Cdc6-induced conformational changes in ORC bound to origin DNA revealed by cryo-electron microscopy

Structure

Volumn 20, Issue 3, 2012, Pages 534-544

  Sun, Jingchuan ^a   Kawakami, Hironori ^b   Zech, Juergen ^c   Speck, Christian ^c   Stillman, Bruce ^b   Li, Huilin ^a,d  

^a BROOKHAVEN NATIONAL LABORATORY   (United States)

^b Simons Center for Quantitative Biology   (United States)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEAL PROTEIN; ARS1 PROTEIN; CELL CYCLE PROTEIN 6; DOUBLE STRANDED DNA; FUNGAL DNA; ORIGIN RECOGNITION COMPLEX; ORIGIN RECOGNITION COMPLEX 1; ORIGIN RECOGNITION COMPLEX 2; ORIGIN RECOGNITION COMPLEX 3; ORIGIN RECOGNITION COMPLEX 4; ORIGIN RECOGNITION COMPLEX 5; ORIGIN RECOGNITION COMPLEX 6; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; DNA PROTEIN COMPLEX; FUNGAL CELL; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE;

CELL CYCLE PROTEINS; CRYOELECTRON MICROSCOPY; DNA-BINDING PROTEINS; MODELS, MOLECULAR; ORIGIN RECOGNITION COMPLEX; PROTEIN CONFORMATION; PROTEIN SUBUNITS; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

ARCHAEA; EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 84863296793     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2012.01.011     Document Type: Article

References (56)

