Prereplication-complex formation: A molecular double take?

Nature Structural and Molecular Biology

Volumn 21, Issue 1, 2014, Pages 20-25

  Yardimci, Hasan ^a,b   Walter, Johannes C ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84893787250     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2738     Document Type: Review

References (55)

1. Bell, S.P. & Kaguni, J.M. Helicase loading at chromosomal origins of replication. Cold Spring Harb. Perspect. Biol. 5, a010124 (2013).
2. Mott, M.L., Erzberger, J.P., Coons, M.M. & Berger, J.M. Structural synergy and molecular crosstalk between bacterial helicase loaders and replication initiators. Cell 135, 623-634 (2008).
3. Siddiqui, K., On, K.F. & Diffley, J.F. Regulating DNA replication in eukarya. Cold Spring Harb. Perspect. Biol. 5, a012930 (2013).
4. Boos, D., Frigola, J. & Diffley, J.F. Activation of the replicative DNA helicase: breaking up is hard to do. Curr. Opin. Cell Biol. 24, 423-430 (2012).
5. Fu, Y.V. et al. Selective bypass of a lagging strand roadblock by the eukaryotic replicative DNA helicase. Cell 146, 931-941 (2011).
6. Tanaka, S. & Araki, H. Helicase activation and establishment of replication forks at chromosomal origins of replication. Cold Spring Harb. Perspect. Biol. doi:10.1101/cshperspect.a010371 (23 July 2013).
7. Arias, E.E. & Walter, J.C. Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev. 21, 497-518 (2007).
8. Kelch, B.A., Makino, D.L., O'Donnell, M. & Kuriyan, J. Clamp loader ATPases and the evolution of DNA replication machinery. BMC Biol. 10, 34 (2012).
9. Arias-Palomo, E., O'Shea, V.L., Hood, I.V. & Berger, J.M. The bacterial DnaC helicase loader is a DnaB ring breaker. Cell 153, 438-448 (2013).
10. This structure of the DnaB-DnaC complex shows how DnaC cracks open the DnaB ring and illustrates the similarity between the loading mechanism of the bacterial helicase and the sliding clamp.
11. Bailey, S., Eliason, W.K. & Steitz, T.A. Structure of hexameric DnaB helicase and its complex with a domain of DnaG primase. Science 318, 459-463 (2007).
12. Galletto, R., Maillard, R., Jezewska, M.J. & Bujalowski, W. Global conformation of the Escherichia coli replication factor DnaC protein in absence and presence of nucleotide cofactors. Biochemistry 43, 10988-11001 (2004).
13. 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).
14. Ludlam, A.V., McNatt, M.W., Carr, K.M. & Kaguni, J.M. Essential amino acids of Escherichia coli DnaC protein in an N-terminal domain interact with DnaB helicase. J. Biol. Chem. 276, 27345-27353 (2001).
15. Bell, S.P. & Stillman, B. ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature 357, 128-134 (1992).
16. Remus, D., Beall, E.L. & Botchan, M.R. DNA topology, not DNA sequence, is a critical determinant for Drosophila ORC-DNA binding. EMBO J. 23, 897-907 (2004).
17. Vashee, S. et al. Sequence-independent DNA binding and replication initiation by the human origin recognition complex. Genes Dev. 17, 1894-1908 (2003).
18. Leonard, A.C. & Mechali, M. DNA replication origins. Cold Spring Harb. Perspect. Biol. 5, a010116 (2013).
19. Bell, S.P., Mitchell, J., Leber, J., Kobayashi, R. & Stillman, B. The multidomain structure of Orc1p reveals similarity to regulators of DNA replication and transcriptional silencing. Cell 83, 563-568 (1995).
20. Perkins, G. & Diffley, J.F. Nucleotide-dependent prereplicative complex assembly by Cdc6p, a homolog of eukaryotic and prokaryotic clamp-loaders. Mol. Cell 2, 23-32 (1998).
21. Speck, C., Chen, Z., Li, H. & Stillman, B. ATPase-dependent cooperative binding of ORC and Cdc6 to origin DNA. Nat. Struct. Mol. Biol. 12, 965-971 (2005).
22. Klemm, R.D., Austin, R.J. & Bell, S.P. Coordinate binding of ATP and origin DNA regulates the ATPase activity of the origin recognition complex. Cell 88, 493-502 (1997).
23. 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).
24. Liu, S. et al. Structural analysis of human Orc6 protein reveals a homology with transcription factor TFIIB. Proc. Natl. Acad. Sci. USA 108, 7373-7378 (2011).
25. Bleichert, F. et al. A Meier-Gorlin syndrome mutation in a conserved C-terminal helix of Orc6 impedes origin recognition complex formation. eLife 2, e00882 (2013).
26. Klemm, R.D. & Bell, S.P. ATP bound to the origin recognition complex is important for preRC formation. Proc. Natl. Acad. Sci. USA 98, 8361-8367 (2001).
