Functional Characterization of Nuclear Localization Signals in Yeast Sm Proteins

REFERENCES

• 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
   PubMed Web of Science ®Google Scholar
• Blum, S., Mueller, M., Schmid, S. R., Linder, P., and Trachsel, H.. 1989. Translation in Saccharomyces cerevisiae: initiation factor 4A-dependent cell-free system. Proc. Natl. Acad. Sci. USA 86:6043–6046
   PubMed Web of Science ®Google Scholar
• Bordonné, R., Banroques, J., Abelson, J., and Guthrie, C.. 1990. Domains of yeast U4 spliceosomal RNA required for PRP4 protein binding, snRNP-snRNP interactions, and pre-mRNA splicing in vivo. Genes Dev. 4:1185–1196
   PubMedGoogle Scholar
• Bordonné, R., and Tarassov, I.. 1996. The yeast SME1 gene encodes the homologue of the human E core protein. Gene 176:111–117
   PubMedGoogle Scholar
• Camasses, A., Bragado-Nilsson, E., Martin, R., Séraphin, B., and Bordonné, R.. 1998. Interactions within the yeast Sm core complex: from proteins to amino acids. Mol. Cell. Biol. 18:1956–1966
   PubMedGoogle Scholar
• Carvalho, T., Almeida, F., Calapez, A., Lafarga, M., Berciano, M. T., and Carmo-Fonseca, M.. 1999. The spinal muscular atrophy disease gene product, SMN: a link between snRNP biogenesis and the Cajal (coiled) body. J. Cell Biol. 147:715–728
   PubMed Web of Science ®Google Scholar
• 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
   PubMedGoogle Scholar
• Dingwall, C., and Laskey, R. A.. 1991. Nuclear targeting sequences—a consensus? Trends Biochem. Sci. 16:478–481
   PubMed Web of Science ®Google Scholar
• Filali, M., Qiu, J., Awasthi, S., Fischer, U., Monos, D., and Kamoun, M.. 1999. Monoclonal antibody specific to a subclass of polyproline-Arg motif provides evidence for the presence of an snRNA-free spliceosomal Sm protein complex in vivo: implications for molecular interactions involving proline-rich sequences of Sm B/B′ proteins. J. Cell. Biochem. 74:168–180
   PubMedGoogle Scholar
• Fink, G. R., and Guthrie, C.. 1991. Guide to yeast genetics and molecular biology. Methods Enzymol. 194:3–21
   PubMedGoogle Scholar
• Fischer, U., and Lührmann, R.. 1990. An essential signaling role for the m3G cap in the transport of U1 snRNP to the nucleus. Science 249:786–790
   PubMed Web of Science ®Google Scholar
• Fischer, U., Darzynkiewicz, E., Tahara, S. M., Dathan, N. A., Lührmann, R., and Mattaj, I. W.. 1991. Diversity in the signals required for nuclear accumulation of U snRNPs and variety in the pathways of nuclear transport. J. Cell Biol. 113:705–714
   PubMedGoogle Scholar
• Fischer, U., Sumpter, V., Sekine, M., Satoh, T., and Lührmann, R.. 1993. Nucleo-cytoplasmic transport of U snRNPs: definition of a nuclear location signal in the Sm core domain that binds a transport receptor independently of the m3G cap. EMBO J. 12:573–583
   PubMed Web of Science ®Google Scholar
• Fischer, U., Heinrich, J., van Zee, K., Fanning, E., and Lührmann, R.. 1994. Nuclear transport of U1 snRNP in somatic cells: differences in signal requirement compared with Xenopus laevis oocytes. J. Cell Biol. 125:971–980
   PubMedGoogle Scholar
• Fischer, U., Liu, Q., and Dreyfuss, G.. 1997. The SMN-SIP1 complex has an essential role in spliceosomal snRNP biogenesis. Cell 90:1023–1029
   PubMed Web of Science ®Google Scholar
• Fromont-Racine, M., Rain, J. C., and Legrain, P.. 1997. Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens. Nat. Genet. 16:277–282
   PubMed Web of Science ®Google Scholar
• Fury, M. G., Zhang, W., Christodoulopoulos, I., and Zieve, G. W.. 1997. Multiple protein:protein interactions between the snRNP common core proteins. Exp. Cell Res. 237:63–69
