Evidence for the presence of a small U5-like RNA in active trans-spliceosomes of Trypanosoma brucei

EMBO Journal

Volumn 15, Issue 15, 1996, Pages 4016-4029

  Dungan, Jan M ^a   Watkins, Kenneth P ^a   Agabian, Nina ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

SL RNA; SLA RNA; Trans splicing; Trypanosoma brucei; U5

Indexed keywords

GUANOSINE DERIVATIVE; PSORALEN; RNA; SMALL NUCLEAR RNA;

ARTICLE; CONTROLLED STUDY; CROSS LINKING; EXON; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN RNA BINDING; RNA ANALYSIS; RNA SEQUENCE; RNA SPLICING; SPLICEOSOME; TRYPANOSOMA BRUCEI;

EUKARYOTA; TRYPANOSOMA; TRYPANOSOMA BRUCEI;

EID: 0029762873     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00775.x     Document Type: Article

References (72)

1. Bach, M. and Lührmann, R. (1991) Protein-RNA interactions in 20S U5 snRNPs. Biochim. Biophys. Acta, 1088, 139-143.
2. Bangs, J.D., Crain, P.F., Hashizume, T., McCloskey, J.A. and Boothroyd, J.C. (1992) Mass spectrometry of mRNA cap 4 from trypanosomatids reveals two novel nucleosides. J. Biol. Chem., 267, 9805-9815.
3. Black, D.L. and Pinto, A.L. (1989) U5 small nuclear ribonucleoprotein: RNA structure analysis and ATP-dependent interaction with U4/U6. Mol. Cell. Biol., 9, 3350-3359.
4. Bonen, L. (1993) Trans-splicing of pre-mRNA in plants, animals and protists. FASEB J., 7, 40-46.
5. Bruzik, J.P., Van, D.K., Hirsh, D. and Steitz, J.A. (1988) Trans splicing involves a novel form of small nuclear ribonucleoprotein particles. Nature, 335, 559-562.
6. Cimino, G.D., Gamper, H.B., Isaacs, S.T. and Hearst, J.E. (1985) Psoralens as photoactive probes of nucleic acid structure and function: organic chemistry, photochemistry, and biochemistry. Annu. Rev. Biochem., 54, 1151-1193.
7. Cooper, M., Johnston, L.H. and Beggs, J.D. (1995) Identification and characterization of Uss1p (Sdb23p): a novel U6 snRNA-associated protein with significant similarity to core proteins of small nuclear ribonucleoproteins. EMBO J., 14, 2066-2075.
8. Cortes, J.J., Sontheimer, E.J., Seiwert, S.D. and Steitz, J.A. (1993) Mutations in the conserved loop of human U5 snRNA generate use of novel cryptic 5′ splice sites in vivo. EMBO J., 12, 5181-5189.
9. Crispino, J.D. and Sharp, P.A. (1995) A U6 snRNA:pre-mRNA interaction can be rate-limiting for U1-independent splicing. Genes Dev., 9, 2314-2323.
10. Crispino, J.D., Blencowe, B.J. and Sharp, P.A. (1994) Complementation by SR proteins of pre-mRNA splicing reactions depleted of U1 snRNP. Science, 265, 1866-1869.
11. Cross, M., Gunzl, A., Palfi, Z. and Bindereif, A. (1991) Analysis of small nuclear ribonucleoproteins (RNPs) in Trypanosoma brucei: structural organization and protein components of the spliced leader RNP. Mol. Cell. Biol., 11, 5516-5526.
12. Donis-Keller, H. (1980) Phy M: an RNase activity specific for U and A residues useful in RNA sequence analysis. Nucleic Acids Res., 8, 3133-3142.
13. Donis-Keller, H., Maxam, A.M. and Gilbert, W. (1977) Mapping adenines, guanines, and pyrimidines in RNA. Nucleic Acids Res., 4, 2527-2538.
14. England, T.E., Bruce, A.G. and Uhlenbeck, O.C. (1980) Specific labeling of 3′ termini of RNA with T4 RNA ligase. Methods Enzymol., 65, 65-74.
15. Fantoni, A., Dare, A.O. and Tschudi, C. (1994) RNA polymerase III-mediated transcription of the trypanosome U2 small nuclear RNA gene is controlled by both intragenic and extragenic regulatory elements. Mol. Cell. Biol., 14, 2021-2028.
