Initiation of DNA replication: Lessons from viral initiator proteins

Nature Reviews Molecular Cell Biology

Volumn 4, Issue 10, 2003, Pages 777-785

  Stenlund, Arne ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYCLINE; DNA; DNA BINDING PROTEIN; DNA POLYMERASE; DNA TOPOISOMERASE; HELICASE; INITIATION FACTOR; INITIATOR PROTEIN; REPLICATION PROTEIN A; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

DNA BINDING; DNA REPLICATION; DNA REPLICATION ORIGIN; ENZYME ACTIVITY; NONHUMAN; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; REVIEW; SIMIAN VIRUS 40; TRANSLATION INITIATION;

ADENOSINE TRIPHOSPHATE; DNA HELICASES; DNA REPLICATION; DNA-BINDING PROTEINS; MODELS, GENETIC; MODELS, MOLECULAR; REPLICATION ORIGIN; VIRAL PROTEINS;

PAPILLOMAVIRUS; SIMIAE; SIMIAN VIRUS 40;

EID: 0141891451     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrm1226     Document Type: Review

References (83)

1. Jacob, F., Brenner, S. & Cuzin, F. On the regulation of DNA replication in bacteria. Cold Spring Harb. Symp. Quant. Biol. 28, 329-348 (1963).
2. Bell, S. P. The origin recognition complex: from simple origins to complex functions. Genes Dev. 16, 659-672 (2002).
3. Sedman, J. & Stenlund, A. Co-operative interaction between the initiator E1 and the transcriptional activator E2 is required for replicator specific DNA replication of bovine papillomavirus in vivo and in vitro. EMBO J. 14, 6218-6228 (1995).
4. Lorimer, H. E., Wang, E. H. & Prives, C. The DNA-binding properties of polyomavirus large T antigen are altered by ATP and other nucleotides. J. Virol. 65, 687-699 (1991).
5. Yang, L. et al. The E1 protein of bovine papilloma virus 1 is an ATP-dependent DNA helicase. Proc. Natl Acad Sci. USA 90, 5086-5090 (1993).
6. Chen, G. & Stenlund, A. Two patches of amino acids on the E2 DNA binding domain define the surface for interaction with E1. J. Virol. 74, 1506-1512 (2000).
7. Berg, M. & Stenlund, A. Functional interactions between papillomavirus E1 and E2 proteins. J. Virol. 71, 3853-3863 (1997).
8. Gillitzer, E., Chen, G. & Stenlund, A. Separate domains in E1 and E2 proteins serve architectural and productive roles for cooperative DNA binding. EMBO J. 19, 3069-3079 (2000).
9. Mohr, I. J. et al. Targeting the E1 replication protein to the papillomavirus origin of replication by complex formation with the E2 transactivator. Science 250, 1694-1699 (1990)
10. Sanders, C. M. & Stenlund, A. Recruitment and loading of the E1 initiator protein: an ATP-dependent process catalysed by a transcription factor. EMBO J. 17, 7044-7055 (1998). This paper describes the original observation that E2 loads the initiator E1 in an ATP-dependent process.
11. Sanders, C. M. & Stenlund, A. Transcription factor-dependent loading of the E1 initiator reveals modular assembly of the papillomavirus origin melting complex. J. Biol. Chem. 275, 3522-3534 (2000).
12. Alberts, B. & Miake-Lye, R. Unscrambling the puzzle of biological machines: the importance of the details. Cell 68, 415-420 (1992).
13. Stenlund, A. E1 initiator DNA binding specificity is unmasked by selective inhibition of non-specific DNA binding. EMBO J. 22, 954-963 (2003).
14. Chuang, R. Y. & Kelly, T. J. The fission yeast homologue of Orc4p binds to replication origin DNA via multiple AT-hooks. Proc. Natl Acad. Sci. USA 96, 2656-2661 (1999)
15. Luo, X., Sanford, D. G., Bullock, P. A. & Bachovchin, W. W. Solution structure of the origin DNA-binding domain of SV40 T-antigen. Nature Struct. Biol. 3, 1034-1039 (1996).
16. Enemark, E. J., Chen, G., Vaughn, D. E., Stenlund, A. & Joshua-Tor, L. Crystal structure of the DNA binding domain of the replication initiation protein E1 from papillomavirus. Mol. Cell 6, 149-158 (2000).
17. Hickman, A. B., Ronning, D. R., Kotin, R. M. & Dyda, F. Structural unity among viral origin binding proteins: crystal structure of the nuclease domain of adeno-associated virus Rep. Mol. Cell 10, 327-337 (2002).
18. Campos-Olivas, R., Louis, J. M., Clerot, D., Gronenborn, B. & Gronenborn, A. M. The structure of a replication initiator unites diverse aspects of nucleic acid metabolism. Proc. Natl Acad. Sci. USA 99, 10310-10315 (2002). References 15-18 describe the highly related DNA-binding domain structures from four viral initiator proteins.
19. Speck, C. & Messer, W. Mechanism of origin unwinding: sequential binding of DnaA to double- and single-stranded DNA. EMBO J. 20, 1469-1476 (2001).
20. Lee, D. G., Makhov, A. M., Klemm, R. D., Griffith, J. D. & Bell, S. P. Regulation of origin recognition complex conformation and ATPase activity: differential effects of single-stranded and double-stranded DNA binding. EMBO J. 19, 4774-4782 (2000).
21. Liu, J. et al. Structure and function of Cdc6/Cdc18: implications for origin recognition and checkpoint control. Mol. Cell 6, 637-648 (2000).
22. Erzberger, J. P., Pirruccello, M. M. & Berger, J. M. The structure of bacterial DnaA: implications for general mechanisms underlying DNA replication initiation. EMBO J. 21, 4763-4773 (2002).
23. Tijan, R. The binding site on SV40 DNA for a T-antigen related protein. Cell 13, 165-179 (1978).
24. Joo, W. S. et al. Purification of the simian virus 40 (SV40) T antigen DNA-binding domain and characterization of its interactions with the SV40 origin. J. Virol. 71, 3972-3985 (1997).
25. Chen, G. & Stenlund, A. Characterization of the DNA-binding domain of the bovine papillomavirus replication initiator E1. J. Virol. 72, 2567-2576 (1998).
26. Chen, G. & Stenlund, A. The E1 initiator recognizes multiple overlapping sites in the papillomavirus origin of DNA replication. J. Virol. 75, 292-302 (2001).
27. Enemark, E. J., Stenlund, A. & Joshua-Tor, L. Crystal structures of two intermediates in the assembly of the papillomavirus replication initiation complex EMBO J. 21, 1487-1496 (2002). Provides the most complete high-resolution description of how initiator proteins bind to DNA.
28. Chen, G. & Stenlund, A. Sequential and ordered assembly of E1 initiator complexes on the papillomavirus origin of DNA replication generates progressive structural changes related to melting. Mol. Cell. Biol. 22, 7712-7720 (2002).
29. Valle, M., Gruss, C., Halmer, L., Carazo, J. M. & Donate, L. E. Large T-antigen double hexamers imaged at the simian virus 40 origin of replication. Mol. Cell. Biol. 20, 34-41 (2000) An EM study providing image reconstructions of the dumb-bell shape that the SV40 T-ag double hexamer adopts when bound to the SV40 origin of DNA replication.
30. Mastrangelo, I. A. et al. ATP-dependent assembly of double hexamers of SV40 T antigen at the viral origin of DNA replication. Nature 338, 658-662 (1989). Describes the original identification of the T-ag double-hexamer complex by STEM (scanning transmission electron microscopy).
