A BBP-Mud2p heterodimer mediates branchpoint recognition and influences splicing substrate abundance in budding yeast

Nucleic Acids Research

Volumn 36, Issue 8, 2008, Pages 2787-2798

  Wang, Qiang ^a,b   Zhang, Li ^a   Lynn, Bert ^a   Rymond, Brian C ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BRANCHPOINT BINDING PROTEIN; FUNGAL RNA; HETERODIMER; MESSENGER RNA; MUD2 PROTEIN; MUTANT PROTEIN; PRION PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BINDING AFFINITY; CELL NUCLEUS; COMPLEX FORMATION; CONTROLLED STUDY; GEL FILTRATION; GENE DELETION; IN VIVO STUDY; MASS SPECTROMETRY; MOLECULAR RECOGNITION; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RNA SPLICING; SACCHAROMYCES CEREVISIAE; SPLICEOSOME; TWO HYBRID SYSTEM;

DIMERIZATION; DNA-BINDING PROTEINS; GENE DELETION; RIBONUCLEOPROTEINS; RNA PRECURSORS; RNA SPLICING; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUPPRESSION, GENETIC; TRANSCRIPTION FACTORS; TWO-HYBRID SYSTEM TECHNIQUES;

MAMMALIA; SACCHAROMYCETALES;

EID: 43349094305     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn144     Document Type: Article

References (74)