16. Frank, D., Roiha, H. and Guthrie, C. (1994) Architecture of the U5 small nuclear RNA. Mol. Cell. Biol., 14, 2180-2190.
17. Garrett-Wheeler, E., Lockard, R.E. and Kumar, A. (1984) Mapping of psoralen crosslinked nucleotides in RNA. Nucleic Acids Res., 12, 3405-3423.
18. Greenberg, J.R. and Burn, V.E. (1988) Proteins associated with rabbit reticulocyte mRNA caps during translation as investigated by photocrosslinking. Nucleic Acids Res., 16, 3437-3454.
19. Gunzl, A., Cross, M. and Bindereif, A. (1992) Domain structure of U2 and U4/U6 small nuclear ribonucleoprotein particles from Trypanosoma brucei: identification of trans-spliceosomal specific RNA-protein interactions. Mol. Cell. Biol., 12, 468-479.
20. Hannon, G.J., Maroney, P.A. and Nilsen, T.W. (1991) U small nuclear ribonucleoprotein requirements for nematode cis- and trans-splicing in vitro. J. Biol. Chem., 266, 22792-22795.
21. Hausner, T.P., Giglio, L.M. and Weiner, A.M. (1990) Evidence for base-pairing between mammalian U2 and U6 small nuclear ribonucleoprotein particles. Genes Dev., 4, 2146-2156.
22. Hermann, H., Fabrizio, P., Raker, V.A., Foulaki, K., Hornig, H., Brahms, H. and Lührmann, R. (1995) snRNP Sm proteins share two evolutionarily conserved sequence motifs which are involved in Sm protein-protein interactions. EMBO J., 14, 2076-2088.
23. Hodges, P.E., Jackson, S.P., Brown, J.D. and Beggs, J.D. (1995) Extraordinary sequence conservation of the PRP8 splicing factor. Yeast, 11, 337-342.
24. Izaurralde, E. and Mattaj, I.W. (1992) Transport of RNA between nucleus and cytoplasm. Semin. Cell Biol., 3, 279-288.
25. Jarmolowski, A. and Mattaj, I.W. (1993) The determinants for Sm protein binding to Xenopus U1 and U5 snRNAs are complex and non-identical. EMBO J., 12, 223-232.
26. Konarska, M.M. (1989) Analysis of splicing complexes and small nuclear ribonucleoprotein particles by native gel electrophoresis. Methods Enzymol., 180, 442-453.
27. Konforti, B.B. and Konarska, M.M. (1995) A short 5′ splice site RNA oligo can participate in both steps of splicing in mammalian extracts. RNA, 1, 815-827.
28. Konforti, B.B., Koziolkiewicz, M.J. and Konarska, M.M. (1993) Disruption of base pairing between the 5′ splice site and the 5′ end of U1 snRNA is required for spliceosome assembly. Cell, 75, 863-873.
29. LeCuyer, K.A. and Crothers, D. (1993) The Leptomonas collosoma spliced leader RNA can switch between two alternate structural forms. Biochemistry, 32, 5301-5311.
30. Lelay-Taha, M.N., Reveillaud, I., Sri-Wadada, J., Brunel, C. and Jeanteur, P. (1986) RNA-protein organization of U1, U5, and U4-U6 small nuclear ribonucleoproteins in HeLa cells. J. Mol. Biol., 189, 519-532.
31. MacMillan, A.M., Query, C.C. Allerson, C.R., Chen, S., Verdine, G.L. and Sharp, P.A. (1994) Dynamic association of proteins with the pre mRNA branch region. Genes Dev., 8, 3008-3020.
32. Madhani, H.D. and Guthrie, C. (1992) A novel base-pairing interaction between U2 and U6 snRNAs suggests a mechanism for the catalytic activation of the spliceosome. Cell, 71, 803-817.
33. Mattaj, I.W. (1988) U snRNP assembly and transport. In Birnstiel, M.L. (ed.), Structure and Function of Major and Minor Small Nuclear Ribonucleoprotein Particles. Springer-Verlag, Berlin, pp. 100-114.
