De novo design of a four-fold symmetric TIM-barrel protein with atomic-level accuracy

Nature Chemical Biology

Volumn 12, Issue 1, 2016, Pages 29-34

  Huang, Po Ssu ^a,b   Feldmeier, Kaspar ^c   Parmeggiani, Fabio ^a,b   Velasco, Dalejandro Fernandez ^d   Hocker, Birte ^c   Baker, David ^a,b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^d UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; PROTEIN; PROTEIN STIM 11; TRIOSEPHOSPHATE ISOMERASE; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; FLUORESCENCE SPECTROSCOPY; GEOMETRY; HYDROGEN BOND; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; THERMODYNAMICS; CHEMISTRY; CIRCULAR DICHROISM; MOLECULAR MODEL; PROCEDURES; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN FOLDING; SYNTHESIS; X RAY CRYSTALLOGRAPHY;

CIRCULAR DICHROISM; CRYSTALLOGRAPHY, X-RAY; HYDROGEN BONDING; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEINS;

EID: 84950276750     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1966     Document Type: Article

References (40)

1. Kuhlman, B. et al. Design of a novel globular protein fold with atomic-level accuracy. Science 302, 1364-1368 (2003).
2. Huang, P.-S. et al. High thermodynamic stability of parametrically designed helical bundles. Science 346, 481-485 (2014).
3. Joh, N.H. et al. De novo design of a transmembrane Zn2+-transporting four-helix bundle. Science 346, 1520-1524 (2014).
4. Koga, N. et al. Principles for designing ideal protein structures. Nature 491, 222-227 (2012).
5. Smadbeck, J. et al. De novo design and experimental characterization of ultrashort self-associating peptides. PLOS Comput. Biol. 10, e1003718 (2014).
6. Bellows-Peterson, M.L. et al. De novo peptide design with C3a receptor agonist and antagonist activities: theoretical predictions and experimental validation. J. Med. Chem. 55, 4159-4168 (2012).
7. Khoury, G.A., Smadbeck, J., Kieslich, C.A. &Floudas, C.A. Protein folding and de novo protein design for biotechnological applications. Trends Biotechnol. 32, 99-109 (2014).
8. Correia, B.E. et al. Proof of principle for epitope-focused vaccine design. Nature 507, 201-206 (2014).
9. Sterner, R. &Hocker, B. Catalytic versatility, stability, and evolution of the (βα)8-barrel enzyme fold. Chem. Rev. 105, 4038-4055 (2005).
10. Gerlt, J.A. New wine from old barrels. Nat. Struct. Biol. 7, 171-173 (2000).
11. Hcker, B. Directed evolution of 8-barrel enzymes. Biomol. Eng. 22, 31-38 (2005).
12. Kiss, G., Celebi Olcum, N., Moretti, R., Baker, D. &Houk, K.N. Computational enzyme design. Angew. Chem. Int. Ed. Engl. 52, 5700-5725 (2013).
13. Hocker, B., Claren, J. &Sterner, R. Mimicking enzyme evolution by generating new (βα)8-barrels from (βα)4-half-barrels. Proc. Natl. Acad. Sci. USA 101, 16448-16453 (2004).
14. Hcker, B., Lochner, A., Seitz, T., Claren, J. &Sterner, R. High-resolution crystal structure of an artificial (βα)8-barrel protein designed from identical half-barrels. Biochemistry 48, 1145-1147 (2009).
15. Claren, J., Malisi, C., H?cker, B. &Sterner, R. Establishing wild-type levels of catalytic activity on natural and artificial (βα)8-barrel protein scaffolds. Proc. Natl. Acad. Sci. USA 106, 3704-3709 (2009).
16. Fortenberry, C. et al. Exploring symmetry as an avenue to the computational design of large protein domains. J. Am. Chem. Soc. 133, 18026-18029 (2011).
17. Goraj, K., Renard, A. &Martial, J.A. Synthesis, purification and initial structural characterization of octarellin, a de novo polypeptide modelled on the /β-barrel Proteins. Protein Eng. 3, 259-266 (1990).
