Designing specific protein-protein interactions using computation, experimental library screening, or integrated methods

Protein Science

Volumn 21, Issue 7, 2012, Pages 949-963

  Chen, T Scott ^a   Keating, Amy E ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Computational modeling; Library screening; Protein design; Protein interaction specificity

Indexed keywords

AMINO ACID SEQUENCE; ANALYTIC METHOD; COMPUTATIONAL STRUCTURE BASED DESIGN; EXPERIMENTAL LIBRARY SCREENING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW;

ANIMALS; COMPUTATIONAL BIOLOGY; HUMANS; MODELS, MOLECULAR; PEPTIDE LIBRARY; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN INTERACTION MAPPING; PROTEINS;

EID: 84862541366     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2096     Document Type: Review

References (174)

1. Pawson T, Nash P (2000) Protein-protein interactions define specificity in signal transduction. Genes Dev 14:1027-1047. (Pubitemid 30324418)
2. Ito T, Chiba T, Ozawa R, Yoshida M, Hattori M, Sakaki Y (2001) A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc Natl Acad Sci USA 98:4569-4574. (Pubitemid 32295017)
3. Gavin AC, Aloy P, Grandi P, Krause R, Boesche M, Marzioch M, Rau C, Jensen LJ, Bastuck S, Dumpelfeld B, Edelmann A, Heurtier MA, Hoffman V, Hoefert C, Klein K, Hudak M, Michon AM, Schelder M, Schirle M, Remor M, Rudi T, Hooper S, Bauer, A., Bouwmeester T, Casari G, Drewes G, Neubauer G, Rick JM, Kuster B, Bork P, Russell R B, Superti-Furga G (2006) Proteome survey reveals modularity of the yeast cell machinery. Nature 440:631-636.
4. Rual JF, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, Li N, Berriz GF, Gibbons FD, Dreze M, Ayivi-Guedehoussou N, Klitgord N, Simon C, Boxem M, Milstein S, Rosenberg J, Goldberg DS, Zhang LV, Wong SL, Franklin G, Li S, Albala J S, Lim J, Fraughton C, Llamosas E, Cevik S, Bex C, Lamesch P, Sikorski RS, Vandenhaute J, Zoghbi HY, Smolyar A, Bosak S, Sequerra R, Doucette-Stamm L, Cusick ME, Hill DE, Roth FP, Vidal M (2005) Towards a proteome-scale map of the human protein-protein interaction network. Nature 437:1173-1178. (Pubitemid 41509356)
5. Newman JR, Keating AE (2003) Comprehensive identification of human bZIP interactions with coiled-coil arrays. Science 300:2097-2101. (Pubitemid 36760137)
6. Stiffler MA, Chen JR, Grantcharova VP, Lei Y, Fuchs D, Allen JE, Zaslavskaia LA, MacBeath G (2007) PDZ domain binding selectivity is optimized across the mouse proteome. Science 317:364-369.
7. Presser A, Elowitz MB, Kellis M, Kishony R (2008) The evolutionary dynamics of the Saccharomyces cerevisiae protein interaction network after duplication. Proc Natl Acad Sci USA 105:950-954. (Pubitemid 351282062)
8. Lee HJ, Zheng JJ (2010) PDZ domains and their binding partners: Structure, specificity, and modification. Cell Commun Signal 8:8.
9. Tonikian R, Zhang Y, Sazinsky SL, Currell B, Yeh JH, Reva B, Held HA, Appleton BA, Evangelista M, Wu Y, Xin X, Chan AC, Seshagiri S, Lasky LA, Sander C, Boone C, Bader GD, Sidhu SS (2008) A specificity map for the PDZ domain family. PLoS Biol 6:e239.
10. Wiedemann U, Boisguerin P, Leben R, Leitner D, Krause G, Moelling K, Volkmer-Engert R, Oschkinat H (2004) Quantification of PDZ domain specificity, prediction of ligand affinity and rational design of super-binding peptides. J Mol Biol 343:703-718. (Pubitemid 39311616)
11. Songyang Z, Shoelson SE, Chaudhuri M, Gish G, Pawson T, Haser WG, King F, Roberts T, Ratnofsky S, Lechleider RJ, et al. (1993) SH2 domains recognize specific phosphopeptide sequences. Cell 72:767-778. (Pubitemid 23093884)
12. Liu BA, Jablonowski K, Shah EE, Engelmann BW, Jones RB, Nash PD (2010) SH2 domains recognize contextual peptide sequence information to determine selectivity. Mol Cell Proteomics 9:2391-2404.
13. Zarrinpar A, Park SH, Lim WA (2003) Optimization of specificity in a cellular protein interaction network by negative selection. Nature 426:676-680. (Pubitemid 38009377)
14. Tonikian R, Xin X, Toret CP, Gfeller D, Landgraf C, Panni S, Paoluzi S, Castagnoli L, Currell B, Seshagiri S, Yu H, Winsor B, Vidal M, Gerstein MB, Bader GD, Volkmer R, Cesareni G, Drubin DG, Kim PM, Sidhu SS, Boone C (2009) Bayesian modeling of the yeast SH3 domain interactome predicts spatiotemporal dynamics of endocytosis proteins. PLoS Biol 7:e1000218.
