1932

Abstract

Solid-state nuclear magnetic resonance (SSNMR) spectroscopy elucidates membrane protein structures and dynamics in atomic detail to yield mechanistic insights. By interrogating membrane proteins in phospholipid bilayers that closely resemble biological membranes, SSNMR spectroscopists have revealed ion conduction mechanisms, substrate transport dynamics, and oligomeric interfaces of seven-transmembrane helix proteins. Research has also identified conformational plasticity underlying virus-cell membrane fusions by complex protein machineries, and β-sheet folding and assembly by amyloidogenic proteins bound to lipid membranes. These studies collectively show that membrane proteins exhibit extensive structural plasticity to carry out their functions. Because of the inherent dependence of NMR frequencies on molecular orientations and the sensitivity of NMR frequencies to dynamical processes on timescales from nanoseconds to seconds, SSNMR spectroscopy is ideally suited to elucidate such structural plasticity, local and global conformational dynamics, protein-lipid and protein-ligand interactions, and protonation states of polar residues. New sensitivity-enhancement techniques, resolution enhancement by ultrahigh magnetic fields, and the advent of 3D and 4D correlation NMR techniques are increasingly aiding these mechanistically important structural studies.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-070816-033712
2018-05-20
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/biophys/47/1/annurev-biophys-070816-033712.html?itemId=/content/journals/10.1146/annurev-biophys-070816-033712&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Acharya A, Carnevale V, Fiorin G, Levine BG, Polishchuk A et al. 2010. Structural mechanism of proton transport through the influenza A M2 protein. PNAS 107:15075–80
    [Google Scholar]
  2. 2.  Akinlolu R, Nam M, Qiang W 2015. Competition between fibrillation and induction of vesicle fusion for the membrane-associated 40-residue β-amyloid peptides. Biochemistry 54:3416–19
    [Google Scholar]
  3. 3.  Andreas LB, Reese M, Eddy MT, Gelev V, Ni QZ et al. 2015. Structure and mechanism of the influenza A M218–60 dimer of dimers. J. Am. Chem. Soc. 137:14877–86
    [Google Scholar]
  4. 4.  Barbet-Massin E, Pell AJ, Retel JS, Andreas LB, Jaudzems K et al. 2014. Rapid proton-detected NMR assignment for proteins with fast magic angle spinning. J. Am. Chem. Soc. 136:12489–97
    [Google Scholar]
  5. 5.  Bhate MP, McDermott AE 2012. Protonation state of E71 in KcsA and its role for channel collapse and inactivation. PNAS 109:15265–70
    [Google Scholar]
  6. 6.  Bright RA, Medina MJ, Xu X, Perez-Oronoz G, Wallis TR et al. 2005. Incidence of adamantane resistance among influenza A (H3N2) viruses isolated worldwide from 1994 to 2005: a cause for concern. Lancet 366:1175–81
    [Google Scholar]
  7. 7.  Cady SD, Goodman C, Tatko C, DeGrado WF, Hong M 2007. Determining the orientation of uniaxially rotating membrane proteins using unoriented samples: a 2H, 13C, and 15N solid-state NMR investigation of the dynamics and orientation of a transmembrane helical bundle. J. Am. Chem. Soc. 129:5719–29
    [Google Scholar]
  8. 8.  Cady SD, Schmidt-Rohr K, Wang J, Soto CS, DeGrado WF, Hong M 2010. Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers. Nature 463:689–92
    [Google Scholar]
  9. 9.  Cady SD, Wang T, Hong M 2011. Membrane-dependent effects of a cytoplasmic helix on the structure and drug binding of the influenza virus M2 protein. J. Am. Chem. Soc. 133:11572–79
    [Google Scholar]