18. Houbrechts, A. et al. Second-generation octarellins: two new de novo (β/α)8 polypeptides designed for investigating the influence of β-residue packing on the α/β-barrel structure stability. Protein Eng. 8, 249-259 (1995).
19. Tanaka, T. et al. Characteristics of a de novo designed protein. Protein Sci. 3, 419-427 (1994).
20. Offredi, F. et al. De novo backbone and sequence design of an idealized α/β-barrel protein: evidence of stable tertiary structure. J. Mol. Biol. 325, 163-174 (2003).
21. Figueroa, M. et al. Octarellin VI: using Rosetta to design a putative artificial (β/α)8 protein. PLoS ONE 8, e71858 (2013).
22. Nagarajan, D., Deka, G. &Rao, M. Design of symmetric TIM barrel proteins from first principles. BMC Biochem. 16, 18 (2015).
23. Murzin, A.G., Lesk, A.M. &Chothia, C. Principles determining the structure of β-sheet barrels in proteins I. A theoretical analysis. J. Mol. Biol. 236, 1369-1381 (1994).
24. Ochoa-Leyva, A. et al. Exploring the structure-function loop adaptability of a (β/α)8-barrel enzyme through loop swapping and hinge variability. J. Mol. Biol. 411, 143-157 (2011).
25. Ochoa-Leyva, A. et al. Protein design through systematic catalytic loop exchange in the (β/α)8 fold. J. Mol. Biol. 387, 949-964 (2009).
26. Huang, P.-S. et al. RosettaRemodel: a generalized framework for flexible backbone protein design. PLoS ONE 6, e24109 (2011).
27. Parmeggiani, F. et al. A general computational approach for repeat protein design. J. Mol. Biol. 427, 563-575 (2015).
28. Yang, X., Kathuria, S.V., Vadrevu, R. &Matthews, C.R. βα-hairpin clamps brace βαβ modules and can make substantive contributions to the stability of TIM barrel proteins. PLoS ONE 4, e7179 (2009).
29. Hocker, B., Beismann-Driemeyer, S., Hettwer, S., Lustig, A. &Sterner, R. Dissection of a (βα)8-barrel enzyme into two folded halves. Nat. Struct. Biol. 8, 32-36 (2001).
30. Romero-Romero, S., Costas, M., Rodriguez-Romero, A. &Fernández-Velasco, D.A. Reversibility and two state behaviour in the thermal unfolding of oligomeric TIM barrel proteins. Phys. Chem. Chem. Phys. 17, 20699-20714 (2015).
31. Zhang, Y. &Skolnick, J. TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Res. 33, 2302-2309 (2005).
32. Minami, S., Sawada, K. &Chikenji, G. MICAN: a protein structure alignment algorithm that can handle multiple-chains, inverse alignments, C(α) only models, alternative alignments, and non-sequential alignments. BMC Bioinformatics 14, 24 (2013).
33. Altschul, S.F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 (1997).
34. Söding, J. Protein homology detection by HMM-HMM comparison. Bioinformatics 21, 951-960 (2005).
35. Remmert, M., Biegert, A., Hauser, A. &Söding, J. HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment. Nat. Methods 9, 173-175 (2012).
36. Farias-Rico, J.A., Schmidt, S. &Höcker, B. Evolutionary relationship of two ancient protein superfolds. Nat. Chem. Biol. 10, 710-715 (2014).
37. Alva, V., Remmert, M., Biegert, A., Lupas, A.N. &Söding, J. A galaxy of folds. Protein Sci. 19, 124-130 (2010).
38. Ramisch, S., Weininger, U., Martinsson, J., Akke, M. &Andre, I. Computational design of a leucine-rich repeat protein with a predefined geometry. Proc. Natl. Acad. Sci. USA 111, 17875-17880 (2014).
39. Giger, L. et al. Evolution of a designed retro-aldolase leads to complete active site remodeling. Nat. Chem. Biol. 9, 494-498 (2013).
40. Kabsch, W. &Sander, C. Dictionary of protein secondary structure-pattern-recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637 (1983).