Biochemical activities of minute virus of mice nonstructural protein NS1 are modulated in vitro by the phosphorylation state of the polypeptide

Journal of Virology

Volumn 72, Issue 10, 1998, Pages 8002-8012

  Nüesch, Jürg P F ^a   Corbau, Romuald ^a   Tattersall, Peter ^b   Rommelaere, Jean ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOPROTEIN; PROTEIN KINASE C; VIRUS PROTEIN;

ARTICLE; DNA BINDING; DNA REPLICATION; ENZYME ACTIVITY; HELA CELL; NONHUMAN; PARVOVIRUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; VACCINIA VIRUS; VIRUS REPLICATION;

EID: 0031714793     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.10.8002-8012.1998     Document Type: Article

References (71)

1. Astell, C. R., Q. Liu, C. E. Harris, J. Brunstein, H. K. Jindal, and P. Tam. 1996. Minute virus of mice cis-acting sequences required for genome replication and the role of the trans-acting viral protein, NS1. Prog. Nucleic Acid Res. Mol. Biol. 55:245-285.
2. Astell, C. R., C. D. Mol, and W. F. Anderson. 1987. Structural and functional homology of parvovirus and papovavirus polypeptides. J. Gen. Virol. 68:885-893.
3. Baas, P. D., and H. S. Jansz. 1988. Single-stranded DNA phage origins. Curr. Top. Microbiol. Immunol. 136:31-70.
4. Baldauf, A. Q., K. Willwand, E. Mumtsidu, J. P. F. Nüesch, and J. Rommelaere. 1997. Specific initiation of replication at the right-end telomere of the closed species of minute virus of mice replicative-form DNA. J. Virol. 71: 971-980.
5. Boyle, W. J., P. van der Geer, and T. Hunter. 1991. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates, p. 110-152. In B. M. S. T. Hunter (ed.), Protein phosphorylation, vol. 201, part B. Academic Press, Inc., San Diego, Calif.
6. Brandenburger, A., D. Legendre, B. Avalosse, and J. Rommelaere. 1990. NS1 and NS2 proteins may act synergistically in the cytopathogenicity of parvovirus MVMp. Virology 174:576-584.
7. Caillet-Fauquet, P., M. Perros, A. Brandenburger, P. Spegelaere, and J. Rommelaere. 1990. Programmed killing of human cells by means of an inducible clone of parvoviral genes encoding non-structural proteins. EMBO J. 9:2989-2995.
8. Cegielska, A., and D. M. Virshup. 1993. Control of simian virus 40 DNA replication by the HeLa cell nuclear kinase casein kinase I. Mol. Cell. Biol. 13:1202-1211.
9. 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.
10. Christensen, J., and J. P. I. Nüesch. Unpublished observations.
11. Christensen, J., S. F. Cotmore, and P. Tattersall. 1995. Minute virus of mice transcriptional activator protein NS1 binds directly to the transactivation region of the viral P38 promoter in a strictly ATP-dependent manner. J. Virol. 69:5422-5430.
12. Christensen, J., S. F. Cotmore, and P. Tattersall. 1997. A novel cellular site-specific DNA-binding protein cooperates with the viral NS1 polypeptide to initiate parvovirus DNA replication. J. Virol. 71:1405-1416.
13. Christensen, J., M. Pederson, B. Aasted, and S. Alexandersen. 1995. Purification and characterization of the major nonstructural protein (NS-1) of Aleutian mink disease parvovirus. J. Virol. 69:1802-1809.
14. Corbau, R., J. P. F. Nüesch, N. Salome, and J. Rommelaere. 1997. Phosphorylation study of minute virus of mice NS1 protein. Presented at the VIIth International Parvovirus Workshop, Heidelberg, Germany.
15. Cornelis, J. J., P. Becquart, N. Duponchel, N. Salomé, B. L. Avalosse, M. Namba, and J. Rommelaere. 1988. Transformation of human fibroblasts by ionizing radiation, a chemical carcinogen, or simian virus 40 correlates with an increase in susceptibility to the autonomous parvoviruses H-1 virus and minute virus of mice. J. Virol. 62:1679-1686.
16. Cotmore, S. F., and P. Tattersall. 1994. An asymmetric nucleotide in the parvoviral 3′ hairpin directs segregation of a single active origin of DNA replication. EMBO J. 13:4145-4152.
17. Cotmore, S. F., J. P. F. Nüesch, and P. Tattersall. 1993. Asymmetric resolution of a parvovirus palindrome in vitro. J. Virol. 67:1579-1589.
18. Cotmore, S. F., and P. Tattersall. 1987. The autonomously replicating parvoviruses of vertebrates. Adv. Virus Res. 33:91-174.
19. Cotmore, S. F., and P. Tattersall. 1995. DNA replication in the autonomous parvoviruses. Semin. Virol. 6:271-281.
20. Cotmore, S. F., and P. Tattersall. 1989. A genome-linked copy of the NS-1 polypeptide is located on the outside of infectious parvovirus particles. J. Virol. 63:3902-3911.
