A new MCM modification cycle regulates DNA replication initiation

Nature Structural and Molecular Biology

Volumn 23, Issue 3, 2016, Pages 209-216

  Wei, Lei ^a,b   Zhao, Xiaolan ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Gerstner Sloan Kettering Graduate School of Biomedical Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA HELICASE; MCM PROTEIN; UNCLASSIFIED DRUG; MINICHROMOSOME MAINTENANCE PROTEIN;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA REPLICATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; SUMOYLATION; YEAST; CELL CYCLE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; SACCHAROMYCES CEREVISIAE;

CELL CYCLE; DNA REPLICATION; GENE EXPRESSION REGULATION, FUNGAL; MINICHROMOSOME MAINTENANCE PROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SACCHAROMYCES CEREVISIAE; SUMOYLATION;

EID: 84959454600     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3173     Document Type: Article

References (45)

1. Tanaka, S., & Araki, H. Multiple regulatory mechanisms to inhibit untimely initiation of DNA replication are important for stable genome maintenances. PLoS Genet 7, e1002136 (2011
2. Zegerman, P., & Diffley, J.F.X. Phosphorylation of Sld2 and Sld3 by cyclin-dependent kinases promotes DNA replication in budding yeast. Nature 445, 281-285 (2007
3. Tanaka S., et al. CDK-dependent phosphorylation of Sld2 and Sld3 initiates DNA replication in budding yeast. Nature 445, 328-332 (2007
4. Sheu, Y.-J., & Stillman, B. The Dbf4-Cdc7 kinase promotes S phase by alleviating an inhibitory activity in Mcm4. Nature 463, 113-117 (2010
5. Jackson, A.P., Laskey, R.A., & Coleman, N. Replication proteins and human disease. Cold Spring Harb. Perspect. Biol. 6, 327-342 (2014
6. Francis, L.I., Randell, J.C.W., Takara, T.J., Uchima, L., & Bell, S.P. Incorporation into the prereplicative complex activates the Mcm2-7 helicase for Cdc7-Dbf4 phosphorylation. Genes Dev. 23, 643-654 (2009
7. Sheu, Y.-J., & Stillman, B. Cdc7-Dbf4 phosphorylates MCM proteins via a docking site-mediated mechanism to promote S phase progression. Mol. Cell 24, 101-113 (2006
8. Randell J.C.W., et al. Mec1 is one of multiple kinases that prime the Mcm2-7 helicase for phosphorylation by Cdc7. Mol. Cell 40, 353-363 (2010
9. Mattarocci S., et al. Rif1 controls DNA replication timing in yeast through the PP1 phosphatase Glc7. Cell Rep. 7, 62-69 (2014
10. Davé, A., Cooley, C., Garg, M., & Bianchi, A. Protein phosphatase 1 recruitment by Rif1 regulates DNA replication origin firing by counteracting DDK activity. Cell Rep. 7, 53-61 (2014
11. Hiraga S., et al. Rif1 controls DNA replication by directing Protein Phosphatase 1 to reverse Cdc7-mediated phosphorylation of the MCM complex. Genes Dev. 28, 372-383 (2014
12. Maric, M., Maculins, T., De Piccoli, G., & Labib, K. Cdc48 and a ubiquitin ligase drive disassembly of the CMG helicase at the end of DNA replication. Science 346, 1253596 (2014
13. Siddiqui, K., On, K.F., & Diffley, J.F.X. Regulating DNA replication in eukarya. Cold Spring Harb. Perspect. Biol. 5, a012930 (2013
14. Fragkos, M., Ganier, O., Coulombe, P., & Méchali, M. DNA replication origin activation in space and time. Nat. Rev. Mol. Cell Biol. 16, 360-374 (2015
15. 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
16. Heller R.C., et al. Eukaryotic origin-dependent DNA replication in vitro reveals sequential action of DDK and S-CDK kinases. Cell 146, 80-91 (2011
17. Gambus A., et al. GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat. Cell Biol. 8, 358-366 (2006
18. Morohashi, H., Maculins, T., & Labib, K. The amino-Terminal TPR domain of Dia2 tethers SCF(Dia2) to the replisome progression complex. Curr. Biol. 19, 1943-1949 (2009
19. Cremona C.A., et al. Extensive DNA damage-induced sumoylation contributes to replication and repair and acts in addition to the mec1 checkpoint. Mol. Cell 45, 422-432 (2012
