Affinage

MCM2

DNA replication licensing factor MCM7 · UniProt P33993

Length
719 aa
Mass
81.3 kDa
Annotated
2026-06-10
100 papers in source corpus 49 papers cited in narrative 47 extracted findings
Cross-family judge vs UniProt: Affinage preferred faithfulness: 8/8 claims corpus-supported (100%)

Mechanistic narrative

Synthesis pass · prose summary of the discoveries below

MCM2 is a subunit of the heterohexameric MCM2-7 replicative helicase that is loaded around origin DNA as a head-to-head double hexamer and subsequently activated to drive replication-fork DNA unwinding (PMID:19896182, PMID:19910535). During licensing, ORC, Cdc6, and Cdt1 cooperatively deposit single Cdt1·Mcm2-7 complexes onto DNA in an ATP-hydrolysis-dependent reaction, and the loaded hexamers dimerize to encircle duplex DNA through their N-terminal rings (PMID:19896182, PMID:19910535, PMID:25319829, PMID:24234446). DNA entry occurs exclusively through the Mcm2-Mcm5 subunit interface, which functions as an ATP-dependent gate that opens during initial DNA association and closes sequentially with Cdt1 release; locking this gate triggers ATPase-driven disassembly, establishing it as the essential loading portal (PMID:28191892, PMID:25085418). Helicase activation in S phase converts the dormant double hexamer into the CMG holo-helicase (Cdc45-MCM2-7-GINS): GINS and Cdc45 bridge and seal the Mcm2-Mcm5 breach to form a topologically closed, processive 3'-to-5' helicase that supports leading-strand synthesis with DNA polymerase ε (PMID:20122406, PMID:21378962, PMID:22474384). CMG formation is gated by Cdc7-Dbf4 (DDK), which physically docks on Mcm2, phosphorylates MCM2 N-terminal sites (including Ser164/Ser170), weakens the Mcm2-Mcm5 interaction to promote ring opening and GINS recruitment, and tunes the number of transient Cdc45-GINS intermediates that determine CMG assembly frequency (PMID:9407029, PMID:19692334, PMID:25471369, PMID:33616038). MCM2 phosphorylation is further controlled by ATM/ATR at Ser92 in the DNA-replication checkpoint and modulated by DDK phosphorylation in response to genotoxic stress (PMID:15448142, PMID:21596784). Beyond its motor role, MCM2 carries a conserved histone-binding domain that engages H3-H4 and, acting within an Mcm2-Ctf4-Polα axis and with FACT, chaperones parental histones to ensure their symmetric inheritance to both daughter strands (PMID:30115746, PMID:26167883, PMID:30244834, PMID:37850662). This histone chaperone function additionally governs epigenetic gene regulation during differentiation and a replication-independent role in cilia gene transcription (PMID:30329080, PMID:36354740).

Mechanistic history

Synthesis pass · year-by-year structured walk · 13 steps
  1. 1993 High

    Established MCM2 as a cell-cycle-regulated chromatin factor required for replication initiation, linking its nuclear/chromatin presence in G1 to origin firing.

    Evidence Immunofluorescence, subcellular fractionation, and 2D gel analysis of replication intermediates in S. cerevisiae mutants

    PMID:8224843

    Open questions at the time
    • Did not define MCM2's biochemical activity
    • Mechanism of chromatin loading unresolved
  2. 1997 High

    Connected MCM2 to a kinase that triggers initiation, identifying Cdc7-Dbf4 as a physical partner and modifier of MCM2.

    Evidence Genetic suppressor screen, co-IP, and in vitro kinase assay in budding yeast

    PMID:9407029

    Open questions at the time
    • Phosphosites not mapped
    • Functional consequence of phosphorylation on helicase activity unknown
  3. 2001 High

    Mapped MCM2 as a bifunctional regulatory subunit with a C-terminal helicase-inhibitory/Mcm4-binding region and an N-terminal histone-binding domain, foreshadowing its dual replication and chaperone roles.

    Evidence In vitro helicase inhibition, GST pulldown, nucleosome assembly, and deletion mutagenesis (mouse Mcm2); yeast two-hybrid identification of HBO1 and AKAP95 partners

    PMID:11278932 PMID:11568184 PMID:12740381

    Open questions at the time
    • Physiological relevance of histone assembly in vivo not established
    • Structural basis of H3-H4 binding unknown
  4. 2006 High

    Localized MCM2-7 with Cdc45 and GINS to the active replication fork and mapped the kinase-target landscape of MCM2's N-terminus.

    Evidence Fork-pausing ChIP in Xenopus extracts; in vitro kinase mapping with mass spectrometry and phospho-specific antibodies for human MCM2

    PMID:16446360 PMID:16483939

    Open questions at the time
    • Did not show how phosphorylation alters helicase activation
    • Cdc45/GINS-MCM2-7 assembly mechanism unresolved
  5. 2009 High

    Reconstituted origin licensing from purified proteins, demonstrating ATP-dependent loading of Mcm2-7 double hexamers and establishing the molecular requirements for pre-RC formation.

    Evidence In vitro reconstitution with purified yeast ORC/Cdc6/Cdt1/Mcm2-7, biochemistry, and EM

    PMID:19896182 PMID:19910535

    Open questions at the time
    • How the loaded double hexamer is activated not addressed
    • Strand engagement geometry unresolved
  6. 2010 High

    Defined CMG as the active helicase form, showing that Cdc45 and GINS dramatically stimulate Mcm2-7 ATPase and helicase activity.

    Evidence Recombinant Drosophila protein biochemistry, ATPase and helicase assays, pairwise binding (GINS-MCM4); MCM-BP-driven MCM2-7 disassembly in Xenopus extracts

    PMID:20122406 PMID:21196493

    Open questions at the time
    • Structural basis of activation not yet visualized
    • Trigger linking S-phase signaling to CMG assembly unclear
  7. 2011 High

    Provided the structural logic of activation: the Mcm2-Mcm5 gap is bridged by Cdc45/GINS and sealed by nucleotide, and DDK phosphorylation of MCM2 promotes ring opening and GINS recruitment.