  10. 10.  Cho MK, Gayen A, Banigan JR, Leninger M, Traaseth NJ 2014. Intrinsic conformational plasticity of native EmrE provides a pathway for multidrug resistance. J. Am. Chem. Soc. 136:8072–80
    [Google Scholar]
  11. 11.  Colvin MT, Andreas LB, Chou JJ, Griffin RG 2014. Proton association constants of His 37 in the influenza-A M218–60 dimer-of-dimers. Biochemistry 53:5987–94
    [Google Scholar]
  12. 12.  Comellas G, Lemkau L, Zhou D, George J, Rienstra C 2012. Stuctural intermediates during α-synuclein fibrillogenesis on phospholipid vesicles. J. Am. Chem. Soc. 134:5090–99
    [Google Scholar]
  13. 13.  Comellas G, Rienstra CM 2013. Protein structure determination by magic-angle spinning solid-state NMR, and insights into the formation, structure, and stability of amyloid fibrils. Annu. Rev. Biophys. 42:515–36
    [Google Scholar]
  14. 14.  Cristian L, Lear JD, DeGrado WF 2003. Use of thiol-disulfide equilibria to measure the energetics of assembly of transmembrane helices in phospholipid bilayers. PNAS 100:14772–77
    [Google Scholar]
  15. 15.  Cuello LG, Jogini V, Cortes DM, Perozo E 2010. Structural mechanism of C-type inactivation in K+ channels. Nature 466:203–8
    [Google Scholar]
  16. 16.  Doyle DA, Cabral JM, Pfuetzner RA, Kuo A, Gulbis JM et al. 1998. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280:69–77
    [Google Scholar]
  17. 17.  Duong-Ly KC, Nanda V, DeGrado WF, Howard KP 2005. The conformation of the pore region of the M2 proton channel depends on lipid bilayer environment. Protein Sci 14:856–61
    [Google Scholar]
  18. 18.  Eddy MT, Andreas L, Teijido O, Su Y, Clark L et al. 2015. Magic angle spinning nuclear magnetic resonance characterization of voltage-dependent anion channel gating in two-dimensional lipid crystalline bilayers. Biochemistry 54:994–1005
    [Google Scholar]
  19. 19.  Eddy MT, Ong TC, Clark L, Teijido O, van der Wel PC et al. 2012. Lipid dynamics and protein-lipid interactions in 2D crystals formed with the beta-barrel integral membrane protein VDAC1. J. Am. Chem. Soc. 134:6375–87
    [Google Scholar]
  20. 20.  Eddy MT, Su Y, Silvers R, Andreas L, Clark L et al. 2015. Lipid bilayer-bound conformation of an integral membrane beta barrel protein by multidimensional MAS NMR. J. Biomol. NMR 61:299–310
    [Google Scholar]
  21. 21.  Eichmann C, Campioni S, Kowal J, Maslennikov I, Gerez J et al. 2016. Preparation and characterization of stable α-synuclein lipoprotein particles. J. Biol. Chem. 291:8516–27
    [Google Scholar]
  22. 22.  Ernst OP, Lodowski DT, Elstner M, Hegemann P, Brown LS, Kandori H 2014. Microbial and animal rhodopsins: structures, functions, and molecular mechanisms. Chem. Rev. 114:126–63
    [Google Scholar]
  23. 23.  Fu R, Miao Y, Qin H, Cross TA 2016. Probing hydronium ion histidine NH exchange rate constants in the M2 channel via indirect observation of dipolar-dephased 15N signals in magic-angle-spinning NMR. J. Am. Chem. Soc. 138:15801–4
    [Google Scholar]
  24. 24.  Fusco G, De Simone A, Gopinath T, Vostrikov V, Vendruscolo M et al. 2014. Direct observation of the three regions in α-synuclein that determine its membrane-bound behaviour. Nat. Comm. 5:3827
    [Google Scholar]
  25. 25.  Fusco G, Pape T, Stephens A, Mahou P, Costa A et al. 2016. Structural basis of synaptic vesicle assembly promoted by α-synuclein. Nat. Comm. 7:12563
    [Google Scholar]
  26. 26.  Gabrys C, Qiang W, Sun Y, Xie L, Schmick S, Weliky D 2013. Solid-state nuclear magnetic resonance measurements of HIV fusion peptides 13CO to lipid 31P proximities support similar partially inserted membrane locations of the α helical and β sheet peptide structures. J. Phys. Chem. A 117:9848–59
