Role of the hydrophilic channels of simian virus 40 T-antigen helicase in DNA replication

Journal of Virology

Volumn 81, Issue 9, 2007, Pages 4510-4519

  Wang, Weiping ^a   Manna, David ^a   Simmons, Daniel T ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DNA FRAGMENT; HELICASE; SINGLE STRANDED DNA; VIRUS DNA; VIRUS T ANTIGEN;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DNA DENATURATION; DNA REPLICATION; ENZYME ACTIVITY; HYDROPHILICITY; NONHUMAN; OLIGOMERIZATION; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SIMIAN VIRUS 40; VIRUS REPLICATION;

ANTIGENS, VIRAL, TUMOR; DNA HELICASES; DNA REPLICATION; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; OLIGONUCLEOTIDES; SIMIAN VIRUS 40;

SIMIAN VIRUS 40;

EID: 34247594803     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00003-07     Document Type: Article

References (79)

1. Ahnert, P., and S. S. Patel. 1997. Asymmetric interactions of hexameric bacteriophage T7 DNA helicase with the 5′- and 3′-tails of the forked DNA substrate. J. Biol. Chem. 272:32267-32273.
2. Alexandrov, A. I., M. R. Botchan, and N. R. Cozzarelli. 2002. 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.
3. Ali, S. H., and J. A. DeCaprio. 2001. Cellular transformation by SV40 large T antigen: interaction with host proteins. Semin. Cancer Biol. 11:15-23.
4. Bochkareva, E., D. Martynowski, A. Seitova, and A. Bochkarev. 2006. Structure of the origin-binding domain of simian virus 40 large T antigen bound to DNA. EMBO J. 25:5961-5969.
5. Borowiec, J. A., F. B. Dean, and J. Hurwitz. 1991. Differential induction of structural changes in the simian virus 40 origin of replication by T antigen. J. Virol. 65:1228-1235.
6. 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.
7. Bullock, P. A. 1997. The initiation of simian virus 40 DNA replication in vitro. Crit. Rev. Bioehem. Mol. Biol. 32:503-568.
8. Campbell, K. S., K. P. Mullane, I. A. Aksoy, H. Stubdal, J. Zalvide, 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.
9. Castella, S., G. Bingham, and C. M. Sanders. 2006. Common determinants in DNA melting and helicase-catalysed DNA unwinding by papillomavirus replication protein E1. Nucleic Acids Res. 34:3008-3019.
10. Chen, L., W. S. Joo, P. A. Bullock, and D. T. Simmons. 1997. The N-terminal side of the origin-binding domain of simian virus 40 large T antigen is involved in A/T untwisting. J. Virol. 71:8743-8749.
11. Collins, K. L., and T. J. Kelly. 1991. Effects of T antigen and replication protein A on the initiation of DNA synthesis by DNA polymerase alpha-primase. Mol. Cell. Biol. 11:2108-2115.
12. Cook, P. R. 1999. The organization of replication and transcription. Science 284:1790-1795.
13. 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.
14. 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.
15. 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.
16. Dornreiter, I., W. C. Copeland, and T. S. Wang. 1993. Initiation of simian virus 40 DNA replication requires the interaction of a specific domain of human DNA polymerase alpha with large T antigen. Mol. Cell. Biol. 13:809-820.
17. Dornreiter, I., L. F. Erdile, I. U. Gilbert, D. von Winkler, T. J. Kelly, and E. Fanning. 1992. Interaction of DNA polymerase alpha-primase with cellular replication protein A and SV40 T antigen. EMBO J. 11:769-776.
18. Egelman, H. H., X. Yu, R. Wild, M. M. Hingorani, and S. S. Patel. 1995. Bacteriophage T7 helicase/primase proteins form rings around single-stranded DNA that suggest a general structure for hexameric helicases. Proc. Natl. Acad. Sci. USA 92:3869-3873.
19. Enemark, E. J., and L. Joshua-Tor. 2006. Mechanism of DNA translocation in a replicative hexameric helicase. Nature 442:270-275.
20. Fanning, E. 1992. Simian virus 40 large T antigen: the puzzle, the pieces, and the emerging picture. J. Virol. 66:1289-1293.
21. Fanning, E., and R. Knippers. 1992. Structure and function of simian virus 40 large tumor antigen. Annu. Rev. Bioehem. 61:55-85.
22. Gai, D., D. Li, C. V. Finkielstein, R. D. Ott, P. Taneja, E. Fanning, and X. S. Chen. 2004. Insights into the oligomeric states, conformational changes, and helicase activities of SV40 large tumor antigen. J. Biol. Chem. 279:38952-38959.