20. Golebiowski F., et al. System-wide changes to SUMO modifications in response to heat shock. Sci. Signal. 2, ra24 (2009
21. Elrouby, N., & Coupland, G. Proteome-wide screens for small ubiquitin-like modifier (SUMO) substrates identify Arabidopsis proteins implicated in diverse biological processes. Proc. Natl. Acad. Sci. USA 107, 17415-17420 (2010
22. Geiss-Friedlander, R., & Melchior, F. Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 8, 947-956 (2007
23. Sarangi, P., & Zhao, X. SUMO-mediated regulation of DNA damage repair and responses. Trends Biochem. Sci. 40, 233-242 (2015
24. Psakhye, I., & Jentsch, S. Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 151, 807-820 (2012
25. Morris J.R., et al. The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 462, 886-890 (2009
26. Galanty Y., et al. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 462, 935-939 (2009
27. Chung, I., & Zhao, X. DNA break-induced sumoylation is enabled by collaboration between a SUMO ligase and the ssDNA-binding complex RPA. Genes Dev. 29, 1593-1598 (2015
28. Sarangi P. et al. A versatile scaffold contributes to damage survival via sumoylation and nuclease interactions. Cell Rep. 9, 143-152 2014
29. Ulrich, H.D., & Davies, A.A. In vivo detection and characterization of sumoylation targets in Saccharomyces cerevisiae. Methods Mol. Biol. 497, 81-103 (2009
30. Nishimura, K., Fukagawa, T., Takisawa, H., Kakimoto, T., & Kanemaki, M. An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat. Methods 6, 917-922 (2009
31. Havens K.A. et al. A synthetic approach reveals extensive tunability of auxin signaling. Plant Physiol. 160, 135-142 2012
32. Crabbé L., et al. Analysis of replication profiles reveals key role of RFC-Ctf18 in yeast replication stress response. Nat. Struct. Mol. Biol. 17, 1391-1397 (2010
33. Zegerman, P., & Diffley, J.F.X. Checkpoint-dependent inhibition of DNA replication initiation by Sld3 and Dbf4 phosphorylation. Nature 467, 474-478 (2010
34. Almedawar, S., Colomina, N., Bermúdez-López, M., Pociño-Merino, I., & Torres-Rosell, J. A SUMO-dependent step during establishment of sister chromatid cohesion. Curr. Biol. 22, 1576-1581 (2012
35. Mossessova, E., & Lima, C.D. Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol. Cell 5, 865-876 (2000
36. Sung M.K., et al. Genome-wide bimolecular fluorescence complementation analysis of SUMO interactome in yeast. Genome Res. 23, 736-746 (2013
37. Desdouets C., et al. Evidence for a Cdc6p-independent mitotic resetting event involving DNA polymerase alpha. EMBO J. 17, 4139-4146 (1998
38. Hawkins M., et al. High-resolution replication profiles define the stochastic nature of genome replication initiation and termination. Cell Rep. 5, 1132-1141 (2013
39. Zhao, X., & Blobel, G. A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization. Proc. Natl. Acad. Sci. USA 102, 4777-4782 (2005
40. 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. USA 94, 5611-5616 (1997
41. Takahashi Y., et al. Cooperation of sumoylated chromosomal proteins in rDNA maintenance. PLoS Genet. 4, e1000215 (2008
42. Friedman, K.L., & Brewer, B.J. Analysis of replication intermediates by two-dimensional agarose gel electrophoresis. Methods Enzymol. 262, 613-627 (1995
43. Hang L.E., et al. Rtt107 Is a multi-functional scaffold supporting replication progression with partner sUMO and ubiquitin ligases. Mol. Cell 60, 268-279 (2015
44. Murakami, H., & Keeney, S. Temporospatial coordination of meiotic DNA replication and recombination via DDK recruitment to replisomes. Cell 158, 861-873 (2014
45. Schepers, A., & Diffley, J.F. Mutational analysis of conserved sequence motifs in the budding yeast Cdc6 protein. J. Mol. Biol. 308, 597-608 (2001