Emerging themes in the computational design of novel enzymes and protein-protein interfaces

FEBS Letters

Volumn 587, Issue 8, 2013, Pages 1147-1154

  Khare, Sagar D ^a   Fleishman, Sarel J ^b  

^a RUTGERS UNIVERSITY   (United States)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Computational design; Energy function; Enzyme; Negative design; Novel protein function; ORBIT; Protein interaction; Rosetta

Indexed keywords

ENZYME; PROTEIN INHIBITOR;

BETA SHEET; BINDING SITE; BIOCHEMISTRY; COMPUTER AIDED DESIGN; COMPUTER PROGRAM; CRYSTAL STRUCTURE; DATA BASE; ENERGY; ENZYME STRUCTURE; HUMAN; MOLECULAR BIOLOGY; PHYSICS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DESIGN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW;

BIOCATALYSIS; COMPUTATIONAL BIOLOGY; ENZYMES; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEINS; SURFACE PROPERTIES; THERMODYNAMICS;

EID: 84876020987     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2012.12.009     Document Type: Review

References (69)

1. J.U. Bowie, R. Luthy, and D. Eisenberg A method to identify protein sequences that fold into a known three-dimensional structure Science 253 1991 164 170
2. B. Kuhlman, and D. Baker Native protein sequences are close to optimal for their structures Proc. Natl. Acad. Sci. USA 97 2000 10383 10388
3. B.I. Dahiyat, and S.L. Mayo Protein design automation Protein Sci. 5 1996 895 903 10.1002/pro.5560050511
4. J.J. Havranek, and P.B. Harbury Automated design of specificity in molecular recognition Nat. Struct. Biol. 10 2003 45 52
5. B.I. Dahiyat, and S.L. Mayo De novo protein design: fully automated sequence selection Science 278 1997 82 87
6. B. Kuhlman, G. Dantas, G.C. Ireton, G. Varani, B.L. Stoddard, and D. Baker Design of a novel globular protein fold with atomic-level accuracy Science 302 2003 1364 1368
7. X. Hu, H. Wang, H. Ke, and B. Kuhlman High-resolution design of a protein loop Proc. Natl. Acad. Sci. USA 104 2007 17668 17673 doi: 0707977104 [pii] 10.1073/pnas.0707977104
8. G.T. Kapp, S. Liu, A. Stein, D.T. Wong, A. Remenyi, B.J. Yeh, J.S. Fraser, J. Taunton, W.A. Lim, and T. Kortemme Control of protein signaling using a computationally designed GTPase/GEF orthogonal pair Proc. Natl. Acad. Sci. USA 109 2012 5277 5282 10.1073/pnas.1114487109
9. D.W. Sammond, Z.M. Eletr, C. Purbeck, and B. Kuhlman Computational design of second-site suppressor mutations at protein-protein interfaces Proteins 78 2010 1055 1065 10.1002/prot.22631
10. K. Deckert, S.J. Budiardjo, L.C. Brunner, S. Lovell, and J. Karanicolas Designing allosteric control into enzymes by chemical rescue of structure J. Am. Chem. Soc. 134 2012 10055 10060 10.1021/ja301409g
11. I. Samish, C.M. MacDermaid, J.M. Perez-Aguilar, and J.G. Saven Theoretical and computational protein design Annu. Rev. Phys. Chem. 62 2011 129 149 10.1146/annurev-physchem-032210-103509
12. R. Wolfenden, and M.J. Snider The depth of chemical time and the power of enzymes as catalysts Acc. Chem. Res. 34 2001 938 945
13. H.W. Hellinga, and F.M. Richards Construction of new ligand binding sites in proteins of known structure. I. Computer-aided modeling of sites with pre-defined geometry J. Mol. Biol. 222 1991 763 785 doi: 0022-2836(91)90510-D [pii]
14. D.E. Robertson, R.S. Farid, C.C. Moser, J.L. Urbauer, S.E. Mulholland, R. Pidikiti, J.D. Lear, A.J. Wand, W.F. DeGrado, and P.L. Dutton Design and synthesis of multi-haem proteins Nature 368 1994 425 432 10.1038/368425a0
15. D.E. Benson, M.S. Wisz, and H.W. Hellinga Rational design of nascent metalloenzymes Proc. Natl. Acad. Sci. USA 97 2000 6292 6297
16. J. Kaplan, and W.F. DeGrado De novo design of catalytic proteins Proc. Natl. Acad. Sci. USA 101 2004 11566 11570
