Nucleocytoplasmic Shuttling of Viral Proteins in Borna Disease Virus Infection

Overview

Journal Viruses

Publisher MDPI

Specialty Microbiology

Date 2013 Aug 23

PMID 23965528

Citations 19

Authors

Tomoyuki Honda

Keizo Tomonaga

Affiliations

Soon will be listed here.

Abstract

Nuclear import and export of viral RNA and proteins are critical to the replication cycle of viruses that replicate in the nucleus. Borna disease virus (BDV) is a nonsegmented, negative-strand RNA virus that belongs to the order Mononegavirales. BDV has several distinguishing features, one of the most striking being the site of its replication. BDV RNA is transcribed and replicated in the nucleus, while most other negative-strand RNA viruses replicate in the cytoplasm. Therefore, the nucleocytoplasmic trafficking of BDV macromolecules plays a key role in virus replication. Growing evidence indicates that several BDV proteins, including the nucleoprotein, phosphoprotein, protein X and large protein, contribute to the nucleocytoplasmic trafficking of BDV ribonucleoprotein (RNP). The directional control of BDV RNP trafficking is likely determined by the ratios of and interactions between the nuclear localization signals and nuclear export signals in the RNP. In this review, we present a comprehensive view of several unique mechanisms that BDV has developed to control its RNP trafficking and discuss the significance of BDV RNP trafficking in the replication cycle of BDV.

Citing Articles

Suppression of Borna Disease Virus Replication during Its Persistent Infection Using the CRISPR/Cas13b System.

Sasaki S, Ogawa H, Katoh H, Honda T Int J Mol Sci. 2024; 25(6).

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In Silico Discovery of Potential Inhibitors Targeting the RNA Binding Loop of ADAR2 and 5-HT2CR from Traditional Chinese Natural Compounds.

Broni E, Ashley C, Velazquez M, Khan S, Striegel A, Sakyi P Int J Mol Sci. 2023; 24(16).

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Impact of Borna Disease Virus Infection on the Transcriptome of Differentiated Neuronal Cells and Its Modulation by Antiviral Treatment.

Teng D, Ueda K, Honda T Viruses. 2023; 15(4).

PMID: 37112922 PMC: 10145824. DOI: 10.3390/v15040942.

Multiple RNA virus matrix proteins interact with SLD5 to manipulate host cell cycle.

Zhu L, Li X, Xu H, Fu L, Gao G, Liu W J Gen Virol. 2021; 102(12).

PMID: 34882534 PMC: 8744269. DOI: 10.1099/jgv.0.001697.

The Borna Disease Virus 2 (BoDV-2) Nucleoprotein Is a Conspecific Protein That Enhances BoDV-1 RNA-Dependent RNA Polymerase Activity.

Kanda T, Horie M, Komatsu Y, Tomonaga K J Virol. 2021; 95(21):e0093621.

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References

Kobayashi T, Zhang G, Lee B, Baba S, Yamashita M, Kamitani W . Modulation of Borna disease virus phosphoprotein nuclear localization by the viral protein X encoded in the overlapping open reading frame. J Virol. 2003; 77(14):8099-107. PMC: 161951. DOI: 10.1128/jvi.77.14.8099-8107.2003. View

Gonzalez-Dunia D, Cubitt B, de la Torre J . Mechanism of Borna disease virus entry into cells. J Virol. 1998; 72(1):783-8. PMC: 109436. DOI: 10.1128/JVI.72.1.783-788.1998. View

Berg M, Ehrenborg C, Blomberg J, Pipkorn R, Berg A . Two domains of the Borna disease virus p40 protein are required for interaction with the p23 protein. J Gen Virol. 1999; 79 ( Pt 12):2957-63. DOI: 10.1099/0022-1317-79-12-2957. View

Hayashi Y, Horie M, Daito T, Honda T, Ikuta K, Tomonaga K . Heat shock cognate protein 70 controls Borna disease virus replication via interaction with the viral non-structural protein X. Microbes Infect. 2009; 11(3):394-402. DOI: 10.1016/j.micinf.2009.01.006. View

Hutchinson E, Fodor E . Nuclear import of the influenza A virus transcriptional machinery. Vaccine. 2012; 30(51):7353-8. DOI: 10.1016/j.vaccine.2012.04.085. View

