Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review
  • Published:

Interaction of retinoblastoma protein family members with large T-antigen of primate polyomaviruses

Oncogene volume 25, pages 5286–5293 (2006)Cite this article

Abstract

The retinoblastoma gene product pRb and other members of the Rb family of pocket proteins have a central role in the regulation of cell cycle progression. Soon after its discovery, pRb was found to interact with the transforming oncoproteins of DNA tumor viruses and this led to rapid advances in our understanding of the mechanisms of viral transformation and cell cycle progression. DNA viruses of the polyomavirus family have small, circular, double-stranded DNA genomes contained within non-enveloped icosahedral capsids and are highly tumorigenic in experimental animals. At least three types of polyomavirus infect humans: JC virus (JCV), BK virus (BKV) and Simian Vacuolating virus-40. The early region of these viruses encodes the transforming proteins large T-antigen and small t-antigen, which are involved in viral replication and also promote transformation of cells in culture and oncogenesis in vivo. Binding of T-antigen to pRb promotes the activation of the E2F family of transcription factors, which induce the expression of cellular genes required for S phase. In the context of lytic infection, this cell cycle progression is necessary for viral replication because polyomaviruses rely on S phase-specific host factors for their DNA synthesis. In the context of cellular transformation and tumorigenesis, T-antigen/pRB interaction is an indispensable event.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  • Attwooll C, Denchi EL, Helin K . (2004). EMBO J 23: 4709–4716.

  • Bagchi S, Weinmann R, Raychaudhuri P . (1991). Cell 65: 1063–1072.

  • Bandara LR, Adamczewski JP, Hunt T, La Thangue NB . (1991). Nature 352: 249–251.

  • Bandara LR, La Thangue NB . (1991). Cell 65: 1053–1061.

  • Blais A, Dynlacht BD . (2004). Curr Opin Genet Dev 14: 527–532.

  • Bollag B, Prins C, Snyder EL, Frisque RJ . (2000). Virology 274: 165–178.

  • Bracken AP, Ciro M, Cocito A, Helin K . (2004). Trends Biocem Sci 29: 409–417.

  • Cantalupo P, Doering A, Sullivan CS, Pal A, Peden KW, Lewis AM et al. (2005). J Virol 79: 13094–13104.

  • Chellappan SP, Hiebert S, Mudryj M, Horowitz JM, Nevins JR . (1991). Cell 65: 1053–1061.

  • Chittenden T, Livingston DM, Kaelin WG . (1991). Cold Spring Harb Symp Quant Biol 56: 187–195.

  • Christensen JB, Imperiale MJ . (1995). J Virol 69: 3945–3948.

  • Cobrinik D . (2005). Oncogene 24: 2796–2809.

  • Cole CN . (1996) In: Fields BN, Knipe DM, Howley PM (eds). Fundamental Virology, 3rd edn, Lippincott, Williams & Wilkins: Philadelphia. pp 917–946.

    Google Scholar 

  • Corallini A, Tognon M, Negrini M, Barbanti-Brodano G . (2001) In: Khalili K, Stoner GL (eds). Human Polyomaviruses: Molecular and Clinical Perspective. Wiley-Liss Inc.: New York. pp 431–460.

    Book  Google Scholar 

  • Courtneidge SA, Smith AE . (1983). Nature 303: 435–439.

  • DeCaprio JA, Ludlow JW, Figge J, Shew JY, Huang CM, Lee WH et al. (1988). Cell 54: 275–283.

  • Del Valle L, Baehring J, Lorenzana C, Giordano A, Khalili K, Croul S . (2001a). Mol Pathol 54: 331–337.

  • Del Valle L, Gordon J, Ferrante P, Khalili K . (2001b) In: Khalili K, Stoner GL (eds). Human Polyomaviruses: Molecular and Clinical Perspective. Wiley-Liss Inc.: New York. pp 409–430.

    Book  Google Scholar 

  • Dimova DK, Dyson NJ . (2005). Oncogene 24: 2810–2826.

  • Dyson N, Bernards R, Friend SH, Gooding LR, Hassell JA, Major EO et al. (1990). J Virol 64: 1353–1356.

  • Dyson N, Buchkovich K, Whyte P, Harlow E . 1989. Cell 58: 249–255.

  • Ewen ME, Ludlow JW, Marsilio E, DeCaprio JA, Millikan RC, Cheng SH et al. (1989). Cell 58: 257–267.

  • Ewen ME, Xing YG, Lawrence JB, Livingston DM . (1991). Cell 66: 1155–1164.