1. Burge,C.B., Tuschl,T. and Sharp,P.A. (1999) Splicing of Precursors to mRNAs by the Spliceosome. In Gesteland,R.F., Cech,T.R. and Atkins,J.F. (eds). The RNA World, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. Kramer,A. and 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.
3. Abovich,N. and Rosbash,M. (1997) Cross-intron bridging interactions in the yeast commitment complex are conserved in mammals. Cell, 89 403-412.
4. Rutz,B. and Seraphin,B. (1999) Transient interaction of BBP/ScSF1 and Mud2 with the splicing machinery affects the kinetics of spliceosome assembly. RNA, 5, 819-831.
5. Gozani,O., Potashkin,J. and Reed,R. (1998) A potential role for U2AF-SAP 155 interactions in recruiting U2 snRNP to the branch site. Mol. Cell Biol., 18, 4752-4760.
6. Wang,Q., He,J., Lynn,B. and Rymond,B.C. (2005) Interactions of the yeast SF3b splicing factor. Mol. Cell Biol., 25, 10745-10754.
7. Brow,D.A. (2002) Allosteric cascade of spliceosome activation. Annu. Rev. Genet., 36, 333-360.
8. Staley,J.P. and Guthrie,C. (1998) Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell, 92, 315-326.
9. 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. Nature, 402, 832-835.
10. Zorio,D.A. and Blumenthal,T. (1999) Both subunits of U2AF recognize the 3′ splice site in Caenorhabditis elegans. Nature, 402, 835-838.
11. Merendino,L., Guth,S., Bilbao,D., Martinez,C. and Valcarcel,J. (1999) Inhibition of msl-2 splicing by Sex-lethal reveals interaction between U2AF35 and the 3′ splice site AG. Nature, 402, 838-841.
12. Zuo,P. and Maniatis,T. (1996) The splicing factor U2AF35 mediates critical protein-protein interactions in constitutive and enhancer-dependent splicing. Genes Dev., 10, 1356-1368.
13. Webb,C.J., Lakhe-Reddy,S., Romfo,C.M. and Wise,J.A. (2005) Analysis of mutant phenotypes and splicing defects demonstrates functional collaboration between the large and small subunits of the essential splicing factor U2AF in vivo. Mol. Biol. Cell, 16, 584-596.
14. Zorio,D.A. and Blumenthal,T. (1999) U2AF35 is encoded by an essential gene clustered in an operon with RRM/cyclophilin in Caenorhabditis elegans. RNA, 5, 487-494.
15. Lacadie,S.A., Tardiff,D.F., Kadener,S. and Rosbash,M. (2006) In vivo commitment to yeast cotranscriptional splicing is sensitive to transcription elongation mutants. Genes Dev., 20, 2055-2066.
16. Berglund,J.A., Chua,K., Abovich,N., Reed,R. and Rosbash,M. (1997) The splicing factor BBP interacts specifically with the pre-mRNA branchpoint sequence UACUAAC. Cell, 89, 781-787.
17. Rymond,B.C. and Rosbash,M. (1985) Cleavage of 5′ splice site and lariat formation are independent of 3′ splice site in yeast mRNA splicing. Nature, 317, 735-737.
18. Abovich,N., Liao,X.C. and 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.
19. Rutz,B. and Seraphin,B. (2000) A dual role for BBP/ScSF1 in nuclear pre-mRNA retention and splicing. EMBO J., 19, 1873-1886.
20. Rain,J.C. and 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.
21. Jensen,T.H., Dower,K., Libri,D. and Rosbash,M. (2003) Early formation of mRNP. License for export or quality control? Mol. Cell, 11, 1129-1138.
22. Huang,T., Vilardell,J. and Query,C.C. (2002) Pre-spliceosome formation in S.pombe requires a stable complex of SF1-U2AF(59)-U2AF(23). EMBO J., 21, 5516-5526.
23. Berglund,J.A., Abovich,N. and Rosbash,M. (1998) A cooperative interaction between U2AF65 and mBBP/SF1 facilitates branchpoint region recognition. Genes Dev., 12, 858-867.
24. Gietz,R.D. and Sugino,A. (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene, 74, 527-534.
25. Kaiser,C., Michaelis,S. and Mitchell,A. (eds) (1994) Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
26. Jacquier,A., Rodriguez,J.R. and Rosbash,M. (1985) A quantitative analysis of the e.ects of 5′ junction and TACTAAC box mutants and mutant combinations on yeast mRNA splicing. Cell, 43, 423-430.
27. Legrain,P. and Rosbash,M. (1989) Some cis- and trans-acting mutants for splicing target pre-mRNA to the cytoplasm. Cell, 57, 573-583.
28. James,P., Halladay,J. and Craig,E.A. (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics, 144, 1425-1436.
29. Teem,J.L. and 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.