31. Sanders, C. M. & Stenlund, A. Mechanism and requirements for bovine papillomavirus, type 1, E1 initiator complex assembly promoted by the E2 transcription factor bound to distal sites. J. Biol. Chem. 276, 23689-23699 (2001).
32. Borowiec, J. A. & Hurwitz, J. ATP stimulates the binding of simian virus 40 (SV40) large tumor antigen to the SV40 origin of replication. Proc. Natl Acad. Sci. USA 85, 64-68 (1988).
33. Deb, S. P. & Tegtmeyer, P. ATP enhances the binding of simian virus 40 large T antigen to the origin of replication. J. Virol. 61, 3649-3654 (1987).
34. Dean, F. B., Dodson, M., Echols, H. & Hurwitz, J. ATP-dependent formation of a specialized nucleoprotein structure by simian virus 40 (SV40) large tumor antigen at the SV40 replication origin. Proc. Natl Acad. Sci. USA 84, 8981-8985 (1987).
35. McVey, D. et al. Phosphorylation of large tumour antigen by cdc2 stimulates SV40 DNA replication. Nature 341, 503-507 (1989).
36. Prives, C. The replication functions of SV40 T antigen are regulated by phosphorylation. Cell 61, 735-738 (1990).
37. Cueille, N., Nougarede, R., Mechali, F., Philippe, M. & Bonne-Andrea, C. Functional interaction between the bovine papillomavirus virus type 1 replicative helicase E1 and cyclin E-Cdk2. J. Virol. 72, 7255-7262 (1998).
38. Ma, T., Zou, N., Lin, B. Y., Chow, L. T. & Harper, J. W. Interaction between cyclin-dependent kinases and human papillomavirus replication-initiation protein E1 is required for efficient viral replication. Proc. Natl Acad. Sci USA 96, 382-387 (1999).
39. Barbaro, B. A., Sreekumar, K. R., Winters, D. R., Prack, A. E. & Bullock, P. A. Phosphorylation of simian virus 40 T antigen on Thr 124 selectively promotes double-hexamer formation on subfragments of the viral core origin. J. Virol. 74, 8601-8613 (2000).
40. Weisshart, K. et al. Two regions of simian virus 4C T antigen determine cooperativity of double-hexamer assembly on the viral origin of DNA replication and promote hexamer interactions during bidirectional origin DNA unwinding. J. Virol. 73, 2201-2211 (1999).
41. Dean, F. B. & Hurwitz, J. Simian virus 40 large T antigen untwists DNA at the origin of DNA replication. J. Biol. Chem. 266, 5062-5071 (1991).
42. Parsons, R., Anderson, M. E. & Tegtmeyer, P. Three domains in the simian virus 40 core origin orchestrate the binding, melting, and DNA helicase activities of T antigen. J. Virol. 64, 509-518 (1990).
43. Borowiec, J. A. & Hurwitz, J. Localized melting and structural changes in the SV40 origin of replication induced by T-antigen. EMBO J. 7, 3149-3158 (1988)
44. Gillette, T. G., Lusky, M. & Borowiec, J. A. Induction of structural changes in the bovine papillomavirus type 1 origin of replication by the viral E1 and E2 proteins. Proc. Natl Acad. Sci. USA 91, 8846-8850 (1994).
45. Sasse-Dwight, S. & Gralla, J. D. Footprinting protein-DNA complexes in vivo. Methods Enzymol 208, 146-168 (1991).
46. VanLoock, M. S., Alexandrov, A., Yu, X., Cozzarelli, N. R. & Egelman, E. H. SV40 large T antigen hexamer structure: domain organization and DNA-induced conformational changes. Curr. Biol. 12, 472-476 (2002).
47. Li, D. et al. Structure of the replicative helicase of the oncoprotein SV40 large tumour antigen. Nature 423, 512-518 (2003). Describes the crystal structure of a hexameric form of the SV40 T-ag helicase domain.
