Structural studies on the reaction of isopenicillin N synthase with the truncated substrate analogues δ-(L-α-aminoadipoyl)-L-cysteinyl- glycine and δ-(L-α-aminoadipoyl)-L-cysteinyl-D-alanine

Biochemistry

Volumn 44, Issue 17, 2005, Pages 6619-6628

  Long, Alexandra J ^a,b   Clifton, Ian J ^a   Roach, Peter L ^c   Baldwin, Jack E ^a   Rutledge, Peter J ^d   Schofield, Christopher J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b ASTRAZENECA   (United Kingdom)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^d UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; COMPLEXATION; CRYSTAL STRUCTURE; HYDROGEN BONDS; MOLECULES; PROTEINS; WATER;

IRON ATOMS; ISOPENICILLIN N SYNTHASE (IPNS); TRIPEPTIDES; WATER LIGANDS;

BIOCHEMISTRY;

ISOPENICILLIN N SYNTHETASE;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; HYDROGEN BOND; HYDROPHILICITY; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; STEREOCHEMISTRY; X RAY DIFFRACTION;

ALANINE; ANAEROBIOSIS; BINDING SITES; CATALYSIS; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; EMERICELLA; FERROUS COMPOUNDS; GLYCINE; NITRIC OXIDE; OLIGOPEPTIDES; OXIDOREDUCTASES; PENICILLINS; SUBSTRATE SPECIFICITY;

EID: 17844410319     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi047478q     Document Type: Article

References (46)

