Origin Licensing Requires ATP Binding and Hydrolysis by the MCM Replicative Helicase

Molecular Cell

Volumn 55, Issue 5, 2014, Pages 666-677

  Coster, Gideon ^a   Frigola, Jordi ^a   Beuron, Fabienne ^b   Morris, EdwardP ^b   Diffley, John F X ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; HELICASE; MINICHROMOSOME MAINTENANCE PROTEIN; ORIGIN RECOGNITION COMPLEX; CDC6 PROTEIN, S CEREVISIAE; CELL CYCLE PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE; CONTROLLED STUDY; DNA REPLICATION; DNA REPLICATION ORIGIN; HYDROLYSIS; LICENSING; MUTANT; NONHUMAN; PROTEIN BINDING; PROTEIN STRUCTURE; WILD TYPE; XENOPUS; AMINO ACID SEQUENCE; BINDING SITE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; SEQUENCE ALIGNMENT;

EUKARYOTA;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; BINDING SITES; CELL CYCLE PROTEINS; DNA REPLICATION; HYDROLYSIS; MINICHROMOSOME MAINTENANCE PROTEINS; MOLECULAR SEQUENCE DATA; ORIGIN RECOGNITION COMPLEX; REPLICATION ORIGIN; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT;

EID: 84921627241     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.06.034     Document Type: Article

References (42)

