Computational design and characterisation of artificial enzymes for Kemp elimination

References

• Radzicka , A. and Wolfenden , R.A. 1995 . A proficient enzyme . Science , 267 : 90 – 93 .
   PubMed Web of Science ®Google Scholar
• Frey , P.A. and Hegeman , A.D. 2007 . Enzymatic Reaction Mechanisms , New York : Oxford University Press .
   Google Scholar
• Rothlisberger , D. , Khersonsky , O. , Wollacott , A.M. , Jiang , L. , Dechancie , J. , Betker , J. , Gallaher , J.L. , Althoff , E.A. , Zanghellini , A. , Dym , O. , Albeck , S. , Houk , K.N. , Tawfik , D.S. and Baker , D. 2008 . Kemp elimination catalysts by computational enzyme design . Nature , 453 : 109 – 195 .
   Web of Science ®Google Scholar
• Bolon , D.N. and Mayo , S.L. 2001 . Enzyme-like proteins by computational design . Proc. Natl Acad. Sci. USA , 98 : 14274 – 14279 .
   PubMed Web of Science ®Google Scholar
• Jiang , L. , Althoff , E.A. , Clemente , F.R. , Doyle , L. , Rothlisberger , D. , Zanghellini , A. , Gallaher , J.L. , Betker , J. , Tanaka , F. , Barbas , C.F. III , Hilvert , D. , Houk , K.N. , Stoddard , B.L. and Baker , D. 2008 . De novo computational design of retro-aldol enzymes . Science , 319 : 1387 – 1391 .
   PubMed Web of Science ®Google Scholar
• Vasileiou , C. , Vaezeslami , S. , Crist , R.M. , Rabado-Smith , M. , Geiger , J.H. and Borthan , B. 2007 . Protein design: Reengineering cellular retinoic acid binding protein II into a Rhodopsin protein mimic . J. Am. Chem. Soc. , 129 : 6140 – 6148 .
   PubMed Web of Science ®Google Scholar
• Pinto , A.L. , Hellinga , H.W. and Caradonna , J.P. 1997 . Construction of a catalytically active iron superoxide dismutase by rational protein design . Proc. Natl Acad. Sci. USA , 94 : 5562 – 5567 .
   PubMed Web of Science ®Google Scholar
• Kaplan , J. and Degrado , W.F. 2004 . De novo design of catalytic proteins . Proc. Natl Acad. Sci. USA , 101 : 11566 – 11570 .
   PubMed Web of Science ®Google Scholar
• Hilvert , D. 2000 . Critical analysis of antibody catalysis . Annu. Rev. Biochem. , 69 : 751 – 793 .
   PubMed Web of Science ®Google Scholar
• Lerner , R.A. , Benkovic , S.J. and Schultz , P.G. 1991 . At the crossroads of chemistry and immunology: Catalytic antibodies . Science , 252 : 659 – 667 .
   PubMed Web of Science ®Google Scholar
• Dahiyat , B.I. and Mayo , S.L. 1996 . Protein design automation . Protein Sci. , 5 : 895 – 903 .
   PubMed Web of Science ®Google Scholar
• Zanghellini , A. , Jiang , L. , Wollacott , A.M. , Cheng , G. , Meiler , J. , Althoff , E.A. , Rothlisberger , D. and Baker , D. 2006 . New algorithms and an in silico benchmark for computational enzyme design . Protein Sci. , 15 : 2785 – 2794 .
   PubMed Web of Science ®Google Scholar
• Ujaque , G. , Tantillo , D.J. , Hu , Y. , Houk , K.N. , Hotta , K. and Hilvert , D. 2002 . Catalysis on the coastline: Theozyme, molecular dynamics, and free energy perturbation analysis of antibody 21D8 catalysis of the decarboxylation of 5-nitro-3-carboxybenzisoxazole . J. Comput. Chem. , 24 : 98 – 110 .
   Web of Science ®Google Scholar
• Thorn , S.N. , Daniels , R.G. , Auditor , M.-T.M. and Hilvert , D. 1995 . Large rate accelerations in antibody catalysis by strategic use of haptenic charge . Nature , 373 : 228 – 230 .
   PubMed Web of Science ®Google Scholar
• Seeback , F.P. and Hilvert , D. 2005 . Positional ordering of reacting groups contributes significantly to the efficiency of proton transfer at an antibody active site . J. Am. Chem. Soc. , 127 : 1307 – 1312 .
