Hostname: page-component-745bb68f8f-g4j75 Total loading time: 0 Render date: 2025-01-27T13:53:01.343Z Has data issue: false hasContentIssue false
  • English
  • Français

Nuclear magnetic resonance (NMR) applied to membrane–protein complexes

Published online by Cambridge University Press:  08 August 2016

Mohammed Kaplan ,
Cecilia Pinto ,
Klaartje Houben  and
Marc Baldus
Mohammed Kaplan
Affiliation:
NMR Spectroscopy Research Group, Bijvoet Center for Biomolecular Research, Utrecht University, Utrecht, The Netherlands
Cecilia Pinto
Affiliation:
NMR Spectroscopy Research Group, Bijvoet Center for Biomolecular Research, Utrecht University, Utrecht, The Netherlands
Klaartje Houben
Affiliation:
NMR Spectroscopy Research Group, Bijvoet Center for Biomolecular Research, Utrecht University, Utrecht, The Netherlands
Marc Baldus*
Affiliation:
NMR Spectroscopy Research Group, Bijvoet Center for Biomolecular Research, Utrecht University, Utrecht, The Netherlands
*
*Author for correspondence: M. Baldus, NMR Spectroscopy Research Group, Bijvoet Center for Biomolecular Research, Utrecht University, Utrecht, The Netherlands. Tel.: +31-30253 3801; Fax: +31-30253 7623; Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Increasing evidence suggests that most proteins occur and function in complexes rather than as isolated entities when embedded in cellular membranes. Nuclear magnetic resonance (NMR) provides increasing possibilities to study structure, dynamics and assembly of such systems. In our review, we discuss recent methodological progress to study membrane–protein complexes (MPCs) by NMR, starting with expression, isotope-labeling and reconstitution protocols. We review approaches to deal with spectral complexity and limited spectral spectroscopic sensitivity that are usually encountered in NMR-based studies of MPCs. We highlight NMR applications in various classes of MPCs, including G-protein-coupled receptors, ion channels and retinal proteins and extend our discussion to protein–protein complexes that span entire cellular compartments or orchestrate processes such as protein transport across or within membranes. These examples demonstrate the growing potential of NMR-based studies of MPCs to provide critical insight into the energetics of protein–ligand and protein–protein interactions that underlie essential biological functions in cellular membranes.

Type
Review
Information
Quarterly Reviews of Biophysics , Volume 49 , 2016 , e15
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ader, C., Pongs, O., Becker, S. & Baldus, M. (2010). Protein dynamics detected in a membrane-embedded potassium channel using two-dimensional solid-state NMR spectroscopy. Biochimica Et Biophysica Acta (BBA) – Biomembranes 1798, 286–290.CrossRefGoogle Scholar
Ader, C., Schneider, R., Hornig, S., Velisetty, P., Vardanyan, V., Giller, K., Ohmert, I., Becker, S., Pongs, O. & Baldus, M. (2009). Coupling of activation and inactivation gate in a K+-channel: potassium and ligand sensitivity. EMBO Journal 28, 2825–2834.CrossRefGoogle Scholar
Ader, C., Schneider, R., Hornig, S., Velisetty, P., Wilson, E. M., Lange, A., Giller, K., Ohmert, I., Martin-Eauclaire, M.-F., Trauner, D., Becker, S., Pongs, O. & Baldus, M. (2008). A structural link between inactivation and block of a K+ channel. Nature Structural & Molecular Biology 15, 605–612.CrossRefGoogle ScholarPubMed
Akin, B. L., Hurley, T. D., Chen, Z. & Jones, L. R. (2013). The structural basis for phospholamban inhibition of the calcium pump in sarcoplasmic reticulum. Journal of Biological Chemistry 288, 30181–30191.Google Scholar
Alia, A., Ganapathy, S. & de Groot, H. J. M. (2009). Magic angle spinning (MAS) NMR: a new tool to study the spatial and electronic structure of photosynthetic complexes. Photosynthesis Research 102, 415–425.CrossRefGoogle Scholar
Andreas, L. B., Barnes, A. B., Corzilius, B., Chou, J. J., Miller, E. A., Caporini, M. A., Rosay, M. M. & Griffin, R. G. (2013). Dynamic nuclear polarization study of inhibitor binding to the M218-60 proton transporter from influenza A. Biochemistry 52, 2774–2782.Google Scholar
Andreas, L. B., Reese, M., Eddy, M. T., Gelev, V., Ni, Q. Z., Miller, E. A., Emsley, L., Pintacuda, G., Chou, J. J. & Griffin, R. G. (2015). Structure and mechanism of the influenza A M2 18–60dimer of dimers. Journal of the American Chemical Society 137, 14877–14886.Google Scholar
Andrew, E. R., Bradbury, A. & Eades, R. G. (1958). Nuclear Magnetic Resonance Spectra from a crystal rotated at high speed. Nature 182, 1659.Google Scholar
Andronesi, O. C., Becker, S., Seidel, K., Heise, H., Young, H. S. & Baldus, M. (2005). Determination of membrane protein structure and dynamics by magic-angle-spinning solid-state NMR spectroscopy. Journal of the American Chemical Society 127, 12965–12974.Google Scholar
Asami, S. & Reif, B. (2013). Proton-detected solid-state NMR spectroscopy at aliphatic sites: application to crystalline systems. Accounts of Chemical Research 46, 2089–2097.Google Scholar
Babu, M., Vlasblom, J., Pu, S., Guo, X., Graham, C., Bean, B. D. M., Burston, H. E., Vizeacoumar, F. J., Snider, J., Phanse, S., Fong, V., Tam, Y. Y. C., Davey, M., Hnatshak, O., Bajaj, N., Chandran, S., Punna, T., Christopolous, C., Wong, V., Yu, A., Zhong, G., Li, J., Stagljar, I., Conibear, E., Wodak, S. J., Emili, A. & Greenblatt, J. F. (2012). Interaction landscape of membrane–protein complexes in Saccharomyces cerevisiae . Nature 489, 585–589.Google Scholar
Bajaj, V. S., Mak-Jurkauskas, M. L., Belenky, M., Herzfeld, J. & Griffin, R. G. (2009). Functional and shunt states of bacteriorhodopsin resolved by 250 GHz dynamic nuclear polarization-enhanced solid-state NMR. Proceedings of the National Academy of Sciences of the United States of America 106, 9244–9249.CrossRefGoogle ScholarPubMed
Bakelar, J., Buchanan, S. K. & Noinaj, N. (2016). The structure of the -barrel assembly machinery complex. Science 351, 180–186.Google Scholar
Baker, L. A. & Baldus, M. (2014). Characterization of membrane protein function by solid-state NMR spectroscopy. Current Opinion in Structural Biology 27, 48–55.Google Scholar
