Which Properties of a Spanning Network of Hydration Water Enable Biological Functions?

Brovchenko, Ivan; Oleinikova, Alla

doi:10.1002/cphc.200800662

Cited by 46 publications

(53 citation statements)

References 69 publications

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“…Although earlier studies have implied NHB water is correlated with protein unfolding (5,83), the relationship between protein functionality and NHB water is still obscure due to experimental difficulties in probing NHB water. Further THz experiments are expected to provide deeper insight into the role of NHB water in the biological functionality of proteins, such as enzyme reactions.…”

Section: Fragmentation Of Water-water Hbsmentioning

confidence: 99%

“…It is widely believed that these peculiar characteristics of water in the vicinity of proteins provide biological functionalities to the protein molecule (4,5). For example, inactive dehydrated enzymes are reactivated when they are covered by at least one layer of water (socalled ''hydration water'') and a strong coupling between the protein and hydration water triggers the protein dynamical transition (5)(6)(7). Liquid water forms a hydrogenbond (HB) network with a distorted tetrahedral structure continuously fluctuating at timescales of subpicoseconds to picoseconds (8)(9)(10)(11).…”

Section: Introductionmentioning

confidence: 99%

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Hydrogen Bond Network of Water around Protein Investigated with Terahertz and Infrared Spectroscopy

Shiraga

Ogawa

Kondo

2016

Biophysical Journal

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The dynamical and structural properties of water at protein interfaces were characterized on the basis of the broadband complex dielectric constant (0.25 to 400 THz) of albumin aqueous solutions. Our analysis of the dielectric responses between 0.25 and 12 THz first revealed hydration water with retarded reorientational dynamics extending~8.5 Å (corresponding to three to four layers) out from the albumin surface. Second, the number of nonhydrogen-bonded water was decreased in the presence of the albumin solute, indicating protein inhibits the fragmentation of the water hydrogen-bond network. Finally, water molecules at the albumin interface were found to form a distorted hydrogen-bond structure due to topological and energetic disorder of the protein surface. In addition, the intramolecular O-H stretching vibration of water (~100 THz), which is sensitive to hydrogen-bond environment, pointed to a trend that hydration water has a larger population of strongly hydrogen-bonded water molecules compared with that of bulk water. From these experimental results, we concluded that the ''strengthened'' water hydrogen bonds at the protein interface dynamically slow down the reorientational motion of water and form the less-defective hydrogen-bond network by inhibiting the fragmentation of water-water hydrogen bonds. Nevertheless, such a strengthened water hydrogen-bond network is composed of heterogeneous hydrogen-bond distances and angles, and thus characterized as structurally ''distorted.''

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Section: Fragmentation Of Water-water Hbsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Hydrogen Bond Network of Water around Protein Investigated with Terahertz and Infrared Spectroscopy

Shiraga

Ogawa

Kondo

2016

Biophysical Journal

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“…When the hydration drops below a threshold of approximately 0.3 g water g −1 dry mass, most bulk water is removed (Brovchenko and Oleinikova, 2008;Ball, 2008), and the mechanism of preferential hydration thus fails to work. Most compatible solutes are unable to protect proteins and membranes beyond this level of dehydration (Hoekstra et al, 2001).…”

Section: Stabilization Of Membrane Structurementioning

confidence: 99%

“…reduce the cell shrinkage (Meryman, 1971;Storey and Storey, 1988). Dehydration, however, also results in increased acidity, increased metal ion concentrations, increased viscosity and tight packing of macromolecules, which, together with thermal stress, threaten the chemical and conformational stability of proteins and other macromolecules (Wang, 1999;Brovchenko and Oleinikova, 2008). Another role for cryoprotectants is to assist in protection/recovery of the functional native state of macromolecules or biological membranes during freezing stress (Timasheff, 1992;Wang, 1999Wang, , 2005Bolen and Baskakov, 2001).…”

Section: Introductionmentioning

confidence: 99%

Arginine and proline applied as food additives stimulate high freeze tolerance in larvae of Drosophila melanogaster