    [Google Scholar]
  27. 27.  Gadsby DC. 2009. Ion channels versus ion pumps: the principal difference, in principle. Nat. Rev. Mol. Cell. Biol. 10:344–352
    [Google Scholar]
  28. 28.  Gayen A, Banigan JR, Traaseth NJ 2013. Ligand-induced conformational changes of the multidrug resistance transporter EmrE probed by oriented solid-state NMR spectroscopy. Angew. Chem. 52:10321–24
    [Google Scholar]
  29. 29.  Gayen A, Leninger M, Traaseth NJ 2016. Protonation of a glutamate residue modulates the dynamics of the drug transporter EmrE. Nat. Chem. Biol. 12:141–45
    [Google Scholar]
  30. 30.  Ghosh U, Xie L, Jia L, Liang S, Weliky D 2015. Closed and semiclosed interhelical structures in membrane versus closed and open structures in detergent for the influenza virus hemagglutinin fusion peptide and correlation of hydrophobic surface area with fusion catalysis. J. Am. Chem. Soc. 137:7548–51
    [Google Scholar]
  31. 31.  Ghosh U, Xie L, Weliky D 2013. Detection of closed influenza virus hemagglutinin fusion peptide structures in membranes by backbone 13CO-14N rotational-echo double-resonance solid-state NMR. J. Biomol. NMR 55:139–46
    [Google Scholar]
  32. 32.  Grandea AG, Olsen OA, Cox TC, Renshaw M, Hammond PW et al. 2010. Human antibodies reveal a protective epitope that is highly conserved among human and nonhuman influenza A viruses. PNAS 107:12658–63
    [Google Scholar]
  33. 33.  Harrison SC. 2008. Viral membrane fusion. Nat. Struct. Mol. Biol. 15:690–98
    [Google Scholar]
  34. 34.  Higgins CF. 2007. Multiple molecular mechanisms for multidrug resistance transporters. Nature 446:749–57
    [Google Scholar]
  35. 35.  Hille B. 1992. Ionic Channels of Excitable Membranes Sunderland, MA: Sinauer
  36. 36.  Hong M, DeGrado WF 2012. Structural basis for proton conduction and inhibition by the influenza M2 protein. Protein Sci 21:1620–33
    [Google Scholar]
  37. 37.  Hong M, Fritzsching KJ, Williams JK 2012. Hydrogen-bonding partner of the proton-conducting histidine in the influenza M2 proton channel revealed from 1H chemical shifts. J. Am. Chem. Soc. 134:14753–55
    [Google Scholar]
  38. 38.  Hoshi T, Zagotta WN, Aldrich RW 1991. Two types of inactivation in Shaker K+ channels: effects of alterations in the carboxy-terminal region. Neuron 7:547–56
    [Google Scholar]
  39. 39.  Hu F, Luo W, Cady SD, Hong M 2011. Conformational plasticity of the influenza A M2 transmembrane peptide in lipid bilayers under varying pH, drug binding and membrane thickness. Biochim. Biophys. Acta 1808:415–23
    [Google Scholar]
  40. 40.  Hu F, Luo W, Hong M 2010. Mechanisms of proton conduction and gating by influenza M2 proton channels from solid-state NMR. Science 330:505–9
    [Google Scholar]
  41. 41.  Hu F, Schmidt-Rohr K, Hong M 2012. NMR detection of pH-dependent histidine-water proton exchange reveals the conduction mechanism of a transmembrane proton channel. J. Am. Chem. Soc. 134:3703–13
    [Google Scholar]
  42. 42.  Hu J, Asbury T, Achuthan S, Li C, Bertram R et al. 2007. Backbone structure of the amantadine-blocked trans-membrane domain M2 proton channel from influenza A virus. Biophys. J. 92:4335–43
    [Google Scholar]
  43. 43.  Hu J, Fu R, Nishimura K, Zhang L, Zhou HX et al. 2006. Histidines, heart of the hydrogen ion channel from influenza A virus: toward an understanding of conductance and proton selectivity. PNAS 103:6865–70
    [Google Scholar]
  44. 44.  Huster D, Yao XL, Hong M 2002. Membrane protein topology probed by 1H spin diffusion from lipids using solid-state NMR spectroscopy. J. Am. Chem. Soc. 124:874–83
