Helicase loading: How to build a MCM2-7 double-hexamer

Seminars in Cell and Developmental Biology

Volumn 30, Issue , 2014, Pages 104-109

  Riera, Alberto ^a   Tognetti, Silvia ^a   Speck, Christian ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

DNA replication; Helicase; Licensing; MCM2 7; Pre RC

Indexed keywords

ADENOSINE TRIPHOSPHATE; CELL CYCLE PROTEIN 6; CHAPERONE; DOUBLE STRANDED DNA; HELICASE; MCM2 7 DOUBLE HEXAMER; ORIGIN RECOGNITION COMPLEX; UNCLASSIFIED DRUG; MINICHROMOSOME MAINTENANCE PROTEIN;

DNA REPLICATION ORIGIN; ENZYME STRUCTURE; GENOMIC INSTABILITY; HYDROLYSIS; PROTEIN FUNCTION; REPLICON; REVIEW; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; DNA REPLICATION; HUMAN; METABOLISM; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE;

BACTERIA (MICROORGANISMS); EUKARYOTA;

ANIMALS; DNA REPLICATION; GENOMIC INSTABILITY; HUMANS; MINICHROMOSOME MAINTENANCE PROTEINS; MODELS, MOLECULAR; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; REPLICATION ORIGIN;

EID: 84901628233     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2014.03.008     Document Type: Review

References (65)

