Retroviral splicing suppressor sequesters a 3′ splice site in a 50S aberrant splicing complex

Molecular and Cellular Biology

Volumn 25, Issue 11, 2005, Pages 4397-4405

  Giles, Keith E ^a,b   Beemon, Karen L ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN NPRP8; SMALL NUCLEAR RIBONUCLEOPROTEIN; SMALL NUCLEAR RNA; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CROSS LINKING; EXON; GROUP SPECIFIC ANTIGEN GENE; IN VITRO STUDY; INTRON; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RETROVIRUS; RNA SPLICING; SEDIMENTATION RATE; SPLICEOSOME; VIRUS GENE; VIRUS REPLICATION; WILD TYPE;

CARRIER PROTEINS; GENES, GAG; GENES, SUPPRESSOR; HUMANS; POINT MUTATION; RETROVIRIDAE; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA SPLICE SITES; RNA SPLICING; RNA, MESSENGER; RNA, VIRAL; SPLICEOSOMES; SUPPRESSION, GENETIC; TRANSCRIPTION, GENETIC; VIRUS REPLICATION;

AVES;

EID: 18944380865     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.11.4397-4405.2005     Document Type: Article

References (50)

1. Amendt, B. A., S. B. Simpson, and C. M. Stoltzfus. 1995. Inhibition of RNA splicing at the Rous sarcoma virus src 3′ splice site is mediated by an interaction between a negative cis element and a chicken embryo fibroblast nuclear factor. J. Virol. 69:5068-5076.
2. Arrigo, S., and K. Beemon. 1988. Regulation of Rous sarcoma virus RNA splicing and stability. Mol. Cell. Biol. 8:4858-4867.
3. Ast, G., and A. M. Weiner. 1997. A novel U1/U5 interaction indicates proximity between U1 and U5 snRNAs during an early step of mRNA splicing. RNA 3:371-381.
4. Burge, C. B., T. Tuschl, and P. A. Sharp. 1999. Splicing of precursors to mRNAs by the spliceosome. In R. F. Gesteland, T. R. Cech, and J. F. Atkins (ed.). The RNA world. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
5. Cabello-Villegas, J., K. E. Giles, A. M. Soto, P. Yu, A. Mougin, K. L. Beemon, and Y. X. Wang. 2004. Solution structure of the pseudo-5′ splice site of a retroviral splicing suppressor. RNA 10:1388-1398.
6. Caputi, M., A. Mayeda, A. R. Krainer, and A. M. Zahler. 1999. hnRNP A/B proteins are required for inhibition of HIV-1 pre-mRNA splicing. EMBO J. 18:4060-4067.
7. Coffin, J. M. 1996. Retroviridae: the viruses and their replication, p. 1767-1848. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, Pa.
8. Cook, C. R., and M. T. McNally. 1999. Interaction between the negative regulator of splicing element and a 3′ splice site: requirement for U1 small nuclear ribonucleoprotein and the 3′ splice site branch point/pyrimidine tract. J. Virol. 73:2394-2400.
9. Das, R., and R. Reed. 1999. Resolution of the mammalian E complex and the ATP-dependent spliceosomal complexes on native agarose mini-gels. RNA 5:1504-1508.
10. 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.
11. Du, H., and M. Rosbash. 2002. The U1 snRNP protein U1C recognizes the 5′ splice site in the absence of base pairing. Nature 419:86-90.
12. Fogel, B. L., and M. T. McNally. 2000. A cellular protein, hnRNP H, binds to the negative regulator of splicing element from Rous sarcoma virus. J. Biol. Chem. 275:32371-32378.
13. Frendewey, D., and W. Keller. 1985. Stepwise assembly of a pre-mRNA splicing complex requires U-snRNPs and specific intron sequences. Cell 42:355-367.
14. 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.
15. Gontarek, R. R. 1994. A Rous sarcoma virus intronic element negatively regulates splicing by binding snRNPs. Ph.D. thesis. The Johns Hopkins University, Baltimore, MD.
16. Gontarek, R. R., M. T. McNally, and K. Beemon. 1993. Mutation of an RSV intronic element abolishes both U11/U12 snRNP binding and negative regulation of splicing. Genes Dev. 7:1926-1936.
17. Grabowski, P. J., S. R. Seiler, and P. A. Sharp. 1985. A multicomponent complex is involved in the splicing of messenger RNA precursors. Cell 42:345-353.
18. Grabowski, P. J., and P. A. Sharp. 1986. Affinity chromatography of splicing complexes: U2, U5, and U4 + U6 small nuclear ribonucleoprotein particles in the spliceosome. Science 233:1294-1299.
19. Hibbert, C. S., R. R. Gontarek, and K. L. Beemon. 1999. The role of overlapping U1 and U11 5′ splice site sequences in a negative regulator of splicing. RNA 5:333-343.
20. Huang, Y., and Z. R. Liu. 2002. The ATPase, RNA unwinding, and RNA binding activities of recombinant p68 RNA helicase. J. Biol. Chem. 277:12810-12815.
21. Jurica, M. S., and M. J. Moore. 2002. Capturing splicing complexes to study structure and mechanism. Methods 28:336-345.
22. 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.
23. Libri, D., F. Duconge, L. Levy, and M. Vinauger. 2002. A role for the Psi-U mismatch in the recognition of the 5′ splice site of yeast introns by the U1 small nuclear ribonucleoprotein particle. J. Biol. Chem. 277:18173-18181.