Baker, L. A., Daniëls, M., van der Cruijsen, E. A. W., Folkers, G. E. & Baldus, M. (2015). Efficient cellular solid-state NMR of membrane proteins by targeted protein labeling. Journal of Biomolecular NMR 62, 199–208.CrossRefGoogle ScholarPubMed
Baldus, M. (2002). Correlation experiments for assignment and structure elucidation of immobilized polypeptides under magic angle spinning. Progress in Nuclear Magnetic Resonance Spectroscopy 41, 1–47.Google Scholar
Baldus, M. (2015). A solid view of membrane proteins in situ . Biophysical Journal 108, 1585–1586.Google Scholar
Barbieri, L., Bertini, I., Luchinat, E., Secci, E., Zhao, Y., Banci, L. & Aricescu, A. R. (2013). Atomic-resolution monitoring of protein maturation in live human cells by nMr. Nature Chemical Biology 9, 297–299.Google Scholar
Becker-Baldus, J., Bamann, C., Saxena, K., Gustmann, H., Brown, L. J., Brown, R. C. D., Reiter, C., Bamberg, E., Wachtveitl, J., Schwalbe, H. & Glaubitz, C. (2015). Enlightening the photoactive site of channelrhodopsin-2 by DNP-enhanced solid-state NMR spectroscopy. Proceedings of the National Academy of Sciences of the United States of America 112, 9896–9901.CrossRefGoogle ScholarPubMed
Bertrand, K., Reverdatto, S., Burz, D. S., Zitomer, R. & Shekhtman, A. (2012). Structure of proteins in eukaryotic compartments. Journal of the American Chemical Society 134, 12798–12806.Google Scholar
Bessman, N. J., Freed, D. M. & Lemmon, M. A. (2014). Putting together structures of epidermal growth factor receptors. Current Opinion in Structural Biology 29, 95–101.Google Scholar
Bhate, M. P. & Mcdermott, A. E. (2012). Protonation state of E71 in KcsA and its role for channel collapse and inactivation. Proceedings of the National Academy of Sciences of the United States of America 109, 15265–15270.Google Scholar
Bokoch, M. P., Zou, Y., Rasmussen, S. G. F., Liu, C. W., Nygaard, R., Rosenbaum, D. M., Fung, J. J., Choi, H.-J., Thian, F. S., Kobilka, T. S., Puglisi, J. D., Weis, W. I., Pardo, L., Prosser, R. S., Mueller, L. & Kobilka, B. K. (2010). Ligand-specific regulation of the extracellular surface of a G-protein-coupled receptor. Nature 463, 108–112.Google Scholar
Cady, S. D., Schmidt-Rohr, K., Wang, J., Soto, C. S., Degrado, W. F. & Hong, M. (2010). Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers. Nature 463, 689–692.Google Scholar
Chae, P. S., Rasmussen, S. G. F., Rana, R. R., Gotfryd, K., Chandra, R., Goren, M. A., Kruse, A. C., Nurva, S., Loland, C. J., Pierre, Y., Drew, D., Popot, J.-L., Picot, D., Fox, B. G., Guan, L., Gether, U., Byrne, B., Kobilka, B. & Gellman, S. H. (2010). Maltose–neopentyl glycol (MNG) amphiphiles for solubilization, stabilization and crystallization of membrane proteins. Nature Methods 7, 1003–1008.CrossRefGoogle ScholarPubMed
Chakrapani, S., Cordero-Morales, J. F., Jogini, V., Pan, A. C., Cortes, D. M., Roux, B. & Perozo, E. (2011). On the structural basis of modal gating behavior in K(+) channels. Nature Structural & Molecular Biology 18, 67–74.Google Scholar
Cho, M.-K., Gayen, A., Banigan, J. R., Leninger, M. & Traaseth, N. J. (2014). Intrinsic conformational plasticity of native EmrE provides a pathway for multidrug resistance. Journal of the American Chemical Society 136, 8072–8080.CrossRefGoogle ScholarPubMed
Costa, T. R. D., Felisberto-Rodrigues, C., Meir, A., Prevost, M. S., Redzej, A., Trokter, M. & Waksman, G. (2015). Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nature Reviews Microbiology 13, 343–359.CrossRefGoogle ScholarPubMed
Cukkemane, A. & Baldus, M. (2013). Characterization of a cyclic nucleotide-activated K +channel and its lipid environment by using solid-state NMR spectroscopy. Chembiochem: a European Journal of Chemical Biology 14, 1789–1798.Google Scholar
Cukkemane, A., Nand, D., Gradmann, S., Weingarth, M., Kaupp, U. B. & Baldus, M. (2012). Solid-state NMR [13C,15N] resonance assignments of the nucleotide-binding domain of a bacterial cyclic nucleotide-gated channel. Biomolecular NMR Assignments 6, 225–229.Google Scholar
Das, R., Andre, I., Shen, Y., Wu, Y., Lemak, A., Bansal, S., Arrowsmith, C. H., Szyperski, T. & Baker, D. (2009). Simultaneous prediction of protein folding and docking at high resolution. Proceedings of the National Academy of Sciences of the United States of America 106, 18978–18983.Google Scholar
Dominguez, C., Boelens, R. & Bonvin, A. M. (2003). HADDOCK: a protein–protein docking approach based on biochemical or biophysical information. Journal of the American Chemical Society 125, 1731–1737.Google Scholar
Dörr, J. M., Koorengevel, M. C., Schäfer, M., Prokofyev, A. V., Scheidelaar, S., van der Cruijsen, E. A. W., Dafforn, T. R., Baldus, M. & Killian, J. A. (2014). Detergent-free isolation, characterization, and functional reconstitution of a tetrameric K+ channel: the power of native nanodiscs. Proceedings of the National Academy of Sciences of the United States of America 111, 18607–18612.Google Scholar
Dürr, U. H. N., Soong, R. & Ramamoorthy, A. (2013). When detergent meets bilayer: birth and coming of age of lipid bicelles. Progress in Nuclear Magnetic Resonance Spectroscopy 69, 1–22.CrossRefGoogle ScholarPubMed
Egorova-Zachernyuk, T. A., Hollander, J., Fraser, N., Gast, P., Hoff, A. J., Cogdell, R., de Groot, H. J. M. & Baldus, M. (2001). Heteronuclear 2D-correlations in a uniformly [13C, 15N] labeled membrane-protein complex at ultra-high magnetic fields. Journal of Biomolecular NMR 19, 243–253.CrossRefGoogle Scholar
Emami, S., Fan, Y., Munro, R., Ladishansky, V. & Brown, L. S. (2013). Yeast-expressed human membrane protein aquaporin-1 yields excellent resolution of solid-state MAS NMR spectra. Journal of Biomolecular NMR 55, 147–155.Google Scholar
Endres, N. F., Das, R., Smith, A. W., Arkhipov, A., Kovacs, E., Huang, Y., Pelton, J. G., Shan, Y., Shaw, D. E., Wemmer, D. E., Groves, J. T. & Kuriyan, J. (2013). Conformational coupling across the plasma membrane in activation of the EGF receptor. Cell 152, 543–556.Google Scholar
Etzkorn, M., Bockmann, A., Lange, A. & Baldus, M. (2004). Probing molecular interfaces using 2D magic-angle-spinning NMR on protein mixtures with different uniform labeling. Journal of the American Chemical Society 126, 14746–14751.Google Scholar
