Sequence requirements for the assembly of simian virus 40 T antigen and the T-antigen origin binding domain on the viral core origin of replication

Journal of Virology

Volumn 73, Issue 9, 1999, Pages 7543-7555

  Kim, Henry Y ^a   Barbaro, Brett A ^a   Joo, Woo S ^a,b   Prack, Andrea E ^a   Sreekumar, K R ^a   Bullock, Peter A ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS T ANTIGEN;

ARTICLE; DNA REPLICATION ORIGIN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DNA BINDING; SIMIAN VIRUS 40; VIRUS CORE; VIRUS REPLICATION;

EID: 0032837332     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.9.7543-7555.1999     Document Type: Article

References (89)

1. Borowiec, J. A. 1992. Inhibition of structural changes in the simian virus 40 core origin of replication by mutation of essential origin sequences. J. Virol. 66:5248-5255.
2. Borowiec, J. A., F. B. Dean, P. A. Bullock, and J. Hurwitz. 1990. Binding and unwinding - how T antigen engages the SV40 origin of DNA replication. Cell 60:181-184.
3. Borowiec, J. A., and J. Hurwitz. 1988. ATP stimulates the binding of the simian virus 40 (SV40) large tumor antigen to the SV40 origin of replication. Proc. Natl. Acad. Sci. USA 85:64-68.
4. Borowiec, J. A., and J. Hurwitz. 1988. Localized melting and structural changes in the SV40 origin of replication induced by T-antigen. EMBO J. 7:3149-3158.
5. Bradley, M. K., T. F. Smith, R. H. Lathrop, D. M. Livingston, and T. A. Webster. 1987. Consensus topography in the ATP binding site of the simian virus 40 and polyomavirus large tumor antigens. Proc. Natl. Acad. Sci. USA 84:4026-4030.
6. Brush, G. S., and T. J. Kelly. 1996. Mechanisms for replicating DNA, p. 1-43. In M. L. DePamphilis (ed.), DNA replication in eukaryotic cells. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
7. Bullock, P. A. 1997. The initiation of simian virus 40 DNA replication in vitro. Crit. Rev. Biochem. Mol. Biol. 32:503-568.
8. Bullock, P. A., W. S. Joo, K. R. Sreekumar, and C. Mellow. 1997. Initiation of SV40 DNA replication in vitro: analysis of the role played by sequences flanking the core origin on initial synthesis events. Virology 227:460-473.
9. Bullock, P. A., Y. S. Seo, and J. Hurwitz. 1989. Initiation of simian virus 40 DNA replication in vitro: pulse-chase experiments identify the first labeled species as topologically unwound. Proc. Natl. Acad. Sci. USA 86:3944-3948.
10. Burhans, W. C., and J. A. Huberman. 1994. DNA replication origins in animal cells: a question of context? Science 263:639-640.
11. Campbell, K. S., K. P. Mullane, I. A. Aksoy, H. Stubdal, J. M. Pipas, P. A. Silver, T. M. Roberts, B. S. Schaffhausen, and J. A. DeCaprio. 1997. DnaJ/hsp40 chaperone domain of SV40 large T antigen promotes efficient viral DNA replication. Genes Dev. 11:1098-1110.
12. Clark, R., K. Peden, J. M. Pipas, D. Nathans, and R. Tjian. 1983. Biochemical activities of T-antigen proteins encoded by simian virus 40 A gene deletion mutants. Mol. Cell. Biol. 3:220-228.
13. Clertant, P., P. Gaudray, E. May, and F. Cuzin. 1984. The nucleotide binding site detected by affinity labeling in the large T proteins of polyoma and SV40 viruses is distinct from their ATPase catalytic site. J. Biol. Chem. 259:15196-15203.
14. Dean, F. B., J. A. Borowiec, T. Eki, and J. Hurwitz. 1992. The simian virus 40 T antigen double hexamer assembles around the DNA at the replication origin. J. Biol. Chem. 267:14129-14137.
