Transcriptional slippage in bacteria: distribution in sequenced genomes and utilization in IS element gene expression

Baranov, Pavel V.; Hammer, Andrew; Zhou, Jiadong; Gesteland, Raymond F.; Atkins, John F.

doi:10.1186/gb-2005-6-3-r25

Cited by 68 publications

(45 citation statements)

References 54 publications

(52 reference statements)

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“…In agreement with the first strategy, there is a significant bias against the occurrence of poly(A) or poly(U) tracts greater than 6–7 nt in coding vs non-coding regions in most bacterial species with A/T rich genomes 30 . Similarly, there are no poly(A) or poly(U) tracts > 6 nt in the T7 genome, and the only occurrence of a U 6 run is at TΦ 34 .…”

Section: Discussionsupporting

confidence: 56%

“…Both T7 and the multisubunit E. coli RNAP have been shown to slip in long poly A and U tracts, and it has been proposed that to prevent frameshifting in vivo the genomes of these organisms have evolved to minimize the average length of such tracts to < 6–7 nt in coding regions 1,30 . The yeast mitochondrial (mt) genome is highly A:T rich and encodes numerous copies of A- and U-tracts of at least 8 nt in length, but is transcribed by an RNAP that consists of a core subunit (Rpo41p) that resembles T7 RNAP 31–33 .…”

Section: Resultsmentioning

confidence: 99%

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The Presence of an RNA:DNA Hybrid That Is Prone to Slippage Promotes Termination by T7 RNA Polymerase

Molodtsov

Anikin

McAllister

2014

Journal of Molecular Biology

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Intrinsic termination signals for multisubunit bacterial RNA polymerases (RNAPs) encode a GC-rich stem-loop structure followed by a polyuridine (poly(U)) tract, and it has been proposed that steric clash of the stem-loop with the exit pore of the RNAP imposes a shearing force on the RNA in the downstream RNA:DNA hybrid, resulting in misalignment of the active site. The structurally unrelated T7 RNAP terminates at a similar type of signal (TΦ), suggesting a common mechanism for termination. In the absence of a hairpin (passive conditions) T7 RNAP slips efficiently in both homopolymeric A and U tracts, and we have found that replacement of the U tract in TΦ with a slippage-prone A tract still allows efficient termination. Under passive conditions, incorporation of a single G residue following a poly(U) tract (which is the situation during termination at TΦ) results in a “locked” complex that is unable to extend the transcript. Our results support a model in which transmission of the shearing force generated by steric clash of the hairpin with the exit pore is promoted by the presence of a slippery tracts downstream, resulting in alterations in the active site and the formation of a locked complex that represents an early step in the termination pathway.

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Section: Discussionsupporting

confidence: 56%

Section: Resultsmentioning

confidence: 99%

The Presence of an RNA:DNA Hybrid That Is Prone to Slippage Promotes Termination by T7 RNA Polymerase

Molodtsov

Anikin

McAllister

2014

Journal of Molecular Biology

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“…The reversion phenomenon is easily induced, and this explains why mutants and revertants have been produced in vitro. On the basis of our data, we think that these mutations resulting in a premature stop codon are unstable, and we prefer to use the name ''split gene'' instead of the previously used terms ''pseudogene'' or ''pseudo-pseudogenes'' (Baranov et al 2005). R. prowazekii therefore is exemplifying the adaptive mutation concept (Rosenberg 2001), i.e., mutations formed in response to an environment.…”

Section: Discussionmentioning

confidence: 96%

Genomic, proteomic, and transcriptomic analysis of virulent and avirulentRickettsia prowazekiireveals its adaptive mutation capabilities

Bechah¹,

Karkouri²,

Mediannikov³

et al. 2010

Genome Res.

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Rickettsia prowazekii, the agent of epidemic typhus, is an obligate intracellular bacterium that is transmitted to human beings by the body louse. Several strains that differ considerably in virulence are recognized, but the genetic basis for these variations has remained unknown since the initial description of the avirulent vaccine strain nearly 70 yr ago. We use a recently developed murine model of epidemic typhus and transcriptomic, proteomic, and genetic techniques to identify the factors associated with virulence. We identified four phenotypes of R. prowazekii that differed in virulence, associated with the up-regulation of antiapoptotic genes or the interferon I pathway in the host cells. Transcriptional and proteomic analyses of R. prowazekii surface protein expression and protein methylation varied with virulence. By sequencing a virulent strain and using comparative genomics, we found hotspots of mutations in homopolymeric tracts of poly(A) and poly(T) in eight genes in an avirulent strain that split and inactivated these genes. These included recO, putative methyltransferase, and exported protein. Passage of the avirulent Madrid E strain in cells or in experimental animals was associated with a cascade of gene reactivations, beginning with recO, that restored the virulent phenotype. An area of genomic plasticity appears to determine virulence in R. prowazekii and represents an example of adaptive mutation for this pathogen.

