Jaagsiekte sheep retrovirus encodes a regulatory factor, Rej, required for synthesis of Gag protein

Journal of Virology

Volumn 83, Issue 23, 2009, Pages 12483-12498

  Hofacre, Andrew ^a   Nitta, Takayuki ^a   Fan, Hung ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; GAG PROTEIN; MESSENGER RNA; METHIONINE; POL PROTEIN; PROTEIN REC; PROTEIN REJ; PROTEIN REM; REGULATOR PROTEIN; REV PROTEIN; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN; VIRUS RNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; ENVELOPE GENE; GENE DELETION; GENE SEQUENCE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; JAAGSIEKTE SHEEP RETROVIRUS; MOLECULAR CLONING; MOUSE; MOUSE MAMMARY TUMOR ONCOVIRUS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN SYNTHESIS; PROVIRUS; RNA SPLICING; VIRUS GENOME;

ANIMALS; CARRIER PROTEINS; CELL LINE; ENDOGENOUS RETROVIRUSES; GENE PRODUCTS, GAG; HUMANS; JAAGSIEKTE SHEEP RETROVIRUS; MAMMARY TUMOR VIRUS, MOUSE; MOLECULAR SEQUENCE DATA; PROVIRUSES; SEQUENCE ANALYSIS, DNA; SEQUENCE DELETION; SEQUENCE HOMOLOGY; VIRAL ENVELOPE PROTEINS; VIRUS REPLICATION;

BETARETROVIRUS; HUMAN ENDOGENOUS RETROVIRUS K; HUMAN IMMUNODEFICIENCY VIRUS; JAAGSIEKTE SHEEP RETROVIRUS; MOUSE MAMMARY TUMOR VIRUS;

EID: 70450164478     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01747-08     Document Type: Article

References (62)