1. Baldwin, J. E., and Schofield, C. J. (1992) The biosynthesis of β-lactams, in The Chemistry of β-Lactams (Page, M. I., Ed.) pp 1-78, Blackie, Glasgow, U.K.
2. Baldwin, J. E. (1985) Recent advances in the chemistry of the β-lactam antibiotics, in Special Publication No. 52 (Brown, A. G., and Roberts, S. M., Eds.) pp 62-85, The Royal Society of Chemistry, London.
3. Baldwin, J. E., and Bradley, M. (1990) Isopenicillin N synthase: mechanistic studies, Chem. Rev. 90, 1079-1088.
4. Roach, P. L., Clifton, I. J., Hensgens, C. M. H., Shibata, N., Schofield, C. J., Hadju, J., and Baldwin, J. E. (1997) Structure of isopenicillin N synthase complexed with substrate and the mechanism of penicillin formation, Nature 387, 827-830.
5. Burzlaff, N. I., Rutledge, P. J., Clifton, I. J., Hensgens, C. M. H., Pickford, M., Adlington, R. M., Roach, P. L., and Baldwin, J. E. (1999) The reaction cycle of isopenicillin N synthase observed by X-ray diffraction, Nature 401, 721-724.
6. Baldwin, J. E., Bradley, M., Adlington, R. M., Norris, W. J., and Turner, N. J. (1991) Further evidence for the involvement of a monocyclic β-lactam in the enzymatic conversion of δ-L-α-aminoadipoyl-L-cysteinyl-D- valine into isopenicillin N, Tetrahedron 47, 457-480.
7. Costas, M., Mehn, M. P., Jensen, M. P., and Que, L. (2004) Dioxygen activation at mononuclear nonheme iron active sites: enzymes, models, and intermediates, Chem. Rev. 104, 939-986.
8. Hausinger, R. P. (2004) Fe(II)/alpha-ketoglutarate-dependent hydroxylases and related enzymes, Crit. Rev. Biochem. Mol. Biol. 39, 21-68.
9. Schofield, C. J., and Zhang, Z. H. (1999) Structural and mechanistic studies on 2-oxoglutarate-dependent oxygenases and related enzymes, Curr. Opin. Struct. Biol. 9, 722-731.
10. Lee, H. J., Lloyd, M. D., Clifton, I. J., Harlos, K., Dubus, A., Baldwin, J. E., Frere, J. M., and Schofield, C. J. (2001) Alteration of the co-substrate selectivity of deacetoxycephalosporin G synthase - The role of arginine 258, J. Biol. Chem. 276, 18290-18295.
11. Baldwin, J. E., Abraham, E. P., Lovel, C. G., and Ting, H.-H. (1984) Inhibition of penicillin biosynthesis by δ-(L-α-amino-δ- adipyl)-L-cysteinylglycine. Evidence for initial β-lactam ring formation, J. Chem. Soc., Chem. Commun., 902-903.
12. Graf, P. (1986) Ph.D. Thesis, Eidgenössischen Technischen Hochschule, Zürich.
13. Sami, M., Brown, T. J. N., Roach, P. L., Schofield, C. J., and Baldwin, J. E. (1997) Glutamine-330 is not essential for activity in isopenicillin N synthase from Aspergillus nidulans, FEBS Lett. 405, 191-194.
14. Baldwin, J. E., Blackburn, J. M., Sutherland, J. D., and Wright, M. C. (1991) High-level soluble expression of isopenicillin N synthase isozymes in E. coli, Tetrahedron 47, 5991-6002.
15. Baldwin, J. E., Adlington, R. M., Domayne-Hayman, B. P., Knight, G., and Ting, H.-H. (1987) Use of the cyclopropylcarbinyl test to detect a radical-like intermediate in penicillin biosynthesis, J. Chem. Soc., Chem. Commun., 1661-1663.
16. Baldwin, J. E., Abraham, E. P., Adlington, R. M., Murphy, J. A., Green, N. B., Ting, H.-H., and Usher, J. J. (1983) Penicillin biosynthesis. On the stereochemistry of carbon-sulphur bond formation with modified substrates, J. Chem. Soc., Chem. Commun., 1319-1320.
17. Roach, P. L., Clifton, I. J., Fulop, V., Harlos, K., Barton, G. J., Hajdu, J., Andersson, I., Schofield, C. J., and Baldwin, J. E. (1995) Crystal structure of isopenicillin N synthase is the first from a new structural family of enzymes, Nature 375, 700-704.
18. Baldwin, J. E., Herchen, S. R., Johnson, B. L., Jung, M., Usher, J. J., and Wan, T. (1981) Synthesis of ACV and some carbon-13 and nitrogen-15 labelled isotopomers, J. Chem. Soc., Perkin Trans. 1, 2253-2257.
19. Bodanzky, M., and Bodanzky, A. (1984) The practice of peptide synthesis, in Reactivity and Structure Concepts in Organic Chemistry (Hafner, K., Rees, C. W., Trost, B. M., Lehn, J. M., Schleyer, R. V. R., and Zahruchik, R., Eds.), Springer-Verlag, Berlin, Germany.
20. Sheehan, J. C., Preston, J., and Cruickshank, P. A. (1965) A rapid synthesis of oligopeptide derivatives without isolation of intermediates, J. Am. Chem. Soc. 87, 2492-2493.
21. Wolfe, S., and Jokinen, M. G. (1979) Total synthesis of δ-(L-α-aminoadipoyl)-L-cysteinyl-D-valine (ACV), a biosynthetic precursor of penicillins and cephalosporins, Can. J. Chem. 57, 1388-1396.
22. Roach, P. L., Clifton, I. J., Hensgens, C. M. H., Shibata, N., Long, A. J., Strange, R. W., Hasnain, S. S., Schofield, C. J., Baldwin, J. E., and Hajdu, J. (1996) Anaerobic crystallisation of an isopenicillin N synthase· Fe(II)·substrate complex demonstrated by X-ray studies, Eur. J. Biochem. 242, 736-740.
23. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-326.
24. Leslie, A. G. W. (1999) Integration of maromolecular diffraction data, Acta Crystallogr., Sect. D 55, 1696-1702.
25. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography, Acta Crystallogr., Sect. D 50, 760-763.
26. Brünger, A. T., Kuriyan, J., and Karplus, M. (1987) Crystallographic R-factor refinement by molecular-dynamics, Science 235, 458-460.
27. Sheldrick, G. M., and Schneider, T. R. (1997) SHELXL: high-resolution refinement, Methods Enzymol. 277, 319-343.
28. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjelgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models, Acta Crystallogr., Sect. A 47, 110-119.
29. Kraulis, P. J. (1991) Molscript - A program to produce both detailed and schematic plots of protein structures, J. Appl. Crystallogr. 24, 946-950.
30. Esnouf, R. M. (1999) Further additions to MolScript version 1.4, including reading and contouring of electron-density maps, Acta Crystallogr., Sect. D 55, 938-940.
31. Merritt, E. A., and Bacon, D. J. (1997) Raster3D: photorealistic molecular graphics, Methods Enzymol. 277, 505-524.
32. Hegg, E. L., and Que, L., Jr. (1997) The 2-His-1-carboxylate facial triad - an emerging structural motif in mononuclear non-heme iron-(II) enzymes, Eur. J. Biochem. 250, 625-629.
33. Zhang, Z., Ren, J. S., Stammers, D. K., Baldwin, J. E., Harlos, K., and Schofield, C. J. (1999) Structural origins of the selectivity of the trifunctional oxygenase clavaminic acid synthase, Nat. Struct. Biol. 7, 127-133.
34. Zhou, J., Gunsior, M., Bachmann, B. O., Townsend, C. A., and Solomon, E. I. (1998) Substrate binding to the alpha-ketoglutarate-dependent non-heme iron enzyme clavaminate synthase 2: coupling mechanism of oxidative decarboxylation and hydroxylation, J. Am. Chem. Soc. 120, 13539-13540.
35. Zhou, J., Kelly, W. L., Bachmann, B. O., Gunsior, M., Townsend, C. A., and Solomon, E. I. (2001) Spectroscopic studies of substrate interactions with clavaminate synthase 2, a multifunctional alpha-KG-dependent non-heme iron enzyme: correlation with mechanisms and reactivities, J. Am. Chem. Soc. 123, 7388-7398.
36. Zhang, Z. H., Ren, J. S., Harlos, K., McKinnon, C. H., Clifton, I. J., and Schofield, C. J. (2002) Crystal structure of a clavaminate synthase-Fe(II)-2-oxoglutarate-substrate-NO complex: evidence for metal centred rearrangements, FEBS Lett. 517, 7-12.
37. Price, J. C., Barr, E. W., Tirupati, B., Bollinger, J. M., and Krebs, C. (2003) The first direct characterization of a high-valent iron intermediate in the reaction of an alpha-ketoglutarate-dependent dioxygenase: a high-spin Fe(IV) complex in taurine/alpha-ketoglutarate dioxygenase (TauD) from Escherichia coli, Biochemistry 42, 7497-7508.
38. Riggs-Gelasco, P. J., Price, J. C., Guyer, R. B., Brehm, J. H., Barr, E. W., Bollinger, J. M., and Krebs, C. (2004) EXAFS spectroscopic evidence for an Fe=O unit in the Fe(IV) intermediate observed during oxygen activation by taurine:alpha-ketoglutarate dioxygenase, J. Am. Chem Soc. 126, 8108-8109.
39. Proshlyakov, D. A., Henshaw, T. F., Monterosso, G. R., Ryle, M. J., and Hausinger, R. P. (2004) Direct detection of oxygen intermediates in the non-heme Fe enzyme taurine/alpha-ketoglutarate dioxygenase, J. Am. Chem. Soc. 126, 1022-1023.
40. Abraham, E. P., Adlington, R. M., Baldwin, J. E., Crimmin, M. J., Field, L. D., Jayatilake, G. S., and White, R. L. (1982) Monocyclic β-lactam tripeptide 1-(D-carboxy-2-methylpropyl)-3-L-(δ-L-2-aminoadipamido)-4-L- mercaptoazetidin-2-one, a putative intermediate in penicillin biosynthesis, J. Chem. Soc., Chem. Commun., 1130-1132.
41. Baldwin, J. E., Abraham, E. P., Adlington, R. M., Crimmin, M. J., Field, L. D., Jayatilake, G. S., White, R. L., and Usher, J. J. (1984) The synthesis and reactions of a monocyclic β-lactam tripeptide, 1-[(1R)-carboxy-2- methylpropyl]-(3R)-[(5S)-5-amino-5-carboxypentariamido]-(4R)-mercaptoazetidin-2- one, a putative intermediate in penicillin biosynthesis, Tetrahedron 40, 1907-1918.
42. Grummitt, A. R., Rutledge, P. J., Clifton, I. J., and Baldwin, J. E. (2004) Active-sile-mediated elimination of hydrogen fluoride from a fluorinated substrate analogue by isopenicillin N synthase, Biochem. J. 382, 659-666.
43. Baldwin, J. E., Adlington, R. M., Basak, A., Flitsch, S. L., Petursson, S., Turner, N. J., and Ting, H.-H. (1986) Enzymatic synthesis of a new type of penicillin, J. Chem. Soc., Chem. Commun., 975-976.
44. 1H NMR observation of the cell-free conversion of δ-(L-α-aminoadipyl)- L-cysteinyl-D-valine and δ-(L-α-aminoadipyl)-L-cysteinyl-D-(-)- isoleucine into penicillins, J. Chem. Soc., Chem. Commun., 917-919.
45. Bahadur, G. A., Baldwin, J. E., Usher, J. J., Abraham, E. P., Jayatilake, G. S., and White, R. L. (1981) Cell-free biosynthesis of penicillins. Conversion of peptides into new β-lactam antibiotics, J. Am. Chem. Soc. 103, 7650-7651.
46. Baldwin, J. E., Adlington, R. M., Turner, N. J., Domayne-Hayman, B. P., Ting, H.-H., Derome, A. E., and Murphy, J. A. (1984) Penicillin biosynthesis: enzymatic synthesis of new cephams, J. Chem. Soc., Chem. Commun., 1167-1170.