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Structural basis of transcription-translation coupling
In bacteria, transcription and translation are coupled processes in which the movement of RNA polymerase (RNAP)-synthesizing messenger RNA (mRNA) is coordinated with the movement of the first ribosome-translating mRNA. Coupling is modulated by the transcription factors NusG (which is thought to brid...
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| Published in: | Science (American Association for the Advancement of Science) 2020-09, Vol.369 (6509), p.1359-1365 |
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| Main Authors: | , , , , , , |
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| container_issue | 6509 |
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| container_title | Science (American Association for the Advancement of Science) |
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| creator | Wang, Chengyuan Molodtsov, Vadim Firlar, Emre Kaelber, Jason T Blaha, Gregor Su, Min Ebright, Richard H |
| description | In bacteria, transcription and translation are coupled processes in which the movement of RNA polymerase (RNAP)-synthesizing messenger RNA (mRNA) is coordinated with the movement of the first ribosome-translating mRNA. Coupling is modulated by the transcription factors NusG (which is thought to bridge RNAP and the ribosome) and NusA. Here, we report cryo-electron microscopy structures of
transcription-translation complexes (TTCs) containing different-length mRNA spacers between RNAP and the ribosome active-center P site. Structures of TTCs containing short spacers show a state incompatible with NusG bridging and NusA binding (TTC-A, previously termed "expressome"). Structures of TTCs containing longer spacers reveal a new state compatible with NusG bridging and NusA binding (TTC-B) and reveal how NusG bridges and NusA binds. We propose that TTC-B mediates NusG- and NusA-dependent transcription-translation coupling. |
| doi_str_mv | 10.1126/science.abb5317 |
| format | article |
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transcription-translation complexes (TTCs) containing different-length mRNA spacers between RNAP and the ribosome active-center P site. Structures of TTCs containing short spacers show a state incompatible with NusG bridging and NusA binding (TTC-A, previously termed "expressome"). Structures of TTCs containing longer spacers reveal a new state compatible with NusG bridging and NusA binding (TTC-B) and reveal how NusG bridges and NusA binds. We propose that TTC-B mediates NusG- and NusA-dependent transcription-translation coupling.</description><identifier>ISSN: 0036-8075</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.abb5317</identifier><identifier>PMID: 32820061</identifier><language>eng</language><publisher>United States: The American Association for the Advancement of Science</publisher><subject>Bacteria ; Binding ; Coupling ; Cryoelectron Microscopy ; DNA-Directed RNA Polymerases - chemistry ; E coli ; Electron microscopy ; Elongated structure ; Escherichia coli - genetics ; Escherichia coli Proteins - chemistry ; Gene Expression Regulation, Bacterial ; Microscopy ; Peptide Elongation Factors - chemistry ; Protein Binding ; Protein Biosynthesis ; Protein Conformation ; RNA polymerase ; RNA, Messenger - chemistry ; Spacers ; Transcription ; Transcription Factors - chemistry ; Transcription, Genetic ; Transcriptional Elongation Factors - chemistry ; Translation</subject><ispartof>Science (American Association for the Advancement of Science), 2020-09, Vol.369 (6509), p.1359-1365</ispartof><rights>Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.</rights><rights>Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c487t-2299b5d9f3bd02847d14222b1d80c82691166f06f6056fbef404b4f54f3dbf303</citedby><cites>FETCH-LOGICAL-c487t-2299b5d9f3bd02847d14222b1d80c82691166f06f6056fbef404b4f54f3dbf303</cites><orcidid>0000-0002-8605-0716 ; 0000-0002-0561-906X ; 0000-0001-7228-0185 ; 0000-0003-3002-4794 ; 0000-0001-8915-7140 ; 0000-0001-9426-1030 ; 0000-0003-0190-6528</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,2884,2885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32820061$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Chengyuan</creatorcontrib><creatorcontrib>Molodtsov, Vadim</creatorcontrib><creatorcontrib>Firlar, Emre</creatorcontrib><creatorcontrib>Kaelber, Jason T</creatorcontrib><creatorcontrib>Blaha, Gregor</creatorcontrib><creatorcontrib>Su, Min</creatorcontrib><creatorcontrib>Ebright, Richard H</creatorcontrib><title>Structural basis of transcription-translation coupling</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>In bacteria, transcription and translation are coupled processes in which the movement of RNA polymerase (RNAP)-synthesizing messenger RNA (mRNA) is coordinated with the movement of the first ribosome-translating mRNA. Coupling is modulated by the transcription factors NusG (which is thought to bridge RNAP and the ribosome) and NusA. Here, we report cryo-electron microscopy structures of