   PubMed Web of Science ®Google Scholar
• Hu , Y. , Houk , K.N. , Kikuchi , K. , Hotta , K. and Hilvert , D. 2004 . Nonspecific medium effects versus specific group positioning in the antibody and albumin catalysis of the base-promoted ring-opening reactions of benzisoxazoles . J. Am. Chem. Soc. , 126 : 8197 – 8205 .
   PubMed Web of Science ®Google Scholar
• Khersonsky , O. , Rothlisberger , D. , Dym , O. , Albeck , S. , Jackson , C.J. , Baker , D. and Tawfik , D.S. 2010 . Evolutionary optimization of computationally designed enzymes: Kemp eliminases of the KE07 series . J. Mol. Biol. , 396 : 1025 – 1042 .
   PubMed Web of Science ®Google Scholar
• Debler , E.W. , Ito , S. , Seebeck , F.P. , Heine , A. , Hilvert , D. and Wilson , I.A. 2005 . Structural origins of efficient proton abstraction from carbon by a catalytic antibody . Proc. Natl Acad. Sci. USA , 102 : 4984 – 4989 .
   PubMed Web of Science ®Google Scholar
• Muller , R. , Debler , E.W. , Steinmann , M. , Seeback , F.P. , Wilson , I.A. and Hilvert , D. 2007 . Bifunctional catalysis of proton transfer at an antibody active site . J. Am. Chem. Soc. , 129 : 460 – 461 .
   PubMed Web of Science ®Google Scholar
• James , L.C. and Tawfik , D.S. 2001 . Catalytic and binding poly-reactivities shared by two unrelated proteins: The potential role of promiscuity in enzyme evolution . Protein Sci. , 10 : 2600 – 2607 .
   PubMed Web of Science ®Google Scholar
• Alexandrova , A.N. , Rothlisberger , D. , Baker , D. and Jorgensen , W.L. 2008 . Catalytic mechanism and performance of computationally designed enzymes for Kemp elimination . J. Am. Chem. Soc. , 130 : 15907 – 15915 .
   PubMed Web of Science ®Google Scholar
• Alexandrova , A.N. and Jorgensen , W.L. 2009 . Origin of the activity drop with the E50D variant of catalytic antibody 34E4 for Kemp elimination . J. Phys. Chem. B , 113 : 497 – 504 .
   PubMed Web of Science ®Google Scholar
• Na , J. , Houk , K.N. and Hilvert , D. 1996 . Transition state of the base-promoted ring-opening of isoxazoles. Theoretical prediction of catalytic functionalities and design of haptens for antibody production . J. Am. Chem. Soc. , 118 : 6462 – 6471 .
   Web of Science ®Google Scholar
• Kiss , G. , Rothlisberger , D. , Baker , D. and Houk , K.N. 2010 . Evaluation and ranking of enzyme designs . Protein Sci. , 19 : 1760 – 1773 .
   PubMed Web of Science ®Google Scholar
• Khersonsky , O. , Rothlisberger , D. , Wollacott , A.M. , Murphy , P. , Dym , O. , Albeck , S. , Kiss , G. , Houk , K.N. , Baker , D. and Tawfik , D.S. in press . Optimization of the in silico designed Kemp eliminase KE70 by computational design and directed evolution . J. Mol. Biol. ,
   Web of Science ®Google Scholar
• Acevedo , O. 2009 . Role of water in the multifaceted catalytic antibody 4B2 for allylic isomerization and Kemp elimination reactions . J. Phys. Chem. B , 113 : 15372 – 15381 .
   PubMed Web of Science ®Google Scholar
• Frushicheva , M.P. , Cao , J. , Chu , Z.T. and Warshel , A. 2010 . Exploring challenges in rational enzyme design by simulating the catalysis in artificial kemp eliminase . Proc. Natl Acad. Sci. USA , 107 : 16869 – 16874 .
   PubMed Web of Science ®Google Scholar
• Ruscio , J.Z. , Kohn , J.E. , Ball , K.A. and Head-Gordon , T. 2009 . The influence of protein dynamics on the success of computational enzyme design . J. Am. Chem. Soc. , 131 : 14111 – 14115 .
   PubMed Web of Science ®Google Scholar
• Dechancie , J. , Clemente , F.R. , Smith , A.J.T. , Gunaydin , H. , Zhao , Y.-L. , Zhang , X. and Houk , K.N. 2007 . How similar are enzyme active site geometries derived from quantum mechanical theozymes to crystal structures of enzyme-inhibitor complexes? Implications for enzyme design . Protein Sci. , 16 : 1851 – 1866 .
