Structure of the Yeast WD40 Domain Protein Cia1, a Component Acting Late in Iron-Sulfur Protein Biogenesis

Structure

Volumn 15, Issue 10, 2007, Pages 1246-1257

  Srinivasan, Vasundara ^a   Netz, Daili J A ^b   Webert, Holger ^b   Mascarenhas, Judita ^b   Pierik, Antonio J ^b   Michel, Hartmut ^a   Lill, Roland ^b  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

PROTEINS

Indexed keywords

CIA1 PROTEIN; IRON SULFUR PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CRYSTAL STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; SITE DIRECTED MUTAGENESIS; YEAST;

AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; CELL CYCLE PROTEINS; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; HUMANS; IRON-SULFUR PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; STRUCTURE-ACTIVITY RELATIONSHIP;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 35148812715     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2007.08.009     Document Type: Article

References (57)

1. Balk J., Pierik A.J., Aguilar Netz D., Mühlenhoff U., and Lill R. The hydrogenase-like Nar1p is essential for maturation of cytosolic and nuclear iron-sulphur proteins. EMBO J. 23 (2004) 2105-2115
2. Balk J., Aguilar Netz D.J., Tepper K., Pierik A.J., and Lill R. The essential WD40 protein Cia1 is involved in a late step of cytosolic and nuclear iron-sulfur protein assembly. Mol. Cell. Biol. 25 (2005) 10833-10841
3. Beinert H., Holm R.H., and Münck E. Iron-sulfur clusters: Nature's modular, multipurpose structures. Science 277 (1997) 653-659
4. Bekri S., Kispal G., Lange H., Fitzsimons E., Tolmie J., Lill R., and Bishop D.F. Human ABC7 transporter: gene structure and mutation causing X-linked sideroblastic anemia with ataxia (XLSA/A) with disruption of cytosolic iron-sulfur protein maturation. Blood 96 (2000) 3256-3264
5. Biederbick A., Stehling O., Rösser R., Niggemeyer B., Nakai Y., Elsässer H.P., and Lill R. Role of human mitochondrial Nfs1 in cytosolic iron-sulfur protein biogenesis and iron regulation. Mol. Cell. Biol. 26 (2006) 5675-5687
6. CCP4 (Collaborative Computational Project, Number 4). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50 (1994) 760-763
7. Cheng Z., Liu Y., Wang C., Parker R., and Song H. Crystal structure of Ski8p, a WD-repeat protein with dual roles in mRNA metabolism and meiotic recombination. Protein Sci. 13 (2004) 2673-2684
8. Costa G.L., Bauer J.C., McGowan B., Angert M., and Weiner M.P. Site-directed mutagenesis using a rapid PCR-based method. Methods Mol. Biol. 57 (1996) 239-248
9. De la Fortelle E., and Bricogne G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276 (1997) 472-494
10. DeLano, W.L. (2002). The PyMOL Molecular Graphics System (http://www.pymol.org).
11. Diekert K., deKroon A.I.P.M., Kispal G., and Lill R. Isolation and sub-fractionation of mitochondria from the yeast Saccharomyces cerevisiae. Methods Cell Biol. 65 (2001) 37-51
12. Dong J., Lai R., Nielsen K., Fekete C.A., Qiu H., and Hinnebusch A.G. The essential ATP-binding cassette protein RLI1 functions in translation by promoting preinitiation complex assembly. J. Biol. Chem. 279 (2004) 42157-42168
13. Ford C.E., Skiba N.P., Bae H., Daaka Y., Reuveny E., Shekter L.R., Rosal R., Weng G., Yang C.S., Iyengar R., et al. Molecular basis for interactions of G protein βγ subunits with effectors. Science 280 (1998) 1271-1274
14. Gerber J., Neumann K., Prohl C., Mühlenhoff U., and Lill R. The yeast scaffold proteins Isu1p and Isu2p are required inside mitochondria for maturation of cytosolic Fe/S proteins. Mol. Cell. Biol. 24 (2004) 4848-4857
15. Ghaemmaghami S., Huh W.K., Bower K., Howson R.W., Belle A., Dephoure N., O'Shea E.K., and Weissman J.S. Global analysis of protein expression in yeast. Nature 425 (2003) 737-741
16. Gietz D., St. Jean A., Woods R.A., and Schiestl R.H. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20 (1992) 1425
17. Gouet P., Courcelle E., Stuart D.I., and Metoz F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15 (1999) 305-308
18. Hausmann A., Aguilar Netz D.J., Balk J., Pierik A.J., Mühlenhoff U., and Lill R. The eukaryotic P-loop NTPase Nbp35: an essential component of the cytosolic and nuclear iron-sulfur protein assembly machinery. Proc. Natl. Acad. Sci. USA 102 (2005) 3266-3271
19. Ho Y., Gruhler A., Heilbut A., Bader G.D., Moore L., Adams S.L., Millar A., Taylor P., Bennett K., Boutilier K., et al. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415 (2002) 180-183
20. Hooft R.W., Vriend G., Sander C., and Abola E.E. Errors in protein structures. Nature 381 (1996) 272
21. Johnstone R.W., Wang J., Tommerup N., Vissing H., Roberts T., and Shi Y. Ciao1 is a novel WD40 protein that interacts with the tumor suppressor protein WT1. J. Biol. Chem. 273 (1998) 10880-10887
22. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47 (1991) 110-119
23. Kabsch W., and Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22 (1983) 2577-2637
