Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014 (2014), Article ID 430508, 13 pages
http://dx.doi.org/10.1155/2014/430508
Research Article

Differential Host Cell Gene Expression and Regulation of Cell Cycle Progression by Nonstructural Protein 11 of Porcine Reproductive and Respiratory Syndrome Virus

1Department of Pathobiology, University of Illinois at Urbana-Champaign, 2001 South Lincoln Avenue, Urbana, IL 61802, USA
2Department of Pathobiology, University of Pennsylvania, 380 South University Avenue, Philadelphia, PA 19104, USA
3Department of Cell and Developmental Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA

Received 17 October 2013; Accepted 7 January 2014; Published 26 February 2014

Academic Editor: Raymond Rowland

Copyright © 2014 Yan Sun 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

  1. E. J. Neumann, J. B. Kliebenstein, C. D. Johnson et al., “Assessment of the economic impact of porcine reproductive and respiratory syndrome on swine production in the United States,” Journal of the American Veterinary Medical Association, vol. 227, no. 3, pp. 385–392, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. A. M. Q. King, M. J. Adams, E. B. Carstens, and E. J. Lefkovitz, Virus Taxonomy Ninth International Report of the International Committee on Taxonomy of Viruses, Elsevier Academic Press, 2012.
  3. K. K. Conzelmann, N. Visser, P. van Woensel, and H. J. Thiel, “Molecular characterization of porcine reproductive and respiratory syndrome virus, a member of the arterivirus group,” Virology, vol. 193, no. 1, pp. 329–339, 1993. View at Publisher · View at Google Scholar · View at Scopus
  4. A. E. Gorbalenya, L. Enjuanes, J. Ziebuhr, and E. J. Snijder, “Nidovirales: evolving the largest RNA virus genome,” Virus Research, vol. 117, no. 1, pp. 17–37, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. J. J. M. Meulenberg, M. M. Hulst, E. J. de Meijer et al., “Lelystad virus, the causative agent of porcine epidemic abortion and respiratory syndrome (PEARS), is related to LDV and EAV,” Virology, vol. 192, no. 1, pp. 62–72, 1993. View at Publisher · View at Google Scholar · View at Scopus
  6. E. J. Snijder, “The arterivirus replicase: the road from RNA to protein(s), and back again,” Advances in Experimental Medicine and Biology, vol. 440, pp. 97–108, 1998. View at Google Scholar · View at Scopus
  7. R. Allende, T. L. Lewis, Z. Lu et al., “North American and European porcine reproductive and respiratory syndrome viruses differ in non-structural protein coding regions,” Journal of General Virology, vol. 80, no. 2, pp. 307–315, 1999. View at Google Scholar · View at Scopus
  8. C. J. Nelsen, M. P. Murtaugh, and K. S. Faaberg, “Porcine reproductive and respiratory syndrome virus comparison: divergent evolution on two continents,” Journal of Virology, vol. 73, no. 1, pp. 270–280, 1999. View at Google Scholar · View at Scopus
  9. A. E. Firth, J. C. Zevenhoven-Dobbe, N. M. Wills et al., “Discovery of a small arterivirus gene that overlaps the gp5 coding sequence and is important for virus production,” Journal of General Virology, vol. 92, no. 5, pp. 1097–1106, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. C. R. Johnson, T. F. Griggs, J. Gnanandarajah, and M. P. Murtaugh, “Novel structural protein in porcine reproductive and respiratory syndrome virus encoded by an alternative orf5 present in all arteriviruses,” Journal of General Virology, vol. 92, no. 5, pp. 1107–1116, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. J. A. den Boon, E. J. Snijder, E. D. Chirnside, A. A. F. de Vries, M. C. Horzinek, and W. J. M. Spaan, “Equine arteritis virus is not a togavirus but belongs to the coronaviruslike superfamily,” Journal of Virology, vol. 65, no. 6, pp. 2910–2920, 1991. View at Google Scholar · View at Scopus
  12. Y. Fang and E. J. Snijder, “The PRRSV replicase: exploring the multifunctionality of an intriguing set of nonstructural proteins,” Virus Research, vol. 154, no. 1-2, pp. 61–76, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Wootton, D. Yoo, and D. Rogan, “Full-length sequence of a Canadian porcine reproductive and respiratory syndrome virus (PRRSV) isolate,” Archives of Virology, vol. 145, no. 11, pp. 2297–2323, 2000. View at Publisher · View at Google Scholar · View at Scopus
