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Dendronic Trimaltoside Amphiphiles (Dtms) for Membrane Protein Study† Cite This: Chem

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Dendronic Trimaltoside Amphiphiles (Dtms) for Membrane Protein Study† Cite This: Chem Chemical Science View Article Online EDGE ARTICLE View Journal | View Issue Dendronic trimaltoside amphiphiles (DTMs) for membrane protein study† Cite this: Chem. Sci.,2017,8,8315 Aiman Sadaf, ‡a Yang Du, ‡b Claudia Santillan, c Jonas S. Mortensen, d Iago Molist, e Alpay B. Seven, f Parameswaran Hariharan, c Georgios Skiniotis, f Claus J. Loland, d Brian K. Kobilka, b Lan Guan, c Bernadette Byrne e and Pil Seok Chae *a The critical contribution of membrane proteins in normal cellular function makes their detailed structure and functional analysis essential. Detergents, amphipathic agents with the ability to maintain membrane proteins in a soluble state in aqueous solution, have key roles in membrane protein manipulation. Structural and functional stability is a prerequisite for biophysical characterization. However, many conventional detergents are limited in their ability to stabilize membrane proteins, making development of novel detergents for membrane protein manipulation an important research area. The architecture of a detergent hydrophobic group, that directly interacts with the hydrophobic segment of membrane Creative Commons Attribution-NonCommercial 3.0 Unported Licence. proteins, is a key factor in dictating their efficacy for both membrane protein solubilization and stabilization. In the current study, we developed two sets of maltoside-based detergents with four alkyl chains by introducing dendronic hydrophobic groups connected to a trimaltoside head group, designated dendronic trimaltosides (DTMs). Representative DTMs conferred enhanced stabilization to multiple membrane proteins compared to the benchmark conventional detergent, DDM. One DTM (i.e., DTM-A6) clearly outperformed DDM in stabilizing human b2 adrenergic receptor (b2AR) and its complex Received 24th August 2017 with G protein. A further evaluation of this DTM led to a clear visualization of b AR-G complex via Accepted 14th October 2017 s 2 s electron microscopic analysis. Thus, the current study not only provides novel detergent tools useful for DOI: 10.1039/c7sc03700g This article is licensed under a membrane protein study, but also suggests that the dendronic architecture has a role in governing rsc.li/chemical-science detergent efficacy for membrane protein stabilization. Open Access Article. Published on 25 October 2017. Downloaded 9/27/2021 11:56:13 PM. Introduction Malfunctions of these bio-macromolecules lead to various health disorders such as cystic brosis, Alzheimer's, cancer and 2 Membrane proteins embedded in cellular membranes account neurodegenerative diseases. Approximately 60% of current 3 for approximately 30% of total gene transcripts.1 Restricted to pharmaceutical agents target membrane proteins. Despite lateral motion, these proteins are of pivotal importance in cell their biochemical and pharmaceutical signicance, the struc- physiology. They include cell surface receptors, signal trans- tural and functional study of membrane proteins lags far ducers, metabolite transporters and membrane channels. behind that of soluble proteins. The paucity of membrane protein structures mainly results from the incompatibility of their physicochemical properties with the prerequisite aDepartment of Bionanotechnology, Hanyang University, Ansan, 155-88, Korea. requirements for biophysical analysis.4 As expected from the E-mail: [email protected] bMolecular and Cellular Physiology, Stanford, CA 94305, USA. E-mail: kobilka@ structure of native membranes, membrane proteins are inser- stanford.edu ted asymmetrically into the bilayer, with the central trans- cDepartment of Cell Physiology and Molecular Biophysics, Center for Membrane membrane segment anked by the two non-identical Protein Research, School of Medicine, Texas Tech University Health Sciences Center, hydrophilic portions. The amphiphilic nature and preferred Lubbock, TX 79430, USA. E-mail: [email protected] orientation contribute to proper functions of these bio- d Center of Neuroscience, University of Copenhagen, DK 2200 Copenhagen, Denmark. macromolecules in the membrane environment, but hampers E-mail: [email protected] their isolation in a soluble and stable state in aqueous media.5 eDepartment of Life Sciences, Imperial College London, London, SW7 2AZ, UK. E-mail: [email protected] Detergent micelles are capable of stabilizing membrane fStructural Biology & Molecular and Cellular Physiology, Stanford, CA 94305, USA. proteins outside the native membranes by encapsulation, 6 E-mail: [email protected] leading to formation of protein-detergent complexes (PDCs). † Electronic supplementary information (ESI) available. See DOI: Thus, detergents are widely used for membrane