Tap and NXT promote translation of unspliced mRNA

Genes and Development

Volumn 17, Issue 24, 2003, Pages 3075-3086

  Jin, Li ^a,b   Guzik, Brian W ^a   Bor, Yeou Cherng ^a   Rekosh, David ^a   Hammarskjöld, Marie Louise ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

mRNA export; Tap NXT; Translational regulation; Unspliced mRNA

Indexed keywords

PROTEIN; PROTEIN P15; TAP PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; INTRON; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS REGULATION; RIBOSOMAL FRAMESHIFTING; RNA SPLICING; TRANSLATION REGULATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ATP-BINDING CASSETTE TRANSPORTERS; CARRIER PROTEINS; CELL LINE; CELL NUCLEUS; FUSION PROTEINS, GAG-POL; HIV CORE PROTEIN P24; HIV-1; HUMANS; MAJOR HISTOCOMPATIBILITY COMPLEX; MUTATION; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; REGULATORY SEQUENCES, NUCLEIC ACID; RETROVIRIDAE; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER;

MAMMALIA; MASON-PFIZER MONKEY VIRUS;

EID: 0347361538     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1155703     Document Type: Article

References (61)

1. Antic, D. and Keene, J.D. 1998. Messenger ribonucleoprotein complexes containing human ELAV proteins: Interactions with cytoskeleton and translational apparatus. J. Cell Sci. 111 (Pt 2): 183-197.
2. Antic, D., Lu, N., and Keene, J.D. 1999. ELAV tumor antigen, Hel-N1, increases translation of neurofilament M mRNA and induces formation of neurites in human teratocarcinoma cells. Genes & Dev. 13: 449-461.
3. Bachi, A., Braun, I.C., Rodrigues, J.P., Pante, N., Ribbeck, K., von Kobbe, C., Kutay, U., Wilm, M., Gorlich, D., Carmo-Fonseca, M., et al. 2000. The C-terminal domain of TAP interacts with the nuclear pore complex and promotes export of specific CTE-bearing RNA substrates. RNA 6: 136-158.
4. Bear, J., Tan, W., Zolotukhin, A.S., Tabernero, C., Hudson, E.A., and Felber, B.K. 1999. Identification of novel import and export signals of human TAP, the protein that binds to the constitutive transport element of the type D retrovirus mRNAs. Mol. Cell. Biol. 19: 6306-6317.
5. Berkowitz, R., Fisher, J., and Goff, S.P. 1996. RNA packaging. In Morphogenesis and maturation of retroviruses (ed. H.-G. Krausslich), pp. 177-218. Springer, Berlin.
6. Black, B.E., Levesque, L., Holaska, J.M., Wood, T.C., and Paschal, B.M. 1999. Identification of an NTF2-related factor that binds Ran-GTP and regulates nuclear protein export. Mol. Cell. Biol. 19: 8616-8624.
7. Braun, I.C., Rohrbach, E., Schmitt, C., and 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.
8. Braun, I.C., Herold, A., Rode, M., Conti, E., and Izaurralde, E. 2001. Overexpression of TAP/p15 heterodimers bypasses nuclear retention and stimulates nuclear mRNA export. J. Biol. Chem. 276: 20536-20543.
9. Bray, M., Prasad, S., Dubay, J.W., Hunter, E., Jeang, K.T., Rekosh, D., and Hammarskjöld, M.L. 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. 91: 1256-1260.
10. Brennan, C.M., Gallouzi, I.E., and Steitz, J.A. 2000. Protein ligands to HuR modulate its interaction with target mRNAs in vivo. J. Cell Biol. 151: 1-14.
11. Calzone, F.J., Angerer, R.C., and Gorovsky, M.A. 1982. Regulation of protein synthesis in Tetrahymena: Isolation and characterization of polysomes by gel filtration and precipitation at pH 5.3. Nucleic Acids Res. 10: 2145-2161.
12. Chang, D.D. and Sharp, P.A. 1989. Regulation by HIV Rev depends upon recognition of splice sites. Cell 59: 789-795.
13. Coyle, J.H., Guzik, B.W., Bor, Y.C., Jin, L., Eisner-Smerage, L., Taylor, S.J., Rekosh, D., and Hammarskjöld, M.L. 2003. Sam68 enhances the cytoplasmic utilization of intron-containing RNA and is functionally regulated by the nuclear kinase Sik/BRK. Mol. Cell. Biol. 23: 92-103.
14. Cullen, B.R. and Malim, M.H. 1992. Secreted placental alkaline phosphatase as a eukaryotic reporter gene. Methods Enzymol. 216: 362-368.
15. Dostie, J. and Dreyfuss, G. 2002. Translation is required to remove Y14 from mRNAs in the cytoplasm. Curr. Biol. 12: 1060-1067.
16. Ernst, R.K., Bray, M., Rekosh, D., and Hammarskjöld, M.-L. 1997a. A structured retroviral RNA element that mediates nucleocytoplasmic export of intron-containing RNA. Mol. Cell. Biol. 17: 135-144.
