Trans mRNA splicing in trypanosomes: Cloning and analysis of a PRP8-homologous gene from Trypanosoma brucei provides evidence for a U5-analogous RNP

EMBO Journal

Volumn 16, Issue 14, 1997, Pages 4433-4440

  Lücke, Stephan ^a   Klöckner, Thomas ^b   Palfi, Zsofia ^a   Boshart, Michael ^b   Bindereif, Albrecht ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

snRNA; snRNP; trans splicing; Trypanosomes; U5

Indexed keywords

ANTIBODY; MESSENGER RNA; SMALL NUCLEAR RIBONUCLEOPROTEIN; SMALL NUCLEAR RNA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENETIC ANALYSIS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; RNA SPLICING; SPLICEOSOME; TRYPANOSOMA BRUCEI;

ANIMALS; CENTRIFUGATION, DENSITY GRADIENT; CLONING, MOLECULAR; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FUNGAL PROTEINS; MOLECULAR SEQUENCE DATA; PRECIPITIN TESTS; RIBONUCLEOPROTEIN, U5 SMALL NUCLEAR; RNA SPLICING; RNA, MESSENGER; RNA, PROTOZOAN; RNA, SMALL NUCLEAR; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; SPLICEOSOMES; TRYPANOSOMA BRUCEI BRUCEI;

TRYPANOSOMA; TRYPANOSOMA BRUCEI;

EID: 0040624056     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.14.4433     Document Type: Article

References (48)

