Pre-mRNA splicing in Schizosaccharomyces pombe. Regulatory role of a kinase conserved from fission yeast to mammals

Current Genetics

Volumn 42, Issue 5, 2003, Pages 241-251

  Kuhn, Andreas N ^a   Käufer, Norbert F ^a  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

Pre mRNA splicing; Prp4p kinase; snRNPs; SR proteins

Indexed keywords

FUNGAL ENZYME; MESSENGER RNA; PROTEIN PRP4P KINASE; RIBONUCLEOPROTEIN; SMALL NUCLEAR RNA; UNCLASSIFIED DRUG;

ACCURACY; DNA FLANKING REGION; EXON; FUNGAL GENETICS; GENE SEQUENCE; GENETIC CONSERVATION; INTRON; MAMMAL; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; RNA SEQUENCE; RNA SPLICING; RNA TRANSCRIPTION; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE; SPLICEOSOME;

EUKARYOTA; MAMMALIA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE;

EID: 0037296419     PISSN: 01728083     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00294-002-0355-2     Document Type: Review

References (94)

1. 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
2. Achsel T, Ahrens K, Brahms H, Teigelkamp S, Lührmann R (1998) The human U5-220kD protein (hPrp8) forms a stable RNA-free complex with several U5-specific proteins, including an RNA unwindase, a homologue of ribosomal elongation factor EF-2, and a novel WD-40 protein. Mol Cell Biol 18:6756-6766
3. Ajuh P, Sleeman J, Chusainow J, Lamond AI (2001) A direct interaction between the carboxyl-terminal region of CDC5L and the WD40 domain of PLRG1 is essential for pre-mRNA splicing. J Biol Chem 276:42370-42381
4. Alahari SK, Schmidt H, Käufer NF (1993) The fission yeast prp4+ gene involved in pre-mRNA splicing codes for a predicted serine/threonine kinase and is essential for growth. Nucleic Acids Res 21:4079-4083
5. Bishop DT, McDonald WH, Gould KL, Forsburg SL (2000) Isolation of an essential Schizosaccharomyces pombe gene, prp31(+), that links splicing and meiosis. Nucleic Acids Res 28:2214-2220
6. Brennwald P, Porter G, Wise JA (1988) U2 small nuclear RNA is remarkably conserved between Schizosaccharomyces pombe and mammals. Mol Cell Biol 8:5575-5580
7. Burge CB, Tuschl TH, Sharp PA (1999) Splicing of precursors to mRNAs by the spliceosomes. In: Gesteland RF, Cech TR, Atkins JF (eds) RNA world II. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y., pp 525-560
8. Collins CA, Guthrie C (1999) Allele-specific genetic interactions between Prp8 and RNA active site residues suggest a function for Prp8 at the catalytic core of the spliceosome. Genes Dev 13:1970-1982
9. Dandekar T, Tollervey D (1989) Cloning of Schizosaccharomyces pombe genes encoding the U1, U2, U3 and U4 snRNAs. Gene 81:227-235
10. Dandekar T, Ribes V, Tollervey D (1989) Schizosaccharomyces pombe U4 small nuclear RNA closely resembles vertebrate U4 and is required for growth. J Mol Biol 208:371-379
11. Dellaire G, Makarov EM, Cowger JJ, Longman D, Sutherland HG, Lührmann R, Torchia J, Bickmore WA (2002) Mammalian PRP4 kinase copurifies and interacts with components of both the U5 snRNP and the N-CoR deacetylase complexes. Mol Cell Biol 22:5141-5156
12. Forsburg SL (1999) The best yeast? Trends Genet 15:340-344
13. Gatermann KB, Hoffmann A, Rosenberg GH, Käufer NF (1989) Introduction of functional artificial introns into the naturally intronless ura4 gene of Schizosaccharomyces pombe. Mol Cell Biol 9:1526-1535
14. Gozani O, Potashkin J, Reed R (1998) A potential role for U2AFSAP 155 interactions in recruiting U2 snRNP to the branch site. Mol Cell Biol 18:4752-4760
15. Graveley BR (2000) Sorting out the complexity of SR protein functions. RNA 6:1197-1211
16. Groß T, Lützelberger M, Weigmann H, Klingenhoff A, Shenoy S, Käufer NF (1997) Functional analysis of the fission yeast Prp4 protein kinase involved in pre-mRNA splicing and isolation of a putative mammalian homologue. Nucleic Acids Res 25:1028-1035
