Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1999 Mar 15;18(6):1642–1652. doi: 10.1093/emboj/18.6.1642

Intronless mRNA transport elements may affect multiple steps of pre-mRNA processing.

Y Huang 1, K M Wimler 1, G G Carmichael 1
PMCID: PMC1171251  PMID: 10075934

Abstract

We have reported recently that a small element within the mouse histone H2a-coding region permits efficient cytoplasmic accumulation of intronless beta-globin cDNA transcripts. This sequence lowers the levels of spliced products from intron-containing constructs and can functionally replace Rev and the Rev-responsive element (RRE) in the nuclear export of unspliced HIV-1-related mRNAs. In work reported here, we further investigate the molecular mechanisms by which this element might work. We demonstrate here through both in vivo and in vitro assays that, in addition to promoting mRNA nuclear export, this element acts as a polyadenylation enhancer and as a potent inhibitor of splicing. Surprisingly, two other described intronless mRNA transport elements (from the herpes simplex virus thymidine kinase gene and hepatitis B virus) appear to function in a similar manner. These findings prompt us to suggest that a general feature of intronless mRNA transport elements might be a collection of phenotypes, including the inhibition of splicing and the enhancement of both polyadenylation and mRNA export.

Full Text

The Full Text of this article is available as a PDF (439.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bogerd H. P., Fridell R. A., Madore S., Cullen B. R. Identification of a novel cellular cofactor for the Rev/Rex class of retroviral regulatory proteins. Cell. 1995 Aug 11;82(3):485–494. doi: 10.1016/0092-8674(95)90437-9. [DOI] [PubMed] [Google Scholar]
  2. Bray M., Prasad S., Dubay J. W., Hunter E., Jeang K. T., Rekosh D., Hammarskjöld M. L. 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 Feb 15;91(4):1256–1260. doi: 10.1073/pnas.91.4.1256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Buchman A. R., Berg P. Comparison of intron-dependent and intron-independent gene expression. Mol Cell Biol. 1988 Oct;8(10):4395–4405. doi: 10.1128/mcb.8.10.4395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cahill K. B., Carmichael G. G. Deletion analysis of the polyomavirus late promoter: evidence for both positive and negative elements in the absence of early proteins. J Virol. 1989 Sep;63(9):3634–3642. doi: 10.1128/jvi.63.9.3634-3642.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Callis J., Fromm M., Walbot V. Introns increase gene expression in cultured maize cells. Genes Dev. 1987 Dec;1(10):1183–1200. doi: 10.1101/gad.1.10.1183. [DOI] [PubMed] [Google Scholar]
  6. Challoner P. B., Moss S. B., Groudine M. Expression of replication-dependent histone genes in avian spermatids involves an alternate pathway of mRNA 3'-end formation. Mol Cell Biol. 1989 Mar;9(3):902–913. doi: 10.1128/mcb.9.3.902. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chang D. D., Sharp P. A. Regulation by HIV Rev depends upon recognition of splice sites. Cell. 1989 Dec 1;59(5):789–795. doi: 10.1016/0092-8674(89)90602-8. [DOI] [PubMed] [Google Scholar]
  8. Cheng G. H., Nandi A., Clerk S., Skoultchi A. I. Different 3'-end processing produces two independently regulated mRNAs from a single H1 histone gene. Proc Natl Acad Sci U S A. 1989 Sep;86(18):7002–7006. doi: 10.1073/pnas.86.18.7002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chung S., Perry R. P. Importance of introns for expression of mouse ribosomal protein gene rpL32. Mol Cell Biol. 1989 May;9(5):2075–2082. doi: 10.1128/mcb.9.5.2075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cochrane A. W., Jones K. S., Beidas S., Dillon P. J., Skalka A. M., Rosen C. A. Identification and characterization of intragenic sequences which repress human immunodeficiency virus structural gene expression. J Virol. 1991 Oct;65(10):5305–5313. doi: 10.1128/jvi.65.10.5305-5313.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Collis P., Antoniou M., Grosveld F. Definition of the minimal requirements within the human beta-globin gene and the dominant control region for high level expression. EMBO J. 1990 Jan;9(1):233–240. doi: 10.1002/j.1460-2075.1990.tb08100.