Roles of nuclear trafficking in infection by cytoplasmic negative-strand RNA viruses: Paramyxoviruses and beyond

Journal of General Virology

Volumn 97, Issue 10, 2016, Pages 2463-2481

  Audsley, Michelle D ^a   Jans, David A ^a   Moseley, Gregory W ^b  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Importin; Lyssavirus; Negative strand RNA virus; Nuclear import; Nucleus; Paramyxovirus

Indexed keywords

ISOPROTEIN; MATRIX PROTEIN; NUCLEOCAPSID PROTEIN; VIRAL PROTEIN; VIRUS PHOSPHOPROTEIN; VIRUS PROTEIN V;

CELL TRANSPORT; DRUG TARGETING; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNE EVASION; MORBILLIVIRUS; NEGATIVE-STRAND RNA VIRUS; NIPAH VIRUS; NONHUMAN; NUCLEAR TRAFFICKING; NUCLEOCYTOPLASMIC TRANSPORT; PARAMYXOVIRIDAE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REVIEW; RNA VIRUS INFECTION; VIRUS ASSEMBLY; VIRUS REPLICATION; ANIMAL; CELL NUCLEUS; CYTOPLASM; GENETICS; HUMAN; PARAMYXOVIRINAE; PARAMYXOVIRUS INFECTION; PHYSIOLOGY; VIROLOGY;

ANIMALS; CELL NUCLEUS; CYTOPLASM; HUMANS; PARAMYXOVIRIDAE INFECTIONS; PARAMYXOVIRINAE; VIRUS ASSEMBLY;

EID: 84991736601     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/jgv.0.000575     Document Type: Review

References (172)

1. Alvisi, G., Jans, D. A., Guo, J., Pinna, L. A. & Ripalti, A. (2005). A protein kinase CK2 site flanking the nuclear targeting signal enhances nuclear transport of human cytomegalovirus ppUL44. Traffic 6, 1002-1013.
2. Amorim, M. J. & Digard, P. (2006). Influenza A virus and the cell nucleus. Vaccine 24, 6651-6655.
3. Andrejeva, J., Childs, K. S., Young, D. F., Carlos, T. S., Stock, N., Goodbourn, S. & Randall, R. E. (2004). The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, MDA-5, and inhibit its activation of the IFN-beta promoter. Proc Natl Acad Sci U S A 101, 17264-17269.
4. Audsley, M. D. & Moseley, G. W. (2013). Paramyxovirus evasion of innate immunity: Diverse strategies for common targets. World J Virol 2, 57-70.
5. Audsley, M. D., Marsh, G. A., Lieu, K. G., Tachedjian, M., Joubert, D. A., Wang, L. F., Jans, D. A. & Moseley, G. W. (2016). The immune evasion function of J and Beilong virus V proteins is distinct from that of other paramyxoviruses, consistent with their inclusion in the proposed genus Jeilongvirus. J Gen Virol 97, 581-592.
6. Bankamp, B., Horikami, S. M., Thompson, P. D., Huber, M., Billeter, M. & Moyer, S. A. (1996). Domains of the measles virus N protein required for binding to P protein and self-assembly. Virology 216, 272-277.
7. Bankamp, B., Wilson, J., Bellini, W. J. & Rota, P. A. (2005). Identification of naturally occurring amino acid variations that affect the ability of the measles virus C protein to regulate genome replication and transcription. Virology 336, 120-129.
8. Bauer, A., Neumann, S., Karger, A., Henning, A. K., Maisner, A., Lamp, B., Dietzel, E., Kwasnitschka, L., Balkema-Buschmann, A. & other authors (2014). ANP32B is a nuclear target of henipavirus M proteins. PLoS One 9, e97233.
9. Bayliss, R., Littlewood, T. & Stewart, M. (2000). Structural basis for the interaction between FxFG nucleoporin repeats and importin-beta in nuclear trafficking. Cell 102, 99-108.
10. Beg, A. A., Ruben, S. M., Scheinman, R. I., Haskill, S., Rosen, C. A. & Baldwin, A. S. (1992). I kappa B interacts with the nuclear localization sequences of the subunits of NF-kappa B: A mechanism for cytoplasmic retention. Genes Dev 6, 1899-1913.
11. Bellini, W. J., Englund, G., Rozenblatt, S., Arnheiter, H. & Richardson, C. D. (1985). Measles virus P gene codes for two proteins. J Virol 53, 908-919.
12. Bernardi, R., Scaglioni, P. P., Bergmann, S., Horn, H. F., Vousden, K. H. & Pandolfi, P. P. (2004). PML regulates p53 stability by sequestering Mdm2 to the nucleolus. Nat Cell Biol 6, 665-672.
13. Bischoff, F. R., Krebber, H., Smirnova, E., Dong, W. & Ponstingl, H. (1995). Co-activation of RanGTPase and inhibition of GTP dissociation by Ran-GTP binding protein RanBP1. EMBO J 14, 705-715.
14. Blondel, D., Regad, T., Poisson, N., Pavie, B., Harper, F., Pandolfi, P. P., De Thé, H. & Chelbi-Alix, M. K. (2002). Rabies virus P and small P products interact directly with PML and reorganize PML nuclear bodies. Oncogene 21, 7957-7970.
15. Brice, A. & Moseley, G. (2013). Viral interactions with microtubules: Orchestrators of host cell biology? Future Virol 8, 229-243.
16. Briese, T., de la Torre, J. C., Lewis, A., Ludwig, H. & Lipkin, W. I. (1992). Borna disease virus, a negative-strand RNA virus, transcribes in the nucleus of infected cells. Proc Natl Acad Sci U S A 89, 11486-11489.
