A De Novo Protein Binding Pair By Computational Design and Directed Evolution

Molecular Cell

Volumn 42, Issue 2, 2011, Pages 250-260

  Karanicolas, John ^a,b   Corn, Jacob E ^a,g   Chen, Irwin ^c   Joachimiak, Lukasz A ^a,h   Dym, Orly ^d   Peck, Sun H ^c   Albeck, Shira ^d   Unger, Tamar ^e   Hu, Wenxin ^a   Liu, Gaohua ^f   Delbecq, Scott ^f   T Montelione, Gaetano ^e   P Spiegel, Clint ^e   Liu, David R ^c   Baker, David ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF KANSAS   (United States)

^c HARVARD UNIVERSITY   (United States)

^d WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^e RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^f WESTERN WASHINGTON UNIVERSITY   (United States)

^g GENENTECH INC   (United States)

^h STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HETERODIMER; PDAR PROTEIN; PRB PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; COMPUTATIONAL FLUID DYNAMICS; CRYSTAL STRUCTURE; MOLECULAR EVOLUTION; POINT MUTATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION;

BINDING SITES; CHEMISTRY TECHNIQUES, ANALYTICAL; COMPUTER-AIDED DESIGN; MODELS, MOLECULAR; MOLECULAR WEIGHT; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; PROTEIN MULTIMERIZATION; PROTEINS; SURFACE PROPERTIES;

EID: 79954633234     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.03.010     Document Type: Article

References (48)

