Rapid screening of yeast mutants with reporters identifies new splicing phenotypes

FEBS Journal

Volumn 280, Issue 11, 2013, Pages 2712-2726

  Dreumont, Natacha ^a,b   Séraphin, Bertrand ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSERM   (France)

Author keywords

pre mRNA; Prp mutants; reporters; Saccharomyces cerevisiae; spliceosome

Indexed keywords

FUNGAL PROTEIN; FUNGAL RNA; MESSENGER RNA PRECURSOR; MUTANT PROTEIN; PRP8 PROTEIN; UNCLASSIFIED DRUG; URN1 PROTEIN;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; FUNGAL GENE; FUNGAL STRAIN; FUNGAL VIABILITY; FUNGUS MUTANT; GENE EXPRESSION REGULATION; GENE MUTATION; GENETIC SCREENING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROLINE RICH PROTEIN DOMAIN; PROTEIN EXPRESSION; REPORTER GENE; RNA SEQUENCE; SENSITIVITY ANALYSIS; SPLICEOSOME; YEAST;

AMINO ACID SEQUENCE; BASE SEQUENCE; GENES, REPORTER; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; RIBONUCLEOPROTEIN, U4-U6 SMALL NUCLEAR; RIBONUCLEOPROTEIN, U5 SMALL NUCLEAR; RNA SPLICE SITES; RNA SPLICING; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPLICEOSOMES;

EID: 84878222925     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12277     Document Type: Article

References (92)