23. Gai, D., R. Roy, C. Wu, and D. T. Simmons. 2000. Topoisomerase I associates specifically with simian virus 40 large-T-antigen double hexamer-origin complexes. J. Virol. 74:5224-5232.
24. Gai, D., R. Zhao, D. Li, C. V. Finkielstein, and X. S. Chen. 2004. Mechanisms of conformational change for a replicative hexameric helicase of SV40 large tumor antigen. Cell 119:47-60.
25. 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.
26. Gomez-Lorenzo, M. G., M. Valle, J. Frank, C. Gruss, C. O. Sorzano, X. S. Chen, L. E. Donate, and J. M. Carazo. 2003. Large T antigen on the simian virus 40 origin of replication: a 3D snapshot prior to DNA replication. EMBO J. 22:6205-6213.
27. Hacker, K. J., and K. A. Johnson. 1997. A hexameric helicase encircles one DNA strand and excludes the other during DNA unwinding. Biochemistry 36:14080-14087.
28. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14:27-28, 33-38.
29. Jiao, J., and D. T. Simmons. 2003. Nonspecific double-stranded DNA binding activity of simian virus 40 large T antigen is involved in melting and unwinding of the origin. J. Virol. 77:12720-12728.
30. 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 simian virus 40 (SV40) T antigen DNA-binding domain and characterization of its interactions with the SV40 origin. J. Virol. 71:3972-3985.
31. Kaplan, D. L., and M. O'Donnell. 2002. DnaB drives DNA branch migration and dislodges proteins while encircling two DNA strands. Mol. Cell 10:647-657.
32. Kaplan, D. L., and M. O'Donnell. 2004. Twin DNA pumps of a hexameric helicase provide power to simultaneously melt two duplexes. Mol. Cell 15:453-465.
33. Kim, H. Y., B. Y. Ahn, and Y. Cho. 2001. Structural basis for the inactivation of retinoblastoma tumor suppressor by SV40 large T antigen. EMBO J. 20:295-304.
34. Li, D., R. Zhao, W. Lilyestrom, D. Gai, R. Zhang, J. A. DeCaprio, E. Fanning, A. Jochimiak, G. Szakonyi, and X. S. Chen. 2003. Structure of the replicative helicase of the oncoprotein SV40 large tumour antigen. Nature 423:512-518.
35. Lin, H.-J. L., R. Upson, and D. T. Simmons. 1992. Nonspecific DNA binding activity of simian virus 40 large T antigen: evidence for the cooperation of two regions for full activity. J. Virol. 66:5443-5452.
36. Loeber, G., R. Parsons, and P. Tegtmeyer. 1989. The zinc finger region of simian virus 40 large T antigen. J. Virol. 63:94-100.
37. Luo, X., D. G. Sanford, P. A. Bullock, and W. W. Bachovchin. 1996. Solution structure of the origin DNA-binding domain of SV40 T-antigen. Nat. Struct. Biol. 3:1034-1039.
38. 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 338:658-662.
39. 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.
40. 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.
41. Meinke, G., P. A. Bullock, and A. Bohm. 2006. Crystal structure of the simian virus 40 large T-antigen origin-binding domain. J. Virol. 80:4304-4312.
42. 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.
43. Mendez, J., and B. Stillman. 2003. Perpetuating the double helix: molecular machines at eukaryotic DNA replication origins. Bioessays 25:1158-1167.
44. 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.
45. 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.
46. Murakami, Y., C. R. Wobbe, L. Weissbach, F. B. Dean, and J. Hurwitz. 1986. Role of DNA polymerase alpha and DNA primase in simian virus 40 DNA replication in vitro. Proc. Natl. Acad. Sci. USA 83:2869-2873.
47. 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.
48. 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.
49. Patel, S. S., and K. M. Picha. 2000. Structure and function of hexameric helicases. Annu. Rev. Bioehem. 69:651-697.
50. Reese, D. K., G. Meinke, A. Kumar, S. Moine, K. Chen, J. L. Sudmeier, W. Bachovchin, A. Bohm, and P. A. Bullock. 2006. Analyses of the interaction between the origin binding domain from simian virus 40 T antigen and single-stranded DNA provide insights into DNA unwinding and initiation of DNA replication. J. Virol. 80:12248-12259.
51. Reese, D. K., K. R. Sreekumar, and P. A. Bullock. 2004. Interactions required for binding of simian virus 40 T antigen to the viral origin and molecular modeling of initial assembly events. J. Virol. 78:2921-2934.
