RRM3_YEAST
ID RRM3_YEAST Reviewed; 723 AA.
AC P38766; D3DKX8;
DT 01-FEB-1995, integrated into UniProtKB/Swiss-Prot.
DT 01-FEB-1995, sequence version 1.
DT 03-AUG-2022, entry version 178.
DE RecName: Full=ATP-dependent DNA helicase RRM3 {ECO:0000255|HAMAP-Rule:MF_03177};
DE EC=3.6.4.12 {ECO:0000255|HAMAP-Rule:MF_03177};
DE AltName: Full=Regulation of Ty1 transposition protein 104;
DE AltName: Full=rDNA recombination mutation protein 3 {ECO:0000255|HAMAP-Rule:MF_03177};
GN Name=RRM3 {ECO:0000255|HAMAP-Rule:MF_03177}; Synonyms=RTT104;
GN OrderedLocusNames=YHR031C;
OS Saccharomyces cerevisiae (strain ATCC 204508 / S288c) (Baker's yeast).
OC Eukaryota; Fungi; Dikarya; Ascomycota; Saccharomycotina; Saccharomycetes;
OC Saccharomycetales; Saccharomycetaceae; Saccharomyces.
OX NCBI_TaxID=559292;
RN [1]
RP NUCLEOTIDE SEQUENCE [LARGE SCALE GENOMIC DNA].
RC STRAIN=ATCC 204508 / S288c;
RX PubMed=8091229; DOI=10.1126/science.8091229;
RA Johnston M., Andrews S., Brinkman R., Cooper J., Ding H., Dover J., Du Z.,
RA Favello A., Fulton L., Gattung S., Geisel C., Kirsten J., Kucaba T.,
RA Hillier L.W., Jier M., Johnston L., Langston Y., Latreille P., Louis E.J.,
RA Macri C., Mardis E., Menezes S., Mouser L., Nhan M., Rifkin L., Riles L.,
RA St Peter H., Trevaskis E., Vaughan K., Vignati D., Wilcox L., Wohldman P.,
RA Waterston R., Wilson R., Vaudin M.;
RT "Complete nucleotide sequence of Saccharomyces cerevisiae chromosome
RT VIII.";
RL Science 265:2077-2082(1994).
RN [2]
RP GENOME REANNOTATION.
RC STRAIN=ATCC 204508 / S288c;
RX PubMed=24374639; DOI=10.1534/g3.113.008995;
RA Engel S.R., Dietrich F.S., Fisk D.G., Binkley G., Balakrishnan R.,
RA Costanzo M.C., Dwight S.S., Hitz B.C., Karra K., Nash R.S., Weng S.,
RA Wong E.D., Lloyd P., Skrzypek M.S., Miyasato S.R., Simison M., Cherry J.M.;
RT "The reference genome sequence of Saccharomyces cerevisiae: Then and now.";
RL G3 (Bethesda) 4:389-398(2014).
RN [3]
RP FUNCTION.
RX PubMed=8293975; DOI=10.1093/genetics/135.3.711;
RA Keil R.L., McWilliams A.D.;
RT "A gene with specific and global effects on recombination of sequences from
RT tandemly repeated genes in Saccharomyces cerevisiae.";
RL Genetics 135:711-718(1993).
RN [4]
RP FUNCTION.
RX PubMed=10693764; DOI=10.1016/s0092-8674(00)80683-2;
RA Ivessa A.S., Zhou J.-Q., Zakian V.A.;
RT "The Saccharomyces Pif1p DNA helicase and the highly related Rrm3p have
RT opposite effects on replication fork progression in ribosomal DNA.";
RL Cell 100:479-489(2000).
RN [5]
RP FUNCTION.
RX PubMed=11779788; DOI=10.1093/genetics/159.4.1449;
RA Scholes D.T., Banerjee M., Bowen B., Curcio M.J.;
RT "Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have
RT conserved roles in genome maintenance.";
RL Genetics 159:1449-1465(2001).
RN [6]
RP FUNCTION, AND DNA-BINDING.
