Helical membrane protein conformations and their environment

European Biophysics Journal

Volumn 42, Issue 10, 2013, Pages 731-755

  Cross, Timothy A ^a,b   Murray, Dylan T ^a,b   Watts, Anthony ^c  

^a FLORIDA STATE UNIVERSITY   (United States)

^b FLORIDA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Lipids; Membrane protein crystallography; Membrane proteins; Solid state NMR

Indexed keywords

DETERGENT; GLYCINE; LIPID; LIPOSOME; MEMBRANE PROTEIN; WATER;

ALPHA HELIX; CELL MEMBRANE; DIELECTRIC CONSTANT; DISULFIDE BOND; ELECTRON DIFFRACTION; ENDOCYTOSIS; GOLGI COMPLEX; HYDROPHILICITY; HYDROPHOBICITY; LIPID BILAYER; MICELLE; MITOCHONDRIAL MEMBRANE; NUCLEAR MAGNETIC RESONANCE; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN STRUCTURE; REVIEW; SOLID STATE; VIRUS RELEASE; X RAY CRYSTALLOGRAPHY;

CELL MEMBRANE; MEMBRANE PROTEINS; MEMBRANES, ARTIFICIAL; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84896689575     PISSN: 01757571     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00249-013-0925-x     Document Type: Review

References (204)

1. Acharya R, Carnevale V, Fiorin G, Levine BG, Polishchuk AL, Balannik V, Samish I, Lamb RA, Pinto LH, DeGrado WF, Klein ML (2010) Structure and mechanism of proton transport through the transmembrane tetrameric M2 protein bundle of the influenza A virus. Proc Natl Acad Sci USA 107(34):15075-15080. doi: 10.1073/pnas.1007071107
2. Adams MN, Christensen ME, He Y, Waterhouse NJ, Hooper JD (2011) The role of palmitoylation in signalling, cellular trafficking and plasma membrane localization of protease-activated receptor-2. PLoS One 6(11):e28018. doi: 10.1371/journal.pone.0028018
3. Agre P (1999) The aquaporins: blueprints for cellular plumbing systems. FASEB J 13(7):A1520
4. Andreas LB, Eddy MT, Pielak RM, Chou J, Griffin RG (2010) Magic angle spinning NMR investigation of influenza A M2(18-60): support for an allosteric mechanism of inhibition. J Am Chem Soc 132(32):10958-10960. doi: 10.1021/ja101537p
5. Anfinsen CB (1973) Principles that govern the folding of protein chains. Science 181(96):223-230
6. Arumugam S, Pascal S, North CL, Hu W, Lee KC, Cotten M, Ketchem RR, Xu F, Brenneman M, Kovacs F, Tian F, Wang A, Huo S, Cross TA (1996) Conformational trapping in a membrane environment: a regulatory mechanism for protein activity? Proc Natl Acad Sci USA 93(12):5872-5876
7. Baenziger JE, Corringer PJ (2011) 3D structure and allosteric modulation of the transmembrane domain of pentameric ligand-gated ion channels. Neuropharmacology 60(1):116-125. doi: 10.1016/j.neuropharm.2010.08.007
8. Baker SM, Buckheit RW, Falk MM (2010) Green-to-red photoconvertible fluorescent proteins: tracking cell and protein dynamics on standard wide-field mercury arc-based microscopes. BMC Cell Biol 11. doi: 10.1186/1471-2121-11-15
9. Balss J, Papatheodorou P, Mehmel M, Baumeister D, Hertel B, Delaroque N, Chatelain FC, Minor DL Jr, Van Etten JL, Rassow J, Moroni A, Thiel G (2008) Transmembrane domain length of viral K+ channels is a signal for mitochondria targeting. Proc Natl Acad Sci USA 105(34):12313-12318. doi: 10.1073/pnas. 0805709105
10. Barron LD, Hecht L, Wilson G (1997) The lubricant of life: a proposal that solvent water promotes extremely fast conformational fluctuations in mobile heteropolypeptide structure. Biochemistry 36(43):13143-13147. doi: 10.1021/bi971323j
11. Barry CE, Lee RE, Mdluli K, Sampson AE, Schroeder BG, Slayden RA, Yuan Y (1998) Mycolic acids: structure, biosynthesis and physiological functions. Prog Lipid Res 37:143-179
12. Bazzacco P, Billon-Denis E, Sharma KS, Catoire LJ, Mary S, Le Bon C, Point E, Baneres JL, Durand G, Zito F, Pucci B, Popot JL (2012) Nonionic homopolymeric amphipols: application to membrane protein folding, cell-free synthesis, and solution nuclear magnetic resonance. Biochemistry 51(7):1416-1430. doi: 10.1021/bi201862v
13. Bill RM, Henderson PJ, Iwata S, Kunji ER, Michel H, Neutze R, Newstead S, Poolman B, Tate CG, Vogel H (2011) Overcoming barriers to membrane protein structure determination. Nat Biotechnol 29(4):335-340. doi: 10.1038/nbt.1833
14. Botelho AV, Huber T, Sakmar TP, Brown MF (2006) Curvature and hydrophobic forces drive oligomerization and modulate activity of rhodopsin in membranes. Biophys J 91(12):4464-4477. doi: 10.1529/biophysj.106.082776
15. Boura E, Rozycki B, Herrick DZ, Chung HS, Vecer J, Eaton WA, Cafiso DS, Hummer G, Hurley JH (2011) Solution structure of the ESCRT-I complex by small-angle X-ray scattering, EPR, and FRET spectroscopy. Proc Natl Acad Sci USA 108(23):9437-9442. doi: 10.1073/pnas.1101763108
16. Brooks CL 3rd (1998) Simulations of protein folding and unfolding. Curr Opin Struct Biol 8(2):222-226
17. 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(7281):689-692. doi: 10.1038/nature08722
18. Cady S, 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(30):11572-11579. doi: 10.1021/Ja202051n
19. Caffrey RE (2010) A review of experimental design best practices for proteomics based biomarker discovery: focus on SELDI-TOF. Methods Mol Biol 641:167-183. doi: 10.1007/978-1-60761-711-2-10
