Enigmatic roles of Mcm10 in DNA replication

Trends in Biochemical Sciences

Volumn 38, Issue 4, 2013, Pages 184-194

  Thu, Yee Mon ^a   Bielinsky, Anja Katrin ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

DNA replication; Double strand breaks; Genome integrity; Mcm10; OB fold; Replication forks; Zn finger domains

Indexed keywords

CELL CYCLE PROTEIN; CELL CYCLE PROTEIN 45; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE DELTA; DNA DIRECTED DNA POLYMERASE EPSILON; DOUBLE STRANDED DNA; HELICASE; MINICHROMOSOME MAINTENANCE PROTEIN; MINICHROMOSOME MAINTENANCE PROTEIN 10; MINICHROMOSOME MAINTENANCE PROTEIN 2; MINICHROMOSOME MAINTENANCE PROTEIN 7; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

CHROMATIN; COMPLEX FORMATION; DNA DENATURATION; DNA REPAIR; DNA REPLICATION; DNA SYNTHESIS; EUKARYOTE; GENE INTERACTION; GENE REPLICATION; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN STRUCTURE; REPLISOME; REVIEW; S PHASE CELL CYCLE CHECKPOINT; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; XENOPUS;

ANIMALS; CELL CYCLE; CHROMATIN; DNA; DNA REPLICATION; DNA, FUNGAL; MINICHROMOSOME MAINTENANCE PROTEINS; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN STRUCTURE, TERTIARY; REPLICATION ORIGIN; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITINATION;

EUKARYOTA;

EID: 84875480804     PISSN: 09680004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tibs.2012.12.003     Document Type: Review

References (77)

