Checkpoint phosphorylation sites on budding yeast Rif1 protect nascent DNA from degradation by Sgs1-Dna2
In budding yeast the Rif1 protein is important for protecting nascent DNA at blocked replication forks, but the mechanism has been unclear. Here we show that budding yeast Rif1 must interact with Protein Phosphatase 1 to protect nascent DNA. In the absence of Rif1, removal of either Dna2 or Sgs1 pre...
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| Veröffentlicht in: | PLoS genetics 2023-11, Vol.19 (11), p.e1011044-e1011044 |
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| creator | Gali, Vamsi Krishna Monerawela, Chandre Laksir, Yassine Hiraga, Shin-Ichiro Donaldson, Anne D |
| description | In budding yeast the Rif1 protein is important for protecting nascent DNA at blocked replication forks, but the mechanism has been unclear. Here we show that budding yeast Rif1 must interact with Protein Phosphatase 1 to protect nascent DNA. In the absence of Rif1, removal of either Dna2 or Sgs1 prevents nascent DNA degradation, implying that Rif1 protects nascent DNA by targeting Protein Phosphatase 1 to oppose degradation by the Sgs1-Dna2 nuclease-helicase complex. This functional role for Rif1 is conserved from yeast to human cells. Yeast Rif1 was previously identified as a target of phosphorylation by the Tel1/Mec1 checkpoint kinases, but the importance of this phosphorylation has been unclear. We find that nascent DNA protection depends on a cluster of Tel1/Mec1 consensus phosphorylation sites in the Rif1 protein sequence, indicating that the intra-S phase checkpoint acts to protect nascent DNA through Rif1 phosphorylation. Our observations uncover the pathway by which budding yeast Rif1 stabilises newly synthesised DNA, highlighting the crucial role Rif1 plays in maintaining genome stability from lower eukaryotes to humans. |
| doi_str_mv | 10.1371/journal.pgen.1011044 |
| format | Article |
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Here we show that budding yeast Rif1 must interact with Protein Phosphatase 1 to protect nascent DNA. In the absence of Rif1, removal of either Dna2 or Sgs1 prevents nascent DNA degradation, implying that Rif1 protects nascent DNA by targeting Protein Phosphatase 1 to oppose degradation by the Sgs1-Dna2 nuclease-helicase complex. This functional role for Rif1 is conserved from yeast to human cells. Yeast Rif1 was previously identified as a target of phosphorylation by the Tel1/Mec1 checkpoint kinases, but the importance of this phosphorylation has been unclear. We find that nascent DNA protection depends on a cluster of Tel1/Mec1 consensus phosphorylation sites in the Rif1 protein sequence, indicating that the intra-S phase checkpoint acts to protect nascent DNA through Rif1 phosphorylation. Our observations uncover the pathway by which budding yeast Rif1 stabilises newly synthesised DNA, highlighting the crucial role Rif1 plays in maintaining genome stability from lower eukaryotes to humans.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1011044</identifier><identifier>PMID: 37956214</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amino acid sequence ; Binding proteins ; Biodegradation ; Brewer's yeast ; Cell cycle ; Cell Cycle Checkpoints ; Cells ; Chemical properties ; Conserved sequence ; Deoxyribonucleic acid ; DNA ; DNA biosynthesis ; DNA helicase ; DNA Helicases - metabolism ; DNA Replication ; Genetic aspects ; Genetic research ; Genomes ; Genomic Instability ; Genomics ; Kinases ; Nuclease ; Nucleotide sequence ; Phosphatase ; Phosphatases ; Phosphoprotein phosphatase ; Phosphorylation ; Physiological aspects ; Protection and preservation ; Protein phosphatase ; Proteins ; Proteolysis ; Replication forks ; Repressor Proteins - metabolism ; RNA Helicases - metabolism ; S phase ; Saccharomyces cerevisiae - cytology ; Saccharomyces cerevisiae - metabolism ; Saccharomyces cerevisiae Proteins - metabolism ; Telomere-Binding Proteins - metabolism ; Yeast</subject><ispartof>PLoS genetics, 