   PubMedGoogle Scholar
• Gottschalk, A., Tang, J., Puig, O., Salgado, J., Neubauer, G., Colot, H. V., Mann, M., Séraphin, B., Rosbash, M., Lührmann, R., and Fabrizio, P.. 1998. A comprehensive biochemical and genetic analysis of the yeast U1 snRNP reveals five novel proteins. RNA 4:374–393
   PubMed Web of Science ®Google Scholar
• Gottschalk, A., Neubauer, G., Banroques, J., Mann, M., Lührmann, R., and Fabrizio, P.. 1999. Identification by mass spectrometry and functional analysis of novel proteins of the yeast [U4/U6.U5] tri-snRNP. EMBO J. 18:4535–4548
   PubMed Web of Science ®Google Scholar
• Hamm, J., Darzynkiewicz, E., Tahara, S. M., and Mattaj, I. W.. 1990. The trimethylguanosine cap structure of U1 snRNA is a component of a bipartite nuclear targeting signal. Cell 62:569–577
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Hill, J., Donald, K. A., Griffiths, D. E., and Donald, G. D.. 1991. DMSO-enhanced whole cell yeast transformation. Nucleic Acids Res. 19:5791
   PubMed Web of Science ®Google Scholar
• Huber, J., Cronshagen, U., Kadokura, M., Marshallsay, C., Wada, T., Sekine, M., and Lührmann, R.. 1998. Snurportin1, an m3G-cap-specific nuclear import receptor with a novel domain structure. EMBO J. 17:4114–4126
   PubMed Web of Science ®Google Scholar
• Izaurralde, E., Jarmolowski, A., Beisel, C., Mattaj, I. W., Dreyfuss, G., and Fischer, U.. 1997. A role for the M9 transport signal of hnRNP A1 in mRNA nuclear export. J. Cell Biol. 137:27–35
   PubMedGoogle Scholar
• Jäkel, S., and Görlich, D.. 1998. Importin β, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J. 17:4491–4502
   PubMed Web of Science ®Google Scholar
• Kambach, C., Walke, S., Young, R., Avis, J. M., de la Fortelle, E., Raker, V. A., Lührmann, R., Li, J., and Nagai, K.. 1999. Crystal structures of two Sm protein complexes and their implications for the assembly of the spliceosomal snRNPs. Cell 96:375–387
   PubMed Web of Science ®Google Scholar
• Krämer, A.. 1996. The structure and function of proteins involved in mammalian pre-mRNA splicing. Annu. Rev. Biochem. 65:367–409
   PubMed Web of Science ®Google Scholar
• Laemmli, U. K.. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
   PubMed Web of Science ®Google Scholar
• Lafontaine, D., and Tollervey, D.. 1996. One-step PCR mediated strategy for the construction of conditionally expressed and epitope tagged yeast proteins. Nucleic Acids Res. 24:3469–3472
   PubMedGoogle Scholar
• Lamond, A. I., and Carmo-Fonseca, M.. 1993. Localisation of splicing snRNPs in mammalian cells. Mol. Biol. Rep. 18:127–133
   PubMedGoogle Scholar
• Lee, M. S., Henry, M., and Silver, P. A.. 1996. A protein that shuttles between the nucleus and the cytoplasm is an important mediator of RNA export. Genes Dev. 10:1233–1246
   PubMed Web of Science ®Google Scholar
• Lehmeier, T., Raker, V., Hermann, H., and Lührmann, R.. 1994. cDNA cloning of the Sm proteins D2 and D3 from human small nuclear ribonucleoproteins: evidence for a direct D1-D2 interaction. Proc. Natl. Acad. Sci. USA 91:12317–12321
   PubMedGoogle Scholar
• Liu, Q., Fischer, U., Wang, F., and Dreyfuss, G.. 1997. The spinal muscular atrophy disease gene product, SMN, and its associated protein SIP1 are in a complex with spliceosomal snRNP proteins. Cell 90:1013–1021
   PubMed Web of Science ®Google Scholar
• Lührmann, R., Kastner, B., and Bach, M.. 1990. Structure of spliceosomal snRNPs and their role in pre-mRNA splicing. Biochim. Biophys. Acta 1087:256–292
   PubMedGoogle Scholar
• Mattaj, I. W.. 1986. Cap trimethylation of U snRNA is cytoplasmic and dependent on U snRNP protein binding. Cell 46:905–911
   PubMed Web of Science ®Google Scholar
