Using natural sequences and modularity to design common and novel protein topologies

Current Opinion in Structural Biology

Volumn 38, Issue , 2016, Pages 26-36

  Broom, Aron ^a   Trainor, Kyle ^a   MacKenzie, Duncan W S ^a   Meiering, Elizabeth M ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR; PROTEIN;

AMINO ACID SEQUENCE; BINDING AFFINITY; LIGAND BINDING; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW; SEQUENCE ALIGNMENT; SIMULATION; STRUCTURE ANALYSIS; THERMODYNAMICS; BIOLOGY; CHEMISTRY; GENETICS; PROCEDURES; PROTEIN ENGINEERING;

AMINO ACID SEQUENCE; COMPUTATIONAL BIOLOGY; PROTEIN ENGINEERING; PROTEINS;

EID: 84971646097     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2016.05.007     Document Type: Review

References (93)

1. Privett H.K., Kiss G., Lee T.M., Blomberg R., Chica R.A., Thomas L.M., Hilvert D., Houk K.N., Mayo S.L. Iterative approach to computational enzyme design. Proc Natl Acad Sci U S A 2012, 109:3790-3795.
2. Zhou H.X., Cross T.A. Influences of membrane mimetic environments on membrane protein structures. Annu Rev Biophys 2013, 42:361-392.
3. Kolodny R., Pereyaslavets L., Samson A.O., Levitt M. On the universe of protein folds. Annu Rev Biophys 2013, 42:559-582.
4. Dahiyat B.I., Mayo S.L. De novo protein design: fully automated sequence selection. Science 1997, 278:82-87.
5. Dantas G., Kuhlman B., Callender D., Wong M., Baker D. A large scale test of computational protein design: folding and stability of nine completely redesigned globular proteins. J Mol Biol 2003, 332:449-460.
6. Watters A.L., Deka P., Corrent C., Callender D., Varani G., Sosnick T., Baker D. The highly cooperative folding of small naturally occurring proteins is likely the result of natural selection. Cell 2007, 128:613-624.
7. Thomson A.R., Wood C.W., Burton A.J., Bartlett G.J., Sessions R.B., Brady R.L., Woolfson D.N. Computational design of water-soluble alpha-helical barrels. Science 2014, 346:485-488.
8. Taylor W.R. A 'periodic table' for protein structures. Nature 2002, 416:657-660.
9. Huang P.S., Oberdorfer G., Xu C., Pei X.Y., Nannenga B.L., Rogers J.M., DiMaio F., Gonen T., Luisi B., Baker D. High thermodynamic stability of parametrically designed helical bundles. Science 2014, 346:481-485.
10. Park K., Shen B.W., Parmeggiani F., Huang P.S., Stoddard B.L., Baker D. Control of repeat-protein curvature by computational protein design. Nat Struct Mol Biol 2015, 22:167-174.
11. Brunette T.J., Parmeggiani F., Huang P.S., Bhabha G., Ekiert D.C., Tsutakawa S.E., Hura G.L., Tainer J.A., Baker D. Exploring the repeat protein universe through computational protein design. Nature 2015, 528:580-584.
12. Woolfson D.N., Bartlett G.J., Burton A.J., Heal J.W., Niitsu A., Thomson A.R., Wood C.W. De novo protein design: how do we expand into the universe of possible protein structures?. Curr Opin Struct Biol 2015, 33:16-26.
13. Currin A., Swainston N., Day P.J., Kell D.B. Synthetic biology for the directed evolution of protein biocatalysts: navigating sequence space intelligently. Chem Soc Rev 2015, 44:1172-1239.
14. Jacobs S.A., Diem M.D., Luo J., Teplyakov A., Obmolova G., Malia T., Gilliland G.L., O'Neil K.T. Design of novel FN3 domains with high stability by a consensus sequence approach. Protein Eng Des Sel 2012, 25:107-117.
15. Porebski B.T., Nickson A.A., Hoke D.E., Hunter M.R., Zhu L., McGowan S., Webb G.I., Buckle A.M. Structural and dynamic properties that govern the stability of an engineered fibronectin type III domain. Protein Eng Des Sel 2015, 28:67-78.