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. Liang C., Weinreich M., Stillman B. ORC and Cdc6p interact and determine the frequency of initiation of DNA replication in the genome. Cell 1995, 81:667-676.
3. Evrin C., Clarke P., Zech J., Lurz R., Sun J., Uhle S., et al. A double-hexameric MCM2-7 complex is loaded onto origin DNA during licensing of eukaryotic DNA replication. Proc Natl Acad Sci U S A 2009, 106:20240-20245.
4. Remus D., Beuron F., Tolun G., Griffith J.D., Morris E.P., Diffley J.F. Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell 2009, 139:719-730.
5. Tanaka S., Araki H. Helicase activation and establishment of replication forks at chromosomal origins of replication. Cold Spring Harb Perspect Biol 2013, 5:a010371.
6. 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 U S A 2006, 103:10236-10241.
7. Fu Y.V., Yardimci H., Long D.T., Ho T.V., Guainazzi A., Bermudez V.P., et al. Selective bypass of a lagging strand roadblock by the eukaryotic replicative DNA helicase. Cell 2011, 146:931-941.
8. Costa A., Ilves I., Tamberg N., Petojevic T., Nogales E., Botchan M.R., et al. The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nat Struct Mol Biol 2011, 18:471-477.
9. Nguyen V.Q., Co C., Li J.J. Cyclin-dependent kinases prevent DNA re-replication through multiple mechanisms. Nature 2001, 411:1068-1073.
10. Arias E.E., Walter J.C. Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev 2007, 21:497-518.
11. Jacob F., Brenner S., Cuzin F. On the regulation of DNA replication in Bacteria. Cold Spring Harbor Symp Quant Biol 1963, 28:329-438.
12. Messer W., Blaesing F., Jakimowicz D., Krause M., Majka J., Nardmann J., et al. Bacterial replication initiator DnaA. Rules for DnaA binding and roles of DnaA in origin unwinding and helicase loading. Biochimie 2001, 83:5-12.
13. Skarstad K., Katayama T. Regulating DNA replication in bacteria. Cold Spring Harb Perspect Biol 2013, 5:a012922.
14. Sekimizu K., Bramhill D., Kornberg A. ATP activates dnaA protein in initiating replication of plasmids bearing the origin of the E. coli chromosome. Cell 1987, 50:259-265.
15. Duderstadt K.E., Chuang K., Berger J.M. DNA stretching by bacterial initiators promotes replication origin opening. Nature 2011, 478:209-213.
16. Baker T.A., Sekimizu K., Funnell B.E., Kornberg A. Extensive unwinding of the plasmid template during staged enzymatic initiation of DNA replication from the origin of the Escherichia coli chromosome. Cell 1986, 45:53-64.
17. Speck C., Weigel C., Messer W. ATP- and ADP-dnaA protein, a molecular switch in gene regulation. Embo J 1999, 18:6169-6176.
18. Speck C., Messer W. Mechanism of origin unwinding: sequential binding of DnaA to double- and single-stranded DNA. Embo J 2001, 20:1469-1476.
19. Mantiero D., Mackenzie A., Donaldson A., Zegerman P. Limiting replication initiation factors execute the temporal programme of origin firing in budding yeast. Embo J 2011, 30:4805-4814.
20. Collart C., Allen G.E., Bradshaw C.R., Smith J.C., Zegerman P. Titration of four replication factors is essential for the Xenopus laevis midblastula transition. Science 2013, 341:893-896.
21. O'Donnell M., Langston L., Stillman B. Principles and concepts of DNA replication in bacteria, archaea, and eukarya. Cold Spring Harb Perspect Biol 2013, 5.
22. Marahrens Y., Stillman B. A yeast chromosomal origin of DNA replication defined by multiple functional elements. Science 1992, 255:817-823.
23. Speck C., Chen Z., Li H., Stillman B. ATPase-dependent cooperative binding of ORC and Cdc6 to origin DNA. Nat Struct Mol Biol 2005, 12:965-971.
24. Speck C., Stillman B. Cdc6 ATPase activity regulates ORC x Cdc6 stability and the selection of specific DNA sequences as origins of DNA replication. J Biol Chem 2007, 282:11705-11714.
25. Mechali M., Yoshida K., Coulombe P., Pasero P. Genetic and epigenetic determinants of DNA replication origins, position and activation. Curr Opin Genet Dev 2013, 23:124-131.
26. MacAlpine H.K., Gordan R., Powell S.K., Hartemink A.J., MacAlpine D.M. Drosophila ORC localizes to open chromatin and marks sites of cohesin complex loading. Genome Res 2010, 20:201-211.
27. Xu J., Yanagisawa Y., Tsankov A.M., Hart C., Aoki K., Kommajosyula N., et al. Genome-wide identification and characterization of replication origins by deep sequencing. Genome Biol 2012, 13:R27.
28. Eaton M.L., Galani K., Kang S., Bell S.P., MacAlpine D.M. Conserved nucleosome positioning defines replication origins. Genes Dev 2010, 24:748-753.
29. Papior P., Arteaga-Salas J.M., Gunther T., Grundhoff A., Schepers A. Open chromatin structures regulate the efficiencies of pre-RC formation and replication initiation in Epstein-Barr virus. J Cell Biol 2012, 198:509-528.
30. Remus D., Beall E.L., Botchan M.R. DNA topology, not DNA sequence, is a critical determinant for Drosophila ORC-DNA binding. Embo J 2004, 23:897-907.
31. Hoshina S., Yura K., Teranishi H., Kiyasu N., Tominaga A., Kadoma H., et al. Human origin recognition complex binds preferentially to G-quadruplex-preferable RNA and single-stranded DNA. J Biol Chem 2013, 288:30161-30171.