15. Chen L, Willis SN, Wei A, Smith BJ, Fletcher JI, Hinds MG, Colman PM, Day CL, Adams JM, Huang DC (2005) Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell 17:393-403. (Pubitemid 40193310)
16. Wojtowicz WM, Wu W, Andre I, Qian B, Baker D, Zipursky SL (2007) A vast repertoire of Dscam binding specificities arises from modular interactions of variable Ig domains. Cell 130:1134-1145. (Pubitemid 47410273)
17. Graveley BR, Kaur A, Gunning D, Zipursky SL, Rowen L, Clemens JC (2004) The organization and evolution of the dipteran and hymenopteran Down syndrome cell adhesion molecule (Dscam) genes. RNA 10:1499-1506. (Pubitemid 39288184)
18. Schreiber G, Keating AE (2011) Protein binding specificity versus promiscuity. Curr Opin Struct Biol 21:50-61.
19. Kaneko T, Sidhu SS, Li SS (2011) Evolving specificity from variability for protein interaction domains. Trends Biochem Sci 36:183-90.
20. Kaneko T, Huang H, Zhao B, Li L, Liu H, Voss CK, Wu C, Schiller MR, Li SS (2010) Loops govern SH2 domain specificity by controlling access to binding pockets. Sci Signal 3:ra34.
21. Appleton BA, Zhang Y, Wu P, Yin JP, Hunziker W, Skelton NJ, Sidhu SS, Wiesmann C (2006) Comparative structural analysis of the Erbin PDZ domain and the first PDZ domain of ZO-1. Insights into determinants of PDZ domain specificity. J Biol Chem 281:22312-22320. (Pubitemid 44181933)
22. Kimber MS, Nachman J, Cunningham AM, Gish GD, Pawson T, Pai EF (2000) Structural basis for specificity switching of the Src SH2 domain. Mol Cell 5:1043-1049.
23. Al-Lazikani B, Lesk AM, Chothia C (1997) Standard conformations for the canonical structures of immunoglobulins. J Mol Biol 273:927-948. (Pubitemid 27493729)
24. Meenan NA, Sharma A, Fleishman SJ, Macdonald CJ, Morel B, Boetzel R, Moore GR, Baker D, Kleanthous C (2010) The structural and energetic basis for high selectivity in a high-affinity protein-protein interaction. Proc Natl Acad Sci USA 107:10080-10085.
25. Vinson C, Acharya A, Taparowsky EJ (2006) Deciphering B-ZIP transcription factor interactions in vitro and in vivo. Biochim Biophys Acta 1759:4-12.
26. Gretes M, Lim DC, de Castro L, Jensen SE, Kang SG, Lee KJ, Strynadka NC (2009) Insights into positive and negative requirements for protein-protein interactions by crystallographic analysis of the beta-lactamase inhibitory proteins BLIP, BLIP-I, and BLP. J Mol Biol 389:289-305.
27. Skelton NJ, Koehler MF, Zobel K, Wong WL, Yeh S, Pisabarro MT, Yin JP, Lasky LA, Sidhu SS (2003) Origins of PDZ domain ligand specificity. Structure determination and mutagenesis of the Erbin PDZ domain. J Biol Chem 278:7645-7654. (Pubitemid 36800774)
28. Songyang Z, Gish G, Mbamalu G, Pawson T, Cantley LC (1995) A single point mutation switches the specificity of group III Src homology (SH) 2 domains to that of group I SH2 domains. J Biol Chem 270:26029-26032.
29. Weng Z, Rickles RJ, Feng S, Richard S, Shaw AS, Schreiber SL, Brugge JS (1995) Structure-function analysis of SH3 domains: SH3 binding specificity altered by single amino acid substitutions. Mol Cell Biol 15:5627-5634.
30. Li W, Dennis CA, Moore GR, James R, Kleanthous C (1997) Protein-protein interaction specificity of Im9 for the endonuclease toxin colicin E9 defined by homologue-scanning mutagenesis. J Biol Chem 272: 22253-22258. (Pubitemid 27382858)
31. Van der Sloot AM, Kiel C, Serrano L, Stricher F (2009) Protein design in biological networks: from manipulating the input to modifying the output. Protein Eng Des Sel 22:537-542.