1. Newman AJ, &, Nagai K, (2010) Structural studies of the spliceosome: blind men and an elephant. Curr Opin Struct Biol 20, 82-89.
2. Wahl MC, Will CL, &, Luhrmann R, (2009) The spliceosome: design principles of a dynamic RNP machine. Cell 136, 701-718.
3. Seraphin B, &, Rosbash M, (1991) The yeast branchpoint sequence is not required for the formation of a stable U1 snRNA-pre-mRNA complex and is recognized in the absence of U2 snRNA. EMBO J 10, 1209-1216.
4. Seraphin B, &, Rosbash M, (1989) Identification of functional U1 snRNA-pre-mRNA complexes committed to spliceosome assembly and splicing. Cell 59, 349-358.
5. Michaud S, &, Reed R, (1993) A functional association between the 5′ and 3′ splice site is established in the earliest prespliceosome complex (E) in mammals. Genes Dev 7, 1008-1020.
6. Berglund JA, Chua K, Abovich N, Reed R, &, Rosbash M, (1997) The splicing factor BBP interacts specifically with the pre-mRNA branchpoint sequence UACUAAC. Cell 89, 781-787.
7. 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.
8. Tardiff DF, Lacadie SA, &, Rosbash M, (2006) A genome-wide analysis indicates that yeast pre-mRNA splicing is predominantly posttranscriptional. Mol Cell 24, 917-929.
9. Huranova M, Ivani I, Benda A, Poser I, Brody Y, Hof M, Shav-Tal Y, Neugebauer KM, &, Stanek D, (2010) The differential interaction of snRNPs with pre-mRNA reveals splicing kinetics in living cells. J Cell Biol 191, 75-86.
10. Hoskins AA, Friedman LJ, Gallagher SS, Crawford DJ, Anderson EG, Wombacher R, Ramirez N, Cornish VW, Gelles J, &, Moore MJ, (2011) Ordered and dynamic assembly of single spliceosomes. Science 331, 1289-1295.
11. Kramer A, &, Utans U, (1991) Three protein factors (SF1, SF3 and U2AF) function in pre-splicing complex formation in addition to snRNPs. EMBO J 10, 1503-1509.
12. Rutz B, &, Seraphin B, (1999) Transient interaction of BBP/ScSF1 and Mud2 with the splicing machinery affects the kinetics of spliceosome assembly. RNA 5, 819-831.
13. Vijayraghavan U, Company M, &, Abelson J, (1989) Isolation and characterization of pre-mRNA splicing mutants of Saccharomyces cerevisiae. Genes Dev 3, 1206-1216.
14. Buchner DA, Trudeau M, &, Meisler MH, (2003) SCNM1, a putative RNA splicing factor that modifies disease severity in mice. Science 301, 967-969.
15. Decourty L, Saveanu C, Zemam K, Hantraye F, Frachon E, Rousselle JC, Fromont-Racine M, &, Jacquier A, (2008) Linking functionally related genes by sensitive and quantitative characterization of genetic interaction profiles. Proc Natl Acad Sci USA 105, 5821-5826.
16. Fabrizio P, Dannenberg J, Dube P, Kastner B, Stark H, Urlaub H, &, Luhrmann R, (2009) The evolutionarily conserved core design of the catalytic activation step of the yeast spliceosome. Mol Cell 36, 593-608.
17. Herold N, Will CL, Wolf E, Kastner B, Urlaub H, &, Luhrmann R, (2009) Conservation of the protein composition and electron microscopy structure of Drosophila melanogaster and human spliceosomal complexes. Mol Cell Biol 29, 281-301.
18. Bessonov S, Anokhina M, Krasauskas A, Golas MM, Sander B, Will CL, Urlaub H, Stark H, &, Luhrmann R, (2010) Characterization of purified human Bact spliceosomal complexes reveals compositional and morphological changes during spliceosome activation and first step catalysis. RNA 16, 2384-2403.
19. Chen YI, Moore RE, Ge HY, Young MK, Lee TD, &, Stevens SW, (2007) Proteomic analysis of in vivo-assembled pre-mRNA splicing complexes expands the catalog of participating factors. Nucleic Acids Res 35, 3928-3944.
20. Jurica MS, &, Moore MJ, (2003) Pre-mRNA splicing: awash in a sea of proteins. Mol Cell 12, 5-14.
21. Zhou Z, Licklider LJ, Gygi SP, &, Reed R, (2002) Comprehensive proteomic analysis of the human spliceosome. Nature 419, 182-185.
22. Qiu ZR, Schwer B, &, Shuman S, (2011) Determinants of Nam8-dependent splicing of meiotic pre-mRNAs. Nucleic Acids Res 39, 3427-3445.
23. Juneau K, Palm C, Miranda M, &, Davis RW, (2007) High-density yeast-tiling array reveals previously undiscovered introns and extensive regulation of meiotic splicing. Proc Natl Acad Sci USA 104, 1522-1527.
