Conserved mechanism for coordinating replication fork helicase assembly with phosphorylation of the helicase

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

Volumn 112, Issue 36, 2015, Pages 11223-11228

  Bruck, Irina ^a   Kaplan, Daniel L ^a  

^a FLORIDA STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; CELL DIVISION CYCLE 45 PROTEIN; DBF4 DEPENDENT KINASE; DNA; HELICASE; INITIATION FACTOR; INITIATION FACTOR SLD3; MINICHROMOSOME MAINTENANCE PROTEIN 2; MINICHROMOSOME MAINTENANCE PROTEIN 3; MINICHROMOSOME MAINTENANCE PROTEIN 4; MINICHROMOSOME MAINTENANCE PROTEIN 5; MINICHROMOSOME MAINTENANCE PROTEIN 6; MINICHROMOSOME MAINTENANCE PROTEIN 7; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG; CDC45 PROTEIN, S CEREVISIAE; CDC7 PROTEIN, S CEREVISIAE; DNA BINDING PROTEIN; MINICHROMOSOME MAINTENANCE PROTEIN; NUCLEAR PROTEIN; PROTEIN BINDING; PROTEIN SERINE THREONINE KINASE; SACCHAROMYCES CEREVISIAE PROTEIN; SLD3 PROTEIN, S CEREVISIAE; TICRR PROTEIN, HUMAN;

ARTICLE; CELL CYCLE S PHASE; CELL GROWTH; CONTROLLED STUDY; DNA REPLICATION; DNA REPLICATION ORIGIN; ENZYME PHOSPHORYLATION; FUNGUS GROWTH; GROWTH INHIBITION; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RING OPENING; SIGNAL TRANSDUCTION; YEAST CELL; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MUTATION; PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL CYCLE PROTEINS; DNA REPLICATION; DNA-BINDING PROTEINS; HUMANS; MINICHROMOSOME MAINTENANCE COMPLEX COMPONENT 2; MINICHROMOSOME MAINTENANCE PROTEINS; MUTATION; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

EID: 84941312545     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1509608112     Document Type: Article

References (39)