17. Brzózka, K., Finke, S. & Conzelmann, K. K. (2005). Identification of the rabies virus alpha/beta interferon antagonist: Phosphoprotein P interferes with phosphorylation of interferon regulatory factor 3. J Virol 79, 7673-7681.
18. Caignard, G., Guerbois, M., Labernardiére, J. L., Jacob, Y., Jones, L. M., Wild, F., Tangy, F., Vidalain, P. O. & Infectious Mapping Project I-MAP (2007). Measles virus V protein blocks Jak1-mediated phosphorylation of STAT1 to escape IFN-alpha/beta signaling. Virology 368, 351-362.
19. Caignard, G., Lucas-Hourani, M., Dhondt, K. P., Labernardiére, J. L., Petit, T., Jacob, Y., Horvat, B., Tangy, F. & Vidalain, P. O. (2013). The V protein of Tioman virus is incapable of blocking type I interferon signaling in human cells. PLoS One 8, e53881.
20. Calado, A., Treichel, N., Müller, E. C., Otto, A. & Kutay, U. (2002). Exportin-5-mediated nuclear export of eukaryotic elongation factor 1A and tRNA. EMBO J 21, 6216-6224.
21. Chelsky, D., Ralph, R. & Jonak, G. (1989). Sequence requirements for synthetic peptide-mediated translocation to the nucleus. Mol Cell Biol 9, 2487-2492.
22. Chenik, M., Chebli, K. & Blondel, D. (1995). Translation initiation at alternate in-frame AUG codons in the rabies virus phosphoprotein mRNA is mediated by a ribosomal leaky scanning mechanism. J Virol 69, 707-712.
23. Childs, K., Stock, N., Ross, C., Andrejeva, J., Hilton, L., Skinner, M., Randall, R. & Goodbourn, S. (2007). Mda-5, but not RIG-I, is a common target for paramyxovirus V proteins. Virology 359, 190-200.
24. Childs, K., Randall, R. & Goodbourn, S. (2012). Paramyxovirus V proteins interact with the RNA helicase LGP2 to inhibit RIG-I-dependent interferon induction. J Virol 86, 3411-3421.
25. Chinnakannan, S. K., Holzer, B., Bernardo, B. S., Nanda, S. K. & Baron, M. D. (2014). Different functions of the common P/V/W and Vspecific domains of rinderpest virus V protein in blocking IFN signalling. J Gen Virol 95, 44-51.
26. Chui, L. W., Vainionpää, R., Marusyk, R., Salmi, A. & Norrby, E. (1986). Nuclear accumulation of measles virus nucleoprotein associated with a temperature-sensitive mutant. J Gen Virol 67, 2153-2161.
27. Ciancanelli, M. J. & Basler, C. F. (2006). Mutation of YMYL in the Nipah virus matrix protein abrogates budding and alters subcellular localization. J Virol 80, 12070-12078.
28. Ciancanelli, M. J., Volchkova, V. A., Shaw, M. L., Volchkov, V. E. & Basler, C. F. (2009). Nipah virus sequesters inactive STAT1 in the nucleus via a P gene-encoded mechanism. J Virol 83, 7828-7841.
29. Coleman, N. A. & Peeples, M. E. (1993). The matrix protein of Newcastle disease virus localizes to the nucleus via a bipartite nuclear localization signal. Virology 195, 596-607.
30. Deffrasnes, C., Marsh, G. A., Foo, C. H., Rootes, C. L., Gould, C. M., Grusovin, J., Monaghan, P., Lo, M. K., Tompkins, S. M. & other authors (2016). Genome-wide siRNA screening at biosafety level 4 reveals a crucial role for fibrillarin in henipavirus infection. PLoS Pathog 12, e1005478.
31. Didcock, L., Young, D. F., Goodbourn, S. & Randall, R. E. (1999). The V protein of simian virus 5 inhibits interferon signalling by targeting STAT1 for proteasome-mediated degradation. J Virol 73, 9928-9933.
32. Duan, Z., Song, Q., Wang, Y., He, L., Chen, J., Zhu, Y., Hu, S. & Liu, X. (2013). Characterization of signal sequences determining the nuclear export of Newcastle disease virus matrix protein. Arch Virol 158, 2589-2595.
33. Fagotto, F., Glück, U. & Gumbiner, B. M. (1998). Nuclear localization signal-independent and importin/karyopherin-independent nuclear import of beta-catenin. Curr Biol 8, 181-190.
34. Ferran, M. C. & Lucas-Lenard, J. M. (1997). The vesicular stomatitis virus matrix protein inhibits transcription from the human beta interferon promoter. J Virol 71, 371-377.
35. Follett, E. A., Pringle, C. R., Wunner, W. H. & Skehel, J. J. (1974). Virus replication in enucleate cells: Vesicular stomatitis virus and influenza virus. J Virol 13, 394-399.
36. Follett, E. A., Pringle, C. R. & Pennington, T. H. (1976). Events following the infections of enucleate cells with measles virus. J Gen Virol 32, 163-175.
37. Fooks, A. R., Banyard, A. C., Horton, D. L., Johnson, N., McElhinney, L. M. & Jackson, A. C. (2014). Current status of rabies and prospects for elimination. Lancet 384, 1389-1399.
38. Fulcher, A. J., Roth, D. M., Fatima, S., Alvisi, G. & Jans, D. A. (2010). The BRCA-1 binding protein BRAP2 is a novel, negative regulator of nuclear import of viral proteins, dependent on phosphorylation flanking the nuclear localization signal. FASEB J 24, 1454-1466.
