Aqueous peptides as experimental models for hydration water dynamics near protein surfaces

Malardier-Jugroot, Cécile; Johnson, Margaret E.; Murarka, Rajesh K.; Head‐Gordon, Teresa

doi:10.1039/b806995f

Cited by 39 publications

(61 citation statements)

References 55 publications

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“…Earlier studies of hydrogen bond lifetimes between water molecules and the protein HP-36 have revealed a significantly heterogeneous distribution of hydrogen bond lifetimes, exhibited around different helices of the protein (33,34). Experimental proof for this fact has been provided before by quasielastic neutron scattering, which showed a heterogeneous dynamic signature for amphiphilic peptides (35). For proteins, the work by Zhang et al (36) was able to map the heterogeneous distribution of the coupled solvation-protein fluctuations at tryptophan probes using coherent femtosecond laser preparation.…”

Section: Resultsmentioning

confidence: 81%

Long-range protein–water dynamics in hyperactive insect antifreeze proteins

Meister

Ebbinghaus

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

234

221

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Antifreeze proteins (AFPs) are specific proteins that are able to lower the freezing point of aqueous solutions relative to the melting point. Hyperactive AFPs, identified in insects, have an especially high ability to depress the freezing point by far exceeding the abilities of other AFPs. In previous studies, we postulated that the activity of AFPs can be attributed to two distinct molecular mechanisms: (i) short-range direct interaction of the protein surface with the growing ice face and (ii) long-range interaction by protein-induced water dynamics extending up to 20 Å from the protein surface. In the present paper, we combine terahertz spectroscopy and molecular simulations to prove that long-range protein-water interactions make essential contributions to the high antifreeze activity of insect AFPs from the beetle Dendroides canadensis. We also support our hypothesis by studying the effect of the addition of the osmolyte sodium citrate.hydration dynamics | THz spetroscopy A ntifreeze proteins (AFPs) and antifreeze glycoproteins (AFGPs) are classes of proteins that suppress ice growth in organisms and thereby enable their survival in subfreezing habitats (1). Despite their similar function, many distinct structures have been identified so far. AFPs have been identified in several organisms, including polar fish (2), insects (3), bacteria (4), and plants (5). Their common characteristic is the depression of the freezing temperatures of ice growth of a solution without depressing the melting point equilibrium of protein solutions. This nonequilibrium phenomenon leads to a difference between the freezing and melting temperature, which is referred to as thermal hysteresis (TH). TH is used as a characteristic measure for antifreeze activity of an AFP (6). AFGPs and AFPs, as extracted from the blood of polar fish, usually exhibit up to 2°of TH activity and are termed moderately active AFPs, whereas insect AFPs can exhibit over 5°of TH and therefore, are referred to as hyperactive AFPs. The work by Raymond and DeVries (7,8) proposed a mechanism in which freezing point depression is achieved by an adsorption-inhibition mechanism, in which the proteins recognize and bind "quasiirreversibly" to an ice surface, thereby preventing growth of ice crystals. The adsorption of the protein is thought to prevent macroscopic ice growth in the hysteresis gap, but microscopic growth occurs at the interface in the form of highly curved fronts between adsorbed antifreeze molecules. This effect will cause a decrease of the local freezing temperature because of the Kelvin effect, while leaving the melting temperature relatively unaffected (7). As recently pointed out in the work by Sharp (9), antifreeze activity involves one of the most difficult recognition problems in biology, the distinction between water as liquid and ice. The initially proposed mechanism builds on a local mechanism. In particular, threonine (Thr) residues were proposed to play a decisive role: their hydroxyl groups were thought to be responsible for the high af...

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Section: Resultsmentioning

confidence: 81%

Long-range protein–water dynamics in hyperactive insect antifreeze proteins

Meister

Ebbinghaus

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

234

221

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“…We have completed molecular dynamics simulations using non-polarizable and polarizable protein force fields to contrast the water dynamics near hydrophilic, N-acetyl-glycine-methylamide (NAGMA), and amphiphilic, N -acetyl-leucine-methylamide (NALMA) peptides as a function of temperature, as models for understanding temperature dependent hydration dynamics near chemically heterogeneous protein surfaces72–76. These simulations are tightly coupled to X-ray diffraction and quasi-elastic neutron scattering (QENS) perfomed on these same systems at the same concentrations.…”