30. Blanton,S., Srinivasan,A. and Rymond,B.C. (1992) PRP38 encodes a yeast protein required for pre-mRNA splicing and maintenance of stable U6 small nuclear RNA levels. Mol. Cell Biol., 12, 3939-3947.
31. Pikielny,C.W. and Rosbash,M. (1985) mRNA splicing efficiency in yeast and the contribution of nonconserved sequences. Cell, 41, 119-126.
32. Wang,Q., Hobbs,K., Lynn,B. and Rymond,B.C. (2003) The Clf1p splicing factor promotes spliceosome assembly through N-terminal tetratricopeptide repeat contacts. J. Biol. Chem., 278, 7875-7883.
33. Puig,O., Caspary,F., Rigaut,G., Rutz,B., Bouveret,E., Bragado-Nilsson,E., Wilm,M. and Seraphin,B. (2001) The tandem affinity purification (TAP) method: A general procedure of protein complex purification. Methods, 24, 218-229.
34. Wang,Q. and Rymond,B.C. (2003) Rds3p is required for stable U2 snRNP recruitment to the splicing apparatus. Mol. Cell. Biol., 23, 7339-7349.
35. Chen,N., Harris,T.W., Antoshechkin,I., Bastiani,C., Bieri,T., Blasiar,D., Bradnam,K., Canaran,P., Chan,J., Chen,C.K. et al. (2005) WormBase: A comprehensive data resource for Caenorhabditis biology and genomics. Nucleic Acids Res., 33, D383-389.
36. Ghaemmaghami,S., Huh,W.K., Bower,K., Howson,R.W., Belle,A., Dephoure,N., O'Shea,E.K. and Weissman,J.S. (2003) Global analysis of protein expression in yeast. Nature, 425, 737-741.
37. Fromont-Racine,M., Rain,J.C. and Legrain,P. (1997) Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens [see comments]. Nat. Genet., 16, 277-282.
38. Chung,S., McLean,M.R. and Rymond,B.C. (1999) Yeast ortholog of the Drosophila crooked neck protein promotes spliceosome assembly through stable U4/U6.U5 snRNP addition. RNA, 5, 1042-1054.
39. Spingola,M., Armisen,J. and Ares,M. Jr. (2004) Mer1p is a modular splicing factor whose function depends on the conserved U2 snRNP protein Snu17p. Nucleic Acids Res., 32, 1242-1250.
40. Rain,J.C., Ra.,Z., Rhani,Z., Legrain,P. and Kramer,A. (1998) Conservation of functional domains involved in RNA binding and protein-protein interactions in human and Saccharomyces cerevisiae pre-mRNA splicing factor SF1. RNA, 4, 551-565.
41. Kistler,A.L. and Guthrie,C. (2001) Deletion of MUD2, the yeast homolog of U2AF65, can bypass the requirement for sub2, an essential spliceosomal ATPase. Genes Dev., 15, 42-49.
42. He,F., Peltz,S.W., Donahue,J.L., Rosbash,M. and Jacobson,A. (1993) Stabilization and ribosome association of unspliced pre-mRNAs in a yeast upf1-mutant. Proc. Natl Acad. Sci. USA, 90, 7034-7038.
43. Seraphin,B. and Rosbash,M. (1989) Identification of functional U1 snRNA-pre-mRNA complexes committed to spliceosome assembly and splicing. Cell, 59, 349-358.
44. Lacadie,S.A. and Rosbash,M. (2005) Cotranscriptional spliceosome assembly dynamics and the role of U1 snRNA:5′ss base pairing in yeast. Mol. Cell, 19, 65-75.
45. Zamore,P.D. and Green,M.R. (1989) Identification, purification, and biochemical characterization of U2 small nuclear ribonucleoprotein auxiliary factor. Proc. Natl Acad. Sci. USA, 86, 9243-9247.
46. Soares,L.M., Zanier,K., Mackereth,C., Sattler,M. and Valcarcel,J. (2006) Intron removal requires proofreading of U2AF/3′ splice site recognition by DEK. Science, 312, 1961-1965.
47. Hastings,M.L., Allemand,E., Duelli,D.M., Myers,M.P. and Krainer,A.R. (2007) Control of pre-mRNA splicing by the general splicing factors PUF60 and U2AF65. PLoS ONE, 2, e538.
48. Page-McCaw,P.S., Amonlirdviman,K. and Sharp,P.A. (1999) PUF60: A novel U2AF65-related splicing activity. RNA, 5, 1548-1560.
49. Lockhart,S.R. and Rymond,B.C. (1994) Commitment of yeast pre-mRNA to the splicing pathway requires a novel U1 small nuclear ribonucleoprotein polypeptide, Prp39p. Mol. Cell Biol., 14, 3623-3633.
50. Scherrer,F.W. Jr. and Spingola,M. (2006) A subset of Mer1p-dependent introns requires Bud13p for splicing activation and nuclear retention. RNA, 12, 1361-1372.
51. Engebrecht,J.A., Voelkel-Meiman,K. and Roeder,G.S. (1991) Meiosis-specific RNA splicing in yeast. Cell, 66, 1257-1268.
52. Puig,O., Gottschalk,A., Fabrizio,P. and Seraphin,B. (1999) Interaction of the U1 snRNP with nonconserved intronic sequences affects 5′ splice site selection. Genes Dev., 13, 569-580.
53. Vincent,K., Wang,Q., Jay,S., Hobbs,K. and Rymond,B.C. (2003) Genetic interactions with CLF1 identify additional pre-mRNA splicing factors and a link between activators of yeast vesicular transport and splicing. Genetics, 164, 895-907.
