The replication of protein A binding site in simian virus 40 (SV40) T antigen and its role in the initial steps of SV40 DNA replication

Journal of Virology

Volumn 72, Issue 12, 1998, Pages 9771-9781

  Weisshart, Klaus ^a   Taneja, Poonam ^b   Fanning, Ellen ^b,c  

^a FRITZ LIPMANN INSTITUTE   (Germany)

^b VANDERBILT INGRAM CANCER CENTER   (United States)

^c VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS PROTEIN; VIRUS T ANTIGEN;

ANTIBODY SPECIFICITY; ARTICLE; BINDING SITE; DNA REPLICATION; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PURIFICATION; SIMIAN VIRUS 40; VIRUS REPLICATION;

EID: 0031775222     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.12.9771-9781.1998     Document Type: Article

References (101)

1. Berger, L. C., D. B. Smith, I. Davidson, J.-J. Hwang, E. Fanning, and A. G. Wildeman. 1996. Interaction between T antigen and the TEA domain of the factor derepresses simian virus 40 late promoter in vivo: identification of the T-antigen domains important for transcriptional control. J. Virol. 70: 1203-1212.
2. Braun, K. A., Y. Lao, Z. He, J. Ingles, and M. S. Wold. 1997. Role of protein-protein interactions in the function of replication protein A (RPA): RPA modulates the activity of DNA polymerase alpha by multiple mechanisms. Biochemistry 36:8443-8454.
3. Brill, S. J., and B. Stillman. 1989. Yeast replication factor-A functions in the unwinding of the SV40 origin of DNA replication. Nature 342:92-95.
4. Brinton, B., and J. A. Hassell. 1996. SV40 and polyoma DNA replication, p. 639-677. In M. L. DePamphilis (ed.), DNA replication in eukaryotic cells. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
5. 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, Plainview, N.Y.
6. Bullock, P. A. 1997. The initiation of simian virus 40 DNA replication in vitro. Crit. Rev. Biochem. Mol. Biol. 32:503-568.
7. Bullock, P. A., Y. S. Seo, and J. Hurwitz. 1989. Initiation of simian virus 40 DNA synthesis in vitro: pulse-chase experiments identify the first labeled species as topologically unwound. Proc. Natl. Acad. Sci. USA 86:3944-3948.
8. Bullock, P. A., Y. S. Seo, and J. Hurwitz. 1991. Initiation of simian virus 40 DNA synthesis in vitro. Mol. Cell. Biol. 11:2350-2361.
9. Bullock, P. A., S. Tevosian, C. Jones, and D. Denis. 1994. Mapping initiation sites for simian virus 40 lagging-strand DNA synthesis events in vitro. Mol. Cell. Biol. 14:5043-5055.
10. Bullock, P. A., and D. Denis. 1995. DNA synthesis generally initiates outside of the simian virus 40 core origin in vitro. Mol. Cell. Biol. 15:173-178.
11. Campbell, K., K. Mullane, I. Aksoy, H. Stubdal, J. Pipas, P. Silver, T. Roberts, B. Schaffhausen, and J. DeCaprio. 1997. DnaJ/hsp40 chaperone domain of SV40 large T antigen promotes efficient viral DNA replication. Genes Dev. 11:1098-1110.
12. Cegielska, A., I. Moarefi, E. Fanning, and D. M. Virshup. 1994. T-antigen kinase inhibits simian virus 40 DNA replication by phosphorylation of intact T antigen on serines 120 and 123. J. Virol. 68:269-275.
13. Clark, R., D. P. Lane, and R. Tjian. 1981. Use of monoclonal antibodies as probes of simian virus 40 T antigen ATPase activity. J. Biol. Chem. 256: 11854-11858.
14. Collins, K. L., and T. J. Kelly. 1991. The effects of T antigen and replication protein A on the initiation of DNA synthesis by DNA polymerase α-primase. Mol. Cell. Biol. 11:2108-2115.
15. Collins, K. L., A. A. R. Russo, B. Y. Tseng, and T. J. Kelly. 1993. The role of the 70 kDa subunit of human DNA polymerase α in DNA replication. EMBO J. 12:4555-4566.
16. Damania, B., and J. C. Alwine. 1996. TAF-like function of SV40 large T antigen. Genes Dev. 10:1369-1381.
