The structural basis for MCM2–7 helicase activation by GINS and Cdc45 (original) (raw)

References

  1. Davey, M.J. & O'Donnell, M. Replicative helicase loaders: ring breakers and ring makers. Curr. Biol. 13, R594–R596 (2003).
    Article CAS PubMed Google Scholar
  2. Funnell, B.E., Baker, T.A. & Kornberg, A. In vitro assembly of a prepriming complex at the origin of the Escherichia coli chromosome. J. Biol. Chem. 262, 10327–10334 (1987).
    CAS PubMed Google Scholar
  3. Davey, M.J., Fang, L., McInerney, P., Georgescu, R.E. & O'Donnell, M. The DnaC helicase loader is a dual ATP/ADP switch protein. EMBO J. 21, 3148–3159 (2002).
    Article CAS PubMed PubMed Central Google Scholar
  4. Valle, M., Gruss, C., Halmer, L., Carazo, J.M. & Donate, L.E. Large T-antigen double hexamers imaged at the simian virus 40 origin of replication. Mol. Cell. Biol. 20, 34–41 (2000).
    Article CAS PubMed PubMed Central Google Scholar
  5. Kumar, A. et al. Model for T-antigen-dependent melting of the simian virus 40 core origin based on studies of the interaction of the beta-hairpin with DNA. J. Virol. 81, 4808–4818 (2007).
    Article CAS PubMed PubMed Central Google Scholar
  6. Schuck, S. & Stenlund, A. Assembly of a double hexameric helicase. Mol. Cell 20, 377–389 (2005).
    Article CAS PubMed Google Scholar
  7. Enemark, E.J. & Joshua-Tor, L. Mechanism of DNA translocation in a replicative hexameric helicase. Nature 442, 270–275 (2006).
    Article CAS PubMed Google Scholar
  8. Bowers, J.L., Randell, J.C., Chen, S. & Bell, S.P. ATP hydrolysis by ORC catalyzes reiterative Mcm2–7 assembly at a defined origin of replication. Mol. Cell 16, 967–978 (2004).
    Article CAS PubMed Google Scholar
  9. Remus, D. et al. Concerted loading of Mcm2–7 double hexamers around DNA during DNA replication origin licensing. Cell 139, 719–730 (2009).
    Article CAS PubMed PubMed Central Google Scholar
  10. Evrin, C. et al. A double-hexameric MCM2–7 complex is loaded onto origin DNA during licensing of eukaryotic DNA replication. Proc. Natl. Acad. Sci. USA 106, 20240–20245 (2009).
    Article CAS PubMed PubMed Central Google Scholar
  11. Moyer, S.E., Lewis, P.W. & Botchan, M.R. Isolation of the Cdc45/Mcm2–7/GINS (CMG) complex, a candidate for the eukaryotic DNA replication fork helicase. Proc. Natl. Acad. Sci. USA 103, 10236–10241 (2006).
    Article CAS PubMed PubMed Central Google Scholar
  12. Gambus, A. et al. GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat. Cell Biol. 8, 358–366 (2006).
    Article CAS PubMed Google Scholar
  13. Remus, D. & Diffley, J.F. Eukaryotic DNA replication control: lock and load, then fire. Curr. Opin. Cell Biol. 21, 771–777 (2009).
    Article CAS PubMed Google Scholar
  14. Calzada, A., Hodgson, B., Kanemaki, M., Bueno, A. & Labib, K. Molecular anatomy and regulation of a stable replisome at a paused eukaryotic DNA replication fork. Genes Dev. 19, 1905–1919 (2005).
    Article CAS PubMed PubMed Central Google Scholar
  15. Ilves, I., Petojevic, T., Pesavento, J.J. & Botchan, M.R. Activation of the MCM2–7 helicase by association with Cdc45 and GINS proteins. Mol. Cell 37, 247–258 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  16. Pacek, M., Tutter, A.V., Kubota, Y., Takisawa, H. & Walter, J.C. Localization of MCM2–7, Cdc45, and GINS to the site of DNA unwinding during eukaryotic DNA replication. Mol. Cell 21, 581–587 (2006).
    Article CAS PubMed Google Scholar
  17. MacNeill, S.A. Structure and function of the GINS complex, a key component of the eukaryotic replisome. Biochem. J. 425, 489–500 (2010).
    Article CAS PubMed Google Scholar
  18. Fletcher, R.J. et al. The structure and function of MCM from archaeal M. thermoautotrophicum. Nat. Struct. Biol. 10, 160–167 (2003).
    Article CAS PubMed Google Scholar
  19. McGeoch, A.T., Trakselis, M.A., Laskey, R.A. & Bell, S.D. Organization of the archaeal MCM complex on DNA and implications for the helicase mechanism. Nat. Struct. Mol. Biol. 12, 756–762 (2005).
