Splicing Functions and Global Dependency on Fission Yeast Slu7 Reveal Diversity in Spliceosome Assembly

REFERENCES

• Burge CB, Tuschl TH, Sharp PA. 1999. Splicing of precursors to mRNAs by the spliceosome, p 525–560.InGesteland RF, Cech TR, Atkins JF (ed),RNA World II. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
   Google Scholar
• Deutsch M, Long M. 1999. Intron-exon structures of eukaryotic model organisms. Nucleic Acids Res. 27:3219–3228.
   PubMed Web of Science ®Google Scholar
• Lim LP, Burge CB. 2001. A computational analysis of sequence features involved in recognition of short introns. Proc. Natl. Acad. Sci. U. S. A. 98:11193–11198.
   PubMed Web of Science ®Google Scholar
• Romfo CM, Alvarez CJ, van Heeckeren WJ, Webb CJ, Wise JA. 2000. Evidence for splice site pairing via intron definition in Schizosaccharomyces pombe. Mol. Cell. Biol. 20:7955–7970.
   PubMed Web of Science ®Google Scholar
• Kupfer DM, Drabenstot SD, Buchanan KL, Lai H, Zhu H, Dyer DW, Roe BA, Murphy JW. 2004. Introns and splicing elements of five diverse fungi. Eukaryot. Cell 3:1088–1100.
   PubMedGoogle Scholar
• Vijayraghavan U, Abelson J. 1990. PRP18, a protein required for the second reaction in pre-mRNA splicing. Mol. Cell. Biol. 10:324–332.
   PubMedGoogle Scholar
• Horowitz DS, Abelson J. 1993. A U5 small nuclear ribonucleoprotein particle protein involved only in the second step of pre-mRNA splicing in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:2959–2970.
   PubMedGoogle Scholar
• Ansari A, Schwer B. 1995. SLU7 and a novel activity, SSF1, act during the PRP16-dependent step of yeast pre-mRNA splicing. EMBO J. 14:4001–4009.
   PubMedGoogle Scholar
• Schwer B, Gross CH. 1998. Prp22, a DExH-box RNA helicase, plays two distinct roles in yeast pre-mRNA splicing. EMBO J. 17:2086–2094.
   PubMed Web of Science ®Google Scholar
• Umen JG, Guthrie C. 1995. The second catalytic step of pre-mRNA splicing. RNA 1:869–885.
   PubMed Web of Science ®Google Scholar
• Grainger RJ, Beggs JD. 2005. Prp8 protein: at the heart of the spliceosome. RNA 11:533–557.
   PubMed Web of Science ®Google Scholar
• Brys A, Schwer B. 1996. Requirement for SLU7 in yeast pre-mRNA splicing is dictated by the distance between the branchpoint and the 3′ splice site. RNA 2:707–717.
   PubMedGoogle Scholar
• Frank D, Patterson B, Guthrie C. 1992. Synthetic lethal mutations suggest interactions between U5 small nuclear RNA and four proteins required for the second step of splicing. Mol. Cell. Biol. 12:5197–5205.
   PubMed Web of Science ®Google Scholar
• Frank D, Guthrie C. 1992. An essential splicing factor, SLU7, mediates 3′ splice site choice in yeast. Genes Dev. 6:2112–2124.
   PubMedGoogle Scholar
• Zhang X, Schwer B. 1997. Functional and physical interaction between the yeast splicing factors Slu7 and Prp18. Nucleic Acids Res. 25:2146–2152.
   PubMedGoogle Scholar
• James SA, Turner W, Schwer B. 2002. How Slu7 and Prp18 cooperate in the second step of yeast pre-mRNA splicing. RNA 8:1068–1077.
   PubMedGoogle Scholar
• Aronova A, Bacikova D, Crotti LB, Horowitz DS, Schwer B. 2007. Functional interactions between Prp8, Prp18, Slu7, and U5 snRNA during the second step of pre-mRNA splicing. RNA 13:1437–1444.
   PubMed Web of Science ®Google Scholar
• Chua K, Reed R. 1999. The RNA splicing factor hSlu7 is required for correct 3′ splice-site choice. Nature 402:207–210.
   PubMed Web of Science ®Google Scholar
• Chua K, Reed R. 1999. Human step II splicing factor hSlu7 functions in restructuring the spliceosome between the catalytic steps of splicing. Genes Dev. 13:841–850.
   PubMedGoogle Scholar
• Shomron N, Alberstein M, Reznik M, Ast G. 2005. Stress alters the subcellular distribution of hSlu7 and thus modulates alternative splicing. J. Cell Sci. 118:1151–1159.