1. Ilves I, Petojevic T, Pesavento J.J., Botchan M.R. (2010) Activation of the MCM2-7 helicase by association with Cdc45 and GINS proteins. Mol Cell 37(2):247-258.
2. Kamimura Y, Tak YS, Sugino A, Araki H. (2001) Sld3, which interacts with Cdc45 (Sld4), functions for chromosomal DNA replication in Saccharomyces cerevisiae. EMBO J 20(8):2097-2107.
3. Kanemaki M, Labib K. (2006) Distinct roles for Sld3 and GINS during establishment and progression of eukaryotic DNA replication forks. EMBO J 25(8):1753-1763.
4. Araki H (2010) Cyclin-dependent kinase-dependent initiation of chromosomal DNA replication. Curr Opin Cell Biol 22(6):766-771.
5. Labib K (2010) How do Cdc7 and cyclin-dependent kinases trigger the initiation of chromosome replication in eukaryotic cells? Genes Dev 24(12):1208-1219.
6. Remus D, et al (2009) Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell 139(4):719-730.
7. 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.
8. Fu YV, et al (2011) Selective bypass of a lagging strand roadblock by the eukaryotic replicative DNA helicase. Cell 146(6):931-941.
9. Zegerman P, Diffley J.F. (2007) Phosphorylation of Sld2 and Sld3 by cyclin-dependent kinases promotes DNA replication in budding yeast. Nature 445 (7125):281-285.
10. Tanaka S, et al (2007) CDK-dependent phosphorylation of Sld2 and Sld3 initiates DNA replication in budding yeast. Nature 445 (7125):328-332.
11. Kumagai A, Shevchenko A, Shevchenko A., Dunphy W.G. (2011) Direct regulation of Treslin by cyclin-dependent kinase is essential for the onset of DNA replication. J Cell Biol 193(6):995-1007.
12. Tak YS, Tanaka Y, Endo S., Kamimura Y, Araki H. (2006) A CDK-catalysed regulatory phosphorylation for formation of the DNA replication complex Sld2-Dpb11. EMBO J 25(9):1987-1996.
13. Kanter DM, Kaplan D.L. (2011) Sld2 binds to origin single-stranded DNA and stimulates DNA annealing. Nucleic Acids Res 39(7):2580-2592.
14. Muramatsu S, Hirai K, Tak Y.S., Kamimura Y., Araki H. (2010) CDK-dependent complex formation between replication proteins Dpb11, Sld2, Pol (epsilon, and GINS in budding yeast. Genes Dev 24(6):602-612.
15. Dhingra N, Bruck I, Smith S., Ning B, Kaplan D.L. (2015) Dpb11 protein helps control assembly of the Cdc45·Mcm2-7·GINS replication fork helicase. J Biol Chem 290(12): 7586-7601.
16. Bruck I, Kaplan D.L. (2011) Origin single-stranded DNA releases Sld3 protein from the Mcm2-7 complex, allowing the GINS tetramer to bind the Mcm2-7 complex. J Biol Chem 286(21):18602-18613.
17. Yeeles JT, Deegan TD, Janska A, Early A., Diffley J.F. (2015) Regulated eukaryotic DNA replication origin firing with purified proteins. Nature 519 (7544):431-435.
18. Sheu YJ, Stillman B. (2010) The Dbf4-Cdc7 kinase promotes S phase by alleviating an inhibitory activity in Mcm4. Nature 463 (7277):113-117.
19. Masai H, et al (2006) Phosphorylation of MCM4 by Cdc7 kinase facilitates its interaction with Cdc45 on the chromatin. J Biol Chem 281(51):39249-39261.
20. Lei M, et al (1997) Mcm2 is a target of regulation by Cdc7-Dbf4 during the initiation of DNA synthesis. Genes Dev 11(24):3365-3374.
21. Bruck I, Kaplan D.L. (2015) The Dbf4-Cdc7 kinase promotes Mcm2-7 ring opening to allow for single-stranded DNA extrusion and helicase assembly. J Biol Chem 290(2): 1210-1221.
22. Bochman ML, Schwacha A. (2008) The Mcm2-7 complex has in vitro helicase activity. Mol Cell 31(2):287-293.
23. Bruck I, Kaplan D.L. (2011) GINS and Sld3 compete with one another for Mcm2-7 and Cdc45 binding. J Biol Chem 286(16):14157-14167.
24. Tanaka S, Nakato R, Katou Y., Shirahige K, Araki H. (2011) Origin association of Sld3, Sld7, and Cdc45 proteins is a key step for determination of origin-firing timing. Curr Biol 21(24):2055-2063.
25. Costa A, et al (2014) DNA binding polarity, dimerization, and ATPase ring remodeling in the CMG helicase of the eukaryotic replisome. Elife Aug 12:e03273.
26. Bruck I, Kaplan D.L. (2014) The replication initiation protein Sld2 regulates helicase assembly. J Biol Chem 289(4):1948-1959.
27. Stead BE, Brandl CJ, Davey M.J. (2011) Phosphorylation of Mcm2 modulates Mcm2-7 activity and affects the cell's response to DNA damage. Nucleic Acids Res 39(16): 6998-7008.
28. Stead BE, Brandl CJ, Sandre M.K., Davey M.J. (2012) Mcm2 phosphorylation and the response to replicative stress. BMC Genet 13:36.
29. Ge XQ, Jackson DA, Blow J.J. (2007) Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev 21(24):3331-3341.
30. Bruck I, Kaplan D. (2009) Dbf4-Cdc7 phosphorylation of Mcm2 is required for cell growth. J Biol Chem 284(42):28823-28831.
31. Montagnoli A, et al (2006) Identification of Mcm2 phosphorylation sites by S-phase-regulating kinases. J Biol Chem 281(15):10281-10290.
32. Mantiero D, Mackenzie A, Donaldson A., Zegerman P. (2011) Limiting replication initiation factors execute the temporal programme of origin firing in budding yeast. EMBO J 30(23):4805-4814.
33. Frigola J, Remus D, Mehanna A., Diffley J.F. (2013) ATPase-dependent quality control of DNA replication origin licensing. Nature 495 (7441):339-343.
34. Samel SA, et al (2014) A unique DNA entry gate serves for regulated loading of the eukaryotic replicative helicase MCM2-7 onto DNA. Genes Dev 28(15):1653-1666.
35. 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.
36. Sheu YJ, Kinney JB, Lengronne A, Pasero P., Stillman B. (2014) Domain within the helicase subunit Mcm4 integrates multiple kinase signals to control DNA replication initiation and fork progression. Proc Natl Acad Sci USA 111(18):E1899-E1908.
37. Sheu Y-J, Stillman B. (2006) Cdc7-Dbf4 phosphorylates MCM proteins via a docking site-mediated mechanism to promote S phase progression. Mol Cell 24(1):101-113.
38. Francis LI, Randell JC, Takara T.J., Uchima L., Bell S.P. (2009) Incorporation into the prereplicative complex activates the Mcm2-7 helicase for Cdc7-Dbf4 phosphorylation. Genes Dev 23(5):643-654.
39. Yardimci H, Loveland AB, Habuchi S, van Oijen AM, Walter J.C. (2010) Uncoupling of sister replisomes during eukaryotic DNA replication. Mol Cell 40(5):834-840.