17. Groß T, Richert K, Mierke C, Lützelberger M, Käufer NF (1998) Identification and characterization of srp1, a gene of fission yeast encoding a RNA binding domain and a RS domain typical of SR splicing factors. Nucleic Acids Res 26:505-511
18. 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
19. 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
20. Hastings ML, Krainer AR (2001) Pre-mRNA splicing in the new millenium. Curr Opin Cell Biol 13:302-309
21. 23 EMBO J 21:5516-5526
22. Johnson TL, Abelson J (2001) Characterization of U4 and U6 interactions with the 5′ splice site using a S. cerevisiae in vitro trans-splicing system. Genes Dev 15:1957-1970
23. Käufer 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
24. Käufer NF, Simanis V, Nurse P (1985) Fission yeast Schizosaccharomyces pombe correctly excises a mammalian RNA transcript intervening sequence. Nature 318:78-80
25. Kim SH, Lin RJ (1993) Pre-mRNA splicing within an assembled yeast spliceosome requires an RNA-dependent ATPase and ATP hydrolysis. Proc Natl Acad Sci USA 90:888-892
26. Kojima T, Zama T, Wada K, Onogi H, Hagiwara M (2001) Cloning of human PRP4 reveals interaction with Clk1. J Biol Chem 276:32247-32256
27. Kuhn AN, Brow DA (2000) Suppressors of a cold-sensitive mutation in yeast U4 RNA define five domains in the splicing factor PrP8 that influence spliceosome activation. Genetics 155:1667-1682
28. Kuhn AN, Käufer NF (2003) Mechanism and control of pre-mRNA splicing. In: Egel R (eds) Molecular biology of Schizosaccharomyces pombe. Springer, Berlin Heidelberg New York (in press)
29. Kuhn AN, Li Z, Brow DA (1999) Splicing factor Prp8 governs U4/ U6 RNA unwinding during activation of the spliceosome. Mol Cell 3:65-75
30. Kuhn AN, Reichl EM, Brow DA (2002) Distinct domains of splicing factor Prp8 mediate different aspects of spliceosome activation. Proc Natl Acad Sci USA 99:9145-9149
31. Le Hir H, Izaurralde E, Maquat LE, Moore MJ (2000) The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J 19:6860-6869
32. Leupold U (1950) Die Vererbung von Homothallie und Heterothallie bei Schizosaccharomyces pombe. C R Trav Lab Carlsberg 24:381-480
33. Lopez PJ, Séraphin B (1999) Genomic-scale quantitative analysis of yeast pre-mRNA splicing: implications for splice-site recognition. RNA 5:1135-1137
34. Lundgren K, Allan S, Urushiyama S, Tani T, Ohshima Y, et al (1996) A connection between pre-mRNA splicing and the cell cycle in fission yeast: cdc28+ is allelic with prp8+ and encodes an RNA-dependent ATPase/helicase. Mol Biol Cell 7:1083-1094
35. Lützelberger M (2000) Prä-mRNA Splicing in der Spalthefe Schizosaccharomyces pombe: in vivo Charakterisierung der Funktion des srp2 Gens. PhD thesis, Technical University, Braunschweig
36. Lützelberger M, Groß T, Käufer NF (1999) Srp2, an SR protein family member of fission yeast: in vivo characterization of its modular domains. Nucleic Acids Res 27:2618-2626
37. Lykke-Andersen J, Shu MD, Steitz JA (2001) Communication of the position of exon-exon junctions to the mRNA surveillance machinery by the protein RNPS1. Science 293:1836-1839
38. Madhani HD, Guthrie C (1992) A novel base-pairing interaction between U2 and U6 snRNAs suggests a mechanism for the catalytic activation of the spliceosome. Cell 71:803-817
39. Makarov EM, Makarova OV, Achsel T, 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
40. Makarova OV, Makarov EM, Liu S, Vornlocher HP, Lührmann R (2002) Protein 61 K, 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
41. 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
42. Mayeda A, Badolato J, Kobayashi R, Zhang MQ, Gardiner EM, Krainer AR (1999) Purification and characterization of human RNPS1: a general activator of pre-mRNA splicing. EMBO J 18:4560-4570
43. McDonald WH, Ohi R, Smelkova N, Frendewey D, Gould KL (1999) Myb-related fission yeast Cdc5p is a component of a 40S snRNP-containing complex and is essential for pre-mRNA splicing. Mol Cell Biol 19:5352-5362