24. Davis CA, Grate L, Spingola M, &, Ares M Jr, (2000) Test of intron predictions reveals novel splice sites, alternatively spliced mRNAs and new introns in meiotically regulated genes of yeast. Nucleic Acids Res 28, 1700-1706.
25. Engebrecht JA, Voelkel-Meiman K, &, Roeder GS, (1991) Meiosis-specific RNA splicing in yeast. Cell 66, 1257-1268.
26. Munding EM, Igel AH, Shiue L, Dorighi KM, Trevino LR, &, Ares M Jr, (2010) Integration of a splicing regulatory network within the meiotic gene expression program of Saccharomyces cerevisiae. Genes Dev 24, 2693-2704.
27. Qiu ZR, Schwer B, &, Shuman S, (2011) Defining the Mer1 and Nam8 meiotic splicing regulons by cDNA rescue. RNA 17, 1648-1654.
28. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, &, Burge CB, (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456, 470-476.
29. Richardson DN, Rogers MF, Labadorf A, Ben-Hur A, Guo H, Paterson AH, &, Reddy AS, (2011) Comparative analysis of serine/arginine-rich proteins across 27 eukaryotes: insights into sub-family classification and extent of alternative splicing. PLoS One 6, e24542.
30. Puig O, Bragado-Nilsson E, Koski T, &, Seraphin B, (2007) The U1 snRNP-associated factor Luc7p affects 5′ splice site selection in yeast and human. Nucleic Acids Res 35, 5874-5885.
31. Forch P, Puig O, Kedersha N, Martinez C, Granneman S, Seraphin B, Anderson P, &, Valcarcel J, (2000) The apoptosis-promoting factor TIA-1 is a regulator of alternative pre-mRNA splicing. Mol Cell 6, 1089-1098.
32. Puig O, Gottschalk A, Fabrizio P, &, Seraphin B, (1999) Interaction of the U1 snRNP with nonconserved intronic sequences affects 5′ splice site selection. Genes Dev 13, 569-580.
33. Lopez PJ, &, Seraphin B, (1999) Genomic-scale quantitative analysis of yeast pre-mRNA splicing: implications for splice-site recognition. RNA 5, 1135-1137.
34. Ares M Jr, Grate L, &, Pauling MH, (1999) A handful of intron-containing genes produces the lion's share of yeast mRNA. RNA 5, 1138-1139.
35. 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.
36. Clark TA, Sugnet CW, &, Ares M Jr, (2002) Genomewide analysis of mRNA processing in yeast using splicing-specific microarrays. Science 296, 907-910.
37. Teem JL, &, Rosbash M, (1983) Expression of a beta-galactosidase gene containing the ribosomal protein 51 intron is sensitive to the rna2 mutation of yeast. Proc Natl Acad Sci USA 80, 4403-4407.
38. Jacquier A, Rodriguez JR, &, Rosbash M, (1985) A quantitative analysis of the effects of 5′ junction and TACTAAC box mutants and mutant combinations on yeast mRNA splicing. Cell 43, 423-430.
39. Goguel V, Liao XL, Rymond BC, &, Rosbash M, (1991) U1 snRNP can influence 3′-splice site selection as well as 5′-splice site selection. Genes Dev 5, 1430-1438.
40. Frank D, &, Guthrie C, (1992) An essential splicing factor, SLU7, mediates 3′ splice site choice in yeast. Genes Dev 6, 2112-2124.
41. Legrain P, &, Rosbash M, (1989) Some cis- and trans-acting mutants for splicing target pre-mRNA to the cytoplasm. Cell 57, 573-583.
42. Caspary F, &, Seraphin B, (1998) The yeast U2A'/U2B complex is required for pre-spliceosome formation. EMBO J 17, 6348-6358.
43. Liao XC, Tang J, &, Rosbash M, (1993) An enhancer screen identifies a gene that encodes the yeast U1 snRNP A protein: implications for snRNP protein function in pre-mRNA splicing. Genes Dev 7, 419-428.
44. Polycarpou-Schwarz M, Gunderson SI, Kandels-Lewis S, Seraphin B, &, Mattaj IW, (1996) Drosophila SNF/D25 combines the functions of the two snRNP proteins U1A and U2B' that are encoded separately in human, potato, and yeast. RNA 2, 11-23.
45. Tang J, &, Rosbash M, (1996) Characterization of yeast U1 snRNP A protein: identification of the N-terminal RNA binding domain (RBD) binding site and evidence that the C-terminal RBD functions in splicing. RNA 2, 1058-1070.
46. Tang J, Abovich N, &, Rosbash M, (1996) Identification and characterization of a yeast gene encoding the U2 small nuclear ribonucleoprotein particle B" protein. Mol Cell Biol 16, 2787-2795.