  • Friend SH, Bernards R, Rogelj S, Weinberg RA, Rapaport JM, Albert DM et al. (1986). Nature 323: 643–646.

  • Friend SH, Horowitz JM, Gerber MR, Wang XF, Bogenmann E, Li FP et al. (1987). Proc Natl Acad Sci USA 84: 9059–9063.

  • Frisque RJ . (2001). J Neurovirol 7: 293–297.

  • Frisque RJ, Bam R, Tyagarajan SK, Tevethia MJ . (2005). J Neurovirol 11(Suppl 2): 65.

  • Frisque RJ, Bollag B, Tyagarajan SK, Kilpatrick LH . (2003). J Neurovirol 9(Suppl 1): 15–20.

  • Fung YK, Murphree AL, T'Ang A, Qian J, Hinrichs SH, Benedict WF . (1987). Science 236: 1657–1661.

  • Garcea RL, Imperiale MJ . (2003). J Virol 77: 5039–5045.

  • Hannon GJ, Demetrick D, Beach D . (1993). Genes Dev 7: 2378–2391.

  • Harlow E, Whyte P, Franza Jr BR, Schley C . (1986). Mol Cell Biol 6: 1579–1589.

  • Harris KF, Christensen JB, Imperiale MJ . (1996). J Virol 70: 2378–2386.

  • Harris KF, Christensen JB, Radany EH, Imperiale MJ . (1998). Mol Cell Biol 18: 1746–1756.

  • Hirsch HH . (2005). Clin Infect Dis 41: 354–360.

  • Howard CM, Claudio PP, De Luca A, Stiegler P, Jori FP, Safdar NM et al. (2000). Cancer Res 60: 2737–2744.

  • Howard CM, Claudio PP, Gallia GL, Gordon J, Giordano GG, Hauck WW et al. (1998). J Natl Cancer Inst 90: 1451–1460.

  • Hu QJ, Dyson N, Harlow E . (1990). EMBO J 9: 1147–1155.

  • Huang S, Wang NP, Tseng BY, Lee WH, Lee EH . (1990). EMBO J 9: 1815–1822.

  • Kelley WL, Georgopoulos C . (1997). Mol Microbiol 25: 913–931.

  • Khalili K, Gordon J, White MK . (2005) In: Ahsan N (ed). Polyomaviruses and Human Diseases. Landes Bioscience: Georgetown, TX, pp 21.1–21.14.

    Google Scholar 

  • Kim HY, Ahn BY, Cho Y . (2001). EMBO J 20: 295–304.

  • Kovesdi I, Reichel R, Nevins JR . (1987). Proc Natl Acad Sci USA 84: 2180–2184.

  • Krynska B, Del Valle L, Gordon J, Otte J, Croul S, Khalili K . (2000). Virology 274: 65–74.

  • Krynska B, Gordon J, Otte J, Franks R, Knobler R, DeLuca A et al. (1997). J Cell Biochem 67: 223–230.

  • Lane DP, Crawford LV . (1979). Nature 278: 261–263.

  • Lee WH, Bookstein R, Hong F, Young LJ, Shew JY, Lee EY . (1987a). Science 235: 1394–1399.

  • Lee WH, Shew JY, Hong FD, Sery TW, Donoso LA, Young LJ et al. (1987b). Nature 329: 642–645.

  • Li Y, Graham C, Lacy S, Duncan AM, Whyte P . (1993). Genes Dev 7: 2366–2377.

  • Lin JY, DeCaprio JA . (2003). J Biol Chem 278: 46482–46487.

  • Ludlow JW . (1993). FASEB J 7: 866–871.

  • Ludlow JW . (1996). J Virol Methods 59: 105–112.

  • Ludlow JW, DeCaprio JA, Huang CM, Lee WH, Paucha E, Livingston DM . (1989). Cell 56: 57–65.

  • Ludlow JW, Shon J, Pipas JM, Livingston DM, DeCaprio JA . (1990). Cell 60: 387–396.

  • Mandl C, Walker DL, Frisque RJ . (1987). J Virol 61: 755–763.

  • Mayol X, Grana X, Baldi A, Sang N, Hu Q, Giordano A . (1993). Oncogene 8: 2561–2566.

  • Nevins JR, Chellappan SP, Mudryj M, Hiebert S, Devoto S, Horowitz J et al. (1991). Cold Spring Harb Symp Quant Biol 56: 157–162.

  • O'Neill FJ, Frisque RJ, Xu X, Hu YX, Carney H . (1995). Oncogene 10: 1131–1139.