Etzkorn, M., Kneuper, H., Dünnwald, P., Vijayan, V., Krämer, J., Griesinger, C., Becker, S., Unden, G. & Baldus, M. (2008). Plasticity of the PAS domain and a potential role for signal transduction in the histidine kinase DcuS. Nature Structural & Molecular Biology 15, 1031–1039.Google Scholar
Etzkorn, M., Martell, S., Andronesi, O. C., Seidel, K., Engelhard, M. & Baldus, M. (2007). Secondary structure, dynamics, and topology of a seven-helix receptor in native membranes, studied by solid-state NMR spectroscopy. Angewandte Chemie International Edition in English 46, 459–462.Google Scholar
Etzkorn, M., Seidel, K., Li, L., Martell, S., Geyer, M., Engelhard, M. & Baldus, M. (2010). Complex formation and light activation in membrane-embedded sensory rhodopsin II as seen by solid-state NMR spectroscopy. Structure (London, England: 1993) 18, 293–300.CrossRefGoogle ScholarPubMed
Fricke, P., Mance, D., Chevelkov, V., Giller, K., Becker, S., Baldus, M. & Lange, A. (2016). High resolution observed in 800 MHz DNP spectra of extremely rigid type III secretion needles. Journal of Biomolecular NMR, in press, doi:10.1007/s10858-016-0044-y.Google Scholar
Fu, R., Wang, X., Li, C., Santiago-Miranda, A. N., Pielak, G. J. & Tian, F. (2011). In situ structural characterization of a recombinant protein in native Escherichia coli membranes with solid-state magic-angle-spinning NMR. Journal of the American Chemical Society 133, 12370–12373.Google Scholar
Gatzeva-Topalova, P. Z., Walton, T. A. & Sousa, M. C. (2008). Crystal structure of YaeT: conformational flexibility and substrate recognition. Structure (London, England: 1993) 16, 1873–1881.Google Scholar
Gatzeva-Topalova, P. Z., Warner, L. R., Pardi, A. & Sousa, M. C. (2010). Structure and flexibility of the complete periplasmic domain of BamA: the protein insertion machine of the outer membrane. Structure 18, 1492–1501.Google Scholar
Gayen, A., Banigan, J. R. & Traaseth, N. J. (2013). Ligand-induced conformational changes of the multidrug resistance transporter EmrE probed by oriented solid-state NMR spectroscopy. Angewandte Chemie International Edition in English 52, 10321–10324.Google Scholar
Gayen, A., Leninger, M. & Traaseth, N. J. (2016). Protonation of a glutamate residue modulates the dynamics of the drug transporter EmrE. Nature Chemical Biology 12, 141–145.Google Scholar
Good, D. B., Wang, S., Ward, M. E., Struppe, J., Brown, L. S., Lewandowski, J. R. & Ladizhansky, V. (2014). Conformational dynamics of a seven transmembrane helical protein anabaena sensory rhodopsin probed by solid-state NMR. Journal of the American Chemical Society 136, 2833–2842.Google Scholar
Gopinath, T. & Veglia, G. (2015). Multiple acquisition of magic angle spinning solid-state NMR experiments using one receiver: application to microcrystalline and membrane protein preparations. Journal of Magnetic Resonance 253(C), 143–153.Google Scholar
Goto, N. K. & Kay, L. E. (2000). New developments in isotope labeling strategies for protein solution NMR spectroscopy. Current Opinion in Structural Biology 10, 585–592.Google Scholar
Gradmann, S., Ader, C., Heinrich, I., Nand, D., Dittmann, M., Cukkemane, A., Dijk, M., Bonvin, A. J. J., Engelhard, M. & Baldus, M. (2012). Rapid prediction of multi-dimensional NMR data sets. Journal of Biomolecular NMR 54, 377–387.Google Scholar
Gu, Y., Li, H., Dong, H., Zeng, Y., Zhang, Z., Paterson, N. G., Stansfeld, P. J., Wang, Z., Zhang, Y., Wang, W. & Dong, C. (2016). Structural basis of outer membrane protein insertion by the BAM complex. Nature 531, 64–69.Google Scholar
Gustavsson, M., Verardi, R. & Mullen, D. G. (2013). Allosteric regulation of SERCA by phosphorylation-mediated conformational shift of phospholamban (pp. 1–27). Proceedings of the National Academy of Sciences of the United States of America 110, 17338–17343.Google Scholar
Hagan, C. L., Silhavy, T. J. & Kahne, D. (2011). β-barrel membrane protein assembly by the bam complex. Annual Review of Biochemistry 80, 189–210.Google Scholar
Hamatsu, J., O'Donovan, D., Tanaka, T., Shirai, T., Hourai, Y., Mikawa, T., Ikeya, T., Mishima, M., Boucher, W., Smith, B. O., Laue, E. D., Shirakawa, M. & Ito, Y. (2013). High-resolution heteronuclear multidimensional NMR of proteins in living insect cells using a baculovirus protein expression system. Journal of the American Chemical Society 135, 1688–1691.Google Scholar
Han, B., Liu, Y., Ginzinger, S. & Wishart, D. (2011). SHIFTX2: significantly improved protein chemical shift prediction. Journal of Biomolecular NMR 50, 43–57.CrossRefGoogle ScholarPubMed
Han, L., Zheng, J., Wang, Y., Yang, X., Liu, Y., Sun, C., Cao, B., Zhou, H., Ni, D., Lou, J., Zhao, Y. & Huang, Y. (2016). Structure of the BAM complex and its implications for biogenesis of outer-membrane proteins. Nature Structural & Molecular Biology 23, 192–196.Google Scholar
Havlin, R. H. & Tycko, R. (2005). Probing site-specific conformational distributions in protein folding with solid-state NMR. Proceedings of the National Academy of Sciences of the United States of America 102, 3284–3289.Google Scholar
Hazelbauer, G. L., Falke, J. J. & Parkinson, J. S. (2008). Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends in Biochemical Sciences 33, 9–19.Google Scholar
Heise, H., Luca, S., de Groot, B. L., Grubmüller, H. & Baldus, M. (2005a). Probing conformational disorder in neurotensin by two-dimensional solid-state NMR and comparison to molecular dynamics simulations. Biophysical Journal 89, 2113–2120.CrossRefGoogle ScholarPubMed
Heise, H., Seidel, K., Etzkorn, M., Becker, S. & Baldus, M. (2005b). 3D NMR spectroscopy for resonance assignment and structure elucidation of proteins under MAS: novel pulse schemes and sensitivity considerations. Journal of Magnetic Resonance 173, 64–74.Google Scholar
Hellmich, U. A., Mönkemeyer, L., Velamakanni, S., van Veen, H. W. & Glaubitz, C. (2015). Effects of nucleotide binding to LmrA: a combined MAS-NMR and solution NMR study. Biochimica et Biophysica Acta (BBA) – Biomembranes 1848, 3158–3165.Google Scholar
Herzfeld, J. & Lansing, J. C. (2002). Magnetic resonance studies of the bacteriorhodopsin pump cycle. Annual Review of Biophysics and Biomolecular Structure 31, 73–95.Google Scholar