27. Sun, J. et al. Cdc6-induced conformational changes in ORC bound to origin DNA revealed by cryo-electron microscopy. Structure 20, 534-544 (2012).
28. Costa, A. et al. The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nat. Struct. Mol. Biol. 18, 471-477 (2011).
29. Fletcher, R.J. et al. The structure and function of MCM from archaeal M. thermoauto-trophicum. Nat. Struct. Biol. 10, 160-167 (2003).
30. 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).
31. Remus, D. et al. Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell 139, 719-730 (2009).
32. 38, this paper shows that MCM2-7 complexes are loaded as highly stable double hexamers during pre-RC formation.
33. Bochman, M.L. & Schwacha, A. The Mcm2-7 complex has in vitro helicase activity. Mol. Cell 31, 287-293 (2008).
34. Tanaka, S. & Diffley, J.F. Interdependent nuclear accumulation of budding yeast Cdt1 and Mcm2-7 during G1 phase. Nat. Cell Biol. 4, 198-207 (2002).
35. Fernández-Cid, A. et al. An ORC/Cdc6/MCM2-7 complex is formed in a multistep reaction to serve as a platform for MCM double-hexamer assembly. Mol. Cell 50, 577-588 (2013). This paper shows that pre-RC formation involves two temporally separable rounds of MCM2-7 loading.
36. Zhang, J. et al. The interacting domains of hCdt1 and hMcm6 involved in the chromatin loading of the MCM complex in human cells. Cell Cycle 9, 4848-4857 (2010).
37. Sun, J. et al. Cryo-EM structure of a helicase loading intermediate containing ORC-Cdc6-Cdt1-MCM2-7 bound to DNA. Nat. Struct. Mol. Biol. 20, 944-951 (2013). This paper suggests that ORC-Cdc6 binds to MCM2-7-Cdt1 analogously to the binding of clamp loaders to clamps.
38. Frigola, J., Remus, D., Mehanna, A. & Diffley, J.F. ATPase-dependent quality control of DNA replication origin licensing. Nature 495, 339-343 (2013).
39. This paper illustrates how ATP hydrolysis aborts nonproductive pre-RC assembly reactions.
40. Donovan, S., Harwood, J., Drury, L.S. & Diffley, J.F. Cdc6p-dependent loading of Mcm proteins onto pre-replicative chromatin in budding yeast. Proc. Natl. Acad. Sci. USA 94, 5611-5616 (1997).
41. 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).
42. Gambus, A., Khoudoli, G.A., Jones, R.C. & Blow, J.J. MCM2-7 form double hexamers at licensed origins in Xenopus egg extract. J. Biol. Chem. 286, 11855-11864 (2011).
43. Randell, J.C., Bowers, J.L., Rodriguez, H.K. & Bell, S.P. Sequential ATP hydrolysis by Cdc6 and ORC directs loading of the Mcm2-7 helicase. Mol. Cell 21, 29-39 (2006).
44. Evrin, C. et al. In the absence of ATPase activity, pre-RC formation is blocked prior to MCM2-7 hexamer dimerization. Nucleic Acids Res. 41, 3162-3172 (2013).
45. Gillespie, P.J., Li, A. & Blow, J.J. Reconstitution of licensed replication origins on Xenopus sperm nuclei using purified proteins. BMC Biochem. 2, 15 (2001).
46. Ying, C.Y. & Gautier, J. The ATPase activity of MCM2-7 is dispensable for pre-RC assembly but is required for DNA unwinding. EMBO J. 24, 4334-4344 (2005).
47. Chen, S. & Bell, S.P. CDK prevents Mcm2-7 helicase loading by inhibiting Cdt1 interaction with Orc6. Genes Dev. 25, 363-372 (2011).
48. Lyubimov, A.Y., Costa, A., Bleichert, F., Botchan, M.R. & Berger, J.M. ATP-dependent conformational dynamics underlie the functional asymmetry of the replicative helicase from a minimalist eukaryote. Proc. Natl. Acad. Sci. USA 109, 11999-12004 (2012).
49. Takara, T.J. & Bell, S.P. Multiple Cdt1 molecules act at each origin to load replication-competent Mcm2-7 helicases. EMBO J. 30, 4885-4896 (2011).
50. Samson, R.Y. & Bell, S.D. MCM loading: an open-and-shut case? Mol. Cell 50, 457-458 (2013).
51. Chen, S., de Vries, M.A. & Bell, S.P. Orc6 is required for dynamic recruitment of Cdt1 during repeated Mcm2-7 loading. Genes Dev. 21, 2897-2907 (2007).
52. Takahashi, T., Ohara, E., Nishitani, H. & Masukata, H. Multiple ORC-binding sites are required for efficient MCM loading and origin firing in fission yeast. EMBO J. 22, 964-974 (2003).
53. Austin, R.J., Orr-Weaver, T.L. & Bell, S.P. Drosophila ORC specifically binds to ACE3, an origin of DNA replication control element. Genes Dev. 13, 2639-2649 (1999).
54. Edgar, B.A. & Orr-Weaver, T.L. Endoreplication cell cycles: more for less. Cell 105, 297-306 (2001).
55. Eaton, M.L., Galani, K., Kang, S., Bell, S.P. & MacAlpine, D.M. Conserved nucleosome positioning defines replication origins. Genes Dev. 24, 748-753 (2010).