Hotspot-centric de novo design of protein binders

Journal of Molecular Biology

Volumn 413, Issue 5, 2011, Pages 1047-1062

  Fleishman, Sarel J ^a,c   Corn, Jacob E ^a,d   Strauch, Eva Maria ^a   Whitehead, Timothy A ^a,e   Karanicolas, John ^a,f   Baker, David ^a,b  

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

^b UNIVERSITY OF WASHINGTON   (United States)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^d GENENTECH INC   (United States)

^e Michigan State University   (United States)

^f UNIVERSITY OF KANSAS   (United States)

Author keywords

antibody engineering; computational design; conformational plasticity; negative design; protein interactions

Indexed keywords

ARGININE; ASPARAGINE; ASPARTIC ACID; BARNASE; BARSTAR; BINDING PROTEIN; COLICIN; COLICIN E9; COLICIN IM9; FC RECEPTOR; GLUTAMINE; HEMAGGLUTININ; HISTIDINE; ISOLEUCINE; LYSOZYME; PHENYLALANINE; PROTEIN BINDER; SCAFFOLD PROTEIN; TRYPTOPHAN; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; COMPUTER AIDED DESIGN; CONFORMATIONAL TRANSITION; DE NOVO DESIGN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; SURFACE PROPERTY;

EID: 80855140813     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.09.001     Document Type: Article

References (60)