    Article CAS PubMed Google Scholar
  20. Iyer, L.M., Leipe, D.D., Koonin, E.V. & Aravind, L. Evolutionary history and higher order classification of AAA+ ATPases. J. Struct. Biol. 146, 11–31 (2004).
    Article CAS PubMed Google Scholar
  21. Davey, M.J., Indiani, C. & O'Donnell, M. Reconstitution of the Mcm2–7p heterohexamer, subunit arrangement, and ATP site architecture. J. Biol. Chem. 278, 4491–4499 (2003).
    Article CAS PubMed Google Scholar
  22. Crevel, G., Ivetic, A., Ohno, K., Yamaguchi, M. & Cotterill, S. Nearest neighbour analysis of MCM protein complexes in Drosophila melanogaster. Nucleic Acids Res. 29, 4834–4842 (2001).
    Article CAS PubMed PubMed Central Google Scholar
  23. Bochman, M.L., Bell, S.P. & Schwacha, A. Subunit organization of Mcm2–7 and the unequal role of active sites in ATP hydrolysis and viability. Mol. Cell. Biol. 28, 5865–5873 (2008).
    Article CAS PubMed PubMed Central Google Scholar
  24. Pape, T. et al. Hexameric ring structure of the full-length archaeal MCM protein complex. EMBO Rep. 4, 1079–1083 (2003).
    Article CAS PubMed PubMed Central Google Scholar
  25. Brewster, A.S. et al. Crystal structure of a near-full-length archaeal MCM: functional insights for an AAA+ hexameric helicase. Proc. Natl. Acad. Sci. USA 105, 20191–20196 (2008).
    Article CAS PubMed PubMed Central Google Scholar
  26. Bae, B. et al. Insights into the architecture of the replicative helicase from the structure of an archaeal MCM homolog. Structure 17, 211–222 (2009).
    Article CAS PubMed Google Scholar
  27. Yu, X. et al. The Methanobacterium thermoautotrophicum MCM protein can form heptameric rings. EMBO Rep. 3, 792–797 (2002).
    Article PubMed PubMed Central Google Scholar
  28. Gómez-Llorente, Y., Fletcher, R.J., Chen, X.S., Carazo, J.M. & San Martin, C. Polymorphism and double hexamer structure in the archaeal minichromosome maintenance (MCM) helicase from Methanobacterium thermoautotrophicum. J. Biol. Chem. 280, 40909–40915 (2005).
    Article PubMed Google Scholar
  29. Costa, A. et al. Structural basis of the Methanothermobacter thermautotrophicus MCM helicase activity. Nucleic Acids Res. 34, 5829–5838 (2006).
    Article CAS PubMed PubMed Central Google Scholar
  30. Chong, J.P., Hayashi, M.K., Simon, M.N., Xu, R.M. & Stillman, B. A double-hexamer archaeal minichromosome maintenance protein is an ATP-dependent DNA helicase. Proc. Natl. Acad. Sci. USA 97, 1530–1535 (2000).
    Article CAS PubMed PubMed Central Google Scholar
  31. Kelman, Z., Lee, J.K. & Hurwitz, J. The single minichromosome maintenance protein of Methanobacterium thermoautotrophicum DeltaH contains DNA helicase activity. Proc. Natl. Acad. Sci. USA 96, 14783–14788 (1999).
    Article CAS PubMed PubMed Central Google Scholar
  32. Bochman, M.L. & Schwacha, A. The Mcm2–7 complex has in vitro helicase activity. Mol. Cell 31, 287–293 (2008).
    Article CAS PubMed Google Scholar
  33. Kanemaki, M., Sanchez-Diaz, A., Gambus, A. & Labib, K. Functional proteomic identification of DNA replication proteins by induced proteolysis in vivo. Nature 423, 720–724 (2003).
    Article CAS PubMed Google Scholar
  34. Takayama, Y. et al. GINS, a novel multiprotein complex required for chromosomal DNA replication in budding yeast. Genes Dev. 17, 1153–1165 (2003).
    Article CAS PubMed PubMed Central Google Scholar
  35. Boskovic, J. et al. Molecular architecture of the human GINS complex. EMBO Rep. 8, 678–684 (2007).
    Article CAS PubMed PubMed Central Google Scholar
  36. Choi, J.M., Lim, H.S., Kim, J.J., Song, O.K. & Cho, Y. Crystal structure of the human GINS complex. Genes Dev. 21, 1316–1321 (2007).
    Article CAS PubMed PubMed Central Google Scholar
  37. Chang, Y.P., Wang, G., Bermudez, V., Hurwitz, J. & Chen, X.S. Crystal structure of the GINS complex and functional insights into its role in DNA replication. Proc. Natl. Acad. Sci. USA 104, 12685–12690 (2007).
