Gammaretroviral pol sequences act in cis to direct polysome loading and NXF1/NXT-dependent protein production by gag-encoded RNA

Retrovirology

Volumn 11, Issue 1, 2014, Pages

  Bartels, Hanni ^a   Luban, Jeremy ^a,b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; GAG PROTEIN; MESSENGER RNA; NUCLEOTIDE; NXF1 PROTEIN; NXT PROTEIN; POL PROTEIN; PROTEIN; UNCLASSIFIED DRUG; VIRUS RNA; NUCLEOCYTOPLASMIC TRANSPORT PROTEIN; NXF1 PROTEIN, HUMAN; RNA BINDING PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; FRAMESHIFT MUTATION; GENE DELETION; HUMAN; HUMAN CELL; MURINE LEUKEMIA VIRUS; NORTHERN BLOTTING; OPEN READING FRAME; PLASMID; POLYSOME; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSLATION; XENOTROPIC MULV RELATED VIRUS; CELL LINE; CYTOPLASM; GENETICS; HEK293 CELL LINE; MASON PFIZER MONKEY VIRUS; RETROVIRUS; RNA SPLICING;

CELL LINE; CYTOPLASM; GAMMARETROVIRUS; GENE PRODUCTS, GAG; HEK293 CELLS; HUMANS; MASON-PFIZER MONKEY VIRUS; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; POLYRIBOSOMES; RNA SPLICING; RNA, MESSENGER; RNA, VIRAL; RNA-BINDING PROTEINS; SEQUENCE DELETION;

EID: 84910039824     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/s12977-014-0073-0     Document Type: Article

References (73)

1. Leblanc J, Weil J, Beemon K. Posttranscriptional regulation of retroviral gene expression: primary RNA transcripts play three roles as pre-mRNA, mRNA, and genomic RNA. Wiley Interdiscip Rev RNA 2013, 4:567-580. 10.1002/wrna.1179, 23754689.
2. Malim MH, Hauber J, Le SY, Maizel JV, Cullen BR. 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. 10.1038/338254a0, 2784194.
3. Stoltzfus CM. Chapter 1. Regulation of HIV-1 alternative RNA splicing and its role in virus replication. Adv Virus Res 2009, 74:1-40. 10.1016/S0065-3527(09)74001-1, 19698894.
4. Bolinger C, Boris-Lawrie K. Mechanisms employed by retroviruses to exploit host factors for translational control of a complicated proteome. Retrovirology 2009, 6:8. 10.1186/1742-4690-6-8, 19166625.
5. Johnson SF, Telesnitsky A. Retroviral RNA dimerization and packaging: the what, how, when, where, and why. PLoS Path 2010, 6:e1001007. 10.1371/journal.ppat.1001007.
6. Purcell DF, Martin MA. Alternative splicing of human immunodeficiency virus type 1 mRNA modulates viral protein expression, replication, and infectivity. J Virol 1993, 67:6365-6378. 8411338.
7. Ocwieja KE, Sherrill-Mix S, Mukherjee R, Custers-Allen R, David P, Brown M, Wang S, Link DR, Olson J, Travers K, Schadt E, Bushman FD. Dynamic regulation of HIV-1 mRNA populations analyzed by single-molecule enrichment and long-read sequencing. Nucleic Acids Res 2012, 40:10345-10355. 10.1093/nar/gks753, 22923523.
8. Cullen BR. Nuclear mRNA export: insights from virology. Trends Biochem Sci 2003, 28:419-424. 10.1016/S0968-0004(03)00142-7, 12932730.
9. Hoskins AA, Moore MJ. The spliceosome: a flexible, reversible macromolecular machine. Trends Biochem Sci 2012, 37:179-188. 10.1016/j.tibs.2012.02.009, 22480731.
10. Dayton AI, Terwilliger EF, Potz J, Kowalski M, Sodroski JG, Haseltine WA. Cis-acting sequences responsive to the rev gene product of the human immunodeficiency virus. J Acquir Immune Defic Syndr 1988, 1:441-452. 2851651.
11. Fornerod M, Ohno M, Yoshida M, Mattaj IW. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 1997, 90:1051-1060. 10.1016/S0092-8674(00)80371-2, 9323133.
