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complex primarily interacts with the single-stranded DNA segment\nMcm4/6/7 binds to ‘bubble’ DNA substrates and unwinds the duplex segments when the central single-stranded segment contains thymine stretches (13). In order to examine the mode of binding of Mcm4/6/7 on bubble DNAs, we conducted nuclease protection assays using labeled bubble substrate DNAs and Mcm4/6/7 in the presence of ATP-γ-S which permits binding to substrate DNA but does not mobilize the helicase. At an optimum concentration of DNase I, strong cleavages were detected on the 21 bp duplex regions at both ends of the substrates, whereas weaker cleavages were detected on the central single-stranded region, consistent with preference of DNase I to double-stranded DNA. With the Bub66/T-rich substrate, strong protection was detected on the entire single-stranded regions of both top and bottom strands with increasing concentration of Mcm4/6/7, consistent with high affinity of Mcm4/6/7 to T-rich bubble sequences (Figure 1A). Similar, but less significant protection was detected on the single-stranded DNA segment with P1 nucleases (Figure 1A), which is specific to single-stranded DNA. The results indicate that the Mcm complex is loaded onto bubble DNA through binding to both strands of the single-stranded region. Careful examination of Mcm4/6/7 footprints on a bubble indicated strong protection on the 5′-half of the top strand and moderate protection on the remaining 3′-half, as well as on several base-pair duplex segment adjacent to the branch point (Figure 1A and data not shown). A similar pattern of protection was observed also on the bottom strand. This suggests that Mcm4/6/7 may bind to a replication bubble substrate with a 2-fold symmetry as a double hexamer (Figure 1A, see the lower scheme), in a manner similar to SV40 T-antigen (21).\nNuclease protection assays were conducted also on a T-tailed Y-fork structure (Figure 1B). Not only the single-stranded tail region but also the 7 bp duplex DNA adjacent to the duplex-to-single-strand junction were protected by Mcm binding from DNaseI digestion. These results indicate that Mcm4/6/7 protein primarily interacts with single-stranded DNA region and that the interaction also spans the duplex segments near the branchpoint of the replication fork.\n\nFormation of double hexameric Mcm4/6/7 complexes facilitates helicase actions on bubble substrates\nThe above results suggest that Mcm4/6/7 generates a double hexameric complex on a bubble, each hexamer of which makes symmetric contact with the 5′-proximal central single-stranded segment. This predicts that the single-stranded segment needs to be of a sufficient length in order to accommodate the Mcm complex. In fact, we previously showed that the Mcm4/6/7 mainly forms a single hexameric complex on bubble-20 (a bubble substrate with 20 nt long central single-stranded segment) and a double hexameric complex on bubble-60 DNA (13). In order to determine the minimum requirement for double-hexamer formation, a set of synthetic bubble-like substrates (Bub-T10, Bub-T20, Bub-T30, Bub-T40 and Bub-T50) that differed in the length of the central unpaired segment were constructed, and the binding and helicase activities of Mcm4/6/7 on these substrates were examined. Mcm4/6/7 was incubated with a radiolabeled synthetic bubble substrate in the presence of 0.5 mM ATP-γ-S to allow complex formation. A half of these reaction mixtures were analyzed for DNA binding in gel shift assays (Figure 2A), and the remainder was further incubated in the presence of 10 mM ATP to measure DNA helicase activity (Figure 2B). Bub-10 generated only a low level of complexes with Mcm4/6/7, and Bub-20 generated primarily a single mobility-shifted form, which may contain a single hexamer of Mcm4/6/7. On Bub-30, significant amount of complexes containing a double hexamer were generated in addition to those containing a single hexamer (Figure 2A) (13,21). The amounts of double hexamer complexes increased on Bub-T40 and Bub-T50 with concomitant decrease of single hexamer complexes (Figure 2A). The results indicate that a single-stranded segment of at least 40 nt long is required for efficient loading of the double-hexameric Mcm helicase on a bubble substrate.\nIn DNA helicase assays, Mcm4/6/7 complex did not show helicase activity on either Bub-10 or Bub-20 substrate. The efficiency of displacement slightly improved as the length of the single-stranded segment increased up to 30 nt. On Bub-T40 and Bub-T50, on the other hand, significant displacement was observed, indicating that a single-stranded segment of at least 40 nt long is required for efficient helicase actions on bubble substrates (Figure 2B). Taken together, the above results are consistent with the notion that the Mcm4/6/7 complex, loaded onto DNA as a double hexameric complex, efficiently unwinds the duplex region of the substrate DNA.\n\nBoth strands of thymine-rich single-stranded segments are required for efficient unwinding of bubble DNA by Mcm4/6/7\nSymmetric binding of the Mcm4/6/7 double hexamer to bubble suggests that each hexamer catalyzes unwinding of one of the two duplex segments. We asked whether activation of both hexamers is required for unwinding of the bubble substrate. The preferred bubble substrate which is efficiently unwound by Mcm4/6/7 contains thymine stretches on both strands of the single-stranded segment. We constructed a hetero-bubble (Bub66/T–G-rich) in which one strand is T-rich (same as Bub66/T-rich) and the other strand is G-rich (same as Bub66/G-rich) (13), and helicase assays were conducted with increasing amount of Mcm4/6/7. Only weak unwinding was detected on this substrate compared to Bub66/T-rich (Figure 3A). Since Mcm4/6/7 can bind to Bub66/T–G-rich and forms a double hexameric complex (data not shown), the defective unwinding is not due to inefficient loading of the helicase onto the substrate. If one hexamer interacting with the thymine-rich strand dissociates from the other hexamer and displaces only one of the duplex segments, then it would result in generation of Y-fork structures which could not be further displaced due to the presence of G-rich 3′-tail and would appear on the gel. However, we did not detect such intermediates during the course of the experiment (Figure 3B), suggesting that bubble can be displaced efficiently only when two molecules of the Mcm4/6/7 hexamers are simultaneously activated.\n\nBinding and helicase actions of Mcm4/6/7 on forked and 3′- or 5′-extension substrates\nIn order to examine more precisely the interaction and helicase actions with forked substrates, Y-fork substrates containing a nascent leading strand (A-fork[3′]), nascent lagging strand (A-fork[5′]), or both of them (A-fork[3′,5′]), as well as 5′-extension or 3′-extension structures were constructed. Mcm4/6/7 bound to A-fork[3′] or A-fork[5′] with affinity similar to that of a simple Y-fork (Figure 4A and data not shown). In contrast, PriA helicase, used as a control, bound to A-fork[3′] more efficiently than to A-fork[5′], as reported previously (23,25). Mcm4/6/7 bound also to 5′-extension and 3′-extension, albeit with slightly reduced affinity compared to A-fork[3′] and A-fork[5′] (Figure 4A). Mcm4/6/7 bound to A-fork[3′,5′] with much lower affinity, and the complex gave rise to a single band. These findings indicate that the Mcm4/6/7 complex is loaded onto DNA preferentially and efficiently through single-stranded region, regardless of the presence of 3′- or 5′-terminus.\nIn contrast, only the substrate containing a 3′ single-stranded DNA tail (A-fork[5′]) was efficiently unwound and A-fork[3′] or A-fork[3′,5′], was not unwound by Mcm4/6/7 (Figure 4B). Absence of helicase actions on A-fork[3′,5′] composed only of duplex regions is expected since double-stranded DNA is not able to activate the ATPase activity of Mcm4/6/7 (10). In contrast, the PriA, a structure-specific helicase used as a control, binds at the fork junction and unwinds the fork and the nascent lagging strand DNA on A-fork[5′], or unwinds the nascent lagging strand on A-fork[3′,5′], as reported before (25). These results indicate that the Mcm4/6/7 complex binds to single-stranded DNA and that its helicase is activated only in the presence of a single-stranded 3′-tail.