The effects of oligomerization on Saccharomyces cerevisiae Mcm4/6/7 function

BMC Biochemistry

Volumn 11, Issue 1, 2010, Pages

  Ma, Xiaoli ^a   Stead, Brent E ^a   Rezvanpour, Atoosa ^a   Davey, Megan J ^a  

^a WESTERN UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ARGININE; MINICHROMOSOME MAINTENANCE PROTEIN 4; MINICHROMOSOME MAINTENANCE PROTEIN 6; MINICHROMOSOME MAINTENANCE PROTEIN 7; OLIGOMER; CDC47 PROTEIN, S CEREVISIAE; CDC54 PROTEIN, S CEREVISIAE; CELL CYCLE PROTEIN; CROSS LINKING REAGENT; DNA BINDING PROTEIN; MCM6 PROTEIN, S CEREVISIAE; NONHISTONE PROTEIN; NUCLEAR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; COMPLEX FORMATION; CROSS LINKING; GENE MUTATION; NONHUMAN; OLIGOMERIZATION; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; CHEMISTRY; METABOLISM; PROTEIN BINDING; PROTEIN MULTIMERIZATION;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATE; CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; CROSS-LINKING REAGENTS; DNA-BINDING PROTEINS; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 77957737377     PISSN: None     EISSN: 14712091     Source Type: Journal    
DOI: 10.1186/1471-2091-11-37     Document Type: Article

References (61)

1. Structure and mechanism of helicases and nucleic acid translocases. MR Singleton MS Dillingham DB Wigley, Annual Review of Biochemistry 2007 76 23 50 10.1146/annurev.biochem.76.052305.115300 17506634
2. Mcm4,6,7 uses a "pump in ring" mechanism to unwind DNA by steric exclusion and actively translocate along a duplex. DL Kaplan MJ Davey M O'Donnell, J Biol Chem 2003 278 49171 49182 10.1074/jbc.M308074200 13679365
3. A rotary pumping model for helicase function of MCM proteins at a distance from replication forks. RA Laskey MA Madine, EMBO Rep 2003 4 26 30 10.1038/sj.embor.embor706 12524516
4. Processive DNA helicase activity of the minichromosome maintenance proteins 4, 6, and 7 complex requires forked DNA structures. JK Lee J Hurwitz, Proc Natl Acad Sci USA 2001 98 54 59 10.1073/pnas.98.1.54 11136247
5. Pumps, paradoxes and ploughshares: mechanism of the MCM2-7 DNA helicase. TS Takahashi DB Wigley JC Walter, Trends in Biochemical Sciences 2005 30 437 444 10.1016/j.tibs.2005.06.007 16002295
6. Mechanism of DNA translocation in a replicative hexameric helicase. EJ Enemark L Joshua-Tor, Nature 2006 442 270 275 10.1038/nature04943 16855583
7. DNA is bound within the central hole to one or two of the six subunits of the T7 DNA helicase. X Yu MM Hingorani SS Patel EH Egelman, Nat Struct Biol 1996 3 740 743 10.1038/nsb0996-740 8784344
8. The Methanothermobacter thermautotrophicus MCM helicase is active as a hexameric ring. JH Shin GY Heo Z Kelman, J Biol Chem 2009 284 540 546 10.1074/jbc.M806803200 19001412
9. NS3 helicase from the hepatitis C virus can function as a monomer or oligomer depending on enzyme and substrate concentrations. TA Jennings SG Mackintosh MK Harrison D Sikora B Sikora B Dave AJ Tackett CE Cameron KD Raney, J Biol Chem 2009 284 4806 4814 10.1074/jbc.M805540200 19088075
10. Eukaryotic MCM proteins: beyond replication initiation. SL Forsburg, Microbiol Mol Biol Rev 2004 68 109 131 10.1128/MMBR.68.1.109-131.2004 15007098
11. The Mcm2-7 Complex Has In Vitro Helicase Activity. ML Bochman A Schwacha, Molecular Cell 2008 31 287 293 10.1016/j.molcel.2008.05.020 18657510
