An NTP-driven mechanism for the nucleotide addition cycle of Escherichia coli RNA polymerase during transcription
The elementary steps of transcription as catalyzed by E. coli RNA polymerase during one and two rounds of the nucleotide addition cycle (NAC) were resolved in rapid kinetic studies. Modelling of stopped-flow kinetic data of pyrophosphate release in a coupled enzyme assay during one round of the NAC...
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| description | The elementary steps of transcription as catalyzed by E. coli RNA polymerase during one and two rounds of the nucleotide addition cycle (NAC) were resolved in rapid kinetic studies. Modelling of stopped-flow kinetic data of pyrophosphate release in a coupled enzyme assay during one round of the NAC indicates that the rate of pyrophosphate release is significantly less than that for nucleotide incorporation. Upon modelling of the stopped-flow kinetic data for pyrophosphate release during two rounds of the NAC, it was observed that the presence of the next nucleotide for incorporation increases the rate of release of the first pyrophosphate equivalent; incorrect nucleotides for incorporation had no effect on the rate of pyrophosphate release. Although the next nucleotide for incorporation increases the rate of pyrophosphate release, it is still significantly less than the rate of incorporation of the first nucleotide. The results from the stopped-flow kinetic studies were confirmed by using quench-flow followed by thin-layer chromatography (QF-TLC) with only the first nucleotide for incorporation labeled on the gamma phosphate with .sup.32 P to monitor pyrophosphate release. Collectively, the results are consistent with an NTP-driven model for the NAC in which the binding of the next cognate nucleotide for incorporation causes a synergistic conformational change in the enzyme that triggers the more rapid release of pyrophosphate, translocation of the enzyme along the DNA template strand and nucleotide incorporation. |
| doi_str_mv | 10.1371/journal.pone.0273746 |
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Modelling of stopped-flow kinetic data of pyrophosphate release in a coupled enzyme assay during one round of the NAC indicates that the rate of pyrophosphate release is significantly less than that for nucleotide incorporation. Upon modelling of the stopped-flow kinetic data for pyrophosphate release during two rounds of the NAC, it was observed that the presence of the next nucleotide for incorporation increases the rate of release of the first pyrophosphate equivalent; incorrect nucleotides for incorporation had no effect on the rate of pyrophosphate release. Although the next nucleotide for incorporation increases the rate of pyrophosphate release, it is still significantly less than the rate of incorporation of the first nucleotide. The results from the stopped-flow kinetic studies were confirmed by using quench-flow followed by thin-layer chromatography (QF-TLC) with only the first nucleotide for incorporation labeled on the gamma phosphate with .sup.32 P to monitor pyrophosphate release. Collectively, the results are consistent with an NTP-driven model for the NAC in which the binding of the next cognate nucleotide for incorporation causes a synergistic conformational change in the enzyme that triggers the more rapid release of pyrophosphate, translocation of the enzyme along the DNA template strand and nucleotide incorporation.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0273746</identifier><language>eng</language><publisher>San Francisco: Public Library of Science</publisher><subject>Addition polymerization ; Analysis ; Biology and Life Sciences ; Chromatography ; Deoxyribonucleic acid ; DNA ; DNA-directed RNA polymerase ; E coli ; Enzymes ; Escherichia coli infections ; Genetic transcription ; Medicine and Health Sciences ; Methods ; Modelling ; Nucleotides ; Physical Sciences ; Prevention ; Research and Analysis Methods ; Ribonucleic acid ; Risk factors ; RNA ; RNA polymerase ; Simulation ; Thin layer chromatography ; Transcription factors ; Translocation</subject><ispartof>PloS one, 2022-10, Vol.17 (10), p.e0273746-e0273746</ispartof><rights>COPYRIGHT 2022 Public Library of Science</rights><rights>2022 Johnson et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2022 Johnson et al 2022 Johnson et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c618t-348be2301704a560ba7d499015dada2cd46d94ac09467c5807f119c16af223ee3</cites><orcidid>0000-0003-4595-9066</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9595533/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9595533/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,2103,2929,23871,27929,27930,53796,53798</link.rule.ids></links><search><contributor>Menéndez-Arias, Luis</contributor><creatorcontrib>Johnson, Ronald S</creatorcontrib><creatorcontrib>Strausbauch, Mark</creatorcontrib><creatorcontrib>McCloud, Christopher</creatorcontrib><title>An NTP-driven mechanism for the nucleotide addition cycle of Escherichia coli RNA polymerase during transcription</title><title>PloS one</title><description>The elementary steps of transcription as catalyzed by E. coli RNA polymerase during one and two rounds of the