15. Dean, F. B., J. A. Borowiec, Y. Ishimi, S. Deb, P. Tegtmeyer, and J. Hurwitz. 1987. Simian virus 40 large tumor antigen requires three core replication origin domains for DNA unwinding and replication in vitro. Proc. Natl. Acad. Sci. USA 84:8267-8271.
16. Dean, F. B., P. Bullock, Y. Murakami, C. R. Wobbe, L. Weissbach, and J. Hurwitz. 1987. 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.
17. Dean, F. B., M. Dodson, H. Echols, and J. Hurwitz. 1987. 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.
18. Dean, F. B., S. H. Lee, A. D. Kwong, P. Bullock, J. A. Borowiec, M. K. Kenny, Y. S. Seo, T. Eki, T. Matsumoto, G. Hodgins, and J. Hurwitz. 1989. SV40 DNA replication in vitro. UCLA Symp. Mol. Cell. Biol. New Ser. 127:315-326.
19. Deb, S., A. L. DeLucia, C.-P. Baur, A. Koff, and P. Tegtmeyer. 1986. Domain structure of the simian virus 40 core origin of replication. Mol. Cell. Biol. 6:1663-1670.
20. Deb, S., A. L. DeLucia, A. Koff, S. Tsui, and P. Tegtmeyer. 1986. The adenine-thymine domain of the simian virus 40 core origin directs DNA bending and coordinately regulates DNA replication. Mol. Cell. Biol. 6:4578-4584.
21. Deb, S., S. Tsui, A. Koff, A. L. DeLucia, R. Parsons, and P. Tegtmeyer. 1987. The T-antigen-binding domain of the simian virus 40 core-origin of replication. J. Virol. 61:2143-2149.
22. Deb, S. P., and P. Tegtmeyer. 1987. ATP enhances the binding of simian virus 40 large T antigen to the origin of replication. J. Virol. 61:3649-3654.
23. DeLucia, A. L., S. Deb, K. Partin, and P. Tegtmeyer. 1986. Functional interactions of the simian virus 40 core origin of replication with flanking regulatory sequences. J. Virol. 57:138-144.
24. DeLucia, A. L., B. A. Lewton, R. Tjian, and P. Tegtmeyer. 1983. Topography of simian virus 40 A protein-DNA complexes: arrangement of pentanucleotide interaction sites at the origin of replication. J. Virol. 46:142-150.
25. DePamphilis, M. L. (ed.). 1996. DNA replication in eukaryotic cells. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
26. DiMaio, D., and D. Nathans. 1980. Cold-sensitive regulatory mutants of simian virus 40. J. Mol. Biol. 140:129-146.
27. Dixon, R. A. F., and D. Nathans. 1985. Purification of simian virus 40 large T antigen by immunoaffinity chromatography. J. Virol. 53:1001-1004.
28. Dodson, M., F. B. Dean, P. Bullock, H. Echols, and J. Hurwitz. 1987. Unwinding of duplex DNA from the SV40 origin of replication by T antigen. Science 238:964-967.
29. Fanning, E., and R. Knippers. 1992. Structure and function of simian virus 40 large tumor antigen. Annu. Rev. Biochem. 61:55-85.
30. Fersht, A. 1984. Enzyme structure and mechanism, 2nd ed. W. H. Freeman & Co., New York, N.Y.
31. Giacherio, D., and L. P. Hager. 1979. A poly(dT)-stimulated ATPase activity associated with simian virus 40 large T antigen. J. Biol. Chem. 254:8117-8120.
32. Goetz, G. S., F. B. Dean, J. Hurwitz, and S. W. Matson. 1988. 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.
33. Gottlieb, P., M. S. Nasoff, E. F. Fisher, A. M. Walsh, and M. H. Caruthers. 1985. Binding studies of SV40 T-antigen to SV40 binding site II. Nucleic Acids Res. 13:6621-6634.