54. Chen,C.H., Yu,W.C., Tsao,T.Y., Wang,L.Y., Chen,H.R., Lin,J.Y., Tsai,W.Y. and Cheng,S.C. (2002) Functional and physical interactions between components of the Prp19p-associated complex. Nucleic Acids Res., 30, 1029-1037.
55. Chung,S., Zhou,Z., Huddleston,K.A., Harrison,D.A., Reed,R., Coleman,T.A. and Rymond,B.C. (2002) Crooked neck is a component of the human spliceosome and implicated in the splicing process. Biophys. Biochem. Acta, 1576, 289-297.
56. Gasch,A., Wiesner,S., Martin-Malpartida,P., Ramirez-Espain,X., Ruiz,L. and Macias,M.J. (2006) The structure of Prp40 FF1 domain and its interaction with the crn-TPR1 motif of Clf1 gives a new insight into the binding mode of FF domains. J. Biol. Chem., 281, 356-364.
57. Lillie,S.H. and Brown,S.S. (1994) Immunofluorescence localization of the unconventional myosin, Myo2p, and the putative kinesin-related protein, Smy1p, to the same regions of polarized growth in Saccharomyces cerevisiae. J. Cell. Biol., 125, 825-842.
58. Nishizawa,K., Freund,C., Li,J., Wagner,G. and Reinherz,E.L. (1998) Identi.cation of a proline-binding motif regulating CD2-triggered T lymphocyte activation. Proc. Natl Acad. Sci. USA, 95, 14897-14902.
59. Kofler,M., Heuer,K., Zech,T. and Freund,C. (2004) Recognition sequences for the GYF domain reveal a possible spliceosomal function of CD2BP2. J. Biol. Chem., 279, 28292-28297.
60. Laggerbauer,B., Liu,S., Makarov,E., Vornlocher,H.P., Makarova,O., Ingelfinger,D., Achsel,T. and Luhrmann,R. (2005) The human U5 snRNP 52K protein (CD2BP2) interacts with U5-102K (hPrp6), a U4/U6.U5 tri-snRNP bridging protein, but dissociates upon tri-snRNP formation. RNA, 11, 598-608.
61. Bialkowska,A. and 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.
62. Stevens,S.W., Barta,I., Ge,H.Y., Moore,R.E., Young,M.K., Lee,T.D. and Abelson,J. (2001) Biochemical and genetic analyses of the U5, U6, and U4/ U6 × U5 small nuclear ribonucleoproteins from Saccharomyces cerevisiae. RNA, 7, 1543-1553.
63. Kofler,M.M. and Freund,C. (2006) The GYF domain. FEBS J., 273 245-256.
64. Georgiev,A., Sjostrom,M. and Wieslander,A. (2007) Binding specificities of the GYF domains from two Saccharomyces cerevisiae Paralogs. Protein Eng. Des. Sel., 20, 443-452.
65. Dziembowski,A., Ventura,A.P., Rutz,B., Caspary,F., Faux,C., Halgand,F., Laprevote,O. and Seraphin,B. (2004) Proteomic analysis identifies a new complex required for nuclear pre-mRNA retention and splicing. EMBO J. 23, 4847-4856.
66. Abovich,N., Legrain,P. and Rosbash,M. (1990) The yeast PRP6 gene encodes a U4/U6 small nuclear ribonucleoprotein particle (snRNP) protein, and the PRP9 gene encodes a protein required for U2 snRNP binding. Mol. Cell Biol., 10, 6417-6425.
67. Galy,V., Gadal,O., Fromont-Racine,M., Romano,A., Jacquier,A. and Nehrbass,U. (2004) Nuclear retention of unspliced mRNAs in yeast is mediated by perinuclear Mlp1. Cell, 116, 63-73.
68. Houseley,J., LaCava,J. and Tollervey,D. (2006) RNA-quality control by the exosome. Nat. Rev. Mol. Cell Biol., 7, 529-539.
69. Rougemaille,M., Gudipati,R.K., Olesen,J.R., Thomsen,R., Seraphin,B., Libri,D. and Jensen,T.H. (2007) Dissecting mechanisms of nuclear mRNA surveillance in THO/sub2 complex mutants. EMBO J, 26, 2317-2326.
70. Huh,W.K., Falvo,J.V., Gerke,L.C., Carroll,A.S., Howson,R.W., Weissman,J.S. and O'Shea,E.K. (2003) Global analysis of protein localization in budding yeast. Nature, 425, 686-691.
71. Blanchette,M., Labourier,E., Green,R.E., Brenner,S.E. and Rio,D.C. (2004) Genome-wide analysis reveals an unexpected function for the Drosophila splicing factor U2AF50 in the nuclear export of intronless mRNAs. Mol. Cell, 14, 775-786.
72. Gama-Carvalho,M., Barbosa-Morais,N.L., Brodsky,A.S., Silver,P.A. and Carmo-Fonseca,M. (2006) Genome-wide identification of functionally distinct subsets of cellular mRNAs associated with two nucleocytoplasmic-shuttling mammalian splicing factors. Genome Biol. 7, R113.
73. Das,R., Yu,J., Zhang,Z., Gygi,M.P., Krainer,A.R., Gygi,S.P. and Reed,R. (2007) SR proteins function in coupling RNAP II transcription to pre-mRNA splicing. Mol. Cell, 26, 867-881.
74. Keene,J.D. (2007) RNA regulons: Coordination of post-transcriptional events. Nat. Rev. Genet., 8, 533-543.