34. McNally, K.P. and Agabian, N. (1992) Trypanosoma brucei spliced-leader RNA methylations are required for trans-splicing in vivo. Mol. Cell. Biol., 12, 4844-4851.
35. Metzenberg, S. and Agabian, N. (1994) Mitochondrial minicircle DNA supports plasmid replication and maintenance in nuclei of Trypanosoma brucei. Proc. Natl Acad. Sci. USA, 91, 5962-5966.
36. Michaeli, S., Roberts, T.G., Watkins, K.P. and Agabian, N. (1990) Isolation of distinct small ribonucleoprotein particles containing the spliced leader and U2 RNAs of Trypanosoma brucei. J. Biol. Chem., 265, 10582-10588.
37. Moore, M.J., Query, C.C. and Sharp, P.A. (1993) Splicing of precursors to mRNAs by the spliceosome. In Gesteland, R.F. and Atkins, J.F. (eds), The RNA World. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 303-358.
38. Mottram, J., Perry, K.L., Lizardi, P.M., Lührmann, R., Agabian, N. and Nelson, R.G. (1989) Isolation and sequence of four small nuclear U RNA genes of Trypanosoma brucei subsp. brucei: Identification of the U2, U4, and U6 RNA analogs. Mol. Cell. Biol., 9, 1212-1223.
39. Newman, A. and Norman, C. (1991) Mutations in yeast U5 snRNA alter the specificity of 5′ splice-site cleavage. Cell, 65, 115-123.
40. Newman, A.J. and Norman, C. (1992) U5 snRNA interacts with exon sequences at 5′ and 3′ splice sites. Cell, 68, 743-754.
41. Newman, A.J., Teigelkamp, S. and Beggs, J.D. (1995) snRNA interactions at 5′ and 3′ splice sites monitored by photoactivated crosslinking in yeast spliceosomes. RNA, 1, 968-980.
42. Nilsen, T.W. (1993) Trans-splicing of nematode premessenger RNA. Annu. Rev. Microbiol., 47, 413-440.
43. Palfi, Z. and Bindereif, A. (1992) Immunological characterization and intracellular localization of trans-spliceosomal small nuclear ribonucleoproteins in Trypanosoma brucei. J. Biol. Chem., 267, 20159-20163.
44. Palfi, Z., Gunzl, A., Cross, M. and Bindereif, A. (1991) Affinity purification of Trypanosoma brucei small nuclear ribonucleoproteins reveals common and specific protein components. Proc. Natl Acad. Sci. USA, 88, 9097-9101.
45. Palfi, Z., Xu, G.L. and Bindereif, A. (1994) Spliced leader-associated RNA of trypanosomes. Sequence conservation and association with protein components common to trans-spliceosomal ribonucleoproteins. J. Biol. Chem., 269, 30620-30625.
46. Patzelt, E., Perry, K.L. and Agabian, N. (1989) Mapping of branch sites in trans-spliced pre-mRNAs of Trypanosoma brucei. Mol. Cell. Biol., 9, 4291-4297.
47. Peattie, D.A. (1979) Direct chemical method for sequencing RNA. Proc. Natl Acad. Sci. USA, 76, 1760-1764.
48. Perry, K.L., Watkins, K.P. and Agabian, N. (1987) Trypanosome mRNAs have unusual 'cap 4' structures acquired by addition of a spliced leader. Proc. Natl Acad. Sci. USA, 84, 8190-8194.
49. Reddy, R. and Busch, H. (1988) Small nuclear RNAs: RNA sequences, structure, and modifications. In Birnstiel, M.L. (ed.), Structure and Function of Major and Minor Small Nuclear Ribonucleoprotein Particles. Springer-Verlag, Berlin, pp. 1-37.
50. Roberts, T.G. (1996) Characterization of components of the trans spliceosome in Trypanosoma brucei brucei. Ph.D. thesis. University of California, Berkeley, USA.
51. Ségault, V., Will, C.L., Sproat, B.S. and Lührmann, R. (1995) In vitro reconstitution of mammalian U2 and U5 snRNPs active in splicing: Sm proteins are functionally interchangeable and are essential for the formation of functional U2 and U5 snRNPs. EMBO J., 14, 4010-4021.