32. Olive M, Williams SC, Dezan C, Johnson PF, Vinson C (1996) Design of a C/EBP-specific, dominant-negative bZIP protein with both inhibitory and gain-of-function properties. J Biol Chem 271:2040-2047. (Pubitemid 26047789)
33. van der Sloot AM, Tur V, Szegezdi E, Mullally MM, Cool RH, Samali A, Serrano L, Quax WJ (2006) Designed tumor necrosis factor-related apoptosis-inducing ligand variants initiating apoptosis exclusively via the DR5 receptor. Proc Natl Acad Sci USA 103:8634-8639. (Pubitemid 43878072)
34. Lee EF, Czabotar PE, van Delft MF, Michalak EM, Boyle MJ, Willis SN, Puthalakath H, Bouillet P, Colman PM, Huang DC, Fairlie WD (2008) A novel BH3 ligand that selectively targets Mcl-1 reveals that apoptosis can proceed without Mcl-1 degradation. J Cell Biol 180:341-355. (Pubitemid 351185920)
35. Bolon DN, Wah DA, Hersch GL, Baker TA, Sauer RT (2004) Bivalent tethering of SspB to ClpXP is required for efficient substrate delivery: a protein-design study. Mol Cell 13:443-449. (Pubitemid 38229816)
36. Szczepek M, Brondani V, Buchel J, Serrano L, Segal DJ, Cathomen T (2007) Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nat Biotechnol 25:786-793. (Pubitemid 47052189)
37. Czyzyk J, Brogdon JL, Badou A, Henegariu O, Preston Hurlburt P, Flavell R, Bottomly K (2003) Activation of CD4 T cells by Raf-independent effectors of Ras. Proc Natl Acad Sci USA 100:6003-6008. (Pubitemid 36576921)
38. Dreze M, Charloteaux B, Milstein S, Vidalain PO, Yildirim MA, Zhong Q, Svrzikapa N, Romero V, Laloux G, Brasseur R, Vandenhaute J, Boxem M, Cusick ME, Hill DE, Vidal M (2009) 'Edgetic' perturbation of a C. elegans BCL2 ortholog. Nat Methods 6:843-849.
39. Bashor CJ, Helman NC, Yan S, Lim WA (2008) Using engineered scaffold interactions to reshape MAP kinase pathway signaling dynamics. Science 319:1539-1543. (Pubitemid 351398185)
40. Kiel C, Yus E, Serrano L (2010) Engineering signal transduction pathways. Cell 140:33-47.
41. Jones S, Thornton JM (1996) Principles of protein-protein interactions. Proc Natl Acad Sci USA 93:13-20. (Pubitemid 26038096)
42. Cunningham BC, Wells JA (1989) High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis. Science 244:1081-1085. (Pubitemid 19152300)
43. Pons J, Rajpal A, Kirsch JF (1999) Energetic analysis of an antigen/antibody interface: alanine scanning mutagenesis and double mutant cycles on the HyHEL-10/lysozyme interaction. Protein Sci 8:958-968. (Pubitemid 29211733)
44. Boersma MD, Sadowsky JD, Tomita YA, Gellman SH (2008) Hydrophile scanning as a complement to alanine scanning for exploring and manipulating protein-protein recognition: application to the Bim BH3 domain. Protein Sci 17:1232-1240. (Pubitemid 351930920)
45. Ponder JW, Richards FM (1987) Tertiary templates for proteins. Use of packing criteria in the enumeration of allowed sequences for different structural classes. J Mol Biol 193:775-791. (Pubitemid 17020078)
46. Butterfoss GL, Kuhlman B (2006) Computer-based design of novel protein structures. Annu Rev Biophys Biomol Struct 35:49-65. (Pubitemid 43877369)
47. Lippow SM, Tidor B (2007) Progress in computational protein design. Curr Opin Biotechnol 18:305-311. (Pubitemid 47385179)
48. Karanicolas J, Kuhlman B (2009) Computational design of affinity and specificity at protein-protein interfaces. Curr Opin Struct Biol 19:458-463.
49. Mandell DJ, Kortemme T (2009) Computer-aided design of functional protein interactions. Nat Chem Biol 5:797-807.
50. Boas FE, Harbury PB (2007) Potential energy functions for protein design. Curr Opin Struct Biol 17:199-204. (Pubitemid 46575252)
51. Ponder JW, Case DA (2003) Force fields for protein simulations. Adv Protein Chem 66:27-85. (Pubitemid 37392314)
52. Roux B, Simonson T (1999) Implicit solvent models. Biophys Chem 78:1-20. (Pubitemid 29206654)
53. Honig B, Nicholls A (1995) Classical electrostatics in biology and chemistry. Science 268:1144-1149.
54. Bashford D, Case DA (2000) Generalized born models of macromolecular solvation effects. Annu Rev Phys Chem 51:129-152.
55. Green DF, Tidor B (2003) Evaluation of electrostatic interactions. Curr Protoc Bioinformatics Chapter 8: Unit 8 3.
56. Eisenberg D, McLachlan AD (1986) Solvation energy in protein folding and binding. Nature 319:199-203. (Pubitemid 16128783)
57. Ooi T, Oobatake M, Nemethy G, Scheraga HA (1987) Accessible surface areas as a measure of the thermodynamic parameters of hydration of peptides. Proc Natl Acad Sci USA 84:3086-3090.
