Mta has properties of an RNA export protein and increases cytoplasmic accumulation of Epstein-Barr virus replication gene mRNA

Journal of Virology

Volumn 72, Issue 12, 1998, Pages 9526-9534

  Semmens, O John ^a,b   Chen, Lin ^a   Sarisky, Robert T ^a   Gao, Zhigang ^a   Zhong, Ling ^a   Hayward, S Diane ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE TRANSFERASE; HYBRID PROTEIN; LEUCINE; MESSENGER RNA; REGULATOR PROTEIN; SIGNAL PEPTIDE; VIRUS RNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; EPSTEIN BARR VIRUS; HELA CELL; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; RNA PROCESSING; VERO CELL; VIRUS GENE; VIRUS REPLICATION;

EID: 0031743482     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.12.9526-9534.1998     Document Type: Article

References (95)

1. Ahmed, Y. F., S. M. Hanly, M. H. Malim, B. R. Cullen, and W. C. Greene. 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.
2. Askovic, S., and R. Baumann. 1997. Activation domain requirements for disruption of Epstein-Barr virus latency by ZEBRA. J Virol. 71:6547-6554.
3. Ausubel, F. M., R. Brent, R. E. Kingston, D. M. David, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1994. Current protocols in molecular biology, vol. 1. John Wiley & Sons, Ins., New York, N.Y.
4. Baer, R., A. T. Bankier, M. D. Biggin, P. L. Deininger, P. J. Farrell, T. J. Gibson, G. Hatfull, G. S. Hudson, S. C. Satchwell, C. Seguin, P. S. Tuffnell, and B. G. Barrell. 1984. Organization of the B95-8 Epstein-Barr virus genome. Nature 310:207-211.
5. Bogerd, A. M., R. A. Fridell, R. E. Benson, J. Hua, and B. R. Cullen. 1996. Protein sequence requirements for function of the human T-cell leukemia virus type 1 Rex nuclear export signal delineated by a novel in vivo randomization-selection assay. Mol. Cell. Biol. 16:4207-4214.
6. 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.
7. Brown, C. R., M. S. Nakamura, J. D. Mosca, G. S. Hayward, S. E. Straus, and L. P. Perera. 1995. Herpes simplex virus trans-regulatory protein ICP27 stabilizes and binds to 3′ ends of labile mRNA. J. Virol. 69:7187-7195.
8. Buisson, M., E. Manet, M.-C. Trescol-Biemont, H. Gruffat, B. Durand, and A. Sergeant. 1989. The Epstein-Barr Virus (EBV) early protein EB2 is a posttranscriptional activator expressed under the control of EBV transcription factors EB1 and R. J. Virol. 63:5276-5284.
9. Chang, D. D., and P. A. Sharp. 1989. Regulation by HIV Rev depends upon recognition of splice sites. Cell 59:789-795.
10. Chen, C., and H. Okayama. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7:2745-2752.
11. Cho, M.-S., K.-T Jeang, and S. D. Hayward. 1985. Localization of the coding region for an Epstein-Barr virus early antigen and inducible expression of this 60-kilodalton nuclear protein in transfected fibroblasts cell lines. J. Virol. 56:852-859.
12. Cook, I. D., F. Shanahan, and P. J. Farrell. 1994. Epstein-Barr virus SM protein. Virology 205:217-227.
13. Defechereux, P., S. Debrus, L. Baudoux, B. Rentier, and J. Piette, 1997. Varicella-zoster virus open reading frame 4 encodes an immediate-early protein with posttranscriptional regulatory properties. J. Virol. 71:7073-7079.
14. Dobblestein, M., J. Roth, W. T. Kimberly, A. J. Levine, and T. Shenk. 1997. Nuclear export of the E1B 55-kDa and E4 34-kDa adenoviral oncoproteins mediated by a rev-like signal sequence. EMBO J. 16:4276-4284.
15. Ernst, R. K., M. Bray, D. Rekosh, and M.-L. Hammarskjold. 1997. A structured retroviral RNA element that mediates nucleocytoplasmic export of intron-containing RNA. Mol. Cell. Biol. 17:135-144.
16. Ernst, R. K., M. Bray, D. Rekosh, and M. L. Hammarskjold. 1997. Secondary structure and mutational analysis of the Mason-Pfizer monkey virus RNA constitutive transport element. RNA 3:210-222.
17. Fischer, U., J. Huber, W. C. Boelens, I. W. Mattaj, and R. Luhrmann. 1995. The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell 82:475-483.