34. Hertz, G. Z., M. R. Young, and J. E. Mertz. 1937. The A+T-rich sequence of the simian virus 40 origin is essential for replication and is involved in bending of the viral DNA. J. Virol. 61:2322-2325.
35. Huang, S. G., K. Weisshart, I. Gilbert, and E. Fanning. 1998. Stoichiometry and mechanisms of assembly of SV40 T antigen complexes with the viral origin of DNA replication and DNA polymerase α-primase. Biochemistry 37:15345-15352.
36. Hurwitz, J., F. B. Dean, A. D. Kwong, and S.-H. Lee. 1990. The in vitro replication of DNA containing the SV40 origin. J. Biol. Chem. 265:18043-18046.
37. Jones, K. A., R. M. Myers, and R. Tjian. 1984. Mutational analysis of simian virus 40 large T antigen DNA binding sites. EMBO J. 3:3247-3255.
38. Joo, W. S., H. Y. Kim, J. D. Purviance, K. R. Sreekumar, and P. A. Bullock. 1998. 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.
39. Joo, W. S., X. Luo, D. Denis, H. Y. Kim, G. J. Rainey, C. Jones, K. R. Sreekumar, and P. A. Bullock. 1997. Purification of the SV40 T-antigen DNA binding domain and characterization of its interactions with the SV40 origin. J. Virol. 71:3972-3985.
40. Kadonaga, J. T., and R. Tjian. 1986. Affinity purification of sequence-specific DNA binding proteins. Proc. Natl. Acad. Sci. USA 83:5889-5893.
41. Kelly, W. L., and S. J. Landry. 1994. Chaperone power in a virus? Trends Biol. Sci. 19:277-278.
42. Korolev, S., J. Hsieh, G. H. Gauss, T. M. Lohman, and G. Waksman. 1997. Major domain swiveling revealed by the crystal structures of complexes of E. coli Rep helicase bound to single-stranded DNA and ADP. Cell 90:635-647.
43. Lewton, B. A., A. L. DeLucia, and P. Tegtmeyer. 1984. Binding of simian virus 40 A protein to DNA with deletions at the origin of replication. J. Virol. 49:9-13.
44. Li, J. J., K. W. C. Peden, R. A. F. Dixon, and T. Kelly. 1986. Functional organization of the simian virus 40 origin of DNA replication. Mol. Cell. Biol. 6:1117-1128.
45. Li, L., B. L. Li, M. Hock, E. Wang, and W. R. Folk. 1995. Sequences flanking the pentanucleotide T-antigen binding sites in the polyomavirus core origin help determine selectivity of DNA replication. J. Virol. 69:7570-7578.
46. Lorimer, H. E., I. Reynisdottir, S. Ness, and C. Prives. 1993. Unusual properties of a replication-defective mutant SV40 large T-antigen. Virology 192:402-414.
47. Lorimer, H. E., E. H. Wang, and C. Prives. 1991. The DNA-binding properties of polyomavirus large T antigen are altered by ATP and other nucleotides. J. Virol. 65:687-699.
48. Luo, X., D. G. Sanford, P. A. Bullock, and W. W. Bachovchin. 1996. Structure of the origin specific DNA binding domain from simian virus 40 T-antigen. Nat. Struct. Biol. 3:1034-1039.
49. Lusky, M., J. Hurwitz, and Y.-S. Seo. 1993. Cooperative assembly of the bovine papilloma virus E1 and E2 proteins on the replication origin requires an intact E2 binding site. J. Biol. Chem. 268:15795-15803.
50. Mastrangelo, I. A., P. V. C. Hough, J. S. Wall, M. Dodson, F. B. Dean, and J. Hurwitz. 1989. ATP-dependent assembly of double hexamers of SV40 T antigen at the viral origin of DNA replication Nature (London) 338:658-662.