12. A DNA helicase activity is associated with an MCM4, -6, and -7 protein complex. Y Ishimi, J Biol Chem 1997 272 24508 24513 10.1074/jbc.272.39.24508 9305914
13. Mcm subunits can assemble into two different active unwinding complexes. DM Kanter I Bruck DL Kaplan, J Biol Chem 2008 283 31172 31182 10.1074/jbc.M804686200 18801730
14. Isolation and characterization of various complexes of the minichromosome maintenance proteins of Schizosaccharomyces pombe. JK Lee J Hurwitz, J Biol Chem 2000 275 18871 18878 10.1074/jbc.M001118200 10770926
15. Activation of the MCM2-7 Helicase by Association with Cdc45 and GINS Proteins. I Ilves T Petojevic JJ Pesavento MR Botchan, 2010 37 247 258 20122406
16. Cdc6p-dependent loading of MCM proteins onto pre-replicative chromatin in budding yeast. S Donovan J Harwood LS Drury JF Diffley, Proc Natl Acad Sci USA 1997 94 5611 5616 10.1073/pnas.94.11.5611 9159120
17. Physical interactions among Mcm proteins and effects of Mcm dosage on DNA replication in Saccharomyces cerevisiae. M Lei Y Kawasaki BK Tye, Mol Cell Biol 1996 16 5081 5090 8756666
18. Replication Dynamics of the Yeast Genome. MK Raghuraman EA Winzeler D Collingwood S Hunt L Wodicka A Conway DJ Lockhart RW Davis BJ Brewer WL Fangman, Science 2001 294 115 121 10.1126/science.294.5540.115 11588253
19. Genome-Wide Distribution of ORC and MCM Proteins in S. cerevisiae: High-Resolution Mapping of Replication Origins. JJ Wyrick JG Aparicio T Chen JD Barnett EG Jennings RA Young SP Bell OM Aparicio, Science 2001 294 2357 2360 10.1126/science.1066101 11743203
20. Global analysis of protein expression in yeast. S Ghaemmaghami WK Huh K Bower RW Howson A Belle N Dephoure EK O'Shea JS Weissman, Nature 2003 425 737 741 10.1038/nature02046 14562106
21. Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. XQ Ge DA Jackson JJ Blow, Genes Dev 2007 21 3331 3341 10.1101/gad.457807 18079179
22. Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. A Ibarra E Schwob J Mendez, Proc Natl Acad Sci USA 2008 105 8956 8961 10.1073/pnas.0803978105 18579778
23. Excess Mcm2-7 license dormant origins of replication that can be used under conditions of replicative stress. AM Woodward T Gohler MG Luciani M Oehlmann X Ge A Gartner DA Jackson JJ Blow, J Cell Biol 2006 173 673 683 10.1083/jcb.200602108 16754955
24. The DNA replication factor MCM5 is essential for Stat1-mediated transcriptional activation. M Snyder W He JJ Zhang, Proc Natl Acad Sci USA 2005 102 14539 14544 10.1073/pnas.0507479102 16199513
25. Ser727-dependent recruitment of MCM5 by Stat1alpha in IFN-gamma-induced transcriptional activation. JJ Zhang Y Zhao BT Chait WW Lathem M Ritzi R Knippers JE Darnell Jr, Embo J 1998 17 6963 6971 10.1093/emboj/17.23.6963 9843502
26. The mini-chromosome maintenance proteins 2-7 (MCM2-7) are necessary for RNA polymerase II (pol II)-mediated transcription. M Snyder XY Huang JJ Zhang, J Biol Chem 2009 284 13466 13472 10.1074/jbc.M809471200 19318354
27. Distinct parts of minichromosome maintenance protein 2 associate with histone H3/H4 and RNA polymerase II holoenzyme. L Holland L Gauthier P Bell-Rogers K Yankulov, Eur J Biochem 2002 269 5192 5202 10.1046/j.1432-1033. 2002.03224.x 12392551
28. A viable allele of Mcm4 causes chromosome instability and mammary adenocarcinomas in mice. N Shima A Alcaraz I Liachko TR Buske CA Andrews RJ Munroe SA Hartford BK Tye JC Schimenti, Nat Genet 2007 39 93 98 10.1038/ng1936 17143284
