The Exon Splicing Silencer in Human Immunodeficiency Virus Type 1 Tat Exon 3 Is Bipartite and Acts Early in Spliceosome Assembly

REFERENCES

• Adams, M. D., R. S. Tarng, and D. C. Rio 1997. The alternative splicing factor PSI regulates P-element third intron splicing in vivo. Genes Dev. 11: 129–138.
   PubMedGoogle Scholar
• Amendt, B. A., D. Hesslein, L.-J. Chang, and C. M. Stoltzfus 1994. Presence of negative and positive cis-acting RNA splicing elements within and flanking the first tat coding exon of human immunodeficiency virus type 1. Mol. Cell. Biol. 14: 3960–3970.
   PubMedGoogle Scholar
• Amendt, B. A., Z.-H. Si, and C. M. Stoltzfus 1995. Presence of exon splicing silencers within human immunodeficiency virus type 1 tat exon 2 and tat-rev exon 3: evidence for inhibition mediated by cellular factors. Mol. Cell. Biol. 15: 4606–4615.
   PubMedGoogle Scholar
• Arrigo, S., and K. Beemon 1988. Regulation of Rous sarcoma virus RNA splicing and stability. Mol. Cell. Biol. 8: 4858–4867.
   PubMedGoogle Scholar
• Bennett, M., M. S. Michaud, J. Kingston, and R. Reed 1992. Protein components specifically associated with pre-spliceosome and spliceosome complexes. Genes Dev. 6: 1986–2000.
   PubMedGoogle Scholar
• Bennett, M., S. Piñol-Roma, D. Staknis, G. Dreyfuss, and R. Reed 1992. Differential binding of heterogeneous nuclear ribonucleoproteins to mRNA precursors prior to spliceosome assembly in vitro. Mol. Cell. Biol. 12: 3165–3175.
   PubMedGoogle Scholar
• Bouck, J., X.-D. Fu, A. M. Skalka, and R. A. Katz 1996. Genetic selection for balanced retroviral splicing: novel regulation involving the second step can be mediated by transitions in the polypyrimidine tract. Mol. Cell. Biol. 15: 2663–2671.
   Google Scholar
• Caputi, M., G. Casari, S. Guenzi, R. Tagliabue, A. Sidoli, C. A. Melo, and F. E. Baralle 1994. A novel bipartite splicing enhancer modulates the differential processing of the human fibronectin EDA exon. Nucleic Acids Res. 22: 1018–1022.
   PubMedGoogle Scholar
• Champion-Arnaud, P., O. Gozani, L. Palandjian, and R. Reed 1995. Accumulation of a novel spliceosomal complex on pre-mRNAs containing branch site mutations. Mol. Cell. Biol. 15: 5750–5756.
   PubMedGoogle Scholar
• Chiara, M. D., O. Gozani, M. Bennett, P. Champion-Arnaud, L. Palandjian, and R. Reed 1996. Identification of proteins that interact with exon sequences, splice sites, and the branchpoint sequence during each stage of spliceosome assembly. Mol. Cell. Biol. 16: 3317–3326.
   PubMedGoogle Scholar
• Coffin, J. M. 1990. Retroviridae and their replication Fields virology. In: Fields, B. N., and D. M. Knipe1437–1500Raven Press, New York, N.Y.
   Google Scholar
• Cullen, B. R. 1991. Regulation of human immunodeficiency virus replication. Annu. Rev. Microbiol. 45: 219–250.
   PubMed Web of Science ®Google Scholar
• Damier, L., L. Domenjoud, and C. Branlant 1997. The D1-A2 and D2-A2 pairs of splice sites from HIV-1 are highly efficient in vitro, in spite of an unusual branch site. Biochem. Biophys. Res. Commun. 237: 182–187.
   PubMedGoogle Scholar
• Del Gatto, F., and R. Breathnach 1995. Exon and intron sequences, respectively, repress and activate splicing of a fibroblast growth factor receptor 2 alternative exon. Mol. Cell. Biol. 15: 4825–4834.
   PubMedGoogle Scholar
• Del Gatto, F., M.-C. Gesnel, and R. Breathnach 1996. The exon sequence TAGG can inhibit splicing. Nucleic Acids Res. 24: 2017–2021.
   PubMedGoogle Scholar
• Dignam, J. D., R. M. Lebovitz, and R. G. Roeder 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11: 1475–1489.
