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      Rrm3 and Pif1 division of labor during replication through leading and lagging strand G-quadruplex

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          Abstract

          Members of the conserved Pif1 family of 5′-3′ DNA helicases can unwind G4s and mitigate their negative impact on genome stability. In Saccharomyces cerevisiae, two Pif1 family members, Pif1 and Rrm3, contribute to the suppression of genomic instability at diverse regions including telomeres, centromeres and tRNA genes. While Pif1 can resolve lagging strand G4s in vivo, little is known regarding Rrm3 function at G4s and its cooperation with Pif1 for G4 replication. Here, we monitored replication through G4 sequences in real time to show that Rrm3 is essential for efficient replisome progression through G4s located on the leading strand template, but not on the lagging strand. We found that Rrm3 importance for replication through G4s is dependent on its catalytic activity and its N-terminal unstructured region. Overall, we show that Rrm3 and Pif1 exhibit a division of labor that enables robust replication fork progression through leading and lagging strand G4s, respectively.

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          Highly accurate protein structure prediction with AlphaFold

          John Jumper, Richard Evans, Alexander Pritzel … (2021)
          Proteins are essential to life, and understanding their structure can facilitate a mechanistic understanding of their function. Through an enormous experimental effort 1 – 4 , the structures of around 100,000 unique proteins have been determined 5 , but this represents a small fraction of the billions of known protein sequences 6 , 7 . Structural coverage is bottlenecked by the months to years of painstaking effort required to determine a single protein structure. Accurate computational approaches are needed to address this gap and to enable large-scale structural bioinformatics. Predicting the three-dimensional structure that a protein will adopt based solely on its amino acid sequence—the structure prediction component of the ‘protein folding problem’ 8 —has been an important open research problem for more than 50 years 9 . Despite recent progress 10 – 14 , existing methods fall far short of atomic accuracy, especially when no homologous structure is available. Here we provide the first computational method that can regularly predict protein structures with atomic accuracy even in cases in which no similar structure is known. We validated an entirely redesigned version of our neural network-based model, AlphaFold, in the challenging 14th Critical Assessment of protein Structure Prediction (CASP14) 15 , demonstrating accuracy competitive with experimental structures in a majority of cases and greatly outperforming other methods. Underpinning the latest version of AlphaFold is a novel machine learning approach that incorporates physical and biological knowledge about protein structure, leveraging multi-sequence alignments, into the design of the deep learning algorithm. AlphaFold predicts protein structures with an accuracy competitive with experimental structures in the majority of cases using a novel deep learning architecture.
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            DNA replication through G-quadruplex motifs is promoted by the Saccharomyces cerevisiae Pif1 DNA helicase.

            Katrin Paeschke, John A Capra, Virginia Zakian (2011)
            G-quadruplex (G4) DNA structures are extremely stable four-stranded secondary structures held together by noncanonical G-G base pairs. Genome-wide chromatin immunoprecipitation was used to determine the in vivo binding sites of the multifunctional Saccharomyces cerevisiae Pif1 DNA helicase, a potent unwinder of G4 structures in vitro. G4 motifs were a significant subset of the high-confidence Pif1-binding sites. Replication slowed in the vicinity of these motifs, and they were prone to breakage in Pif1-deficient cells, whereas non-G4 Pif1-binding sites did not show this behavior. Introducing many copies of G4 motifs caused slow growth in replication-stressed Pif1-deficient cells, which was relieved by spontaneous mutations that eliminated their ability to form G4 structures, bind Pif1, slow DNA replication, and stimulate DNA breakage. These data suggest that G4 structures form in vivo and that they are resolved by Pif1 to prevent replication fork stalling and DNA breakage. Copyright © 2011 Elsevier Inc. All rights reserved.
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              Prevalence of quadruplexes in the human genome