    Evidence Single-particle EM of Mcm2-7/CMG; biochemical ring-opening and ssDNA extrusion assays; GINS/Sld3 competition assays; Xenopus CMG assembly

    PMID:21282109 PMID:21378962 PMID:21460226 PMID:25471369

    Open questions at the time
    • Near-atomic loading-intermediate structures still lacking
    • Order of phosphorylation events and gate dynamics not resolved at high resolution
  8. 2014 High

    Resolved the mechanics of the Mcm2-Mcm5 gate as the exclusive DNA entry portal and dissected subunit-specific ATPase requirements for loading versus activation.

    Evidence Chemical-biology gate-locking, systematic ATPase-site mutagenesis, in vitro loading and in vivo replication assays; OCM-intermediate EM and DDK phosphomimetic genetics

    PMID:21596784 PMID:24234446 PMID:25085418 PMID:25087876 PMID:25319829

    Open questions at the time
    • How gate opening is coordinated with double-hexamer formation incompletely defined
    • In vivo gate dynamics during activation not directly observed
  9. 2015 High

    Defined the atomic basis of MCM2 histone chaperoning, showing its HBD captures H3-H4 by hijacking nucleosomal DNA contacts and co-chaperones with ASF1.

    Evidence X-ray/NMR structures of human MCM2 HBD with H3-H4, mutagenesis, and cell proliferation assays

    PMID:26167883

    Open questions at the time
    • Did not establish strand-specific histone segregation in vivo
    • Coupling to the moving replisome unresolved
  10. 2017 High

    Captured loading and double-hexamer structures at near-atomic resolution and observed gate opening/closing in real time, mechanistically linking ATP hydrolysis to ring closure and Cdt1 release.

    Evidence Cryo-EM of the OCCM and Mcm2-7 double hexamer on DNA; single-molecule FRET/colocalization spectroscopy

    PMID:28191892 PMID:28191893 PMID:29078375

    Open questions at the time
    • Conformational path from double hexamer to CMG not fully visualized
    • Strand-separation transition during activation inferred, not directly captured
  11. 2018 High

    Demonstrated that MCM2's histone-binding domain enforces symmetric parental-histone inheritance, embedding it in an Mcm2-Ctf4-Polα axis that biases transfer to the lagging strand.

    Evidence SCAR-seq/strand-specific histone profiling with MCM2 HBD mutants in mouse ES cells and yeast; epistasis with Ctf4 and Polα mutants; cohesin loading studies

    PMID:29611806 PMID:30115746 PMID:30244834

    Open questions at the time
    • How leading-strand histone deposition is achieved not fully defined
    • Whether histone transfer feeds back on fork progression unknown
  12. 2021 High

    Refined the activation mechanism, showing DDK phosphorylation of multiple N-terminal tail sites scales the multiplicity of transient Cdc45-GINS intermediates to set CMG-formation frequency.

    Evidence Single-molecule colocalization with DDK phosphorylation titration and in vitro reconstitution; cryo-EM of Dbf4 HBRCT anchoring DDK across the double hexamer

    PMID:33616038 PMID:35614055

    Open questions at the time
    • Precise phosphosite-to-intermediate correspondence not fully mapped
    • Coordination of cross-hexamer phosphorylation with origin firing kinetics unresolved
  13. 2022 Medium

    Extended MCM2 histone function to epigenetic gene regulation and identified MCMBP-dependent hexamer assembly as upstream of MCM2-7 licensing capacity.

    Evidence MCM2-2A histone-binding mutant ChIP/ATAC-seq and Asf1a co-IP in mouse ES cells; auxin-degron depletion of MCMBP with MCM3 interaction analysis in human cells; FACT-MCM2 ternary complex studies

    PMID:35438632 PMID:36354740 PMID:37850662

    Open questions at the time
    • Single-lab studies
    • Direct causal chain from histone mis-segregation to transcriptional defects incompletely defined
    • Reconstitution of FACT-MCM2 histone hand-off lacking

Open questions

Synthesis pass · forward-looking unresolved questions
  • It remains unresolved how MCM2's checkpoint phosphorylation (ATM/ATR Ser92; PTEN-controlled Ser41), O-GlcNAcylation, and replication-independent transcriptional roles are mechanistically integrated with its core helicase and histone-chaperone functions.
  • In vitro reconstitution of PTEN phosphatase activity on MCM2 lacking
  • Functional link between O-GlcNAcylation and helicase loading not mechanistically resolved
  • Replication-independent cilia transcription role rests on single-lab knockdown evidence

Mechanism profile

Synthesis pass · controlled-vocabulary classification · explore literature graph →
Molecular activity
GO:0042393 histone binding 4 GO:0140657 ATP-dependent activity 4 GO:0003677 DNA binding 3 GO:0140097 catalytic activity, acting on DNA 3 GO:0140096 catalytic activity, acting on a protein 1
Localization
GO:0000228 nuclear chromosome 3 GO:0005634 nucleus 3
Pathway
R-HSA-69306 DNA Replication 4 R-HSA-1640170 Cell Cycle 3 R-HSA-4839726 Chromatin organization 3 R-HSA-8953897 Cellular responses to stimuli 2
Partners
ASF1ACDC45CDC7CTF4DBF4HBO1MCM4MCM5
Complex memberships
CMG (Cdc45-MCM2-7-GINS) complexMCM2-7 helicasepre-replicative complex (ORC-Cdc6-Cdt1-Mcm2-7)