58. Lazaridis T, Karplus M (1999) Effective energy function for proteins in solution. Proteins 35:133-152. (Pubitemid 29165128)
59. Levy RM, Zhang LY, Gallicchio E, Felts AK (2003) On the nonpolar hydration free energy of proteins: surface area and continuum solvent models for the solute-solvent interaction energy. J Am Chem Soc 125:9523-9530. (Pubitemid 36936069)
60. Chen J, Brooks CL, III. (2008) Implicit modeling of nonpolar solvation for simulating protein folding and conformational transitions. Phys Chem Chem Phys 10:471-481.
61. Miyazawa S, Jernigan RL (1996) Residue-residue potentials with a favorable contact pair term and an unfavorable high packing density term, for simulation and threading. J Mol Biol 256:623-644. (Pubitemid 26107211)
62. Zhou H, Zhou Y (2002) Distance-scaled, finite ideal-gas reference state improves structure-derived potentials of mean force for structure selection and stability prediction. Protein Sci 11:2714-2726. (Pubitemid 35191145)
63. Shen MY, Sali A (2006) Statistical potential for assessment and prediction of protein structures. Protein Sci 15:2507-2524.
64. Carter CW Jr, LeFebvre BC, Cammer SA, Tropsha A, Edgell MH (2001) Four-body potentials reveal protein-specific correlations to stability changes caused by hydrophobic core mutations. J Mol Biol 311:625-638. (Pubitemid 32803725)
65. Feng Y, Kloczkowski A, Jernigan RL (2007) Four-body contact potentials derived from two protein datasets to discriminate native structures from decoys. Proteins 68:57-66. (Pubitemid 46876534)
66. DeWitte RS, Shakhnovich EI (1994) Pseudodihedrals: simplified protein backbone representation with knowledge-based energy. Protein Sci 3:1570-1581. (Pubitemid 24314475)
67. Lu M, Dousis AD, Ma J (2008) OPUS-PSP: an orientation-dependent statistical all-atom potential derived from side-chain packing. J Mol Biol 376:288-301.
68. Summa CM, Levitt M, Degrado WF (2005) An atomic environment potential for use in protein structure prediction. J Mol Biol 352:986-1001. (Pubitemid 41267083)
69. Misura KM, Morozov AV, Baker D (2004) Analysis of anisotropic side-chain packing in proteins and application to high-resolution structure prediction. J Mol Biol 342:651-664. (Pubitemid 39149764)
70. Morozov AV, Kortemme T, Tsemekhman K, Baker D (2004) Close agreement between the orientation dependence of hydrogen bonds observed in protein structures and quantum mechanical calculations. Proc Natl Acad Sci USA 101:6946-6951. (Pubitemid 38596423)
71. Thomas PD, Dill KA (1996) Statistical potentials extracted from protein structures: how accurate are they? J Mol Biol 257:457-469. (Pubitemid 26114046)
72. Skolnick J (2006) In quest of an empirical potential for protein structure prediction. Curr Opin Struct Biol 16:166-171.
73. Lu L, Lu H, Skolnick J (2002) MULTIPROSPECTOR: an algorithm for the prediction of protein-protein interactions by multimeric threading. Proteins 49:350-364. (Pubitemid 35231471)
74. Clark LA, van Vlijmen HW (2008) A knowledge-based forcefield for protein-protein interface design. Proteins 70:1540-1550. (Pubitemid 351304111)
75. Das R, Baker D (2008) Macromolecular modeling with rosetta. Annu Rev Biochem 77:363-382.
76. Grigoryan G, Keating AE (2006) Structure-based prediction of bZIP partnering specificity. J Mol Biol 355:1125-1142. (Pubitemid 43012152)
77. Alvizo O, Mayo SL (2008) Evaluating and optimizing computational protein design force fields using fixed composition-based negative design. Proc Natl Acad Sci USA 105:12242-12247.
78. Bolon DN, Grant RA, Baker TA, Sauer RT (2005) Specificity versus stability in computational protein design. Proc Natl Acad Sci USA 102:12724-12729. (Pubitemid 41279433)
79. Grigoryan G, Reinke AW, Keating AE (2009) Design of protein-interaction specificity gives selective bZIP-binding peptides. Nature 458:859-864.
80. Havranek JJ, Harbury PB (2003) Automated design of specificity in molecular recognition. Nat Struct Biol 10:45-52. (Pubitemid 36034176)
81. Fromer M, Shifman JM (2009) Tradeoff between stability and multispecificity in the design of promiscuous proteins. PLoS Comput Biol 5:e1000627.
