Folding of class a β-lactamases is rate-limited by peptide bond isomerization and occurs via parallel pathways

Biochemistry

Volumn 49, Issue 19, 2010, Pages 4264-4275

  Vandenameele, Julie ^a   Lejeune, Annabelle ^a   Di Paolo, Alexandre ^a   Brans, Alain ^a   Frère, Jean Marie ^a   Schmid, Franz X ^b   Matagne, André ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; CIS/TRANS ISOMERIZATION; CLASS A; CONFORMATIONAL FOLDING; ENZYMATIC ACTIVITIES; FOLDED PROTEINS; FOLDING KINETICS; FOLDING MECHANISM; KINETIC PHASE; LACTAMASES; MIXING EXPERIMENTS; MONOMERIC PROTEINS; PARALLEL PATHWAYS; PEPTIDE BONDS; REFOLDING; REFOLDING REACTION; SLOW PHASE; SPECTROSCOPIC PROBES; TEM;

ELECTRON TRANSITIONS; ENZYMES; ISOMERIZATION; ISOMERS; SPECTROSCOPIC ANALYSIS;

PEPTIDES;

BETA LACTAMASE; BETA LACTAMASE TEM 1; GLUTAMINE; LEUCINE; PROLINE;

ARTICLE; CHEMICAL BOND; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SUBSTRATE; ISOMERIZATION; KINETICS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; SPECTROSCOPY;

BETA-LACTAMASES; CIRCULAR DICHROISM; KINETICS; LEUCINE; MODELS, MOLECULAR; PROLINE; PROTEIN CONFORMATION; PROTEIN FOLDING; RECOMBINANT PROTEINS; STEREOISOMERISM; THERMODYNAMICS;

EID: 77952373685     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100369d     Document Type: Article

References (44)