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cullen B. R. Mechanism of action of regulatory proteins encoded by complex retroviruses. Microbiol Rev. 1992 Sep;56(3):375–394. doi: 10.1128/mr.56.3.375-394.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Deng T. L., Li Y., Johnson L. F. Thymidylate synthase gene expression is stimulated by some (but not all) introns. Nucleic Acids Res. 1989 Jan 25;17(2):645–658. doi: 10.1093/nar/17.2.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dignam J. D., Lebovitz R. M., Roeder R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. doi: 10.1093/nar/11.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Donello J. E., Beeche A. A., Smith G. J., 3rd, Lucero G. R., Hope T. J. The hepatitis B virus posttranscriptional regulatory element is composed of two subelements. J Virol. 1996 Jul;70(7):4345–4351. doi: 10.1128/jvi.70.7.4345-4351.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Eckner R., Ellmeier W., Birnstiel M. L. Mature mRNA 3' end formation stimulates RNA export from the nucleus. EMBO J. 1991 Nov;10(11):3513–3522. doi: 10.1002/j.1460-2075.1991.tb04915.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Felber B. K., Hadzopoulou-Cladaras M., Cladaras C., Copeland T., Pavlakis G. N. rev protein of human immunodeficiency virus type 1 affects the stability and transport of the viral mRNA. Proc Natl Acad Sci U S A. 1989 Mar;86(5):1495–1499. doi: 10.1073/pnas.86.5.1495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fischer U., Huber J., Boelens W. C., Mattaj I. W., Lührmann R. The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell. 1995 Aug 11;82(3):475–483. doi: 10.1016/0092-8674(95)90436-0. [DOI] [PubMed] [Google Scholar]
  19. Fornerod M., Ohno M., Yoshida M., Mattaj I. W. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell. 1997 Sep 19;90(6):1051–1060. doi: 10.1016/s0092-8674(00)80371-2. [DOI] [PubMed] [Google Scholar]
  20. Fornerod M., van Deursen J., van Baal S., Reynolds A., Davis D., Murti K. G., Fransen J., Grosveld G. The human homologue of yeast CRM1 is in a dynamic subcomplex with CAN/Nup214 and a novel nuclear pore component Nup88. EMBO J. 1997 Feb 17;16(4):807–816. doi: 10.1093/emboj/16.4.807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Fritz C. C., Zapp M. L., Green M. R. A human nucleoporin-like protein that specifically interacts with HIV Rev. Nature. 1995 Aug 10;376(6540):530–533. doi: 10.1038/376530a0. [DOI] [PubMed] [Google Scholar]
  22. Gasser C. S., Simonsen C. C., Schilling J. W., Schimke R. T. Expression of abbreviated mouse dihydrofolate reductase genes in cultured hamster cells. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6522–6526. doi: 10.1073/pnas.79.21.6522. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Gruss P., Lai C. J., Dhar R., Khoury G. Splicing as a requirement for biogenesis of functional 16S mRNA of simian virus 40. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4317–4321. doi: 10.1073/pnas.76.9.4317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Grüter P., Tabernero C., von Kobbe C., Schmitt C., Saavedra C., Bachi A., Wilm M., Felber B. K., Izaurralde E. TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol Cell. 1998 Apr;1(5):649–659. doi: 10.1016/s1097-2765(00)80065-9. [DOI] [PubMed] [Google Scholar]
  25. Görlich D., Dabrowski M., Bischoff F. R., Kutay U., Bork P., Hartmann E., Prehn S., Izaurralde E. A novel class of RanGTP binding proteins. J Cell Biol. 1997 Jul 14;138(1):65–80. doi: 10.1083/jcb.138.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hadzopoulou-Cladaras M., Felber B. K., Cladaras C., Athanassopoulos A., Tse A., Pavlakis G. N. 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. 1989 Mar;63(3):1265–1274. doi: 10.1128/jvi.63.3.1265-1274.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hamer D. H., Leder P. Splicing and the formation of stable RNA. Cell. 1979 Dec;18(4):1299–1302. doi: 10.1016/0092-8674(79)90240-x. [DOI] [PubMed] [Google Scholar]