Higman, V., Flinders, J., Hiller, M., Jehle, S., Markovic, S., Fiedler, S., van Rossum, B.-J. & Oschkinat, H. (2009). Assigning large proteins in the solid state: a MAS NMR resonance assignment strategy using selectively and extensively 13C-labelled proteins. Journal of Biomolecular NMR 44, 245–260.Google Scholar
Hong, M. & Jakes, K. (1999). Selective and extensive C-13 labeling of a membrane protein for solid-state NMR investigations. Journal of Biomolecular NMR 14, 71–74.Google Scholar
Hong, M., Zhang, Y. & Hu, F. (2012). Membrane protein structure and dynamics from NMR spectroscopy. Annual Review of Physical Chemistry 63, 1–24.CrossRefGoogle ScholarPubMed
Hu, F., Luo, W. & Hong, M. (2010). Mechanisms of proton conduction and gating in influenza M2 proton channels from solid-state NMR. Science 330, 505–508.Google Scholar
Huber, M., Hiller, S., Schanda, P., Ernst, M., Böckmann, A., Verel, R. & Meier, B. H. (2011). A proton-detected 4D solid-state NMR experiment for protein structure determination. Chemphyschem 12, 915–918.Google Scholar
Imai, S., Osawa, M., Mita, K., Toyonaga, S., Machiyama, A., Ueda, T., Takeuchi, K., Oiki, S. & Shimada, I. (2012). Functional equilibrium of the KcsA structure revealed by NMR. Journal of Biological Chemistry 287, 39634–39641.CrossRefGoogle ScholarPubMed
Ishii, Y. & Tycko, R. (2000). Sensitivity enhancement in solid state 15N NMR by indirect detection with high-speed magic angle spinning. Journal of Magnetic Resonance 142, 199–204.CrossRefGoogle ScholarPubMed
Jacso, T., Franks, W. T., Rose, H., Fink, U., Broecker, J., Keller, S., Oschkinat, H. & Reif, B. (2012). Characterization of membrane proteins in isolated native cellular membranes by dynamic nuclear polarization solid-state NMR spectroscopy without purification and reconstitution. Angewandte Chemie International Edition in English 51, 432–435.Google Scholar
Jantschke, A., Koers, E., Mance, D., Weingarth, M., Brunner, E. & Baldus, M. (2015). Insight into the supramolecular architecture of intact diatom biosilica from DNP-supported solid-state NMR spectroscopy. Angewandte Chemie International Edition in English 54, 15069–15073.CrossRefGoogle ScholarPubMed
Jelinski, L. W., Sullivan, C. E. & Torchia, D. A. (1980). H-2 NMR-study of molecular-motion in collagen fibrils. Nature 284, 531–534.Google Scholar
Kainosho, M., Torizawa, T., Iwashita, Y., Terauchi, T., Mei Ono, A. & Güntert, P. (2006). Optimal isotope labelling for NMR protein structure determinations. Nature 440, 52–57.CrossRefGoogle ScholarPubMed
Kang, S.-J., Todokoro, Y., Yumen, I., Shen, B., Iwasaki, I., Suzuki, T., Miyagi, A., Yoshida, M., Fujiwara, T. & Akutsu, H. (2014). Active-site structure of the thermophilic Foc-subunit ring in membranes elucidated by solid-state NMR. Biophysical Journal 106, 390–398.Google Scholar
Kaplan, M., Cukkemane, A., van Zundert, G. C. P., Narasimhan, S., Daniëls, M., Mance, D., Waksman, G., Bonvin, A. M. J. J., Fronzes, R., Folkers, G. E. & Baldus, M. (2015). Probing a cell-embedded megadalton protein complex by DNP-supported solid-state NMR. Nature Methods 12, 649–652.Google Scholar
Kim, S., Malinverni, J. C., Sliz, P., Silhavy, T. J., Harrison, S. C. & Kahne, D. (2007). Structure and function of an essential component of the outer membrane protein assembly machine. Science 317, 961–964.Google Scholar
Kimata, N., Reeves, P. J. & Smith, S. O. (2015). Uncovering the triggers for GPCR activation using solid-state NMR spectroscopy. Journal of Magnetic Resonance 253, 111–118.Google Scholar
Kleanthous, C., Rassam, P. & Baumann, C. G. (2015). Protein–protein interactions and the spatiotemporal dynamics of bacterial outer membrane proteins. Current Opinion in Structural Biology 35, 109–115.CrossRefGoogle ScholarPubMed
Knowles, T. J., Jeeves, M., Bobat, S., Dancea, F., McClelland, D., Palmer, T., Overduin, M. & Henderson, I. R. (2008). Fold and function of polypeptide transport-associated domains responsible for delivering unfolded proteins to membranes. Molecular Microbiology 68, 1216–1227.Google Scholar
Koers, E. J., López-Deber, M. P., Weingarth, M., Nand, D., Hickman, D. T., Mlaki Ndao, D., Reis, P., Granet, A., Pfeifer, A., Muhs, A. & Baldus, M. (2013). Dynamic nuclear polarization NMR spectroscopy: revealing multiple conformations in lipid-anchored peptide vaccines. Angewandte Chemie International Edition in English 52, 10905–10908.CrossRefGoogle ScholarPubMed
Koers, E. J., van der Cruijsen, E. A. W., Rosay, M., Weingarth, M., Prokofyev, A., Sauvee, C., Ouari, O., van der Zwan, J., Pongs, O., Tordo, P., Maas, W. E. & Baldus, M. (2014). NMR-based structural biology enhanced by dynamic nuclear polarization at high magnetic field. Journal of Biomolecular NMR 60, 157–168.Google Scholar
Kofuku, Y., Ueda, T., Okude, J., Shiraishi, Y., Kondo, K., Mizumura, T., Suzuki, S. & Shimada, I. (2014). Functional dynamics of deuterated β 2-adrenergic receptor in lipid bilayers revealed by NMR spectroscopy. Angewandte Chemie International Edition in English 53, 13376–13379.CrossRefGoogle ScholarPubMed
Kovacs, E., Zorn, J. A., Huang, Y., Barros, T. & Kuriyan, J. (2015). A structural perspective on the regulation of the epidermal growth factor receptor. Annual Review of Biochemistry 84, 739–764.Google Scholar
Kulminskaya, N. V., Pedersen, M. Ø., Bjerring, M., Underhaug, J., Miller, M., Frigaard, N.-U., Nielsen, J. T. & Nielsen, N. C. (2012). In situ solid-state NMR spectroscopy of protein in heterogeneous membranes: the baseplate antenna complex of Chlorobaculum tepidum. Angewandte Chemie International Edition in English 51, 6891–6895.Google Scholar
Lange, A., Becker, S., Seidel, K., Giller, K., Pongs, O. & Baldus, M. (2005). A concept for rapid protein-structure determination by solid-state NMR spectroscopy. Angewandte Chemie International Edition in English 44, 2089–2092.Google Scholar
Lange, A., Giller, K., Hornig, S., Martin-Eauclaire, M.-F., Pongs, O., Becker, S. & Baldus, M. (2006). Toxin-induced conformational changes in a potassium channel revealed by solid-state NMR. Nature 440, 959–962.Google Scholar
Lange, V., Becker-Baldus, J., Kunert, B., van Rossum, B.-J., Casagrande, F., Engel, A., Roske, Y., Scheffel, F. M., Schneider, E. & Oschkinat, H. (2010). A MAS NMR study of the bacterial ABC transporter ArtMP. Chembiochem: a European Journal of Chemical Biology 11, 547–555.Google Scholar