transcription-translation complexes (TTCs) containing different-length mRNA spacers between RNAP and the ribosome active-center P site. Structures of TTCs containing short spacers show a state incompatible with NusG bridging and NusA binding (TTC-A, previously termed "expressome"). Structures of TTCs containing longer spacers reveal a new state compatible with NusG bridging and NusA binding (TTC-B) and reveal how NusG bridges and NusA binds. We propose that TTC-B mediates NusG- and NusA-dependent transcription-translation coupling.</description><subject>Bacteria</subject><subject>Binding</subject><subject>Coupling</subject><subject>Cryoelectron Microscopy</subject><subject>DNA-Directed RNA Polymerases - chemistry</subject><subject>E coli</subject><subject>Electron microscopy</subject><subject>Elongated structure</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli Proteins - chemistry</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Microscopy</subject><subject>Peptide Elongation Factors - chemistry</subject><subject>Protein Binding</subject><subject>Protein Biosynthesis</subject><subject>Protein Conformation</subject><subject>RNA polymerase</subject><subject>RNA, Messenger - chemistry</subject><subject>Spacers</subject><subject>Transcription</subject><subject>Transcription Factors - chemistry</subject><subject>Transcription, Genetic</subject><subject>Transcriptional Elongation Factors - 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chemistry</topic><topic>E coli</topic><topic>Electron microscopy</topic><topic>Elongated structure</topic><topic>Escherichia coli - genetics</topic><topic>Escherichia coli Proteins - chemistry</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Microscopy</topic><topic>Peptide Elongation Factors - chemistry</topic><topic>Protein Binding</topic><topic>Protein Biosynthesis</topic><topic>Protein Conformation</topic><topic>RNA polymerase</topic><topic>RNA, Messenger - chemistry</topic><topic>Spacers</topic><topic>Transcription</topic><topic>Transcription Factors - chemistry</topic><topic>Transcription, Genetic</topic><topic>Transcriptional Elongation Factors - chemistry</topic><topic>Translation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Chengyuan</creatorcontrib><creatorcontrib>Molodtsov, Vadim</creatorcontrib><creatorcontrib>Firlar, Emre</creatorcontrib><creatorcontrib>Kaelber, Jason T</creatorcontrib><creatorcontrib>Blaha, Gregor</creatorcontrib><creatorcontrib>Su, Min</creatorcontrib><creatorcontrib>Ebright, Richard H</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aluminium Industry Abstracts</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Ceramic Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Computer and Information Systems Abstracts</collection><collection>Corrosion Abstracts</collection><collection>Ecology Abstracts</collection><collection>Electronics & Communications Abstracts</collection><collection>Engineered Materials Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Materials Business File</collection><collection>Mechanical & Transportation Engineering Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Engineering Research Database</collection><collection>Aerospace Database</collection><collection>Copper Technical Reference Library</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts Academic</collection><collection>Computer and Information Systems Abstracts Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Science (American Association for the Advancement of Science)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Chengyuan</au><au>Molodtsov, Vadim</au><au>Firlar, Emre</au><au>Kaelber, Jason T</au><au>Blaha, Gregor</au><au>Su, Min</au><au>Ebright, Richard H</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Structural basis of transcription-translation coupling</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><addtitle>Science</addtitle><date>2020-09-11</date><risdate>2020</risdate><volume>369</volume><issue>6509</issue><spage>1359</spage><epage>1365</epage><pages>1359-1365</pages><issn>0036-8075</issn><eissn>1095-9203</eissn><abstract>In bacteria, transcription and translation are coupled processes in which the movement of RNA polymerase (RNAP)-synthesizing messenger RNA (mRNA) is coordinated with the movement of the first ribosome-translating mRNA. Coupling is modulated by the transcription factors NusG (which is thought to bridge RNAP and the ribosome) and NusA. Here, we report cryo-electron microscopy structures of
transcription-translation complexes (TTCs) containing different-length mRNA spacers between RNAP and the ribosome active-center P site. Structures of TTCs containing short spacers show a state incompatible with NusG bridging and NusA binding (TTC-A, previously termed "expressome"). Structures of TTCs containing longer spacers reveal a new state compatible with NusG bridging and NusA binding (TTC-B) and reveal how NusG bridges and NusA binds. We propose that TTC-B mediates NusG- and NusA-dependent transcription-translation coupling.</abstract><cop>United States</cop><pub>The American Association for the Advancement of Science</pub><pmid>32820061</pmid><doi>10.1126/science.abb5317</doi><tpages>7</tpages><orcidid>https://orcid.org/0000-0002-8605-0716</orcidid><orcidid>https://orcid.org/0000-0002-0561-906X</orcidid><orcidid>https://orcid.org/0000-0001-7228-0185</orcidid><orcidid>https://orcid.org/0000-0003-3002-4794</orcidid><orcidid>https://orcid.org/0000-0001-8915-7140</orcidid><orcidid>https://orcid.org/0000-0001-9426-1030</orcidid><orcidid>https://orcid.org/0000-0003-0190-6528</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Bacteria Binding Coupling Cryoelectron Microscopy DNA-Directed RNA Polymerases - chemistry E coli Electron microscopy Elongated structure Escherichia coli - genetics Escherichia coli Proteins - chemistry Gene Expression Regulation, Bacterial Microscopy Peptide Elongation Factors - chemistry Protein Binding Protein Biosynthesis Protein Conformation RNA polymerase RNA, Messenger - chemistry Spacers Transcription Transcription Factors - chemistry Transcription, Genetic Transcriptional Elongation Factors - chemistry Translation |
| title | Structural basis of transcription-translation coupling |
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