Murine leukemia virus uses NXF1 for nuclear export of spliced and unspliced viral transcripts

Journal of Virology

Volumn 88, Issue 8, 2014, Pages 4069-4082

  Sakuma, Toshie ^a   Davila, Jaime I ^a   Malcolm, Jessica A ^a   Kocher, Jean Pierre A ^a   Tonne, Jason M ^a   Ikeda, Yasuhiro ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENVELOPE PROTEIN; GAG PROTEIN; PROTEIN NXF1; REV PROTEIN; UNCLASSIFIED DRUG; VIRUS RECEPTOR; VIRUS RNA;

ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; CYTOPLASM; GENE EXPRESSION; MURINE LEUKEMIA VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA SPLICING; RNA STABILITY; RNA TRANSCRIPTION; SEQUENCE ANALYSIS; STRUCTURAL GENE; VIRUS GENE; VIRUS TRANSCRIPTION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BASE SEQUENCE; CELL LINE; CELL NUCLEUS; GENE PRODUCTS, REV; LEUKEMIA VIRUS, MURINE; MICE; MOLECULAR SEQUENCE DATA; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; RETROVIRIDAE INFECTIONS; RNA SPLICING; RNA, VIRAL; RODENT DISEASES;

EID: 84896070554     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03584-13     Document Type: Article

References (71)

1. Ner-Gaon H, Halachmi R, Savaldi-Goldstein S, Rubin E, Ophir R, Fluhr R. 2004. Intron retention is a major phenomenon in alternative splicing in Arabidopsis. Plant J. 39:877-885. http://dx.doi.org/10.1111/j.1365-313X.2004.02172.x.
2. Indik S, Gunzburg WH, Salmons B, Rouault F. 2005. A novel, mouse mammary tumor virus encoded protein with Rev-like properties. Virology 337:1-6. http://dx.doi.org/10.1016/j.virol.2005.03.040.
3. Sakuma T, Barry MA, Ikeda Y. 2012. Lentiviral vectors: basic to translational. Biochem. J. 443:603-618. http://dx.doi.org/10.1042/BJ20120146.
4. Sandri-Goldin RM. 2004. Viral regulation of mRNA export. J. Virol. 78:4389-4396. http://dx.doi.org/10.1128/JVI.78.9.4389-4396.2004.
5. Cullen BR. 2005. Human immunodeficiency virus: nuclear RNA export unwound. Nature 433:26-27. http://dx.doi.org/10.1038/433026a.
6. Zapp ML, Green MR. 1989. Sequence-specific RNA binding by the HIV-1 Rev protein. Nature 342:714-716. http://dx.doi.org/10.1038/342714a0.
7. Daly TJ, Cook KS, Gray GS, Maione TE, Rusche JR. 1989. Specific binding of HIV-1 recombinant Rev protein to the Rev-responsive element in vitro. Nature 342:816-819. http://dx.doi.org/10.1038/342816a0.
8. Popa I, Harris ME, Donello JE, Hope TJ. 2002. CRM1-dependent function of a cis-acting RNA export element. Mol. Cell. Biol. 22:2057-2067. http://dx.doi.org/10.1128/MCB.22.7.2057-2067.2002.
9. Ahmed YF, Hanly SM, Malim MH, Cullen BR, Greene WC. 1990. Structure-function analyses of the HTLV-I Rex and HIV-1 Rev RNA response elements: insights into the mechanism of Rex and Rev action. Genes Dev. 4:1014-1022.
10. Hanly SM, Rimsky LT, Malim MH, Kim JH, Hauber J, Duc Dodon M, Le SY, Maizel JV, Cullen BR, Greene WC. 1989. Comparative analysis of the HTLV-I Rex and HIV-1 Rev trans-regulatory proteins and their RNA response elements. Genes Dev. 3:1534-1544. http://dx.doi.org/10.1101/gad.3.10.1534.
11. Mertz JA, Simper MS, Lozano MM, Payne SM, Dudley JP. 2005. Mouse mammary tumor virus encodes a self-regulatory RNA export protein and is a complex retrovirus. J. Virol. 79:14737-14747. http://dx.doi.org/10.1128/JVI.79.23.14737-14747.2005.