1. Bell S.P., Stillman B. ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature 1992, 357:128-134.
2. Bochman M.L., Schwacha A. The Mcm2-7 complex has invitro helicase activity. Mol. Cell 2008, 31:287-293.
3. 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. 2008, 28:5865-5873.
4. 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 2004, 16:967-978.
5. Chesnokov I., Remus D., Botchan M. Functional analysis of mutant and wild-type Drosophila origin recognition complex. Proc. Natl. Acad. Sci. USA 2001, 98:11997-12002.
6. Costa A., Ilves I., Tamberg N., Petojevic T., Nogales E., Botchan M.R., Berger J.M. The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nat. Struct. Mol. Biol. 2011, 18:471-477.
7. Costa A., Hood I.V., Berger J.M. Mechanisms for initiating cellular DNA replication. Annu. Rev. Biochem. 2013, 82:25-54.
8. Dean F.B., Borowiec J.A., Eki T., Hurwitz J. The simian virus 40T antigen double hexamer assembles around the DNA at the replication origin. J. Biol. Chem. 1992, 267:14129-14137.
9. Erzberger J.P., Berger J.M. Evolutionary relationships and structural mechanisms of AAA+ proteins. Annu. Rev. Biophys. Biomol. Struct. 2006, 35:93-114.
10. Evrin C., Clarke P., Zech J., Lurz R., Sun J., Uhle S., Li H., Stillman B., Speck C. A double-hexameric MCM2-7 complex is loaded onto origin DNA during licensing of eukaryotic DNA replication. Proc. Natl. Acad. Sci. USA 2009, 106:20240-20245.
11. Evrin C., Fernández-Cid A., Zech J., Herrera M.C., Riera A., Clarke P., Brill S., Lurz R., Speck C. In the absence of ATPase activity, pre-RC formation is blocked prior to MCM2-7 hexamer dimerization. Nucleic Acids Res. 2013, 41:3162-3172.
12. Fernández-Cid A., Riera A., Tognetti S., Herrera M.C., Samel S., Evrin C., Winkler C., Gardenal E., Uhle S., Speck C. An ORC/Cdc6/MCM2-7 complex is formed in a multistep reaction to serve as a platform for MCM double-hexamer assembly. Mol. Cell 2013, 50:577-588.
13. Frigola J., Remus D., Mehanna A., Diffley J.F.X. ATPase-dependent quality control of DNA replication origin licensing. Nature 2013, 495:339-343.
14. Frolova N.S., Schek N., Tikhmyanova N., Coleman T.R. Xenopus Cdc6 performs separate functions in initiating DNA replication. Mol. Biol. Cell 2002, 13:1298-1312.
15. Giordano-Coltart J., Ying C.Y., Gautier J., Hurwitz J. Studies of the properties of human origin recognition complex and its Walker A motif mutants. Proc. Natl. Acad. Sci. USA 2005, 102:69-74.
16. Gómez E.B., Catlett M.G., Forsburg S.L. Different phenotypes invivo are associated with ATPase motif mutations in Schizosaccharomyces pombe minichromosome maintenance proteins. Genetics 2002, 160:1305-1318.
17. Houchens C.R., Lu W., Chuang R.Y., Frattini M.G., Fuller A., Simancek P., Kelly T.J. Multiple mechanisms contribute to Schizosaccharomyces pombe origin recognition complex-DNA interactions. J. Biol. Chem. 2008, 283:30216-30224.
18. 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 2010, 37:247-258.
19. Kawasaki Y., Kim H.D., Kojima A., Seki T., Sugino A. Reconstitution of Saccharomyces cerevisiae prereplicative complex assembly invitro. Genes Cells 2006, 11:745-756.
20. Klemm R.D., Bell S.P. ATP bound to the origin recognition complex is important for preRC formation. Proc. Natl. Acad. Sci. USA 2001, 98:8361-8367.
21. 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 1997, 88:493-502.
22. Labib K., Tercero J.A., Diffley J.F.X. Uninterrupted MCM2-7 function required for DNA replication fork progression. Science 2000, 288:1643-1647.
23. Masai H., Matsumoto S., You Z., Yoshizawa-Sugata N., Oda M. Eukaryotic chromosome DNA replication: where, when, and how?. Annu. Rev. Biochem. 2010, 79:89-130.
24. Mastrangelo I.A., Hough P.V., Wall J.S., Dodson M., Dean F.B., Hurwitz J. ATP-dependent assembly of double hexamers of SV40T antigen at the viral origin of DNA replication. Nature 1989, 338:658-662.
25. Méchali M. Eukaryotic DNA replication origins: many choices for appropriate answers. Nat. Rev. Mol. Cell Biol. 2010, 11:728-738.
26. Moreau M.J., McGeoch A.T., Lowe A.R., Itzhaki L.S., Bell S.D. ATPase site architecture and helicase mechanism of an archaeal MCM. Mol. Cell 2007, 28:304-314.
27. Perkins G., Diffley J.F.X. Nucleotide-dependent prereplicative complex assembly by Cdc6p, a homolog of eukaryotic and prokaryotic clamp-loaders. Mol. Cell 1998, 2:23-32.
28. Randell J.C., Bowers J.L., Rodríguez H.K., Bell S.P. Sequential ATP hydrolysis by Cdc6 and ORC directs loading of the Mcm2-7 helicase. Mol. Cell 2006, 21:29-39.
29. Ranjan A., Gossen M. A structural role for ATP in the formation and stability of the human origin recognition complex. Proc. Natl. Acad. Sci. USA 2006, 103:4864-4869.
30. Remus D., Beuron F., Tolun G., Griffith J.D., Morris E.P., Diffley J.F.X. Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell 2009, 139:719-730.
31. Rowles A., Chong J.P., Brown L., Howell M., Evan G.I., Blow J.J. Interaction between the origin recognition complex and the replication licensing system in Xenopus. Cell 1996, 87:287-296.
32. Schwacha A., Bell S.P. Interactions between two catalytically distinct MCM subgroups are essential for coordinated ATP hydrolysis and DNA replication. Mol. Cell 2001, 8:1093-1104.
33. Siddiqui K., Stillman B. ATP-dependent assembly of the human origin recognition complex. J. Biol. Chem. 2007, 282:32370-32383.
34. Skarstad K., Katayama T. Regulating DNA replication in bacteria. Cold Spring Harb. Perspect. Biol. 2013, 5:a012922.
35. Sun J., Evrin C., Samel S.A., Fernández-Cid A., Riera A., Kawakami H., Stillman B., Speck C., Li H. Cryo-EM structure of a helicase loading intermediate containing ORC-Cdc6-Cdt1-MCM2-7 bound to DNA. Nat. Struct. Mol. Biol. 2013, 20:944-951.
36. Tanaka S., Diffley J.F. Interdependent nuclear accumulation of budding yeast Cdt1 and Mcm2-7 during G1 phase. Nat. Cell Biol. 2002, 4:198-207.
37. Tang G., Peng L., Baldwin P.R., Mann D.S., Jiang W., Rees I., Ludtke S.J. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 2007, 157:38-46.
38. Vashee S., Cvetic C., Lu W., Simancek P., Kelly T.J., Walter J.C. Sequence-independent DNA binding and replication initiation by the human origin recognition complex. Genes Dev. 2003, 17:1894-1908.
39. Weinreich M., Liang C., Stillman B. The Cdc6p nucleotide-binding motif is required for loading mcm proteins onto chromatin. Proc. Natl. Acad. Sci. USA 1999, 96:441-446.
40. Yardimci H., Walter J.C. Prereplication-complex formation: a molecular double take?. Nat. Struct. Mol. Biol. 2014, 21:20-25.
41. Yekezare M., Gómez-González B., Diffley J.F.X. Controlling DNA replication origins in response to DNA damage - inhibit globally, activate locally. J. Cell Sci. 2013, 126:1297-1306.
42. 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. 2005, 24:4334-4344.