NXF1 and CRM1 nuclear export pathways orchestrate nuclear export, translation and packaging of murine leukaemia retrovirus unspliced RNA

References

• Kanopka A, Muhlemann O, Akusjarvi G. Inhibition by SR proteins splicing of a regulated adenovirus pre-mRNA. Nature. 1996;381:535–538.
   PubMed Web of Science ®Google Scholar
• Jang SK, Wimmer E. Cap-independent translation of encephalomyocarditis virus RNA: structural elements of the internal ribosomal entry site and involvement of a cellular 57-kD RNA-binding protein. Genes Dev. 1990;4:1560–1572.
   PubMed Web of Science ®Google Scholar
• Bray M, Prasad S, Dubay JW, et al. A small element from the Mason-Pfizer monkey virus genome makes human immunodeficiency virus type 1 expression and replication Rev- independent. Proc Natl Acad Sci U S A. 1994;91:1256–1260.
   PubMed Web of Science ®Google Scholar
• Fornerod M, Ohno M, Yoshida M, et al. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell. 1997;90:1051–1060.
   PubMed Web of Science ®Google Scholar
• Houzet L, Battini JL, Bernard E, et al. A new retroelement constituted by a natural alternatively spliced RNA of murine replication-competent retroviruses. Embo J. 2003;22:4866–4875.
   PubMed Web of Science ®Google Scholar
• Dorman N, Lever A. Comparison of viral genomic RNA sorting mechanisms in human immunodeficiency virus type 1 (HIV-1), HIV-2, and moloney murine leukemia virus. J Virol. 2000;74:11413–11417.
   PubMed Web of Science ®Google Scholar
• Mougel M, Zhang Y, Barklis E. cis-Active structural motifs involved in specific encapsidation of Moloney murine leukemia virus RNA. J Virol. 1996;70:5043–5050.
   PubMed Web of Science ®Google Scholar
• D’Souza V, Summers MF. Structural basis for packaging the dimeric genome of Moloney murine leukaemia virus. Nature. 2004;431:586–590.
   PubMed Web of Science ®Google Scholar
• Mougel M, Barklis E. A role for two hairpin structures as a core RNA encapsidation signal in murine leukemia virus virions. J Virol. 1997;71:8061–8065.
   PubMed Web of Science ®Google Scholar
• Smagulova F, Maurel S, Morichaud Z, et al. The highly structured encapsidation signal of MuLV RNA is involved in the nuclear export of its unspliced RNA. J Mol Biol. 2005;354:1118–1128.
   PubMed Web of Science ®Google Scholar
• Basyuk E, Boulon S, Skou Pedersen F, et al. The packaging signal of MLV is an integrated module that mediates intracellular transport of genomic RNAs. J Mol Biol. 2005;354:330–339.
   PubMed Web of Science ®Google Scholar
• Malim MH, Hauber J, Le SY, et al. The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature. 1989;338:254–257.
   PubMed Web of Science ®Google Scholar
• Pessel-Vivares L, Ferrer M, Lainé S, et al. MLV requires Tap/NXF1-dependent pathway to export its unspliced RNA to the cytoplasm and to express both spliced and unspliced RNAs. Retrovirology. 2014;11:21.
   PubMed Web of Science ®Google Scholar
• Bartels H, Luban J. Gammaretroviral pol sequences act in cis to direct polysome loading and NXF1/NXT-dependent protein production by gag -encoded RNA. Retrovirology. 2014;11:73.
   PubMed Web of Science ®Google Scholar
• Sakuma T, Davila JI, Malcolm JA, et al. Murine leukemia virus uses NXF1 for nuclear export of spliced and unspliced viral transcripts. J Virol. 2014;88:4069–4082.
   PubMed Web of Science ®Google Scholar
• Pilkington GR, Purzycka KJ, Bear J, et al. Gammaretrovirus mRNA expression is mediated by a novel, bipartite post-transcriptional regulatory element. Nucleic Acids Res. 2014;42:11092–11106.