  28. Harris M. E., Böhni R., Schneiderman M. H., Ramamurthy L., Schümperli D., Marzluff W. F. Regulation of histone mRNA in the unperturbed cell cycle: evidence suggesting control at two posttranscriptional steps. Mol Cell Biol. 1991 May;11(5):2416–2424. doi: 10.1128/mcb.11.5.2416. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hattori K., Angel P., Le Beau M. M., Karin M. Structure and chromosomal localization of the functional intronless human JUN protooncogene. Proc Natl Acad Sci U S A. 1988 Dec;85(23):9148–9152. doi: 10.1073/pnas.85.23.9148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hentschel C. C., Birnstiel M. L. The organization and expression of histone gene families. Cell. 1981 Aug;25(2):301–313. doi: 10.1016/0092-8674(81)90048-9. [DOI] [PubMed] [Google Scholar]
  31. Hope T. J., McDonald D., Huang X. J., Low J., Parslow T. G. Mutational analysis of the human immunodeficiency virus type 1 Rev transactivator: essential residues near the amino terminus. J Virol. 1990 Nov;64(11):5360–5366. doi: 10.1128/jvi.64.11.5360-5366.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Huang J., Liang T. J. A novel hepatitis B virus (HBV) genetic element with Rev response element-like properties that is essential for expression of HBV gene products. Mol Cell Biol. 1993 Dec;13(12):7476–7486. doi: 10.1128/mcb.13.12.7476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Huang M. T., Gorman C. M. Intervening sequences increase efficiency of RNA 3' processing and accumulation of cytoplasmic RNA. Nucleic Acids Res. 1990 Feb 25;18(4):937–947. doi: 10.1093/nar/18.4.937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Huang Y., Carmichael G. G. A suboptimal 5' splice site is a cis-acting determinant of nuclear export of polyomavirus late mRNAs. Mol Cell Biol. 1996 Nov;16(11):6046–6054. doi: 10.1128/mcb.16.11.6046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Huang Y., Carmichael G. G. Role of polyadenylation in nucleocytoplasmic transport of mRNA. Mol Cell Biol. 1996 Apr;16(4):1534–1542. doi: 10.1128/mcb.16.4.1534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Huang Y., Carmichael G. G. 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 Sep 16;94(19):10104–10109. doi: 10.1073/pnas.94.19.10104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Huang Z. M., Yen T. S. Role of the hepatitis B virus posttranscriptional regulatory element in export of intronless transcripts. Mol Cell Biol. 1995 Jul;15(7):3864–3869. doi: 10.1128/mcb.15.7.3864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Jonsson J. J., Foresman M. D., Wilson N., McIvor R. S. Intron requirement for expression of the human purine nucleoside phosphorylase gene. Nucleic Acids Res. 1992 Jun 25;20(12):3191–3198. doi: 10.1093/nar/20.12.3191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Kalland K. H., Szilvay A. M., Brokstad K. A., Saetrevik W., Haukenes G. The human immunodeficiency virus type 1 Rev protein shuttles between the cytoplasm and nuclear compartments. Mol Cell Biol. 1994 Nov;14(11):7436–7444. doi: 10.1128/mcb.14.11.7436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Kedes L. H. Histone genes and histone messengers. Annu Rev Biochem. 1979;48:837–870. doi: 10.1146/annurev.bi.48.070179.004201. [DOI] [PubMed] [Google Scholar]
  41. Kirsh A. L., Groudine M., Challoner P. B. Polyadenylation and U7 snRNP-mediated cleavage: alternative modes of RNA 3' processing in two avian histone H1 genes. Genes Dev. 1989 Dec;3(12B):2172–2179. doi: 10.1101/gad.3.12b.2172. [DOI] [PubMed] [Google Scholar]
  42. Kobilka B. K., Frielle T., Collins S., Yang-Feng T., Kobilka T. S., Francke U., Lefkowitz R. J., Caron M. G. An intronless gene encoding a potential member of the family of receptors coupled to guanine nucleotide regulatory proteins. Nature. 1987 Sep 3;329(6134):75–79. doi: 10.1038/329075a0. [DOI] [PubMed] [Google Scholar]
  43. Legrain P., Rosbash M. Some cis- and trans-acting mutants for splicing target pre-mRNA to the cytoplasm. Cell. 1989 May 19;57(4):573–583. doi: 10.1016/0092-8674(89)90127-x. [DOI] [PubMed] [Google Scholar]
  44. Levine B. J., Chodchoy N., Marzluff W. F., Skoultchi A. I. Coupling of replication type histone mRNA levels to DNA synthesis requires the stem-loop sequence at the 3' end of the mRNA. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6189–6193. doi: 10.1073/pnas.84.17.6189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Liu X., Mertz J. E. HnRNP L binds a cis-acting RNA sequence element that enables intron-dependent gene expression. Genes Dev. 1995 Jul 15;9(14):1766–1780. doi: 10.1101/gad.9.14.1766. [DOI] [PubMed] [Google Scholar]