Evidence

Reading pass · 47 per-paper findings extracted from the source corpus
Year Finding Method Journal Conf PMIDs
2009 Reconstitution with purified budding yeast proteins demonstrated that ORC, Cdc6, and Cdt1 cooperatively load single Cdt1·Mcm2-7 heptamers onto origin DNA, resulting in stable head-to-head Mcm2-7 double hexamers encircling DNA via their N-terminal rings; once loaded, Mcm2-7 can slide passively along double-stranded DNA. In vitro reconstitution with purified proteins, biochemical assays, electron microscopy Cell High 19896182 19910535
2009 Reconstitution of S. cerevisiae pre-RC formation showed that MCM2-7 loading onto origin DNA requires all pre-RC proteins (ORC, Cdc6, Cdt1), origin DNA, and ATP hydrolysis; MCM2-7 transitions from a single hexamer in solution to a double hexamer around DNA during loading. In vitro reconstitution with purified proteins, electron microscopy, biochemical fractionation Proceedings of the National Academy of Sciences of the United States of America High 19910535
2010 The Drosophila MCM2-7 helicase is activated into the CMG (Cdc45-MCM2-7-GINS) complex: association with Cdc45 and the four GINS proteins elevates ATP hydrolysis rates by ~100-fold, confers robust helicase activity on circular templates, and improves DNA substrate affinity; GINS binds specifically to the MCM4 subunit. Recombinant protein biochemistry, in vitro ATPase assay, helicase assay, pairwise binding assays Molecular cell High 20122406
2011 Single-particle EM structures of Mcm2-7 and the CMG complex showed that Mcm2-7 adopts a lock-washer spiral or planar gapped-ring form with a breach between Mcm2 and Mcm5; GINS and Cdc45 bridge this gap to form a topologically closed assembly, and nucleotide binding further seals the Mcm2-Mcm5 discontinuity, explaining how CMG activates helicase activity. Single-particle electron microscopy, structural analysis, nucleotide-binding experiments Nature structural & molecular biology High 21378962
2006 Using biotin-streptavidin-induced replication fork pausing in Xenopus egg extracts with chromatin immunoprecipitation, MCM2-7, Cdc45, and GINS were identified as components enriched at the replication fork (the 'unwindosome'), and in the presence of aphidicolin (helicase-polymerase uncoupling), only Cdc45, GINS, and MCM2-7 were enriched at the pause site. Replication fork pausing assay, chromatin immunoprecipitation, Xenopus egg extracts Molecular cell High 16483939
1997 DBF4 (encoding the regulatory subunit of Cdc7-Dbf4 kinase) was identified as a second-site suppressor of mcm2-1 in S. cerevisiae; Cdc7-Dbf4 physically interacts with Mcm2, phosphorylates Mcm2 and three other Mcm2-7 family members in vitro, and blocking Cdc7-Dbf4 kinase activity at G1-to-S phase transition blocks phosphorylation of Mcm2, indicating that Cdc7-Dbf4 phosphorylation of Mcm2 is a critical step in replication initiation. Genetic suppressor screen, co-immunoprecipitation, in vitro kinase assay, cell-cycle analysis Genes & development High 9407029
2008 Purified S. cerevisiae Mcm2-7 complex exhibits DNA helicase activity when reaction conditions putatively close the Mcm2/5 gate; differences in linear ssDNA association rate and circular ssDNA binding between Mcm2-7 and Mcm467 depend on the Mcm2/5 interface, which functions as an ATP-dependent gate. In vitro helicase assay, ssDNA/dsDNA binding assays, comparative biochemistry of subcomplexes Molecular cell High 18657510
2018 MCM2 contains a histone-binding domain (HBD) that chaperones parental histones H3-H4 at replication forks; cells with histone-binding mutations in MCM2 show markedly increased segregation of parental histones to the leading strand, demonstrating that MCM2 is required for symmetric inheritance of histone PTMs to both sister chromatids. SCAR-seq (sister chromatid analysis of replication), histone-binding mutations in mouse ES cells, genome-wide strand-specific histone profiling Science (New York, N.Y.) High 30115746
2015 Crystal/NMR structures showed human MCM2 HBD binds an H3-H4 tetramer (hijacking nucleosomal DNA interaction sites) or an H3-H4 dimer co-chaperoned with ASF1; mutational analyses confirmed the MCM2 HBD is required for MCM2-7 histone-chaperone function and normal cell proliferation, and MCM2 can chaperone both new and old H3-H4 as well as H3.3 and CENPA variants. X-ray/NMR structure determination, site-directed mutagenesis, cell proliferation assays, histone binding assays Nature structural & molecular biology High 26167883
2018 The MCM2 subunit of the CMG helicase facilitates transfer of parental (H3-H4)2 tetramers to lagging-strand DNA; mutation of the conserved MCM2 histone-binding domain causes a marked enrichment of parental (H3-H4)2 on the leading strand; similar lagging-strand transfer defects occur with Ctf4 and Pol-alpha primase mutants, placing MCM2 in a Mcm2-Ctf4-Polα axis for parental histone transfer. Histone strand-specific sequencing, genetic epistasis with Ctf4 and Polα mutants, chromatin fractionation in yeast Molecular cell High 30244834
1993 MCM2 (and MCM3) in S. cerevisiae show cell-cycle-regulated nuclear localization: they enter the nucleus at the end of mitosis, persist through G1, and disappear from the nucleus at the beginning of S phase; a fraction becomes tightly chromatin-associated in G1, and reduction of function decreases frequency of initiation at chromosomal replication origins. Immunofluorescence, subcellular fractionation, 2D gel electrophoresis of replication intermediates, genetic mutant analysis Genes & development High 8224843
1995 Human BM28 (MCM2) is chromatin-associated (DNase I-sensitive) in G1 and early S phase nuclei; it is progressively lost from chromatin as S phase proceeds and exhibits cell-cycle-dependent changes in electrophoretic mobility consistent with phosphorylation, with a hyperphosphorylated fast-migrating form appearing during S phase. Detergent extraction, DNase I digestion, immunofluorescence, gel electrophoresis, cell cycle fractionation The Journal of cell biology High 7790346
