Self-assembly of trehalose molecules on a lysozyme surface: the broken glass hypothesis

Fedorov, Maxim V.; Goodman, Jonathan M.; Nerukh, Dmitry; Schumm, Stephan

doi:10.1039/c0cp01705a

Cited by 53 publications

(54 citation statements)

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“…In this condition also the average number of hydrogen bonds, in which each water molecule is involved, was found to increase. These observations confirmed that the water replacement and water entrapment hypotheses are not mutually exclusive; this was also pointed out by recent MD simulations showing that trehalose molecules assemble in distinctive clusters on the surface of the protein; the flexibility of the protein backbone is then reduced due to the presence of these sugar patches [25].…”

Section: Introductionsupporting

confidence: 70%

Proteins in amorphous saccharide matrices: Structural and dynamical insights on bioprotection

et al. 2013

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Abstract. Bioprotection by sugars, and in particular trehalose peculiarity, is a relevant topic due to the implications in several fields. The underlying mechanisms are not yet clearly elucidated, and remain the focus of current investigations. Here we revisit data obtained at our lab on binary sugar/water and ternary protein/sugar/water systems, in wide ranges of water content and temperature, in the light of the current literature. The data here discussed come from complementary techniques (Infrared Spectroscopy, Molecular Dynamics simulations, Small Angle X-ray Scattering and Calorimetry), which provided a consistent description of the bioprotection by sugars from the atomistic to the macroscopic level. We present a picture, which suggests that protein bioprotection can be explained in terms of a strong coupling of the biomolecule surface to the matrix via extended hydrogen-bond networks, whose properties are defined by all components of the systems, and are strongly dependent on water content. Furthermore, the data show how carbohydrates having similar hydrogen-bonding capabilities exhibit different efficiency in preserving biostructures.

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Section: Introductionsupporting

confidence: 70%

Proteins in amorphous saccharide matrices: Structural and dynamical insights on bioprotection

et al. 2013

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“…This was also pointed out by simulations on LSZ-trehalose solutions, where trehalose clusters were found at the LSZ surface, reducing the flexibility of the protein backbone [144].…”

Section: Atomistic Levelmentioning

confidence: 78%

Proteins in Saccharides Matrices and the Trehalose Peculiarity: Biochemical and Biophysical Properties

Cordone¹,

Cupane²,

Emanuele

et al. 2015

COC

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Immobilization of proteins and other biomolecules in saccharide matrices leads to a series of peculiar properties that are relevant from the point of view of both biochemistry and biophysics, and have important implications on related fields such as food industry, pharmaceutics, and medicine. In the last years, the properties of biomolecules embedded into glassy matrices and/or highly concentrated solutions of saccharides have been thoroughly investigated, at the molecular level, through in vivo, in vitro, and in silico studies. These systems show an outstanding ability to protect biostructures against stress conditions; various mechanisms appear to be at the basis of such bioprotection, that in the case of some sugars (in particular trehalose) is peculiarly effective.Here we review recent results obtained in our and other laboratories on ternary protein-sugar-water systems that have been typically studied in wide ranges of water content and temperature. Data from a large set of complementary experimental techniques provide a consistent description of structural, dynamical and functional properties of these systems, from atomistic to thermodynamic level.In the emerging picture, the stabilizing effect induced on the encapsulated systems might be attributed to a strong biomolecule-matrix coupling, mediated by extended hydrogen-bond networks, whose specific properties are determined by the saccharide composition and structure, and depend on water content.

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“…It was suggested that the high glass transition temperature of trehalose may lead to formation of a glassy matrix during cooling, preventing its crystallization. This vitrification hypothesis alone, however, may not be sufficient to explain why trehalose may remain soluble in the winter hemolymph because the solubility of trehalose in actual hemolymph would be lower than that in water (as the water activity is lower in such a complex system) and the winter temperatures typically fluctuate considerably over the winter, but are often higher than the glass transition temperature (9,(32)(33)(34)(35). Such phase transitions of the hemolymph components are a potential cause of low temperature damage in freeze-avoiding insects (36).…”

Section: Resultsmentioning

confidence: 99%

Antifreeze proteins govern the precipitation of trehalose in a freezing-avoiding insect at low temperature

Wen

Wang

Duman

et al. 2016

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

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The remarkable adaptive strategies of insects to extreme environments are linked to the biochemical compounds in their body fluids. Trehalose, a versatile sugar molecule, can accumulate to high levels in freeze-tolerant and freeze-avoiding insects, functioning as a cryoprotectant and a supercooling agent. Antifreeze proteins (AFPs), known to protect organisms from freezing by lowering the freezing temperature and deferring the growth of ice, are present at high levels in some freeze-avoiding insects in winter, and yet, paradoxically are found in some freeze-tolerant insects. Here, we report a previously unidentified role for AFPs in effectively inhibiting trehalose precipitation in the hemolymph (or blood) of overwintering beetle larvae. We determine the trehalose level (29.6 ± 0.6 mg/mL) in the larval hemolymph of a beetle, Dendroides canadensis, and demonstrate that the hemolymph AFPs are crucial for inhibiting trehalose crystallization, whereas the presence of trehalose also enhances the antifreeze activity of AFPs. To dissect the molecular mechanism, we examine the molecular recognition between AFP and trehalose crystal interfaces using molecular dynamics simulations. The theory corroborates the experiments and shows preferential strong binding of the AFP to the fast growing surfaces of the sugar crystal. This newly uncovered role for AFPs may help explain the long-speculated role of AFPs in freeze-tolerant species. We propose that the presence of high levels of molecules important for survival but prone to precipitation in poikilotherms (their body temperature can vary considerably) needs a companion mechanism to prevent the precipitation and here present, to our knowledge, the first example. Such a combination of trehalose and AFPs also provides a novel approach for cold protection and for trehalose crystallization inhibition in industrial applications.T rehalose is a multifunctional nonreducing disaccharide, occurring naturally in all kingdoms (1-4). In addition to being an energy and carbon source, this sugar protects cells and proteins against injuries in extreme environments (1, 2, 4), prevents osteoporosis (5), alleviates certain diseases (6), and acts as a signal molecule in plants (7). Due to its bioprotective properties, trehalose is a potentially useful protectant of cells and proteins in numerous applications (2,8). Its practical use, however, can be impaired by the fact that this sugar is prone to crystallization, in particular, when its aqueous solution is under fluctuating low temperatures. For example, the crystallization of trehalose dihydrate during the freeze-drying processes or from solutions at low temperatures would significantly jeopardize its ability to protect biomolecules (8-10). In comparison with other common sugars including sucrose, trehalose has a high propensity to crystallize at low temperature, forming trehalose dihydrate crystals. This propensity is due to: (i) the solubility of trehalose in water decreases dramatically or exponentially as temperature decreases (few data at...

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Self-assembly of trehalose molecules on a lysozyme surface: the broken glass hypothesis

Cited by 53 publications

References 50 publications

Proteins in amorphous saccharide matrices: Structural and dynamical insights on bioprotection

Proteins in amorphous saccharide matrices: Structural and dynamical insights on bioprotection

Proteins in Saccharides Matrices and the Trehalose Peculiarity: Biochemical and Biophysical Properties

Antifreeze proteins govern the precipitation of trehalose in a freezing-avoiding insect at low temperature

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