16. Aerts D., Verhaeghe T., Joosten H.J., Vriend G., Soetaert W., Desmet T. Consensus engineering of sucrose phosphorylase: the outcome reflects the sequence input. Biotechnol Bioeng 2013, 110:2563-2572.
17. Risso V.A., Gavira J.A., Gaucher E.A., Sanchez-Ruiz J.M. Phenotypic comparisons of consensus variants versus laboratory resurrections of Precambrian proteins. Proteins 2014, 82:887-896.
18. Wheeler LC, Limc SA, Marqusee S, Harms MJ: The thermostability and specificity of ancient proteins. Curr Opin Struct Biol in press. doi:10.1016/j.sbi.2016.05.015.
19. Lees JG, Dawson NL, Sillitoe I, Orengo CA: Functional innovation from changes in protein domains and their combinations. Curr Opin Struct Biol in press. doi:10.1016/j.sbi.2016.05.016.
20. Toth-Petroczy A., Tawfik D.S. The robustness and innovability of protein folds. Curr Opin Struct Biol 2014, 26:131-138.
21. Rockah-Shmuel L., Toth-Petroczy A., Tawfik D.S. Systematic mapping of protein mutational space by prolonged drift reveals the deleterious effects of seemingly neutral mutations. PLoS Comput Biol 2015, 11:e1004421.
22. Magliery T.J. Protein stability: computation, sequence statistics, and new experimental methods. Curr Opin Struct Biol 2015, 33:161-168.
23. Halabi N., Rivoire O., Leibler S., Ranganathan R. Protein sectors: evolutionary units of three-dimensional structure. Cell 2009, 138:774-786.
24. Marks D.S., Hopf T.A., Sander C. Protein structure prediction from sequence variation. Nat Biotechnol 2012, 30:1072-1080.
25. Sullivan B.J., Nguyen T., Durani V., Mathur D., Rojas S., Thomas M., Syu T., Magliery T.J. Stabilizing proteins from sequence statistics: the interplay of conservation and correlation in triosephosphate isomerase stability. J Mol Biol 2012, 420:384-399.
26. Murphy G.S., Mills J.L., Miley M.J., Machius M., Szyperski T., Kuhlman B. Increasing sequence diversity with flexible backbone protein design: the complete redesign of a protein hydrophobic core. Structure 2012, 20:1086-1096.
27. Koga N., Tatsumi-Koga R., Liu G., Xiao R., Acton T.B., Montelione G.T., Baker D. Principles for designing ideal protein structures. Nature 2012, 491:222-227.
28. Soding J., Lupas A.N. More than the sum of their parts: on the evolution of proteins from peptides. Bioessays 2003, 25:837-846.
29. Nepomnyachiy S., Ben-Tal N., Kolodny R. Global view of the protein universe. Proc Natl Acad Sci U S A 2014, 111:11691-11696.
30. Pitman D.J., Schenkelberg C.D., Huang Y.M., Teets F.D., Ditursi D., Bystroff C. Improving computational efficiency and tractability of protein design using a piecemeal approach. A strategy for parallel and distributed protein design. Bioinformatics 2014, 30:1138-1145.
31. Balaji S. Internal symmetry in protein structures: prevalence, functional relevance and evolution. Curr Opin Struct Biol 2015, 32:156-166.
32. Broom A., Doxey A.C., Lobsanov Y.D., Berthin L.G., Rose D.R., Howell P.L., McConkey B.J., Meiering E.M. Modular evolution and the origins of symmetry: reconstruction of a three-fold symmetric globular protein. Structure 2012, 20:161-171.
33. Voet A.R., Noguchi H., Addy C., Simoncini D., Terada D., Unzai S., Park S.Y., Zhang K.Y., Tame J.R. Computational design of a self-assembling symmetrical beta-propeller protein. Proc Natl Acad Sci U S A 2014, 111:15102-15107.
34. Huang P.S., Feldmeier K., Parmeggiani F., Fernandez Velasco D.A., Hocker B., Baker D. De novo design of a four-fold symmetric TIM-barrel protein with atomic-level accuracy. Nat Chem Biol 2016, 12:29-34.
