Deuterated detergents for structural and functional studies of membrane proteins: Properties, chemical synthesis and applications

References

• Alexandrov AI, Mileni M, Chien EY, Hanson MA, Stevens RC. 2008. Microscale fluorescent thermal stability assay for membrane proteins. Structure 16:351–359
   PubMed Web of Science ®Google Scholar
• Almeida FC, Opella SJ. 1997. fd coat protein structure in membrane environments: structural dynamics of the loop between the hydrophobic trans-membrane helix and the amphipathic in-plane helix. J Mol Biol 270:481–495
   PubMed Web of Science ®Google Scholar
• Andreeva BM. 2001. Separation of hydrogen isotopes in H₂O-H₂S system. Separat Sci Technol 36:1949–1989
   Web of Science ®Google Scholar
• Arachea BT, Sun Z, Potente N, Malik R, Isailovic D, Viola RE. 2012. Detergent selection for enhanced extraction of membrane proteins. Protein Expr Purif 86:12–20
   PubMed Web of Science ®Google Scholar
• Arnold T, Linke D. 2008. The use of detergents to purify membrane proteins. Curr Protoc Protein Sci Chapter 4:Unit 4.8.1–4.8.30
   PubMedGoogle Scholar
• Arora A. 2013. Solution NMR spectroscopy for the determination of structures of membrane proteins in a lipid environment. Methods Mol Biol 974:389–413
   PubMedGoogle Scholar
• Arora A, Abildgaard F, Bushweller JH, Tamm LK. 2001. Structure of outer membrane protein A transmembrane domain by NMR spectroscopy. Nat Struct Biol 8:334–338
   PubMedGoogle Scholar
• Arora A, Tamm LK. 2001. Biophysical approaches to membrane protein structure determination. Curr Opin Struct Biol 11:540–547
   PubMed Web of Science ®Google Scholar
• Arseniev AS, Barsukov IL, Bystrov VF, Lomize AL, Ovchinnikov YuA. 1985. 1H-NMR study of gramicidin A transmembrane ion channel. Head-to-head right-handed, single-stranded helices. FEBS Lett 186:168–174
   PubMed Web of Science ®Google Scholar
• Atzrodt J, Derdau V, Fey T, Zimmermann J. 2007. The renaissance of H/D exchange. Angew Chem Int Ed 46:7744–7765
   PubMed Web of Science ®Google Scholar
• Baldwin JE, Gallagher SS, Leber PA, Raghavan AS, Shukla R. 2004. Deuterium kinetic isotope effects and mechanism of the thermal isomerization of bicyclo[4.2.0]oct-7-ene to 1,3-cyclooctadiene. J Org Chem 69:7212–7219
   PubMed Web of Science ®Google Scholar
• Bay DC, Budiman RA, Nieh MP, Turner RJ. 2010. Multimeric forms of the small multidrug resistance protein EmrE in anionic detergent. Biochim Biophys Acta 1798:526–535
   PubMed Web of Science ®Google Scholar
• Bayburt TH, Sligar SG. 2010. Membrane protein assembly into nanodiscs. FEBS Lett 584:1721–1727
   PubMed Web of Science ®Google Scholar
• Bayrhuber M, Meins T, Habeck M, Becker S, Giller K, Villinger S, Vonrhein C, Griesinger C, Zweckstetter M, Zeth K. 2008. Structure of the human voltage-dependent anion channel. Proc Natl Acad Sci USA 105:15370–15375
   PubMed Web of Science ®Google Scholar
• Berardi MJ, Shih WM, Harrison SC, Chou JJ. 2011. Mitochondrial uncoupling protein 2 structure determined by NMR molecular fragment searching. Nature 476:109–113
   PubMed Web of Science ®Google Scholar
• Bettaney KE, Sukumar P, Hussain R, Siligardi G, Henderson PJ, Patching SG. 2013. A systematic approach to the amplified expression, functional characterization and purification of inositol transporters from Bacillus subtilis. Mol Membr Biol 30:3–14
   PubMed Web of Science ®Google Scholar
• Bigeleisen J, Goeppert-Mayer M. 1947. Calculation of equilibrium constants for isotopic exchange reaction. J Phys Chem 15:261
   Web of Science ®Google Scholar
• Bond PJ, Sansom MS. 2003. Membrane protein dynamics versus environment: simulations of OmpA in a micelle and in a bilayer. J Mol Biol 329:1035–1053
   PubMed Web of Science ®Google Scholar
• Bondarenko V, Mowrey D, Tillman T, Cui T, Liu LT, Xu Y, Tang P. 2012. NMR structures of the transmembrane domains of the α4β2 nAChR. Biochim Biophys Acta 1818:1261–1268
   PubMed Web of Science ®Google Scholar
• Breyton C, Gabel F, Lethier M, Flayhan A, Durand G, Jault JM, Juillan-Binard C, Imbert L, Moulin M, Ravaud S, Härtlein M, Ebel C. 2013. Small angle neutron scattering for the study of solubilised membrane proteins. Eur Phys J E Soft Matter 36:71
   PubMed Web of Science ®Google Scholar
• Brown LR. 1979. Use of fully deuterated micelles for conformational studies of membrane proteins by high resolution 1H nuclear magnetic resonance. Biochim Biophys Acta 557:135–148
   PubMed Web of Science ®Google Scholar
• Brown LR, Wüthrich K. 1981. Melittin bound to dodecylphosphocholine micelles. H-NMR assignments and global conformational features. Biochim Biophys Acta 647:95–111
   PubMed Web of Science ®Google Scholar
• Buck-Koehntop BA, Mascioni A, Buffy JJ, Veglia G. 2005. Structure, dynamics, and membrane topology of stannin: a mediator of neuronal cell apoptosis induced by trimethyltin chloride. J Mol Biol 354:652–665
   PubMed Web of Science ®Google Scholar