\n\n3′-extension with poly(dT) tail is displaced by Mcm4/6/7\nIt has been reported that the 3′-extension can be unwound by the archaeal Mcm homohexamer but not by fission and budding yeast Mcm complexes (14,26,27). We have constructed 3′-extension substrates containing poly(dT), poly(dA), poly(dC) and poly(dG) 3′-tails in order to examine whether mouse Mcm4/6/7 can displace these substrates. We first found that Mcm4/6/7 binds to dT-, dC- and dG-3′-extension with similar affinity, and to dA-3′-extension with much lower affinity (Figure 5A). This is consistent with the previous results that Mcm4/6/7 binds to 50mer oligo-dT, -dC and -dG, but not to a 50mer oligo-dA (13). We found that dT-tailed 3′-extension was displaced efficiently by Mcm 4/6/7 while almost no or very little activity was detected on other substrates (Figure 5B and C). This is in sharp contrast to yeast Mcm4/6/7 helicases which are not capable of unwinding 3′-extension substrates. Furthermore, dT-tailed 5′-extension, to which Mcm4/6/7 could bind, was not displaced by the Mcm helicase. The addition of the 5′-tail to dT-tailed 3′-extension further stimulated the displacement (Figure 5D), confirming the previous report that the fork structures facilitate the helicase action. Thus, these results further strengthen our conclusion that the mammalian Mcm helicase is generally activated by the thymine-stretch on the 3′-single-stranded tail.\n\nThe effects of the thymine content of the 3′-tail on Mcm helicase activity\nWe next examined more systematically the effect of the compositions of the thymine residues of the 3′-tail on the Mcm helicase activity. A partial heteroduplex M13 single-stranded DNA containing a 37 bp duplex region in the presence or absence of the 50 nt long 3′-tail of various nucleotide compositions were constructed and the unwinding by mouse Mcm4/6/7 was examined (Figure 6A). Due to its low processivity, Mcm4/6/7 barely displaced the annealed 37mer oligonucleotide without a 3′-tail (37mer; Figure 6A). Only weak helicase activity was observed on the substrate carrying the 3′-tail of 25 repeats of TA dinucleotide (37-TA25; Figure 6A), whereas strong helicase activity was observed on 37-TTA17. Increase of thymine content on the 3′-tail did not further increase the extent of unwinding (37-TTTA13, 37-TTTTA10 and 37-T50; Figure 6A), suggesting that 17 repeats of TT dinucleotides (67% thymine) may be sufficient for activation of Mcm helicase. It should be noted that the TA25 tail would self-anneal and this would prevent the loading of Mcm, since the 3′-tail containing TTAA13 or TTTAAA8 did not enhance the unwinding either (data not shown). Therefore, we next examined the effects of repeating sequences of thymine and cytosine (Figure 6B). Partial heteroduplex substrates containing the 3′-tail of TC25, TTCC13, TTTCCC8, TTTTCCCC6, TTCC17 were displaced by the Mcm4/6/7 complex to the extent similar to that achieved by TTA17, suggesting that 50% thymine content is sufficient for full activation of Mcm helicase. TTCC13 and TTCC17 were displaced to a similar extent, consistent with the earlier result that a 40 nt tail is sufficient for activation (13). However, the efficiency of the displacement significantly decreased as the thymine content of the 3′-tail dropped to 33%, as in TAA17 or TCC17 (Figure 6B and C). Thus, the minimal thymine content required for activation of the Mcm helicase may be somewhere between 33 and 50%.\n\nDUE sequences from the c-myc origin activate Mcm helicase\nOur previous studies have shown that the sequences containing periodic (dT)n tracts derived from the human lamin B2 origin (48% thymine content) can serve as an efficient activator for the Mcm helicase on a bubble, and replacement of thymines with guanines abolished the helicase activation (13,28). In order to examine other natural replication origins with different thymine contents for the ability to activate Mcm helicase on a bubble substrate, we constructed new bubble substrates, Bub82/c-myc, containing sequences derived from the DUE (DNA unwinding element) region of the human c-myc origin which is essential for c-myc replicator activity (29,30). The unpaired segment in Bub82/c-myc/DUE contains one strand of DUE and that in Bub82/c-myc/DUE-C contains another strand. This DUE is believed to coincide with the initially unwound region of the c-myc origin (29), and its deletion substantially reduced the replicator activity (30). Mcm4/6/7 unwound Bub82/lamin B2 (thymine 48%), Bub82/c-myc/DUE (37%) and Bub82/c-myc/DUE-C (39%) with similar efficiency (Figure 7A), indicating that the sequences from the c-myc origin also can serve as efficient activators of the Mcm helicase. This result also indicates that sequences with 37% thymine content can activate Mcm4/6/7 to displace 24 nt duplex on both sides in a bubble substrate, suggesting that the not only thymine content but also the sequence context may affect the Mcm helicase activation.\nIn gel shift assays, MCM4/6/7 bound to all the three bubbles, although the affinity to Bub82/c-myc/DUE and to Bub82/c-myc/DUE-C is slightly lower than that to Bub-82/lamin B2 (Figure 7B). Therefore, helicase and DNA binding activities do not necessarily correlate with each other. This was also indicated by our previous results that guanine and cytosine stretches can bind to Mcm but cannot activate the helicase (13).\n\nDNA unwinding by Mcm4/6/7 is inhibited by the GC-rich sequences on the duplex segment\nOur results indicate that thymine-rich single-stranded DNA is required for initial loading and activation of the Mcm helicase. However, it is not known whether thymine sequences are required for processive unwinding of duplex DNA. Therefore, we have examined whether the nucleotide composition of the duplex region affects its unwinding activity. To address this issue, we constructed a series of T-tailed Y-fork structures (T-fork) containing various sequences in the duplex segment. They carried varied contents of cytosine residues on the 3′-tail strand. In gel shift assays, Mcm4/6/7 bound to these Y-fork substrates with identical affinity (Figure 8A), consistent with the notion that the Mcm4/6/7 binds to single-stranded tails. However, in DNA helicase assays, T-fork/(C:G)49 was hardly displaced by Mcm4/6/7, but was readily displaced by SV40 T-antigen DNA helicase (Figure 8B). When thymine or adenine is inserted as every third nucleotide (repeats of CCT or CCA), the extent of unwinding increased (T-fork/(CCT:GGA)16 and T-fork/(CCA:GGT)16). The efficiency of unwinding is roughly correlated with the content of GC pairs in the duplex segment [T-fork/(CCAA:GGTT)12, T-fork/(CCTT:GGAA)12, T-fork/(CAAA:GTTT)12 and T-fork/(CTTT:GAAA)12; Figure 8B]. It appears that the duplex segment containing \u003c50% GC pairs is efficiently unwound (Figure 8C).\nWe next examined the effect of GC-rich segments on a partial heteroduplex DNA on a single-stranded circular DNA. We have constructed two sets of 5′-tailed partial heteroduplex DNA substrates containing duplex regions of variable lengths; one on M13mp18 vector and the other on M13mp19 containing a 66 nt long G-rich segment downstream of the hybridizing oligonucleotide. We found that the Mcm4/6/7 helicase can displace duplex DNA up to 350 nt long on its own on the former substrate (Figure 8D, left), consistent with previous results (13). In contrast, displacement was inhibited over the GC-rich segments on the latter substrate (Figure 8D, right panel), although displacement up to 250 nt in length, albeit at a reduced level, was observed at a high concentration of Mcm4/6/7 complex. This result is consistent with that on Y-fork and indicates that GC-rich duplex segment is inhibitory for unwinding by the Mcm helicase. These results may indicate that the presence of thymine–adenine pairs with a certain frequency in the duplex region may facilitate continuous unwinding by Mcm4/6/7. Alternatively, Mcm4/6/7 is not efficient enough to displace thermodynamically stable GC-base-paired segment.\nIn order to distinguish these two possibilities, we designed a new T-fork substrate containing inosine (I) residue instead of guanosine residue. The thermal stability of the I:C base pair is lower than that of the G:C base pair in duplex DNA due to loss of one hydrogen bond and is even lower than A:T base pair (31). We constructed the T-tailed fork substrates containing the (GCC:CGG)10, (GCC:CIG)10 or (GAA:CTT)10 duplex DNA segment (Figure 8E). Mcm4/6/7 hardly displaced the 31 nt long duplex of GCC:CGG repeats, whereas the T-fork/(GAA:CTT)10 was displaced efficiently, as described above. T-fork/(GCC:CIG)10 was displaced with efficiency much greater than that of T-fork/(GCC:CGG)10, indicating that the thermostability of the duplex segment, not the lack of AT base pair, is responsible for inability of Mcm4/6/7 to displace the duplex."}