RX PubMed=12050116; DOI=10.1101/gad.982902;
RA Ivessa A.S., Zhou J.Q., Schulz V.P., Monson E.K., Zakian V.A.;
RT "Saccharomyces Rrm3p, a 5' to 3' DNA helicase that promotes replication
RT fork progression through telomeric and subtelomeric DNA.";
RL Genes Dev. 16:1383-1396(2002).
RN [7]
RP INTERACTION WITH POL30, AND MUTAGENESIS OF PHE-41 AND PHE-42.
RX PubMed=12239216; DOI=10.1074/jbc.m207263200;
RA Schmidt K.H., Derry K.L., Kolodner R.D.;
RT "Saccharomyces cerevisiae RRM3, a 5' to 3' DNA helicase, physically
RT interacts with proliferating cell nuclear antigen.";
RL J. Biol. Chem. 277:45331-45337(2002).
RN [8]
RP FUNCTION.
RX PubMed=12686542; DOI=10.1074/jbc.m301610200;
RA Weitao T., Budd M., Hoopes L.L., Campbell J.L.;
RT "Dna2 helicase/nuclease causes replicative fork stalling and double-strand
RT breaks in the ribosomal DNA of Saccharomyces cerevisiae.";
RL J. Biol. Chem. 278:22513-22522(2003).
RN [9]
RP FUNCTION.
RX PubMed=14690605; DOI=10.1016/s1097-2765(03)00456-8;
RA Ivessa A.S., Lenzmeier B.A., Bessler J.B., Goudsouzian L.K.,
RA Schnakenberg S.L., Zakian V.A.;
RT "The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past
RT nonhistone protein-DNA complexes.";
RL Mol. Cell 12:1525-1536(2003).
RN [10]
RP LEVEL OF PROTEIN EXPRESSION [LARGE SCALE ANALYSIS].
RX PubMed=14562106; DOI=10.1038/nature02046;
RA Ghaemmaghami S., Huh W.-K., Bower K., Howson R.W., Belle A., Dephoure N.,
RA O'Shea E.K., Weissman J.S.;
RT "Global analysis of protein expression in yeast.";
RL Nature 425:737-741(2003).
RN [11]
RP FUNCTION.
RX PubMed=15037547; DOI=10.1101/gad.1154704;
RA Torres J.Z., Bessler J.B., Zakian V.A.;
RT "Local chromatin structure at the ribosomal DNA causes replication fork
RT pausing and genome instability in the absence of the S. cerevisiae DNA
RT helicase Rrm3p.";
RL Genes Dev. 18:498-503(2004).
RN [12]
RP FUNCTION, AND DOMAIN.
RX PubMed=15579680; DOI=10.1534/genetics.104.028035;
RA Bessler J.B., Zakian V.A.;
RT "The amino terminus of the Saccharomyces cerevisiae DNA helicase Rrm3p
RT modulates protein function altering replication and checkpoint activity.";
RL Genetics 168:1205-1218(2004).
RN [13]
RP FUNCTION.
RX PubMed=15060144; DOI=10.1128/mcb.24.8.3198-3212.2004;
RA Torres J.Z., Schnakenberg S.L., Zakian V.A.;
RT "Saccharomyces cerevisiae Rrm3p DNA helicase promotes genome integrity by
RT preventing replication fork stalling: viability of rrm3 cells requires the
RT intra-S-phase checkpoint and fork restart activities.";
RL Mol. Cell. Biol. 24:3198-3212(2004).
RN [14]
RP FUNCTION.
RX PubMed=15060145; DOI=10.1128/mcb.24.8.3213-3226.2004;
RA Schmidt K.H., Kolodner R.D.;
RT "Requirement of Rrm3 helicase for repair of spontaneous DNA lesions in
RT cells lacking Srs2 or Sgs1 helicase.";
RL Mol. Cell. Biol. 24:3213-3226(2004).
RN [15]
RP FUNCTION.
RX PubMed=15082794; DOI=10.1128/mcb.24.9.4019-4031.2004;
RA Makovets S., Herskowitz I., Blackburn E.H.;
RT "Anatomy and dynamics of DNA replication fork movement in yeast telomeric
RT regions.";
RL Mol. Cell. Biol. 24:4019-4031(2004).
RN [16]
RP FUNCTION.