17. Dean, F. B., P. A. 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.
18. 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.
19. 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.
20. Denis, D., and P. A. Bullock. 1993. Primer-DNA formation during simian virus 40 DNA replication in vitro. Mol. Cell. Biol. 13:2882-2890.
21. Dickmanns, A., A. Zeitvogel, F. Simmersbach, R. Weber, A. K. Arthur, S. Dehde, A. G. Wildeman, and E. Fanning. 1994. The kinetics of simian virus 40-induced progression of quiescent cells into S phase depend on four independent functions of large T antigen. J. Virol. 68:5496-5508.
22. Dodson, M., F. B. Dean, P. Bullock, H. Echols, and J. Hurwits. 1987. Unwinding of duplex DNA from the SV40 origin of replication by T antigen. Science 238:964-968.
23. Dornreiter, I., W. C. Copeland, and T. S.-F. Wang. 1993. Initiation of simian virus 40 DNA replication requires the interaction of a specific domain of human DNA polymerase α with large T antigen. Mol. Cell. Biol. 13:809-820.
24. Dornreiter, I., L. F. Erdile, I. U. Gilbert, D. von Winkler, T. J. Kelly, and E. Fanning. 1992. Interaction of DNA polymerase α-primase with cellular replication protein A and SV40 T antigen. EMBO J. 11:769-776.
25. Dornreiter, I., A. Höss, A. K. Arthur, and E. Fanning. 1990. SV40 T antigen binds directly to the large subunit of DNA polymerase alpha. EMBO J. 9: 3329-3336.
26. Erdile, L. F., W. D. Heyer, R. Kolodner, and T. J. Kelly. 1991. Characterization of a cDNA encoding the 70-kDa single-stranded DNA-binding subunit of human replication protein A and the role of the protein in DNA replication. J. Biol. Chem. 266:12090-12096.
27. Fairman, M. P., and B. Stillman. 1988. Cellular factor required for multiple stages of SV40 replication in vitro. EMBO J. 7:1211-1218.
28. Fanning, E. 1994. Control of SV40 DNA replication by protein phosphorylation: a model for cellular DNA replication? Trends Cell Biol. 4:250-255.
29. Fanning, E., and R. Knippers. 1992. Structure and function of simian virus 40 large tumor antigen. Annu. Rev. Biochem. 61:55-85.
30. Gannon, J. V., and D. P. Lane. 1987. p53 and DNA polymerase α compete for binding to SV40 T antigen. Nature (London) 329:456-458.
31. Gannon, J. V., and D. P. Lane. 1990. Interactions between SV40 T antigen and DNA polymerase α. New Biol. 2:84-92.
32. Gomes, X. V., and M. S. Wold. 1995. Structural analysis of human replication protein A: mapping functional domains of the 70-kDa subunit. J. Biol. Chem. 270:4534-4543.
33. Grosse, F. Personal communication.
34. Gruda, M., J. Zabolotny, J. Xiao, I. Davidson, and J. Alwine. 1993. Transcriptional activation by simian virus 40 large T antigen: interactions with multiple components of the transcription complex. Mol. Cell. Biol. 13:961-969.
35. Gurney, E. G., R. O. Harrison, and J. Fenno. 1980. Monoclonal antibodies against simian virus 40 T antigens: evidence for distinct subclasses of large T antigen and for similarities among nonviral T antigens. J. Virol. 34:752-763.
36. Gurney, E. G., D. Tamowsky, and W. Deppert. 1986. Antigenic binding sites of monoclonal antibodies specific for simian virus 40 large T. J. Virol. 57: 1168-1172.
37. Harlow, E., L. V. Crawford, D. C. Pim, and N. M. Williamson. 1981. Monoclonal antibodies specific for simian virus 40 tumor antigen. J. Virol. 39:861-869.
38. Henricksen, L. A., C. B. Umbricht, and M. S. Wold. 1994. Recombinant replication protein A: expression, complex formation, and functional characterization. J. Biol. Chem. 269:11121-11132.