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complex primarily interacts with the single-stranded DNA segment\nMcm4/6/7 binds to ‘bubble’ DNA substrates and unwinds the duplex segments when the central single-stranded segment contains thymine stretches (13). In order to examine the mode of binding of Mcm4/6/7 on bubble DNAs, we conducted nuclease protection assays using labeled bubble substrate DNAs and Mcm4/6/7 in the presence of ATP-γ-S which permits binding to substrate DNA but does not mobilize the helicase. At an optimum concentration of DNase I, strong cleavages were detected on the 21 bp duplex regions at both ends of the substrates, whereas weaker cleavages were detected on the central single-stranded region, consistent with preference of DNase I to double-stranded DNA. With the Bub66/T-rich substrate, strong protection was detected on the entire single-stranded regions of both top and bottom strands with increasing concentration of Mcm4/6/7, consistent with high affinity of Mcm4/6/7 to T-rich bubble sequences (Figure 1A). Similar, but less significant protection was detected on the single-stranded DNA segment with P1 nucleases (Figure 1A), which is specific to single-stranded DNA. The results indicate that the Mcm complex is loaded onto bubble DNA through binding to both strands of the single-stranded region. Careful examination of Mcm4/6/7 footprints on a bubble indicated strong protection on the 5′-half of the top strand and moderate protection on the remaining 3′-half, as well as on several base-pair duplex segment adjacent to the branch point (Figure 1A and data not shown). A similar pattern of protection was observed also on the bottom strand. This suggests that Mcm4/6/7 may bind to a replication bubble substrate with a 2-fold symmetry as a double hexamer (Figure 1A, see the lower scheme), in a manner similar to SV40 T-antigen (21).\nNuclease protection assays were conducted also on a T-tailed Y-fork structure (Figure 1B). Not only the single-stranded tail region but also the 7 bp duplex DNA adjacent to the duplex-to-single-strand junction were protected by Mcm binding from DNaseI digestion. These results indicate that Mcm4/6/7 protein primarily interacts with single-stranded DNA region and that the interaction also spans the duplex segments near the branchpoint of the replication fork.\n\nFormation of double hexameric Mcm4/6/7 complexes facilitates helicase actions on bubble substrates\nThe above results suggest that Mcm4/6/7 generates a double hexameric complex on a bubble, each hexamer of which makes symmetric contact with the 5′-proximal central single-stranded segment. This predicts that the single-stranded segment needs to be of a sufficient length in order to accommodate the Mcm complex. In fact, we previously showed that the Mcm4/6/7 mainly forms a single hexameric complex on bubble-20 (a bubble substrate with 20 nt long central single-stranded segment) and a double hexameric complex on bubble-60 DNA (13). In order to determine the minimum requirement for double-hexamer formation, a set of synthetic bubble-like substrates (Bub-T10, Bub-T20, Bub-T30, Bub-T40 and Bub-T50) that differed in the length of the central unpaired segment were constructed, and the binding and helicase activities of Mcm4/6/7 on these substrates were examined. Mcm4/6/7 was incubated with a radiolabeled synthetic bubble substrate in the presence of 0.5 mM ATP-γ-S to allow complex formation. A half of these reaction mixtures were analyzed for DNA binding in gel shift assays (Figure 2A), and the remainder was further incubated in the presence of 10 mM ATP to measure DNA helicase activity (Figure 2B). Bub-10 generated only a low level of complexes with Mcm4/6/7, and Bub-20 generated primarily a single mobility-shifted form, which may contain a single hexamer of Mcm4/6/7. On Bub-30, significant amount of complexes containing a double hexamer were generated in addition to those containing a single hexamer (Figure 2A) (13,21). The amounts of double hexamer complexes increased on Bub-T40 and Bub-T50 with concomitant decrease of single hexamer complexes (Figure 2A). The results indicate that a single-stranded segment of at least 40 nt long is required for efficient loading of the double-hexameric Mcm helicase on a bubble substrate.\nIn DNA helicase assays, Mcm4/6/7 complex did not show helicase activity on either Bub-10 or Bub-20 substrate. The efficiency of displacement slightly improved as the length of the single-stranded segment increased up to 30 nt. On Bub-T40 and Bub-T50, on the other hand, significant displacement was observed, indicating that a single-stranded segment of at least 40 nt long is required for efficient helicase actions on bubble substrates (Figure 2B). Taken together, the above results are consistent with the notion that the Mcm4/6/7 complex, loaded onto DNA as a double hexameric complex, efficiently unwinds the duplex region of the substrate DNA.\n\nBoth strands of thymine-rich single-stranded segments are required for efficient unwinding of bubble DNA by Mcm4/6/7\nSymmetric binding of the Mcm4/6/7 double hexamer to bubble suggests that each hexamer catalyzes unwinding of one of the two duplex segments. We asked whether activation of both hexamers is required for unwinding of the bubble substrate. The preferred bubble substrate which is efficiently unwound by Mcm4/6/7 contains thymine stretches on both strands of the single-stranded segment. We constructed a hetero-bubble (Bub66/T–G-rich) in which one strand is T-rich (same as Bub66/T-rich) and the other strand is G-rich (same as Bub66/G-rich) (13), and helicase assays were conducted with increasing amount of Mcm4/6/7. Only weak unwinding was detected on this substrate compared to Bub66/T-rich (Figure 3A). Since Mcm4/6/7 can bind to Bub66/T–G-rich and forms a double hexameric complex (data not shown), the defective unwinding is not due to inefficient loading of the helicase onto the substrate. If one hexamer interacting with the thymine-rich strand dissociates from the other hexamer and displaces only one of the duplex segments, then it would result in generation of Y-fork structures which could not be further displaced due to the presence of G-rich 3′-tail and would appear on the gel. However, we did not detect such intermediates during the course of the experiment (Figure 3B), suggesting that bubble can be displaced efficiently only when two molecules of the Mcm4/6/7 hexamers are simultaneously activated.\n\nBinding and helicase actions of Mcm4/6/7 on forked and 3′- or 5′-extension substrates\nIn order to examine more precisely the interaction and helicase actions with forked substrates, Y-fork substrates containing a nascent leading strand (A-fork[3′]), nascent lagging strand (A-fork[5′]), or both of them (A-fork[3′,5′]), as well as 5′-extension or 3′-extension structures were constructed. Mcm4/6/7 bound to A-fork[3′] or A-fork[5′] with affinity similar to that of a simple Y-fork (Figure 4A and data not shown). In contrast, PriA helicase, used as a control, bound to A-fork[3′] more efficiently than to A-fork[5′], as reported previously (23,25). Mcm4/6/7 bound also to 5′-extension and 3′-extension, albeit with slightly reduced affinity compared to A-fork[3′] and A-fork[5′] (Figure 4A). Mcm4/6/7 bound to A-fork[3′,5′] with much lower affinity, and the complex gave rise to a single band. These findings indicate that the Mcm4/6/7 complex is loaded onto DNA preferentially and efficiently through single-stranded region, regardless of the presence of 3′- or 5′-terminus.\nIn contrast, only the substrate containing a 3′ single-stranded DNA tail (A-fork[5′]) was efficiently unwound and A-fork[3′] or A-fork[3′,5′], was not unwound by Mcm4/6/7 (Figure 4B). Absence of helicase actions on A-fork[3′,5′] composed only of duplex regions is expected since double-stranded DNA is not able to activate the ATPase activity of Mcm4/6/7 (10). In contrast, the PriA, a structure-specific helicase used as a control, binds at the fork junction and unwinds the fork and the nascent lagging strand DNA on A-fork[5′], or unwinds the nascent lagging strand on A-fork[3′,5′], as reported before (25). These results indicate that the Mcm4/6/7 complex binds to single-stranded DNA and that its helicase is activated only in the presence of a single-stranded 3′-tail.\n\n3′-extension with poly(dT) tail is displaced by Mcm4/6/7\nIt has been reported that the 3′-extension can be unwound by the archaeal Mcm homohexamer but not by fission and budding yeast Mcm complexes (14,26,27). We have constructed 3′-extension substrates containing poly(dT), poly(dA), poly(dC) and poly(dG) 3′-tails in order to examine whether mouse Mcm4/6/7 can displace these substrates. We first found that Mcm4/6/7 binds to dT-, dC- and dG-3′-extension with similar affinity, and to dA-3′-extension with much lower affinity (Figure 5A). This is consistent with the previous results that Mcm4/6/7 binds to 50mer oligo-dT, -dC and -dG, but not to a 50mer oligo-dA (13). We found that dT-tailed 3′-extension was displaced efficiently by Mcm 4/6/7 while almost no or very little activity was detected on other substrates (Figure 5B and C). This is in sharp contrast to yeast Mcm4/6/7 helicases which are not capable of unwinding 3′-extension substrates. Furthermore, dT-tailed 5′-extension, to which Mcm4/6/7 could bind, was not displaced by the Mcm helicase. The addition of the 5′-tail to dT-tailed 3′-extension further stimulated the displacement (Figure 5D), confirming the previous report that the fork structures facilitate the helicase action. Thus, these results further strengthen our conclusion that the mammalian Mcm helicase is generally activated by the thymine-stretch on the 3′-single-stranded tail.