   PubMed Web of Science ®Google Scholar
• Pessel-Vivares L, Houzet L, Lainé S, et al. Insights into the nuclear export of murine leukemia virus intron-containing RNA. RNA Biol. 2015;12:942–949.
   PubMed Web of Science ®Google Scholar
• Sherer NM, Swanson CM, Papaioannou S, et al. Matrix mediates the functional link between human immunodeficiency virus type 1 RNA nuclear export elements and the assembly competency of Gag in murine cells. J Virol. 2009;83:8525–8535.
   PubMed Web of Science ®Google Scholar
• Swanson CM, Puffer BA, Ahmad KM, et al. Retroviral mRNA nuclear export elements regulate protein function and virion assembly. Embo J. 2004;23:2632–2640.
   PubMed Web of Science ®Google Scholar
• Volkova NA, Fomina EG, Smolnikova VV, et al. The U3 region of Moloney murine leukemia virus contains position-independent cis-acting sequences involved in the nuclear export of full-length viral transcripts. J Biol Chem. 2014;289:20158–20169.
   PubMed Web of Science ®Google Scholar
• Jouvenet N, Lainé S, Pessel-Vivares L, et al. Cell biology of retroviral RNA packaging. RNA Biol. 2011;8:1–9.
   Web of Science ®Google Scholar
• Jouvenet N, Simon SM. Viral houseguests undertake interior redesign. Cell. 2011;141:754–756.
   Web of Science ®Google Scholar
• Popa I, Harris ME, Donello JE, Hope TJ. CRM1-Dependent Function of a cis-acting RNA export element. Mol Cell Biol. 2002;22:2057–2067.
   Google Scholar
• Ferrer M, Henriet S, Chamontin C, et al. From cells to virus particles: quantitative methods to monitor RNA packaging. Viruses. 2016;8:1–16.
   Web of Science ®Google Scholar
• Ferrer M, Clerté C, Chamontin C, et al. Imaging HIV-1 RNA dimerization in cells by multicolor super-resolution and fluctuation microscopies. Nucleic Acids Res. 2016;44:7922–7934.
   PubMed Web of Science ®Google Scholar
• Okamura M, Inose H, Masuda S. RNA export through the NPC in Eukaryotes. Genes. 2015; 6:124–149.
   Google Scholar
• Saavedra C, Felber B, Izaurralde E. The simian retrovirus-1 constitutive transport element, unlike the HIV- 1 RRE, uses factors required for cellular mRNA export. Curr Biol. 1997;7:619–628.
   PubMed Web of Science ®Google Scholar
• Askjaer P, Bachi A, Wilm M, et al. RanGTP-regulated interactions of CRM1 with nucleoporins and a shuttling DEAD-box helicase. Mol Cell Biol. 1999;19:6276–6285.
   Google Scholar
• Fischer U, Huber J, Boelens WC, et al. The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell. 1995;82:475–483.
   PubMed Web of Science ®Google Scholar
• Ernst RK, Bray M, Rekosh D, et al. A structured retroviral RNA element that mediates nucleocytoplasmic export of intron-containing RNA. Mol Cell Biol. 1997;17:135–144.
   PubMed Web of Science ®Google Scholar
• Pasquinelli AE, Ernst RK, Lund E, et al. The constitutive transport element (CTE) of Mason-Pfizer monkey virus (MPMV) accesses a cellular mRNA export pathway. Embo J. 1997;16:7500–7510.
   PubMed Web of Science ®Google Scholar
• LeBlanc JJ, Uddowla S, Abraham B, et al. Tap and Dbp5, but not Gag, are involved in DR-mediated nuclear export of unspliced Rous sarcoma virus RNA. Virology. 2007;363:376–386.