12. Sodroski J, Goh WC, Rosen C, Dayton A, Terwilliger E, Haseltine W. A second post-transcriptional trans-activator gene required for HTLV-III replication. Nature 1986, 321:412-417. 10.1038/321412a0, 3012355.
13. Rizvi TA, Schmidt RD, Lew KA. Mason-Pfizer monkey virus (MPMV) constitutive transport element (CTE) functions in a position-dependent manner. Virology 1997, 236:118-129. 10.1006/viro.1997.8728, 9299624.
14. Bray M, Prasad S, Dubay JW, Hunter E, Jeang KT, Rekosh D, Hammarskjold ML. 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. 10.1073/pnas.91.4.1256, 8108397.
15. Hull S, Boris-Lawrie K. Analysis of synergy between divergent simple retrovirus posttranscriptional control elements. Virology 2003, 317:146-154. 10.1016/j.virol.2003.08.037, 14675633.
16. Pasquinelli AE, Ernst RK, Lund E, Grimm C, Zapp ML, Rekosh D, Hammarskjold ML, Dahlberg JE. The constitutive transport element (CTE) of Mason-Pfizer monkey virus (MPMV) accesses a cellular mRNA export pathway. EMBO J 1997, 16:7500-7510. 10.1093/emboj/16.24.7500, 9405378.
17. Boeras I, Sakalian M, West JT. Translation of MMTV Gag requires nuclear events involving splicing motifs in addition to the viral Rem protein and RmRE. Retrovirology 2012, 9:8. 10.1186/1742-4690-9-8, 22277305.
18. Nitta T, Hofacre A, Hull S, Fan H. Identification and mutational analysis of a Rej response element in Jaagsiekte sheep retrovirus RNA. J Virol 2009, 83:12499-12511. 10.1128/JVI.01754-08, 19776134.
19. Aschoff JM, Foster D, Coffin JM. Point mutations in the avian sarcoma/leukosis virus 3' untranslated region result in a packaging defect. J Virol 1999, 73:7421-7429. 10438832.
20. Ogert RA, Lee LH, Beemon KL. Avian retroviral RNA element promotes unspliced RNA accumulation in the cytoplasm. J Virol 1996, 70:3834-3843. 8648719.
21. Paca RE, Ogert RA, Hibbert CS, Izaurralde E, Beemon KL. Rous sarcoma virus DR posttranscriptional elements use a novel RNA export pathway. J Virol 2000, 74:9507-9514. 10.1128/JVI.74.20.9507-9514.2000, 11000220.
22. Yang J, Cullen BR. Structural and functional analysis of the avian leukemia virus constitutive transport element. RNA 1999, 5:1645-1655. 10.1017/S1355838299991616, 10606274.
23. Orlova M, Yueh A, Leung J, Goff SP. Reverse transcriptase of Moloney murine leukemia virus binds to eukaryotic release factor 1 to modulate suppression of translational termination. Cell 2003, 115:319-331. 10.1016/S0092-8674(03)00805-5, 14636559.
24. Lazo PA, Prasad V, Tsichlis PN. Splice acceptor site for the env message of Moloney murine leukemia virus. J Virol 1987, 61:2038-2041. 3573155.
25. Oshima M, Odawara T, Matano T, Sakahira H, Kuchino Y, Iwamoto A, Yoshikura H. Possible role of splice acceptor site in expression of unspliced gag-containing message of Moloney murine leukemia virus. J Virol 1996, 70:2286-2295. 8642655.
26. Urisman A, Molinaro RJ, Fischer N, Plummer SJ, Casey G, Klein EA, Malathi K, Magi-Galluzzi C, Tubbs RR, Ganem D, Silverman RH, DeRisi JL. Identification of a novel Gammaretrovirus in prostate tumors of patients homozygous for R462Q RNASEL variant. PLoS Pathog 2006, 2:e25. 10.1371/journal.ppat.0020025, 16609730.
27. Hebsgaard SM, Korning PG, Tolstrup N, Engelbrecht J, Rouze P, Brunak S. Splice site prediction in Arabidopsis thaliana pre-mRNA by combining local and global sequence information. Nucleic Acids Res 1996, 24:3439-3452. 10.1093/nar/24.17.3439, 8811101.
