3'-cyclic phosphorylation of U6 snRNA leads to recruitment of recycling factor p110 through LSm proteins

RNA

Volumn 14, Issue 8, 2008, Pages 1532-1538

  Licht, Konstantin ^a   Medenbach, Jan ^a   Lührmann, Reinhard ^b   Kambach, Christian ^c   Bindereif, Albrecht ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^c PAUL SCHERRER INSTITUTE   (Switzerland)

Author keywords

La antigen; Sm like proteins; snRNP recycling; Splicing; U6 snRNA

Indexed keywords

PROTEIN P110; SMALL NUCLEAR RNA;

ARTICLE; BIOGENESIS; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION;

AUTOANTIGENS; BASE SEQUENCE; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; RIBONUCLEOPROTEIN, U4-U6 SMALL NUCLEAR; RIBONUCLEOPROTEINS; RNA SPLICING; RNA, SMALL NUCLEAR; RNA-BINDING PROTEINS;

EID: 47949110828     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1129608     Document Type: Article

References (39)

1. Achsel, T., Brahms, H., Kastner, B., Bachi, A., Wilm, M., and Lührmann, R. 1999. A doughnut-shaped heteromer of human Sm-like proteins binds to the 3′-end of U6 snRNA, thereby facilitating U4/U6 duplex formation in vitro. EMBO J. 18: 5789-5802.
2. Bell, M., Schreiner, S., Damianov, A., Reddy, R., and Bindereif, A. 2002. p110, a novel human U6 snRNP protein and U4/U6 snRNP recycling factor. EMBO J. 21: 2724-2735.
3. Bessonov, S., Anokhina, M., Will, C.L., Urlaub, H., and Lührmann, R. 2008. Isolation of an active step I spliceosome and composition of its RNP core. Nature 452: 846-850.
4. Brow, D.A. 2002. Allosteric cascade of spliceosome activation. Annu. Rev. Genet. 36: 333-360.
5. Cameron, V. and Uhlenbeck, O.C. 1977. 3′-Phosphatase activity in T4 polynucleotide kinase. Biochemistry 16: 5120-5126.
6. Chan, S.P., Kao, D.I., Tsai, W.Y., and Cheng, S.C. 2003. The prp19p-associated complex in spliceosome activation. Science 302: 279-282.
7. Damianov, A., Schreiner, S., and Bindereif, A. 2004. Recycling of the U12-type spliceosome requires p110, a component of the U6atac snRNP. Mol. Cell. Biol. 24: 1700-1708.
8. Dignam, J.D., Lebovitz, R.M., and Roeder, R.G. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11: 1475-1489.
9. Genschik, P., Billy, E., Swianiewicz, M., and Filipowicz, W. 1997. The human RNA 3′-terminal phosphate cyclase is a member of a new family of proteins conserved in Eucarya, Bacteria, and Archaea. EMBO J. 16: 2955-2967.
10. Gu, J., Shumyatsky, G., Makan, N., and Reddy, R. 1997. Formation of 2′,3′-cyclic phosphates at the 3′-end of human U6 small nuclear RNA in vitro. Identification of 2′,3′-cyclic phosphates at the 3′-ends of human signal recognition particle and mitochondrial RNA processing RNAs. J. Biol. Chem. 272: 21989-21993.
11. Karaduman, R., Fabrizi, P., Hartmuth, K., Urlaub, H., and Lührmann, R. 2006. RNA structure and RNA-protein interactions in purified yeast U6 snRNPs. J. Mol. Biol. 356: 1248-1262.
12. Khusial, P., Plaag, R., and Zieve, G.W. 2005. LSm proteins form heptameric rings that bind to RNA via repeating motifs. Trends Biochem. Sci. 30: 522-528.
13. Lange, T.S. and Gerbi, S.A. 2000. Transient nucleolar localization of U6 small nuclear RNA in Xenopus laevis oocytes. Mol. Biol. Cell 11: 2419-2428.
14. Lund, E. and Dahlberg, J.E. 1992. Cyclic 2′,3′-phosphates and non-templated nucleotides at the 3′-end of spliceosomal U6 small nuclear RNA's. Science 255: 327-330.
15. Mayes, A.E., Verdone, L., Legrain, P., and Beggs, J.D. 1999. Chracterization of Sm-like proteins in yeast and their association with U6 snRNA. EMBO J. 18: 4321-4331.
16. Medenbach, J., Schreiner, S., Liu, S., Lührmann, R., and Bindereif, A. 2004. Human U4/U6 snRNP recycling factor p110: Mutational analysis reveals the function of the tetratricopeptide repeat domain in recycling. Mol. Cell. Biol. 24: 7392-7401.
17. Milligan, J.F., Groebe, D.R., Witherell, G.W., and Uhlenbeck, O.C. 1987. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res. 15: 8783-8798.