  14. K. A. Ivanov, T. Hertzig, M. Rozanov et al., “Major genetic marker of nidoviruses encodes a replicative endoribonuclease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 34, pp. 12694–12699, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. D. D. Nedialkova, R. Ulferts, E. van den Born et al., “Biochemical characterization of arterivirus nonstructural protein 11 reveals the nidovirus-wide conservation of a replicative endoribonuclease,” Journal of Virology, vol. 83, no. 11, pp. 5671–5682, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. C. C. Posthuma, D. D. Nedialkova, J. C. Zevenhoven-Dobbe, J. H. Blokhuis, A. E. Gorbalenya, and E. J. Snijder, “Site-directed mutagenesis of the nidovirus replicative endoribonuclease NendoU exerts pleiotropic effects on the arterivirus life cycle,” Journal of Virology, vol. 80, no. 4, pp. 1653–1661, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. D. Yoo, C. Song, Y. Sun, Y. Du, O. Kim, and H. C. Liu, “Modulation of host cell responses and evasion strategies for porcine reproductive and respiratory syndrome virus,” Virus Research, vol. 154, no. 1-2, pp. 48–60, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. L. K. Beura, S. N. Sarkar, B. Kwon et al., “Porcine reproductive and respiratory syndrome virus nonstructural protein 1β modulates host innate immune response by antagonizing IRF3 activation,” Journal of Virology, vol. 84, no. 3, pp. 1574–1584, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Xiao, D. Mo, Q. Wang et al., “Aberrant host immune response induced by highly virulent PRRSV identified by digital gene expression tag profiling,” BMC Genomics, vol. 11, no. 1, article 544, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. P. Zhou, S. Zhai, X. Zhou et al., “Molecular characterization of transcriptome-wide interactions between highly pathogenic porcine reproductive and respiratory syndrome virus and porcine alveolar macrophages in vivo,” International Journal of Biological Sciences, vol. 7, no. 7, pp. 947–959, 2011. View at Google Scholar · View at Scopus
  21. H. S. Kim, J. Kwang, I. J. Yoon, H. S. Joo, and M. L. Frey, “Enhanced replication of porcine reproductive and respiratory syndrome (PRRS) virus in a homogeneous subpopulation of MA-104 [MA104] cell line,” Archives of Virology, vol. 133, no. 3-4, pp. 477–483, 1993. View at Google Scholar · View at Scopus
  22. R. C. Gentleman, V. J. Carey, D. M. Bates et al., “Bioconductor: open software development for computational biology and bioinformatics,” Genome Biology, vol. 5, no. 10, article R80, 2004. View at Google Scholar · View at Scopus
  23. R. A. Irizarry, B. Hobbs, F. Collin et al., “Exploration, normalization, and summaries of high density oligonucleotide array probe level data,” Biostatistics, vol. 4, no. 2, pp. 249–264, 2003. View at Google Scholar · View at Scopus
  24. G. K. Smyth, “Linear models and empirical bayes methods for assessing differential expression in microarray experiments,” Statistical Applications in Genetics and Molecular Biology, vol. 3, no. 1, article 3, 2004. View at Google Scholar · View at Scopus
  25. G. K. Smyth, R. Gentleman, V. Carey, S. Dudoit, R. Irizarry, and W. Huber, “Limma: linear models for microarray data,” in Bioinformatics and Computational Biology Solutions Using R and Bioconductor, pp. 397–420, Springer, New York, NY, USA, 2005. View at Google Scholar
  26. Y. Benjamini and Y. Hochberg, “Controlling the false discovery rate: a practical and powerful approach to multiple testing,” Journal of the Royal Statistical Society B, vol. 57, pp. 289–300, 1995. View at Google Scholar
  27. K. Bhardwaj, L. Guarino, and C. C. Kao, “The severe acute respiratory syndrome coronavirus Nsp15 protein is an endoribonuclease that prefers manganese as a cofactor,” Journal of Virology, vol. 78, no. 22, pp. 12218–12224, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. P. Gál, J. Dobó, P. Závodszky, and R. B. M. Sim, “Early complement proteases: C1r, C1s and MASPs. A structural insight into activation and functions,” Molecular Immunology, vol. 46, no. 14, pp. 2745–2752, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Sahu and J. D. Lambris, “Structure and biology of complement protein C3, a connecting link between innate and acquired immunity,” Immunological Reviews, vol. 180, pp. 35–48, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. K. L. Jeffrey, M. Camps, C. Rommel, and C. R. Mackay, “Targeting dual-specificity phosphatases: manipulating MAP kinase signalling and immune responses,” Nature Reviews Drug Discovery, vol. 6, no. 5, pp. 391–403, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. C. J. Caunt, C. A. Rivers, B. L. Conway-Campbell, M. R. Norman, and C. A. McArdle, “Epidermal growth factor receptor and protein kinase C signaling to ERK2: spatiotemporal regulation of ERK2 by dual specificity phosphatases,” The Journal of Biological Chemistry, vol. 283, no. 10, pp. 6241–6252, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. A. L. Silvers, M. A. Bachelor, and G. T. Bowden, “The role of JNK and p38 MAPK activities in UVA-induced signaling pathways leading to AP-1 activation and c-Fos expression,” Neoplasia, vol. 5, no. 4, pp. 319–329, 2003. View at Google Scholar · View at Scopus
