The modular structure of Escherichia coli threonyl‐tRNA synthetase as both an enzyme and a regulator of gene expression
Summary In addition to its role in tRNA aminoacylation, Escherichia coli threonyl‐tRNA synthetase is a regulatory protein which binds a site, called the operator, located in the leader of its own mRNA and inhibits translational initiation by competing with ribosome binding. This work shows that the...
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| Veröffentlicht in: | Molecular microbiology 2003-02, Vol.47 (4), p.961-974 |
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| creator | Caillet, Joël Nogueira, Teresa Masquida, Benoît Winter, Flore Graffe, Monique Dock‐Brégeon, Anne‐Catherine Torres‐Larios, Alfredo Sankaranarayanan, Rajan Westhof, Eric Ehresmann, Bernard Ehresmann, Chantal Romby, Pascale Springer, Mathias |
| description | Summary
In addition to its role in tRNA aminoacylation, Escherichia coli threonyl‐tRNA synthetase is a regulatory protein which binds a site, called the operator, located in the leader of its own mRNA and inhibits translational initiation by competing with ribosome binding. This work shows that the two essential steps of regulation, operator recognition and inhibition of ribosome binding, are performed by different domains of the protein. The catalytic and the C‐terminal domain of the protein are involved in binding the two anticodon arm‐like structures in the operator whereas the N‐terminal domain of the enzyme is responsible for the competition with the ribosome. This is the first demonstration of a modular structure for a translational repressor and is reminiscent of that of transcriptional regulators. The mimicry between the operator and tRNA, suspected on the basis of previous experiments, is further supported by the fact that identical regions of the synthetase recognize both the operator and the tRNA anticodon arm. Based on these results, and recent structural data, we have constructed a computer‐derived molecular model for the operator‐threonyl‐tRNA synthetase complex, which sheds light on several essential aspects of the regulatory mechanism. |
| doi_str_mv | 10.1046/j.1365-2958.2003.03364.x |
| format | Article |
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In addition to its role in tRNA aminoacylation, Escherichia coli threonyl‐tRNA synthetase is a regulatory protein which binds a site, called the operator, located in the leader of its own mRNA and inhibits translational initiation by competing with ribosome binding. This work shows that the two essential steps of regulation, operator recognition and inhibition of ribosome binding, are performed by different domains of the protein. The catalytic and the C‐terminal domain of the protein are involved in binding the two anticodon arm‐like structures in the operator whereas the N‐terminal domain of the enzyme is responsible for the competition with the ribosome. This is the first demonstration of a modular structure for a translational repressor and is reminiscent of that of transcriptional regulators. The mimicry between the operator and tRNA, suspected on the basis of previous experiments, is further supported by the fact that identical regions of the synthetase recognize both the operator and the tRNA anticodon arm. Based on these results, and recent structural data, we have constructed a computer‐derived molecular model for the operator‐threonyl‐tRNA synthetase complex, which sheds light on several essential aspects of the regulatory mechanism.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1046/j.1365-2958.2003.03364.x</identifier><identifier>PMID: 12581352</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Science Ltd</publisher><subject>Binding Sites ; Binding, Competitive ; Biochemistry, Molecular Biology ; Escherichia coli - enzymology ; Escherichia coli - genetics ; Evolution, Molecular ; Gene Expression Regulation, Bacterial ; Genes, Bacterial ; Life Sciences ; Macromolecular Substances ; Models, Molecular ; Molecular Mimicry ; Molecular Structure ; Mutation ; Operator Regions, Genetic ; Protein Structure, Tertiary ; Protein Subunits ; Ribosomes - metabolism ; RNA, Bacterial - chemistry ; RNA, Bacterial - metabolism ; RNA, Messenger - metabolism ; RNA, Transfer, Amino Acyl - chemistry ; RNA, Transfer, Amino Acyl - metabolism ; Threonine-tRNA Ligase - chemistry ; Threonine-tRNA Ligase - genetics ; Threonine-tRNA Ligase - metabolism</subject><ispartof>Molecular microbiology, 2003-02, Vol.47 (4), p.961-974</ispartof><rights>Copyright Blackwell Scientific Publications Ltd. Feb 2003</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5734-bc3c63a88ddc8e1949d9305ec97292912ccbd496ce5b2b24ede570e5430a1bd83</citedby><cites>FETCH-LOGICAL-c5734-bc3c63a88ddc8e1949d9305ec97292912ccbd496ce5b2b24ede570e5430a1bd83</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1046%2Fj.1365-2958.2003.03364.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1046%2Fj.1365-2958.2003.03364.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,780,784,885,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/12581352$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04142408$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Caillet, Joël</creatorcontrib><creatorcontrib>Nogueira, Teresa</creatorcontrib><creatorcontrib>Masquida, Benoît</creatorcontrib><creatorcontrib>Winter, Flore</creatorcontrib><creatorcontrib>Graffe, Monique</creatorcontrib><creatorcontrib>Dock‐Brégeon, Anne‐Catherine</creatorcontrib><creatorcontrib>Torres‐Larios, Alfredo</creatorcontrib><creatorcontrib>Sankaranarayanan, Rajan</creatorcontrib><creatorcontrib>Westhof, Eric</creatorcontrib><creatorcontrib>Ehresmann, Bernard</creatorcontrib><creatorcontrib>Ehresmann, Chantal</creatorcontrib><creatorcontrib>Romby, Pascale</creatorcontrib><creatorcontrib>Springer, Mathias</creatorcontrib><title>The modular structure of Escherichia coli threonyl‐tRNA synthetase as both an enzyme and a regulator of gene expression</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
In addition to its role in tRNA aminoacylation, Escherichia coli threonyl‐tRNA synthetase is a regulatory protein which binds a site, called the operator, located in the leader of its own mRNA and inhibits translational initiation by competing with ribosome binding. This work shows that the two essential steps of regulation, operator recognition and inhibition of ribosome binding, are performed by different domains of the protein. The catalytic and the C‐terminal domain of the protein are involved in binding the two anticodon arm‐like structures in the operator whereas the N‐terminal domain of the enzyme is responsible for the competition with the ribosome. This is the first demonstration of a modular structure for a translational repressor and is reminiscent of that of transcriptional regulators. The mimicry between the operator and tRNA, suspected on the basis of previous experiments, is further supported by the fact that identical regions of the synthetase recognize both the operator and the tRNA anticodon arm. Based on these results, and recent structural data, we have constructed a computer‐derived molecular model for the operator‐threonyl‐tRNA synthetase complex, which sheds light on several essential aspects of the regulatory mechanism.</description><subject>Binding Sites</subject><subject>Binding, Competitive</subject><subject>Biochemistry, Molecular Biology</subject><subject>Escherichia coli - enzymology</subject><subject>Escherichia coli - genetics</subject><subject>Evolution, Molecular</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Genes, Bacterial</subject><subject>Life Sciences</subject><subject>Macromolecular Substances</subject><subject>Models, Molecular</subject><subject>Molecular Mimicry</subject><subject>Molecular Structure</subject><subject>Mutation</subject><subject>Operator Regions, Genetic</subject><subject>Protein Structure, Tertiary</subject><subject>Protein Subunits</subject><subject>Ribosomes - metabolism</subject><subject>RNA, Bacterial - chemistry</subject><subject>RNA, Bacterial - metabolism</subject><subject>RNA, Messenger - metabolism</subject><subject>RNA, Transfer, Amino Acyl - chemistry</subject><subject>RNA, Transfer, Amino Acyl - metabolism</subject><subject>Threonine-tRNA Ligase - chemistry</subject><subject>Threonine-tRNA Ligase - genetics</subject><subject>Threonine-tRNA