Sequence-specific RNA recognition by an RGG motif connects U1 and U2 snRNP for spliceosome assembly
In mammals, the structural basis for the interaction between U1 and U2 small nuclear ribonucleoproteins (snRNPs) during the early steps of splicing is still elusive. The binding of the ubiquitin-like (UBL) domain of SF3A1 to the stem-loop 4 of U1 snRNP (U1-SL4) contributes to this interaction. Here,...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2022-02, Vol.119 (6), p.1-11 |
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| creator | de Vries, Tebbe Martelly, William Campagne, Sébastien Sabath, Kevin Sarnowski, Chris P. Wong, Jason Leitner, Alexander Jonas, Stefanie Sharma, Shalini Allain, Frédéric H.-T. |
| description | In mammals, the structural basis for the interaction between U1 and U2 small nuclear ribonucleoproteins (snRNPs) during the early steps of splicing is still elusive. The binding of the ubiquitin-like (UBL) domain of SF3A1 to the stem-loop 4 of U1 snRNP (U1-SL4) contributes to this interaction. Here, we determined the 3D structure of the complex between the UBL of SF3A1 and U1-SL4 RNA. Our crystallography, NMR spectroscopy, and cross-linking mass spectrometry data show that SF3A1-UBL recognizes, sequence specifically, the GCG/CGC RNA stem and the apical UUCG tetraloop of U1-SL4. In vitro and in vivo mutational analyses support the observed intermolecular contacts and demonstrate that the carboxyl-terminal arginine-glycine-glycine-arginine (RGGR) motif of SF3A1-UBL binds sequence specifically by inserting into the RNA major groove. Thus, the characterization of the SF3A1-UBL/U1-SL4 complex expands the repertoire of RNA binding domains and reveals the capacity of RGG/RG motifs to bind RNA in a sequence-specific manner. |
| doi_str_mv | 10.1073/pnas.2114092119 |
| format | Article |
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The binding of the ubiquitin-like (UBL) domain of SF3A1 to the stem-loop 4 of U1 snRNP (U1-SL4) contributes to this interaction. Here, we determined the 3D structure of the complex between the UBL of SF3A1 and U1-SL4 RNA. Our crystallography, NMR spectroscopy, and cross-linking mass spectrometry data show that SF3A1-UBL recognizes, sequence specifically, the GCG/CGC RNA stem and the apical UUCG tetraloop of U1-SL4. In vitro and in vivo mutational analyses support the observed intermolecular contacts and demonstrate that the carboxyl-terminal arginine-glycine-glycine-arginine (RGGR) motif of SF3A1-UBL binds sequence specifically by inserting into the RNA major groove. Thus, the characterization of the SF3A1-UBL/U1-SL4 complex expands the repertoire of RNA binding domains and reveals the capacity of RGG/RG motifs to bind RNA in a sequence-specific manner.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.2114092119</identifier><identifier>PMID: 35101980</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Binding ; Biological Sciences ; Crosslinking ; Crystallography ; Crystallography, X-Ray ; Glycine ; Grooves ; Humans ; Life Sciences ; Magnetic resonance spectroscopy ; Mass spectrometry ; Mass spectroscopy ; NMR ; NMR spectroscopy ; Nuclear magnetic resonance ; Nuclear Magnetic Resonance, Biomolecular ; Nucleotide Motifs ; Nucleotide sequence ; Ribonucleic acid ; Ribonucleoprotein, U1 Small Nuclear - chemistry ; Ribonucleoprotein, U1 Small Nuclear - genetics ; Ribonucleoprotein, U2 Small Nuclear - chemistry ; Ribonucleoprotein, U2 Small Nuclear - genetics ; Ribonucleoproteins ; Ribonucleoproteins (small nuclear) ; Ribonucleoproteins (U2 small nuclear) ; RNA ; RNA Splicing Factors - chemistry ; RNA Splicing Factors - genetics ; Splicing ; Ubiquitin</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2022-02, Vol.119 (6), p.1-11</ispartof><rights>Copyright © 2022 the Author(s). Published by PNAS.</rights><rights>Copyright National Academy of Sciences Feb 8, 2022</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>Copyright © 2022 the Author(s). 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| subjects | Binding Biological Sciences Crosslinking Crystallography Crystallography, X-Ray Glycine Grooves Humans Life Sciences Magnetic resonance spectroscopy Mass spectrometry Mass spectroscopy NMR NMR spectroscopy Nuclear magnetic resonance Nuclear Magnetic Resonance, Biomolecular Nucleotide Motifs Nucleotide sequence Ribonucleic acid Ribonucleoprotein, U1 Small Nuclear - chemistry Ribonucleoprotein, U1 Small Nuclear - genetics Ribonucleoprotein, U2 Small Nuclear - chemistry Ribonucleoprotein, U2 Small Nuclear - genetics Ribonucleoproteins Ribonucleoproteins (small nuclear) Ribonucleoproteins (U2 small nuclear) RNA RNA Splicing Factors - chemistry RNA Splicing Factors - genetics Splicing Ubiquitin |
| title | Sequence-specific RNA recognition by an RGG motif connects U1 and U2 snRNP for spliceosome assembly |
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