35. Parmeggiani F., Huang P.S., Vorobiev S., Xiao R., Park K., Caprari S., Su M., Seetharaman J., Mao L., Janjua H., et al. A general computational approach for repeat protein design. J Mol Biol 2015, 427:563-575.
36. Orengo C.A., Jones D.T., Thornton J.M. Protein superfamilies and domain superfolds. Nature 1994, 372:631-634.
37. Lobb B, Doxey AC: Novel function discovery through sequence and structural data mining. Curr Opin Struct Biol in press. doi:10.1016/j.sbi.2016.05.017.
38. Hocker B. Design of proteins from smaller fragments-learning from evolution. Curr Opin Struct Biol 2014, 27:56-62.
39. Bharat T.A., Eisenbeis S., Zeth K., Hocker B. A beta alpha-barrel built by the combination of fragments from different folds. Proc Natl Acad Sci U S A 2008, 105:9942-9947.
40. Hocker B., Claren J., Sterner R. Mimicking enzyme evolution by generating new (betaalpha)8-barrels from (betaalpha)4-half-barrels. Proc Natl Acad Sci U S A 2004, 101:16448-16453.
41. Richter M., Bosnali M., Carstensen L., Seitz T., Durchschlag H., Blanquart S., Merkl R., Sterner R. Computational and experimental evidence for the evolution of a (beta alpha)8-barrel protein from an ancestral quarter-barrel stabilised by disulfide bonds. J Mol Biol 2010, 398:763-773.
42. Smock R.G., Yadid I., Dym O., Clarke J., Tawfik D.S. De novo evolutionary emergence of a symmetrical protein is shaped by folding constraints. Cell 2016, 164:476-486.
43. Voigt C.A., Martinez C., Wang Z.G., Mayo S.L., Arnold F.H. Protein building blocks preserved by recombination. Nat Struct Biol 2002, 9:553-558.
44. Trudeau D.L., Smith M.A., Arnold F.H. Innovation by homologous recombination. Curr Opin Chem Biol 2013, 17:902-909.
45. Kufner K., Lipps G. Construction of a chimeric thermoacidophilic beta-endoglucanase. BMC Biochem 2013, 14:11.
46. van Beek H.L., de Gonzalo G., Fraaije M.W. Blending Baeyer-Villiger monooxygenases: using a robust BVMO as a scaffold for creating chimeric enzymes with novel catalytic properties. Chem Commun (Camb) 2012, 48:3288-3290.
47. Zhou X., Gao L., Yang G., Liu D., Bai A., Li B., Deng Z., Feng Y. Design of hyperthermophilic lipase chimeras by key motif-directed recombination. Chembiochem 2015, 16:455-462.
48. Gobeil S.M., Clouthier C.M., Park J., Gagne D., Berghuis A.M., Doucet N., Pelletier J.N. Maintenance of native-like protein dynamics may not be required for engineering functional proteins. Chem Biol 2014, 21:1330-1340.
49. Rogers R.L., Hartl D.L. Chimeric genes as a source of rapid evolution in Drosophila melanogaster. Mol Biol Evol 2012, 29:517-529.
50. Cui Y., Wong W.H., Bornberg-Bauer E., Chan H.S. Recombinatoric exploration of novel folded structures: a heteropolymer-based model of protein evolutionary landscapes. Proc Natl Acad Sci U S A 2002, 99:809-814.
51. Eisenbeis S., Proffitt W., Coles M., Truffault V., Shanmugaratnam S., Meiler J., Hocker B. Potential of fragment recombination for rational design of proteins. J Am Chem Soc 2012, 134:4019-4022.
52. Javadi Y., Itzhaki L.S. Tandem-repeat proteins: regularity plus modularity equals design-ability. Curr Opin Struct Biol 2013, 23:622-631.
53. Boersma Y.L., Pluckthun A. DARPins and other repeat protein scaffolds: advances in engineering and applications. Curr Opin Biotechnol 2011, 22:849-857.