\n\nThe effects of the thymine content of the 3′-tail on Mcm helicase activity\nWe next examined more systematically the effect of the compositions of the thymine residues of the 3′-tail on the Mcm helicase activity. A partial heteroduplex M13 single-stranded DNA containing a 37 bp duplex region in the presence or absence of the 50 nt long 3′-tail of various nucleotide compositions were constructed and the unwinding by mouse Mcm4/6/7 was examined (Figure 6A). Due to its low processivity, Mcm4/6/7 barely displaced the annealed 37mer oligonucleotide without a 3′-tail (37mer; Figure 6A). Only weak helicase activity was observed on the substrate carrying the 3′-tail of 25 repeats of TA dinucleotide (37-TA25; Figure 6A), whereas strong helicase activity was observed on 37-TTA17. Increase of thymine content on the 3′-tail did not further increase the extent of unwinding (37-TTTA13, 37-TTTTA10 and 37-T50; Figure 6A), suggesting that 17 repeats of TT dinucleotides (67% thymine) may be sufficient for activation of Mcm helicase. It should be noted that the TA25 tail would self-anneal and this would prevent the loading of Mcm, since the 3′-tail containing TTAA13 or TTTAAA8 did not enhance the unwinding either (data not shown). Therefore, we next examined the effects of repeating sequences of thymine and cytosine (Figure 6B). Partial heteroduplex substrates containing the 3′-tail of TC25, TTCC13, TTTCCC8, TTTTCCCC6, TTCC17 were displaced by the Mcm4/6/7 complex to the extent similar to that achieved by TTA17, suggesting that 50% thymine content is sufficient for full activation of Mcm helicase. TTCC13 and TTCC17 were displaced to a similar extent, consistent with the earlier result that a 40 nt tail is sufficient for activation (13). However, the efficiency of the displacement significantly decreased as the thymine content of the 3′-tail dropped to 33%, as in TAA17 or TCC17 (Figure 6B and C). Thus, the minimal thymine content required for activation of the Mcm helicase may be somewhere between 33 and 50%.\n\nDUE sequences from the c-myc origin activate Mcm helicase\nOur previous studies have shown that the sequences containing periodic (dT)n tracts derived from the human lamin B2 origin (48% thymine content) can serve as an efficient activator for the Mcm helicase on a bubble, and replacement of thymines with guanines abolished the helicase activation (13,28). In order to examine other natural replication origins with different thymine contents for the ability to activate Mcm helicase on a bubble substrate, we constructed new bubble substrates, Bub82/c-myc, containing sequences derived from the DUE (DNA unwinding element) region of the human c-myc origin which is essential for c-myc replicator activity (29,30). The unpaired segment in Bub82/c-myc/DUE contains one strand of DUE and that in Bub82/c-myc/DUE-C contains another strand. This DUE is believed to coincide with the initially unwound region of the c-myc origin (29), and its deletion substantially reduced the replicator activity (30). Mcm4/6/7 unwound Bub82/lamin B2 (thymine 48%), Bub82/c-myc/DUE (37%) and Bub82/c-myc/DUE-C (39%) with similar efficiency (Figure 7A), indicating that the sequences from the c-myc origin also can serve as efficient activators of the Mcm helicase. This result also indicates that sequences with 37% thymine content can activate Mcm4/6/7 to displace 24 nt duplex on both sides in a bubble substrate, suggesting that the not only thymine content but also the sequence context may affect the Mcm helicase activation.\nIn gel shift assays, MCM4/6/7 bound to all the three bubbles, although the affinity to Bub82/c-myc/DUE and to Bub82/c-myc/DUE-C is slightly lower than that to Bub-82/lamin B2 (Figure 7B). Therefore, helicase and DNA binding activities do not necessarily correlate with each other. This was also indicated by our previous results that guanine and cytosine stretches can bind to Mcm but cannot activate the helicase (13).\n\nDNA unwinding by Mcm4/6/7 is inhibited by the GC-rich sequences on the duplex segment\nOur results indicate that thymine-rich single-stranded DNA is required for initial loading and activation of the Mcm helicase. However, it is not known whether thymine sequences are required for processive unwinding of duplex DNA. Therefore, we have examined whether the nucleotide composition of the duplex region affects its unwinding activity. To address this issue, we constructed a series of T-tailed Y-fork structures (T-fork) containing various sequences in the duplex segment. They carried varied contents of cytosine residues on the 3′-tail strand. In gel shift assays, Mcm4/6/7 bound to these Y-fork substrates with identical affinity (Figure 8A), consistent with the notion that the Mcm4/6/7 binds to single-stranded tails. However, in DNA helicase assays, T-fork/(C:G)49 was hardly displaced by Mcm4/6/7, but was readily displaced by SV40 T-antigen DNA helicase (Figure 8B). When thymine or adenine is inserted as every third nucleotide (repeats of CCT or CCA), the extent of unwinding increased (T-fork/(CCT:GGA)16 and T-fork/(CCA:GGT)16). The efficiency of unwinding is roughly correlated with the content of GC pairs in the duplex segment [T-fork/(CCAA:GGTT)12, T-fork/(CCTT:GGAA)12, T-fork/(CAAA:GTTT)12 and T-fork/(CTTT:GAAA)12; Figure 8B]. It appears that the duplex segment containing \u003c50% GC pairs is efficiently unwound (Figure 8C).\nWe next examined the effect of GC-rich segments on a partial heteroduplex DNA on a single-stranded circular DNA. We have constructed two sets of 5′-tailed partial heteroduplex DNA substrates containing duplex regions of variable lengths; one on M13mp18 vector and the other on M13mp19 containing a 66 nt long G-rich segment downstream of the hybridizing oligonucleotide. We found that the Mcm4/6/7 helicase can displace duplex DNA up to 350 nt long on its own on the former substrate (Figure 8D, left), consistent with previous results (13). In contrast, displacement was inhibited over the GC-rich segments on the latter substrate (Figure 8D, right panel), although displacement up to 250 nt in length, albeit at a reduced level, was observed at a high concentration of Mcm4/6/7 complex. This result is consistent with that on Y-fork and indicates that GC-rich duplex segment is inhibitory for unwinding by the Mcm helicase. These results may indicate that the presence of thymine–adenine pairs with a certain frequency in the duplex region may facilitate continuous unwinding by Mcm4/6/7. Alternatively, Mcm4/6/7 is not efficient enough to displace thermodynamically stable GC-base-paired segment.\nIn order to distinguish these two possibilities, we designed a new T-fork substrate containing inosine (I) residue instead of guanosine residue. The thermal stability of the I:C base pair is lower than that of the G:C base pair in duplex DNA due to loss of one hydrogen bond and is even lower than A:T base pair (31). We constructed the T-tailed fork substrates containing the (GCC:CGG)10, (GCC:CIG)10 or (GAA:CTT)10 duplex DNA segment (Figure 8E). Mcm4/6/7 hardly displaced the 31 nt long duplex of GCC:CGG repeats, whereas the T-fork/(GAA:CTT)10 was displaced efficiently, as described above. T-fork/(GCC:CIG)10 was displaced with efficiency much greater than that of T-fork/(GCC:CGG)10, indicating that the thermostability of the duplex segment, not the lack of AT base pair, is responsible for inability of Mcm4/6/7 to displace the duplex."}

