Cdc45 (cell division cycle protein 45) guards the gate of the eukaryote replisome helicase stabilizing leading strand engagement

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 3, 2015, Pages E249-E258

  Petojevic, Tatjana ^a,b   Pesavento, James J ^a   Costa, Alessandro ^c   Liang, Jingdan ^a   Wang, Zhijun ^a   Berger, James M ^d   Botchan, Michael R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c London Research Institute   (United Kingdom)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cdc45; CMG helicase; DNA replication; Mcm2 5 gate; RecJ fold

Indexed keywords

CELL DIVISION CYCLE PROTEIN 45; DOUBLE STRANDED DNA; HELICASE; PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; DNA; DNA HELICASE; FLUORESCENT DYE;

ARTICLE; COMPLEX FORMATION; CROSS LINKING; DNA CONFORMATION; DNA CROSS LINKING; DNA STRAND; ENZYME ACTIVITY; EUKARYOTE; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; REPLISOME; AMINO ACID SEQUENCE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; SEQUENCE HOMOLOGY;

EUKARYOTA;

AMINO ACID SEQUENCE; CELL CYCLE PROTEINS; DNA; DNA HELICASES; FLUORESCENT DYES; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84921486481     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1422003112     Document Type: Article

References (48)

1. Yardimci H, Walter JC (2014) Prereplication-complex formation: A molecular double take? Nat Struct Mol Biol 21(1):20-25.
2. Heller RC, et al. (2011) Eukaryotic origin-dependent DNA replication in vitro reveals sequential action of DDK and S-CDK kinases. Cell 146(1):80-91.
3. Moyer SE, Lewis PW, Botchan MR (2006) Isolation of the Cdc45/Mcm2-7/GINS (CMG) complex, a candidate for the eukaryotic DNA replication fork helicase. Proc Natl Acad Sci USA 103(27):10236-10241.
4. Ilves I, Petojevic T, Pesavento JJ, Botchan MR (2010) Activation of the MCM2-7 helicase by association with Cdc45 and GINS proteins. Mol Cell 37(2):247-258.
5. Aparicio T, Ibarra A, Méndez J (2006) Cdc45-MCM-GINS, a new power player for DNA replication. Cell Div 1:18.
6. Pacek M, Tutter AV, Kubota Y, Takisawa H, Walter JC (2006) Localization of MCM2-7, Cdc45, and GINS to the site of DNA unwinding during eukaryotic DNA replication. Mol Cell 21(4):581-587.
7. Kang YH, Galal WC, Farina A, Tappin I, Hurwitz J (2012) Properties of the human Cdc45/Mcm2-7/GINS helicase complex and its action with DNA polymerase epsilon in rolling circle DNA synthesis. Proc Natl Acad Sci USA 109(16):6042-6047.
8. Remus D, et al. (2009) Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell 139(4):719-730.
9. Evrin C, et al. (2009) A double-hexameric MCM2-7 complex is loaded onto origin DNA during licensing of eukaryotic DNA replication. Proc Natl Acad Sci USA 106(48): 20240-20245.
10. Fu YV, et al. (2011) Selective bypass of a lagging strand roadblock by the eukaryotic replicative DNA helicase. Cell 146(6):931-941.
11. Graham BW, Schauer GD, Leuba SH, Trakselis MA (2011) Steric exclusion and wrapping of the excluded DNA strand occurs along discrete external binding paths during MCM helicase unwinding. Nucleic Acids Res 39(15):6585-6595.
12. Rothenberg E, Trakselis MA, Bell SD, Ha T (2007) MCM forked substrate specificity involves dynamic interaction with the 5′-tail. J Biol Chem 282(47):34229-34234.
13. Costa A, et al. (2008) Cryo-electron microscopy reveals a novel DNA-binding site on the MCM helicase. EMBO J 27(16):2250-2258.
14. Froelich CA, Kang S, Epling LB, Bell SP, Enemark EJ (2014) A conserved MCM singlestranded DNA binding element is essential for replication initiation. eLife 3:e01993.
15. Gambus A, et al. (2009) A key role for Ctf4 in coupling the MCM2-7 helicase to DNA polymerase alpha within the eukaryotic replisome. EMBO J 28(19):2992-3004.
16. Im JS, et al. (2009) 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(37): 15628-15632.
17. Langston LD, et al. (2014) CMG helicase and DNA polymerase e form a functional 15-subunit holoenzyme for eukaryotic leading-strand DNA replication. Proc Natl Acad Sci USA 111(43):15390-15395.
18. Costa A, et al. (2011) The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nat Struct Mol Biol 18(4):471-477.
19. Bochman ML, Schwacha A (2008) The Mcm2-7 complex has in vitro helicase activity. Mol Cell 31(2):287-293.
20. Costa A, et al. (2014) DNA binding polarity, dimerization, and ATPase ring remodeling in the CMG helicase of the eukaryotic replisome. eLife 3:e03273.