1. Arrigo, S. J., and I. S. Chen. 1991. Rev is necessary for translation but not cytoplasmic accumulation of HIV-1 vif, vpr, and env/vpu 2 RNAs. Genes Dev. 5:808-819.
2. Boese, A., M. Sauter, U. Galli, B. Best, H. Herbst, J. Mayer, E. Kremmer, K. Roemer, and N. Mueller-Lantzsch. 2000. Human endogenous retrovirus protein cORF supports cell transformation and associates with the promyelocytic leukemia zinc finger protein. Oncogene 19:4328-4336. (Pubitemid 30744362)
3. Bogerd, H. P., A. Echarri, T. M. Ross, and B. R. Cullen. 1998. Inhibition of human immunodeficiency virus Rev and human T-cell leukemia virus Rex function, but not Mason-Pfizer monkey virus constitutive transport element activity, by a mutant human nucleoporin targeted to Crm1. J. Virol. 72:8627-8635.
4. Bray, M., S. Prasad, J. W. Dubay, E. Hunter, K. T. Jeang, D. Rekosh, and M. L. Hammarskjold. 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. USA 91:1256-1260.
5. Butsch, M., S. Hull, Y. Wang, T. M. Roberts, and K. Boris-Lawrie. 1999. The 5′ RNA terminus of spleen necrosis virus contains a novel posttranscriptional control element that facilitates human immunodeficiency virus Rev/ RRE-independent Gag production. J. Virol. 73:4847-4855. (Pubitemid 29246745)
6. Caporale, M., F. Arnaud, M. Mura, M. Golder, C. Murgia, and M. Palmarini. 2009. The signal peptide of a simple retrovirus envelope functions as a posttranscriptional regulator of viral gene expression. J. Virol. 83:4591-4604.
7. Chan, W. Y., Q. R. Liu, J. Borjigin, H. Busch, O. M. Rennert, L. A. Tease, and P. K. Chan. 1989. Characterization of the cDNA encoding human nucleophosmin and studies of its role in normal and abnormal growth. Biochemistry 28:1033-1039.
8. Cochrane, A. W., A. Perkins, and C. A. Rosen. 1990. Identification of sequences important in the nucleolar localization of human immunodeficiency virus Rev: relevance of nucleolar localization to function. J. Virol. 64:881-885.
9. Cousens, C., E. Minguijon, R. G. Dalziel, A. Ortin, M. Garcia, J. Park, L. Gonzalez, J. M. Sharp, and M. de las Heras. 1999. Complete sequence of enzootic nasal tumor virus, a retrovirus associated with transmissible intranasal tumors of sheep. J. Virol. 73:3986-3993.
10. Cullen, B. R. 2003. Nuclear mRNA export: insights from virology. Trends Biochem. Sci. 28:419-424.
11. Cullen, B. R., J. Hauber, K. Campbell, J. G. Sodroski, W. A. Haseltine, and C. A. Rosen. 1988. Subcellular localization of the human immunodeficiency virus trans-acting art gene product. J. Virol. 62:2498-2501.
12. D'Agostino, D. M., B. K. Felber, J. E. Harrison, and G. N. Pavlakis. 1992. The Rev protein of human immunodeficiency virus type 1 promotes polysomal association and translation of gag/pol and vpu/env mRNAs. Mol. Cell. Biol. 12:1375-1386.
13. Dirks, C., F. M. Duh, S. K. Rai, M. I. Lerman, and A. D. Miller. 2002. Mechanism of cell entry and transformation by enzootic nasal tumor virus. J. Virol. 76:2141-2149. (Pubitemid 34150681)
14. Dultz, E., M. Hildenbeutel, B. Martoglio, J. Hochman, B. Dobberstein, and K. Kapp. 2008. The signal peptide of the mouse mammary tumor virus Rem protein is released from the endoplasmic reticulum membrane and accumulates in nucleoli. J. Biol. Chem. 283:9966-9976.
15. Felber, B. K., M. Hadzopoulou-Cladaras, C. Cladaras, T. Copeland, and G. N. Pavlakis. 1989. rev protein of human immunodeficiency virus type 1 affects the stability and transport of the viral mRNA. Proc. Natl. Acad. Sci. USA 86:1495-1499.
16. Geiselhart, V., P. Bastone, T. Kempf, M. Schnolzer, and M. Lochelt. 2004. Furin-mediated cleavage of the feline foamy virus Env leader protein. J. Virol. 78:13573-13581. (Pubitemid 39612757)
17. Gruter, P., C. Tabernero, C. von Kobbe, C. Schmitt, C. Saavedra, A. Bachi, M. Wilm, B. K. Felber, and E. Izaurralde. 1998. TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol. Cell 1:649-659. (Pubitemid 128379243)
18. Guzik, B. W., L. Levesque, S. Prasad, Y. C. Bor, B. E. Black, B. M. Paschal, D. Rekosh, and M. L. Hammarskjold. 2001. NXT1 (p15) is a crucial cellular cofactor in TAP-dependent export of intron-containing RNA in mammalian cells. Mol. Cell. Biol. 21:2545-2554.