2006 In vitro kinase assays with mass spectrometry mapped multiple phosphorylation sites on the N-terminus of human MCM2: Cdc7 phosphorylates at least three sites (one overlapping with ATR sites), CDK1/CDK2 phosphorylate three Ser/Pro sites, and CK2 phosphorylates a unique site; anti-phosphopeptide antibodies confirmed all sites are phosphorylated in cells, and Cdc7-dependent sites fluctuate with cell-cycle kinetics while CDK sites are constitutively phosphorylated. In vitro kinase assay, mass spectrometry, phospho-specific antibodies, cell-cycle synchronization The Journal of biological chemistry High 16446360
2004 In Xenopus egg extracts, Mcm2 was identified as an ATM-binding protein; Mcm2 is phosphorylated at Ser92 in response to double-strand DNA breaks or replication blocks, involving both ATM and ATR; both kinases directly phosphorylate Mcm2 at Ser92 in cell-free kinase assays; immunodepletion of both ATM and ATR abrogated the checkpoint block to chromosomal DNA replication. Co-immunoprecipitation, cell-free kinase assay, immunodepletion in Xenopus egg extracts, checkpoint assays The Journal of biological chemistry High 15448142
2017 Cryo-EM structure at 3.9 Å of the S. cerevisiae ORC-Cdc6-Cdt1-Mcm2-7 (OCCM) complex on DNA showed that Cdt1 adopts a three-domain configuration embracing Mcm2, Mcm4, and Mcm6 (~half of the hexamer); flexible Mcm2-7 WHDs engage ORC-Cdc6; the Mcm2-7 C-tier AAA+ ring is closed by an Mcm5 loop embracing Mcm2, but the N-tier Mcm2-Mcm5 interface remains open; DNA passes through both rings. Cryo-electron microscopy (3.9 Å), biochemical reconstitution Nature structural & molecular biology High 28191893
2017 Using single-molecule FRET and colocalization spectroscopy, the two Mcm2-7 rings were shown to be open (at the Mcm2-Mcm5 gate) during initial DNA association and close sequentially concomitant with Cdt1 release; ATP hydrolysis by Mcm2-7 is coupled to ring closure and Cdt1 release; failure to load the first Mcm2-7 prevented recruitment of the second. Single-molecule FRET, colocalization single-molecule spectroscopy, in vitro reconstitution Nature structural & molecular biology High 28191892
2017 Cryo-EM structure of the Mcm2-7 double hexamer (DH) on dsDNA revealed zigzagged DNA in the central channel; PS1 loops of Mcm3, 4, 6, and 7 (but not Mcm2 and Mcm5) engage the lagging strand; the architecture places each DNA strand in front of the two Mcm2-Mcm5 gates, and N-tier ring tilting/shifting is proposed to drive strand separation and lagging-strand extrusion upon activation. Cryo-electron microscopy structural analysis Proceedings of the National Academy of Sciences of the United States of America High 29078375
2009 Dbf4 forms a heterodimer with Cdc7 and this species phosphorylates Mcm2 with substantially higher specific activity than Cdc7 alone; Dbf4 alone binds tightly to Mcm2 while Cdc7 alone binds weakly, indicating Dbf4 recruits Cdc7 to phosphorylate Mcm2; DDK phosphorylates Mcm2 at Ser-164 and Ser-170; expression of mcm2-S170A is lethal in mcm2Δ cells but rescued by the DDK-bypass mcm5-bob1 allele. Biochemical reconstitution, in vitro kinase assay, yeast genetics (lethality, bypass suppressor) The Journal of biological chemistry High 19692334
2014 Chemical biology approach demonstrated that regulated Mcm2-7 helicase loading onto origin DNA occurs exclusively through the Mcm2-Mcm5 subunit interface as the DNA entry gate; inhibition of DNA insertion through this gate triggers ATPase-driven complex disassembly in vitro; in vivo, Mcm2/Mcm5 gate opening is essential for helicase loading onto chromatin and cell cycle progression. Chemical crosslinking (chemical biology), in vitro loading assay, in vivo chromatin binding, cell cycle analysis Genes & development High 25085418
2014 Mutational analysis of all six Mcm2-7 ATPase sites showed that ATP binding and hydrolysis by different subunits are required for distinct steps: some ATPase mutants are defective in initial Mcm2-7 recruitment or Cdt1 release during loading, while a subset that completes loading fails at helicase activation steps including DNA association maintenance, GINS recruitment, or DNA unwinding. ATPase-motif mutagenesis, in vitro helicase loading assay, in vivo replication assays Molecular cell High 25087876
2001 Yeast two-hybrid screen and biochemical confirmation (GST pulldown, immunoprecipitation) identified HBO1 (MYST family histone acetyltransferase) as a direct MCM2-interacting protein; interaction requires an N-terminal domain of MCM2 and the C2HC zinc finger of HBO1; a reverse two-hybrid selection and suppressor mutagenesis confirmed the interaction interface. Yeast two-hybrid, GST pulldown, co-immunoprecipitation, reverse two-hybrid, suppressor genetics The Journal of biological chemistry High 11278932
2003 AKAP95 was identified as an MCM2-interacting protein by yeast two-hybrid; interaction was confirmed by GST precipitation and co-immunoprecipitation from chromatin; disruption of AKAP95-MCM2 interaction with an AKAP95(1-195) peptide in HeLa nuclei abolished initiation of DNA replication in G1 and elongation phase in vitro; depletion of AKAP95 partially depletes MCM2 and abolishes replication, restored by recombinant AKAP95. Yeast two-hybrid, GST pulldown, co-immunoprecipitation, in vitro replication assay, nuclear microinjection/depletion The Journal of biological chemistry High 12740381
2015 PTEN physically associates with MCM2 and acts as a phosphatase to dephosphorylate MCM2 at Ser41 (S41); PTEN disruption results in unrestrained replication fork progression under replicative stress, similar to cells expressing phosphomimic MCM2-S41D; PTEN is required for prevention of chromosomal aberrations under replication stress. Co-immunoprecipitation, phosphatase assay, replication fork assay (DNA fiber), chromosomal aberration analysis, phosphomimic mutant expression Cell reports Medium 26549452
