Structure of the eukaryotic replicative CMG helicase suggests a pumpjack motion for translocation

Nature Structural and Molecular Biology

Volumn 23, Issue 3, 2016, Pages 217-224

  Yuan, Zuanning ^a,b   Bai, Lin ^b   Sun, Jingchuan ^b   Georgescu, Roxana ^c   Liu, Jun ^d   O'Donnell, Michael E ^c   Li, Huilin ^a,b  

^a STONY BROOK UNIVERSITY   (United States)

^b BROOKHAVEN NATIONAL LABORATORY   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CMG HELICASE; DOUBLE STRANDED DNA; FUNGAL ENZYME; HELICASE; UNCLASSIFIED DRUG; WINGED HELIX TRANSCRIPTION FACTOR; DNA HELICASE;

ARTICLE; CONTROLLED STUDY; DNA DENATURATION; ENZYME CONFORMATION; ENZYME STRUCTURE; MOTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SACCHAROMYCES CEREVISIAE; CHEMISTRY; CRYOELECTRON MICROSCOPY; DNA REPLICATION; ENZYMOLOGY; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION; ULTRASTRUCTURE;

CRYOELECTRON MICROSCOPY; DNA HELICASES; DNA REPLICATION; MODELS, MOLECULAR; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE;

EID: 84959552559     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3170     Document Type: Article

References (65)

