Species-specific replication of simian virus 40 DNA in vitro requires the p180 subunit of human DNA polymerase α-primase

Molecular and Cellular Biology

Volumn 16, Issue 1, 1996, Pages 94-104

  Stadlbauer, Franz ^a,d   Voitenleitner, Christian ^a,b   Brückner, Andrea ^a,e   Fanning, Ellen ^a,b   Nasheuer, Heinz Peter ^a,c  

^a UNIVERSITY OF MUNICH   (Germany)

^b VANDERBILT UNIVERSITY   (United States)

^c IMB Jena   (Germany)

^d Fa Bios GmbH   (Germany)

^e UNIVERSITY HOSPITAL ERLANGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

SIMIAE; SIMIAN VIRUS; SIMIAN VIRUS 40; UNIDENTIFIED BACULOVIRUS;

DNA HYBRID; DNA POLYMERASE; DNA PRIMASE;

ARTICLE; DNA REPLICATION; ENZYME SUBUNIT; HUMAN; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIMIAN VIRUS 40; SPECIES DIFFERENCE; VIRUS CELL INTERACTION; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANIMAL; DNA PRIMASE; DNA REPLICATION; DNA, VIRAL; HUMAN; IN VITRO; MICE; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; RNA NUCLEOTIDYLTRANSFERASES; SEQUENCE HOMOLOGY, AMINO ACID; SIMIAN VIRUS 40; SPECIES SPECIFICITY; SUPPORT, NON-U.S. GOV'T; VIRUS REPLICATION;

EID: 0029656206     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.16.1.94     Document Type: Article

References (78)

