Structural basis for antibody catalysis of a cationic cyclization reaction

Journal of Molecular Biology

Volumn 329, Issue 1, 2003, Pages 69-83

  Zhu, Xueyong ^a   Heine, Andreas ^a,c   Monnat, Frédéric ^b   Houk, K N ^b   Janda, Kim D ^a   Wilson, Ian A ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Catalytic antibody; Cation interaction; Cationic cyclization reaction; Crystal structure; Molecular modeling

Indexed keywords

AROMATIC COMPOUND; BENZOIC ACID; CATALYTIC ANTIBODY; CYCLOHEXANOL DERIVATIVE; CYCLOHEXENE DERIVATIVE; ESTER DERIVATIVE; HAPTEN; IMMUNOGLOBULIN F(AB) FRAGMENT; LIGAND; SOLVENT; TRYPTOPHAN; WATER;

ANTIBODY STRUCTURE; ANTIGEN BINDING; ARTICLE; CALCULATION; CATALYSIS; CHEMICAL INTERACTION; CHEMICAL REACTION; COMPARATIVE STUDY; CRYSTAL STRUCTURE; CYCLIZATION; HAPTEN CARRIER COMPLEX; MOLECULAR MODEL; MOLECULE; PRIORITY JOURNAL;

EID: 0038369888     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00406-6     Document Type: Article

References (61)