12. Nitta T, Hofacre A, Hull S, Fan H. 2009. Identification and mutational analysis of a Rej response element in Jaagsiekte sheep retrovirus RNA. J. Virol. 83:12499-12511. http://dx.doi.org/10.1128/JVI.01754-08.
13. Bodem J, Schied T, Gabriel R, Rammling M, Rethwilm A. 2011. Foamy virus nuclear RNA export is distinct from that of other retroviruses. J. Virol. 85:2333-2341. http://dx.doi.org/10.1128/JVI.01518-10.
14. Bray M, Prasad S, Dubay JW, Hunter E, Jeang KT, Rekosh D, Hammarskjold ML. 1994. 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. 91:1256-1260. http://dx.doi.org/10.1073/pnas.91.4.1256.
15. Swanson CM, Puffer BA, Ahmad KM, Doms RW, Malim MH. 2004. Retroviral mRNA nuclear export elements regulate protein function and virion assembly. EMBO J. 23:2632-2640. http://dx.doi.org/10.1038/sj.emboj.7600270.
16. Li Y, Bor YC, Misawa Y, Xue Y, Rekosh D, Hammarskjold ML. 2006. An intron with a constitutive transport element is retained in a Tap messenger RNA. Nature 443:234-237. http://dx.doi.org/10.1038/nature05107.
17. Yang J, Cullen BR. 1999. Structural and functional analysis of the avian leukemia virus constitutive transport element. RNA 5:1645-1655. http://dx.doi.org/10.1017/S1355838299991616.
18. Paca RE, Ogert RA, Hibbert CS, Izaurralde E, Beemon KL. 2000. Rous sarcoma virus DR posttranscriptional elements use a novel RNA export pathway. J. Virol. 74:9507-9514. http://dx.doi.org/10.1128/JVI.74.20.9507-9514.2000.
19. LeBlanc JJ, Uddowla S, Abraham B, Clatterbuck S, Beemon KL. 2007. Tap and Dbp5, but not Gag, are involved in DR-mediated nuclear export of unspliced Rous sarcoma virus RNA. Virology 363:376-386. http://dx.doi.org/10.1016/j.virol.2007.01.026.
20. Trubetskoy AM, Okenquist SA, Lenz J. 1999. R region sequences in the long terminal repeat of a murine retrovirus specifically increase expression of unspliced RNAs. J. Virol. 73:3477-3483.
21. Kraunus J, Zychlinski D, Heise T, Galla M, Bohne J, Baum C. 2006. Murine leukemia virus regulates alternative splicing through sequences upstream of the 5= splice site. J. Biol. Chem. 281:37381-37390. http://dx.doi.org/10.1074/jbc. M601537200.
22. Sakuma T, Ravin SS, Tonne JM, Thatava T, Ohmine S, Takeuchi Y, Malech HL, Ikeda Y. 2010. Characterization of retroviral and lentiviral vectors pseudotyped with XMRV envelope glycoprotein. Hum. Gene Ther. 21:1665-1673. http://dx.doi.org/10.1089/hum.2010.063.
23. Miller AD, Law MF, Verma IM. 1985. Generation of helper-free amphotropic retroviruses that transduce a dominant-acting, methotrexateresistant dihydrofolate reductase gene. Mol. Cell. Biol. 5:431-437.
24. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY. 2010. Long noncoding RNA as modular scaffold of histone modification complexes. Science 329:689-693. http://dx.doi.org/10.1126/science.1192002.
25. Sakuma R, Sakuma T, Ohmine S, Silverman RH, Ikeda Y. 2010. Xenotropic murine leukemia virus-related virus is susceptible to AZT. Virology 397:1-6. http://dx.doi.org/10.1016/j.virol.2009.11.013.
26. Sakuma T, Hue S, Squillace KA, Tonne JM, Blackburn PR, Ohmine S, Thatava T, Towers GJ, Ikeda Y. 2011. No evidence of XMRV in prostate cancer cohorts in the Midwestern United States. Retrovirology 8:23. http://dx.doi.org/10.1186/1742-4690-8-23.