   PubMed Web of Science ®Google Scholar
• Tantillo , D.J. , Chen , J. and Houk , K.N. 1998 . Theozymes and compuzymes: Theoretical models for biological catalysis . Curr. Opin. Chem. Biol. , 2 : 743 – 750 .
   PubMed Web of Science ®Google Scholar
• Parr , R.G. and Yang , W. 1989 . Density-Functional Theory of Atoms and Molecules , Oxford : Oxford University Press .
   Google Scholar
• Becke , A.D. 1993 . Density-functional thermochemistry. III. The role of exact exchange . J. Chem. Phys. , 98 : 5648 – 5652 .
   Web of Science ®Google Scholar
• Perdew , J.P. , Chevary , J.A. , Vosko , S. , Jackson , K.A. , Pederson , M.R. , Singh , D.J. and Fiolhais , C. 1992 . Atoms, molecules, solids, and surfaces: Applications of the generalized gradient approximation for exchange and correlation . Phys. Rev. B , 46 : 6671 – 6687 .
   PubMed Web of Science ®Google Scholar
• Head-Gordon , M. , Pople , J.A. and Frisch , M.J. 1988 . MP2 energy evaluation by direct methods . Chem. Phys. Lett. , 153 : 503 – 506 .
   Web of Science ®Google Scholar
• Frisch , M.J. , Head-Gordon , M. and Pople , J.A. 1990 . Direct MP2 gradient method . Chem. Phys. Lett. , 166 : 275 – 280 .
   Web of Science ®Google Scholar
• Frisch , M.J. , Head-Gordon , M. and Pople , J.A. 1990 . Semi-direct algorithms for the MP2 energy and gradient . Chem. Phys. Lett. , 166 : 281 – 289 .
   Web of Science ®Google Scholar
• Frisch , M.J. , Trucks , G.W. , Schlegel , H.B. , Scuseria , G.E. , Robb , M.A. , Cheeseman , J.R. , Scalmani , G. , Barone , V. , Mennucci , B. , Petersson , G.A. , Nakatsuji , H. , Caricato , M. , Li , X. , Hratchian , H.P. , Izmaylov , A.F. , Bloino , J. , Zheng , G. , Sonnenberg , J.L. , Hada , M. , Ehara , M. , Toyota , K. , Fukuda , R. , Hasegawa , J. , Ishida , M. , Nakajima , T. , Honda , Y. , Kitao , O. , Nakai , H. , Vreven , T. , Montgomery, Jr. , J.A. , Peralta , J.E. , Ogliaro , F. , Bearpark , M. , Heyd , J.J. , Brothers , E. , Kudin , K.N. , Staroverov , V.N. , Kobayashi , R. , Normand , J. , Raghavachari , K. , Rendell , A. , Burant , J.C. , Iyengar , S.S. , Tomasi , J. , Cossi , M. , Rega , N. , Millam , J.M. , Klene , M. , Knox , J.E. , Cross , J.B. , Bakken , V. , Adamo , C. , Jaramillo , J. , Gomperts , R. , Stratmann , R.E. , Yazyev , O. , Austin , A.J. , Cammi , R. , Pomelli , C. , Ochterski , J.W. , Martin , R.L. , Morokuma , K. , Zakrzewski , V.G. , Voth , G.A. , Salvador , P. , Dannenberg , J.J. , Dapprich , S. , Daniels , A.D. , Farkas , O. , Foresman , J.B. , Ortiz , J.V. , Cioslowski , J. and Fox , D.J. 2009 . Gaussian 09, Revision A.02 , Gaussian, Inc: Wallingford CT
   Google Scholar
• Kuhlman , B. , Dantas , G. , Ireton , G.C. , Varani , B. , Stoddard , B.L. and Baker , D. 2003 . Design of a novel globular protein fold with atomic-level accuracy . Science , : 302
   Google Scholar
• Meiler , J. and Baker , D. 2006 . ROSETTALIGAND: Protein-small molecule docking with full side-chain flexibility . Proteins , 65 : 538 – 548 .
   PubMed Web of Science ®Google Scholar
• Acevedo , O. and Jorgensen , W.L. 2005 . Influence of inter- and intramolecular hydrogen bonding on Kemp decarboxylations from QM/MM simulations . J. Am. Chem. Soc. , 127 : 8829 – 8834 .
