Physicochemical nature of sodium dodecyl sulfate interactions with bovine serum albumin revealed by interdisciplinary approaches

https://doi.org/10.1016/j.molliq.2021.117185Get rights and content

Highlights

  • SDS-BSA binding mode is pH- and temperature-dependent.

  • Two SDS molecules bind to the first binding site of BSA in a pH-independent manner.

  • The second binding site of BSA is pH-dependent.

  • SDS binding in the first binding site is stronger than in the second one.

  • Physicochemical basis of the SDS-BSA interactions are uncovered.

Abstract

To rigorously characterize the interactions of sodium dodecyl sulfate (SDS) with bovine serum albumin (BSA) a set of experimental methods, namely isothermal titration calorimetry, conductometric titration, steady-state fluorescence spectroscopy, differential scanning calorimetry and circular dichroism spectroscopy, supported by in silico analysis have been applied. The influence of pH and temperature on the binding mode has been revealed. At a low molar ratio of SDS to BSA up to ca. 16:1, there are at least two structurally distinct binding sites in BSA. The formation of SDS-BSA complexes is an enthalpy-driven process in which the van der Waals interactions play a crucial role. The first binding site, located close to the Trp-134 residue within the sub-domain IA, is pH-independent and binds two molecules of SDS per one molecule of BSA whereas the total number of SDS molecules bound to the second site of albumin is affected by temperature and pH. The saturation of the first binding site of BSA (ca. 0.009 mg of SDS per 1 mg of BSA) is sufficient to thermally stabilize the helical conformation of BSA. The presented results have important structural and thermodynamic implications to understand the influence of a widely used anionic surfactant on globular protein functionality in modern branches of chemistry.

Introduction

Surfactants are the subject of interest to many research groups since it has been found that they can be utilized in several industrial and technical applications, including detergent industry, food chemistry, drug delivery, and cosmetic preparation as well as developments in life sciences [1], [2], [3], [4]. Much attention has been focused on studies of surfactant interactions with biologically relevant macromolecules such as proteins [5], [6], [7], [8], [9], [10], [11].

An excellent review on the protein - surfactant interactions provided by Otzen reveals the most important techniques for analysing these interactions and highlights the different issues related to this field, namely the impact of surfactant on protein denaturation, binding affinity and unfolding processes [12]. The macromolecule - surfactant interactions depend on many factors, including the topology of the investigated surfactant species (monomeric and micelle forms), a chemical structure of a surfactant (anionic, cationic, amphoteric or non-ionic) as well as experimental conditions (pH, temperature). A remarkable degree of specificity and high affinity of surfactants towards proteins results in changes in their physicochemical properties. Consequently the conformational changes and the saturation of the binding sites of a macromolecule affect its biological activity upon a complex formation.

The understanding of the thermodynamic and thermal stability of the binding process and the structural changes of a protein in the presence of ubiquitous surfactants may be helpful for an in-depth interpretation of a surfactant role underlying biologically relevant protein’s functions. Moreover, it is fundamental from the viewpoint of the surfactants application in environmental processes and the pharmaceutical industry [13]. In this paper, we report the influence of pH and temperature on the interactions of the sodium dodecyl sulfate (SDS), a common, anionic surfactant, with the protein bovine serum albumin (BSA). As far as we are concerned, there are few reports on the SDS – BSA interactions [14], [15], [16], [17], [18], [19]. However, in contrast to these previous studies, we have focused our attention on a low SDS to BSA molar ratio range. Furthermore, the experimental and in silico data related to the structural impact of pH and temperature on the potential binding sites and poses of BSA have been discussed.

Section snippets

Materials

Bovine serum albumin (BSA, lyophilized powder, ≥96%, Sigma-Aldrich, Poland), sodium dodecyl sulfate (SDS, BioUltra, for molecular biology, ≥99%, Sigma-Aldrich, Poland), sodium cacodylate trihydrate (Caco, ≥99%, Sigma-Aldrich, Poland) were used as obtained without further purification. Double-distilled water with conductivity not exceeding 0.18 μS cm−1 was used for preparations of aqueous solutions.