    [Google Scholar]
  45. 45.  Kim SS, Upshur MA, Saotome K, Sahu ID, McCarrick RM et al. 2015. Cholesterol-dependent conformational exchange of the C-terminal domain of the Influenza A M2 protein. Biochemistry 54:7157–67
    [Google Scholar]
  46. 46.  Koebnik R, Locher KP, Van Gelder P 2000. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol. Microbiol. 37:239–53
    [Google Scholar]
  47. 47.  Korshavn K, Bhunia A, Lim M, Ramamoorthy A 2016. Amyloid-β adopts a conserved, partially folded structure upon binding to zwitterionic lipid bilayers prior to amyloid formation. Chem. Commun. 52:882–85
    [Google Scholar]
  48. 48.  Korshavn K, Satriano C, Lin Y, Zhang R, Dulchavsky M et al. 2017. Reduced lipid bilayer thickness regulates the aggregation and cytotoxicity of amyloid-β. J. Biol. Chem. 292:4638–50
    [Google Scholar]
  49. 49.  Kotler S, Walsh P, Brender J, Ramamoorthy A 2014. Differences between amyloid-β aggregation in solution and on the membrane: insights into elucidation of the mechanistic details of Alzheimer's disease. Chem. Soc. Rev. 43:6692–700
    [Google Scholar]
  50. 50.  Kwon B, Hong M 2016. The influenza M2 ectodomain regulates the conformational equilibria of the transmembrane proton channel: insights from solid-state nuclear magnetic resonance. Biochemistry 55:5387–97
    [Google Scholar]
  51. 51.  Kwon B, Tietze D, White PB, Liao SY, Hong M 2015. Chemical ligation of the influenza M2 protein for solid-state NMR characterization of the cytoplasmic domain structure. Protein Sci 24:1087–99
    [Google Scholar]
  52. 52.  Lehner I, Basting D, Meyer B, Haase W, Manolikas T et al. 2008. The key residue for substrate transport (Glu14) in the EmrE dimer is asymmetric. J. Biol. Chem. 283:3281–88
    [Google Scholar]
  53. 53.  Lehnert E, Mao JF, Mehdipour AR, Hummers G, Abele R et al. 2016. Antigenic peptide recognition on the human ABC transporter TAP resolved by DNP-enhanced solid-state NMR spectroscopy. J. Am. Chem. Soc. 138:13967–74
    [Google Scholar]
  54. 54.  Liao SY, Fritzsching KJ, Hong M 2013. Conformational analysis of the full-length M2 protein of the influenza A virus using solid-state NMR. Protein Sci 22:1623–38
    [Google Scholar]
  55. 55.  Liao SY, Yang Y, Tietze D, Hong M 2015. The influenza M2 cytoplasmic tail changes the proton-exchange equilibria and the backbone conformation of the transmembrane histidine residue to facilitate proton conduction. J. Am. Chem. Soc. 137:6067–77
    [Google Scholar]
  56. 56.  Long SB, Tao X, Campbell EB, MacKinnon R 2007. Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature 450:376–83
    [Google Scholar]
  57. 57.  Luo W, Cady SD, Hong M 2009. Immobilization of the influenza A M2 transmembrane peptide in virus-envelope mimetic lipid membranes: a solid-state NMR investigation. Biochemistry 48:6361–68
    [Google Scholar]
  58. 58.  Luo W, Mani R, Hong M 2007. Sidechain conformation and gating of the M2 transmembrane peptide proton channel of influenza A virus from solid-state NMR. J. Phys. Chem. 111:10825–32
    [Google Scholar]
  59. 59.  Ma CL, Polishchuk AL, Ohigashi Y, Stouffer AL, Schon A et al. 2009. Identification of the functional core of the influenza A virus A/M2 proton-selective ion channel. PNAS 106:12283–88
    [Google Scholar]
  60. 60.  Maciejko J, Mehler M, Kaur J, Lieblein T, Morgner N et al. 2015. Visualizing specific cross-protomer interactions in the homo-oligomeric membrane protein proteorhodopsin by dynamic-nuclear-polarization-enhanced solid-state NMR. J. Am. Chem. Soc. 137:9032–43
    [Google Scholar]
