The Nedd4−1 WW Domain Recognizes the PY Motif Peptide through Coupled Folding and Binding Equilibria

July 24, 2017

Title

The Nedd4−1 WW Domain Recognizes the PY Motif Peptide through Coupled Folding and Binding Equilibria

Author

Vineet Panwalkar, Philipp Neudecker, Michael Schmitz, Justin Lecher, Marianne Schulte, Karima Medini, Matthias Stoldt, Margaret A. Brimble, Dieter Willbold, Andrew J. Dingley

Year

2015

Journal

Biochemistry

Abstract

The four WW domains of human Nedd4–1 (neuronal precursor cell expressed developmentally downregulated gene 4–1) interact with the PPxY (PY) motifs of the human epithelial Na+ channel (hENaC) subunits, with the third WW domain (WW3*) showing the highest affinity. We have shown previously that the α-hENaC PY motif binding interface of WW3* undergoes conformational exchange on the millisecond time scale, indicating that conformational sampling plays a role in peptide recognition. To further understand this role, the structure and dynamics of hNedd4–1 WW3* were investigated. The nuclear Overhauser effect-derived structure of apo-WW3* resembles the domain in complex with the α-hENaC peptide, although particular side chain conformations change upon peptide binding, which was further investigated by molecular dynamics simulations. Model-free analysis of the 15N nuclear magnetic resonance spin relaxation data showed that the apo and peptide-bound states of WW3* have similar backbone picosecond to nanosecond time scale dynamics. However, apo-WW3* exhibits pronounced chemical exchange on the millisecond time scale that is quenched upon peptide binding. 1HNand 15N Carr–Purcell–Meiboom–Gill (CPMG) relaxation dispersion experiments at various temperatures revealed that apo-WW3* exists in an equilibrium between the natively folded peptide binding-competent state and a random coil-like denatured state. The thermodynamics of the folding equilibrium was determined by fitting a thermal denaturation profile monitored by circular dichroism spectroscopy in combination with the CPMG data, leading to the conclusion that the unfolded state is populated to ∼20% at 37 °C. These results show that the binding of the hNedd4–1 WW3* domain to α-hENaC is coupled to the folding equilibrium.

Instrument

J-1100

Keywords

Circular dichroism, Protein folding, Ligand binding, Thermodynamics, Secondary structure, Protein denaturation, Biochemistry