27. Wang L, Wang S, Li W. 2012. RSeQC: quality control of RNA-seq experiments. Bioinformatics 28:2184-2185. http://dx.doi.org/10.1093/bioinformatics/bts356.
28. Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105-1111. http://dx.doi.org/10.1093/bioinformatics/btp120.
29. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. http://dx.doi.org/10.1186/gb-2009-10-3-r25.
30. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760. http://dx.doi.org/10.1093/bioinformatics/btp324.
31. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA. 2010. The Genome Analysis Toolkit: a MapReduce framework for analyzing nextgeneration DNA sequencing data. Genome Res. 20:1297-1303. http://dx.doi.org/10.1101/gr.107524.110.
32. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139-140. http://dx.doi.org/10.1093/bioi nformatics/btp616.
33. Berlioz C, Darlix JL. 1995. An internal ribosomal entry mechanism promotes translation of murine leukemia virus gag polyprotein precursors. J. Virol. 69:2214-2222.
34. Carroll R, Derse D. 1993. Translation of equine infectious anemia virus bicistronic tat-revmRNArequires leaky ribosome scanning of the tatCTG initiation codon. J. Virol. 67:1433-1440.
35. Ernst RK, Bray M, Rekosh D, Hammarskjold ML. 1997. Secondary structure and mutational analysis of the Mason-Pfizer monkey virus RNA constitutive transport element. RNA 3:210-222.
36. Tabernero C, Zolotukhin AS, Valentin A, Pavlakis GN, Felber BK. 1996. The posttranscriptional control element of the simian retrovirus type 1 forms an extensive RNA secondary structure necessary for its function. J. Virol. 70:5998-6011.
37. Singh R, Green MR. 1993. Sequence-specific binding of transfer RNA by glyceraldehyde-3-phosphate dehydrogenase. Science 259:365-368. http://dx.doi.org/10.1126/science.8420004.
38. Mingot JM, Kostka S, Kraft R, Hartmann E, Gorlich D. 2001. Importin 13: a novel mediator of nuclear import and export. EMBO J. 20:3685-3694. http://dx.doi.org/10.1093/emboj/20.14.3685.
39. Kutay U, BischoffFR, Kostka S, Kraft R, Gorlich D. 1997. Export of importin alpha from the nucleus is mediated by a specific nuclear transport factor. Cell 90:1061-1071. http://dx.doi.org/10.1016/S0092-8674 (00)80372-4.
40. Kurisaki A, Kurisaki K, Kowanetz M, Sugino H, Yoneda Y, Heldin CH, Moustakas A. 2006. The mechanism of nuclear export of Smad3 involves exportin 4 and Ran. Mol. Cell. Biol. 26:1318-1332. http://dx.doi.org/10.1128/MCB.26.4.1318-1332.2006.
41. Lipowsky G, BischoffFR, Schwarzmaier P, Kraft R, Kostka S, Hartmann E, Kutay U, Gorlich D. 2000. Exportin 4: a mediator of a novel nuclear export pathway in higher eukaryotes. EMBO J. 19:4362-4371. http://dx.doi.org/10.1093/emboj/19.16.4362.
42. Brownawell AM, Macara IG. 2002. Exportin-5, a novel karyopherin, mediates nuclear export of double-stranded RNA binding proteins. J. Cell Biol. 156:53-64. http://dx.doi.org/10.1083/jcb.200110082.
43. Bohnsack MT, Regener K, Schwappach B, Saffrich R, Paraskeva E, Hartmann E, Gorlich D. 2002. Exp5 exports eEF1A via tRNA from nuclei and synergizes with other transport pathways to confine translation to the cytoplasm. EMBO J. 21:6205-6215. http://dx.doi.org/10.1093/emboj/cdf613.
44. Calado A, Treichel N, Muller EC, Otto A, Kutay U. 2002. Exportin-5-mediated nuclear export of eukaryotic elongation factor 1A and tRNA. EMBO J. 21:6216-6224. http://dx.doi.org/10.1093/emboj/cdf620.
