A Herpesvirus Protein Selectively Inhibits Cellular mRNA Nuclear Export

Cell Host and Microbe

Volumn 20, Issue 5, 2016, Pages 642-653

  Gong, Danyang ^a   Kim, Yong Hoon ^a   Xiao, Yuchen ^b   Du, Yushen ^a   Xie, Yafang ^a   Lee, Kevin K ^b   Feng, Jun ^a   Farhat, Nisar ^a   Zhao, Dawei ^a   Shu, Sara ^a   Dai, Xinghong ^a   Chanda, Sumit K ^c   Rana, Tariq M ^b   Krogan, Nevan J ^d   Sun, Ren ^a   Wu, Ting Ting ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BURNHAM INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

3 UTR; herpesvirus; KSHV; late gene; mRNA nuclear export; Nup98; ORF10; Rae1

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; CELL NUCLEUS DNA; MESSENGER RNA; NUCLEAR RNA; NUCLEOPORIN 98; ORF10 PROTEIN; POLYADENYLATED RNA; RAE1 PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRAL PROTEIN; NUCLEAR MATRIX PROTEIN; NUCLEOCYTOPLASMIC TRANSPORT PROTEIN; PROTEIN BINDING; RAE1 PROTEIN, HUMAN;

3' UNTRANSLATED REGION; ARTICLE; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; HEK293 CELL LINE; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RENAL CANCER CELL LINE; RNA TRANSPORT; VERO CELL LINE; VIRION; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS INHIBITION; VIRUS REPLICATION; ANIMAL; BIOLOGICAL MODEL; CELL LINE; GENE EXPRESSION REGULATION; HOST PATHOGEN INTERACTION; METABOLISM; NUCLEOCYTOPLASMIC TRANSPORT; PHYSIOLOGY;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL LINE; GENE EXPRESSION REGULATION; HERPESVIRUS 8, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; MODELS, BIOLOGICAL; NUCLEAR MATRIX-ASSOCIATED PROTEINS; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; PROTEIN BINDING; RNA, MESSENGER; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84994726281     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2016.10.004     Document Type: Article

References (35)