   PubMed Web of Science ®Google Scholar
• Dantas , G. , Kuhlman , B. , Callender , D. , Wong , M. and Baker , D. 2003 . A large scale test of computational protein design: Folding and stability of nine completely redesigned globular proteins . J. Mol. Biol. , 332 : 449 – 460 .
   PubMed Web of Science ®Google Scholar
• Ulmschneider , J.P. and Jorgensen , W.L. 2004 . Monte Carlo backbone sampling for nucleic acids using concerted rotations including variable bond angles . J. Phys. Chem. B , 108 : 16883 – 16892 .
   Web of Science ®Google Scholar
• Ulmschneider , J.P. and Jorgensen , W.L. 2004 . Polypeptide folding using Monte Carlo sampling, concerted rotation, and continum solvation . J. Am. Chem. Soc. , 126 : 1849 – 1857 .
   PubMed Web of Science ®Google Scholar
• Proctor , E.A. , Ding , F. and Dokholyan , N.V. 2010 . “ Discrete molecular dynamics ” . Wiley Interdisciplinary Reviews: Computational Molecular Science
   Google Scholar
• Ding , F. and Dokholyan , N.V. 2005 . Trends Biotechnol. , 23 : 450 – 455 . Simple but predictive protein models
   PubMed Web of Science ®Google Scholar
• Jorgensen , W.L. and Tirado-Rives , J. 2005 . Molecular modeling of organic and biomolecular systems using BOSS and MCPRO . J. Comput. Chem. , 26 : 1689 – 1700 .
   PubMed Web of Science ®Google Scholar
• Repasky , M.P. , Chandrasekhar , J. and Jorgensen , W.L. 2002 . DDG/PM3 and PDDG/MNDO: Improved semiempirical methods . J. Comput. Chem. , 23 : 1601 – 1622 .
   PubMed Web of Science ®Google Scholar
• Tubert-Brohman , I. , Guimaraes , C.R.W. , Repasky , M.P. and Jorgensen , W.L. 2004 . Extension of the PDDG/PM3 and PDDG/MNDO semiempirical molecular orbital methods to halogens . J. Comput. Chem. , 25 : 138 – 150 .
   PubMed Web of Science ®Google Scholar
• Jorgensen , W.L. , Maxwell , D.S. and Tirado-Rives , J. 1996 . Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids . J. Am. Chem. Soc. , 118 : 11225 – 11236 .
   Web of Science ®Google Scholar
• Jorgensen , W.L. , Chandrasekhar , J. , Madure , J.D. , Impey , W. and Klein , M.L. 1983 . Comparison of simple potential functions for simulating liquid water . J. Chem. Phys. , 79 : 926 – 935 .
   Web of Science ®Google Scholar
• Jorgensen , W.L. and Jenson , C. 1998 . Temperature dependence of TIP3P, SPC, and TIP4P water from NPT Monte Carlo simulations: Seeking a temperature of maximum density . J. Comput. Chem. , 19 : 1179 – 1186 .
   Web of Science ®Google Scholar
• Tubert-Brohman , I. , Acevedo , O. and Jorgensen , W.L. 2006 . Elucidation of hydrolysis mechanisms for fatty acid amide hydrolase and its Lys142Ala variant via QM/MM simulations . J. Am. Chem. Soc. , 128 : 16904 – 16913 .
   PubMed Web of Science ®Google Scholar
• Genre-Grandpierre , A. , Tellier , C. , Loirat , M. , Blanchard , D. , Hodgson , D.R.W. , Hollfelder , H. and Kirby , A.J. 1997 . Catalysis of the Kemp elimination by antibodies elicited against a cationic hapten . Bioorg. Med. Chem. Lett. , 7 : 2497 – 2502 .
   Web of Science ®Google Scholar
• Kikuchi , K. , Hannak , R.B. , Guo , M.-J. , Kirby , A.J. and Hilvert , D. 2006 . Toward bifunctional antibody catalysis . Bioorg. Med. Chem. , 14 : 6189 – 6196 .
   PubMed Web of Science ®Google Scholar
• Hilvert , D. 1996 . Albumin-catalyzed proton transfer . J. Am. Chem. Soc. , 118 : 8184
   Web of Science ®Google Scholar
• Chica , R.A. , Doucet , N. and Pelletier , J.N. 2005 . Engineering enzyme activity by semi-rational approaches: Combining the benefits of directed evolution and rational design . Curr. Opin. Chem. Biol. , 16 : 378 – 384 .
   Web of Science ®Google Scholar