Structural basis for specific recognition of multiple mRNA targets by a PUF regulatory protein
Caenorhabditis elegans fem-3 binding factor (FBF) is a founding member of the PUMILIO/FBF (PUF) family of mRNA regulatory proteins. It regulates multiple mRNAs critical for stem cell maintenance and germline development. Here, we report crystal structures of FBF in complex with 6 different 9-nt RNA...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2009-12, Vol.106 (48), p.20186-20191 |
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| container_title | Proceedings of the National Academy of Sciences - PNAS |
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| creator | Wang, Yeming Opperman, Laura Wickens, Marvin Hall, Traci M. Tanaka |
| description | Caenorhabditis elegans fem-3 binding factor (FBF) is a founding member of the PUMILIO/FBF (PUF) family of mRNA regulatory proteins. It regulates multiple mRNAs critical for stem cell maintenance and germline development. Here, we report crystal structures of FBF in complex with 6 different 9-nt RNA sequences, including elements from 4 natural mRNAs. These structures reveal that FBF binds to conserved bases at positions 1-3 and 7-8. The key specificity determinant of FBF vs. other PUF proteins lies in positions 4-6. In FBF/RNA complexes, these bases stack directly with one another and turn away from the RNA-binding surface. A short region of FBF is sufficient to impart its unique specificity and lies directly opposite the flipped bases. We suggest that this region imposes a flattened curvature on the protein; hence, the requirement for the additional nucleotide. The principles of FBF/RNA recognition suggest a general mechanism by which PUF proteins recognize distinct families of RNAs yet exploit very nearly identical atomic contacts in doing so. |
| doi_str_mv | 10.1073/pnas.0812076106 |
| format | Article |
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Tanaka</creator><creatorcontrib>Wang, Yeming ; Opperman, Laura ; Wickens, Marvin ; Hall, Traci M. Tanaka ; Argonne National Lab. (ANL), Argonne, IL (United States)</creatorcontrib><description>Caenorhabditis elegans fem-3 binding factor (FBF) is a founding member of the PUMILIO/FBF (PUF) family of mRNA regulatory proteins. It regulates multiple mRNAs critical for stem cell maintenance and germline development. Here, we report crystal structures of FBF in complex with 6 different 9-nt RNA sequences, including elements from 4 natural mRNAs. These structures reveal that FBF binds to conserved bases at positions 1-3 and 7-8. The key specificity determinant of FBF vs. other PUF proteins lies in positions 4-6. In FBF/RNA complexes, these bases stack directly with one another and turn away from the RNA-binding surface. A short region of FBF is sufficient to impart its unique specificity and lies directly opposite the flipped bases. We suggest that this region imposes a flattened curvature on the protein; hence, the requirement for the additional nucleotide. The principles of FBF/RNA recognition suggest a general mechanism by which PUF proteins recognize distinct families of RNAs yet exploit very nearly identical atomic contacts in doing so.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.0812076106</identifier><identifier>PMID: 19901328</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animals ; Atoms ; Bacteria ; Biochemistry ; Biological Sciences ; Caenorhabditis elegans - metabolism ; Caenorhabditis elegans Proteins - chemistry ; Caenorhabditis elegans Proteins - metabolism ; Chemical bases ; Chimeras ; CRYSTAL STRUCTURE ; Crystallography ; Curvature ; Electrophoretic Mobility Shift Assay ; Germ cells ; MAINTENANCE ; MATERIALS SCIENCE ; Messenger RNA ; Models, Molecular ; Nucleotide sequences ; PROTEINS ; Ribonucleic acid ; RNA ; RNA, Messenger - metabolism ; RNA-Binding Proteins - chemistry ; RNA-Binding Proteins - metabolism ; SPECIFICITY ; STEM CELLS ; TARGETS ; Two-Hybrid System Techniques ; Yeasts</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2009-12, Vol.106 (48), p.20186-20191</ispartof><rights>Copyright National Academy of Sciences Dec 1, 2009</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c617t-f441bd8cc9f11a86510909f4cbe115709ee5afcbedb4a8d5c2c91edebd6a2a143</citedby><cites>FETCH-LOGICAL-c617t-f441bd8cc9f11a86510909f4cbe115709ee5afcbedb4a8d5c2c91edebd6a2a143</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/106/48.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/25593350$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/25593350$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19901328$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/biblio/1006077$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Yeming</creatorcontrib><creatorcontrib>Opperman, Laura</creatorcontrib><creatorcontrib>Wickens, Marvin</creatorcontrib><creatorcontrib>Hall, Traci M. Tanaka</creatorcontrib><creatorcontrib>Argonne National Lab. (ANL), Argonne, IL (United States)</creatorcontrib><title>Structural basis for specific recognition of multiple mRNA targets by a PUF regulatory protein</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Caenorhabditis elegans fem-3 binding factor (FBF) is a founding member of the PUMILIO/FBF (PUF) family of mRNA regulatory proteins. It regulates multiple mRNAs critical for stem cell maintenance and germline development. Here, we report crystal structures of FBF in complex with 6 different 9-nt RNA sequences, including elements from 4 natural mRNAs. These structures reveal that FBF binds to conserved bases at positions 1-3 and 7-8. The key specificity determinant of FBF vs. other PUF proteins lies in positions 4-6. In FBF/RNA complexes, these bases stack directly with one another and turn away from the RNA-binding surface. A short region of FBF is sufficient to impart its unique specificity and lies directly opposite the flipped bases. We suggest that this region imposes a flattened curvature on the protein; hence, the requirement for the additional nucleotide. 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| subjects | Animals Atoms Bacteria Biochemistry Biological Sciences Caenorhabditis elegans - metabolism Caenorhabditis elegans Proteins - chemistry Caenorhabditis elegans Proteins - metabolism Chemical bases Chimeras CRYSTAL STRUCTURE Crystallography Curvature Electrophoretic Mobility Shift Assay Germ cells MAINTENANCE MATERIALS SCIENCE Messenger RNA Models, Molecular Nucleotide sequences PROTEINS Ribonucleic acid RNA RNA, Messenger - metabolism RNA-Binding Proteins - chemistry RNA-Binding Proteins - metabolism SPECIFICITY STEM CELLS TARGETS Two-Hybrid System Techniques Yeasts |
| title | Structural basis for specific recognition of multiple mRNA targets by a PUF regulatory protein |
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