Lemaster, D. M. & Kushlan, D. M. (1996). Dynamical mapping of E-coli thioredoxin via C-13 NMR relaxation analysis. Journal of the American Chemical Society 118, 9255–9264.Google Scholar
Lemmon, M. A. & Schlessinger, J. (2010). Cell signaling by receptor tyrosine kinases. Cell 141, 1117–1134.Google Scholar
Lewis, B. A., Harbison, G. S., Herzfeld, J. & Griffin, R. G. (1985). NMR structural-analysis of a membrane-protein – bacteriorhodopsin peptide backbone orientation and motion. Biochemistry 24, 4671–4679.Google Scholar
Linden, A. H., Lange, S., Franks, W. T., Akbey, Ü., Specker, E., van Rossum, B.-J. & Oschkinat, H. (2011). Neurotoxin II bound to acetylcholine receptors in native membranes studied by dynamic nuclear polarization NMR. Journal of the American Chemical Society 133, 19266–19269.Google Scholar
Liu, J., Liu, C., Fan, Y., Munro, R. A., Ladishansky, V., Brown, L. S. & Wang, S. (2016). Sparse 13C labelling for solid-state NMR studies of P. pastoris expressed eukaryotic seven-transmembrane proteins. Journal of Biomolecular NMR 65, 7–13.Google Scholar
Liu, J. J., Horst, R., Katritch, V., Stevens, R. C. & Wuthrich, K. (2012). Biased signaling pathways in 2-adrenergic receptor characterized by 19F-NMR. Science 335, 1106–1110.Google Scholar
Lopez, J. J., Shukla, A. K., Reinhart, C., Schwalbe, H., Michel, H. & Glaubitz, C. (2008). The structure of the neuropeptide bradykinin bound to the human G-protein coupled receptor bradykinin B2 as determined by solid-state NMR spectroscopy. Angewandte Chemie International Edition in English 47, 1668–1671.CrossRefGoogle Scholar
Loquet, A., Sgourakis, N. G., Gupta, R., Giller, K., Riedel, D., Goosmann, C., Griesinger, C., Kolbe, M., Baker, D., Becker, S. & Lange, A. (2012). Atomic model of the type III secretion system needle. Nature 486, 276–279.Google Scholar
Low, H. H., Gubellini, F., Rivera-Calzada, A., Braun, N., Connery, S., Dujeancourt, A., Lu, F., Redzej, A., Fronzes, R., Orlova, E. V. & Waksman, G. (2014). Structure of a type IV secretion system. Nature 508, 550–553.Google Scholar
Lowe, I. J. (1959). Free induction decays of rotating solids. Physical Review Letters 2, 285–287.Google Scholar
Luca, S., Filippov, D. V., van Boom, J. H., Oschkinat, H., de Groot, J. & Baldus, M. (2001). Secondary chemical shifts in immobilized peptides and proteins: a qualitative basis for structure refinement under magic angle spinning. Journal of Biomolecular NMR 20, 325–331.CrossRefGoogle ScholarPubMed
Luca, S., White, J. F., Sohal, A. K., Filippov, D. V., van Boom, J. H., Grisshammer, R. & Baldus, M. (2003). The conformation of neurotensin bound to its G protein-coupled receptor. Proceedings of the National Academy of Sciences of the United States of America 100, 10706–10711.Google Scholar
Maciejko, J., Mehler, M., Kaur, J., Lieblein, T., Morgner, N., Ouari, O., Tordo, P., Becker-Baldus, J. & Glaubitz, C. (2015). Visualizing specific cross-protomer interactions in the homo-oligomeric membrane protein proteorhodopsin by dynamic-nuclear-polarization-enhanced solid-state NMR. Journal of the American Chemical Society 137, 9032–9043.Google Scholar
Maeda, S. & Schertler, G. F. (2013). Production of GPCR and GPCR complexes for structure determination. Current Opinion in Structural Biology 23, 381–392.CrossRefGoogle ScholarPubMed
Mak-Jurkauskas, M. L., Bajaj, V. S., Hornstein, M. K., Belenky, M., Griffin, R. G. & Herzfeld, J. (2008). Energy transformations early in the bacteriorhodopsin photocycle revealed by DNP-enhanced solid-state NMR. Proceedings of the National Academy of Sciences of the United States of America 105, 883–888.Google Scholar
Mance, D., Gast, P., Huber, M., Baldus, M. & Ivanov, K. L. (2015a). The magnetic field dependence of cross-effect dynamic nuclear polarization under magic angle spinning. Journal of Chemical Physics 142, 234201.Google Scholar
Mance, D., Sinnige, T., Kaplan, M., Narasimhan, S., Daniëls, M., Houben, K., Baldus, M. & Weingarth, M. (2015b). An efficient labelling approach to harness backbone and side-chain protons in 1H-detected solid-state NMR spectroscopy. Angewandte Chemie International Edition in English 54, 15799–15803.Google Scholar
Mascher, T., Helmann, J. D. & Unden, G. (2006). Stimulus perception in bacterial signal-transducing histidine kinases. Microbiology and Molecular Biology Reviews 70, 910–938.Google Scholar
Mathies, G., Caporini, M. A., Michaelis, V. K., Liu, Y., Hu, K.-N., Mance, D., Zweier, J. L., Rosay, M., Baldus, M. & Griffin, R. G. (2015). Efficient dynamic nuclear polarization at 800 MHz/527 GHz with trityl-nitroxide biradicals. Angewandte Chemie International Edition in English 54, 11770–11776.Google Scholar
Matsushita, C., Tamagaki, H., Miyazawa, Y., Aimoto, S., Smith, S. O. & Sato, T. (2013). Transmembrane helix orientation influences membrane binding of the intracellular juxtamembrane domain in Neu receptor peptides. Proceedings of the National Academy of Sciences of the United States of America 110, 1646–1651.Google Scholar
Mcdermott, A., Zysmilich, M. G. & Polenova, T. (1998). Solid state NMR studies of photoinduced polarization in photosynthetic reaction centers: mechanism and simulations. Solid State Nuclear Magnetic Resonance 11, 21–47.Google Scholar
Mertz, B., Struts, A. V., Feller, S. E. & Brown, M. F. (2012). Molecular simulations and solid-state NMR investigate dynamical structure in rhodopsin activation. Biochimica et Biophysica Acta (BBA) – Biomembranes 1818, 241–251.Google Scholar
Miao, Y. & Cross, T. A. (2013). Solid state NMR and protein–protein interactions in membranes. Current Opinion in Structural Biology 23, 919–928.Google Scholar
Morgado, L., Zeth, K., Burmann, B. M., Maier, T. & Hiller, S. (2015). Characterization of the insertase BamA in three different membrane mimetics by solution NMR spectroscopy. Journal of Biomolecular Nuclear Magnetic Resonance 61, 333–345.Google Scholar
Morrison, E. A., DeKoster, G. T., Dutta, S., Vafabakhsh, R., Clarkson, M. W., Bahl, A., Kern, D., Ha, T. & Henzler-Wildman, K. A. (2011). Antiparallel EmrE exports drugs by exchanging between asymmetric structures. Nature 481, 45–50.Google Scholar