54. Ferreiro D.U., Walczak A.M., Komives E.A., Wolynes P.G. The energy landscapes of repeat-containing proteins: topology, cooperativity, and the folding funnels of one-dimensional architectures. PLoS Comput Biol 2008, 4:e1000070.
55. Wetzel S.K., Settanni G., Kenig M., Binz H.K., Pluckthun A. Folding and unfolding mechanism of highly stable full-consensus ankyrin repeat proteins. J Mol Biol 2008, 376:241-257.
56. Hagai T., Azia A., Trizac E., Levy Y. Modulation of folding kinetics of repeat proteins: interplay between intra- and interdomain interactions. Biophys J 2012, 103:1555-1565.
57. Marold J.D., Kavran J.M., Bowman G.D., Barrick D. A Naturally occurring repeat protein with high internal sequence identity defines a new class of TPR-like proteins. Structure 2015, 23:2055-2065.
58. Broom A., Ma S.M., Xia K., Rafalia H., Trainor K., Colon W., Gosavi S., Meiering E.M. Designed protein reveals structural determinants of extreme kinetic stability. Proc Natl Acad Sci U S A 2015, 112:14605-14610.
59. Abkevich V.I., Gutin A.M., Shakhnovich E.I. Impact of local and non-local interactions on thermodynamics and kinetics of protein folding. J Mol Biol 1995, 252:460-471.
60. Sawyer N., Chen J., Regan L. All repeats are not equal: a module-based approach to guide repeat protein design. J Mol Biol 2013, 425:1826-1838.
61. Voet A.R., Noguchi H., Addy C., Zhang K.Y., Tame J.R. Biomineralization of a cadmium chloride nanocrystal by a designed symmetrical protein. Angew Chem Int Ed Engl 2015, 54:9857-9860.
62. Fortenberry C., Bowman E.A., Proffitt W., Dorr B., Combs S., Harp J., Mizoue L., Meiler J. Exploring symmetry as an avenue to the computational design of large protein domains. J Am Chem Soc 2011, 133:18026-18029.
63. Carstensen L., Sperl J.M., Bocola M., List F., Schmid F.X., Sterner R. Conservation of the folding mechanism between designed primordial (betaalpha)8-barrel proteins and their modern descendant. J Am Chem Soc 2012, 134:12786-12791.
64. Figueroa M., Oliveira N., Lejeune A., Kaufmann K.W., Dorr B.M., Matagne A., Martial J.A., Meiler J., Van de Weerdt C. Octarellin VI: using rosetta to design a putative artificial (beta/alpha)8 protein. PLoS One 2013, 8:e71858.
65. Nagarajan D., Deka G., Rao M. Design of symmetric TIM barrel proteins from first principles. BMC Biochem 2015, 16:18.
66. Broom A., Gosavi S., Meiering E.M. Protein unfolding rates correlate as strongly as folding rates with native structure. Protein Sci 2015, 24:580-587.
67. Lee J., Blaber S.I., Dubey V.K., Blaber M. A polypeptide "building block" for the beta-trefoil fold identified by "top-down symmetric deconstruction". J Mol Biol 2011, 407:744-763.
68. Longo L.M., Lee J., Tenorio C.A., Blaber M. Alternative folding nuclei definitions facilitate the evolution of a symmetric protein fold from a smaller peptide motif. Structure 2013, 21:2042-2050.
69. Grigoryan G., Degrado W.F. Probing designability via a generalized model of helical bundle geometry. J Mol Biol 2011, 405:1079-1100.
70. Harbury P.B., Zhang T., Kim P.S., Alber T. A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science 1993, 262:1401-1407.
71. Gradisar H., Bozic S., Doles T., Vengust D., Hafner-Bratkovic I., Mertelj A., Webb B., Sali A., Klavzar S., Jerala R. Design of a single-chain polypeptide tetrahedron assembled from coiled-coil segments. Nat Chem Biol 2013, 9:362-366.
72. Fletcher J.M., Harniman R.L., Barnes F.R., Boyle A.L., Collins A., Mantell J., Sharp T.H., Antognozzi M., Booth P.J., Linden N., et al. Self-assembling cages from coiled-coil peptide modules. Science 2013, 340:595-599.