28. Brunak S, Engelbrecht J, Knudsen S. Prediction of human mRNA donor and acceptor sites from the DNA sequence. J Mol Biol 1991, 220:49-65. 10.1016/0022-2836(91)90380-O, 2067018.
29. Coyle JH, Guzik BW, Bor YC, Jin L, Eisner-Smerage L, Taylor SJ, Rekosh D, Hammarskjold ML. Sam68 enhances the cytoplasmic utilization of intron-containing RNA and is functionally regulated by the nuclear kinase Sik/BRK. Mol Cell Biol 2003, 23:92-103. 10.1128/MCB.23.1.92-103.2003, 12482964.
30. Li Y, Bor YC, Misawa Y, Xue Y, Rekosh D, Hammarskjold ML. An intron with a constitutive transport element is retained in a Tap messenger RNA. Nature 2006, 443:234-237. 10.1038/nature05107, 16971948.
31. Jin L, Guzik BW, Bor YC, Rekosh D, Hammarskjold ML. Tap and NXT promote translation of unspliced mRNA. Genes Dev 2003, 17:3075-3086. 10.1101/gad.1155703, 14701875.
32. Gruter P, Tabernero C, von Kobbe C, Schmitt C, Saavedra C, Bachi A, Wilm M, Felber BK, Izaurralde E. TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol Cell 1998, 1:649-659. 10.1016/S1097-2765(00)80065-9, 9660949.
33. Teplova M, Wohlbold L, Khin NW, Izaurralde E, Patel DJ. Structure-function studies of nucleocytoplasmic transport of retroviral genomic RNA by mRNA export factor TAP. Nat Struct Mol Biol 2011, 18:990-998. 10.1038/nsmb.2094, 21822283.
34. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003, 31:3406-3415. 10.1093/nar/gkg595, 12824337.
35. Braun IC, Rohrbach E, Schmitt C, Izaurralde E. 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 1999, 18:1953-1965. 10.1093/emboj/18.7.1953, 10202158.
36. Ernst RK, Bray M, Rekosh D, Hammarskjold ML. A structured retroviral RNA element that mediates nucleocytoplasmic export of intron-containing RNA. Mol Cell Biol 1997, 17:135-144. 8972193.
37. Kang Y, Bogerd HP, Yang J, Cullen BR. Analysis of the RNA binding specificity of the human tap protein, a constitutive transport element-specific nuclear RNA export factor. Virology 1999, 262:200-209. 10.1006/viro.1999.9906, 10489353.
38. Ho DN, Coburn GA, Kang Y, Cullen BR, Georgiadis MM. The crystal structure and mutational analysis of a novel RNA-binding domain found in the human Tap nuclear mRNA export factor. Proc Natl Acad Sci U S A 2002, 99:1888-1893. 10.1073/pnas.042698599, 11854490.
39. Coburn GA, Wiegand HL, Kang Y, Ho DN, Georgiadis MM, Cullen BR. Using viral species specificity to define a critical protein/RNA interaction surface. Genes Dev 2001, 15:1194-1205. 10.1101/gad.888201, 11358864.
40. Pertel T, Hausmann S, Morger D, Zuger S, Guerra J, Lascano J, Reinhard C, Santoni FA, Uchil PD, Chatel L, Bisiaux A, Albert ML, Strambio de Castillia C, Mothes W, Pizzato M, Grütter MG, Luban J. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 2011, 472:361-365. 10.1038/nature09976, 21512573.
41. De Iaco A, Luban J. Inhibition of HIV-1 infection by TNPO3 depletion is determined by capsid and detectable after viral cDNA enters the nucleus. Retrovirology 2011, 8:98. 10.1186/1742-4690-8-98, 22145813.
42. Swartz JE, Bor YC, Misawa Y, Rekosh D, Hammarskjold ML. The shuttling SR protein 9G8 plays a role in translation of unspliced mRNA containing a constitutive transport element. J Biol Chem 2007, 282:19844-19853. 10.1074/jbc.M701660200, 17513303.
