Gene Symbol: RRM3
Description: Rrm3p
Alias: RTT104, Rrm3p
Species: Saccharomyces cerevisiae S288c

Top Publications

  1. Ivessa A, Lenzmeier B, Bessler J, Goudsouzian L, Schnakenberg S, Zakian V. The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past nonhistone protein-DNA complexes. Mol Cell. 2003;12:1525-36 pubmed
    ..While replication of most of the yeast genome was not dependent upon Rrm3p, in its absence, replication forks paused and often broke at an estimated 1400 discrete sites, including tRNA ..
  2. Ivessa A, Zhou J, Schulz V, Monson E, Zakian V. Saccharomyces Rrm3p, a 5' to 3' DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev. 2002;16:1383-96 pubmed
    ..This slowing was greatly exacerbated in the absence of RRM3, shown here to encode a 5' to 3' DNA helicase. Rrm3p-dependent fork progression was seen at a modified Chromosome VII-L telomere, at the natural X-bearing Chromosome ..
  3. Gibson D, Aparicio J, Hu F, Aparicio O. Diminished S-phase cyclin-dependent kinase function elicits vital Rad53-dependent checkpoint responses in Saccharomyces cerevisiae. Mol Cell Biol. 2004;24:10208-22 pubmed
    ..Consistent with the notion that decreased S-CDK function creates stress at replication forks, deletion of RRM3 helicase, which facilitates replisome progression, greatly diminished the growth of clb5Delta cells...
  4. Azvolinsky A, Dunaway S, Torres J, Bessler J, Zakian V. The S. cerevisiae Rrm3p DNA helicase moves with the replication fork and affects replication of all yeast chromosomes. Genes Dev. 2006;20:3104-16 pubmed
    The Saccharomyces cerevisiae DNA helicase Rrm3p is needed for normal fork progression through >1000 discrete sites scattered throughout the genome...
  5. Schmidt K, Kolodner R. Suppression of spontaneous genome rearrangements in yeast DNA helicase mutants. Proc Natl Acad Sci U S A. 2006;103:18196-201 pubmed
    Saccharomyces cerevisiae mutants lacking two of the three DNA helicases Sgs1, Srs2, and Rrm3 exhibit slow growth that is suppressed by disrupting homologous recombination...
  6. Sacher M, Pfander B, Hoege C, Jentsch S. Control of Rad52 recombination activity by double-strand break-induced SUMO modification. Nat Cell Biol. 2006;8:1284-90 pubmed
    ..Furthermore, our data indicate that sumoylation becomes particularly relevant for those Rad52 molecules that are engaged in recombination. ..
  7. Mohanty B, Bairwa N, Bastia D. The Tof1p-Csm3p protein complex counteracts the Rrm3p helicase to control replication termination of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 2006;103:897-902 pubmed
    ..checkpoint protein complex of Tof1p and Csm3p that protect stalled forks at Ter sites against the activity of the Rrm3p helicase ("sweepase")...
  8. Fachinetti D, Bermejo R, Cocito A, Minardi S, Katou Y, Kanoh Y, et al. Replication termination at eukaryotic chromosomes is mediated by Top2 and occurs at genomic loci containing pausing elements. Mol Cell. 2010;39:595-605 pubmed publisher
    ..TERs contain fork pausing elements that influence fork progression and merging. The Rrm3 DNA helicase assists fork progression across TERs, counteracting the accumulation of X-shaped structures...
  9. Ivessa A, Zhou J, Zakian V. The Saccharomyces Pif1p DNA helicase and the highly related Rrm3p have opposite effects on replication fork progression in ribosomal DNA. Cell. 2000;100:479-89 pubmed
    ..The Pif1p helicase and the highly related Rrm3p were rDNA associated in vivo. Both proteins affected rDNA replication but had opposing effects on fork progression...

More Information


  1. Tran P, Pohl T, Chen C, Chan A, Pott S, Zakian V. PIF1 family DNA helicases suppress R-loop mediated genome instability at tRNA genes. Nat Commun. 2017;8:15025 pubmed publisher
    Saccharomyces cerevisiae encodes two Pif1 family DNA helicases, Pif1 and Rrm3. Rrm3 promotes DNA replication past stable protein complexes at tRNA genes (tDNAs)...
  2. Esta A, Ma E, Dupaigne P, Maloisel L, Guerois R, Le Cam E, et al. Rad52 sumoylation prevents the toxicity of unproductive Rad51 filaments independently of the anti-recombinase Srs2. PLoS Genet. 2013;9:e1003833 pubmed publisher
    ..This conclusion is strengthened by the finding that Rad52 is often associated with complete Rad51 filaments in vitro...
  3. Dubarry M, Loiodice I, Chen C, Thermes C, Taddei A. Tight protein-DNA interactions favor gene silencing. Genes Dev. 2011;25:1365-70 pubmed publisher
    ..Importantly, lack of the replication fork-associated helicase Rrm3 enhances this induced gene repression...
  4. Beyer T, Weinert T. Ontogeny of Unstable Chromosomes Generated by Telomere Error in Budding Yeast. PLoS Genet. 2016;12:e1006345 pubmed publisher
    ..Defects in Tel1 and in Rrm3, a checkpoint protein kinase with a role in telomere maintenance and a DNA helicase, respectively, synergize ..
  5. Rossi S, Ajazi A, Carotenuto W, Foiani M, Giannattasio M. Rad53-Mediated Regulation of Rrm3 and Pif1 DNA Helicases Contributes to Prevention of Aberrant Fork Transitions under Replication Stress. Cell Rep. 2015;13:80-92 pubmed publisher
    ..Here, we show that Rrm3 and Pif1, DNA helicases assisting fork progression across pausing sites, are detrimental in rad53 mutants ..
  6. Rossi S, Carotenuto W, Giannattasio M. Genome-wide localization of Rrm3 and Pif1 DNA helicases at stalled active and inactive DNA replication forks of Saccharomyces cerevisiae. Genom Data. 2016;7:162-5 pubmed publisher
    ..We present datasets deposited in the gene expression omnibus (GEO) database under accession number GSE68214, which show how the DNA helicases Rrm3 and Pif1 (8) associate to active and inactive DNA replication forks.
  7. Stamenova R, Maxwell P, Kenny A, Curcio M. Rrm3 protects the Saccharomyces cerevisiae genome from instability at nascent sites of retrotransposition. Genetics. 2009;182:711-23 pubmed publisher
    The DNA helicase Rrm3 promotes replication fork progression through >1000 discrete genomic regions and represses the cDNA-mediated mobility of the Ty1 retrotransposon...
  8. Osmundson J, Kumar J, Yeung R, Smith D. Pif1-family helicases cooperatively suppress widespread replication-fork arrest at tRNA genes. Nat Struct Mol Biol. 2017;24:162-170 pubmed publisher
    Saccharomyces cerevisiae expresses two Pif1-family helicases-Pif1 and Rrm3-which have been reported to play distinct roles in numerous nuclear processes...
  9. Matsuda K, Makise M, Sueyasu Y, Takehara M, Asano T, Mizushima T. Yeast two-hybrid analysis of the origin recognition complex of Saccharomyces cerevisiae: interaction between subunits and identification of binding proteins. FEMS Yeast Res. 2007;7:1263-9 pubmed
    ..several proteins that interact with ORC subunits; Sir4p and Mad1p interact with Orc2p; Cac1p and Ykr077wp with Orc3p; Rrm3p and Swi6p with Orc5p; and Mih1p with Orc6p. We discuss roles of these interactions in functions of ORC.
  10. Morohashi H, Maculins T, Labib K. The amino-terminal TPR domain of Dia2 tethers SCF(Dia2) to the replisome progression complex. Curr Biol. 2009;19:1943-9 pubmed publisher
    ..Our findings suggest that the amino-terminal domains of other F box proteins might also play an analogous regulatory role, controlling the localization of the cognate SCF complexes. ..
  11. Schmidt K, Derry K, Kolodner R. Saccharomyces cerevisiae RRM3, a 5' to 3' DNA helicase, physically interacts with proliferating cell nuclear antigen. J Biol Chem. 2002;277:45331-7 pubmed
    ..The first new PCNA-binding protein identified in this manner is the 5' to 3' DNA helicase RRM3. Yeast two-hybrid tests show that N-terminal deletions of RRM3, which remove the PIP-box but leave the helicase ..
  12. Hashash N, Johnson A, Cha R. Regulation of fragile sites expression in budding yeast by MEC1, RRM3 and hydroxyurea. J Cell Sci. 2011;124:181-5 pubmed publisher
    ..Here, we investigated this by examining the combined effects of rrm3?, mec1 and hydroxyurea (HU), three conditions that induce fragile sites, on expression of the replication slow zone ..