39. Garcin, D., Marq, J. B., Strahle, L., le Mercier, P. & Kolakofsky, D. (2002). All four Sendai Virus C proteins bind Stat1, but only the larger forms also induce its mono-ubiquitination and degradation. Virology 295, 256-265.
40. Ghildyal, R., Mills, J., Murray, M., Vardaxis, N. & Meanger, J. (2002). Respiratory syncytial virus matrix protein associates with nucleocapsids in infected cells. J Gen Virol 83, 753-757.
41. Ghildyal, R., Baulch-Brown, C., Mills, J. & Meanger, J. (2003). The matrix protein of human respiratory syncytial virus localises to the nucleus of infected cells and inhibits transcription. Arch Virol 148, 1419-1429.
42. Ghildyal, R., Ho, A., Wagstaff, K. M., Dias, M. M., Barton, C. L., Jans, P., Bardin, P. & Jans, D. A. (2005). Nuclear import of the respiratory syncytial virus matrix protein is mediated by importin beta1 independent of importin alpha. Biochemistry 44, 12887-12895.
43. Ghildyal, R., Ho, A., Dias, M., Soegiyono, L., Bardin, P. G., Tran, K. C., Teng, M. N. & Jans, D. A. (2009). The respiratory syncytial virus matrix protein possesses a Crm1-mediated nuclear export mechanism. J Virol 83, 5353-5362.
44. Glodowski, D. R., Petersen, J. M. & Dahlberg, J. E. (2002). Complex nuclear localization signals in the matrix protein of vesicular stomatitis virus. J Biol Chem 277, 46864-46870.
45. Goodbourn, S. & Randall, R. E. (2009). The regulation of type I interferon production by paramyxoviruses. J Interferon Cytokine Res 29, 539-547.
46. Grogan, C. C. & Moyer, S. A. (2001). Sendai virus wild-type and mutant C proteins show a direct correlation between L polymerase binding and inhibition of viral RNA synthesis. Virology 288, 96-108.
47. Hagmaier, K., Stock, N., Precious, B., Childs, K., Wang, L. F., Goodbourn, S. & Randall, R. E. (2007). Mapuera virus, a rubulavirus that inhibits interferon signalling in a wide variety of mammalian cells without degrading STATs. J Gen Virol 88, 956-966.
48. Hausmann, S., Garcin, D., Delenda, C. & Kolakofsky, D. (1999). The versatility of paramyxovirus RNA polymerase stuttering. J Virol 73, 5568-5576.
49. Her, L. S., Lund, E. & Dahlberg, J. E. (1997). Inhibition of Ran guanosine triphosphatase-dependent nuclear transport by the matrix protein of vesicular stomatitis virus. Science 276, 1845-1848.
50. Holaska, J. M., Black, B. E., Love, D. C., Hanover, J. A., Leszyk, J. & Paschal, B. M. (2001). Calreticulin Is a receptor for nuclear export. J Cell Biol 152, 127-140.
51. Horikami, S. M., Hector, R. E., Smallwood, S. & Moyer, S. A. (1997). The Sendai virus C protein binds the L polymerase protein to inhibit viral RNA synthesis. Virology 235, 261-270.
52. Hübner, S., Xiao, C. Y. & Jans, D. A. (1997). The protein kinase CK2 site (Ser111/112) enhances recognition of the simian virus 40 large T-antigen nuclear localization sequence by importin. J Biol Chem 272, 17191-17195.
53. Irie, T., Nagata, N., Yoshida, T. & Sakaguchi, T. (2008). Recruitment of Alix/AIP1 to the plasma membrane by Sendai virus C protein facilitates budding of virus-like particles. Virology 371, 108-120.
54. Irie, T., Kiyotani, K., Igarashi, T., Yoshida, A. & Sakaguchi, T. (2012). Inhibition of interferon regulatory factor 3 activation by paramyxovirus V protein. J Virol 86, 7136-7145.
55. Irie, T., Yoshida, A. & Sakaguchi, T. (2013). Clustered basic amino acids of the small sendai virus C protein Y1 are critical to its RAN GTPase-mediated nuclear localization. PLoS One 8, e73740.
56. Ito, M., Takeuchi, T., Nishio, M., Kawano, M., Komada, H., Tsurudome, M. & Ito, Y. (2004). Early stage of establishment of persistent Sendai virus infection: Unstable dynamic phase and then selection of viruses which are tightly cell associated, temperature sensitive, and capable of establishing persistent infection. J Virol 78, 11939-11951.
57. Ito, M., Iwasaki, M., Takeda, M., Nakamura, T., Yanagi, Y. & Ohno, S. (2013). Measles virus nonstructural C protein modulates viral RNA polymerase activity by interacting with host protein SHCBP1. J Virol 87, 9633-9642.
58. Ito, N., Moseley, G. W., Blondel, D., Shimizu, K., Rowe, C. L., Ito, Y., Masatani, T., Nakagawa, K., Jans, D. A. & Sugiyama, M. (2010). Role of interferon antagonist activity of rabies virus phosphoprotein in viral pathogenicity. J Virol 84, 6699-6710.
59. Ito, N., Moseley, G. W. & Sugiyama, M. (2016). The importance of immune evasion in the pathogenesis of rabies virus. J Vet Med Sci 78, 1089-1098.
60. Iwasaki, M., Takeda, M., Shirogane, Y., Nakatsu, Y., Nakamura, T. & Yanagi, Y. (2009). The matrix protein of measles virus regulates viral RNA synthesis and assembly by interacting with the nucleocapsid protein. J Virol 83, 10374-10383.