43. Swanson CM, Sherer NM, Malim MH. SRp40 and SRp55 promote the translation of unspliced human immunodeficiency virus type 1 RNA. J Virol 2010, 84:6748-6759. 10.1128/JVI.02526-09, 20427542.
44. Sanford JR, Gray NK, Beckmann K, Caceres JF. A novel role for shuttling SR proteins in mRNA translation. Genes Dev 2004, 18:755-768. 10.1101/gad.286404, 15082528.
45. Huang Y, Gattoni R, Stevenin J, Steitz JA. SR splicing factors serve as adapter proteins for TAP-dependent mRNA export. Mol Cell 2003, 11:837-843. 10.1016/S1097-2765(03)00089-3, 12667464.
46. Huang Y, Steitz JA. Splicing factors SRp20 and 9G8 promote the nucleocytoplasmic export of mRNA. Mol Cell 2001, 7:899-905. 10.1016/S1097-2765(01)00233-7, 11336712.
47. Escudero-Paunetto L, Li L, Hernandez FP, Sandri-Goldin RM. SR proteins SRp20 and 9G8 contribute to efficient export of herpes simplex virus 1 mRNAs. Virology 2010, 401:155-164. 10.1016/j.virol.2010.02.023, 20227104.
48. Ote I, Lebrun M, Vandevenne P, Bontems S, Medina-Palazon C, Manet E, Piette J, Sadzot-Delvaux C. Varicella-zoster virus IE4 protein interacts with SR proteins and exports mRNAs through the TAP/NXF1 pathway. PLoS One 2009, 4:e7882. 10.1371/journal.pone.0007882, 19924249.
49. Caceres JF, Screaton GR, Krainer AR. A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes Dev 1998, 12:55-66. 10.1101/gad.12.1.55, 9420331.
50. Huang Y, Steitz JA. SRprises along a messenger's journey. Mol Cell 2005, 17:613-615. 10.1016/j.molcel.2005.02.020, 15749011.
51. Hargous Y, Hautbergue GM, Tintaru AM, Skrisovska L, Golovanov AP, Stevenin J, Lian LY, Wilson SA, Allain FH. Molecular basis of RNA recognition and TAP binding by the SR proteins SRp20 and 9G8. EMBO J 2006, 25:5126-5137. 10.1038/sj.emboj.7601385, 17036044.
52. Sakuma T, Davila JI, Malcolm JA, Kocher JP, Tonne JM, Ikeda Y. Murine leukemia virus uses NXF1 for nuclear export of spliced and unspliced viral transcripts. J Virol 2014, 88:4069-4082. 10.1128/JVI.03584-13, 24478440.
53. Paprotka T, Delviks-Frankenberry KA, Cingoz O, Martinez A, Kung HJ, Tepper CG, Hu WS, Fivash MJ, Coffin JM, Pathak VK. Recombinant origin of the retrovirus XMRV. Science 2011, 333:97-101. 10.1126/science.1205292, 21628392.
54. Shabalina SA, Ogurtsov AY, Spiridonov AN, Novichkov PS, Spiridonov NA, Koonin EV. Distinct patterns of expression and evolution of intronless and intron-containing mammalian genes. Mol Biol Evol 2010, 27:1745-1749. 10.1093/molbev/msq086, 20360214.
55. Gilbert W, Guthrie C. The Glc7p nuclear phosphatase promotes mRNA export by facilitating association of Mex67p with mRNA. Mol Cell 2004, 13:201-212. 10.1016/S1097-2765(04)00030-9, 14759366.
56. Huang Y, Carmichael GG. The mouse histone H2a gene contains a small element that facilitates cytoplasmic accumulation of intronless gene transcripts and of unspliced HIV-1-related mRNAs. Proc Natl Acad Sci U S A 1997, 94:10104-10109. 10.1073/pnas.94.19.10104, 9294170.
57. Huang Y, Wimler KM, Carmichael GG. Intronless mRNA transport elements may affect multiple steps of pre-mRNA processing. EMBO J 1999, 18:1642-1652. 10.1093/emboj/18.6.1642, 10075934.
58. Erkmann JA, Sanchez R, Treichel N, Marzluff WF, Kutay U. Nuclear export of metazoan replication-dependent histone mRNAs is dependent on RNA length and is mediated by TAP. RNA 2005, 11:45-58. 10.1261/rna.7189205, 15611298.