Conductometric analysis

A microtitration unit (Cerko Lab System, Poland) fitted with a 5 mL syringe (Hamilton, Poland) and

Critical micelle concentration (CMC) of SDS in cacodylate buffer

Surfactant molecules reveal tendency to self-association and formation of ordered structures (micelles). Thus, the investigations of systems in which surfactants are involved require determination of the critical micelle concentration (CMC) [31], [32]. The presence of monomeric surfactants (below the CMC) and micelles modifies solution properties as well as has a considerable impact on their interaction’s mode with various proteins [33], [34], [35]. The CMC value depends on many factors, among

Conclusions

In this study, we showed that a low concentration of SDS (0.009 mg/1 mg SDS/BSA) significantly affects the BSA structure, which may have an impact on its biological functions. It should be stressed that the binding constant and the stoichiometry of the resulting BSA complexes are so-called condition-dependent parameters as their values often depend on experimental conditions (pH and temperature). Furthermore, the determination of the binding properties of BSA is not always straightforward,

CRediT authorship contribution statement

Aleksandra Tesmar: Conceptualization, Data curation. Małgorzata M. Kogut: Methodology, Investigation. Krzysztof Żamojć: Methodology, Investigation. Ola Grabowska: Investigation, Resources. Katarzyna Chmur: Investigation, Resources. Sergey A. Samsonov: Methodology, Supervision. Joanna Makowska: Methodology, Investigation. Dariusz Wyrzykowski: Conceptualization, Project administration, Writing - review & editing. Lech Chmurzyński: Supervision, Writing - review & editing.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This work was supported by the Polish National Science Centre under Grant No. 2016/23/D/ST4/01576. Theoretical research was funded by National Science Centre of Poland, grant number UMO-2018/30/E/ST4/00037. Computational resources were provided by the Polish Grid Infrastructure (PL-GRID, grants plgionsgpu, plggagstr2), ZIH at TU Dresden (grant p_gag) and the local cluster PIASEK at the Faculty of Chemistry, University of Gdansk.

References (57)

  • D. Kelley et al.

    Interactions of bovine serum albumin with ionic surfactants in aqueous solutions

    Food Hydrocoll.

    (2003)
  • E.L. Gelamo et al.

    Spectroscopic studies on the interaction of bovine (BSA) and human (HSA) serum albumins with ionic surfactants

    Spectrochim. Acta A

    (2000)
  • J.T. Pelton et al.

    Spectroscopic methods for analysis of protein secondary structure

    Anal. Biochem.

    (2000)
  • E. Fuguet et al.

    Critical micelle concentration of surfactants in aqueous buffered and unbuffered systems

    Anal. Chim. Acta

    (2005)
  • A. Zdziennicka et al.

    Critical micelle concentration of some surfactants and thermodynamic parameters of their micellization

    Fluid Ph. Equilibria

    (2012)
  • R. Patel et al.

    The use of isothermal titration calorimetry to assess the solubility enhancement of simvastatin by a range of surfactants

    Thermochim. Acta

    (2007)
  • P. Chakrabarti et al.

    Geometry of nonbonded interactions involving planar groups in proteins

    Prog. Biophys. Mol. Biol.

    (2007)
  • D.L. Cramer et al.

    Some thermodynamic effects of varying nonpolar surfaces in protein ligand interactions

    European J. Med. Chem.

    (2020)
  • Zhiyong Tian et al.

    Investigation of the interaction of a polyamine-modified flavonoid with bovine serum albumin (BSA) by spectroscopic methods and molecular simulation

    J. Photochem. Photobiol. B: Biology

    (2020)
  • B.L. Wang et al.

    Investigation on the binding behavior between BSA and lenvatinib with the help of various spectroscopic and in silico methods

    J. Mol. Struct.

    (2020)
  • X. Wei et al.

    Synthesis, characterization, DNA/BSA interactions and in vitro cytotoxicity study of palladium(II) complexes of hispolon derivatives

    J. Inorg. Biochem.

    (2020)
  • Krzysztof Żamojć et al.

    The influence of the type of substituents and the solvent on the interactions between different coumarins and selected TEMPO analogues–Fluorescence quenching studies

    Chem. Phys.

    (2018)
  • T. Song et al.

    A review of the role and mechanism of surfactants in the morphology control of metal nanoparticles

    Nanoscale

    (2021)
  • J. Song et al.

    Prolamin-based complexes: Structure design and food-related applications

    Compr. Rev. Food Sci. Food Saf.

    (2021)
  • K.K. Andersen et al.

    A global study of myoglobin–surfactant interactions

    Langmuir

    (2008)
  • M. Aguirre-Ramírez et al.

    Surfactants: physicochemical interactions with biological macromolecules

    Biotechnol. Lett.

    (2021)
  • A. Chakraborty et al.

    Photoinduced electron transfer in a protein-surfactant complex: probing the interaction of SDS with BSA

    J. Phys. Chem. B

    (2006)
  • T. Chakraborty et al.

    Physicochemical and conformational studies on BSA-surfactant interaction in aqueous medium

    Langmuir

    (2009)
  • Cited by (0)

    1

    Authors contributed equally.

    View full text