2001 Mouse Mcm2 inhibits Mcm4,6,7 helicase activity; the C-terminal half of Mcm2 binds Mcm4 and can disassemble the Mcm4,6,7 hexamer; the N-terminal region of Mcm2 contains the major Cdc7-mediated phosphorylation sites and a histone-binding domain enabling Mcm2 to assemble nucleosome-like structures with H3/H4 in vitro; a nuclear localization signal was also mapped. In vitro helicase inhibition assay, GST pulldown/binding assay, in vitro kinase assay, nucleosome assembly assay, deletion mutagenesis The Journal of biological chemistry High 11568184
2010 MCM-BP exists in a stable complex with MCM7 (but not the MCM2-7 hexamer) and accumulates in nuclei in late S phase; MCM-BP immunodepletion in Xenopus egg extracts inhibits replication-dependent MCM dissociation without affecting pre-RC formation or DNA replication; excess MCM-BP promotes disassembly of the MCM2-7 complex and releases MCM2-7 from late-S-phase chromatin in a replication-dependent manner. Co-immunoprecipitation, immunodepletion in Xenopus extracts, chromatin fractionation, in vitro disassembly assay Genes & development High 21196493
2011 MCM2-7 in Xenopus egg extracts is present at licensed origins as a double heterohexamer prior to replication initiation; after initiation, MCM2-7 associates with Cdc45 and GINS to form a stable CMG complex at replication forks. Size-exclusion chromatography, native gel analysis, co-immunoprecipitation, Xenopus egg extracts The Journal of biological chemistry High 21282109
2011 In budding yeast, Dbf4-Cdc7 phosphorylation of Mcm2 in vivo (during S phase) weakens the interaction between Mcm2 and Mcm5 in vitro and promotes Mcm2-7 ring opening at the Mcm2-Mcm5 interface; this ring opening allows ssDNA extrusion from the central channel, which in turn triggers GINS attachment to Mcm2-7. In vivo phosphorylation analysis, in vitro ring-opening assay, ssDNA extrusion assay, co-immunoprecipitation (GINS-Mcm2-7 interaction) The Journal of biological chemistry Medium 25471369
2011 GINS and Sld3 compete for binding to both Mcm2-7 and Cdc45; origin ssDNA disrupts the Sld3-Mcm2-7 interaction while promoting GINS-Mcm2-7 association, facilitating CMG complex formation; a ternary CMS complex (Cdc45-Mcm2-7-Sld3) has 1:1:1 stoichiometry, as does the CMG complex. Purified protein binding assays, competition assays, size-exclusion chromatography, stoichiometry analysis The Journal of biological chemistry Medium 21362622 21460226
2012 The human CMG complex purified from baculovirus-infected cells binds ssDNA with Mg2+ and ATP, has maximal helicase activity on forked DNA substrates, translocates 3' to 5' along the leading strand, unwinds duplexes up to 500 bp, and in combination with DNA polymerase ε supports leading-strand synthesis products >10 kb on circular templates. Purified recombinant protein biochemistry, helicase assay, rolling circle DNA synthesis assay Proceedings of the National Academy of Sciences of the United States of America High 22474384
2013 Human Ctf4 (hCtf4) interacts with the CMG complex; the hCtf4-CMG complex was isolated by in vitro reconstitution, co-infection, and from HeLa chromatin; hCtf4 exists as a homodimer within the complex; hCtf4-CMG retains DNA helicase activity with increased salt resistance compared to CMG alone; the homodimeric Ctf4 acts as a platform linking DNA polymerase α to the CMG complex. In vitro reconstitution, co-infection in insect cells, HeLa chromatin immunoprecipitation, helicase assay, stoichiometry analysis Proceedings of the National Academy of Sciences of the United States of America High 24255107
2009 In human cells, interactions between CMG components (Cdc45, Mcm2-7, GINS) detected by bimolecular fluorescence complementation occur only after the G1/S transition; stable CMG association requires CDK and Cdc7 kinase activities as well as RecQL4, Ctf4/And-1, and Mcm10, but not TopBP1 (unlike in yeast). Bimolecular fluorescence complementation (BiFC) in HeLa cells, siRNA knockdown, CDK inhibitor treatment Proceedings of the National Academy of Sciences of the United States of America Medium 19805216
2011 NMR structure of the human Cdt1(410-440)/MCM6(708-821) complex revealed that charge complementarity drives the specific Cdt1-Mcm6 interaction; alanine substitutions of conserved interacting residues in yeast Cdt1 and Mcm6 caused defective DNA replication and impaired chromatin loading of Mcm2, resulting in cell death. NMR structure determination, site-directed mutagenesis, in vivo DNA replication assay, chromatin fractionation Nucleic acids research High 22140117
2014 Structural intermediates revealed that ORC-Cdc6 first recruits a single Cdt1-Mcm2-7 to form an ORC-Cdc6-Mcm2-7 (OCM) complex after Cdt1 release; only the OCM (not the initial OCCM) is competent for Mcm2-7 dimerization; the head-to-head Mcm2-7 double hexamer generates a novel protein surface creating a multisubunit binding site for S-phase kinase; loaded double hexamer lacks ATPase activity essential for DNA helicase. EM structural analysis, biochemical intermediates, mutant analysis, kinase binding assay Genes & development High 24234446 25319829
2021 Using single-molecule biochemistry, DDK phosphorylation of multiple N-terminal tail phosphorylation sites on Mcm2-7 modulates the number of transient Cdc45-tail-GINS (CtG) intermediates formed per Mcm2-7; higher CtG multiplicity increases frequency of CMG formation; DDK acts in the first of two stages of Cdc45/GINS recruitment. Single-molecule colocalization assay, DDK phosphorylation titration, in vitro reconstitution eLife High 33616038
2022 Cryo-EM and biochemical analysis showed that the HBRCT domain of Dbf4 anchors DDK to Mcm2, and this anchoring supports DDK binding across the MCM2-7 double-hexamer interface, enabling phosphorylation of Mcm4 on the opposite hexamer; rotation of DDK around this anchor allows phosphorylation of Mcm2 and Mcm6. Cryo-electron microscopy, biochemical kinase assays, domain mutagenesis Nature communications High 35614055