18. Mörl, M., Lizano, E., Willkomm, D.K., and Hartmann, R.K. 2005. Production of RNAs with homogeneous 5′-and 3′-ends. In Handbook of RNA biochemistry (eds. R.K. Hartmann et al.), pp. 22-35. Wiley-VCH, Weinheim, Germany.
19. Pruijn, G.J., Slobbe, R.L., and van Venrooij, W.J. 1991. Analysis of protein-RNA interactions within Ro ribonucleoprotein complexes. Nucleic Acids Res. 19: 5173-5180.
20. Rader, S.D. and Guthrie, C. 2002. A conserved Lsm-interaction motif in Prp24 required for efficient U4/U6 di-snRNP formation. RNA 8: 1378-1392.
21. Raghunathan, P.L. and Guthrie, C. 1998. A spliceosomal recycling factor that reanneals U4 and U6 small nuclear ribonucleoprotein particles. Science 279: 857-860.
22. Salgado-Garrido, J., Bragado-Nilsson, E., Kandels-Lewis, S., and Séraphin, B. 1999. Sm and Sm-like proteins assemble in two related complexes of deep evolutionary origin. EMBO J. 18: 3451-3462.
23. 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.
24. Shannon, K.W. and Guthrie, C. 1991. Suppressors of a U4 snRNA mutation define a novel U6 snRNP protein with RNA-binding motifs. Genes & Dev. 5: 773-785.
25. Shimba, S. and Reddy, R. 1994. Purification of human U6 small nuclear RNA capping enzyme. Evidence for a common capping enzyme for gamma-monomethyl- capped small RNAs. J. Biol. Chem. 269: 12419-12423.
26. Spiller, M.P., Boon, K.L., Reijns, M.A., and Beggs, J.D. 2007. The Lsm2-8 complex determines nuclear localization of the spliceosomal U6 snRNA. Nucleic Acids Res. 35: 923-929.
27. Stanek, D., Rader, S.D., Klingauf, M., and Neugebauer, K.M. 2003. Targeting of U4/U6 small nuclear RNP assembly factor SART3/ p110 to Cajal bodies. J. Cell Biol. 160: 505-516.
28. Tazi, J., Forne, T., Jeanteur, P., Cathala, G., and Brunel, C. 1993. Mammalian U6 small nuclear RNA undergoes 3′-end modifications within the spliceosome. Mol. Cell. Biol. 13: 1641-1650.
29. Teplova, M., Yuan, Y.R., Phan, A.T., Malinina, L., Ilin, S., Teplov, A., and Patel, D.J. 2006. Structural basis for recognition and sequestration of UUU(OH) 3′-termini of nascent RNA polymerase III transcripts by La, a rheumatic disease autoantigen. Mol. Cell 21: 75-85.
30. Trippe, R., Sandrock, B., and Benecke, B.J. 1998. A highly specific terminal uridylyl transferase modifies the 3′-end of U6 small nuclear RNA. Nucleic Acids Res. 26: 3119-3126.
31. Trippe, R., Guschina, E., Hossbach, M., Urlaub, H., Lührmann, R., and Benecke, B.J. 2006. Identification, cloning, and functional analysis of the human U6 snRNA-specific terminal uridylyl transferase. RNA 12: 1494-1504.
32. Tycowski, K.T., Aab, A., and Steitz, J.A. 2004. Guide RNAs with 5′-caps and novel box C/D snoRNA-like domains for modification of snRNAs in metazoa. Curr. Biol. 14: 1985-1995.
33. Tycowski, K.T., You, Z.H., Graham, P.J., and Steitz, J.A. 1998. Modification of U6 spliceosomal RNA is guided by other small RNAs. Mol. Cell 2: 629-638.
34. Verdone, L., Galardi, S., Page, D., and Beggs, J.D. 2004. Lsm proteins promote regeneration of pre-mRNA splicing activity. Curr. Biol. 14: 1487-1491.
35. Vidal, V.P., Verdone, L., Mayes, A.E., and Beggs, J.D. 1999. Characterization of U6 snRNA-protein interactions. RNA 5: 1470-1481.
36. Wersig, C. and Bindereif, A. 1990. Conserved domains of human U4 snRNA required for snRNP and spliceosome assembly. Nucleic Acids Res. 18: 6223-6229.
37. Will, C.L. and Lührmann, R. 2001. Spliceosomal UsnRNP biogenesis, structure and function. Curr. Opin. Cell Biol. 13: 290-301.
38. Wolff, T. and Bindereif, A. 1993. Conformational changes of U6 RNA during the spliceosome cycle: An intramolecular helix is essential both for initiating the U4-U6 interaction and for the first step of splicing. Genes & Dev. 7: 1377-1389.
39. Zaric, B., Chami, M., Remigy, H., Engel, A., Ballmer-Hofer, K., Winkler, F.K., and Kambach, C. 2005. Reconstitution of two recombinant LSm protein complexes reveals aspects of their architecture, assembly, and function. J. Biol. Chem. 280: 16066-16075.