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. 2018 Jan;50(1):125-140.
doi: 10.1007/s00726-017-2499-x. Epub 2017 Oct 17.

Taurine as a Water Structure Breaker and Protein Stabilizer

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Free PMC article

Taurine as a Water Structure Breaker and Protein Stabilizer

P Bruździak et al. Amino Acids. .
Free PMC article

Abstract

The enhancing effect on the water structure has been confirmed for most of the osmolytes exhibiting both stabilizing and destabilizing properties in regard to proteins. The presented work concerns osmolytes, which should be classified as "structure breaking" solutes: taurine and N,N,N-trimethyltaurine (TMT). Here, we combine FTIR spectroscopy, DSC calorimetry and DFT calculations to gain an insight into the interactions between osmolytes and two proteins: lysozyme and ubiquitin. Despite high structural similarity, both osmolytes exert different influence on protein stability: taurine is a stabilizer, TMT is a denaturant. We show also that taurine amino group interacts directly with the side chains of proteins, whereas TMT does not interact with proteins at all. Although two solutes weaken on average the structure of the surrounding water, their hydration spheres are different. Taurine is surrounded by two populations of water molecules: bonded with weak H-bonds around sulfonate group, and strongly bonded around amino group. The strong hydrogen-bonded network of water molecules around the amino group of taurine further improves properties of enhanced protein hydration sphere and stabilizes the native protein form. Direct interactions of this group with surface side chains provide a proper orientation of taurine and prevents the [Formula: see text] group from negative influence. The weakened [Formula: see text] hydration sphere of TMT breaks up the hydrogen-bonded network of water around the protein and destabilizes it. However, TMT at low concentration stabilize both proteins to a small extent. This effect can be attributed to an actual osmophobic effect which is overcome if the concentration increases.

Keywords: DFT calculations; DSC calorimetry; FTIR spectroscopy; Hydration; Protein interactions; Taurine.

Conflict of interest statement

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

This article does not contain any studies with human participants or animals performed by any of the authors, thus no informed consent was required in this study.

Figures

Fig. 1
Fig. 1
The dependencies of lysozyme and ubiquitin denaturation temperature versus taurine (a, b) or TMT (c, d) molality. Dashed lines are presented only for visual purposes
Fig. 2
Fig. 2
a, b Bulk (black), highly (red) and less (green) protein-affected spectra of taurine in the spectral region of NH bending vibration. c, d Bulk (black) and protein-affected (red) FTIR spectra of taurine in the spectral region of SO3- stretching vibrations. e, f Bulk (black) and protein-affected (red) FTIR spectra of TMT in the spectral region of SO3- stretching vibrations. Area of all spectra were normalized to a unitary area
Fig. 3
Fig. 3
a, b Affected numbers, N, of taurine molecules at various molalities (circles) in solutions of a lysozyme and b ubiquitin decomposed into two differently affected contributions: highly affected one (squares) and less affected one (triangles). c Preferential interaction coefficients, derived from spectroscopic data, corresponding to highly affected taurine molecules in these systems. Dashed lines are presented only for visual purposes and have no physical meaning
Fig. 4
Fig. 4
Optimized structures of taurine, TMT, ARG, FOR and H2O for which DFT energies and frequencies were calculated (M06-2X/aug-cc-pVTZ with CPCM water solvent model). Names of all molecules and complexes correspond to the ones presented in Table 1. c Represents cyclic form of taurine
Fig. 5
Fig. 5
TMT-affected spectra for all studied temperatures decomposed into component bands. Solid line: original affected spectrum; dotted line: sum of the component bands (covered by the solid line of the original spectrum); dashed line: OD component band
Fig. 6
Fig. 6
Taurine-affected spectra for all studied temperatures decomposed into component bands. Solid line: original affected spectrum; dotted line: sum of the component bands (covered by the solid line of the original spectrum); dashed line: OD component band
Fig. 7
Fig. 7
The optimized structures of hydrated complexes of a TMT and b taurine calculated in the PCM model and corresponding vibrational frequencies (cm−1) obtained from transformation of interatomic oxygen–oxygen distances (R OO) to the OD band position of HDO (ν OD) with the aid of the empirical relations (Eq. 1). Positions of the OD bands visible in the taurine-affected water spectra (Fig. 6) are put in frames. Hydrogen bonds indicated by dashed lines
Fig. 8
Fig. 8
a, b Interatomic oxygen–oxygen distance distributions function derived from the HDO spectra affected by (a) TMT (Fig. 5) and b taurine (Fig. 6). c, d Differences between interatomic oxygen–oxygen distance distribution function of solute-affected water, P a(R OO) and the “bulk” water, P b(R OO) (Fig. S5, ESM) for c TMT and d taurine. The vertical dashed line corresponds to the value of the most probable oxygen–oxygen distance in bulk water at 25 °C (2.823 Å, see Table 3)

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