20. Can TV, Sharma M, Hung I, Gor'kov PL, Brey WW, Cross TA (2012) Magic angle spinning and oriented sample solid-state NMR structural restraints combine for influenza A M2 protein functional insights. J Am Chem Soc 134:9022-9025. doi: 10.1021/ja3004039
21. Cantor RS (1999) Lipid composition and the lateral pressure profile in bilayers. Biophys J 76(5):2625-2639
22. Cevc G, Marsh D (1987) Phospholipid bilayers: physical principles and models, vol 5. Cell Biology. Wiley, New York
23. Cherezov V, Clogston J, Misquitta Y, Abdel-Gawad W, Caffrey M (2002) Membrane protein crystallization in meso: lipid type-tailoring of the cubic phase. Biophys J 83(6):3393-3407. doi: 10.1016/S0006-3495(02)75339-3
24. Clayton GM, Altieri S, Heginbotham L, Unger VM, Morais-Cabral JH (2008) Structure of the transmembrane regions of a bacterial cyclic nucleotide-regulated channel. Proc Natl Acad Sci USA 105(5):1511-1515. doi: 10.1073/pnas.0711533105
25. Cook GA, Opella SJ (2011) Secondary structure, dynamics, and architecture of the p7 membrane protein from hepatitis C virus by NMR spectroscopy. Biochim Biophys Acta 1808(6):1448-1453. doi: 10.1016/j.bbamem.2010.08.010
26. Cross TA, Opella SJ (1994) Solid state NMR structural studies of peptides and proteins in membranes. Curr Opin Struct Biol 4:574-581
27. Cross TA, Sharma M, Yi M, Zhou HX (2011) Influence of solubilizing environments on membrane protein structures. Trends Biochem Sci 36(2):117-125. doi: 10.1016/j.tibs.2010.07.005
28. Das BB, Nothnagel HJ, Lu GJ, Son WS, Tian Y, Marassi FM, Opella SJ (2012) Structure determination of a membrane protein in proteoliposomes. J Am Chem Soc 134(4):2047-2056. doi: 10.1021/ja209464f
29. Dawson JP, Weinger JS, Engelman DM (2002) Motifs of serine and threonine can drive association of transmembrane helices. J Mol Biol 316(3):799-805. doi: 10.1006/jmbi.2001.5353
30. De Angelis AA, Opella SJ (2007) Bicelle samples for solid-state NMR of membrane proteins. Nat Protoc 2(10):2332-2338. doi: 10.1038/nprot.2007.329
31. de Planque MR, Bonev BB, Demmers JA, Greathouse DV, Koeppe RE 2nd, Separovic F, Watts A, Killian JA (2003) Interfacial anchor properties of tryptophan residues in transmembrane peptides can dominate over hydrophobic matching effects in peptide-lipid interactions. Biochemistry 42(18):5341-5348. doi: 10.1021/bi027000r
32. Dill KA, Koppel DE, Cantor RS, Dill JD, Bendedouch D, Chen SH (1984) Molecular-conformations in surfactant micelles. Nature 309(5963):42-45
33. Dong H, Sharma M, Zhou HX, Cross TA (2012) Glycines: role in alpha-helical membrane protein structures and a potential indicator of native conformation. Biochemistry 51(24):4779-4789. doi: 10.1021/bi300090x
34. Dowhan W, Bogdanov M (2009) Lipid-dependent membrane protein topogenesis. Annu Rev Biochem 78:515-540. doi: 10.1146/annurev.biochem.77.060806.091251
35. Drin G, Antonny B (2010) Amphipathic helices and membrane curvature. FEBS Lett 584(9):1840-1847. doi: 10.1016/j.febslet.2009.10.022
36. 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 14:856-861
37. Dupuy AD, Engelman DM (2008) Protein area occupancy at the center of the red blood cell membrane. Proc Natl Acad Sci USA 105(8):2848-2852. doi: 10.1073/pnas.0712379105
38. Earnest TN, Herzfeld J, Rothschild KJ (1990) Polarized Fourier-transform infrared-spectroscopy of bacteriorhodopsin - transmembrane alpha-helices are resistant to hydrogen-deuterium exchange. Biophys J 58(6):1539-1546
39. Esmann M, Watts A, Marsh D (1985) Spin-label studies of lipid-protein interactions in sodium-potassium ATPase membranes from rectal glands of Squalus acanthias. Biochemistry 24(6):1386-1393. doi: 10.1021/bi00327a016
40. Etzkorn M, Raschle T, Hagn F, Gelev V, Rice AJ, Walz T, Wagner G (2013) Cell-free expressed bacteriorhodopsin in different soluble membrane mimetics: biophysical properties and NMR accessibility. Structure 21(3):394-401. doi: 10.1016/j.str.2013.01.005
41. Feng L, Yan H, Wu Z, Yan N, Wang Z, Jeffrey PD, Shi Y (2007) Structure of a site-2 protease family intramembrane metalloprotease. Science 318(5856):1608-1612. doi: 10.1126/science.1150755
42. Finkelstein A (1976) Water and nonelectrolyte permeability of lipid bilayer membranes. J Gen Physiol 68(2):127-135
43. Fretten P, Morris SJ, Watts A, Marsh D (1980) Lipid-lipid and lipid-protein interactions in chromaffin granule membranes: A spin label ESR study. Biochim Biophys Acta (BBA) - Biomembranes. 598 (2):247-259 doi: 10.1016/0005-2736(80)90003-6
44. Fu R, Cross TA (1999) Solid-state nuclear magnetic resonance investigation of protein and polypeptide structure. Annu Rev Biophys Biomol Struct 28:235-268. doi: 10.1146/annurev.biophys.28.1.235
45. Fu R, Wang X, Li C, Santiago-Miranda AN, Pielak GJ, Tian F (2011) In situ structural characterization of a recombinant protein in native Escherichia coli membranes with solid-state magic-angle-spinning NMR. J Am Chem Soc 133(32):12370-12373. doi: 10.1021/ja204062v