RX PubMed=15542831; DOI=10.1128/mcb.24.23.10208-10222.2004;
RA Gibson D.G., Aparicio J.G., Hu F., Aparicio O.M.;
RT "Diminished S-phase cyclin-dependent kinase function elicits vital Rad53-
RT dependent checkpoint responses in Saccharomyces cerevisiae.";
RL Mol. Cell. Biol. 24:10208-10222(2004).
RN [17]
RP FUNCTION.
RX PubMed=15775982; DOI=10.1038/sj.emboj.7600602;
RA Prado F., Aguilera A.;
RT "Impairment of replication fork progression mediates RNA polII
RT transcription-associated recombination.";
RL EMBO J. 24:1267-1276(2005).
RN [18]
RP FUNCTION.
RX PubMed=15907372; DOI=10.1016/j.gene.2005.03.031;
RA O'Rourke T.W., Doudican N.A., Zhang H., Eaton J.S., Doetsch P.W.,
RA Shadel G.S.;
RT "Differential involvement of the related DNA helicases Pif1p and Rrm3p in
RT mtDNA point mutagenesis and stability.";
RL Gene 354:86-92(2005).
RN [19]
RP RECRUITMENT TO PAUSED REPLISOME.
RX PubMed=16103218; DOI=10.1101/gad.337205;
RA Calzada A., Hodgson B., Kanemaki M., Bueno A., Labib K.;
RT "Molecular anatomy and regulation of a stable replisome at a paused
RT eukaryotic DNA replication fork.";
RL Genes Dev. 19:1905-1919(2005).
RN [20]
RP INTERACTION WITH DEF1.
RX PubMed=15863512; DOI=10.1074/jbc.m413562200;
RA Chen Y.B., Yang C.P., Li R.X., Zeng R., Zhou J.Q.;
RT "Def1p is involved in telomere maintenance in budding yeast.";
RL J. Biol. Chem. 280:24784-24791(2005).
RN [21]
RP FUNCTION.
RX PubMed=15829566; DOI=10.1091/mbc.e05-01-0053;
RA Taylor S.D., Zhang H., Eaton J.S., Rodeheffer M.S., Lebedeva M.A.,
RA O'rourke T.W., Siede W., Shadel G.S.;
RT "The conserved Mec1/Rad53 nuclear checkpoint pathway regulates
RT mitochondrial DNA copy number in Saccharomyces cerevisiae.";
RL Mol. Biol. Cell 16:3010-3018(2005).
RN [22]
RP FUNCTION.
RX PubMed=16137624; DOI=10.1016/j.molcel.2005.06.037;
RA Szyjka S.J., Viggiani C.J., Aparicio O.M.;
RT "Mrc1 is required for normal progression of replication forks throughout
RT chromatin in S. cerevisiae.";
RL Mol. Cell 19:691-697(2005).
RN [23]
RP FUNCTION.
RX PubMed=16327883; DOI=10.1371/journal.pgen.0010061;
RA Budd M.E., Tong A.H., Polaczek P., Peng X., Boone C., Campbell J.L.;
RT "A network of multi-tasking proteins at the DNA replication fork preserves
RT genome stability.";
RL PLoS Genet. 1:E61-E61(2005).
RN [24]
RP FUNCTION.
RX PubMed=16631586; DOI=10.1016/j.cub.2006.02.071;
RA Luke B., Versini G., Jaquenoud M., Zaidi I.W., Kurz T., Pintard L.,
RA Pasero P., Peter M.;
RT "The cullin Rtt101p promotes replication fork progression through damaged
RT DNA and natural pause sites.";
RL Curr. Biol. 16:786-792(2006).
RN [25]
RP FUNCTION, AND DNA-BINDING.
RX PubMed=17114583; DOI=10.1101/gad.1478906;
RA Azvolinsky A., Dunaway S., Torres J.Z., Bessler J.B., Zakian V.A.;
RT "The S. cerevisiae Rrm3p DNA helicase moves with the replication fork and
RT affects replication of all yeast chromosomes.";
RL Genes Dev. 20:3104-3116(2006).
RN [26]
RP PHOSPHORYLATION [LARGE SCALE ANALYSIS] AT SER-64, AND IDENTIFICATION BY
RP MASS SPECTROMETRY [LARGE SCALE ANALYSIS].