18. Fischer, U., S. Meyer, M. Teufel, C. Heckel, R. Luhrmann, and G. Rautmann. 1994. Evidence that HIV-1 Rev directly promotes the nuclear export of unspliced RNA. EMBO J. 13:4105-4112.
19. Fixman, E. D., G. S. Hayward, and S. D. Hayward. 1995. Replication of Epstein-Barr virus oriLyt: lack of a dedicated virally encoded origin-binding protein and dependence on Zta in cotransfection assays. J. Virol. 69:2998-3006.
20. Fixman, E. D., G. S. Hayward, and S. D. Hayward. 1992. trans-acting requirements for replication of Epstein-Barr virus ori-Lyt. J. Virol. 66:5030-5039.
21. Flemington, E. K., A. E. Goldfeld, and S. H. Speck. 1991. Efficient transcription of the Epstein-Barr virus immediate-early BZLF1 and BRLF1 genes requires protein synthesis. J. Virol. 65:7073-7077.
22. Fornerod, M., M. Ohno, M. Yoshida, and I. W. Mattaj. 1997. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90:1051-1060.
23. Fu, X. D., and T. Maniatis. 1990. Factor required for mammalian spliceosome assembly is localized to discrete regions in the nucleus. Nature 343: 437-441.
24. Gao, Z., A. Krithivas, J. E. Finan, O. J. Semmes, S. Zhou, Y. Wang, and S. D. Hayward. 1998. The Epstein-Barr virus proteins lytic transactivator Zta interacts with the helicase-primase replication. J. Virol. 72:8559-8567.
25. Hadzopoulou-Cladaras, M. 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.
26. Hammarskjold, M.-L., J. Heimer, B. Hammarskjold, I. Sangwan, L. Albert, and D. Rekosh. 1989. Regulation of human immunodeficiency virus env expression by the rev gene product. J. Virol. 63:1959-1966.
27. Hardy, W. R., and R. M. Sandri-Goldin. 1994. Herpes simplex virus inhibits host cell splicing, and regulatory protein ICP27 is required for this effect. J. Virol. 68:7790-7799.
28. k. Science 265:92-95.
29. Hibbard, M. K., and R. M. Sandri-Goldin. 1995. Arginine-rich regions succeeding the nuclear localization region of the herpes simplex virus type 1 regulatory protein ICP27 are required for efficient nuclear localization and late gene expression. J. Virol. 69:4656-4667.
30. Hidaka, M., J. Inoue, M. Yoshida, and M. Seiki. 1998. Post-transcriptional regulator (rex) of HTLV-1 initiates expression of viral structural proteins but suppresses expression of regulatory proteins. EMBO J. 7:519-523.
31. Hope, T. J. 1997. Viral RNA export. Chem. Biol. 4:335-344.
32. Inchauspe, G., and J. M. Ostrove. 1989. Differential regulation by varicellazoster virus (VZV) and herpes simplex virus type-1 trans-activating genes. Virology 173:710-714.
33. Ingram A., A. Phelan, J. Dunlop, and J. B. Clements. 1996. Immediate early protein IE63 of herpes simplex virus type 1 binds RNA directly. J. Gen. Virol. 77:1847-1851.
34. Kalland, K. H., A. M. Szilvay, K. A. Brokstad, W. Saetrevik, and G. Haukenes. 1994. The human immunodeficiency virus type 1 Rev protein shuttles between the cytoplasm and nuclear compartments. Mol. Cell. Biol. 14:7436-7444.
35. Kalland, K. H., A. M. Szilvay, E. Langhohff, and G. Haukenes. 1994. Subcellular distribution of human immunodeficiency virus type 1 Rev and colocalization of Rev with RNA splicing factors in a speckled pattern in the nucleoplasm. J. Virol. 68:1475-1485.
36. Kenney, S., E. Holley-Guthrie, E. C. Mar, aod M. Smith. 1989. The Epstein-Barr virus BMLF1 promoter contains an enhancer element that is responsive to the BZLF1 and BRLF1 transactivators. J. Virol. 63:3878-3883.
37. Kenney, S., J. Kamine, E. Holley-Guthrie, E. C. Mar, J. C. Lin, D. Markovitz, and J. Pagano. 1989. The Epstein-Barr virus immediate-early gene product, BMLF1, acts in trans by posttranscriptional mechanism which is reporter gene dependent. J. Virol. 63:3870-3877.
38. Kim, F. J., A. A. Beeche, J. J. Hunter, D. J. Chin, and T. J. Hope. 1996. Characterization of the nuclear export signal of human T-cell lymphotropic virus type 1 Rex reveals that nuclear export is mediated by position-variable hydrophobic interactions. Mol. Cell. Biol. 16:5147-5155.
