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Research Paper

Importin α5 negatively regulates importin β1-mediated nuclear import of Newcastle disease virus matrix protein and viral replication and pathogenicity in chicken fibroblasts

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Pages 783-803 | Received 09 Nov 2017, Accepted 28 Feb 2018, Published online: 24 Apr 2018

References

  • Miller PJ, Decanini EL, Afonso CL. Newcastle disease: evolution of genotypes and the related diagnostic challenges. Infect Genet Evol. 2010;10:26–35.
  • Ganar K, Das M, Sinha S, et al. Newcastle disease virus: current status and our understanding. Virus Res. 2014;184:71–81.
  • Duan ZQ, Xu HQ, Ji XQ, et al. Recombinant Newcastle disease virus-vectored vaccines against human and animal infectious diseases. Future Microbiol. 2015;10:1307–23.
  • Battisti AJ, Meng G, Winkler DC, et al. Structure and assembly of a paramyxovirus matrix protein. Proc Natl Acad Sci U S A. 2012;109:13996–4000.
  • Harrison MS, Sakaguchi T, Schmitt AP. Paramyxovirus assembly and budding: building particles that transmit infections. Int J Biochem Cell Biol. 2010;42:1416–29.
  • Pantua HD, McGinnes LW, Peeples ME, et al. Requirements for the assembly and release of Newcastle disease virus-like particles. J Virol. 2006;80:11062–73.
  • Peeples ME. Differential detergent treatment allows immunofluorescent localization of the Newcastle disease virus matrix protein within the nucleus of infected cells. Virology. 1988;162:255–9.
  • Peeples ME, Wang C, Gupta KC, et al. 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. 1992;66:3263–9.
  • Duan Z, Li QH, He L, et al. Application of green fluorescent protein-labeled assay for the study of subcellular localization of Newcastle disease virus matrix protein. J Virol Methods. 2013;194:118–22.
  • Ghildyal R, Baulch-Brown C, Mills J, et al. The matrix protein of human respiratory syncytial virus localises to the nucleus of infected cells and inhibits transcription. Arch Virol. 2003;148:1419–29.
  • Rajani KR, Pettit Kneller EL, McKenzie MO, et al. Complexes of vesicular stomatitis virus matrix protein with host Rae1 and Nup98 involved in inhibition of host transcription. PLoS Pathog. 2012;8:e1002929.
  • Iwasaki M, Takeda M, Shirogane Y, et al. The matrix protein of measles virus regulates viral RNA synthesis and assembly by interacting with the nucleocapsid protein. J Virol. 2009;83:10374–83.
  • Hiscox JA, Whitehouse A, Matthews DA. Nucleolar proteomics and viral infection. Proteomics. 2010;10:4077–86.
  • Rawlinson SM, Moseley GW. The nucleolar interface of RNA viruses. Cell Microbiol. 2015;17:1108–20.
  • Wulan WN, Heydet D, Walker EJ, et al. Nucleocytoplasmic transport of nucleocapsid proteins of enveloped RNA viruses. Front Microbiol. 2015;6:553.
  • Duan Z, Chen J, Xu H, et al. The nucleolar phosphoprotein B23 targets Newcastle disease virus matrix protein to the nucleoli and facilitates viral replication. Virology. 2014;452–453:212–22.
  • Coleman NA, Peeples ME. The matrix protein of Newcastle disease virus localizes to the nucleus via a bipartite nuclear localization signal. Virology. 1993;195:596–607.
  • Pouton CW, Wagstaff KM, Roth DM, et al. Targeted delivery to the nucleus. Adv Drug Deliv Rev. 2007;59:698–717.
  • Twyffels L, Gueydan C, Kruys V. Transportin-1 and Transportin-2: protein nuclear import and beyond. FEBS Lett. 2014;588:1857–68.
  • Miyamoto Y, Yamada K, Yoneda Y. Importin α: a key molecule in nuclear transport and non-transport functions. J Biochem. 2016;160:69–75.