82. Dunbrack RL, Jr (2002) Rotamer libraries in the 21st century. Curr Opin Struct Biol 12:431-440.
83. Baldwin EP, Hajiseyedjavadi O, Baase WA, Matthews BW (1993) The role of backbone flexibility in the accommodation of variants that repack the core of T4 lysozyme. Science 262:1715-1718. (Pubitemid 24030091)
84. Lim WA, Hodel A, Sauer RT, Richards FM (1994) The crystal structure of a mutant protein with altered but improved hydrophobic core packing. Proc Natl Acad Sci USA 91:423-427. (Pubitemid 24018717)
85. Mandell DJ, Kortemme T (2009) Backbone flexibility in computational protein design. Curr Opin Biotechnol 20:420-428.
86. Harbury PB, Plecs JJ, Tidor B, Alber T, Kim PS (1998) High-resolution protein design with backbone freedom. Science 282:1462-1467. (Pubitemid 28538602)
87. Desjarlais JR, Handel TM (1999) Side-chain and backbone flexibility in protein core design. J Mol Biol 290:305-318. (Pubitemid 29308592)
88. Fu X, Apgar JR, Keating AE (2007) Modeling backbone flexibility to achieve sequence diversity: the design of novel alpha-helical ligands for Bcl-xL. J Mol Biol 371:1099-1117. (Pubitemid 47101807)
89. Smith CA, Kortemme T (2008) Backrub-like backbone simulation recapitulates natural protein conformational variability and improves mutant side-chain prediction. J Mol Biol 380:742-756.
90. Smith, CA, Kortemme T (2010) Structure-based prediction of the peptide sequence space recognized by natural and synthetic PDZ domains. J Mol Biol 402:460-474.
91. Benedix A, Becker CM, de Groot BL, Caflisch A, Bockmann RA (2009) Predicting free energy changes using structural ensembles. Nat Methods 6:3-4.
92. Desmet J, De Maeyer M, Hazes B, Lasters I (1992) The dead-end elimination theorem and its use in protein side-chain positioning. Nature 356:539-542.
93. Desmet J, Spriet J, Lasters I (2002) Fast and accurate side-chain topology and energy refinement (FASTER) as a new method for protein structure optimization. Proteins 48:31-43. (Pubitemid 34595046)
94. Leach AR, Lemon AP (1998) Exploring the conformational space of protein side chains using dead-end elimination and the A&z.ast; algorithm. Proteins 33:227-239. (Pubitemid 28457975)
95. Kingsford CL, Chazelle B, Singh M (2005) Solving and analyzing side-chain positioning problems using linear and integer programming. Bioinformatics 21:1028-1036. (Pubitemid 40467925)
96. Lee C (1994) Predicting protein mutant energetics by self-consistent ensemble optimization. J Mol Biol 236:918-39.
97. Voigt CA, Gordon DB, Mayo SL (2000) Trading accuracy for speed: a quantitative comparison of search algorithms in protein sequence design. J Mol Biol 299:789-803.
98. Georgiev I, Keedy D, Richardson JS, Richardson DC, Donald BR (2008) Algorithm for backrub motions in protein design. Bioinformatics 24:i196-204. (Pubitemid 351911674)
99. Georgiev I, Lilien RH, Donald BR (2008) The minimized dead-end elimination criterion and its application to protein redesign in a hybrid scoring and search algorithm for computing partition functions over molecular ensembles. J Comput Chem 29:1527-1542.
100. Barth P, Alber T, Harbury PB (2007) Accurate, conformation-dependent predictions of solvent effects on protein ionization constants. Proc Natl Acad Sci USA 104:4898-4903. (Pubitemid 47186148)
101. Green DF, Dennis AT, Fam PS, Tidor B, Jasanoff A (2006) Rational design of new binding specificity by simultaneous mutagenesis of calmodulin and a target peptide. Biochemistry 45:12547-12559. (Pubitemid 44583697)
102. Grigoryan G, Zhou F, Lustig SR, Ceder G, Morgan D, Keating AE (2006) Ultra-fast evaluation of protein energies directly from sequence. PLoS Comput Biol 2:e63.
103. Kortemme T, Joachimiak LA, Bullock AN, Schuler AD, Stoddard BL, Baker D (2004). Computational redesign of protein-protein interaction specificity. Nat Struct Mol Biol 11:371-379. (Pubitemid 38436803)
104. Ali MH, Taylor CM, Grigoryan G, Allen KN, Imperiali B, Keating, AE (2005). Design of a heterospecific, tetrameric, 21-residue miniprotein with mixed alpha/beta structure. Structure 13:225-234. (Pubitemid 40247698)
105. Sammond DW, Eletr ZM, Purbeck C, Kuhlman B (2010) Computational design of second-site suppressor mutations at protein-protein interfaces. Proteins 78:1055-1065.
106. Potapov V, Reichmann D, Abramovich R, Filchtinski D, Zohar N, Ben Halevy D, Edelman M, Sobolev V, Schreiber G (2008) Computational redesign of a protein-protein interface for high affinity and binding specificity using modular architecture and naturally occurring template fragments. J Mol Biol 384:109-119.
107. Barth P, Schoeffler A, Alber T (2008) Targeting metastable coiled-coil domains by computational design. J Am Chem Soc 130:12038-12044.
108. Yosef E, Politi R, Choi MH, Shifman, JM (2009) Computational design of calmodulin mutants with up to 900-fold increase in binding specificity. J Mol Biol 385:1470-1480.