  61. 61.  Mandala VS, Liao SY, Kwon B, Hong M 2017. Structural basis for asymmetric conductance of the influenza M2 proton channel investigated by solid-state NMR spectroscopy. J. Mol. Biol. 429:2192–210
    [Google Scholar]
  62. 62.  McCown MF, Pekosz A 2006. Distinct domains of the influenza a virus M2 protein cytoplasmic tail mediate binding to the M1 protein and facilitate infectious virus production. J. Virol. 80:8178–89
    [Google Scholar]
  63. 63.  Miao Y, Fu R, Zhou HX, Cross TA 2015. Dynamic short hydrogen bonds in histidine tetrad of full-length M2 proton channel reveal tetrameric structural heterogeneity and functional mechanism. Structure 23:2300–8
    [Google Scholar]
  64. 64.  Morrison EA, DeKoster GT, Dutta S, Vafabakhsh R, Clarkson MW et al. 2011. Antiparallel EmrE exports drugs by exchanging between asymmetric structures. Nature 481:45–50
    [Google Scholar]
  65. 65.  Ni QZ, Daviso E, Can TV, Markhasin E, Jawla SK et al. 2013. High frequency dynamic nuclear polarization. Acc. Chem. Res. 46:1933–41
    [Google Scholar]
  66. 66.  Niu Z, Zhao W, Zhang Z, Xiao F, Tang X, Yang J 2014. The molecular structure of Alzheimer β-amyloid fibrils formed in the presence of phospholipid vesicles. Angew. Chem. 53:9294–97
    [Google Scholar]
  67. 67.  Ong YS, Lakatos A, Becker-Baldus J, Pos KM, Glaubitz C 2013. Detecting substrates bound to the secondary multidrug efflux pump EmrE by DNP-enhanced solid-state NMR. J. Am. Chem. Soc. 135:15754–62
    [Google Scholar]
  68. 68.  Park EK, Castrucci MR, Portner A, Kawaoka Y 1998. The M2 ectodomain is important for its incorporation into influenza A virions. J. Virol. 72:2449–55
    [Google Scholar]
  69. 69.  Pielak RM, Chou JJ 2011. Influenza M2 proton channels. Biochim. Biophys. Acta 1808:522–29
    [Google Scholar]
  70. 70.  Pierce KL, Premont RT, Lefkowitz RJ 2002. Seven-transmembrane receptors. Nat. Rev. Mol. Cell. Biol. 3:639–50
    [Google Scholar]
  71. 71.  Pinto LH, Dieckmann GR, Gandhi CS, Papworth CG, Braman J et al. 1997. A functionally defined model for the M2 proton channel of influenza A virus suggests a mechanism for its ion selectivity. PNAS 94:11301–6
    [Google Scholar]
  72. 72.  Pinto LH, Lamb RA 2006. The M2 proton channels of influenza A and B viruses. J. Biol. Chem. 281:8997–9000
    [Google Scholar]
  73. 73.  Qiang W, Akinlolu R, Nam M, Shu N 2014. Structural evolution and membrane interaction of the 40-residue β amyloid peptides: differences in the initial proximity between peptides and the membrane bilayer studied by solid-state nuclear magnetic resonance spectroscopy. Biochemistry 53:7503–14
    [Google Scholar]
  74. 74.  Qiang W, Yau W-M, Schulte J 2015. Fibrillation of β amyloid peptides in the presence of phospholipid bilayers and the consequent membrane disruption. Biochim. Biophys. Acta 1848:266–76
    [Google Scholar]
  75. 75.  Ratnayake P, Sackett K, Nethercott M, Weliky D 2015. pH-dependent vesicle fusion induced by the ectodomain of the human immunodeficiency virus membrane fusion protein gp41: two kinetically distinct processes and fully-membrane-associated gp41 with predominant β sheet fusion peptide conformation. Biochim. Biophys. Acta Biomem. 1848:289–98
    [Google Scholar]
  76. 76.  Rossman JS, Jing X, Leser GP, Lamb RA 2010. Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 142:902–13
    [Google Scholar]
  77. 77.  Sackett K, Nethercott M, Zheng Z, Weliky D 2014. Solid-state NMR spectroscopy of the HIV gp41 membrane fusion protein supports intermolecular antiparallel β sheet fusion peptide structure in the final six-helix bundle state. J. Mol. Biol. 426:1077–94
    [Google Scholar]