51. McEntee, K., G. M. Weinstock, and I. R. Lehman. 1980. recA protein-catalyzed strand assimilation: stimulation by Escherichia coli single-stranded DNA-binding protein. Proc. Natl. Acad. Sci. USA 77:857-861.
52. McVey, D., B. Woelker, and P. Tegtmeyer. 1996. Mechanisms of simian virus 40 T-antigen activation by phosphorylation of threonine 124. J. Virol. 70: 3887-3893.
53. Mohr, I. J., M. P. Fairman, B. Stillman, and Y. Gluzman. 1989. Large T-antigen mutants define multiple steps in the initiation of simian virus 40 DNA replication. J. Virol. 63:4181-4188.
54. Müller, D., I. Ugi, K. Ballas, P. Reiser, R. Henning, and M. Montenarh. 1987. The AT-rich sequence of the SV40 control region influences the binding of SV40 T antigen to binding sites II and III. Virology 161:81-90.
55. Murakami, Y., and J. Hurwitz. 1993. DNA polymerase α stimulates the ATP-dependent binding of simian virus tumor T antigen to the SV40 origin of replication. J. Biol. Chem. 268:11018-11027.
56. Myers, R. M., and R. Tjian. 1980. Construction and analysis of simian virus 40 origins defective in tumor antigen binding and DNA replication. Proc. Natl. Acad. Sci. USA 77:6491-6495.
57. O'Reilly, D. R., and L. K. Miller. 1988. Expression and complex formation of simian virus 40 large T antigen and mouse p53 in insect cells. J. Virol. 62:3109-3119.
58. Parsons, R., M. E. Anderson, and P. Tegtmeyer. 1990. 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.
59. Parsons, R. E., J. E. Stenger, S. Ray, R. Welker, M. E. Anderson, and P. Tegtmeyer. 1991. Cooperative assembly of simian virus 40 T-antigen hexamers on functional halves of the replication origin. J. Virol. 65:2798-2806.
60. Reynisdottir, I., H. E. Lorimer, P. N. Friedman, E. H. Wang, and C. Prives. 1993. Phosphorylation and active ATP hydrolysis are not required for SV40 T antigen hexamer formation. J. Biol. Chem. 268:24647-24654.
61. Roberts, J. 1989. Simian virus 40 (SV40) large tumor antigen causes stepwise changes in SV40 origin structure during initiation of DNA replication. Proc. Natl. Acad. Sci. USA 86:3939-3943.
62. Ryder, K., E. Vakalopoulou, R. Mertz, I. Mastrangelo, P. Hough, P. Tegtmeyer, and E. Fanning. 1985. Seventeen base pairs of region I encode a novel tripartite binding signal for SV40 T antigen. Cell 42:539-548.
63. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
64. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
65. San Martin, M. C., C. Gruss, and J. M. Carazo. 1997. Six molecules of SV40 large T antigen assemble in a propeller-shaped particle around a channel. J. Mol. Biol. 268:15-20.
66. SenGupta, D. J., and J. A. Borowiec. 1994. Strand and face: the topography of interactions between the SV40 origin of replication and T-antigen during the initiation of replication. EMBO J. 13:982-992.
67. SenGupta, D. J., and J. A. Borowiec. 1992. Strand-specific recognition of a synthetic DNA replication fork by the SV40 large tumor antigen. Science 256:1656-1661.
68. Simanis, V., and D. P. Lane. 1985. An immunoaffinity purification procedure for SV40 large T antigen. Virology 144:88-100.
69. Simmons, D. T., G. Loeber, and P. Tegtmeyer. 1990. Four major sequence elements of simian virus 40 large T antigen coordinate its specific and nonspecific DNA binding. J. Virol. 64:1973-1983.
70. Simmons, D. T., K. Wun-Kim, and W. Young. 1990. Identification of simian virus 40 T-antigen residues important for specific and nonspecific binding to DNA and for helicase activity. J. Virol. 64:4858-4865.