• Mattaj, I. W.. 1988. U snRNP assembly and transport Structure and function of the major and minor small nuclear ribonucleoprotein particles. Birnstiel, M. L. 303–357 Springer-Verlag, Berlin, Germany
   Google Scholar
• Mattaj, I. W.. 1998. Ribonucleoprotein assembly: clues from spinal muscular atrophy. Curr. Biol. 8:R93–R95
   PubMedGoogle Scholar
• Mattaj, I. W., and Englmeier, L.. 1998. Nucleocytoplasmic transport: the soluble phase. Annu. Rev. Biochem. 67:265–306
   PubMed Web of Science ®Google Scholar
• Mayes, A. E., Verdone, L., Legrain, P., and Beggs, J. D.. 1999. Characterization of Sm-like proteins in yeast and their association with U6 snRNA. EMBO J. 18:4321–4331
   PubMed Web of Science ®Google Scholar
• Michaud, N., and Goldfarb, D.. 1992. Microinjected U snRNAs are imported to oocyte nuclei via the nuclear pore complex by three distinguishable targeting pathways. J. Cell Biol. 116:851–861
   PubMedGoogle Scholar
• Mumberg, D., Muller, R., and Funk, M.. 1994. Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res. 22:5767–5768
   PubMed Web of Science ®Google Scholar
• Nelissen, R. L., Will, C. L., van Venrooij, W. J., and Lührmann, R.. 1994. The association of the U1-specific 70K and C proteins with U1 snRNPs is mediated in part by common U snRNP proteins. EMBO J. 13:4113–4125
   PubMed Web of Science ®Google Scholar
• Niedenthal, R. K., Riles, L., Johnston, M., and Hegemann, J. H.. 1996. Green fluorescent protein as a marker for gene expression and subcellular localization in budding yeast. Yeast 12:773–786
   PubMed Web of Science ®Google Scholar
• Palacios, I., Hetzer, M., Adam, S. A., and Mattaj, I. W.. 1997. Nuclear import of U snRNPs requires importin β. EMBO J. 16:6783–6792
   PubMed Web of Science ®Google Scholar
• Pellizzoni, L., Charroux, B., and Dreyfuss, G.. 1999. SMN mutants of spinal muscular atrophy patients are defective in binding to snRNP proteins. Proc. Natl. Acad. Sci. USA 96:11167–11172
   PubMed Web of Science ®Google Scholar
• Plessel, G., Fischer, U., and Lührmann, R.. 1994. m3G cap hypermethylation of U1 small nuclear ribonucleoprotein (snRNP) in vitro: evidence that the U1 small nuclear RNA-(guanosine-N2)-methyltransferase is a non-snRNP cytoplasmic protein that requires a binding site on the Sm core domain. Mol. Cell. Biol. 14:4160–4172
   PubMed Web of Science ®Google Scholar
• Raker, V. A., Plessel, G., and Lührmann, R.. 1996. The snRNP core assembly pathway: identification of stable core protein heteromeric complexes and an snRNP subcore particle in vitro. EMBO J. 15:2256–2269
   PubMedGoogle Scholar
• Robbins, J., Dilworth, S. M., Laskey, R. A., and Dingwall, C.. 1991. Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 64:615–623
   PubMed Web of Science ®Google Scholar
• Rokeach, L. A., Haselby, J. A., and Hoch, S. O.. 1988. Molecular cloning of a cDNA encoding the human Sm-D autoantigen. Proc. Natl. Acad. Sci. USA 85:4832–4836
   PubMed Web of Science ®Google Scholar
• Rout, M. P., Blobel, G., and Aitchison, J. D.. 1997. A distinct nuclear import pathway used by ribosomal proteins. Cell 89:715–725
   PubMed Web of Science ®Google Scholar
• Roy, J., Zheng, B., Rymond, B. C., Woolford, J. L.Jr.. 1995. Structurally related but functionally distinct yeast Sm D core small nuclear ribonucleoprotein particle proteins. Mol. Cell. Biol. 15:445–455
   PubMedGoogle Scholar
• Russo, G., Ricciardelli, G., and Pietropaolo, C.. 1997. Different domains cooperate to target the human ribosomal L7a protein to the nucleus and to the nucleoli. J. Biol. Chem. 272:5229–5235
   PubMedGoogle Scholar
