Interaction of Tyrosine Analogues with Quaternary Ammonium Head

Feb 6, 2018 - The concentration of CTAB (75 mM) and amino acid esters (37 mM), i.e., at XTYOE/TYDE = 0.33 was chosen as it is an intermediate between ...
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Article Cite This: J. Phys. Chem. B XXXX, XXX, XXX−XXX

Interaction of Tyrosine Analogues with Quaternary Ammonium Head Groups at the Micelle/Water Interface and Contrasting Effect of Molecular Folding on the Hydrophobic Outcome and End-Cap Geometry Gulmi Chakraborty,† Madhurima Paul Chowdhury,† P. A. Hassan,‡ Koji Tsuchiya,∥ Kanjiro Torigoe,§ and Swapan K. Saha*,† †

Department of Chemistry, University of North Bengal, Darjeeling 734 013, India Chemistry Division, Bhabha Atmoic Research Centre, Trombay, Mumbai 400085, India ∥ Research Institute for Science and Technology, Tokyo University of Science, 2641 Yamazaki, Noda, Chiba 278-8510, Japan § Department of Pure and Applied Chemistry, Tokyo University of Science, 2641 Yamazaki, Noda, Tokyo 278-8510, Japan ‡

S Supporting Information *

ABSTRACT: The surface property of the cationic micelles of cetyltrimethylammonium bromide (CTAB) in an aqueous medium is highly modified in the presence of tyrosineoctyl ester (TYOE) and tyrosinedodecyl ester (TYDE), the models for aromatic amino acid side chains of transmembrane proteins. While the synergistic interaction between the quaternary ammonium head group of CTAB and the π-electron cloud of aromatic amino acid ester is influenced by the relative orientation and the unusual molecular geometry of the latter, this eventually triggers a morphology transition of the spherical micelle to cylindrical/wormlike micelles and imparts a strong viscoelasticity in the medium. Physical characteristics of the elongated micelles have been investigated by high resolution transmission electron microscopy (HRTEM) and the small angle neutron scattering (SANS) technique; the complex fluidic nature of the system is investigated by a dynamic rheological measurement. The intermolecular interactions have been recognized via 1H NMR and 2D nuclear Overhauser effect spectroscopy (NOESY), and the unambiguous geometry of the end-caps of the rods has been ascertained for the first time. While the interplay between lipids and transmembrane proteins is thought to be crucial in controlling the membrane shape of the cells during many vital events such as cellular fission, fusion, and virus entry, the observed tuning of the micellar surface curvature via the cation−π interaction involving tyrosine analogues is thought provoking and opens up an avenue for new physical chemistry research on a vital biological phenomena.

1. INTRODUCTION Most cellular membranes are complex assemblies of different lipids and proteins, in which phospholipids are the major building blocks. One of the most abundant phospholipids in animals and plants is phosphatidylcholine (lecithin). It is a neutral or zwitterionic phospholipid (with a quaternary ammonium cation and phosphate anion) over a range of pH. Cellular membranes have a low bending modulus and are thin and fluidic in nature. They are highly flexible and permit a selective passage of materials into and out of the cells besides allowing a lateral flow of membrane components into itself.1 A number of different types of proteins also form an integral part of the cell membrane. These functional protein molecules are bound to the cell membrane through different mechanisms and perform various tasks. Some of these crucial proteins are either transmembrane proteins, which extend across the lipid bilayer, or intercellular anchored proteins, which do not span the © XXXX American Chemical Society

membrane but are covalently attached to the inner surface by fatty acids or phospholipids. Peripheral proteins are weakly bound to the membrane surface by noncovalent interactions with other membrane proteins, but most of the proteins of the plasma membrane that are exposed to cell surface are covalently linked to some sugar molecules.2−5 The transmembrane proteins, viz., α-helical bundles and β-barrel proteins, populate the aromatic amino acids (especially, tyrosine, tryptophan, and histidine) at the membrane/water interface where they form functionally significant H bonds with interfacial water. The prevalent understanding is that these residues help the anchoring of membrane proteins to the biological membranes via interaction with the lipid head groups. In membrane Received: November 11, 2017 Revised: February 1, 2018 Published: February 6, 2018 A

DOI: 10.1021/acs.jpcb.7b11167 J. Phys. Chem. B XXXX, XXX, XXX−XXX


The Journal of Physical Chemistry B

topology are produced as a result of a complex interplay between membrane proteins, lipids, and certain physical forces. Therefore, it is tempting to further examine the efficiency of the present amino acid systems as the promoter in tuning the morphology transition of cationic micelles (viz., CTAB micelles) and also examine some related aspects in order to understand if such an exclusive role could be played by aromatic amino acid residues at the membrane/water interface during the complex topological maneuvering.

