Reactibodies generated by kinetic selection couple chemical reactivity with favorable protein dynamics

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 38, 2011, Pages 15954-15959

  Smirnov, Ivan ^a,b   Carletti, Eugeńie ^c   Kurkova, Inna ^a   Nachon, Florian ^d   Nicolet, Yvain ^c   Mitkevich, Vladimir A ^e   Deb́at, Heĺeǹe ^f,g   Avalle, Beŕanger̀e ^h   Belogurov Jr , Alexey A ^a,i   Kuznetsov, Nikita ^j   Reshetnyak, Andrey ^k   Masson, Patrick ^d   Tonevitsky, Alexander G ^l   Ponomarenko, Natalia ^a   Makarov, Alexander A ^e   Friboulet, Alain ^h   Tramontano, Alfonso ^m   Gabibov, Alexander ^a,b,i  

^a SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^d INSTITUT DE RECHERCHE BIOMÉDICALE DES ARMÉES   (France)

^e ENGELHARDT INSTITUTE OF MOLECULAR BIOLOGY   (Russian Federation)

^f LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

^g CNRS   (France)

^h UNIVERSITÉ DE TECHNOLOGIE DE COMPIÈGNE   (France)

ⁱ INSTITUTE OF GENE BIOLOGY   (Russian Federation)

^j INSTITUTE OF CHEMICAL BIOLOGY AND FUNDAMENTAL MEDICINE   (Russian Federation)

^k YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^l INSTITUTE OF GENERAL PATHOLOGY AND PATHOPHYSIOLOGY   (Russian Federation)

^m UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

Catalytic antibodies; Crystal structure; Insecticide; Organophosphate hydrolysis

Indexed keywords

ANTIBODY; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN LIGHT CHAIN; PARAOXON; PHOSPHONIC ACID DERIVATIVE; PROTEIN; REACTIBODY; TYROSINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTIBODY COMBINING SITE; ANTIBODY ISOLATION; ANTIBODY LIBRARY; ANTIBODY STRUCTURE; ANTIGEN BINDING; ARTICLE; BIOCATALYST; CATALYSIS; COVALENT BOND; CRYSTAL STRUCTURE; DEPHOSPHORYLATION; ENZYME ACTIVE SITE; ENZYME KINETICS; ENZYME MECHANISM; HYDROGEN BOND; HYDROLYSIS; MOLECULAR DOCKING; NUCLEOPHILICITY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; STEADY STATE; STEREOCHEMISTRY;

ALGORITHMS; AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES; BINDING SITES; CALORIMETRY; CHO CELLS; COMPLEMENTARITY DETERMINING REGIONS; CRICETINAE; CRICETULUS; CRYSTALLOGRAPHY, X-RAY; HUMANS; IMMUNOGLOBULIN LIGHT CHAINS; IMMUNOGLOBULIN VARIABLE REGION; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEINS; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; THERMODYNAMICS;

EID: 80053135167     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1108460108     Document Type: Article

References (41)