• Bystrov VF, Arseniev AS, Barsukov IL, Lomize AL. 1986. 2D NMR of single and double stranded helices of gramicidin A in micelles and solutions. Bull Magn Reson 8:84–94
   Google Scholar
• Call ME, Schnell JR, Xu C, Lutz RA, Chou JJ, Wucherpfennig KW. 2006. The structure of the zetazeta transmembrane dimer reveals features essential for its assembly with the T cell receptor. Cell 127:355–368
   PubMed Web of Science ®Google Scholar
• Call ME, Wucherpfennig KW, Chou JJ. 2010. The structural basis for intramembrane assembly of an activating immunoreceptor complex. Nat Immunol 11:1023–1029
   PubMed Web of Science ®Google Scholar
• Chen L, Lai C, Lai J, Tian C. 2011. Expression, purification, detergent screening and solution NMR backbone assignment of the human potassium channel accessory subunit MiRP1. Protein Expr Purif 76:205–210
   PubMed Web of Science ®Google Scholar
• Chen W, Gamache E, Rosenman DJ, Xie J, Lopez MM, Li YM, Wang C. 2014. Familial Alzheimer’s mutations within APPTM increase Aβ42 production by enhancing accessibility of ɛ-cleavage site. Nat Commun 5:3037
   PubMed Web of Science ®Google Scholar
• Chill JH, Louis JM, Miller C, Bax A. 2006. NMR study of the tetrameric KcsA potassium channel in detergent micelles. Protein Sci 15:684–698
   PubMed Web of Science ®Google Scholar
• Ciaccafava A, De Poulpiquet A, Infossi P, Robert S, Gadiou R, Giudici-Orticoni MT, Lecomte S, Lojou E. 2012. A friendly detergent for H2 oxidation by Aquifex aeolicus membrane-bound hydrogenase immobilized on graphite and Self-Assembled-Monolayer-modified gold electrode. Electrochimica Acta 82:115–125
   Web of Science ®Google Scholar
• Cierpicki T, Liang B, Tamm LK, Bushweller JH. 2006. Increasing the accuracy of solution NMR structures of membrane proteins by application of residual dipolar couplings. High-resolution structure of outer membrane protein A. J Am Chem Soc 128:6947–6951
   PubMed Web of Science ®Google Scholar
• Clantin B, Delattre AS, Rucktooa P, Saint N, Méli AC, Locht C, et al. 2007. Structure of the membrane protein FhaC: a member of the Omp85-TpsB transporter superfamily. Science 317:957–961
   PubMed Web of Science ®Google Scholar
• Cleland WW. 2005. The use of isotope effects to determine enzyme mechanisms. Arch Biochem Biophys 433:2–12
   PubMed Web of Science ®Google Scholar
• Columbus L, Lipfert J, Jambunathan K, Fox DA, Sim AY, Doniach S, Lesley SA. 2009. Mixing and matching detergents for membrane protein NMR structure determination. J Am Chem Soc 131:7320–7326
   PubMed Web of Science ®Google Scholar
• Cowan SW, Garavito RM, Jansonius JN, Jenkins JA, Karlsson R, König N, et al. 1995. The structure of OmpF porin in a tetragonal crystal form. Structure 3:1041–1050
   PubMed Web of Science ®Google Scholar
• Damberg P, Jarvet J, Gräslund A. 2001. Micellar systems as solvents in peptide and protein structure determination. Methods Enzymol 339:271–285
   PubMed Web of Science ®Google Scholar
• de Ghellinck A, Schaller H, Laux V, Haertlein M, Sferrazza M, Maréchal E, et al. 2014. Production and analysis of perdeuterated lipids from Pichia pastoris cells. PLoS One 9:e92999
   PubMed Web of Science ®Google Scholar
• Demura M, Yoshida T, Hirokawa T, Kumaki Y, Aizawa T, Nitta K, et al. 2005. Interaction of dopamine and acetylcholine with an amphiphilic resorcinarene receptor in aqueous micelle system. Bioorg Med Chem Lett 15:1367–1370
   PubMed Web of Science ®Google Scholar
• Dürr UH, Gildenberg M, Ramamoorthy A. 2012. The magic of bicelles lights up membrane protein structure. Chem Rev 112:6054–6074
   PubMed Web of Science ®Google Scholar
• Dürr UH, Soong R, Ramamoorthy A. 2013. When detergent meets bilayer: birth and coming of age of lipid bicelles. Prog Nucl Magn Reson Spectrosc 69:1–22
   PubMed Web of Science ®Google Scholar
• Fisher SJ, Helliwell JR. 2008. An investigation into structural changes due to deuteration. Acta Crystallogr A 64(Pt 3):359–367
   PubMedGoogle Scholar
• Franzin CM, Teriete P, Marassi FM. 2007. Structural similarity of a membrane protein in micelles and membranes. J Am Chem Soc 129:8078–8079
   PubMed Web of Science ®Google Scholar
• Gabel F, Lensink MF, Clantin B, Jacob-Dubuisson F, Villeret V, Ebel C. 2014. Probing the conformation of FhaC with small-angle neutron scattering and molecular modeling. Biophys J 107:185–196
   PubMed Web of Science ®Google Scholar
• Garavito RM, Ferguson-Miller S. 2001. Detergents as tools in membrane biochemistry. J Biol Chem 276:32403–32406
   PubMed Web of Science ®Google Scholar
• Gayen S, Li Q, Kim YM, Kang C. 2013. Structure of the C-terminal region of the Frizzled receptor 1 in detergent micelles. Molecules 18:8579–8590
   PubMed Web of Science ®Google Scholar
• Gong XM, Ding Y, Yu J, Yao Y, Marassi FM. 2015. Structure of the Na,K-ATPase regulatory protein FXYD2b in micelles: implications for membrane-water interfacial arginines. Biochim Biophys Acta 1848(1 Pt B):299–306
   PubMed Web of Science ®Google Scholar