109. Reinke AW, Grigoryan G, Keating AE (2010) Identification of bZIP interaction partners of viral proteins HBZ, MEQ, BZLF1, and K-bZIP using coiled-coil arrays. Biochemistry 49:1985-1997.
110. Chen TS, Reinke AW, Keating AE (2011) Design of peptide inhibitors that bind the bZIP domain of Epstein-Barr virus protein BZLF1. J Mol Biol 408:304-320.
111. Sharabi O, Dekel A, Shifman JM (2011) Triathlon for energy functions: who is the winner for design of protein-protein interactions? Proteins 79:1487-1498.
112. Ramachandran S, Kota P, Ding F, Dokholyan NV (2011) Automated minimization of steric clashes in protein structures. Proteins 79:261-270.
113. Guerois R, Nielsen JE, Serrano L (2002) Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. J Mol Biol 320:369-387. (Pubitemid 34722226)
114. Pokala N, Handel TM (2005) Energy functions for protein design: adjustment with protein-protein complex affinities, models for the unfolded state, and negative design of solubility and specificity. J Mol Biol 347:203-227. (Pubitemid 40283639)
115. Yin S, Ding F, Dokholyan NV (2007) Modeling backbone flexibility improves protein stability estimation. Structure 15:1567-1576. (Pubitemid 350213412)
116. Potapov V, Cohen M, Schreiber G (2009) Assessing computational methods for predicting protein stability upon mutation: good on average but not in the details. Protein Eng Des Sel 22:553-560.
117. Lippow SM, Wittrup KD, Tidor B (2007) Computational design of antibody-affinity improvement beyond in vivo maturation. Nat Biotechnol 25:1171-1176. (Pubitemid 47538113)
118. Sammond DW, Eletr ZM, Purbeck C, Kimple RJ, Siderovski DP, Kuhlman B (2007) Structure-based protocol for identifying mutations that enhance protein-protein binding affinities. J Mol Biol 371:1392-1404. (Pubitemid 47198253)
119. Chen JR, Chang BH, Allen JE, Stiffler MA, MacBeath G (2008) Predicting PDZ domain-peptide interactions from primary sequences. Nat Biotechnol 26:1041-1045.
120. Gfeller D, Butty F, Wierzbicka M, Verschueren E, Vanhee P, Huang H, Ernst A, Dar N, Stagljar I, Serrano L, Sidhu SS, Bader GD, Kim PM (2011) The multiple-specificity landscape of modular peptide recognition domains. Mol Syst Biol 7:484.
121. Fong JH, Keating AE, Singh M (2004) Predicting specificity in bZIP coiled-coil protein interactions. Genome Biol 5:R11.
122. Acharya A, Rishi V, Vinson C (2006) Stability of 100 homo and heterotypic coiled-coil a-a' pairs for ten amino acids (A, L, I, V, N, K, S, T, E, and R). Biochemistry 45:11324-11332. (Pubitemid 44453980)
123. Skerker JM, Perchuk BS, Siryaporn A, Lubin EA, Ashenberg O, Goulian M, Laub MT (2008) Rewiring the specificity of two-component signal transduction systems. Cell 133:1043-1054. (Pubitemid 351787742)
124. Ashenberg O, Rozen-Gagnon K, Laub MT, Keating AE (2011) Determinants of homodimerization specificity in histidine kinases. J Mol Biol 413:222-235.
125. Jackel C, Kast P, Hilvert D (2008) Protein design by directed evolution. Annu Rev Biophys 37:153-173.
126. Cirino PC, Mayer KM, Umeno D (2003) Generating mutant libraries using error-prone PCR. Methods Mol Biol 231:3-9.
127. Shivange AV, Marienhagen J, Mundhada H, Schenk A, Schwaneberg U (2009) Advances in generating functional diversity for directed protein evolution. Curr Opin Chem Biol 13:19-25.
128. Mena MA, Daugherty PS (2005) Automated design of degenerate codon libraries. Protein Eng Des Sel 18:559-561. (Pubitemid 41668821)
129. Hayes RJ, Bentzien J, Ary ML, Hwang MY, Jacinto JM, Vielmetter J, Kundu A, Dahiyat BI (2002) Combining computational and experimental screening for rapid optimization of protein properties. Proc Natl Acad Sci USA 99:15926-15931. (Pubitemid 35462725)
130. Kayushin AL, Korosteleva MD, Miroshnikov AI, Kosch W, Zubov D, Piel N (1996) A convenient approach to the synthesis of trinucleotide phosphoramidites-synthons for the generation of oligonucleotide/peptide libraries. Nucleic Acids Res 24:3748-3755. (Pubitemid 26335384)
131. Zhao H, Arnold FH (1997) Optimization of DNA shuffling for high fidelity recombination. Nucleic Acids Res 25:1307-1308. (Pubitemid 27303227)
132. Frieder D, Larijani M, Tang E, Parsa JY, Basit W, Martin A (2006) Antibody diversification: mutational mechanisms and oncogenesis. Immunol Res 35:75-88. (Pubitemid 44547504)
133. Levin AM, Weiss GA (2006) Optimizing the affinity and specificity of proteins with molecular display. Mol Biosyst 2:49-57.