17. -. 1997b. Secondary structure and mutational analysis of the Mason-Pfizer monkey virus RNA constitutive transport element. RNA 3: 210-222.
18. Fan, X.C. and Steitz, J.A. 1998. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17:3448-3460.
19. Fornerod, M., Ohno, M., Yoshida, M., and Mattaj, I.W. 1997. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90: 1051-1060.
20. Fribourg, S., Braun, I.C., Izaurralde, E., and Conti, E. 2001. Structural basis for the recognition of a nucleoporin FG repeat by the NTF2-like domain of the TAP/p15 mRNA nuclear export factor. Mol. Cell 8: 645-656.
21. Frints, S.G., Jun, L., Fryns, J.P., Devriendt, K., Teulingkx, R., Berghe, L.V., Vos, B.D., Borghgraef, M., Chelly, J., Portes, V.D., et al. 2003. Inv(X)(p21.1;q22.1) in a man with mental retardation, short stature, general muscle wasting, and facial dysmorphism: Clinical study and mutation analysis of the NXF5 Gene. Am. J. Med. Genet. 119A: 367-374.
22. Graham, F.L. and van der Eb, A.J. 1973. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 52:456-467.
23. Gruter, P., Tabernero, C., von, K.C., Schmitt, C., Saavedra, C., Bachi, A., Wilm, M., Felber, B.K., and Izaurralde, E. 1998. TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol. Cell 1: 649-659.
24. Guzik, B.W., Levesque, L., Prasad, S., Bor, Y.C., Black, B.E., Paschal, B.M., Rekosh, D., and Hammarskjöld, M.L. 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.
25. Hadzopoulou-Cladaras, M., Felber, B.K., Cladaras, C., Athanassopoulos, A., Tse, A., and Pavlakis, G.N. 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. Hammarskjöld, M.L. 1997. Regulation of retroviral RNA export. Semin. Cell Dev. Biol. 8: 83-90.
27. -. 2001. Constitutive transport element-mediated nuclear export. Curr. Top. Microbiol. Immunol. 259:77-93.
28. Hammarskjöld, M.L., Wang, S.-C., and Klein, G. 1986. High-level expression of the Epstein-Barr virus EBNA1 protein in CV1 cells and human lymphoid cells using a SV40 late replacement vector. Gene 43: 41-50.
29. Hammarskjöld, M.L., Heimer, J., Hammarskjöld, B., Sangwan, I., Albert, L., and Rekosh, D. 1989. Regulation of human immunodeficiency virus env expression by the rev gene product. J. Virol. 63: 1959-1966.
30. Hammarskjöld, M.L., Li, H., Rekosh, D., and Prasad, S. 1994. Human immunodeficiency virus env expression becomes Rev-independent if the env region is not defined as an intron. J. Virol. 68:951-958.
31. Herold, A., Suyama, M., Rodrigues, J.P., Braun, I.C., Kutay, U., Carmo-Fonseca, M., Bork, P., and Izaurralde, E. 2000. TAP (NXF1) belongs to a multigene family of putative RNA export factors with a conserved modular architecture. Mol. Cell. Biol. 20: 8996-9008.
32. Horton, R.M. 1995. PCR-mediated recombination and mutagenesis. SOEing together tailor-made genes. Mol. Biotechnol. 3: 93-99.
33. Horton, R.M., Cai, Z.L., Ho, S.N., and Pease, L.R. 1990. Gene splicing by overlap extension: Tailor-made genes using the polymerase chain reaction. Biotechniques 8: 528-535.
34. Johannes, G. and Sarnow, P. 1998. Cap-independent polysomal association of natural mRNAs encoding c-myc, BiP, and eIF4G conferred by internal ribosome entry sites. RNA 4: 1500-1513.
35. Jun, L., Frints, S., Duhamel, H., Herold, A., Abad-Rodrigues, J., Dotti, C., Izaurralde, E., Marynen, P., and Froyen, G. 2001. NXF5, a novel member of the nuclear RNA export factor family, is lost in a male patient with a syndromic form of mental retardation. Curr. Biol. 11: 1381-1391.
36. Kang, Y. and Cullen, B.R. 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.
37. Katahira, J., Strasser, K., Podtelejnikov, A., Mann, M., Jung, J.U., and Hurt, E. 1999. The Mex67p-mediated nuclear mRNA export pathway is conserved from yeast to human. EMBO J. 18: 2593-2609.
38. Keene, J.D. and Tenenbaum, S.A. 2002. Eukaryotic mRNPs may represent posttranscriptional operons. Mol. Cell 9: 1161-1167.
39. Kim, V.N., Yong, J., Kataoka, N., Abel, L., Diem, M.D., and Dreyfuss, G. 2001. The Y14 protein communicates to the cytoplasm the position of exon-exon junctions. EMBO J. 20:2062-2068.