  46. Liu X., Mertz J. E. Polyadenylation site selection cannot occur in vivo after excision of the 3'-terminal intron. Nucleic Acids Res. 1993 Nov 11;21(22):5256–5263. doi: 10.1093/nar/21.22.5256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Liu X., Mertz J. E. Sequence of the polypyrimidine tract of the 3'-terminal 3' splicing signal can affect intron-dependent pre-mRNA processing in vivo. Nucleic Acids Res. 1996 May 1;24(9):1765–1773. doi: 10.1093/nar/24.9.1765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Lu X. B., Heimer J., Rekosh D., Hammarskjöld M. L. U1 small nuclear RNA plays a direct role in the formation of a rev-regulated human immunodeficiency virus env mRNA that remains unspliced. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7598–7602. doi: 10.1073/pnas.87.19.7598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Lutz C. S., Alwine J. C. Direct interaction of the U1 snRNP-A protein with the upstream efficiency element of the SV40 late polyadenylation signal. Genes Dev. 1994 Mar 1;8(5):576–586. doi: 10.1101/gad.8.5.576. [DOI] [PubMed] [Google Scholar]
  50. Malim M. H., Cullen B. R. Rev and the fate of pre-mRNA in the nucleus: implications for the regulation of RNA processing in eukaryotes. Mol Cell Biol. 1993 Oct;13(10):6180–6189. doi: 10.1128/mcb.13.10.6180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Mannironi C., Bonner W. M., Hatch C. L. H2A.X. a histone isoprotein with a conserved C-terminal sequence, is encoded by a novel mRNA with both DNA replication type and polyA 3' processing signals. Nucleic Acids Res. 1989 Nov 25;17(22):9113–9126. doi: 10.1093/nar/17.22.9113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Marzluff W. F. Histone 3' ends: essential and regulatory functions. Gene Expr. 1992;2(2):93–97. [PMC free article] [PubMed] [Google Scholar]
  53. Meyer B. E., Malim M. H. The HIV-1 Rev trans-activator shuttles between the nucleus and the cytoplasm. Genes Dev. 1994 Jul 1;8(13):1538–1547. doi: 10.1101/gad.8.13.1538. [DOI] [PubMed] [Google Scholar]
  54. Mikaélian I., Krieg M., Gait M. J., Karn J. Interactions of INS (CRS) elements and the splicing machinery regulate the production of Rev-responsive mRNAs. J Mol Biol. 1996 Mar 29;257(2):246–264. doi: 10.1006/jmbi.1996.0160. [DOI] [PubMed] [Google Scholar]
  55. Moss S. B., Ferry R. A., Groudine M. An alternative pathway of histone mRNA 3' end formation in mouse round spermatids. Nucleic Acids Res. 1994 Aug 11;22(15):3160–3166. doi: 10.1093/nar/22.15.3160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Nagata S., Mantei N., Weissmann C. The structure of one of the eight or more distinct chromosomal genes for human interferon-alpha. Nature. 1980 Oct 2;287(5781):401–408. doi: 10.1038/287401a0. [DOI] [PubMed] [Google Scholar]
  57. Nasioulas G., Zolotukhin A. S., Tabernero C., Solomin L., Cunningham C. P., Pavlakis G. N., Felber B. K. Elements distinct from human immunodeficiency virus type 1 splice sites are responsible for the Rev dependence of env mRNA. J Virol. 1994 May;68(5):2986–2993. doi: 10.1128/jvi.68.5.2986-2993.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Nesic D., Cheng J., Maquat L. E. Sequences within the last intron function in RNA 3'-end formation in cultured cells. Mol Cell Biol. 1993 Jun;13(6):3359–3369. doi: 10.1128/mcb.13.6.3359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Neuberger M. S., Williams G. T. The intron requirement for immunoglobulin gene expression is dependent upon the promoter. Nucleic Acids Res. 1988 Jul 25;16(14B):6713–6724. doi: 10.1093/nar/16.14.6713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Nishi K., Yoshida M., Fujiwara D., Nishikawa M., Horinouchi S., Beppu T. Leptomycin B targets a regulatory cascade of crm1, a fission yeast nuclear protein, involved in control of higher order chromosome structure and gene expression. J Biol Chem. 1994 Mar 4;269(9):6320–6324. [PubMed] [Google Scholar]
  61. Niwa M., MacDonald C. C., Berget S. M. Are vertebrate exons scanned during splice-site selection? Nature. 1992 Nov 19;360(6401):277–280. doi: 10.1038/360277a0. [DOI] [PubMed] [Google Scholar]
  62. Niwa M., Rose S. D., Berget S. M. In vitro polyadenylation is stimulated by the presence of an upstream intron. Genes Dev. 1990 Sep;4(9):1552–1559. doi: 10.1101/gad.4.9.1552. [DOI] [PubMed] [Google Scholar]