  13. Chang M, Bellaoui M, Zhang C, Desai R, Morozov P, Delgado Cruzata L, et al. RMI1/NCE4, a suppressor of genome instability, encodes a member of the RecQ helicase/Topo III complex. EMBO J. 2005;24:2024-33 pubmed
    ..In addition, rmi1Delta strains fail to fully activate Rad53 upon exposure to DNA-damaging agents, suggesting that Rmi1 is also an important part of the Rad53-dependent DNA damage response. ..
  14. Torres J, Schnakenberg S, Zakian V. Saccharomyces cerevisiae Rrm3p DNA helicase promotes genome integrity by preventing replication fork stalling: viability of rrm3 cells requires the intra-S-phase checkpoint and fork restart activities. Mol Cell Biol. 2004;24:3198-212 pubmed
    b>Rrm3p is a 5'-to-3' DNA helicase that helps replication forks traverse protein-DNA complexes. Its absence leads to increased fork stalling and breakage at over 1,000 specific sites located throughout the Saccharomyces cerevisiae genome...
  15. Cheng X, Qin Y, Ivessa A. Loss of mitochondrial DNA under genotoxic stress conditions in the absence of the yeast DNA helicase Pif1p occurs independently of the DNA helicase Rrm3p. Mol Genet Genomics. 2009;281:635-45 pubmed publisher
    ..process of mutant yeast cells lacking the PIF1 DNA helicase is partly rescued in the absence of the DNA helicase RRM3. The rescue effect is likely due to the increase in the deoxynucleoside triphosphates (dNTPs) pool caused by the ..
  16. Fernius J, Marston A. Establishment of cohesion at the pericentromere by the Ctf19 kinetochore subcomplex and the replication fork-associated factor, Csm3. PLoS Genet. 2009;5:e1000629 pubmed publisher
    ..We propose that the Ctf19 complex ensures additional loading of cohesin at centromeres prior to passage of the replication fork, thereby ensuring its incorporation into functional linkages through a process requiring Csm3. ..
  17. Prado F, Aguilera A. Impairment of replication fork progression mediates RNA polII transcription-associated recombination. EMBO J. 2005;24:1267-76 pubmed
    ..The Rrm3 helicase, which is required for replication fork progression through nucleoprotein complexes, facilitates ..
  18. Weitao T, Budd M, Hoopes L, Campbell J. Dna2 helicase/nuclease causes replicative fork stalling and double-strand breaks in the ribosomal DNA of Saccharomyces cerevisiae. J Biol Chem. 2003;278:22513-22 pubmed
  19. Keogh M, Kim J, Downey M, Fillingham J, Chowdhury D, Harrison J, et al. A phosphatase complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery. Nature. 2006;439:497-501 pubmed
    ..The dephosphorylation of gammaH2AX by the HTP-C is necessary for efficient recovery from the DNA damage checkpoint. ..
  20. Zamir L, Zaretsky M, Fridman Y, Ner Gaon H, Rubin E, Aharoni A. Tight coevolution of proliferating cell nuclear antigen (PCNA)-partner interaction networks in fungi leads to interspecies network incompatibility. Proc Natl Acad Sci U S A. 2012;109:E406-14 pubmed publisher
    ..Our results indicate that the coevolution of PPI networks can form functional barriers between fungal species, and thus can promote and fix speciation...
  21. Paeschke K, Bochman M, Garcia P, Cejka P, Friedman K, Kowalczykowski S, et al. Pif1 family helicases suppress genome instability at G-quadruplex motifs. Nature. 2013;497:458-62 pubmed publisher
    ..Furthermore, when expressed in yeast, human PIF1 suppressed both G-quadruplex-associated DNA damage and telomere lengthening. ..
  22. Mirzaei H, Syed S, Kennedy J, Schmidt K. Sgs1 truncations induce genome rearrangements but suppress detrimental effects of BLM overexpression in Saccharomyces cerevisiae. J Mol Biol. 2011;405:877-91 pubmed publisher
    ..The functionality of this chimera suggests that it is the disordered N-terminus, a site of protein binding and posttranslational modification, that confers species specificity to these two RecQ-like proteins. ..