19. Hadzopoulou-Cladaras, M., B. K. Felber, C. Cladaras, A. Athanassopoulos, A. Tse, and G. N. Pavlakis. 1989. The rev (trs/art) protein of human immunodeficiency virus type 1 affects viral mRNA and protein expression via a cis-acting sequence in the env region. J. Virol. 63:1265-1274. (Pubitemid 19061368)
20. gag. J. Virol. 80: 3765-3772.
21. Hartman, T. R., S. Qian, C. Bolinger, S. Fernandez, D. R. Schoenberg, and K. Boris-Lawrie. 2006. RNA helicase A is necessary for translation of selected messenger RNAs. Nat. Struct. Mol. Biol. 13:509-516.
22. Henderson, B. R., and P. Percipalle. 1997. Interactions between HIV Rev and nuclear import and export factors: the Rev nuclear localisation signal mediates specific binding to human importin-beta. J. Mol. Biol. 274:693-707.
23. Hofacre, A., and H. Fan. 2004. Multiple domains of the Jaagsiekte sheep retrovirus envelope protein are required for transformation of rodent fibroblasts. J. Virol. 78:10479-10489. (Pubitemid 39258373)
24. Hope, T. J., X. J. Huang, D. McDonald, and T. G. Parslow. 1990. Steroidreceptor fusion of the human immunodeficiency virus type 1 Rev transactivator: mapping cryptic functions of the arginine-rich motif. Proc. Natl. Acad. Sci. USA 87:7787-7791.
25. Hull, S., and K. Boris-Lawrie. 2002. RU5 of Mason-Pfizer monkey virus 5′ long terminal repeat enhances cytoplasmic expression of human immunode- ficiency virus type 1 gag-pol and nonviral reporter RNA. J. Virol. 76:10211-10218.
26. Hull, S., and H. Fan. 2006. Mutational analysis of the cytoplasmic tail of Jaagsiekte sheep retrovirus envelope protein. J. Virol. 80:8069-8080. (Pubitemid 44182307)
27. Indik, S., W. H. Gunzburg, B. Salmons, and F. Rouault. 2005. A novel, mouse mammary tumor virus encoded protein with Rev-like properties. Virology 337:1-6. (Pubitemid 40725435)
28. Inoue, J., M. Yoshida, and M. Seiki. 1987. Transcriptional (p40x) and post-transcriptional (p27x-III) regulators are required for the expression and replication of human T-cell leukemia virus type I genes. Proc. Natl. Acad. Sci. USA 84:3653-3657.
29. Jin, L., B. W. Guzik, Y. C. Bor, D. Rekosh, and M. L. Hammarskjold. 2003. Tap and NXT promote translation of unspliced mRNA. Genes Dev. 17: 3075-3086. (Pubitemid 38040771)
30. Kimura, T., I. Hashimoto, M. Nishikawa, and J. I. Fujisawa. 1996. A role for Rev in the association of HIV-1 gag mRNA with cytoskeletal beta-actin and viral protein expression. Biochimie 78:1075-1080. (Pubitemid 27193129)
31. Kimura, T., I. Hashimoto, A. Yamamoto, M. Nishikawa, and J. I. Fujisawa. 2000. Rev-dependent association of the intron-containing HIV-1 gag mRNA with the nuclear actin bundles and the inhibition of its nucleocytoplasmic transport by latrunculin-B. Genes Cells 5:289-307. (Pubitemid 30253179)
32. Kohler, A., and E. Hurt. 2007. Exporting RNA from the nucleus to the cytoplasm. Nat. Rev. Mol. Cell Biol. 8:761-773.
33. Kusuhara, K., M. Anderson, S. M. Pettiford, and P. L. Green. 1999. Human T-cell leukemia virus type 2 Rex protein increases stability and promotes nuclear to cytoplasmic transport of gag/pol and env RNAs. J. Virol. 73:8112-8119. (Pubitemid 29441671)
34. Lawrence, J. B., A. W. Cochrane, C. V. Johnson, A. Perkins, and C. A. Rosen. 1991. The HIV-1 Rev protein: a model system for coupled RNA transport and translation. New Biol. 3:1220-1232.
35. LeBlanc, J. J., S. Uddowla, B. Abraham, S. Clatterbuck, and K. L. Beemon. 2007. Tap and Dbp5, but not Gag, are involved in DR-mediated nuclear export of unspliced Rous sarcoma virus RNA. Virology 363:376-386.
36. Lemberg, M. K., F. A. Bland, A. Weihofen, V. M. Braud, and B. Martoglio. 2001. Intramembrane proteolysis of signal peptides: an essential step in the generation of HLA-E epitopes. J. Immunol. 167:6441-6446.
37. Linder, P. 2004. Molecular biology. The life of RNA with proteins. Science 304:694-695.
38. Löwer, R., R. R. Tönjes, C. Korbmacher, R. Kurth, and J. Löwer. 1995. Identification of a Rev-related protein by analysis of spliced transcripts of the human endogenous retroviruses HTDV/HERV-K. J. Virol. 69:141-149. (Pubitemid 24378787)
39. Maeda, N., Y. Inoshima, D. A. Fruman, S. M. Brachmann, and H. Fan. 2003. Transformation of mouse fibroblasts by Jaagsiekte sheep retrovirus envelope does not require phosphatidylinositol 3-kinase. J. Virol. 77:9951-9959. (Pubitemid 37122076)
