Table of Contents Author Guidelines Submit a Manuscript
Journal of Biomedicine and Biotechnology
Volume 2011 (2011), Article ID 369648, 23 pages
http://dx.doi.org/10.1155/2011/369648
Review Article

The Multifaceted Poliovirus 2A Protease: Regulation of Gene Expression by Picornavirus Proteases

1European Molecular Biology Laboratory (EMBL), Meyerhofstrasse 1, 69117 Heidelberg, Germany
2Centro de Biología Molecular Severo Ochoa (CSIC-UAM), C/ Nicolas Cabrera 1, Universidad Autónoma de Madrid, Cantoblanco. 28049 Madrid, Spain

Received 28 October 2010; Revised 18 January 2011; Accepted 17 February 2011

Academic Editor: Decheng Yang

Copyright © 2011 Alfredo Castelló 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. L. Tong, “Viral proteases,” Chemical Reviews, vol. 102, no. 12, pp. 4609–4626, 2002. View at Publisher · View at Google Scholar · View at Scopus
  2. T. Skern, B. Hampölz, A. Guarné et al., “Structure and function of picornavirus proteinases,” in Molecular Biology of Picornaviruses, B. L. Semler and E. Wimmer, Eds., pp. 199–212, ASM Press, Washington, DC, USA, 2002. View at Google Scholar
  3. A. D. Frankel and J. A. T. Young, “HIV-1: fifteen proteins and an RNA,” Annual Review of Biochemistry, vol. 67, pp. 1–25, 1998. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. J. Seipelt, A. Guarné, E. Bergmann et al., “The structures of picornaviral proteinases,” Virus Research, vol. 62, no. 2, pp. 159–168, 1999. View at Publisher · View at Google Scholar · View at Scopus
  5. I. N. Clarke and P. R. Lambden, “Organization and expression of calicivirus genes,” Journal of Infectious Diseases, vol. 181, supplement 2, pp. S309–S316, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  6. R. M. Flügel and K. I. Pfrepper, “Proteolytic processing of foamy virus Gag and Pol proteins,” Current Topics in Microbiology and Immunology, vol. 277, pp. 63–88, 2003. View at Google Scholar · View at Scopus
  7. A. D. Davidson, “Chapter 2. New insights into flavivirus nonstructural protein 5,” Advances in Virus Research, vol. 74, pp. 41–101, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. B. Blondel, F. Colbère-Garapin, T. Couderc, A. Wirotius, and F. Guivel-Benhassine, “Poliovirus, pathogenesis of poliomyelitis, and apoptosis,” Current Topics in Microbiology and Immunology, vol. 289, pp. 25–56, 2005. View at Google Scholar · View at Scopus
  9. B. Blondel, T. Couderc, Y. Simonin, A. S. Gosselin, and F. Guivel-Benhassine, “Poliovirus and apoptosis,” Progress in Molecular and Subcellular Biology, vol. 36, pp. 151–169, 2004. View at Google Scholar · View at Scopus
  10. R. Aldabe and L. Carrasco, “Induction of membrane proliferation by poliovirus proteins 2C and 2BC,” Biochemical and Biophysical Research Communications, vol. 206, no. 1, pp. 64–76, 1995. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. V. I. Agol, G. A. Belov, K. Bienz et al., “Two types of death of poliovirus-infected cells: caspase involvement in the apoptosis but not cytopathic effect,” Virology, vol. 252, no. 2, pp. 343–353, 1998. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. C. Calandria, A. Irurzun, A. Barco, and L. Carrasco, “Individual expression of poliovirus 2A and 3C induces activation of caspase-3 and PARP cleavage in HeLa cells,” Virus Research, vol. 104, no. 1, pp. 39–49, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. G. J. Belsham and N. Sonenberg, “Picornavirus RNA translation: roles for cellular proteins,” Trends in Microbiology, vol. 8, no. 7, pp. 330–335, 2000. View at Publisher · View at Google Scholar · View at Scopus
  14. R. E. Lloyd, “Translational control by viral proteinases,” Virus Research, vol. 119, no. 1, pp. 76–88, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  15. K. E. Gustin and P. Sarnow, “Effects of poliovirus infection on nucleo-cytoplasmic trafficking and nuclear pore complex composition,” EMBO Journal, vol. 20, no. 1-2, pp. 240–249, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  16. N. Park, P. Katikaneni, T. Skern, and K. E. Gustin, “Differential targeting of nuclear pore complex proteins in poliovirus-infected cells,” Journal of Virology, vol. 82, no. 4, pp. 1647–1655, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  17. A. Castelló, J. M. Izquierdo, E. Welnowska, and L. Carrasco, “RNA nuclear export is blocked by poliovirus 2A protease and is concomitant with nucleoporin cleavage,” Journal of Cell Science, vol. 122, no. 20, pp. 3799–3809, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  18. N. Nathanson, “The pathogenesis of poliomyelitis: what we don't know,” Advances in Virus Research, vol. 71, pp. 1–50, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. J. M. Hogle, “Poliovirus cell entry: common structural themes in viral cell entry pathways,” Annual Review of Microbiology, vol. 56, pp. 677–702, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. V. R. Racaniello, “One hundred years of poliovirus pathogenesis,” Virology, vol. 344, no. 1, pp. 9–16, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  21. E. Wimmer, C. U. T. Hellen, and X. Cao, “Genetics of poliovirus,” Annual Review of Genetics, vol. 27, pp. 353–436, 1993. View at Google Scholar · View at Scopus
  22. V. A. Agol, “Picornavirus genome: an overview,” in Molecular Biology of Picornaviruses, B. L. Semler and E. Wimmer, Eds., pp. 127–148, ASM Press, Washington, DC, USA, 2002. View at Google Scholar
  23. L. E. C. Leong, C. T. Cornell, and B. L. Semler, “Processing determinants and functions of cleavage products of picornavirus polyproteins,” in Molecular Biology of Picornaviruses, B. L. Semler and E. Wimmer, Eds., pp. 187–198, ASM Press, Washington, DC, USA, 2002. View at Google Scholar
  24. C. K. Lee and E. Wimmer, “Proteolytic processing of poliovirus polyprotein: elimination of 2A(pro)-mediated, alternative cleavage of polypeptide 3CD by in vitro mutagenesis,” Virology, vol. 166, no. 2, pp. 405–414, 1988. View at Google Scholar · View at Scopus
  25. C. E. Cameron, D. W. Gohara, and J. J. Arnold, “Poliovirus RNA-dependent RNA polymerase (3Dpol): structure, function, and mechanism,” in Molecular Biology of Picornaviruses, B. L. Semler and E. Wimmer, Eds., pp. 255–268, ASM Press, Washington, DC, USA, 2002. View at Google Scholar
  26. A. V. Paul, “Possible Unifying mechanism of picornavirus genome replication,” in Molecular Biology of Picornaviruses, B. L. Semler and E. Wimmer, Eds., pp. 227–246, ASM Press, Washington, DC, USA, 2002. View at Google Scholar
  27. A. V. Paul, J. H. Van Boom, D. Filippov, and E. Wimmer, “Protein-primed RNA synthesis by purified poliovirus RNA polymerase,” Nature, vol. 393, no. 6682, pp. 280–284, 1998. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  28. M. J. Almela, M. E. Gonzalez, and L. Carrasco, “Inhibitors of poliovirus uncoating efficiently block the early membrane permeabilization induced by virus particles,” Journal of Virology, vol. 65, no. 5, pp. 2572–2577, 1991. View at Google Scholar · View at Scopus
