The Mini-Chromosome Maintenance (Mcm) Complexes Interact with DNA Polymerase α-Primase and Stimulate Its Ability to Synthesize RNA Primers

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  You, Zhiying ^a   De Falco, Mariarosaria ^b   Kamada, Katsuhiko ^c   Pisani, Francesca M ^b   Masai, Hisao ^a  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^b INSTITUTE OF PROTEIN BIOCHEMISTRY   (Italy)

^c Japan Science and Technology Agency   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DNA DIRECTED DNA POLYMERASE ALPHA; DNA PRIMASE; GLYCEROL; HELICASE; HETERODIMER; MINICHROMOSOME MAINTENANCE PROTEIN; MINICHROMOSOME MAINTENANCE PROTEIN 2; MINICHROMOSOME MAINTENANCE PROTEIN 3; MINICHROMOSOME MAINTENANCE PROTEIN 4; MINICHROMOSOME MAINTENANCE PROTEIN 5; MINICHROMOSOME MAINTENANCE PROTEIN 6; MINICHROMOSOME MAINTENANCE PROTEIN 7; PRIMER RNA; PROTEIN P48; PROTEIN P58; ADENOSINE TRIPHOSPHATASE; DNA DIRECTED DNA POLYMERASE BETA; DNA HELICASE; DNA POLYMERASE ALPHA-PRIMASE; MULTIPROTEIN COMPLEX; PROTEIN BINDING; PROTEIN SUBUNIT; RNA; RNA PRIMERS; SINGLE STRANDED DNA;

ANIMAL CELL; ARTICLE; CHROMOSOME; DENSITY GRADIENT CENTRIFUGATION; DNA PROTEIN COMPLEX; DNA SYNTHESIS; EUKARYOTE; GEL MOBILITY SHIFT ASSAY; HUMAN; MOUSE; NONHUMAN; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN HYDROLYSIS; PROTEIN SUBUNIT; RNA SYNTHESIS; ANIMAL; BIOSYNTHESIS; HYDROLYSIS; METABOLISM;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANIMALS; DNA HELICASES; DNA POLYMERASE I; DNA PRIMASE; DNA, SINGLE-STRANDED; HUMANS; HYDROLYSIS; MICE; MINICHROMOSOME MAINTENANCE PROTEINS; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; PROTEIN SUBUNITS; RNA;

EID: 84882735325     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072408     Document Type: Article

References (58)

