305981
  38. Chemical shift mapping of the RNA-binding interface of the multiple-RBD protein sex-lethal.
    Biochemistry. 1997 Nov 25;36(47):14306-17 PMID: 9398148
  39. Measurement of HN-H alpha J couplings in calcium-free calmodulin using new 2D and 3D water-flip-back methods.
    J Biomol NMR. 1994 Nov;4(6):871-8 PMID: 7812158
  40. Initiation of encephalomyocarditis virus RNA translation: the authentic initiation site is not selected by a scanning mechanism.
    EMBO J. 1990 Nov;9(11):3753-9 PMID: 2170120
  41. AURELIA, a program for computer-aided analysis of multidimensional NMR spectra.
    J Biomol NMR. 1995 Nov;6(3):255-70 PMID: 22910849
  42. Translation of encephalomyocarditis virus RNA: parameters influencing the selection of the internal initiation site.
    EMBO J. 1994 Apr 1;13(7):1673-81 PMID: 8157006
  43. Isolation of a mammalian homologue of a fission yeast differentiation regulator.
    Mol Cell Biol. 1999 May;19(5):3829-41 PMID: 10207106
  44. Crystal structure of the two RNA binding domains of human hnRNP A1 at 1.75 A resolution.
    Nat Struct Biol. 1997 Mar;4(3):215-22 PMID: 9164463
  45. Structure, backbone dynamics and interactions with RNA of the C-terminal RNA-binding domain of a mouse neural RNA-binding protein, Musashi1.
    J Mol Biol. 1999 Mar 26;287(2):315-30 PMID: 10080895
  46. Changes in side-chain and backbone dynamics identify determinants of specificity in RNA recognition by human U1A protein.
    J Mol Biol. 1999 Dec 10;294(4):967-79 PMID: 10588900
  47. Determination of three-dimensional structures of proteins by simulated annealing with interproton distance restraints. Application to crambin, potato carboxypeptidase inhibitor and barley serine proteinase inhibitor 2.
    Protein Eng. 1988 Apr;2(1):27-38 PMID: 2855369
  48. Crystal structure at 1.92 A resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin.
    Nature. 1994 Dec 1;372(6505):432-8 PMID: 7984237
  49. Structural basis of the RNA-binding specificity of human U1A protein.
    EMBO J. 1997 Sep 15;16(18):5764-72 PMID: 9312034
  50. Crystal structure of the two-RRM domain of hnRNP A1 (UP1) complexed with single-stranded telomeric DNA.
    Genes Dev. 1999 May 1;13(9):1102-15 PMID: 10323862
  51. Crystal structure of the spliceosomal U2B"-U2A' protein complex bound to a fragment of U2 small nuclear RNA.
    Nature. 1998 Aug 13;394(6694):645-50 PMID: 9716128
  52. Polypyrimidine tract binding protein functions as a repressor to regulate alternative splicing of alpha-actinin mutally exclusive exons.
    Mol Cell Biol. 1999 Apr;19(4):2699-711 PMID: 10082536
  53. Cap-independent translation of encephalomyocarditis virus RNA: structural elements of the internal ribosomal entry site and involvement of a cellular 57-kD RNA-binding protein.
    Genes Dev. 1990 Sep;4(9):1560-72 PMID: 2174810
  54. The polypyrimidine tract binding protein (PTB) requirement for internal initiation of translation of cardiovirus RNAs is conditional rather than absolute.
    RNA. 1998 Jun;4(6):626-38 PMID: 9622122
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2000-06-15
Pages
3132-41
Language
English
Region
England
NLM ID
8208664
PMCID
PMC203357
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · JE514316 · United Kingdom
Databases
PDB
Analysis Services
Analysis Services

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