  29. M. A. Sanz, A. Castelló, and L. Carrasco, “Viral translation is coupled to transcription in sindbis virus-infected cells,” Journal of Virology, vol. 81, no. 13, pp. 7061–7068, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. R. Guinea and L. Carrasco, “Phospholipid biosynthesis and poliovirus genome replication, two coupled phenomena,” EMBO Journal, vol. 9, no. 6, pp. 2011–2016, 1990. View at Google Scholar · View at Scopus
  31. L. Carrasco, R. Guinea, A. Irurzun, and A. Barco, “Effects of viral replication on cellular membrane metabolism and function,” in Molecular Biology of Picornaviruses, B. L. Semler and E. Wimmer, Eds., pp. 337–356, ASM Press, Washington, DC, USA, 2002. View at Google Scholar
  32. A. Agirre, A. Barco, L. Carrasco, and J. L. Nieva, “Viroporin-mediated membrane permeabilization: pore formation by nonstructural poliovirus 2B protein,” Journal of Biological Chemistry, vol. 277, no. 43, pp. 40434–40441, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. M. E. Gonzalez and L. Carrasco, “Viroporins,” FEBS Letters, vol. 552, no. 1, pp. 28–34, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. N. Kitamura, B. L. Semler, P. G. Rothberg et al., “Primary structure, gene organization and polypeptide expression of poliovirus RNA,” Nature, vol. 291, no. 5816, pp. 547–553, 1981. View at Google Scholar · View at Scopus
  35. J. M. Hogle, M. Chow, and D. J. Filman, “Three-dimensional structure of poliovirus at 2.9 Å resolution,” Science, vol. 229, no. 4720, pp. 1358–1365, 1985. View at Google Scholar · View at Scopus
  36. J. Pelletier and N. Sonenberg, “Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA,” Nature, vol. 334, no. 6180, pp. 320–325, 1988. View at Google Scholar · View at Scopus
  37. A. Molla, A. V. Paul, and E. Wimmer, “Cell-free, de novo synthesis of poliovirus,” Science, vol. 254, no. 5038, pp. 1647–1651, 1991. View at Google Scholar · View at Scopus
  38. E. Wimmer, S. Mueller, T. M. Tumpey, and J. K. Taubenberger, “Synthetic viruses: a new opportunity to understand and prevent viral disease,” Nature Biotechnology, vol. 27, no. 12, pp. 1163–1172, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. D. Etchison, S. C. Milburn, I. Edery, N. Sonenberg, and J. W. Hershey, “Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220,000-dalton polypeptide associated with eucaryotc initiation factor 3 and a cap binding protein complex,” Journal of Biological Chemistry, vol. 257, no. 24, pp. 14806–14810, 1982. View at Google Scholar
  40. M. D. Ryan and M. Flint, “Virus-encoded proteinases of the picornavirus super-group,” Journal of General Virology, vol. 78, no. 4, pp. 699–723, 1997. View at Google Scholar · View at Scopus
  41. A. C. Palmenberg, D. Neubauer, and T. Skern, “Genome organization and encoded proteins,” in The Picornaviruses, E. Eherenfeld, E. Domingo, and R. Roos, Eds., pp. 3–17, ASM Press, Washington, DC, USA, 2010. View at Google Scholar
  42. A. Guarné, J. Tormo, R. Kirchweger, D. Pfistermueller, I. Fita, and T. Skern, “Structure of the foot-and-mouth disease virus leader protease: a papain-like fold adapted for self-processing and eIF4G recognition,” EMBO Journal, vol. 17, no. 24, pp. 7469–7479, 1998. View at Publisher · View at Google Scholar · View at PubMed
  43. A. Guarné, B. Hampoelz, W. Glaser et al., “Structural and biochemical features distinguish the foot-and-mouth disease virus leader proteinase from other papain-like enzymes,” Journal of Molecular Biology, vol. 302, no. 5, pp. 1227–1240, 2000. View at Publisher · View at Google Scholar · View at PubMed
  44. M. E. Piccone, E. Rieder, P. W. Mason, and M. J. Grubman, “The foot-and-mouth disease virus leader proteinase gene is not required for viral replication,” Journal of Virology, vol. 69, no. 9, pp. 5376–5382, 1995. View at Google Scholar
  45. T. De Los Santos, S. De Avila Botton, R. Weiblen, and M. J. Grubman, “The leader proteinase of foot-and-mouth disease virus inhibits the induction of beta interferon mRNA and blocks the host innate immune response,” Journal of Virology, vol. 80, no. 4, pp. 1906–1914, 2006. View at Publisher · View at Google Scholar · View at PubMed
  46. T. De Los Santos, F. D. S. Segundo, J. Zhu, M. Koster, C. C. A. Dias, and M. J. Grubman, “A conserved domain in the leader proteinase of foot-and-mouth disease virus is required for proper subcellular localization and function,” Journal of Virology, vol. 83, no. 4, pp. 1800–1810, 2009. View at Publisher · View at Google Scholar · View at PubMed
  47. S. V. Hato, F. Sorgeloos, C. Ricour et al., “Differential IFN-α/β production suppressing capacities of the leader proteins of mengovirus and foot-and-mouth disease virus,” Cellular Microbiology, vol. 12, no. 3, pp. 310–317, 2010. View at Publisher · View at Google Scholar · View at PubMed
  48. M. A. Devaney, V. N. Vakharia, R. E. Lloyd, E. Ehrenfeld, and M. J. Grubman, “Leader protein of foot-and-mouth disease virus is required for cleavage of the p220 component of the cap-binding protein complex,” Journal of Virology, vol. 62, no. 11, pp. 4407–4409, 1988. View at Google Scholar
  49. R. E. Lloyd, M. J. Grubman, and E. Ehrenfeld, “Relationship of p220 cleavage during picornavirus infection to 2A proteinase sequencing,” Journal of Virology, vol. 62, no. 11, pp. 4216–4223, 1988. View at Google Scholar
  50. W. Glaser and T. Skern, “Extremely efficient cleavage of eIF4G by picornaviral proteinases L and 2A in vitro,” FEBS Letters, vol. 480, no. 2-3, pp. 151–155, 2000. View at Publisher · View at Google Scholar
  51. M. D. Ryan and J. Drew, “Foot-and-mouth disease virus 2A oligopeptide mediated cleavage of an artificial polyprotein,” EMBO Journal, vol. 13, no. 4, pp. 928–933, 1994. View at Google Scholar
  52. M. L. L. Donnelly, G. Luke, A. Mehrotra et al., “Analysis of the aphthovirus 2A/2B polyprotein 'cleavage' mechanism indicates not a proteolytic reaction, but a novel translational effect: a putative ribosomal 'skip',” Journal of General Virology, vol. 82, no. 5, pp. 1013–1025, 2001. View at Google Scholar
  53. M. L. L. Donnelly, D. Gani, M. Flint, S. Monaghan, and M. D. Ryan, “The cleavage activities of aphthovirus and cardiovirus 2A proteins,” Journal of General Virology, vol. 78, no. 1, pp. 13–21, 1997. View at Google Scholar
  54. H. Konig and B. Rosenwirth, “Purification and partial characterization of poliovirus protease 2A by means of a functional assay,” Journal of Virology, vol. 62, no. 4, pp. 1243–1250, 1988. View at Google Scholar
  55. M. J. H. Nicklin, K. S. Harris, P. V. Pallai, and E. Wimmer, “Poliovirus proteinase 3C: large-scale expression, purification, and specific cleavage activity on natural and synthetic substrates in vitro,” Journal of Virology, vol. 62, no. 12, pp. 4586–4593, 1988. View at Google Scholar
  56. J. N. Burroughs, D. V. Sangar, B. E. Clarke et al., “Multiple proteases in foot-and-mouth disease virus replication,” Journal of Virology, vol. 50, no. 3, pp. 878–883, 1984. View at Google Scholar
  57. L. G. Kleina and M. J. Grubman, “Antiviral effects of a thiol protease inhibitor on foot-and-mouth disease virus,” Journal of Virology, vol. 66, no. 12, pp. 7168–7175, 1992. View at Google Scholar