  33. K. Shuai and B. Liu, “Regulation of gene-activation pathways by pias proteins in the immune system,” Nature Reviews Immunology, vol. 5, no. 8, pp. 593–605, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. K. A. Wilkinson and J. M. Henley, “Mechanisms, regulation and consequences of protein SUMOylation,” Biochemical Journal, vol. 428, no. 2, pp. 133–145, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. D. Lim, K. M. Jocelyn, G. W. Yip, and B. H. Bay, “Silencing the Metallothionein-2A gene inhibits cell cycle progression from G1- to S-phase involving ATM and cdc25A signaling in breast cancer cells,” Cancer Letters, vol. 276, no. 1, pp. 109–117, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. P. Liu, L. R. Barkley, T. Day et al., “The Chk1-mediated S-phase checkpoint targets initiation factor Cdc45 via a Cdc25A/Cdk2-independent mechanism,” The Journal of Biological Chemistry, vol. 281, no. 41, pp. 30631–30644, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. A. J. Moss, S. Sharma, and N. P. J. Brindle, “Rational design and protein engineering of growth factors for regenerative medicine and tissue engineering,” Biochemical Society Transactions, vol. 37, no. 4, pp. 717–721, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Labib, S. E. Kearsey, and J. F. X. Diffley, “MCM2-7 proteins are essential components of prereplicative complexes that accumulate cooperatively in the nucleus during G1-phase and are required to establish, but not maintain, the S-phase checkpoint,” Molecular Biology of the Cell, vol. 12, no. 11, pp. 3658–3667, 2001. View at Google Scholar · View at Scopus
  39. T. S. Takahashi, D. B. Wigley, and J. C. Walter, “Pumps, paradoxes and ploughshares: mechanism of the MCM2-7 DNA helicase,” Trends in Biochemical Sciences, vol. 30, no. 8, pp. 437–444, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. Y. J. Lee and C. Lee, “Stress-activated protein kinases are involved in porcine reproductive and respiratory syndrome virus infection and modulate virus-induced cytokine production,” Virology, vol. 427, no. 2, pp. 80–89, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Bhardwaj, P. Liu, J. L. Leibowitz, and C. C. Kao, “The coronavirus endoribonuclease nsp15 interacts with retinoblastoma tumor suppressor protein,” Journal of Virology, vol. 86, no. 8, pp. 4294–4304, 2012. View at Publisher · View at Google Scholar
  42. T. D. Friedrich, E. Bedner, Z. Darzynkiewicz, and J. M. Lehman, “Distinct patterns of MCM protein binding in nuclei of S phase and rereplicating SV40-infected monkey kidney cells,” Cytometry A, vol. 68, no. 1, pp. 10–18, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Nash, W. Chen, and N. Muzyczka, “Complete in vitro reconstitution of adeno-associated virus DNA replication requires the minichromosome maintenance complex proteins,” Journal of Virology, vol. 82, no. 3, pp. 1458–1464, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. W. Stedman, Z. Deng, F. Lu, and P. M. Lieberman, “ORC, MCM, and histone hyperacetylation at the Kaposi's sarcoma-associated herpesvirus latent replication origin,” Journal of Virology, vol. 78, no. 22, pp. 12566–12575, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Kawaguchi and K. Nagata, “De novo replication of the influenza virus RNA genome is regulated by DNA replicative helicase, MCM,” EMBO Journal, vol. 26, no. 21, pp. 4566–4575, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. D. Yoo, S. K. Wootton, G. Li, C. Song, and R. R. Rowland, “Colocalization and interaction of the porcine arterivirus nucleocapsid protein with the small nucleolar RNA-associated protein fibrillarin,” Journal of Virology, vol. 77, no. 22, pp. 12173–12183, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. C. Song, R. Lu, D. Bienzle, H. C. Liu, and D. Yoo, “Interaction of the porcine reproductive and respiratory syndrome virus nucleocapsid protein with the inhibitor of MyoD family-a domain-containing protein,” Biological Chemistry, vol. 390, no. 3, pp. 215–223, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. T. M. Young, Q. Wang, T. Pe'ery, and M. B. Mathews, “The human I-mfa domain-containing protein, HIC, interacts with cyclin T1 and modulates P-TEFb-dependent transcription,” Molecular and Cellular Biology, vol. 23, no. 18, pp. 6373–6384, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. Y. Sun, N. Chen, and D. Yoo, “Inhibition of type I IFN by nsp11 of PRRSV,” in Proceedings of the 30th Annual Meeting, American Society of Virology, Twin City, Minn, USA, July 2011.