61. Jacob, Y., Badrane, H., Ceccaldi, P. E. & Tordo, N. (2000). Cytoplasmic dynein LC8 interacts with lyssavirus phosphoprotein. J Virol 74, 10217-10222.
62. Joubert, D. A., Blasdell, K. R., Audsley, M. D., Trinidad, L., Monaghan, P., Dave, K. A., Lieu, K. G., Amos-Ritchie, R., Jans, D. A. & other authors (2014). Bovine ephemeral fever rhabdovirus a1 protein has viroporin-like properties and binds importin b1 and importin 7. J Virol 88, 1591-1603.
63. Jul-Larsen, A., Grudic, A., Bjerkvig, R. & Bøe, S. O. (2010). Subcellular distribution of nuclear import-defective isoforms of the promyelocytic leukemia protein. BMC Mol Biol 11, 89.
64. Kalderon, D., Roberts, B. L., Richardson, W. D. & Smith, A. E. (1984). A short amino acid sequence able to specify nuclear location. Cell 39, 499-509.
65. Kaur, G. & Jans, D. A. (2011). Dual nuclear import mechanisms of sex determining factor SRY: Intracellular Ca2+ as a switch. FASEB J 25, 665-675.
66. Kaur, G., Lieu, K. G. & Jans, D. A. (2013). 70-kDa heat shock cognate protein hsc70 mediates calmodulin-dependent nuclear import of the sex-determining factor SRY. J Biol Chem 288, 4148-4157.
67. Kelley, J. B., Talley, A. M., Spencer, A., Gioeli, D. & Paschal, B. M. (2010). Karyopherin alpha7 (KPNA7), a divergent member of the importin alpha family of nuclear import receptors. BMC Cell Biol 11, 63.
68. Kitamura, R., Sekimoto, T., Ito, S., Harada, S., Yamagata, H., Masai, H., Yoneda, Y. & Yanagi, K. (2006). Nuclear import of Epstein-Barr virus nuclear antigen 1 mediated by NPI-1 (Importin alpha5) is up-and down-regulated by phosphorylation of the nuclear localization signal for which Lys379 and Arg380 are essential. J Virol 80, 1979-1991.
69. Kubota, T., Yokosawa, N., Yokota, S. & Fujii, N. (2001). C terminal CYS-RICH region of mumps virus structural V protein correlates with block of interferon alpha and gamma signal transduction pathway through decrease of STAT 1-alpha. Biochem Biophys Res Commun 283, 255-259.
70. Kubota, T., Yokosawa, N., Yokota, S. & Fujii, N. (2002). Association of mumps virus V protein with RACK1 results in dissociation of STAT-1 from the alpha interferon receptor complex. J Virol 76, 12676-12682.
71. Kudo, N., Wolff, B., Sekimoto, T., Schreiner, E. P., Yoneda, Y., Yanagida, M., Horinouchi, S. & Yoshida, M. (1998). Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp Cell Res 242, 540-547.
72. La Cour, T., Kiemer, L., Mølgaard, A., Gupta, R., Skriver, K. & Brunak, S. (2004). Analysis and prediction of leucine-rich nuclear export signals. Protein Eng Des Sel 17, 527-536.
73. Lamb, R. A. & Parks, G. D. (2007). Paramyxoviridae: The viruses and their replication. In Fields Virology, 5th edn, Edited by D. M. Knipe & P. M. Howley. Philadelphia, PA: Lippincott Williams & Wilkins.
74. Lieu, K. G., Brice, A., Wiltzer, L., Hirst, B., Jans, D. A., Blondel, D. & Moseley, G. W. (2013). The rabies virus interferon antagonist P protein interacts with activated STAT3 and inhibits Gp130 receptor signaling. J Virol 87, 8261-8265.
75. Lieu, K. G., Shim, E. H., Wang, J., Lokareddy, R. K., Tao, T., Cingolani, G., Zambetti, G. P. & Jans, D. A. (2014). The p53-induced factor Ei24 inhibits nuclear import through an importin b-binding-like domain. J Cell Biol 205, 301-312.
76. Lim, R. Y., Aebi, U. & Fahrenkrog, B. (2008). Towards reconciling structure and function in the nuclear pore complex. Histochem Cell Biol 129, 105-116.
77. Liston, P., DiFlumeri, C. & Briedis, D. J. (1995). Protein interactions entered into by the measles virus P, V, and C proteins. Virus Res 38, 241-259.
78. Lo, M. K., Miller, D., Aljofan, M., Mungall, B. A., Rollin, P. E., Bellini, W. J. & Rota, P. A. (2010). Characterization of the antiviral and inflammatory responses against Nipah virus in endothelial cells and neurons. Virology 404, 78-88.
79. Lu, L. L., Puri, M., Horvath, C. M. & Sen, G. C. (2008). Select paramyxoviral V proteins inhibit IRF3 activation by acting as alternative substrates for inhibitor of kappaB kinase epsilon (IKKe)/TBK1. J Biol Chem 283, 14269-14276.
80. Ludlow, L. E., Lo, M. K., Rodriguez, J. J., Rota, P. A. & Horvath, C. M. (2008). Henipavirus V protein association with Polo-like kinase reveals functional overlap with STAT1 binding and interferon evasion. J Virol 82, 6259-6271.
81. Lyles, D. S., Puddington, L. & McCreedy, B. J. (1988). Vesicular stomatitis virusMprotein in the nuclei of infected cells. J Virol 62, 4387-4392.
82. Marchenko, N. D., Hanel, W., Li, D., Becker, K., Reich, N. & Moll, U. M. (2010). Stress-mediated nuclear stabilization of p53 is regulated by ubiquitination and importin-alpha3 binding. Cell Death Differ 17, 255-267.