1. Johnson W.S. Nonenzymic biogenetic-like olefinic cyclizations. Acc. Chem. Res. 1:1968;1-8.
2. Abe I., Rohmer M., Prestwich G.D. Enzymatic cyclization of squalene and oxidosqualene to sterols and triterpenes. Chem. Rev. 93:1993;2189-2206.
3. Johnson W.S., Chenera B., Tham F.S., Kullnig R.K. The fluorine atom as a cation stabilizing auxiliary in biomimetic polyene cyclizations.1. Background and exploratory experiments. J. Am. Chem. Soc. 115:1993;493-497.
4. Sutherland J.K. Trost B.M., Fleming I. Comprehensive Organic Synthesis. vol. 3:1991;Pergamon Press, Oxford.
5. Olah G.A., Schleyer R. Carbonium Ions. 1992;Wiley Interscience, New York.
6. Li T., Janda K.D., Ashley J.A., Lerner R.A. Antibody catalyzed cationic cyclization. Science. 264:1994;1289-1293.
7. Sutherland J.K. The initiation of cyclization using 3-methylcyclohex-2-enone derivatives. Chem. Soc. Rev. 9:1980;265-280.
8. Wendt K.U., Schulz G.E. Isoprenoid biosynthesis: manifold chemistry catalyzed by similar enzymes. Structure. 6:1998;127-133.
9. Lesburg C.A., Caruthers J.M., Paschall C.M., Christianson D.W. Managing and manipulating carbocations in biology: terpenoid cyclase structure and mechanism. Curr. Opin. Struct. Biol. 8:1998;695-703.
10. Starks C.M., Back K.W., Chappell J., Noel J.P. Structural basis for cyclic terpene biosynthesis by tobacco 5-epi-aristolochene synthase. Science. 277:1997;1815-1820.
11. Lesburg C.A., Zhai G.Z., Cane D.E., Christianson D.W. Crystal structure of pentalenene synthase: mechanistic insights on terpenoid cyclization reactions in biology. Science. 277:1997;1820-1824.
12. Caruthers J.M., Kang I., Rynkiewicz M.J., Cane D.E., Christianson D.W. Crystal structure determination of aristolochene synthase from the blue cheese mold, Penicillium roqueforti. J. Biol. Chem. 275:2000;25533-25539.
13. Rynkiewicz M.J., Cane D.E., Christianson D.W. Structure of trichodiene synthase from Fusarium sporotrichioides provides mechanistic inferences on the terpene cyclization cascade. Proc. Natl Acad. Sci. USA. 98:2001;13543-13548.
14. Wendt K.U., Poralla K., Schulz G.E. Structure and function of a squalene cyclase. Science. 277:1997;1811-1815.
15. Whittington D.A., Wise M.L., Urbansky M., Coates R.M., Croteau R.B., Christianson D.W. Bornyl diphosphate synthase: structure and strategy for carbocation manipulation by a terpenoid cyclase. Proc. Natl Acad. Sci. USA. 99:2002;15375-15380.
16. Li T., Lerner R.A., Janda K.D. Antibody catalyzed cationic reactions: rerouting of chemical transformations via antibody catalysis. Acc. Chem. Res. 30:1997;115-121.
17. Wentworth P. Jr, Jones L.H., Wentworth A.D., Zhu X., Larsen N.A., Wilson I.A., et al. Antibody catalysis of the oxidation of water. Science. 293:2001;1806-1811.
18. Al-Lazikani B., Lesk A.M., Chothia C. Standard conformations for the canonical structures of immunoglobulins. J. Mol. Biol. 273:1997;927-948.
19. Kabat E.A., Wu T.T., Perry H.M., Gottesman K.S., Foeller C. Sequences of Proteins of Immunological Interest. 5th edit. 1991;National Institutes of Health, Bethesda.
20. Morea V., Tramontano A., Rustici M., Chothia C., Lesk A.M. Conformations of the third hypervariable region in the VH domain of immunoglobulins. J. Mol. Biol. 275:1998;269-294.
21. Wilson I.A., Stanfield R.L. Antibody antigen interactions - new structures and new conformational changes. Curr. Opin. Struct. Biol. 4:1994;857-867.
22. Arevalo J.H., Stura E.A., Taussig M.J., Wilson I.A. 3-Dimensional structure of an anti-steroid Fab′ and progesterone Fab′ complex. J. Mol. Biol. 231:1993;103-118.
23. Wentworth P. Jr, Wentworth A.D., Zhu X., Wilson I.A., Janda K.D., Eschenmoser A., Lerner R.A. Evidence for the production of trioxygen species during antibody-catalyzed chemical modification of antigens. Proc. Natl Acad. Sci. USA. 100:2003;1490-1493.
24. Larsen N.A., Turner J.M., Stevens J., Rosser S.J., Basran A., Lerner R.A., et al. Crystal structure of a bacterial cocaine esterase. Nature Struct. Biol. 9:2002;17-21.
25. Almrud J.J., Kern A.D., Wang S.C., Czerwinski R.M., Johnson W.H., Murzin A.G., et al. The crystal structure of YdcE, a 4-oxalocrotonate tautomerase homologue from Escherichia coli, confirms the structural basis for oligomer diversity. Biochemistry. 41:2002;12010-12024.
26. Steegborn C., Danot O., Huber R., Clausen T. Crystal structure of transcription factor MaIT domain III: a novel helix repeat fold implicated in regulated oligomerization. Structure. 9:2001;1051-1060.
27. Declercq J.P., Evrard C., Clippe A., Vander Stricht D., Bernard A., Knoops B. Crystal structure of human peroxiredoxin 5, a novel type of mammalian peroxiredoxin at 1.5 angstrom resolution. J. Mol. Biol. 311:2001;751-759.
28. Goodsell D.S., Olson A.J. Automated docking of substrates to proteins by simulated annealing. Proteins: Struct. Funct. Genet. 8:1990;195-202.
29. Morris G.M., Goodsell D.S., Huey R., Olson A.J. Distributed automated docking of flexible ligands to proteins: parallel applications of AutoDock 2.4. J. Comp.-Aided Mol. Des. 10:1996;293-304.