21. Cotmore, S. F., J. P. Nüesch, and P. Tattersall. 1992. In vitro excision and replication of 5′ telomeres of minute virus of mice DNA from cloned palindromic concatemer junctions. Virology 190:365-377.
22. Cotmore, S. F., and P. Tattersall. 1992. In vivo resolution of circular plasmids containing concatemer junction fragments from minute virus of mice DNA and their subsequent replication as linear molecules. J. Virol. 66:420-431.
23. Cotmore, S. F., and P. Tattersall. 1988. The NS-1 polypeptide of minute virus of mice is covalently attached to the 5′ termini of duplex replicative-form DNA and progeny single strands. J. Virol. 62:851-860.
24. Cotmore, S. F., and P. Tattersall. 1986. The NS1 polypeptide of the autonomous parvovirus MVM is a nuclear phosphoprotein. Virus Res. 4:243-250.
25. 2-3. J. Virol. 69:1652-1660.
26. Cotmore, S. F., and P. Tattersall. 1986. Organization of nonstructural genes of the autonomous parvovirus minute virus of mice. J. Virol. 58:724-732.
27. Cotmore, S. F., and P. Tattersall. 1997. Resolution of the MVM right-end (5′) hairpin: viral sequences and trans-acting factors required to allow NS1 to nick the origin. Presented at the VIIth International Parvovirus Workshop, Heidelberg, Germany.
28. Dettwiler, S., R. Corbau, J. Rommelaere, and J. P. F. Nüesch. 1997. Replicative functions of MVM NS1 are regulated by members of the protein kinase C family. Presented at the VIIth International Parvovirus Workshop, Heidelberg, Germany.
29. Doerig, C., B. Hirt, J.-P. Antonietti, and P. Beard. 1990. Nonstructural protein of parvoviruses B19 and minute virus of mice controls transcription. J. Virol. 64:387-396.
30. Doerig, C., G. McMaster, J. Sogo, H. Bruggmann, and P. Beard. 1986. Nucleoprotein complexes of minute virus of mice have a distinct structure different from that of chromatin. J. Virol. 58:817-824.
31. Fanning, E. 1992. Simian virus 40 large T antigen: the puzzle, the pieces, and the emerging picture. J. Virol. 66:1289-1293.
32. Fuerst, T. R., E. G. Niles, F. W. Studier, and B. Moss. 1986. Eucaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc. Natl. Acad. Sci. USA 83:8122-8126.
33. Hoffmann, I. 1996. Cyclin-dependent protein kinases and the regulation of the eucaryotic cell cycle, p. 179-201. In F. Marks (ed.), Protein phosphorylation. VCH Verlagsgesellschaft mbH, Weinheim, Germany.
34. Hübscher, U., G. Maga, and V. N. Podust. 1997. DNA replication accessory proteins, p. 525-543. In M. L. dePamphilis (ed.), DNA replication in eukaryotic cells. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
35. Inamoto, S., Y. Yoshioka, and E. Ohtsubo. 1991. Site- and strand-specific nicking in vitro at oriT by the traY-tral endonuclease of plasmid R100. J. Biol. Chem. 266:10086-10092.
36. Jindal, H. K., C. B. Yong, G. M. Wilson, P. Tam, and C. R. Astell. 1994. Mutations in the NTP-binding motif of minute virus of mice (MVM) NS1 protein uncouple ATPase and DNA helicase functions. J. Biol. Chem. 269:3283-3289,
37. Legendre, D., and J. Rommelaere. 1994. Targeting of promoters for trans activation by a carboxy-terminal domain of the NS-1 protein of the parvovirus minute virus of mice. J. Virol. 68:7974-7985.
38. Legendre, D., and J. Rommelaere. 1992. Terminal regions of the NS-1 protein of the parvovirus minute virus of mice are involved in cytotoxicity and promoter trans inhibition. J. Virol. 66:5705-5713.
39. Li, X., and S. L. Rhode III. 1990. Mutation of lysine 405 to serine in the parvovirus H-1 NS1 abolishes its functions for viral DNA replication, late promoter trans activation, and cytotoxicity. J. Virol. 64:4654-4660.
40. 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.
41. Mackett, M., G. L. Smith, and B. Moss. 1985. The construction and characterization of vaccinia virus recombinants expressing foreign genes. In D. M. Glover (ed.), DNA cloning: a practical approach. IRL Press, Oxford, United Kingdom.
42. Mansfield, M. 1994. Protein blotting, a practical approach, p. 33-52. IRL Press, Oxford, United Kingdom.
43. Marks, F. 1996. The brain of the cell, p. 1-35. In F. Marks (ed.), Protein phosphorylation. VCH Verlagsgesellschaft mbH, Weinheim, Germany.
44. Marks, F., and M. Gschwendt. 1996. Protein kinase C, p. 81-116. In F. Marks (ed.), Protein phosphorylation. VCH Verlagsgesellschaft mbH, Weinheim, Germany.
45. 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.
46. 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.
47. 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.
