Crystal structure of Ski8p, a WD-repeat protein with dual roles in mRNA metabolism and meiotic recombination

Protein Science

Volumn 13, Issue 10, 2004, Pages 2673-2684

  Cheng, Zhihong ^a   Liu, Yuying ^a   Wang, Chernhoe ^a   Parker, Roy ^b   Song, Haiwei ^a,c  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Meiotic recombination; mRNA decay; Protein crystallography; WD repeat

Indexed keywords

AMINO ACID; MESSENGER RNA; PROTEIN;

ARTICLE; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; HYDROPHOBICITY; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; RNA METABOLISM; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; CRYSTALLOGRAPHY; ESTERASES; MEIOSIS; MOLECULAR SEQUENCE DATA; MUTAGENESIS; MUTATION; NUCLEAR PROTEINS; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; RECOMBINATION, GENETIC; REPETITIVE SEQUENCES, AMINO ACID; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURAL HOMOLOGY, PROTEIN;

BACTERIA (MICROORGANISMS); SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 4644355036     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.04856504     Document Type: Article

References (60)

1. Allmang, C., Petfalski, E., Podtelejnikov, A., Mann, M., Tollervey, D., and Mitchell, P. 1999. The yeast exosome and human PM-Scl are related complexes of 3′ → 5′ exonucleases. Genes & Dev. 13: 2148-2158.
2. Aloy, P., Bottcher, B., Ceulemans, H., Leutwein, C., Mellwig, C., Fischer, S., Gavin, A.C., Bork, P., Superti-Furga, G., Serrano, L., et al. 2004. Structure-based assembly of protein complexes in yeast. Science 303: 2026-2029.
3. Araki, Y., Takahashi, S., Kobayashi, T., Kajiho, H., Hoshino, S., and Katada, T. 2001. Ski7p G protein interacts with the exosome and the Ski complex for 3′-to-5′ mRNA decay in yeast. EMBO J. 20: 4684-4693.
4. Arora, C., Kee, K., Maleki, S., and Keeney, S. 2004. Antiviral protein Ski8 is a direct partner of Spo11 in meiotic DNA break formation, independent of its cytoplasmic role in RNA metabolism. Mol. Cell 13: 549-559.
5. Brown, J.T., Bai, X., and Johnson, A.W. 2000. The yeast antiviral proteins Ski2p, Ski3p, and Ski8p exist as a complex in vivo. RNA 6: 449-457.
6. Brunger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., et al. 1998. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D 54: 905-921.
7. Cao, D. and Parker, R. 2003. Computational modeling and experimental analysis of nonsense-mediated decay in yeast. Cell 113: 533-545.
8. Chen, C.Y., Gherzi, R., Ong, S.E., Chan, E.L., Raijmakers, R., Pruijn, G.J., Stoecklin, G., Moroni, C., Mann, M., and Karin, M. 2001. AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107: 451-464.
9. Evans, D.H., Li, Y.F., Fox, M.E., and Smith, G.R. 1997. A WD repeat protein, Rec 14, essential for meiotic recombination in Schizosaccharomyces pombe. Genetics 146: 1253-1264.
10. Fox, M.E. and Smith, G.R. 1998. Control of meiotic recombination in Schizosaccharomyces pombe. Prog. Nucleic Acid Res. Mol. Biol. 61: 345-378.
11. Frischmeyer, P.A. and Dietz, H.C. 1999. Nonsense-mediated mRNA decay in health and disease. Hum. Mol. Genet. 8: 1893-1900.
12. Frischmeyer, P.A., van Hoof, A., O'Donnell, K., Guerrerio, A.L., Parker, R., and Dietz, H.C. 2002. An mRNA surveillance mechanism that eliminates transcripts lacking termination codons. Science 295: 2258-2261.
13. Gardiner, J.M., Bullard, S.A., Chrome, C., and Malone, R.E. 1997. Molecular and genetic analysis of REC103, an early meiotic recombination gene in yeast. Genetics 146: 1265-1274.
14. Gaudet, R., Bohm, A., and Sigler, P.B. 1996. Crystal structure at 2.4 angstroms resolution of the complex of transducin βγ and its regulator, phosducin. Cell 87: 577-588.
