Structure-function analysis of the Yhc1 subunit of yeast U1 snRNP and genetic interactions of Yhc1 with Mud2, Nam8, Mud1, Tgs1, U1 snRNA, SmD3 and Prp28

Nucleic Acids Research

Volumn 42, Issue 7, 2014, Pages 4697-4711

  Schwer, Beate ^a   Shuman, Stewart ^b  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEAD BOX PROTEIN; FUNGAL PROTEIN; PRP28 PROTEIN; SMALL NUCLEAR RNA; UNCLASSIFIED DRUG; YHC1 PROTEIN;

ALLELE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; FUNGUS GROWTH; GENE; GENE INTERACTION; MOLECULAR INTERACTION; MUD1 GENE; MUD2 GENE; MUTATIONAL ANALYSIS; NAM8 GENE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; PRP28 GENE; SMD3 GENE; STRUCTURE ACTIVITY RELATION; YHC1 GENE;

ALANINE; BINDING SITES; DEAD-BOX RNA HELICASES; HUMANS; METHYLTRANSFERASES; MUTATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RIBONUCLEOPROTEIN, U1 SMALL NUCLEAR; RIBONUCLEOPROTEINS; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA, SMALL NUCLEAR; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE DELETION; ZINC;

EID: 84899019119     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku097     Document Type: Article

References (49)

