Phosphorylation of the viral nonstructural protein NS1 during MVMp infection of A9 cells

Virology

Volumn 259, Issue 2, 1999, Pages 402-415

  Corbau, Romuald ^a   Salomé, Nathalie ^a   Rommelaere, Jean ^a   Nüesch, Jürg P F ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Nonstructural protein NS1; Parvovirus MVM; Phosphorylation; Virus cycle

Indexed keywords

PHOSPHOPROTEIN; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; COVALENT BOND; CYTOPATHOGENIC EFFECT; DNA REPLICATION; FIBROBLAST CULTURE; GENE AMPLIFICATION; MOUSE; NONHUMAN; PARVOVIRUS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; VIRUS INFECTION;

ANIMALIA; DNA VIRUSES; PARVOVIRUS;

EID: 0033526831     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1006/viro.1999.9786     Document Type: Article

References (66)

1. Anouja F., Wattiez R., Mousset S., Caillet-Fauquet P. The cytotoxicity of the parvovirus minute virus of mice nonstructural protein NS1 is related to changes in the synthesis and phosphorylation of cell proteins. J. Virol. 71:1997;4671-4678.
2. Astell C. R., Mol C. D., Anderson W. F. Structural and functional homology of parvovirus and papovavirus polypeptides. J. Gen. Virol. 68:1987;885-893.
3. Astell C. R., Liu Q., Harris C. E., Brunstein J., Jindal H. K., Tam P. Minute virus of mice cis-acting sequences required for genome replication and the role of the trans-acting viral protein, NS1. Prog. Nucleic Acids Res. Mol. Biol. 55:1996;245-285.
4. Baldauf A., Willwand K., Mumtsidu E., Nüesch J. P. F., Rommelaere J. Formation of circular replicative form (RF) from single-stranded virion DNA and initiation of DNA replication at the RF 5′ telomere induced by the MVM nonstructural protein NS1. J. Virol. 71:1997;971-980.
5. Ball-Goodrich L. J., Tattersall P. Two amino acid substitutions within the capsid are coordinately required for acquisition of fibrotropism by the lymphotropic strain of minute virus of mice. J. Virol. 66:1992;3415-3423.
6. Bodnar J. W., Hanson P. I., Polvino-Bodnar M., Zempsky W., Ward D. The terminal regions of adenovirus and minute virus of mice DNAs are preferentially associated with the nuclear matrix in infected cells. J. Virol. 63:1989;4344-4353.
7. Boyle W. J., van der Geer P., Hunter T. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Hunter A. B. M. S. T. Protein Phosphorylation Part B. 1991;110-152 Academic Press, San Diego.
8. Brandenburger A., Legendre D., Avalosse B., Rommelaere J. NS1 and NS2 proteins may act synergistically in the cytopathogenicity of parvovirus MVMp. Virology. 174:1990;576-584.
9. Brockhaus K., Plaza S., Pintel D. J., Rommelaere J., Salomé N. Non-structural proteins NS2 of minute virus of mice associate in vivo with 14-3-3 protein family members. J. Virol. 70:1996;7527-7534.
10. Caillet-Fauquet P., Perros M., Brandenburger A., Spegelaere P., Rommelaere J. Programmed killing of human cells by means of an inducible clone of parvoviral genes encoding non-structural proteins. EMBO J. 9:1990;2989-2995.
11. Christensen J., Cotmore S. F., Tattersall P. 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. 69:1995a;5422-5430.
12. Christensen J., Pederson M., Aasted B., Alexandersen S. Purification and characterization of the major non-structural protein (NS1) of Aleutian mink disease parvovirus. J. Virol. 69:1995b;1802-1809.
13. Christensen J., Cotmore S. F., Tattersall P. A novel cellular site-specific DNA-binding protein co-operates with the viral NS1 polypeptide to initiate parvoviral DNA replication. J. Virol. 71:1997;1405-1416.
14. Cotmore S. F., Tattersall P. The NS1 polypeptide of the autonomous parvovirus MVM is a nuclear phosphoprotein. Virus Res. 4:1986;243-250.
15. Cotmore S. F., Tattersall P. The autonomously replicating parvoviruses of vertebrates. Adv. Virus Res. 33:1987;91-174.
16. Cotmore S. F., Tattersall P. The NS1 polypeptide of minute virus of mice is covalently attached to the 5′ termini of duplex replicative-form DNA and progeny single strands. J. Virol. 62:1988;851-860.
17. Cotmore S. F., Tattersall P. A genome-linked copy of the NS1 polypeptide is located on the outside of infectious parvovirus particles. J. Virol. 63:1989;3902-3911.
18. Cotmore S. F., Tattersall P. Alternate splicing in a parvoviral non-structural gene links a common amino-terminal sequence to downstream domains which confer radically different localization and turnover characteristics. Virology. 177:1990;477-487.