nucleotide addition cycle (NAC) were resolved in rapid kinetic studies. Modelling of stopped-flow kinetic data of pyrophosphate release in a coupled enzyme assay during one round of the NAC indicates that the rate of pyrophosphate release is significantly less than that for nucleotide incorporation. Upon modelling of the stopped-flow kinetic data for pyrophosphate release during two rounds of the NAC, it was observed that the presence of the next nucleotide for incorporation increases the rate of release of the first pyrophosphate equivalent; incorrect nucleotides for incorporation had no effect on the rate of pyrophosphate release. Although the next nucleotide for incorporation increases the rate of pyrophosphate release, it is still significantly less than the rate of incorporation of the first nucleotide. The results from the stopped-flow kinetic studies were confirmed by using quench-flow followed by thin-layer chromatography (QF-TLC) with only the first nucleotide for incorporation labeled on the gamma phosphate with .sup.32 P to monitor pyrophosphate release. Collectively, the results are consistent with an NTP-driven model for the NAC in which the binding of the next cognate nucleotide for incorporation causes a synergistic conformational change in the enzyme that triggers the more rapid release of pyrophosphate, translocation of the enzyme along the DNA template strand and nucleotide incorporation.</description><subject>Addition polymerization</subject><subject>Analysis</subject><subject>Biology and Life Sciences</subject><subject>Chromatography</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA-directed RNA polymerase</subject><subject>E coli</subject><subject>Enzymes</subject><subject>Escherichia coli infections</subject><subject>Genetic transcription</subject><subject>Medicine and Health Sciences</subject><subject>Methods</subject><subject>Modelling</subject><subject>Nucleotides</subject><subject>Physical Sciences</subject><subject>Prevention</subject><subject>Research and Analysis Methods</subject><subject>Ribonucleic acid</subject><subject>Risk factors</subject><subject>RNA</subject><subject>RNA polymerase</subject><subject>Simulation</subject><subject>Thin layer chromatography</subject><subject>Transcription 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Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Johnson, Ronald S</au><au>Strausbauch, Mark</au><au>McCloud, Christopher</au><au>Menéndez-Arias, Luis</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>An NTP-driven mechanism for the nucleotide addition cycle of Escherichia coli RNA polymerase during transcription</atitle><jtitle>PloS one</jtitle><date>2022-10-25</date><risdate>2022</risdate><volume>17</volume><issue>10</issue><spage>e0273746</spage><epage>e0273746</epage><pages>e0273746-e0273746</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The elementary steps of transcription as catalyzed by E. coli RNA polymerase during one and two rounds of the nucleotide addition cycle (NAC) were resolved in rapid kinetic studies. Modelling of stopped-flow kinetic data of pyrophosphate release in a coupled enzyme assay during one round of the NAC indicates that the rate of pyrophosphate release is significantly less than that for nucleotide incorporation. Upon modelling of the stopped-flow kinetic data for pyrophosphate release during two rounds of the NAC, it was observed that the presence of the next nucleotide for incorporation increases the rate of release of the first pyrophosphate equivalent; incorrect nucleotides for incorporation had no effect on the rate of pyrophosphate release. Although the next nucleotide for incorporation increases the rate of pyrophosphate release, it is still significantly less than the rate of incorporation of the first nucleotide. The results from the stopped-flow kinetic studies were confirmed by using quench-flow followed by thin-layer chromatography (QF-TLC) with only the first nucleotide for incorporation labeled on the gamma phosphate with .sup.32 P to monitor pyrophosphate release. Collectively, the results are consistent with an NTP-driven model for the NAC in which the binding of the next cognate nucleotide for incorporation causes a synergistic conformational change in the enzyme that triggers the more rapid release of pyrophosphate, translocation of the enzyme along the DNA template strand and nucleotide incorporation.</abstract><cop>San Francisco</cop><pub>Public Library of Science</pub><doi>10.1371/journal.pone.0273746</doi><tpages>e0273746</tpages><orcidid>https://orcid.org/0000-0003-4595-9066</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Addition polymerization Analysis Biology and Life Sciences Chromatography Deoxyribonucleic acid DNA DNA-directed RNA polymerase E coli Enzymes Escherichia coli infections Genetic transcription Medicine and Health Sciences Methods Modelling Nucleotides Physical Sciences Prevention Research and Analysis Methods Ribonucleic acid Risk factors RNA RNA polymerase Simulation Thin layer chromatography Transcription factors Translocation |
| title | An NTP-driven mechanism for the nucleotide addition cycle of Escherichia coli RNA polymerase during transcription |
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