Concerted interaction between origin recognition complex (ORC), nucleosomes and replication origin DNA ensures stable ORC-origin binding

Genes to Cells

Volumn 18, Issue 9, 2013, Pages 764-779

  Hizume, Kohji ^a,b   Yagura, Masaru ^a   Araki, Hiroyuki ^a,b  

^a NATIONAL INSTITUTE OF GENETICS   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

NAKED DNA; ORIGIN RECOGNITION COMPLEX; ORIGIN RECOGNITION COMPLEX 1; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING AFFINITY; CHROMATIN; COMPLEX FORMATION; DNA REPLICATION; MOLECULAR IMAGING; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN INTERACTION;

EUKARYOTA;

EID: 84883167380     PISSN: 13569597     EISSN: 13652443     Source Type: Journal    
DOI: 10.1111/gtc.12073     Document Type: Article

References (62)

1. Alexiadis, V., Varga-Weisz, P.D., Bonte, E., Becker, P.B. & Gruss, C. (1998) In vitro chromatin remodelling by chromatin accessibility complex (CHRAC) at the SV40 origin of DNA replication. EMBO J. 17, 3428-3438.
2. Austin, R.J., Orr-Weaver, T.L. & Bell, S.P. (1999) Drosophila ORC specifically binds to ACE3, an origin of DNA replication control element. Genes Dev. 13, 2639-2649.
3. Bell, S.P., Kobayashi, R. & Stillman, B. (1993) Yeast origin recognition complex functions in transcription silencing and DNA replication. Science 262, 1844-1849.
4. Bell, S.P., Mitchell, J., Leber, J., Kobayashi, R. & Stillman, B. (1995) The multidomain structure of Orc1p reveals similarity to regulators of DNA replication and transcriptional silencing. Cell 83, 563-568.
5. Bell, S.P. & Stillman, B. (1992) ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature 357, 128-134.
6. Berbenetz, N.M., Nislow, C. & Brown, G.W. (2010) Diversity of eukaryotic DNA replication origins revealed by genome-wide analysis of chromatin structure. PLoS Genet. 6, e1001092.
7. Berezney, R., Dubey, D.D. & Huberman, J.A. (2000) Heterogeneity of eukaryotic replicons, replicon clusters, and replication foci. Chromosoma 108, 471-484.
8. Carey, M.F., Peterson, C.L. & Smale, S.T. (2009) In vivo DNase I, MNase, and restriction enzyme footprinting via ligation-mediated polymerase chain reaction (LM-PCR). Cold Spring Harb. Protoc. 4, 1108-1120.
9. Chan, C.S. & Tye, B.K. (1980) Autonomously replicating sequences in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 77, 6329-6333.
10. Chang, F., Theis, J.F., Miller, J., Nieduszynski, C.A., Newlon, C.S. & Weinreich, M. (2008) Analysis of chromosome III replicators reveals an unusual structure for the ARS318 silencer origin and a conserved WTW sequence within the origin recognition complex binding site. Mol. Cell. Biol. 28, 5071-5081.
11. Chastain, P.D. , Bowers, J.L., Lee, D.G., Bell, S.P. & Griffith, J.D. (2004) Mapping subunit location on the Saccharomyces cerevisiae origin recognition complex free and bound to DNA using a novel nanoscale biopointer. J. Biol. Chem. 279, 36354-36362.
12. Chen, Z., Speck, C., Wendel, P., Tang, C., Stillman, B. & Li, H. (2008) The architecture of the DNA replication origin recognition complex in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 105, 10326-10331.
13. Chong, J.P., Mahbubani, H.M., Khoo, C.Y. & Blow, J.J. (1995) Purification of an MCM-containing complex as a component of the DNA replication licensing system. Nature 375, 418-421.
14. Clarey, M.G., Botchan, M. & Nogales, E. (2008) Single particle EM studies of the Drosophila melanogaster origin recognition complex and evidence for DNA wrapping. J. Struct. Biol. 164, 241-249.
15. Diffley, J.F., Cocker, J.H., Dowell, S.J. & Rowley, A. (1994) Two steps in the assembly of complexes at yeast replication origins in vivo. Cell 78, 303-316.
16. Donovan, S., Dowell, S., Diffley, J.F. & Rowley, A. (1999) Purification of yeast replication origin binding proteins. In: Eukaryotic DNA Replication (ed. S. Cotterill ), pp. 43-65. Oxford, UK: Oxford University Press.
17. Duncker, B.P., Chesnokov, I.N. & McConkey, B.J. (2009) The origin recognition complex protein family. Genome Biol. 10, 214.
18. Eaton, M.L., Galani, K., Kang, S., Bell, S.P. & MacAlpine, D.M. (2010) Conserved nucleosome positioning defines replication origins. Genes Dev. 24, 748-753.
