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PMID: 8794316 Published · ppublish English Journal Article

Simian virus 40 small t antigen activates the carboxyl-terminal transforming p53-binding domain of large T antigen.

Journal of virology ·Vol. 70 ·No. 10 ·1996-10-00 ·Pages 6781-9

Zerrahn J, Tiemann F, Deppert W

Abstract

Expression of the simian virus 40 large T antigen (large T) in F111 rat fibroblasts generated only minimal transformants (e.g., F5 cells). Interestingly, F111-derived cells expressing only an amino-terminal fragment of large T spanning amino acids 1 to 147 (e.g., FR3 cells), revealed the same minimal transformed phenotype as F111 cells expressing full-length large T. This suggested that in F5 cells the transforming domain of large T contained within the C-terminal half of the large T molecule, and spanning the p53 binding domain, was not active. Progression to a more transformed phenotype by coexpression of small t antigen (small t) could be achieved in F5 cells but not in FR3 cells. Small-t-induced progression of F5 cells correlated with metabolic stabilization of p53 in complex with large T: whereas in F5 cells the half-life of p53 in complex with large T was only slightly elevated compared with that of (uncomplexed) p53 in parental F111 cells or that in FR3 cells, coexpression of small t in F5 cells led to metabolic stabilization and to high-level accumulation of p53 complexed to large T. In contrast, coexpression of small t had no effect on p53 stabilization or accumulation in FR3 cells. This finding strongly supports the assumption that the mere physical interaction of large T with p53, and thus p53 inactivation, in F5 cells expressing large T only does not reflect the main transforming activity of the C-terminal transforming domain of large T. In contrast, we assume that the transforming potential of this domain requires activation by a cellular function(s) which is mediated by small t and correlates with metabolic stabilization of p53.

MeSH Terms
Animals Antigens, Viral, Tumor/metabolism Cell Transformation, Viral Fibroblasts/virology Phosphorylation Rats Sequence Analysis Simian virus 40/immunology
Chemicals
Antigens, Viral, Tumor
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Zerrahn J
Heinrich-Pette-Institut für Experimentelle Virologie und Immunologie an der Universität Hamburg, Germany.
Tiemann F
Deppert W
References (87)
87 references, click to expand
  1. The retinoblastoma protein and cell cycle control.
    Cell. 1995 May 5;81(3):323-30 PMID: 7736585
  2. Association of insulin receptor substrate 1 with simian virus 40 large T antigen.
    Mol Cell Biol. 1995 Aug;15(8):4232-39 PMID: 7542742
  3. Complex of simian virus large T antigen and p53 can bind DNA specifically.
    Anticancer Res. 1995 Jul-Aug;15(4):1375-80 PMID: 7654024
  4. Cooperation of simian virus 40 large and small T antigens in metabolic stabilization of tumor suppressor p53 during cellular transformation.
    J Virol. 1995 Oct;69(10):6115-21 PMID: 7666515
  5. Apoptosis, cancer and the p53 tumour suppressor gene.
    Cancer Metastasis Rev. 1995 Jun;14(2):149-61 PMID: 7554031
  6. Tumour suppressors, kinases and clamps: how p53 regulates the cell cycle in response to DNA damage.
    Bioessays. 1995 Jun;17(6):501-8 PMID: 7575491
  7. DNA damage responses: p53 induction, cell cycle perturbations, and apoptosis.
    Cold Spring Harb Symp Quant Biol. 1994;59:277-86 PMID: 7587079
  8. The transforming oncoproteins determine the mechanism by which p53 suppresses cell transformation: pRb-mediated growth arrest or apoptosis.
    Oncogene. 1995 Dec 21;11(12):2535-45 PMID: 8545110
  9. Regulatory interactions among E2Fs and cell cycle control proteins.
    Curr Top Microbiol Immunol. 1996;208:31-61 PMID: 8575212
  10. The SV40 large T antigen and adenovirus E1a oncoproteins interact with distinct isoforms of the transcriptional co-activator, p300.
    EMBO J. 1996 May 1;15(9):2236-48 PMID: 8641289
  11. Association of a cellular heat shock protein with simian virus 40 large T antigen in transformed cells.
    J Virol. 1989 Sep;63(9):3961-73 PMID: 2760986
  12. Cooperation of SV40 large T antigen and the cellular protein p53 in maintenance of cell transformation.
    Oncogene. 1989 Sep;4(9):1103-10 PMID: 2674854
  13. Polyoma small and middle T antigens and SV40 small t antigen form stable complexes with protein phosphatase 2A.
    Cell. 1990 Jan 12;60(1):167-76 PMID: 2153055
  14. Simian virus 40 large T antigen induces or activates a protein kinase which phosphorylates the transformation-associated protein p53.