15. Goebl, M. and Yanagida, M. 1991. The TPR snap helix: A novel protein repeat motif from mitosis to transcription. Trends Biochem. Sci. 16: 173-177.
16. Jacobs Anderson, J.S. and Parker, R. 1998. The 3′ to 5′ degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 3′ to 5′ exonucleases of the exosome complex. EMBO J. 17: 1497-1506.
17. Jones, T.A., Zou, J.Y., Cowan, S.W., and Kjeldgaard, M. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47: 110-119.
18. Komachi, K. and Johnson, A.D. 1997. Residues in the WD repeats of Tup1 required for interaction with α2. Mol. Cell Biol. 17: 6023-6028.
19. Kraulis, P.J. 1991. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24: 946-950.
20. Lambright, D.G., Sondek, J., Bohm, A., Skiba, N.P., Hamm, H.E., and Sigler, P.B. 1996. The 2.0 Å crystal structure of a heterotrimeric G protein. Nature 379: 311-319.
21. Laskowski, R.A., Moss, D.S., and Thornton, J.M. 1993. Main-chain bond lengths and bond angles in protein structures. J. Mol. Biol. 231: 1049-1067.
22. Lejeune, F., Li, X., and Maquat, L.E. 2003. Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol. Cell 12: 675-687.
23. Malone, R.E., Bullard, S., Hermiston, M., Rieger, R., Cool, M., and Galbraith, A. 1991. Isolation of mutants defective in early steps of meiotic recombination in the yeast Saccharomyces cerevisiae. Genetics 128: 79-88.
24. Maquat, L.E. 2002. Molecular biology. Skiing toward nonstop mRNA decay. Science 295: 2221-2222.
25. Masison, D.C., Blanc, A., Ribas, J.C., Carroll, K., Sonenberg, N., and Wickner, R.B. 1995. Decoying the cap-mRNA degradation system by a double-stranded RNA virus and poly(A)-mRNA surveillance by a yeast antiviral system. Mol. Cell. Biol. 15: 2763-2771.
26. Matsumoto, Y., Sarkar, G., Sommer, S.S., and Wickner, R.B. 1993. A yeast antiviral protein, SKI8, shares a repeated amino acid sequence pattern with β-subunits of G proteins and several other proteins. Yeast 9: 43-51.
27. Mitchell, P. and Tollervey, D. 2001. mRNA turnover. Curr. Opin. Cell Biol. 13: 320-325.
28. -. 2003. An NMD pathway in yeast involving accelerated deadenylation and exosome-mediated 3′ → 5′ degradation. Mol. Cell 11: 1405-1413.
29. Mitchell, P., Petfalski, E., Shevchenko, A., Mann, M., and Tollervey, D. 1997. The exosome: A conserved eukaryotic RNA processing complex containing multiple 3′ → 5′ exoribonucleases. Cell 91: 457-466.
30. Muhlrad, D. and Parker, R. 1994. Premature translational termination triggers mRNA decapping. Nature 370: 578-581.
31. Mukherjee, D., Gao, M., O'Connor, J.P., Raijmakers, R., Pruijn, G., Lutz, C.S., and Wilusz, J. 2002. The mammalian exosome mediates the efficient degradation of mRNAs that contain AU-rich elements. EMBO J. 21: 165-174.
32. Murshudov, G.N., Vagin, A.A., and Dodson, E.J. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 53: 240-255.
33. Neer, E.J., Schmidt, C.J., Nambudripad, R., and Smith, T.F. 1994. The ancient regulatory-protein family of WD-repeat proteins. Nature 371: 297-300.
34. Nicholls, A., Sharp, K.A., and Honig, B. 1991. Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11: 281-296.
35. Otwinowski, Z. and Minor, W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276: 307-326.
36. Parker, R. and Song, H. 2004. The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 11: 121-127.
37. Pecina, A., Smith, K.N., Mezard, C., Murakami, H., Ohta, K., and Nicolas, A. 2002. Targeted stimulation of meiotic recombination. Cell 111: 173-184.
38. Pickles, L.M., Roe, S.M., Hemingway, E.J., Stifani, S., and Pearl, L.H. 2002. Crystal structure of the C-terminal WD40 repeat domain of the human Groucho/TLE1 transcriptional corepressor. Structure (Camb) 10: 751-761.