1. Bell, S.P., and Stillman, B. (1992). ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature 357, 128-134.
2. Bell, S.P., Mitchell, J., Leber, J., Kobayashi, R., and Stillman, B. (1995). The multidomain structure of Orc1p reveals similarity to regulators of DNA replication and transcriptional silencing. Cell 83, 563-568.
3. Bell, S.P., and Dutta, A. (2002). DNA replication in eukaryotic cells. Annu. Rev. Biochem. 71, 333-374. (Pubitemid 34800224)
4. Bochman, M.L., and Schwacha, A. (2008). The Mcm2-7 complex has in vitro helicase activity. Mol. Cell 31, 287-293. (Pubitemid 352001397)
5. Botchan, M., and Berger, J. (2010). DNA replication: making two forks from one prereplication complex. Mol. Cell 40, 860-861.
6. Bowers, J.L., Randell, J.C., Chen, S., and Bell, S.P. (2004). ATP hydrolysis by ORC catalyzes reiterative Mcm2-7 assembly at a defined origin of replication. Mol. Cell 16, 967-978. (Pubitemid 40018406)
7. Chastain, P.D., II, Bowers, J.L., Lee, D.G., Bell, S.P., and 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. (Pubitemid 39128973)
8. Chen, S., de Vries, M.A., and Bell, S.P. (2007). Orc6 is required for dynamic recruitment of Cdt1 during repeated Mcm2-7 loading. Genes Dev. 21, 2897-2907. (Pubitemid 350133438)
9. Chen, Z., Speck, C., Wendel, P., Tang, C., Stillman, B., and Li, H. (2008). The architecture of the DNA replication origin recognition complex in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 105, 10326-10331.
10. Chesnokov, I.N., Chesnokova, O.N., and Botchan, M. (2003). A cytokinetic function of Drosophila ORC6 protein resides in a domain distinct from its replication activity. Proc. Natl. Acad. Sci. USA 100, 9150-9155. (Pubitemid 37033898)
11. Clarey, M.G., Erzberger, J.P., Grob, P., Leschziner, A.E., Berger, J.M., Nogales, E., and Botchan, M. (2006). Nucleotide-dependent conformational changes in the DnaA-like core of the origin recognition complex. Nat. Struct. Mol. Biol. 13, 684-690. (Pubitemid 44175160)
12. Clarey, M.G., Botchan, M., and 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.
13. Dhar, S.K., Delmolino, L., and Dutta, A. (2001). Architecture of the human origin recognition complex. J. Biol. Chem. 276, 29067-29071.
14. Duderstadt, K.E., Mott, M.L., Crisona, N.J., Chuang, K., Yang, H., and Berger, J.M. (2010). Origin remodeling and opening in bacteria rely on distinct assembly states of the DnaA initiator. J. Biol. Chem. 285, 28229-28239.
15. Dueber, E.L., Corn, J.E., Bell, S.D., and Berger, J.M. (2007). Replication origin recognition and deformation by a heterodimeric archaeal Orc1 complex. Science 317, 1210-1213.
16. Duncker, B.P., Chesnokov, I.N., and McConkey, B.J. (2009). The origin recognition complex protein family. Genome Biol. 10, 214.
17. Eaton, M.L., Galani, K., Kang, S., Bell, S.P., and MacAlpine, D.M. (2010). Conserved nucleosome positioning defines replication origins. Genes Dev. 24, 748-753.
18. Erzberger, J.P., Mott, M.L., and Berger, J.M. (2006). Structural basis for ATP-dependent DnaA assembly and replication-origin remodeling. Nat. Struct. Mol. Biol. 13, 676-683. (Pubitemid 44175159)
19. Evrin, C., Clarke, P., Zech, J., Lurz, R., Sun, J., Uhle, S., Li, H., Stillman, B., and Speck, C. (2009). A double-hexameric MCM2-7 complex is loaded onto origin DNA during licensing of eukaryotic DNA replication. Proc. Natl. Acad. Sci. USA 106, 20240-20245.
20. Gaudier, M., Schuwirth, B.S., Westcott, S.L., and Wigley, D.B. (2007). Structural basis of DNA replication origin recognition by an ORC protein. Science 317, 1213-1216.
21. Grigorieff, N. (2000). Resolution measurement in structures derived from single particles. Acta Crystallogr. D Biol. Crystallogr. 56, 1270-1277.
22. Houchens, C.R., Lu,W.,Chuang, R.Y., Frattini,M.G., Fuller, A., Simancek, P.,and Kelly, T.J. (2008). Multiple mechanisms contribute to Schizosaccharomyces pombe origin recognition complex-DNA interactions. J. Biol. Chem. 283, 30216-30224.
23. Hsu, H.C., Stillman, B., and Xu, R.M. (2005). Structural basis for origin recognition complex 1 protein-silence information regulator 1 protein interaction in epigenetic silencing. Proc. Natl. Acad. Sci. USA 102, 8519-8524. (Pubitemid 40862768)
24. Iyer, L.M., Leipe, D.D., Koonin, E.V., and Aravind, L. (2004). Evolutionary history and higher order classification of AAA+ ATPases. J. Struct. Biol. 146, 11-31. (Pubitemid 38369015)
25. Jang, S.W., Elsasser, S., Campbell, J.L., and Kim, J. (2001). Identification of Cdc6 protein domains involved in interaction with Mcm2 protein and Cdc4 protein in budding yeast cells. Biochem. J. 354, 655-661. (Pubitemid 32269729)
26. Kawakami, H., and Katayama, T. (2010). DnaA, ORC, and Cdc6: similarity beyond the domains of life and diversity. Biochem. Cell Biol. 88, 49-62.
27. Kelley, L.A., and Sternberg, M.J. (2009). Protein structure prediction on the web: a case study using the Phyre server. Nat. Protoc. 4, 363-371.