    J Virol. 1990 Feb;64(2):672-9 PMID: 2153233
  15. Mutational analysis of simian virus 40 small-t antigen.
    J Virol. 1990 Jun;64(6):2895-900 PMID: 2159550
  16. The p53 protein and its interactions with the oncogene products of the small DNA tumor viruses.
    Virology. 1990 Aug;177(2):419-26 PMID: 2142553
  17. Association of simian virus 40 small-t antigen with the 61-kilodalton component of a cellular protein complex.
    J Virol. 1990 Nov;64(11):5649-51 PMID: 2170691
  18. Different tumor-derived p53 mutants exhibit distinct biological activities.
    Science. 1990 Oct 5;250(4977):113-6 PMID: 2218501
  19. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53.
    Cell. 1990 Dec 21;63(6):1129-36 PMID: 2175676
  20. Tumor suppressor genes.
    Cell. 1991 Jan 25;64(2):313-26 PMID: 1988150
  21. p53 mutations: gains or losses?
    J Cell Biochem. 1991 Jan;45(1):22-9 PMID: 2005181
  22. Control of protein phosphatase 2A by simian virus 40 small-t antigen.
    Mol Cell Biol. 1991 Apr;11(4):1988-95 PMID: 1706474
  23. Dephosphorylation of simian virus 40 large-T antigen and p53 protein by protein phosphatase 2A: inhibition by small-t antigen.
    Mol Cell Biol. 1991 Apr;11(4):1996-2003 PMID: 1848668
  24. Separation of lytic and transforming functions of the simian virus 40 A region: two mutants which are temperature sensitive for lytic functions have opposite effects on transformation.
    J Virol. 1981 May;38(2):518-28 PMID: 6264125
  25. Monoclonal antibodies specific for simian virus 40 tumor antigens.
    J Virol. 1981 Sep;39(3):861-9 PMID: 6169844
  26. Transformation by purified early genes of simian virus 40.
    Virology. 1984 Mar;133(2):341-53 PMID: 6324456
  27. Transgenic mice harboring SV40 T-antigen genes develop characteristic brain tumors.
    Cell. 1984 Jun;37(2):367-79 PMID: 6327063
  28. Structural prerequisites of simian virus 40 large T antigen for the maintenance of cell transformation.
    EMBO J. 1985 Nov;4(11):2941-7 PMID: 2998768
  29. Antigenic binding sites of monoclonal antibodies specific for simian virus 40 large T antigen.
    J Virol. 1986 Mar;57(3):1168-72 PMID: 2419584
  30. Large T antigens of simian virus 40 and polyomavirus efficiently establish primary fibroblasts.
    J Virol. 1986 Sep;59(3):746-50 PMID: 3016337
  31. Recombinant retroviruses encoding simian virus 40 large T antigen and polyomavirus large and middle T antigens.
    Mol Cell Biol. 1986 Apr;6(4):1204-17 PMID: 3023876
  32. Evidence for free and metabolically stable p53 protein in nuclear subfractions of simian virus 40-transformed cells.
    Mol Cell Biol. 1986 Jun;6(6):2233-40 PMID: 3023923
  33. Complete interaction of cellular 56,000- and 32,000-Mr proteins with simian virus 40 small-t antigen in productively infected cells.
    J Virol. 1987 Apr;61(4):1240-3 PMID: 3029419
  34. Two regions of the adenovirus early region 1A proteins are required for transformation.
    J Virol. 1988 Jan;62(1):257-65 PMID: 2960834
  35. Modulation of p53 protein expression during cellular transformation with simian virus 40.
    Mol Cell Biol. 1987 Dec;7(12):4453-63 PMID: 2830494
  36. Simian virus 40 large-T antigen expresses a biological activity complementary to the p300-associated transforming function of the adenovirus E1A gene products.