   PubMed Web of Science ®Google Scholar
• Zhou Z, Reed R. 1998. Human homologs of yeast prp16 and prp17 reveal conservation of the mechanism for catalytic step II of pre-mRNA splicing. EMBO J. 17:2095–2106.
   PubMedGoogle Scholar
• Horowitz DS, Krainer AR. 1997. A human protein required for the second step of pre-mRNA splicing is functionally related to a yeast splicing factor. Genes Dev. 11:139–151.
   PubMedGoogle Scholar
• Kaufer NF, Potashkin J. 2000. Analysis of the splicing machinery in fission yeast: a comparison with budding yeast and mammals. Nucleic Acids Res. 28:3003–3010.
   PubMed Web of Science ®Google Scholar
• Kuhn AN, Kaufer NF. 2003. Pre-mRNA splicing in Schizosaccharomyces pombe: regulatory role of a kinase conserved from fission yeast to mammals. Curr. Genet. 42:241–251.
   PubMed Web of Science ®Google Scholar
• Newo AN, Lutzelberger M, Bottner CA, Wehland J, Wissing J, Jansch L, Kaufer NF. 2007. Proteomic analysis of the U1 snRNP of Schizosaccharomyces pombe reveals three essential organism-specific proteins. Nucleic Acids Res. 35:1391–1401.
   PubMedGoogle Scholar
• Ohi MD, Link AJ, Ren L, Jennings JL, McDonald WH, Gould KL. 2002. Proteomics analysis reveals stable multiprotein complexes in both fission and budding yeasts containing Myb-related Cdc5p/Cef1p, novel pre-mRNA splicing factors, and snRNAs. Mol. Cell. Biol. 22:2011–2024.
   PubMed Web of Science ®Google Scholar
• Ohi MD, Ren L, Wall JS, Gould KL, Walz T. 2007. Structural characterization of the fission yeast U5.U2/U6 spliceosome complex. Proc. Natl. Acad. Sci. U. S. A. 104:3195–3200.
   PubMedGoogle Scholar
• Huang T, Vilardell J, Query CC. 2002. Pre-spliceosome formation in S. pombe requires a stable complex of SF1-U2AF59-U2AF23. EMBO J. 21:5516–5526.
   PubMedGoogle Scholar
• Potashkin J, Li R, Frendewey D. 1989. Pre-mRNA splicing mutants of Schizosaccharomyces pombe. EMBO J. 8:551–559.
   PubMedGoogle Scholar
• Habara Y, Urushiyama S, Tani T, Ohshima Y. 1998. The fission yeast prp10+ gene involved in pre-mRNA splicing encodes a homologue of highly conserved splicing factor, SAP155. Nucleic Acids Res. 26:5662–5669.
   PubMed Web of Science ®Google Scholar
• Romfo CM, Lakhe-Reddy S, Wise JA. 1999. Molecular genetic analysis of U2AF59 in Schizosaccharomyces pombe: differential sensitivity of introns to mutational inactivation. RNA 5:49–65.
   PubMedGoogle Scholar
• Habara Y, Urushiyama S, Shibuya T, Ohshima Y, Tani T. 2001. Mutation in the prp12+ gene encoding a homolog of SAP130/SF3b130 causes differential inhibition of pre-mRNA splicing and arrest of cell-cycle progression in Schizosaccharomyces pombe. RNA 7:671–681.
   PubMed Web of Science ®Google Scholar
• Bottner CA, Schmidt H, Vogel S, Michele M, Kaufer NF. 2005. Multiple genetic and biochemical interactions of Brr2, Prp8, Prp31, Prp1 and Prp4 kinase suggest a function in the control of the activation of spliceosomes in Schizosaccharomyces pombe. Curr. Genet. 48:151–161.
   PubMedGoogle Scholar
• Sridharan V, Heimiller J, Singh R. 2011. Genomic mRNA profiling reveals compensatory mechanisms for the requirement of the essential splicing factor U2AF. Mol. Cell. Biol. 31:652–661.
   PubMed Web of Science ®Google Scholar
• Sridharan V, Singh R. 2007. A conditional role of U2AF in splicing of introns with unconventional polypyrimidine tracts. Mol. Cell. Biol. 27:7334–7344.
   PubMedGoogle Scholar
• Sapra AK, Arava Y, Khandelia P, Vijayraghavan U. 2004. Genome-wide analysis of pre-mRNA splicing: intron features govern the requirement for the second-step factor, Prp17 in Saccharomyces cerevisiae and Schizosaccharomyces pombe. J. Biol. Chem. 279:52437–52446.