47. Gottschalk A, Neubauer G, Banroques J, Mann M, Luhrmann R, &, 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.
48. Stevens SW, &, 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.
49. Lybarger S, Beickman K, Brown V, Dembla-Rajpal N, Morey K, Seipelt R, &, Rymond BC, (1999) Elevated levels of a U4/U6.U5 snRNP-associated protein, Spp 381p, rescue a mutant defective in spliceosome maturation. Mol Cell Biol 19, 577-584.
50. Colot HV, Stutz F, &, Rosbash M, (1996) The yeast splicing factor Mud13p is a commitment complex component and corresponds to CBP20, the small subunit of the nuclear cap-binding complex. Genes Dev 10, 1699-1708.
51. Lewis JD, Gorlich D, &, Mattaj IW, (1996) A yeast cap binding protein complex (yCBC) acts at an early step in pre-mRNA splicing. Nucleic Acids Res 24, 3332-3336.
52. Chen CH, Tsai WY, Chen HR, Wang CH, &, Cheng SC, (2001) Identification and characterization of two novel components of the Prp19p-associated complex, Ntc30p and Ntc20p. J Biol Chem 276, 488-494.
53. Brooks MA, Dziembowski A, Quevillon-Cheruel S, Henriot V, Faux C, van Tilbeurgh H, &, Seraphin B, (2009) Structure of the yeast Pml1 splicing factor and its integration into the RES complex. Nucleic Acids Res 37, 129-143.
54. Dziembowski A, Ventura AP, Rutz B, Caspary F, Faux C, Halgand F, Laprevote O, &, Seraphin B, (2004) Proteomic analysis identifies a new complex required for nuclear pre-mRNA retention and splicing. EMBO J 23, 4847-4856.
55. Chen CH, Yu WC, Tsao TY, Wang LY, Chen HR, Lin JY, Tsai WY, &, Cheng SC, (2002) Functional and physical interactions between components of the Prp19p-associated complex. Nucleic Acids Res 30, 1029-1037.
56. Ohi MD, &, Gould KL, (2002) Characterization of interactions among the Cef1p-Prp19p-associated splicing complex. RNA 8, 798-815.
57. Xu D, &, Friesen JD, (2001) Splicing factor slt11p and its involvement in formation of U2/U6 helix II in activation of the yeast spliceosome. Mol Cell Biol 21, 1011-1023.
58. 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.
59. Ren L, McLean JR, Hazbun TR, Fields S, Vander Kooi C, Ohi MD, &, Gould KL, (2011) Systematic two-hybrid and comparative proteomic analyses reveal novel yeast pre-mRNA splicing factors connected to Prp19. PLoS One 6, e16719.
60. Fromont-Racine M, Rain JC, &, Legrain P, (1997) Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens. Nat Genet 16, 277-282.
61. Ash MR, Faelber K, Kosslick D, Albert GI, Roske Y, Kofler M, Schuemann M, Krause E, &, Freund C, (2010) Conserved beta-hairpin recognition by the GYF domains of Smy2 and GIGYF2 in mRNA surveillance and vesicular transport complexes. Structure 18, 944-954.
62. Nishizawa K, Freund C, Li J, Wagner G, &, Reinherz EL, (1998) Identification of a proline-binding motif regulating CD2-triggered T lymphocyte activation. Proc Natl Acad Sci USA 95, 14897-14902.
63. Wang Q, Zhang L, Lynn B, &, Rymond BC, (2008) A BBP-Mud2p heterodimer mediates branchpoint recognition and influences splicing substrate abundance in budding yeast. Nucleic Acids Res 36, 2787-2798.
64. Görnemann J, Barrandon C, Hujer K, Rutz B, Rigaut G, Kotovic KM, Faux C, Neugebauer KM, &, Séraphin B, (2011) Cotranscriptional spliceosome assembly and splicing are independent of the Prp40p WW domain. RNA 17, 2119-2129.
65. Abovich N, &, Rosbash M, (1997) Cross-intron bridging interactions in the yeast commitment complex are conserved in mammals. Cell 89, 403-412.
66. Abovich N, Liao XC, &, Rosbash M, (1994) The yeast MUD2 protein: an interaction with PRP11 defines a bridge between commitment complexes and U2 snRNP addition. Genes Dev 8, 843-854.
67. Gottschalk A, Tang J, Puig O, Salgado J, Neubauer G, Colot HV, Mann M, Seraphin B, Rosbash M, Luhrmann R, et al,. (1998) A comprehensive biochemical and genetic analysis of the yeast U1 snRNP reveals five novel proteins. RNA 4, 374-393.
68. Neubauer G, Gottschalk A, Fabrizio P, Seraphin B, Luhrmann R, &, Mann M, (1997) Identification of the proteins of the yeast U1 small nuclear ribonucleoprotein complex by mass spectrometry. Proc Natl Acad Sci USA 94, 385-390.