  23. Mohanty B, Bairwa N, Bastia D. Contrasting roles of checkpoint proteins as recombination modulators at Fob1-Ter complexes with or without fork arrest. Eukaryot Cell. 2009;8:487-95 pubmed publisher
    ..The work also showed that the two pathways were Rad52 dependent but Rad51 independent. Since Ter sites occur in the intergenic spacer of rDNA from yeast to humans, the mechanism is likely to be of widespread occurrence. ..
  24. Bessler J, Zakian V. The amino terminus of the Saccharomyces cerevisiae DNA helicase Rrm3p modulates protein function altering replication and checkpoint activity. Genetics. 2004;168:1205-18 pubmed
    ..The Saccharomyces cerevisiae genome encodes two Pif1 family members, Rrm3p and Pif1p, that have very different functions...
  25. Schmidt K, Wu J, Kolodner R. Control of translocations between highly diverged genes by Sgs1, the Saccharomyces cerevisiae homolog of the Bloom's syndrome protein. Mol Cell Biol. 2006;26:5406-20 pubmed
    ..checkpoint proteins Mec3, Rad24, Rad9, or Rfc5, the chromatin assembly factors Cac1 or Asf1, and the DNA helicase Rrm3. The S-phase checkpoint kinase and telomere maintenance factor Tel1, a homolog of the human ataxia telangiectasia (..
  26. Moriel Carretero M, Aguilera A. A postincision-deficient TFIIH causes replication fork breakage and uncovers alternative Rad51- or Pol32-mediated restart mechanisms. Mol Cell. 2010;37:690-701 pubmed publisher
    ..Our results define the genetic and molecular hallmarks of replication fork breakage and restart and bring insights to understand specific NER-related human syndromes. ..
  27. O Rourke T, Doudican N, Zhang H, Eaton J, Doetsch P, Shadel G. Differential involvement of the related DNA helicases Pif1p and Rrm3p in mtDNA point mutagenesis and stability. Gene. 2005;354:86-92 pubmed
    ..Altogether, our results define a novel role for Rrm3p in mitochondrial function and indicate that Pif1p and Rrm3p influence a common process (or processes) involved in ..
  28. Schmidt K, Kolodner R. Requirement of Rrm3 helicase for repair of spontaneous DNA lesions in cells lacking Srs2 or Sgs1 helicase. Mol Cell Biol. 2004;24:3213-26 pubmed
    The Rrm3 DNA helicase of Saccharomyces cerevisiae interacts with proliferating cell nuclear antigen and is required for replication fork progression through ribosomal DNA repeats and subtelomeric and telomeric DNA...
  29. Chen Y, Yang C, Li R, Zeng R, Zhou J. Def1p is involved in telomere maintenance in budding yeast. J Biol Chem. 2005;280:24784-91 pubmed
    Saccharomyces Rrm3p, a member of Pif1 5'-3' DNA helicase subfamily, helps replication forks traverse protein-DNA complexes, including the telomere. Here we have identified an Rrm3p interaction protein known to be Def1p...
  30. Schmidt K, Viebranz E, Harris L, Mirzaei Souderjani H, Syed S, Medicus R. Defects in DNA lesion bypass lead to spontaneous chromosomal rearrangements and increased cell death. Eukaryot Cell. 2010;9:315-24 pubmed publisher
  31. Wyse B, Oshidari R, Rowlands H, Abbasi S, Yankulov K. RRM3 regulates epigenetic conversions in Saccharomyces cerevisiae in conjunction with Chromatin Assembly Factor I. Nucleus. 2016;7:405-14 pubmed publisher
    ..Finally, we demonstrate that Rrm3p and CAF-I compete for the binding to the DNA replication clamp PCNA (Proliferating Cell Nuclear Antigen)...
  32. Muñoz Galvan S, Garcia Rubio M, Ortega P, Ruiz J, Jimeno S, Pardo B, et al. A new role for Rrm3 in repair of replication-born DNA breakage by sister chromatid recombination. PLoS Genet. 2017;13:e1006781 pubmed publisher
    ..The Rrm3 helicase is a replisome component that promotes replication upon fork stalling, accumulates at highly transcribed ..