19. Cotmore S. F., Nüesch J. P., Tattersall P. In vitro excision and replication of 5′ telomeres of minute virus of mice DNA from cloned palindromic concatemer junctions. Virology. 190:1992;365-377.
20. Cotmore S. F., Tattersall P. 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. 66:1992;420-431.
21. Cotmore S. F., Nüesch J. P., Tattersall P. Asymmetric resolution of a parvovirus palindrome in vitro. J. Virol. 67:1993;1579-1589.
22. Cotmore S. F., Tattersall P. DNA replication in the autonomous parvoviruses. Semin. Virol. 6:1995;271-281.
23. Cotmore S. F., Christensen J., Nüesch J. P., Tattersall P. The NS1 polypeptide of the murine parvovirus minute virus of mice binds to DNA sequences containing the motif [ACCA]2-3. J. Virol. 69:1995;1652-1660.
24. Cotmore S. F., D'Abramo A. M., Carbonell L. F., Bratton J., Tattersall P. The NS2 polypeptide of parvovirus MVM is required for capsid assembly in murine cells. Virology. 231:1997;267-289.
25. Cotmore S. F., Tattersall P. High-mobility group 1/2 proteins are essential for initiating rolling circle DNA replication at a parvovirus hairpin origin. J. Virol. 72:1998;8477-8484.
26. Cziepluch C., Kordes E., Poirey R., Grewenig A., Rommelaere J., Jauniaux J.-C. Identification of a novel cellular TPR containing protein, SGT, that interacts with the nonstructural protein NS1 of parvovirus H-1. J. Virol. 72:1998;4149-4156.
27. Deleu L., Fuks F., Spitkovsky D., Horlein R., Faisst S., Rommelaere J. Opposite transcriptional effects of cyclic AMP responsive elements on confluent or p27-kip-expressing cells versus serum-starved or growing cells. Mol. Cell. Biol. 18:1998;409-419.
28. Doerig C., Hirt B., Antonietti J. P., Beard P. Non-structural proteins of parvovirus B19 and minute virus of mice control transcription. J. Virol. 64:1990;387-396.
29. Eng W. K., Pandit S. D., Sternglanz R. Mapping of the active site tyrosine of eucaryotic DNA topoisomerases. J. Biol. Chem. 264:1989;13373-13376.
30. Jindal H. K., Yong C. B., Wilson G. M., Tam P., Astell C. R. Mutations in the NTP-binding motif of minute virus of mice (MVM) NS1 protein uncouple ATPase and DNA helicase functions. J. Biol. Chem. 269:1994;3283-3289.
31. Kornberg A., Baker T. A. DNA Replication. 1992;Freeman, New York.
32. Krady J. K., Ward D. C. Transcriptional activation by the parvoviral nonstructural protein NS-1 is mediated via a direct interaction with Sp1. Mol. Cell. Biol. 15:1995;524-533.
33. Legendre D., Rommelaere J. Terminal regions of the NS1 protein of the parvovirus minute virus of mice are involved in cytotoxicity and promoter trans-inhibition. J. Virol. 66:1992;5705-5713.
34. Legendre D., Rommelaere J. Targeting of promoters for trans-activation by a carboxy-terminal domain of the NS1 protein of the parvovirus minute virus of mice. J. Virol. 68:1994;7974-7985.
35. Li X., Rhode S. L. III. 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. 64:1990;4654-4660.
36. Lopez-Guerrero J. A., Rayet B., Tuyinder M., Rommelaere J., Dinsart C. Constitutive activation of U937 promonocytic cell clones selected for their resistance to parvovirus H-1 infection. Blood. 89:1997;1642-1653.
37. Lorson C., Pearson J., Burger L., Pintel D. J. An Sp1-binding site and TATA element are sufficient to support full transactivation by proximally bound NS1 protein of minute virus of mice. Virology. 240:1998;326-337.
38. Mackett M., Smith G. L., Moss B. The construction and characterization of vaccinia virus recombinants expressing foreign genes. Glover D. M. DNA Cloning: A Practical Approach. 1985;IRL Press, Oxford.
39. Marks F., Gschwendt M. Protein kinase C. Marks F. Protein Phosphorylation. 1996;81-116 VCH, Weinheim.
40. Merchlinsky M. J., Tattersall P., Leary J. J., Cotmore S. F., Gardiner E. M., Ward D. C. Construction of an infectious molecular clone of the autonomous parvovirus minute virus of mice. J. Virol. 47:1983;227-232.
41. Molitor T. W., Joo H. S., Collett M. S. Identification and characterization of a porcine parvovirus non-structural polypeptide. J. Virol. 55:1985;554-559.
42. Moss B., Elroy-Stein O., Mizukami T., Alexander W. A., Fuerst T. Product review. New mammalian expression vectors. Nature. 348:1990;91-92.
43. Mousset S., Ouadrhiri Y., Caillet Fauquet P., Rommelaere J. The cytotoxicity of the autonomous parvovirus minute virus of mice non-structural proteins in FR3T3 rat cells depends on oncogene expression. J. Virol. 68:1994;6446-6453.