   PubMedGoogle Scholar
• Moreno S, Klar A, Nurse P. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:795–823.
   PubMed Web of Science ®Google Scholar
• Sato M, Dhut S, Toda T. 2005. New drug-resistant cassettes for gene disruption and epitope tagging in Schizosaccharomyces pombe. Yeast 22:583–591.
   PubMed Web of Science ®Google Scholar
• Spirek M, Benko Z, Carnecka M, Rumpf C, Cipak L, Batova M, Marova I, Nam M, Kim DU, Park HO, Hayles J, Hoe KL, Nurse P, Gregan J. 2010. S. pombe genome deletion project: an update. Cell Cycle 9:2399–2402.
   PubMed Web of Science ®Google Scholar
• Shomron N, Reznik M, Ast G. 2004. Splicing factor hSlu7 contains a unique functional domain required to retain the protein within the nucleus. Mol. Biol. Cell 15:3782–3795.
   PubMedGoogle Scholar
• Varadarajan R, Nagarajaram HA, Ramakrishnan C. 1996. A procedure for the prediction of temperature-sensitive mutants of a globular protein based solely on the amino acid sequence. Proc. Natl. Acad. Sci. U. S. A. 93:13908–13913.
   PubMed Web of Science ®Google Scholar
• Potashkin J, Naik K, Wentz-Hunter K. 1993. U2AF homolog required for splicing in vivo. Science 262:573–575.
   PubMedGoogle Scholar
• Clark TA, Sugnet CW, Ares MJr. 2002. Genomewide analysis of mRNA processing in yeast using splicing-specific microarrays. Science 296:907–910.
   PubMedGoogle Scholar
• Pleiss JA, Whitworth GB, Bergkessel M, Guthrie C. 2007. Rapid, transcript-specific changes in splicing in response to environmental stress. Mol. Cell 27:928–937.
   PubMed Web of Science ®Google Scholar
• Pleiss JA, Whitworth GB, Bergkessel M, Guthrie C. 2007. Transcript specificity in yeast pre-mRNA splicing revealed by mutations in core spliceosomal components. PLoS Biol. 5(4):e90. doi:10.1371/journal.pbio.0050090.
   PubMedGoogle Scholar
• Nam K, Lee G, Trambley J, Devine SE, Boeke JD. 1997. Severe growth defect in a Schizosaccharomyces pombe mutant defective in intron lariat degradation. Mol. Cell. Biol. 17:809–818.
   PubMedGoogle Scholar
• Wilhelm BT, Marguerat S, Watt S, Schubert F, Wood V, Goodhead I, Penkett CJ, Rogers J, Bahler J. 2008. Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 453:1239–1243.
   PubMed Web of Science ®Google Scholar
• Seshadri V, Vaidya Vijayraghavan VCU. 1996. Genetic studies of the PRP17 gene of Saccharomyces cerevisiae: a domain essential for function maps to a nonconserved region of the protein. Genetics 143:45–55.
   PubMedGoogle Scholar
• Xu D, Field DJ, Tang SJ, Moris A, Bobechko BP, Friesen JD. 1998. Synthetic lethality of yeast slt mutations with U2 small nuclear RNA mutations suggests functional interactions between U2 and U5 snRNPs that are important for both steps of pre-mRNA splicing. Mol. Cell. Biol. 18:2055–2066.
   PubMed Web of Science ®Google Scholar
• Urushiyama S, Tani T, Ohshima Y. 1997. The prp1+ gene required for pre-mRNA splicing in Schizosaccharomyces pombe encodes a protein that contains TPR motifs and is similar to Prp6p of budding yeast. Genetics 147:101–115.
   PubMedGoogle Scholar
• Alberstein M, Amit M, Vaknin K, O'Donnell A, Farhy C, Lerenthal Y, Shomron N, Shaham O, Sharrocks AD, Ashery-Padan R, Ast G. 2007. Regulation of transcription of the RNA splicing factor hSlu7 by Elk-1 and Sp1 affects alternative splicing. RNA 13:1988–1999.
   PubMedGoogle Scholar
• Albulescu LO, Sabet N, Gudipati M, Stepankiw N, Bergman ZJ, Huffaker TC, Pleiss JA. 2012. A quantitative, high-throughput reverse genetic screen reveals novel connections between pre-mRNA splicing and 5′ and 3′ end transcript determinants. PLoS Genet. 8(3):e1002530. doi:10.1371/journal.pgen.1002530.