48. Borowiec, J. A., Dean, F. B. & Hurwitz, J. Differential induction of structural changes in the simian virus 40 origin of replication by T antigen. J. Virol. 65, 1228-1235 (1991).
49. Goetz, G. S., Dean, F. B., Hurwitz, J. & Matson, S. W. The unwinding of duplex regions in DNA by the simian virus 40 large tumor antigen-associated DNA helicase activity. J. Biol. Chem. 263, 383-392 (1988).
50. Dean, F. B. et al. Simian virus 40 (SV40) DNA replication: SV40 large T antigen unwinds DNA containing the SV40 origin of replication Proc. Natl Acad. Sci. USA 84, 16-20 (1987).
51. Lin, B. Y., Makhov, A. M., Giffith, J. D., Broker, T. R. & Chow, L. T. Chaperone proteins abrogate inhibition of the human papillomavirus (HPV) E1 replicative helicase by the HPV E2 protein. Mol. Cell. Biol. 22, 6592-6604 (2002).
52. Smelkova, N. V. & Borowiec, J. A. Synthetic DNA replication bubbles bound and unwound with twofold symmetry by a simian virus 40 T-antigen double hexamer. J. Virol. 72, 8676-8681 (1998).
53. Dodson, M., Dean, F. B., Bullock, P., Echols, H. & Hurwitz, J. Unwinding of duplex DNA from the SV40 ongin of replication by T antigen. Science 238, 964-967 (1987).
54. Fouts, E. T., Yu, X., Egelman, E. H. & Botchan, M. R. Biochemical and electron microscopic image analysis of the hexameric E1 helicase. J. Biol. Chem. 274, 4447-4458 (1999).
55. Sedman, J. & Stenlund, A. The papillomavirus E1 protein forms a DNA-dependent hexameric complex with ATPase and DNA helicase activities. J Virol. 72, 6893-6897 (1998).
56. Seo, Y. S., Muller, F., Lusky, M. & Hurwitz, J. Bovine papilloma virus (BPV)-encoded E1 protein contains multiple activities required for BPV DNA replication. Proc. Natl Acad. Sci. USA 90, 702-706 (1993).
57. Patel, S. S. & Picha, K. M. Structure and function of hexameric helicases. Annu. Rev. Biochem. 69, 651-697 (2000).
58. Wessel, R., Schweizer, J. & Stahl, H. Simian virus 40 T-antigen DNA helicase is a hexamer which forms a binary complex during bidirectional unwinding from the viral origin of DNA replication. J. Virol. 66, 804-815 (1992). The original observation of the T-ag double hexamer as a functional entity - a 'helicase machine'.
59. Smelkova, N. V. & Borowiec, J. A. Dimerization of simian virus 40 T-antigen hexamers activates T-antigen DNA helicase activity. J. Virol. 71, 8766-8773 (1997).
60. Alexandrov, A. I., Botchan, M. R. & Cozzarelli, N. R. Characterization of simian virus 40 T-antigen double hexamers bound to a replication fork. The active form of the helicase. J. Biol. Chem. 277, 44886-44897 (2002).
61. Joo, W. S., Kim, H. Y., Purviance, J. D., Sreekumar, K. R. & Bullock, P. A. Assembly of T-antigen double hexamers on the simian virus 40 core origin requires only a subset of the available binding sites. Mol. Cell. Biol. 18, 2677-2687 (1998).
62. West, S. C. DNA helicases: new breeds of translocating motors and molecular pumps. Cell 86, 177-180 (1996).
63. Kaplan, D. L. & O'Donnell, M. DnaB drives DNA branch migration and dislodges proteins while encircling two DNA strands. Mol. Cell 10, 647-657 (2002).
64. Labib, K. & Diffley, J. F. Is the MCM2-7 complex the eukaryotic DNA replication fork helicase? Curr. Opin. Genet. Dev. 11, 64-70 (2001).
65. Tye, B. K. MCM proteins in DNA replication. Annu. Rev. Biochem. 68, 649-686 (1999).