1. Fabrizio, P., Dannenberg, J., Dube, P., Kastner, B., Stark, H., Urlaub, H. and Luhrmann, R. (2009) The evolutionarily conserved core design of the catalytic activation step of the yeast spliceosome. Mol. Cell, 36, 593-608.
2. Warlocki, Z., Odenwalder, P., Schitzova, J., Platzmann, F., Stark, H., Urlaub, H., Ficner, R., Fabrizio, P. and Luhrmann, R. (2009) Reconstitution of both steps of Saccharomyces cerevisiae splicing with purified spliceosomal components. Nat. Struct. Mol. Biol., 16, 1237-1243.
3. Hoskins, A.A., Friedman, L.J., Gallagher, S.S., Crawford, D.J., Anderson, E.G., Wombacher, R., Ramirez, N., Cornish, V.W., Gelles, J. and Moore, M.J. (2011) Ordered and dynamic assembly of single spliceosomes. Science, 331, 1289-1295.
4. Chen, J.Y., Stands, L., Staley, J.P., Jackups, R.R., Latus, L.J. and Chang, T.H. (2001) Specific alterations of U1-C protein or U1 small nuclear RNA can eliminate the requirement of Prp28p, an essential DEAD box splicing factor. Mol. Cell, 7, 227-232. (Pubitemid 32162915)
5. Staley, J.P. and Guthrie, C. (1999) An RNA switch at the 5' splice site requires ATP and the DEAD box protein Prp28p. Mol. Cell, 3, 55-64. (Pubitemid 29292477)
6. Tang, J., Abovich, N, Fleming, M.J., Seraphin, B. and Rosbash, M. (1997) Identification and characterization of a yeast homolog of U1 snRNP-specific protein C. EMBO J., 13, 4082-4091. (Pubitemid 27281023)
7. Gottschalk, A., Tang, J., Puig, O., Salgado, J., Neubauer, G, Colot, H.V., 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. (Pubitemid 28160780)
8. Fortes, P., Bilbao-Cortes, D., Fornerod, M., Rigaut, G, Raymond, W., Seraphin, B. and Mattaj, I.W. (1999) Luc7p, a novel yeast U1 snRNP protein with a role in 5' splice site recognition. Genes Dev., 13, 2425-2438. (Pubitemid 29453613)
9. Schwer, B., Erdjument-Bromage, H. and Shuman, S. (2011) Composition of yeast snRNPs and snoRNPs in the absence of trimethylguanosine caps reveals nuclear cap binding protein as a gained U1 component implicated in the cold-sensitivity of tgs1A cells. Nucleic Acids Res., 39, 6715-6728.
10. Pomeranz Krummel, DA., Oubridge, C, Leung, A.K.W., Li, J. and Nagai, K. (2009) Crystal structure of human spliceosomal U1 snRNP at 5.5 A resolution. Nature, 458, 475-480.
11. Weber, G, Trowitzsch, S., Kastner, B., Luhrmann, R. and Wahl, M.C. (2010) Functional organization of the Sm core in the crystal structure of human U1 snRNP. EMBO J., 29, 4172-4184.
12. Van der Feltz, C, Anthony, K, Brilot, A. and Pomeranz Krummel, DA. (2012) Architecture of the spliceosome. Biochemistry, 51, 3321-3333.
13. Siliciano, P.G and Guthrie, C. (1988) 5' splice site selection in yeast: genetic alterations in base-pairing with U1 reveal additional requirements. Genes Dev., 2, 1258-1267.
14. Seraphin, B., Kretzner, L. and 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.
15. Siliciano, P.G, Kivens, W.J. and Guthrie, C. (1991) More than half of yeast U1 snRNA is dispensable for growth. Nucleic Acids Res., 19, 6367-6372. (Pubitemid 21913061)
16. Liao, X., Kretzner, L., Seraphin, B. and Rosbash, M. (1990) Universally conserved and yeast-specific U1 snRNA sequences are important but not essential for U1 snRNP function. Genes Dev., 4, 1766-1774.
17. Hausmann, S., Zheng, S., Costanzo, M., Brost, R.L., Garcin, D., Boone, C, Shuman, S. and Schwer, B. (2008) Genetic and biochemical analysis of yeast and human cap trimethylguanosine synthase: functional overlap of TMG caps, snRNP components, pre-mRNA splicing factors, and RNA decay pathways. J. Biol. Chem., 283, 31706-31718.
18. Liao, X.C, Tang, J. and Rosbash, M. (1991) 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. (Pubitemid 23139235)
19. 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. (Pubitemid 24130457)
20. Chang, J., Schwer, B. and Shuman, S. (2010) Mutational analyses of trimethylguanosine synthase (Tgs1) and Mud2: proteins implicated in pre-mRNA splicing. RNA, 16, 1018-1031.
21. Qiu, Z.R., Schwer, B. and Shuman, S. (2011) Determinants of Nam8-dependent splicing of meiotic pre-mRNAs. Nucleic Acids Res., 39, 3427-3445.
22. Hilleren, P.J., Kao, H.Y. and Siliciano, P.G (1995) The amino-terminal domain of yeast U1-70K is necessary and sufficient for function. Mol. Cell. Biol., 15, 6341-6350.
23. Ester, C. and Uetz, P. (2008) The FF domains of yeast U1 snRNP protein Prp40 mediate interactions with Luc7 and Snu71. BMC Biochem., 9, 29.
24. Gornemann, J., Barrandon, C, Hujer, K, Rutz, B., Rigaut, G, Kotovic, K.M., Faux, C, Neugebauer, K.M. and Seraphin, B. (2011) Cotranscriptional spliceosome assembly and splicing are independent of the Prp40p WW domain. RNA, 17, 2119-2129.
25. Schwer, B., Chang, J. and Shuman, S. (2013) Structure-function analysis of the 5' end of yeast U1 snRNA highlights genetic interactions with the Msl5"Mud2 branchpoint binding complex and other spliceosome assembly factors. Nucleic Acids Res., 41, 7485-7500.