134. Sidhu SS, Koide S (2007) Phage display for engineering and analyzing protein interaction interfaces. Curr Opin Struct Biol 17:481-487. (Pubitemid 47451773)
135. Georgiou G, Poetschke HL, Stathopoulos C, Francisco JA (1993) Practical applications of engineering gram-negative bacterial cell surfaces. Trends Biotechnol 11:6-10. (Pubitemid 23036145)
136. Feldhaus MJ, Siegel RW, Opresko LK, Coleman JR, Feldhaus JM, Yeung YA, Cochran JR, Heinzelman P, Colby D, Swers J, Graff C, Wiley HS, Wittrup KD (2003) Flow-cytometric isolation of human antibodies from a nonimmune Saccharomyces cerevisiae surface display library. Nat Biotechnol 21:163-170. (Pubitemid 36188215)
137. Roberts RW, Szostak JW (1997) RNA-peptide fusions for the in vitro selection of peptides and proteins. Proc Natl Acad Sci USA 94:12297-12302. (Pubitemid 27492522)
138. Hanes J, Pluckthun A (1997) In vitro selection and evolution of functional proteins by using ribosome display. Proc Natl Acad Sci USA 94:4937-4942. (Pubitemid 27214714)
139. Norman TC, Smith DL, Sorger PK, Drees BL, O'Rourke SM, Hughes TR, Roberts CJ, Friend SH, Fields S, Murray AW (1999) Genetic selection of peptide inhibitors of biological pathways. Science 285:591-595.
140. Pelletier JN, Arndt KM, Pluckthun A, Michnick SW (1999) An in vivo library-versus-library selection of optimized protein-protein interactions. Nat Biotechnol 17:683-690. (Pubitemid 29316147)
141. Magliery TJ, Wilson CG, Pan W, Mishler D, Ghosh I, Hamilton AD, Regan L (2005) Detecting protein-protein interactions with a green fluorescent protein fragment reassembly trap: scope and mechanism. J Am Chem Soc 127:146-157. (Pubitemid 40094379)
142. Mason JM, Schmitz MA, Muller KM, Arndt KM (2006) Semirational design of Jun-Fos coiled coils with increased affinity: universal implications for leucine zipper prediction and design. Proc Natl Acad Sci USA 103:8989-8994. (Pubitemid 43902521)
143. Levin KB, Dym O, Albeck S, Magdassi S, Keeble AH, Kleanthous C, Tawfik DS (2009) Following evolutionary paths to protein-protein interactions with high affinity and selectivity. Nat Struct Mol Biol 16:1049-1055.
144. Mason JM, Muller KM, Arndt KM (2007) Positive aspects of negative design: simultaneous selection of specificity and interaction stability. Biochemistry 46:4804-4814. (Pubitemid 46651203)
145. Dutta S, Gulla S, Chen TS, Fire E, Grant RA, Keating AE (2010) Determinants of BH3 binding specificity for Mcl-1 versus Bcl-xL. J Mol Biol 398:747-762.
146. Abe Y, Yoshikawa T, Inoue M, Nomura T, Furuya T, Yamashita T, Nagano K, Nabeshi H, Yoshioka Y, Mukai Y, Nakagawa S, Kamada H, Tsutsumi Y, Tsunoda S (2011) Fine tuning of receptor-selectivity for tumor necrosis factor-alpha using a phage display system with one-step competitive panning. Biomaterials 32:5498-5504.
147. Matsumura N, Tsuji T, Sumida T, Kokubo M, Onimaru M, Doi N, Takashima H, Miyamoto-Sato E, Yanagawa H (2010) mRNA display selection of a high-affinity, Bcl-X(L)-specific binding peptide. FASEB J 24:2201-2210.
148. Ernst A, Gfeller D, Kan Z, Seshagiri S, Kim PM, Bader GD, Sidhu SS (2010) Coevolution of PDZ domain-ligand interactions analyzed by high-throughput phage display and deep sequencing. Mol Biosyst 6:1782-1790.
149. Voigt CA, Mayo SL, Arnold FH, Wang ZG (2001) Computational method to reduce the search space for directed protein evolution. Proc Natl Acad Sci USA 98:3778-3783. (Pubitemid 32249848)
150. Voigt CA, Martinez C, Wang ZG, Mayo SL, Arnold FH (2002) Protein building blocks preserved by recombination. Nat Struct Biol 9:553-558. (Pubitemid 34693812)
151. Treynor TP, Vizcarra CL, Nedelcu D, Mayo SL (2007) Computationally designed libraries of fluorescent proteins evaluated by preservation and diversity of function. Proc Natl Acad Sci USA 104:48-53. (Pubitemid 46067982)
152. Allen BD, Nisthal A, Mayo SL (2010) Experimental library screening demonstrates the successful application of computational protein design to large structural ensembles. Proc Natl Acad Sci USA 107:19838-19843.