Pletnikov M, Rubin S, Vasudevan K, Moran T, Carbone K . Developmental brain injury associated with abnormal play behavior in neonatally Borna disease virus-infected Lewis rats: a model of autism. Behav Brain Res. 1999; 100(1-2):43-50. DOI: 10.1016/s0166-4328(98)00111-9. View

Hornig M, Solbrig M, Horscroft N, Weissenbock H, Lipkin W . Borna disease virus infection of adult and neonatal rats: models for neuropsychiatric disease. Curr Top Microbiol Immunol. 2001; 253:157-77. DOI: 10.1007/978-3-662-10356-2_8. View

Briese T, Schneemann A, Lewis A, Park Y, Kim S, Ludwig H . Genomic organization of Borna disease virus. Proc Natl Acad Sci U S A. 1994; 91(10):4362-6. PMC: 43785. DOI: 10.1073/pnas.91.10.4362. View

Kobayashi T, Shoya Y, Koda T, Takashima I, Lai P, Ikuta K . Nuclear targeting activity associated with the amino terminal region of the Borna disease virus nucleoprotein. Virology. 1998; 243(1):188-97. DOI: 10.1006/viro.1998.9049. View

10.

Kobayashi T, Kamitani W, Zhang G, Watanabe M, Tomonaga K, Ikuta K . Borna disease virus nucleoprotein requires both nuclear localization and export activities for viral nucleocytoplasmic shuttling. J Virol. 2001; 75(7):3404-12. PMC: 114133. DOI: 10.1128/JVI.75.7.3404-3412.2001. View

11.

Wolff T, Unterstab G, Heins G, Richt J, Kann M . Characterization of an unusual importin alpha binding motif in the borna disease virus p10 protein that directs nuclear import. J Biol Chem. 2002; 277(14):12151-7. DOI: 10.1074/jbc.M109103200. View

12.

Schwemmle M, Salvatore M, Shi L, Richt J, Lee C, Lipkin W . Interactions of the borna disease virus P, N, and X proteins and their functional implications. J Biol Chem. 1998; 273(15):9007-12. DOI: 10.1074/jbc.273.15.9007. View

13.

Kraus I, Eickmann M, Kiermayer S, Scheffczik H, Fluess M, Richt J . Open reading frame III of borna disease virus encodes a nonglycosylated matrix protein. J Virol. 2001; 75(24):12098-104. PMC: 116105. DOI: 10.1128/JVI.75.24.12098-12104.2001. View

14.

Rudolph M, Kraus I, Dickmanns A, Eickmann M, Garten W, Ficner R . Crystal structure of the borna disease virus nucleoprotein. Structure. 2003; 11(10):1219-26. DOI: 10.1016/j.str.2003.08.011. View

15.

Pyper J, Gartner A . Molecular basis for the differential subcellular localization of the 38- and 39-kilodalton structural proteins of Borna disease virus. J Virol. 1997; 71(7):5133-9. PMC: 191748. DOI: 10.1128/JVI.71.7.5133-5139.1997. View

16.

Matsumoto Y, Hayashi Y, Omori H, Honda T, Daito T, Horie M . Bornavirus closely associates and segregates with host chromosomes to ensure persistent intranuclear infection. Cell Host Microbe. 2012; 11(5):492-503. DOI: 10.1016/j.chom.2012.04.009. View

17.

Chase G, Mayer D, Hildebrand A, Frank R, Hayashi Y, Tomonaga K . Borna disease virus matrix protein is an integral component of the viral ribonucleoprotein complex that does not interfere with polymerase activity. J Virol. 2006; 81(2):743-9. PMC: 1797437. DOI: 10.1128/JVI.01351-06. View

18.

Nakielny S, Dreyfuss G . Transport of proteins and RNAs in and out of the nucleus. Cell. 2000; 99(7):677-90. DOI: 10.1016/s0092-8674(00)81666-9. View

19.

Neumann P, Lieber D, Meyer S, Dautel P, Kerth A, Kraus I . Crystal structure of the Borna disease virus matrix protein (BDV-M) reveals ssRNA binding properties. Proc Natl Acad Sci U S A. 2009; 106(10):3710-5. PMC: 2656145. DOI: 10.1073/pnas.0808101106. View

20.

Whittaker G, Helenius A . Nuclear import and export of viruses and virus genomes. Virology. 1998; 246(1):1-23. DOI: 10.1006/viro.1998.9165. View