46. Fujiyoshi Y (2011) Electron crystallography for structural and functional studies of membrane proteins. J Electron Microsc 60(Suppl 1):S149-S159. doi: 10.1093/jmicro/dfr033
47. Gabrielsen M, Kroner F, Black I, Isaacs NW, Roe AJ, McLuskey K (2011) High-throughput identification of purification conditions leads to preliminary crystallization conditions for three inner membrane proteins. Mol Membr Biol 28(7-8):445-453. doi: 10.3109/09687688.2011.628954
48. Gautier A, Mott HR, Bostock MJ, Kirkpatrick JP, Nietlispach D (2010) Structure determination of the seven-helix transmembrane receptor sensory rhodopsin II by solution NMR spectroscopy. Nat Struct Mol Biol 17(6):768-774. doi: 10.1038/nsmb.1807
49. Gilbert NC, Bartlett SG, Waight MT, Neau DB, Boeglin WE, Brash AR, Newcomer ME (2011) The structure of human 5-lipoxygenase. Science 331(6014):217-219. doi: 10.1126/science.1197203
50. Gonzales EB, Kawate T, Gouaux E (2009) Pore architecture and ion sites in acid-sensing ion channels and P2X receptors. Nature 460(7255):599-604. doi: 10.1038/nature08218
51. Grage SL, Keleshian AM, Turdzeladze T, Battle AR, Tay WC, May RP, Holt SA, Contera SA, Haertlein M, Moulin M, Pal P, Rohde PR, Forsyth VT, Watts A, Huang KC, Ulrich AS, Martinac B (2011) Bilayer-mediated clustering and functional interaction of MscL channels. Biophys J 100(5):1252-1260. doi: 10.1016/j.bpj.2011.01.023
52. Grigorieff N, Ceska TA, Downing KH, Baldwin JM, Henderson R (1996) Electron-crystallographic refinement of the structure of bacteriorhodopsin. J Mol Biol 259(3):393-421. doi: 10.1006/jmbi.1996.0328
53. Gruner SM (1985) Intrinsic curvature hypothesis for biomembrane lipid composition: a role for nonbilayer lipids. Proc Natl Acad Sci USA 82(11):3665-3669
54. 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(5):1919-1925. doi: 10.1021/ja310901f
55. Helfrich W (1973) Elastic properties of lipid bilayers: theory and possible experiments. Zeitschrift fur Naturforschung Teil C: Biochemie, Biophysik, Biologie, Virologie 28(11):693-703
56. Henderson R, Unwin PN (1975) Three-dimensional model of purple membrane obtained by electron microscopy. Nature 257(5521):28-32
57. Hernandez-Guzman FG, Higashiyama T, Pangborn W, Osawa Y, Ghosh D (2003) Structure of human estrone sulfatase suggests functional roles of membrane association. J Biol Chem 278(25):22989-22997. doi: 10.1074/jbc.M211497200
58. Higman VA, Varga K, Aslimovska L, Judge PJ, Sperling LJ, Rienstra CM, Watts A (2011) The conformation of bacteriorhodopsin loops in purple membranes resolved by solid-state MAS NMR spectroscopy. Angew Chem Int Ed Engl. doi: 10.1002/anie.201100730
59. Holdbrook DA, Leung YM, Piggot TJ, Marius P, Williamson PT, Khalid S (2010) Stability and membrane orientation of the fukutin transmembrane domain: a combined multiscale molecular dynamics and circular dichroism study. Biochemistry 49(51):10796-10802. doi: 10.1021/bi101743w
60. Holm PJ, Morgenstern R, Hebert H (2002) The 3-D structure of microsomal glutathione transferase 1 at 6 A resolution as determined by electron crystallography of p22(1)2(1) crystals. Biochim Biophys Acta 1594(2):276-285
61. Hu W, Cross TA (1995) Tryptophan hydrogen-bonding and electric-dipole moments - functional roles in the gramicidin channel and implications for membrane-proteins. Biochemistry 34(43):14147-14155
62. Hu J, Asbury T, Achuthan S, Li C, Bertram R, Quine JR, Fu R, Cross TA (2007a) Backbone structure of the amantadine-blocked trans-membrane domain M2 proton channel from Influenza A virus. Biophys J 92(12):4335-4343. doi: 10.1529/biophysj.106.090183
63. Hu J, Fu R, Cross TA (2007b) The chemical and dynamical influence of the anti-viral drug amantadine on the M2 proton channel transmembrane domain. Biophys J 93(1):276-283. doi: 10.1529/biophysj.106.102103
64. Huang L, McDermott AE (2008) Partial site-specific assignment of a uniformly 13C, 15N enriched membrane protein, light-harvesting complex 1 (LH1), by solid state NMR. Biochim Biophys Acta 1777:1098-1108
65. Hunte C, Richers S (2008) Lipids and membrane protein structures. Curr Opin Struct Biol 18(4):406-411. doi: 10.1016/j.sbi.2008.03.008
66. Inaba K, Murakami S, Nakagawa A, Iida H, Kinjo M, Ito K, Suzuki M (2009) Dynamic nature of disulphide bond formation catalysts revealed by crystal structures of DsbB. EMBO J 28(6):779-791. doi: 10.1038/emboj.2009.21
67. Jacso T, Franks WT, 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. Angew Chem Int Ed Engl 51(2):432-435. doi: 10.1002/anie.201104987
68. Javadpour MM, Eilers M, Groesbeek M, Smith SO (1999) Helix packing in polytopic membrane proteins: role of glycine in transmembrane helix association. Biophys J 77:1609-1618
69. Jeschke G (2012) DEER distance measurements on proteins. Annu Rev Phys Chem 63:419-446. doi: 10.1146/annurev-physchem-032511-143716
70. Judge PJ, Watts A (2011) Recent contributions from solid-state NMR to the understanding of membrane protein structure and function. Curr Opin Chem Biol 15(5):690-695. doi: 10.1016/j.cbpa.2011.07.021
71. Kaiser HJ, Orlowski A, Rog T, Nyholm TK, Chai W, Feizi T, Lingwood D, Vattulainen I, Simons K (2011) Lateral sorting in model membranes by cholesterol-mediated hydrophobic matching. Proc Natl Acad Sci USA 108(40):16628-16633. doi: 10.1073/pnas.1103742108
72. Kalyanasundaram K, Thomas JK (1977) Solvent-dependent fluorescence of pyrene-3-carboxaldehyde and its applications in estimation of polarity at micelle-water interfaces. J Phys Chem-Us 81(23):2176-2180
73. Kamihira M, Watts A (2006) Functionally relevant coupled dynamic profile of bacteriorhodopsin and lipids in purple membranes. Biochemistry 45(13):4304-4313. doi: 10.1021/bi051756j
74. Kamihira M, Vosegaard T, Mason AJ, Straus SK, Nielsen NC, Watts A (2005) Structural and orientational constraints of bacteriorhodopsin in purple membranes determined by oriented-sample solid-state NMR spectroscopy. J Struct Biol 149(1):7-16. doi: 10.1016/j.jsb.2004.10.002
75. Kang C, Li Q (2011) Solution NMR study of integral membrane proteins. Curr Opin Chem Biol 15(4):560-569. doi: 10.1016/j.cbpa.2011.05.025
76. Kawate T, Michel JC, Birdsong WT, Gouaux E (2009) Crystal structure of the ATP-gated P2X(4) ion channel in the closed state. Nature 460(7255):592-598. doi: 10.1038/nature08198
77. Ketchem RR, Hu W, Cross TA (1993) High-resolution conformation of gramicidin A in a lipid bilayer by solid-state NMR. Science 261(5127):1457-1460
78. Ketchem R, Roux B, Cross T (1997) High-resolution polypeptide structure in a lamellar phase lipid environment from solid state NMR derived orientational constraints. Structure 5(12):1655-1669
79. Khare D, Oldham ML, Orelle C, Davidson AL, Chen J (2009) Alternating access in maltose transporter mediated by rigid-body rotations. Mol Cell 33(4):528-536. doi: 10.1016/j.molcel.2009.01.035
80. Killian JA (1998) Hydrophobic mismatch between proteins and lipids in membranes. BBA Rev Biomembranes 1376(3):401-416. doi: 10.1016/S0304-4157(98) 00017-3
81. Killian JA, Nyholm TK (2006) Peptides in lipid bilayers: the power of simple models. Curr Opin Struct Biol 16(4):473-479. doi: S0959-440X(06)00111- 410.1016/j.sbi.2006.06.007
82. Killian JA, von Heijne G (2000) How proteins adapt to a membrane-water interface. Trends Biochem Sci 25(9):429-434
83. Kim S, Cross TA (2002) Uniformity, ideality, and hydrogen bonds in transmembrane alpha-helices. Biophys J 83(4):2084-2095. doi: 10.1016/S0006-3495(02)73969-6
84. Kleiger G, Grothe R, Mallick P, Eisenberg D (2002) GXXXG and AXXXA: common alpha-helical interaction motifs in proteins, particularly in extremophiles. Biochemistry 41(19):5990-5997
85. Klibanov AM (1989) Enzymatic catalysis in anhydrous organic solvents. Trends Biochem Sci 14(4):141-144. doi: 10.1016/0968-0004(89)90146-1
86. Krueger-Koplin RD, Sorgen PL, Krueger-Koplin ST, Rivera-Torres IO, Cahill SM, Hicks DB, Grinius L, Krulwich TA, Girvin ME (2004) An evaluation of detergents for NMR structural studies of membrane proteins. J Biomol NMR 28(1):43-57. doi: 10.1023/B:JNMR.0000012875.80898.8f
87. Lange A, Giller K, Hornig S, Martin-Eauclaire MF, Pongs O, Becker S, Baldus M (2006) Toxin-induced conformational changes in a potassium channel revealed by solid-state NMR. Nature 440(7086):959-962. doi: 10.1038/nature04649
88. Lee AG (2003) Lipid-protein interactions in biological membranes: a structural perspective. Biochim Biophys Acta 1612(1):1-40
89. Lee MC, Orci L, Hamamoto S, Futai E, Ravazzola M, Schekman R (2005) Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle. Cell 122(4):605-617. doi: 10.1016/j.cell.2005.07.025
90. Li C, Gao P, Qin H, Chase R, Gor'kov PL, Brey WW, Cross TA (2007) Uniformly aligned full-length membrane proteins in liquid crystalline bilayers for structural characterization. J Am Chem Soc 129(17):5304-5305. doi: 10.1021/ja068402f
91. Li Y, Berthold DA, Gennis RB, Rienstra CM (2008) Chemical shift assignment of the transmembrane helices of DsbB, a 20-kDa integral membrane enzyme, by 3D magic-angle spinning NMR spectroscopy. Protein Sci Publ Protein Soc 17(2):199-204. doi: 10.1110/ps.073225008
92. Liao J, Li H, Zeng W, Sauer DB, Belmares R, Jiang Y (2012) Structural insight into the ion-exchange mechanism of the sodium/calcium exchanger. Science 335(6069):686-690. doi: 10.1126/science.1215759
93. Lin SM, Tsai JY, Hsiao CD, Huang YT, Chiu CL, Liu MH, Tung JY, Liu TH, Pan RL, Sun YJ (2012) Crystal structure of a membrane-embedded H+-translocating pyrophosphatase. Nature 484(7394):399-403. doi: 10.1038/nature10963
94. Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327(5961):46-50. doi: 10.1126/science.1174621
95. Lipfert J, Columbus L, Chu VB, Lesley SA, Doniach S (2007) Size and shape of detergent micelles determined by small-angle X-ray scattering. J Phys Chem B 111(43):12427-12438. doi: 10.1021/jp073016l
96. Long AR, O'Brien CC, Malhotra K, Schwall CT, Albert AD, Watts A, Alder NN (2013) A detergent-free strategy for the reconstitution of active enzyme complexes from native biological membranes into nanoscale discs. BMC Biotechnol 13:41. doi: 10.1186/1472-6750-13-41