RX PubMed=18407956; DOI=10.1074/mcp.m700468-mcp200;
RA Albuquerque C.P., Smolka M.B., Payne S.H., Bafna V., Eng J., Zhou H.;
RT "A multidimensional chromatography technology for in-depth phosphoproteome
RT analysis.";
RL Mol. Cell. Proteomics 7:1389-1396(2008).
RN [27]
RP FUNCTION.
RX PubMed=19168400; DOI=10.1016/j.dnarep.2008.12.010;
RA de la Loza M.C., Wellinger R.E., Aguilera A.;
RT "Stimulation of direct-repeat recombination by RNA polymerase III
RT transcription.";
RL DNA Repair 8:620-626(2009).
RN [28]
RP FUNCTION.
RX PubMed=19414561; DOI=10.1534/genetics.109.104208;
RA Stamenova R., Maxwell P.H., Kenny A.E., Curcio M.J.;
RT "Rrm3 protects the Saccharomyces cerevisiae genome from instability at
RT nascent sites of retrotransposition.";
RL Genetics 182:711-723(2009).
RN [29]
RP FUNCTION.
RX PubMed=21087929; DOI=10.1074/jbc.m110.189456;
RA Bairwa N.K., Mohanty B.K., Stamenova R., Curcio M.J., Bastia D.;
RT "The intra-S phase checkpoint protein Tof1 collaborates with the helicase
RT Rrm3 and the F-box protein Dia2 to maintain genome stability in
RT Saccharomyces cerevisiae.";
RL J. Biol. Chem. 286:2445-2454(2011).
RN [30]
RP FUNCTION.
RX PubMed=21172804; DOI=10.1242/jcs.077313;
RA Hashash N., Johnson A.L., Cha R.S.;
RT "Regulation of fragile sites expression in budding yeast by MEC1, RRM3 and
RT hydroxyurea.";
RL J. Cell Sci. 124:181-185(2011).
RN [31]
RP FUNCTION IN G4-UNWINDING.
RX PubMed=23657261; DOI=10.1038/nature12149;
RA Paeschke K., Bochman M.L., Garcia P.D., Cejka P., Friedman K.L.,
RA Kowalczykowski S.C., Zakian V.A.;
RT "Pif1 family helicases suppress genome instability at G-quadruplex
RT motifs.";
RL Nature 497:458-462(2013).
CC -!- FUNCTION: 5' to 3' DNA replicative helicase recruited to paused
CC replisomes to promote fork progression throughout nonhistone protein-
CC DNA complexes, naturally occurring impediments that are encountered in
CC each S phase where replication forks pauses. Needed for normal fork
CC progression through over 1000 discrete sites scattered throughout the
CC genome, like rDNA, tRNA genes, centromeres, active replication origins,
CC or transcriptional silencers. Required for timely replication of the
CC telomere and subtelomeric DNA and for wild-type levels of telomeric
CC silencing. Involved in regulation of Ty1 transposition and protects the
CC genome from instability at nascent sites of retrotransposition.
CC Involved in DNA repair during stalled replication fork, regulation of
CC fragile sites expression and essential for genome stability. Also plays
CC a role in mtDNA replication. Has G-quadruplex (G4) unwinding activity
CC and can suppress G4-induced genome instability when PIF1 levels are
CC low. {ECO:0000269|PubMed:10693764, ECO:0000269|PubMed:11779788,
CC ECO:0000269|PubMed:12050116, ECO:0000269|PubMed:12686542,
CC ECO:0000269|PubMed:14690605, ECO:0000269|PubMed:15037547,
CC ECO:0000269|PubMed:15060144, ECO:0000269|PubMed:15060145,
CC ECO:0000269|PubMed:15082794, ECO:0000269|PubMed:15542831,
CC ECO:0000269|PubMed:15579680, ECO:0000269|PubMed:15775982,
CC ECO:0000269|PubMed:15829566, ECO:0000269|PubMed:15907372,
CC ECO:0000269|PubMed:16137624, ECO:0000269|PubMed:16327883,
CC ECO:0000269|PubMed:16631586, ECO:0000269|PubMed:17114583,
CC ECO:0000269|PubMed:19168400, ECO:0000269|PubMed:19414561,
CC ECO:0000269|PubMed:21087929, ECO:0000269|PubMed:21172804,
CC ECO:0000269|PubMed:23657261, ECO:0000269|PubMed:8293975}.