39. Herbig, U., K. Weisshart, P. Taneja, and E. Fanning. Interaction of the transcription factor TFIID with SV40 large T antigen interferes with replication of SV40 DNA in vitro. Submitted for publication.
40. Herendeen, D., and T. J. Kelly. 1996. SV40 DNA replication, p. 29-65. In J. J. Blow (ed.), Eukaryotic DNA replication. Oxford University Press, New York, N.Y.
41. Huang, S.-G., K. Weisshart, I. Gilbert, and E. Fanning. Stoichiometry and mechanism of assembly of SV40 T antigen complexes with the viral origin or DNA replication and DNA polymerase α-primase. Biochemistry, in press.
42. Ishimi, Y., A. Chaude, P. Bullock, and J. Hurwitz. 1988. Complete enzymatic synthesis of DNA containing the SV40 origin of replication. J. Biol. Chem. 263:19723-19733.
43. Johnston, S. D., X.-M. Yu, and J. E. Mertz. 1996. The major transcriptional transactivation domain of simian virus 40 large T antigen associates non-concurrently with multiple components of the transcriptional preinitiation complex. J. Virol. 70:1191-1202.
44. Joo, W. X., X. Luo, D. Denis, H. Y. Kim, G. J. Rainey, C. Jones, K. R. Sreekumar, and P. A. Bullock. 1997. 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.
45. Kenny, M. K., S.-H. Lee, and J. Hurwitz. 1989. Multiple functions of human single-stranded DNA binding protein in simian virus 40 DNA replication: single-strand stabilization and stimulation of DNA polymerase α and δ. Proc. Natl. Acad. Sci. USA 86:9757-9761.
46. Kenny, M. K., U. Schlegel, H. Furneaux, and J. Hurwitz. 1990. The role of human single-stranded DNA binding protein and its individual subunits in simian virus 40 DNA replication. J. Biol. Chem. 265:7693-7700.
47. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
48. Lai, J., and W. Herr. 1992. Ethidium bromide provides a simple tool for establishing genuine DNA-independent protein associations. Proc. Natl. Acad. Sci. USA 89:6958-6962.
49. Lee, S.-H., and D. K. Kim. 1995. The role of the 34-kDa subunit of human replication protein in simian virus 40 DNA replication in vitro. J. Biol. Chem. 270:12801-12807.
50. Lee, S.-H., T. Iki, and J. Hurwitz. 1989. Synthesis of DNA containing the simian virus 40 origin of replication by the combined action of DNA polymerase α and δ. Proc. Natl. Acad. Sci. USA 86:7361-7365.
51. L control. Biochemistry 25:21-25.
52. Luo, X., D. G. Sanford, P. A. Bullock, and W. W. Bachovchin. 1996. Solution structure of the origin specific DNA binding domain from simian virus 40 T-antigen. Nat. Struct. Biol. 3:1034-1039.
53. MacArthur, H., and G. Walter. 1984. Monoclonal antibodies specific for the carboxy terminus of simian virus 40 large T antigen. J. Virol. 52:483-491.
54. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
55. Mastrangelo, I. A., P. V. C. Hough, V. G. Wilson, J. S. Wall, J. F. Hainfeld, and P. Tegtmeyer. 1989. ATP-dependent assembly of double hexamers of SV40 T antigen at the viral origin of DNA replication. Nature (London) 338:658-662.
56. Matsumoto, T., T. Eki, and J. Hurwitz. 1990. Studies on the initiation and elongation reactions in the simian virus 40 DNA replication system. Proc. Natl. Acad. Sci. USA 87:9712-9716.
57. McVey, D., S. Ray, Y. Gluzman, L. Berger, A. G. Wildeman, D. R. Marshak, and P. Tegtmeyer. 1993. cdc2 phosphorylation of threonine 124 activates the origin-unwinding functions of simian virus 40 T antigen. J. Virol. 67: 5206-5215.
58. 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.
59. Melendy, T. Personal communication.
60. Melendy, T., and B. Stillman. 1993. An interaction between replication protein A and SV40 T antigen appears essential for primosome assembly during SV40 DNA replication. J. Biol. Chem. 268:3389-3395.