Morrison, E. A. & Henzler-Wildman, K. A. (2014). Transported substrate determines exchange rate in the multidrug resistance transporter EmrE. Journal of Biological Chemistry 289, 6825–6836.Google Scholar
Motlagh, H. N., Wrabl, J. O., Li, J. & Hilser, V. J. (2014). The ensemble nature of allostery. Nature 508, 331–339.CrossRefGoogle ScholarPubMed
Nadaud, P. S., Helmus, J. J., Höfer, N. & Jaroniec, C. P. (2007). Long-range structural restraints in spin-labeled proteins probed by solid-state nuclear magnetic resonance spectroscopy. Journal of the American Chemical Society 129, 7502–7503.CrossRefGoogle ScholarPubMed
Nand, D., Cukkemane, A., Becker, S. & Baldus, M. (2012). Fractional deuteration applied to biomolecular solid-state NMR spectroscopy. Journal of Biomolecular NMR 52, 91–101.CrossRefGoogle ScholarPubMed
Ni, Q. Z., Daviso, E., Can, T. V., Markhasin, E., Jawla, S. K., Swager, T. M., Temkin, R. J., Herzfeld, J. & Griffin, R. G. (2013). High frequency dynamic nuclear polarization. Accounts of Chemical Research 46, 1933–1941.Google Scholar
Nielsen, J. T. & Nielsen, N. C. (2014). VirtualSpectrum, a tool for simulating peak list for multi-dimensional NMR spectra. Journal of Biomolecular NMR 60, 51–66.Google Scholar
Noinaj, N., Rollauer, S. E. & Buchanan, S. K. (2015). The β-barrel membrane protein insertase machinery from Gram-negative bacteria. Current Opinion in Structural Biology 31, 35–42.CrossRefGoogle ScholarPubMed
Nygaard, R., Zou, Y., Dror, R. O., Mildorf, T. J., Arlow, D. H., Manglik, A., Pan, A. C., Liu, C. W., Fung, J. J., Bokoch, M. P., Thian, F. S., Kobilka, T. S., Shaw, D. E., Mueller, L., Prosser, R. S. & Kobilka, B. K. (2013). The dynamic process of & beta 2-adrenergic receptor activation. Cell 152, 532–542.Google Scholar
O'Connor, C., White, K. L., Doncescu, N., Didenko, T., Roth, B. L., Czaplicki, G., Stevens, R. C., Wüthrich, K. & Milon, A. (2015). NMR structure and dynamics of the agonist dynorphin peptide bound to the human kappa opioid receptor. Proceedings of the National Academy of Sciences of the United States of America of the United States of America 112, 11852–11857.Google Scholar
Oldfield, E., Kinsey, R. A. & Kintanar, A. (1982). Recent advances in the study of bacteriorhodopsin dynamic structure using high-field solid-state nuclear magnetic-resonance spectroscopy. Methods in Enzymology 88, 310–325.Google Scholar
Ong, Y. S., Lakatos, A., Becker-Baldus, J., Pos, K. M. & Glaubitz, C. (2013). Detecting substrates bound to the secondary multidrug efflux pump EmrE by DNP-enhanced solid-state NMR. Journal of the American Chemical Society 135, 15754–15762.Google Scholar
Opefi, C. A., Tranter, D., Smith, S. O. & Reeves, P. J. (2015). Construction of stable mammalian cell lines for inducible expression of g protein- coupled receptors. Methods in Enzymology 556, 283–305.Google Scholar
Opella, S. J. (2013). Structure determination of membrane proteins in their native phospholipid bilayer environment by rotationally aligned solid-state NMR spectroscopy. Accounts of Chemical Research 46, 2145–2153.Google Scholar
Otting, G. (2010). Protein NMR using paramagnetic ions. Annual Review of Biophysics 39, 387–405.Google Scholar
Oxenoid, K. & Chou, J. J. (2013). The present and future of solution NMR in investigating the structure and dynamics of channels and transporters. Current Opinion in Structural Biology 23, 547–554.Google Scholar
Pandit, A., Reus, M., Morosinotto, T., Bassi, R., Holzwarth, A. R. & de Groot, H. J. M. (2013). An NMR comparison of the light-harvesting complex II (LHCII) in active and photoprotective states reveals subtle changes in the chlorophyll a ground-state electronic structures. Biochimica et Biophysica Acta 1827, 738–744.Google Scholar
Paramasivam, S., Suiter, C. L., Hou, G., Sun, S., Palmer, M., Hoch, J. C., Rovnyak, D. & Polenova, T. (2012). Enhanced sensitivity by nonuniform sampling enables multidimensional MAS NMR spectroscopy of protein assemblies. Journal of Physical Chemistry B 116, 7416–7427.Google Scholar
Park, S. H., Das, B. B., Casagrande, F., Tian, Y., Nothnagel, H. J., Chu, M., Kiefer, H., Maier, K., De Angelis, A. A., Marassi, F. M. & Opella, S. J. (2012). Structure of the chemokine receptor CXCR1 in phospholipid bilayers. Nature 491, 779–783.Google Scholar
Poyraz, O., Schmidt, H., Seidel, K., Delissen, F., Ader, C., Tenenboim, H., Goosmann, C., Laube, B., Thünemann, A. F., Zychlinsky, A., Baldus, M., Lange, A., Griesinger, C. & Kolbe, M. (2010). Protein refolding is required for assembly of the type three secretion needle. Nature Structural & Molecular Biology 17, 788–792.Google Scholar
Radoicic, J., Lu, G. J. & Opella, S. J. (2014). NMR structures of membrane proteins in phospholipid bilayers. Quarterly Reviews of Biophysics 47, 249–283.CrossRefGoogle ScholarPubMed
Ratnala, V. R. P., Kiihne, S. R., Buda, F., Leurs, R., de Groot, H. J. M. & Degrip, W. J. (2007). Solid-state NMR evidence for a protonation switch in the binding pocket of the H1 receptor upon binding of the agonist histamine. Journal of the American Chemical Society 129, 867–872.Google Scholar
Reggie, L., Lopez, J. J., Collinson, I., Glaubitz, C. & Lorch, M. (2011). Dynamic nuclear polarization-enhanced solid-state NMR of a 13C-labeled signal peptide bound to lipid-reconstituted sec translocon. Journal of the American Chemical Society 133, 19084–19086.Google Scholar
Renault, M., Bos, M. P., Tommassen, J. & Baldus, M. (2011). Solid-state NMR on a large multidomain integral membrane protein: the outer membrane protein assembly factor BamA. Journal of the American Chemical Society 133, 4175–4177.Google Scholar
Renault, M., Cukkemane, A. & Baldus, M. (2010). Solid-state NMR spectroscopy on complex biomolecules. Angewandte Chemie International Edition in English 49, 8346–8357.Google Scholar
Renault, M., Pawsey, S., Bos, M. P., Koers, E. J., Nand, D., Tommassen-van Boxtel, R., Rosay, M., Tommassen, J., Maas, W. E. & Baldus, M. (2012a). Solid-state NMR spectroscopy on cellular preparations enhanced by dynamic nuclear polarization. Angewandte Chemie International Edition in English 51, 2998–3001.Google Scholar