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complex primarily interacts with the single-stranded DNA segment\nMcm4/6/7 binds to ‘bubble’ DNA substrates and unwinds the duplex segments when the central single-stranded segment contains thymine stretches (13). In order to examine the mode of binding of Mcm4/6/7 on bubble DNAs, we conducted nuclease protection assays using labeled bubble substrate DNAs and Mcm4/6/7 in the presence of ATP-γ-S which permits binding to substrate DNA but does not mobilize the helicase. At an optimum concentration of DNase I, strong cleavages were detected on the 21 bp duplex regions at both ends of the substrates, whereas weaker cleavages were detected on the central single-stranded region, consistent with preference of DNase I to double-stranded DNA. With the Bub66/T-rich substrate, strong protection was detected on the entire single-stranded regions of both top and bottom strands with increasing concentration of Mcm4/6/7, consistent with high affinity of Mcm4/6/7 to T-rich bubble sequences (Figure 1A). Similar, but less significant protection was detected on the single-stranded DNA segment with P1 nucleases (Figure 1A), which is specific to single-stranded DNA. The results indicate that the Mcm complex is loaded onto bubble DNA through binding to both strands of the single-stranded region. Careful examination of Mcm4/6/7 footprints on a bubble indicated strong protection on the 5′-half of the top strand and moderate protection on the remaining 3′-half, as well as on several base-pair duplex segment adjacent to the branch point (Figure 1A and data not shown). A similar pattern of protection was observed also on the bottom strand. This suggests that Mcm4/6/7 may bind to a replication bubble substrate with a 2-fold symmetry as a double hexamer (Figure 1A, see the lower scheme), in a manner similar to SV40 T-antigen (21).\nNuclease protection assays were conducted also on a T-tailed Y-fork structure (Figure 1B). Not only the single-stranded tail region but also the 7 bp duplex DNA adjacent to the duplex-to-single-strand junction were protected by Mcm binding from DNaseI digestion. These results indicate that Mcm4/6/7 protein primarily interacts with single-stranded DNA region and that the interaction also spans the duplex segments near the branchpoint of the replication fork.\n\nFormation of double hexameric Mcm4/6/7 complexes facilitates helicase actions on bubble substrates\nThe above results suggest that Mcm4/6/7 generates a double hexameric complex on a bubble, each hexamer of which makes symmetric contact with the 5′-proximal central single-stranded segment. This predicts that the single-stranded segment needs to be of a sufficient length in order to accommodate the Mcm complex. In fact, we previously showed that the Mcm4/6/7 mainly forms a single hexameric complex on bubble-20 (a bubble substrate with 20 nt long central single-stranded segment) and a double hexameric complex on bubble-60 DNA (13). In order to determine the minimum requirement for double-hexamer formation, a set of synthetic bubble-like substrates (Bub-T10, Bub-T20, Bub-T30, Bub-T40 and Bub-T50) that differed in the length of the central unpaired segment were constructed, and the binding and helicase activities of Mcm4/6/7 on these substrates were examined. Mcm4/6/7 was incubated with a radiolabeled synthetic bubble substrate in the presence of 0.5 mM ATP-γ-S to allow complex formation. A half of these reaction mixtures were analyzed for DNA binding in gel shift assays (Figure 2A), and the remainder was further incubated in the presence of 10 mM ATP to measure DNA helicase activity (Figure 2B). Bub-10 generated only a low level of complexes with Mcm4/6/7, and Bub-20 generated primarily a single mobility-shifted form, which may contain a single hexamer of Mcm4/6/7. On Bub-30, significant amount of complexes containing a double hexamer were generated in addition to those containing a single hexamer (Figure 2A) (13,21). The amounts of double hexamer complexes increased on Bub-T40 and Bub-T50 with concomitant decrease of single hexamer complexes (Figure 2A). The results indicate that a single-stranded segment of at least 40 nt long is required for efficient loading of the double-hexameric Mcm helicase on a bubble substrate.\nIn DNA helicase assays, Mcm4/6/7 complex did not show helicase activity on either Bub-10 or Bub-20 substrate. The efficiency of displacement slightly improved as the length of the single-stranded segment increased up to 30 nt. On Bub-T40 and Bub-T50, on the other hand, significant displacement was observed, indicating that a single-stranded segment of at least 40 nt long is required for efficient helicase actions on bubble substrates (Figure 2B). Taken together, the above results are consistent with the notion that the Mcm4/6/7 complex, loaded onto DNA as a double hexameric complex, efficiently unwinds the duplex region of the substrate DNA.\n\nBoth strands of thymine-rich single-stranded segments are required for efficient unwinding of bubble DNA by Mcm4/6/7\nSymmetric binding of the Mcm4/6/7 double hexamer to bubble suggests that each hexamer catalyzes unwinding of one of the two duplex segments. We asked whether activation of both hexamers is required for unwinding of the bubble substrate. The preferred bubble substrate which is efficiently unwound by Mcm4/6/7 contains thymine stretches on both strands of the single-stranded segment. We constructed a hetero-bubble (Bub66/T–G-rich) in which one strand is T-rich (same as Bub66/T-rich) and the other strand is G-rich (same as Bub66/G-rich) (13), and helicase assays were conducted with increasing amount of Mcm4/6/7. Only weak unwinding was detected on this substrate compared to Bub66/T-rich (Figure 3A). Since Mcm4/6/7 can bind to Bub66/T–G-rich and forms a double hexameric complex (data not shown), the defective unwinding is not due to inefficient loading of the helicase onto the substrate. If one hexamer interacting with the thymine-rich strand dissociates from the other hexamer and displaces only one of the duplex segments, then it would result in generation of Y-fork structures which could not be further displaced due to the presence of G-rich 3′-tail and would appear on the gel. However, we did not detect such intermediates during the course of the experiment (Figure 3B), suggesting that bubble can be displaced efficiently only when two molecules of the Mcm4/6/7 hexamers are simultaneously activated.\n\nBinding and helicase actions of Mcm4/6/7 on forked and 3′- or 5′-extension substrates\nIn order to examine more precisely the interaction and helicase actions with forked substrates, Y-fork substrates containing a nascent leading strand (A-fork[3′]), nascent lagging strand (A-fork[5′]), or both of them (A-fork[3′,5′]), as well as 5′-extension or 3′-extension structures were constructed. Mcm4/6/7 bound to A-fork[3′] or A-fork[5′] with affinity similar to that of a simple Y-fork (Figure 4A and data not shown). In contrast, PriA helicase, used as a control, bound to A-fork[3′] more efficiently than to A-fork[5′], as reported previously (23,25). Mcm4/6/7 bound also to 5′-extension and 3′-extension, albeit with slightly reduced affinity compared to A-fork[3′] and A-fork[5′] (Figure 4A). Mcm4/6/7 bound to A-fork[3′,5′] with much lower affinity, and the complex gave rise to a single band. These findings indicate that the Mcm4/6/7 complex is loaded onto DNA preferentially and efficiently through single-stranded region, regardless of the presence of 3′- or 5′-terminus.\nIn contrast, only the substrate containing a 3′ single-stranded DNA tail (A-fork[5′]) was efficiently unwound and A-fork[3′] or A-fork[3′,5′], was not unwound by Mcm4/6/7 (Figure 4B). Absence of helicase actions on A-fork[3′,5′] composed only of duplex regions is expected since double-stranded DNA is not able to activate the ATPase activity of Mcm4/6/7 (10). In contrast, the PriA, a structure-specific helicase used as a control, binds at the fork junction and unwinds the fork and the nascent lagging strand DNA on A-fork[5′], or unwinds the nascent lagging strand on A-fork[3′,5′], as reported before (25). These results indicate that the Mcm4/6/7 complex binds to single-stranded DNA and that its helicase is activated only in the presence of a single-stranded 3′-tail.\n\n3′-extension with poly(dT) tail is displaced by Mcm4/6/7\nIt has been reported that the 3′-extension can be unwound by the archaeal Mcm homohexamer but not by fission and budding yeast Mcm complexes (14,26,27). We have constructed 3′-extension substrates containing poly(dT), poly(dA), poly(dC) and poly(dG) 3′-tails in order to examine whether mouse Mcm4/6/7 can displace these substrates. We first found that Mcm4/6/7 binds to dT-, dC- and dG-3′-extension with similar affinity, and to dA-3′-extension with much lower affinity (Figure 5A). This is consistent with the previous results that Mcm4/6/7 binds to 50mer oligo-dT, -dC and -dG, but not to a 50mer oligo-dA (13). We found that dT-tailed 3′-extension was displaced efficiently by Mcm 4/6/7 while almost no or very little activity was detected on other substrates (Figure 5B and C). This is in sharp contrast to yeast Mcm4/6/7 helicases which are not capable of unwinding 3′-extension substrates. Furthermore, dT-tailed 5′-extension, to which Mcm4/6/7 could bind, was not displaced by the Mcm helicase. The addition of the 5′-tail to dT-tailed 3′-extension further stimulated the displacement (Figure 5D), confirming the previous report that the fork structures facilitate the helicase action. Thus, these results further strengthen our conclusion that the mammalian Mcm helicase is generally activated by the thymine-stretch on the 3′-single-stranded tail.