   PubMed Web of Science ®Google Scholar
• Kemler I, Saenz D, Poeschla E. Feline immunodeficiency virus Gag is a nuclear shuttling protein. J Virol. 2012;86:8402–8411.
   Google Scholar
• Scheifele LZ, Garbitt RA, Rhoads JD, et al. Nuclear entry and CRM1-dependent nuclear export of the Rous sarcoma virus Gag polyprotein. Proc Natl Acad Sci. 2002;99:3944–3949.
   PubMed Web of Science ®Google Scholar
• Renault N, Tobaly-Tapiero J, Paris J, et al. A nuclear export signal within the structural Gag protein is required for prototype foamy virus replication. Retrovirology. 2011;8:6.
   PubMed Web of Science ®Google Scholar
• Hanly SM, Rimsky LT, Malim MH, et al. Comparative analysis of the HTLV-I Rex and HIV-1 Rev trans-regulatory proteins and their RNA response elements. Genes Dev. 1989;3:1534–1544.
   PubMed Web of Science ®Google Scholar
• Hidaka M, Inoue J, Yoshida M, et al. Post-transcriptional Regulator (rex) of HTLV-I initiates expression of viral structural proteins but suppresses expression of regulatory proteins. EMBO. 1988;7:519–523.
   PubMed Web of Science ®Google Scholar
• Mertz JA, Simper MS, Lozano MM, et al. Mouse mammary tumor virus encodes a self-regulatory RNA export protein and is a complex retrovirus. J Virol. 2005;79:14737–14747.
   Google Scholar
• Nash MA, Meyer MK, Decker GL, et al. A subset of Pr65gag is nucleus associated in murine leukemia virus-infected cells. J Virol. 1993;67:1350–1356.
   PubMed Web of Science ®Google Scholar
• Levin JG, Grimley PM, Ramseur JM, et al. Deficiency of 60 to 70S RNA in murine leukemia virus particles assembled in cells treated with actinomycin D. J Virol. 1974;14:152–161.
   PubMed Web of Science ®Google Scholar
• Garbitt-Hirst R, Kenney SP, Parent LJ. Genetic evidence for a connection between Rous Sarcoma virus Gag nuclear trafficking and genomic RNA packaging. J Virol. 2009;83:6790–6797.
   PubMed Web of Science ®Google Scholar
• Gudleski N, Flanagan JM, Ryan EP, et al. Directionality of nucleocytoplasmic transport of the retroviral gag protein depends on sequential binding of karyopherins and viral RNA. Proc Natl Acad Sci. 2010;107:9358–9363.
   PubMed Web of Science ®Google Scholar
• Bohl CR, Brown SM, Weldon RA. The pp24 phosphoprotein of Mason-Pfizer monkey virus contributes to viral genome packaging. Retrovirology. 2005;2:1–14.
   PubMed Web of Science ®Google Scholar
• Pocock GM, Becker JT, Swanson CM, et al. HIV-1 and M-PMV RNA nuclear export elements program viral genomes for distinct cytoplasmic trafficking behaviors. PLoS Pathog. 2016;12:1–30.
   Web of Science ®Google Scholar
• Zheng Y-H, Yu H-F, Peterlin BM. Human p32 protein relieves a post-transcriptional block to HIV replication in murine cells. Nat Cell Biol. 2003;5:611–618.
   PubMed Web of Science ®Google Scholar
• Cupelli L, Okenquist SA, Trubetskoy A, et al. The secondary structure of the R region of a murine leukemia virus is important for stimulation of long terminal repeat-driven gene expression. J Virol. 1998;72:7807–7814.
   PubMed Web of Science ®Google Scholar
• Trubetskoy AM, Okenquist SA, Lenz J. R region sequences in the long terminal repeat of a murine retrovirus specifically increase expression of unspliced RNAs. J Virol. 1999;73:3477–3483.