1. 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
2. Remus D., et al. Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell 139, 719-730 (2009
3. Botchan, M., & Berger, J. DNA replication: making two forks from one prereplication complex. Mol. Cell 40, 860-861 (2010
4. Yeeles, J.T., Deegan, T.D., Janska, A., Early, A., & Diffley, J.F. Regulated eukaryotic DNA replication origin firing with purified proteins. Nature 519, 431-435 (2015
5. 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
6. 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
7. Makarova, K.S., Koonin, E.V., & Kelman, Z. The CMG (CDC45/RecJ, MCM, GINS) complex is a conserved component of the DNA replication system in all archaea and eukaryotes. Biol. Direct 7, 7 (2012
8. Slaymaker, I.M., & Chen, X.S. MCM structure and mechanics: what we have learned from archaeal MCM. Subcell. Biochem. 62, 89-111 (2012
9. 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
10. Enemark, E.J., & Joshua-Tor, L. Mechanism of DNA translocation in a replicative hexameric helicase. Nature 442, 270-275 (2006
11. Singleton, M.R., Sawaya, M.R., Ellenberger, T., & Wigley, D.B. Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides. Cell 101, 589-600 (2000
12. Miller, J.M., Arachea, B.T., Epling, L.B., & Enemark, E.J. Analysis of the crystal structure of an active MCM hexamer. eLife 3, e03433 (2014
13. Li N., et al. Structure of the eukaryotic MCM complex at 3.8 Å. Nature 524, 186-191 (2015
14. Costa, A., et al. DNA binding polarity, dimerization, and ATPase ring remodeling in the CMG helicase of the eukaryotic replisome. eLife 3, e03273 (2014
15. Costa A., et al. The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nat. Struct. Mol. Biol. 18, 471-477 (2011
16. Sun J., et al. The architecture of a eukaryotic replisome. Nat. Struct. Mol. Biol. 22, 976-982 (2015
17. Lyubimov, A.Y., Strycharska, M., & Berger, J.M. The nuts and bolts of ring-Translocase structure and mechanism. Curr. Opin. Struct. Biol. 21, 240-248 (2011
18. Bochman, M.L., & Schwacha, A. The Mcm complex: unwinding the mechanism of a replicative helicase. Microbiol. Mol. Biol. Rev. 73, 652-683 (2009
19. Itsathitphaisarn, O., Wing, R.A., Eliason, W.K., Wang, J., & Steitz, T.A. The hexameric helicase DnaB adopts a nonplanar conformation during translocation. Cell 151, 267-277 (2012
20. Fu Y.V., et al. Selective bypass of a lagging strand roadblock by the eukaryotic replicative DNA helicase. Cell 146, 931-941 (2011
21. Chen B., & Frank, J. Two promising future developments of cryo-EM: capturing short-lived states and mapping a continuum of states of a macromolecule. Microscopy (Oxf.) doi: 10.1093/jmicro/dfv344 (31 October 2015
22. 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
23. 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
24. 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
25. Froelich, C.A., Kang, S., Epling, L.B., Bell, S.P, & Enemark, E.J. A conserved MCM single-stranded DNA binding element is essential for replication initiation. eLife 3 e01993 2014
26. 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
27. Samel S.A. et al. A unique DNA entry gate serves for regulated loading of the eukaryotic replicative helicase MCM2-7 onto DNA. Genes Dev. 28, 1653-1666 2014
28. Petojevic T., et al. Cdc45 (cell division cycle protein 45) guards the gate of the Eukaryote Replisome helicase stabilizing leading strand engagement. Proc. Natl. Acad. Sci. USA 112, E249-E258 (2015
29. Rothenberg, E., Trakselis, M.A., Bell, S.D., & Ha, T. MCM forked substrate specificity involves dynamic interaction with the 5'-Tail. J. Biol. Chem. 282, 34229-34234 (2007
30. Simon, A.C., et al A Ctf4 trimer couples the CMG helicase to DNA polymerase a in the eukaryotic replisome. Nature 510 293-297 2014
31. Onesti, S., & MacNeill, S.A. Structure and evolutionary origins of the CMG complex. Chromosoma 122, 47-53 (2013
32. Krastanova I., et al. Structural and functional insights into the DNA replication factor Cdc45 reveal an evolutionary relationship to the DHH family of phosphoesterases. J. Biol. Chem. 287, 4121-4128 (2012
33. Sanchez-Pulido, L., & Ponting, C.P. Cdc45: the missing RecJ ortholog in eukaryotes? Bioinformatics 27, 1885-1888 (2011
34. Lairson, L.L., Henrissat, B., Davies, G.J., & Withers, S.G. Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 77, 521-555 (2008
35. Wakamatsu T., et al. Structure of RecJ exonuclease defines its specificity for single-stranded DNA. J. Biol. Chem. 285, 9762-9769 (2010
36. Yamagata, A., Kakuta, Y., Masui, R., & Fukuyama, K. The crystal structure of exonuclease RecJ bound to Mn2+ ion suggests how its characteristic motifs are involved in exonuclease activity. Proc. Natl. Acad. Sci. USA 99, 5908-5912 (2002
37. Niedziela-Majka, A., Chesnik, M.A., Tomko, E.J., & Lohman, T.M. Bacillus stearothermophilus PcrA monomer is a single-stranded DNA translocase but not a processive helicase in vitro. J. Biol. Chem. 282, 27076-27085 (2007
38. Velankar, S.S., Soultanas, P., Dillingham, M.S., Subramanya, H.S., & Wigley, D.B. Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell 97, 75-84 (1999
39. Fischer, C.J., Maluf, N.K., & Lohman, T.M. Mechanism of ATP-dependent translocation of E. coli UvrD monomers along single-stranded DNA. J. Mol. Biol. 344, 1287-1309 (2004
40. Lee, J.Y., & Yang, W. UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke. Cell 127, 1349-1360 (2006
41. Rad, B., & Kowalczykowski, S.C. Efficient coupling of ATP hydrolysis to translocation by RecQ helicase. Proc. Natl. Acad. Sci. USA 109, 1443-1448 (2012
42. Bjornson, K.P., Wong, I., & Lohman, T.M. ATP hydrolysis stimulates binding and release of single stranded DNA from alternating subunits of the dimeric E. coli Rep helicase: implications for ATP-driven helicase translocation. J. Mol. Biol. 263, 411-422 (1996
43. Singleton, M.R., Dillingham, M.S., & Wigley, D.B. Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 76, 23-50 (2007
44. Eisenmesser E.Z., et al. Intrinsic dynamics of an enzyme underlies catalysis. Nature 438, 117-121 (2005
45. Frauenfelder, H., Sligar, S.G., & Wolynes, P.G. The energy landscapes and motions of proteins. Science 254, 1598-1603 (1991
46. Henzler-Wildman, K., & Kern, D. Dynamic personalities of proteins. Nature 450, 964-972 (2007
47. 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
48. Bowman, G.D., ODonnell, M., & Kuriyan, J. Structural analysis of a eukaryotic sliding DNA clamp-clamp loader complex. Nature 429, 724-730 (2004
49. Simonetta K.R., et al. The mechanism of ATP-dependent primer-Template recognition by a clamp loader complex. Cell 137, 659-671 (2009
50. Kelch, B.A., Makino, D.L., ODonnell, M., & Kuriyan, J. How a DNA polymerase clamp loader opens a sliding clamp. Science 334, 1675-1680 (2011
51. Skordalakes, E., & Berger, J.M. Structure of the Rho transcription terminator: mechanism of mRNA recognition and helicase loading. Cell 114, 135-146 (2003
52. 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 28, 304-314 (2007
53. Li X., et al. Electron counting and beam-induced motion correction enable near-Atomic-resolution single-particle cryo-EM. Nat. Methods 10, 584-590 (2013
54. Rohou, A., & Grigorieff, N. CTFFIND4: fast and accurate defocus estimation from electron micrographs. J. Struct. Biol. 192, 216-221 (2015
55. Scheres, S.H. Semi-Automated selection of cryo-EM particles in RELION-1.3. J. Struct. Biol. 189, 114-122 (2015
56. Scheres, S.H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012
57. Wang R.Y., et al. De novo protein structure determination from near-Atomic-resolution cryo-EM maps. Nat. Methods 12, 335-338 (2015
58. Biasini M., et al. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 42, W252-W258 (2014
59. Emsley, P., & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004
60. Pettersen E.F., et al. UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004
61. Afonine P.V., et al. Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D Biol. Crystallogr. 68, 352-367 (2012
62. Adams P.D., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010
63. Amunts A., et al. Structure of the yeast mitochondrial large ribosomal subunit. Science 343, 1485-1489 (2014
64. Wei Z., et al. Characterization and structure determination of the Cdt1 binding domain of human minichromosome maintenance (Mcm) 6. J. Biol. Chem. 285, 12469-12473 (2010
65. Chen V.B., et al. MolProbity: all-Atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21 (2010