17. A.L. Pinto, H.W. Hellinga, and J.P. Caradonna Construction of a catalytically active iron superoxide dismutase by rational protein design Proc. Natl. Acad. Sci. USA 94 1997 5562 5567
18. D.N. Bolon, and S.L. Mayo Enzyme-like proteins by computational design Proc. Natl. Acad. Sci. USA 98 2001 14274 14279
19. R. Wolfenden Transition state analog inhibitors and enzyme catalysis Annu. Rev. Biophys. Bioeng. 5 1976 271 306 10.1146/annurev.bb.05.060176.001415
20. A. Warshel, P.K. Sharma, M. Kato, Y. Xiang, H. Liu, and M.H. Olsson Electrostatic basis for enzyme catalysis Chem. Rev. 106 2006 3210 3235 10.1021/cr0503106
21. D.J. Tantillo, J. Chen, and K.N. Houk Theozymes and compuzymes: theoretical models for biological catalysis Curr. Opin. Chem. Biol. 2 1998 743 750
22. V.L. Schramm Enzymatic transition states, transition-state analogs, dynamics, thermodynamics, and lifetimes Annu. Rev. Biochem. 80 2011 703 732 10.1146/annurev-biochem-061809-100742
23. A. Zanghellini, L. Jiang, A.M. Wollacott, G. Cheng, J. Meiler, E.A. Althoff, D. Rothlisberger, and D. Baker New algorithms and an in silico benchmark for computational enzyme design Protein Sci. 15 2006 2785 2794 doi: 15/12/2785 [pii] 10.1110/ps.062353106
24. J.K. Lassila, H.K. Privett, B.D. Allen, and S.L. Mayo Combinatorial methods for small-molecule placement in computational enzyme design Proc. Natl. Acad. Sci. USA 103 2006 16710 16715 10.1073/pnas.0607691103
25. F. Richter, A. Leaver-Fay, S.D. Khare, S. Bjelic, and D. Baker De novo enzyme design using Rosetta3 PLoS ONE 6 2011 e19230 10.1371/journal.pone.0019230
26. D. Rothlisberger, O. Khersonsky, A.M. Wollacott, L. Jiang, J. DeChancie, J. Betker, J.L. Gallaher, E.A. Althoff, A. Zanghellini, and O. Dym Kemp elimination catalysts by computational enzyme design Nature 453 2008 190 195 doi: nature06879 [pii] 10.1038/nature06879
27. L. Jiang, E.A. Althoff, F.R. Clemente, L. Doyle, D. Rothlisberger, A. Zanghellini, J.L. Gallaher, J.L. Betker, F. Tanaka, and C.F. Barbas 3rd De novo computational design of retro-aldol enzymes Science 319 2008 1387 1391 10.1126/science.1152692
28. O. Khersonsky, D. Rothlisberger, A.M. Wollacott, P. Murphy, O. Dym, S. Albeck, G. Kiss, K.N. Houk, D. Baker, and D.S. Tawfik Optimization of the in-silico-designed kemp eliminase KE70 by computational design and directed evolution J. Mol. Biol. 407 2011 391 412 doi: S0022-2836(11)00084-2 [pii] 10.1016/j.jmb.2011.01.041
29. E.A. Althoff, L. Wang, L. Jiang, L. Giger, J.K. Lassila, Z. Wang, M. Smith, S. Hari, P. Kast, and D. Herschlag Robust design and optimization of retroaldol enzymes Protein Sci. 21 2012 717 726 10.1002/pro.2059
30. O. Khersonsky, D. Rothlisberger, O. Dym, S. Albeck, C.J. Jackson, D. Baker, and D.S. Tawfik Evolutionary optimization of computationally designed enzymes: Kemp eliminases of the KE07 series J. Mol. Biol. 396 2010 1025 1042 10.1016/j.jmb.2009.12.031
31. J.K. Lassila, D. Baker, and D. Herschlag Origins of catalysis by computationally designed retroaldolase enzymes Proc. Natl. Acad. Sci. USA 107 2010 4937 4942 10.1073/pnas.0913638107
32. L. Wang, E.A. Althoff, J. Bolduc, L. Jiang, J. Moody, J.K. Lassila, L. Giger, D. Hilvert, B. Stoddard, and D. Baker Structural analyses of covalent enzyme-substrate analog complexes reveal the strengths and limitations of de novo enzyme design J. Mol. Biol. 2011 10.1016/j.jmb.2011.10.043
33. O. Khersonsky, G. Kiss, D. Rothlisberger, O. Dym, S. Albeck, K.N. Houk, D. Baker, and D.S. Tawfik Bridging the gaps in design methodologies by evolutionary optimization of the stability and proficiency of designed Kemp eliminase KE59 Proc. Natl. Acad. Sci. USA 109 2012 10358 10363 10.1073/pnas.1121063109
