Strategies for crystallization and structure determination of very large macromolecular assemblies

Current Opinion in Structural Biology

Volumn 17, Issue 5, 2007, Pages 572-579

  Mueller, Marcus ^a   Jenni, Simon ^a   Ban, Nenad ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

FAS ANTIGEN; RNA POLYMERASE;

CRYSTAL STRUCTURE; CRYSTALLIZATION; ELECTRON MICROSCOPY; IMAGE ANALYSIS; MACROMOLECULE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PURIFICATION; PROTEIN STRUCTURE; REVIEW; ROBOTICS; TEMPERATURE SENSITIVITY; X RAY CRYSTALLOGRAPHY; X RAY DIFFRACTION;

CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; ELECTROSTATICS; FATTY ACID SYNTHETASE COMPLEX, TYPE II; MACROMOLECULAR SUBSTANCES; MODELS, MOLECULAR; MOLECULAR STRUCTURE; MURAMIDASE; RNA POLYMERASE II;

EID: 35548958606     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2007.09.004     Document Type: Review

References (51)

1. Rossmann M.G. Ab-initio phase determination and phase extension using non-crystallographic symmetry. Curr Opin Struct Biol 5 (1995) 650-655
2. Baker T.S., and Johnson J.E. Principles of virus structure determination. In: Chui W., Burnett R.M., and Garcea R.L. (Eds). Structural Biology of Viruses (1997), Oxford University Press 38-79
3. Jenni S., Leibundgut M., Boehringer D., Frick C., Mikolasek B., and Ban N. Structure of fungal fatty acid synthase and implications for iterative substrate shuttling. Science 316 (2007) 254-261
4. Clemons W.M., Brodersen D.E., McCutcheon J.P., May J.L.C., Carter A.P., Morgan-Warren R.J., Wimberly B.T., and Ramakrishnan V. Crystal structure of the 30 S ribosomal subunit from Thermus thermophilus: purification, crystallization and structure determination. J Mol Biol 310 (2001) 827-843. This detailed paper provides a wealth of information about the biochemical and crystallographic procedures used for the structure determination of the small ribosomal subunit.
5. Schuwirth B.S., Borovinskaya M.A., Hau C.W., Zhang W., Vila-Sanjurjo A., Holton J.M., and Cate J.H.D. Structures of the bacterial ribosome at 3.5 Å resolution. Science 310 (2005) 827-834
6. Selmer M., Dunham C.M., Murphy F.V., Weixlbaumer A., Petry S., Kelley A.C., Weir J.R., and Ramakrishnan V. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313 (2006) 1935-1942
7. Maier T., Jenni S., and Ban N. Architecture of mammalian fatty acid synthase at 4.5 Å resolution. Science 311 (2006) 1258-1262
8. Heras B., and Martin J.L. Post-crystallization treatments for improving diffraction quality of protein crystals. Acta Crystallogr D Biol Crystallogr 61 (2005) 1173-1180. This review provides a comprehensive overview of postcrystallization methods that can significantly improve diffraction quality of crystals. Protocols for annealing, dehydration, soaking, and crosslinking are outlined and examples for their successful application are provided.
9. Cramer P., Bushnell D.A., and Kornberg R.D. Structural basis of transcription: RNA polymerase II at 2.8 Å resolution. Science 292 (2001) 1863-1876. This paper describes the structure determination of a 470 kDa RNA polymerase. Many examples for the application of methods discussed in this review, such as postcrystallization treatments or sequence markers to trace the polypeptide chain, are described.
10. Garman E. 'Cool' crystals: macromolecular cryocrystallography and radiation damage. Curr Opin Struct Biol 13 (2003) 545-551
11. Kriminski S., Caylor C.L., Nonato M.C., Finkelstein K.D., and Thorne R.E. Flash-cooling and annealing of protein crystals. Acta Crystallogr D Biol Crystallogr 58 (2002) 459-471
12. Mueller D.M., Puri N., Kabaleeswaran V., Terry C., Leslie A.G.W., and Walker J.E. Crystallization and preliminary crystallographic studies of the mitochondrial F-1-ATPase from the yeast Saccharomyces cerevisiae. Acta Crystallogr D Biol Crystallogr 60 (2004) 1441-1444
13. Ban N., Nissen P., Hansen J., Moore P.B., and Steitz T.A. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289 (2000) 905-920