83. Masatani, T., Ozawa, M., Yamada, K., Ito, N., Horie, M., Matsuu, A., Okuya, K., Tsukiyama-Kohara, K., Sugiyama, M. & Nishizono, A. (2016). Contribution of the interaction between the rabies virus P protein and I-kappa B kinase e to the inhibition of type I IFN induction signalling. J Gen Virol 97, 316-326.
84. Mashtalir, N., Daou, S., Barbour, H., Sen, N. N., Gagnon, J., Hammond-Martel, I., Dar, H. H., Therrien, M. & Affar, B. (2014). Autodeubiquitination protects the tumor suppressor BAP1 from cytoplasmic sequestration mediated by the atypical ubiquitin ligase UBE2O. Mol Cell 54, 392-406.
85. Mateo, M., Reid, S. P., Leung, L. W., Basler, C. F. & Volchkov, V. E. (2010). Ebolavirus VP24 binding to karyopherins is required for inhibition of interferon signaling. J Virol 84, 1169-1175.
86. Medzhitov, R. (2007). Recognition of microorganisms and activation of the immune response. Nature 449, 819-826.
87. Monaghan, P., Green, D., Pallister, J., Klein, R., White, J., Williams, C., McMillan, P., Tilley, L., Lampe, M. & other authors (2014). Detailed morphological characterisation of Hendra virus infection of different cell types using super-resolution and conventional imaging. Virol J 11, 200.
88. Moroianu, J., Blobel, G. & Radu, A. (1996). Nuclear protein import: Ran-GTP dissociates the karyopherin alphabeta heterodimer by displacing alpha from an overlapping binding site on beta. Proc Natl Acad Sci U S A 93, 7059-7062.
89. Mosammaparast, N. & Pemberton, L. F. (2004). Karyopherins: From nuclear-transport mediators to nuclear-function regulators. Trends Cell Biol 14, 547-556.
90. Moseley, G. W., Filmer, R. P., DeJesus, M. A. & Jans, D. A. (2007a). Nucleocytoplasmic distribution of rabies virus P-protein is regulated by phosphorylation adjacent to C-terminal nuclear import and export signals. Biochemistry 46, 12053-12061.
91. Moseley, G. W., Roth, D. M., DeJesus, M. A., Leyton, D. L., Filmer, R. P., Pouton, C. W. & Jans, D. A. (2007b). Dynein light chain association sequences can facilitate nuclear protein import. Mol Biol Cell 18, 3204-3213.
92. Moseley, G. W., Lahaye, X., Roth, D. M., Oksayan, S., Filmer, R. P., Rowe, C. L., Blondel, D. & Jans, D. A. (2009). Dual modes of rabies Pprotein association with microtubules: A novel strategy to suppress the antiviral response. J Cell Sci 122, 3652-3662.
93. Nakai, M. & Imagawa, D. T. (1969). Electron microscopy of measles virus replication. J Virol 3, 187-197.
94. Nanda, S. K. & Baron, M. D. (2006). Rinderpest virus blocks type I and type II interferon action: Role of structural and nonstructural proteins. J Virol 80, 7555-7568.
95. Nath, S. T. & Nayak, D. P. (1990). Function of two discrete regions is required for nuclear localization of polymerase basic protein 1 of A/WSN/ 33 influenza virus (H1 N1). Mol Cell Biol 10, 4139-4145.
96. Nishie, T., Nagata, K. & Takeuchi, K. (2007). The C protein of wild-type measles virus has the ability to shuttle between the nucleus and the cytoplasm. Microbes Infect 9, 344-354.
97. Nishio, M., Tsurudome, M., Ito, M., Kawano, M., Kusagawa, S., Komada, H. & Ito, Y. (1999). Isolation of monoclonal antibodies directed against the V protein of human parainfluenza virus type 2 and localization of the V protein in virus-infected cells. Med Microbiol Immunol 188, 79-82.
98. Nishio, M., Tsurudome, M., Ito, M., Kawano, M., Komada, H. & Ito, Y. (2003). Characterization of Sendai virus persistently infected L929 cells and Sendai virus pi strain: Recombinant Sendai viruses having Mpi protein shows lower cytotoxicity and are incapable of establishing persistent infection. Virology 314, 110-124.
99. Oglesbee, M. & Krakowka, S. (1993). Cellular stress response induces selective intranuclear trafficking and accumulation of morbillivirus major core protein. Lab Invest 68, 109-117.
100. Oksayan, S., Ito, N., Moseley, G. & Blondel, D. (2012a). Subcellular trafficking in rhabdovirus infection and immune evasion: A novel target for therapeutics. Infect Disord Drug Targets 12, 38-58.
101. Oksayan, S., Wiltzer, L., Rowe, C. L., Blondel, D., Jans, D. A. & Moseley, G. W. (2012b). A novel nuclear trafficking module regulates the nucleocytoplasmic localization of the rabies virus interferon antagonist, P protein. J Biol Chem 287, 28112-28121.
102. Oksayan, S., Nikolic, J., David, C. T., Blondel, D., Jans, D. A. & Moseley, G. W. (2015). Identification of a role for nucleolin in rabies virus infection. J Virol 89, 1939-1943.
103. Palmeri, D. & Malim, M. H. (1999). Importin beta can mediate the nuclear import of an arginine-rich nuclear localization signal in the absence of importin alpha. Mol Cell Biol 19, 1218-1225.
104. Palosaari, H., Parisien, J. P., Rodriguez, J. J., Ulane, C. M. & Horvath, C. M. (2003). STAT protein interference and suppression of cytokine signal transduction by measles virus V protein. J Virol 77, 7635-7644.