  • Pagnani M, Corallini A, Caputo A, Altavilla G, Selvatici R, Catozzi L et al. (1988). Int J Cancer 42: 405–413.

  • Pipas JM . (1992). J Virol 66: 3979–3985.

  • Prins C, Frisque RJ . (2001). J Neurovirol 7: 250–264.

  • Raychaudhuri P, Bagchi S, Devoto SH, Kraus VB, Moran E, Nevins JR . (1991). Genes Dev 5: 1200–1211.

  • Reichel R, Kovesdi I, Nevins JR . (1987). Cell 48: 501–506.

  • Saenz Robles MT, Symonds H, Chen J, Van Dyke T . (1994). Mol Cell Biol 14: 2686–2698.

  • Stubdal H, Zalvide J, Campbell KS, Schweitzer C, Roberts TM, DeCaprio JA . (1997). Mol Cell Biol 17: 4979–4990.

  • Stubdal H, Zalvide J, DeCaprio JA . (1996). J Virol 70: 2781–2788.

  • Sullivan CS, Baker AE, Pipas JM . (2004). Virology 320: 218–228.

  • Sullivan CS, Cantalupo P, Pipas JM . (2000a). Mol Cell Biol 20: 6233–6243.

  • Sullivan CS, Pipas JM . (2002). Microbiol Mol Biol Rev 66: 179–202.

  • Sullivan CS, Tremblay JD, Fewell SW, Lewis JA, Brodsky JL, Pipas JM . (2000b). Mol Cell Biol 20: 5749–5757.

  • Tavis JE, Trowbridge PW, Frisque RJ . (1994). Virology 199: 384–392.

  • Tevethia MJ, Lacko HA, Kierstead TD, Thompson DL . (1997). J Virol 71: 1888–1896.

  • Tognon M, Corallini A, Martini F, Negrini M, Barbanti-Brodano G . (2003). Oncogene 22: 5192–5200.

  • Trifillis P, Picardi J, Awline JC . (1990). J Virol 64: 1345–1347.

  • Trowbridge PW, Frisque RJ . (1995). J Neurovirol 1: 195–206.

  • Tyagarajan SK, Frisque RJ . (2005). J Neurovirol 11(Suppl 2): 43.

  • Weinberg RA . (1995). Cell 81: 323–330.

  • Weinberg RA . (1996). Cell 85: 457–459.

  • White MK, Gordon J, Reiss K, Del Valle L, Croul S et al. (2005). Brain Res Brain Res Rev 50: 69–85.

  • White MK, Khalili K . (2004a). Virology 324: 1–16.

  • White MK, Khalili K . (2004b). Gene Ther Mol Biol 8: 19–30.

  • White MK, Khalili K . (2005). Eur J Cancer 41: 2537–2548.

  • Whyte P, Buchkovich KJ, Horowitz JM, Friend SH, Raybuck M, Weinberg RA et al. (1988a). Nature 334: 124–129.

  • Whyte P, Ruley HE, Harlow E . (1988b). J Virol 62: 257–265.

  • Whyte P, Williamson NM, Harlow E . (1989). Cell 56: 67–75.

  • Wolf DA, Hermking H, Albert T, Herzinger T, Kind P, Eick D . (1995). Oncogene 10: 2067–2078.

  • Yee SP, Branton PE . (1985). Virology 147: 142–153.

  • Zalvide J, Decaprio JA . (1995). Mol Cell Biol 15: 5800–5810.

  • Zalvide J, Stubdal H, DeCaprio JA . (1998). Mol Cell Biol 18: 1408–1415.

Download references

Acknowledgements

We thank past and present members of the Center for Neurovirology for their insightful discussion and sharing of ideas and reagents, and Dr Luis Del Valle for providing immunohistochemistry images. We also thank C Schriver for editorial assistance. This work was supported by grants awarded by the National Institute of Health to KK.

Author information

Authors and Affiliations

  1. Department of Neuroscience, Center for Neurovirology, Temple University School of Medicine, Philadelphia, PA, USA

    M K White & K Khalili

Authors
  1. M K White
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K Khalili
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K Khalili.

Rights and permissions

Reprints and permissions

About this article

Cite this article

White, M., Khalili, K. Interaction of retinoblastoma protein family members with large T-antigen of primate polyomaviruses. Oncogene 25, 5286–5293 (2006). https://doi.org/10.1038/sj.onc.1209618

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.onc.1209618

Keywords

This article is cited by

Search

Advanced search

Quick links