   PubMed Web of Science ®Google Scholar
• Dyhr-Mikkelsen, H., and J. Kjems 1995. Inefficient spliceosome assembly and abnormal branch site selection in splicing of an HIV-1 transcript in vitro. J. Biol. Chem. 270: 24060–24066.
   PubMedGoogle Scholar
• Felber, B. K., C. M. Drysdale, and G. N. Pavlakis 1990. Feedback regulation of human immunodeficiency virus type 1 expression by the Rev protein. J. Virol. 64: 3734–3741.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• Fu, X.-D., R. A. Katz, A. M. Skalka, and T. Maniatis 1991. The role of branchpoint and 3′-exon sequences in the control of balanced splicing of avian retrovirus RNA. Genes Dev. 5: 211–220.
   PubMedGoogle Scholar
• Guatelli, J. C., T. R. Gingeras, and D. D. Richman 1990. Alternative splice acceptor utilization during human immunodeficiency virus type 1 infection of cultured cells. J. Virol. 64: 4093–4098.
   PubMedGoogle Scholar
• Katz, R. A., and A. M. Skalka 1990. Control of retroviral RNA splicing through maintenance of suboptimal processing signals. Mol. Cell. Biol. 10: 696–704.
   PubMedGoogle Scholar
• Konarska, M. M. 1989. Analysis of splicing complexes and small ribonucleoprotein particles by native gel electrophoresis. Methods Enzymol. 180: 442–453.
   PubMedGoogle Scholar
• Konarska, M. M., and P. A. Sharp 1986. Electrophoretic separation of complexes involved in the splicing of precursors to mRNA. Cell 46: 845–855.
   PubMed Web of Science ®Google Scholar
• Krainer, A. R., T. Maniatis, B. Ruskin, and M. R. Green 1984. Normal and mutant human beta-globin pre-mRNAs are faithfully and efficiently spliced in vitro. Cell 36: 993–1005.
   PubMedGoogle Scholar
• Kramer, A. 1996. The structure and function of proteins involved in mammalian pre-mRNA splicing. Annu. Rev. Biochem. 65: 367–409.
   PubMed Web of Science ®Google Scholar
• Liaw, G. 1994. Improved protocol for directional multimerization of a DNA fragment. BioTechniques 17: 668–670.
   PubMedGoogle Scholar
• Luciw, P. A. 1996. Human immunodeficiency viruses and their replication Fields virology. In: Fields, B. N., D. M. Knipe, and P. M. Howley1881–1952Lippincott-Raven Publishers, Philadephia, Pa.
   Google Scholar
• Michaud, S., and R. Reed 1991. An ATP-independent complex commits pre-mRNA to the mammalian spliceosome assembly pathway. Genes Dev. 5: 2534–2546.
   PubMedGoogle Scholar
• Michaud, S., and R. Reed 1993. A functional association between the 5′ and 3′ splice site is established in the earliest prespliceosome (E) complex in mammals. Genes Dev. 7: 1008–10020.
   PubMed Web of Science ®Google Scholar
• Moore, M. J., C. C. Query, and P. A. Sharp 1993. Splicing of precursors to mRNAs by the spliceosome The RNA world. In: Gesteland, R. F., and J. R. Atkins303–357Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Muesing, M. A., D. H. Smith, C. D. Cabradilla, C. V. Benton, L. A. Lasky, and D. J. Capon 1985. Nucleic acid structure and expression of the human AIDS/lymphadenopathy retrovirus. Nature 313: 450–458.
   PubMed Web of Science ®Google Scholar
• O’Reilly, M. M., M. T. McNally, and K. L. Beemon 1995. Two strong 5′ splice sites and competing suboptimal 3′ splice sites involved in alternative splicing of human immunodeficiency virus type 1 RNA. Virology 213: 373–385.
   PubMedGoogle Scholar
• Purcell, D. F. J., and M. A. Martin 1993. Alternative splicing of human immunodeficiency virus type 1 mRNA modulates viral protein expression, replication, and infectivity. J. Virol. 67: 6365–6378.
   PubMed Web of Science ®Google Scholar
• Robert-Guroff, M., M. Popovic, S. Gartner, P. Markham, R. C. Gallo, and M. S. Reitz 1990. Structure and expression of tat-, rev-, and nef-specific transcripts of human immunodeficiency virus type 1 in infected lymphocytes and macrophages. J. Virol. 64: 3391–3398.