• Goñi FM, Alonso A. 2000. Spectroscopic techniques in the study of membrane solubilization, reconstitution and permeabilization by detergents. Biochim Biophys Acta 1508:51–68
   PubMed Web of Science ®Google Scholar
• Guengerich FP. 2013. Kinetic deuterium isotope effects in cytochrome P450 oxidation reactions. J Labelled Comp Radiopharm 56:428–431
   PubMed Web of Science ®Google Scholar
• Hagn F, Etzkorn M, Raschle T, Wagner G. 2013. Optimized phospholipid bilayer nanodiscs facilitate high-resolution structure determination of membrane proteins. J Am Chem Soc 135:1919–1925
   PubMed Web of Science ®Google Scholar
• He X, Morris JJ, Noll BC, Brown SN, Henderson KW. 2006. Kinetics and mechanism of ketone enolization mediated by magnesium bis(hexamethyldisilazide). J Am Chem Soc 128:13599–135610
   PubMed Web of Science ®Google Scholar
• He Y, Wang K, Yan N. 2014. The recombinant expression systems for structure determination of eukaryotic membrane proteins. Protein Cell 5:658–672
   PubMed Web of Science ®Google Scholar
• Hiller S, Garces RG, Malia TJ, Orekhov VY, Colombini M, Wagner G. 2008. Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321:1206–1210
   PubMed Web of Science ®Google Scholar
• Hiller S, Wagner G. 2009. The role of solution NMR in the structure determinations of VDAC-1 and other membrane proteins. Curr Opin Struct Biol 19:396–401
   PubMed Web of Science ®Google Scholar
• Hines HD, Thomas RK, Garrett PR, Rennie GK, Penfold J. 1997. Investigation of mixing in binary surfactant solutions by surface tension and neutron reflection: anionic/nonionic and zwitterionic/nonionic mixtures. J Phys Chem B 101:9215–9223
   Web of Science ®Google Scholar
• Hiruma-Shimizu K, Kalverda AP, Henderson PJF, Homans SW, Patching SG. 2014. Synthesis of uniformly deuterated n-dodecyl-β-D-maltoside (d39-DDM) for solubilisation of membrane proteins in TROSY NMR experiments. J Label Compd Radiopharm 57:737–743
   PubMed Web of Science ®Google Scholar
• Hochuli M, Szyperski T, Wüthrich K. 2000. Deuterium isotope effects on the central carbon metabolism of Escherichia coli cells grown on a D2O-containing minimal medium. J Biomol NMR 17:33–42
   PubMed Web of Science ®Google Scholar
• Hoffman JM, Habecker CN, Pietruszkiewicz AM, Bolhofer WA, Cragoe EJ Jr, Torchiana ML, Hirschmann R. 1983. A deuterium isotope effect on the inhibition of gastric secretion by N,N-dimethyl-N′-[2-(diisopropylamino)ethyl]-N′-(4,6-dimethyl-2-pyridyl)urea. Synthesis of metabolites. J Med Chem 26:1650–1653
   PubMed Web of Science ®Google Scholar
• Holding AFC, Ross WA. 1958. The laboratory preparation of lithium deuteride and lithium aluminium deuteride, J Appl Chem 8:321–324
   Google Scholar
• Hori Y, Demura M, Iwadate M, Ulrich AS, Niidome T, Aoyagi H, Asakura T. 2001. Interaction of mastoparan with membranes studied by 1H-NMR spectroscopy in detergent micelles and by solid-state 2H-NMR and 15N-NMR spectroscopy in oriented lipid bilayers. Eur J Biochem 268:302–309
   PubMedGoogle Scholar
• Horst R, Horwich AL, Wüthrich K. 2011. Translational diffusion of macromolecular assemblies measured using transverse-relaxation-optimized pulsed field gradient NMR. J Am Chem Soc 133:16354–16357
   PubMed Web of Science ®Google Scholar
• Horst R, Stanczak P, Serrano P, Wüthrich K. 2012. Translational diffusion measurements by microcoil NMR in aqueous solutions of the Fos-10 detergent-solubilized membrane protein OmpX. J Phys Chem B 116:6775–6780
   PubMed Web of Science ®Google Scholar
• Howell SC, Mesleh MF, Opella SJ. 2005. NMR structure determination of a membrane protein with two transmembrane helices in micelles: MerF of the bacterial mercury detoxification system. Biochemistry 44:5196–5206
   PubMed Web of Science ®Google Scholar
• Hsiao CY, Ottaway CA, Wetlaufer DB. 1974. Preparation of fully deuterated fatty acids by simple method. Lipids 9:913–915
   PubMed Web of Science ®Google Scholar
• Huang C, Mohanty S, Banerjee M. 2010. A novel method of production and biophysical characterization of the catalytic domain of yeast oligosaccharyl transferase. Biochemistry 49:1115–1126
   PubMed Web of Science ®Google Scholar
• Hwang PM, Choy WY, Lo EI, Chen L, Forman-Kay JD, Raetz CR, et al. 2002. Solution structure and dynamics of the outer membrane enzyme PagP by NMR. Proc Natl Acad Sci USA 99:13560–13565
   PubMed Web of Science ®Google Scholar
• Imai S, Osawa M, Takeuchi K, Shimada I. 2010. Structural basis underlying the dual gate properties of KcsA. Proc Natl Acad Sci USA 107:6216–6221
   PubMed Web of Science ®Google Scholar
• Inagaki S, Ghirlando R, Grisshammer R. 2013. Biophysical characterization of membrane proteins in nanodiscs. Methods 59:287–300
   PubMed Web of Science ®Google Scholar
• Isaacs NS. Physical organic chemistry. New York: Longman; 1987
   Google Scholar
• Jaremko L, Jaremko M, Giller K, Becker S, Zweckstetter M. 2014. Structure of the mitochondrial translocator protein in complex with a diagnostic ligand. Science 343:1363–1366