39. Rhee, S.K., Icho, T., and Wickner, R.B. 1989. Structure and nuclear localization signal of the SKI3 antiviral protein of Saccharomyces cerevisiae. Yeast 5: 149-158.
40. Smith, T.F., Gaitatzes, C., Saxena, K., and Neer, E.J. 1999. The WD repeat: A common architecture for diverse functions. Trends Biochem. Sci. 24: 181-185.
41. Sondek, J., Bohm, A., Lambright, D.G., Hamm, H.E., and Sigler, P.B. 1996. Crystal structure of a G-protein β γ dimer at 2.1 Å resolution. Nature 379: 369-374.
42. Sprague, E.R., Redd, M.J., Johnson, A.D., and Wolberger, C. 2000. Structure of the C-terminal domain of Tup1, a corepressor of transcription in yeast. EMBO J. 19: 3016-3027.
43. Surosky, R.T., Strich, R., and Esposito, R.E. 1994. The yeast UME5 gene regulates the stability of meiotic mRNAs in response to glucose. Mol. Cell Biol. 14: 3446-3458.
44. Takahashi, S., Araki, Y., Sakuno, T., and Katada, T. 2003. Interaction between Ski7p and Upf1p is required for nonsense-mediated 3′-to-5′ mRNA decay in yeast. EMBO J. 22: 3951-3959.
45. Terwilliger, T.C. 2002. Automated structure solution, density modification and model building. Acta Crystallogr. D 58: 1937-1940.
46. Terwilliger, T.C. and Berendzen, J. 1999. Automated MAD and MIR structure solution. Acta Crystallogr. D 55: 849-861.
47. Tesse, S., Storlazzi, A., Kleckner, N., Gargano, S., and Zickler, D. 2003. Localization and roles of Ski8p protein in Sordaria meiosis and delineation of three mechanistically distinct steps of meiotic homolog juxtaposition. Proc. Natl. Acad. Sci. 100: 12865-12870.
48. Toh, E., Guerry, P., and Wickner, R.B. 1978. Chromosomal superkiller mutants of Saccharomyces cerevisiae. J. Bacteriol. 136: 1002-1007.
49. Tucker, M. and Parker, R. 2000. Mechanisms and control of mRNA decapping in Saccharomyces cerevisiae. Annu. Rev. Biochem. 69: 571-595.
50. Uetz, P., Giot, L., Cagney, G., Mansfield, T.A., Judson, R.S., Knight, J.R., Lockshon, D., Narayan, V., Srinivasan, M., Pochart, P., et al. 2000. A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403: 623-627.
51. van der Voorn, L. and Ploegh, H.L. 1992. The WD-40 repeat. FEBS Lett. 307: 131-134.
52. van Hoof, A. and Parker, R. 1999. The exosome: A proteasome for RNA? Cell 99: 347-350.
53. van Hoof, A., Lennertz, P., and Parker, R. 2000. Yeast exosome mutants accumulate 3′-extended polyadenylated forms of U4 small nuclear RNA and small nucleolar RNAs. Mol. Cell. Biol. 20: 441-452.
54. van Hoof, A., Frischmeyer, P.A., Dietz, H.C., and Parker, R. 2002. Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science 295: 2262-2264.
55. Voegtli, W.C., Madrona, A.Y., and Wilson, D.K. 2003. The structure of Aip1p, a WD repeat protein that regulates Cofilin-mediated actin depolymerization. J. Biol. Chem. 278: 34373-34379.
56. Wall, M.A., Coleman, D.E., Lee, E., Iniguez-Lluhi, J.A., Posner, B.A., Gilman, A.G., and Sprang, S.R. 1995. The structure of the G protein heterotrimer Gi α 1 β 1 γ 2. Cell 83: 1047-1058.
57. Wang, Z. and Kiledjian, M. 2001. Functional link between the mammalian exosome and mRNA decapping. Cell 107: 751-762.
58. Waterhouse, P.M., Wang, M.B., and Lough, T. 2001. Gene silencing as an adaptive defence against viruses. Nature 411: 834-842.
59. Widner, W.R. and Wickner, R.B. 1993. Evidence that the SKI antiviral system of Saccharomyces cerevisiae acts by blocking expression of viral mRNA. Mol. Cell. Biol. 13: 4331-4341.
60. Wu, G., Xu, G., Schulman, B.A., Jeffrey, P.D., Harper, J.W., and Pavletich, N.P. 2003. Structure of a β-TrCP1-Skp1-β-catenin complex: Destruction motif binding and lysine specificity of the SCF(β-TrCP1) ubiquitin ligase. Mol. Cell 11: 1445-1456.