32. Thomae A.W., Pich D., Brocher J., Spindler M.P., Berens C., Hock R., et al. Interaction between HMGA1a and the origin recognition complex creates site-specific replication origins. Proc Natl Acad Sci U S A 2008, 105:1692-1697.
33. Shen Z., Sathyan K.M., Geng Y., Zheng R., Chakraborty A., Freeman B., et al. A WD-repeat protein stabilizes ORC binding to chromatin. Mol Cell 2010, 40:99-111.
34. Vermeulen M., Eberl H.C., Matarese F., Marks H., Denissov S., Butter F., et al. Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 2010, 142:967-980.
35. Thomae A.W., Baltin J., Pich D., Deutsch M.J., Ravasz M., Zeller K., et al. Different roles of the human Orc6 protein in the replication initiation process. Cell Mol Life Sci 2011, 68:3741-3756.
36. Takeda D.Y., Shibata Y., Parvin J.D., Dutta A. Recruitment of ORC or CDC6 to DNA is sufficient to create an artificial origin of replication in mammalian cells. Genes Dev 2005, 19:2827-2836.
37. Blow J.J., Ge X.Q., Jackson D.A. How dormant origins promote complete genome replication. Trends Biochem Sci 2011, 36:405-414.
38. 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.
39. 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.
40. Takahashi N., Yamaguchi Y., Yamairi F., Makise M., Takenaka H., Tsuchiya T., et al. Analysis on origin recognition complex containing Orc5p with defective Walker A motif. J Biol Chem 2004, 279:8469-8477.
41. Chesnokov I.N., Chesnokova O.N., Botchan M. A cytokinetic function of Drosophila ORC6 protein resides in a domain distinct from its replication activity. Proc Natl Acad Sci U S A 2003, 100:9150-9155.
42. Sun J., Kawakami H., Zech J., Speck C., Stillman B., Li H. Cdc6-induced conformational changes in ORC bound to origin DNA revealed by cryo-electron microscopy. Structure 2012, 20:534-544.
43. Sun J., Evrin C., Samel S.A., Fernandez-Cid A., Riera A., Kawakami H., et al. 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.
44. 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.
45. Frigola J., Remus D., Mehanna A., Diffley J.F. ATPase-dependent quality control of DNA replication origin licensing. Nature 2013, 495:339-343.
46. Evrin C., Fernandez-Cid A., Zech J., Herrera M.C., Riera A., Clarke P., et al. In the absence of ATPase activity, pre-RC formation is blocked prior to MCM2-7 hexamer dimerization. Nucleic Acids Res 2013, 41:3162-3172.
47. Fernandez-Cid A., Riera A., Tognetti S., Herrera M.C., Samel S., Evrin C., 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 2013, 50:577-588.
48. 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 2006, 21:29-39.
49. 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.
50. Kornberg A. Control of initiation of the Escherichia coli chromosome. Cold Spring Harb Symp Quant Biol 1991, 56:275-278.
51. Arias-Palomo E., O'Shea V.L., Hood I.V., Berger J.M. The bacterial DnaC helicase loader is a DnaB ring breaker. Cell 2013, 153:438-448.
52. Riera A., Li H., Speck C. Seeing is believing: the MCM2-7 helicase trapped in complex with its DNA loader. Cell Cycle 2013, 12:2917-2918.
53. Yardimci H., Walter J.C. Prereplication-complex formation: a molecular double take. Nat Struct Mol Biol 2014, 21:20-25.
54. Evrin C., Fernandez-Cid A., Riera A., Zech J., Clarke P., Herrera M.C., et al. The ORC/Cdc6/MCM2-7 complex facilitates MCM2-7 dimerization during prereplicative complex formation. Nucleic Acids Res 2014, 42:2257-2269.
55. Nieduszynski C.A., Knox Y., Donaldson A.D. Genome-wide identification of replication origins in yeast by comparative genomics. Genes Dev 2006, 20:1874-1879.
56. Hartl F.U., Hayer-Hartl M. Converging concepts of protein folding in vitro and in vivo. Nat Struct Mol Biol 2009, 16:574-581.
57. Ransom M., Dennehey B.K., Tyler J.K. Chaperoning histones during DNA replication and repair. Cell 2010, 140:183-195.
58. 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 U S A 1997, 94:5611-5616.
59. Ibarra A., Schwob E., Mendez J. Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc Natl Acad Sci U S A 2008, 105:8956-8961.
60. Ge X.Q., Jackson D.A., Blow J.J. Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev 2007, 21:3331-3341.
61. Neelsen K.J., Zanini I.M., Mijic S., Herrador R., Zellweger R., Ray Chaudhuri A., et al. Deregulated origin licensing leads to chromosomal breaks by rereplication of a gapped DNA template. Genes Dev 2013, 27:2537-2542.
62. Hook S.S., Lin J.J., Dutta A. Mechanisms to control rereplication and implications for cancer. Curr Opin Cell Biol 2007, 19:663-671.
63. Archambault V., Ikui A.E., Drapkin B.J., Cross F.R. Disruption of mechanisms that prevent rereplication triggers a DNA damage response. Mol Cell Biol 2005, 25:6707-6721.
64. Shreeram S., Sparks A., Lane D.P., Blow J.J. Cell type-specific responses of human cells to inhibition of replication licensing. Oncogene 2002, 21:6624-6632.
65. Blow J.J., Gillespie P.J. Replication licensing and cancer - a fatal entanglement. Nat Rev Cancer 2008, 8:799-806.