Advances in Virology
Volume 2010 (2010), Article ID 368068, 9 pages
http://dx.doi.org/10.1155/2010/368068
Review Article
Novel Roles of the Picornaviral 3D Polymerase in Viral Pathogenesis
1Department of Neurology, Mayo Clinic, Rochester, MN 55905, USA
2Department of Immunology, Mayo Clinic, Rochester, MN 55905, USA
Received 25 March 2010; Accepted 26 May 2010
Academic Editor: George N. Pavlakis
Copyright © 2010 Jason Kerkvliet et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Linked References
- R. Franklin and D. Baltimore, “Patterns of macromolecular synthesis in normal and virus-infected mammalian cells,” Cold Spring Harbor Symposia on Quantitative Biology, vol. 27, pp. 175–198, 1962. View at Google Scholar
- L. A. Caliguiri and I. Tamm, “Membranous structures associated with translation and transcription of poliovirus RNA,” Science, vol. 166, no. 3907, pp. 885–886, 1969. View at Google Scholar · View at Scopus
- K. L. Neufeld, O. C. Richards, and E. Ehrenfeld, “Purification, characterization, and comparison of poliovirus RNA polymerase from native and recombinant sources,” Journal of Biological Chemistry, vol. 266, no. 35, pp. 24212–24219, 1991. View at Google Scholar · View at Scopus
- S. J. Plotch, O. Palant, and Y. Gluzman, “Purification and properties of poliovirus RNA polymerase expressed in Escherichia coli,” Journal of Virology, vol. 63, no. 1, pp. 216–225, 1989. View at Google Scholar · View at Scopus
- J. Kerkvliet, L. Zoecklein, L. Papke et al., “Transgenic expression of the 3D polymerase inhibits Theiler's virus infection and demyelination,” Journal of Virology, vol. 83, no. 23, pp. 12279–12289, 2009. View at Publisher · View at Google Scholar · View at Scopus
- S. F. Altschul, T. L. Madden, A. A. Schäffer et al., “Gapped BLAST and PSI-BLAST: a new generation of protein database search programs,” Nucleic Acids Research, vol. 25, no. 17, pp. 3389–3402, 1997. View at Publisher · View at Google Scholar · View at Scopus
- S. F. Altschul, J. C. Wootton, E. M. Gertz et al., “Protein database searches using compositionally adjusted substitution matrices,” FEBS Journal, vol. 272, no. 20, pp. 5101–5109, 2005. View at Publisher · View at Google Scholar · View at Scopus
- C. Ferrer-Orta, A. Arias, R. Perez-Luque, C. Escarmís, E. Domingo, and N. Verdaguer, “Structure of foot-and-mouth disease virus RNA-dependent RNA polymerase and its complex with a template-primer RNA,” Journal of Biological Chemistry, vol. 279, no. 45, pp. 47212–47221, 2004. View at Publisher · View at Google Scholar · View at Scopus
- J. L. Hansen, A. M. Long, and S. C. Schultz, “Structure of the RNA-dependent RNA polymerase of poliovirus,” Structure, vol. 5, no. 8, pp. 1109–1122, 1997. View at Google Scholar · View at Scopus
- R. A. Love, K. A. Maegley, X. Yu et al., “The crystal structure of the RNA-dependent RNA polymerase from human rhinovirus: a dual function target for common cold antiviral therapy,” Structure, vol. 12, no. 8, pp. 1533–1544, 2004. View at Publisher · View at Google Scholar · View at Scopus
- A. A. Thompson and O. B. Peersen, “Structural basis for proteolysis-dependent activation of the poliovirus RNA-dependent RNA polymerase,” EMBO Journal, vol. 23, no. 17, pp. 3462–3471, 2004. View at Publisher · View at Google Scholar · View at Scopus
- J. A. Bruenn, “A structural and primary sequence comparison of the viral RNA-dependent RNA polymerases,” Nucleic Acids Research, vol. 31, no. 7, pp. 1821–1829, 2003. View at Publisher · View at Google Scholar · View at Scopus
- J. Lescar and B. Canard, “RNA-dependent RNA polymerases from flaviviruses and Picornaviridae,” Current Opinion in Structural Biology, vol. 19, no. 6, pp. 759–767, 2009. View at Publisher · View at Google Scholar · View at Scopus