44. McKie AB, McHale JC, Keen TJ, Tarttelin EE, Goliath R et al (2001) Mutations in the pre-mRNA splicing factor gene PRPC8 in autosomal dominant Retinitis pigmentosa (RP13). Hum Mol Genet 10:1555-1562
45. McKinney R, Wentz-Hunter K, Schmidt H, Potashkin J (1997) Molecular characterization of a novel fission yeast gene spUAP2 that interacts with the splicing factor spU2AF59. Curr Genet 32:323-330
46. Mermoud JE, Cohen P, Lamond AI (1992) Ser/Thr-specific protein phosphatases are required for both catalytic steps of pre-mRNA splicing. Nucleic Acids Res 20:5263-5269
47. Murray MV, Kobayashi R, Krainer AR (1999) The type 2C Ser/ Thr phosphatase PP2Cγ is a pre-mRNA splicing factor. Genes Dev 13:87-97
48. Nilsen TW (2002) The spliceosome: no assembly required? Mol Cell 9:8-9
49. van Nues RW, Beggs JD (2001) Functional contacts with a range of splicing proteins suggest a central role for Brr2p in the dynamic control of the order of events in spliceosomes of Saccharomyces cerevisiae. Genetics 157:1451-1467
50. Ohi MD, Gould KL (2002) Characterization of interactions among the Cef1p-Prp19p-associated splicing complex. RNA 8:798-815
51. 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
52. Ohi R, McCollum D, Hirani B, Den Haese GJ, Zhang X, et al (1994) The Schizosaccharomyces pombe cdc5 + gene encodes an essential protein with homology to c-Myb. EMBO J 13:471-483
53. Philips AV, Cooper TA (2000) RNA processing and human disease. Cell Mol Life Sci 57:235-249
54. Porter G, Brennwald P, Wise JA (1990) U1 small nuclear RNA from Schizosaccharomyces pombe has unique and conserved features and is encoded by an essential single-copy gene. Mol Cell Biol 10:2874-2881
55. Potashkin J, Li R, Frendewey D (1989) Pre-mRNA splicing mutants of Schizosaccharomyces pombe. EMBO J 8:551-559
56. Potashkin J, Naik K, Wentz-Hunter K (1993) U2AF homolog required for splicing in vivo. Science 262:573-575
57. Potashkin J, Kim D, Fons M, Humphrey T, Frendewey D (1998) Cell-division-cycle defects associated with fission yeast pre-mRNA splicing mutants. Curr Genet 34:153-163
58. Prabhala G, Rosenberg GH, Käufer NF (1992) Architectural features of pre-mRNA introns in the fission yeast Schizosaccharomyces pombe. Yeast 8:171-182
59. Reich CI, van Hoy 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
60. Richert K (2002) Untersuchungen zur Aufklärung des prä-mRNA Spleissvorgangs im der Spalthefe Schizosaccharomyces pombe: genetische und biochemische Charakterisierung der Interaktionen des prp4 Gens. PhD thesis, Technical University, Braunschweig
61. Richert K, Schmidt H, Groß T, Käufer NF (2002) The deubiquitinating enzyme Ubp21p of fission yeast stabilizes a mutant form of protein kinase Prp4p. Mol Genet Genomics 267:88-95
62. Romfo CM, Alvarez CJ, Heeckeren WJ van, Webb CJ, Wise JA (2000) Evidence for splice site pairing via intron definition in Schizosaccharomyces pombe. Mol Cell Biol 20:7955-7970
63. Rosenberg GH, Alahari SK, Käufer NF (1991) prp4 from Schizosaccharomyces pombe, a mutant deficient in pre-mRNA splicing isolated using genes containing artificial introns. Mol Gen Genet 226:305-309
64. Schmidt H, Richert K, Drakas RA, Käufer NF (1999) spp42, identified as a classical suppressor of prp4-73, which encodes a kinase involved in pre-mRNA splicing in fission yeast, is a homologue of the splicing factor Prp8p. Genetics 153:1183-1191
65. Schwelnus W, Richert K, Opitz F, Groß T, Habara Y, et al (2001) Fission yeast Prp4p kinase regulates pre-mRNA splicing by phosphorylating a non-SR-splicing factor. EMBO Rep 2:35-41
66. Siatecka M, Reyes JL, Konarska MM (1999) Functional interactions of Prp8 with both splice sites at the spliceosomal catalytic center. Genes Dev 13:1983-1993
67. Sipiczki M (2000) Where does fission yeast sit on the tree of life? Genome Biol 1:1-4
68. Small K, Brennwald P, Skinner H, Schaefer K, Wise JA (1989) Sequence and structure of U5 snRNA from Schizosaccharomyces pombe. Nucleic Acids Res 17:9483