40. Maeda, N., M. Palmarini, C. Murgia, and H. Fan. 2001. Direct transformation of rodent fibroblasts by Jaagsiekte sheep retrovirus DNA. Proc. Natl. Acad. Sci. USA 98:4449-4454.
41. Malim, M. H., J. Hauber, S. Y. Le, J. V. Maizel, and B. R. Cullen. 1989. The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature 338:254-257.
42. Malim, M. H., L. S. Tiley, D. F. McCarn, J. R. Rusche, J. Hauber, and B. R. Cullen. 1990. HIV-1 structural gene expression requires binding of the Rev trans-activator to its RNA target sequence. Cell 60:675-683. (Pubitemid 20083823)
43. Martoglio, B. 2003. Intramembrane proteolysis and post-targeting functions of signal peptides. Biochem. Soc. Trans. 31:1243-1247.
44. McGee-Estrada, K., and H. Fan. 2007. Comparison of LTR enhancer elements in sheep beta retroviruses: insights into the basis for tissue-specific expression. Virus Genes 35:303-312. (Pubitemid 47087535)
45. Mertz, J. A., M. S. Simper, M. M. Lozano, S. M. Payne, and J. P. Dudley. 2005. Mouse mammary tumor virus encodes a self-regulatory RNA export protein and is a complex retrovirus. J. Virol. 79:14737-14747.
46. Neville, M., F. Stutz, L. Lee, L. I. Davis, and M. Rosbash. 1997. The importin- beta family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export. Curr. Biol. 7:767-775.
47. Nitta, T., A. Hofacre, S. Hull, and H. Fan. 2009. Identification and mutational analysis of a Rej response element in Jaagsiekte sheep retrovirus RNA. J. Virol. 83:12499-12511.
48. Paca, R. E., R. A. Ogert, C. S. Hibbert, E. Izaurralde, and K. L. Beemon. 2000. Rous sarcoma virus DR posttranscriptional elements use a novel RNA export pathway. J. Virol. 74:9507-9514.
49. Palmarini, M., N. Maeda, C. Murgia, C. De-Fraja, A. Hofacre, and H. Fan. 2001. A phosphatidylinositol 3-kinase docking site in the cytoplasmic tail of the Jaagsiekte sheep retrovirus transmembrane protein is essential for envelope-induced transformation of NIH 3T3 cells. J. Virol. 75:11002-11009. (Pubitemid 33031567)
50. Palmarini, M., C. Murgia, and H. Fan. 2002. Spliced and prematurely polyadenylated Jaagsiekte sheep retrovirus-specific RNAs from infected or transfected cells. Virology 294:180-188. (Pubitemid 34921300)
51. Palmarini, M., J. M. Sharp, M. de las Heras, and H. Fan. 1999. Jaagsiekte sheep retrovirus is necessary and sufficient to induce a contagious lung cancer in sheep. J. Virol. 73:6964-6972.
52. Palmarini, M., J. M. Sharp, C. Lee, and H. Fan. 1999. In vitro infection of ovine cell lines by Jaagsiekte sheep retrovirus. J. Virol. 73:10070-10078.
53. Peng, S. S., C. Y. Chen, N. Xu, and A. B. Shyu. 1998. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J. 17:3461-3470.
54. Perales, C., L. Carrasco, and M. E. Gonzalez. 2005. Regulation of HIV-1 env mRNA translation by Rev protein. Biochim. Biophys. Acta 1743:169-175.
55. Rosen, C. A., E. Terwilliger, A. Dayton, J. G. Sodroski, and W. A. Haseltine. 1988. Intragenic cis-acting art gene-responsive sequences of the human immunodeficiency virus. Proc. Natl. Acad. Sci. USA 85:2071-2075.
56. Sharp, J. M., and A. J. Herring. 1983. Sheep pulmonary adenomatosis: demonstration of a protein which cross-reacts with the major core proteins of Mason-Pfizer monkey virus and mouse mammary tumour virus. J. Gen. Virol. 64:2323-2327.
57. Siomi, H., H. Shida, S. H. Nam, T. Nosaka, M. Maki, and M. Hatanaka. 1988. Sequence requirements for nucleolar localization of human T cell leukemia virus type I pX protein, which regulates viral RNA processing. Cell 55:197-209. (Pubitemid 18256759)
58. Walter, P., and A. E. Johnson. 1994. Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu. Rev. Cell Biol. 10:87-119.
59. Wang, W., H. Furneaux, H. Cheng, M. C. Caldwell, D. Hutter, Y. Liu, N. Holbrook, and M. Gorospe. 2000. HuR regulates p21 mRNA stabilization by UV light. Mol. Cell. Biol. 20:760-769.
60. Weihofen, A., and B. Martoglio. 2003. Intramembrane-cleaving proteases: controlled liberation of proteins and bioactive peptides. Trends Cell Biol. 13:71-78. (Pubitemid 36135888)
61. York, D. F., R. Vigne, D. W. Verwoerd, and G. Querat. 1992. Nucleotide sequence of the Jaagsiekte retrovirus, an exogenous and endogenous type D and B retrovirus of sheep and goats. J. Virol. 66:4930-4939.
62. Zapp, M. L., and M. R. Green. 1989. Sequence-specific RNA binding by the HIV-1 Rev protein. Nature 342:714-716. (Pubitemid 20001594)