   PubMed Web of Science ®Google Scholar
• Kalverda AP, Gowdy J, Thompson GS, Homans SW, Henderson PJ, Patching SG. 2014. TROSY NMR with a 52 kDa sugar transport protein and the binding of a small-molecule inhibitor. Mol Membr Biol 31:131–140
   PubMed Web of Science ®Google Scholar
• Kang HJ, Lee C, Drew D. 2013. Breaking the barriers in membrane protein crystallography. Int J Biochem Cell Biol 45:636–644
   PubMed Web of Science ®Google Scholar
• Katz JJ. 1965. Chemical and biological studies with deuterium. Pennsylvania: Pennsylvania State University, University Park. 1–100
   Google Scholar
• Keana JF, Roman RB. 1978. Improved synthesis of n-octyl-beta-D-glucoside: a nonionic detergent of considerable potential in membrane biochemistry. Membr Biochem 1:323–327
   PubMed Web of Science ®Google Scholar
• Kelly SM, Price NC. 2000. The use of circular dichroism in the investigation of protein structure and function. Curr Protein Pept Sci 1:349–384
   PubMed Web of Science ®Google Scholar
• Kim HJ, Howell SC, Van Horn WD, Jeon YH, Sanders CR. 2009. Recent advances in the application of solution NMR spectroscopy to multi-span integral membrane proteins. Prog Nucl Magn Reson Spectrosc 55:335–360
   PubMed Web of Science ®Google Scholar
• Klammt C, Schwarz D, Fendler K, Haase W, Dötsch V, Bernhard F. 2005. Evaluation of detergents for the soluble expression of alpha-helical and beta-barrel-type integral membrane proteins by a preparative scale individual cell-free expression system. FEBS J 272:6024–6038
   PubMed Web of Science ®Google Scholar
• Klammt C, Maslennikov I, Bayrhuber M, Eichmann C, Vajpai N, Chiu EJ, et al. 2012. Facile backbone structure determination of human membrane proteins by NMR spectroscopy. Nat Methods 9:834–839
   PubMed Web of Science ®Google Scholar
• Koch HJ, Stuart RS. 1978. The synthesis of per-C-deuterated D-glucose. Carbohyd Res 64:127–134
   Web of Science ®Google Scholar
• Korchuganov DS, Gagnidze IE, Tkach EN, Schulga AA, Kirpichnikov MP, Arseniev AS. 2004. Determination of protein rotational correlation time from NMR relaxation data at various solvent viscosities. J Biomol NMR 30:431–442
   PubMed Web of Science ®Google Scholar
• Krueger-Koplin RD, Sorgen PL, Krueger-Koplin ST, Rivera-Torres IO, Cahill SM, Hicks DB, et al. 2004. An evaluation of detergents for NMR structural studies of membrane proteins. J Biomol NMR 28:43–57
   PubMed Web of Science ®Google Scholar
• Krumbiegel P. 2011. Large deuterium isotope effects and their use: a historical review. Isotopes Environ Health Stud 47:1–17
   PubMed Web of Science ®Google Scholar
• Lee D, Hilty C, Wider G, Wüthrich K. 2006. Effective rotational correlation times of proteins from NMR relaxation interference. J Magn Reson 178:72–76
   PubMed Web of Science ®Google Scholar
• Leitch LC, Morse AT. 1952. Synthesis of organic deuterium compounds III. 1,2-dibromoethane-d and its derivatives. Can J Chem 30:924–932
   Web of Science ®Google Scholar
• le Maire M, Champeil P, Moller JV. 2000. Interaction of membrane proteins and lipids with solubilizing detergents. Biochim Biophys Acta 1508:86–111
   PubMed Web of Science ®Google Scholar
• Liang B, Tamm LK. 2007. Structure of outer membrane protein G by solution NMR spectroscopy. Proc Natl Acad Sci USA 104:16140–16145
   PubMed Web of Science ®Google Scholar
• Lin SH, Guidotti G. 2009. Purification of membrane proteins. Methods Enzymol 463:619–629
   PubMed Web of Science ®Google Scholar
• Linke D 2009. Detergents: an overview. Methods Enzymol 463:603–617
   PubMed Web of Science ®Google Scholar
• Liu L, Westler WM, den Boon JA, Wang X, Diaz A, Steinberg HA, Ahlquist P. 2009. An amphipathic alpha-helix controls multiple roles of brome mosaic virus protein 1a in RNA replication complex assembly and function. PLoS Pathog 5:e1000351
   PubMed Web of Science ®Google Scholar
• Magolda RL, Johnson PR. 1985. A new efficient and versatile synthesis of alkyl phosphorylcholines. Tet Lett 26:1167–1170
   Web of Science ®Google Scholar
• Manley PW, Blasco F, Mestan J, Aichholz R. 2013. The kinetic deuterium isotope effect as applied to metabolic deactivation of imatinib to the des-methyl metabolite, CGP74588. Bioorg Med Chem 21:3231–3239
   PubMed Web of Science ®Google Scholar
• Maslennikov I, Kefala G, Johnson C, Riek R, Choe S, Kwiatkowski W. 2007. NMR spectroscopic and analytical ultracentrifuge analysis of membrane protein detergent complexes. BMC Struct Biol 7:74
   PubMed Web of Science ®Google Scholar
• Maslennikov I, Choe S. 2013. Advances in NMR structures of integral membrane proteins. Curr Opin Struct Biol 23:555–562
   PubMed Web of Science ®Google Scholar
• Matsuo K, Gekko K. 2013. Circular-dichroism and synchrotron-radiation circular-dichroism spectroscopy as tools to monitor protein structure in a lipid environment. Methods Mol Biol 974:151–176
   PubMedGoogle Scholar