Renault, M., Tommassen-Van Boxtel, R., Bos, M. P., Post, J. A., Tommassen, J. & Baldus, M. (2012b). Cellular solid-state nuclear magnetic resonance spectroscopy. Proceedings of the National Academy of Sciences of the United States of America 109, 4863–4868.CrossRefGoogle ScholarPubMed
Ricci, D. P. & Silhavy, T. J. (2012). Biochimica et Biophysica Acta. Biochimica Et Biophysica Acta (BBA) – Biomembranes 1818, 1067–1084.Google Scholar
Ritchie, T. K., Grinkova, Y. V., Bayburt, T. H., Denisov, I. G., Zolnerciks, J. K., Atkins, W. M. & Sligar, S. G. (2009). Reconstitution of membrane proteins in phospholipid bilayer nanodiscs. Methods in Enzymology 464, 211–231.Google Scholar
Rivera-Calzada, A., Fronzes, R. E. M., Savva, C. G., Chandran, V., Lian, P. W., Laeremans, T., Pardon, E., Steyaert, J., Remaut, H., Waksman, G. & Orlova, E. V. (2013). Structure of a bacterial type IV secretion core complex at subnanometre resolution. EMBO Journal 32, 1195–1204.Google Scholar
Roman-Hernandez, G., Peterson, J. H. & Bernstein, H. D. (2014). Reconstitution of bacterial autotransporter assembly using purified components. eLife 3, e04234.Google Scholar
Rosen, M. K., Gardner, K. H., Willis, R. C., Parris, W. E., Pawson, T. & Kay, L. E. (1996). Selective methyl group protonation of perdeuterated proteins. Journal of Molecular Biology 263, 627–636.Google Scholar
Rosenzweig, R. & Kay, L. E. (2014). Bringing dynamic molecular machines into focus by methyl-TROSY NMR. Annual Review of Biochemistry 83, 291–315.Google Scholar
Sauvee, C., Rosay, M., Casano, G., Aussenac, F., Weber, R. T., Ouari, O. & Tordo, P. (2013). Highly efficient, water-soluble polarizing agents for dynamic nuclear polarization at high frequency. Angewandte Chemie International Edition in English 52, 10858–10861.Google Scholar
Schneider, R., Ader, C., Lange, A., Giller, K., Hornig, S., Pongs, O., Becker, S. & Baldus, M. (2008). Solid-state NMR spectroscopy applied to a chimeric potassium channel in lipid bilayers. Journal of the American Chemical Society 130, 7427–7435.Google Scholar
Schneider, R., Seidel, K., Etzkorn, M., Lange, A., Becker, S. & Baldus, M. (2010). Probing molecular motion by double-quantum (13C,13C) solid-state NMR spectroscopy: application to ubiquitin. Journal of the American Chemical Society 132, 223–233.Google Scholar
Schnell, J. R. & Chou, J. J. (2008). Structure and mechanism of the M2 proton channel of influenza A virus. Nature 451, 591–595.Google Scholar
Schwarz, D., Dötsch, V. & Bernhard, F. (2008). Production of membrane proteins using cell-free expression systems. Proteomics 8, 3933–3946.CrossRefGoogle ScholarPubMed
Seelig, J. & Gally, H. U. (1976). Investigation of phosphatidylethanolamine bilayers by deuterium and phosphorus-31 nuclear magnetic resonance. Biochemistry 15, 5199–5204.CrossRefGoogle ScholarPubMed
Seidel, K., Andronesi, O. C., Krebs, J., Griesinger, C., Young, H. S., Becker, S. & Baldus, M. (2008). Structural characterization of Ca 2+-ATPase-bound phospholamban in lipid bilayers by solid-state Nuclear Magnetic Resonance (NMR) spectroscopy. Biochemistry 47, 4369–4376.Google Scholar
Shahid, S. A., Bardiaux, B., Franks, W. T., Krabben, L., Habeck, M., van Rossum, B.-J. & Linke, D. (2012a). Membrane-protein structure determination by solid-state NMR spectroscopy of microcrystals. Nature Methods 9, 1212–1217.Google Scholar
Shahid, S. A., Markovic, S., Linke, D. & van Rossum, B.-J. (2012b). Assignment and secondary structure of the YadA membrane protein by solid-state MAS NMR. Scientific Reports 2, 803.Google Scholar
Shahid, S. A., Nagaraj, M., Chauhan, N., Franks, T. W., Bardiaux, B., Habeck, M., Orwick-Rydmark, M., Linke, D. & van Rossum, B.-J. (2015). Solid-state NMR study of the YadA membrane-anchor domain in the bacterial outer membrane. Angewandte Chemie International Edition in English 54, 12602–12606.Google Scholar
Sharma, M., Yi, M., Dong, H., Qin, H., Peterson, E., Busath, D. D., Zhou, H. X. & Cross, T. A. (2010). Insight into the mechanism of the influenza a proton channel from a structure in a lipid bilayer. Science 330, 509–512.Google Scholar
Sinnige, T., Daniëls, M., Baldus, M. & Weingarth, M. (2014a). Proton clouds to measure long-range contacts between nonexchangeable side chain protons in solid-state NMR. Journal of the American Chemical Society 136, 4452–4455.Google Scholar
Sinnige, T., Houben, K., Pritisanac, I., Renault, M., Boelens, R. & Baldus, M. (2015a). Insight into the conformational stability of membrane-embedded BamA using a combined solution and solid-state NMR approach. Journal of Biomolecular NMR 61, 321–332.Google Scholar
Sinnige, T., Weingarth, M., Daniëls, M., Boelens, R., Bonvin, A. M. J. J., Houben, K. & Baldus, M. (2015b). Conformational plasticity of the POTRA 5 domain in the outer membrane protein assembly factor BamA. Structure (London, England: 1993) 23, 1317–1324.CrossRefGoogle ScholarPubMed
Sinnige, T., Weingarth, M., Renault, M., Baker, L., Tommassen, J. & Baldus, M. (2014b). Solid-state NMR studies of full-length BamA in lipid bilayers suggest limited overall POTRA mobility. Journal of Molecular Biology 426, 2009–2021.Google Scholar
Song, C., Hu, K.-N., Joo, C.-G., Swager, T. M. & Griffin, R. G. (2006). TOTAPOL: a biradical polarizing agent for dynamic nuclear polarization experiments in aqueous media. Journal of the American Chemical Society 128, 11385–11390.Google Scholar
Sounier, R., Mas, C., Steyaert, J., Laeremans, T., Manglik, A., Huang, W., Kobilka, B. K., Demene, H. & Granier, S. (2015). Propagation of conformational changes during μ-opioid receptor activation. Nature 524, 375–378.CrossRefGoogle ScholarPubMed
Sperling, L. J., Tang, M., Berthold, D. A., Nesbitt, A. E., Gennis, R. B. & Rienstra, C. M. (2013). Solid-state NMR study of a 41 kDa membrane protein complex DsbA/DsbB. Journal of Physical Chemistry B 117, 6052–6060.Google Scholar
Sprangers, R., Velyvis, A. & Kay, L. E. (2007). Solution NMR of supramolecular complexes: providing new insights into function. Nature Methods 4, 697–703.Google Scholar
Stouffer, A. L., Acharya, R., Salom, D., Levine, A. S., Di Costanzo, L., Soto, C. S., Tereshko, V., Nanda, V., Stayrook, S. & DeGrado, W. F. (2008). Structural basis for the function and inhibition of an influenza virus proton channel. Nature 451, 596–599.Google Scholar