26. Chang, J., Schwer, B. and Shuman, S. (2012) Structure-function analysis and genetic interactions of the yeast branchpoint binding protein Msl5. Nucleic Acids Res., 40, 4539-4552.
27. Colot, H.V., Stutz, F. and 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. (Pubitemid 26268873)
28. Abovich, N. and Rosbash, M. (1997) Cross-intron bridging interactions in the yeast commitment complex are conserved in mammals. Cell, 89, 403-412. (Pubitemid 27220885)
29. Tang, J., Abovich, N. and 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.
30. Fortes, P., Kufel, J., Fornerod, M., Polycarpou-Schwarz, M., Lafontaine, D., Tollervey, D. and Mattaj, I.W. (1999) Genetic and physical interaction involving the yeast nuclear cap-binding complex. Mol. Cell. Biol., 19, 6543-6553. (Pubitemid 29441839)
31. Tong, A.H., Evangelista, M., Parsons, A.B., Xu, H., Bader, G.D., Page, N, Robinson, M., Raghibizadeh, S., Hogue, C.W., Bussey, H. et al. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science, 294, 2364-2368. (Pubitemid 33140562)
32. Wilmes, GM., Bergkessel, M., Bandyopadhyay, S., Shales, M., Braberg, H., Cagney, G, Collins, S.R., Whitworth, GB., Kress, T.L., Weissman, J.S. et al. (2008) A genetic interaction map of RNA-processing factors reveals links between Sem1/Dss1-containing complexes and mRNA export and splicing. Mol. Cell, 32, 735-746.
33. Costanzo, M., Baryshnikova, A., Bellay, J., Kim, Y., Spear, E.D., Sevier, C.S., Ding, H., Koh, J.L., Toufighi, K, Mostafavi, S. et al. (2010) The genetic landscape of a cell. Science, 327, 425-431.
34. Qiu, Z.R., Chico, L., Chang, J., Shuman, S. and Schwer, B. (2012) Genetic interactions of hypomorphic mutations in the m7G cap binding pocket of yeast nuclear cap binding complex: an essential role for Cbc2 in meiosis via splicing of MER3 pre-mRNA. RNA, 18, 1996-2011.
35. Calero, G, Wilson, K.F., Ly, T., Rios-Steiner, J.L., Clardy, J.C. and Cerione, RA. (2002) Structural basis of m7GpppG binding to the nuclear cap-binding protein complex. Nat. Struct. Biol., 9, 912-917. (Pubitemid 35417059)
36. Mazza, C, Segref, A., Mattaj, I.W. and Cusack, S. (2002) Large-scale induced fit recognition of an m7GpppG cap analogue by the human nuclear cap-binding complex. EMBO J., 21, 5548-5557. (Pubitemid 35231034)
37. Liu, Z., Luyten, I., Bottomley, M.J., Messias, A.C, Houngninou-Molango, S., Sprangers, R., Zanier, K, Kramer, A. and Sattler, M. (2001) Structural basis for recognition of the intron branch site RNA by splicing factor 1. Science, 294, 1098-1102. (Pubitemid 33041864)
38. Muto, Y., Pomeranz Krummel, D., Oubridge, C., Hernandez, H., Robinson, C.V., Neihaus, D. and Nagai, K. (2004) The structure and biochemical properties of the human spliceosomal protein U1C. J. Mol. Biol., 341, 185-198. (Pubitemid 39090644)
39. Nelissen, R.L.H., Heinrichs, V., Habets, W.J., Simons, F., Luhrmann, R. and van Venrooij, W.J. (1991) Zinc finger-like structure in U1-specific protein C is essential for specific binding to U1 snRNP. Nucleic Acids Res., 19, 449-454. (Pubitemid 21897025)
40. 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. (Pubitemid 29131882)
41. Du, H. and Rosbash, M. (2002) The U1 snRNP protein U1C recognizes the 5′ splice site in the absence of base pairing. Nature, 419, 86-90. (Pubitemid 34987875)
42. Will, C.L., Rumpler, S., Gunnewiek, J.K., van Venrooij, W.J. and Luhrmann, R. (1996) In vitro reconstitution of mammalian U1 snRNPs active in splicing: the U1-C protein enhances the formation of early (E) spliceosomal complexes. Nucleic Acids Res., 24, 4614-4623. (Pubitemid 26413336)
43. Mouaikel, J., Verheggen, C., Bertrand, E., Tazi, J. and Bordonne, R. (2002) Hypermethylation of the cap structure of both yeast snRNAs and snoRNAs requires a conserved methyltransferase that is localized to the nucleolus. Mol. Cell, 9, 891-901. (Pubitemid 34454898)
44. Hausmann, S. and Shuman, S. (2005) Specificity and mechanism of RNA cap guanine-N2 methyltransferase (Tgs1). J. Biol. Chem., 280, 4021-4024. (Pubitemid 40288564)
45. Strauss, E.J. and Guthrie, C. (1994) PRP28, a DEAD-box protein, is required for the first step of mRNA splicing in vitro. Nucleic Acids Res., 22, 3187-3193. (Pubitemid 24260655)
46. Chang, T.H., Latus, L.J., Liu, Z. and Abbott, J.M. (1997) Genetic interactions of conserved regions in the DEAD-box protein Prp28p. Nucleic Acids Res., 24, 5033-5040. (Pubitemid 28022266)
47. Hage, R., Tung, L., Du, H., Stands, L., Rosbash, M. and Chang, T.H. (2009) A targeted bypass screen identifies Ynl187p, Prp42p, Snu71p, and Cbp80p for stable U1 snRNP/pre-mRNA interaction. Mol. Cell. Biol., 29, 3941-3952.
48. Sengoku, T., Nureki, O., Nakamura, A., Kobayashi, S. and Yokoyama, S. (2006) Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell, 125, 287-300.
49. Balzer, R.J. and Henry, M.F. (2008) Snu56p is required for Mer1p-activates meiotic splicing. Mol. Cell. Biol., 28, 2497-2508. (Pubitemid 351542352)