34. H.K. Privett, G. Kiss, T.M. Lee, R. Blomberg, R.A. Chica, L.M. Thomas, D. Hilvert, K.N. Houk, and S.L. Mayo Iterative approach to computational enzyme design Proc. Natl. Acad. Sci. USA 109 2012 3790 3795 10.1073/pnas.1118082108
35. G. Kiss, D. Rothlisberger, D. Baker, and K.N. Houk Evaluation and ranking of enzyme designs Protein Sci. 19 2010 1760 1773 10.1002/pro.462
36. F. Richter, R. Blomberg, S.D. Khare, G. Kiss, A.P. Kuzin, A.J. Smith, J. Gallaher, Z. Pianowski, R.C. Helgeson, and A. Grjasnow Computational design of catalytic dyads and oxyanion holes for ester hydrolysis J. Am. Chem. Soc. 134 2012 16197 16206 10.1021/ja3037367
37. A. Warshel Electrostatic origin of the catalytic power of enzymes and the role of preorganized active sites J. Biol. Chem. 273 1998 27035 27038
38. S.D. Khare, Y. Kipnis, P. Greisen Jr.; R. Takeuchi, Y. Ashani, M. Goldsmith, Y. Song, J.L. Gallaher, I. Silman, and H. Leader Computational redesign of a mononuclear zinc metalloenzyme for organophosphate hydrolysis Nat. Chem. Biol. 8 2012 294 300 10.1038/nchembio.777
39. A.N. Alexandrova, D. Rothlisberger, D. Baker, and W.L. Jorgensen Catalytic mechanism and performance of computationally designed enzymes for Kemp elimination J. Am. Chem. Soc. 130 2008 15907 15915 10.1021/ja804040s
40. M.P. Frushicheva, J. Cao, Z.T. Chu, and A. Warshel Exploring challenges in rational enzyme design by simulating the catalysis in artificial kemp eliminase Proc. Natl. Acad. Sci. USA 107 2010 16869 16874 10.1073/pnas. 1010381107
41. M.P. Frushicheva, J. Cao, and A. Warshel Challenges and advances in validating enzyme design proposals: the case of kemp eliminase catalysis Biochemistry 50 2011 3849 3858 10.1021/bi200063a
42. D. Baker An exciting but challenging road ahead for computational enzyme design Protein Sci. 19 2010 1817 1819 10.1002/pro.481
43. P.S. Huang, J.J. Love, and S.L. Mayo A de novo designed protein protein interface Protein Sci. 16 2007 2770 2774 doi: 16/12/2770 [pii] 10.1110/ps.073125207
44. R.K. Jha, A. Leaver-Fay, S. Yin, Y. Wu, G.L. Butterfoss, T. Szyperski, N.V. Dokholyan, and B. Kuhlman Computational design of a PAK1 binding protein J. Mol. Biol. 400 2010 257 270 doi: S0022-2836(10)00472-9 [pii] 10.1016/j.jmb.2010.05.006
45. H.K. Binz, P. Amstutz, A. Kohl, M.T. Stumpp, C. Briand, P. Forrer, M.G. Grutter, and A. Pluckthun High-affinity binders selected from designed ankyrin repeat protein libraries Nat. Biotechnol. 22 2004 575 582
46. J. Karanicolas, J.E. Corn, I. Chen, L.A. Joachimiak, O. Dym, S.H. Peck, S. Albeck, T. Unger, W. Hu, and G. Liu A de novo protein binding pair by computational design and directed evolution Mol. Cell. 42 2011 250 260 doi: S1097-2765(11)00208-5 [pii] 10.1016/j.molcel.2011.03.010
47. A.A. Bogan, and K.S. Thorn Anatomy of hot spots in protein interfaces J. Mol. Biol. 280 1998 1 9 doi: S0022-2836(98)91843-5 [pii] 10.1006/jmbi.1998.1843
48. P.B. Stranges, M. Machius, M.J. Miley, A. Tripathy, and B. Kuhlman Computational design of a symmetric homodimer using beta-strand assembly Proc. Natl. Acad. Sci. USA 108 2011 20562 20567 10.1073/pnas.1115124108
49. C.A. Rohl, C.E. Strauss, K.M. Misura, and D. Baker Protein structure prediction using Rosetta Methods Enzymol. 383 2004 66 93 10.1016/S0076-6879(04) 83004-0
50. B.S. Der, M. Machius, M.J. Miley, J.L. Mills, T. Szyperski, and B. Kuhlman Metal-mediated affinity and orientation specificity in a computationally designed protein homodimer J. Am. Chem. Soc. 134 2012 375 385 10.1021/ja208015j
51. J.D. Brodin, X.I. Ambroggio, C. Tang, K.N. Parent, T.S. Baker, and F.A. Tezcan Metal-directed, chemically tunable assembly of one-, two- and three-dimensional crystalline protein arrays Nat. Chem. 4 2012 375 382 10.1038/nchem.1290