• Mészáros R, Varga I, Gilányi T. 2005. Effect of polymer molecular weight on the polymer/surfactant interaction. J Phys Chem B 109:13538–13544
   PubMed Web of Science ®Google Scholar
• Meyer A, Dierks K, Hussein R, Brillet K, Brognaro H, Betzel C. 2015. Systematic analysis of protein-detergent complexes applying dynamic light scattering to optimize solutions for crystallization trials. Acta Crystallogr F Struct Biol Commun 71(Pt 1):75–81
   PubMed Web of Science ®Google Scholar
• Miles AJ, Wallace BA. 2006. Synchrotron radiation circular dichroism spectroscopy of proteins and applications in structural and functional genomics. Chem Soc Rev 35:39–51
   PubMed Web of Science ®Google Scholar
• Miskolzie M, Lucyk S, Kotovych G. 2003. NMR conformational studies of micelle-bound orexin-B: a neuropeptide involved in the sleep/awake cycle and feeding regulation. J Biomol Struct Dyn 21:341–351
   PubMed Web of Science ®Google Scholar
• Mitsuda Y, Kono J. 2012. Anionic surfactant compositions with good fluidity and storage stability. Japan patent 2012092163
   Google Scholar
• Mittermaier A, Kay LE. 2002. Effect of deuteration on some structural parameters of methyl groups in proteins as evaluated by residual dipolar couplings. J Biomol NMR 23:35–45
   PubMed Web of Science ®Google Scholar
• Miyamoto K, Togiya K. 2011. Solution structure of LC4 transmembrane segment of CCR5. PLoS One 6:e20452
   PubMed Web of Science ®Google Scholar
• Montserret R, Saint N, Vanbelle C, Salvay AG, Simorre JP, Ebel C, Sapay N, et al. 2010. NMR structure and ion channel activity of the p7 protein from hepatitis C virus. J Biol Chem 285:31446–31461
   PubMed Web of Science ®Google Scholar
• Moreland JL, Gramada A, Buzko OV, Zhang Q, Bourne PE. 2005. The Molecular Biology Toolkit (MBT): a modular platform for developing molecular visualization applications. BMC Bioinformatics 6:21
   PubMed Web of Science ®Google Scholar
• Murad S, Chen RH, Kishimoto Y. 1977. alpha-Hydroxylation of fatty acids in brain. Substrate specificity and deuterium isotope effect. J Biol Chem 252:5206–5210
   PubMed Web of Science ®Google Scholar
• Nadeau VG, Rath A, Deber CM. 2012. Sequence hydropathy dominates membrane protein response to detergent solubilization. Biochemistry 51:6228–6237
   PubMed Web of Science ®Google Scholar
• Nadezhdin KD, Bocharova OV, Bocharov EV, Arseniev AS. 2011. Structural and dynamic study of the transmembrane domain of the amyloid precursor protein. Acta Naturae 3:69–76
   PubMed Web of Science ®Google Scholar
• Nadezhdin KD, Bocharova OV, Bocharov EV, Arseniev AS. 2012. Dimeric structure of transmembrane domain of amyloid precursor protein in micellar environment. FEBS Lett 586:1687–1692
   PubMed Web of Science ®Google Scholar
• Neale C, Ghanei H, Holyoake J, Bishop RE, Privé GG, Pomès R. 2013. Detergent-mediated protein aggregation. Chem Phys Lipids 169:72–84
   PubMed Web of Science ®Google Scholar
• Newstead S, Ferrandon S, Iwata S. 2008. Rationalizing alpha-helical membrane protein crystallization. Protein Sci 17:466–472
   PubMed Web of Science ®Google Scholar
• Nietlispach D, Gautier A. 2011. Solution NMR studies of polytopic α-helical membrane proteins. Curr Opin Struct Biol 21:497–508
   PubMed Web of Science ®Google Scholar
• Oliver RC, Lipfert J, Fox DA, Lo RH, Doniach S, Columbus L. 2013. Dependence of micelle size and shape on detergent alkyl chain length and head group. PLoS One 8:e62488
   PubMed Web of Science ®Google Scholar
• O’Malley MA, Helgeson ME, Wagner NJ, Robinson AS. 2011. Toward rational design of protein detergent complexes: determinants of mixed micelles that are critical for the in vitro stabilization of a G-protein coupled receptor. Biophys J 101:1938–1948
   PubMed Web of Science ®Google Scholar
• O’Neil JD, Sykes BD. 1989. Side-chain dynamics of a detergent-solubilized membrane protein: measurement of tryptophan and glutamine hydrogen-exchange rates in M13 coat protein by 1H NMR spectroscopy. Biochemistry 28:6736–6345
   PubMed Web of Science ®Google Scholar
• Orädd G, Lindblom G, Arvidson G, Gunnarsson K. 1995. Phase equilibria and molecular packing in the N,N-dimethyldodecylamine oxide/gramicidin D/water system studied by 2H nuclear magnetic resonance spectroscopy. Biophys J 68:547–557
   PubMed Web of Science ®Google Scholar
• OuYang B, Xie S, Berardi MJ, Zhao X, Dev J, Yu W, et al. 2013. Unusual architecture of the p7 channel from hepatitis C virus. Nature 498:521–525
   PubMed Web of Science ®Google Scholar
• Oxenoid K, Chou JJ. 2005. The structure of phospholamban pentamer reveals a channel-like architecture in membranes. Proc Natl Acad Sci USA 102:10870–10875
   PubMed Web of Science ®Google Scholar
• Page RC, Moore JD, Nguyen HB, Sharma M, Chase R, Gao FP, et al. 2006. Comprehensive evaluation of solution nuclear magnetic resonance spectroscopy sample preparation for helical integral membrane proteins. J Struct Funct Genomics 7:51–64
   PubMedGoogle Scholar