48. Merchlinsky, M. J., P. J. Tattersall, J. J. Leary, S. F. Cotmore, E. M. Gardiner, and D. C. Ward. 1983. Construction of an infectious molecular clone of the autonomous parvovirus minute virus of mice. J. Virol. 47: 227-232.
49. Moarefi, I. F., D. Small, I. Gilbert, M. Höpfner, S. K. Randall, C. Schneider, A. A. 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 unwinding. J. Virol. 67:4992-5002.
50. Molitor, T. W., H. S. Joo, and M. S. Collett. 1985. Identification and characterization of a porcine parvovirus nonstructural polypeptide. J. Virol. 55: 554-559.
51. Moss, B., O. Elroy Stein, T. Mizukami, W. A. Alexander, and T. R. Fuerst. 1990. Product review. New mammalian expression vectors. Nature 348:91-92.
52. Mousset, S., Y. Ouadrhiri, P. Caillet-Fauquet, and J. Rommelaere. 1994. The cytotoxicity of the autonomous parvovirus minute virus of mice nonstructural proteins in FR3T3 rat cells depends on oncogene expression. J. Virol. 68:6446-6453.
53. Nüesch, J. P., S. F. Cotmore, and P. Tattersall. 1992. Expression of functional parvoviral NS1 from recombinant vaccinia virus: effects of mutations in the nucleotide-binding motif. Virology 191:406-416.
54. Nüesch, J. P., and P. Tattersall. 1993. Nuclear targeting of the parvoviral replicator protein molecule NS1: evidence for self-association prior to nuclear transport. Virology 196:637-651.
55. Nüesch, J. P., R. Corbau, P. Tattersall, and J. Rommelaere. 1996. Replication activities of MVM NS1 are regulated through phosphorylation. Presented at the 15th Annual Meeting of the American Society for Virology, London, Ontario, Canada.
56. Nüesch, J. P., S. F. Cotmore, and P. Tattersall. 1995. Sequence motifs in the replicator protein of parvovirus MVM essential for nicking and covalent attachment to the viral origin: identification of the linking tyrosine. Virology 209:122-135.
57. Nüesch, J. P. F. Unpublished observations.
58. Parsons, R. E., J. E. Stenger, S. Ray, R. Welker, M. E. Andersen, 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.
59. Prives, C. 1990. The replication functions of SV40 T antigen are regulated by phosphorylation. Cell 61:735-738.
60. Pujol, A., L. Deleu, J. P. F. Nüesch, C. Cziepluch, J.-C. Jauniaux, and J. Rommelaere. 1997. Inhibition of parvovirus minute virus of mice replication by a peptide involved in the oligomerization of nonstructural protein NS1. J. Virol. 71:7393-7403.
61. Rhode, S. L., III, and S. M. Richard. 1987. Characterization of the transactivation-responsive element of the parvovirus H-1 P38 promoter. J. Virol. 61:2807-2815.
62. Schoborg, R. V., and D. J. Pintel. 1991. Accumulation of MVM gene products is differentially regulated by transcription initiation. Virology 181:22-34.
63. Skiadopoulos, M. H., and E. A. Faust. 1993. Mutational analysis of conserved tyrosines in the NS1 protein of the parvovirus minute virus of mice. Virology 194:509-517.
64. Snyder, R. O., R. J. Samulski, and N. Muzyczka. 1990. In vitro resolution of covalently joined AAV chromosome ends. Cell 60:105-113.
65. Sung, P., D. Higgins, L. Prakash, and S. Prakash. 1988. Mutation of lysine-48 to arginine in the yeast RAD3 protein abolishes ATPase and DNA helicase activities but not the ability to bind ATP. EMBO J. 7:3263-3269.
66. Tattersall, P., and D. C. Ward. 1976. Rolling hairpin model for replication of parvovirus and linear chromosomal DNA. Nature 263:106-109.
67. Vanacker, J.-M., and J. Rommelaere. 1995. Non-structural proteins of autonomous parvoviruses: from cellular effects to molecular mechanisms. Semin. Virol. 6:291-297.
68. Vanacker, J.-M., R. Corbau, G. Adelmant, M. Perros, V. Laudet, and J. Rommelaere. 1996. Transactivation of a cellular promoter by the NS1 protein of the parvovirus minute virus of mice through a putative hormone-responsive element. J. Virol. 70:2369-2377.
69. Wang, E. H., and C. Prives. 1991. ATP induces the assembly of polyomavirus large tumor antigen into hexamers. Virology 184:90-98.
70. Wilson, G. M., H. K. Jindal, D. E. Yeung, W. Chen, and C. R. Astell. 1991. Expression of minute virus of mice major non-structural protein in insect cells: purification and identification of ATPase and helicase activities. Virology 185:90-98.
71. Woodgett, J. R. 1991. Use of synthetic peptides mimicking phosphorylation sites for affinity purification of protein-serine kinases, p. 169-178. In B. M. S. T. Hunter (ed.), Protein phosphorylation, vol. 200, part A. Academic Press, Inc., San Diego, Calif.