2013 Dbf4 interacts most strongly with Mcm2 (via an N-terminal docking domain) while Cdc7 interacts with Mcm4 and Mcm5; combining mutations in Mcm2 docking domain (Mcm2ΔDDD) and Mcm4 docking domain (Mcm4ΔDDD) is synthetically lethal, indicating overlapping roles in DDK-MCM ring association at replication origins. Two-hybrid, co-immunoprecipitation, genetic epistasis (synthetic lethality), deletion mutagenesis The Journal of biological chemistry High 23549044
2011 In phosphorylation modulation experiments: DDK phosphorylation of Mcm2 at S164/S170 reduced helicase activity of Mcm2-7 in vitro while increasing DNA binding; the phosphomimetic mcm2-EE suppresses MMS/caffeine sensitivity of DDK-deficient cells; the mcm2-AA strain (alanine at S164/S170) accumulates more RPA foci, is sensitive to MMS/caffeine/HU, indicating DDK phosphorylation of Mcm2 modulates Mcm2-7 activity in response to DNA damage. In vitro helicase assay, in vitro DNA binding assay, yeast genetic analysis, RPA focus counting Nucleic acids research High 21596784
2019 A conserved Mcm4 N-terminal motif is required for stable Mcm2-7 double-hexamer (DH) formation; mutations permitting two hexamer loads but blocking DH stability show that DH formation is required for extensive origin DNA unwinding but not initial DNA melting or recruitment of helicase-activation proteins (Cdc45, GINS, Mcm10). Single-molecule biochemistry, in vitro origin DNA unwinding assay, helicase activation recruitment assay, mutant Mcm4 analysis eLife High 31385807
2018 In human cells, cohesin loading onto chromosomes during early S phase requires the MCM2-7 replicative helicase and DDK kinase; cohesin and its loader SCC2/4 (NIPBL/MAU2) associate with DDK and phosphorylated MCM2-7; this association does not require MCM2-7 activation by CDC45/GINS but requires fork-stabilizing replisome components for persistence; inactivation of these components impairs cohesin loading and causes interphase cohesion defects. Co-immunoprecipitation, siRNA knockdown, chromatin fractionation, sister chromatid cohesion assay eLife Medium 29611806
2022 MCMBP associates with MCM3 and is required for assembly of the MCM2-7 hexamer in human cells; acute MCMBP depletion reduces MCM2-7 hexamer levels using nascent MCM3, decreases replication licensing, and causes p53-null cells to enter S phase with accumulation of DNA damage. Auxin-inducible degron depletion, co-immunoprecipitation, chromatin fractionation, cell proliferation and DNA damage assays eLife High 35438632
2019 In resting (non-cycling) human cells and zebrafish, MCM2 has a replication-independent function in cilia formation; MCM2 depletion promotes transcription of a subset of cilia-inhibiting genes; chromatin immunoprecipitation showed MCM2 binds to transcription start sites of cilia-inhibiting genes, suggesting MCM2 blocks RNA Pol II transcription of these genes. siRNA knockdown in non-cycling fibroblasts, zebrafish morpholino knockdown, ChIP, cilia length/structure analysis Nucleic acids research Medium 30329080
2018 O-GlcNAc transferase (OGT) stably associates with multiple MCM2-7 subunits including MCM2; O-GlcNAcylation of MCM proteins occurs predominantly in the chromatin-bound fraction; OGT silencing decreases chromatin binding of MCM2, MCM6, and MCM7, and destabilizes MCM2/6 and MCM4/7 interactions in the chromatin-enriched fraction. Co-immunoprecipitation, OGT knockdown, chromatin fractionation, MCM interaction analysis Cellular and molecular life sciences : CMLS Medium 30069701
2013 Ciprofloxacin preferentially inhibits Mcm2-7 helicase activity in vitro compared to other tested helicases; the mcm4chaos3 mutant exhibits increased ciprofloxacin resistance; ciprofloxacin prevents proliferation of yeast and human cells at concentrations similar to those inhibiting DNA unwinding. In vitro helicase inhibition assay, cell proliferation assay, drug resistance genetics Bioscience reports Medium 24001138
2023 The N-terminus of Spt16 (FACT subunit) interacts with the MCM2-7 replicative helicase and facilitates formation of a ternary complex of FACT, histone H3/H4, and the Mcm2 histone-binding domain; this interaction is required for efficient parental histone recycling and transfer to lagging strands; deletion of the Spt16-N domain weakens the FACT-MCM interaction and reduces lagging-strand parental histone recycling. Co-immunoprecipitation, histone ChIP-seq (strand-specific), genetic/domain deletion analysis in yeast Nucleic acids research Medium 37850662
2022 The MCM2-2A mutation (defective in histone H3-H4 binding) in mouse ES cells causes defects in silencing pluripotent genes and induction of lineage-specific genes during differentiation; MCM2-2A cells show reduced binding to Asf1a (histone chaperone for nucleosome disassembly at bivalent chromatin domains), and MCM2 binding at gene promoters is reduced; MCM2 localizes to transcription start sites and loss of MCM2 histone-binding reduces chromatin accessibility at bivalent domains in neural precursor cells. Genetic mutation analysis in mouse ES cells, ChIP, ATAC-seq, co-immunoprecipitation with Asf1a, differentiation assays eLife Medium 36354740
2000 Mcm10 physically interacts with members of the MCM2-7 complex and mediates MCM2-7 association with replication origins; a specific Mcm10-Mcm7 interaction is required for replication initiation; double mutations mcm10-1/mcm7-1 (cdc47-1) are allele-specifically complementary, restoring Mcm10-Mcm7 interaction and correcting replication initiation defects including stalling at origins. Co-immunoprecipitation, genetic epistasis (double mutant rescue), chromatin fractionation Genes & development High 10783164
2013 CDK2/cyclinA phosphorylation of MCM4 (in the MCM2-7 complex) inhibits MCM2-7 DNA binding ability as shown by gel-shift analysis; mutation of six Ser/Thr residues in the MCM4 N-terminal region to alanine renders MCM2-7 insensitive to CDK-mediated inhibition of DNA binding, providing a direct mechanism by which CDK prevents MCM2-7 chromatin re-loading. In vitro kinase assay, gel-shift DNA binding assay, alanine substitution mutagenesis Journal of biochemistry Medium 23864661