61. Moarefi, I. F., D. Small, I. Gilbert, M. Hoepfner, S. K. Randall, C. Schneider, A. R. R. Russo, U. Ramsperger, A. K. Arthur, H. Stahl, T. J. Kelly, and E. Fanning. 1993. Mutation of the cyclin-dependent kinase phosphorylation site in simian virus 40 (SV40) large T antigen specifically blocks SV40 origin DNA binding. J. Virol. 67:4992-5002.
62. Mole, S. E., J. V. Gannon, M. J. Ford, and D. P. Lane. 1987. Structure and function of large T antigen. Philos. Trans. R. Soc. Lond. Ser. B 317:455-469.
63. Murakami, Y., C. R. Wobbe, L. Weissbach, F. B. Dean, and J. Hurwitz. 1986. Role of DNA polymerase α and DNA primase in simian virus 40 DNA replication in vitro. Proc. Natl. Acad. Sci. USA 83:2869-2873.
64. Murakami, Y., T. Eki, and J. Hurwitz. 1992. Studies on the initiation of simian virus 40 replication in vitro: RNA primer synthesis and its elongation. Proc. Natl. Acad. Sci. USA 89:952-956.
65. Murakami, Y., and J. Hurwitz. 1993. Functional interactions between SV40 T antigen and other replication proteins at the replication fork. J. Biol. Chem. 268:11008-11017.
66. Murakami, Y., and J. Hurwitz. 1993. DNA polymerase α stimulates the ATP-dependent binding of simian virus 40 tumor (T) antigen to the SV40 origin of replication. J. Biol. Chem. 268:11018-11027.
67. Nasheuer, H.-P., D. von Winkler, C. Scheider, I. Dornreiter, I. Gilbert, and E. Fanning. 1992. Purification and functional characterization of bovine RP-A in an in vitro SV40 DNA replication system. Chromosoma 102: S52-S59.
68. 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.
69. Schneider, C., K. Weisshart, L. A. Guarino, I. Dornreiter, and E. Fanning. 1994. Species-specific functional interaction of DNA polymerase α-primase with simian virus 40 (SV40) T antigen require SV40 origin DNA. Mol. Cell. Biol. 14:3176-3185.
70. 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.
71. Simmons, D. T., T. Melendy, D. Usher, and B. Stillman. 1996. Simian virus 40 large T antigen binds to topoisomerase I. Virology 222:365-374.
72. Smale, S. T., and R. Tjian. 1986. T-antigen-DNA polymerase alpha complex implicated in simian virus 40 DNA replication. Mol. Cell. Biol. 6:4077-4087.
73. 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.
74. Smith, D. B., and K. S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67:31-40.
75. 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.
76. Stadlbauer, F., A. Brückner, C. Rehfuess, C. Eckershorn, F. Lottspeich, V. Förster, B.-Y. Tseng, and H.-P. Nasheuer. 1994. DNA replication in vitro by recombinant DNA-polymerase α-primase. Eur. J. Biochem. 222:781-793.
77. Stadlbauer, F., C. Voitenleitner, A. Brückner, E. Fanning, and H.-P. Nasheuer. 1996. Species-specific replication of simian virus 40 DNA in vitro requires the p180 subunit of human DNA polymerase α-primase. Mol. Cell. Biol. 16:94-1104.
78. Stigger, E., F. Dean, J. Hurwitz, and S.-H. Lee. 1994. Reconstitution of functional human single-stranded DNA-binding protein from individual subunits expressed by recombinant baculoviruses. Proc. Natl. Acad. Sci. USA 91:579-583.
79. Stillman, B. 1996. Comparison of DNA replication in cells from prokarya and eukarya, p. 435-160. In M. L. DePamphilis (ed.), DNA replication in eukaryotic cells. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
80. Strausfeld, U., and A. Richter. 1989. Simultaneous purification of DNA topoisomerases I and II from eucaryotic cells. Prep. Biochem. 19:37-48.
81. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
82. Tsurimoto, T., and B. Stillman. 1989. Multiple replication factors augment DNA synthesis by two eukaryotic DNA polymerases, α and δ. EMBO J. 8: 3883-3889.