- E. K. O'Reilly and C. C. Kao, “Analysis of RNA-dependent RNA polymerase structure and function as guided by known polymerase structures and computer predictions of secondary structure,” Virology, vol. 252, no. 2, pp. 287–303, 1998. View at Publisher · View at Google Scholar · View at Scopus
- J. F. Spagnolo, E. Rossignol, E. Bullitt, and K. Kirkegaard, “Enzymatic and nonenzymatic functions of viral RNA-dependent RNA polymerases within oligomeric arrays,” RNA, vol. 16, no. 2, pp. 382–393, 2010. View at Publisher · View at Google Scholar · View at Scopus
- G. Campagnola, M. Weygandt, K. Scoggin, and O. Peersen, “Crystal structure of coxsackievirus B3 highlights the functional importance of residue 5 in picornavirus polymerases,” Journal of Virology, vol. 82, no. 19, pp. 9458–9464, 2008. View at Publisher · View at Google Scholar · View at Scopus
- J. D. Pata, S. C. Schultz, and K. Kirkegaard, “Functional oligomerization of poliovirus RNA-dependent RNA polymerase,” RNA, vol. 1, no. 5, pp. 466–477, 1995. View at Google Scholar · View at Scopus
- J. M. Lyle, E. Bullitt, K. Bienz, and K. Kirkegaard, “Visualization and functional analysis of RNA-dependent RNA polymerase lattices,” Science, vol. 296, no. 5576, pp. 2218–2222, 2002. View at Publisher · View at Google Scholar · View at Scopus
- H. B. Pathak, S. K. B. Ghosh, A. W. Roberts et al., “Structure-function relationships of the RNA-dependent RNA polymerase from poliovirus (): a surface of the primary oligomerization domain functions in capsid precursor processing and VPg uridylylation,” Journal of Biological Chemistry, vol. 277, no. 35, pp. 31551–31562, 2002. View at Publisher · View at Google Scholar · View at Scopus
- S. D. Hobson, E. S. Rosenblum, O. C. Richards, K. Richmond, K. Kirkegaard, and S. C. Schultz, “Oligomeric structures of poliovirus polymerase are important for function,” EMBO Journal, vol. 20, no. 5, pp. 1153–1163, 2001. View at Publisher · View at Google Scholar · View at Scopus
- K. Fujita, S. S. Krishnakumar, D. Franco, A. V. Paul, E. London, and E. Wimmer, “Membrane topography of the hydrophobic anchor sequence of poliovirus 3A and 3AB proteins and the functional effect of 3A/3AB membrane association upon RNA replication,” Biochemistry, vol. 46, no. 17, pp. 5185–5199, 2007. View at Publisher · View at Google Scholar · View at Scopus
- A. Gruez, B. Selisko, M. Roberts et al., “The crystal structure of coxsackievirus B3 RNA-dependent RNA polymerase in complex with its protein primer VPg confirms the existence of a second VPg binding site on Picornaviridae polymerases,” Journal of Virology, vol. 82, no. 19, pp. 9577–9590, 2008. View at Publisher · View at Google Scholar · View at Scopus
- D. M. Strauss and D. S. Wuttke, “Characterization of protein-protein interactions critical for poliovirus replication: analysis of 3AB and VPg binding to the RNA-dependent RNA polymerase,” Journal of Virology, vol. 81, no. 12, pp. 6369–6378, 2007. View at Publisher · View at Google Scholar · View at Scopus
- H. B. Pathak, J. J. Arnold, P. N. Wiegand, M. R. S. Hargittai, and C. E. Cameron, “Picornavirus genome replication: assembly and organization of the VPg uridylylation ribonucleoprotein (initiation) complex,” Journal of Biological Chemistry, vol. 282, no. 22, pp. 16202–16213, 2007. View at Publisher · View at Google Scholar · View at Scopus
- M. Shen, Z. J. Reitman, Y. Zhao et al., “Picornavirus genome replication: identification of the surface of the poliovirus (PV) 3C dimer that interacts with PV during VPg uridylylation and construction of a structural model for the PV 3C2- complex,” Journal of Biological Chemistry, vol. 283, no. 2, pp. 875–888, 2008. View at Publisher · View at Google Scholar · View at Scopus