40. Le Hir, H., Gatfield, D., Izaurralde, E., and Moore, M.J. 2001. The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO J. 20: 4987-4997.
41. Le Hir, H., Nott, A., and Moore, MJ. 2003. How introns influence and enhance eukaryotic gene expression. Trends Biochem. Sci. 28: 215-220.
42. Legrain, P. and Rosbash, M. 1989. Some cis- and trans-acting mutants for splicing target pre-mRNA to the cytoplasm. Cell 57: 573-583.
43. Levesque, L., Guzik, B., Guan, T., Coyle, J., Black, B.E., Rekosh, D., Hammarskjöld, M.L., and Paschal, B.M. 2001. RNA export mediated by Tap involves NXT1-dependent interactions with the nuclear pore complex. J. Biol. Chem. 276: 44953-44962.
44. Lu, S. and Cullen, B.R. 2003. Analysis of the stimulatory effect of splicing on mRNA production and utilization in mammalian cells. RNA 9: 618-630.
45. Malim, M.H., Hauber, J., Le, S.V., Maizel, J.V., and Cullen, B.R. 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.
46. Maquat, L.E. and Carmichael, G.G. 2001. Quality control of mRNA function. Cell 104: 173-176.
47. Neville, M., Stutz, E., Lee, L., Davis, L.I., and Rosbash, M. 1997. The importin-β family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export. Curr. Biol. 7: 767-775.
48. Nott, A., Meislin, S.H., and Moore, M.J. 2003. A quantitative analysis of intron effects on mammalian gene expression. RNA 9: 607-617.
49. Otero, G.C., Harris, M.E., Donello, J.E., and Hope, T.J. 1998. Leptomycin B inhibits equine infectious anemia virus Rev and feline immunodeficiency virus rev function but not the function of the hepatitis B virus posttranscriptional regulatory element. J. Virol. 72: 7593-7597.
50. Pasquinelli, A.E., Ernst, R.K., Lund, E., Grimm, C., Zapp, M.L., Rekosh, D., Hammarskjöld, M.L., and Dahlberg, J.E. 1997. The constitutive transport element (CTE) of Mason-Pfizer monkey virus (MPMV) accesses a cellular mRNA export pathway. EMBO J. 16: 7500-7510.
51. Pear, W.S., Nolan, G.P., Scott, M.L., and Baltimore, D. 1993. Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. 90: 8392-8396.
52. Pollard, V.W. and Malim, M.H. 1998. The HIV-1 Rev protein. Annu. Rev. Microbiol. 52: 491-532.
53. Saavedra, C., Felber, B., and Izaurralde, E. 1997. The simian retrovirus-1 constitutive transport element, unlike the HIV-1 RRE, uses factors required for cellular mRNA export. Curr. Biol. 7: 619-628.
54. + RNA and nuclear pores. EMBO J. 16: 3256-3271.
55. Smith, A.J., Cho, M.I., Hammarskjöld, M.L., and Rekosh, D. 1990. Human immunodeficiency virus type 1 Pr55gag and Pr160gag-pol expressed from a simian virus 40 late replacement vector are efficiently processed and assembled into viruslike particles. J. Virol. 64: 2743-2750.
56. Smith, A.J., Srinivasakumar, N., Hammarskjöld, M.L., and Rekosh, D. 1993. Requirements for incorporation of Pr160gag-pol from human immunodeficiency virus type 1 into viruslike particles. J. Virol. 67: 2266-2275.
57. Srinivasakumar, N., Chazal, N., Helga, M.C., Prasad, S., Hammarskjöld, M.L., and Rekosh, D. 1997. The effect of viral regulatory protein expression on gene delivery by human immunodeficiency virus type 1 vectors produced in stable packaging cell lines. J. Virol. 71: 5841-5848.
58. Wehrly, K. and Chesebro, B. 1997. p24 antigen capture assay for quantification of human immunodeficiency virus using readily available inexpensive reagents. Methods 12: 288-293.
59. Wiegand, H.L., Coburn, G.A., Zeng, Y., Kang, Y., Bogerd, H.P., and Cullen, B.R. 2002. Formation of Tap/NXT1 heterodimers activates Tap-dependent nuclear mRNA export by enhancing recruitment to nuclear pore complexes. Mol. Cell. Biol. 22: 245-256.
60. Yoon, D.W., Lee, H., Seol, W., DeMaria, M., Rosenzweig, M., and Jung, J.U. 1997. Tap: A novel cellular protein that interacts with Tip of herpesvirus saimiri and induces lymphocyte aggregation. Immunity 6: 571-82.
61. Zolotukhin, A.S., Valentin, A., Pavlakis, G.N., and Felber, B.K. 1994. Continuous propagation of RRE- and Rev-RRE- human immunodeficiency virus type 1 molecular clones containing a cis-acting element of simian retrovirus type 1 in human peripheral blood lymphocytes. J. Virol. 68: 7944-7952.