105. Pasdeloup, D., Poisson, N., Raux, H., Gaudin, Y., Ruigrok, R. W. & Blondel, D. (2005). Nucleocytoplasmic shuttling of the rabies virus P protein requires a nuclear localization signal and a CRM1-dependent nuclear export signal. Virology 334, 284-293.
106. Paterson, R. G., Leser, G. P., Shaughnessy, M. A. & Lamb, R. A. (1995). The paramyxovirus SV5 V protein binds two atoms of zinc and is a structural component of virions. Virology 208, 121-131.
107. Peeples, M. E., Wang, C., Gupta, K. C. & Coleman, N. (1992). Nuclear entry and nucleolar localization of the Newcastle disease virus (NDV) matrix protein occur early in infection and do not require other NDV proteins. J Virol 66, 3263-3269.
108. Pei, Z., Harrison, M. S. & Schmitt, A. P. (2011). Parainfluenza virus 5 M protein interaction with host protein 14-3-3 negatively affects virus particle formation. J Virol 85, 2050-2059.
109. Pentecost, M., Vashisht, A. A., Lester, T., Voros, T., Beaty, S. M., Park, A., Wang, Y. E., Yun, T. E., Freiberg, A. N. & other authors (2015). Evidence for ubiquitin-regulated nuclear and subnuclear trafficking among Paramyxovirinae matrix proteins. PLoS Pathog 11, e1004739.
110. Perwitasari, O., Johnson, S., Yan, X., Howerth, E., Shacham, S., Landesman, Y., Baloglu, E., McCauley, D., Tamir, S. & other authors (2014). Verdinexor, a novel selective inhibitor of nuclear export, reduces influenza a virus replication in vitro and in vivo. J Virol 88, 10228-10243.
111. Petersen, J. M., Her, L. S., Varvel, V., Lund, E. & Dahlberg, J. E. (2000). The matrix protein of vesicular stomatitis virus inhibits nucleocytoplasmic transport when it is in the nucleus and associated with nuclear pore complexes. Mol Cell Biol 20, 8590-8601.
112. Poon, I. K. & Jans, D. A. (2005). Regulation of nuclear transport: Central role in development and transformation? Traffic 6, 173-186.
113. Portner, A., Gupta, K. C., Seyer, J. M., Beachey, E. H. & Kingsbury, D. W. (1986). Localization and characterization of Sendai virus nonstructural C and C' proteins by antibodies against synthetic peptides. Virus Res 66, 109-121.
114. Pouton, C. W., Wagstaff, K. M., Roth, D. M., Moseley, G. W. & Jans, D. A. (2007). Targeted delivery to the nucleus. Adv Drug Deliv Rev 59, 698-717.
115. Precious, B., Young, D. F., Bermingham, A., Fearns, R., Ryan, M. & Randall, R. E. (1995). Inducible expression of the P, V, and NP genes of the paramyxovirus simian virus 5 in cell lines and an examination of NP-P and NP-V interactions. J Virol 69, 8001-8010.
116. Puri, M., Lemon, K., Duprex, W. P., Rima, B. K. & Horvath, C. M. (2009). A point mutation, E95D, in the mumps virus V protein disengages STAT3 targeting from STAT1 targeting. J Virol 83, 6347-6356.
117. Ramachandran, A., Parisien, J. P. & Horvath, C. M. (2008). STAT2 is a primary target for measles virus V protein-mediated alpha/beta interferon signaling inhibition. J Virol 82, 8330-8338.
118. Ramachandran, A. & Horvath, C. M. (2010). Dissociation of paramyxovirus interferon evasion activities: Universal and virus-specific requirements for conserved V protein amino acids in MDA5 interference. J Virol 84, 11152-11163.
119. Randall, R. E. & Bermingham, A. (1996). NP:P and NP:V interactions of the paramyxovirus simian virus 5 examined using a novel protein:protein capture assay. Virology 224, 121-129.
120. Rawlinson, S. M. & Moseley, G. W. (2015). The nucleolar interface of RNA viruses. Cell Microbiol 17, 1108-1120.
121. Redinbaugh, M. G. & Hogenhout, S. A. (2005). Plant rhabdoviruses. Curr Top Microbiol Immunol 292, 143-163.
122. Reich, N. C. & Liu, L. (2006). Tracking STAT nuclear traffic. Nat Rev Immunol 6, 602-612.
123. Reutter, G. L., Cortese-Grogan, C., Wilson, J. & Moyer, S. A. (2001). Mutations in the measles virus C protein that up regulate viral RNA synthesis. Virology 285, 100-109.
124. Rexach, M. & Blobel, G. (1995). Protein import into nuclei: Association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell 83, 683-692.
125. Rieder, M., Brzózka, K., Pfaller, C. K., Cox, J. H., Stitz, L. & Conzelmann, K. K. (2011). Genetic dissection of interferon-antagonistic functions of rabies virus phosphoprotein: Inhibition of interferon regulatory factor 3 activation is important for pathogenicity. J Virol 85, 842-852.
126. Robbins, J., Dilworth, S. M., Laskey, R. A. & Dingwall, C. (1991). Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: Identification of a class of bipartite nuclear targeting sequence. Cell 64, 615-623.
127. Rodríguez, J. A. (2014). Interplay between nuclear transport and ubiquitin/ SUMO modifications in the regulation of cancer-related proteins. Semin Cancer Biol 27, 11-19.
128. Rodriguez, J. J. & Horvath, C. M. (2004). Host evasion by emerging paramyxoviruses: Hendra virus and Nipah virus V proteins inhibit interferon signaling. Viral Immunol 17, 210-219.