97. Lu M, Fu D (2007) Structure of the zinc transporter YiiP. Science 317(5845):1746-1748. doi: 10.1126/science.1143748
98. Marassi FM, Das BB, Lu GJ, Nothnagel HJ, Park SH, Son WS, Tian Y, Opella SJ (2011) Structure determination of membrane proteins in five easy pieces. Methods 55(4):363-369. doi: 10.1016/j.ymeth.2011.09.009
99. Marius P, Zagnoni M, Sandison ME, East JM, Morgan H, Lee AG (2008) Binding of anionic lipids to at least three nonannular sites on the potassium channel KcsA is required for channel opening. Biophys J 94(5):1689-1698. doi: 10.1529/biophysj.107.117507
100. Marius P, de Planque MR, Williamson PT (2012a) Probing the interaction of lipids with the non-annular binding sites of the potassium channel KcsA by magic-angle spinning NMR. Biochim Biophys Acta 1818(1):90-96. doi: 10.1016/j.bbamem.2011.09.017
101. Marius P, Leung YM, Piggot TJ, Khalid S, Williamson PT (2012b) Probing the oligomeric state and interaction surfaces of Fukutin-I in dilauroylphosphatidylcholine bilayers. Euro Biophys J EBJ 41(2):199-207. doi: 10.1007/s00249-011-0773-5
102. Marsh D (2001) Polarity and permeation profiles in lipid membranes. Proc Natl Acad Sci USA 98(14):7777-7782. doi: 10.1073/pnas.131023798
103. Marsh D (2007) Lateral pressure profile, spontaneous curvature frustration, and the incorporation and conformation of proteins in membranes. Biophys J 93(11):3884-3899. doi: 10.1529/biophysj.107.107938
104. Marsh D (2008) Energetics of hydrophobic matching in lipid-protein interactions. Biophys J 94(10):3996-4013. doi: 10.1529/biophysj.107.121475
105. Marsh D, Pali T (2013) Orientation and conformation of lipids in crystals of transmembrane proteins. Euro Biophys J EBJ 42(2-3):119-146. doi: 10.1007/s00249-012-0816-6
106. Marsh D, Watts A (1982) Spin-labelling and lipid-protein interactions in membranes. In: Jost PC, Griffith OH (eds) Lipid-protein interactions. Wiley, New York
107. Maslennikov I, Klammt C, Hwang E, Kefala G, Okamura M, Esquivies L, Mors K, Glaubitz C, Kwiatkowski W, Jeon YH, Choe S (2010) Membrane domain structures of three classes of histidine kinase receptors by cell-free expression and rapid NMR analysis. Proc Natl Acad Sci USA 107(24):10902-10907. doi: 10.1073/pnas.1001656107
108. Mathai JC, Sprott GD, Zeidel ML (2001) Molecular mechanisms of water and solute transport across archaebacterial lipid membranes. J Biol Chem 276(29):27266-27271
109. McLuskey K, Roszak AW, Zhu Y, Isaacs NW (2010) Crystal structures of all-alpha type membrane proteins. Euro Biophys J EBJ 39(5):723-755. doi: 10.1007/s00249-009-0546-6
110. Menger FM, Boyer BJ (1980) Water penetration into micelles as determined by optical-rotary dispersion. J Am Chem Soc 102(18):5936-5938
111. Miao Y, Qin H, Fu R, Sharma M, Can TV, Hung I, Luca S, Gor'kov PL, Brey WW, Cross TA (2012) M2 proton channel structural validation from full-length protein samples in synthetic bilayers and E. coli membranes. Angew Chem Int Ed Engl 51:8383-8386. doi: 10.1002/anie.201204666
112. Muller SA, Muller DJ, Engel A (2011) Assessing the structure and function of single biomolecules with scanning transmission electron and atomic force microscopes. Micron 42(2):186-195. doi: 10.1016/j.micron.2010.10.002
113. Murray DT, Das N, Cross TA (2013) Solid state NMR strategy for characterizing native membrane protein structures. Acc Chem Res. doi: 10.1021/ar3003442
114. Nakamura T, Shinoda W, Ikeshoji T (2011) Novel numerical method for calculating the pressure tensor in spherical coordinates for molecular systems. J Chem Phys 135(9):094106. doi: 10.1063/1.3626410
115. Nath A, Atkins WM, Sligar SG (2007) Applications of phospholipid bilayer nanodiscs in the study of membranes and membrane proteins. Biochemistry 46(8):2059-2069. doi: 10.1021/bi602371n
116. Negishi L, Mitaku S (2011) Electrostatic effects influence the formation of two-dimensional crystals of bacteriorhodopsin reconstituted into dimyristoylphosphatidylcholine membranes. J Biochem 150(1):113-119. doi: 10.1093/jb/mvr043
117. Nishimura K, Kim S, Zhang L, Cross TA (2002) The closed state of a H+ channel helical bundle: combining precise orientational and distance restraints from solid state NMR. Biochemistry 41:13170-13177
118. Nymeyer H, Zhou HX (2008) A method to determine dielectric constants in nonhomogeneous systems: application to biological membranes. Biophys J 94(4):1185-1193. doi: 10.1529/biophysj.107.117770
119. Orwick M, Lovett JE, Graziadei A, Lindholm L, Hicks M, Watts A (2012a) Detergent-free incorporation of a seven-transmembrane receptor protein into nanosized bilayer Lipodisq particles for functional and biophysical studies. Nano Lett
120. Orwick MC, Judge PJ, Procek J, Lindholm L, Graziadei A, Engel A, Grobner G, Watts A (2012b) Detergent-free formation and physicochemical characterization of nanosized lipid-polymer complexes: lipodisq. Angew Chem Int Ed Engl 51(19):4653-4657. doi: 10.1002/anie.201201355
121. Page RC, Kim S, Cross TA (2008) Transmembrane helix uniformity examined by spectral mapping of torsion angles. Structure 16(5):787-797. doi: 10.1016/j.str.2008.02.018
122. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Le Trong I, Teller DC, Okada T, Stenkamp RE, Yamamoto M, Miyano M (2000) Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289(5480):739-745
123. Park SH, Opella SJ (2005) Tilt angle of a trans-membrane helix is determined by hydrophobic mismatch. J Mol Biol 350(2):310-318. doi: 10.1016/j.jmb.2005.05.004
124. Park SH, Das BB, Casagrande F, Tian Y, Nothnagel HJ, Chu M, Kiefer H, Maier K, De Angelis AA, Marassi FM, Opella SJ (2012) Structure of the chemokine receptor CXCR1 in phospholipid bilayers. Nature 491(7426):779-783. doi: 10.1038/nature11580
125. Payandeh J, Scheuer T, Zheng N, Catterall WA (2011) The crystal structure of a voltage-gated sodium channel. Nature 475(7356):353-358. doi: 10.1038/nature10238
126. Pebay-Peyroula E, Rosenbusch JP (2001) High-resolution structures and dynamics of membrane protein-lipid complexes: a critique. Curr Opin Struct Biol 11(4):427-432
127. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, Evans PR, McMahon HT (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303(5657):495-499. doi: 10.1126/science.1092586
128. Phillips R, Ursell T, Wiggins P, Sens P (2009) Emerging roles for lipids in shaping membrane-protein function. Nature 459(7245):379-385. doi: 10.1038/nature08147
129. Pielak RM, Chou JJ (2010) Solution NMR structure of the V27A drug resistant mutant of influenza A M2 channel. Biochem Biophys Res Commun 401(1):58-63. doi: 10.1016/j.bbrc.2010.09.008
130. Pinkett HW, Lee AT, Lum P, Locher KP, Rees DC (2007) An inward-facing conformation of a putative metal-chelate-type ABC transporter. Science 315(5810):373-377. doi: 10.1126/science.1133488
131. Podo F, Ray A, Nemethy G (1973) Structure and hydration of nonionic detergent micelles - high-resolution nuclear magnetic-resonance study. J Am Chem Soc 95(19):6164-6171
132. Popot JL, Engelman DM (2000) Helical membrane protein folding, stability, and evolution. Annu Rev Biochem 69:881-922. doi: 10.1146/annurev.biochem.69.1. 881
133. Powl AM, East JM, Lee AG (2008) Anionic phospholipids affect the rate and extent of flux through the mechanosensitive channel of large conductance MscL. Biochemistry 47(14):4317-4328. doi: 10.1021/bi702409t
134. Raja M, Spelbrink RE, de Kruijff B, Killian JA (2007) Phosphatidic acid plays a special role in stabilizing and folding of the tetrameric potassium channel KcsA. FEBS Lett 581(29):5715-5722. doi: 10.1016/j.febslet.2007.11.039
135. Raschle T, Hiller S, Etzkorn M, Wagner G (2010) Nonmicellar systems for solution NMR spectroscopy of membrane proteins. Curr Opin Struct Biol 20(4):471-479. doi: 10.1016/j.sbi.2010.05.006
136. Reichow SL, Gonen T (2009) Lipid-protein interactions probed by electron crystallography. Curr Opin Struct Biol 19(5):560-565. doi: 10.1016/j.sbi.2009. 07.012
137. Renault M, Tommassen-van Boxtel R, Bos MP, Post JA, Tommassen J, Baldus M (2012) Cellular solid-state nuclear magnetic resonance spectroscopy. Proc Natl Acad Sci USA 109(13):4863-4868. doi: 10.1073/pnas.1116478109
138. Robinson A, Lorch M, Batchelor R (2011) Stabilizing membrane proteins in detergent and lipid systems in production of membrane proteins: strategies for expression and isolation. Wiley, New York
139. 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(5713):1317-1321. doi: 10.1126/science.1106392
140. Rosenbaum DM, Rasmussen SG, Kobilka BK (2009) The structure and function of G-protein-coupled receptors. Nature 459(7245):356-363. doi: 10.1038/nature08144
141. Rossman JS, Lamb RA (2011) Influenza virus assembly and budding. Virology 411(2):229-236. doi: 10.1016/j.virol.2010.12.003
142. Rossman JS, Jing XH, Leser GP, Lamb RA (2010) Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 142(6):902-913. doi: 10.1016/j.cell.2010.08.029
143. Rothman JE, Lenard J (1977) Membrane asymmetry. Science 195(4280):743-753
144. Russ WP, Engelman DM (2000) The GxxxG motif: a framework for transmembrane helix-helix association. J Mol Biol 296(3):911-919. doi: 10.1006/jmbi.1999.3489
145. Sabra MC, Uitdehaag JC, Watts A (1998) General model for lipid-mediated two-dimensional array formation of membrane proteins: application to bacteriorhodopsin. Biophys J 75(3):1180-1188. doi: 10.1016/S0006-3495(98)74037-8
146. Sanders CR, Mittendorf KF (2011) Tolerance to changes in membrane lipid composition as a selected trait of membrane proteins. Biochemistry 50(37):7858-7867. doi: 10.1021/bi2011527
147. Scheiffele P, Roth MG, Simons K (1997) Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J 16(18):5501-5508
148. Schnell JR, Chou JJ (2008) Structure and mechanism of the M2 proton channel of influenza A virus. Nature 451(7178):591-595. doi: 10.1038/nature06531
149. Schroeder C, Heider H, Moncke-Buchner E, Lin TI (2005) The influenza virus ion channel and maturation cofactor M2 is a cholesterol-binding protein. Eur Biophys J Biophys 34(1):52-66. doi: 10.1007/s00249-004-0424-1
150. Schulz GE (2011) A new classification of membrane protein crystals. J Mol Biol 407(5):640-646. doi: 10.1016/j.jmb.2011.02.003