Source papers

Stage 0 corpus · 100 papers · ranked by NIH iCite citations
Year Title Journal Citations PMID
2009 Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell 550 19896182
2010 Activation of the MCM2-7 helicase by association with Cdc45 and GINS proteins. Molecular cell 456 20122406
2009 A double-hexameric MCM2-7 complex is loaded onto origin DNA during licensing of eukaryotic DNA replication. Proceedings of the National Academy of Sciences of the United States of America 440 19910535
2006 Localization of MCM2-7, Cdc45, and GINS to the site of DNA unwinding during eukaryotic DNA replication. Molecular cell 306 16483939
2011 The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nature structural & molecular biology 270 21378962
1997 Mcm2 is a target of regulation by Cdc7-Dbf4 during the initiation of DNA synthesis. Genes & development 259 9407029
2008 The Mcm2-7 complex has in vitro helicase activity. Molecular cell 240 18657510
2018 MCM2 promotes symmetric inheritance of modified histones during DNA replication. Science (New York, N.Y.) 229 30115746
1995 BM28, a human member of the MCM2-3-5 family, is displaced from chromatin during DNA replication. The Journal of cell biology 223 7790346
1993 Cell cycle-regulated nuclear localization of MCM2 and MCM3, which are required for the initiation of DNA synthesis at chromosomal replication origins in yeast. Genes & development 210 8224843
2015 A unique binding mode enables MCM2 to chaperone histones H3-H4 at replication forks. Nature structural & molecular biology 197 26167883
1991 Mcm2 and Mcm3, two proteins important for ARS activity, are related in structure and function. Genes & development 184 2044961
2006 Identification of Mcm2 phosphorylation sites by S-phase-regulating kinases. The Journal of biological chemistry 176 16446360
2018 The Mcm2-Ctf4-Polα Axis Facilitates Parental Histone H3-H4 Transfer to Lagging Strands. Molecular cell 164 30244834
2016 Long noncoding RNA FTX inhibits hepatocellular carcinoma proliferation and metastasis by binding MCM2 and miR-374a. Oncogene 162 27065331
2009 Assembly of the Cdc45-Mcm2-7-GINS complex in human cells requires the Ctf4/And-1, RecQL4, and Mcm10 proteins. Proceedings of the National Academy of Sciences of the United States of America 162 19805216
2001 Replication factors MCM2 and ORC1 interact with the histone acetyltransferase HBO1. The Journal of biological chemistry 162 11278932
2007 Reduced Mcm2 expression results in severe stem/progenitor cell deficiency and cancer. Stem cells (Dayton, Ohio) 145 17717065
2000 Mcm10 and the MCM2-7 complex interact to initiate DNA synthesis and to release replication factors from origins. Genes & development 142 10783164
2017 Structural basis of Mcm2-7 replicative helicase loading by ORC-Cdc6 and Cdt1. Nature structural & molecular biology 141 28191893
2005 Pumps, paradoxes and ploughshares: mechanism of the MCM2-7 DNA helicase. Trends in biochemical sciences 127 16002295
2001 Is the MCM2-7 complex the eukaryotic DNA replication fork helicase? Current opinion in genetics & development 127 11163153
2005 MCM8 is an MCM2-7-related protein that functions as a DNA helicase during replication elongation and not initiation. Cell 116 15707891
2012 Properties of the human Cdc45/Mcm2-7/GINS helicase complex and its action with DNA polymerase epsilon in rolling circle DNA synthesis. Proceedings of the National Academy of Sciences of the United States of America 113 22474384
2011 MCM2-7 form double hexamers at licensed origins in Xenopus egg extract. The Journal of biological chemistry 111 21282109
2004 Mcm2 is a direct substrate of ATM and ATR during DNA damage and DNA replication checkpoint responses. The Journal of biological chemistry 111 15448142
2014 A unique DNA entry gate serves for regulated loading of the eukaryotic replicative helicase MCM2-7 onto DNA. Genes & development 104 25085418
2017 Open-ringed structure of the Cdt1-Mcm2-7 complex as a precursor of the MCM double hexamer. Nature structural & molecular biology 95 28191894
2014 Multiple functions for Mcm2-7 ATPase motifs during replication initiation. Molecular cell 91 25087876
2017 Cryo-EM structure of Mcm2-7 double hexamer on DNA suggests a lagging-strand DNA extrusion model. Proceedings of the National Academy of Sciences of the United States of America 89 29078375
2014 Structural and mechanistic insights into Mcm2-7 double-hexamer assembly and function. Genes & development 86 25319829
2010 DNA damage response and tumorigenesis in Mcm2-deficient mice. Oncogene 82 20440269
1995 Cell proliferation and DNA replication defects in a Drosophila MCM2 mutant. Genes & development 79 7622035
2000 An MCM2-related gene is expressed in proliferating cells of intact and regenerating planarians. Developmental dynamics : an official publication of the American Association of Anatomists 78 10906779
1998 HsMCM2/BM28: a novel proliferation marker for human tumors and normal tissues. Laboratory investigation; a journal of technical methods and pathology 77 9461123
2010 Incremental genetic perturbations to MCM2-7 expression and subcellular distribution reveal exquisite sensitivity of mice to DNA replication stress. PLoS genetics 76 20838603
2018 Regulation of MCM2-7 function. Genes & genetic systems 75 30369561
2017 Mechanism and timing of Mcm2-7 ring closure during DNA replication origin licensing. Nature structural & molecular biology 69 28191892
2015 Dynamic loading and redistribution of the Mcm2-7 helicase complex through the cell cycle. The EMBO journal 69 25555795
1994 The fission yeast cdc19+ gene encodes a member of the MCM family of replication proteins. Journal of cell science 69 7876346
2014 The Mcm2-7 replicative helicase: a promising chemotherapeutic target. BioMed research international 67 25243149
2007 Differences in the single-stranded DNA binding activities of MCM2-7 and MCM467: MCM2 and MCM5 define a slow ATP-dependent step. The Journal of biological chemistry 66 17895243
2017 MCM2: An alternative to Ki-67 for measuring breast cancer cell proliferation. Modern pathology : an official journal of the United States and Canadian Academy of Pathology, Inc 62 28084344
2008 Expression of Mcm-2, Ki-67 and geminin in benign and malignant salivary gland tumours. Journal of oral pathology & medicine : official publication of the International Association of Oral Pathologists and the American Academy of Oral Pathology 59 18248354
2018 MCM2-7-dependent cohesin loading during S phase promotes sister-chromatid cohesion. eLife 58 29611806
2018 Role of MCM2-7 protein phosphorylation in human cancer cells. Cell & bioscience 58 30062004
2007 Interactions of human Cdc45 with the Mcm2-7 complex, the GINS complex, and DNA polymerases delta and epsilon during S phase. Genes to cells : devoted to molecular & cellular mechanisms 57 17573775
2009 Dbf4-Cdc7 phosphorylation of Mcm2 is required for cell growth. The Journal of biological chemistry 55 19692334
2010 Clinicopathological features and immunohistochemical expression of p53, Ki-67, Mcm-2 and Mcm-5 in proliferative verrucous leukoplakia. Journal of oral pathology & medicine : official publication of the International Association of Oral Pathologists and the American Academy of Oral Pathology 53 20412398