1. Bell S.P., Dutta A. DNA replication in eukaryotic cells. Annu. Rev. Biochem. 2002, 71:333-374.
2. Masai H., et al. Eukaryotic chromosome DNA replication: where, when, and how?. Annu. Rev. Biochem. 2011, 79:89-130.
3. Moyer S.E., et al. 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.
4. Wohlschlegel J.A., et al. Xenopus Mcm10 binds to origins of DNA replication after Mcm2-7 and stimulates origin binding of Cdc45. Mol. Cell 2002, 9:233-240.
5. Kanke M., et al. Mcm10 plays an essential role in origin DNA unwinding after loading of the CMG components. EMBO J. 2012, 31:2182-2194.
6. van Deursen F., et al. Mcm10 associates with the loaded DNA helicase at replication origins and defines a novel step in its activation. EMBO J. 2012, 31:2195-2206.
7. Watase G., et al. Mcm10 plays a role in functioning of the eukaryotic replicative DNA helicase, Cdc45-Mcm-GINS. Curr. Biol. 2012, 22:343-349.
8. Heller R.C., et al. Eukaryotic origin-dependent DNA replication in vitro reveals sequential action of DDK and S-CDK kinases. Cell 2011, 146:80-91.
9. Solomon N.A., et al. Genetic and molecular analysis of DNA43 and DNA52: two new cell-cycle genes in Saccharomyces cerevisiae. Yeast 1992, 8:273-289.
10. Merchant A.M., et al. A lesion in the DNA replication initiation factor Mcm10 induces pausing of elongation forks through chromosomal replication origins in Saccharomyces cerevisiae. Mol. Cell. Biol. 1997, 17:3261-3271.
11. Ricke R.M., Bielinsky A.K. Mcm10 regulates the stability and chromatin association of DNA polymerase-α. Mol. Cell 2004, 16:173-185.
12. Gregan J., et al. Fission yeast Cdc23/Mcm10 functions after pre-replicative complex formation to promote Cdc45 chromatin binding. Mol. Biol. Cell 2003, 14:3876-3887.
13. Sawyer S.L., et al. Mcm10 and Cdc45 cooperate in origin activation in Saccharomyces cerevisiae. J. Mol. Biol. 2004, 340:195-202.
14. Yang X., et al. Nuclear distribution and chromatin association of DNA polymerase α-primase is affected by TEV protease cleavage of Cdc23 (Mcm10) in fission yeast. BMC Mol. Biol. 2005, 6:13.
15. Fien K., et al. Primer utilization by DNA polymerase α-primase is influenced by its interaction with Mcm10p. J. Biol. Chem. 2004, 279:16144-16153.
16. Robertson P.D., et al. Domain architecture and biochemical characterization of vertebrate Mcm10. J. Biol. Chem. 2008, 283:3338-3348.
17. Warren E.M., et al. Structural basis for DNA binding by replication initiator Mcm10. Structure 2008, 16:1892-1901.
18. Eisenberg S., et al. Novel DNA binding properties of the Mcm10 protein from Saccharomyces cerevisiae. J. Biol. Chem. 2009, 284:25412-25420.
19. Warren E.M., et al. Physical interactions between Mcm10, DNA, and DNA polymerase α. J. Biol. Chem. 2009, 284:24662-24672.
20. Robertson P.D., et al. Solution NMR structure of the C-terminal DNA binding domain of Mcm10 reveals a conserved MCM motif. J. Biol. Chem. 2010, 285:22942-22949.
21. Remus D., et al. Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell 2009, 139:719-730.
22. Gambus A., et al. GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat. Cell Biol. 2006, 8:358-366.
23. Fu Y.V., et al. Selective bypass of a lagging strand roadblock by the eukaryotic replicative DNA helicase. Cell 2011, 146:931-941.
24. Du W., et al. Structural biology of replication initiation factor Mcm10. Subcell. Biochem. 2012, 62:197-216.
25. Xu X., et al. MCM10 mediates RECQ4 association with MCM2-7 helicase complex during DNA replication. EMBO J. 2009, 28:3005-3014.
26. Sangrithi M.N., et al. Initiation of DNA replication requires the RECQL4 protein mutated in Rothmund-Thomson syndrome. Cell 2005, 121:887-898.
27. Matsuno K., et al. The N-terminal noncatalytic region of Xenopus RecQ4 is required for chromatin binding of DNA polymerase α in the initiation of DNA replication. Mol. Cell. Biol. 2006, 26:4843-4852.
28. Ohlenschlager O., et al. The N-terminus of the human RecQL4 helicase is a homeodomain-like DNA interaction motif. Nucleic Acids Res. 2012, 40:8309-8324.
29. Zhu W., et al. Mcm10 and And-1/CTF4 recruit DNA polymerase α to chromatin for initiation of DNA replication. Genes Dev. 2007, 21:2288-2299.
30. Ricke R.M., Bielinsky A.K. A conserved Hsp10-like domain in Mcm10 is required to stabilize the catalytic subunit of DNA polymerase-α in budding yeast. J. Biol. Chem. 2006, 281:18414-18425.
31. Chattopadhyay S., Bielinsky A.K. Human Mcm10 regulates the catalytic subunit of DNA polymerase-α and prevents DNA damage during replication. Mol. Biol. Cell 2007, 18:4085-4095.
32. Wawrousek K.E., et al. Xenopus DNA2 is a helicase/nuclease that is found in complexes with replication proteins And-1/Ctf4 and Mcm10 and DSB response proteins Nbs1 and ATM. Cell Cycle 2010, 9:1156-1166.
33. Apger J., et al. Multiple functions for Drosophila Mcm10 suggested through analysis of two Mcm10 mutant alleles. Genetics 2010, 185:1151-1165.
34. Gosnell J.A., Christensen T.W. Drosophila Ctf4 is essential for efficient DNA replication and normal cell cycle progression. BMC Mol. Biol. 2011, 12:13.
35. Lee C., et al. Alternative mechanisms for coordinating polymerase α and MCM helicase. Mol. Cell. Biol. 2010, 30:423-435.
36. Wang J., et al. Ctf4p facilitates Mcm10p to promote DNA replication in budding yeast. Biochem. Biophys. Res. Commun. 2010, 395:336-341.
37. Haworth J., et al. Ubc4 and Not4 regulate steady-state levels of DNA polymerase-α to promote efficient and accurate DNA replication. Mol. Biol. Cell 2010, 21:3205-3219.
38. Raveendranathan M., et al. Genome-wide replication profiles of S-phase checkpoint mutants reveal fragile sites in yeast. EMBO J. 2006, 25:3627-3639.
39. Taylor M., et al. Mcm10 interacts with Rad4/Cut5(TopBP1) and its association with origins of DNA replication is dependent on Rad4/Cut5(TopBP1). DNA Repair (Amst.) 2011, 10:1154-1163.
40. Pacek M., et al. Localization of MCM2-7, Cdc45, and GINS to the site of DNA unwinding during eukaryotic DNA replication. Mol. Cell 2006, 21:581-587.
41. + (MCM10) and interactions with replication checkpoints. Genetics 2001, 159:471-486.
42. Cobb J.A., et al. Replisome instability, fork collapse, and gross chromosomal rearrangements arise synergistically from Mec1 kinase and RecQ helicase mutations. Genes Dev. 2005, 19:3055-3069.
43. Das-Bradoo S., et al. Interaction between PCNA and diubiquitinated Mcm10 is essential for cell growth in budding yeast. Mol. Cell. Biol. 2006, 26:4806-4817.
44. 2 phase. Nucleic Acids Res. 2000, 28:4769-4777.
45. Cook C.R., et al. A novel zinc finger is required for Mcm10 homocomplex assembly. J. Biol. Chem. 2003, 278:36051-36058.
46. Okorokov A.L., et al. Hexameric ring structure of human MCM10 DNA replication factor. EMBO Rep. 2007, 8:925-930.
47. Dalrymple B.P., et al. A universal protein-protein interaction motif in the eubacterial DNA replication and repair systems. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:11627-11632.
48. Yoshida K., Inoue I. Expression of MCM10 and TopBP1 is regulated by cell proliferation and UV irradiation via the E2F transcription factor. Oncogene 2004, 23:6250-6260.
49. Izumi M., et al. Cell cycle-dependent proteolysis and phosphorylation of human Mcm10. J. Biol. Chem. 2001, 276:48526-48531.
50. Sharma A., et al. Ultraviolet radiation stress triggers the down-regulation of essential replication factor Mcm10. J. Biol. Chem. 2010, 285:8352-8362.
51. Kaur M., et al. CRL4-DDB1-VPRBP ubiquitin ligase mediates the stress triggered proteolysis of Mcm10. Nucleic Acids Res. 2012, 40:7332-7346.
52. Lee J.K., et al. The Cdc23 (Mcm10) protein is required for the phosphorylation of minichromosome maintenance complex by the Dfp1-Hsk1 kinase. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:2334-2339.
53. Matsuoka S., et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007, 316:1160-1166.
54. Paulsen R.D., et al. A genome-wide siRNA screen reveals diverse cellular processes and pathways that mediate genome stability. Mol. Cell 2009, 35:228-239.
55. Lukas C., et al. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat. Cell Biol. 2011, 13:243-253.
56. Park J.H., et al. Knockdown of human MCM10 exhibits delayed and incomplete chromosome replication. Biochem. Biophys. Res. Commun. 2008, 365:575-582.
57. Park J.H., et al. Knockdown of human MCM10 activates G2 checkpoint pathway. Biochem. Biophys. Res. Commun. 2008, 365:490-495.
58. Douglas N.L., et al. Dual roles for Mcm10 in DNA replication initiation and silencing at the mating-type loci. Mol. Biol. Rep. 2005, 32:197-204.
59. Liachko I., Tye B.K. Mcm10 is required for the maintenance of transcriptional silencing in Saccharomyces cerevisiae. Genetics 2005, 171:503-515.
60. Liachko I., Tye B.K. Mcm10 mediates the interaction between DNA replication and silencing machineries. Genetics 2009, 181:379-391.
61. Locovei A.M., et al. The CENP-B homolog, Abp1, interacts with the initiation protein Cdc23 (MCM10) and is required for efficient DNA replication in fission yeast. Cell Div. 2006, 1:27.
62. Wu C., et al. Integrating gene expression and protein-protein interaction network to prioritize cancer-associated genes. BMC Bioinformatics 2012, 13:182.
63. Koppen A., et al. Direct regulation of the minichromosome maintenance complex by MYCN in neuroblastoma. Eur. J. Cancer 2007, 43:2413-2422.
64. Garcia-Aragoncillo E., et al. DAX1, a direct target of EWS/FLI1 oncoprotein, is a principal regulator of cell-cycle progression in Ewing's tumor cells. Oncogene 2008, 27:6034-6043.
65. Koh J.L., et al. DRYGIN: a database of quantitative genetic interaction networks in yeast. Nucleic Acids Res. 2010, 38:502-507.
66. Kawasaki Y., et al. Interactions between Mcm10p and other replication factors are required for proper initiation and elongation of chromosomal DNA replication in Saccharomyces cerevisiae. Genes Cells 2000, 5:975-989.
67. Homesley L., et al. Mcm10 and the MCM2-7 complex interact to initiate DNA synthesis and to release replication factors from origins. Genes Dev. 2000, 14:913-926.
68. Araki Y., et al. Budding yeast mcm10/dna43 mutant requires a novel repair pathway for viability. Genes Cells 2003, 8:465-480.
69. Hart E.A., et al. Fission yeast Cdc23 interactions with DNA replication initiation proteins. Curr. Genet. 2002, 41:342-348.
70. Nagai S., et al. Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 2008, 322:597-602.
71. Aparicio J.G., et al. The Rpd3-Sin3 histone deacetylase regulates replication timing and enables intra-S origin control in Saccharomyces cerevisiae. Mol. Cell. Biol. 2004, 24:4769-4780.
72. Knott S.R., et al. Genome-wide replication profiles indicate an expansive role for Rpd3L in regulating replication initiation timing or efficiency, and reveal genomic loci of Rpd3 function in Saccharomyces cerevisiae. Genes Dev. 2009, 23:1077-1090.
73. Mayer M.L., et al. Identification of RFC (Ctf18p, Ctf8p, Dcc1p): an alternative RFC complex required for sister chromatid cohesion in S. cerevisiae. Mol. Cell 2001, 7:959-970.
74. Crabbe L., et al. Analysis of replication profiles reveals key role of RFC-Ctf18 in yeast replication stress response. Nat. Struct. Mol. Biol. 2010, 17:1391-1397.
75. Gellon L., et al. New functions of Ctf18-RFC in preserving genome stability outside its role in sister chromatid cohesion. PLoS Genet. 2011, 7:e1001298.
76. Bermudez V.P., et al. The alternative Ctf18-Dcc1-Ctf8-replication factor C complex required for sister chromatid cohesion loads proliferating cell nuclear antigen onto DNA. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:10237-10242.
77. Ramachandran N., et al. Self-assembling protein microarrays. Science 2004, 305:86-90.