1. Bennett, E. R., M. Naujokas, and J. A. Hassell. 1989. Requirements for species-specific papovavirus DNA replication. J. Virol 63:5371-5385.
2. Berko Flint, Y., S. Karby, D. Hassin, and S, Lavi. 1990. Carcinogen induced DNA amplification in vitro, overreplication of the simian virus 40 origin region in extracts from carcinogen-treated CO60 cells. Mol. Cell. Biol 10: 75-83.
3. Bradford, M. M. 1976 A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of dye-binding. Anal. Biochem. 72:248-254.
4. Brückner, A., F. Stadlbauer, L. A. Guarino, A. Brunahl, C. Schneider, C. Rehfuess. C. Prives, E. Fanning, and H.-P. Nasheuer. 1995. The mouse DNA polymerase α-primase subunit p48 mediates species-specific replication of polyomavirus DNA in vitro. Mol. Cell. Biol 15:1716-1724
5. Brunahl, A., and E. Fanning. Unpublished data.
6. 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.
7. Bullock, P. A., S. Tevosian, C. Jones, and D. Denis. 1994. Mapping initiation sites for simian virus 40 DNA synthesis events in vitro. Mol. Cell. Biol. 14: 5043-5055
8. Challberg, M., and T. J. Kelly. 1989. Animal virus DNA replication. Annu Rev Biochem. 58:671-717.
9. Cohen, S., D. Hassin, S. Karby, and S. Lavi. 1994 Hairpin structures are the primary amplification products: a novel mechanism for generation of inverted repeats during gene amplification. Mol. Cell. Biol. 14:7782-7791.
10. 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.
11. Collins, K. L., A. A. R. Russo, B. Y. Tseng, and T. J. Kelly. 1993. The role of the 70kDa subunit of human DNA polymerase α in DNA replication. EMBO J 12:4555-4566
12. Cowie, A., and R. Kamen. 1986. Guanine nucleotide contacts within viral DNA sequences bound by polyomavirus large T antigen. J. Virol. 57:505-514.
13. 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.
14. 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.
15. Denis, D., and P. Bullock. 1993. Primer DNA formation during simian virus 40 DNA replication in vitro. Mol Cell. Biol. 13:2882-2890
16. Diffley, J. F. X. 1992 Early events in eukaryotic DNA replication Trends Cell Biol. 2:298-303.
17. 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 a with large T antigen. Mol. Cell. Biol. 13:809-820
18. Dornreiter, I., S. Dehde, M. Hauser, H.-P. Nasheuer, and E. Fanning. Unpublished data
19. 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.
20. Dornreiter, I., A. Höss, A. K. Arthur, and E. Fanning. 1990. SV40 T antigen binds directly to the catalytic subunit of DNA polymerase α. EMBO J. 9: 3329-3336.
21. Eki, T., T. Enomoto, C. Masutani, A. Miyajima, R. Takada, Y. Murakami, T. Ohno, F. Hanaoka, and M. Ui. 1991. Mouse DNA primase plays the principal role in determination of permissiveness for polyomavirus DNA replication. J. Virol. 65:4874-4881.
22. Eki, T., F. Hanaoka, T. Kohda, M. Seki, M. Ui, and T. Enomoto. 1995 Efficient replication of polyomavirus in a cell-free system supplemented with Escherichia coli single-stranded DNA binding protein, which exhibits species specificity in the requirement for DNA polymerase α-primase. J. Biochem. 118:435-441.
23. Eki, T., T. Matsumoto, Y. Murakami, and J. Hurwitz. 1992. The replication of DNA containing the simian virus, 40 origin by the monopolymerase and dipolymerase systems J Biol Chem. 267:7284-7294
24. Erdile, L. F., K. L. Collins, A. Russo, P. Simancek, D. Small, C. Umbricht, D. Virshup, L. Cheng, S. Randall, D. Weinberg, I. Moarefi, E. Fanning, and T. Kelly. 1991. Initiation of SV40 DNA replication mechanism and control. Cold Spring Harbor Symp. Quant. Biol. 56:303-313.
25. Fanning, E. 1994. Control of SV40 DNA replication by protein phosphorylation a model for cellular DNA replication? Trends Cell Biol. 4:250-255.
26. Fanning, E., and R. Knippers. 1992 Structure and function of simian virus 40 large T antigen. Annu. Rev. Biochem. 61:55-85.
27. Gannon, J. V., and D. P. Lane. 1990. Interactions between SV40 T antigen and DNA polymerase α. New Biol. 2:84-92.
28. 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.
29. Ishimi, Y., A. Claude, P. Bullock, and J. Hurwitz. 1988. Complete enzymatic synthesis of DNA containing the SV40 origin of replication J. Biol. Chem. 263:19723-19733.
30. Kamakaka, R. T., P. D. Kaufman, B. Stillman, P. G. Mitsis, and J. T. Kadonaga. 1994. Simian virus 40 origin- and T-antigen-dependent DNA replication with Drosophila factors in vitro Mol Cell Biol 14:5114-5122.
31. Kelly, T. J. 1988. SV40 DNA replication J. Biol. Chem. 263:17889-17892.
32. 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.
33. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
34. Lee, S. H., and J. Hurwitz. 1990. Mechanism of elongation of primed DNA by DNA polymerase δ, proliferating cell nuclear antigen, and activator 1. Proc Natl. Acad. Sci. USA 87:5672-5676.
35. Lee, S. H., A. D. Kwong, Z. Q. Pan, and J. Hurwitz. 1991. Studies on the activator 1 protein complex, an accessory factor for proliferating cell nuclear antigen-dependent DNA polymerase δ. J. Biol. Chem. 266:594-602.
36. Li, J. J., and T. J. Kelly. 1984 Simian virus 40 DNA replication in vitro Proc. Natl Acad. Sci. USA 81:6973-6977.
37. Li, J. J., and T. J. Kelly. 1985. Simian virus 40 DNA replication in vitro, specificity of initiation and evidence for bidirectional replication. Mol. Cell. Biol. 5:1238-1246.
38. Longhese, M. P., L. Jovine, P. Plevani, and G. Lucchini. 1993. Conditional mutations in the yeast DNA primase genes affect different aspects of DNA metabolism and interactions in the DNA polymerase α-pnmase complex. Genetics 133:183-191.
39. Longhese, M. P., P. Plevani, and G. Lucchini. 1994. Replication factor A is required in vivo for DNA replication, repair, and recombination. Mol. Cell. Biol. 14:7884-7890.