59. Hautbergue GM, Hung ML, Golovanov AP, Lian LY, Wilson SA. Mutually exclusive interactions drive handover of mRNA from export adaptors to TAP. Proc Natl Acad Sci U S A 2008, 105:5154-5159. 10.1073/pnas.0709167105, 18364396.
60. Sanford JR, Ellis J, Caceres JF. Multiple roles of arginine/serine-rich splicing factors in RNA processing. Biochem Soc Trans 2005, 33:443-446. 10.1042/BST0330443, 15916537.
61. Strasser K, Hurt E. Yra1p, a conserved nuclear RNA-binding protein, interacts directly with Mex67p and is required for mRNA export. EMBO J 2000, 19:410-420. 10.1093/emboj/19.3.410, 10722314.
62. Stutz F, Bachi A, Doerks T, Braun IC, Seraphin B, Wilm M, Bork P, Izaurralde E. REF, an evolutionary conserved family of hnRNP-like proteins, interacts with TAP/Mex67p and participates in mRNA nuclear export. RNA 2000, 6:638-650. 10.1017/S1355838200000078, 10786854.
63. 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. 10.1016/S0960-9822(06)00288-0, 9285715.
64. Sanford JR, Ellis JD, Cazalla D, Caceres JF. Reversible phosphorylation differentially affects nuclear and cytoplasmic functions of splicing factor 2/alternative splicing factor. Proc Natl Acad Sci U S A 2005, 102:15042-15047. 10.1073/pnas.0507827102, 16210245.
65. Lawrence JB, Singer RH. Intracellular localization of messenger RNAs for cytoskeletal proteins. Cell 1986, 45:407-415. 10.1016/0092-8674(86)90326-0, 3698103.
66. Kislauskis EH, Li Z, Singer RH, Taneja KL. Isoform-specific 3'-untranslated sequences sort alpha-cardiac and beta-cytoplasmic actin messenger RNAs to different cytoplasmic compartments. J Cell Biol 1993, 123:165-172. 10.1083/jcb.123.1.165, 8408195.
67. Zhang HL, Eom T, Oleynikov Y, Shenoy SM, Liebelt DA, Dictenberg JB, Singer RH, Bassell GJ. Neurotrophin-induced transport of a beta-actin mRNP complex increases beta-actin levels and stimulates growth cone motility. Neuron 2001, 31:261-275. 10.1016/S0896-6273(01)00357-9, 11502257.
68. Shestakova EA, Wyckoff J, Jones J, Singer RH, Condeelis J. Correlation of beta-actin messenger RNA localization with metastatic potential in rat adenocarcinoma cell lines. Cancer Res 1999, 59:1202-1205. 10096548.
69. Shestakova EA, Singer RH, Condeelis J. The physiological significance of beta -actin mRNA localization in determining cell polarity and directional motility. Proc Natl Acad Sci U S A 2001, 98:7045-7050. 10.1073/pnas.121146098, 11416185.
70. Huttelmaier S, Zenklusen D, Lederer M, Dictenberg J, Lorenz M, Meng X, Bassell GJ, Condeelis J, Singer RH. Spatial regulation of beta-actin translation by Src-dependent phosphorylation of ZBP1. Nature 2005, 438:512-515. 10.1038/nature04115, 16306994.
71. Frosst P, Guan T, Subauste C, Hahn K, Gerace L. Tpr is localized within the nuclear basket of the pore complex and has a role in nuclear protein export. J Cell Biol 2002, 156:617-630. 10.1083/jcb.200106046, 11839768.
72. Cordes VC, Reidenbach S, Rackwitz HR, Franke WW. Identification of protein p270/Tpr as a constitutive component of the nuclear pore complex-attached intranuclear filaments. J Cell Biol 1997, 136:515-529. 10.1083/jcb.136.3.515, 9024684.
73. Coyle JH, Bor YC, Rekosh D, Hammarskjold ML. The Tpr protein regulates export of mRNAs with retained introns that traffic through the Nxf1 pathway. RNA 2011, 17:1344-1356. 10.1261/rna.2616111, 21613532.