  • Goldfarb DS, Corbett AH, Mason DA, et al. Importin α: a multipurpose nuclear-transport receptor. Trends Cell Biol. 2004;14:505–14.
  • Lange A, Mills RE, Lange CJ, et al. Classical nuclear localization signals: definition, function, and interaction with importin alpha. J Biol Chem. 2007;282:5101–5.
  • Xu DR, Farmer A, Chook YM. Recognition of nuclear targeting signals by karyopherin-β proteins. Curr Opin Struc Biol. 2010;20:782–90.
  • Lott K, Cingolani G. The importin beta binding domain as a master regulator of nucleocytoplasmic transport. Biochim Biophys Acta. 2011;1813:1578–92.
  • Soniat M, Chook YM. Nuclear localization signals for four distinct karyopherin-beta nuclear import systems. Biochem J. 2015;468:353–62.
  • Sekimoto T, Miyamoto Y, Arai S, et al. Importin alpha protein acts as a negative regulator for Snail protein nuclear import. J Biol Chem. 2011;286:15126–31.
  • Forwood JK, Jans DA. Nuclear import pathway of the telomere elongation suppressor TRF1: inhibition by importin alpha. Biochemistry. 2002;41:9333–40.
  • Lopez-Denman AJ, Mackenzie JM. The importance of the nucleus during flavivirus replication. Viruses. 2017;9:e14.
  • Tu MY, Liu F, Chen S, et al. Role of capsid proteins in parvoviruses infection. Virol J. 2015;12:114.
  • Wang C, Zhu CX, Wei F, et al. Nuclear localization and cleavage of STAT6 is induced by Kaposi's sarcoma-associated herpesvirus for viral latency. PLoS Pathog. 2017;13:e1006124.
  • Widana Gamage SMK, Dietzgen RG. Intracellular localization, interactions and functions of Capsicum chlorosis virus proteins. Front Microbiol. 2017;8:612.
  • Lee C, Hodgins D, Calvert JG, et al. Mutations within the nuclear localization signal of the porcine reproductive and respiratory syndrome virus nucleocapsid protein attenuate virus replication. Virology. 2006;346:238–50.
  • Mori Y, Okabayashi T, Yamashita T, et al. Nuclear localization of Japanese encephalitis virus core protein enhances viral replication. J Virol. 2005;79:3448–58.
  • Katoh H, Okamoto T, Fukuhara T, et al. Japanese encephalitis virus core protein inhibits stress granule formation through an interaction with caprin-1 and facilitates viral propagation. J Virol. 2013;87:489–502.
  • Ghildyal R, Ho A, Wagstaff KM, et al. Nuclear import of the respiratory syncytial virus matrix protein is mediated by importin beta1 independent of importin alpha. Biochemistry. 2005;44:12887–95.
  • Ghildyal R, Ho A, Dias M, et al. The respiratory syncytial virus matrix protein possesses a Crm1-mediated nuclear export mechanism. J Virol. 2009;83:5353–62.
  • Quan Y, Ji ZL, Wang X, et al. Evolutionary and transcriptional analysis of karyopherin beta superfamily proteins. Mol Cell Proteomics. 2008;7:1254–69.
  • Huang Y, Zhang J, Halawa MA, et al. Nuclear localization signals of varicella zoster virus ORF4. Virus Genes. 2014;48:243–51.
  • Li Y, Zhao L, Wang SA, et al. Identification of a novel NLS of herpes simplex virus type 1 (HSV-1) VP19C and its nuclear localization is required for efficient production of HSV-1. J Gen Virol. 2012;93:1869–75.
  • Li ML, Wang SA, Cai MS, et al. Characterization of molecular determinants for nucleocytoplasmic shuttling of PRV UL54. Virology. 2011;417:385–93.
  • Cheng F, McLaughlin PJ, Zagon IS. Regulation of cell proliferation by the opioid growth factor receptor is dependent on karyopherin beta and Ran for nucleocytoplasmic trafficking. Exp Biol Med. 2010;235:1093–101.
  • Kurisaki A, Kose S, Yoneda Y, et al. Transforming growth factor-beta induces nuclear import of Smad3 in an importin-beta1 and Ran-dependent manner. Mol Biol Cell. 2001;12:1079–91.