40. 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.
41. 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.
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. Moarefi, I., D. Small, I. Gilbert, M. Höpfner, S. Randall, C. Schneider, A. A. 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 (SV40) large T antigen specifically blocks SV40 origin DNA unwinding. J. Virol. 67:4492-5002
44. Moses, K., and C. Prives. 1994. A unique subpopulation of murine DNA polymerase α-primase specifically interacts with polyoma virus T antigen and stimulates DNA replication Mol. Cell. Biol. 14:2767-2776.
45. 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.
46. Murakami, Y., T. Eki, M. Yamada, C. Prives, and J. Hurwitz. 1986. Species-specific in vitro synthesis of DNA containing the polyoma virus origin of replication. Proc. Natl. Acad. Sci. USA 83:6347-6351.
47. Murakami, Y., and J. Hurwitz. 1993 DNA polymerase alpha stimulates the ATP-dependent binding of simian virus tumor T antigen to the SV40 origin of replication J Biol. Chem. 268:11018-11027.
48. 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.
49. Nasheuer, H.-P., and F. Grosse. 1987. Immunoaffinity-purined DNA polymerase α displays novel properties. Biochemistry 26:8458-8466.
50. Nasheuer, H.-P., and F. Grosse. 1988. DNA polymerase α-primase from calf thymus Determination of the polypeptide responsible for primase activity. J. Biol. Chem 263:8981-8988.
51. Nasheuer, H.-P., D. von Winkler, C. Schneider, 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.
52. Nethanel, T., and G. Kaufmann. 1990. Two DNA polymerases may be required for synthesis of the lagging DNA strand of simian virus 40 J. Virol. 64:5912-5918.
53. Nethanel, T., T. Ziotkin, and G. Kaufmann. 1992. Assembly of simian virus 40 Okazaki pieces from DNA primers is rcversibly arrested by ATP depletion. J. Virol. 66:6634-6640
54. Pomerantz, B. J., and J. A. Hassell. 1984. Polyomavirus and simian virus 40 large T antigens bind to common DNA sequences. J. Virol. 49:925-937.
55. Prelich, G., and B. Stillman. 1988. Coordinated leading and lagging strand synthesis during SV40 DNA replication in vitro requires PCNA. Cell 53: 117-126.
56. Prives, C. 1990 The replication functions of SV40 T antigen are regulated by phosphorylation. Cell 61:735-738.
57. Rice, W. C., H. E. Lorimer, C. Prives, and L. K. Miller. 1987. Expression of polyoma virus large T antigen by using a baculovirus vector J. Virol. 61: 1712-1716
58. Schneider, C., K. Weißhart, L. A. Guarino, I. Dornreiter, and E. Fanning. 1994 Species specific functional interactions of DNA polymerase α-primase with SV40 T antigen require SV40 origin DNA. Mol. Cell Biol. 14:3176-3185
59. Schneider, C., D. von Winkler, I. Dornreiter, H.-P. Nasheuer, I. Gilbert, S. Dehde, A. K. Arthur, and E. Fanning. 1992. Bovine RP-A functions in SV40 DNA replication in vitro, but bovine polymerase α-primase inhibits replication competitively, p. 385-397. In P. Hughes, E. Fanning, and M. Kohiyama (ed.), Regulatory mechanisms of DNA replication. Springer Verlag, Berlin.
60. Smale, S. T., and R. Tjian. 1986. T antigen-DNA polymerase α complex implicated in simian virus 40 DNA replication. Mol. Cell. Biol. 6:4077-4087.
61. Sogo, J. M., H. Stahl, T. Koller, and R. Knippers. 1986 Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures. J Mol. Biol. 189:189-204
62. Stadlbauer, F. 1995. Molekulare Charakterisierung der Wirtszellspezifitat der DNA-Replikation von Papovaviren. PhD. Thesis Ludwig-Maximilians-Universität Munchen, Munich, Germany.
63. Stadlbauer, F., A. Brueckner, C. Rehfuess, C. Eckerskorn, 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.
64. Stahl, H., P. Droge, and R. Knippers. 1986. DNA helicase activity of SV40 large tumor antigen. EMBO J 5:1939-1944.
65. Stillman, B. 1989. Initiation of eucaryotic DNA replication in vitro Annu Rev. Cell Biol. 5:197-245
66. Tanaka, S., S.-Z. Hu, T. S.-F. Wang, and D. Korn. 1982. Preparation and preliminary characterization of monoclonal antibodies against human DNA polymerase alpha J Biol. Chem 257:8386-8390
67. Tooze, J. 1981. Molecular biology of tumor virus, part 2. DNA tumor viruses Cold Spring Harbor Laboratory. Cold Spring Harbor, N.Y.
68. Tsurimoto, T., T. Melendy, and B. Stillman. 1990 Sequential initiation of lagging and leading strand synthesis by two different polymerase complexes at the SV40 DNA replication origin Nature (London) 346:534-539.
69. 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
70. Tsurimoto, T., and B. Stillman. 1991. 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
71. Tsurimoto, T., and B. Stillman. 1991. Replication factors required for SV40 DNA replication in vitro. II Switching of DNA polymerase α and δ during initiation of leading and lagging strand synthesis. J. Biol. Chem. 266:1961-1968.
72. Waga, S., G. Bauer, and B. Stillman. 1994. Reconstitution of complete SV40 DNA replication with purified replication factors. J Biol. Chem. 269:10923-10934.
73. 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.
74. Wang, E. H., and C. Prives. 1991. ATP induces the assembly of polyoma large T antigen into hexamers. Virology 184:399-403.
75. Wang, E. H., and C. Prives. 1991. DNA helicase and duplex DNA fragment unwinding activities of polyoma and simian virus 40 large T antigen display similarities and differences. J. Biol. Chem. 266:12668-12675.
76. Wang, T. S.-F. 1991. Eukaryotic DNA polymerases. Annu. Rev. Biochem. 60: 513-552.
77. 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.
78. 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.