Košťál

Korbelová

Poupardin

et al. 2016

Journal of Experimental Biology

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The fruit fly Drosophila melanogaster is an insect of tropical origin. Its larval stage is evolutionarily adapted for rapid growth and development under warm conditions and shows high sensitivity to cold. In this study, we further developed an optimal acclimation and freezing protocol that significantly improves larval freeze tolerance (an ability to survive at −5°C when most of the freezable fraction of water is converted to ice). Using the optimal protocol, freeze survival to adult stage increased from 0.7% to 12.6% in the larvae fed standard diet (agar, sugar, yeast, cornmeal). Next, we fed the larvae diets augmented with 31 different amino compounds, administered in different concentrations, and observed their effects on larval metabolomic composition, viability, rate of development and freeze tolerance. While some diet additives were toxic, others showed positive effects on freeze tolerance. Statistical correlation revealed tight association between high freeze tolerance and high levels of amino compounds involved in arginine and proline metabolism. Proline-and arginine-augmented diets showed the highest potential, improving freeze survival to 42.1% and 50.6%, respectively. Two plausible mechanisms by which high concentrations of proline and arginine might stimulate high freeze tolerance are discussed: (i) proline, probably in combination with trehalose, could reduce partial unfolding of proteins and prevent membrane fusions in the larvae exposed to thermal stress ( prior to freezing) or during freeze dehydration; (ii) both arginine and proline are exceptional among amino compounds in their ability to form supramolecular aggregates which probably bind partially unfolded proteins and inhibit their aggregation under increasing freeze dehydration.

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“…The hydration shell consists of Ϸ2 layers of water that surround proteins as shown in Fig. 1 (7)(8)(9)(10)(11)(12). Protein functions depend on the degree of hydration, h, defined as the weight ratio of water to protein.…”

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confidence: 99%

A unified model of protein dynamics

Frauenfelder

Chen

Berendzen

et al. 2009

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

689

809

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beta process ͉ dielectric ͉ hydration ͉ solvent P roteins are dynamic systems that interact strongly with their environment (1). Most texts and publications show proteins in unique conformations and naked, without hydration shell and bulk solvent, while fluctuations are rarely mentioned. The unified model of protein dynamics presented here is a radical departure from this picture. In this model, the protein provides the structure for the biological function, but it is dynamically passive. The fluctuations in the bulk solvent power and control the large-scale motions and shape changes of the protein in a diffusive manner (2-4), whereas the fluctuations in the hydration shell power and control the internal protein motions such as ligand migration (5, 6). The hydration shell consists of Ϸ2 layers of water that surround proteins as shown in Fig. 1 (7-12). Protein functions depend on the degree of hydration, h, defined as the weight ratio of water to protein. Dehydrated proteins do not function. Some proteins begin to work at h Ϸ 0.2 (11) but full function may require h Ͼ 1. The controls exerted by the bulk solvent and the hydration shell are possible because the protein interior is fluid-like (13); the intrinsic viscosity of a protein is small, about like water (14-16). The image of the protein being essentially passive and being slaved to the environment is not an idle speculation. It is based on experiments using myoglobin (Mb) that led to the seminal concepts that underlie the present work: (i) Proteins do not exist in a unique conformation; they can assume a very large number of conformational substates (CS) (17, 18). (ii) The CS can be described by an energy landscape (17). (iii) The landscape is organized in a hierarchy; there are energy valleys within energy valleys within energy valleys (19). The description of the effects of the bulk solvent and the hydration shell is based on these concepts. Because knowledge of the fluctuations in glass-forming liquids and of the energy landscape of proteins is essential for understanding these results, we discuss these topics first.The ␣ and ␤ Processes (20, 21) Glass-forming liquids have two types of equilibrium fluctuations, ␣ and ␤.* One tool to study these fluctuations is dielectric relaxation spectroscopy (21). The sample is placed in a capacitor, a sine-wave voltage U 1 ( ) of frequency is applied, and the resulting current is converted into a voltage U 2 ( ) that characterizes the dielectric spectrum. Our spectra exhibit two prominent peaks that characterize ␣, or primary, and ␤, or secondary, relaxations. The ␣ process describes structural fluctuations. The mechanical Maxwell relation,connects the rate coefficient k ␣ (T) for the ␣ fluctuations to the viscosity (T). Here, G 0 is the infinite-frequency shear modulus that depends only weakly on temperature and on the material.Author contributions: H.F., G.C., J.B., P.W.F., H.J., B.H.M., I.R.S., J.S., and R.D.Y. designed research, performed research, contributed new reagents/analytic tools, analyzed data, and wrote ...

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Which Properties of a Spanning Network of Hydration Water Enable Biological Functions?

Cited by 46 publications

References 69 publications

Hydrogen Bond Network of Water around Protein Investigated with Terahertz and Infrared Spectroscopy

Hydrogen Bond Network of Water around Protein Investigated with Terahertz and Infrared Spectroscopy

Arginine and proline applied as food additives stimulate high freeze tolerance in larvae of Drosophila melanogaster

A unified model of protein dynamics

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