    Article CAS PubMed PubMed Central Google Scholar
  38. Kamada, K., Kubota, Y., Arata, T., Shindo, Y. & Hanaoka, F. Structure of the human GINS complex and its assembly and functional interface in replication initiation. Nat. Struct. Mol. Biol. 14, 388–396 (2007).
    Article CAS PubMed Google Scholar
  39. Grob, P. et al. Cryo-electron microscopy studies of human TFIID: conformational breathing in the integration of gene regulatory cues. Structure 14, 511–520 (2006).
    Article CAS PubMed Google Scholar
  40. van Heel, M., Harauz, G., Orlova, E.V., Schmidt, R. & Schatz, M. A new generation of the IMAGIC image processing system. J. Struct. Biol. 116, 17–24 (1996).
    Article CAS PubMed Google Scholar
  41. Im, J.S. et al. Assembly of the Cdc45-Mcm2–7-GINS complex in human cells requires the Ctf4/And-1, RecQL4, and Mcm10 proteins. Proc. Natl. Acad. Sci. USA 106, 15628–15632 (2009).
    Article CAS PubMed PubMed Central Google Scholar
  42. Makarova, K.S., Wolf, Y.I., Mekhedov, S.L., Mirkin, B.G. & Koonin, E.V. Ancestral paralogs and pseudoparalogs and their role in the emergence of the eukaryotic cell. Nucleic Acids Res. 33, 4626–4638 (2005).
    Article CAS PubMed PubMed Central Google Scholar
  43. Marinsek, N. et al. GINS, a central nexus in the archaeal DNA replication fork. EMBO Rep. 7, 539–545 (2006).
    CAS PubMed PubMed Central Google Scholar
  44. Dean, F.B., Borowiec, J.A., Eki, T. & Hurwitz, J. The simian virus 40 T antigen double hexamer assembles around the DNA at the replication origin. J. Biol. Chem. 267, 14129–14137 (1992).
    CAS PubMed Google Scholar
  45. Fouts, E.T., Yu, X., Egelman, E.H. & Botchan, M.R. Biochemical and electron microscopic image analysis of the hexameric E1 helicase. J. Biol. Chem. 274, 4447–4458 (1999).
    Article CAS PubMed Google Scholar
  46. Bochman, M.L. & Schwacha, A. Differences in the single-stranded DNA binding activities of MCM2–7 and MCM467: MCM2 and MCM5 define a slow ATP-dependent step. J. Biol. Chem. 282, 33795–33804 (2007).
    Article CAS PubMed Google Scholar
  47. Labib, K. & Gambus, A. A key role for the GINS complex at DNA replication forks. Trends Cell Biol. 17, 271–278 (2007).
    Article CAS PubMed Google Scholar
  48. Takahashi, T.S., Wigley, D.B. & Walter, J.C. Pumps, paradoxes and ploughshares: mechanism of the MCM2–7 DNA helicase. Trends Biochem. Sci. 30, 437–444 (2005).
    Article CAS PubMed Google Scholar
  49. Takara, T.J. & Bell, S.P. Putting two heads together to unwind DNA. Cell 139, 652–654 (2009).
    Article CAS PubMed Google Scholar
  50. Yardimci, H., Loveland, A.B., Habuchi, S., van Oijen, A.M. & Walter, J.C. Uncoupling of sister replisomes during eukaryotic DNA replication. Mol. Cell 40, 834–840 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  51. Gould, A.D. & Shilton, B.H. Studies of the maltose transport system reveal a mechanism for coupling ATP hydrolysis to substrate translocation without direct recognition of substrate. J. Biol. Chem. 285, 11290–11296 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  52. Ludtke, S.J., Baldwin, P.R. & Chiu, W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82–97 (1999).
    Article CAS PubMed Google Scholar
  53. Voss, N.R., Yoshioka, C.K., Radermacher, M., Potter, C.S. & Carragher, B. DoG Picker and TiltPicker: software tools to facilitate particle selection in single particle electron microscopy. J. Struct. Biol. 166, 205–213 (2009).
    Article CAS PubMed PubMed Central Google Scholar
  54. van Heel, M. et al. Single-particle electron cryo-microscopy: towards atomic resolution. Q. Rev. Biophys. 33, 307–369 (2000).
    Article CAS PubMed Google Scholar
  55. Frank, J. et al. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116, 190–199 (1996).
    Article CAS PubMed Google Scholar
  56. Boekema, E.J., Berden, J.A. & van Heel, M.G. Structure of mitochondrial F1-ATPase studied by electron microscopy and image processing. Biochim. Biophys. Acta 851, 353–360 (1986).
    Article CAS PubMed Google Scholar
  57. Pettersen, E.F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
    Article CAS PubMed Google Scholar
  58. Arnold, K., Bordoli, L., Kopp, J. & Schwede, T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195–201 (2006).
    Article CAS PubMed Google Scholar
  59. Krissinel, E. & Henrick, K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60, 2256–2268 (2004).
    Article CAS PubMed Google Scholar

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