   PubMedGoogle Scholar
• Rhind N, Chen Z, Yassour M, Thompson DA, Haas BJ, Habib N, Wapinski I, Roy S, Lin MF, Heiman DI, Young SK, Furuya K, Guo Y, Pidoux A, Chen HM, Robbertse B, Goldberg JM, Aoki K, Bayne EH, Berlin AM, Desjardins CA, Dobbs E, Dukaj L, Fan L, FitzGerald MG, French C, Gujja S, Hansen K, Keifenheim D, Levin JZ, Mosher RA, MullerCAPfiffner Priest JM, Russ C, Smialowska A, Swoboda P, Sykes SM, Vaughn M, Vengrova S, Yoder R, Zeng Q, Allshire R, Baulcombe D, Birren BW, Brown W, Ekwall K, Kellis M, Leatherwood J, Levin H, Margalit H, Martienssen R, Nieduszynski CA, Spatafora JW, Friedman N, Dalgaard JZ, Baumann P, Niki H, Regev A, Nusbaum C. 2011. Comparative functional genomics of the fission yeasts. Science 332:930–936.
   PubMed Web of Science ®Google Scholar
• Reich CI, VanHoy RW, Porter GL, Wise JA. 1992. Mutations at the 3′ splice site can be suppressed by compensatory base changes in U1 snRNA in fission yeast. Cell 69:1159–1169.
   PubMedGoogle Scholar
• Goodall GJ, Filipowicz W. 1989. The AU-rich sequences present in the introns of plant nuclear pre-mRNAs are required for splicing. Cell 58:473–483.
   PubMedGoogle Scholar
• Conrad R, Lea K, Blumenthal T. 1995. SL1 trans-splicing specified by AU-rich synthetic RNA inserted at the 5′ end of Caenorhabditis elegans pre-mRNA. RNA 1:164–170.
   PubMedGoogle Scholar
• Csank C, Taylor FM, Martindale DW. 1990. Nuclear pre-mRNA introns: analysis and comparison of intron sequences from Tetrahymena thermophila and other eukaryotes. Nucleic Acids Res. 18:5133–5141.
   PubMed Web of Science ®Google Scholar
• McCullough AJ, Schuler MA. 1993. AU-rich intronic elements affect pre-mRNA 5′ splice site selection in Drosophila melanogaster. Mol. Cell. Biol. 13:7689–7697.
   PubMedGoogle Scholar
• Lutzelberger M, Bottner CA, Schwelnus W, Zock-Emmenthal S, Razanau A, Kaufer NF. 2010. The N-terminus of Prp1 (Prp6/U5-102 K) is essential for spliceosome activation in vivo. Nucleic Acids Res. 38:1610–1622.
   PubMedGoogle Scholar
• Makarova OV, Makarov EM, Urlaub H, Will CL, Gentzel M, Wilm M, LŸhrmann R. 2004. A subset of human 35S U5 proteins, including Prp19, function prior to catalytic step 1 of splicing. EMBO J. 23:2381–2391.
   PubMed Web of Science ®Google Scholar
• Ryan CJ, Roguev A, Patrick K, Xu J, Jahari H, Tong Z, Beltrao P, Shales M, Qu H, Collins SR, Kliegman JI, Jiang L, Kuo D, Tosti E, Kim HS, Edelmann W, Keogh MC, Greene D, Tang C, Cunningham P, Shokat KM, Cagney G, Svensson JP, Guthrie C, Espenshade PJ, Ideker T, Krogan NJ. 2012. Hierarchical modularity and the evolution of genetic interactomes across species. Mol. Cell 46:691–704.
   PubMed Web of Science ®Google Scholar
• Smith DJ, Query CC, Konarska MM. 2008. “Nought may endure but mutability”: spliceosome dynamics and the regulation of splicing. Mol. Cell 30:657–666.
   PubMed Web of Science ®Google Scholar
• Stevens SW, Ryan DE, Ge HY, Moore RE, Young MK, Lee TD, Abelson J. 2002. Composition and functional characterization of the yeast spliceosomal penta-snRNP. Mol. Cell 9:31–44.
   PubMed Web of Science ®Google Scholar
• Abelson J, Blanco M, Ditzler MA, Fuller F, Aravamudhan P, Wood M, Villa T, Ryan DE, Pleiss JA, Maeder C, Guthrie C, Walter NG. 2010. Conformational dynamics of single pre-mRNA molecules during in vitro splicing. Nat. Struct. Mol. Biol. 17:504–512.
   PubMedGoogle Scholar
• Maroney PA, Romfo CM, Nilsen TW. 2000. Functional recognition of 5′ splice site by U4/U6.U5 tri-snRNP defines a novel ATP-dependent step in early spliceosome assembly. Mol. Cell 6:317–328.
   PubMed Web of Science ®Google Scholar