151. Seelig J, Browning JL (1978) General features of phospholipid conformation in membranes. FEBS Lett 92(1):41-44
152. Seelig A, Seelig J (1974) The dynamic structure of fatty acyl chains in a phospholipid bilayer measured by deuterium magnetic resonance. Biochemistry 13(23):4839-4845
153. Selmi DN, Adamson RJ, Attrill H, Goddard AD, Gilbert RJ, Watts A, Turberfield AJ (2011) DNA-templated protein arrays for single-molecule imaging. Nano Lett 11(2):657-660. doi: 10.1021/nl1037769
154. Separovic F, Killian JA, Cotten M, Busath DD, Cross TA (2011) Modeling the membrane environment for membrane proteins. Biophys J 100(8):2073-2074. doi: 10.1016/j.bpj.2011.02.058
155. Sharma M, Yi M, Dong H, Qin H, Peterson E, Busath DD, Zhou HX, Cross TA (2010) Insight into the mechanism of the influenza A proton channel from a structure in a lipid bilayer. Science 330(6003):509-512. doi: 10.1126/science.1191750
156. Shi L, Ladizhansky V (2012) Magic angle spinning solid-state NMR experiments for structural characterization of proteins. Methods Mol Biol 895:153-165. doi: 10.1007/978-1-61779-927-3-12
157. Simon SA, McIntosh TJ, Latorre R (1982) Influence of cholesterol on water penetration into bilayers. Science 216(4541):65-67
158. Simons K, Sampaio JL (2011) Membrane organization and lipid rafts. CSH Perspect Biol 3(10). doi 10.1101/cshperspect.a004697
159. Sivertsen AC, Bayro MJ, Belenky M, Griffin RG, Herzfeld J (2009) Solid-state NMR evidence for inequivalent GvpA subunits in gas vesicles. J Mol Biol 387(4):1032-1039. doi: 10.1016/j.jmb.2009.02.015
160. Sixl F, Watts A (1982) Interactions between phospholipid head groups at membrane interfaces: a deuterium and phosphorus nuclear magnetic resonance and spin-label electron spin resonance study. Biochemistry 21(25):6446-6452
161. Sobolevsky AI, Rosconi MP, Gouaux E (2009) X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 462(7274):745-756. doi: 10.1038/nature08624
162. Sonntag Y, Musgaard M, Olesen C, Schiott B, Moller JV, Nissen P, Thogersen L (2011) Mutual adaptation of a membrane protein and its lipid bilayer during conformational changes. Nat Commun 2:304. doi: 10.1038/ncomms1307
163. Stansfeld PJ, Jefferys EE, Sansom MS (2013) Multiscale simulations reveal conserved patterns of lipid interactions with aquaporins. Structure 21(5):810-819. doi: 10.1016/j.str.2013.03.005
164. Steffen MA, Lao KQ, Boxer SG (1994) Dielectric asymmetry in the photosynthetic reaction-center. Science 264(5160):810-816
165. Steinbacher S, Bass R, Strop P, Rees DC (2007) Structures of the prokaryotic mechanosensitive channels MscL and MscS. Curr Top Membr 58:1-24
166. Stern HA, Feller SE (2003) Calculation of the dielectric permittivity profile for a nonuniform system: application to a lipid bilayer simulation. J Chem Phys 118(7):3401-3412. doi: 10.1063/1.1537244
167. Sternberg B, Gale P, Watts A (1989) The effect of temperature and protein content on the dispersive properties of bacteriorhodopsin from H. halobium in reconstituted DMPC complexes free of endogenous purple membrane lipids: a freeze-fracture electron microscopy study. Biochim Biophys Acta 980:117-126
168. Sternberg B, L'Hostis C, Whiteway CA, Watts A (1992) The essential role of specific Halobacterium halobium polar lipids in 2D-array formation of bacteriorhodopsin. Biochim Biophys Acta 1108(1):21-30
169. Sternberg B, Watts A, Cejka Z (1993) Lipid-induced modulation of the protein packing in two-dimensional crystals of bacteriorhodopsin. J Struct Biol 110:196-204
170. Stockton GW, Johnson KG, Butler K, Tulloch AP, Boulanger Y, Smith ICP, Davis JH, Bloom M (1977) Deuterium NMR study of lipid organisation in Acholeplasma laidlawiimembranes. Nature 269:267-268
171. Stouffer AL, Acharya R, Salom D, Levine AS, Di Costanzo L, Soto CS, Tereshko V, Nanda V, Stayrook S, DeGrado WF (2008) Structural basis for the function and inhibition of an influenza virus proton channel. Nature 451:596-599
172. Strandberg E, Ozdirekcan S, Rijkers DT, van der Wel PC, Koeppe RE 2nd, Liskamp RM, Killian JA (2004) Tilt angles of transmembrane model peptides in oriented and non-oriented lipid bilayers as determined by 2H solid-state NMR. Biophys J 86(6):3709-3721. doi: 10.1529/biophysj.103.03540286/6/3709
173. Su Y, Hong M (2011) Conformational disorder of membrane peptides investigated from solid-state NMR line widths and line shapes. J Phys Chem B 115(36):10758-10767. doi: 10.1021/jp205002n
174. Sulistijo ES, Mackenzie KR (2009) Structural basis for dimerization of the BNIP3 transmembrane domain. Biochemistry 48(23):5106-5120. doi: 10.1021/bi802245u
175. Tamm LK, Liang B (2006) NMR of membrane proteins in solution. Prog Nucl Magn Reson Spectrosc 48:201-210
176. Tanford C (1973) The hydrophobic effect: formation of micelles and biological membranes. Wiley, New York
177. Tieleman DP, Marrink SJ, Berendsen HJ (1997) A computer perspective of membranes: molecular dynamics studies of lipid bilayer systems. Biochim Biophys Acta 1331(3):235-270
