Computational design of a protein crystal

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 19, 2012, Pages 7304-7309

  Lanci, Christopher J ^a   MacDermaid, Christopher M ^a   Kang, Seung Gu ^a   Acharya, Rudresh ^a   North, Benjamin ^a   Yang, Xi ^a   Qiu, X Jade ^a,b   DeGrado, William F ^a,b   Saven, Jeffery G ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Biomaterials; Computational protein design; Crystal engineering; Protein crystallization; Self assembly

Indexed keywords

PROTEIN;

ARTICLE; CRYSTAL STRUCTURE; CRYSTALLIZATION; MODEL; PRIORITY JOURNAL;

COMPUTATIONAL BIOLOGY; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEINS; REPRODUCIBILITY OF RESULTS;

EID: 84860799377     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1112595109     Document Type: Article

References (62)

1. Braga D, Grepioni F, Desiraju G (1998) Crystal engineering and organometallic architecture. Chem Rev 98:1375-1405. (Pubitemid 128635958)
2. Yeates TO, Padilla JE (2002) Designing supramolecular protein assemblies. Curr Opin Struct Biol 12:464-470.
3. Sleytr UB, Sara M, Pum D, Schuster B (2001) Characterization and use of crystalline bacterial cell surface layers. Prog Surf Sci 68:231-278. (Pubitemid 32903623)
4. Hollingsworth MD (2002) Crystal engineering: from structure to function. Science 295:2410-2413.
5. Seeman NC (1982) Nucleic acid junctions and lattices. J Theor Biol 99:237-247.
6. Holman KT, Pivovar AM, Ward MD (2001) Engineering crystal symmetry and polar order in molecular host frameworks. Science 294:1907-1911. (Pubitemid 33101583)
7. Desiraju GR (2007) Crystal engineering: A holistic view. Angewandte Chemie-International Edition 46:8342-8356.
8. Price WN, 2nd, et al. (2009) Understanding the physical properties that control protein crystallization by analysis of large-scale experimental data. Nat Biotechnol 27:51-57.
9. Glaser R (2007) Polar order by rational design: Crystal engineering with parallel beloamphiphile monolayers. Acc Chem Res 40:9-17.
10. Terwilliger TC, Stuart D, Yokoyama S (2009) Lessons from Structural Genomics. Annu Rev Biophys 38:371-383.
11. Chandonia JM, Brenner SE (2006) The impact of structural genomics: Expectations and outcomes. Science 311:347-351.
12. Margolin AL, Navia MA (2001) Protein crystals as novel catalytic materials. Angewandte Chemie-International Edition 40:2204-2222.
13. Derewenda ZS (2010) Application of protein engineering to enhance crystallizability and improve crystal properties. Acta Crystallogr D Biol Crystallogr 66(Pt 5): 604-615.
14. Cooper D, et al. (2007) Protein crystallization by surface entropy reduction: optimization of the SER strategy. Acta Crystallogr D Biol Crystallogr 63(Pt 5):636-645. (Pubitemid 46661535)
15. Goldschmidt L, Cooper DR, Derewenda ZS, Eisenberg D (2007) Toward rational protein crystallization: A Web server for the design of crystallizable protein variants. Protein Sci 16:1569-1576. (Pubitemid 47195684)
16. Banatao DR, et al. (2006) An approach to crystallizing proteins by synthetic symmetrization. Proc Natl Acad Sci USA 103:16230-16235. (Pubitemid 44715179)
17. Andre I, Strauss CEM, Kaplan DB, Bradley P, Baker D (2008) Emergence of symmetry in homooligomeric biological assemblies. Proc Natl Acad Sci USA 105:16148-16152.
18. Yamada H, et al. (2007) 'Crystal lattice engineering', an approach to engineer protein crystal contacts by creating intermolecular symmetry: crystallization and structure determination of a mutant human RNase 1 with a hydrophobic interface of leucines. Protein Sci 16:1389-1397. (Pubitemid 46984873)