\n\nThe effects of the thymine content of the 3′-tail on Mcm helicase activity\nWe next examined more systematically the effect of the compositions of the thymine residues of the 3′-tail on the Mcm helicase activity. A partial heteroduplex M13 single-stranded DNA containing a 37 bp duplex region in the presence or absence of the 50 nt long 3′-tail of various nucleotide compositions were constructed and the unwinding by mouse Mcm4/6/7 was examined (Figure 6A). Due to its low processivity, Mcm4/6/7 barely displaced the annealed 37mer oligonucleotide without a 3′-tail (37mer; Figure 6A). Only weak helicase activity was observed on the substrate carrying the 3′-tail of 25 repeats of TA dinucleotide (37-TA25; Figure 6A), whereas strong helicase activity was observed on 37-TTA17. Increase of thymine content on the 3′-tail did not further increase the extent of unwinding (37-TTTA13, 37-TTTTA10 and 37-T50; Figure 6A), suggesting that 17 repeats of TT dinucleotides (67% thymine) may be sufficient for activation of Mcm helicase. It should be noted that the TA25 tail would self-anneal and this would prevent the loading of Mcm, since the 3′-tail containing TTAA13 or TTTAAA8 did not enhance the unwinding either (data not shown). Therefore, we next examined the effects of repeating sequences of thymine and cytosine (Figure 6B). Partial heteroduplex substrates containing the 3′-tail of TC25, TTCC13, TTTCCC8, TTTTCCCC6, TTCC17 were displaced by the Mcm4/6/7 complex to the extent similar to that achieved by TTA17, suggesting that 50% thymine content is sufficient for full activation of Mcm helicase. TTCC13 and TTCC17 were displaced to a similar extent, consistent with the earlier result that a 40 nt tail is sufficient for activation (13). However, the efficiency of the displacement significantly decreased as the thymine content of the 3′-tail dropped to 33%, as in TAA17 or TCC17 (Figure 6B and C). Thus, the minimal thymine content required for activation of the Mcm helicase may be somewhere between 33 and 50%.\n\nDUE sequences from the c-myc origin activate Mcm helicase\nOur previous studies have shown that the sequences containing periodic (dT)n tracts derived from the human lamin B2 origin (48% thymine content) can serve as an efficient activator for the Mcm helicase on a bubble, and replacement of thymines with guanines abolished the helicase activation (13,28). In order to examine other natural replication origins with different thymine contents for the ability to activate Mcm helicase on a bubble substrate, we constructed new bubble substrates, Bub82/c-myc, containing sequences derived from the DUE (DNA unwinding element) region of the human c-myc origin which is essential for c-myc replicator activity (29,30). The unpaired segment in Bub82/c-myc/DUE contains one strand of DUE and that in Bub82/c-myc/DUE-C contains another strand. This DUE is believed to coincide with the initially unwound region of the c-myc origin (29), and its deletion substantially reduced the replicator activity (30). Mcm4/6/7 unwound Bub82/lamin B2 (thymine 48%), Bub82/c-myc/DUE (37%) and Bub82/c-myc/DUE-C (39%) with similar efficiency (Figure 7A), indicating that the sequences from the c-myc origin also can serve as efficient activators of the Mcm helicase. This result also indicates that sequences with 37% thymine content can activate Mcm4/6/7 to displace 24 nt duplex on both sides in a bubble substrate, suggesting that the not only thymine content but also the sequence context may affect the Mcm helicase activation.\nIn gel shift assays, MCM4/6/7 bound to all the three bubbles, although the affinity to Bub82/c-myc/DUE and to Bub82/c-myc/DUE-C is slightly lower than that to Bub-82/lamin B2 (Figure 7B). Therefore, helicase and DNA binding activities do not necessarily correlate with each other. This was also indicated by our previous results that guanine and cytosine stretches can bind to Mcm but cannot activate the helicase (13).\n\nDNA unwinding by Mcm4/6/7 is inhibited by the GC-rich sequences on the duplex segment\nOur results indicate that thymine-rich single-stranded DNA is required for initial loading and activation of the Mcm helicase. However, it is not known whether thymine sequences are required for processive unwinding of duplex DNA. Therefore, we have examined whether the nucleotide composition of the duplex region affects its unwinding activity. To address this issue, we constructed a series of T-tailed Y-fork structures (T-fork) containing various sequences in the duplex segment. They carried varied contents of cytosine residues on the 3′-tail strand. In gel shift assays, Mcm4/6/7 bound to these Y-fork substrates with identical affinity (Figure 8A), consistent with the notion that the Mcm4/6/7 binds to single-stranded tails. However, in DNA helicase assays, T-fork/(C:G)49 was hardly displaced by Mcm4/6/7, but was readily displaced by SV40 T-antigen DNA helicase (Figure 8B). When thymine or adenine is inserted as every third nucleotide (repeats of CCT or CCA), the extent of unwinding increased (T-fork/(CCT:GGA)16 and T-fork/(CCA:GGT)16). The efficiency of unwinding is roughly correlated with the content of GC pairs in the duplex segment [T-fork/(CCAA:GGTT)12, T-fork/(CCTT:GGAA)12, T-fork/(CAAA:GTTT)12 and T-fork/(CTTT:GAAA)12; Figure 8B]. It appears that the duplex segment containing \u003c50% GC pairs is efficiently unwound (Figure 8C).\nWe next examined the effect of GC-rich segments on a partial heteroduplex DNA on a single-stranded circular DNA. We have constructed two sets of 5′-tailed partial heteroduplex DNA substrates containing duplex regions of variable lengths; one on M13mp18 vector and the other on M13mp19 containing a 66 nt long G-rich segment downstream of the hybridizing oligonucleotide. We found that the Mcm4/6/7 helicase can displace duplex DNA up to 350 nt long on its own on the former substrate (Figure 8D, left), consistent with previous results (13). In contrast, displacement was inhibited over the GC-rich segments on the latter substrate (Figure 8D, right panel), although displacement up to 250 nt in length, albeit at a reduced level, was observed at a high concentration of Mcm4/6/7 complex. This result is consistent with that on Y-fork and indicates that GC-rich duplex segment is inhibitory for unwinding by the Mcm helicase. These results may indicate that the presence of thymine–adenine pairs with a certain frequency in the duplex region may facilitate continuous unwinding by Mcm4/6/7. Alternatively, Mcm4/6/7 is not efficient enough to displace thermodynamically stable GC-base-paired segment.\nIn order to distinguish these two possibilities, we designed a new T-fork substrate containing inosine (I) residue instead of guanosine residue. The thermal stability of the I:C base pair is lower than that of the G:C base pair in duplex DNA due to loss of one hydrogen bond and is even lower than A:T base pair (31). We constructed the T-tailed fork substrates containing the (GCC:CGG)10, (GCC:CIG)10 or (GAA:CTT)10 duplex DNA segment (Figure 8E). Mcm4/6/7 hardly displaced the 31 nt long duplex of GCC:CGG repeats, whereas the T-fork/(GAA:CTT)10 was displaced efficiently, as described above. T-fork/(GCC:CIG)10 was displaced with efficiency much greater than that of T-fork/(GCC:CGG)10, indicating that the thermostability of the duplex segment, not the lack of AT base pair, is responsible for inability of Mcm4/6/7 to displace the duplex."}

{"project":"2_test","denotations":[{"id":"15917436-14609960-76775508","span":{"begin":226,"end":228},"obj":"14609960"},{"id":"15917436-9765408-76775509","span":{"begin":1846,"end":1848},"obj":"9765408"},{"id":"15917436-14609960-76775510","span":{"begin":2945,"end":2947},"obj":"14609960"},{"id":"15917436-14609960-76775511","span":{"begin":3947,"end":3949},"obj":"14609960"},{"id":"15917436-9765408-76775512","span":{"begin":3950,"end":3952},"obj":"9765408"},{"id":"15917436-14609960-76775513","span":{"begin":5572,"end":5574},"obj":"14609960"},{"id":"15917436-12151393-76775514","span":{"begin":7094,"end":7096},"obj":"12151393"},{"id":"15917436-12917421-76775515","span":{"begin":7097,"end":7099},"obj":"12917421"},{"id":"15917436-9305914-76775516","span":{"begin":7885,"end":7887},"obj":"9305914"},{"id":"15917436-12917421-76775517","span":{"begin":8136,"end":8138},"obj":"12917421"},{"id":"15917436-11136247-76775518","span":{"begin":8505,"end":8507},"obj":"11136247"},{"id":"15917436-13679365-76775519","span":{"begin":8508,"end":8510},"obj":"13679365"},{"id":"15917436-12975364-76775520","span":{"begin":8511,"end":8513},"obj":"12975364"},{"id":"15917436-14609960-76775521","span":{"begin":8973,"end":8975},"obj":"14609960"},{"id":"15917436-14609960-76775522","span":{"begin":11464,"end":11466},"obj":"14609960"},{"id":"15917436-14609960-76775523","span":{"begin":12097,"end":12099},"obj":"14609960"},{"id":"15917436-10720330-76775524","span":{"begin":12100,"end":12102},"obj":"10720330"},{"id":"15917436-7935372-76775525","span":{"begin":12455,"end":12457},"obj":"7935372"},{"id":"15917436-12589000-76775526","span":{"begin":12458,"end":12460},"obj":"12589000"},{"id":"15917436-7935372-76775527","span":{"begin":12673,"end":12675},"obj":"7935372"},{"id":"15917436-12589000-76775528","span":{"begin":12742,"end":12744},"obj":"12589000"},{"id":"15917436-14609960-76775529","span":{"begin":13674,"end":13676},"obj":"14609960"},{"id":"15917436-14609960-76775530","span":{"begin":15657,"end":15659},"obj":"14609960"},{"id":"15917436-4080553-76775531","span":{"begin":16633,"end":16635},"obj":"4080553"}],"text":"RESULTS\n\nMcm4/6/7 