2023-11, Vol.19 (11), p.e1011044-e1011044</ispartof><rights>Copyright: © 2023 Gali et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 Gali et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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Here we show that budding yeast Rif1 must interact with Protein Phosphatase 1 to protect nascent DNA. In the absence of Rif1, removal of either Dna2 or Sgs1 prevents nascent DNA degradation, implying that Rif1 protects nascent DNA by targeting Protein Phosphatase 1 to oppose degradation by the Sgs1-Dna2 nuclease-helicase complex. This functional role for Rif1 is conserved from yeast to human cells. Yeast Rif1 was previously identified as a target of phosphorylation by the Tel1/Mec1 checkpoint kinases, but the importance of this phosphorylation has been unclear. We find that nascent DNA protection depends on a cluster of Tel1/Mec1 consensus phosphorylation sites in the Rif1 protein sequence, indicating that the intra-S phase checkpoint acts to protect nascent DNA through Rif1 phosphorylation. 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Academic</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gali, Vamsi Krishna</au><au>Monerawela, Chandre</au><au>Laksir, Yassine</au><au>Hiraga, Shin-Ichiro</au><au>Donaldson, Anne D</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Checkpoint phosphorylation sites on budding yeast Rif1 protect nascent DNA from degradation by Sgs1-Dna2</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2023-11-13</date><risdate>2023</risdate><volume>19</volume><issue>11</issue><spage>e1011044</spage><epage>e1011044</epage><pages>e1011044-e1011044</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>In budding yeast the Rif1 protein is important for protecting nascent DNA at blocked replication forks, but the mechanism has been unclear. Here we show that budding yeast Rif1 must interact with Protein Phosphatase 1 to protect nascent DNA. In the absence of Rif1, removal of either Dna2 or Sgs1 prevents nascent DNA degradation, implying that Rif1 protects nascent DNA by targeting Protein Phosphatase 1 to oppose degradation by the Sgs1-Dna2 nuclease-helicase complex. This functional role for Rif1 is conserved from yeast to human cells. Yeast Rif1 was previously identified as a target of phosphorylation by the Tel1/Mec1 checkpoint kinases, but the importance of this phosphorylation has been unclear. We find that nascent DNA protection depends on a cluster of Tel1/Mec1 consensus phosphorylation sites in the Rif1 protein sequence, indicating that the intra-S phase checkpoint acts to protect nascent DNA through Rif1 phosphorylation. Our observations uncover the pathway by which budding yeast Rif1 stabilises newly synthesised DNA, highlighting the crucial role Rif1 plays in maintaining genome stability from lower eukaryotes to humans.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>37956214</pmid><doi>10.1371/journal.pgen.1011044</doi><tpages>e1011044</tpages><orcidid>https://orcid.org/0000-0001-7842-8136</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Amino acid sequence Binding proteins Biodegradation Brewer's yeast Cell cycle Cell Cycle Checkpoints Cells Chemical properties Conserved sequence Deoxyribonucleic acid DNA DNA biosynthesis DNA helicase DNA Helicases - metabolism DNA Replication Genetic aspects Genetic research Genomes Genomic Instability Genomics Kinases Nuclease Nucleotide sequence Phosphatase Phosphatases Phosphoprotein phosphatase Phosphorylation Physiological aspects Protection and preservation Protein phosphatase Proteins Proteolysis Replication forks Repressor Proteins - metabolism RNA Helicases - metabolism S phase Saccharomyces cerevisiae - cytology Saccharomyces cerevisiae - metabolism Saccharomyces cerevisiae Proteins - metabolism Telomere-Binding Proteins - metabolism Yeast |
| title | Checkpoint phosphorylation sites on budding yeast Rif1 protect nascent DNA from degradation by Sgs1-Dna2 |
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