19. Zheng J, et al. (2009) From molecular to macroscopic via the rational design of a self-assembled 3D DNA crystal. Nature 461:74-77.
20. Padilla JE, Colovos C, Yeates TO (2001) Nanohedra: using symmetry to design self assembling protein cages, layers, crystals, and filaments. Proc Natl Acad Sci USA 98:2217-2221. (Pubitemid 32209462)
21. Chruszcz M, et al. (2008) Analysis of solvent content and oligomeric states in protein crystals - does symmetry matter? Protein Sci 17:623-632. (Pubitemid 351480856)
22. Kortemme T, Baker D (2004) Computational design of protein-protein interactions. Curr Opin Chem Biol 8:91-97. (Pubitemid 38201483)
23. Kang SG, Saven JG (2007) Computational protein design: structure, function and combinatorial diversity. Curr Opin Chem Biol 11:329-334.
24. Grigoryan G, Reinke AW, Keating AE (2009) Design of protein-interaction specificity gives selective bZIP-binding peptides. Nature 458:859-U852.
25. Jha RK, et al. (2010) Computational design of a PAK1 binding protein. J Mol Biol 400:257-270.
26. Friedland GD, Kortemme T (2010) Designing ensembles in conformational and sequence space to characterize and engineer proteins. Curr Opin Struct Biol 20:377-384.
27. Samish I, MacDermaid CM, Perez-Aguilar JM, Saven JG (2011) Theoretical and computational protein design. Annu Rev Phys Chem 62:129-149.
28. Khersonsky O, et al. (2011) Optimization of the in-silico-designed Kemp eliminase KE70 by computational design and directed evolution. J Mol Biol 407:391-412.
29. Fleishman SJ, et al. (2011) Computational design of proteins targeting the conserved stem region of influenza hemagglutinin. Science 332:816-821.
30. Calhoun JR, et al. (2003) Computational design and characterization of a monomeric helical dinuclear metalloprotein. J Mol Biol 334:1101-1115. (Pubitemid 37485692)
31. Kono H, Saven JG (2001) Statistical theory for protein combinatorial libraries. Packing interactions, backbone flexibility, and the sequence variability of a main-chain structure. J Mol Biol 306:607-628. (Pubitemid 33027726)
32. Butterfoss GL, Kuhlman B (2006) Computer-based design of novel protein structures. Annu Rev Bioph Biom 35:49-65. (Pubitemid 43877369)
33. Grigoryan G, Keating AE (2008) Structural specificity in coiled-coil interactions. Curr Opin Struc Biol 18:477-483.
34. Ghirlanda G, Lear JD, Ogihara NL, Eisenberg D, DeGrado WF (2002) A hierarchic approach to the design of hexameric helical barrels. J Mol Biol 319:243-253. (Pubitemid 34729499)
35. Grigoryan G, et al. (2011) Computational design of virus-like protein assemblies on carbon nanotube surfaces. Science 332:1071-1076.
36. North B, Summa CM, Ghirlanda G, DeGrado WF (2001) D(n)-symmetrical tertiary templates for the design of tubular proteins. J Mol Biol 311:1081-1090. (Pubitemid 32803722)
37. Gonzalez L, Jr, Brown RA, Richardson D, Alber T (1996) Crystal structures of a single coiled-coil peptide in two oligomeric states reveal the basis for structural polymorphism. Nat Struct Biol 3:1002-1009.
38. Gonzalez L, Jr, Plecs JJ, Alber T (1996) An engineered allosteric switch in leucine-zipper oligomerization. Nat Struct Biol 3:510-515. (Pubitemid 26174699)
39. Ogihara NL, Weiss MS, Degrado WF, Eisenberg D (1997) The crystal structure of the designed trimeric coiled coil coil-VaLd: implications for engineering crystals and supramolecular assemblies. Protein Sci 6:80-88. (Pubitemid 27045246)
40. Wukovitz SW, Yeates TO (1995) Why protein crystals favour some space-groups over others. Nat Struct Biol 2:1062-1067.
