PDB ID or protein name

Comparison with experimental data

The results of our calculations are consistent with experimental studies of 24 transmembrane and 42 peripheral proteins. The experimental approaches included X-ray scattering of native biological membranes (XSC); hydrophobic matching studies (HM), neutron diffraction (ND), electron cryo-microscopy (EM), chemical modification (CM), fluorescence (FL), spin labeling (SL), attenuated total reflection fourier transform infrared spectroscopy(ATR FTIR) and NMR.

Table 2a. Comparison of computational results for transmembrane proteins with experimental studies of protein orientations in membranes.
Protein PDB id Method Reference
Rhodopsin 1gzm XSC, SL, CL, EM Blaurock and Wilkins 1972; Barclay and Findlay 1984, Davison and Findlay 1986a,b; Hubbell et al. 2003, Krebs et al. 2003
Bacteriorhodopsin 1py6   SL, NMR, HM Altenbach et al. 1990, 1994; Piknova et al. 1993; Dumas et al. 1999; Greenhalgh et al. 1991; Kamihira et al. 2005
Sensory rhodopsin II 1h2s SL Wegener et al. 2000
Photoreaction center from Rh. Spaeroides 1rzh XSC, HM, ND Pape et al. 1974; Riegler and Mohwald 1986, Roth et al. 1991
Photoreaction center from Rh. Viridis 1dxr ND Roth et al. 1989
Cytochrome c oxidase 1v55 HM Montecucco et al. 1982
V-type Na+-ATPase 1yce EM Vonck et al., 2002
Ca2+-ATPase 2agv HM Cornea and Thomas 1994, Lee 1998
Protein translocase SecY 1rh5 EM Breyton et al., 2002
Lactose permease LacY 2cfp CL, SL, ATR FTIR Voss et al. 1996, LeCoutre et al. 1997, Frilingos et al. 1998, Kwaw 2001, Venkatesan 2000a,b,c, Zhang et al. 2003, Zhao et al. 1999, Guan et al. 2002, Ermolova et al. 2003
Na+/H+ antiporter 1zcd SL Hilger et al. 2005
Phospholamban  1zll ATR FTIR Arkin et al. 1995
K+ channel KcsA 1r3j SL, HM, ATR FTIR Perozo et al. 1998; LeCoutre et al. 1998; Gross et al. 1999; Gross and Hubbell 2002; Williamson et al. 2002, 2003;
MscL channel 1msl SL, FL, HM Perozo et al. 2001; Powl et al. 2003, 2005
Acetylcholine receptor 2bg9 FL Chattopadhyay and McNamee 1991
OmpA 1qjp FL, ATR FTIR Kleinschmidt and Tamm 1999; Ramakrishnan et al. 2005
OmpX 1qj8 NMR Fernandez et al., 2002
OmpLA phospholipase 1qd6 ND Snijder et al. 2003
OmpF trimeric porin 1hxx HM, ND O’Keeffe et al. 2000,; Pebay-Peyrola et al. 1995
FhuA receptor 1qfg ATR FTIR Ramakrishnan et al. 2005
BtuB transporter 1nqe SL Fanucci et al. 2002
FepA receptor 1fep SL Klug et al. 1997
α-hemolysin 7ahl FL Raja et al. 1999
Gramicidin A 1grm HM, NMR, ATR FTIR Nabedryk et al., 1982; Elliott et al. 1983; Harroun et al. 1999; Andronesi et al., 2004; Andersen et al., 2005; Kota et al. 2004