Ligase - metabolism</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2003</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkc1u1DAURi0EokPhFZDFAolFUv8m9oLFqGpppSmVUJHYWY5zp8koiQc7KZOueASekSch6YyK1A2sbF2f-13bByFMSUqJyE42KeWZTJiWKmWE8JRwnol09wwtHg-eowXRkiRcsW9H6FWMG0IoJxl_iY4ok4pyyRZovKkAt74cGhtw7MPg-iEA9mt8Fl0FoXZVbbHzTY37KoDvxub3z1_9l89LHMeur6C3EbCNuPB9hW2Hobsf26nSldjiALdTcO_DHHgLHWDYbQPEWPvuNXqxtk2EN4f1GH09P7s5vUhW158uT5erxMmci6Rw3GXcKlWWTgHVQpeaEwlO50wzTZlzRSl05kAWrGACSpA5ASk4sbQoFT9GH_a5lW3MNtStDaPxtjYXy5WZa0RQwQRRd3Ri3-_ZbfDfB4i9aevooGlsB36IJueE6umn_wlSlWU5z-fp756AGz-EbnqwoTqTjCipJ0jtIRd8jAHWj_ekxMzCzcbMXs3s1czCzYNws5ta3x7yh6KF8m_jwfAEfNwDP-oGxv8ONldXl_OO_wGZnLqQ</recordid><startdate>200302</startdate><enddate>200302</enddate><creator>Caillet, Joël</creator><creator>Nogueira, Teresa</creator><creator>Masquida, Benoît</creator><creator>Winter, Flore</creator><creator>Graffe, Monique</creator><creator>Dock‐Brégeon, Anne‐Catherine</creator><creator>Torres‐Larios, Alfredo</creator><creator>Sankaranarayanan, Rajan</creator><creator>Westhof, Eric</creator><creator>Ehresmann, Bernard</creator><creator>Ehresmann, Chantal</creator><creator>Romby, Pascale</creator><creator>Springer, Mathias</creator><general>Blackwell Science Ltd</general><general>Blackwell Publishing Ltd</general><general>Wiley</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope></search><sort><creationdate>200302</creationdate><title>The modular structure of Escherichia coli threonyl‐tRNA synthetase as both an enzyme and a regulator of gene expression</title><author>Caillet, Joël ; 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In addition to its role in tRNA aminoacylation, Escherichia coli threonyl‐tRNA synthetase is a regulatory protein which binds a site, called the operator, located in the leader of its own mRNA and inhibits translational initiation by competing with ribosome binding. This work shows that the two essential steps of regulation, operator recognition and inhibition of ribosome binding, are performed by different domains of the protein. The catalytic and the C‐terminal domain of the protein are involved in binding the two anticodon arm‐like structures in the operator whereas the N‐terminal domain of the enzyme is responsible for the competition with the ribosome. This is the first demonstration of a modular structure for a translational repressor and is reminiscent of that of transcriptional regulators. The mimicry between the operator and tRNA, suspected on the basis of previous experiments, is further supported by the fact that identical regions of the synthetase recognize both the operator and the tRNA anticodon arm. Based on these results, and recent structural data, we have constructed a computer‐derived molecular model for the operator‐threonyl‐tRNA synthetase complex, which sheds light on several essential aspects of the regulatory mechanism.</abstract><cop>Oxford, UK</cop><pub>Blackwell Science Ltd</pub><pmid>12581352</pmid><doi>10.1046/j.1365-2958.2003.03364.x</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Molecular microbiology, 2003-02, Vol.47 (4), p.961-974 |
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| source | MEDLINE; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Wiley Free Content; Free Full-Text Journals in Chemistry |
| subjects | Binding Sites Binding, Competitive Biochemistry, Molecular Biology Escherichia coli - enzymology Escherichia coli - genetics Evolution, Molecular Gene Expression Regulation, Bacterial Genes, Bacterial Life Sciences Macromolecular Substances Models, Molecular Molecular Mimicry Molecular Structure Mutation Operator Regions, Genetic Protein Structure, Tertiary Protein Subunits Ribosomes - metabolism RNA, Bacterial - chemistry RNA, Bacterial - metabolism RNA, Messenger - metabolism RNA, Transfer, Amino Acyl - chemistry RNA, Transfer, Amino Acyl - metabolism Threonine-tRNA Ligase - chemistry Threonine-tRNA Ligase - genetics Threonine-tRNA Ligase - metabolism |
| title | The modular structure of Escherichia coli threonyl‐tRNA synthetase as both an enzyme and a regulator of gene expression |
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