41. Duan Y, et al. (2003) A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J Comput Chem 24:1999-2012.
42. Fu X, Kono H, Saven JG (2003) Probabilistic approach to the design of symmetric protein quaternary structures. Protein Eng 16:971-977. (Pubitemid 38281747)
43. Yang X, Saven JG (2005) Computational methods for protein design and protein sequence variability: Biased Monte Carlo and replica exchange. Chem Phys Lett 401:205-210.
44. Kim S, et al. (2005) Transmembrane glycine zippers: physiological and pathological roles in membrane proteins. Proc Natl Acad Sci USA 102:14278-14283. (Pubitemid 41429689)
45. Senes A, Gerstein M, Engelman DM (2000) Statistical analysis of amino acid patterns in transmembrane helices: The GxxxG motif occurs frequently and in association with beta-branched residues at neighboring positions. J Mol Biol 296:921-936.
46. Walters RFS, DeGrado WF (2006) Helix-packing motifs in membrane proteins. Proc Natl Acad Sci USA 103:13658-13663. (Pubitemid 44413963)
47. Bender GM, et al. (2007) De novo design of a single-chain diphenylporphyrin metalloprotein. J Am Chem Soc 129:10732-10740. (Pubitemid 350067483)
48. Zou JM, Saven JG (2000) Statistical theory of combinatorial libraries of folding proteins: Energetic discrimination of a target structure. J Mol Biol 296:281-294.
49. O'Neil KT, DeGrado WF (1990) A thermodynamic scale for the helix-forming tendencies of the commonly occurring amino acids. Science 250:646-651. (Pubitemid 120034280)
50. Kleiger G, Eisenberg D (2002) GXXXG and GXXXA motifs stabilize FAD and NAD(P)- binding Rossmann folds through C-alpha-H center dot center dot center dot O hydrogen bonds and van der Waals interactions. J Mol Biol 323:69-76. (Pubitemid 35168480)
51. Moore DT, Berger BW, DeGrado WF (2008) Protein-protein interactions in the membrane: sequence, structural, and biological motifs. Structure 16:991-1001. (Pubitemid 351899292)
52. Dasgupta S, Iyer GH, Bryant SH, Lawrence CE, Bell JA (1997) Extent and nature of contacts between protein molecules in crystal lattices and between subunits of protein oligomers. Proteins 28:494-514. (Pubitemid 27328566)
53. Juers DH, Matthews BW (2001) Reversible lattice repacking illustrates the temperature dependence of macromolecular interactions. J Mol Biol 311:851-862. (Pubitemid 32803740)
54. Derewenda Z (2004) Rational protein crystallization by mutational surface engineering. Structure 12:529-535.
55. Matthews BW (1968) Solvent content of protein crystals. J Mol Biol 33:491-497.
56. Kantardjieff KA, Rupp B (2003) Matthews coefficient probabilities: Improved estimates for unit cell contents of proteins, DNA, and protein-nucleic acid complex crystals. Protein Sci 12:1865-1871. (Pubitemid 37022809)
57. Derewenda Z, et al. (2007) Protein crystallization by surface entropy reduction: optimization of the SER strategy. Acta Crystallogr D 63:636-645. (Pubitemid 46661535)
58. Grueninger D, et al. (2008) Designed protein-protein association. Science 319:206-209.
59. Derewenda Z, Vekilov P (2006) Entropy and surface engineering in protein crystallization. Acta Crystallogr D 62:116-124.
60. MacKerell AD, et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102:3586-3616.
61. Mackerell AD, Feig M, Brooks CL (2004) Extending the treatment of backbone energetics in protein force fields: Limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J Comput Chem 25:1400-1415.
62. Dunbrack RL, Karplus M (1993) Backbone-dependent rotamer library for proteins - application to side-chain prediction. J Mol Biol 230:543-574.