1. Koide A., and Koide S. Monobodies: antibody mimics based on the scaffold of the fibronectin type III domain Methods Mol. Biol. 352 2007 95 109
2. Binz H.K., Amstutz P., Kohl A., Stumpp M.T., Briand C., and Forrer P. High-affinity binders selected from designed ankyrin repeat protein libraries Nat. Biotechnol. 22 2004 575 582 (Pubitemid 38590636)
3. Binz H.K., Amstutz P., and Pluckthun A. Engineering novel binding proteins from nonimmunoglobulin domains Nat. Biotechnol. 23 2005 1257 1268 (Pubitemid 41486853)
4. Binz H.K., and Pluckthun A. Engineered proteins as specific binding reagents Curr. Opin. Biotechnol. 16 2005 459 469 (Pubitemid 41114852)
5. Binz H.K., Stumpp M.T., Forrer P., Amstutz P., and Pluckthun A. Designing repeat proteins: well-expressed, soluble and stable proteins from combinatorial libraries of consensus ankyrin repeat proteins J. Mol. Biol. 332 2003 489 503 (Pubitemid 37020959)
6. Lo Conte L., Chothia C., and Janin J. The atomic structure of protein-protein recognition sites J. Mol. Biol. 285 1999 2177 2198 (Pubitemid 29078179)
7. Lawrence M.C., and Colman P.M. Shape complementarity at protein/protein interfaces J. Mol. Biol. 234 1993 946 950 (Pubitemid 24027225)
8. Nassar N., Hoffman G.R., Manor D., Clardy J.C., and Cerione R.A. Structures of Cdc42 bound to the active and catalytically compromised forms of Cdc42GAP Nat. Struct. Biol. 5 1998 1047 1052 (Pubitemid 28546267)
9. Stebbins C.E., and Galan J.E. Modulation of host signaling by a bacterial mimic: structure of the Salmonella effector SptP bound to Rac1 Mol. Cell 6 2000 1449 1460 (Pubitemid 32045936)
10. DeLano W.L. The PyMOL Molecular Graphics Systems 2002 DeLano Scientific Palo Alto, CA
11. Bogan A.A., and Thorn K.S. Anatomy of hot spots in protein interfaces J. Mol. Biol. 280 1998 1 9 (Pubitemid 28312802)
12. Clackson T., and Wells J.A. A hot spot of binding energy in a hormone-receptor interface Science 267 1995 383 386
13. Clackson T., Ultsch M.H., Wells J.A., and 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. 277 1998 1111 1128 (Pubitemid 28190850)
14. Ofran Y., and Rost B. Protein-protein interaction hotspots carved into sequences PLoS Comput. Biol. 3 2007 e119
15. Hu Z., Ma B., Wolfson H., and Nussinov R. Conservation of polar residues as hot spots at protein interfaces Proteins 39 2000 331 342 (Pubitemid 30414171)
16. Ma B., Elkayam T., Wolfson H., and Nussinov R. Protein-protein interactions: structurally conserved residues distinguish between binding sites and exposed protein surfaces Proc. Natl Acad. Sci. USA 100 2003 5772 5777 (Pubitemid 36576883)
17. Stebbins C.E., and Galan J.E. Structural mimicry in bacterial virulence Nature 412 2001 701 705 (Pubitemid 32771986)
18. Liu S., Zhu X., Liang H., Cao A., Chang Z., and Lai L. Nonnatural protein-protein interaction-pair design by key residues grafting Proc. Natl Acad. Sci. USA 104 2007 5330 5335 (Pubitemid 47175680)
19. Havranek J.J., and Baker D. Motif-directed flexible backbone design of functional interactions Protein Sci. 18 2009 1293 1305
20. Fleishman S.J., Khare S.D., Koga N., and Baker D. Restricted sidechain plasticity in the structures of native proteins and complexes Protein Sci. 20 2011 753 757
21. Karanicolas J., Corn J.E., Chen I., Joachimiak L.A., Dym O., and Peck S.H. A de novo protein binding pair by computational design and directed evolution Mol. Cell 42 2011 250 260
22. Richardson J.S., Richardson D.C., Tweedy N.B., Gernert K.M., Quinn T.P., and Hecht M.H. Looking at proteins: representations, folding, packing, and design. Biophysical Society National Lecture, 1992 Biophys. J. 63 1992 1185 1209
23. Havranek J.J., and Harbury P.B. Automated design of specificity in molecular recognition Nat. Struct. Biol. 10 2003 45 52 (Pubitemid 36034176)
24. Grigoryan G., Reinke A.W., and Keating A.E. Design of protein-interaction specificity gives selective bZIP-binding peptides Nature 458 2009 859 864
25. Fleishman S.J., Whitehead T.A., Ekiert D.C., Dreyfus C., Corn J.E., and Strauch E.M. Computational design of proteins targeting the conserved stem region of influenza hemagglutinin Science 332 2011 816 821
26. Gray J.J., Moughon S., Wang C., Schueler-Furman O., Kuhlman B., Rohl C.A., and Baker D. Protein-protein docking with simultaneous optimization of rigid-body displacement and side-chain conformations J. Mol. Biol. 331 2003 281 299 (Pubitemid 36870793)
27. Fleishman, S. J., Leaver-Fay, A., Corn, J. E., Strauch, E. M., Khare, S. D., Koga, N., et al. (2011). RosettaScripts: a scripting language interface to the Rosetta macromolecular modeling suite. PLoS ONE, in press.
28. Ben-Shimon A., and Eisenstein M. Computational mapping of anchoring spots on protein surfaces J. Mol. Biol. 402 2010 259 277
29. Kuhlmann U.C., Pommer A.J., Moore G.R., James R., and Kleanthous C. Specificity in protein-protein interactions: the structural basis for dual recognition in endonuclease colicin-immunity protein complexes J. Mol. Biol. 301 2000 1163 1178
30. Schneidman-Duhovny D., Inbar Y., Nussinov R., and Wolfson H.J. PatchDock and SymmDock: servers for rigid and symmetric docking Nucleic Acids Res. 33 2005 W363 W367 (Pubitemid 44529944)