19. Gaczynska, M., Osmulski, P.A., Jiang, Y., Lee, J.K., Bermudez, V. & Hurwitz, J. (2004) Atomic force microscopic analysis of the binding of the Schizosaccharomyces pombe origin recognition complex and the spOrc4 protein with origin DNA. Proc. Natl Acad. Sci. USA 101, 17952-17957.
20. Gilmore, J.L., Suzuki, Y., Tamulaitis, G., Siksnys, V., Takeyasu, K. & Lyubchenko, Y.L. (2009) Single-molecule dynamics of the DNA-EcoRII protein complexes revealed with high-speed atomic force microscopy. Biochemistry (Mosc) 48, 10492-10498.
21. Gregory, P.D., Barbaric, S. & Horz, W. (1999) Restriction nucleases as probes for chromatin structure. Methods Mol. Biol. 119, 417-425.
22. Hizume, K., Araki, S., Hata, K., Prieto, E., Kundu, T.K., Yoshikawa, K. & Takeyasu, K. (2010) Nano-scale analyses of the chromatin decompaction induced by histone acetylation. Arch. Histol. Cytol. 73, 149-163.
23. Hizume, K., Nakai, T., Araki, S., Prieto, E., Yoshikawa, K. & Takeyasu, K. (2009) Removal of histone tails from nucleosome dissects the physical mechanisms of salt-induced aggregation, linker histone H1-induced compaction, and 30-nm fiber formation of the nucleosome array. Ultramicroscopy 109, 868-873.
24. Hizume, K., Yoshimura, S.H. & Takeyasu, K. (2005) Linker histone H1 per se can induce three-dimensional folding of chromatin fiber. Biochemistry (Mosc) 44, 12978-12989.
25. Johnson, A., Li, G., Sikorski, T.W., Buratowski, S., Woodcock, C.L. & Moazed, D. (2009) Reconstitution of heterochromatin-dependent transcriptional gene silencing. Mol. Cell 35, 769-781.
26. Kawasaki, Y., Kim, H.D., Kojima, A., Seki, T. & Sugino, A. (2006) Reconstitution of Saccharomyces cerevisiae prereplicative complex assembly in vitro. Genes Cells 11, 745-756.
27. Klemm, R.D., Austin, R.J. & Bell, S.P. (1997) Coordinate binding of ATP and origin DNA regulates the ATPase activity of the origin recognition complex. Cell 88, 493-502.
28. Kong, D. & DePamphilis, M.L. (2001) Site-specific DNA binding of the Schizosaccharomyces pombe origin recognition complex is determined by the Orc4 subunit. Mol. Cell. Biol. 21, 8095-8103.
29. Kubota, Y., Mimura, S., Nishimoto, S., Takisawa, H. & Nojima, H. (1995) Identification of the yeast MCM3-related protein as a component of Xenopus DNA replication licensing factor. Cell 81, 601-609.
30. Kuo, A.J., Song, J., Cheung, P., Ishibe-Murakami, S., Yamazoe, S., Chen, J.K., Patel, D.J. & Gozani, O. (2012) The BAH domain of ORC1 links H4K20me2 to DNA replication licensing and Meier-Gorlin syndrome. Nature 484, 115-119.
31. Lee, D.G. & Bell, S.P. (1997) Architecture of the yeast origin recognition complex bound to origins of DNA replication. Mol. Cell. Biol. 17, 7159-7168.
32. Lee, J.K., Moon, K.Y., Jiang, Y. & Hurwitz, J. (2001) The Schizosaccharomyces pombe origin recognition complex interacts with multiple AT-rich regions of the replication origin DNA by means of the AT-hook domains of the spOrc4 protein. Proc. Natl Acad. Sci. USA 98, 13589-13594.
33. Li, G., Levitus, M., Bustamante, C. & Widom, J. (2005) Rapid spontaneous accessibility of nucleosomal DNA. Nat. Struct. Mol. Biol. 12, 46-53.
34. Lipford, J.R. & Bell, S.P. (2001) Nucleosomes positioned by ORC facilitate the initiation of DNA replication. Mol. Cell 7, 21-30.
35. Luger, K., Mader, A.W., Richmond, R.K., Sargent, D.F. & Richmond, T.J. (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251-260.
36. MacAlpine, H.K., Gordan, R., Powell, S.K., Hartemink, A.J. & MacAlpine, D.M. (2010) Drosophila ORC localizes to open chromatin and marks sites of cohesin complex loading. Genome Res. 20, 201-211.
37. Madine, M.A., Khoo, C.Y., Mills, A.D. & Laskey, R.A. (1995) MCM3 complex required for cell cycle regulation of DNA replication in vertebrate cells. Nature 375, 421-424.
38. Maiorano, D., Moreau, J. & Mechali, M. (2000) XCDT1 is required for the assembly of pre-replicative complexes in Xenopus laevis. Nature 404, 622-625.
39. Matsumoto, T., Go, K., Hyodo, M., Koiwai, K., Maezawa, S., Hayano, T., Suzuki, M. & Koiwai, O. (2012) BRCT domain of DNA polymerase mu has DNA-binding activity and promotes the DNA polymerization activity. Genes Cells 17, 790-806.