              Julian Huppert, Shankar Balasubramanian (2005)
              Guanine-rich DNA sequences of a particular form have the ability to fold into four-stranded structures called G-quadruplexes. In this paper, we present a working rule to predict which primary sequences can form this structure, and describe a search algorithm to identify such sequences in genomic DNA. We count the number of quadruplexes found in the human genome and compare that with the figure predicted by modelling DNA as a Bernoulli stream or as a Markov chain, using windows of various sizes. We demonstrate that the distribution of loop lengths is significantly different from what would be expected in a random case, providing an indication of the number of potentially relevant quadruplex-forming sequences. In particular, we show that there is a significant repression of quadruplexes in the coding strand of exonic regions, which suggests that quadruplex-forming patterns are disfavoured in sequences that will form RNA.
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                Author and article information

                Contributors
                Mor Varon
                Daniel Dovrat
                Jonathan Heuzé:
                ORCID: https://orcid.org/0009-0008-2870-521X
                Ioannis Tsirkas
                Saurabh P Singh
                Philippe Pasero:
                ORCID: https://orcid.org/0000-0001-5891-0822
                Roberto Galletto
                Amir Aharoni:
                ORCID: https://orcid.org/0000-0003-2701-6996
                Journal
                Journal ID (nlm-ta): Nucleic Acids Res
                Journal ID (iso-abbrev): Nucleic Acids Res
                Journal ID (publisher-id): nar
                Title: Nucleic Acids Research
                Publisher: Oxford University Press
                ISSN (Print): 0305-1048
                ISSN (Electronic): 1362-4962
                Publication date Collection: 28 February 2024
                Publication date (Electronic): 20 December 2023
                Publication date PMC-release: 20 December 2023
                Volume: 52
                Issue: 4
                Pages: 1753-1762
                Affiliations
                Department of Life Sciences and the National Institute for Biotechnology in the Negev, Ben-Gurion University of the Negev , Be’er Sheva 84105, Israel
                Department of Life Sciences and the National Institute for Biotechnology in the Negev, Ben-Gurion University of the Negev , Be’er Sheva 84105, Israel
                Institut de Génétique Humaine, CNRS, Université de Montpellier, Equipe Labellisée Ligue Contre le Cancer , 34396 Montpellier, France
                Department of Life Sciences and the National Institute for Biotechnology in the Negev, Ben-Gurion University of the Negev , Be’er Sheva 84105, Israel
                Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine , St. Louis, MO 63110, USA
                Institut de Génétique Humaine, CNRS, Université de Montpellier, Equipe Labellisée Ligue Contre le Cancer , 34396 Montpellier, France
                Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine , St. Louis, MO 63110, USA
                Department of Life Sciences and the National Institute for Biotechnology in the Negev, Ben-Gurion University of the Negev , Be’er Sheva 84105, Israel
                Author notes
                To whom correspondence should be addressed. Tel: +972 8 6472645; Email: aaharoni@ 123456bgu.ac.il
                Author information
                https://orcid.org/0009-0008-2870-521X
                https://orcid.org/0000-0001-5891-0822
                https://orcid.org/0000-0003-2701-6996
                Article
                Publisher ID: gkad1205
                DOI: 10.1093/nar/gkad1205
                PMC ID: 10899776
                PubMed ID: 38117984
                SO-VID: 6d75cf2f-3fe4-486c-ae6e-ceed00b0fa69
                Copyright © © The Author(s) 2023. Published by Oxford University Press on behalf of Nucleic Acids Research.
                License:

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Date accepted : 06 December 2023
                Date revision received : 03 December 2023
                Date received : 17 January 2023
                Page count
                Pages: 10
                Funding
                Funded by: Israeli Science foundation;
                Award ID: 707/21
                Funded by: Binational Science Foundation;
                Award ID: 2019617
                Award ID: 2021737
                Funded by: National Institutes of Health, DOI 10.13039/100000002;
                Award ID: 1R35GM139508
                Categories
                Subject: AcademicSubjects/SCI00010
                Subject: Genome Integrity, Repair and Replication

                ScienceOpen disciplines: Genetics
                Data availability:
                ScienceOpen disciplines: Genetics

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