protein 10.1039/c7sc03700g manipulation including solubilization, stabilization and ‡ These authors contributed equally to this work. This journal is © The Royal Society of Chemistry 2017 Chem. Sci.,2017,8,8315–8324 | 8315 View Article Online Chemical Science Edge Article crystallization. Non-ionic amphiphiles are of prime importance conformational/congurational exibility in detergent stabili- for membrane protein study mainly due to their superior ability zation efficacy could be explained by the recent studies on to stabilize membrane proteins compared to other zwitter-ionic butane-tetraol maltosides (BTMs),17 NBMs,13e and RGAs/ or ionic detergents with charged head groups. This is well NDTs.13f,14f In the present study, we have designed and synthe- illustrated by the fact that 75% of structurally characterised sized two sets of novel amphiphiles containing a dendronic a-helical membrane proteins were isolated and manipulated in hydrophobic group, the rst example of this type of group being one of four non-ionic detergents (OG (n-octyl-b-D-glucoside), NG introduced into a detergent for membrane protein study. (n-nonyl-b-D-glucoside), DM (n-decyl-b-D-maltoside), or DDM (n- Because of the presence of a trimaltoside head and dendronic dodecyl-b-D-maltoside)), along with a zwitterionic detergent, tail groups, these agents were designated dendronic trimalto- LDAO (lauryldimethylamine-N-oxide).7 Despite their wide- side amphiphiles (DTMs). When these agents were evaluated spread use for membrane protein structural studies, these with several membrane proteins, some of these agents dis- detergents are oen suboptimal inducing membrane protein played enhanced protein stabilization efficacy compared to denaturation and/or aggregation.8 These classical detergents a gold standard detergent (DDM). In addition, negative stain are structurally simple, typically having a exible alkyl tail and electron microscopic (EM) analysis revealed that a representa- a large hydrophilic head group. In contrast, membrane proteins tive of the DTMs can be effectively used for clear visualization of are highly diverse in terms of their three dimensional structures membrane protein complexes with multi-domains architecture. and biophysical properties. The large gap in structure diversity between conventional detergents and membrane proteins Results and discussion indicates that novel detergents distinct from conventional agents in terms of architecture/chemical properties are neces- The novel agents examined in this study bear three maltosides sary to advance membrane protein research.9 and four alkyl chains as the head and tail groups, respectively, Over the past two decades, many efforts have been made to connected to each other via a neopentyl glycol linker ff Creative Commons Attribution-NonCommercial 3.0 Unported Licence. develop novel classes of amphiphiles, architecturally di erent (Scheme 1). The hydrophobic group of the DTMs has dendronic from conventional detergents.10 Peptide amphiphiles with architecture with two branch points (a and b in Scheme 1). The a-helical (e.g., lipopeptide detergents (LPDs))11a or b-sheet rst branch point (a) was connected to the second point (b in structure (b-peptides (BPs))11b have been developed. Polymeric Scheme) by an ether linkage, while the second branch point was amphiphiles were invented and frequently used alone (e.g., connected to the terminal alkyl chains either directly (DTM-As) amphipols (Apols) and styrene-maleic acid (SMA) polymer),12a–c or through an additional ether linkage (DTM-Es). It is notable or in a combination with a patch of lipid bilayers (e.g., nano- that the dendronic hydrophobic group introduced here enabled discs (NDs))12d for membrane protein studies. This disc system, us to rst develop novel amphiphiles containing four alkyl similar to bicelles in architecture,12e provides a mimetic envi- chains diverging from a single focal point (c). Because of the This article is licensed under a ronment closer to the native membrane than detergent micel- presence of the multiple alkyl chains, these agents have high les.12f However, most of these agents are heterogenous, hydrophobic density and show multi-valency effect.18 These generally hard to prepare on a large scale, or oen inefficient at have critical inuences on the ability of any detergent to effec- extracting membrane proteins from the membranes. In this tively stabilise and solubilize membrane proteins, as supported Open Access Article. Published on 25 October 2017. Downloaded 9/27/2021 11:56:13 PM. context, small amphipathic agents are advantageous over the by results obtained for the TPAs,13b–d mesitylene-cored glucoside peptide- or polymer-based amphiphiles. Representatives of amphiphiles (MGAs),19 and adamantane-based amphiphiles small amphiphiles include rigid hydrophobic group-bearing (ADAs).20 The DTMs are structurally different from
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