40. Mechali, M. (2010) Eukaryotic DNA replication origins: many choices for appropriate answers. Nat. Rev. Mol. Cell Biol. 11, 728-738.
41. Miyagi, A., Ando, T. & Lyubchenko, Y.L. (2011) Dynamics of nucleosomes assessed with time-lapse high-speed atomic force microscopy. Biochemistry (Mosc) 50, 7901-7908.
42. Moyer, S.E., Lewis, P.W. & Botchan, M.R. (2006) Isolation of the Cdc45/Mcm2-7/GINS (CMG) complex, a candidate for the eukaryotic DNA replication fork helicase. Proc. Natl Acad. Sci. USA 103, 10236-10241.
43. Muller, P., Park, S., Shor, E., Huebert, D.J., Warren, C.L., Ansari, A.Z., Weinreich, M., Eaton, M.L., MacAlpine, D.M. & Fox, C.A. (2010) The conserved bromo-adjacent homology domain of yeast Orc1 functions in the selection of DNA replication origins within chromatin. Genes Dev. 24, 1418-1433.
44. Muramatsu, S., Hirai, K., Tak, Y.S., Kamimura, Y. & Araki, H. (2010) CDK-dependent complex formation between replication proteins Dpb11, Sld2, Polε, and GINS in budding yeast. Genes Dev. 24, 602-612.
45. Newlon, C.S. & Theis, J.F. (1993) The structure and function of yeast ARS elements. Curr. Opin. Genet. Dev. 3, 752-758.
46. Nishitani, H., Lygerou, Z., Nishimoto, T. & Nurse, P. (2000) The Cdt1 protein is required to license DNA for replication in fission yeast. Nature 404, 625-628.
47. Noguchi, K., Vassilev, A., Ghosh, S., Yates, J.L. & DePamphilis, M.L. (2006) The BAH domain facilitates the ability of human Orc1 protein to activate replication origins in vivo. EMBO J. 25, 5372-5382.
48. Ohniwa, R.L., Morikawa, K., Takeshita, S.L., Kim, J., Ohta, T., Wada, C. & Takeyasu, K. (2007) Transcription-coupled nucleoid architecture in bacteria. Genes Cells 12, 1141-1152.
49. Prieto, E., Hizume, K., Kobori, T., Yoshimura, S.H. & Takeyasu, K. (2012) Core histone charge and linker histone H1 effects on the chromatin structure of Schizosaccharomyces pombe. Biosci. Biotechnol. Biochem. 76, 2261-2266.
50. Rao, H. & Stillman, B. (1995) The origin recognition complex interacts with a bipartite DNA binding site within yeast replicators. Proc. Natl Acad. Sci. USA 92, 2224-2228.
51. Remus, D., Beuron, F., Tolun, G., Griffith, J.D., Morris, E.P. & Diffley, J.F. (2009) Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell 139, 719-730.
52. Simpson, R.T. (1990) Nucleosome positioning can affect the function of a cis-acting DNA element in vivo. Nature 343, 387-389.
53. Speck, C., Chen, Z., Li, H. & Stillman, B. (2005) ATPase-dependent cooperative binding of ORC and Cdc6 to origin DNA. Nat. Struct. Mol. Biol. 12, 965-971.
54. Suzuki, Y., Higuchi, Y., Hizume, K., Yokokawa, M., Yoshimura, S.H., Yoshikawa, K. & Takeyasu, K. (2010) Molecular dynamics of DNA and nucleosomes in solution studied by fast-scanning atomic force microscopy. Ultramicroscopy 110, 682-688.
55. Tanaka, S., Umemori, T., Hirai, K., Muramatsu, S., Kamimura, Y. & Araki, H. (2007) CDK-dependent phosphorylation of Sld2 and Sld3 initiates DNA replication in budding yeast. Nature 445, 328-332.
56. Tanaka, T., Umemori, T., Endo, S., Muramatsu, S., Kanemaki, M., Kamimura, Y., Obuse, C. & Araki, H. (2011) Sld7, an Sld3-associated protein required for efficient chromosomal DNA replication in budding yeast. EMBO J. 30, 2019-2030.
57. Unnikrishnan, A., Gafken, P.R. & Tsukiyama, T. (2010) Dynamic changes in histone acetylation regulate origins of DNA replication. Nat. Struct. Mol. Biol. 17, 430-437.
58. Varga-Weisz, P.D., Wilm, M., Bonte, E., Dumas, K., Mann, M. & Becker, P.B. (1997) Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II. Nature 388, 598-602.
59. Vary, J.C. Jr, Fazzio, T.G. & Tsukiyama, T. (2004) Assembly of yeast chromatin using ISWI complexes. Methods Enzymol. 375, 88-102.
60. Vary, J.C. Jr, Gangaraju, V.K., Qin, J., Landel, C.C., Kooperberg, C., Bartholomew, B. & Tsukiyama, T. (2003) Yeast Isw1p forms two separable complexes in vivo. Mol. Cell. Biol. 23, 80-91.
61. Weinreich, M., Liang, C. & Stillman, B. (1999) The Cdc6p nucleotide-binding motif is required for loading mcm proteins onto chromatin. Proc. Natl Acad. Sci. USA 96, 441-446.
62. Zegerman, P. & Diffley, J.F. (2007) Phosphorylation of Sld2 and Sld3 by cyclin-dependent kinases promotes DNA replication in budding yeast. Nature 445, 281-285.