14. Cramer P., Bushnell D.A., Fu J.H., Gnatt A.L., Maier-Davis B., Thompson N.E., Burgess R.R., Edwards A.M., David P.R., and Kornberg R.D. Architecture of RNA polymerase II and implications for the transcription mechanism. Science 288 (2000) 640-649
15. Brueckner F., Hennecke U., Carell T., and Cramer P. CPD damage recognition by transcribing RNA polymerase II. Science 315 (2007) 859-862
16. Southworth-Davies R.J., and Garman E.F. Radioprotectant screening for cryocrystallography. J Synchrot Radiat 14 (2007) 73-83
17. Kauffmann B., Weiss M.S., Lamzin V.S., and Schmidt A. How to avoid premature decay of your macromolecular crystal: a quick soak for long life. Structure 14 (2006) 1099-1105
18. Kettenberger H., Armache K.J., and Cramer P. Architecture of the RNA polymerase II-TFIIS complex and implications for mRNA cleavage. Cell 114 (2003) 347-357
19. Broennimann C., Eikenberry E.F., Henrich B., Horisberger R., Huelsen G., Pohl E., Schmitt B., Schulze-Briese C., Suzuki M., Tomizaki T., et al. The PILATUS 1M detector. J Synchrot Radiat 13 (2006) 120-130
20. Dauter Z. Data-collection strategies. Acta Crystallogr D Biol Crystallogr 55 (1999) 1703-1717
21. Leibundgut M., Jenni S., Frick C., and Ban N. Structural basis for substrate delivery by acyl carrier protein in the yeast fatty acid synthase. Science 316 (2007) 288-290
22. Abrahams J.P., and Ban N. X-ray crystallographic structure determination of large asymmetric macromolecular assemblies. Methods Enzymol 374 (2003) 163-188. This review describes strategies for structure determination of large asymmetric assemblies and highlights the power of solvent flipping in large unit cells. The theoretical basis of this phenomenon is provided and the practical aspects are illustrated with the large ribosomal subunit as an example.
23. Berk V., Zhang W., Pai R.D., and Cate J.H.D. Structural basis for mRNA and tRNA positioning on the ribosome. Proc Natl Acad Sci U S A 103 (2006) 15830-15834
24. Petry S., Brodersen D.E., Murphy F.V., Dunham C.M., Selmer M., Tarry M.J., Kelley A.C., and Ramakrishnan V. Crystal structures of the ribosome in complex with release factors RF1 and RF2 bound to a cognate stop codon. Cell 123 (2005) 1255-1266
25. Schalch T., Duda S., Sargent D.F., and Richmond T.J. X-ray structure of a tetranucleosome and its implications for the chromatin fibre. Nature 436 (2005) 138-141
26. Ravelli R.B.G., Nanao M.H., Lovering A., White S., and McSweeney S. Phasing in the presence of radiation damage. J Synchrot Radiat 12 (2005) 276-284. In this paper, the influence of radiation damage on phasing by anomalous dispersion is systematically investigated. Datasets with different degrees of radiation damage and redundancy as well as zero-dose extrapolated and constant-dose interpolated datasets are compared by their statistics for substructure determination and phasing. The paper provides valuable insights on how redundancy and radiation damage influence structure determination.
27. Gonzalez A. Optimizing data collection for structure determination. Acta Crystallogr D Biol Crystallogr 59 (2003) 1935-1942
28. Cate J.H., Yusupov M.M., Yusupova G.Z., Earnest T.N., and Noller H.F. X-ray crystal structures of 70S ribosome functional complexes. Science 285 (1999) 2095-2104
29. Tang Y.Y., Kim C.Y., Mathews I.I., Cane D.E., and Khosla C. The 2.7 Å crystal structure of a 194-kDa homodimeric fragment of the 6-deoxyerythronolide B synthase. Proc Natl Acad Sci U S A 103 (2006) 11124-11129. This paper is a remarkable example of multiwavelength anomalous dispersion phasing in a large asymmetric unit. At 4.7 Å resolution 85 selenium sites were found in an asymmetric unit containing 582 kDa of protein.
30. Rice L.M., Earnest T.N., and Brunger A.T. Single-wavelength anomalous diffraction phasing revisited. Acta Crystallogr D Biol Crystallogr 56 (2000) 1413-1420