CC -!- CATALYTIC ACTIVITY:
CC Reaction=ATP + H2O = ADP + H(+) + phosphate; Xref=Rhea:RHEA:13065,
CC ChEBI:CHEBI:15377, ChEBI:CHEBI:15378, ChEBI:CHEBI:30616,
CC ChEBI:CHEBI:43474, ChEBI:CHEBI:456216; EC=3.6.4.12;
CC Evidence={ECO:0000255|HAMAP-Rule:MF_03177};
CC -!- SUBUNIT: Interacts with DEF1 and POL30. {ECO:0000269|PubMed:12239216,
CC ECO:0000269|PubMed:15863512}.
CC -!- SUBCELLULAR LOCATION: Nucleus. Chromosome, telomere.
CC -!- DOMAIN: The N-terminal part (residues 1 to 249) is essential for
CC function and confers locus specificity. {ECO:0000269|PubMed:15579680}.
CC -!- MISCELLANEOUS: Present with 656 molecules/cell in log phase SD medium.
CC {ECO:0000269|PubMed:14562106}.
CC -!- SIMILARITY: Belongs to the helicase family. {ECO:0000305}.
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DR EMBL; U00062; AAB68913.1; -; Genomic_DNA.
DR EMBL; BK006934; DAA06722.1; -; Genomic_DNA.
DR PIR; S46744; S46744.
DR RefSeq; NP_011896.1; NM_001179161.1.
DR AlphaFoldDB; P38766; -.
DR SMR; P38766; -.
DR BioGRID; 36462; 341.
DR DIP; DIP-2858N; -.
DR ELM; P38766; -.
DR IntAct; P38766; 5.
DR MINT; P38766; -.
DR STRING; 4932.YHR031C; -.
DR iPTMnet; P38766; -.
DR MaxQB; P38766; -.
DR PaxDb; P38766; -.
DR PRIDE; P38766; -.
DR EnsemblFungi; YHR031C_mRNA; YHR031C; YHR031C.
DR GeneID; 856426; -.
DR KEGG; sce:YHR031C; -.
DR SGD; S000001073; RRM3.
DR VEuPathDB; FungiDB:YHR031C; -.
DR eggNOG; KOG0987; Eukaryota.
DR HOGENOM; CLU_001613_0_2_1; -.
DR InParanoid; P38766; -.
DR OMA; PIMLCWA; -.
DR BioCyc; YEAST:G3O-31091-MON; -.
DR PRO; PR:P38766; -.
DR Proteomes; UP000002311; Chromosome VIII.
DR RNAct; P38766; protein.
DR GO; GO:0000781; C:chromosome, telomeric region; IEA:UniProtKB-SubCell.
DR GO; GO:0043596; C:nuclear replication fork; IDA:SGD.
DR GO; GO:0005657; C:replication fork; IDA:SGD.
DR GO; GO:0043139; F:5'-3' DNA helicase activity; IEA:UniProtKB-UniRule.
DR GO; GO:0005524; F:ATP binding; IEA:UniProtKB-UniRule.
DR GO; GO:0016887; F:ATP hydrolysis activity; IEA:RHEA.
DR GO; GO:0003678; F:DNA helicase activity; IDA:SGD.
DR GO; GO:0051880; F:G-quadruplex DNA binding; IEA:UniProtKB-UniRule.
DR GO; GO:0032508; P:DNA duplex unwinding; IBA:GO_Central.
DR GO; GO:0006281; P:DNA repair; IEA:UniProtKB-UniRule.
DR GO; GO:0006260; P:DNA replication; IMP:SGD.
DR GO; GO:0044806; P:G-quadruplex DNA unwinding; IMP:SGD.
DR GO; GO:0000002; P:mitochondrial genome maintenance; IGI:SGD.
DR GO; GO:0098781; P:ncRNA transcription; IMP:SGD.
DR GO; GO:0097046; P:replication fork progression beyond termination site; IMP:SGD.