52. Séraphin, B. (1995) Sm and Sm-like proteins belong to a large family: identification of proteins of the U6 as well as the U1, U2, U4 and U5 snRNPs. EMBO J., 14, 2089-2098.
53. Shambaugh, J.D., Hannon, G.E. and Nilsen, T.W. (1994) The spliceosomal U small nuclear RNAs of Ascaris lumbricoides. Mol. Biochem. Parasitol., 64, 349-352.
54. Singh, R. and Reddy, R. (1989) Gamma-monomethyl phosphate: a cap structure in spliceosomal U6 small nuclear RNA. Proc. Natl Acad. Sci. USA, 86, 8280-8283.
55. Sontheimer, E.J. and Steitz, J.A. (1993) The U5 and U6 small nuclear RNAs as active site components of the spliceosome. Science, 262, 1989-1996.
56. Steitz, J.A. (1992) Splicing takes a Holliday. Science, 257, 888-889.
57. Szkukalek, A., Myslinski, E., Mougin, A., Lührmann, R. and Branlant, C. (1995) Phylogenetic conservation of modified nucleotides in the terminal loop 1 of the spliceosomal U5 snRNA. Biochimie, 77, 16-21.
58. Tarn, W.-Y. and Steitz, J.A. (1995) SR proteins can compensate for the loss of U1 snRNP functions in vitro. Genes Dev., 8, 2704-2717.
59. Terns, M.P., Grimm, C., Lund, E. and Dahlberg, J.E. (1995) A common maturation pathway for small nucleolar RNAs. EMBO J., 14, 4860-4871.
60. Thomas, J., Lea, K., Zucker, A.E. and Blumenthal, T. (1990) The spliceosomal snRNAs of Caenorhabditis elegans. Nucleic Acids Res., 18, 2633-2642.
61. Thompson, J.F. and Hearst, J.E. (1983) Structure of E. coli 16S RNA elucidated by psoralen crosslinking. Cell, 32, 1355-1365.
62. Tschudi, C. and Ullu, E. (1990) Destruction of U2, U4, or U6 small nuclear RNA blocks trans splicing in trypanosome cells. Cell, 61, 459-466.
63. Tschudi, C., Richards, F.F. and Ullu, E. (1986) The U2 RNA analogue of T. brucei gambiense: implications for a splicing mechanism in trypanosomes. Nucleic Acids Res., 14, 8893-8903.
64. Tschudi, C., Krainer, A.R. and Ullu, E. (1988) The U6 small nuclear RNA from Trypanosoma brucei. Nucleic Acids Res., 16, 11375.
65. Ullu, E. and Tschudi, C. (1990) Permeable trypanosome cells as a model system for transcription and trans-splicing. Nucleic Acids Res., 18, 3319-3326.
66. Umen, J.G. and Guthrie, C. (1995) The second catalytic step of pre-mRNA splicing. RNA, 1, 869-885.
67. Wassarman, D.A. and Steitz, J.A. (1992) Interactions of small nuclear RNAs with precursor messenger RNA during in vitro splicing. Science, 257, 1918-1925.
68. Watkins, K.P. and Agabian, N. (1991) In vivo UV crosslinking of U snRNAs that participate in trypanosome trans-splicing. Genes Dev., 5, 1859-1869.
69. Watkins, K.P., Dungan, J.M. and Agabian, N. (1994) Identification of a small RNA that interacts with the 5′ splice site of the Trypanosoma brucei spliced leader RNA in vivo. Cell, 76, 171-182.
70. Will, C.L., Behrens, S.E. and Lührmann, R. (1993) Protein composition of mammalian spliceosomal snRNPs. Mol. Biol. Rep., 18, 121-126.
71. Wyatt, J.R., Sontheimer, E.J. and Steitz, J.A. (1992) Site-specific crosslinking of mammalian U5 snRNP to the 5′ splice site before the first step of pre-mRNA splicing. Genes Dev., 6, 2542-2553.
72. Zuker, M., Jaeger, J.A. and Turner, D.H. (1991) A comparison of optimal and suboptimal RNA secondary structures predicted by free energy minimization with structures determined by phylogenetic comparison. Nucleic Acids Res., 19, 2707-2714.