1. Creighton, T. E. and Pain, R. H. (1980) Unfolding and refolding of Staphylococcus aureus penicillinase by urea-gradient electrophoresis J. Mol. Biol. 137, 431-436
2. Craig, S., Hollecker, M., Creighton, T. E., and Pain, R. H. (1985) Single amino acid mutations block a late step in the folding of beta-lactamase from Staphylococcus aureus J. Mol. Biol. 185, 681-687
3. Lejeune, A., Vanhove, M., Lamotte-Brasseur, J., Pain, R. H., Frère, J.-M., and Matagne, A. (2001) Quantitative analysis of the stabilization by substrate of Staphylococcus aureus PC1 β-lactamase Chem. Biol. 8, 831-842
4. Lejeune, A., Pain, R. H., Charlier, P., Frère, J.-M., and Matagne, A. (2008) TEM-1 β-lactamase folds in a nonhierarchical manner with transient non-native interactions involving the C-terminal region Biochemistry 47, 1186-1193
5. Mitchinson, C. and Pain, R. H. (1985) Effects of sulphate and urea on the stability and reversible unfolding of β-lactamase from Staphylococcus aureus. Implications for the folding pathway of β-lactamase J. Mol. Biol. 184, 331-342
6. Vanhove, M., Raquet, X., and Frère, J.-M. (1995) Investigation of the folding pathway of the TEM-1 β-lactamase Proteins 22, 110-118
7. Vanhove, M., Raquet, X., Palzkill, T., Pain, R. H., and Frère, J.-M. (1996) The rate-limiting step in the folding of the cis-Pro167Thr mutant of TEM-1 β-lactamase is the trans to cis isomerization of a non-proline peptide bond Proteins 25, 104-111
8. Vanhove, M., Lejeune, A., Guillaume, G., Virden, R., Pain, R. H., Schmid, F. X., and Frère, J.-M. (1998) A collapsed intermediate with nonnative packing of hydrophobic residues in the folding of TEM-1 β-lactamase Biochemistry 37, 1941-1950
9. Wheeler, K. A., Hawkins, A. R., Pain, R., and Virden, R. (1998) The slow step of folding of Staphylococcus aureus PC1 β-lactamase involves the collapse of a surface loop rate limited by the trans to cis isomerization of a non-proline peptide bond Proteins 33, 550-557
10. Herzberg, O. (1991) Refined crystal structure of β-lactamase from Staphylococcus aureus PC1 at 2.0 Å resolution J. Mol. Biol. 217, 701-719
11. Knox, J. R. and Moews, P. C. (1991) Beta-lactamase of Bacillus licheniformis 749/C. Refinement at 2 Å resolution and analysis of hydration J. Mol. Biol. 220, 435-455
12. Lamotte-Brasseur, J., Dive, G., Dideberg, O., Charlier, P., Frère, J.-M., and Ghuysen, J.-M. (1991) Mechanism of acyl transfer by the class A serine β-lactamase of Streptomyces albus G Biochem. J. 279, 213-221
13. Samraoui, B., Sutton, B. J., Todd, R. J., Artymiuk, P. J., Waley, S. G., and Phillips, D. C. (1986) Tertiary structural similarity between a class A β-lactamase and a penicillin-sensitive d -alanyl carboxypeptidase- transpeptidase Nature 320, 378-380
14. Strynadka, N. C., Adachi, H., Jensen, S. E., Johns, K., Sielecki, A., Betzel, C., Sutoh, K., and James, M. N. (1992) Molecular structure of the acyl-enzyme intermediate in β-lactam hydrolysis at 1.7 Å resolution Nature 359, 700-705
15. Swaren, P., Maveyraud, L., Raquet, X., Cabantous, S., Duez, C., Pedelacq, J. D., Mariotte-Boyer, S., Mourey, L., Labia, R., Nicolas-Chanoine, M. H., Nordmann, P., Frère, J.-M., and Samama, J. P. (1998) X-ray analysis of the NMC-A β-lactamase at 1.64 Å resolution, a class A carbapenemase with broad substrate specificity J. Biol. Chem. 273, 26714-26721
16. Tranier, S., Bouthors, A. T., Maveyraud, L., Guillet, V., Sougakoff, W., and Samama, J. P. (2000) The high resolution crystal structure for class A β-lactamase PER-1 reveals the bases for its increase in breadth of activity J. Biol. Chem. 275, 28075-28082
17. Leszczynski, J. F. and Rose, G. D. (1986) Loops in globular proteins: a novel category of secondary structure Science 234, 849-855
18. Herzberg, O. and Moult, J. (1987) Bacterial resistance to β-lactam antibiotics: crystal structure of β-lactamase from Staphylococcus aureus PC1 at 2.5 Å resolution Science 236, 694-701
19. Herzberg, O., Kapadia, G., Blanco, B., Smith, T. S., and Coulson, A. (1991) Structural basis for the inactivation of the P54 mutant of beta-lactamase from Staphylococcus aureus PC1 Biochemistry 30, 9503-9509
20. Gibson, R. M., Christensen, H., and Waley, S. G. (1990) Site-directed mutagenesis of β-lactamase I. Single and double mutants of Glu-166 and Lys-73 Biochem. J. 272, 613-619