Takahashi, H., Ayala, I., Bardet, M., de Paëpe, G., Simorre, J.-P. & Hediger, S. (2013). Solid-state NMR on bacterial cells: selective cell wall signal enhancement and resolution improvement using dynamic nuclear polarization. Journal of the American Chemical Society 135, 5105–5110.Google Scholar
Tang, M., Comellas, G. & Rienstra, C. M. (2013). Advanced solid-state NMR approaches for structure determination of membrane proteins and amyloid fibrils. Accounts of Chemical Research 46, 2080–2088.Google Scholar
Tribet, C., Audebert, R. & Popot, J. L. (1996). Amphipols: polymers that keep membrane proteins soluble in aqueous solutions. Proceedings of the National Academy of Sciences of the United States of America 93, 15047–15050.Google Scholar
van der Cruijsen, E. A. W., Koers, E. J., Sauvee, C., Hulse, R. E., Weingarth, M., Ouari, O., Perozo, E., Tordo, P. & Baldus, M. (2015). Biomolecular DNP-supported NMR spectroscopy using site-directed spin labeling. Chemistry – a European Journal 21, 12971–12977.Google Scholar
van der Cruijsen, E. A. W., Nand, D., Weingarth, M., Prokofyev, A., Hornig, S., Cukkemane, A. A., Bonvin, A. M. J. J., Becker, S., Hulse, R. E., Perozo, E., Pongs, O. & Baldus, M. (2013). Importance of lipid–pore loop interface for potassium channel structure and function. Proceedings of the National Academy of Sciences of the United States of America 110, 13008–13013.Google Scholar
van Meer, G., Voelker, D. R. & Feigenson, G. W. (2008). Membrane lipids: where they are and how they behave. Nature Reviews Molecular Cell Biology 9, 112–124.Google Scholar
Vardy, E. & Roth, B. L. (2013). Conformational ensembles in GPCR activation. Cell 152, 385–386.CrossRefGoogle ScholarPubMed
von Heijne, G. (2007). The membrane protein universe: what's out there and why bother? Journal of Internal Medicine 261, 543–557.Google Scholar
Walther, D. M., Papic, D. & Bos, M. P. (2009). Signals in bacterial β-barrel proteins are functional in eukaryotic cells for targeting to and assembly in mitochondria. Proceedings of the National Academy of Sciences of the United States of America 106, 2531–2536.Google Scholar
Wang, S. & Ladizhansky, V. (2014). Recent advances in magic angle spinning solid state NMR of membrane proteins. Progress in Nuclear Magnetic Resonance Spectroscopy 82(C), 1–26.Google Scholar
Wang, S., Munro, R. A., Kim, S.-Y., Jung, K.-H., Brown, L. S. & Ladizhansky, V. (2012). Paramagnetic relaxation enhancement reveals oligomerization interface of a membrane protein. Journal of the American Chemical Society 134, 16995–16998.Google Scholar
Wang, S., Munro, R. A., Shi, L., Kawamura, I., Okitsu, T., Wada, A., Kim, S.-Y., Jung, K.-H., Brown, L. S. & Ladizhansky, V. (2013). Solid-state NMR spectroscopy structure determination of a lipid-embedded heptahelical membrane protein. Nature Methods 10, 1007–1012.Google Scholar
Wang, T., Salazar, A., Zabotina, O. A. & Hong, M. (2014). Structure and dynamics of Brachypodium primary cell wall polysaccharides from two-dimensional 13C solid-state Nuclear Magnetic Resonance Spectroscopy. Biochemistry 53, 2840–2854.Google Scholar
Ward, M. E., Wang, S., Munro, R., Ritz, E., Hung, I., Gor'kov, P. L., Jiang, Y., Liang, H., Brown, L. S. & Ladizhansky, V. (2015). In situ structural studies of anabaena sensory rhodopsin in the E. coli membrane. Biophysical Journal 108, 1683–1696.Google Scholar
Weingarth, M., Ader, C., Melquiond, A. S. J., Nand, D., Pongs, O., Becker, S., Bonvin, A. M. J. J. & Baldus, M. (2012). Supramolecular structure of membrane-associated polypeptides by combining solid-state NMR and molecular dynamics simulations. Biophysical Journal 103, 29–37.Google Scholar
Weingarth, M. & Baldus, M. (2013). Solid-state NMR-based approaches for supramolecular structure elucidation. Accounts of Chemical Research 46, 2037–2046.Google Scholar
Weingarth, M., Prokofyev, A., van der Cruijsen, E. A. W., Nand, D., Bonvin, A. M. J. J., Pongs, O. & Baldus, M. (2013). Structural determinants of specific lipid binding to potassium channels. Journal of the American Chemical Society 135, 3983–3988.CrossRefGoogle ScholarPubMed
Weingarth, M., van der Cruijsen, E. A. W., Ostmeyer, J., Lievestro, S., Roux, B. & Baldus, M. (2014). Quantitative analysis of the water occupancy around the selectivity filter of a K+ channel in different gating modes. Journal of the American Chemical Society 136, 2000–2007.Google Scholar
White, J. F., Noinaj, N., Shibata, Y., Love, J., Kloss, B., Xu, F., Gvozdenovic-Jeremic, J., Shah, P., Shiloach, J., Tate, C. G. & Grisshammer, R. (2012). Structure of the agonist-bound neurotensin receptor. Nature 490, 508–513.CrossRefGoogle ScholarPubMed
Yamamoto, K., Caporini, M. A., Im, S.-C., Waskell, L. & Ramamoorthy, A. (2015). Cellular solid-state NMR investigation of a membrane protein using dynamic nuclear polarization. Biochimica Et Biophysica Acta (BBA)– Biomembranes 1848(PB), 342–349.Google Scholar
Yarov-Yarovoy, V., Schonbrun, J. & Baker, D. (2006). Multipass membrane protein structure prediction using Rosetta. Proteins: Structure, Function, and Bioinformatics 62, 1010–1025.Google Scholar
Zhang, M., Huang, R., Im, S.-C., Waskell, L. & Ramamoorthy, A. (2015). Effects of membrane mimetics on cytochrome P450–cytochrome b5 interactions characterized by NMR spectroscopy. Journal of Biological Chemistry 290, 12705–12718.Google Scholar
Zhou, H.-X. & Cross, T. A. (2013). Influences of membrane mimetic environments on membrane protein structures. Annual Review of Biophysics 42, 361–392.Google Scholar
Zhou, Y., Cierpicki, T., Jimenez, R. H. F., Lukasik, S. M., Ellena, J. F., Cafiso, D. S., Kadokura, H., Beckwith, J. & Bushweller, J. H. (2008). NMR solution structure of the integral membrane enzyme DsbB: functional insights into DsbB-catalyzed disulfide bond formation. Molecular Cell 31, 896–908.CrossRefGoogle ScholarPubMed
Zhuang, T. & Tamm, L. K. (2014). Control of the conductance of engineered protein nanopores through concerted loop motions. Angewandte Chemie International Edition 53, 5897–5902.CrossRefGoogle ScholarPubMed
Zorman, S., Botte, M., Jiang, Q., Collinson, I. & Schaffitzel, C. (2015). Advances and challenges of membrane–protein complex production. Current Opinion in Structural Biology 32, 123–130.Google Scholar