• Pagliano C, Barera S, Chimirri F, Saracco G, Barber J. 2012. Comparison of the α and β isomeric forms of the detergent n-dodecyl-D-maltoside for solubilizing photosynthetic complexes from pea thylakoid membranes. Biochim Biophys Acta 1817:1506–1515
   PubMed Web of Science ®Google Scholar
• Parker JL, Newstead S. 2012. Current trends in α-helical membrane protein crystallization: an update. Protein Sci 21:1358–1365
   PubMed Web of Science ®Google Scholar
• Pascal RA, Baum MW, Wagner CK, Rodgers LR, Huang DS. 1986. Measurement of deuterium kinetic isotope effects in organic and biochemical reactions by natural abundance deuterium NMR spectroscopy. J Am Chem Soc 108:6477–6482
   Web of Science ®Google Scholar
• Patching SG. 2011. NMR structures of polytopic integral membrane proteins. Mol Membr Biol 28:370–397
   PubMed Web of Science ®Google Scholar
• Patching SG, Edara S, Ma P, Nakayama J, Hussain R, Siligardi G, Phillips-Jones MK. 2012. Interactions of the intact FsrC membrane histidine kinase with its pheromone ligand GBAP revealed through synchrotron radiation circular dichroism. Biochim Biophys Acta 1818:1595–1602
   PubMed Web of Science ®Google Scholar
• Patzelt H, Simon B, terLaak A, Kessler B, Kühne R, Schmieder P, Oesterhelt D, Oschkinat H. 2002. The structures of the active center in dark-adapted bacteriorhodopsin by solution-state NMR spectroscopy. Proc Natl Acad Sci USA 99:9765–9770
   PubMed Web of Science ®Google Scholar
• Pautsch A, Schulz GE. 1998. Structure of the outer membrane protein A transmembrane domain. Nat Struct Biol 5:1013–1017
   PubMedGoogle Scholar
• Pautsch A, Schulz GE. 2000. High-resolution structure of the OmpA membrane domain. J Mol Biol 298:273–282
   PubMed Web of Science ®Google Scholar
• Pebay-Peyroula E, Garavito RM, Rosenbusch JP, Zulauf M, Timmins PA. 1995. Detergent structure in tetragonal crystals of OmpF porin. Structure 3:1051–1059
   PubMed Web of Science ®Google Scholar
• Pedras MS, Minic Z, Sarma-Mamillapalle VK. 2011. Brassinin oxidase mediated transformation of the phytoalexin brassinin: structure of the elusive co-product, deuterium isotope effect and stereoselectivity. Bioorg Med Chem 19:1390–1399
   PubMed Web of Science ®Google Scholar
• Persky A, Kuppermann A. 1974. An apparatus for the production of high isotopic purity deuterium, J Phys E: Scientific Instruments 7:889–890
   Google Scholar
• Popot JL. 2010. Amphipols, nanodiscs, and fluorinated surfactants: three nonconventional approaches to studying membrane proteins in aqueous solutions. Annu Rev Biochem 79:737–775
   PubMed Web of Science ®Google Scholar
• Postis VL, Deacon SE, Roach PC, Wright GS, Xia X, Ingram JC, et al. 2008. A high-throughput assay of membrane protein stability. Mol Membr Biol 25:617–624
   PubMed Web of Science ®Google Scholar
• Privé GG. 2007. Detergents for the stabilization and crystallization of membrane proteins. Methods 41:388–397
   PubMed Web of Science ®Google Scholar
• Raman P, Cherezov V, Caffrey M. 2006. The Membrane Protein Data Bank. Cell Mol Life Sci 63:36–51
   PubMed Web of Science ®Google Scholar
• Reardon PN, Sage H, Dennison SM, Martin JW, Donald BR, Alam SM, et al. 2014. Structure of an HIV-1-neutralizing antibody target, the lipid-bound gp41 envelope membrane proximal region trimer. Proc Natl Acad Sci USA 111:1391–1396
   PubMed Web of Science ®Google Scholar
• Reckel S, Hiller. 2013. Perspectives of solution NMR spectroscopy for structural and functional studies of integral membrane proteins. Molec Phys 111:843–849
   Web of Science ®Google Scholar
• Renaud, RN, Leitch LC. 1968. Reinvestigation of the Polonovski reaction. Synthesis of deuterated dimethylamine and formaldehyde. Can J Chem 46:385–390
   Web of Science ®Google Scholar
• Roche J, Louis JM, Grishaev A, Ying J, Bax A. 2014. Dissociation of the trimeric gp41 ectodomain at the lipid-water interface suggests an active role in HIV-1 Env-mediated membrane fusion. Proc Natl Acad Sci USA 111:3425–3430
   PubMed Web of Science ®Google Scholar
• Roosild TP, Greenwald J, Vega M, Castronovo S, Riek R, Choe S. 2005. NMR structure of Mistic, a membrane-integrating protein for membrane protein expression. Science 307:1317–1321
   PubMed Web of Science ®Google Scholar
• Rouse SL, Marcoux J, Robinson CV, Sansom MS. 2013. Dodecyl maltoside protects membrane proteins in vacuo. Biophys J 105:648–656
   PubMed Web of Science ®Google Scholar
• Rosevear P, VanAken T, Baxter J, Ferguson-Miller S. 1980. Alkyl glycoside detergents: a simpler synthesis and their effects on kinetic and physical properties of cytochrome c oxidase. Biochemistry 19:4108–4115
   PubMed Web of Science ®Google Scholar
• Saunders WH Jr, Edison DH. 1960. Mechanisms of elimination reactions. IV. Deuterium isotope effects in E2 reactions of some 2-phenylethyl derivatives. J Am Chem Soc 82:138–142
   Web of Science ®Google Scholar