129. Rodriguez, J. J., Cruz, C. D. & Horvath, C. M. (2004). Identification of the nuclear export signal and STAT-binding domains of the Nipah virus V protein reveals mechanisms underlying interferon evasion. J Virol 78, 5358-5367.
130. Roth, D. M., Moseley, G. W., Glover, D., Pouton, C. W. & Jans, D. A. (2007). A microtubule-facilitated nuclear import pathway for cancer regulatory proteins. Traffic 8, 673-686.
131. Roth, D. M., Harper, I., Pouton, C. W. & Jans, D. A. (2009). Modulation of nucleocytoplasmic trafficking by retention in cytoplasm or nucleus. J Cell Biochem 107, 1160-1167.
132. Röthlisberger, A., Wiener, D., Schweizer, M., Peterhans, E., Zurbriggen, A. & Plattet, P. (2010). Two domains of the V protein of virulent canine distemper virus selectively inhibit STAT1 and STAT2 nuclear import. J Virol 84, 6328-6343.
133. Rowe, C. L., Wagstaff, K. M., Oksayan, S., Glover, D. J., Jans, D. A. & Moseley, G. W. (2016). Nuclear trafficking of the rabies virus interferon antagonist P-protein is regulated by an importin-binding nuclear localization sequence in the C-terminal domain. PLoS One 11, e0150477.
134. Samuel, A. S., Paldurai, A., Kumar, S., Collins, P. L. & Samal, S. K. (2010). Complete genome sequence of avian paramyxovirus (APMV) serotype 5 completes the analysis of nine APMV serotypes and reveals the longest APMV genome. PLoS One 5, e9269.
135. Sato, H., Masuda, M., Miura, R., Yoneda, M. & Kai, C. (2006). Morbillivirus nucleoprotein possesses a novel nuclear localization signal and a CRM1-independent nuclear export signal. Virology 352, 121-130.
136. Schluederberg, A. & Chavanich, S. (1974). The role of the nucleus in measles virus replication. Med Microbiol Immunol 160, 85-90.
137. Schuhmann, K. M., Pfaller, C. K. & Conzelmann, K. K. (2011). The measles virus V protein binds to p65 (RelA) to suppress NF-kappaB activity. J Virol 85, 3162-3171.
138. Shaw, M. L., García-Sastre, A., Palese, P. & Basler, C. F. (2004). Nipah virus V andW proteins have a common STAT1-binding domain yet inhibit STAT1 activation from the cytoplasmic and nuclear compartments, respectively. J Virol 78, 5633-5641.
139. Shaw, M. L., Cardenas, W. B., Zamarin, D., Palese, P. & Basler, C. F. (2005). Nuclear localization of the Nipah virusWprotein allows for inhibition of both virus-and toll-like receptor 3-triggered signaling pathways. J Virol 79, 6078-6088.
140. Sleeman, K., Bankamp, B., Hummel, K. B., Lo, M. K., Bellini, W. J. & Rota, P. A. (2008). The C, V andWproteins of Nipah virus inhibit minigenome replication. J Gen Virol 89, 1300-1308.
141. Sparrer, K. M., Pfaller, C. K. & Conzelmann, K. K. (2012). Measles virus C protein interferes with Beta interferon transcription in the nucleus. J Virol 86, 796-805.
142. Stüven, T., Hartmann, E. & Görlich, D. (2003). Exportin 6: A novel nuclear export receptor that is specific for profilin.actin complexes. EMBO J 22, 5928-5940.
143. Sugai, A., Sato, H., Hagiwara, K., Kozuka-Hata, H., Oyama, M., Yoneda, M. & Kai, C. (2014). Newly identified minor phosphorylation site threonine-279 of measles virus nucleoprotein is a prerequisite for nucleocapsid formation. J Virol 88, 1140-1149.
144. Sun, W., McCrory, T. S., Khaw, W. Y., Petzing, S., Myers, T. & Schmitt, A. P. (2014). Matrix proteins of Nipah and Hendra viruses interact with beta subunits of AP-3 complexes. J Virol 88, 13099-13110.
145. Suryanarayana, K., Baczko, K., ter Meulen, V. & Wagner, R. R. (1994). Transcription inhibition and other properties of matrix proteins expressed by M genes cloned from measles viruses and diseased human brain tissue. J Virol 68, 1532-1543.
146. Swanson, J. A. & McNeil, P. L. (1987). Nuclear reassembly excludes large macromolecules. Science 238, 548-550.
147. Sweetman, D. A., Miskin, J. & Baron, M. D. (2001). Rinderpest virus C and V proteins interact with the major (L) component of the viral polymerase. Virology 281, 193-204.
148. Takayama, I., Sato, H., Watanabe, A., Omi-Furutani, M., Sugai, A., Kanki, K., Yoneda, M. & Kai, C. (2012). The nucleocapsid protein of measles virus blocks host interferon response. Virology 424, 45-55.
149. Tay, M. Y., Fraser, J. E., Chan, W. K., Moreland, N. J., Rathore, A. P., Wang, C., Vasudevan, S. G. & Jans, D. A. (2013). Nuclear localization of dengue virus (DENV) 1-4 non-structural protein 5; protection against all 4 DENV serotypes by the inhibitor Ivermectin. Antiviral Res 99, 301-306.
150. tenOever, B. R., Servant, M. J., Grandvaux, N., Lin, R. & Hiscott, J. (2002). Recognition of the measles virus nucleocapsid as a mechanism of IRF-3 activation. J Virol 76, 3659-3669.