73. Potapov V., Kaplan J.B., Keating A.E. Data-driven prediction and design of bZIP coiled-coil interactions. PLoS Comput Biol 2015, 11:e1004046.
74. Nick Pace C., Scholtz J.M., Grimsley G.R. Forces stabilizing proteins. FEBS Lett 2014, 588:2177-2184.
75. Sheffler W., Baker D. RosettaHoles: rapid assessment of protein core packing for structure prediction, refinement, design, and validation. Protein Sci 2009, 18:229-239.
76. Dai L., Yang Y., Kim H.R., Zhou Y. Improving computational protein design by using structure-derived sequence profile. Proteins 2010, 78:2338-2348.
77. Schymkowitz J., Borg J., Stricher F., Nys R., Rousseau F., Serrano L. The FoldX web server: an online force field. Nucleic Acids Res 2005, 33:W382-W388.
78. Mitra P., Shultis D., Brender J.R., Czajka J., Marsh D., Gray F., Cierpicki T., Zhang Y. An evolution-based approach to de novo protein design and case study on Mycobacterium tuberculosis. PLoS Comput Biol 2013, 9:e1003298.
79. Xiong P., Wang M., Zhou X., Zhang T., Zhang J., Chen Q., Liu H. Protein design with a comprehensive statistical energy function and boosted by experimental selection for foldability. Nat Commun 2014, 5:5330.
80. Potapov V., Cohen M., Schreiber G. Assessing computational methods for predicting protein stability upon mutation: good on average but not in the details. Protein Eng Des Sel 2009, 22:553-560.
81. Khan S., Vihinen M. Performance of protein stability predictors. Hum Mutat 2010, 31:675-684.
82. Das R. Four small puzzles that Rosetta doesn't solve. PLoS One 2011, 6:e20044.
83. Murphy G.S., Sathyamoorthy B., Der B.S., Machius M.C., Pulavarti S.V., Szyperski T., Kuhlman B. Computational de novo design of a four-helix bundle protein - DND_4HB. Protein Sci 2015, 24:434-445.
84. Ollikainen N., Kortemme T. Computational protein design quantifies structural constraints on amino acid covariation. PLoS Comput Biol 2013, 9:e1003313.
85. Zhang Z., Chan H.S. Competition between native topology and nonnative interactions in simple and complex folding kinetics of natural and designed proteins. Proc Natl Acad Sci U S A 2010, 107:2920-2925.
86. Yadahalli S., Gosavi S. Designing cooperativity into the designed protein Top7. Proteins 2014, 82:364-374.
87. Truong H.H., Kim B.L., Schafer N.P., Wolynes P.G. Funneling and frustration in the energy landscapes of some designed and simplified proteins. J Chem Phys 2013, 139:121908.
88. Tzul F.O., Schweiker K.L., Makhatadze G.I. Modulation of folding energy landscape by charge-charge interactions: linking experiments with computational modeling. Proc Natl Acad Sci U S A 2015, 112:E259-E266.
89. Chung H.S., Piana-Agostinetti S., Shaw D.E., Eaton W.A. Structural origin of slow diffusion in protein folding. Science 2015, 349:1504-1510.
90. Giri Rao V.H., Gosavi S. Using the folding landscapes of proteins to understand protein function. Curr Opin Struct Biol 2016, 36:67-74.
91. Mou Y., Huang P.S., Thomas L.M., Mayo S.L. Using molecular dynamics simulations as an aid in the prediction of domain swapping of computationally designed protein variants. J Mol Biol 2015, 427:2697-2706.
92. Jacak R., Leaver-Fay A., Kuhlman B. Computational protein design with explicit consideration of surface hydrophobic patches. Proteins 2012, 80:825-838.
93. Der B.S., Kluwe C., Miklos A.E., Jacak R., Lyskov S., Gray J.J., Georgiou G., Ellington A.D., Kuhlman B. Alternative computational protocols for supercharging protein surfaces for reversible unfolding and retention of stability. PLoS One 2013, 8:e64363.