   PubMedGoogle Scholar
• Sambrook, J., E. F. Fritsch, and T. Maniatis 1989. Molecular cloning: a laboratory manual2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
   Google Scholar
• Schwartz, S., B. Felber, and G. N. Pavlakis 1991. Expression of human immunodeficiency virus type 1 vif and vpr mRNAs is rev-dependent and regulated by splicing. Virology 183: 677–686.
   PubMedGoogle Scholar
• Schwartz, S., B. K. Felber, D. M. Benko, E.-M. Fenyö, and G. N. Pavlakis 1990. Cloning and functional analysis of multiply spliced mRNA species of human immunodeficiency virus type 1. J. Virol. 64: 2519–2529.
   PubMed Web of Science ®Google Scholar
• Si, Z., B. A. Amendt, and C. M. Stoltzfus 1997. Splicing efficiency of HIV-1 tat RNA is determined by both a suboptimal 3′ splice site and a 10 nucleotide exon splicing silencer element located within tat exon 2. Nucleic Acids Res. 25: 861–867.
   PubMedGoogle Scholar
• Siebel, C. W., A. Admon, and D. C. Rio 1995. Soma-specific expression and cloning of PSI, a negative regulator of P element pre-mRNA splicing. Genes Dev. 9: 269–283.
   PubMedGoogle Scholar
• Siebel, C. W., R. Kanaar, and D. C. Rio 1994. Regulation of tissue-specific P-element pre-mRNA splicing requires the RNA-binding protein PSI. Genes Dev. 8: 1713–1725.
   PubMedGoogle Scholar
• Staffa, A., and A. Cochrane 1995. Identification of positive and negative splicing regulatory elements within the terminal tat-rev exon of human immunodeficiency virus type 1. Mol. Cell. Biol. 15: 4597–4605.
   PubMedGoogle Scholar
• Staffa, A., and A. Cochrane 1994. The tat/rev intron of human immunodeficiency virus type 1 is inefficiently spliced because of suboptimal signals in the 3′ splice site. J. Virol. 68: 3071–3079.
   PubMedGoogle Scholar
• Staknis, D., and R. Reed 1994. Direct interactions between pre-mRNA and six U2 small nuclear ribonucleoproteins during spliceosome assembly. Mol. Cell. Biol. 14: 2994–3005.
   PubMedGoogle Scholar
• Stoltzfus, C. M. 1988. Synthesis and processing of avian sarcoma retrovirus RNA. Adv. Virus Res. 35: 1–37.
   PubMedGoogle Scholar
• Stoltzfus, C. M., and S. J. Fogarty 1989. Multiple regions in the Rous sarcoma virus src gene intron act in cis to affect the accumulation of unspliced RNA. J. Virol. 63: 1669–1676.
   PubMed Web of Science ®Google Scholar
• Touchman, J. W., I. D’Souza, C. A. Heckman, R. Zhou, N. W. Biggart, Murphy E. C., Jr. 1995. Branchpoint and polypyrimidine tract mutations mediating the loss and partial recovery of the Moloney murine sarcoma virus MuSVts110 thermosensitive splicing phenotype. J. Virol. 69: 7724–7733.
   PubMedGoogle Scholar
• Valcarcel, J., R. Singh, P. D. Zamore, and M. R. Green 1993. The protein Sex-lethal antagonizes the splicing factor U2AF to regulate alternative splicing of transformer pre-mRNA. Nature 362: 171–175.
   PubMed Web of Science ®Google Scholar
• Vilardell, J., and J. R. Warner 1994. Regulation of splicing at an intermediate step in the formation of the spliceosome. Genes Dev. 8: 211–220.
   PubMed Web of Science ®Google Scholar
• Vogt, P. K. 1997. Historical introduction to the general properties of retroviruses Retroviruses. In: Coffin, J. M., S. H. Hughes, and H. E. Varmus1–26Cold Spring Harbor Laboratory Press, Plainview, N.Y.
   Google Scholar
• Wentz, M. P., B. E. Moore, M. W. Cloyd, S. M. Berget, and L. A. Donehower 1997. A naturally arising mutation of a potential silencer of exon splicing in human immunodeficiency virus type 1 induces dominant aberrant splicing and arrests virus production. J. Virol. 71: 8542–8551.
   PubMedGoogle Scholar
• Zhang, L., and C. M. Stoltzfus 1995. A suboptimal src 3′ splice site is necessary for efficient replication of Rous sarcoma virus. Virology 206: 1099–1107.
   PubMedGoogle Scholar