31. Abrahams J.P., Lutter R., Todd R.J., van Raaij M.J., Leslie A.G., and Walker J.E. Inherent asymmetry of the structure of F1-ATPase from bovine heart mitochondria at 6.5 Å resolution. EMBO J 12 (1993) 1775-1780
32. Ban N., Freeborn B., Nissen P., Penczek P., Grassucci R.A., Sweet R., Frank J., Moore P.B., and Steitz T.A. A 9 Å resolution X-ray crystallographic map of the large ribosomal subunit. Cell 93 (1998) 1105-1115
33. Ban N., Nissen P., Hansen J., Capel M., Moore P.B., and Steitz T.A. Placement of protein and RNA structures into a 5 Å-resolution map of the 50S ribosomal subunit. Nature 400 (1999) 841-847
34. Clemons Jr. W.M., May J.L., Wimberly B.T., McCutcheon J.P., Capel M.S., and Ramakrishnan V. Structure of a bacterial 30S ribosomal subunit at 5.5 Å resolution. Nature 400 (1999) 833-840
35. Murakami K.S., Masuda S., Campbell E.A., Muzzin O., and Darst S.A. Structural basis of transcription initiation: an RNA polymerase holoenzyme-DNA complex. Science 296 (2002) 1285-1290
36. Ben-Shem A., Frolow F., and Nelson N. Crystal structure of plant photosystem I. Nature 426 (2003) 630-635
37. Jenni S., Leibundgut M., Maier T., and Ban N. Architecture of a fungal fatty acid synthase at 5 Å resolution. Science 311 (2006) 1263-1267. This paper describes the structure determination of a 2.6 MDa complex at medium resolution. In this case, it was possible to comprehensively interpret medium resolution maps using structures previously determined at high resolution and to establish the overall architecture of the complex. Valuable information about the structure determination is provided in the supplementary material accompanying this paper.
38. McCoy A.J. Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr D Biol Crystallogr 63 (2007) 32-41
39. Janssen B.J., Christodoulidou A., McCarthy A., Lambris J.D., and Gros P. Structure of C3b reveals conformational changes that underlie complement activity. Nature 444 (2006) 213-216
40. Dauter Z. Use of polynuclear metal clusters in protein crystallography. C R Chim 8 (2005) 1808-1814. Heavy atom clusters are particularly useful for phasing large macromolecular complexes. This review discusses the diffraction properties of metal clusters and provides a compilation of clusters which have been successfully used for structure determination together with examples of their application.
41. Schneider T.R., and Sheldrick G.M. Substructure solution with SHELXD. Acta Crystallogr D Biol Crystallogr 58 (2002) 1772-1779
42. Weeks C.M., and Miller R. The design and implementation of SnB version 2.0. J Appl Crystallogr 32 (1999) 120-124
43. Matthews B.W. Five retracted structure reports: inverted or incorrect?. Protein Sci 16 (2007) 1013-1016
44. Furnham N., Dore A.S., Chirgadze D.Y., de Bakker P.I., Depristo M.A., and Blundell T.L. Knowledge-based real-space explorations for low-resolution structure determination. Structure 14 (2006) 1313-1320
45. Brunger A.T. Low-resolution crystallography is coming of age. Structure 13 (2005) 171-172
46. Rees B., Jenner L., and Yusupov M. Bulk-solvent correction in large macromolecular structures. Acta Crystallogr D Biol Crystallogr 61 (2005) 1299-1301
47. Afonine P.V., Grosse-Kunstleve R.W., and Adams P.D. A robust bulk-solvent correction and anisotropic scaling procedure. Acta Crystallogr D Biol Crystallogr 61 (2005) 850-855
48. Afonine P.V., Grosse-Kunstleve R.W., and Adams P.D. The Phenix refinement framework. CCP4 Newslett 42 (2005) 8
49. Lomakin I.B., Xiong Y., and Steitz T.A. The crystal structure of yeast fatty acid synthase, a cellular machine with eight active sites working together. Cell 129 (2007) 319-332
50. Bass R.B., Strop P., Barclay M., and Rees D.C. Crystal structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel. Science 298 (2002) 1582-1587
51. Bushnell D.A., Cramer P., and Kornberg R.D. Selenomethionine incorporation in Saccharomyces cerevisiae RNA polymerase II. Structure 9 (2001) R11-R14