  63. Ogert R. A., Lee L. H., Beemon K. L. Avian retroviral RNA element promotes unspliced RNA accumulation in the cytoplasm. J Virol. 1996 Jun;70(6):3834–3843. doi: 10.1128/jvi.70.6.3834-3843.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Pandey N. B., Chodchoy N., Liu T. J., Marzluff W. F. Introns in histone genes alter the distribution of 3' ends. Nucleic Acids Res. 1990 Jun 11;18(11):3161–3170. doi: 10.1093/nar/18.11.3161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Pasquinelli A. E., Ernst R. K., Lund E., Grimm C., Zapp M. L., Rekosh D., Hammarskjöld M. L., Dahlberg J. E. The constitutive transport element (CTE) of Mason-Pfizer monkey virus (MPMV) accesses a cellular mRNA export pathway. EMBO J. 1997 Dec 15;16(24):7500–7510. doi: 10.1093/emboj/16.24.7500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Peterlin B. M., Luciw P. A., Barr P. J., Walker M. D. Elevated levels of mRNA can account for the trans-activation of human immunodeficiency virus. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9734–9738. doi: 10.1073/pnas.83.24.9734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Rosen C. A., Terwilliger E., Dayton A., Sodroski J. G., Haseltine W. A. Intragenic cis-acting art gene-responsive sequences of the human immunodeficiency virus. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2071–2075. doi: 10.1073/pnas.85.7.2071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Ryu W. S., Mertz J. E. Simian virus 40 late transcripts lacking excisable intervening sequences are defective in both stability in the nucleus and transport to the cytoplasm. J Virol. 1989 Oct;63(10):4386–4394. doi: 10.1128/jvi.63.10.4386-4394.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Schwartz S., Felber B. K., Pavlakis G. N. Distinct RNA sequences in the gag region of human immunodeficiency virus type 1 decrease RNA stability and inhibit expression in the absence of Rev protein. J Virol. 1992 Jan;66(1):150–159. doi: 10.1128/jvi.66.1.150-159.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Sittman D. B., Graves R. A., Marzluff W. F. Histone mRNA concentrations are regulated at the level of transcription and mRNA degradation. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1849–1853. doi: 10.1073/pnas.80.7.1849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Stutz F., Neville M., Rosbash M. Identification of a novel nuclear pore-associated protein as a functional target of the HIV-1 Rev protein in yeast. Cell. 1995 Aug 11;82(3):495–506. doi: 10.1016/0092-8674(95)90438-7. [DOI] [PubMed] [Google Scholar]
  72. Stutz F., Rosbash M. A functional interaction between Rev and yeast pre-mRNA is related to splicing complex formation. EMBO J. 1994 Sep 1;13(17):4096–4104. doi: 10.1002/j.1460-2075.1994.tb06727.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Tang H., Gaietta G. M., Fischer W. H., Ellisman M. H., Wong-Staal F. A cellular cofactor for the constitutive transport element of type D retrovirus. Science. 1997 May 30;276(5317):1412–1415. doi: 10.1126/science.276.5317.1412. [DOI] [PubMed] [Google Scholar]
  74. Wassarman K. M., Steitz J. A. Association with terminal exons in pre-mRNAs: a new role for the U1 snRNP? Genes Dev. 1993 Apr;7(4):647–659. doi: 10.1101/gad.7.4.647. [DOI] [PubMed] [Google Scholar]
  75. Wilusz J., Shenk T. A 64 kd nuclear protein binds to RNA segments that include the AAUAAA polyadenylation motif. Cell. 1988 Jan 29;52(2):221–228. doi: 10.1016/0092-8674(88)90510-7. [DOI] [PubMed] [Google Scholar]
  76. Wolff B., Sanglier J. J., Wang Y. Leptomycin B is an inhibitor of nuclear export: inhibition of nucleo-cytoplasmic translocation of the human immunodeficiency virus type 1 (HIV-1) Rev protein and Rev-dependent mRNA. Chem Biol. 1997 Feb;4(2):139–147. doi: 10.1016/s1074-5521(97)90257-x. [DOI] [PubMed] [Google Scholar]
  77. Zapp M. L., Hope T. J., Parslow T. G., Green M. R. Oligomerization and RNA binding domains of the type 1 human immunodeficiency virus Rev protein: a dual function for an arginine-rich binding motif. Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7734–7738. doi: 10.1073/pnas.88.17.7734. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES