Splicing of a rare class of introns by the U12-dependent spliceosome

References

Berget, S.M. (1995). Exon recognition in vertebrate splicing. J. Biol. Chem.270, 2411–2414.10.1074/jbc.270.6.2411Search in Google Scholar

Black, D.L. (2003). Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem.72, 291–336.10.1146/annurev.biochem.72.121801.161720Search in Google Scholar

Burge, C.B., Padgett, R.A., and Sharp, P.A. (1998). Evolutionary fates and origins of U12-type introns. Mol. Cell2, 773–785.10.1016/S1097-2765(00)80292-0Search in Google Scholar

Burge, C.B., Tuschl, T., and Sharp, P.A. (1999). Splicing of precursors to mRNAs by the spliceosomes. In: The RNA world, 2nd edition, R.F. Gesteland, T.R. Cech and J.F. Atkins, eds. (Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press), pp. 525–560.Search in Google Scholar

Collins, C.A. and Guthrie, C. (2000). The question remains: is the spliceosome a ribozyme? Nat. Struct. Biol.7, 850–854.Search in Google Scholar

Dietrich, R.C., Incorvaia, R., and Padgett, R.A. (1997). Terminal intron dinucleotide sequences do not distinguish between U2- and U12-dependent introns. Mol. Cell1, 151–160.10.1016/S1097-2765(00)80016-7Search in Google Scholar

Dietrich, R.C., Peris, M.J., Seyboldt, A.S., and Padgett, R.A. (2001a). Role of the 3′ splice site in U12-dependent intron splicing. Mol. Cell. Biol.21, 1942–1952.10.1128/MCB.21.6.1942-1952.2001Search in Google Scholar

Dietrich, R.C., Shukla, G.C., Fuller, J.D., and Padgett, R.A. (2001b). Alternative splicing of U12-dependent introns in vivo responds to purine-rich enhancers. RNA7, 1378–1388.Search in Google Scholar

Dönmez, G., Hartmuth, K., and Lührmann, R. (2004). Modified nucleotides at the 5′ end of human U2 snRNA are required for spliceosomal E-complex formation. RNA10, 1925–1933.10.1261/rna.7186504Search in Google Scholar

Frilander, M.J. and Steitz, J.A. (1999). Initial recognition of U12-dependent introns requires both U11/5′ splice-site and U12/branchpoint interactions. Genes Dev.13, 851–863.10.1101/gad.13.7.851Search in Google Scholar

Frilander, M.J. and Steitz, J.A. (2001). Dynamic exchanges of RNA interactions leading to catalytic core formation in the U12-dependent spliceosome. Mol. Cell7, 217–226.10.1016/S1097-2765(01)00169-1Search in Google Scholar

Frilander, M.J. and Meng, X. (2005). Proximity of the U12 snRNA with both the 5′ splice site and the branch point during the early stages of spliceosome assembly. Mol. Cell. Biol., in press.10.1128/MCB.25.12.4813-4825.2005Search in Google Scholar PubMed PubMed Central

Golas, M.M., Sander, B., Will, C.L., Lührmann, R., and Stark, H. (2003). Molecular architecture of the multiprotein splicing factor SF3b. Science300, 980–984.10.1126/science.1084155Search in Google Scholar PubMed

Golas, M.M., Sander, B., Will, C.L., Lührmann, R., and Stark, H. (2005). Major conformational change in the protein complex SF3b upon integration into the spliceosomal U11/U12 di-snRNP as revealed by electron cryomicroscopy. Mol. Cell17, 869–883.10.1016/j.molcel.2005.02.016Search in Google Scholar

Gozani, O., Feld, R., and Reed, R. (1996). Evidence that sequence-independent binding of highly conserved U2 snRNP proteins upstream of the branch site is required for assembly of spliceosomal complex A. Genes Dev.10, 233–243.10.1101/gad.10.2.233Search in Google Scholar

Graveley, B.R. (2001). Alternative splicing: increasing diversity in the proteomic world. Trends Genet.17, 100–107.10.1016/S0168-9525(00)02176-4Search in Google Scholar

Guthrie, C. and Patterson, B. (1988). Spliceosomal snRNAs. Annu. Rev. Genet.22, 387–419.10.1146/annurev.ge.22.120188.002131Search in Google Scholar PubMed

Hall, S.L. and Padgett, R.A. (1994). Conserved sequences in a class of rare eukaryotic nuclear introns with non-consensus splice sites. J. Mol. Biol.239, 357–365.10.1006/jmbi.1994.1377Search in Google Scholar PubMed

Hall, S.L. and Padgett, R.A. (1996). Requirement of U12 snRNA for in vivo splicing of a minor class of eukaryotic nuclearpre-mRNA introns. Science271, 1716–1718.10.1126/science.271.5256.1716Search in Google Scholar PubMed

Hartmuth, K., Urlaub, H., Vornlocher, H.P., Will, C.L., Gentzel, M., Wilm, M., and Lührmann, R. (2002). Protein composition of human prespliceosomes isolated by a tobramycin affinity-selection method. Proc. Natl. Acad. Sci. USA99, 16719–16724.10.1073/pnas.262483899Search in Google Scholar PubMed PubMed Central

Hastings, M.L. and Krainer, A.R. (2001). Functions of SR proteins in the U12-dependent AT-AC pre-mRNA splicing pathway. RNA7, 471–482.10.1017/S1355838201002552Search in Google Scholar

Hastings, M.L., Resta, N., Traum, D., Stella, A., Guanti, G., and Krainer, A.R. (2005). An LKB1 AT-AC intron mutation causes Peutz-Jeghers syndrome via splicing at noncanonical cryptic splice sites. Nat. Struct. Mol. Biol.12, 54–59.10.1038/nsmb873Search in Google Scholar PubMed

Horowitz, D.S., Kobayashi, R., and Krainer, A.R. (1997). A new cyclophilin and the human homologues of yeast Prp3 and Prp4 form a complex associated with U4/U6 snRNPs. RNA3, 1374–1387.Search in Google Scholar

Incorvaia, R. and Padgett, R.A. (1998). Base pairing with U6atac snRNA is required for 5′ splice site activation of U12-dependent introns in vivo. RNA4, 709–718.10.1017/S1355838298980207Search in Google Scholar PubMed PubMed Central

Jackson, I.J. (1991). A reappraisal of non-consensus mRNA splice sites. Nucleic Acids Res.19, 3795–3798.10.1093/nar/19.14.3795Search in Google Scholar

Jurica, M.S., Licklider, L.J., Gygi, S.R., Grigorieff, N., and Moore, M.J. (2002). Purification and characterization of native spliceosomes suitable for three-dimensional structural analysis. RNA8, 426–439.10.1017/S1355838202021088Search in Google Scholar

Jurica, M.S. and Moore, M.J. (2003). Pre-mRNA splicing: awash in a sea of proteins. Mol. Cell12, 5–14.10.1016/S1097-2765(03)00270-3Search in Google Scholar

Kolossova, I. and Padgett, R.A. (1997). U11 snRNA interacts in vivo with the 5′ splice site of U12-dependent (AU-AC)pre-mRNA introns. RNA3, 227–233.Search in Google Scholar

Levine, A. and Durbin, R. (2001). A computational scan for U12-dependent introns in the human genome sequence. Nucleic Acids Res.29, 4006–4013.10.1093/nar/29.19.4006Search in Google Scholar

Luo, H.R., Moreau, G.A., Levin, N., and Moore, M.J. (1999). The human Prp8 protein is a component of both U2- and U12-dependent spliceosomes. RNA5, 893–908.10.1017/S1355838299990520Search in Google Scholar

Lynch, M. and Richardson, A.O. (2002). The evolution of spliceosomal introns. Curr. Opin. Genet. Dev.12, 701–710.10.1016/S0959-437X(02)00360-XSearch in Google Scholar

Makarov, E.M., Makarova, O.V., Achsel, T., and Lührmann, R. (2000). The human homologue of the yeast splicing factor prp6p contains multiple TPR elements and is stably associated with the U5 snRNP via protein-protein interactions. J. Mol. Biol.298, 567–575.10.1006/jmbi.2000.3685Search in Google Scholar PubMed

Makarov, E.M., Makarova, O.V., Urlaub, H., Gentzel, M., Will, C.L., Wilm, M., and Lührmann, R. (2002). Small nuclear ribonucleoprotein remodeling during catalytic activation of the spliceosome. Science298, 2205–2208.10.1126/science.1077783Search in Google Scholar PubMed

Makarova, O.V., Makarov, E.M., Liu, S., Vornlocher, H.P., and Lührmann, R. (2002). Protein 61K, encoded by a gene (PRPF31) linked to autosomal dominant retinitis pigmentosa, is required for U4/U6*U5 tri-snRNP formation and pre-mRNA splicing. EMBO J.21, 1148–1157.10.1093/emboj/21.5.1148Search in Google Scholar PubMed PubMed Central

Makarova, O.V., Makarov, E.M., Urlaub, H., Will, C.L., Gentzel, M., Wilm, M., and Lührmann, R. (2004). A subset of human 35S U5 proteins, including Prp19, function prior to catalytic step 1 of splicing. EMBO J.23, 2381–2391.10.1038/sj.emboj.7600241Search in Google Scholar PubMed PubMed Central

Manley, J.L. and Tacke, R. (1996). SR proteins and splicing control. Genes Dev.10, 1569–1579.10.1101/gad.10.13.1569Search in Google Scholar

Massenet, S. and Branlant, C. (1999). A limited number of pseudouridine residues in the human atac spliceosomal UsnRNAs as compared to human major spliceosomal UsnRNAs. RNA5, 1495–1503.10.1017/S1355838299991537Search in Google Scholar

Montzka, K.A. and Steitz, J.A. (1988). Additional low-abundance human small nuclear ribonucleoproteins: U11, U12, etc. Proc. Natl. Acad. Sci. USA85, 8885–8889.10.1073/pnas.85.23.8885Search in Google Scholar

Moore, M.J., Query, C.C., and Sharp, P.A. (1993). Splicing of precursors to mRNA by the spliceosome. In: The RNA World, R.F. Gesteland and J.F. Atkins, eds. (Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press), pp. 303–357.Search in Google Scholar

Nilsen, T.W. (1998). RNA-RNA interactions in nuclear pre-mRNA splicing. In: RNA Structure and Function, R.W. Simons and M. Grunberg-Manago, eds. (Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press), pp. 279–308.Search in Google Scholar

Nottrott, S., Hartmuth, K., Fabrizio, P., Urlaub, H., Vidovic, I., Ficner, R., and Lührmann, R. (1999). Functional interaction of a novel 15.5kD [U4/U6.U5] tri-snRNP protein with the 5′ stem-loop of U4 snRNA. EMBO J.18, 6119–6133.Search in Google Scholar

Nottrott, S., Urlaub, H., and Lührmann, R. (2002). Hierarchical, clustered protein interactions with U4/U6 snRNA: a biochemical role for U4/U6 proteins. EMBO J.21, 5527–5538.10.1093/emboj/cdf544Search in Google Scholar

Padgett, R.A. and Shukla, G.C. (2002). A revised model for U4atac/U6atac snRNA base pairing. RNA8, 125–128.10.1017/S1355838202017156Search in Google Scholar

Patel, A.A. and Steitz, J.A. (2003). Splicing double: insights from the second spliceosome. Nat. Rev. Mol. Cell. Biol.4, 960–970.10.1038/nrm1259Search in Google Scholar

Patel, A.A., McCarthy, M., and Steitz, J.A. (2002). The splicing of U12-type introns can be a rate-limiting step in gene expression. EMBO J.21, 3804–3815.10.1093/emboj/cdf297Search in Google Scholar

Rappsilber, J., Ryder, U., Lamond, A.I. and Mann, M. (2002). Large-scale proteomic analysis of the human spliceosome. Genome Res.12, 1231–1245.10.1101/gr.473902Search in Google Scholar

Reed, R. (1996). Initial splice-site recognition and pairing during pre-mRNA splicing. Curr. Opin. Genet. Dev.6, 215–220.10.1016/S0959-437X(96)80053-0Search in Google Scholar

Reed, R. and Palandjian, L. (1997). Spliceosome assembly. In: Eukaryotic mRNA processing, A.R. Krainer, ed. (Oxford, UK: IRL Press), pp. 103–129.Search in Google Scholar

Sanford, J.R., Longman, D., and Caceres, J.F. (2003). Multiple roles of the SR protein family in splicing regulation. Prog. Mol. Subcell. Biol.31, 33–58.10.1007/978-3-662-09728-1_2Search in Google Scholar PubMed

Sashital, D.G., Cornilescu, G., McManus, C.J., Brow, D.A., and Butcher, S.E. (2004). U2-U6 RNA folding reveals a group II intron-like domain and a four-helix junction. Nat. Struct. Mol. Biol.11, 1237–1242.10.1038/nsmb863Search in Google Scholar

Scamborova, P., Wong, A., and Steitz, J.A. (2004). An intronic enhancer regulates splicing of the twintron of Drosophila melanogaster prospero pre-mRNA by two different spliceosomes. Mol. Cell. Biol.24, 1855–1869.10.1128/MCB.24.5.1855-1869.2004Search in Google Scholar

Schaffert, N., Hossbach, M., Heintzmann, R., Achsel, T., and Lührmann, R. (2004). RNAi knockdown of hPrp31 leads to an accumulation of U4/U6 di-snRNPs in Cajal bodies. EMBO J.23, 3000–3009.10.1038/sj.emboj.7600296Search in Google Scholar

Schneider, C., Will, C.L., Makarova, O.V., Makarov, E.M., and Lührmann, R. (2002). Human U4/U6.U5 and U4atac/U6atac.U5 tri-snRNPs exhibit similar protein compositions. Mol. Cell. Biol.22, 3219–3229.Search in Google Scholar

Schneider, C., Will, C.L., Brosius, J., Frilander, M.J., and Lührmann, R. (2004). Identification of an evolutionarily divergent U11 small nuclear ribonucleoprotein particle in Drosophila. Proc. Natl. Acad. Sci. USA101, 9584–9589.10.1073/pnas.0403400101Search in Google Scholar

Shukla, G.C. and Padgett, R.A. (1999). Conservation of functional features of U6atac and U12 snRNAs between vertebrates and higher plants. RNA5, 525–538.10.1017/S1355838299982213Search in Google Scholar

Shukla, G.C. and Padgett, R.A. (2001). The intramolecular stem-loop structure of U6 snRNA can functionally replace the U6atac snRNA stem-loop. RNA7, 94–105.10.1017/S1355838201000218Search in Google Scholar

Shukla, G.C. and Padgett, R.A. (2002). A catalytically active group II intron domain 5 can function in the U12-dependent spliceosome. Mol. Cell9, 1145–1150.10.1016/S1097-2765(02)00505-1Search in Google Scholar

Shukla, G.C. and Padgett, R.A. (2004). U4 small nuclear RNA can function in both the major and minor spliceosomes. Proc. Natl. Acad. Sci. USA101, 93–98.10.1073/pnas.0304919101Search in Google Scholar PubMed PubMed Central

Sontheimer, E.J., Sun, S., and Piccirilli, J.A. (1997). Metal ion catalysis during splicing of premessenger RNA. Nature388, 801–805.10.1038/42068Search in Google Scholar PubMed

Sun, J.S. and Manley, J.L. (1995). A novel U2-U6 snRNA structure is necessary for mammalian mRNA splicing. Genes Dev.9, 843–854.10.1101/gad.9.7.843Search in Google Scholar PubMed

Tarn, W.Y. and Steitz, J.A. (1996a). Highly diverged U4 and U6 small nuclear RNAs required for splicing rare AT-AC introns. Science273, 1824–1832.10.1126/science.273.5283.1824Search in Google Scholar

Tarn, W.Y. and Steitz, J.A. (1996b). A novel spliceosome containing U11, U12, and U5 snRNPs excises a minor class (AT-AC) intron in vitro. Cell84, 801–811.10.1016/S0092-8674(00)81057-0Search in Google Scholar

Tarn, W.Y. and Steitz, J.A. (1997). Pre-mRNA splicing: the discovery of a new spliceosome doubles the challenge. Trends Biochem. Sci.22, 132–137.10.1016/S0968-0004(97)01018-9Search in Google Scholar

Teigelkamp, S., Achsel, T., Mundt, C., Gothel, S.F., Cronshagen, U., Lane, W.S., Marahiel, M., and Lührmann, R. (1998). The 20kD protein of human [U4/U6.U5] tri-snRNPs is a novel cyclophilin that forms a complex with the U4/U6-specific 60kD and 90kD proteins. RNA4, 127–141.Search in Google Scholar

Valadkhan, S. and Manley, J.L. (2001). Splicing-related catalysis by protein-free snRNAs. Nature413, 701–707.10.1038/35099500Search in Google Scholar

Valadkhan, S. and Manley, J.L. (2003). Characterization of the catalytic activity of U2 and U6 snRNAs. RNA9, 892–904.10.1261/rna.5440303Search in Google Scholar

Wassarman, K.M. and Steitz, J.A. (1992). The low-abundance U11 and U12 small nuclear ribonucleoproteins (snRNPs) interact to form a two-snRNP complex. Mol. Cell. Biol.12, 1276–1285.Search in Google Scholar

Will, C.L. and Lührmann, R. (1997). Protein functions in pre-mRNA splicing. Curr. Opin. Cell Biol.9, 320–328.10.1016/S0955-0674(97)80003-8Search in Google Scholar

Will, C.L. and Lührmann, R. (2001). Spliceosomal UsnRNP biogenesis, structure and function. Curr. Opin. Cell Biol.13, 290–301.10.1016/S0955-0674(00)00211-8Search in Google Scholar