1. Masai H, Matsumoto S, You Z, Yoshizawa-Sugata N, Oda M, (2010) Eukaryotic chromosome DNA replication: where, when, and how? Annu Rev Biochem 79: 89-130.
2. Ishimi Y, (1997) A DNA helicase activity is associated with an MCM4,-6, and-7 protein complex. J Biol Chem 272: 24508-24513.
3. You Z, Komamura Y, Ishimi Y, (1999) Biochemical analysis of the intrinsic Mcm4-Mcm6-mcm7 DNA helicase activity. Mol Cell Biol 19: 8003-8015.
4. Kaplan DL, Davey MJ, O'Donnell M, (2003) Mcm4,6,7 uses a "pump in ring" mechanism to unwind DNA by steric exclusion and actively translocate along a duplex. J Biol Chem 278: 49171-49182.
5. You Z, Masai H, (2008) Cdt1 forms a complex with the minichromosome maintenance protein (MCM) and activates its helicase activity. J Biol Chem 283: 24469-24477.
6. Bochman ML, Schwacha A, (2008) The Mcm2-7 complex has in vitro helicase activity. Mol Cell 31: 287-293.
7. Bochman ML, Schwacha A, (2009) The Mcm complex: unwinding the mechanism of a replicative helicase. Microbiol Mol Biol Rev 73: 652-683.
8. 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: 247-258.
9. Gambus A, Jones RC, Sanchez-Diaz A, Kanemaki M, van Deursen F, et al. (2006) GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat Cell Biol 8: 358-366.
10. Gambus A, van Deursen F, Polychronopoulos D, Foltman M, Jones RC, 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: 2992-3004.
11. Marinsek N, Barry ER, Makarova KS, Dionne I, Koonin EV, et al. (2006) GINS, a central nexus in the archaeal DNA replication fork. EMBO Rep 7: 539-545.
12. Yoshimochi T, Fujikane R, Kawanami M, Matsunaga F, Ishino Y, (2008) The GINS complex from Pyrococcus furiosus stimulates the MCM helicase activity. J Biol Chem 283: 1601-1609.
13. De Falco M, Ferrari E, De Felice M, Rossi M, Hubscher U, et al. (2007) The human GINS complex binds to and specifically stimulates human DNA polymerase alpha-primase. EMBO Rep 8: 99-103.
14. Arezi B, Kuchta RD, (2000) Eukaryotic DNA primase. Trends Biochem Sci 25: 572-576.
15. Kuchta RD, Stengel G, (2010) Mechanism and evolution of DNA primases. Biochim Biophys Acta 1804: 1180-1189.
16. Corn JE, Pelton JG, Berger JM, (2008) Identification of a DNA primase template tracking site redefines the geometry of primer synthesis. Nat Struct Mol Biol 15: 163-169.
17. Arai K, Kornberg A, (1979) A general priming system employing only dnaB protein and primase for DNA replication. Proc Natl Acad Sci U S A 76: 4308-4312.
18. Lu YB, Ratnakar PV, Mohanty BK, Bastia D, (1996) Direct physical interaction between DnaG primase and DnaB helicase of Escherichia coli is necessary for optimal synthesis of primer RNA. Proc Natl Acad Sci U S A 93: 12902-12907.
19. Mitkova AV, Khopde SM, Biswas SB, (2003) Mechanism and stoichiometry of interaction of DnaG primase with DnaB helicase of Escherichia coli in RNA primer synthesis. J Biol Chem 278: 52253-52261.
20. Wang G, Klein MG, Tokonzaba E, Zhang Y, Holden LG, et al. (2008) The structure of a DnaB-family replicative helicase and its interactions with primase. Nat Struct Mol Biol 15: 94-100.
21. Bird LE, Pan H, Soultanas P, Wigley DB, (2000) Mapping protein-protein interactions within a stable complex of DNA primase and DnaB helicase from Bacillus stearothermophilus. Biochemistry 39: 171-182.
22. Corn JE, Berger JM, (2006) Regulation of bacterial priming and daughter strand synthesis through helicase-primase interactions. Nucleic Acids Res 34: 4082-4088.
23. Bailey S, Eliason WK, Steitz TA, (2007) Structure of hexameric DnaB helicase and its complex with a domain of DnaG primase. Science 318: 459-463.
24. Patel SS, Pandey M, Nandakumar D, (2011) Dynamic coupling between the motors of DNA replication: hexameric helicase, DNA polymerase, and primase. Curr Opin Chem Biol 15: 595-605.
25. Johnson DE, Takahashi M, Hamdan SM, Lee SJ, Richardson CC, (2007) Exchange of DNA polymerases at the replication fork of bacteriophage T7. Proc Natl Acad Sci U S A 104: 5312-5317.
26. Stano NM, Jeong YJ, Donmez I, Tummalapalli P, Levin MK, et al. (2005) DNA synthesis provides the driving force to accelerate DNA unwinding by a helicase. Nature 435: 370-373.
27. Pandey M, Syed S, Donmez I, Patel G, Ha T, et al. (2009) Coordinating DNA replication by means of priming loop and differential synthesis rate. Nature 462: 940-943.
28. Hinton DM, Nossal NG, (1987) Bacteriophage T4 DNA primase-helicase. Characterization of oligomer synthesis by T4 61 protein alone and in conjunction with T4 41 protein. J Biol Chem 262: 10873-10878.
29. Valentine AM, Ishmael FT, Shier VK, Benkovic SJ, (2001) A zinc ribbon protein in DNA replication: primer synthesis and macromolecular interactions by the bacteriophage T4 primase. Biochemistry 40: 15074-15085.
30. Yang J, Xi J, Zhuang Z, Benkovic SJ, (2005) The oligomeric T4 primase is the functional form during replication. J Biol Chem 280: 25416-25423.