complex primarily interacts with the single-stranded DNA segment\nMcm4/6/7 binds to ‘bubble’ DNA substrates and unwinds the duplex segments when the central single-stranded segment contains thymine stretches (13). In order to examine the mode of binding of Mcm4/6/7 on bubble DNAs, we conducted nuclease protection assays using labeled bubble substrate DNAs and Mcm4/6/7 in the presence of ATP-γ-S which permits binding to substrate DNA but does not mobilize the helicase. At an optimum concentration of DNase I, strong cleavages were detected on the 21 bp duplex regions at both ends of the substrates, whereas weaker cleavages were detected on the central single-stranded region, consistent with preference of DNase I to double-stranded DNA. With the Bub66/T-rich substrate, strong protection was detected on the entire single-stranded regions of both top and bottom strands with increasing concentration of Mcm4/6/7, consistent with high affinity of Mcm4/6/7 to T-rich bubble sequences (Figure 1A). Similar, but less significant protection was detected on the single-stranded DNA segment with P1 nucleases (Figure 1A), which is specific to single-stranded DNA. The results indicate that the Mcm complex is loaded onto bubble DNA through binding to both strands of the single-stranded region. Careful examination of Mcm4/6/7 footprints on a bubble indicated strong protection on the 5′-half of the top strand and moderate protection on the remaining 3′-half, as well as on several base-pair duplex segment adjacent to the branch point (Figure 1A and data not shown). A similar pattern of protection was observed also on the bottom strand. This suggests that Mcm4/6/7 may bind to a replication bubble substrate with a 2-fold symmetry as a double hexamer (Figure 1A, see the lower scheme), in a manner similar to SV40 T-antigen (21).\nNuclease protection assays were conducted also on a T-tailed Y-fork structure (Figure 1B). Not only the single-stranded tail region but also the 7 bp duplex DNA adjacent to the duplex-to-single-strand junction were protected by Mcm binding from DNaseI digestion. These results indicate that Mcm4/6/7 protein primarily interacts with single-stranded DNA region and that the interaction also spans the duplex segments near the branchpoint of the replication fork.\n\nFormation of double hexameric Mcm4/6/7 complexes facilitates helicase actions on bubble substrates\nThe above results suggest that Mcm4/6/7 generates a double hexameric complex on a bubble, each hexamer of which makes symmetric contact with the 5′-proximal central single-stranded segment. This predicts that the single-stranded segment needs to be of a sufficient length in order to accommodate the Mcm complex. In fact, we previously showed that the Mcm4/6/7 mainly forms a single hexameric complex on bubble-20 (a bubble substrate with 20 nt long central single-stranded segment) and a double hexameric complex on bubble-60 DNA (13). In order to determine the minimum requirement for double-hexamer formation, a set of synthetic bubble-like substrates (Bub-T10, Bub-T20, Bub-T30, Bub-T40 and Bub-T50) that differed in the length of the central unpaired segment were constructed, and the binding and helicase activities of Mcm4/6/7 on these substrates were examined. Mcm4/6/7 was incubated with a radiolabeled synthetic bubble substrate in the presence of 0.5 mM ATP-γ-S to allow complex formation. A half of these reaction mixtures were analyzed for DNA binding in gel shift assays (Figure 2A), and the remainder was further incubated in the presence of 10 mM ATP to measure DNA helicase activity (Figure 2B). Bub-10 generated only a low level of complexes with Mcm4/6/7, and Bub-20 generated primarily a single mobility-shifted form, which may contain a single hexamer of Mcm4/6/7. On Bub-30, significant amount of complexes containing a double hexamer were generated in addition to those containing a single hexamer (Figure 2A) (13,21). The amounts of double hexamer complexes increased on Bub-T40 and Bub-T50 with concomitant decrease of single hexamer complexes (Figure 2A). The results indicate that a single-stranded segment of at least 40 nt long is required for efficient loading of the double-hexameric Mcm helicase on a bubble substrate.\nIn DNA helicase assays, Mcm4/6/7 complex did not show helicase activity on either Bub-10 or Bub-20 substrate. The efficiency of displacement slightly improved as the length of the single-stranded segment increased up to 30 nt. On Bub-T40 and Bub-T50, on the other hand, significant displacement was observed, indicating that a single-stranded segment of at least 40 nt long is required for efficient helicase actions on bubble substrates (Figure 2B). Taken together, the above results are consistent with the notion that the Mcm4/6/7 complex, loaded onto DNA as a double hexameric complex, efficiently unwinds the duplex region of the substrate DNA.\n\nBoth strands of thymine-rich single-stranded segments are required for efficient unwinding of bubble DNA by Mcm4/6/7\nSymmetric binding of the Mcm4/6/7 double hexamer to bubble suggests that each hexamer catalyzes unwinding of one of the two duplex segments. We asked whether activation of both hexamers is required for unwinding of the bubble substrate. The preferred bubble substrate which is efficiently unwound by Mcm4/6/7 contains thymine stretches on both strands of the single-stranded segment. We constructed a hetero-bubble (Bub66/T–G-rich) in which one strand is T-rich (same as Bub66/T-rich) and the other strand is G-rich (same as Bub66/G-rich) (13), and helicase assays were conducted with increasing amount of Mcm4/6/7. Only weak unwinding was detected on this substrate compared to Bub66/T-rich (Figure 3A). Since Mcm4/6/7 can bind to Bub66/T–G-rich and forms a double hexameric complex (data not shown), the defective unwinding is not due to inefficient loading of the helicase onto the substrate. If one hexamer interacting with the thymine-rich strand dissociates from the other hexamer and displaces only one of the duplex segments, then it would result in generation of Y-fork structures which could not be further displaced due to the presence of G-rich 3′-tail and would appear on the gel. However, we did not detect such intermediates during the course of the experiment (Figure 3B), suggesting that bubble can be displaced efficiently only when two molecules of the Mcm4/6/7 hexamers are simultaneously activated.\n\nBinding and helicase actions of Mcm4/6/7 on forked and 3′- or 5′-extension substrates\nIn order to examine more precisely the interaction and helicase actions with forked substrates, Y-fork substrates containing a nascent leading strand (A-fork[3′]), nascent lagging strand (A-fork[5′]), or both of them (A-fork[3′,5′]), as well as 5′-extension or 3′-extension structures were constructed. Mcm4/6/7 bound to A-fork[3′] or A-fork[5′] with affinity similar to that of a simple Y-fork (Figure 4A and data not shown). In contrast, PriA helicase, used as a control, bound to A-fork[3′] more efficiently than to A-fork[5′], as reported previously (23,25). Mcm4/6/7 bound also to 5′-extension and 3′-extension, albeit with slightly reduced affinity compared to A-fork[3′] and A-fork[5′] (Figure 4A). Mcm4/6/7 bound to A-fork[3′,5′] with much lower affinity, and the complex gave rise to a single band. These findings indicate that the Mcm4/6/7 complex is loaded onto DNA preferentially and efficiently through single-stranded region, regardless of the presence of 3′- or 5′-terminus.\nIn contrast, only the substrate containing a 3′ single-stranded DNA tail (A-fork[5′]) was efficiently unwound and A-fork[3′] or A-fork[3′,5′], was not unwound by Mcm4/6/7 (Figure 4B). Absence of helicase actions on A-fork[3′,5′] composed only of duplex regions is expected since double-stranded DNA is not able to activate the ATPase activity of Mcm4/6/7 (10). In contrast, the PriA, a structure-specific helicase used as a control, binds at the fork junction and unwinds the fork and the nascent lagging strand DNA on A-fork[5′], or unwinds the nascent lagging strand on A-fork[3′,5′], as reported before (25). These results indicate that the Mcm4/6/7 complex binds to single-stranded DNA and that its helicase is activated only in the presence of a single-stranded 3′-tail.