    Mol Cell Biol. 1991 Apr;11(4):2116-24 PMID: 1848672
  37. Mapping the transcriptional transactivation function of simian virus 40 large T antigen.
    J Virol. 1991 Jun;65(6):2778-90 PMID: 1851853
  38. Wild-type but not mutant p53 immunopurified proteins bind to sequences adjacent to the SV40 origin of replication.
    Cell. 1991 Jun 14;65(6):1083-91 PMID: 1646078
  39. Simian virus 40 large T antigen: the puzzle, the pieces, and the emerging picture.
    J Virol. 1992 Mar;66(3):1289-93 PMID: 1310750
  40. Involvement of simian virus 40 (SV40) small t antigen in trans activation of SV40 early and late promoters.
    J Virol. 1992 Mar;66(3):1489-94 PMID: 1310761
  41. Simian virus 40 large T antigen stably complexes with a 185-kilodalton host protein.
    J Virol. 1992 Mar;66(3):1752-60 PMID: 1310776
  42. Simian virus 40 small t antigen trans activates the adenovirus E2A promoter by using mechanisms distinct from those used by adenovirus E1A.
    J Virol. 1992 Apr;66(4):2551-5 PMID: 1532215
  43. Intracistronic complementation reveals a new function of SV40 T antigen that co-operates with Rb and p53 binding to stimulate DNA synthesis in quiescent cells.
    Oncogene. 1992 May;7(5):837-47 PMID: 1570154
  44. Inhibition of p53 transactivation required for transformation by adenovirus early 1B protein.
    Nature. 1992 May 7;357(6373):82-5 PMID: 1533443
  45. Species-specific phosphorylation of mouse and rat p53 in simian virus 40-transformed cells.
    J Virol. 1992 Jun;66(6):3846-59 PMID: 1316485
  46. Common and unique features of T antigens encoded by the polyomavirus group.
    J Virol. 1992 Jul;66(7):3979-85 PMID: 1318392
  47. Functional consequences of the interactions of the p53 tumor suppressor protein and SV40 large tumor antigen.
    Cold Spring Harb Symp Quant Biol. 1991;56:227-35 PMID: 1668081
  48. Cancer. p53, guardian of the genome.
    Nature. 1992 Jul 2;358(6381):15-6 PMID: 1614522
  49. Wild-type p53 activates transcription in vitro.
    Nature. 1992 Jul 2;358(6381):83-6 PMID: 1614538
  50. Correlation between the conformational phenotype of p53 and its subcellular location.
    Oncogene. 1992 Jul;7(7):1371-81 PMID: 1620550
  51. p53 function and dysfunction.
    Cell. 1992 Aug 21;70(4):523-6 PMID: 1505019
  52. Site-specific binding of wild-type p53 to cellular DNA is inhibited by SV40 T antigen and mutant p53.
    Genes Dev. 1992 Oct;6(10):1886-98 PMID: 1398068
  53. Identification of binding sites on the regulatory A subunit of protein phosphatase 2A for the catalytic C subunit and for tumor antigens of simian virus 40 and polyomavirus.
    Mol Cell Biol. 1992 Nov;12(11):4872-82 PMID: 1328865
  54. The growth-stimulatory effect of simian virus 40 T antigen requires the interaction of insulinlike growth factor 1 with its receptor.
    Mol Cell Biol. 1992 Nov;12(11):5069-77 PMID: 1406682
  55. E2F: a link between the Rb tumor suppressor protein and viral oncoproteins.
    Science. 1992 Oct 16;258(5081):424-9 PMID: 1411535
  56. The transcriptional transactivation function of wild-type p53 is inhibited by SV40 large T-antigen and by HPV-16 E6 oncoprotein.
    EMBO J. 1992 Dec;11(13):5013-20 PMID: 1464323
  57. Analysis of simian virus 40 small t antigen-induced progression of rat F111 cells minimally transformed by large T antigen.
    J Virol. 1993 Mar;67(3):1555-63 PMID: 8382310
  58. Abrogation of p53-mediated transactivation by SV40 large T antigen.
    Oncogene. 1993 Mar;8(3):543-8 PMID: 8382354
  59. A nonselective analysis of SV40 transformation of mouse 3T3 cells.
    Virology. 1974 Jun;59(2):477-89 PMID: 4364825
  60. I. In vitrol transformation of rat embryo cells: correlations with the known tumorigenic activities of chemicals in rodents.
    In Vitro. 1975 Mar-Apr;11(2):107-16 PMID: 50281
  61. Viable deletion mutants in the simian virus 40 early region.
    Proc Natl Acad Sci U S A. 1978 Sep;75(9):4455-9 PMID: 212752
  62. T antigen is bound to a host protein in SV40-transformed cells.
    Nature. 1979 Mar 15;278(5701):261-3 PMID: 218111
  63. Characterization of a 54K dalton cellular SV40 tumor antigen present in SV40-transformed cells and uninfected embryonal carcinoma cells.