1. Benkovic SJ, Hammes-Schiffer S (2003) A perspective on enzyme catalysis. Science 301: 1196-1202. (Pubitemid 37052200)
2. Tawfik DS (2010) Messy biology and the origins of evolutionary innovations. Nat Chem Biol 6:692-696.
3. Gupta RD, et al. (2011) Directed evolution of hydrolases for prevention of G-type nerve agent intoxication. Nat Chem Biol 7:120-125.
4. Belogurov A, Jr., Kozyr A, Ponomarenko N, Gabibov A (2009) Catalytic antibodies: Balancing between Dr. Jekyll and Mr. Hyde. Bioessays 31:1161-1171.
5. Lerner RA, Benkovic SJ, Schultz PG (1991) At the crossroads of chemistry and immunology: Catalytic antibodies. Science 252:659-667. (Pubitemid 21916986)
6. Savinov SN, Hirschmann R, Benkovic SJ, Smith AB, 3rd (2003) Investigation of an antibody- ligase. Evidence for strain-induced catalysis. Bioorg Med Chem Lett 13: 1321-1324. (Pubitemid 36351343)
7. Stewart JD, Roberts VA, Thomas NR, Getzoff ED, Benkovic SJ (1994) Site-directed mutagenesis of a catalytic antibody: An arginine and a histidine residue play key roles. Biochemistry 33:1994-2003. (Pubitemid 24099593)
8. Wagner J, Lerner RA, Barbas CF, 3rd (1995) Efficient aldolase catalytic antibodies that use the enamine mechanism of natural enzymes. Science 270:1797-1800. (Pubitemid 26007222)
9. Zhu X, et al. (2004) The origin of enantioselectivity in aldolase antibodies: Crystal structure, site-directed mutagenesis, and computational analysis. J Mol Biol 343:1269-1280. (Pubitemid 39387826)
10. Barbas CF, 3rd, et al. (1997) Immune versus natural selection: Antibody aldolases with enzymic rates but broader scope. Science 278:2085-2092.
11. Demuth HU, et al. (1988) Molecular interactions in intermediate and transition states in the self-stimulated inhibition of enzymes. Pharmazie 43:262-264.
12. Soumillion P, Fastrez J (2001) Novel concepts for selection of catalytic activity. Curr Opin Biotechnol 12:387-394. (Pubitemid 32718793)
13. Cesaro-Tadic S, et al. (2003) Turnover-based in vitro selection and evolution of biocatalysts from a fully synthetic antibody library. Nat Biotechnol 21:679-685. (Pubitemid 36638096)
14. Reshetnyak AV, et al. (2007) Routes to covalent catalysis by reactive selection for nascent protein nucleophiles. J Am Chem Soc 129:16175-16182.
15. Kuzmic P (1996) Program DYNAFIT for the analysis of enzyme kinetic data: Application to HIV proteinase. Anal Biochem 237:260-273.
16. Oleksyszyn J, Boduszek B, Kam CM, Powers JC (1994) Novel amidine-containing peptidyl phosphonates as irreversible inhibitors for blood coagulation and related serine proteases. J Med Chem 37:226-231. (Pubitemid 24063040)
17. Kim YR, et al. (2006) Heavy and light chain variable single domains of an anti-DNA binding antibody hydrolyze both double- and single-stranded DNAs without sequence specificity. J Biol Chem 281:15287-15295.
18. Schuermann JP, Prewitt SP, Davies C, Deutscher SL, Tanner JJ (2005) Evidence for structural plasticity of heavy chain complementarity-determining region 3 in antibody- ssDNA recognition. J Mol Biol 347:965-978. (Pubitemid 40392477)
19. Patten PA, et al. (1996) The immunological evolution of catalysis. Science 271: 1086-1091. (Pubitemid 26075223)
20. Scotti C, Gherardi E (2006) Structural basis of affinity maturation of the TEPC15/ Vkappa45.1 anti-2-phenyl-5-oxazolone antibodies. J Mol Biol 359:1161-1169. (Pubitemid 43903496)
21. Zhu X, Tanaka F, Lerner RA, Barbas CF, 3rd, Wilson IA (2009) Direct observation of an enamine intermediate in amine catalysis. J Am Chem Soc 131:18206-18207.
22. Carletti E, et al. (2009) Structure-activity analysis of aging and reactivation of human butyrylcholinesterase inhibited by analogues of tabun. Biochem J 421:97-106.
23. Sanson B, et al. (2009) Crystallographic snapshots of nonaged and aged conjugates of soman with acetylcholinesterase, and of a ternary complex of the aged conjugate with pralidoxime. J Med Chem 52:7593-7603.
24. Dvir H, Silman I, Harel M, Rosenberry TL, Sussman JL (2010) Acetylcholinesterase: From 3D structure to function. Chem Biol Interact 187:10-22.
25. Foote J, Milstein C (1994) Conformational isomerism and the diversity of antibodies. Proc Natl Acad Sci USA 91:10370-10374. (Pubitemid 24328998)
26. Lindner AB, Eshhar Z, Tawfik DS (1999) Conformational changes affect binding and catalysis by ester-hydrolysing antibodies. J Mol Biol 285:421-430. (Pubitemid 29034054)
27. James LC, Roversi P, Tawfik DS (2003) Antibody multispecificity mediated by conformational diversity. Science 299:1362-1367. (Pubitemid 36254643)
28. Wade H, Scanlan TS (2003) Binding and catalysis: A thermodynamic study on a catalytic antibody system. ChemBioChem 4:537-540. (Pubitemid 36749626)
29. Debord J, Harel M, Verneuil B, Bollinger JC, Dantoine T (2009) Microcalorimetric study of the inhibition of butyrylcholinesterase by paraoxon. Anal Biochem 389:97-101.
30. Connelly PR, Thomson JA (1992) Heat capacity changes and hydrophobic interactions in the binding of FK506 and rapamycin to the FK506 binding protein. Proc Natl Acad Sci USA 89:4781-4785.
31. Jelesarov I, Bosshard HR (1999) Isothermal titration calorimetry and differential scanning calorimetry as complementary tools to investigate the energetics of biomolecular recognition. J Mol Recognit 12:3-18. (Pubitemid 29160432)
32. Hammes GG, Chang YC, Oas TG (2009) Conformational selection or induced fit: A flux description of reaction mechanism. Proc Natl Acad Sci USA 106:13737-13741.
33. Becker EL (1967) The relationship of the structure of phosphonate esters to their ability to inhibit chymotrypsin, trypsin, acetylcholinesterase and C'Ia. Biochim Biophys Acta 147:289-296.
34. Tramontano A, Ivanov B, Gololobov G, Paul S (2000) Inhibition and labeling of enzymes and abzymes by phosphonate diesters. Appl Biochem Biotechnol 83: 233-242.
35. Jackson DS, et al. (1998) Synthesis and evaluation of diphenyl phosphonate esters as inhibitors of the trypsin-like granzymes A and K and mast cell tryptase. J Med Chem 41:2289-2301. (Pubitemid 28285731)
36. Boduszek B, et al. (1994) Dipeptide phosphonates as inhibitors of dipeptidyl peptidase IV. J Med Chem 37:3969-3976. (Pubitemid 24379686)
37. Griffiths AD, et al. (1994) Isolation of high affinity human antibodies directly from large synthetic repertoires. EMBO J 13:3245-3260. (Pubitemid 24226939)
38. Yin J, Beuscher AE, 4th, Andryski SE, Stevens RC, Schultz PG (2003) Structural plasticity and the evolution of antibody affinity and specificity. J Mol Biol 330:651-656.
39. Wedemayer GJ, Patten PA, Wang LH, Schultz PG, Stevens RC (1997) Structural insights into the evolution of an antibody combining site. Science 276:1665-1669. (Pubitemid 27421966)
40. Henzler-Wildman KA, et al. (2007) Intrinsic motions along an enzymatic reaction trajectory. Nature 450:838-844. (Pubitemid 350231334)
41. Jackson CJ, et al. (2009) Conformational sampling, catalysis, and evolution of the bacterial phosphotriesterase. Proc Natl Acad Sci USA 106:21631-21636.