153. Chica RA, Moore MM, Allen BD, Mayo SL (2010) Generation of longer emission wavelength red fluorescent proteins using computationally designed libraries. Proc Natl Acad Sci USA 107:20257-20262.
154. Barderas R, Desmet J, Timmerman P, Meloen R, Casal JI (2008) Affinity maturation of antibodies assisted by in silico modeling. Proc Natl Acad Sci USA 105:9029-9034.
155. Guntas G, Purbeck C, Kuhlman B (2010) Engineering a protein-protein interface using a computationally designed library. Proc Natl Acad Sci USA 107:19296-19301. 156.
156. Grove TZ, Hands M, Regan L (2010) Creating novel proteins by combining design and selection. Protein Eng Des Sel 23:449-455.
157. Lippow SM, Moon TS, Basu S, Yoon SH, Li X, Chapman BA, Robison K, Lipovsek D, Prather KL (2010) Engineering enzyme specificity using computational design of a defined-sequence library. Chem Biol 17:1306-1315.
158. Saraf MC, Moore GL, Goodey NM, Cao VY, Benkovic SJ, Maranas CD (2006) IPRO: an iterative computational protein library redesign and optimization procedure. Biophys J 90:4167-4180. (Pubitemid 43846131)
159. Pantazes RJ, Saraf MC, Maranas CD (2007) Optimal protein library design using recombination or point mutations based on sequence-based scoring functions. Protein Eng Des Sel 20:361-373. (Pubitemid 47428963)
160. Parker AS, Griswold KE, Bailey-Kellogg C (2011) Optimization of combinatorial mutagenesis. J Comput Biol 18:1743-1756.
161. Wang W, Saven JG (2002) Designing gene libraries from protein profiles
162. 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)
163. Otey CR, Landwehr M, Endelman JB, Hiraga K, Bloom JD, Arnold FH (2006) Structure-guided recombination creates an artificial family of cytochromes P450. PLoS Biol 4:e112.
164. Heinzelman P, Snow CD, Smith MA, Yu X, Kannan A, Boulware K, Villalobos A, Govindarajan S, Minshull J, Arnold FH (2009) SCHEMA recombination of a fungal cellulase uncovers a single mutation that contributes markedly to stability. J Biol Chem 284:26229-26233.
165. Khersonsky O, Rothlisberger D, Wollacott AM, Murphy P, Dym O, Albeck S, Kiss G, Houk KN, Baker D, Tawfik DS (2011) Optimization of the in-silico-designed kemp eliminase KE70 by computational design and directed evolution. J Mol Biol 407:391-412.
166. Karanicolas J, Corn JE, Chen I, Joachimiak LA, Dym O, Peck SH, Albeck S, Unger T, Hu W, Liu G, Delbecq S, Montelione GT, Spiegel CP, Liu DR, Baker D (2010). A de novo protein binding pair by computational design and directed evolution. Mol Cell 42:250-260.
167. Fleishman SJ, Whitehead TA, Ekiert DC, Dreyfus C, Corn JE, Strauch EM, Wilson IA, Baker D (2011) Computational design of proteins targeting the conserved stem region of influenza hemagglutinin. Science 332:816-821.
168. Rothlisberger D, Khersonsky O, Wollacott AM, Jiang L, DeChancie J, Betker J, Gallaher JL, Althoff EA, Zanghellini A, Dym O, Albeck S, Houk KN, Tawfik DS, Baker D (2008). Kemp elimination catalysts by computational enzyme design. Nature 453:190-195. (Pubitemid 351667979)
169. Musacchio A, Saraste M, Wilmanns M (1994) High-resolution crystal structures of tyrosine kinase SH3 domains complexed with proline-rich peptides. Nat Struct Biol 1:546-551.
170. Poy F, Yaffe MB, Sayos J, Saxena K, Morra M, Sumegi J, Cantley LC, Terhorst C, Eck MJ (1999) Crystal structures of the XLP protein SAP reveal a class of SH2 domains with extended, phosphotyrosine-independent sequence recognition. Mol Cell 4:555-561. (Pubitemid 29531135)
171. Birrane G, Chung J, Ladias JA (2003) Novel mode of ligand recognition by the Erbin PDZ domain. J Biol Chem 278:1399-13402.
172. Glover JN, Harrison SC (1995) Crystal structure of the heterodimeric bZIP transcription factor c-Fos-c-Jun bound to DNA. Nature 373:257-261.
173. Fire E, Gulla SV, Grant RA, Keating AE (2010) Mcl-1-Bim complexes accommodate surprising point mutations via minor structural changes. Protein Sci 19:507-519.
174. Meijers R, Puettmann-Holgado R, Skiniotis G, Liu JH, Walz T, Wang JH, Schmucker D (2007) Structural basis of Dscam isoform specificity. Nature 449:487-491. (Pubitemid 47509544)