83. Tsurimoto, T., M. P. Fairman, and B. Stillman. 1989. Simian virus 40 DNA replication in vitro: identification of multiple stages of initiation. Mol. Cell. Biol. 9:3839-3849.
84. Tsurimoto, T., T. Melendy, and B. Stillman. 1990. Sequential initiation of lagging and leading strand synthesis by two different polymerase complexes at the SV40 replication origin. Nature (London) 346:534-539.
85. 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.
86. Voitenleitner, C., E. Fanning, and H.-P. Nasheuer. 1997. Phosphorylation of DNA polymerase α-primase by cyclin A-dependent kinases regulates initiation of DNA replication in vitro. Oncogene 14:1611-1615.
87. Waga, S., and B. Stillman. 1994. Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro. Nature (London) 369:207-212.
88. Waga, S., G. Bauer, and B. Stillman. 1994. Reconstitution of complete SV40 DNA replication with purified replication factors. J. Biol. Chem. 269: 10923-10934.
89. Weinberg, D. H., K. L. Collins, P. Simancek, A. Russo, M. S. Wold, D. M. Virshup, and T. J. Kelly. 1990. Reconstitution of simian virus 40 DNA replication with purified proteins. Proc. Natl. Acad. Sci. USA 87:8692-8696.
90. Weisshart, K., M. K. Bradley, B. M. Weiner, C. Schneider, I. Moarefi, E. Fanning, and A. K. Arthur. 1996. An N-terminal deletion mutant of simian virus 40 (SV40) large T antigen oligomerizes incorrectly on SV40 DNA but retains the ability to bind to DNA polymerase α and replicate SV40 DNA in vitro. J. Virol. 70:3509-3516.
91. Weisshart, K., P. Taneja, I. Boche, A. Brunahl, and E. Fanning. Unpublished data.
92. Weisshart, K., P. Taneja, A. Jenne, U. Herbig, D. T. Simmons, and E. Fanning. Two regions of SV40 T antigen determine cooperativity of double hexamer assembly on the viral origin of DNA replication and promote hexamer interactions during bidirectional origin DNA unwinding. Submitted for publication.
93. Wessel, R., J. Schweizer, and H. Stahl. 1992. Simian virus 40 large T antigen DNA helicase is a hexamer which forms a binary complex during the elongation process of simian virus 40 DNA replication. J. Virol. 66:804-815.
94. Wiekowski, M., P. Droege, and H. Stahl. 1987. Monoclonal antibodies as probes for a function of large T antigen during the elongation process of simian virus 40 DNA replication. J. Virol. 61:411-418.
95. Wobbe, C. R., L. Weissbach, J. A. Borowiec, F. B. Dean, Y. Murakami, P. Bullock, and J. Hurwitz. 1987. Replication of simian virus 40 origin-containing DNA in vitro with purified proteins. Proc. Natl. Acad. Sci. USA 84: 1834-1838.
96. Wold, M. S. 1997. Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem. 66:61-92.
97. Wold, M. S., and T. J. Kelly. 1988. Purification and characterization of replication protein A, a cellular protein required for in vitro replication of simian virus 40 DNA. Proc. Natl. Acad. Sci. USA 85:2523-2527.
98. Wun-Kim, K., and D. T. Simmons. 1990. Mapping of helicase and helicase substrate-binding domains on simian virus 40 large T antigen. J. Virol. 64: 2014-2020.
99. Wun-Kim, K., R. H. Upson, W. Young, and D. T. Simmons. 1993. The DNA binding domain of simian virus large T antigen has multiple functions. J. Virol. 67:7608-7611.
100. Yang, L., M. S. Wold, J. J. Li, T. J. Kelly, and L. F. Liu. 1987. Roles of DNA topoisomerases in simian virus 40 DNA replication in vitro. Proc. Natl. Acad. Sci. USA 84:950-954.
101. Zhang, D., L. Frappier, E. Gibbs, J. Hurwitz, and M. O'Donnell. 1998. Human RPA (hSSB) intracts with EBNA1, the latent origin binding protein of Epstein-Barr virus. Nucleic Acids Res. 26:631-637.