45. Gwizdek C, Ossareh-Nazari B, Brownawell AM, Doglio A, Bertrand E, Macara IG, Dargemont C. 2003. Exportin-5 mediates nuclear export of minihelix-containing RNAs. J. Biol. Chem. 278:5505-5508. http://dx.doi.org/10.1074/jbc. C200668200.
46. Stade K, Ford CS, Guthrie C, Weis K. 1997. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 90:1041-1050. http://dx.doi.org/10.1016/S0092-8674(00)80370-0.
47. Fornerod M, Ohno M, Yoshida M, Mattaj IW. 1997. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90:1051-1060. http://dx.doi.org/10.1016/S0092-8674(00)80371-2.
48. Stuven T, Hartmann E, Gorlich D. 2003. Exportin 6: a novel nuclear export receptor that is specific for profilin. actin complexes. EMBO J. 22: 5928-5940. http://dx.doi.org/10.1093/emboj/cdg565.
49. Mingot JM, Bohnsack MT, Jakle U, Gorlich D. 2004. Exportin 7 defines a novel general nuclear export pathway. EMBO J. 23:3227-3236. http://dx.doi.org/10.1038/sj.emboj.7600338.
50. Paprotka T, Delviks-Frankenberry KA, Cingoz O, Martinez A, Kung HJ, Tepper CG, Hu WS, Fivash MJ, Jr, Coffin JM, Pathak VK. 2011. Recombinant origin of the retrovirus XMRV. Science 333:97-101. http://dx.doi.org/10.1126/science.1205292.
51. Wickramasinghe VO, McMurtrie PI, Mills AD, Takei Y, Penrhyn-Lowe S, Amagase Y, Main S, Marr J, Stewart M, Laskey RA. 2010. mRNA export from mammalian cell nuclei is dependent on GANP. Curr. Biol. 20:25-31. http://dx.doi.org/10.1016/j.cub.2009.10.078.
52. Oshima M, Odawara T, Matano T, Sakahira H, Kuchino Y, Iwamoto A, Yoshikura H. 1996. Possible role of splice acceptor site in expression of unspliced gag-containing message of Moloney murine leukemia virus. J. Virol. 70:2286-2295.
53. Wodrich H, Bohne J, Gumz E, Welker R, Krausslich HG. 2001. A new RNA element located in the coding region of a murine endogenous retrovirus can functionally replace the Rev/Rev-responsive element system in human immunodeficiency virus type 1 Gag expression. J. Virol. 75: 10670-10682. http://dx.doi.org/10.1128/JVI.75.22.10670-10682.2001.
54. Rodrigues JP, Rode M, Gatfield D, Blencowe BJ, Carmo-Fonseca M, Izaurralde E. 2001. REF proteins mediate the export of spliced and unspliced mRNAs from the nucleus. Proc. Natl. Acad. Sci. U. S. A. 98:1030-1035. http://dx.doi.org/10.1073/pnas.98.3.1030.
55. Zolotukhin AS, Tan W, Bear J, Smulevitch S, Felber BK. 2002. U2AF participates in the binding of TAP (NXF1) to mRNA. J. Biol. Chem. 277: 3935-3942. http://dx.doi.org/10.1074/jbc. M107598200.
56. Hautbergue GM, Hung ML, Walsh MJ, Snijders AP, Chang CT, Jones R, Ponting CP, Dickman MJ, Wilson SA. 2009. UIF, a new mRNA export adaptor that works together with REF/ALY, requires FACT for recruitment to mRNA. Curr. Biol. 19:1918-1924. http://dx.doi.org/10.1016/j.cub.2009.09.041.
57. Viphakone N, Hautbergue GM, Walsh M, Chang CT, Holland A, Folco EG, Reed R, Wilson SA. 2012. TREX exposes the RNA-binding domain of Nxf1 to enable mRNA export. Nat. Commun. 3:1006. http://dx.doi.org/10.1038/ncomms2005.