  58. A. E. Gorbalenya, E. V. Koonin, and M. M. C. Lai, “Putative papain-related thiol proteases of positive-strand RNA viruses. Identification of rubi- and aphthovirus proteases and delineation of a novel conserved domain associated with proteases of rubi, α- and coronaviruses,” FEBS Letters, vol. 288, no. 1-2, pp. 201–205, 1991. View at Publisher · View at Google Scholar
  59. M. E. Piccone, M. Zellner, T. F. Kumosinski, P. W. Mason, and M. J. Grubman, “Identification of the active-site residues of the L proteinase of foot- and-mouth disease virus,” Journal of Virology, vol. 69, no. 8, pp. 4950–4956, 1995. View at Google Scholar
  60. P. J. Roberts and G. J. Belsham, “Identification of critical amino acids within the foot-and-mouth disease virus leader protein, a cysteine protease,” Virology, vol. 213, no. 1, pp. 140–146, 1995. View at Publisher · View at Google Scholar · View at PubMed
  61. V. M. Blinov, A. E. Gorbalenia, and A. P. Donchenko, “Structural similarity of poliovirus cysteine proteinase P3-7c and cellular serine proteinase of trypsin,” Doklady Akademii Nauk SSSR, vol. 279, no. 2, pp. 502–505, 1984. View at Google Scholar
  62. A. E. Gorbalenya, A. P. Donchenko, V. M. Blinov, and E. V. Koonin, “Cysteine proteases of positive strand RNA viruses and chymotrypsin-like serin proteases: a distinct protein superfamily with a common structural fold,” FEBS Letters, vol. 243, no. 2, pp. 103–114, 1989. View at Publisher · View at Google Scholar
  63. J. F. Bazan and R. J. Fletterick, “Viral cysteine proteases are homologous to the trypsin-like family of serine proteases: structural and functional implications,” Proceedings of the National Academy of Sciences of the United States of America, vol. 85, no. 21, pp. 7872–7876, 1988. View at Google Scholar
  64. H. Toyoda, M. J. H. Nicklin, M. G. Murray et al., “A second virus-encoded proteinase involved in proteolytic processing of poliovirus polyprotein,” Cell, vol. 45, no. 5, pp. 761–770, 1986. View at Google Scholar
  65. T. Skern, W. Sommergruber, H. Auer et al., “Substrate requirements of a human rhinoviral 2A proteinase,” Virology, vol. 181, no. 1, pp. 46–54, 1991. View at Publisher · View at Google Scholar
  66. C. U. T. Hellen, C. K. Lee, and E. Wimmer, “Determinants of substrate recognition by poliovirus 2A proteinase,” Journal of Virology, vol. 66, no. 6, pp. 3330–3338, 1992. View at Google Scholar
  67. W. Sommergruber, H. Ahorn, A. Zophel et al., “Cleavage specificity on synthetic peptide substrates of human rhinovirus 2 proteinase 2A,” Journal of Biological Chemistry, vol. 267, no. 31, pp. 22639–22644, 1992. View at Google Scholar
  68. I. Ventoso, A. Barco, and L. Carrasco, “Genetic selection of poliovirus 2A(pro)-binding peptides,” Journal of Virology, vol. 73, no. 1, pp. 814–818, 1999. View at Google Scholar
  69. S. F. Yu and R. E. Lloyd, “Identification of essential amino acid residues in the functional activity of poliovirus 2A protease,” Virology, vol. 182, no. 2, pp. 615–625, 1991. View at Publisher · View at Google Scholar
  70. W. Sommergruber, J. Seipelt, F. Fessl, T. Skern, H. D. Liebig, and G. Casari, “Mutational analyses support a model for the HRV2 2A proteinase,” Virology, vol. 234, no. 2, pp. 203–214, 1997. View at Publisher · View at Google Scholar · View at PubMed
  71. J. F. W. Petersen, M. M. Cherney, H. D. Liebig, T. Skern, E. Kuechler, and M. N. G. James, “The structure of the 2A proteinase from a common cold virus: a proteinase responsible for the shut-off of host-cell protein synthesis,” EMBO Journal, vol. 18, no. 20, pp. 5463–5475, 1999. View at Publisher · View at Google Scholar · View at PubMed
  72. S. F. Yu and R. E. Lloyd, “Characterization of the roles of conserved cysteine and histidine residues in poliovirus 2A protease,” Virology, vol. 186, no. 2, pp. 725–735, 1992. View at Publisher · View at Google Scholar
  73. W. Sommergruber, G. Casari, F. Fessl, J. Seipelt, and T. Skern, “The 2A proteinase of human rhinovirus is a zinc containing enzyme,” Virology, vol. 204, no. 2, pp. 815–818, 1994. View at Publisher · View at Google Scholar · View at PubMed
  74. T. Voss, R. Meyer, and W. Sommergruber, “Spectroscopic characterization of rhinoviral protease 2A: Zn is essential for the structural integrity,” Protein Science, vol. 4, no. 12, pp. 2526–2531, 1995. View at Google Scholar
  75. A. Barco, I. Ventoso, and L. Carrasco, “The yeast Saccharomyces cerevisiae as a genetic system for obtaining variants of poliovirus protease 2A,” Journal of Biological Chemistry, vol. 272, no. 19, pp. 12683–12691, 1997. View at Publisher · View at Google Scholar
  76. I. Ventoso, A. Barco, and L. Carrasco, “Mutational analysis of poliovirus 2A(pro): distinct inhibitory functions of 2A(pro) on translation and transcription,” Journal of Biological Chemistry, vol. 273, no. 43, pp. 27960–27967, 1998. View at Publisher · View at Google Scholar
  77. S. F. Yu, P. Benton, M. Bovee, J. Sessions, and R. E. Lloyd, “Defective RNA replication by poliovirus mutants deficient in 2A protease cleavage activity,” Journal of Virology, vol. 69, no. 1, pp. 247–252, 1995. View at Google Scholar
  78. H. Igarashi, Y. Yoshino, M. Miyazawa, H. Horie, S. Ohka, and A. Nomoto, “2A protease is not a prerequisite for poliovirus replication,” Journal of Virology, vol. 84, no. 12, pp. 5947–5957, 2010. View at Publisher · View at Google Scholar · View at PubMed
  79. J. M. Morrison and V. R. Racaniello, “Proteinase 2A is essential for enterovirus replication in type I interferon-treated cells,” Journal of Virology, vol. 83, no. 9, pp. 4412–4422, 2009. View at Publisher · View at Google Scholar · View at PubMed
  80. N. L. Teterina, E. A. Levenson, and E. Ehrenfeld, “Viable polioviruses that encode 2A proteins with fluorescent protein tags,” Journal of Virology, vol. 84, no. 3, pp. 1477–1488, 2010. View at Publisher · View at Google Scholar · View at PubMed
  81. N. Sonenberg and A. G. Hinnebusch, “Regulation of translation initiation in eukaryotes: mechanisms and biological targets,” Cell, vol. 136, no. 4, pp. 731–745, 2009. View at Publisher · View at Google Scholar · View at PubMed
  82. R. J. Jackson, C. U. T. Hellen, and T. V. Pestova, “The mechanism of eukaryotic translation initiation and principles of its regulation,” Nature Reviews Molecular Cell Biology, vol. 11, no. 2, pp. 113–127, 2010. View at Publisher · View at Google Scholar · View at PubMed
  83. A. C. Gingras, B. Raught, and N. Sonenberg, “eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation,” Annual Review of Biochemistry, vol. 68, pp. 913–963, 1999. View at Publisher · View at Google Scholar · View at PubMed
  84. F. Gebauer and M. W. Hentze, “Molecular mechanisms of translational control,” Nature Reviews Molecular Cell Biology, vol. 5, no. 10, pp. 827–835, 2004. View at Publisher · View at Google Scholar · View at PubMed
  85. M. W. Hentze, “eIF4G: a multipurpose ribosome adapter?” Science, vol. 275, no. 5299, pp. 500–501, 1997. View at Publisher · View at Google Scholar
  86. S. J. Morley, P. S. Curtis, and V. M. Pain, “elF4G: translation's mystery factor begins to yield its secrets,” RNA, vol. 3, no. 10, pp. 1085–1104, 1997. View at Google Scholar
  87. H. Imataka and N. Sonenberg, “Human eukaryotic translation initiation factor 4G (eIF4G) possesses two separate and independent binding sites for eIF4A,” Molecular and Cellular Biology, vol. 17, no. 12, pp. 6940–6947, 1997. View at Google Scholar
  88. H. Imataka, A. Gradi, and N. Sonenberg, “A newly identified N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation,” EMBO Journal, vol. 17, no. 24, pp. 7480–7489, 1998. View at Publisher · View at Google Scholar · View at PubMed
  89. S. E. Wells, P. E. Hillner, R. D. Vale, and A. B. Sachs, “Circularization of mRNA by eukaryotic translation initiation factors,” Molecular Cell, vol. 2, no. 1, pp. 135–140, 1998. View at Google Scholar
  90. R. Fukunaga and T. Hunter, “MNK1, a new MAP kinase-activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates,” EMBO Journal, vol. 16, no. 8, pp. 1921–1933, 1997. View at Publisher · View at Google Scholar · View at PubMed
  91. A. J. Waskiewicz, A. Flynn, C. G. Proud, and J. A. Cooper, “Mitogen-activated protein kinases activate the serine/threonine kinases Mnk1 and Mnk2,” EMBO Journal, vol. 16, no. 8, pp. 1909–1920, 1997. View at Publisher · View at Google Scholar · View at PubMed
  92. S. Pyronnet, H. Imataka, A. C. Gingras, R. Fukunaga, T. Hunter, and N. Sonenberg, “Human eukaryotic translation initiation factor 4G (eIF4G) recruits Mnk1 to phosphorylate eIF4E,” EMBO Journal, vol. 18, no. 1, pp. 270–279, 1999. View at Publisher · View at Google Scholar · View at PubMed
  93. I. Mohr, “Phosphorylation and dephosphorylation events that regulate viral mRNA translation,” Virus Research, vol. 119, no. 1, pp. 89–99, 2006. View at Publisher · View at Google Scholar · View at PubMed
  94. J. D. Richter and N. Sonenberg, “Regulation of cap-dependent translation by eIF4E inhibitory proteins,” Nature, vol. 433, no. 7025, pp. 477–480, 2005. View at Publisher · View at Google Scholar · View at PubMed
  95. A. Castello, E. Alvarez, and L. Carrasco, “Differential cleavage of eIF4GI and eIF4GII in mammalian cells: effects on translation,” Journal of Biological Chemistry, vol. 281, no. 44, pp. 33206–33216, 2006. View at Publisher · View at Google Scholar · View at PubMed
  96. E. Welnowska, A. Castelló, P. Moral, and L. Carrasco, “Translation of mRNAs from vesicular stomatitis virus and vaccinia virus is differentially blocked in cells with depletion of eIF4GI and/or eIF4GII,” Journal of Molecular Biology, vol. 394, no. 3, pp. 506–521, 2009. View at Publisher · View at Google Scholar · View at PubMed
  97. W. E. Marissen and R. E. Lloyd, “Eukaryotic translation initiation factor 4G is targeted for proteolytic cleavage by caspase 3 during inhibition of translation in apoptotic cells,” Molecular and Cellular Biology, vol. 18, no. 12, pp. 7565–7574, 1998. View at Google Scholar
  98. S. Caron, M. Charon, E. Cramer, N. Sonenberg, and I. Dusanter-Fourt, “Selective modification of eukaryotic initiation factor 4F (eIF4F) at the onset of cell differentiation: recruitment of eIF4GII and long-lasting phosphorylation of eIF4E,” Molecular and Cellular Biology, vol. 24, no. 11, pp. 4920–4928, 2004. View at Publisher · View at Google Scholar · View at PubMed
  99. B. Raught, A. C. Gingras, S. P. Gygi et al., “Serum-stimulated, rapamycin-sensitive phosphorylation sites in the eukaryotic: translation initiation factor 4GI,” EMBO Journal, vol. 19, no. 3, pp. 434–444, 2000. View at Google Scholar
  100. J. Ling, S. J. Morley, and J. A. Traugh, “Inhibition of cap-dependent translation via phosphorylation of eIF4G by protein kinase Pak2,” EMBO Journal, vol. 24, no. 23, pp. 4094–4105, 2005. View at Publisher · View at Google Scholar · View at PubMed
  101. S. Pyronnet, J. Dostie, and N. Sonenberg, “Suppression of cap-dependent translation in mitosis,” Genes and Development, vol. 15, no. 16, pp. 2083–2093, 2001. View at Publisher · View at Google Scholar · View at PubMed
  102. H. Qin, B. Raught, N. Sonenberg, E. G. Goldstein, and A. M. Edelman, “Phosphorylation screening identifies translational initiation factor 4GII as an intracellular target of Ca2+/calmodulin-dependent protein kinase I,” Journal of Biological Chemistry, vol. 278, no. 49, pp. 48570–48579, 2003. View at Publisher · View at Google Scholar · View at PubMed
  103. M. Bushell, D. Poncet, W. E. Marissen et al., “Cleavage of polypeptide chain initiation factor eIF4GI during apoptosis in lymphoma cells: characterisation of an internal fragment generated by caspase-3-mediated cleavage,” Cell Death and Differentiation, vol. 7, no. 7, pp. 628–636, 2000. View at Google Scholar
  104. W. E. Marissen, A. Gradi, N. Sonenberg, and R. E. Lloyd, “Cleavage of eukaryotic translation initiation factor 4GII correlates with translation inhibition during apoptosis,” Cell Death and Differentiation, vol. 7, no. 12, pp. 1234–1243, 2000. View at Publisher · View at Google Scholar · View at PubMed
  105. M. P. Byrd, M. Zamora, and R. E. Lloyd, “Translation of eukaryotic translation initiation factor 4GI (eIF4GI) proceeds from multiple mRNAs containing a novel cap-dependent internal ribosome entry site (IRES) that is active during poliovirus infection,” Journal of Biological Chemistry, vol. 280, no. 19, pp. 18610–18622, 2005. View at Publisher · View at Google Scholar · View at PubMed
  106. M. P. Byrd, M. Zamora, and R. E. Lloyd, “Generation of multiple isoforms of eukaryotic translation initiation factor 4GI by use of alternate translation initiation codons,” Molecular and Cellular Biology, vol. 22, no. 13, pp. 4499–4511, 2002. View at Publisher · View at Google Scholar
  107. M. J. Coldwell and S. J. Morley, “Specific isoforms of translation initiation factor 4GI show differences in translational activity,” Molecular and Cellular Biology, vol. 26, no. 22, pp. 8448–8460, 2006. View at Publisher · View at Google Scholar · View at PubMed
  108. R. Leibowitz and S. Penman, “Regulation of protein synthesis in HeLa cells. 3. Inhibition during poliovirus infection,” Journal of Virology, vol. 8, no. 5, pp. 661–668, 1971. View at Google Scholar
  109. T. Helentjaris and E. Ehrenfeld, “Control of protein synthesis in extracts from poliovirus-infected cells. I. mRNA discrimination by crude initiation factors,” Journal of Virology, vol. 26, no. 2, pp. 510–521, 1978. View at Google Scholar
  110. H. G. Krausslich, M. J. H. Nicklin, H. Toyoda, D. Etchison, and E. Wimmer, “Poliovirus proteinase 2A induces cleavage of eucaryotic initiation factor 4f polypeptide p220,” Journal of Virology, vol. 61, no. 9, pp. 2711–2718, 1987. View at Google Scholar
  111. I. Ventoso and L. Carrasco, “A poliovirus 2A(pro) mutant unable to cleave 3CD shows inefficient viral protein synthesis and transactivation defects,” Journal of Virology, vol. 69, no. 10, pp. 6280–6288, 1995. View at Google Scholar
  112. M. L. Bovee, B. J. Lamphear, R. E. Rhoads, and R. E. Lloyd, “Direct cleavage of elF4G by poliovirus 2A protease is inefficient in vitro,” Virology, vol. 245, no. 2, pp. 241–249, 1998. View at Publisher · View at Google Scholar
  113. D. Ethison and S. Fout, “Human rhinovirus 14 infection of HeLa cells results in the proteolytic cleavage of the p220 cap-binding complex subunit and inactivates globin mRNA translation in vitro,” Journal of Virology, vol. 54, no. 2, pp. 634–638, 1985. View at Google Scholar
  114. B. J. Lamphear, R. Yan, F. Yang et al., “Mapping the cleavage site in protein synthesis initiation factor eIF-4γ of the 2A proteases from human Coxsackievirus and rhinovirus,” Journal of Biological Chemistry, vol. 268, no. 26, pp. 19200–19203, 1993. View at Google Scholar
  115. W. Sommergruber, H. Ahorn, H. Klump et al., “2A proteinases of coxsackie- and rhinovirus cleave peptides derived from eIF-4 gamma via a common recognition motif,” Virology, vol. 198, pp. 741–745, 1994. View at Google Scholar
  116. A. Haghighat, Y. Svitkin, I. Novoa, E. Kuechler, T. Skern, and N. Sonenberg, “The eIF4G-eIF4E complex is the target for direct cleavage by the rhinovirus 2A proteinase,” Journal of Virology, vol. 70, no. 12, pp. 8444–8450, 1996. View at Google Scholar
  117. I. Ventoso, S. E. MacMillan, J. W. B. Hershey, and L. Carrasco, “Poliovirus 2A proteinase cleaves directly the eIF-4G subunit of eIF-4F complex,” FEBS Letters, vol. 435, no. 1, pp. 79–83, 1998. View at Publisher · View at Google Scholar
  118. E. E. Wyckoff, R. E. Lloyd, and E. Ehrenfeld, “Relationship of eukaryotic initiation factor 3 to poliovirus-induced p220 cleavage activity,” Journal of Virology, vol. 66, no. 5, pp. 2943–2951, 1992. View at Google Scholar
  119. M. Zamora, W. E. Marissen, and R. E. Lloyd, “Multiple eIF4GI-specific protease activities present in uninfected and poliovirus-infected cells,” Journal of Virology, vol. 76, no. 1, pp. 165–177, 2002. View at Publisher · View at Google Scholar
  120. L. Perez and L. Carrasco, “Lack of direct correlation between p220 cleavage and the shut-off of host translation after poliovirus infection,” Virology, vol. 189, no. 1, pp. 178–186, 1992. View at Publisher · View at Google Scholar
  121. A. Irurzun, S. Sanchez-Palomino, I. Novoa, and L. Carrasco, “Monensin and nigericin prevent the inhibition of host translation by poliovirus, without affecting p220 cleavage,” Journal of Virology, vol. 69, no. 12, pp. 7453–7460, 1995. View at Google Scholar
  122. A. Gradi, Y. V. Svitkin, H. Imataka, and N. Sonenberg, “Proteolysis of human eukaryotic translation initiation factor eIF4GII, but not EIF4GI, coincides with the shutoff of host protein synthesis after poliovirus infection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 19, pp. 11089–11094, 1998. View at Publisher · View at Google Scholar
  123. Y. V. Svitkin, A. Gradi, H. Imataka, S. Morino, and N. Sonenberg, “Eukaryotic initiation factor 4GII (eIF4GII), but not eIF4GI, cleavage correlates with inhibition of host cell protein synthesis after human rhinovirus infection,” Journal of Virology, vol. 73, no. 4, pp. 3467–3472, 1999. View at Google Scholar
  124. F. Martinez-Abarca, M. A. Alonso, and L. Carrasco, “High level expression in Escherichia coli cells and purification of poliovirus protein 2A(pro),” Journal of General Virology, vol. 74, no. 12, pp. 2645–2652, 1993. View at Google Scholar
  125. I. Novoa, F. Martínez-Abarca, P. Fortes, J. Ortín, and L. Carrasco, “Cleavage of p220 by purified poliovirus 2A(pro) in cell-free systems: effects on translation of capped and uncapped mRNAs,” Biochemistry, vol. 36, no. 25, pp. 7802–7809, 1997. View at Publisher · View at Google Scholar · View at PubMed
  126. Y. V. Svitkin, H. Imataka, K. Khaleghpour, A. Kahvejian, H. D. Liebig, and N. Sonenberg, “Poly(A)-binding protein interaction with elF4G stimulates picornavirus IRES-dependent translation,” RNA, vol. 7, no. 12, pp. 1743–1752, 2001. View at Google Scholar
  127. A. Castelló, D. Franco, P. Moral-López et al., “HIV-1 protease inhibits cap-and poly(A)-dependent translation upon eIF4GI and PABP cleavage,” PLoS One, vol. 4, no. 11, Article ID e7997, 2009. View at Publisher · View at Google Scholar · View at PubMed
  128. X. H. Sun and D. Baltimore, “Human immunodeficiency virus tat-activated expression of poliovirus protein 2A inhibits mRNA translation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 7, pp. 2143–2146, 1989. View at Google Scholar
  129. M. V. Davies, J. Pelletier, K. Meerovitch, N. Sonenberg, and R. J. Kaufman, “The effect of poliovirus proteinase 2A(pro) expression on cellular metabolism. Inhibition of DNA replication, RNA polymerase II transcription, and translation,” Journal of Biological Chemistry, vol. 266, no. 22, pp. 14714–14720, 1991. View at Google Scholar
  130. R. Aldabe, E. Feduchi, I. Novoa, and L. Carrasco, “Expression of poliovirus 2A(pro) in mammalian cells: effects on translation,” FEBS Letters, vol. 377, no. 1, pp. 1–5, 1995. View at Publisher · View at Google Scholar
  131. R. Aldabe, E. Feduchi, I. Novoa, and L. Carrasco, “Efficient cleavage of p220 by poliovirus 2A(pro) expression in mammalian cells: effects on vaccinia virus,” Biochemical and Biophysical Research Communications, vol. 215, no. 3, pp. 928–936, 1995. View at Publisher · View at Google Scholar
  132. I. Novoa, E. Feduchi, and L. Carrasco, “Hybrid proteins between pseudomonas exotoxin a and poliovirus protease 2A(pro),” FEBS Letters, vol. 355, no. 1, pp. 45–48, 1994. View at Publisher · View at Google Scholar
  133. E. Feduchi, R. Aldabe, I. Novoa, and L. Carrasco, “Effects of poliovirus 2A(pro) on vaccinia virus gene expression,” European Journal of Biochemistry, vol. 234, no. 3, pp. 849–854, 1995. View at Google Scholar
  134. E. Alvarez, L. Menéndez-Arias, and L. Carrasco, “The eukaryotic translation initiation factor 4GI is cleaved by different retroviral proteases,” Journal of Virology, vol. 77, no. 23, pp. 12392–12400, 2003. View at Publisher · View at Google Scholar
  135. I. Novoa, M. Cotten, and L. Carrasco, “Hybrid proteins between pseudomonas aeruginosa exotoxin A and poliovirus 2Apro cleave p220 in HeLa cells,” Journal of Virology, vol. 70, no. 5, pp. 3319–3324, 1996. View at Google Scholar
  136. I. Novoa and L. Carrasco, “Cleavage of eukaryotic translation initiation factor 4G by exogenously added hybrid proteins containing poliovirus 2A(pro) in HeLa cells: effects on gene expression,” Molecular and Cellular Biology, vol. 19, no. 4, pp. 2445–2454, 1999. View at Google Scholar
  137. A. Barco, E. Feduchi, and L. Carrasco, “A stable HeLa cell line that inducibly expresses poliovirus 2A(pro): effects on cellular and viral gene expression,” Journal of Virology, vol. 74, no. 5, pp. 2383–2392, 2000. View at Publisher · View at Google Scholar
  138. D. Goldstaub, A. Gradi, Z. Bercovitch et al., “Poliovirus 2A protease induces apoptotic cell death,” Molecular and Cellular Biology, vol. 20, no. 4, pp. 1271–1277, 2000. View at Publisher · View at Google Scholar
  139. F. Lejeune, A. C. Ranganathan, and L. E. Maquat, “eIF4G is required for the pioneer round of translation in mammalian cells,” Nature Structural and Molecular Biology, vol. 11, no. 10, pp. 992–1000, 2004. View at Publisher · View at Google Scholar · View at PubMed
  140. M. Joachims, P. C. Van Breugel, and R. E. Lloyd, “Cleavage of poly(A)-binding protein by enterovirus proteases concurrent with inhibition of translation in vitro,” Journal of Virology, vol. 73, no. 1, pp. 718–727, 1999. View at Google Scholar
  141. V. Kerekatte, B. D. Keiper, C. Badorff, A. Cat, K. U. Knowlton, and R. E. Rhoads, “Cleavage of poly(A)-binding protein by coxsackievirus 2A protease in vitro and in vivo: another mechanism for host protein synthesis shutoff?” Journal of Virology, vol. 73, no. 1, pp. 709–717, 1999. View at Google Scholar
  142. N. M. Kuyumcu-Martinez, M. Joachims, and R. E. Lloyd, “Efficient cleavage of ribosome-associated poly(A)-binding protein by enterovirus 3C protease,” Journal of Virology, vol. 76, no. 5, pp. 2062–2074, 2002. View at Publisher · View at Google Scholar
  143. N. M. Kuyumcu-Martinez, M. E. Van Eden, P. Younan, and R. E. Lloyd, “Cleavage of poly(A)-binding protein by poliovirus 3C protease inhibits host cell translation: a novel mechanism for host translation shutoff,” Molecular and Cellular Biology, vol. 24, no. 4, pp. 1779–1790, 2004. View at Publisher · View at Google Scholar
  144. R. Kirchweger, E. Ziegler, B. J. Lamphear et al., “Foot-and-mouth disease virus leader proteinase: purification of the Lb form and determination of its cleavage site on eIF-4γ,” Journal of Virology, vol. 68, no. 9, pp. 5677–5684, 1994. View at Google Scholar
  145. G. J. Belsham, G. M. McInerney, and N. Ross-Smith, “Foot-and-mouth disease virus 3C protease induces cleavage of translation initiation factors eIF4A and eIF4G within infected cells,” Journal of Virology, vol. 74, no. 1, pp. 272–280, 2000. View at Google Scholar
  146. A. Gradi, N. Foeger, R. Strong et al., “Cleavage of eukaryotic translation initiation factor 4GII within foot-and-mouth disease virus-infected cells: identification of the L-protease cleavage site in vitro,” Journal of Virology, vol. 78, no. 7, pp. 3271–3278, 2004. View at Publisher · View at Google Scholar
  147. R. Strong and G. J. Belsham, “Sequential modification of translation initiation factor elF4Gl by two different foot-and-mouth disease virus proteases within infected baby hamster kidney cells: identification of the 3C cleavage site,” Journal of General Virology, vol. 85, no. 10, pp. 2953–2962, 2004. View at Publisher · View at Google Scholar · View at PubMed
  148. D. Prevot, J. L. Darlix, and T. Ohlmann, “Conducting the initiation of protein synthesis: the role of eIF4G,” Biology of the Cell, vol. 95, no. 3-4, pp. 141–156, 2003. View at Publisher · View at Google Scholar
  149. I. Ventoso, R. Blanco, C. Perales, and L. Carrasco, “HIV-1 protease cleaves eukaryotic initiation factor 4G and inhibits cap-dependent translation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 23, pp. 12966–12971, 2001. View at Publisher · View at Google Scholar · View at PubMed
  150. T. Ohlmann, D. Prevot, D. Décimo et al., “In vitro cleavage of eIF4GI but not eIF4GII by HIV-1 protease and its effects on translation in the rabbit reticulocyte lysate system,” Journal of Molecular Biology, vol. 318, no. 1, pp. 9–20, 2002. View at Publisher · View at Google Scholar · View at PubMed
  151. C. Perales, L. Carrasco, and I. Ventoso, “Cleavage of eIF4G by HIV-1 protease: effects on translation,” FEBS Letters, vol. 533, no. 1-3, pp. 89–94, 2003. View at Publisher · View at Google Scholar
  152. E. Alvarez, A. Castelló, L. Menéndez-Arias, and L. Carrasco, “HIV protease cleaves poly(A)-binding protein,” Biochemical Journal, vol. 396, no. 2, pp. 219–226, 2006. View at Publisher · View at Google Scholar · View at PubMed
  153. Y. M. Michel, D. Poncet, M. Piron, K. M. Kean, and A. M. Borman, “Cap-poly(A) synergy in mammalian cell-free extracts. Investigation of the requirements for poly(A)-mediated stimulation of translation initiation,” Journal of Biological Chemistry, vol. 275, no. 41, pp. 32268–32276, 2000. View at Google Scholar
  154. M. López-Lastra, C. Gabus, and J. L. Darlix, “Characterization of an internal ribosomal entry segment within the 5' leader of avian reticuloendotheliosis virus type A RNA and development of novel MLV-REV-Based retroviral vectors,” Human Gene Therapy, vol. 8, no. 16, pp. 1855–1865, 1997. View at Google Scholar
  155. T. Ohlmann, M. Lopez-Lastra, and J. L. Darlix, “An internal ribosome entry segment promotes translation of the simian immunodeficiency virus genomic RNA,” Journal of Biological Chemistry, vol. 275, no. 16, pp. 11899–11906, 2000. View at Publisher · View at Google Scholar
  156. A. Brasey, M. Lopez-Lastra, T. Ohlmann et al., “The leader of human immunodeficiency virus type 1 genomic RNA harbors an internal ribosome entry segment that is active during the G/M phase of the cell cycle,” Journal of Virology, vol. 77, no. 7, pp. 3939–3949, 2003. View at Publisher · View at Google Scholar
  157. M. M. Willcocks, M. J. Carter, and L. O. Roberts, “Cleavage of eukaryotic initiation factor elF4G and inhibition of host-cell protein synthesis during feline calicivirus infection,” Journal of General Virology, vol. 85, no. 5, pp. 1125–1130, 2004. View at Publisher · View at Google Scholar
  158. M. Kuyumcu-Martinez, G. Belliot, S. V. Sosnovtsev, K. O. Chang, K. Y. Green, and R. E. Lloyd, “Calicivirus 3C-like proteinase inhibits cellular translation by cleavage of poly(A)-binding protein,” Journal of Virology, vol. 78, no. 15, pp. 8172–8182, 2004. View at Publisher · View at Google Scholar · View at PubMed
  159. K. E. Gustin and P. Sarnow, “Inhibition of nuclear import and alteration of nuclear pore complex composition by rhinovirus,” Journal of Virology, vol. 76, no. 17, pp. 8787–8796, 2002. View at Publisher · View at Google Scholar
  160. F. W. Porter and A. C. Palmenberg, “Leader-induced phosphorylation of nucleoporins correlates with nuclear trafficking inhibition by cardioviruses,” Journal of Virology, vol. 83, no. 4, pp. 1941–1951, 2009. View at Publisher · View at Google Scholar · View at PubMed
  161. C. Von Kobbe, J. M. A. Van Deursen, J. P. Rodrigues et al., “Vesicular stomatitis virus matrix protein inhibits host cell gene expression by targeting the nucleoporin Nup98,” Molecular Cell, vol. 6, no. 5, pp. 1243–1252, 2000. View at Google Scholar
  162. N. Satterly, P. L. Tsai, J. Van Deursen et al., “Influenza virus targets the mRNA export machinery and the nuclear pore complex,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 6, pp. 1853–1858, 2007. View at Publisher · View at Google Scholar · View at PubMed
  163. A. Köhler and E. Hurt, “Exporting RNA from the nucleus to the cytoplasm,” Nature Reviews Molecular Cell Biology, vol. 8, no. 10, pp. 761–773, 2007. View at Publisher · View at Google Scholar · View at PubMed
  164. L. J. Terry, E. B. Shows, and S. R. Wente, “Crossing the nuclear envelope: hierarchical regulation of nucleocytoplasmic transport,” Science, vol. 318, no. 5855, pp. 1412–1416, 2007. View at Publisher · View at Google Scholar · View at PubMed
  165. M. P. Rout, J. D. Aitchison, A. Suprapto, K. Hjertaas, Y. Zhao, and B. T. Chait, “The yeast nuclear pore complex: composition, architecture, transport mechanism,” Journal of Cell Biology, vol. 148, no. 4, pp. 635–651, 2000. View at Publisher · View at Google Scholar
  166. J. M. Cronshaw, A. N. Krutchinsky, W. Zhang, B. T. Chait, and M. L. J. Matunis, “Proteomic analysis of the mammalian nuclear pore complex,” Journal of Cell Biology, vol. 158, no. 5, pp. 915–927, 2002. View at Publisher · View at Google Scholar · View at PubMed
  167. S. Wälde and R. H. Kehlenbach, “The Part and the Whole: functions of nucleoporins in nucleocytoplasmic transport,” Trends in Cell Biology, vol. 20, pp. 461–469, 2010. View at Publisher · View at Google Scholar · View at PubMed
  168. N. Panté and M. Kann, “Nuclear pore complex is able to transport macromolecules with diameters of about 39 nm,” Molecular Biology of the Cell, vol. 13, no. 2, pp. 425–434, 2002. View at Publisher · View at Google Scholar · View at PubMed
  169. H. Fried and U. Kutay, “Nucleocytoplasmic transport: taking an inventory,” Cellular and Molecular Life Sciences, vol. 60, no. 8, pp. 1659–1688, 2003. View at Publisher · View at Google Scholar · View at PubMed
  170. C. Strambio-De-Castillia, M. Niepel, and M. P. Rout, “The nuclear pore complex: bridging nuclear transport and gene regulation,” Nature Reviews Molecular Cell Biology, vol. 11, no. 7, pp. 490–501, 2010. View at Publisher · View at Google Scholar · View at PubMed
  171. B. Friedrich, C. Quensel, T. Sommer, E. Hartmann, and M. Köhler, “Nuclear localization signal and protein context both mediate importin α specificity of nuclear import substrates,” Molecular and Cellular Biology, vol. 26, no. 23, pp. 8697–8709, 2006. View at Publisher · View at Google Scholar · View at PubMed
  172. I. K. H. Poon and D. A. Jans, “Regulation of nuclear transport: central role in development and transformation?” Traffic, vol. 6, no. 3, pp. 173–186, 2005. View at Publisher · View at Google Scholar · View at PubMed
  173. M. Kanai, K. Hanashiro, S. H. Kim et al., “Inhibition of Crm1-p53 interaction and nuclear export of p53 by poly(ADP-ribosyl)ation,” Nature Cell Biology, vol. 9, no. 10, pp. 1175–1183, 2007. View at Publisher · View at Google Scholar · View at PubMed
  174. W. A. Smith, B. T. Schurter, F. Wong-Staal, and M. David, “Arginine methylation of RNA helicase A determines its subcellular localization,” Journal of Biological Chemistry, vol. 279, no. 22, pp. 22795–22798, 2004. View at Publisher · View at Google Scholar · View at PubMed
  175. U. Kutay, G. Lipowsky, E. Izaurralde et al., “Identification of a tRNA-specific nuclear export receptor,” Molecular Cell, vol. 1, no. 3, pp. 359–369, 1998. View at Google Scholar
  176. G. J. Arts, M. Fornerod, and I. W. Mattaj, “Identification of a nuclear export receptor for tRNA,” Current Biology, vol. 8, no. 6, pp. 305–314, 1998. View at Google Scholar
  177. A. Calado, N. Treichel, E. C. Müller, A. Otto, and U. Kutay, “Exportin-5-mediated nuclear export of eukaryotic elongation factor 1A and tRNA,” EMBO Journal, vol. 21, no. 22, pp. 6216–6224, 2002. View at Publisher · View at Google Scholar
  178. M. Ohno, A. Segref, A. Bachi, M. Wilm, and I. W. Mattaj, “PHAX, a mediator of U snRNA nuclear export whose activity is regulated by phosphorylation,” Cell, vol. 101, no. 2, pp. 187–198, 2000. View at Publisher · View at Google Scholar
  179. J. H. N. Ho, G. Kallstrom, and A. W. Johnson, “Nmd3p is a Crm1p-dependent adapter protein for nuclear export of the large ribosomal subunit,” Journal of Cell Biology, vol. 151, no. 5, pp. 1057–1066, 2000. View at Publisher · View at Google Scholar
  180. T. A. Nissan, J. Baßler, E. Petfalski, D. Tollervey, and E. Hurt, “60S pre-ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm,” EMBO Journal, vol. 21, no. 20, pp. 5539–5547, 2002. View at Publisher · View at Google Scholar
  181. J. Hedges, M. West, and A. W. Johnson, “Release of the export adapter, Nmd3p, from the 60S ribosomal subunit requires Rpl10p and the cytoplasmic GTPase Lsg1p,” EMBO Journal, vol. 24, no. 3, pp. 567–579, 2005. View at Publisher · View at Google Scholar · View at PubMed
  182. H. Cheng, K. Dufu, C. S. Lee, J. L. Hsu, A. Dias, and R. Reed, “Human mRNA export machinery recruited to the 5' end of mRNA,” Cell, vol. 127, no. 7, pp. 1389–1400, 2006. View at Publisher · View at Google Scholar · View at PubMed
  183. K. Strasser and E. Hurt, “Splicing factor Sub2p is required for nuclear mRNA export through its interaction with Yra1p,” Nature, vol. 413, no. 6856, pp. 648–652, 2001. View at Publisher · View at Google Scholar · View at PubMed
  184. H. Le Hir, D. Gatfield, E. Izaurralde, and M. J. Moore, “The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay,” EMBO Journal, vol. 20, no. 17, pp. 4987–4997, 2001. View at Publisher · View at Google Scholar · View at PubMed
  185. N. Kataoka, M. D. Diem, V. N. Kim, J. Yong, and G. Dreyfuss, “Magoh, a human homolog of Drosophila mago nashi protein, is a component of the splicing-dependent exon-exon junction complex,” EMBO Journal, vol. 20, no. 22, pp. 6424–6433, 2001. View at Publisher · View at Google Scholar · View at PubMed
  186. K. N. Clouse, M. J. Luo, Z. Zhou, and R. Reed, “A Ran-independent pathway for export of spliced mRNA,” Nature Cell Biology, vol. 3, no. 1, pp. 97–99, 2001. View at Publisher · View at Google Scholar · View at PubMed
  187. I. E. Gallouzi and J. A. Steitz, “Delineation of mRNA export pathways by the use of cell-permeable peptides,” Science, vol. 294, no. 5548, pp. 1895–1901, 2001. View at Publisher · View at Google Scholar · View at PubMed
  188. S. Waggoner and P. Sarnow, “Viral ribonucleoprotein complex formation and nucleolar-cytoplasmic relocalization of nucleolin in poliovirus-infected cells,” Journal of Virology, vol. 72, no. 8, pp. 6699–6709, 1998. View at Google Scholar
  189. K. E. Gustin, “Inhibition of nucleo-cytoplasmic trafficking by RNA viruses: targeting the nuclear pore complex,” Virus Research, vol. 95, no. 1-2, pp. 35–44, 2003. View at Publisher · View at Google Scholar
  190. K. Meerovitch, J. Pelletier, and N. Sonenberg, “A cellular protein that binds to the 5'-noncoding region of poliovirus RNA: implications for internal translation initiation,” Genes & Development, vol. 3, no. 7, pp. 1026–1034, 1989. View at Google Scholar
  191. C. U. T. Hellen, G. W. Witherell, M. Schmid et al., “A cytoplasmic 57-kDa protein that is required for translation of picornavirus RNA by internal ribosomal entry is identical to the nuclear pyrimidine tract-binding protein,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 16, pp. 7642–7646, 1993. View at Google Scholar
  192. A. E. Mcbride, A. Schlegel, and K. Kirkegaard, “Human protein Sam68 relocalization and interaction with poliovirus RNA polymerase in infected cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 6, pp. 2296–2301, 1996. View at Publisher · View at Google Scholar
  193. K. Shiroki, T. Isoyama, S. Kuge et al., “Intracellular redistribution of truncated La protein produced by poliovirus 3C(pro)-mediated cleavage,” Journal of Virology, vol. 73, no. 3, pp. 2193–2200, 1999. View at Google Scholar
  194. A. E. McBride, S. J. Taylor, D. Shalloway, and K. Kirkegaard, “KH domain integrity is required for wild-type localization of Sam68,” Experimental Cell Research, vol. 241, no. 1, pp. 84–95, 1998. View at Publisher · View at Google Scholar · View at PubMed
  195. S. H. Back, Y. K. Kim, W. J. Kim et al., “Translation of polioviral mRNA is inhibited by cleavage of polypyrimidine tract-binding proteins executed by polioviral 3C(pro),” Journal of Virology, vol. 76, no. 5, pp. 2529–2542, 2002. View at Publisher · View at Google Scholar
  196. G. A. Belov, P. V. Lidsky, O. V. Mikitas et al., “Bidirectional increase in permeability of nuclear envelope upon poliovirus infection and accompanying alterations of nuclear pores,” Journal of Virology, vol. 78, no. 18, pp. 10166–10177, 2004. View at Publisher · View at Google Scholar · View at PubMed
  197. P. Ranjan, J. B. Bowzard, J. W. Schwerzmann, V. Jeisy-Scott, T. Fujita, and S. Sambhara, “Cytoplasmic nucleic acid sensors in antiviral immunity,” Trends in Molecular Medicine, vol. 15, no. 8, pp. 359–368, 2009. View at Publisher · View at Google Scholar · View at PubMed
  198. J. R. Ball and K. S. Ullman, “Versatility at the nuclear pore complex: lessons learned from the nucleoporin Nup153,” Chromosoma, vol. 114, no. 5, pp. 319–330, 2005. View at Publisher · View at Google Scholar · View at PubMed
  199. B. Buendia, A. Santa-Maria, and J. C. Courvalin, “Caspase-dependent proteolysis of integral and peripheral proteins of nuclear membranes and nuclear pore complex proteins during apoptosis,” Journal of Cell Science, vol. 112, no. 11, pp. 1743–1753, 1999. View at Google Scholar
  200. N. Park, T. Skern, and K. E. Gustin, “Specific cleavage of the nuclear pore complex protein Nup62 by a viral protease,” Journal of Biological Chemistry, vol. 285, no. 37, pp. 28796–28805, 2010. View at Publisher · View at Google Scholar · View at PubMed
  201. J. Enninga, D. E. Levy, G. Blobel, and B. M. A. Fontoura, “Role of nucleoporin induction in releasing an mRNA nuclear export block,” Science, vol. 295, no. 5559, pp. 1523–1525, 2002. View at Publisher · View at Google Scholar · View at PubMed
  202. P. V. Lidsky, S. Hato, M. V. Bardina et al., “Nucleocytoplasmic traffic disorder induced by cardioviruses,” Journal of Virology, vol. 80, no. 6, pp. 2705–2717, 2006. View at Publisher · View at Google Scholar · View at PubMed
  203. F. W. Porter, Y. A. Bochkov, A. J. Albee, C. Wiese, and A. C. Palmenberg, “A picornavirus protein interacts with Ran-GTPase and disrupts nucleocytoplasmic transport,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 33, pp. 12417–12422, 2006. View at Publisher · View at Google Scholar · View at PubMed
  204. C. M. T. Dvorak, D. J. Hall, M. Hill et al., “Leader protein of encephalomyocarditis virus binds zinc, is phosphorylated during viral infection, and affects the efficiency of genome translation,” Virology, vol. 290, no. 2, pp. 261–271, 2001. View at Publisher · View at Google Scholar · View at PubMed
  205. L. S. Her, E. Lund, and J. E. Dahlberg, “Inhibition of ran guanosine triphosphatase-dependent nuclear transport by the matrix protein of vesicular stomatitis virus,” Science, vol. 276, no. 5320, pp. 1845–1848, 1997. View at Publisher · View at Google Scholar
  206. P. A. Faria, P. Chakraborty, A. Levay et al., “VSV disrupts the Rae1/mrnp41 mRNA nuclear export pathway,” Molecular Cell, vol. 17, no. 1, pp. 93–102, 2005. View at Publisher · View at Google Scholar · View at PubMed
  207. P. Fortes, A. Beloso, and J. Ortin, “Influenza virus NS1 protein inhibits pre-mRNA splicing and blocks mRNA nucleocytoplasmic transport,” EMBO Journal, vol. 13, no. 3, pp. 704–712, 1994. View at Google Scholar
  208. A. Pichlmair, O. Schulz, C. P. Tan et al., “RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates,” Science, vol. 314, no. 5801, pp. 997–1001, 2006. View at Publisher · View at Google Scholar · View at PubMed
  209. M. Mibayashi, L. Martínez-Sobrido, Y. M. Loo, W. B. Cárdenas, M. Gale Jr., and A. García-Sastre, “Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus,” Journal of Virology, vol. 81, no. 2, pp. 514–524, 2007. View at Publisher · View at Google Scholar · View at PubMed
  210. C. Carissimi, L. Saieva, J. Baccon et al., “Gemin8 is a novel component of the survival motor neuron complex and functions in small nuclear ribonucleoprotein assembly,” Journal of Biological Chemistry, vol. 281, no. 12, pp. 8126–8134, 2006. View at Publisher · View at Google Scholar · View at PubMed
  211. C. Carissimi, L. Saieva, F. Gabanella, and L. Pellizzoni, “Gemin8 is required for the architecture and function of the survival motor neuron complex,” Journal of Biological Chemistry, vol. 281, no. 48, pp. 37009–37016, 2006. View at Publisher · View at Google Scholar · View at PubMed
  212. G. Meister, D. Bühler, R. Pillai, F. Lottspeich, and U. Fischer, “A multiprotein complex mediates the ATP-dependent assembly of spliceosomal U snRNPs,” Nature Cell Biology, vol. 3, no. 11, pp. 945–949, 2001. View at Publisher · View at Google Scholar · View at PubMed
  213. G. Meister, S. Hannus, O. Plöttner et al., “SMNrp is an essential pre-mRNA splicing factor required for the formation of the mature spliceosome,” EMBO Journal, vol. 20, no. 9, pp. 2304–2314, 2001. View at Publisher · View at Google Scholar · View at PubMed
  214. T. J. Golembe, J. Yong, and G. Dreyfuss, “Specific sequence features, recognized by the SMN complex, identify snRNAs and determine their fate as snRNPs,” Molecular and Cellular Biology, vol. 25, no. 24, pp. 10989–11004, 2005. View at Publisher · View at Google Scholar · View at PubMed
  215. T. Kiss, “Biogenesis of small nuclear RNPs,” Journal of Cell Science, vol. 117, no. 25, pp. 5949–5951, 2004. View at Publisher · View at Google Scholar · View at PubMed
  216. L. L. Almstead and P. Sarnow, “Inhibition of U snRNP assembly by a virus-encoded proteinase,” Genes and Development, vol. 21, no. 9, pp. 1086–1097, 2007. View at Publisher · View at Google Scholar · View at PubMed
  217. P. Yalamanchili, R. Banerjee, and A. Dasgupta, “Poliovirus-encoded protease 2A(Pro) cleaves the TATA-binding protein but does not inhibit host cell RNA polymerase II transcription in vitro,” Journal of Virology, vol. 71, no. 9, pp. 6881–6886, 1997. View at Google Scholar
  218. M. K. Weidman, R. Sharma, S. Raychaudhuri, P. Kundu, W. Tsai, and A. Dasgupta, “The interaction of cytoplasmic RNA viruses with the nucleus,” Virus Research, vol. 95, no. 1-2, pp. 75–85, 2003. View at Publisher · View at Google Scholar
  219. N. Blom, J. Hansen, D. Blaas, and S. Brunak, “Cleavage site analysis in picornaviral polyproteins: discovering cellular targets by neural networks,” Protein Science, vol. 5, no. 11, pp. 2203–2216, 1996. View at Google Scholar
  220. C. Badorff, G. H. Lee, B. J. Lamphear et al., “Enteroviral protease 2A cleaves dystrophin: evidence of cytoskeletal disruption in an acquired cardiomyopathy,” Nature Medicine, vol. 5, no. 3, pp. 320–326, 1999. View at Publisher · View at Google Scholar · View at PubMed
  221. J. Seipelt, H. D. Liebig, W. Sommergruber, C. Gerner, and E. Kuechler, “2A proteinase of human rhinovirus cleaves cytokeratin 8 in infected HeLa cells,” Journal of Biological Chemistry, vol. 275, no. 26, pp. 20084–20089, 2000. View at Publisher · View at Google Scholar