  • Reid SP, Valmas C, Martinez O, et al. Ebola virus VP24 proteins inhibit the interaction of NPI-1 subfamily karyopherin alpha proteins with activated STAT1. J Virol. 2007;81:13469–77.
  • Guo H, Mao R, Block TM, et al. Production and function of the cytoplasmic deproteinized relaxed circular DNA of hepadnaviruses. J Virol. 2010;84:387–96.
  • Cansizoglu AE, Lee BJ, Zhang ZC, et al. Structure-based design of a pathway-specific nuclear import inhibitor. Nat Struct Mol Biol. 2007;14:452–4.
  • Kosugi S, Hasebe M, Entani T, et al. Design of peptide inhibitors for the importin alpha/beta nuclear import pathway by activity-based profiling. Chem Biol. 2008;15:940–9.
  • Palacios I, Weis K, Klebe C, et al. RAN/TC4 mutants identify a common requirement for snRNP and protein import into the nucleus. J Cell Biol. 1996;133:485–94.
  • Clarkson WD, Corbett AH, Paschal BM, et al. Nuclear protein import is decreased by engineered mutants of nuclear transport factor 2 (NTF2) that do not bind GDP-Ran. J Mol Biol. 1997;272:716–30.
  • Ribbeck K, Lipowsky G, Kent HM, et al. NTF2 mediates nuclear import of Ran. EMBO J. 1998;17:6587–98.
  • Wagstaff KM, Sivakumaran H, Heaton SM, et al. Ivermectin is a specific inhibitor of importin α/β-mediated nuclear import able to inhibit replication of HIV-1 and dengue virus. Biochem J. 2012;443:851–6.
  • Köhler M, Fiebeler A, Hartwig M, et al. Differential expression of classical nuclear transport factors during cellular proliferation and differentiation. Cell Physiol Biochem. 2002;12:335–44.
  • Pumroy RA, Cingolani G. Diversification of importin-alpha isoforms in cellular trafficking and disease states. Biochem J. 2015;466:13–28.
  • Kimoto C, Moriyama T, Tsujii A, et al. Functional characterization of importin α8 as a classical nuclear localization signal receptor. Biochim Biophys Acta. 2015;1853:2676–83.
  • Smith EC, Popa A, Chang A, et al. Viral entry mechanisms: the increasing diversity of paramyxovirus entry. FEBS J. 2009;276:7217–27.
  • Plattet P, Plemper RK. Envelope protein dynamics in paramyxovirus entry. MBio. 2013;4:e00413–13.
  • Dortmans JC, Koch G, Rottier PJ, et al. Virulence of Newcastle disease virus: what is known so far? Vet Res. 2011;42:122.
  • Ghildyal R, Ho A, Jans DA. Central role of the respiratory syncytial virus matrix protein in infection. FEMS Microbiol Rev. 2006;30:692–705.
  • Wang YE, Park A, Lake M, et al. Ubiquitin-regulated nuclear-cytoplasmic trafficking of the Nipah virus matrix protein is important for viral budding. PLoS Pathogen. 2010;6:e1001186.
  • Watkinson RE, Lee B. Nipah virus matrix protein: expert hacker of cellular machines. FEBS Lett. 2016;590:2494–511.
  • Duan Z, Song Q, Wang Y, et al. Characterization of signal sequences determining the nuclear export of Newcastle disease virus matrix protein. Arch Virol. 2013;158:2589–95.
  • Duan Z, Li J, Zhu J, et al. A single amino acid mutation, R42A, in the Newcastle disease virus matrix protein abrogates its nuclear localization and attenuates viral replication and pathogenicity. J Gen Virol. 2014;95:1067–73.
  • Duan Z, Hu Z, Zhu J, et al. Mutations in the FPIV motif of Newcastle disease virus matrix protein attenuate virus replication and reduce virus budding. Arch Virol. 2014;159:1813–9.