31. Collins KL, Kelly TJ, (1991) Effects of T antigen and replication protein A on the initiation of DNA synthesis by DNA polymerase alpha-primase. Mol Cell Biol 11: 2108-2115.
32. Schneider C, Weisshart K, Guarino LA, Dornreiter I, Fanning E, (1994) Species-specific functional interactions of DNA polymerase alpha-primase with simian virus 40 (SV40) T antigen require SV40 origin DNA. Mol Cell Biol 14: 3176-3185.
33. Weisshart K, Forster H, Kremmer E, Schlott B, Grosse F, et al. (2000) Protein-protein interactions of the primase subunits p58 and p48 with simian virus 40 T antigen are required for efficient primer synthesis in a cell-free system. J Biol Chem 275: 17328-17337.
34. Saitoh A, Tada S, Katada T, Enomoto T, (1995) Stimulation of mouse DNA primase-catalyzed oligoribonucleotide synthesis by mouse DNA helicase B. Nucleic Acids Res. 23: 2014-2018.
35. Kawaguchi A, Nagata K, (2007) De novo replication of the influenza virus RNA genome is regulated by DNA replicative helicase, MCM. EMBO J 26: 4566-4575.
36. McGeoch AT, Bell SD, (2005) Eukaryotic/archaeal primase and MCM proteins encoded in a bacteriophage genome. Cell 120: 167-168.
37. Sanchez-Berrondo J, Mesa P, Ibarra A, Martinez-Jimenez MI, Blanco L, et al. (2012) Molecular architecture of a multifunctional MCM complex. Nucleic Acids Res 40: 1366-1380.
38. Bauer RJ, Graham BW, Trakselis MA (2013) Novel Interaction of the Bacterial-Like DnaG Primase with the MCM Helicase in Archaea. J Mol Biol.
39. Thommes P, Fett R, Schray B, Burkhart R, Barnes M, et al. (1992) Properties of the nuclear P1 protein, a mammalian homologue of the yeast Mcm3 replication protein. Nucleic Acids Res 20: 1069-1074.
40. Mizuno T, Yamagishi K, Miyazawa H, Hanaoka F, (1999) Molecular architecture of the mouse DNA polymerase alpha-primase complex. Mol Cell Biol 19: 7886-7896.
41. You Z, Ishimi Y, Mizuno T, Sugasawa K, Hanaoka F, et al. (2003) Thymine-rich single-stranded DNA activates Mcm4/6/7 helicase on Y-fork and bubble-like substrates. Embo J 22: 6148-6160.
42. 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: 33795-33804.
43. Holmes AM, Cheriathundam E, Bollum FJ, Chang LM, (1985) Initiation of DNA synthesis by the calf thymus DNA polymerase-primase complex. J Biol Chem 260: 10840-10846.
44. Patel SS, Picha KM, (2000) Structure and function of hexameric helicases. Annu Rev Biochem 69: 651-697.
45. Arai K, Kornberg A, (1981) Mechanism of dnaB protein action. III. Allosteric role of ATP in the alteration of DNA structure by dnaB protein in priming replication. J Biol Chem 256: 5260-5266.
46. Shrimankar P, Stordal L, Maurer R, (1992) Purification and characterization of a mutant DnaB protein specifically defective in ATP hydrolysis. J Bacteriol 174: 7689-7696.
47. Sato M, Gotow T, You Z, Komamura-Kohno Y, Uchiyama Y, et al. (2000) Electron microscopic observation and single-stranded DNA binding activity of the Mcm4,6,7 complex. J Mol Biol 300: 421-431.
48. Frick DN, Richardson CC, (2001) DNA primases. Annu Rev Biochem 70: 39-80.
49. Nunez-Ramirez R, Klinge S, Sauguet L, Melero R, Recuero-Checa MA, et al. (2011) Flexible tethering of primase and DNA Pol alpha in the eukaryotic primosome. Nucleic Acids Res 39: 8187-8199.
50. Kukimoto I, Igaki H, Kanda T, (1999) Human CDC45 protein binds to minichromosome maintenance 7 protein and the p70 subunit of DNA polymerase alpha. Eur J Biochem 265: 936-943.
51. Ricke RM, Bielinsky AK, (2004) Mcm10 regulates the stability and chromatin association of DNA polymerase-alpha. Mol Cell 16: 173-185.
52. Zhu W, Ukomadu C, Jha S, Senga T, Dhar SK, et al. (2007) Mcm10 and And-1/CTF4 recruit DNA polymerase alpha to chromatin for initiation of DNA replication. Genes Dev 21: 2288-2299.
53. Mimura S, Takisawa H, (1998) Xenopus Cdc45-dependent loading of DNA polymerase alpha onto chromatin under the control of S-phase Cdk. Embo J 17: 5699-5707.
54. Kanke M, Kodama Y, Takahashi TS, Nakagawa T, Masukata H, (2012) Mcm10 plays an essential role in origin DNA unwinding after loading of the CMG components. EMBO J 31: 2182-2194.
55. van Deursen F, Sengupta S, De Piccoli G, Sanchez-Diaz A, Labib K, (2012) Mcm10 associates with the loaded DNA helicase at replication origins and defines a novel step in its activation. EMBO J 31: 2195-2206.
56. Costa A, Ilves I, Tamberg N, Petojevic T, Nogales E, et al. (2011) The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nat Struct Mol Biol 18: 471-477.
57. Manosas M, Spiering MM, Zhuang Z, Benkovic SJ, Croquette V, (2009) Coupling DNA unwinding activity with primer synthesis in the bacteriophage T4 primosome. Nat Chem Biol 5: 904-912.
58. Schneider A, Smith RW, Kautz AR, Weisshart K, Grosse F, et al. (1998) Primase activity of human DNA polymerase alpha-primase. Divalent cations stabilize the enzyme activity of the p48 subunit. J Biol Chem 273: 21608-21615.