    Cell. 1979 May;17(1):43-52 PMID: 222475
  64. Fluorescent phallotoxin, a tool for the visualization of cellular actin.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4498-502 PMID: 291981
  65. SV40 large tumor antigen forms a specific complex with the product of the retinoblastoma susceptibility gene.
    Cell. 1988 Jul 15;54(2):275-83 PMID: 2839300
  66. trans-activation of RNA polymerase II and III promoters by SV40 small t antigen.
    Cell. 1988 Dec 23;55(6):1171-7 PMID: 3203384
  67. Mutants with changes within or near a hydrophobic region of simian virus 40 large tumor antigen are defective for binding cellular protein p53.
    Virology. 1989 Jan;168(1):13-21 PMID: 2535898
  68. When the products of oncogenes and anti-oncogenes meet.
    Cell. 1989 Jan 13;56(1):1-3 PMID: 2642742
  69. Cellular targets for transformation by the adenovirus E1A proteins.
    Cell. 1989 Jan 13;56(1):67-75 PMID: 2521301
  70. The cellular 107K protein that binds to adenovirus E1A also associates with the large T antigens of SV40 and JC virus.
    Cell. 1989 Jul 28;58(2):249-55 PMID: 2546678
  71. An N-terminal transformation-governing sequence of SV40 large T antigen contributes to the binding of both p110Rb and a second cellular protein, p120.
    Cell. 1989 Jul 28;58(2):257-67 PMID: 2526683
  72. A cell culture model system for genetic analyses of the cell cycle by targeted homologous recombination.
    Oncogene. 1993 Apr;8(4):899-907 PMID: 8455944
  73. The p53 tumor suppressor protein: meeting review.
    Genes Dev. 1993 Apr;7(4):529-34 PMID: 8096197
  74. p53 is required for radiation-induced apoptosis in mouse thymocytes.
    Nature. 1993 Apr 29;362(6423):847-9 PMID: 8479522
  75. Gain of function mutations in p53.
    Nat Genet. 1993 May;4(1):42-6 PMID: 8099841
  76. The tumor suppressor genes.
    Annu Rev Biochem. 1993;62:623-51 PMID: 8394683
  77. The tumor suppressor p53.
    Biochim Biophys Acta. 1993 Aug 23;1155(2):181-205 PMID: 8357826
  78. Independent expression of the transforming amino-terminal domain of SV40 large I antigen from an alternatively spliced third SV40 early mRNA.
    EMBO J. 1993 Dec;12(12):4739-46 PMID: 8223482
  79. The amino-terminal functions of the simian virus 40 large T antigen are required to overcome wild-type p53-mediated growth arrest of cells.
    J Virol. 1994 Mar;68(3):1334-41 PMID: 8107198
  80. The role of the insulin-like growth factor I receptor in the transformation by simian virus 40 T antigen.
    Oncogene. 1994 Mar;9(3):825-31 PMID: 8108125
  81. Sequence-specific transcriptional activation is essential for growth suppression by p53.
    Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):1998-2002 PMID: 8134338
  82. Stabilization of the tumor suppressor p53 during cellular transformation by simian virus 40: influence of viral and cellular factors and biological consequences.
    J Virol. 1994 May;68(5):2869-78 PMID: 8151757
  83. DRTF1/E2F: an expanding family of heterodimeric transcription factors implicated in cell-cycle control.
    Trends Biochem Sci. 1994 Mar;19(3):108-14 PMID: 8203017
  84. Immortalization of BALB/c mouse embryo fibroblasts alters SV40 large T-antigen interactions with the tumor suppressor p53 and results in a reduced SV40 transformation-efficiency.
    Oncogene. 1994 Jul;9(7):1907-15 PMID: 8208537
  85. Transrepression of RNA polymerase II promoters by the simian virus 40 small t antigen.
    J Virol. 1994 Oct;68(10):6180-7 PMID: 8083958
  86. The yin and yang of p53 in cellular proliferation.
    Semin Cancer Biol. 1994 Jun;5(3):187-202 PMID: 7948947
  87. The tumor suppressor protein p53: a receptor to genotoxic stress that controls cell growth and survival.
    Curr Opin Oncol. 1995 Jan;7(1):76-82 PMID: 7696367
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1996-10-00
Pages
6781-9
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC190722
Subset
IM
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