44. Naeger L. K., Cater J., Pintel D. J. The small non-structural protein (NS2) of minute virus of mice is required for efficient DNA replication and infectious virus production in a cell-type-specific manner. J. Virol. 64:1990;6166-6175.
45. Nüesch J. P., Cotmore S. F., Tattersall P. Expression of functional parvoviral NS1 from recombinant vaccinia virus: Effects of mutations in the nucleotide-binding motif. Virology. 191:1992;406-416.
46. Nüesch J. P., Tattersall P. Nuclear targeting of the parvoviral replicator protein molecule NS1: Evidence for self-association prior to nuclear transport. Virology. 196:1993;637-651.
47. Nüesch J. P., Cotmore S. F., Tattersall P. 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. 209:1995;122-135.
48. Nüesch J. P. F., Corbau R., Tattersall P., Rommelaere J. Biochemical activities of minute virus of mice nonstructural protein NS1 are modulated by the phosphorylation state of the polypeptide. J. Virol. 72:1998a;8002-8012.
49. Nüesch J. P. F., Dettwiler S., Corbau R., Rommelaere J. Replicative functions of minute virus of mice NS1 protein are regulated in vitro by phosphorylation through protein kinase C. J. Virol. 72:1998b;9966-9977.
50. Oleksiewicz M. B., Costello F., Huhtanen M., Wolfinbarger J. B., Alexanderson S., Bloom M. E. Subcellular localization of Aleutian mink disease parvovirus proteins and DNA during permissive infection of Brandell feline kidney cells. J. Virol. 70:1996;3242-3247.
51. Oleksiewicz M. B., Alexanderson S. S-phase dependent cell cycle disturbances caused by Aleutian mink disease parvovirus. J. Virol. 71:1997;1386-1396.
52. Op de Beek A. A. F., Mousset S., Rommelaere J., Caillet-Fauquet P. The nonstructural proteins of the autonomous parvovirus minute virus of mice interfere with the cell cycle, inducing accumulation in G2. Cell Growth Differ. 6:1995;781-787.
53. Op de Beek A., Caillet-Fauquet P. The NS1 protein of the autonomous parvovirus minute virus of mice blocks cellular DNA replication: A consequence of lesions to the chromatin? J. Virol. 71:1997;5323-5329.
54. Parker P. J., Dekker L. V. Protein Kinase C. 1997;Springer, New York/Berlin.
55. Pujol A., Deleu L., Nüesch J. P. F., Cziepluch C., Jauniaux J.-C., Rommelaere J. Inhibition of parvovirus minute virus of mice replication by a peptide involved in the oligomerization of the nonstructural protein NS1. J. Virol. 71:1997;7393-7403.
56. Rayet B., Lopez-Guerrero J.-A., Rommelaere J., Dinsart C. Induction of programmed cell death by parvovirus H-1 in U937 cells: Connection with the tumor necrosis factor alpha signalling pathway. J. Virol. 72:1998;8893-8903.
57. Rhode S. L. I., Richard S. M. Characterization of the trans-activation-responsive element of the parvovirus H-1 P38 promoter. J. Virol. 61:1987;2807-2815.
58. Santaren J. F., Ramirez J. C., Almendral J. M. Protein species of the parvovirus minute virus of mice strain MVMp: Involvement of phosphorylated VP2 subtypes in viral morphogenesis. J. Virol. 67:1993;5126-5138.
59. Schaegger H., von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:1987;368-379.
60. Schoborg R. V., Pintel D. J. Accumulation of MVM gene products is differentially regulated by transcription initiation. Virology. 181:1991;22-34.
61. Skiadopoulos M. H., Faust E. A. Mutational analysis of conserved tyrosines in the NS1 protein of the parvovirus minute virus of mice. Virology. 194:1993;509-517.
62. Tullis G., Schoborg R. V., Pintel D. J. Characterization of the temporal accumulation of minute virus of mice replicative intermediates. J. Gen. Virol. 75:1994;1633-1646.
63. Vanacker J.-M., Rommelaere J. Non-structural proteins of autonomous parvoviruses: From cellular effects to molecular mechanisms. Semin. Virol. 6:1995;291-297.
64. Vanacker J.-M., Corbau R., Adelmant G., Perros M., Laudet V., Rommelaere J. Transactivation of a cellular promoter by the NS1 protein of the parvovirus minute virus of mice through a putative hormone-responsive element. J. Virol. 70:1996;2369-2377.
65. Weisshart K., Fanning E. Roles of phosphorylation in DNA replication. DePamphilis M. L. DNA Replication in Eucaryotic Cells. 1996;295-330 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
66. Wilson G. M., Jindal H. K., Yeung D. E., Chen W., Astell C. R. Expression of minute virus of mice major non-structural protein in insect cells: Purification and identification of ATPase and helicase activities. Virology. 185:1991;90-98.