Table 2b. Comparison of computational results for peripheral proteins with experimental studies of protein orientations in membranes.
Protein superfamily PDB id References
Signal peptidase 1kn9 Kim et al. 1995
Cytochrome c 1hrc Kostrewa et al. 2000
Annexins 1a8a, 1dm5 Campos et al. 1998; Isas et al. 2004
Heme-dependent peroxidases 1q4g Spencer et al. 1999
Phospholipase A2 1poa, 1poc, 1n28, 1vap, 1le6 Lin et al. 1998; Bollinger et al. 2004; Stahelin and Cho 2001; Canaan et al. 2002; Stahelin and Cho 2001; Bezzine et al. 2002; Sumandea et al. 1999; Lathrop et al. 2001
Lysophospholipase-like 1cjy Stahelin and Cho 2001
15-Lipoxygenase 1lox Walther et al. 2004
8R-Lipoxygenase 1zq4 Oldham et al. 2005
Phospholipase C 1ca1, 1gyg Jepson et al. 2001
C2 domain 1dsy, 1rsy, 1uov, 1rlw, 1gmi, 1a25, 1d5r Mamberg et al., 2003; Frazier et al., 2003; Kohout et al., 2003; Rufener et al., 2005; Corbalan-Garcia et al. 2003; Gerber et al. 2002; Nalefski et al. 2001; Das et al. 2003
C1 domain 1ptr, 1faq Wang et al. 2001; Johnson and Cornell 1999
ENTH/VHS domain 1h0a Stahelin et al. 2003
PX domain 1h6h, 1o7k, 1kq6 Stahelin et al. 2003
PH domain 1mai Wang et al. 1999
Galactose-binding domain-like 1sdd, 1d7p, 1czs Koppaka and Lenz 1996; Peng et al. 2005; Gilbert et al. 2002; Kim et al. 2000
Anemone cytolysin 1iaz Abderluh et al. 2005
PLC-like phosphodiesterases 2ptd, 1djx Feng et al. 2003; Ananthanarayanan et al. 2002
PreATP-grasp domain 1auv Cheetham et al. 2001
FAD-linked reductases 1coy Chen et al. 2000
Perfringolysin 1pfo Ramachandran et al. 2005
Omega toxin-like 1d1h, 1s6x Phillips et al. 2005; Jung et al. 2005, 2006
Scorpion toxin-like 2crd Ben-Tal et al. 1997
Snake toxin-like 1ffj, 1h0j, 1tgx Dubovskii et al. 2001; Huang et al. 2003; Batenburg et al. 1985
GLA-domain 1dan, 1pfx, 1lqv McCalllum et al. 1996; Mutucumarana et al. 1992; Yegneswaran et al. 1997; Zaal et al. 1998
FYVE/PHD zinc finger 1hyi, 1vfy Kutateladze and Overduin, 2001, Brunecky et al. 2005, Blatner et al. 2004
Peptaibols 1amt, 1ih9, 1joh Barranger-Mathys and Cafiso 1996, Bak et al. 2001; Bechinger et al. 2001, Kropacheva et al. 2005
Lantibiotic peptides 1wco van der Hooven et al. 1996, Hsu et al. 2002, 2004, Bonev et al. 2000
Lactoferricin B 1lfc Nguen et al. 2005
Magainin 2mag Matsuzaki et al. 1994; Marassi et al. 2000
Surfactant protein C 1spf Plasencia et al. 2004
Macrocyclic bacteriocins 1pxq Thennarasu et al. 2005
Peptide hormones 1icy Thomas et al. 2005
Alpha-synuclein 1xq8 Jao et al. 2004
Alpha-toxin 1olp Clark et al. 2003
Daptomycin 1t5n Lakey and Ptak 1998
Cyclotides 1nb1 Kamimori et al. 2005
Octreotide 1soc Beschiaschvili and Seelig 1992
Alpha/beta-hydrolases 1eth Tsujita and Brockman 1987
Gramicidin S 1tk2 Abraham et al. 2005
 

Comparison with hydrophobic thicknesses of artificial bilayers that provide maximal biological activity of a transmembrane protein, maximal lipid-protein binding affinity, or whose temperature of phase transition was not affected by the protein



Table 3. Comparison of calculated hydrophobic thicknesses of TM proteins (Dcalc) and thicknesses of matching artificial membranes (Dexper).

Proteins
PDB id
Dcalc (Å)
Dexper (Å)a
References
Gramicidin A
22.5±1.2
~22
Elliott et al. 1983; Harroun et al. 1999
OmpF trimeric channel
24.2±0.8
~21
O’Keeffe et al. 2000
KcsA potassium channel
33.1±1.0
~34
Williamson et al. 2002, 2003

Ca2+-ATPase, E2 state (Ca-free)

29.0±1.5
~27
Cornea and Thomas 1994, Lee 1998

Ca2+-ATPase, E2·Pi state

30.0±1.5

Ca2+-ATPase, E1·2Ca state

29.0±2.8

Ca2+-ATPase, E1·ATP state

27.0±1.2

Ca2+-ATPase, E1P·ADP state

30.5±1.0
MscL mechanosensitive channel
26.5±3.8
24-25
Powl et al. 2003, 2005
Bacteriorhodopsin
31.0±2.5
~32
Piknova et al. 1993, Dumas et al. 1999

Cytochrome c oxidase

25.4±1.8
~27
Montecucco et al. 1982

Photoreaction center

30.0±1.2
~30
Riegler and Mohwald 1986
35 ±5
Pape et al. 1974
Rhodopsin
32.4±1.7
~30
Blaurock and Wilkins 1972

aDexper values are obtained by subtracting 10 Å (Nagle and Tristam-Nagle 2000) from the phosphate-to-phosphate distances determined by X-ray scattering for the matching lipid bilayers (Lewis and Engelman, 1983,Dumas et al. 1999).

Blaurock A.E. and Wilkins M.H.F. (1972) Structure of retinal photoreceptor membranes. Nature 236: 313-314.

Cornea, R.L., and Thomas, D.D. (1994) Effect of membrane thickness on the molecular dynamics and enzymatic activity of recobnstituted Ca-ATPase. Biochemistry 33: 2912-2920.

Dumas F., Lebrun M.C., and Tocanne J.F. (1999) Is the protein/lipid hydrophobic matching principle relevant to membrane organization and functions? FEBS Lett.458: 271-277.

Eliott J.R., Needham D., Dilger J.P., and Haydon D.A. (1983) The effects of bilayer thickness and tension on gramicidin single-channel lifetime.  Biochim. Biophys. Acta 735: 95-103.

Harroun T.A., Heller W.T., Weiss T.M., Yang L., and Huang H.W. (1999) Experimental evidence for hydrophobic matching and membrane-mediated interactions in lipid bilayers containing gramicidin. Biophys. J. 76: 937-945.