24. Kispal G., Csere P., Prohl C., and Lill R. The mitochondrial proteins Atm1p and Nfs1p are required for biogenesis of cytosolic Fe/S proteins. EMBO J. 18 (1999) 3981-3989
25. Kispal G., Sipos K., Lange H., Fekete Z., Bedekovics T., Janaky T., Bassler J., Aguilar Netz D.J., Balk J., Rotte C., et al. Biogenesis of cytosolic ribosomes requires the essential iron-sulphur protein Rli1p and mitochondria. EMBO J. 24 (2005) 589-598
26. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24 (1991) 946-950
27. Krogan N.J., Cagney G., Yu H., Zhong G., Guo X., Ignatchenko A., Li J., Pu S., Datta N., Tikuisis A.P., et al. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440 (2006) 637-643
28. Lambright D.G., Sondek J., Bohm A., Skiba N.P., Hamm H.E., and Sigler P.B. The 2.0 Å crystal structure of a heterotrimeric G protein. Nature 379 (1996) 311-319
29. Landau M., Mayrose I., Rosenberg Y., Glaser F., Martz E., Pupko T., and Ben-Tal N. ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 33 (2005) W299-W302
30. Lange H., Lisowsky T., Gerber J., Mühlenhoff U., Kispal G., and Lill R. An essential function of the mitochondrial sulfhydryl oxidase Erv1p/ALR in the maturation of cytosolic Fe/S proteins. EMBO Rep. 2 (2001) 715-720
31. Laskowski R.A., Moss D.S., and Thornton J.M. Main-chain bond lengths and bond angles in protein structures. J. Mol. Biol. 231 (1993) 1049-1067
32. Lill R., and Mühlenhoff U. Iron-sulfur protein biogenesis in eukaryotes. Trends Biochem. Sci. 30 (2005) 133-141
33. Lill R., and Mühlenhoff U. Iron-sulfur protein biogenesis in eukaryotes: components and mechanisms. Annu. Rev. Cell Dev. Biol. 22 (2006) 457-486
34. Matthews B.W. Solvent content of protein crystals. J. Mol. Biol. 33 (1968) 491-497
35. Merritt E.A., and Murphy M.E. Raster3D Version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 50 (1994) 869-873
36. Morris R.J., Perrakis A., and Lamzin V.S. ARP/wARP and automatic interpretation of protein electron density maps. Methods Enzymol. 374 (2003) 229-244
37. Mühlenhoff U., Richhardt N., Ristow M., Kispal G., and Lill R. The yeast frataxin homologue Yfh1p plays a specific role in the maturation of cellular Fe/S proteins. Hum. Mol. Genet. 11 (2002) 2025-2036
38. Mumberg D., Müller R., and Funk M. Yeast vectors for controlled expression of heterologous proteins in different genetic backgrounds. Gene 156 (1995) 119-122
39. Neer E.J., Schmidt C.J., Nambudripad R., and Smith T.F. The ancient regulatory-protein family of WD-repeat proteins. Nature 371 (1994) 297-300
40. Netz D.J.A., Pierik A.J., Stümpfig M., Mühlenhoff U., and Lill R. The Cfd1-Nbp35 complex acts as a scaffold for iron-sulfur protein assembly in the yeast cytosol. Nat. Chem. Biol. 3 (2007) 278-286
41. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
42. Radford S.J., Goley E., Baxter K., McMahan S., and Sekelsky J. Drosophila ERCC1 is required for a subset of MEI-9-dependent meiotic crossovers. Genetics 170 (2005) 1737-1745
43. Rouault T.A., and Tong W.H. Iron-sulphur cluster biogenesis and mitochondrial iron homeostasis. Nat. Rev. Mol. Cell Biol. 6 (2005) 345-351
44. Roy A., Solodovnikova N., Nicholson T., Antholine W., and Walden W.E. A novel eukaryotic factor for cytosolic Fe-S cluster assembly. EMBO J. 22 (2003) 4826-4835
45. Sambrook J., and Russell D.W. Molecular Cloning: A Laboratory Manual. Third Edition (2001), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
46. Schwede T., Kopp J., Guex N., and Peitsch M.C. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31 (2003) 3381-3385
47. Sheldrick G., and Schneider T. SHELXL: high resolution refinement. Methods Enzymol. 277 (1997) 319-343
48. Sherman F. Getting started with yeast. Methods Enzymol. 194 (1991) 3-21
49. Smith T.F., Gaitatzes C., Saxena K., and Neer E.J. The WD repeat: a common architecture for diverse functions. Trends Biochem. Sci. 24 (1999) 181-185
50. Sondek J., Bohm A., Lambright D.G., Hamm H.E., and Sigler P.B. Crystal structure of a G-protein βγ dimer at 2.1 Å resolution. Nature 379 (1996) 369-374
51. Sprague E.R., Redd M.J., Johnson A.D., and Wolberger C. Structure of the C-terminal domain of Tup1, a corepressor of transcription in yeast. EMBO J. 19 (2000) 3016-3027
52. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
53. Van Duyne G.D., Standaert R.F., Karplus P.A., Schreiber S.L., and Clardy J. Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J. Mol. Biol. 229 (1993) 105-124
54. 2. Cell 83 (1995) 1047-1058
55. Wilson R.B., and Roof D.M. Respiratory deficiency due to loss of mitochondrial DNA in yeast lacking the frataxin homologue. Nat. Genet. 16 (1997) 352-357
56. Wingert R.A., Galloway J.L., Barut B., Foott H., Fraenkel P., Axe J.L., Weber G.J., Dooley K., Davidson A.J., Schmid B., et al. Deficiency of glutaredoxin 5 reveals Fe-S clusters are required for vertebrate haem synthesis. Nature 436 (2005) 1035-1039
57. Yarunin A., Panse V., Petfalski E., Tollervey D., and Hurt E. Functional link between ribosome formation and biogenesis of iron-sulfur proteins. EMBO J. 24 (2005) 580-588