The Right-Handed Parallel β-Helix Topology of Erwinia chrysanthemi Pectin Methylesterase Is Intimately Associated with Both Sequential Folding and Resistance to High Pressure.
circular dichroism; contact order; dry molten globule; high pressure; kinetic intermediate; parallel β-helix; protein folding; repeat proteins; sequential pathway; Carboxylic Ester Hydrolases; pectinesterase; Amino Acid Motifs; Carboxylic Ester Hydrolases/chemistry; Circular Dichroism; Dickeya chrysanthemi/metabolism; Hydrogen-Ion Concentration; Kinetics; Linear Models; Models, Molecular; Pressure; Protein Binding; Protein Conformation; Protein Denaturation; Protein Folding; Protein Structure, Secondary; Spectrophotometry, Ultraviolet; Temperature; Thermodynamics; Dickeya chrysanthemi; Biochemistry; Molecular Biology
Abstract :
[en] The complex topologies of large multi-domain globular proteins make the study of their folding and assembly particularly demanding. It is often characterized by complex kinetics and undesired side reactions, such as aggregation. The structural simplicity of tandem-repeat proteins, which are characterized by the repetition of a basic structural motif and are stabilized exclusively by sequentially localized contacts, has provided opportunities for dissecting their folding landscapes. In this study, we focus on the Erwinia chrysanthemi pectin methylesterase (342 residues), an all-β pectinolytic enzyme with a right-handed parallel β-helix structure. Chemicals and pressure were chosen as denaturants and a variety of optical techniques were used in conjunction with stopped-flow equipment to investigate the folding mechanism of the enzyme at 25 °C. Under equilibrium conditions, both chemical- and pressure-induced unfolding show two-state transitions, with average conformational stability (ΔG° = 35 ± 5 kJ·mol-1) but exceptionally high resistance to pressure (Pm = 800 ± 7 MPa). Stopped-flow kinetic experiments revealed a very rapid (τ < 1 ms) hydrophobic collapse accompanied by the formation of an extended secondary structure but did not reveal stable tertiary contacts. This is followed by three distinct cooperative phases and the significant population of two intermediate species. The kinetics followed by intrinsic fluorescence shows a lag phase, strongly indicating that these intermediates are productive species on a sequential folding pathway, for which we propose a plausible model. These combined data demonstrate that even a large repeat protein can fold in a highly cooperative manner.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Guillerm, Jessica ; Université de Liège - ULiège > Centres généraux > Centre d'ingénierie des protéines
Frère, Jean-Marie ; Université de Liège - ULiège > Département des sciences de la vie > Centre d'Ingénierie des Protéines (CIP)
Meersman, Filip; Department of Chemistry, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerp, Belgium
Matagne, André ; Université de Liège - ULiège > Département des sciences de la vie > Enzymologie et repliement des protéines
Language :
English
Title :
The Right-Handed Parallel β-Helix Topology of Erwinia chrysanthemi Pectin Methylesterase Is Intimately Associated with Both Sequential Folding and Resistance to High Pressure.
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE] BELSPO - Politique scientifique fédérale [BE]
Funding text :
This work was supported in part by grants from the Fonds de la Recherche Fondamentale et Collective (contract numbers 2.4550.05, 2.4524.03 and 2.4511.06) and by the Belgian program of Interuniversity Attraction Poles initiated by the Federal Office for Scientific Technical and Cultural Affairs (PAI n◦ P5/33 and P6/19). J.G. was recipient of a F.R.I.A. fellowship.
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