52. S.J. Fleishman, S.D. Khare, N. Koga, and D. Baker Restricted sidechain plasticity in the structures of native proteins and complexes Protein Sci. 20 2011 753 757
53. S.J. Fleishman, J.E. Corn, E.M. Strauch, T.A. Whitehead, J. Karanicolas, and D. Baker Hotspot-centric de novo design of protein binders J. Mol. Biol. 413 2011 1047 1062 10.1016/j.jmb.2011.09.001
54. S.J. Fleishman, T.A. Whitehead, D.C. Ekiert, C. Dreyfus, J.E. Corn, E.-M. Strauch, I.A. Wilson, and D. Baker Computational design of proteins targeting the conserved stem region of influenza hemagglutinin Science 332 2011 816 821
55. T.A. Whitehead, A. Chevalier, Y. Song, C. Dreyfus, S.J. Fleishman, C. De Mattos, C.A. Myers, H. Kamisetty, P. Blair, and I.A. Wilson Optimization of affinity, specificity and function of designed influenza inhibitors using deep sequencing Nat. Biotechnol. 30 2012 543 548 10.1038/nbt.2214
56. S.J. Fleishman, T.A. Whitehead, E.M. Strauch, J.E. Corn, S. Qin, H.X. Zhou, J.C. Mitchell, O.N. Demerdash, M. Takeda-Shitaka, and G. Terashi Community-wide assessment of protein-interface modeling suggests improvements to design methodology J. Mol. Biol. 414 2011 289 302 10.1016/j.jmb.2011.09.031
57. N.P. King, W. Sheffler, M.R. Sawaya, B.S. Vollmar, J.P. Sumida, I. Andre, T. Gonen, T.O. Yeates, and D. Baker Computational design of self-assembling protein nanomaterials with atomic level accuracy Science 336 2012 1171 1174 10.1126/science.1219364
58. C.J. Lanci, C.M. MacDermaid, S.G. Kang, R. Acharya, B. North, X. Yang, X.J. Qiu, W.F. DeGrado, and J.G. Saven Computational design of a protein crystal Proc. Natl. Acad. Sci. USA 109 2012 7304 7309 10.1073/pnas.1112595109
59. Y.T. Lai, N.P. King, and T.O. Yeates Principles for designing ordered protein assemblies Trends Cell Biol. 2012 10.1016/j.tcb.2012.08.004
60. S.J. Fleishman, and D. Baker Role of the biomolecular energy gap in protein design, structure, and evolution Cell 149 2012 262 273 10.1016/j.cell.2012.03.016
61. C.B. Eiben, J.B. Siegel, J.B. Bale, S. Cooper, F. Khatib, B.W. Shen, F. Players, B.L. Stoddard, Z. Popovic, and D. Baker Increased Diels-Alderase activity through backbone remodeling guided by Foldit players Nat. Biotechnol. 30 2012 190 192 10.1038/nbt.2109
62. T. Kortemme, A.V. Morozov, and D. Baker An orientation-dependent hydrogen bonding potential improves prediction of specificity and structure for proteins and protein-protein complexes J. Mol. Biol. 326 2003 1239 1259
63. T. Lazaridis, and M. Karplus Effective energy function for proteins in solution Proteins 35 1999 133 152 doi: 10.1002/(SICI)1097-0134(19990501)35: 2<133::AID-PROT1>3.0.CO;2-N [pii]
64. R.L. Dunbrack Jr.; and M. Karplus Conformational analysis of the backbone-dependent rotamer preferences of protein sidechains Nat. Struct. Biol. 1 1994 334 340
65. V. Munoz, and L. Serrano Intrinsic secondary structure propensities of the amino acids, using statistical phi-psi matrices: comparison with experimental scales Proteins 20 1994 301 311 10.1002/prot.340200403
66. S. Miyazawa, and R.L. Jernigan A new substitution matrix for protein sequence searches based on contact frequencies in protein structures Method Enzymol. 6 1993 267 278
67. Y. Song, M. Tyka, A. Leaver-Fay, J. Thompson, and D. Baker Structure-guided forcefield optimization Proteins 79 2011 1898 1909 10.1002/prot.23013
68. DeLano WL (2002) The PyMol Molecular Graphics Systems. DeLano Scientific, Palo Alto, CA, USA.
69. P.B. Stranges, and B. Kuhlman A comparison of successful and failed protein interface designs highlights the challenges of designing buried hydrogen bonds Protein Sci. 22 2013 74 82