  78. 78.  Saotome K, Duong-Ly KC, Howard KP 2015. Influenza A M2 protein conformation depends on choice of model membrane. Biopolymers 104:405–11
    [Google Scholar]
  79. 79.  Schmick S, Weliky D 2010. Major antiparallel and minor parallel β sheet populations detected in the membrane-associated human immunodeficiency virus fusion peptide. Biochemistry 49:10623–35
    [Google Scholar]
  80. 80.  Schneider R, Ader C, Lange A, Giller K, Hornig S et al. 2008. Solid-state NMR spectroscopy applied to a chimeric potassium channel in lipid bilayers. J. Am. Chem. Soc. 130:7427–35
    [Google Scholar]
  81. 81.  Schnell JR, Chou JJ 2008. Structure and mechanism of the M2 proton channel of influenza A virus. Nature 451:591–95
    [Google Scholar]
  82. 82.  Sergeyev IV, Itin B, Rogawski R, Day LA, McDermott AE 2017. Efficient assignment and NMR analysis of an intact virus using sequential side-chain correlations and DNP sensitization. PNAS 114:5171–76
    [Google Scholar]
  83. 83.  Sharma M, Yi M, Dong H, Qin H, Peterson E et al. 2010. Insight into the mechanism of the influenza A proton channel from a structure in a lipid bilayer. Science 330:509–12
    [Google Scholar]
  84. 84.  Stouffer AL, Acharya R, Salom D, Levine AS, Di Costanzo L et al. 2008. Structural basis for the function and inhibition of an influenza virus proton channel. Nature 451:596–99
    [Google Scholar]
  85. 85.  Tang M, Comellas G, Rienstra CM 2013. Advanced solid-state NMR approaches for structure determination of membrane proteins and amyloid fibrils. Acc. Chem. Res. 46:2080–88
    [Google Scholar]
  86. 86.  Thomaston JL, Alfonso-Prieto M, Woldeyes RA, Fraser JS, Klein ML et al. 2015. High-resolution structures of the M2 channel from influenza A virus reveal dynamic pathways for proton stabilization and transduction. PNAS 112:14260–65
    [Google Scholar]
  87. 87.  Thompson AN, Posson DJ, Parsa PV, Nimigean CM 2008. Molecular mechanism of pH sensing in KcsA potassium channels. PNAS 105:6900–5
    [Google Scholar]
  88. 88.  Tuttle M, Comellas G, Nieuwkoop A, Covell D, Berthold D et al. 2016. Solid-state NMR structure of a pathogenic fibril of full-length human α-synuclein. Nat. Struct. Mol. Biol 23:409–15
    [Google Scholar]
  89. 89.  Tycko R, Wickner RB 2013. Molecular structures of amyloid and prion fibrils: consensus versus controversy. Acc. Chem. Res. 46:1487–96
    [Google Scholar]
  90. 90.  Unwin N. 1989. The structure of ion channels in membranes of excitable cells. Neuron 3:665–76
    [Google Scholar]
  91. 91.  van der Cruijsen EA, Nand D, Weingarth M, Prokofyev A, Hornig S et al. 2013. Importance of lipid-pore loop interface for potassium channel structure and function. PNAS 110:13008–13
    [Google Scholar]
  92. 92.  van der Cruijsen EAW, Prokofyev AV, Pongs O, Baldus M 2017. Probing conformational changes during the gating cycle of a potassium channel in lipid bilayers. Biophys. J. 112:99–108
    [Google Scholar]
  93. 93.  Wang S, Munro RA, Kim SY, Jung KH, Brown LS, Ladizhansky V 2012. Paramagnetic relaxation enhancement reveals oligomerization interface of a membrane protein. J. Am. Chem. Soc. 134:16995–98
    [Google Scholar]
  94. 94.  Wang SL, Munro RA, Shi LC, Kawamura I, Okitsu T et al. 2013. Solid-state NMR spectroscopy structure determination of a lipid-embedded heptahelical membrane protein. Nat. Methods 10:1007–12
    [Google Scholar]
  95. 95.  Wang T, Cady SD, Hong M 2012. NMR determination of protein partitioning into membrane domains with different curvatures and application to the influenza M2 peptide. Biophys. J. 102:787–94
    [Google Scholar]