21. Leung, Y. C., Robinson, C. V., Aplin, R. T., and Waley, S. G. (1994) Site-directed mutagenesis of β-lactamase I: role of Glu-166 Biochem. J. 299, 671-678
22. Fonzé, E., Vanhove, M., Dive, G., Sauvage, E., Frère, J.-M., and Charlier, P. (2002) Crystal structures of the Bacillus licheniformis BS3 class A β-lactamase and of the acyl-enzyme adduct formed with cefoxitin Biochemistry 41, 1877-1885
23. Dubus, A., Wilkin, J. M., Raquet, X., Normark, S., and Frère, J.-M. (1994) Catalytic mechanism of active-site serine beta-lactamases: role of the conserved hydroxy group of the Lys-Thr(Ser)-Gly triad Biochem. J. 301, 485-494
24. Matagne, A., Joris, B., Van Beeumen, J., and Frère, J.-M. (1991) Ragged N-termini and other variants of class A β-lactamases analysed by chromatofocusing Biochem. J. 273, 503-510
25. Cheggour, A., Fanuel, L., Duez, C., Joris, B., Bouilenne, F., Devreese, B., Van Driessche, G., Van Beeumen, J., Frère, J.-M., and Goffin, C. (2002) The dppA gene of Bacillus subtilis encodes a new d -aminopeptidase Mol. Microbiol. 38, 504-513
26. Nordmann, P., Ronco, E., Naas, T., Duport, C., Michel-Briand, Y., and Labia, R. (1993) Characterization of a novel extended-spectrum β-lactamase from Pseudomonas aeruginosa Antimicrob. Agents Chemother. 37, 962-969
27. Matagne, A., Misselyn-Bauduin, A. M., Joris, B., Erpicum, T., Granier, B., and Frère, J.-M. (1990) The diversity of the catalytic properties of class A β-lactamases Biochem. J. 265, 131-146
28. Dumoulin, M., Conrath, K., Van Meirhaeghe, A., Meersman, F., Heremans, K., Frenken, L. G., Muyldermans, S., Wyns, L., and Matagne, A. (2002) Single-domain antibody fragments with high conformational stability Protein Sci. 11, 500-515 (Pubitemid 34171255)
29. Nozaki, Y. (1972) The preparation of guanidine hydrochloride Methods Enzymol. 26, 43-50
30. Santoro, M. M. and Bolen, D. W. (1988) Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants Biochemistry 27, 8063-8068
31. Pace, C. N. (1990) Measuring and increasing protein stability Trends Biotechnol. 8, 93-98
32. Atkins, P. W. (1994) Physical Chemistry, pp 927-959, Oxford University Press, Oxford.
33. Fersht, A. R. (1998) Structure and Mechanism in Protein Science - A Guide to Enzyme Catalysis and Protein Folding, pp 54 59, W. H. Freeman, New York.
34. Matagne, A., Jamin, M., Chung, E. W., Robinson, C. V., Radford, S. E., and Dobson, C. M. (2000) Thermal unfolding of an intermediate is associated with non-Arrhenius kinetics in the folding of hen lysozyme J. Mol. Biol. 297, 193-210
35. Vandenameele, J. (2009) Caractérisation des proprié tés de folding de la β-lactamase de classe A Bacillus licheniformis BS3, Ph.D. Thesis, University of Liège.
36. Brandts, J. F., Halvorson, H. R., and Brennan, M. (1975) Consideration of the possibility that the slow step in protein denaturation reactions is due to cis-trans isomerism of proline residues Biochemistry 14, 4953-4963
37. Kiefhaber, T., Kohler, H. H., and Schmid, F. X. (1992) Kinetic coupling between protein folding and prolyl isomerization. I. Theoretical models J. Mol. Biol. 224, 217-229
38. Balbach, J. and Schmid, F. X. (2000) Proline isomerization and its catalysis in protein folding, in Mechanisms of Protein Folding (Pain, R. H., Ed.) 2 nd ed., pp 212-249, Oxford University Press, Oxford.
39. Odefey, C., Mayr, L. M., and Schmid, F. X. (1995) Non-prolyl cis-trans peptide bond isomerization as a rate-determining step in protein unfolding and refolding J. Mol. Biol. 245, 69-78
40. Scholz, C., Scherer, G., Mayr, L. M., Schindler, T., Fischer, G., and Schmid, F. X. (1998) Prolyl isomerases do not catalyze isomerization of non-prolyl peptide bonds Biol. Chem. 379, 361-365
41. Robson, B. and Pain, R. H. (1976) The mechanism of folding of globular proteins. Equilibria and kinetics of conformational transitions of penicillinase from Staphylococcus aureus involving a state of intermediate conformation Biochem. J. 155, 331-344
42. Myers, J. K., Pace, C. N., and Scholtz, J. M. (1995) Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding Protein Sci. 4, 2138-2148
43. Ptitsyn, O. B., Pain, R. H., Semisotnov, G. V., Zerovnik, E., and Razgulyaev, O. I. (1990) Evidence for a molten globule state as a general intermediate in protein folding FEBS Lett. 262, 20-24
44. Lejeune, A. (2001) Etude du folding des β-lactamases de classe A, Ph.D. Thesis, University of Liège.