151. Tober, C., Seufert, M., Schneider, H., Billeter, M. A., Johnston, I. C., Niewiesk, S., ter Meulen, V. & Schneider-Schaulies, S. (1998). Expression of measles virus V protein is associated with pathogenicity and control of viral RNA synthesis. J Virol 72, 8124-8132.
152. Ulane, C. M. & Horvath, C. M. (2002). Paramyxoviruses SV5 and HPIV2 assemble STAT protein ubiquitin ligase complexes from cellular components. Virology 304, 160-166.
153. Ulane, C. M., Rodriguez, J. J., Parisien, J. P. & Horvath, C. M. (2003). STAT3 ubiquitylation and degradation by mumps virus suppress cytokine and oncogene signaling. J Virol 77, 6385-6393.
154. Vidy, A., Chelbi-Alix, M. & Blondel, D. (2005). Rabies virus P protein interacts with STAT1 and inhibits interferon signal transduction pathways. J Virol 79, 14411-14420.
155. Walker, P. J., Dietzgen, R. G., Joubert, D. A. & Blasdell, K. R. (2011). Rhabdovirus accessory genes. Virus Res 162, 110-125.
156. Wang, P., Palese, P. & O’Neill, R. E. (1997). The NPI-1/NPI-3 (karyopherin alpha) binding site on the influenza a virus nucleoprotein NP is a nonconventional nuclear localization signal. J Virol 71, 1850-1856.
157. Wang, Y. E., Park, A., Lake, M., Pentecost, M., Torres, B., Yun, T. E., Wolf, M. C., Holbrook, M. R., Freiberg, A. N. & Lee, B. (2010). Ubiquitinregulated nuclear-cytoplasmic trafficking of the Nipah virus matrix protein is important for viral budding. PLoS Pathog 6, e1001186.
158. Wardrop, E. A. & Briedis, D. J. (1991). Characterization of V protein in measles virus-infected cells. J Virol 65, 3421-3428.
159. Watanabe, A., Yoneda, M., Ikeda, F., Sugai, A., Sato, H. & Kai, C. (2011). Peroxiredoxin 1 is required for efficient transcription and replication of measles virus. J Virol 85, 2247-2253.
160. Watanabe, N., Kawano, M., Tsurudome, M., Kusagawa, S., Nishio, M., Komada, H., Shima, T. & Ito, Y. (1996). Identification of the sequences responsible for nuclear targeting of the V protein of human parainfluenza virus type 2. J Gen Virol 77, 327-338.
161. Wiltzer, L., Larrous, F., Oksayan, S., Ito, N., Marsh, G. A., Wang, L. F., Blondel, D., Bourhy, H., Jans, D. A. & Moseley, G. W. (2012). Conservation of a unique mechanism of immune evasion across the lyssavirus genus. J Virol 86, 10194-10199.
162. World Health Organisation (2014). Measles: Factsheet No. 286: World Health Organisation. http://www.who.int/mediacentre/factsheets/fs286/en/ index.html.
163. Woo, P. C., Lau, S. K., Wong, B. H., Fan, R. Y., Wong, A. Y., Zhang, A. J., Wu, Y., Choi, G. K., Li, K. S. & other authors (2012). Feline morbillivirus, a previously undescribed paramyxovirus associated with tubulointerstitial nephritis in domestic cats. Proc Natl Acad Sci U S A 109, 5435-5440.
164. Xiao, C. Y., Hübner, S. & Jans, D. A. (1997). SV40 large tumor antigen nuclear import is regulated by the double-stranded DNA-dependent protein kinase site (serine 120) flanking the nuclear localization sequence. J Biol Chem 272, 22191-22198.
165. Xu, W., Edwards, M. R., Borek, D. M., Feagins, A. R., Mittal, A., Alinger, J. B., Berry, K. N., Yen, B., Hamilton, J. & other authors (2014). Ebola virus VP24 targets a unique NLS binding site on karyopherin alpha 5 to selectively compete with nuclear import of phosphorylated STAT1. Cell Host Microbe 16, 187-200.
166. Yamada, H., Hayata, S., Omata-Yamada, T., Taira, H., Mizumoto, K. & Iwasaki, K. (1990). Association of the Sendai virus C protein with nucleocapsids. Arch Virol 113, 245-253.
167. Yasuhara, N., Oka, M. & Yoneda, Y. (2009). The role of the nuclear transport system in cell differentiation. Semin Cell Dev Biol 20, 590-599.
168. Yi, R., Qin, Y., Macara, I. G. & Cullen, B. R. (2003). Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev 17, 3011-3016.
169. Yokota, S., Saito, H., Kubota, T., Yokosawa, N., Amano, K. & Fujii, N. (2003). Measles virus suppresses interferon-alpha signaling pathway: Suppression of Jak1 phosphorylation and association of viral accessory proteins, C and V, with interferon-alpha receptor complex. Virology 306, 135-146.
170. Yokoya, F., Imamoto, N., Tachibana, T. & Yoneda, Y. (1999). Beta-Catenin can be transported into the nucleus in a Ran-unassisted manner. Mol Biol Cell 10, 1119-1131.
171. Yoshida, T., Nagai Y’Yoshii, S., Maeno, K. & Matsumoto, T. (1976). Membrane (M) protein of HVJ (Sendai virus): Its role in virus assembly. Virology 71, 143-161.
172. Zhang, X., Bourhis, J. M., Longhi, S., Carsillo, T., Buccellato, M., Morin, B., Canard, B. & Oglesbee, M. (2005). Hsp72 recognizes a P binding motif in the measles virus N protein C-terminus. Virology 337, 162-174.