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“…This is especially evident in the case of the pglA ST3787 and pglA FAM18 alleles, which were associated with levels of disaccharide glycoform expression that were only 20-to 25-fold reduced from the level seen in the pglA N400 background. We propose that these alleles are examples of what have been termed "expressed pseudogenes" (16) or "pseudopseudogenes" (6), in which significant levels of gene product are expressed from out-of-frame alleles. Specifically, the poly(G) stretches contained within these pglA alleles are sequence patterns for nonstandard decoding at the levels of both programmed ribosomal frameshifting and programmed transcriptional realignment (23).…”

Section: Discussionmentioning

confidence: 99%

Hypomorphic Glycosyltransferase Alleles and Recoding at Contingency Loci Influence Glycan Microheterogeneity in the Protein Glycosylation System of Neisseria Species

Johannessen¹,

Koomey²,

Børud³

2012

J. Bacteriol.

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As more bacterial protein glycosylation systems are identified and characterized, a central question that arises is, what governs the prevalence of particular glycans associated with them? In addition, accumulating evidence shows that bacterial protein glycans can be subject to the phenomenon of microheterogeneity, in which variant glycan structures are found at specific attachment sites of a given glycoprotein. Although factors underlying microheterogeneity in reconstituted expression systems have been identified and modeled, those impacting natural systems largely remain enigmatic. On the basis of a sensitive and specific glycan serotyping system, microheterogeneity has been reported for the broad-spectrum, O-linked protein glycosylation system in species within the genus Neisseria. To elucidate the mechanisms involved, a genetic approach was used to identify a hypomorphic allele of pglA (encoding the PglA galactosyltransferase) as a significant contributor to simultaneous expression of multiple glycoforms. Moreover, this phenotype was mapped to a single amino acid polymorphism in PglA. Further analyses revealed that many pglA phase-off variants (containing out-of-frame configurations in simple nucleotide repeats within the open reading frame) were associated with disproportionally high levels of the N,N=-diacetylbacillosamine-Gal disaccharide glycoform generated by PglA. This phenotype is emblematic of nonstandard decoding involving programmed ribosomal frameshifting and/or programmed transcriptional realignment. Together, these findings provide new information regarding the mechanisms of neisserial protein glycan microheterogeneity and the anticipatory nature of contingency loci. P rotein glycosylation systems based on both N-and O-linked modifications are well documented in eubacteria. In addition to the distinctions based on the nature of site attachment, bacterial protein glycosylation systems can be differentiated on the basis of whether they are dedicated to a single class of proteins or target a broad spectrum of protein substrates. These systems can also be classified as to the degree of glycan diversity observed within and between related species. For example, in the type IV pilus (Tfp) O-linked glycosylation in Pseudomonas aeruginosa, some strains utilize the endogenous O-antigen unit found in lipopolysaccharide (LPS; which in itself varies between strains), while others employ D-arabinofuranose moieties synthesized by an apparently dedicated biosynthetic machinery (11, 28). In the N-linked, broad-spectrum protein glycosylation system of Campylobacter jejuni, a conserved heptasaccharide has been presumed to be highly disseminated. Major disparities in protein glycan diversification have been observed for flagellum-associated, O-linked systems, with those in Campylobacter, Helicobacter, and Clostridium exhibiting high levels of intra-and interstrain variation, while the system in P. aeruginosa appears to be limited to two major glycoforms (4,10,13,26). Why protein-associated glycans display high intr...

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Transcriptional slippage in bacteria: distribution in sequenced genomes and utilization in IS element gene expression

Cited by 68 publications

References 54 publications

The Presence of an RNA:DNA Hybrid That Is Prone to Slippage Promotes Termination by T7 RNA Polymerase

The Presence of an RNA:DNA Hybrid That Is Prone to Slippage Promotes Termination by T7 RNA Polymerase

Genomic, proteomic, and transcriptomic analysis of virulent and avirulentRickettsia prowazekiireveals its adaptive mutation capabilities

Hypomorphic Glycosyltransferase Alleles and Recoding at Contingency Loci Influence Glycan Microheterogeneity in the Protein Glycosylation System of Neisseria Species

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