29. Minichromosome maintenance proteins interact with checkpoint and recombination proteins to promote s-phase genome stability. JM Bailis DD Luche T Hunter SL Forsburg, Mol Cell Biol 2008 28 1724 1738 10.1128/MCB.01717-07 18180284
30. Deregulated minichromosomal maintenance protein MCM7 contributes to oncogene driven tumorigenesis. KA Honeycutt Z Chen MI Koster M Miers J Nuchtern J Hicks DR Roop JM Shohet, Oncogene 2006 25 4027 4032 10.1038/sj.onc.1209435 16518415
31. Functional cooperation between FACT and MCM helicase facilitates initiation of chromatin DNA replication. BC Tan CT Chien S Hirose SC Lee, Embo J 2006 25 3975 3985 10.1038/sj.emboj.7601271 16902406
32. Regulation of replication fork progression through histone supply and demand. A Groth A Corpet AJ Cook D Roche J Bartek J Lukas G Almouzni, Science 2007 318 1928 1931 10.1126/science.1148992 18096807
33. Biochemical function of mouse minichromosome maintenance 2 protein. Y Ishimi Y Komamura Z You H Kimura, J Biol Chem 1998 273 8369 8375 10.1074/jbc.273.14.8369 9525946
34. Biochemical activities associated with mouse Mcm2 protein. Y Ishimi Y Komamura-Kohno K Arai H Masai, J Biol Chem 2001 276 42744 42752 10.1074/jbc.M106861200 11568184
35. Reconstitution of the Mcm2-7p heterohexamer, subunit arrangement, and ATP site architecture. MJ Davey C Indiani M O'Donnell, J Biol Chem 2003 278 4491 4499 10.1074/jbc.M210511200 12480933
36. Interactions between two catalytically distinct MCM subgroups are essential for coordinated ATP hydrolysis and DNA replication. A Schwacha SP Bell, Mol Cell 2001 8 1093 1104 10.1016/S1097-2765(01)00389-6 11741544
37. Biochemical analysis of the intrinsic Mcm4-Mcm6-mcm7 DNA helicase activity. Z You Y Komamura Y Ishimi, Mol Cell Biol 1999 19 8003 8015 10567526
38. Differences in the single-stranded DNA binding activities of MCM2-7 and MCM467: MCM2 and MCM5 define a slow ATP-dependent step. ML Bochman A Schwacha, J Biol Chem 2007 282 33795 33804 10.1074/jbc.M703824200 17895243
39. Cdt1 forms a complex with the minichromosome maintenance protein (MCM) and activates its helicase activity. Z You H Masai, J Biol Chem 2008 283 24469 24477 10.1074/jbc.M803212200 18606811
40. Electron microscopic observation and single-stranded DNA binding activity of the Mcm4,6,7 complex. M Sato T Gotow Z You Y Komamura-Kohno Y Uchiyama N Yabuta H Nojima Y Ishimi, J Mol Biol 2000 300 421 431 10.1006/jmbi.2000.3865 10884341
41. Cooperative Interactions of Nucleotide Ligands Are Linked to Oligomerization and DNA Binding in Bacteriophage T7 Gene 4 Helicases. MM Hingorani SS Patel, Biochemistry 1996 35 2218 2228 10.1021/bi9521497 8652563
42. Global Conformational Transitions in Escherichia coli Primary Replicative Helicase DnaB Protein Induced by ATP, ADP, and Single-stranded DNA Binding. MJ Jezewska W Bujalowski, J Biol Chem 1996 271 4261 4265 10.1074/jbc.271.8.4261 8626772
43. ATP-dependent assembly of double hexamers of SV40 T antigen at the viral origin of DNA replication. IA Mastrangelo PV Hough JS Wall M Dodson FB Dean J Hurwitz, Nature 1989 338 658 662 10.1038/338658a0 2539565
44. A two-protein strategy for the functional loading of a cellular replicative DNA helicase. M Velten S McGovern S Marsin SD Ehrlich P Noirot P Polard, Mol Cell 2003 11 1009 1020 10.1016/S1097-2765(03)00130-8 12718886
