Thermal stability of the hydrogen-bonded water network in the hydration shell of islet amyloid polypeptide

Abstract

The effect of temperature on the connectivity of hydrogen bonds in the hydration shells of the islet amyloid polypeptides (IAPPs) is studied by means of computer simulations. The hydrogen-bonded network of hydration water homogeneously envelopes a peptide at low temperature and breaks into an ensemble of small clusters upon heating. This thermal break occurs via a percolation transition, which is not found to be sensitive to the chemical modifications of IAPP (IAPP with and without a disulfide bridge, human and rat IAPP). The radius of gyration of IAPP starts to increase when the hydration water network breaks upon heating. The fluctuations of the number of intra-peptide hydrogen bonds show negative correlation with the fraction of molecules in the largest cluster of hydration water. The thermal stability of the network of hydration water is enhanced upon increasing number of intra-peptide hydrogen bonds, which makes the peptide surface more hydrophobic. The thermal stabilities of the hydrogen-bonded water networks in the hydration shells of IAPPs and of several other biomolecules are found to be rather similar: the network breaks between 300 and 330 K, i.e., in the temperature interval where the biological activity of living organisms is maximal.

Water Molecular System Dynamics Associated with Amyloidogenic Nucleation as Revealed by Real Time Near Infrared Spectroscopy and Aquaphotomics

“…The role of water molecules in amyloid formation has been explored mainly by means of computer simulation [38] and experimental strategy for direct observation of water structures has been restricted to several techniques such as magnetic resonance spectroscopy [39], [40] and calorimetric analysis [20], [41] because of fundamental difficulty in detecting dynamics of water molecules. This time, we have applied near infrared spectroscopy and aquaphotomics method to examine non-invasively time-resolved behavior of the whole process of fibrillation of insulin.…”

Effects of Lid 1 Mutagenesis on Lid Displacement, Catalytic Performances and Thermostability of Cold-active Pseudomonas AMS8 Lipase in Toluene

“…The key indicators to describe temperature-dependence in this cold-active lipases are through protein compactness and surface area solvent accessibility (SASA). H-bond networks are crucial for protein compactness and when these interactions broke at high temperature (causing structure flexibility), both R g and SASA started to increase [ 35 ]. In Fig.…”

Hydrogen-bonded network of hydration water around model solutes

“…The state with the largest water cluster containing most of the hydration water (right peak of the distribution P(S max /N 1 )) should be considered as more ordered. The center of mass of such a large cluster is close to the solute center 19 indicating homogeneous coverage of a solute surface by the spanning H-bonded network of hydration water. Such a spanning network is absent in the state corresponding to the left peak of the distribution P(S max /N 1 ), where only small H-bonded clusters of hydration water exist and this state should be considered as more disordered.…”

“…A similar thermal breakage of the spanning network of hydration water has been observed in the hydration shells of various biomolecules and of the model cylindrical pores and it can be well described as a quasi-2D percolation transition, which is rounded due to the finite size of the hydration shell. 17,19,21 The mean cluster size S mean in finite systems shows a maximum close to the percolation threshold. Indeed, a clear maximum of S mean is seen in the temperature dependence shown in Fig.…”

“…16 Two qualitatively different clustering states of hydration water have been found in the simulation studies of various polypeptides in liquid water. At low temperatures, polypeptide is covered homogeneously by the spanning H-bonded network of hydration water, [17][18][19][20][21] which can be considered as a liquid clathrate-like shell. Upon heating, this spanning network breaks via a percolation transition, which is smeared out in some temperature range due to the finite size of polypeptides.…”