39. Kjems, J., M. Brown, D. D. Chang, and P. A. Sharp. 1991. Structural analysis of the interaction between the human immunodeficiency virus Rev protein and the Rev response element. Proc. Natl. Acad. Sci. USA 88:683-687.
40. Lieberman, P. M., P. O'Hare, G. S. Hayward, and S. D. Hayward. 1986. Promiscuous trans-activation of gene expression by an Epstein-Barr virus-encoded early nuclear protein. J. Virol. 60:140-148.
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. McCarthy, A. M., L. McMahan, and P. A. Schaffer. 1989. Herpes simplex virus type 1 ICP27 deletion mutants exhibit altered patterns of transcription and are DNA deficient. J. Virol. 63:18-27.
43. McGregor, F., A. Phelan, J. Dunlop, and J. B. Clements. 1996. Regulation of herpes simplex virus poly(A) site usage and the action of immediate-early protein IE63 in the early-late switch. J. Virol. 70:1931-1940.
44. McLauchlan, J., A. Phelan, C. Loney, R. M. Sandri-Goldin, and J. B. Clements. 1992. Herpes simplex virus IE63 acts at the posttranscriptional level to stimulate viral mRNA 3′ processing. J. Virol. 66:6939-6945.
45. McMahan, L., and P. A. Schaffer. 1990. The repressing and enhancing functions of the herpes simplex virus regulatory protein ICP27 map to C-terminal regions and are required to modulate viral gene expression very early in infection. J. Virol. 64:3471-3485.
46. Mears, W. E., and S. A. Rice. 1996. The RGG box motif of the herpes simplex virus ICP27 protein mediates an RNA-binding activity and determines in vivo methylation. J. Virol. 70:7445-7453.
47. Mellinghoff, I., M. Daibata, R. E. Humphreys, C. Mulder, K. Takada, and T. Sairenji. 1991. Early events in Epstein-Barr virus genome expression after activation: regulation by second messengers of B cell activation. Virology 185:922-928.
48. Meyer, B. E., and M. H. Malim. 1994. The HIV-1 Rev trans-activator shuttles between the nucleus and the cytoplasm. Genes Dev. 8:1538-1547.
49. Meyer, B. E., J. L. Meinkoth, and M. H. Malim. 1996. Nuclear transport of human immunodeficiency virus type 1, visna virus, and equine infectious anemia virus Rev proteins: identification of a family of transferable nuclear export signals. J. Virol. 70:2350-2359.
50. Moriuchi, H., M. Moriuchi, H. A. Smith, and J. I. Cohen. 1994. Varicellazoster virus open reading frame 4 protein is functionally distinct from and does not complement its herpes simplex virus type 1 homolog, ICP27. J. Virol. 68:1987-1992.
51. Murphy R., and S. R. Wente. 1996. An RNA-export mediator with an essential nuclear export signal. Nature 383:357-360.
52. Nicholas, J., K. R. Cameron, H. Coleman, C. Newman, and R. W. Honess. 1992. Analysis of nucleotide sequence of the rightmost 43 kbp of herpesvirus saimiri (HSV) L-DNA: general conservation of genetic organization between HVS and Epstein-Barr virus. Virology 188:296-310.
53. Nicholas, J., U. A. Gompels, M. A. Craxton, and R. W. Honess. 1988. Conservation of sequence and function between the product of the 52-kilodalton immediate-early gene of herpesvirus saimiri and the BMLF1-encoded transcriptional effector (EB2) of Epstein-Barr virus. J. Virol. 62: 3250-3257.
54. Oguro, M. O., N. Shimizu, Y. Ono, and K. Takada. 1987. Both the rightward and the leftward open reading frames within the BamHI M DNA fragment of Epstein-Barr virus act as trans-activators of gene expression. J. Virol. 61:3310-3313.
55. Ossareh-Nazari, B., F. Bachelerie, and C. Dargemont. 1997. Evidence for a role of CRM1 in signal-mediated nuclear protein export. Science 278:141-144.
56. Pasquinelli, A. E., M. A. Powers, E. Lund, D. Forbes, and J. E. Dahlberg. 1997. Inhibition of mRNA export in vertebrate cells by nuclear export signal conjugates. Proc. Natl. Acad. Sci. USA 94:14393-14399.