- J. Lama, A. V. Paul, K. S. Harris, and E. Wimmer, “Properties of purified recombinant poliovirus protein 3AB as substrate for viral proteinases and as co-factor for RNA polymerase ,” Journal of Biological Chemistry, vol. 269, no. 1, pp. 66–70, 1994. View at Google Scholar · View at Scopus
- H. Oh, H. B. Pathak, I. G. Goodfellow, J. J. Arnold, and C. E. Cameron, “Insight into poliovirus genome replication and encapsidation obtained from studies of 3B-3C cleavage site mutants,” Journal of Virology, vol. 83, no. 18, pp. 9370–9387, 2009. View at Publisher · View at Google Scholar · View at Scopus
- H. B. Pathak, H. Oh, I. G. Goodfellow, J. J. Arnold, and C. E. Cameron, “Picornavirus genome replication: roles of precursor proteins and rate-limiting steps in oriI-dependent VPg uridylylation,” Journal of Biological Chemistry, vol. 283, no. 45, pp. 30677–30688, 2008. View at Publisher · View at Google Scholar · View at Scopus
- O. C. Richards, J. F. Spagnolo, J. M. Lyle, S. E. Vleck, R. D. Kuchta, and K. Kirkegaard, “Intramolecular and intermolecular uridylylation by poliovirus RNA-dependent RNA polymerase,” Journal of Virology, vol. 80, no. 15, pp. 7405–7415, 2006. View at Publisher · View at Google Scholar · View at Scopus
- T. C. Appleby, H. Luecke, J. Shim et al., “Crystal structure of complete rhinovirus RNA polymerase suggests front loading of protein primer,” Journal of Virology, vol. 79, no. 1, pp. 277–288, 2005. View at Publisher · View at Google Scholar · View at Scopus
- A. V. Paul, J. Yin, J. Mugavero, E. Rieder, Y. Liu, and E. Wimmer, “A “slide-back” mechanism for the initiation of protein-primed RNA synthesis by the RNA polymerase of poliovirus,” Journal of Biological Chemistry, vol. 278, no. 45, pp. 43951–43960, 2003. View at Publisher · View at Google Scholar · View at Scopus
- B. J. Morasco, N. Sharma, J. Parilla, and J. B. Flanegan, “Poliovirus cre (2C)-dependent synthesis of VPgpUpU is required for positive- but not negative-strand RNA synthesis,” Journal of Virology, vol. 77, no. 9, pp. 5136–5144, 2003. View at Publisher · View at Google Scholar · View at Scopus
- K. E. Murray and D. J. Barton, “Poliovirus CRE-dependent VPg uridylylation is required for positive-strand RNA synthesis but not for negative-strand RNA synthesis,” Journal of Virology, vol. 77, no. 8, pp. 4739–4750, 2003. View at Publisher · View at Google Scholar · View at Scopus
- J. Chen, J. B. Anderson, C. DeWeese-Scott et al., “MMDB: entrez's 3D-structure database,” Nucleic Acids Research, vol. 31, no. 1, pp. 474–477, 2003. View at Publisher · View at Google Scholar · View at Scopus
- Y. Wang, K. J. Addess, J. Chen et al., “MMDB: annotating protein sequences with Entrez's 3D-structure database,” Nucleic Acids Research, vol. 35, no. 1, pp. D298–D300, 2007. View at Publisher · View at Google Scholar · View at Scopus
- A. Azoulay, M. Brahic, and J.-F. Bureau, “FVB mice transgenic for the H-2Db gene become resistant to persistent infection by Theiler's virus,” Journal of Virology, vol. 68, no. 6, pp. 4049–4052, 1994. View at Google Scholar · View at Scopus
- A. K. Patick, L. R. Pease, C. S. David, and M. Rodriguez, “Major histocompatibility complex-conferred resistance to Theiler's virus-induced demyelinating disease is inherited as a dominant trait in B10 congenic mice,” Journal of Virology, vol. 64, no. 11, pp. 5570–5576, 1990. View at Google Scholar · View at Scopus
- M. Rodriguez and C. S. David, “H-2 Dd transgene suppresses Theiler's virus-induced demyelination in susceptible strains of mice,” Journal of neurovirology, vol. 1, no. 1, pp. 111–117, 1995. View at Google Scholar · View at Scopus