   PubMed Web of Science ®Google Scholar
• Scheifele LZ, Ryan EP, Parent LJ. Detailed mapping of the nuclear export signal in the Rous Sarcoma virus Gag protein. J Virol. 2005;79:8732–8741.
   PubMed Web of Science ®Google Scholar
• Baluyot MF, Grosse SA, Lyddon TD, et al. CRM1-dependent trafficking of retroviral Gag proteins revisited. J Virol. 2012;86:4696–4700.
   PubMed Web of Science ®Google Scholar
• D’Souza V, Summers MF. How retroviruses select their genomes. Nat Rev Microbiol. 2005;3:643–655.
   PubMed Web of Science ®Google Scholar
• Mailler E, Bernacchi S, Marquet R, et al. The life-cycle of the HIV-1 Gag – RNA complex. Viruses. 2016;1–19.
   Google Scholar
• Chamontin C, Yu B, Racine PJ, et al. MoMuLV and HIV-1 nucleocapsid proteins have a common role in genomic RNA packaging but different in late reverse transcription. PLoS One. 2012;7:e51534.
   Web of Science ®Google Scholar
• Mark-Danieli M, Laham N, Kenan-Eichler M, et al. Single point mutations in the zinc finger motifs of the human immunodeficiency virus type 1 nucleocapsid alter RNA binding specificities of the gag protein and enhance packaging and infectivity. J Virol. 2005;79:7756–7767.
   PubMed Web of Science ®Google Scholar
• Jouvenet N, Simon SM, Bieniasz PD. Imaging the interaction of HIV-1 genomes and Gag during assembly of individual viral particles. Proc Natl Acad Sci U S A. 2009;106:19114–19119.
   PubMed Web of Science ®Google Scholar
• Maurel S, Houzet L, Garcia EL, et al. Characterization of a natural heterodimer between MLV genomic RNA and the SD’ retroelement generated by alternative splicing. RNA. 2007;13:2266–2276.
   PubMed Web of Science ®Google Scholar
• Rasmussen SV, Pedersen FS. Co-localization of gammaretroviral RNAs at their transcription site favours co-packaging. J Gen Virol. 2006;87:2279–2289.
   PubMed Web of Science ®Google Scholar
• Maurel S, Mougel M. Murine leukemia virus RNA dimerization is coupled to transcription and splicing processes. Retrovirology. 2010;7:1–8.
   PubMed Web of Science ®Google Scholar
• Courtney DG, Chalem A, Bogerd HP, et al. Extensive epitranscriptomic methylation of A and C residues on murine leukemia virus transcripts enhances viral gene expression. MBio. 2019;10:1–12.
   Web of Science ®Google Scholar
• Sambrook J, Russell DW. Molecular cloning: a laboratory manual. 3th ed. New York: Cold Spring Harbor Laboratory; 2001.
   Google Scholar
• Shinnick TM, Lerner RA, Sutcliffe JG. Nucleotide sequence of Moloney murine leukaemia virus. Nature. 1981;293:543–548.
   PubMed Web of Science ®Google Scholar
• Jouvenet N, Neil S, Zhadina M, et al. Hatziioannou T and Bieniasz P. Broad-spectrum inhibition of retroviral and filoviral particle release by tetherin. J Virol. 2009;83(4):1837–1844.
   PubMed Web of Science ®Google Scholar
• Boireau S, Maiuri P, Basyuk E, et al. The transcriptional cycle of HIV-1 in real-time and live cells. J Cell Biol. 2007;179:291–304.
   PubMed Web of Science ®Google Scholar
• Voelkel C, Galla M, Maetzig T, et al. Protein transduction from retroviral Gag precursors. Proc Natl Acad Sci. 2010;107:7805–7810.
   PubMed Web of Science ®Google Scholar
• Dejardin J, Bompard-Marechal G, Audit M, et al. A Novel subgenomic murine leukemia virus RNA transcript results from alternative splicing. J Virol. 2000;74:3709–3714.
   PubMed Web of Science ®Google Scholar