Will, C.L., Schneider, C., Reed, R., and Lührmann, R. (1999). Identification of both shared and distinct proteins in the major and minor spliceosomes. Science284, 2003–2005.10.1126/science.284.5422.2003Search in Google Scholar PubMed

Will, C.L., Schneider, C., MacMillan, A.M., Katopodis, N.F., Neubauer, G., Wilm, M., Lührmann, R., and Query, C.C. (2001). A novel U2 and U11/U12 snRNP protein that associates with the pre-mRNA branch site. EMBO J.20, 4536–4546.10.1093/emboj/20.16.4536Search in Google Scholar PubMed PubMed Central

Will, C.L., Urlaub, H., Achsel, T., Gentzel, M., Wilm, M., and Lührmann, R. (2002). Characterization of novel SF3b and 17S U2 snRNP proteins, including a human Prp5p homologue and an SF3b DEAD-box protein. EMBO J.21, 4978–4988.10.1093/emboj/cdf480Search in Google Scholar PubMed PubMed Central

Will, C.L., Schneider, C., Hossbach, M., Urlaub, H., Rauhut, R., Elbashir, S., Tuschl, T., and Lührmann, R. (2004). The human 18S U11/U12 snRNP contains a set of novel proteins not found in the U2-dependent spliceosome. RNA10, 929–941.10.1261/rna.7320604Search in Google Scholar PubMed PubMed Central

Wu, Q. and Krainer, A.R. (1996). U1-mediated exon definition interactions between AT-AC and GT-AG introns. Science274, 1005–1008.10.1126/science.274.5289.1005Search in Google Scholar PubMed

Wu, Q. and Krainer, A.R. (1997). Splicing of a divergent subclass of AT-AC introns requires the major spliceosomal snRNAs. RNA3, 586–601.Search in Google Scholar

Wu, Q. and Krainer, A.R. (1998). Purine-rich enhancers function in the AT-AC pre-mRNA splicing pathway and do so independently of intact U1 snRNP. RNA4, 1664–1673.10.1017/S1355838298981432Search in Google Scholar PubMed PubMed Central

Wu, Q. and Krainer, A.R. (1999). AT-AC pre-mRNA splicing mechanisms and conservation of minor introns in voltage-gated ion channel genes. Mol. Cell. Biol.19, 3225–3236.10.1128/MCB.19.5.3225Search in Google Scholar PubMed PubMed Central

Wu, S., Romfo, C.M., Nilsen, T.W., and Green, M.R. (1999). Functional recognition of the 3′ splice site AG by the splicing factor U2AF35. Nature402, 832–835.10.1038/45590Search in Google Scholar PubMed

Xu, Y.Z., Newnham, C.M., Kameoka, S., Huang, T., Konarska, M.M., and Query, C.C. (2004). Prp5 bridges U1 and U2 snRNPs and enables stable U2 snRNP association with intron RNA. EMBO J.23, 376–385.10.1038/sj.emboj.7600050Search in Google Scholar PubMed PubMed Central

Yean, S.L., Wuenschell, G., Termini, J., and Lin, R.J. (2000). Metal-ion coordination by U6 small nuclear RNA contributes to catalysis in the spliceosome. Nature408, 881–884.10.1038/35048617Search in Google Scholar PubMed PubMed Central

Yu, Y.T. and Steitz, J.A. (1997). Site-specific crosslinking of mammalian U11 and U6atac to the 5′ splice site of an AT-AC intron. Proc. Natl. Acad. Sci. USA94, 6030–6035.10.1073/pnas.94.12.6030Search in Google Scholar PubMed PubMed Central

Yu, Y.T., Shu, M.D., and Steitz, J.A. (1998). Modifications of U2 snRNA are required for snRNP assembly and pre-mRNA splicing. EMBO J.17, 5783–5795.10.1093/emboj/17.19.5783Search in Google Scholar PubMed PubMed Central

Yu, Y.-T., Scharl, E.C., Smith, C.M., and Steitz, J.A. (1999). The Growing World of Small Nuclear Ribonucleoproteins. In: The RNA World, 2nd edition, R.F. Gesteland, T.R. Cech, and J.F. Atkins, eds. (Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press), pp. 487–524.Search in Google Scholar

Zhou, Z., Licklider, L.J., Gygi, S.P., and Reed, R. (2002). Comprehensive proteomic analysis of the human spliceosome. Nature419, 182–185.10.1038/nature01031Search in Google Scholar PubMed