- L. Fiette, C. Aubert, M. Brahic, and C. P. Rossi, “Theiler's virus infection of β2-microglobulin-deficient mice,” Journal of Virology, vol. 67, no. 1, pp. 589–592, 1993. View at Google Scholar · View at Scopus
- P. D. Murray, K. D. Pavelko, J. Leibowitz, X. Lin, and M. Rodriguez, “ and T cells make discrete contributions to demyelination and neurologic disease in a viral model of multiple sclerosis,” Journal of Virology, vol. 72, no. 9, pp. 7320–7329, 1998. View at Google Scholar · View at Scopus
- M. Rodriguez, A. J. Dunkel, R. L. Thiemann, J. Leibowitz, M. Zijlstra, and R. Jaenisch, “Abrogation of resistance to Theiler's virus-induced demyelination in H-2b mice deficient in β2-microglobulin,” Journal of Immunology, vol. 151, no. 1, pp. 266–276, 1993. View at Google Scholar · View at Scopus
- X. Lin, M. K. Njenga, A. J. Johnson et al., “Transgenic expression of Theiler's murine encephalomyelitis virus genes in H-2b mice inhibits resistance to virus-induced demyelination,” Journal of Virology, vol. 76, no. 15, pp. 7799–7811, 2002. View at Publisher · View at Google Scholar · View at Scopus
- Y. V. Mendez-Fernandez, A. J. Johnson, M. Rodriguez, and L. R. Pease, “Clearance of Theiler's virus infection depends on the ability to generate a T cell response against a single immunodominant viral peptide,” European Journal of Immunology, vol. 33, no. 9, pp. 2501–2510, 2003. View at Publisher · View at Google Scholar · View at Scopus
- S. D. Miller, R. J. Clatch, D. C. Pevear, J. Trotter, and H. Lipton, “Class II-restricted T cell responses in Theiler's murine encephalomyelitis virus (TMEV)-induced demyelinating disease. I. Cross-specificity among TMEV substrains and related picornaviruses, but not myelin proteins,” Journal of Immunology, vol. 138, no. 11, pp. 3776–3784, 1987. View at Google Scholar · View at Scopus
- Y.-H. Jin, B. Kang, and B. S. Kim, “Theiler's virus infection induces a predominant pathogenic T cell response to RNA polymerase in susceptible SJL/J mice,” Journal of Virology, vol. 83, no. 21, pp. 10981–10992, 2009. View at Publisher · View at Google Scholar · View at Scopus
- A. V. Paul, X. Cao, K. S. Harris, J. Lama, and E. Wimmer, “Studies with poliovirus polymerase . Stimulation of poly(U) synthesis in vitro by purified poliovirus protein 3AB,” Journal of Biological Chemistry, vol. 269, no. 46, pp. 29173–29181, 1994. View at Google Scholar · View at Scopus
- O. C. Richards and E. Ehrenfeld, “Effects of poliovirus 3AB protein on 3D polymerase-catalyzed reaction,” Journal of Biological Chemistry, vol. 273, no. 21, pp. 12832–12840, 1998. View at Publisher · View at Google Scholar · View at Scopus
- V. Rodriguez-Wells, S. J. Plotch, and J. J. DeStefano, “Primer-dependent synthesis by poliovirus RNA-dependent RNA polymerase (),” Nucleic Acids Research, vol. 29, no. 13, pp. 2715–2724, 2001. View at Google Scholar · View at Scopus
- L. Malmgaard, “Induction and regulation of IFNs during viral infections,” Journal of Interferon and Cytokine Research, vol. 24, no. 8, pp. 439–454, 2004. View at Publisher · View at Google Scholar · View at Scopus
- C. E. Samuel, “Antiviral actions of interferons,” Clinical Microbiology Reviews, vol. 14, no. 4, pp. 778–809, 2001. View at Publisher · View at Google Scholar · View at Scopus
- S. P. Amineva, A. G. Aminev, A. C. Palmenberg, and J. E. Gern, “Rhinovirus 3C protease precursors 3CD and 3C localize to the nuclei of infected cells,” Journal of General Virology, vol. 85, no. 10, pp. 2969–2979, 2004. View at Publisher · View at Google Scholar · View at Scopus
- R. Sharma, S. Raychaudhuri, and A. Dasgupta, “Nuclear entry of poliovirus protease-polymerase precursor 3CD: implications for host cell transcription shut-off,” Virology, vol. 320, no. 2, pp. 195–205, 2004. View at Publisher · View at Google Scholar · View at Scopus