71. Smelkova, N. V., and J. A. Borowiec. 1997. Dimerization of simian virus 40 T-antigen hexamers activates T-antigen DNA helicase activity. J. Virol. 71: 8766-8773.
72. Srinivasan, A., A. J. McClellan, J. Vartikar, I. Marks, P. Cantalupo, Y. Li, P. Whyte, K. Rundell, J. L. Brodsky, and J. M. Pipas. 1997. The amino-terminal transforming region of simian virus 40 large T and small t antigens functions as a J domain. Mol. Cell. Biol. 17:4761-4773.
73. Stahl, H., P. Droge, and R. Knippers. 1986. DNA helicase activity of SV40 large tumor antigen. EMBO J. 5:1939-1944.
74. Stillman, B., R. D. Gerard, R. A. Guggenheimer, and Y. Gluzman. 1985. T antigen and template requirement for SV40 DNA replication in vitro. EMBO J. 4:2933-2939.
75. Studwell, P. S., and M. O'Donnell. 1990. Processive replication is contingent on the exonuclease subunit of DNA polymerase III holoenzyme. J. Biol. Chem. 265:1171-1178.
76. Subramanya, H. S., L. E. Bird, J. A. Brannigan, and D. B. Wigley. 1996. Crystal structure of a DExx box DNA helicase. Nature 384:379-383.
77. Tegtmeyer, P., B. A. Lewton, A. L. DeLucia, V. G. Wilson, and K. Ryder. 1983. Topography of simian virus 40 A protein-DNA complexes: arrangement of protein bound to the origin of replication. J. Virol. 46:151-161.
78. Tjian, R. 1978. The binding site on SV40 DNA for a T-antigen related protein. Cell 13:165-179.
79. Tooze, J. 1981. DNA tumor viruses, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
80. Velankar, S. S., P. Soultanas, M. S. Dillingham, H. S. Subramanya, and D. B. Wigley. 1999. Crystal structures of complexes of PcrA DNA Helicase with a DNA substrate indicate an inchworm mechanism. Cell 97:75-84.
81. Virshup, D. M., A. A. R. Russo, and T. J. Kelly. 1992. Mechanism of activation of simian virus 40 DNA replication by protein phosphatase 2A. Mol. Cell. Biol. 12:4883-4895.
82. Waga, S., and B. Stillman. 1998. The DNA replication fork in eukaryotic cells. Annu. Rev. Biochem. 67:721-751.
83. Weisshart, K., P. Taneja, A. Jenne, U. Herbig, D. T. Simmons, and E. Fanning. 1999. Two regions of simian virus 40 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.
84. Wessel, R., J. Schweizer, and H. Stahl. 1992. 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.
85. Wobbe, C. R., F. Dean, L. Weissbach, and J. Hurwitz. 1985. In vitro replication of duplex circular DNA containing the simian virus 40 DNA origin site. Proc. Natl. Acad. Sci. USA 82:5710-5714.
86. Wold, M. S., J. J. Li, and T. J. Kelly. 1987. Initiation of simian virus 40 DNA replication in vitro: large-tumor-antigen- and origin-dependent unwinding of the template. Proc. Natl. Acad. Sci. USA 84:3643-3647.
87. Wold, M. S., D. H. Weinberg, D. M. Virshup, J. J. Li, and T. J. Kelly. 1989. Identification of cellular proteins required for simian virus 40 DNA replication. J. Biol. Chem. 264:2801-2809.
88. Wu, C., D. Edgil, and D. T. Simmons. 1998. The origin DNA-binding and single-stranded DNA-binding domains of simian virus large T antigen are distinct. J. Virol. 72:10256-10259.
89. Wun-Kim, K., R. Upson, W. Young, T. Melendy, B. Stillman, and D. T. Simmons. 1993. The DNA-binding domain of simian virus 40 tumor antigen has multiple functions. J. Virol. 67:7608-7611.