Abstract
Our aim was to search for new cellular binding partners for the E6 and E7 oncogenes of beta human papillomaviruses (HPV), whose direct role in skin carcinogenesis has not been thoroughly investigated. By employing glutathione S-transferase pulldown and coimmunoprecipitation, we identified nuclear myosin 1c as a binding partner of HPV 8 E7 protein. As nuclear myosin 1c is an essential component of the RNA polymerase I transcription complex, we studied the effects of HPV 8 E7 protein expression on ribosomal RNA (rRNA) expression. Here we show that the activity of RNA polymerase I is decreased and that pre-rRNA expression is consequently reduced due to HPV 8 E7 expression. However, the expression levels of mature cytoplasmic 18S and 28S rRNA are retained. We propose that by relieving their resources from the energy-consuming process of rRNA transcription, HPV 8 E7 expressing cells might support more efficient virus replication in the differentiating epithelium.
Similar content being viewed by others
References
S. Smola, Adv. Exp. Med. Biol. 810, 192–207 (2014)
J. Haedicke, T. Iftner, Radiother. Oncol. 108, 397–402 (2013)
K.D. Quint, R.E. Genders, M.N. de Koning, C. Borgogna, M. Gariglio, J.N. Bouwes Bavinck, J. Doorbar, M.C. Feltkamp, J. Pathol. 235, 342–354 (2015)
M. Hufbauer, D. Lazić, B. Akgül, J.L. Brandsma, H. Pfister, S.J. Weissenborn, Virology 403, 128–136 (2010)
A. Schmitt, J.B. Harry, B. Rapp, F.O. Wettstein, T. Iftner, J. Virol. 68, 7051–7059 (1994)
B. Akgül, L. Ghali, D. Davies, H. Pfister, I.M. Leigh, A. Storey, Exp. Dermatol. 16, 590–599 (2007)
R. Ghittoni, R. Accardi, U. Hasan, T. Gheit, B. Sylla, M. Tommasino, Virus Genes 40, 1–13 (2010)
B. Zhang, W. Chen, A. Roman, Proc. Natl. Acad. Sci. USA 103, 437–442 (2006)
C. Enzenauer, G. Mengus, A. Lavigne, I. Davidson, H. Pfister, M. May, Intervirology 41, 80–90 (1998)
M.J. Tan, E.A. White, M.E. Sowa, J.W. Harper, J.C. Aster, P.M. Howley, Proc. Natl. Acad. Sci. USA 109, E1473–E1480 (2012)
N. Brimer, C. Lyons, A.E. Wallberg, S.B.V. Pol, Oncogene 31, 4639–4646 (2012)
E. Sankovski, A. Männik, J. Geimanen, E. Ustav, M. Ustav, J. Virol. 88, 961–973 (2014)
I. Grummt, R. Voit, Cell Cycle 9, 225–226 (2010)
C. Mayer, H. Bierhoff, I. Grummt, Genes Dev. 19, 933–941 (2005)
S. Hoppe, H. Bierhoff, I. Cado, A. Weber, M. Tiebe, I. Grummt, R. Voit, Proc. Natl. Acad. Sci. USA 106, 17781–17786 (2009)
J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.Y. Tinevez, D.J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, A. Cardona, Nat. Methods 9, 676–682 (2012)
J. Yue, R. Shukla, R. Accardi, I. Zanella-Cleon, M. Siouda, M.P. Cros, V. Krutovskikh, I. Hussain, Y. Niu, S. Hu, M. Becchi, P. Jurdic, M. Tommasino, B.S. Sylla, J. Virol. 85, 8477–8494 (2011)
P. Percipalle, N. Fomproix, E. Cavellán, R. Voit, G. Reimer, T. Krüger, J. Thyberg, U. Scheer, I. Grummt, A.K. Farrants, EMBO Rep. 7, 525–530 (2006)
N. Fomproix, P. Percipalle, Exp. Cell Res. 294, 140–148 (2004)
V.V. Philimonenko, J. Zhao, S. Iben, H. Dingová, K. Kyselá, M. Kahle, H. Zentgraf, W.A. Hofmann, P. de Lanerolle, P. Hozák, I. Grummt, Nat. Cell Biol. 6, 1165–1172 (2004)
W.A. Hofmann, T. Johnson, M. Klapczynski, J.L. Fan, P. de Lanerolle, Biochem. Cell Biol. 84, 418–426 (2006)
J. Ye, J. Zhao, U. Hoffmann-Rohrer, I. Grummt, Genes Dev. 22, 322–330 (2008)
B. Akgül, P. Zigrino, D. Frith, S. Hanrahan, A. Storey, Virology 386, 1–5 (2009)
E.A. White, M.E. Sowa, M.J.A. Tan, S. Jeudy, S.D. Hayes, S. Santha, K. Münger, J.W. Harper, P.M. Howley, Proc. Natl. Acad. Sci. USA 109, E260–E267 (2012)
I. Dichamp, P. Séité, G. Agius, A. Barbarin, A. Beby-Defaux, PLoS ONE (2014). doi:10.1371/journal.pone.0096136
B. Almuzzaini, A.A. Sarshad, A.K.O. Farrants, P. Percipalle, BMC Biol. (2015). doi:10.1186/s12915-015-0147-z
T. Steinberg, N. Ziegler, A. Alonso, A. Kohl, E. Müssig, S. Proksch, S. Schulz, P. Tomakidi, Cell Calcium 49, 259–271 (2011)
J. Houseley, D. Tollervey, Cell 136, 763–776 (2009)
L.X.T. Nguyen, A. Raval, J.S. Garcia, B.S. Mitchell, Cell Physiol. 230, 1181–1188 (2015)
S.A. Liebhaber, S. Wolf, D. Schlessinger, Cell 13, 121–127 (1978)
S. Bergner, G. Halec, M. Schmitt, F. Aubin, A. Alonso, E. Auvinen, Cells Tissues Organs 201, 97–108 (2016)
K. Münger, J.R. Basile, S. Duensing, A. Eichten, S.L. Gonzalez, M. Grace, V.L. Zacny, Oncogene 20, 7888–7898 (2001)
S. Heuser, M. Hufbauer, J. Steiger, J. Marshall, A. Sterner-Kock, C. Mauch, P. Zigrino, B. Akgül, Oncogene 35, 4529–4539 (2016)
Acknowledgements
Funding for this work was provided by Canceropole du Grand-Est, France, Deutsches Krebsforschungszentrum, Heidelberg, Germany, and the Finnish Society of Sciences and Letters. Dr. Herbert Pfister (University of Cologne, Germany) is greatly acknowledged for the cloned sequences of HPV 5 and HPV 8.
Author information
Authors and Affiliations
Contributions
All authors have contributed to the design (EO, RV, FA, AA, EA), experimentation (EO, ER, FA), result interpretation (EO, ER, RV, FA, AA, EA) and/or writing (EO, ER, RV, FA, AA, EA) of this work.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Research involving human participants and/or animals
The research presented here does not involve human participants of experimentation on animals.
Informed consent
Informed consent is not required because no human participants were involved in the work.
Additional information
Edited by Hartmut Hengel.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Oswald, E., Reinz, E., Voit, R. et al. Human papillomavirus type 8 E7 protein binds nuclear myosin 1c and downregulates the expression of pre-rRNA. Virus Genes 53, 807–813 (2017). https://doi.org/10.1007/s11262-017-1491-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11262-017-1491-6