69. Smith CW, Valcárcel J (2000) Alternative pre-mRNA splicing: the logic of combinatorial control. Trends Biochem Sci 25:381-388
70. Sontheimer EJ, Sun S, Piccirilli JA (1997) Metal ion catalysis during splicing of premessenger RNA. Nature 388:801-805
71. Spingola M, Grate L, Haussler D, Ares Jr M (1999) Genome-wide bioinformatic and molecular analysis of introns in Saccharomyces cerevisiae. RNA 5:221-234
72. Stern B, Nurse P (1996) A quantitative model for the cdc2 control of S phase and mitosis in fission yeast. Trends Genet 12:345-350
73. Stevens SW, Ryan DE, Ge HY, Moore RE, Young MK, et al (2002) Composition and functional characterization of the yeast spliceosomal penta-snRNP. Mol Cell 9:31-44
74. Sun JS, Manley JL (1995) A novel U2-U6 snRNA structure is necessary for mammalian mRNA splicing. Genes Dev 9:843-854
75. Takeuchi M, Yanagida M (1993) A mitotic role for a novel fission yeast protein kinase Dsk1 with cell cycle stage dependent phosphorylation and localization. Mol Biol Cell 4:247-260
76. Tang Z, Yanagida M, Lin RJ (1998) Fission yeast mitotic regulator Dsk1 is an SR protein-specific kinase. J Biol Chem 273:5963-5969
77. Tang Z, Kuo T, Shen J, Lin RJ (2000) Biochemical and genetic conservation of fission yeast Dsk1 and human SR protein-specific kinase 1. Mol Cell Biol 20:816-824
78. Tang Z, Käufer NF, Lin RJ (2002) Interactions between two fission yeast SR-related proteins and their modulation by phosphorylation. Biochem J DOI 10.1042/BJ20021133
79. Tani T, Ohshima Y (1989) The gene for the U6 small nuclear RNA in fission yeast has an intron. Nature 337:87-90
80. Tsai WY, Chow YT, Chen HR, Huang KT, Hong RI, et al (1999) Ceflp is a component of the Prp19p-associated complex and essential for pre-mRNA splicing. J Biol Chem 274:9455-9462
81. Umen JG, Guthrie C (1995) A novel role for a U5 snRNP protein in 3′ splice site selection. Genes Dev 9:855-868
82. Urushiyama S, Tani T, Ohshima Y (1996) Isolation of novel pre-mRNA splicing mutants of Schizosaccharomyces pombe. Mol Gen Genet 253:118-127
83. 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
84. Valadkhan S, Manley JL (2001) Splicing-related catalysis by protein-free snRNAs. Nature 413:701-707
85. Vithana EN, Abu-Safieh L, Allen MJ, Carey A, Papaioannou M et al. (2001) A human homolog of yeast pre-mRNA splicing gene, PRP31, underlies autosomal dominant Retinitis pigmentosa on chromosome 19q13.4 (RP11). Mol Cell 8:375-381
86. Wang C, Chua K, Seghezzi W, Lees E, Gozani O, Reed R (1998) Phosphorylation of spliceosomal protein SAP 155 coupled with splicing catalysis. Genes Dev 12:1409-1014
87. Weidenhammer EM, Ruiz-Noriega M, Woolford Jr JL (1997) Prp31p promotes the association of the U4/U6·U5 tri-snRNP with prespliceosomes to form spliceosomes in Saccharomyces cerevisiae. Mol Cell Biol 17:3580-3588
88. Wentz-Hunter K, Potashkin J (1996) The small subunit of the splicing factor U2AF is conserved in fission yeast. Nucleic Acids Res 24:1849-1854
89. Wood V, Gwilliam R, Rajandream MA, Lyne M, Lyne R, et al (2002) The genome sequence of Schizosaccharomyces pombe. Nature 415:871-880
90. 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
91. Yan D, Perriman R, Igel H, Howe KJ, Neville M, Ares Jr M (1998) CUS2, a yeast homolog of human Tat-SF1, rescues function of misfolded U2 through an unusual RNA recognition motif. Mol Cell Biol 18:5000-5009
92. Yean SL, Wuenschell G, Termini J, Lin RJ (2000) Metal-ion coordination by U6 small nuclear RNA contributes to catalysis in the spliceosome. Nature 408:881-884
93. Zamore PD, Green MR (1989) Identification, purification, and biochemical characterization of U2 small nuclear ribonucleoprotein auxiliary factor. Proc Natl Acad Sci USA 86:9243-9247
94. Zhou Q, Sharp PA (1996) Tat-SF1: cofactor for stimulation of transcriptional elongation by HIV-1 Tat. Science 274:605-610