66. Tye, B. K. & Sawyer, S. The hexameric eukaryotic MCM helicase: building symmetry from nonidentical parts J. Biol. Chem. 275, 34833-34836 (2000).
67. Ishimi, Y. A DNA helicase activity is associated with an MCM4,-6, and-7 protein complex. J. Biol. Chem. 272, 24508-24513 (1997).
68. Laskey, R. A. & Madine, M. A. A rotary pumping model for helicase function of MCM proteins at a distance from replication forks. EMBO Rep. 4, 26-30 (2003).
69. Fletcher, R. J. et al. The structure and function of MCM from archaeal M. thermoautotrophicum. Nature Struct. Biol. 10, 160-167 (2003).
70. Chong, J. P., Hayashi, M. K., Simon, M. N., Xu, R. M. & Stillman, B. A double-hexamer archaeal minichromosome maintenance protein is an ATP-dependent DNA helicase. Proc. Natl Acad. Sci. USA 97, 1530-1535 (2000).
71. Kelman, Z., Lee, J. K. & Hurwitz, J. The single minichromosome maintenance protein of Methanobacterium thermoautotrophicum DeltaH contains DNA helicase activity. Proc. Natl Acad. Sci. USA 96, 14783-14788 (1999).
72. Shechter, D. F., Ying, C. Y. & Gautier, J. The intrinsic DNA helicase activity of Methanobacterium thermoautotrophicum delta H minichromosome maintenance protein. J. Biol. Chem. 275, 15049-15059 (2000). References 70-72 identify the Methanobacterium MCM helicase as a double hexamer.
73. Han, Y., Loo, Y. M., Militello, K. T. & Melendy, T. Interactions of the papovavirus DNA replication initiator proteins, bovine papilromavirus type 1 E1 and simian virus 40 large T antigen, with human replication protein A. J. Virol. 73, 4899-4907 (1999).
74. Simmons, D. T., Melendy, T. Usher, D. & Stillman, B. Simian virus 40 large T antigen binds to topoisomerase I. Virology 222, 365-374 (1996).
75. Dornreiter, I., Hoss, A., Arthur, A. K. & Fanning, E. SV40 T antigen binds directly to the large subunit of purified DNA polymerase α. EMBO J. 9, 3329-3336 (1990)
76. Park, P. et al. The cellular DNA polymerase α-primase is required for papillomavirus DNA replication and associates with the viral E1 helicase. Proc Natl Acad. Sci. USA 91, 8700-8704 (1994).
77. Thommes, P. et al. Properties of the nuclear P1 protein, a mammalian homologue of the yeast Mcm3 replication protein. Nucl. Acids Res. 20, 1069-1074 (1992).
78. Marahrens, Y. & Stillman, B. A yeast chromosomal origin of DNA replication defined by multiple functional elements. Science 255, 817-823 (1992).
79. Bell, S. P. & Stillman, B. ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature 357, 128-134 (1992).
80. Wilmes, G. M. & Bell, S. P. The B2 element of the Saccharomyces cerevisiae ARS1 origin of replication requires specific sequences to facilitate pre-RC formation Proc. Natl Acad. Sci. USA 99, 101-106 (2002).
81. Kelman, Z. & O'Donnell, M. DNA polymerase III holoenzyme: structure and function of a chromosomal replicating machine. Annu. Rev. Biochem. 64, 171-200 (1995)
82. Tsurimoto, T. & Stillman, B. Replication factors required for SV40 DNA replication in vitro. I. DNA structure-specific recognition of a primer-template junction by eukaryotic DNA polymerases and their accessory proteins. J. Biol. Chem. 266, 1950-1960 (1991).
83. Wahle, E., Lasken, R. S. & Kornberg, A. The dnaB-dnaC replication protein complex of Escherichia coli. II. Role of the complex in mobilizing dnaB functions. J. Biol. Chem. 264, 2469-2475 (1989).