69. Rain JC, &, Legrain P, (1997) In vivo commitment to splicing in yeast involves the nucleotide upstream from the branch site conserved sequence and the Mud2 protein. EMBO J 16, 1759-1771.
70. Umen JG, &, Guthrie C, (1995) A novel role for a U5 snRNP protein in 3′ splice site selection. Genes Dev 9, 855-868.
71. Luukkonen BG, &, Seraphin B, (1997) The role of branchpoint-3′ splice site spacing and interaction between intron terminal nucleotides in 3′ splice site selection in Saccharomyces cerevisiae. EMBO J 16, 779-792.
72. Egecioglu DE, Kawashima TR, &, Chanfreau GF, (2011) Quality control of MATa1 splicing and exon skipping by nuclear RNA degradation. Nucleic Acids Res 40, 1787-1796.
73. He F, Peltz SW, Donahue JL, Rosbash M, &, Jacobson A, (1993) Stabilization and ribosome association of unspliced pre-mRNAs in a yeast upf1-mutant. Proc Natl Acad Sci USA 90, 7034-7038.
74. Rutz B, &, Seraphin B, (2000) A dual role for BBP/ScSF1 in nuclear pre-mRNA retention and splicing. EMBO J 19, 1873-1886.
75. Boon KL, Norman CM, Grainger RJ, Newman AJ, &, Beggs JD, (2006) Prp8p dissection reveals domain structure and protein interaction sites. RNA 12, 198-205.
76. Bouveret E, Rigaut G, Shevchenko A, Wilm M, &, Seraphin B, (2000) A Sm-like protein complex that participates in mRNA degradation. EMBO J 19, 1661-1671.
77. Fortes P, Bilbao-Cortes D, Fornerod M, Rigaut G, Raymond W, Seraphin B, &, Mattaj IW, (1999) Luc7p, a novel yeast U1 snRNP protein with a role in 5′ splice site recognition. Genes Dev 13, 2425-2438.
78. Brown JD, &, Beggs JD, (1992) Roles of PRP8 protein in the assembly of splicing complexes. EMBO J 11, 3721-3729.
79. Park JW, Parisky K, Celotto AM, Reenan RA, &, Graveley BR, (2004) Identification of alternative splicing regulators by RNA interference in Drosophila. Proc Natl Acad Sci USA 101, 15974-15979.
80. Mishra SK, Ammon T, Popowicz GM, Krajewski M, Nagel RJ, Ares M Jr, Holak TA, &, Jentsch S, (2011) Role of the ubiquitin-like protein Hub1 in splice-site usage and alternative splicing. Nature 474, 173-178.
81. Grainger RJ, &, Beggs JD, (2005) Prp8 protein: at the heart of the spliceosome. RNA 11, 533-557.
82. Pena V, Rozov A, Fabrizio P, Luhrmann R, &, Wahl MC, (2008) Structure and function of an RNase H domain at the heart of the spliceosome. EMBO J 27, 2929-2940.
83. Galej WP, Oubridge C, Newman AJ, &, Nagai K, (2013) Crystal structure of Prp8 reveals active site cavity of the spliceosome. Nature 493, 638-643.
84. Freund C, Schmalz HG, Sticht J, &, Kuhne R, (2008) Proline-rich sequence recognition domains (PRD): ligands, function and inhibition. Handb Exp Pharmacol 186, 407-429.
85. Bialkowska A, &, Kurlandzka A, (2002) Proteins interacting with Lin 1p, a putative link between chromosome segregation, mRNA splicing and DNA replication in Saccharomyces cerevisiae. Yeast 19, 1323-1333.
86. Janowicz A, Michalak M, &, Krebs J, (2011) Stress induced subcellular distribution of ALG-2, RBM22 and hSlu7. Biochim Biophys Acta 1813, 1045-1049.
87. Sanchez-Alvarez M, Montes M, Sanchez-Hernandez N, Hernandez-Munain C, &, Sune C, (2010) Differential effects of sumoylation on transcription and alternative splicing by transcription elongation regulator 1 (TCERG1). J Biol Chem 285, 15220-15233.
88. Seraphin B, Kretzner L, &, Rosbash M, (1988) A U1 snRNA:pre-mRNA base pairing interaction is required early in yeast spliceosome assembly but does not uniquely define the 5′ cleavage site. EMBO J 7, 2533-2538.
89. Rigaut G, Shevchenko A, Rutz B, Wilm M, Mann M, &, Seraphin B, (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 17, 1030-1032.
90. Lygerou Z, Mitchell P, Petfalski E, Seraphin B, &, Tollervey D, (1994) The POP1 gene encodes a protein component common to the RNase MRP and RNase P ribonucleoproteins. Genes Dev 8, 1423-1433.
91. Rose MD, &, Broach JR, (1991) Cloning genes by complementation in yeast. Methods Enzymol 194, 195-230.
92. Guarente L, Yocum RR, &, Gifford P, (1982) A GAL10-CYC1 hybrid yeast promoter identifies the GAL4 regulatory region as an upstream site. Proc Natl Acad Sci USA 79, 7410-7414.