proteins, these residues have been demonstrated to orient themselves to face the lipid head groups and are a part of the so-called “aromatic belt”.6−9 A highly significant noncovalent interaction, which is believed to occur abundantly in biological systems, is the cation−π interaction, the weak attractive interaction that exists between the cationic species and π-electron cloud of an aromatic ring.10−13 However, the relevance of this interaction in biological structures has been recognized only in recent years. While the majority of X-ray crystal structure analyses reveal the cation−π interaction as one of the main forces that stabilizes protein folding and protein complexes with small molecules, most of the above findings are the results achieved either through theoretical or indirect experiments. Therefore, investigations aimed at individual interactions by other lead techniques are of extreme importance for better understanding of the forces in complex biological organizations.14−16 Furthermore, neurotransmitters transmit signals across a chemical synapse from one neuron (nerve cell) to another target neuron where the synapse binds a specific receptor in the membrane. It is understood that almost all of the neurotransmitters contain a cationic center, and a common strategy for the biological recognition of a cation is the cation−π interaction. The nicotinic acetylcholine receptor is an example of a ligand-gated ion channel.17,18 Aromatic amino acids have been found to contribute to the agonist binding site, suggesting the involvement of the cation−π interaction in the binding of the quaternary amino group of the agonist, acetylcholine. Therefore, it is imperative to say that the studies on the interaction of aromatic amino acids with such cationic species such as the quaternary ammonium group at the membrane/ water interface are of particular importance, but, surprisingly, a report of such a fundamental study is lacking in the literature. In view of the inherent complexity of the biomembrane systems, the use of suitable models for the aromatic amino acid residues of such proteins would indeed be helpful. In spite of the importance, very few model systems have been developed to help understand the behavior of aromatic amino acids, viz., tyrosine and tryptophan residues in the membrane. Tyrosine and tryptophan octyl esters are recognized as the important models for the membrane bound aromatic residues.19−24 It is interesting to note that fluorescence properties of long chain esters of tryptophan (L-tryptophanoctyl ester), incorporated in the model membrane of surfactant micelles, have been shown to be similar to that of the tryptophan residue of transmembrane proteins. Recently, it has been shown that the occurrence of hydrophilic and hydrophobic blocks in octyl and dodecyl esters of tyrosine, as well as in octyl ester of tryptophan, leads to the molecular folding of these aromatic systems in aqueous solutions, and eventually, a fascinating high order morphology of the exclusive aggregates is formed.25 These self-assembled systems also exhibit a great promise toward applications as bioinspired drug carriers. In this paper, the result of the detail study on the interaction of cetyltrimethylammonium bromide (CTAB) micelles with tyrosine octyl and dodecyl esters with regard to their exclusive molecular geometries is reported. It will be interesting to pay attention as well, in this context, to the shape of the biological membrane and the mechanism of its tuning in various vital processes like cell fusion and fission. Biological membranes exhibit various function-related shapes, and the mechanism by which these shapes are created is largely unclear. It is generally believed that the changes of membrane

2. MATERIALS AND METHODS 2.1. Materials. L-Tyrosineoctyl ester (TYOE) and Ltyrosine dodecyl ester (TYDE) were synthesized in our laboratory following the procedure published previously.3 CTAB was purchased from Fluka (Switzerland). D2O for the NMR study was purchased from Aldrich (USA). The purity of all of the chemicals was greater than 99.5%, and the chemicals were used as received. All experiments were done with deionized and doubly distilled water with a pH range 6.5−7 and a specific conductance below 2 μS cm−1. 2.2. Methods. 2.2.1. Tensiometry. Tensiometric measurements were performed on a Krüss K9 tensiometer (Germany), based on the Du Nóuy ring detachment method, fitted with an Omniiset temperature bath with a precision of ±0.1 °C. If not stated otherwise, all solutions were freshly prepared before the experiments. Double distilled deionized water was used in the preparation of all of the samples. Before each measurement, the platinum ring was thoroughly cleaned with a 1:1 acetone−water solution and heated under an oxidizing flame until a glowing temperature was attained. After every addition, the experimental solution was stirred for 5 min for homogeneity and equilibrated for 10 min. For each measurement, three to five subsequent readings were taken for concordance. The standard deviation was