• Rymond, B. C.. 1993. Convergent transcripts of the yeast PRP38-SMD1 locus encode two essential splicing factors, including the D1 core polypeptide of small nuclear ribonucleoprotein particles. Proc. Natl. Acad. Sci. USA 90:848–852
   PubMedGoogle Scholar
• Rymond, B. C., Rokeach, L. A., and Hoch, S. O.. 1993. Human snRNP polypeptide D1 promotes pre-mRNA splicing in yeast and defines nonessential yeast Smd1p sequences. Nucleic Acids Res. 21:3501–3505
   PubMedGoogle Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Sambrook, J., Fritsch, E. F., and Maniatis, T.. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y
   Google Scholar
• Sauterer, R. A., Goyal, A., and Zieve, G. W.. 1989. 1990. Cytoplasmic assembly of small nuclear ribonucleoprotein particles from 6 S and 20 S RNA-free intermediates in L929 mouse fibroblasts. J. Biol. Chem. 265:1048–1058
   Google Scholar
• Schägger, H., and von Jagow, G.. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368–379
   PubMed Web of Science ®Google Scholar
• Schlenstedt, G., Smirnova, E., Deane, R., Solsbacher, J., Kutay, U., Görlich, D., Ponstingl, H., and Bischoff, F. R.. 1997. Yrb4p, a yeast Ran-GTP-binding protein involved in import of ribosomal protein L25 into the nucleus. EMBO J. 16:6237–6249
   PubMed Web of Science ®Google Scholar
• Schmidt, C., Lipsius, E., and Kruppa, J.. 1995. Nuclear and nucleolar targeting of human ribosomal protein S6. Mol. Biol. Cell 6:1875–1885
   PubMedGoogle Scholar
• Séraphin, B., and Rosbash, M.. 1989. Identification of functional U1 snRNA-pre-mRNA complexes committed to spliceosome assembly and splicing. Cell 59:349–358
   PubMed Web of Science ®Google Scholar
• 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
   PubMedGoogle Scholar
• Séraphin, B., and Kandels-Lewis, S.. 1996. An efficient PCR mutagenesis strategy without gel purification [correction of purification] step that is amenable to automation. Nucleic Acids Res. 24:3276–3277
   PubMedGoogle Scholar
• Sikorski, R. S., and Hieter, P.. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19–27
   PubMed Web of Science ®Google Scholar
• Sleeman, J., Lyon, C. E., Platani, M., Kreivi, J. P., and Lamond, A. I.. 1998. Dynamic interactions between splicing snRNPs, coiled bodies and nucleoli revealed using snRNP protein fusions to the green fluorescent protein. Exp. Cell Res. 243:290–304
   PubMed Web of Science ®Google Scholar
• Spector, D. L.. 1993. Nuclear organization of pre-mRNA processing. Curr. Opin. Cell Biol. 5:442–447
   PubMedGoogle Scholar
• Staley, J. P., and Guthrie, C.. 1998. Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 92:315–326
   PubMed Web of Science ®Google Scholar
• Stevens, S. W., and Abelson, J.. 1999. Purification of the yeast U4/U6.U5 small nuclear ribonucleoprotein particle and identification of its proteins. Proc. Natl. Acad. Sci. USA 96:7226–7231
   PubMedGoogle Scholar
• van Dam, A., Winkel, I., Zijlstra-Baalbergen, J., Smeenk, R., and Cuypers, H. T.. 1989. Cloned human snRNP proteins B and B′ differ only in their carboxy-terminal part. EMBO J. 8:3853–3860
   PubMedGoogle Scholar
• Wach, A., Brachat, A., Pohlmann, R., and Philippsen, P.. 1994. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10:1793–1808
   PubMed Web of Science ®Google Scholar
• Zhang, D., and Rosbash, M.. 1999. Identification of eight proteins that cross-link to pre-mRNA in the yeast commitment complex. Genes Dev. 13:581–592
   PubMed Web of Science ®Google Scholar
• Zieve, G. W.. 1999. The cytoplasmic sites of the snRNP protein complexes are punctate structures that are responsive to changes in metabolism and intracellular architecture. Exp. Cell Res. 247:249–256
   PubMedGoogle Scholar