30. Morris G.M., Goodsell D.S., Halliday R.S., Huey R., Hart W.E., Belew R.K., Olson A.J. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J. Comput. Chem. 19:1998;1639-1662.
31. Connolly M.L. Analytical molecular-surface calculation. J. Appl. Crystallog. 16:1983;548-558.
32. Sheriff S., Hendrickson W.A., Smith J.L. Structure of myohemerythrin in the azidomet state at 1.7/1.3 Å resolution. J. Mol. Biol. 197:1987;273-296.
33. Johnson G., Wu T.T. Kabat database and its applications: future directions. Nucl. Acids Res. 29:2001;205-206.
34. Becke A.D. Density-functional thermochemistry. II. The effect of the Perdew-Wang generalized-gradient correlation correction. J. Chem. Phys. 97:1992;9173-9177.
35. Lee C., Yang W., Parr R.G. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys. Rev. B: Condens. Matter. 37:1988;785-789.
36. Janda K.D., Weinhouse M.I., Schloeder D.M., Lerner R.A., Benkovic S.J. Bait and switch strategy for obtaining catalytic antibodies with acyl-transfer capabilities. J. Am. Chem. Soc. 112:1990;1274-1275.
37. Dougherty D.A. Cation-π interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp. Science. 271:1996;163-168.
38. Schreiner P.R., Schleyer P.R., Schaefer H.F. III. Why the classical and nonclassical norbornyl cations do not resemble the 2-endo- and 2-exo-norbornyl solvolysis transition states. J. Org. Chem. 62:1997;4216-4228.
39. Uggerud E., Bache-Andreassen L. Theoretical models and experimental data for reactions between water and protonated alcohols: substitution and elimination mechanisms. Chem. Eur. J. 5:1999;1917-1930.
40. Lambert J.B., Emblidge R.W., Malany S. The question of vertical or nonvertical participation of silicon β to a cation in the antiperiplanar stereochemistry. J. Am. Chem. Soc. 115:1993;1317-1320.
41. Rauk A., Sorensen T.S., Maerker C., de Carneiro J.W., Sieber S., Schleyer P.V.R. Axial and equatorial 1-methyl-1-cyclohexyl cation isomers both have chair conformations but differ in C-C and C-H hyperconjugation modes. J. Am. Chem. Soc. 118:1996;3761-3762.
42. Gabelica V., Kresge A.J. Protonation of trimethylsilyl-substituted carbon-carbon multiple bonds in aliphatic systems. Conformational dependence of the β-silyl stabilization of carbocations. J. Am. Chem. Soc. 118:1996;3838-3841.
43. Akiya N., Savage P.E. Kinetics and mechanism of cyclohexanol dehydration in high-temperature water. Ind. Eng. Chem. Res. 40:2001;1822-1831.
44. Hasserodt J., Janda K.D., Lerner R.A. Antibody catalyzed terpenoid cyclization. J. Am. Chem. Soc. 118:1996;11654-11655.
45. Li T., Janda K.D., Lerner R.A. Cationic cyclopropanation by antibody catalysis. Nature. 379:1996;326-327.
46. Hasserodt J., Janda K.D., Lerner R.A. Formation of bridge-methylated decalins by antibody-catalyzed tandem cationic cyclization. J. Am. Chem. Soc. 119:1997;5993-5998.
47. Hasserodt J., Janda K.D., Lerner R.A. Antibodies mimic natural oxidosqualene-cyclase action in steroid ring A formation. J. Am. Chem. Soc. 122:2000;40-45.
48. Paschall C.M., Hasserodt J., Jones T., Lerner R.A., Janda K.D., Christianson D.W. Convergence of catalytic antibody and terpene cyclase mechanisms: polyene cyclization directed by carbocation-π interactions. Angew. Chem. Int. Ed. 38:1999;1743-1747.
49. Harlow K.U., Lane D. Antibodies: A Laboratory Manual. 1988;Cold Spring Harbor Press, Cold Spring Harbor, NY.
50. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
51. Fitzgerald P.M.D. Merlot, an integrated package of computer programs for the determination of crystal structures by molecular replacement. J. Appl. Crystallog. 21:1988;273-278.
52. Navaza J. Amore-an automated package for molecular replacement. Acta Crystallog. A50:1994;157-163.
53. Pokkuluri P.R., Bouthillier F., Li Y.G., Kuderova A., Lee J., Cygler M. Preparation, characterization and crystallization of an antibody Fab fragment that recognizes RNA - crystal structures of native Fab and 3 Fab-mononucleotide complexes. J. Mol. Biol. 243:1994;283-297.
54. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D. 54:1998;905-921.
55. Sheldrick G.M., Schneider T.R. SHELXL: high resolution refinement. Methods Enzymol. 277:1997;319-343.
56. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R. et al. (1998). Gaussian 98, Revision A.9, Gaussian, Inc., Pittsburgh PA.
57. Besler B.H., Merz K.M. Jr, Kollman P.A. Atomic charges derived from semiempirical methods. J. Comput. Chem. 11:1990;431-439.
58. Singh U.C., Kollman P.A. An approach to computing electrostatic charges for molecules. J. Comput. Chem. 5:1984;129-145.
59. Nicholls A., Sharp K.A., Honig B. Protein folding and association - insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11:1991;281-296.
60. Esnouf R.M. Further additions to MolScript version 1.4, including reading and contouring of electron-density maps. Acta Crystallog. sect. D. 55:1999;938-940.
61. Merritt E.A., Murphy M.E.P. Raster3d Version 2.0 - a program for photorealistic molecular graphics. Acta Crystallog. sect. D. 50:1994;869-873.