  • Khattar SK, Yan Y, Panda A, et al. A Y526Q mutation in the Newcastle disease virus HN protein reduces its functional activities and attenuates virus replication and pathogenicity. J Virol. 2009;83:7779–82.
  • Palmeri D, Malim MH. Importin beta can mediate the nuclear import of an arginine-rich nuclear localization signal in the absence of importin alpha. Mol Cell Biol. 1999;19:1218–25.
  • Truant R, Cullen BR. The arginine-rich domains present in human immunodeficiency virus type 1 Tat and Rev function as direct importin beta-dependent nuclear localization signals. Mol Cell Biol. 1999;19:1210–7.
  • Xiao Z, Liu X, Lodish HF. Importin beta mediates nuclear translocation of Smad 3. J Biol Chem. 2000;275:23425–8.
  • Bai L, Michael WM, Yan S. Importin β-dependent nuclear import of TopBP1 in ATR-Chk1 checkpoint in Xenopus egg extracts. Cell Signal. 2014;26:857–67.
  • Duan ZQ, Zhao JF, Xu HQ, et al. Characterization of the nuclear import pathway for BLM protein. Arch Biochem Biophys. 2017;634:57–68.
  • Nadler SG, Tritschler D, Haffar OK, et al. Differential expression and sequence-specific interaction of karyopherin alpha with nuclear localization sequences. J Biol Chem. 1997;272:4310–5.
  • Tsuji L, Takumi T, Imamoto N, et al. Identification of novel homologues of mouse importin alpha, the alpha subunit of the nuclear pore-targeting complex, and their tissue-specific expression. FEBS Lett. 1997;416:30–4.
  • Zachariae U, Grubmuller H. Importin-beta: structural and dynamic determinants of a molecular spring. Structure. 2008;16:906–15.
  • Conti E, Muller CW, Stewart M. Karyopherin flexibility in nucleocytoplasmic transport. Curr Opin Struct Biol. 2006;16:237–44.
  • Cingolani G, Bednenko J, Gillespie MT, et al. Molecular basis for the recognition of a nonclassical nuclear localization signal by importin beta. Mol Cell. 2002;10:1345–53.
  • Choi S, Yamashita E, Yasuhara N, et al. Structural basis for the selective nuclear import of the C2H2 zinc-finger protein Snail by importin β. Acta Crystallogr D Biol Crystallogr. 2014;70:1050–60.
  • Lee SJ, Sekimoto T, Yamashita E, et al. The structure of importin-beta bound to SREBP-2: nuclear import of a transcription factor. Science. 2003;302:1571–5.
  • Buchholz UJ, Finke S, Conzelmann KK. Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J Virol. 1999;73:251–9.
  • Duan ZQ, Ji XQ, Xu HQ, et al. Rescue of duck-origin virulent Newcastle disease virus from cloned cDNA and stable expression of the red fluorescent protein. Virol Reports.2016:97–103.
  • Li X, Li X, Cao H, et al. Engagement of new castle disease virus (NDV) matrix (M) protein with charged multivesicular body protein (CHMP) 4 facilitates viral replication. Virus Res. 2013;171:80–8.
  • Wang MQ, Wang LL, Guo Y, et al. The broad pattern recognition spectrum of the Toll-like receptor in mollusk Zhikong scallop Chlamys farreri. Dev Comp Immunol. 2015;52:192–201.
  • Merle E, Rose RC, LeRoux L, et al. Nuclear import of HPV11 L1 capsid protein is mediated by karyopherin α2β1 heterodimers. J Cell Biochem. 1999;74:628–37.
  • Alexander DJ. In A Laboratory Manual for the Isolation and Identification of Avian Pathogens, 3rd edn, pp.114–120. Edited by H. G. Purchase, L. H. Arp, C. H. Domermuth, & J. E. Pearson. Kennett Square, PA: American Association for Avian Pathologists, Inc. 1989;
  • Lundberg L, Pinkham C, Baer A, et al. Nuclear import and export inhibitors alter capsid protein distribution in mammalian cells and reduce Venezuelan Equine Encephalitis Virus replication. Antiviral Res. 2013;100:662–72.