1. Agabian, N. (1990) Trans splicing of nuclear pre-mRNAs. Cell, 61, 1157-1160.
2. Anderson, G.J., Bach, M., Lührmann, R. and Beggs, J.D. (1989) Conservation between yeast and man of a protein asssociated with U5 small nuclear ribonucleoprotein. Nature, 342, 819-822.
3. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. and Struhl, K. (eds) (1987) Current Protocols in Molecular Biology. Greene Publishing Associates and Wiley-Interscience, New York.
4. Boshart, M., Weih, F., Nichols, M. and Schutz, G. (1991) The tissue-specific extinguisher locus TSE1 encodes a regulatory subunit of cAMP-dependent protein kinase. Cell, 66, 849-859.
5. Brown, J.D. and Beggs, J.D. (1992) Roles of PRP8 protein in the assembly of splicing complexes. EMBO J., 11, 3721-3729.
6. Brun, R. and Schönenberger, M. (1979) Cultivation and in vitro cloning of procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Acta Tropica, 36, 289-292.
7. Bruzik, J.P., Van Doren, K. Hirsh, D. and Steitz, J.A. (1988) Trans splicing involves a novel form of small nuclear ribonucleoprotein particles. Nature, 335, 559-562.
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. Cross, G.A.M. (1975) Identification, purification and properties of clone specific glycoprotein antigens constituting the surface coat of Trypanosoma brucei. Parasitologv, 71, 393-417.
10. Cross, M., Günzl, 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.
11. Cross, M., Wieland, B., Palfi, Z., Günzl, A., Röthlisberger, U., Lahm, H.-W. and Bindereif, A. (1993) The trans-spliceosomal U2 snRNP protein 40K of Trypanosoma brucei: Cloning and analysis of functional domains reveals homology to a mammalian snRNP protein. EMBO J., 12, 1239-1248.
12. Devereux, J., Haeberli, P. and Smithies, O. (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res., 12, 387-395.
13. Dignam, D.L., Lebovitz, R.M. and Roeder, R.D. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res., 11, 1475-1489.
14. Dungan, J.M., Watkins, K.P. and Agabian, N. (1996) Evidence for the presence of a small U5-like RNA in active trans-spliceosomes of Trypanosoma brucei. EMBO J., 15, 4016-4029.
15. England, T.E. and Uhlenbeck, O.C. (1978) 3′-terminal labelling of RNA with T4 RNA ligase. Nature, 275, 560-561.
16. Frank, D.N., Roiha, H. and Guthrie, C. (1994) Architecture of the U5 small nuclear RNA. Mol. Cell. Biol., 14, 2180-2190.
17. Günzl, 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.
18. Guthrie, C. and Patterson, B. (1988) Spliceosomal snRNAs. Annu. Rev. Genet., 22, 387-419.
19. Hodges, P.E., Jackson, S.R. Brown, J.D. and Beggs, J.D. (1995) Extraordinary sequence conservation of the PRP8 splicing factor. Yeast, 11, 337-342.
20. Jackson, S.P., Lossky, M. and Beggs, J.D. (1988) Cloning of the RNA8 gene of Saccharomyces cerevisiae, detection of the RNA8 protein, and demonstration that it is essential for nuclear pre-mRNA splicing. Mol. Cell. Biol., 8, 1067-1075.
21. Lelay-Taha, M.-N., Reveillaud, I., Sri-Widada, D.M., 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.
22. Maroney, P.A., Yu, Y.-T., Jankowska, M. and Nilsen, T. (1996) Direct analysis of nematode cis- and trans-spliceosomes: a functional role for U5 snRNA in spliced leader addition trans-splicing and the identification of novel Sm snRNPs. RNA, 2, 735-745.
23. 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.
24. Murphy, W.J., Watkins, K.P. and Agabian, N. (1986) Identification of a novel Y branch structure as an intermediate in trypanosome mRNA processing: evidence for trans splicing. Cell, 47, 517-525.
25. Newman, A.J. and Norman, C. (1991) Mutations in yeast U5 snRNA alter the specificity of 5′ splice-site cleavage. Cell, 65, 115-123.
26. Newman, A.J. and Norman, C. (1992) U5 snRNA interacts with exon sequences at 5′ and 3′ splice sites. Cell, 68, 743-754.
27. Nilsen, T.W. (1993) Trans-splicing of nematode premessenger RNA. Annu. Rev. Microbiol., 47, 413-440.
28. Nilsen, T.W. (1995) Trans-splicing: an update. Mol. Biochem. Parasitol., 73, 1-6.
29. O'Keefe, R.T., Norman, C. and Newman A.J. (1996) The invariant U5 snRNA loop 1 sequence is dispensable for the first catalytic step of pre-mRNA splicing. Cell, 86, 679-689.
30. 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.
31. Palfi, Z., Günzl, 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.
32. Palfi, Z., Xu, G.-L. and Bindereif, A. (1994) Spliced leader-associated RNA of trypanosomes. J. Biol. Chem., 269, 30620-30625.
33. Pringle, J.R., Adams, A.E.M., Drubin, D.G. and Haarer, B.K. (1991) Immunofluorescence methods for yeast. Methods Enzymol., 194, 565-602.
34. Reyes, J.L., Kois, P., Konforti, B.B. and Konarska, M.M. (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.
35. 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.
36. Spirin, A.S. (1969) Informosomes. Eur. J. Biochem., 10, 20-35.
37. Staknis, D. and Reed, R. (1994) Direct interactions between pre-mRNA and six U2 small nuclear ribonucleoproteins during spliceosome assembly. Mol. Cell. Biol., 14, 2994-3005.
38. Steitz, J.A. (1992) Splicing takes a holliday. Science, 257, 888-889.
39. Sutton, R.E. and Boothroyd, J.C. (1986) Evidence for trans splicing in trypanosomes. Cell, 47, 527-535.
40. Teigelkamp, S., Newman, A.J. and Beggs, J.D. (1995a) Extensive interactions of PRP8 protein with the 5′ and 3′ splice sites during splicing suggest a role in stabilization of exon alignment by U5 snRNA. EMBO J., 14, 2602-2612.
41. Teigelkamp, S., Whittaker, E. and Beggs, J.D. (1995b) Interaction of the yeast splicing factor PRP8 with substrate RNA during both steps of splicing. Nucleic Acids Res., 23, 320-326.
42. 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.
43. Umen, J.G. and Guthrie, C. (1995a) A novel role for a U5 snRNP protein in 3′ splice site selection. Genes Dev., 9, 855-868.
44. Umen, J.G. and Guthrie, C. (1995b) Prp16p, Slu7p, and PRP8p interact with the 3′ splice site in two distinct stages during the second catalytic step of pre-mRNA splicing. RNA, 1, 584-597.
45. Umen, J.G. and Guthrie, C. (1996) Mutagenesis of the yeast gene PRP8 reveals domains governing the specificity and fidelity of 3′ splice site selection. Genetics, 143, 723-739.
46. Vassella, E. and Boshart, M. (1996) High-molecular mass agarose matrix supports growth of bloodstream forms of pleomorphic Trypanosoma brucei strains in axenic culture. Mol. Biochem. Parasitol., 82, 91-105.
47. Whittaker, E. and Beggs, J.D. (1991) The yeast PRP8 protein interacts directly with pre-mRNA. Nucleic Acids Res., 19, 5483-5489.
48. Wyatt, J.R., Sontheimer, E.J. and Steitz, J.A. (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.