178. Timasheff SN (1993) The control of protein stability and association by weak interactions with water: how do solvents affect these processes? Annu Rev Biophys Biomol Struct 22:67-97
179. Traüble H (1971) Movement of molecules across lipid membranes - molecular theory. J Membrane Biol 4(2):193
180. Turro NJ, Okubo T (1981) Micellar micro-viscosity of ionic surfactants under high-pressure. J Am Chem Soc 103(24):7224-7228
181. Ujwal R, Bowie JU (2011) Crystallizing membrane proteins using lipidic bicelles. Methods 55(4):337-341. doi: 10.1016/j.ymeth.2011.09.020
182. van den Brink, van der Laan E, Killian JA, de Kruijff B (2004) Nonbilayer lipids affect peripheral and integral membrane proteins via changes in the lateral pressure profile. Biochim Biophys Acta 1666 (1-2):275-288. doi: 10.1016/j.bbamem.2004.06.010
183. Van Horn WD, Kim HJ, Ellis CD, Hadziselimovic A, Sulistijo ES, Karra MD, Tian C, Sonnichsen FD, Sanders CR (2009) Solution nuclear magnetic resonance structure of membrane-integral diacylglycerol kinase. Science 324(5935):1726-1729. doi: 10.1126/science.1171716
184. van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9(2):112-124. doi: 10.1038/nrm2330
185. Verardi R, Shi L, Traaseth NJ, Walsh N, Veglia G (2011) Structural topology of phospholamban pentamer in lipid bilayers by a hybrid solution and solid-state NMR method. Proc Natl Acad Sci USA 108(22):9101-9106. doi: 10.1073/pnas.1016535108
186. Verkleij AJ, Zwaal RF, Roelofsen B, Comfurius P, Kastelijn D, van Deenen LL (1973) The asymmetric distribution of phospholipids in the human red cell membrane. A combined study using phospholipases and freeze-etch electron microscopy. Biochim Biophys Acta 323(2):178-193
187. Vinothkumar KR, Henderson R (2010) Structures of membrane proteins. Q Rev Biophys 43(1):65-158. doi: 10.1017/S0033583510000041
188. von Heijne G (1992) Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J Mol Biol 225(2):487-494
189. Watts A (1998) Solid-state NMR approaches for studying the interaction of peptides and proteins with membranes. Biochim Biophys Acta 1376(3):297-318
190. Watts A, Venien-Bryan C, Sami M, Whiteway C, Boulter J, Sternberg B (1993) Lipid-protein interactions in controlled membrane protein array and crystal formation. In: Watts A (ed) Protein lipid interactions, new comprehensive biochemistry. Elsevier, Amsterdam, pp 351-370
191. Watts A, Straus SK, Grage S, Kamihira M, Lam YH, Xhao Z (2004) Membrane protein structure determination using solid state NMR. In: Downing K (ed) Methods in molecular biology - techniques in protein NMR, vol 278. Humana, New Jersey, pp 403-474
192. White SH, Wiener MC (1996) The liquid-crystalline structure of fluid lipid bilayer membranes. In: Merz KM, Roux B (eds) Biological membranes: a molecular perspective from computation and experiment. Birkhauser, Boston, pp 127-144
193. Wiener MC, White SH (1992) Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of x-ray and neutron diffraction data III. Complete structure. Biophys J 61(2):434-447. doi: 10.1016/S0006-3495(92)81849-0
194. Wisedchaisri G, Reichow SL, Gonen T (2011) Advances in structural and functional analysis of membrane proteins by electron crystallography. Structure 19(10):1381-1393. doi: 10.1016/j.str.2011.09.001
195. Xu F, Cross TA (1999) Water: foldase activity in catalyzing polypeptide conformational rearrangements. Proc Natl Acad Sci USA 96(16):9057-9061
196. Xu F, Wang A, Vaughn JB Jr, Cross TA (1996) A catalytic role for protic solvents in conformational interconversion. J Am Chem Soc 118:9176-9177
197. Zaccai G (2000) How soft is a protein? A protein dynamics force constant measured by neutron scattering. Science 288(5471):1604-1607
198. Zhang J, Pekosz A, Lamb RA (2000) Influenza virus assembly and lipid raft microdomains: a role for the cytoplasmic tails of the spike glycoproteins. J Virol 74(10):4634-4644
199. Zhang H, Kurisu G, Smith JL, Cramer WA (2003) A defined protein-detergent-lipid complex for crystallization of integral membrane proteins: the cytochrome b6f complex of oxygenic photosynthesis. Proc Natl Acad Sci USA 100(9):5160-5163. doi: 10.1073/pnas.0931431100
200. Zhang P, Wang J, Shi Y (2010) Structure and mechanism of the S component of a bacterial ECF transporter. Nature 468(7324):717-720. doi: 10.1038/nature09488
201. Zhou HX (2009) Crowding effects of membrane proteins. J Phys Chem B 113(23):7995-8005. doi: 10.1021/jp8107446
202. Zhou HX, Cross T (2013a) Influences of membranes mimetic environments on membrane proteins structures. Annu Rev Biophys 42(16):1-32
203. Zhou HX, Cross TA (2013b) Modeling the membrane environment has implications for membrane protein structure and function: influenza A M2 protein. Protein Sci Publ Protein Soc 22(4):381-394. doi: 10.1002/pro.2232
204. Zhou Y, Cierpicki T, Jimenez RH, Lukasik SM, Ellena JF, Cafiso DS, Kadokura H, Beckwith J, Bushweller JH (2008) NMR solution structure of the integral membrane enzyme DsbB: functional insights into DsbB-catalyzed disulfide bond formation. Mol Cell 31(6):896-908. doi: 10.1016/j.molcel.2008.08.028