Section: Condensed Phase Structure and Dynamicsmentioning

confidence: 99%

“…Given the qualitative improvement in solution structure using the AMOEBA model, we also compared the changes in water dynamics as a function of temperature against our experimental data. Based on quasi-elastic neutron scattering (QENS) experiments, the amphiphilic NALMA peptide solution exhibits two translational relaxations at low temperatures, while the hydrophilic peptide shows only a single translational process, with transport properties of water near both peptide chemistries being very suppressed with respect to bulk dynamics 75,76. This is a real stress test for any force field given the range of dynamical trends that depend on amino acid chemistry and temperature.…”

Section: Condensed Phase Structure and Dynamicsmentioning

confidence: 99%

Current Status of the AMOEBA Polarizable Force Field

Ponder¹,

Wu²,

et al. 2010

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Molecular force fields have been approaching a generational transition over the past several years, moving away from well-established and well-tuned, but intrinsically limited, fixed point charge models towards more intricate and expensive polarizable models that should allow more accurate description of molecular properties. The recently introduced AMOEBA force field is a leading publicly available example of this next generation of theoretical model, but to date has only received relatively limited validation, which we address here. We show that the AMOEBA force field is in fact a significant improvement over fixed charge models for small molecule structural and thermodynamic observables in particular, although further fine-tuning is necessary to describe solvation free energies of drug-like small molecules, dynamical properties away from ambient conditions, and possible improvements in aromatic interactions. State of the art electronic structure calculations reveal generally very good agreement with AMOEBA for demanding problems such as relative conformational energies of the alanine tetrapeptide and isomers of water sulfate complexes. AMOEBA is shown to be especially successful on protein-ligand binding and computational X-ray crystallography where polarization and accurate electrostatics are critical.

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“…Interfacial water plays a very important role in the structure and the dynamics of proteins as it shapes the potential energy landscape that governs their folding, structure, stability, and function. [7][8][9] Protein dynamics seems to be slaved to the dynamics of water fluctuations. [10] On the other hand, protein activity is also related to its dynamics, so that gaining insight into the properties of interfacial water becomes crucial to understand the microscopic mechanisms of protein function.…”

Section: Introductionmentioning

confidence: 99%

“…[10] On the other hand, protein activity is also related to its dynamics, so that gaining insight into the properties of interfacial water becomes crucial to understand the microscopic mechanisms of protein function. [9,11] A large variety of techniques have been used to address the question of the structure and dynamics of interfacial water, also called hydration water, [7] over several time scales, from Xray crystallography to dielectric spectroscopy (microseconds to 0.1 ns), [12,13] magnetic relaxation dispersion spectroscopy and terahertz spectroscopy (picoseconds), [7,14,15] inelastic neutron scattering (0.1-100 ps), [16] or fluorescence and photon-echo…”

Section: Introductionmentioning

confidence: 99%

Site‐Dependent Excited‐State Dynamics of a Fluorescent Probe Bound to Avidin and Streptavidin

et al. 2009

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Sensing protein environment: The femtosecond fluorescence dynamics of a molecular probe attached to avidin and streptavidin (see figure) depends markedly on the location of the probe and on the protein. These differences reflect not only the protein primary and tertiary structures but also the effect of the surrounding water molecules. The excited‐state dynamics of biotin–spacer–Lucifer‐Yellow (LY) constructs bound to avidin (Avi) and streptavidin (Sav) was investigated using femtosecond spectroscopy. Two different locations in the proteins, identified by molecular dynamics simulations of Sav, namely the entrance of the binding pocket and the protein surface, were probed by varying the length of the spacer. A reduction of the excited‐state lifetime, stronger in Sav than in Avi, was observed with the long spacer construct. Transient absorption measurements show that this effect originates from an electron transfer quenching of LY, most probably by a nearby tryptophan residue. The local environment of the LY chromophore could be probed by measuring the time‐dependent polarisation anisotropy and Stokes shift of the fluorescence. Substantial differences in both dynamics were observed. The fluorescence anisotropy decays analysed by using the wobbling‐in‐a‐cone model reveal a much more constrained environment of the chromophore with the short spacer. Moreover, the dynamic Stokes shift is multiphasic in all cases, with a ∼1 ps component that can be ascribed to diffusive motion of bulk‐like water molecules, and with slower components with time constants varying not only with the spacer, but with the protein as well. These slow components, which depend strongly on the local environment of the probe, are ascribed to the motion of the hydration layer coupled to the conformational dynamics of the protein.

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Aqueous peptides as experimental models for hydration water dynamics near protein surfaces

Cited by 39 publications

References 55 publications

Long-range protein–water dynamics in hyperactive insect antifreeze proteins

Long-range protein–water dynamics in hyperactive insect antifreeze proteins

Current Status of the AMOEBA Polarizable Force Field

Site‐Dependent Excited‐State Dynamics of a Fluorescent Probe Bound to Avidin and Streptavidin

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