• Schubert M, Kolbe M, Kessler B, Oesterhelt D, Schmieder P. 2002. Heteronuclear multidimensional NMR spectroscopy of solubilized membrane proteins: resonance assignment of native bacteriorhodopsin. Chembiochem 3:1019–1023
   PubMed Web of Science ®Google Scholar
• Seddon AM, Curnow P, Booth PJ. 2004. Membrane proteins, lipids and detergents: not just a soap opera. Biochim Biophys Acta 1666:105–117
   PubMed Web of Science ®Google Scholar
• Shao L, Hewitt MC. 2010. The kinetic isotope effect in the search for deuterated drugs. Drug News Perspect 23:398–404
   PubMedGoogle Scholar
• Sharma R, Strelevitz TJ, Gao H, Clark AJ, Schildknegt K, Obach RS, Ripp SL, Spracklin DK, Tremaine LM, Vaz AD. 2012. Deuterium isotope effects on drug pharmacokinetics. I. System-dependent effects of specific deuteration with aldehyde oxidase cleared drugs. Drug Metab Dispos 40:625–634
   PubMed Web of Science ®Google Scholar
• Shenkarev ZO, Paramonov AS, Lyukmanova EN, Shingarova LN, Yakimov SA, Dubinnyi MA, et al. 2010. NMR structural and dynamical investigation of the isolated voltage-sensing domain of the potassium channel KvAP: implications for voltage gating. J Am Chem Soc 132:5630–5637
   PubMed Web of Science ®Google Scholar
• Siligardi G, Hussain R, Patching SG, Phillips-Jones MK. 2014. Ligand- and drug-binding studies of membrane proteins revealed through circular dichroism spectroscopy. Biochim Biophys Acta 1838(1 Pt A):34–42
   PubMed Web of Science ®Google Scholar
• Simmons EM, Hartwig JF. 2012. On the interpretation of deuterium kinetic isotope effects in C-H bond functionalizations by transition-metal complexes. Angew Chem Int Ed 51:3066–3072
   PubMed Web of Science ®Google Scholar
• Slotboom DJ, Duurkens RH, Olieman K, Erkens GB. 2008. Static light scattering to characterize membrane proteins in detergent solution. Methods 46:73–82
   PubMed Web of Science ®Google Scholar
• Sonoda Y, Newstead S, Hu NJ, Alguel Y, Nji E, Beis K, et al. 2011. Benchmarking membrane protein detergent stability for improving throughput of high-resolution X-ray structures. Structure 19:17–25
   PubMed Web of Science ®Google Scholar
• Stanczak P, Horst R, Serrano P, Wüthrich K. 2009. NMR characterization of membrane protein-detergent micelle solutions by use of microcoil equipment. J Am Chem Soc 131:18450–18456
   PubMed Web of Science ®Google Scholar
• Stanczak P, Zhang Q, Horst R, Serrano P, Wüthrich K. 2012. Micro-coil NMR to monitor optimization of the reconstitution conditions for the integral membrane protein OmpW in detergent micelles. J Biomol NMR 54:129–133
   PubMed Web of Science ®Google Scholar
• Takei K, Tsuto K, Miyamoto S, Wakatsuki J. 1985. Anionic surfactants: lauric products. J Am Oil Chem Soc 62:341–347
   Web of Science ®Google Scholar
• Takeuchi K, Takahashi H, Kawano S, Shimada I. 2007. Identification and characterization of the slowly exchanging pH-dependent conformational rearrangement in KcsA. J Biol Chem 282:15179–15186
   PubMed Web of Science ®Google Scholar
• Tang P, Simplaceanu V, Xu Y. 1999. Structural consequences of anesthetic and nonimmobilizer interaction with gramicidin A channels. Biophys J 76:2346–2350
   PubMed Web of Science ®Google Scholar
• Tate CG. 2010. Practical considerations of membrane protein instability during purification and crystallisation. Methods Mol Biol 601:187–203
   PubMedGoogle Scholar
• Teriete P, Franzin CM, Choi J, Marassi FM. 2007. Structure of the Na,K-ATPase regulatory protein FXYD1 in micelles. Biochemistry 46:6774–6783
   PubMed Web of Science ®Google Scholar
• Thomas AF. 1971. Deuterium labeling in organic chemistry. New York: Appleton-Century
   Google Scholar
• Timmins GS. 2014. Deuterated drugs: where are we now? Expert Opin Ther Pat 24:1067–1075
   PubMed Web of Science ®Google Scholar
• Török Z, Szalontai B, Joó F, Wistrom CA, Vigh L. 1993. Homogeneous catalytic deuteration of fatty acyl chains as a tool to detect lipid phase transitions in specific membrane domains: a Fourier Transform Infrared spectroscopic study. Biochem Biophys Res Commun 192:518–524
   PubMed Web of Science ®Google Scholar
• Tulumello DV, Deber CM. 2012. Efficiency of detergents at maintaining membrane protein structures in their biologically relevant forms. Biochim Biophys Acta 1818:1351–1358
   PubMed Web of Science ®Google Scholar
• Ujwal R, Cascio D, Colletier JP, Faham S, Zhang J, Toro L, et al. 2008. The crystal structure of mouse VDAC1 at 2.3 Å resolution reveals mechanistic insights into metabolite gating. Proc Natl Acad Sci USA 105:17742–17747
   PubMed Web of Science ®Google Scholar
• Urey HC, Brickwedde FG, Murphy GM. 1932. A hydrogen isotope of mass 2 and its concentration. Phys Rev 39:164
   Google Scholar
• Vacklin HP, Tiberg F, Thomas RK. 2005a. Formation of supported phospholipid bilayers via co-adsorption with beta-D-dodecyl maltoside. Biochim Biophys Acta – Biomembranes 1668:17–24
   PubMed Web of Science ®Google Scholar
• Vacklin HP, Tiberg F, Fragneto G, Thomas RK. 2005b. Composition of supported model membranes determined by neutron reflection. Langmuir 21:2827–2837