52. Sawaya, M. R., S. Guo, S. Tabor, C. C. Richardson, and T. Ellenberger. 1999. Crystal structure of the helicase domain from the replicative helicase-primase of bacteriophage T7. Cell 99:167-177.
53. Schuck, S., and A. Stenlund. 2005. Assembly of a double hexameric helicase. Mol. Cell 20:377-389.
54. Sclafani, R. A., R. J. Fletcher, and X. S. Chen. 2004. Two heads are better than one: regulation of DNA replication by hexameric helicases. Genes Dev. 18:2039-2045.
55. Seinsoth, S., H. Uhlmann-Schiffler, and H. Stahl. 2003. Bidirectional DNA unwinding by a ternary complex of T antigen, nucleolin and topoisomerase 1. EMBO Rep. 4:263-268.
56. 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.
57. Shen, J., D. Gai, A. Patrick, W. B. Greenleaf, and X. S. Chen. 2005. The roles of the residues on the channel beta-hairpin and loop structures of simian virus 40 hexameric helicase. Proc. Natl. Acad. Sci. USA 102:11248-11253.
58. Simmons, D. T. 2000. SV40 large T antigen: functions in DNA replication and transformation. Adv. Virus Res. 55:75-134.
59. Simmons, D. T., D. Gai, R. Parsons, A. Debes, and R. Roy. 2004. Assembly of the replication initiation complex on SV40 origin DNA. Nucleic Acids Res. 32:1103-1112.
60. Simmons, D. T., R. Roy, L. Chen, D. Gai, and P. W. Trowbridge. 1998. The activity of topoisomerase 1 is modulated by large T antigen during unwinding of the SV40 origin. J. Biol. Chem. 273:20390-20396.
61. Simmons, D. T., P. W. Trowbridge, and R. Roy. 1998. Topoisomerase 1 stimulates SV40 T antigen-mediated DNA replication and inhibits T antigen's ability to unwind DNA at nonorigin sites. Virology 242:435-443.
62. 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.
63. Singleton, M. R., M. R. Sawaya, T. Ellenberger, and D. B. Wigley. 2000. Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides. Cell 101:589-600.
64. 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.
65. Stillman, B., R. D. Gerard, R. A. Guggenheimer, and Y. Gluzman. 1985. T antigen and template requirements for SV40 DNA replication in vitro. EMBO J. 4:2933-2939.
66. Stillman, B. W., and Y. Gluzman. 1985. Replication and supercoiling of simian virus 40 DNA in cell extracts from human cells. Mol. Cell. Biol. 5:2051-2060.
67. Sullivan, C. S., and J. M. Pipas. 2002. T antigens of simian virus 40: molecular chaperones for viral replication and tumorigenesis. Microbiol. Mol. Biol. Rev. 66:179-202.
68. Titolo, S., E. Weichner, P. W. White, and J. Archambault. 2003. Characterization of the DNA-binding properties of the origin-binding domain of simian virus 40 large T antigen by fluorescence anisotropy. J. Virol. 77:5512-5518.
69. Trowbridge, P. W., R. Roy, and D. T. Simmons. 1999. Human topoisomerase I promotes initiation of simian virus 40 DNA replication in vitro. Mol. Cell. Biol. 19:1686-1694.
70. Valle, M., X. S. Chen, L. E. Donate, E. Fanning, and J. M. Carazo. 2006. Structural basis for the cooperative assembly of large T antigen on the origin of replication. J. Mol. Biol. 357:1295-1305.
71. VanLoock, M. S., A. Alexandrov, X. Yu, N. R. Cozzarelli, and E. H. Egelman. 2002. SV40 large T antigen hexamer structure: domain organization and DNA-induced conformational changes. Curr. Biol. 12:472-476.
72. 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.
73. Wessel, R., U. Ramsperger, H. Stahl, and R. Knippers. 1992. The interaction of SV40 large T antigen with unspecific double-stranded DNA: an electron microscopic study. Virology 189:293-303.
74. 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.
75. Wiekowski, M., M. W. Schwarz, and H. Stahl. 1988. Simian virus 40 large T antigen DNA helicase. Characterization of the ATPase-dependent DNA unwinding activity and its substrate requirements. J. Biol. Chem. 263:436-442.
76. Wold, M. S., and T. 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.
77. Wu, C., R. Roy, and D. T. Simmons. 2001. Role of single-stranded DNA binding activitv of T antigen in simian virus 40 DNA replication. J. Virol. 75:2839-2847.
78. 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.
79. Yu, X., and E. H. Egelman. 1997. The RecA hexamer is a structural homologue of ring helicases. Nat. Struct. Biol. 4:101-104.