Mechanisms of Bacterial Transcription Termination: All Good Things Must End

Ray-Soni, Ananya; Bellecourt, Michael J.; Landick, Robert

doi:10.1146/annurev-biochem-060815-014844

Cited by 301 publications

(371 citation statements)

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“…Transcription of palindromic DNA sequences causes RNA hairpins to form. RNA secondary structure formation within the narrow RNA exit pathway influences the conformation of the flap domain and then in turn causes transcription pausing and termination (Ray-Soni et al, 2016). …”

Section: Introductionmentioning

confidence: 99%

An Introduction to the Structure and Function of the Catalytic Core Enzyme of Escherichia coli RNA Polymerase

Sutherland

Murakami

2018

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RNA polymerase (RNAP) is the essential enzyme responsible for transcribing the genetic information stored in DNA to RNA. Understanding the structure and function of RNAP is important for those who study basic principles in gene expression, such as the mechanisms of transcription and its regulation, as well as translational sciences such as antibiotic development. With over a half-century of investigations, there is a wealth of information available on the structure and function of Escherichia coli RNAP. This review introduces the structural features of E. coli RNAP, organized by subunit, giving information on the function, location, and conservation of these features to early stage investigators who have just started their research of E. coli RNAP.

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Section: Introductionmentioning

confidence: 99%

An Introduction to the Structure and Function of the Catalytic Core Enzyme of Escherichia coli RNA Polymerase

Sutherland

Murakami

2018

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“…The sRNA genes possess a typical Rho-independent or factor-independent or intrinsic transcription terminator encoding a GC-rich RNA hairpin followed by a run of T residues (d'Aubenton Carafa et al 1990;Ray-Soni et al 2016). We demonstrated previously that transcription termination at the sRNA genes is enhanced under stress conditions and thereby contributes to an efficient production of active sRNAs (Morita et al 2015).…”

Section: Introductionmentioning

confidence: 99%

“…This implies that the modulation of the termination position at the Rho-independent terminators of sRNA genes is quite important for biosynthesis of functional sRNAs. The stability of the terminator RNA hairpin and the length of the T residue stretch are known to be major determinants for the efficiency of transcription termination, although DNA sequences around terminators also affect the termination efficiency (Lynn et al 1988;Cheng et al 1991;Reynolds et al 1992;Ray-Soni et al 2016). When the terminator hairpin is too weak, elongating RNA polymerase mostly reads through the terminator, resulting in extended forms of sRNAs, which are nonfunctional (Morita et al 2015).…”

Section: Introductionmentioning

confidence: 99%

Role of the terminator hairpin in the biogenesis of functional Hfq-binding sRNAs

Morita

Nishino

Aiba

2017

RNA

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Rho-independent transcription terminators of the genes encoding bacterial Hfq-binding sRNAs possess a set of seven or more T residues at the 3 ′ ′ ′ ′ ′ end, as noted in previous studies. Here, we have studied the role of the terminator hairpin in the biogenesis of sRNAs focusing on SgrS and RyhB in Escherichia coli. We constructed variant sRNA genes in which the GC-rich inverted repeat sequences are extended to stabilize the terminator hairpins. We demonstrate that the extension of the hairpin stem leads to generation of heterogeneous transcripts in which the poly(U) tail is shortened. The transcripts with shortened poly(U) tails no longer bind to Hfq and lose the ability to repress the target mRNAs. The shortened transcripts are generated in an in vitro transcription system with purified RNA polymerase, indicating that the generation of shortened transcripts is caused by premature transcription termination. We conclude that the terminator structure of sRNA genes is optimized to generate functional sRNAs. Thus, the Rho-independent terminators of sRNA genes possess two common features: a long T residue stretch that is a prerequisite for generation of functional sRNAs and a moderate strength of hairpin structure that ensures the termination at the seventh or longer position within the consecutive T stretch. The modulation of the termination position at the Rho-independent terminators is critical for biosynthesis of functional sRNAs.

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“…In contrast to the role of nucleic acid (NA) base pairing, the contributions of structural changes in RNAP modules and domains to termination remain incompletely described (25,27). A complexity of multiple moving domains and refolding modules is a common feature of macromolecular machines that process information in RNA and DNA.…”

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confidence: 99%

Trigger loop dynamics can explain stimulation of intrinsic termination by bacterial RNA polymerase without terminator hairpin contact

Ray-Soni

Mooney

Landick

2017

Proc. Natl. Acad. Sci. U.S.A.

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In bacteria, intrinsic termination signals cause disassembly of the highly stable elongating transcription complex (EC) over windows of two to three nucleotides after kilobases of RNA synthesis. Intrinsic termination is caused by the formation of a nascent RNA hairpin adjacent to a weak RNA−DNA hybrid within RNA polymerase (RNAP). Although the contributions of RNA and DNA sequences to termination are largely understood, the roles of conformational changes in RNAP are less well described. The polymorphous trigger loop (TL), which folds into the trigger helices to promote nucleotide addition, also is proposed to drive termination by folding into the trigger helices and contacting the terminator hairpin after invasion of the hairpin in the RNAP main cleft [Epshtein V, Cardinale CJ, Ruckenstein AE, Borukhov S, Nudler E (2007) Mol Cell 28:991-1001]. To investigate the contribution of the TL to intrinsic termination, we developed a kinetic assay that distinguishes effects of TL alterations on the rate at which ECs terminate from effects of the TL on the nucleotide addition rate that indirectly affect termination efficiency by altering the time window in which termination can occur. We confirmed that the TL stimulates termination rate, but found that stabilizing either the folded or unfolded TL conformation decreased termination rate. We propose that conformational fluctuations of the TL (TL dynamics), not TL-hairpin contact, aid termination by increasing EC conformational diversity and thus access to favorable termination pathways. We also report that the TL and the TL sequence insertion (SI3) increase overall termination efficiency by stimulating pausing, which increases the flux of ECs into the termination pathway.T ranscription termination is an essential process in all organisms that releases the RNA chain and DNA template from transcribing RNA polymerase (RNAP). Termination prevents unwanted gene expression (1), recycles RNAP for new initiation events (2), and prevents genome-destabilizing collisions with the replication machinery (3). In bacteria, intrinsic termination of the elongating transcription complex (EC) can occur without accessory factors in response to a signal in the DNA and newly synthesized RNA. Intrinsic termination occurs over a 2-to 3-nt window of EC destabilization (4) and is caused by the formation of a GC-rich RNA hairpin in the RNA exit channel of RNAP, immediately upstream of a 3′-terminal, ∼8-nt U-rich RNA tract (U-tract; Fig. 1A). Precise termination of the highly stable EC requires rapid entry into a termination pathway before continued nucleotide addition moves the EC beyond the region of destabilization (4-6).A thermodynamic termination model posits that the relative free energy barriers to termination versus elongation determine the fraction of ECs that terminate; thus, termination efficiency (TE) is kinetically determined by competing rates of nucleotide addition and termination (5, 7) (Fig. 1B). The EC is stabilized by polar and van der Waals contacts between RNAP and (i) the 9-to ...

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Mechanisms of Bacterial Transcription Termination: All Good Things Must End

Cited by 301 publications

References 154 publications

An Introduction to the Structure and Function of the Catalytic Core Enzyme of Escherichia coli RNA Polymerase

An Introduction to the Structure and Function of the Catalytic Core Enzyme of Escherichia coli RNA Polymerase

Role of the terminator hairpin in the biogenesis of functional Hfq-binding sRNAs

Trigger loop dynamics can explain stimulation of intrinsic termination by bacterial RNA polymerase without terminator hairpin contact

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