2010 MCM-BP regulates unloading of the MCM2-7 helicase in late S phase. Genes & development 53 21196493
2022 MCM2 in human cancer: functions, mechanisms, and clinical significance. Molecular medicine (Cambridge, Mass.) 50 36303105
2015 PTEN Controls the DNA Replication Process through MCM2 in Response to Replicative Stress. Cell reports 50 26549452
2001 Biochemical activities associated with mouse Mcm2 protein. The Journal of biological chemistry 49 11568184
2015 MCM2 is a therapeutic target of lovastatin in human non-small cell lung carcinomas. Oncology reports 46 25738322
2013 Ciprofloxacin is an inhibitor of the Mcm2-7 replicative helicase. Bioscience reports 46 24001138
2011 The Cdc45·Mcm2-7·GINS protein complex in trypanosomes regulates DNA replication and interacts with two Orc1-like proteins in the origin recognition complex. The Journal of biological chemistry 45 21799014
2013 High incidence of DNA ploidy abnormalities and increased Mcm2 expression may predict malignant change in oral proliferative verrucous leukoplakia. Histopathology 44 23347057
2006 Stem cell markers: ABCG2 and MCM2 expression in retinoblastoma. The British journal of ophthalmology 44 16556617
2013 Interaction between human Ctf4 and the Cdc45/Mcm2-7/GINS (CMG) replicative helicase. Proceedings of the National Academy of Sciences of the United States of America 43 24255107
2012 Post-transcriptional homeostasis and regulation of MCM2-7 in mammalian cells. Nucleic acids research 43 22362746
2010 MCM-2 and MCM-5 expression in gastric adenocarcinoma: clinical significance and comparison with Ki-67 proliferative marker. Digestive diseases and sciences 43 20694513
2003 Protein kinase A-anchoring protein AKAP95 interacts with MCM2, a regulator of DNA replication. The Journal of biological chemistry 43 12740381
2011 Correlation between expression of metallothionein and expression of Ki-67 and MCM-2 proliferation markers in non-small cell lung cancer. Anticancer research 42 21868526
2012 The eukaryotic Mcm2-7 replicative helicase. Sub-cellular biochemistry 39 22918583
2022 MCM2 promotes the stemness and sorafenib resistance of hepatocellular carcinoma cells via hippo signaling. Cell death discovery 38 36243809
2014 Switch on the engine: how the eukaryotic replicative helicase MCM2-7 becomes activated. Chromosoma 38 25308420
2011 Structural insights into the Cdt1-mediated MCM2-7 chromatin loading. Nucleic acids research 37 22140117
2019 Inhibition of MCM2 enhances the sensitivity of ovarian cancer cell to carboplatin. Molecular medicine reports 35 31322224
2019 A conserved Mcm4 motif is required for Mcm2-7 double-hexamer formation and origin DNA unwinding. eLife 33 31385807
2013 Dbf4 and Cdc7 proteins promote DNA replication through interactions with distinct Mcm2-7 protein subunits. The Journal of biological chemistry 33 23549044
2022 The structural basis of Cdc7-Dbf4 kinase dependent targeting and phosphorylation of the MCM2-7 double hexamer. Nature communications 31 35614055
2017 MCM2-regulated functional networks in lung cancer by multi-dimensional proteomic approach. Scientific reports 31 29038488
2022 Mcm2 promotes stem cell differentiation via its ability to bind H3-H4. eLife 30 36354740
2021 DDK regulates replication initiation by controlling the multiplicity of Cdc45-GINS binding to Mcm2-7. eLife 29 33616038
2013 The ORC/Cdc6/MCM2-7 complex facilitates MCM2-7 dimerization during prereplicative complex formation. Nucleic acids research 29 24234446
2021 MCM2-7 complex is a novel druggable target for neuroendocrine prostate cancer. Scientific reports 27 34172788
2011 CDC19 encoding pyruvate kinase is important for high-temperature tolerance in Saccharomyces cerevisiae. New biotechnology 27 21459167
2011 Origin single-stranded DNA releases Sld3 protein from the Mcm2-7 complex, allowing the GINS tetramer to bind the Mcm2-7 complex. The Journal of biological chemistry 27 21460226
2019 Sir2 suppresses transcription-mediated displacement of Mcm2-7 replicative helicases at the ribosomal DNA repeats. PLoS genetics 26 31083663
2014 Correlation of MCM2 detection with stage and virology of cervical cancer. The International journal of biological markers 26 24706378
2011 Phosphorylation of Mcm2 modulates Mcm2-7 activity and affects the cell's response to DNA damage. Nucleic acids research 26 21596784
2022 MCMBP promotes the assembly of the MCM2-7 hetero-hexamer to ensure robust DNA replication in human cells. eLife 25 35438632
2014 The Dbf4-Cdc7 kinase promotes Mcm2-7 ring opening to allow for single-stranded DNA extrusion and helicase assembly. The Journal of biological chemistry 25 25471369
2013 Inhibition of DNA binding of MCM2-7 complex by phosphorylation with cyclin-dependent kinases. Journal of biochemistry 25 23864661
2020 Establishment of a CALU, AURKA, and MCM2 gene panel for discrimination of metastasis from primary colon and lung cancers. PloS one 24 32469983
2019 Targeting CDC7 sensitizes resistance melanoma cells to BRAFV600E-specific inhibitor by blocking the CDC7/MCM2-7 pathway. Scientific reports 24 31578454
2015 Minichromosome maintenance-2 (MCM2) expression differentiates oral squamous cell carcinoma from pre-cancerous lesions. The Malaysian journal of pathology 24 26712671
2011 GINS and Sld3 compete with one another for Mcm2-7 and Cdc45 binding. The Journal of biological chemistry 24 21362622
2018 A hydrophobic low-complexity region regulates aggregation of the yeast pyruvate kinase Cdc19 into amyloid-like aggregates in vitro. The Journal of biological chemistry 23 29853641
2010 Interaction of human MCM2-7 proteins with TIM, TIPIN and Rb. Journal of biochemistry 22 20299328
2023 The assembly of the MCM2-7 hetero-hexamer and its significance in DNA replication. Biochemical Society transactions 21 37145026
2023 The N-terminus of Spt16 anchors FACT to MCM2-7 for parental histone recycling. Nucleic acids research 21 37850662
2019 Resting cells rely on the DNA helicase component MCM2 to build cilia. Nucleic acids research 21 30329080
2018 Proteomic Analysis and NIR-II Imaging of MCM2 Protein in Hepatocellular Carcinoma. Journal of proteome research 21 29750532
1994 The human gene for nuclear protein BM28 (CDCL1), a new member of the early S-phase family of proteins, maps to chromosome band 3q21. Cytogenetics and cell genetics 21 8258304
2018 O-GlcNAc transferase associates with the MCM2-7 complex and its silencing destabilizes MCM-MCM interactions. Cellular and molecular life sciences : CMLS 20 30069701
2015 Dpb11 protein helps control assembly of the Cdc45·Mcm2-7·GINS replication fork helicase. The Journal of biological chemistry 19 25659432
2014 Helicase loading: how to build a MCM2-7 double-hexamer. Seminars in cell & developmental biology 19 24637008
2021 MCM2-7 in Clear Cell Renal Cell Carcinoma: MCM7 Promotes Tumor Cell Proliferation. Frontiers in oncology 18 34993142
2012 Mcm2 phosphorylation and the response to replicative stress. BMC genetics 18 22564307

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