31. Kuhlman B., Dantas G., Ireton G.C., Varani G., Stoddard B.L., and Baker D. Design of a novel globular protein fold with atomic-level accuracy Science 302 2003 1364 1368 (Pubitemid 37452172)
32. Kortemme T., and Baker D. A simple physical model for binding energy hot spots in protein-protein complexes Proc. Natl Acad. Sci. USA 99 2002 14116 14121 (Pubitemid 35257634)
33. Kellogg E.H., Leaver-Fay A., and Baker D. Role of conformational sampling in computing mutation-induced changes in protein structure and stability Proteins 79 2011 830 838
34. Idusogie E.E., Presta L.G., Gazzano-Santoro H., Totpal K., Wong P.Y., and Ultsch M. Mapping of the C1q binding site on rituxan, a chimeric antibody with a human IgG1 Fc J. Immunol. 164 2000 4178 4184 (Pubitemid 30215076)
35. Stanfield R.L., Dooley H., Flajnik M.F., and Wilson I.A. Crystal structure of a shark single-domain antibody V region in complex with lysozyme Science 305 2004 1770 1773 (Pubitemid 39249643)
36. Buckle A.M., Schreiber G., and Fersht A.R. Protein-protein recognition: crystal structural analysis of a barnase-barstar complex at 2.0-Å resolution Biochemistry 33 1994 8878 8889 (Pubitemid 24257995)
37. Ekiert D.C., Bhabha G., Elsliger M.A., Friesen R.H., Jongeneelen M., and Throsby M. Antibody recognition of a highly conserved influenza virus epitope Science 324 2009 246 251
38. Schreiber G., and Fersht A.R. Rapid, electrostatically assisted association of proteins Nat. Struct. Biol. 3 1996 427 431 (Pubitemid 26139441)
39. Wallis R., Moore G.R., James R., and Kleanthous C. Protein-protein interactions in colicin E9 DNase-immunity protein complexes. 1. Diffusion-controlled association and femtomolar binding for the cognate complex Biochemistry 34 1995 13743 13750
40. Braisted A.C., and Wells J.A. Minimizing a binding domain from protein A Proc. Natl Acad. Sci. USA 93 1996 5688 5692 (Pubitemid 26190741)
41. Zanghellini A., Jiang L., Wollacott A.M., Cheng G., Meiler J., and Althoff E.A. New algorithms and an in silico benchmark for computational enzyme design Protein Sci. 15 2006 2785 2794 (Pubitemid 44833759)
42. Guharoy M., and Chakrabarti P. Conservation and relative importance of residues across protein-protein interfaces Proc. Natl Acad. Sci. USA 102 2005 15447 15452 (Pubitemid 41528077)
43. Pal G., Kouadio J.L., Artis D.R., Kossiakoff A.A., and Sidhu S.S. Comprehensive and quantitative mapping of energy landscapes for protein-protein interactions by rapid combinatorial scanning J. Biol. Chem. 281 2006 22378 22385 (Pubitemid 44181940)
44. Humphris E.L., and Kortemme T. Prediction of protein-protein interface sequence diversity using flexible backbone computational protein design Structure 16 2008 1777 1788
45. Jin L., and Wells J.A. Dissecting the energetics of an antibody-antigen interface by alanine shaving and molecular grafting Protein Sci. 3 1994 2351 2357
46. Castro M.J., and Anderson S. Alanine point-mutations in the reactive region of bovine pancreatic trypsin inhibitor: effects on the kinetics and thermodynamics of binding to β-trypsin and α-chymotrypsin Biochemistry 35 1996 11435 11446 (Pubitemid 26299318)
47. Sharabi O., Dekel A., and Shifman J.M. Triathlon for energy functions: who is the winner for design of protein-protein interactions? Proteins 79 2011 1487 1498
48. Mandell D.J., Coutsias E.A., and Kortemme T. Sub-angstrom accuracy in protein loop reconstruction by robotics-inspired conformational sampling Nat. Methods 6 2009 551 552
49. Murphy P.M., Bolduc J.M., Gallaher J.L., Stoddard B.L., and Baker D. Alteration of enzyme specificity by computational loop remodeling and design Proc. Natl Acad. Sci. USA 106 2009 9215 9220
50. Pierce B., and Weng Z. ZRANK: reranking protein docking predictions with an optimized energy function Proteins 67 2007 1078 1086 (Pubitemid 46753952)
51. Chen R., Li L., and Weng Z. ZDOCK: an initial-stage protein-docking algorithm Proteins 52 2003 80 87 (Pubitemid 36648854)
52. Hwang H., Pierce B., Mintseris J., Janin J., and Weng Z. Protein-protein docking benchmark version 3.0 Proteins 73 2008 705 709 (Pubitemid 352788651)
53. Bowie J.U., Luthy R., and Eisenberg D. A method to identify protein sequences that fold into a known three-dimensional structure Science 253 1991 164 170 (Pubitemid 21917131)
54. Moore G.E. Lithography and the future of Moore's law Proc. SPIE 2438 1995
55. Joachimiak A. High-throughput crystallography for structural genomics Curr. Opin. Struct. Biol. 19 2009 573 584
56. PPI webserver: fast and accurate in silico alanine scanning for scoring protein-protein interactions Nucleic Acids Res. 38 2010 W480 W486
57. Kortemme T., Kim D.E., and Baker D. Computational alanine scanning of protein-protein interfaces Sci. STKE 2004 2004 pl2
58. Dunbrack R.L. Jr., and Karplus M. Conformational analysis of the backbone-dependent rotamer preferences of protein sidechains Nat. Struct. Biol. 1 1994 334 340
59. Das R., and Baker D. Macromolecular modeling with Rosetta Annu. Rev. Biochem. 77 2008 363 382
60. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 1994 760 763