   PubMed Web of Science ®Google Scholar
• van Heyningen WE, Rittenberg D, Schoenheimer R. 1938. The preparation of fatty acids containing deuterium. J Biol Chem 125:495–500
   Google Scholar
• Van Horn WD, Kim HJ, Ellis CD, Hadziselimovic A, Sulistijo ES, Karra MD, et al. 2009. Solution nuclear magnetic resonance structure of membrane-integral diacylglycerol kinase. Science 324:1726–1729
   PubMed Web of Science ®Google Scholar
• Vergis JM, Purdy MD, Wiener MC. 2010. A high-throughput differential filtration assay to screen and select detergents for membrane proteins. Anal Biochem 407:1–11
   PubMed Web of Science ®Google Scholar
• Vostrikov VV, Mote KR, Verardi R, Veglia G. 2013. Structural dynamics and topology of phosphorylated phospholamban homopentamer reveal its role in the regulation of calcium transport. Structure 21:2119–2130
   PubMed Web of Science ®Google Scholar
• Wade D. 1999. Deuterium isotope effects on noncovalent interactions between molecules. Chem Biol Interact 117:191–217
   PubMed Web of Science ®Google Scholar
• Walther R, Fahlbusch K, Sievert R, Gottschalk G. 1981. Formation of trideuteromethane from deuterated trimethylamine or methylamine by Methanosarcina barkeri. J Bacteriol 148:371–373
   PubMed Web of Science ®Google Scholar
• Ward A, Sanderson NM, O’Reilly J, Rutherford NG, Poolman B, Henderson PJF. 2000. The amplified expression, identification, purification, assay and properties of hexahistidine-tagged bacterial membrane transport proteins. In: Baldwin SA, editor. Membrane transport – a practical approach. Oxford: Blackwell. pp. 141–166
   Google Scholar
• Warschawski DE, Arnold AA, Beaugrand M, Gravel A, Chartrand É, Marcotte I. 2011. Choosing membrane mimetics for NMR structural studies of transmembrane proteins. Biochim Biophys Acta 1808:1957–1974
   PubMed Web of Science ®Google Scholar
• Washburn EW, Urey HC. 1932. Concentration of the H isotope of hydrogen by the fractional electrolysis of water. Proc Natl Acad Sci USA 18:496–498
   PubMedGoogle Scholar
• Westheimer FH 1961. The magnitude of the primary kinetic isotope effect for compounds of hydrogen and deuterium. Chem Rev 61:265–273
   Web of Science ®Google Scholar
• White RD, Gandolfi AJ, Bowden GT, Sipes IG. 1983. Deuterium isotope effect on the metabolism and toxicity of 1,2-dibromoethane. Toxicol Appl Pharmacol 69:170–178
   PubMed Web of Science ®Google Scholar
• Wiberg KB. 1955. The deuterium isotope effect. Chem Rev 55:713–743
   Web of Science ®Google Scholar
• Yamamoto G. 2000. Preparation of sulfuric acid esters for anionic surfactants. Japan patent 2000247947
   Google Scholar
• Yang CS, Ishizaki H. 1992. Deuterium isotope effect on the metabolism of N-nitrosodimethylamine and related compounds by cytochrome P4502E1. Xenobiotica 22:1165–1173
   PubMed Web of Science ®Google Scholar
• Yao S, Weber DK, Separovic F, Keizer DW. 2014. Measuring translational diffusion coefficients of peptides and proteins by PFG-NMR using band-selective RF pulses. Eur Biophys J 2014;43:331–339
   Google Scholar
• Yeh AP, McMillan A, Stowell MH. 2006. Rapid and simple protein-stability screens: application to membrane proteins. Acta Crystallogr D Biol Crystallogr 62(Pt 4):451–457
   PubMedGoogle Scholar
• Yoshimura Y, Shimizu H, Hiroshi Hinoub H, Nishimura S-I. 2005. A novel glycosylation concept; microwave-assisted acetal-exchange type glycosylations from methyl glycosides as donors. Tet Lett 46:4701–4705
   Web of Science ®Google Scholar
• Yu PH, Durden DA, Davis BA, Boulton AA. 1987. Deuterium isotope effect in gamma-aminobutyric acid transamination: determination of rate-limiting step. J Neurochem 48:440–446
   PubMed Web of Science ®Google Scholar
• Yu L, Sun C, Song D, Shen J, Xu N, Gunasekera A, et al. 2005. Nuclear magnetic resonance structural studies of a potassium channel-charybdotoxin complex. Biochemistry 44:15834–15841
   PubMed Web of Science ®Google Scholar
• Zhang Q, Horst R, Geralt M, Ma X, Hong WX, Finn MG, et al. 2008. Microscale NMR screening of new detergents for membrane protein structural biology. J Am Chem Soc 130:7357–7363
   PubMed Web of Science ®Google Scholar
• Zhou FX, Cocco MJ, Russ WP, Brunger AT, Engelman DM. 2000. Interhelical hydrogen bonding drives strong interactions in membrane proteins. Nat Struct Biol 7:154–160
   PubMedGoogle Scholar
• Zhou Y, Cierpicki T, Jimenez RH, Lukasik SM, Ellena JF, Cafiso DS, et al. 2008. NMR solution structure of the integral membrane enzyme DsbB: functional insights into DsbB-catalyzed disulfide bond formation. Mol Cell 31:896–908
   PubMed Web of Science ®Google Scholar
• Zhou HX, Cross TA. 2013. Influences of membrane mimetic environments on membrane protein structures. Annu Rev Biophys 42:361–392
   PubMed Web of Science ®Google Scholar
• Zoonens M, Popot JL. 2014. Amphipols for each season. J Membr Biol 247:759–796
   PubMed Web of Science ®Google Scholar