DR GO; GO:0071932; P:replication fork reversal; IGI:SGD.
DR GO; GO:0000723; P:telomere maintenance; IEA:InterPro.
DR Gene3D; 3.40.50.300; -; 1.
DR HAMAP; MF_03176; PIF1; 1.
DR HAMAP; MF_03177; RRM3; 1.
DR InterPro; IPR003593; AAA+_ATPase.
DR InterPro; IPR010285; DNA_helicase_pif1-like.
DR InterPro; IPR027417; P-loop_NTPase.
DR InterPro; IPR028880; Rrm3.
DR Pfam; PF05970; PIF1; 1.
DR SMART; SM00382; AAA; 1.
DR SUPFAM; SSF52540; SSF52540; 2.
PE 1: Evidence at protein level;
KW ATP-binding; Chromosome; DNA damage; DNA repair; DNA-binding; Helicase;
KW Hydrolase; Nucleotide-binding; Nucleus; Phosphoprotein; Reference proteome;
KW Telomere.
FT CHAIN 1..723
FT /note="ATP-dependent DNA helicase RRM3"
FT /id="PRO_0000101986"
FT DNA_BIND 682..701
FT /evidence="ECO:0000255|HAMAP-Rule:MF_03177"
FT REGION 1..31
FT /note="Disordered"
FT /evidence="ECO:0000256|SAM:MobiDB-lite"
FT REGION 61..101
FT /note="Disordered"
FT /evidence="ECO:0000256|SAM:MobiDB-lite"
FT COMPBIAS 78..97
FT /note="Polar residues"
FT /evidence="ECO:0000256|SAM:MobiDB-lite"
FT BINDING 254..261
FT /ligand="ATP"
FT /ligand_id="ChEBI:CHEBI:30616"
FT /evidence="ECO:0000255|HAMAP-Rule:MF_03177"
FT MOD_RES 64
FT /note="Phosphoserine"
FT /evidence="ECO:0007744|PubMed:18407956"
FT MUTAGEN 41
FT /note="F->A,D: Reduces the interaction with POL30; when
FT associated with A-42 or D-42."
FT /evidence="ECO:0000269|PubMed:12239216"
FT MUTAGEN 42
FT /note="F->A,D: Reduces the interaction with POL30; when
FT associated with A-42 or D-42."
FT /evidence="ECO:0000269|PubMed:12239216"
SQ SEQUENCE 723 AA; 81581 MW; 8E0010ABB870CAB6 CRC64;
MFRSHASGNK KQWSKRSSNG STPAASASGS HAYRQQTLSS FFMGCGKKSA AASKNSTTII
DLESGDEGNR NITAPPRPRL IRNNSSSLFS QSQGSFGDDD PDAEFKKLVD VPRLNSYKKS
SRSLSMTSSL HKTASASTTQ KTYHFDEDET LREVTSVKSN SRQLSFTSTI NIEDSSMKLS
TDSERPAKRS KPSMEFQGLK LTVPKKIKPL LRKTVSNMDS MNHRSASSPV VLTMEQERVV
NLIVKKRTNV FYTGSAGTGK SVILQTIIRQ LSSLYGKESI AITASTGLAA VTIGGSTLHK
WSGIGIGNKT IDQLVKKIQS QKDLLAAWRY TKVLIIDEIS MVDGNLLDKL EQIARRIRKN
DDPFGGIQLV LTGDFFQLPP VAKKDEHNVV KFCFESEMWK RCIQKTILLT KVFRQQDNKL
IDILNAIRYG ELTVDIAKTI RNLNRDIDYA DGIAPTELYA TRREVELSNV KKLQSLPGDL
YEFKAVDNAP ERYQAILDSS LMVEKVVALK EDAQVMMLKN KPDVELVNGS LGKVLFFVTE
SLVVKMKEIY KIVDDEVVMD MRLVSRVIGN PLLKESKEFR QDLNARPLAR LERLKILINY
AVKISPHKEK FPYVRWTVGK NKYIHELMVP ERFPIDIPRE NVGLERTQIP LMLCWALSIH
KAQGQTIQRL KVDLRRIFEA GQVYVALSRA VTMDTLQVLN FDPGKIRTNE RVKDFYKRLE
TLK