57. Perera, L. P., S. Kaushal, P. R. Kinchington, J. D. Mosca, G. S. Hayward, and S. E. Strauss. 1994. Varicella-zoster virus open reading frame 4 encodes a transcriptional activator that is functionally distinct from that of herpes simplex virus homology ICP27. J. Virol. 68:2468-2477.
58. Pfitzner, A. J., J. L. Strominger, and S. H. Speck. 1987. Characterization of a cDNA clone corresponding to a transcript from the Epstein-Barr virus BamHI M fragment: evidence for overlapping mRNAs. J. Virol. 61:2943-2946.
59. Phelan, A., M. Carmo-Fonseca, J. McLauchlaw, A. I. Lamond, and J. B. Clements. 1993. A herpes simplex virus type 1 immediate-early gene product, IE63, regulates small nuclear ribonucleoprotein distribution. Proc. Natl. Acad. Sci. USA 90:9056-9060.
60. Phelan, A., and J. B. Clements. 1997. Herpes simplex virus type 1 immediate early protein IE63 shuttles between nuclear compartments and the cytoplasm. J. Gen. Virol. 78:3327-3331.
61. Phelan, A., J. Dunlop, and J. B. Clements. 1996. Herpes simplex virus type 1 protein IE63 affects the nuclear export of virus intron-containing transcripts. J. Virol. 70:5255-5265.
62. Ren, D., L. F. Lee, and P. M. Coussens. 1994. Identification and characterization of Marek's disease virus genes homologus to ICP27 and glycoprotein K of herpes simplex virus-1. Virology 204:242-250.
63. Rice, S. A., and D. M. Knipe. 1990. Genetic evidence for two distinct transactivation functions of the herpes simplex virus alpha protein ICP27. J. Virol. 64:1704-1715.
64. Rice, S. A., and V. Lam. 1994. Amino acid substitution mutations in the herpes simplex virus ICP27 protein define an essential gene regulation function. J. Virol. 68:823-833.
65. Rice, S. A., V. Lam, and D. M. Knipe. 1993. The acidic amino-terminal region of herpes simplex virus type 1 alpha protein ICP27 is required for an essential lytic function. J. Virol. 67:1778-1787.
66. Russo, J. J., R. A. Bohenzky, M.-C. Chein, J. Chen, M. Yan, D. Maddalena, J. P. Parry, D. Peruzzi, I. S. Edelman, Y. Chang, and P. S. Moore. 1996. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc. Natl. Acad. Sci. USA 93:14862-14867.
67. Sample, J., G. Lancz, and M. Nonoyama. 1986. Mapping of genes in BamHI fragment M of Epstein-Barr virus DNA that may determine the fate of viral infection. J. Virol. 57:145-154.
68. Sandri-Goldin, R. M. 1998. ICP27 mediates HSV RNA export by shuttling through a leucine-rich nuclear export siganl and binding viral intronless RNAs through an RGG motif. Genes Dev. 12:868-879.
69. Sandri-Goldin, R. M., and M. K. Hibbard. 1996. The herpes simples virus type 1 regulatory protein ICP27 coimmunoprecipitates with anti-Sm anti-serum, and the C terminus appears to be required for this interaction. J. Virol. 70:108-118.
70. Sandri-Goldin, R. M., M. K. Hibbard, and M. A. Hardwicke. 1995. The C-Terminal repressor region of herpes simplex virus type 1 ICP27 is required for the redistribution of small nuclear ribonucleoprotein particles and splicing factor SC35; however, these alterations are not sufficient to inhibit host cell splicing. J. Virol. 69:6063-6076.
71. Sandri-Goldin, R. M., and G. E. Mendoza. 1992. A herpesvirus regulatory protein appears to act post-transcriptionally by affecting mRNA processing. Genes Dev. 6:848-863.
72. Sarisky, R. T., Z. Gao, P. M. Lieberman, E. D. Fixman, G. S. Hayward, and S. D. Hayward. 1996. A replication function associated with the activation domain of the Epstein-Barr virus Zta transactivator. J. Virol. 70:8340-8347.
73. Schepers, A., D. Pich, and W. Hammerschmidt. 1996. Activation of oriLyt, the lytic origin of DNA replication of Epstein-Barr virus, BZLF1. Virology 220:367-376.
74. Schepers, A., D. Pich, and W. Hammerschmidt. 1993. A transcription factor with homology to the AP-1 family links RNA transcription and DNA replication in the lytic cycle of Epstein-Barr virus. EMBO J. 12:3921-3929.
75. Schoborg, R. V., and J. E. Clements. 1996. Definition of the RRE binding and activation domains of the caprine arthritis encephalitis virus Rev protein. Virology 226:113-121.