24. Liu, Z. R. 2002. p68 RNA helicase is an essential human splicing factor that acts at the U1 snRNA-5′ splice site duplex. Mol. Cell. Biol. 22:5443-5450.
25. Lund, M., and J. Kjems. 2002. Defining a 5′ splice site by functional selection in the presence and absence of U1 snRNA 5′ end. RNA 8:166-179.
26. Luo, H. R., G. A. Moreau, N. Levin, and M. J. Moore. 1999. The human Prp8 protein is a component of both U2- and U12-dependent spliceosomes. RNA 5:893-908.
27. Makarova, O. V., E. M. Makarov, H. Urlaub, C. L. Will, M. Gentzel, M. Wilm, and R. Luhrmann. 2004. A subset of human 35S U5 proteins, including Prp19, function prior to catalytic step 1 of splicing. EMBO J. 23:2381-2391.
28. Malca, H., N. Shomron, and G. Ast. 2003. The U1 snRNP base pairs with the 5′ splice site within a penta-snRNP complex. Mol. Cell. Biol. 23:3442-3455.
29. Maroney, P. A., C. M. Romfo, and T. W. Nilsen. 2000. Functional recognition of 5′ splice site by U4/U6.U5 tri-snRNP defines a novel ATP-dependent step in early spliceosome assembly. Mol. Cell 6:317-328.
30. Maroney, P. A., C. M. Romfo, and T. W. Nilsen. 2000. Nuclease protection of RNAs containing site-specific labels: a rapid method for mapping RNA-protein interactions. RNA 6:1905-1909.
31. McNally, L. M., and M. T. McNally. 1998. An RNA splicing enhancer-like sequence is a component of a splicing inhibitor element from Rous sarcoma virus. Mol. Cell. Biol. 18:3103-3111.
32. McNally, L. M., and M. T. McNally. 1996. SR protein splicing factors interact with the Rous sarcoma virus negative regulator of splicing element. J. Virol. 70:1163-1172.
33. McNally, L. M., and M. T. McNally. 1999. U1 small nuclear ribonucleoprotein and splicing inhibition by the Rous sarcoma virus negative regulator of splicing element. J. Virol. 73:2385-2393.
34. McNally, M. T., and K. Beemon. 1992. Intronic sequences and 3′ splice sites control Rous sarcoma virus RNA splicing. J. Virol. 66:6-11.
35. McNally, M. T., R. R. Gontarek, and K. Beemon. 1991. Characterization of Rous sarcoma virus intronic sequences that negatively regulate splicing. Virology 185:99-108.
36. Nilsen, T. W. 1994. RNA-RNA interactions in the spliceosome: unraveling the ties that bind. Cell 78:1-4.
37. O'Sullivan, C. T., T. S. Polony, R. E. Paca, and K. L. Beemon. 2002. Rous sarcoma virus negative regulator of splicing selectively suppresses src mRNA splicing and promotes polyadenylation. Virology 302:405-412.
38. Paca, R. E., C. S. Hibbert, C. T. O'Sullivan, and K. L. Beemon. 2001. Retroviral splicing suppressor requires three nonconsensus uridines in a 5′ splice site-like sequence. J. Virol. 75:7763-7768.
39. Rabson, A. B., and B. J. Graves. 1997. Synthesis and processing of viral RNA, p. 205-261. In J. M. Coffin, S. H. Hughes, and H. E. Varmus (ed.), Retroviruses, second ed. Cold Spring Harbor Laboratory Press, Woodbury, N.Y.
40. Reyes, J. L., P. Kois, B. B. Konforti, and M. M. Konarska. 1996. The canonical GU dinucleotide at the 5′ splice site is recognized by p220 of the U5 snRNP within the spliceosome. RNA 2:213-225.
41. Siebel, C. W., L. D. Fresco, and D. C. Rio. 1992. The mechanism of somatic inhibition of Drosophila P-element pre-mRNA splicing: multiprotein complexes at an exon pseudo-5′ splice site control U1 snRNP binding. Genes Dev. 6:1386-1401.
42. Sorek, R., R. Shamir, and G. Ast. 2004. How prevalent is functional alternative splicing in the human genome? Trends Genet. 20:68-71.
43. Staley, J. P., and C. Guthrie. 1998. Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 92:315-326.
44. Staley, J. P., and C. Guthrie. 1999. An RNA switch at the 5′ splice site requires ATP and the DEAD box protein Prp28p. Mol. Cell 3:55-64.
45. Stevens, S. W., D. E. Ryan, H. Y. Ge, R. E. Moore, M. K. Young, T. D. Lee, and J. Abelson. 2002. Composition and functional characterization of the yeast spliceosomal penta-snRNP. Mol. Cell 9:31-44.
46. Tarn, W. Y., and J. A. Steitz. 1996. A novel spliceosome containing U11, U12, and U5 snRNPs excises a minor class (AT-AC) intron in vitro. Cell 84:801-811.
47. Thanaraj, T. A., S. Stamm, F. Clark, J. J. Riethoven, V. Le Texier, and J. Muilu. 2004. ASD: the Alternative Splicing Database. Nucleic Acids Res. 32(Database issue):D64-D69.
48. Turner, I. A., C. M. Norman, M. J. Churcher, and A. J. Newman. 2004. Roles of the U5 snRNP in spliceosome dynamics and catalysis. Biochem. Soc. Trans. 32:928-931.
49. Wu, S., and M. R. Green. 1997. Identification of a human protein that recognizes the 3′ splice site during the second step of pre-mRNA splicing. EMBO J. 16:4421-4432.
50. Wyatt, J. R., E. J. Sontheimer, and J. A. Steitz. 1992. Site-specific cross-linking of mammalian U5 snRNP to the 5′ splice site before the first step of pre-mRNA splicing. Genes Dev. 6:2542-2553.