45. The P1 plasmid partition protein ParA. A role for ATP in site-specific DNA binding. MJ Davey BE Funnell, J Biol Chem 1994 269 29908 29913 7961987
46. ATP binding and hydrolysis by Mcm2 regulate DNA binding by Mcm complexes. BE Stead CD Sorbara CJ Brandl MJ Davey, Journal of Molecular Biology 2009 391 301 313 10.1016/j.jmb.2009.06.038 19540846
47. Subunit organization of Mcm2-7 and the unequal role of active sites in ATP hydrolysis and viability. ML Bochman SP Bell A Schwacha, Mol Cell Biol 2008 28 5865 5873 10.1128/MCB.00161-08 18662997
48. The simian virus 40 T antigen double hexamer assembles around the DNA at the replication origin. FB Dean JA Borowiec T Eki J Hurwitz, J Biol Chem 1992 267 14129 14137 1321135
49. Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. D Remus F Beuron G Tolun JD Griffith EP Morris JF Diffley, Cell 2009 139 719 730 10.1016/j.cell.2009.10.015 19896182
50. A double-hexameric MCM2-7 complex is loaded onto origin DNA during licensing of eukaryotic DNA replication. C Evrin P Clarke J Zech R Lurz J Sun S Uhle H Li B Stillman C Speck, Proc Natl Acad Sci USA 2009 106 20240 20245 10.1073/pnas.0911500106 19910535
51. Replisome assembly at oriC, the replication origin of E. coli, reveals an explanation for initiation sites outside an origin. L Fang MJ Davey M O'Donnell, Mol Cell 1999 4 541 553 10.1016/S1097-2765(00)80205-1 10549286
52. Characterization of Schizosaccharomyces pombe mcm7(+) and cdc23(+) (MCM10) and interactions with replication checkpoints. DT Liang SL Forsburg, Genetics 2001 159 471 486 11606526
53. Mammalian Mcm2/4/6/7 complex forms a toroidal structure. N Yabuta N Kajimura K Mayanagi M Sato T Gotow Y Uchiyama Y Ishimi H Nojima, Genes to Cells 2003 8 413 421 10.1046/j.1365-2443.2003.00645.x 12694531
54. Roles of Mcm7 and Mcm4 subunits in the DNA helicase activity of the mouse Mcm4/6/7 complex. Z You Y Ishimi H Masai F Hanaoka, J Biol Chem 2002 277 42471 42479 10.1074/jbc.M205769200 12207017
55. Localization of MCM2-7, Cdc45, and GINS to the site of DNA unwinding during eukaryotic DNA replication. M Pacek AV Tutter Y Kubota H Takisawa JC Walter, Mol Cell 2006 21 581 587 10.1016/j.molcel.2006.01.030 16483939
56. Structure of the replicative helicase of the oncoprotein SV40 large tumour antigen. D Li R Zhao W Lilyestrom D Gai R Zhang JA DeCaprio E Fanning A Jochimiak G Szakonyi XS Chen, Nature 2003 423 512 518 10.1038/nature01691 12774115
57. Rapid and efficient site-directed mutagenesis by single-tube 'megaprimer' PCR method. SH Ke EL Madison, Nucleic Acids Res 1997 25 3371 3372 10.1093/nar/25.16.3371 9241254
58. Genetic applications of an inverse polymerase chain reaction. H Ochman AS Gerber DL Hartl, Genetics 1988 120 621 623 2852134
59. Covalent attachment of DNA to agarose. Improved synthesis and use in affinity chromatography. DJ Arndt-Jovin TM Jovin W Bahr AM Frischauf M Marquardt, Eur J Biochem 1975 54 411 418 10.1111/j.1432-1033.1975.tb04151.x 1100376
60. Proteins and sodium dodecyl sulfate: molecular weight determination on polyacrylamide gels and related procedures. K Weber M Osborn, The Proteins New York: Academic Press, Neurath H, Hill RL, Third 1975 I 180 221
61. Sequential MCM/P1 subcomplex assembly is required to form a heterohexamer with replication licensing activity. TA Prokhorova JJ Blow, J Biol Chem 2000 275 2491 2498 10.1074/jbc.275.4.2491 10644704