76. Seedorf, M., and P. A. Silver. 1997. Importin/karyopherin protein family members required for mRNA export from the nucleus. Proc. Natl. Acad. Sci. USA 94:8590-8595.
77. Seiki, M., J. Inoue, M. Hidaka, and M. Yoshida. 1988. Two cis-acting elements responsible for posttranscriptional trans-regulation of gene expression of human T-cell leukemia virus type 1. Proc. Natl. Acad. Sci. USA 85:7124-7128.
78. Sinclair, A. J., M. Brimmel, F. Shanahan, and P. J. Farrell. 1991. Pathways of activation of the Epstein-Barr virus productive cycle. J. Virol. 65:2237-2244.
79. Singh, M., C. Fraefel, L. J. Bello, W. C. Lawrence, and M. Schwyzer. 1996. Identification and characterization of BICP27, an early protein of bovine herpesvirus 1 which may stimulate mRNA 3′ processing. J. Gen. Virol. 77:615-625.
80. Smith I. L., M. Hardwicke, and R. M. Sandri-Goldin. 1992. Evidence that the herpes simplex virus immediate early protein ICP27 acts post-transcriptionally during infection to regulate gene expression. Virology 186:74-86.
81. Smith, I. L., R. E. Sekulovich, M. A. Hardwicke, and R. M. Sandri-Goldin. 1991. Mutations in the activation region of herpes simplex virus regulatory protein ICP27 can be trans dominant. J. Virol. 65:3656-3666.
82. Smith, R. H., Y. Zhao, and D. J. O'Callaghan. 1993. The equine herpesvirus 1 (EHV-1) UL3 gene, an ICP27 homolog, is necessary for full activation of gene expression directed by an EHV-1 late promoter. J. Virol. 67:1105-1109.
83. Soliman, T. M., R. M. Sandri-Goldin, and S. J. Silverstein. 1997. Shuttling of the herpes simplex virus type 1 regulatory protein ICP27 between the nucleus and cytoplasm mediates the expression of late proteins. J. Virol. 71:9188-9197.
84. Stade, K., C. S. Ford, C. Guthrie, and K. Weis. 1997. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 90:1041-1050.
85. Takada, K., and Y. Ono. 1989. Synchronous and sequential activation of latently infected Epstein-Barr virus genomes. J. Virol. 63:445-449.
86. Ullman, K. S., M. A. Powers, and D. J. Forbes. 1997. Nuclear export receptors: from importin to exportin. Cell 90:967-970. (Comment.)
87. Uprichard, S. L., and D. M. Knipe. 1996. Herpes simplex ICP27 mutant viruses exhibit reduced expression of specific DNA replication genes. J. Virol. 70:1969-1980.
88. Wang, Y., J. E. Finan, J. M. Middeldorp, and S. D. Hayward. 1997. P32/TAP, a cellular protein that interacts with EBNA-1 of Epstein-Barr virus. Virology 236:18-29.
89. Wen, W., J. L. Meinkoth, R. Y. Tsien, and S. S. Taylor. 1995. Identification of a signal for rapid export of proteins from the nucleus. Cell 82:463-473.
90. Whitehouse, A., M. Cooper, and D. M. Meredith. 1998. The immediate-early gene product encoded by open reading frame 57 of herpesvirus saimiri modulates gene expression at a posttranscriptional level. J. Virol. 72:857-861.
91. Winkler, M., S. A. Rice, and T. Stamminger. 1994. UL69 of human cytomegalovirus, an open reading frame with homology to ICP27 of herpes simplex virus, encodes a transactivator of gene expression. J. Virol. 68:3943-3954.
92. Wong, K. M., and A. J. Levine. 1989. Characterization of proteins encoded by the Epstein-Barr virus transactivator gene BMLF1. Virology 168:101-111.
93. Zhao, Y., V. R. Holden, R. N. Harty, and D. J. O'Callaghan. 1992. Identification and transcriptional analyses of the UL3 and UL4 genes of equine herpesvirus 1, homologs of the ICP27 and glycoprotein K genes of herpes simplex virus. J. Virol. 66:5363-5372.
94. Zhao, Y., V. R. Holden, R. H. Smith, and D. J. O'Callaghan. 1995. Regulatory function of the equine herpesvirus 1 ICP27 gene product. J. Virol. 69:2786-2793.
95. Zhong, L., and G. S. Hayward. 1997. Assembly of complete, functionally active herpes simplex virus DNA replication compartments and recruitment of associated viral and cellular proteins in transient cotransfection assays. J. Virol. 3146:-3160.