58. Morita M, Kuba K, Ichikawa A, Nakayama M, Katahira J, Iwamoto R, Watanebe T, Sakabe S, Daidoji T, Nakamura S, Kadowaki A, Ohto T, Nakanishi H, Taguchi R, Nakaya T, Murakami M, Yoneda Y, Arai H, Kawaoka Y, Penninger JM, Arita M, Imai Y. 2013. The lipid mediator protectin D1 inhibits influenza virus replication and improves severe influenza. Cell 153:112-125. http://dx.doi.org/10.1016/j.cell.2013.02.027.
59. Gruter P, Tabernero C, von Kobbe C, Schmitt C, Saavedra C, Bachi A, Wilm M, Felber BK, Izaurralde E. 1998. TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol. Cell 1:649-659. http://dx.doi.org/10.1016/S1097-2765(00)80065-9.
60. Braun IC, Rohrbach E, Schmitt C, Izaurralde E. 1999. TAP binds to the constitutive transport element (CTE) through a novel RNA-binding motif that is sufficient to promote CTE-dependent RNA export from the nucleus. EMBO J. 18:1953-1965. http://dx.doi.org/10.1093/emboj/18.7.1953.
61. Teplova M, Wohlbold L, Khin NW, Izaurralde E, Patel DJ. 2011. Structure-function studies of nucleocytoplasmic transport of retroviral genomic RNA by mRNA export factor TAP. Nat. Struct. Mol. Biol. 18: 990-998. http://dx.doi.org/10.1038/nsmb.2094.
62. Kang Y, Cullen BR. 1999. The human Tap protein is a nuclear mRNA export factor that contains novel RNA-binding and nucleocytoplasmic transport sequences. Genes Dev. 13:1126-1139. http://dx.doi.org/10.1101/gad.13.9.1126.
63. Luo MJ, Reed R. 1999. Splicing is required for rapid and efficient mRNA export in metazoans. Proc. Natl. Acad. Sci. U. S. A. 96:14937-14942. http://dx.doi.org/10.1073/pnas.96.26.14937.
64. Cupelli L, Okenquist SA, Trubetskoy A, Lenz J. 1998. 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. 72: 7807-7814.
65. Cullen BR. 2000. Connections between the processing and nuclear export of mRNA: evidence for an export license? Proc. Natl. Acad. Sci. U. S. A. 97:4-6. http://dx.doi.org/10.1073/pnas.97.1.4.
66. Lei H, Dias AP, Reed R. 2011. Export and stability of naturally intronless mRNAs require specific coding region sequences and the TREX mRNA export complex. Proc. Natl. Acad. Sci. U. S. A. 108:17985-17990. http://dx.doi.org/10.1073/pnas.1113076108.
67. Anko ML, Neugebauer KM. 2012. RNA-protein interactions in vivo: global gets specific. Trends Biochem. Sci. 37:255-262. http://dx.doi.org/10.1016/j.tibs.2012.02.005.
68. Johnson LA, Sandri-Goldin RM. 2009. Efficient nuclear export of herpes simplex virus 1 transcripts requires both RNA binding by ICP27 and ICP27 interaction with TAP/NXF1. J. Virol. 83:1184-1192. http://dx.doi.org/10.1128/JVI.02010-08.
69. Kim M, Bellini M, Ceman S. 2009. Fragile X mental retardation protein FMRPbinds mRNAs in the nucleus. Mol. Cell. Biol. 29:214-228. http://dx.doi.org/10.1128/MCB.01377-08.
70. Jin L, Guzik BW, Bor YC, Rekosh D, Hammarskjold ML. 2003. Tap and NXT promote translation of unspliced mRNA. Genes Dev. 17:3075-3086. http://dx.doi.org/10.1101/gad.1155703.
71. Sakuma T, Tonne JM, Squillace KA, Ohmine S, Thatava T, Peng KW, Barry MA, Ikeda Y. 2011. Early events in retrovirus XMRV infection of the wild-derived mouse Mus pahari. J. Virol. 85:1205-1213. http://dx.doi.org/10.1128/JVI.00886-10.