1. Aharoni A., Gaidukov L., Khersonsky O., Mc Q.G.S., Roodveldt C., Tawfik D.S. The 'evolvability' of promiscuous protein functions. Nat. Genet. 2005, 37:73-76.
2. Aloy P., Ceulemans H., Stark A., Russell R.B. The relationship between sequence and interaction divergence in proteins. J. Mol. Biol. 2003, 332:989-998.
3. Apgar J.R., Gutwin K.N., Keating A.E. Predicting helix orientation for coiled-coil dimers. Proteins 2008, 72:1048-1065.
4. Batchelor A.H., Piper D.E., de la Brousse F.C., McKnight S.L., Wolberger C. The structure of GABPalpha/beta: an ETS domain- ankyrin repeat heterodimer bound to DNA. Science 1998, 279:1037-1041.
5. Binz H.K., Amstutz P., Pluckthun A. Engineering novel binding proteins from nonimmunoglobulin domains. Nat. Biotechnol. 2005, 23:1257-1268.
6. Bogan A.A., Thorn K.S. Anatomy of hot spots in protein interfaces. J. Mol. Biol. 1998, 280:1-9.
7. Bridgham J.T., Carroll S.M., Thornton J.W. Evolution of hormone-receptor complexity by molecular exploitation. Science 2006, 312:97-101.
8. Clackson T., Ultsch M.H., Wells J.A., de Vos A.M. Structural and functional analysis of the 1:1 growth hormone:receptor complex reveals the molecular basis for receptor affinity. J. Mol. Biol. 1998, 277:1111-1128.
9. Clackson T., Wells J.A. A Hot-Spot of Binding-Energy in a Hormone-Receptor. Interface Sci. 1995, 267:383-386.
10. Collins C.H., Leadbetter J.R., Arnold F.H. Dual selection enhances the signaling specificity of a variant of the quorum-sensing transcriptional activator LuxR. Nat. Biotechnol. 2006, 24:708-712.
11. Dantas G., Corrent C., Reichow S.L., Havranek J.J., Eletr Z.M., Isern N.G., Kuhlman B., Varani G., Merritt E.A., Baker D. High-resolution structural and thermodynamic analysis of extreme stabilization of human procarboxypeptidase by computational protein design. J. Mol. Biol. 2007, 366:1209-1221.
12. 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.
13. DeLano W.L. PyMol 2004, DeLano Scientific, San Carlos, CA.
14. Foit L., Morgan G.J., Kern M.J., Steimer L.R., von Hacht A.A., Titchmarsh J., Warriner S.L., Radford S.E., Bardwell J.C. Optimizing protein stability in vivo. Mol. Cell 2009, 36:861-871.
15. Grigoryan G., Keating A.E. Structure-based prediction of bZIP partnering specificity. J. Mol. Biol. 2006, 355:1125-1142.
16. Grigoryan G., Reinke A.W., Keating A.E. Design of protein-interaction specificity gives selective bZIP-binding peptides. Nature 2009, 458:859-864.
17. Guharoy M.P.C. Conservation and relative importance of residues across protein-protein interfaces. Proc. Natl. Acad. Sci. USA 2005, 102:15447-15452.
18. Hackel B.J., Kapila A., Wittrup K.D. Picomolar affinity fibronectin domains engineered utilizing loop length diversity, recursive mutagenesis, and loop shuffling. J. Mol. Biol. 2008, 381:1238-1252.
19. Horn J.R., Sosnick T.R., Kossiakoff A.A. Principal determinants leading to transition state formation of a protein-protein complex, orientation trumps side-chain interactions. Proc. Natl. Acad. Sci. USA 2009, 106:2559-2564.
20. Huang P.S., Love J.J., Mayo S.L. A de novo designed protein protein interface. Protein Sci. 2007, 16:2770-2774.
21. James L.C., Tawfik D.S. Conformational diversity and protein evolution-a 60-year-old hypothesis revisited. Trends Biochem. Sci. 2003, 28:361-368.
22. Jha R.K., Leaver-Fay A., Yin S., Wu Y., Butterfoss G.L., Szyperski T., Dokholyan N.V., Kuhlman B. Computational Design of a PAK1 Binding Protein. J. Mol. Biol. 2010, 400:257-270.
23. Kang S.A., Crane B.R. Effects of interface mutations on association modes and electron-transfer rates between proteins. Proc. Natl. Acad. Sci. USA 2005, 102:15465-15470.
24. Khersonsky O., Roodveldt C., Tawfik D.S. Enzyme promiscuity: evolutionary and mechanistic aspects. Curr. Opin. Chem. Biol. 2006, 10:498-508.
25. Kohl A., Amstutz P., Parizek P., Binz H.K., Briand C., Capitani G., Forrer P., Pluckthun A., Grutter M.G. Allosteric inhibition of aminoglycoside phosphotransferase by a designed ankyrin repeat protein. Structure 2005, 13:1131-1141.
26. Kortemme T., Joachimiak L.A., Bullock A.N., Schuler A.D., Stoddard B.L., Baker D. Computational redesign of protein-protein interaction specificity. Nat. Struct. Mol. Biol. 2004, 11:371-379.
27. Kuhlman B., Dantas G., Ireton G.C., Varani G., Stoddard B.L., Baker D. Design of a novel globular protein fold with atomic-level accuracy. Science 2003, 302:1364-1368.
28. Letunic I., Copley R.R., Pils B., Pinkert S., Schultz J., Bork P. SMART 5: domains in the context of genomes and networks. Nucleic Acids Res. 2006, 34:D257-D260.
29. Li X., Keskin O., Ma B.Y., Nussinov R., Liang J. Protein-protein interactions: Hot spots and structurally conserved residues often locate in complemented pockets that pre-organized in the unbound states: Implications for docking. J. Mol. Biol. 2004, 344:781-795.
30. London N., Schueler-Furman O. Funnel hunting in a rough terrain: Learning and discriminating native energy funnels. Structure 2008, 16:269-279.
31. Mandell D.J., Kortemme T. Backbone flexibility in computational protein design. Curr. Opin. Biotechnol. 2009, 20:420-428.
32. Mandell D.J., Kortemme T. Computer-aided design of functional protein interactions. Nat. Chem. Biol. 2009, 5:797-807.
33. Moreira I.S., Fernandes P.A., Ramos M.J. Computational alanine scanning mutagenesis-an improved methodological approach. J. Comput. Chem. 2007, 28:644-654.
34. Mosavi L.K., Cammett T.J., Desrosiers D.C., Peng Z.Y. The ankyrin repeat as molecular architecture for protein recognition. Protein Sci. 2004, 13:1435-1448.
35. Mukherjee S., Zhang Y. MM-align: a quick algorithm for aligning multiple-chain protein complex structures using iterative dynamic programming. Nucleic Acids Res. 2009, 37:e83.
36. Pan X., Luhrmann A., Satoh A., Laskowski-Arce M.A., Roy C.R. Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors. Science 2008, 320:1651-1654.
37. Park S.Y., Beel B.D., Simon M.I., Bilwes A.M., Crane B.R. In different organisms, the mode of interaction between two signaling proteins is not necessarily conserved. Proc. Natl. Acad. Sci. USA 2004, 101:11646-11651.
38. Rajamani D., Thiel S., Vajda S., Camacho C.J. Anchor residues in protein-protein interactions. Proc. Natl. Acad. Sci. USA 2004, 101:11287-11292.
39. Reinke A.W., Grant R.A., Keating A.E. A synthetic coiled-coil interactome provides heterospecific modules for molecular engineering. J. Am. Chem. Soc. 2010, 132:6025-6031.
40. Schlosshauer M., Baker D. Realistic protein-protein association rates from a simple diffusional model neglecting long-range interactions, free energy barriers, and landscape ruggedness. Protein Sci. 2004, 13:1660-1669.
41. Schneidman-Duhovny D., Inbar Y., Polak V., Shatsky M., Halperin I., Benyamini H., Barzilai A., Dror O., Haspel N., Nussinov R., et al. Taking geometry to its edge: fast unbound rigid (and hinge-bent) docking. Proteins 2003, 52:107-112.
42. Sheffler W., Baker D. RosettaHoles: rapid assessment of protein core packing for structure prediction, refinement, design, and validation. Protein Sci. 2009, 18:229-239.
43. Shifman J.M., Mayo S.L. Modulating calmodulin binding specificity through computational protein design. J. Mol. Biol. 2002, 323:417-423.
44. Steiner D., Forrer P., Pluckthun A. Efficient selection of DARPins with sub-nanomolar affinities using SRP phage display. J. Mol. Biol. 2008, 382:1211-1227.
45. Xu L., Aha P., Gu K., Kuimelis R.G., Kurz M., Lam T., Lim A.C., Liu H., Lohse P.A., Sun L., et al. Directed evolution of high-affinity antibody mimics using mRNA display. Chem. Biol. 2002, 9:933-942.
46. Yu D., Volkov A.N., Tang C. Characterizing dynamic protein-protein interactions using differentially scaled paramagnetic relaxation enhancement. J. Am. Chem. Soc. 2009, 131:17291-17297.
47. Zaccolo M., Williams D.M., Brown D.M., Gherardi E. An approach to random mutagenesis of DNA using mixtures of triphosphate derivatives of nucleoside analogues. J. Mol. Biol. 1996, 255:589-603.
48. Zhang Y., Skolnick J. TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Res. 2005, 33:2302-2309.