21. Krastanova I, et al. (2012) Structural and functional insights into the DNA replication factor Cdc45 reveal an evolutionary relationship to the DHH family of phosphoesterases. J Biol Chem 287(6):4121-4128.
22. Szambowska A, et al. (2014) DNA binding properties of human Cdc45 suggest a function as molecular wedge for DNA unwinding. Nucleic Acids Res 42(4): 2308-2319.
23. Bruck I, Kaplan DL (2013) Cdc45 protein-single-stranded DNA interaction is important for stalling the helicase during replication stress. J Biol Chem 288(11):7550-7563.
24. Boskovic J, et al. (2007) Molecular architecture of the human GINS complex. EMBO Rep 8(7):678-684.
25. Miller JM, Arachea BT, Epling LB, Enemark EJ (2014) Analysis of the crystal structure of an active MCM hexamer. eLife 3:e03433.
26. Sanchez-Pulido L, Ponting CP (2011) Cdc45: The missing RecJ ortholog in eukaryotes? Bioinformatics 27(14):1885-1888.
27. Bochman ML, Schwacha A (2007) 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(46):33795-33804.
28. Lee JK, Hurwitz J (2001) Processive DNA helicase activity of the minichromosome maintenance proteins 4, 6, and 7 complex requires forked DNA structures. Proc Natl Acad Sci USA 98(1):54-59.
29. You Z, et al. (2003) Thymine-rich single-stranded DNA activates Mcm4/6/7 helicase on Y-fork and bubble-like substrates. EMBO J 22(22):6148-6160.
30. Morimoto S, et al. (1998) Hydroxyl radical-induced cross-linking of thymine and lysine: Identification of the primary structure and mechanism. Bioorg Med Chem Lett 8(7): 865-870.
31. Evans MD, Dizdaroglu M, Cooke MS (2004) Oxidative DNA damage and disease: Induction, repair and significance. Mutat Res 567(1):1-61.
32. Brewster AS, Slaymaker IM, Afif SA, Chen XS (2010) Mutational analysis of an archaeal minichromosome maintenance protein exterior hairpin reveals critical residues for helicase activity and DNA binding. BMC Mol Biol 11:62.
33. Enemark EJ, Joshua-Tor L (2006) Mechanism of DNA translocation in a replicative hexameric helicase. Nature 442(7100):270-275.
34. Gai D, Zhao R, Li D, Finkielstein CV, Chen XS (2004) Mechanisms of conformational change for a replicative hexameric helicase of SV40 large tumor antigen. Cell 119(1): 47-60.
35. McGeoch AT, Trakselis MA, Laskey RA, Bell SD (2005) Organization of the archaeal MCM complex on DNA and implications for the helicase mechanism. Nat Struct Mol Biol 12(9):756-762.
36. Lam SK, et al. (2013) The PS1 hairpin of Mcm3 is essential for viability and for DNA unwinding in vitro. PLoS ONE 8(12):e82177.
37. Brewster AS, et al. (2008) Crystal structure of a near-full-length archaeal MCM: Functional insights for an AAA+ hexameric helicase. Proc Natl Acad Sci USA 105(51): 20191-20196.
38. Jaroszewski L, Rychlewski L, Li Z, Li W, Godzik A (2005) FFAS03: A server for profile-profile sequence alignments. Nucleic Acids Res 33(Web Server issue):W284-W288.
39. Lyubimov AY, Costa A, Bleichert F, Botchan MR, Berger JM (2012) ATP-dependent conformational dynamics underlie the functional asymmetry of the replicative helicase from a minimalist eukaryote. Proc Natl Acad Sci USA 109(30):11999-12004.
40. Sun J, et al. (2013) Cryo-EM structure of a helicase loading intermediate containing ORC-Cdc6-Cdt1-MCM2-7 bound to DNA. Nat Struct Mol Biol 20(8):944-951.
41. Kang S, Warner MD, Bell SP (2014) Multiple functions for Mcm2-7 ATPase motifs during replication initiation. Mol Cell 55(5):655-665.
42. Coster G, Frigola J, Beuron F, Morris EP, Diffley JF (2014) Origin licensing requires ATP binding and hydrolysis by the MCM replicative helicase. Mol Cell 55(5):666-677.
43. Sun J, et al. (2014) Structural and mechanistic insights into Mcm2-7 double-hexamer assembly and function. Genes Dev 28(20):2291-2303.
44. Yuan H, et al. (2013) RecJ-like protein from Pyrococcus furiosus has 3?-5? exonuclease activity on RNA: Implications for proofreading of 3?-mismatched RNA primers in DNA replication. Nucleic Acids Res 41(11):5817-5826.
45. Marinsek N, et al. (2006) GINS, a central nexus in the archaeal DNA replication fork. EMBO Rep 7(5):539-545.
46. Li Z, et al. (2011) A novel DNA nuclease is stimulated by association with the GINS complex. Nucleic Acids Res 39(14):6114-6123.
47. Hashimoto Y, Puddu F, Costanzo V (2012) RAD51- and MRE11-dependent reassembly of uncoupled CMG helicase complex at collapsed replication forks. Nat Struct Mol Biol 19(1):17-24.
48. Bell SD, Botchan MR (2013) The minichromosome maintenance replicative helicase. Cold Spring Harb Perspect Biol 5(11):a012807.