28. Klemm, R.D., Austin, R.J., and Bell, S.P. (1997). Coordinate binding of ATP and origin DNA regulates the ATPase activity of the origin recognition complex. Cell 88, 493-502. (Pubitemid 27154414)
29. Kornberg, A., and Baker, T.A. (1992). DNA Replication, Second Edition (New York: Freeman).
30. Labib, K. (2011). Building a double hexamer of DNA helicase at eukaryotic replication origins. EMBO J. 30, 4853-4855.
31. Lee, D.G., and Bell, S.P. (1997). Architecture of the yeast origin recognition complex bound to origins of DNA replication. Mol. Cell. Biol. 17, 7159-7168. (Pubitemid 27505946)
32. Lee, D.G., Makhov, A.M., Klemm, R.D., Griffith, J.D., and Bell, S.P. (2000). Regulation of origin recognition complex conformation and ATPase activity: differential effects of single-stranded and double-stranded DNA binding. EMBO J. 19, 4774-4782.
33. Liang, C., Weinreich, M., and Stillman, B. (1995). ORC and Cdc6p interact and determine the frequency of initiation of DNA replication in the genome. Cell 81, 667-676.
34. Liu, J., Smith, C.L., DeRyckere, D., DeAngelis, K., Martin, G.S., and Berger, J.M. (2000). Structure and function of Cdc6/Cdc18: implications for origin recognition and checkpoint control. Mol. Cell 6, 637-648.
35. Liu, X., Bushnell, D.A., Wang, D., Calero, G., and Kornberg, R.D. (2010). Structure of an RNA polymerase II-TFIIB complex and the transcription initiation mechanism. Science 327, 206-209.
36. Ludtke, S.J., Baldwin, P.R., and Chiu, W. (1999). EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97. (Pubitemid 30013436)
37. Mizushima, T., Takahashi, N., and Stillman, B. (2000). Cdc6p modulates the structure and DNA binding activity of the origin recognition complex in vitro. Genes Dev. 14, 1631-1641. (Pubitemid 30460912)
38. Mott, M.L., and Berger, J.M. (2007). DNA replication initiation: mechanisms and regulation in bacteria. Nat. Rev. Microbiol. 5, 343-354. (Pubitemid 46605488)
39. Müller, P., Park, S., Shor, E., Huebert, D.J., Warren, C.L., Ansari, A.Z., Weinreich, M., Eaton, M.L., MacAlpine, D.M., and 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.
40. Onishi, M., Liou, G.G., Buchberger, J.R., Walz, T., and Moazed, D. (2007). Role of the conserved Sir3-BAH domain in nucleosome binding and silent chromatin assembly. Mol. Cell 28, 1015-1028. (Pubitemid 350297032)
41. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., and Ferrin, T.E. (2004). UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612.
42. Pintilie, G.D., Zhang, J., Goddard, T.D., Chiu, W., and Gossard, D.C. (2010). Quantitative analysis of cryo-EM density map segmentation by watershed and scale-space filtering, and fitting of structures by alignment to regions. J. Struct. Biol. 170, 427-438.
43. Randell, J.C., Bowers, J.L., Rodríguez, H.K., and Bell, S.P. (2006). Sequential ATP hydrolysis by Cdc6 and ORC directs loading of the Mcm2-7 helicase. Mol. Cell 21, 29-39. (Pubitemid 43017846)
44. Remus, D., and Diffley, J.F. (2009). Eukaryotic DNA replication control: lock and load, then fire. Curr. Opin. Cell Biol. 21, 771-777.
45. Remus, D., Beall, E.L., and Botchan, M.R. (2004). DNA topology, not DNA sequence, is a critical determinant for Drosophila ORC-DNA binding. EMBO J. 23, 897-907. (Pubitemid 38418756)
46. Remus, D., Beuron, F., Tolun, G., Griffith, J.D., Morris, E.P., and Diffley, J.F. (2009). Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell 139, 719-730.
47. Siddiqui, K., and Stillman, B. (2007). ATP-dependent assembly of the human origin recognition complex. J. Biol. Chem. 282, 32370-32383. (Pubitemid 350106415)
48. Singleton, M.R., Morales, R., Grainge, I., Cook, N., Isupov, M.N., and Wigley, D.B. (2004). Conformational changes induced by nucleotide binding in Cdc6/ORC from Aeropyrum pernix. J. Mol. Biol. 343, 547-557. (Pubitemid 39311604)
49. Speck, C., and Stillman, B. (2007). Cdc6 ATPase activity regulates ORC$Cdc6 stability and the selection of specific DNA sequences as origins of DNA replication. J. Biol. Chem. 282, 11705-11714. (Pubitemid 47100659)
50. Speck, C., Chen, Z., Li, H., and Stillman, B. (2005). ATPase-dependent cooperative binding of ORC and Cdc6 to origin DNA. Nat. Struct. Mol. Biol. 12, 965-971.
51. Stillman, B. (2005). Origin recognition and the chromosome cycle. FEBS Lett. 579, 877-884.
52. Takara, T.J., and Bell, S.P. (2011). Multiple Cdt1 molecules act at each origin to load replication-competent Mcm2-7 helicases. EMBO J. 30, 4885-4896.
53. Tsai, F.T., and Sigler, P.B. (2000). Structural basis of preinitiation complex assembly on human pol II promoters. EMBO J. 19, 25-36. (Pubitemid 30009222)
54. Tsakraklides, V., and Bell, S.P. (2010). Dynamics of pre-replicative complex assembly. J. Biol. Chem. 285, 9437-9443.
55. Vashee, S., Simancek, P., Challberg, M.D., and Kelly, T.J. (2001). Assembly of the human origin recognition complex. J. Biol. Chem. 276, 26666-26673.
56. Zhang, Z., Hayashi, M.K., Merkel, O., Stillman, B., and Xu, R.M. (2002). Structure and function of the BAH-containing domain of Orc1p in epigenetic silencing. EMBO J. 21, 4600-4611. (Pubitemid 34984347)