  33. Kaniak Golik A, Kuberska R, Dzierzbicki P, Sledziewska Gojska E. Activation of Dun1 in response to nuclear DNA instability accounts for the increase in mitochondrial point mutations in Rad27/FEN1 deficient S. cerevisiae. PLoS ONE. 2017;12:e0180153 pubmed publisher
    ..Consistently, we show that mitochondrial mutations occurring more frequently in yeast devoid of Rrm3, a DNA helicase involved in rDNA replication, are also dependent on Dun1...
  34. Bairwa N, Mohanty B, Stamenova R, Curcio M, Bastia D. The intra-S phase checkpoint protein Tof1 collaborates with the helicase Rrm3 and the F-box protein Dia2 to maintain genome stability in Saccharomyces cerevisiae. J Biol Chem. 2011;286:2445-54 pubmed publisher
    The intra-S phase checkpoint protein complex Tof1/Csm3 of Saccharomyces cerevisiae antagonizes Rrm3 helicase to modulate replication fork arrest not only at the replication termini of rDNA but also at strong nonhistone protein binding ..
  35. Syed S, Desler C, Rasmussen L, Schmidt K. A Novel Rrm3 Function in Restricting DNA Replication via an Orc5-Binding Domain Is Genetically Separable from Rrm3 Function as an ATPase/Helicase in Facilitating Fork Progression. PLoS Genet. 2016;12:e1006451 pubmed publisher
    ..Here, we report that Rrm3 associates with a subset of replication origins and controls DNA synthesis during replication stress...
  36. Koren A, Soifer I, Barkai N. MRC1-dependent scaling of the budding yeast DNA replication timing program. Genome Res. 2010;20:781-90 pubmed publisher
    ..Mrc1 emerges as a regulator of this robustness of the replication program. ..
  37. Branzei D, Sollier J, Liberi G, Zhao X, Maeda D, Seki M, et al. Ubc9- and mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell. 2006;127:509-22 pubmed
    ..Our results indicate that Ubc9- and Mms21-mediated sumoylation functions as a regulatory mechanism, different from that of replication checkpoints, to prevent pathological accumulation of cruciform structures at damaged forks. ..
  38. Szyjka S, Viggiani C, Aparicio O. Mrc1 is required for normal progression of replication forks throughout chromatin in S. cerevisiae. Mol Cell. 2005;19:691-7 pubmed
    ..Analysis of genetic interactions with Rrm3, a DNA helicase required to resolve paused forks, indicates that Mrc1 checkpoint signaling is dispensable for the ..
  39. Taylor S, Zhang H, Eaton J, Rodeheffer M, Lebedeva M, O Rourke T, et al. The conserved Mec1/Rad53 nuclear checkpoint pathway regulates mitochondrial DNA copy number in Saccharomyces cerevisiae. Mol Biol Cell. 2005;16:3010-8 pubmed
    ..Our previous investigations of the related DNA helicases Pif1p and Rrm3p uncovered a role for these factors and the conserved Mec1/Rad53 nuclear checkpoint pathway in mtDNA mutagenesis ..
  40. Menolfi D, Delamarre A, Lengronne A, Pasero P, Branzei D. Essential Roles of the Smc5/6 Complex in Replication through Natural Pausing Sites and Endogenous DNA Damage Tolerance. Mol Cell. 2015;60:835-46 pubmed publisher
  41. Torres J, Bessler J, Zakian V. Local chromatin structure at the ribosomal DNA causes replication fork pausing and genome instability in the absence of the S. cerevisiae DNA helicase Rrm3p. Genes Dev. 2004;18:498-503 pubmed
    Lack of the yeast Rrm3p DNA helicase causes replication defects at multiple sites within ribosomal DNA (rDNA), including at the replication fork barrier (RFB). These defects were unaltered in rrm3 sir2 cells...
  42. Ohya T, Arai H, Kubota Y, Shinagawa H, Hishida T. A SUMO-like domain protein, Esc2, is required for genome integrity and sister chromatid cohesion in Saccharomyces cerevisiae. Genetics. 2008;180:41-50 pubmed publisher
    ..in sister chromatid cohesion and have a reduced life span, and these effects are enhanced by deletion of the RRM3 gene that is a Pif1-like DNA helicase...
  43. Putnam C, Hayes T, Kolodner R. Post-replication repair suppresses duplication-mediated genome instability. PLoS Genet. 2010;6:e1000933 pubmed publisher
    ..Our analysis is consistent with models in which PRR prevents replication damage from becoming double strand breaks (DSBs) and/or regulates the activity of HR on DSBs. ..