1. Aubry, V., Mure, F., Mariamé, B., Deschamps, T., Wyrwicz, L.S., Manet, E., Gruffat, H., Epstein-Barr virus late gene transcription depends on the assembly of a virus-specific preinitiation complex. J. Virol. 88 (2014), 12825–12838.
2. Babu, J.R., Jeganathan, K.B., Baker, D.J., Wu, X., Kang-Decker, N., van Deursen, J.M., Rae1 is an essential mitotic checkpoint regulator that cooperates with Bub3 to prevent chromosome missegregation. J. Cell Biol. 160 (2003), 341–353.
3. Bisson, S.A., Page, A.L., Ganem, D., A Kaposi's sarcoma-associated herpesvirus protein that forms inhibitory complexes with type I interferon receptor subunits, Jak and STAT proteins, and blocks interferon-mediated signal transduction. J. Virol. 83 (2009), 5056–5066.
4. Blevins, M.B., Smith, A.M., Phillips, E.M., Powers, M.A., Complex formation among the RNA export proteins Nup98, Rae1/Gle2, and TAP. J. Biol. Chem. 278 (2003), 20979–20988.
5. Brown, J.A., Bharathi, A., Ghosh, A., Whalen, W., Fitzgerald, E., Dhar, R., A mutation in the Schizosaccharomyces pombe rae1 gene causes defects in poly(A)+ RNA export and in the cytoskeleton. J. Biol. Chem. 270 (1995), 7411–7419.
6. Brulois, K.F., Chang, H., Lee, A.S., Ensser, A., Wong, L.Y., Toth, Z., Lee, S.H., Lee, H.R., Myoung, J., Ganem, D., et al. Construction and manipulation of a new Kaposi's sarcoma-associated herpesvirus bacterial artificial chromosome clone. J. Virol. 86 (2012), 9708–9720.
7. Carmody, S.R., Wente, S.R., mRNA nuclear export at a glance. J. Cell Sci. 122 (2009), 1933–1937.
8. Chakraborty, P., Seemann, J., Mishra, R.K., Wei, J.H., Weil, L., Nussenzveig, D.R., Heiber, J., Barber, G.N., Dasso, M., Fontoura, B.M., Vesicular stomatitis virus inhibits mitotic progression and triggers cell death. EMBO Rep. 10 (2009), 1154–1160.
9. Chen, I.H.B., Sciabica, K.S., Sandri-Goldin, R.M., ICP27 interacts with the RNA export factor Aly/REF to direct herpes simplex virus type 1 intronless mRNAs to the TAP export pathway. J. Virol. 76 (2002), 12877–12889.
10. Davis, Z.H., Verschueren, E., Jang, G.M., Kleffman, K., Johnson, J.R., Park, J., Von Dollen, J., Maher, M.C., Johnson, T., Newton, W., et al. Global mapping of herpesvirus-host protein complexes reveals a transcription strategy for late genes. Mol. Cell 57 (2015), 349–360.
11. Faria, P.A., Chakraborty, P., Levay, A., Barber, G.N., Ezelle, H.J., Enninga, J., Arana, C., van Deursen, J., Fontoura, B.M., VSV disrupts the Rae1/mrnp41 mRNA nuclear export pathway. Mol. Cell 17 (2005), 93–102.
12. Glaunsinger, B., Ganem, D., Lytic KSHV infection inhibits host gene expression by accelerating global mRNA turnover. Mol. Cell 13 (2004), 713–723.
13. Gong, D., Wu, N.C., Xie, Y., Feng, J., Tong, L., Brulois, K.F., Luan, H., Du, Y., Jung, J.U., Wang, C.Y., et al. Kaposi's sarcoma-associated herpesvirus ORF18 and ORF30 are essential for late gene expression during lytic replication. J. Virol. 88 (2014), 11369–11382.
14. Grünwald, D., Singer, R.H., Rout, M., Nuclear export dynamics of RNA-protein complexes. Nature 475 (2011), 333–341.
15. Keene, J.D., RNA regulons: coordination of post-transcriptional events. Nat. Rev. Genet. 8 (2007), 533–543.
16. Koffa, M.D., Clements, J.B., Izaurralde, E., Wadd, S., Wilson, S.A., Mattaj, I.W., Kuersten, S., Herpes simplex virus ICP27 protein provides viral mRNAs with access to the cellular mRNA export pathway. EMBO J. 20 (2001), 5769–5778.
17. Kraemer, D., Blobel, G., mRNA binding protein mrnp 41 localizes to both nucleus and cytoplasm. Proc. Natl. Acad. Sci. USA 94 (1997), 9119–9124.
18. Kumar, G.R., Glaunsinger, B.A., Nuclear import of cytoplasmic poly(A) binding protein restricts gene expression via hyperadenylation and nuclear retention of mRNA. Mol. Cell. Biol. 30 (2010), 4996–5008.
19. Leang, R.S., Wu, T.T., Hwang, S., Liang, L.T., Tong, L., Truong, J.T., Sun, R., The anti-interferon activity of conserved viral dUTPase ORF54 is essential for an effective MHV-68 infection. PLoS Pathog., 7, 2011, e1002292.
20. Lee, Y.J., Glaunsinger, B.A., Aberrant herpesvirus-induced polyadenylation correlates with cellular messenger RNA destruction. PLoS Biol., 7, 2009, e1000107.
21. Levanon, D., Glusman, G., Bangsow, T., Ben-Asher, E., Male, D.A., Avidan, N., Bangsow, C., Hattori, M., Taylor, T.D., Taudien, S., et al. Architecture and anatomy of the genomic locus encoding the human leukemia-associated transcription factor RUNX1/AML1. Gene 262 (2001), 23–33.
22. Malik, P., Blackbourn, D.J., Clements, J.B., The evolutionarily conserved Kaposi's sarcoma-associated herpesvirus ORF57 protein interacts with REF protein and acts as an RNA export factor. J. Biol. Chem. 279 (2004), 33001–33011.
23. Müller-McNicoll, M., Neugebauer, K.M., How cells get the message: dynamic assembly and function of mRNA-protein complexes. Nat. Rev. Genet. 14 (2013), 275–287.
24. Murphy, R., Watkins, J.L., Wente, S.R., GLE2, a Saccharomyces cerevisiae homologue of the Schizosaccharomyces pombe export factor RAE1, is required for nuclear pore complex structure and function. Mol. Biol. Cell 7 (1996), 1921–1937.
25. Powers, M.A., Forbes, D.J., Nuclear transport: beginning to gel?. Curr. Biol. 22 (2012), R1006–R1009.
26. Pritchard, C.E.J., Fornerod, M., Kasper, L.H., van Deursen, J.M.A., RAE1 is a shuttling mRNA export factor that binds to a GLEBS-like NUP98 motif at the nuclear pore complex through multiple domains. J. Cell Biol. 145 (1999), 237–254.
27. Quan, B., Seo, H.S., Blobel, G., Ren, Y., Vesiculoviral matrix (M) protein occupies nucleic acid binding site at nucleoporin pair (Rae1 ⋅ Nup98). Proc. Natl. Acad. Sci. USA 111 (2014), 9127–9132.
28. Satterly, N., Tsai, P.L., van Deursen, J., Nussenzveig, D.R., Wang, Y., Faria, P.A., Levay, A., Levy, D.E., Fontoura, B.M.A., Influenza virus targets the mRNA export machinery and the nuclear pore complex. Proc. Natl. Acad. Sci. USA 104 (2007), 1853–1858.
29. Strambio-De-Castillia, C., Niepel, M., Rout, M.P., The nuclear pore complex: bridging nuclear transport and gene regulation. Nat. Rev. Mol. Cell Biol. 11 (2010), 490–501.
30. von Kobbe, C., van Deursen, J.M., Rodrigues, J.P., Sitterlin, D., Bachi, A., Wu, X., Wilm, M., Carmo-Fonseca, M., Izaurralde, E., Vesicular stomatitis virus matrix protein inhibits host cell gene expression by targeting the nucleoporin Nup98. Mol. Cell 6 (2000), 1243–1252.
31. Wang, Y., Zhu, W., Levy, D.E., Nuclear and cytoplasmic mRNA quantification by SYBR green based real-time RT-PCR. Methods 39 (2006), 356–362.
32. Wickramasinghe, V.O., Laskey, R.A., Control of mammalian gene expression by selective mRNA export. Nat. Rev. Mol. Cell Biol. 16 (2015), 431–442.
33. Wu, T.T., Park, T., Kim, H., Tran, T., Tong, L., Martinez-Guzman, D., Reyes, N., Deng, H., Sun, R., ORF30 and ORF34 are essential for expression of late genes in murine gammaherpesvirus 68. J. Virol. 83 (2009), 2265–2273.
34. Wu, T.T., Liao, H.I., Tong, L., Leang, R.S., Smith, G., Sun, R., Construction and characterization of an infectious murine gammaherpesivrus-68 bacterial artificial chromosome. J. Biomed. Biotechnol., 2011, 2011, 926258.
35. Yarbrough, M.L., Mata, M.A., Sakthivel, R., Fontoura, B.M.A., Viral subversion of nucleocytoplasmic trafficking. Traffic 15 (2014), 127–140.