\n\n3′-extension with poly(dT) tail is displaced by Mcm4/6/7\nIt has been reported that the 3′-extension can be unwound by the archaeal Mcm homohexamer but not by fission and budding yeast Mcm complexes (14,26,27). We have constructed 3′-extension substrates containing poly(dT), poly(dA), poly(dC) and poly(dG) 3′-tails in order to examine whether mouse Mcm4/6/7 can displace these substrates. We first found that Mcm4/6/7 binds to dT-, dC- and dG-3′-extension with similar affinity, and to dA-3′-extension with much lower affinity (Figure 5A). This is consistent with the previous results that Mcm4/6/7 binds to 50mer oligo-dT, -dC and -dG, but not to a 50mer oligo-dA (13). We found that dT-tailed 3′-extension was displaced efficiently by Mcm 4/6/7 while almost no or very little activity was detected on other substrates (Figure 5B and C). This is in sharp contrast to yeast Mcm4/6/7 helicases which are not capable of unwinding 3′-extension substrates. Furthermore, dT-tailed 5′-extension, to which Mcm4/6/7 could bind, was not displaced by the Mcm helicase. The addition of the 5′-tail to dT-tailed 3′-extension further stimulated the displacement (Figure 5D), confirming the previous report that the fork structures facilitate the helicase action. Thus, these results further strengthen our conclusion that the mammalian Mcm helicase is generally activated by the thymine-stretch on the 3′-single-stranded tail.\n\nThe effects of the thymine content of the 3′-tail on Mcm helicase activity\nWe next examined more systematically the effect of the compositions of the thymine residues of the 3′-tail on the Mcm helicase activity. A partial heteroduplex M13 single-stranded DNA containing a 37 bp duplex region in the presence or absence of the 50 nt long 3′-tail of various nucleotide compositions were constructed and the unwinding by mouse Mcm4/6/7 was examined (Figure 6A). Due to its low processivity, Mcm4/6/7 barely displaced the annealed 37mer oligonucleotide without a 3′-tail (37mer; Figure 6A). Only weak helicase activity was observed on the substrate carrying the 3′-tail of 25 repeats of TA dinucleotide (37-TA25; Figure 6A), whereas strong helicase activity was observed on 37-TTA17. Increase of thymine content on the 3′-tail did not further increase the extent of unwinding (37-TTTA13, 37-TTTTA10 and 37-T50; Figure 6A), suggesting that 17 repeats of TT dinucleotides (67% thymine) may be sufficient for activation of Mcm helicase. It should be noted that the TA25 tail would self-anneal and this would prevent the loading of Mcm, since the 3′-tail containing TTAA13 or TTTAAA8 did not enhance the unwinding either (data not shown). Therefore, we next examined the effects of repeating sequences of thymine and cytosine (Figure 6B). Partial heteroduplex substrates containing the 3′-tail of TC25, TTCC13, TTTCCC8, TTTTCCCC6, TTCC17 were displaced by the Mcm4/6/7 complex to the extent similar to that achieved by TTA17, suggesting that 50% thymine content is sufficient for full activation of Mcm helicase. TTCC13 and TTCC17 were displaced to a similar extent, consistent with the earlier result that a 40 nt tail is sufficient for activation (13). However, the efficiency of the displacement significantly decreased as the thymine content of the 3′-tail dropped to 33%, as in TAA17 or TCC17 (Figure 6B and C). Thus, the minimal thymine content required for activation of the Mcm helicase may be somewhere between 33 and 50%.\n\nDUE sequences from the c-myc origin activate Mcm helicase\nOur previous studies have shown that the sequences containing periodic (dT)n tracts derived from the human lamin B2 origin (48% thymine content) can serve as an efficient activator for the Mcm helicase on a bubble, and replacement of thymines with guanines abolished the helicase activation (13,28). In order to examine other natural replication origins with different thymine contents for the ability to activate Mcm helicase on a bubble substrate, we constructed new bubble substrates, Bub82/c-myc, containing sequences derived from the DUE (DNA unwinding element) region of the human c-myc origin which is essential for c-myc replicator activity (29,30). The unpaired segment in Bub82/c-myc/DUE contains one strand of DUE and that in Bub82/c-myc/DUE-C contains another strand. This DUE is believed to coincide with the initially unwound region of the c-myc origin (29), and its deletion substantially reduced the replicator activity (30). Mcm4/6/7 unwound Bub82/lamin B2 (thymine 48%), Bub82/c-myc/DUE (37%) and Bub82/c-myc/DUE-C (39%) with similar efficiency (Figure 7A), indicating that the sequences from the c-myc origin also can serve as efficient activators of the Mcm helicase. This result also indicates that sequences with 37% thymine content can activate Mcm4/6/7 to displace 24 nt duplex on both sides in a bubble substrate, suggesting that the not only thymine content but also the sequence context may affect the Mcm helicase activation.\nIn gel shift assays, MCM4/6/7 bound to all the three bubbles, although the affinity to Bub82/c-myc/DUE and to Bub82/c-myc/DUE-C is slightly lower than that to Bub-82/lamin B2 (Figure 7B). Therefore, helicase and DNA binding activities do not necessarily correlate with each other. This was also indicated by our previous results that guanine and cytosine stretches can bind to Mcm but cannot activate the helicase (13).\n\nDNA unwinding by Mcm4/6/7 is inhibited by the GC-rich sequences on the duplex segment\nOur results indicate that thymine-rich single-stranded DNA is required for initial loading and activation of the Mcm helicase. However, it is not known whether thymine sequences are required for processive unwinding of duplex DNA. Therefore, we have examined whether the nucleotide composition of the duplex region affects its unwinding activity. To address this issue, we constructed a series of T-tailed Y-fork structures (T-fork) containing various sequences in the duplex segment. They carried varied contents of cytosine residues on the 3′-tail strand. In gel shift assays, Mcm4/6/7 bound to these Y-fork substrates with identical affinity (Figure 8A), consistent with the notion that the Mcm4/6/7 binds to single-stranded tails. However, in DNA helicase assays, T-fork/(C:G)49 was hardly displaced by Mcm4/6/7, but was readily displaced by SV40 T-antigen DNA helicase (Figure 8B). When thymine or adenine is inserted as every third nucleotide (repeats of CCT or CCA), the extent of unwinding increased (T-fork/(CCT:GGA)16 and T-fork/(CCA:GGT)16). The efficiency of unwinding is roughly correlated with the content of GC pairs in the duplex segment [T-fork/(CCAA:GGTT)12, T-fork/(CCTT:GGAA)12, T-fork/(CAAA:GTTT)12 and T-fork/(CTTT:GAAA)12; Figure 8B]. It appears that the duplex segment containing \u003c50% GC pairs is efficiently unwound (Figure 8C).\nWe next examined the effect of GC-rich segments on a partial heteroduplex DNA on a single-stranded circular DNA. We have constructed two sets of 5′-tailed partial heteroduplex DNA substrates containing duplex regions of variable lengths; one on M13mp18 vector and the other on M13mp19 containing a 66 nt long G-rich segment downstream of the hybridizing oligonucleotide. We found that the Mcm4/6/7 helicase can displace duplex DNA up to 350 nt long on its own on the former substrate (Figure 8D, left), consistent with previous results (13). In contrast, displacement was inhibited over the GC-rich segments on the latter substrate (Figure 8D, right panel), although displacement up to 250 nt in length, albeit at a reduced level, was observed at a high concentration of Mcm4/6/7 complex. This result is consistent with that on Y-fork and indicates that GC-rich duplex segment is inhibitory for unwinding by the Mcm helicase. These results may indicate that the presence of thymine–adenine pairs with a certain frequency in the duplex region may facilitate continuous unwinding by Mcm4/6/7. Alternatively, Mcm4/6/7 is not efficient enough to displace thermodynamically stable GC-base-paired segment.\nIn order to distinguish these two possibilities, we designed a new T-fork substrate containing inosine (I) residue instead of guanosine residue. The thermal stability of the I:C base pair is lower than that of the G:C base pair in duplex DNA due to loss of one hydrogen bond and is even lower than A:T base pair (31). We constructed the T-tailed fork substrates containing the (GCC:CGG)10, (GCC:CIG)10 or (GAA:CTT)10 duplex DNA segment (Figure 8E). Mcm4/6/7 hardly displaced the 31 nt long duplex of GCC:CGG repeats, whereas the T-fork/(GAA:CTT)10 was displaced efficiently, as described above. T-fork/(GCC:CIG)10 was displaced with efficiency much greater than that of T-fork/(GCC:CGG)10, indicating that the thermostability of the duplex segment, not the lack of AT base pair, is responsible for inability of Mcm4/6/7 to displace the duplex."}