  96. 96.  Ward ME, Wang SL, Munro R, Ritz E, Hung I et al. 2015. In situ structural studies of anabaena sensory rhodopsin in the E. coli membrane. Biophys. J. 108:1683–96
    [Google Scholar]
  97. 97.  Weingarth M, Prokofyev A, van der Cruijsen EA, Nand D, Bonvin AM et al. 2013. Structural determinants of specific lipid binding to potassium channels. J. Am. Chem. Soc. 135:3983–88
    [Google Scholar]
  98. 98.  White JM, Delos SE, Brecher M, Schornberg K 2008. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit. Rev. Biochem. Mol. Biol. 43:189–219
    [Google Scholar]
  99. 99.  White PB, Hong M 2015. 15N and 1H solid-state NMR investigation of a canonical low-barrier hydrogen-bond compound: 1,8-bis(dimethylamino)naphthalene. J. Phys. Chem. B 119:11581–89
    [Google Scholar]
  100. 100.  Williams JK, Hong M 2014. Probing membrane protein structure using water polarization transfer solid-state NMR. J. Magn. Reson. 247:118–27
    [Google Scholar]
  101. 101.  Williams JK, Schmidt-Rohr K, Hong M 2015. Aromatic spectral editing techniques for magic-angle-spinning solid-state NMR spectroscopy of uniformly 13C-labeled proteins. Solid State Nucl. Magn. Reson. 72:118–26
    [Google Scholar]
  102. 102.  Williams JK, Tietze D, Lee M, Wang J, Hong M 2016. Solid-state NMR investigation of the conformation, proton conduction, and hydration of the influenza B virus M2 transmembrane proton channel. J. Am. Chem. Soc. 138:8143–55
    [Google Scholar]
  103. 103.  Williams JK, Tietze D, Wang J, Wu Y, DeGrado WF, Hong M 2013. Drug-induced conformational and dynamical changes of the S31N mutant of the influenza M2 proton channel investigated by solid-state NMR. J. Am. Chem. Soc. 135:9885–97
    [Google Scholar]
  104. 104.  Williams JK, Zhang Y, Schmidt-Rohr K, Hong M 2013. pH-dependent conformation, dynamics, and aromatic interaction of the gating tryptophan residue of the influenza M2 proton channel from solid-state NMR. Biophys. J. 104:1698–708
    [Google Scholar]
  105. 105.  Wylie BJ, Bhate MP, McDermott AE 2014. Transmembrane allosteric coupling of the gates in a potassium channel. PNAS 111:185–90
    [Google Scholar]
  106. 106.  Yao H, Hong M 2013. Membrane-dependent conformation, dynamics, and lipid interactins of the fusion peptide of the paramyxovirus PIV5 from solid-state NMR. J. Mol. Biol. 425:563–76
    [Google Scholar]
  107. 107.  Yao H, Hong M 2014. Conformation and lipid interaction of the fusion peptide of the paramyxovirus PIV5 in anionic and negative-curvature membranes from solid-state NMR. J. Am. Chem. Soc. 136:2611–24
    [Google Scholar]
  108. 108.  Yao H, Lee M, Liao S, Hong M 2016. Solid-state nuclear magnetic resonance investigation of the structural topology and lipid interactions of a viral fusion protein chimera containing the fusion peptide and transmembrane domain. Biochemistry 55:6787–800
    [Google Scholar]
  109. 109.  Yao H, Lee M, Waring A, Wong G, Hong M 2015. Viral fusion protein transmembrane domain adopts β-strand structure to facilitate membrane topological changes for virus-cell fusion. PNAS 112:10926–31
    [Google Scholar]
  110. 110.  Zhou HX, Cross TA 2013. Influences of membrane mimetic environments on membrane protein structures. Annu. Rev. Biophys. 42:361–92
    [Google Scholar]
  111. 111.  Zhou Y, Morais-Cabral JH, Kaufman A, MacKinnon R 2001. Chemistry of ion coordination and hydration revealed by a K+ channel–Fab complex at 2.0 Å resolution. Nature 414:43–48
    [Google Scholar]
/content/journals/10.1146/annurev-biophys-070816-033712
Loading
/content/journals/10.1146/annurev-biophys-070816-033712
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error