Yeast Helicase Pif1 Unwinds RNA:DNA Hybrids with Higher Processivity than DNA:DNA Duplexes

Chib, Shubeena; Byrd, Alicia K.; Raney, Kevin D.

doi:10.1074/jbc.m115.688648

Cited by 40 publications

(44 citation statements)

References 56 publications

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“…The homolog of PcrA in E. coli, UvrD, has been shown to unwind RNA:DNA hybrids in vitro (Matson, 1989). In yeast, the PcrA homolog Pif1 has been shown to preferentially unwind RNA:DNA hybrids over DNA:DNA hybrids (Boulé and Zakian, 2007;Chib et al, 2016). Interestingly however, despite the established role of helicases in R-loop processing, here we find that helicases are not sufficient to process excess R-loop formation, specifically in head-on genes.…”

Section: Discussioncontrasting

confidence: 62%

Head-on replication-transcription collisions lead to formation of life threatening R-loops

et al. 2017

Preprint

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Encounters between transcription and DNA replication machineries lead to conflicts that shape genomes, influence evolution, and lead to genetic diseases in humans. Although unclear why, head-on transcription (lagging strand genes) is especially disruptive to replication, increases DNA breaks, and promotes mutagenesis. Here, we show that head-on replication-transcription conflicts lead to pervasive RNA:DNA hybrid formation in Bacillus subtilis. We find that replication beyond head-on conflict regions requires the activity of a RNA:DNA hybrid processing enzyme, RNase HIII. Remarkably, pervasive RNA:DNA hybrid formation at head-on genes completely stops replication and inhibits gene expression in a replication-dependent manner. Accordingly, we find that resolution of head-on conflicts by RNase HIII is crucial for survival upon exposure to various stresses, as many stress response genes are encoded head-on to replication. We conclude that R-loops, RNA:DNA hybrids formed outside of the transcription bubble, exacerbate head-on replication-transcription conflicts, thereby threatening life, especially upon exposure to environmental stresses.

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Section: Discussioncontrasting

confidence: 62%

Head-on replication-transcription collisions lead to formation of life threatening R-loops

et al. 2017

Preprint

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“…However, R-loops must be problematic to some degree even in low-bias organisms such as E. coli given that modulating RNase HI levels can impact survival defects associated with rDNA inversions (Boubakri et al, 2010; Zhang et al, 2014). Interestingly, accessory helicases have been implicated in R-loop processing and conflict resolution across species (Boubakri et al, 2010; Merrikh et al, 2015; Matson, 1989; Boulé and Zakian, 2007; Chib et al, 2016), but in the case of head-on genes, our data suggest that they are not sufficient to clear the R-loops. Perhaps this is the reason for the presence of RNase HIII in organisms with higher co-orientation biases.…”

Section: Discussionmentioning

confidence: 57%

Replication-Transcription Conflicts Generate R-Loops that Orchestrate Bacterial Stress Survival and Pathogenesis

Lang

Hall

Merrikh

et al. 2017

Cell

197

287

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SUMMARY Replication-transcription collisions shape genomes, influence evolution, and promote genetic diseases. Although unclear why, head-on transcription (lagging strand genes) is especially disruptive to replication and promotes genomic instability. Here, we find that head-on collisions promote R-loop formation in Bacillus subtilis. We show that pervasive R-loop formation at head-on collision regions completely blocks replication, elevates mutagenesis, and inhibits gene expression. Accordingly, the activity of the R-loop processing enzyme RNase HIII at collision regions is crucial for stress survival in B. subtilis, as many stress response genes are head-on to replication. Remarkably, without RNase HIII, the ability of the intracellular pathogen Listeria monocytogenes to infect and replicate in hosts is weakened significantly, most likely because many virulence genes are head-on to replication. We conclude that the detrimental effects of head-on collisions stem primarily from excessive R-loop formation and that the resolution of these structures is critical for bacterial stress survival and pathogenesis.

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“…[31]). ScPif1 is more active on forked DNA molecules and even more active on RNA:DNA hybrids, which it unwinds efficiently even under single cycle conditions [71–73]. Likewise, ScPif1 efficiently unwinds a variety of G4 structures (but not all [74]), and the rate of this unwinding is not affected measurably by the presence of a DNA trap [36,72,75].…”

Section: Biochemical Functions Of Pif1 Family Helicases Provide Himentioning

confidence: 99%

Getting it done at the ends: Pif1 family DNA helicases and telomeres

Geronimo

Zakian

2016

DNA Repair

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It is widely appreciated that the ends of linear DNA molecules cannot be fully replicated by the conventional replication apparatus. Less well known is that semi-conservative replication of telomeric DNA also presents problems for DNA replication. These problems likely arise from the atypical chromatin structure of telomeres, the GC-richness of telomeric DNA that makes it prone to forming DNA secondary structures, and from RNA-DNA hybrids, formed by transcripts of one or both DNA strands. Given the different aspects of telomeres that complicate their replication, it is not surprising that multiple DNA helicases promote replication of telomeric DNA. This review focuses on one such class of DNA helicases, the Pif1 family of 5′–3′ DNA helicases. In budding and fission yeasts, Pif1 family helicases impact both telomerase-mediated and semi-conservative replication of telomeric DNA as well as recombination-mediated telomere lengthening.

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Yeast Helicase Pif1 Unwinds RNA:DNA Hybrids with Higher Processivity than DNA:DNA Duplexes

Cited by 40 publications

References 56 publications

Head-on replication-transcription collisions lead to formation of life threatening R-loops

Head-on replication-transcription collisions lead to formation of life threatening R-loops

Replication-Transcription Conflicts Generate R-Loops that Orchestrate Bacterial Stress Survival and Pathogenesis

Getting it done at the ends: Pif1 family DNA helicases and telomeres

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