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RNA extension drives a stepwise displacement of an initiation-factor structural module in initial transcription.

Li L, Molodtsov V, Lin W, Ebright RH, Zhang Y
Proc Natl Acad Sci U S A 117 5801-5809 (2020)
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Cited: 17 times
EuropePMC logo PMID: 32127479

Abstract

All organisms-bacteria, archaea, and eukaryotes-have a transcription initiation factor that contains a structural module that binds within the RNA polymerase (RNAP) active-center cleft and interacts with template-strand single-stranded DNA (ssDNA) in the immediate vicinity of the RNAP active center. This transcription initiation-factor structural module preorganizes template-strand ssDNA to engage the RNAP active center, thereby facilitating binding of initiating nucleotides and enabling transcription initiation from initiating mononucleotides. However, this transcription initiation-factor structural module occupies the path of nascent RNA and thus presumably must be displaced before or during initial transcription. Here, we report four sets of crystal structures of bacterial initially transcribing complexes that demonstrate and define details of stepwise, RNA-extension-driven displacement of the "σ-finger" of the bacterial transcription initiation factor σ. The structures reveal that-for both the primary σ-factor and extracytoplasmic (ECF) σ-factors, and for both 5'-triphosphate RNA and 5'-hydroxy RNA-the "σ-finger" is displaced in stepwise fashion, progressively folding back upon itself, driven by collision with the RNA 5'-end, upon extension of nascent RNA from ∼5 nt to ∼10 nt.

Articles - 6kql mentioned but not cited (1)

  1. RNA extension drives a stepwise displacement of an initiation-factor structural module in initial transcription. Li L, Molodtsov V, Lin W, Ebright RH, Zhang Y. Proc Natl Acad Sci U S A 117 5801-5809 (2020)


Reviews citing this publication (3)

  1. Diverse and unified mechanisms of transcription initiation in bacteria. Chen J, Boyaci H, Campbell EA. Nat Rev Microbiol 19 95-109 (2021)
  2. The Context-Dependent Influence of Promoter Sequence Motifs on Transcription Initiation Kinetics and Regulation. Jensen D, Galburt EA. J Bacteriol 203 e00512-20 (2021)
  3. The σ Subunit-Remodeling Factors: An Emerging Paradigms of Transcription Regulation. Vishwakarma RK, Brodolin K. Front Microbiol 11 1798 (2020)

Articles citing this publication (13)

  1. Structural basis for transcription inhibition by E. coli SspA. Wang F, Shi J, He D, Tong B, Zhang C, Wen A, Zhang Y, Feng Y, Lin W. Nucleic Acids Res 48 9931-9942 (2020)
  2. Temperature effects on RNA polymerase initiation kinetics reveal which open complex initiates and that bubble collapse is stepwise. Plaskon DM, Henderson KL, Felth LC, Molzahn CM, Evensen C, Dyke S, Shkel IA, Record MT. Proc Natl Acad Sci U S A 118 e2021941118 (2021)
  3. Design, Synthesis, and Characterization of TNP-2198, a Dual-Targeted Rifamycin-Nitroimidazole Conjugate with Potent Activity against Microaerophilic and Anaerobic Bacterial Pathogens. Ma Z, He S, Yuan Y, Zhuang Z, Liu Y, Wang H, Chen J, Xu X, Ding C, Molodtsov V, Lin W, Robertson GT, Weiss WJ, Pulse M, Nguyen P, Duncan L, Doyle T, Ebright RH, Lynch AS. J Med Chem 65 4481-4495 (2022)
  4. Structural and mechanistic basis of σ-dependent transcriptional pausing. Pukhrambam C, Molodtsov V, Kooshkbaghi M, Tareen A, Vu H, Skalenko KS, Su M, Yin Z, Winkelman JT, Kinney JB, Ebright RH, Nickels BE. Proc Natl Acad Sci U S A 119 e2201301119 (2022)
  5. Region 4 of the RNA polymerase σ subunit counteracts pausing during initial transcription. Brodolin K, Morichaud Z. J Biol Chem 296 100253 (2021)
  6. Rhodobacter sphaeroides CarD Negatively Regulates Its Own Promoter. Henry KK, Ross W, Gourse RL. J Bacteriol 203 e0021021 (2021)
  7. Structural Insights into Transcription Initiation from De Novo RNA Synthesis to Transitioning into Elongation. Zuo Y, De S, Feng Y, Steitz TA. iScience 23 101445 (2020)
  8. Structural and mechanistic basis of reiterative transcription initiation. Liu Y, Yu L, Pukhrambam C, Winkelman JT, Firlar E, Kaelber JT, Zhang Y, Nickels BE, Ebright RH. Proc Natl Acad Sci U S A 119 e2115746119 (2022)
  9. DomainMapper: Accurate domain structure annotation including those with non-contiguous topologies. Manriquez-Sandoval E, Fried SD. Protein Sci 31 e4465 (2022)
  10. Universal functions of the σ finger in alternative σ factors during transcription initiation by bacterial RNA polymerase. Oguienko A, Petushkov I, Pupov D, Esyunina D, Kulbachinskiy A. RNA Biol 18 2028-2037 (2021)
  11. Identification and Structural Modeling of the RNA Polymerase Omega Subunits in Chlamydiae and Other Obligate Intracellular Bacteria. Cheng A, Wan D, Ghatak A, Wang C, Feng D, Fondell JD, Ebright RH, Fan H. mBio 14 e0349922 (2023)
  12. Step-by-Step Regulation of Productive and Abortive Transcription Initiation by Pyrophosphorolysis. Plaskon D, Evensen C, Henderson K, Palatnik B, Ishikuri T, Wang HC, Doughty S, Thomas Record M. J Mol Biol 434 167621 (2022)
  13. Structural basis of σ54 displacement and promoter escape in bacterial transcription. Gao F, Ye F, Zhang B, Cronin N, Buck M, Zhang X. Proc Natl Acad Sci U S A 121 e2309670120 (2024)


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