Lee A.G. (1998) How lipids interact with an intrinsic membrane protein: the case of the calcium pump. Biochim. Biophys. Acta 1376: 381-390.

Lee A.G.(2003)Lipid-protein interactions in biological membranes: a structural perspective.  Biochim. Biophys. Acta 1612: 1-40.

Lee A.G. (2004) How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta 1666: 62-87.

Lewis, B.A., and Engelman, D.M. (1983) Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles. J Mol Biol. 166: 211-217.

O"Keeffe A.H., East J.M., and Lee A.G. (2000) Selectivity in lipid binding to the bacterial outer membrane protein OmpF. Biophys. J.79: 2066-2074.

Montecucco C., Smith G.A., Dabbeni-sala F., Johansson A., Galante Y.M. and Bisson R. (1982) Bilayer thickness and enzymatic activity in the mitochondrial cytochrome c oxidase and ATPase complex. FEBS Lett. 144: 145-148.

Nagle, J.F., and Tristram-Nagle, S. 2000. Structure of lipid bilayers. Biochim. Biophys. Acta 1469: 159-195.

Pape E.H., Menke W., Weick D., and Hoseman R. (1974) Small-angle X-ray scattering of the thylakoid membranes of Rhodopseudomonas spheroides in aqueous solution. Biophys. J. 14: 221.

Piknova B., Perochon E., and Tocanne J.-F. (1993) Hydrophobic mismatch and long-range protein/lipid interactions in bacteriorhodopsin/phosphatidylcholine vesicles. Eur. J. Biochem. 218: 385-396.

Powl A.M., East J.M., and Lee A.G. (2003) Lipid-protein interactions studied by introduction of a tryptophan residue: The mechanosensitive channel MscL. Biochemistry 42: 14306-14317.

Riegler J. and Mohwald H. (1986) Elastic interactions of photosynthetic reaction center proteins affecting phase transitions and protein distributions. Biophys. J. 49: 1111-1118.

Williamson I.M., Alvis S.J., East J.M., and Lee A.G. (2003) The potassium channel KcsA and its interaction with the lipid bilayer. Cell Mol. Life Sci. 60: 1581-1590.2.

Williamson, I.M., Alvis, S.J., East, J.M., and Lee, A.G. (2002) Interactions of phospholipids with the potassium channel KcsA. Biophys. J. 83: 2026-2038.

Comparison with thickness of biological membranes determined by X-ray scattering



Table 4. Calculated hydrophobic thicknesses of proteins from different biological membranes (Dmin, Dmax, Daver).
Membrane type
 
Nprotb
Hydrophobic thickness (D), Å
Dmin-Dmax
Daver± S.E.M.
Dmembra

Outer membrane (gram-negative bacteria)

24
21.1-25.8
23.7±1.3
-

Cell wall membrane (Mycobacteria)

1
43.8
43.8
-
Inner membrane of bacteria
27
23.4-33.9
29.0±2.6
 
Inner membrane of bacteria (E. coli)
13
23.4-33.9
29.0±2.9
27.5
Archaebacterial membrane
6
27.5-30.9
29.2±1.1
-
Inner mitochondrial membrane
4
25.4-28.0
27.0±1.1
-
Thylakoid membrane
4
28.0-32.5
30.3±1.8
-
Eukaryotic plasma membrane (apical)
4
29.2-32.4
31.0±1.1
32.5
Endoplasmic reticulum membrane
3
29.1-32.0
30.9±1.3
27.5

a The hydrophobic thicknesses of membranes (Dmembr) are obtained by subtracting 10 Å from phosphate-to-phosphate distances determined by solution X-ray scattering (Mitra et al., 2004).

b In this statistics, each group of homologous TM proteins with sequence identity higher 50% was represented by a single structure determined with the highest resolution. A few proteins with questionable parameters were also excluded.

Mitra K., Ubarretxena-Belandia T., Taguchi T., Warren G., and Engelman D.M. (2004) Modulation of the bilayer thickness of exocytic pathway membranes by membrane proteins rather than cholesterol. Proc. Nat. Acad. Sci. USA 101: 4083-4088.

Site-directed chemical and spin labeling of lactose permease and rhodopsin

Site-directed

Figure 4. Comparison of calculated membrane boundaries of lactose permease (1pv6) with its modification by polar cross-linking reagent (A, red) and with its modification by NEM and spin labels (B, red for NEM-modified residues, blue for residues inaccessible to NEM and green for spin-labeled lipid-accessible residues). The residues accessible to water (red) are located either within ~5 Å from the hydrophobic membrane border, or inside the polar channel. In contrast, water-inaccessible residues (blue and green) are lociated inside the nonpolar membrane core, facing the lipids.

(1gzm, native membrane)               B (1gzm, detergent)

Comparison

Figure 5. A) Hydrophobic boundaries of rhodopsin calculated with lipid bilayer solvation parameters (Table 1 Methods). This shows that the calculated membrane boundaries are in accordance with chemical modification studies of rhodopsin in native membranes by polar probes (red) and hydrophobic probes (blue). B) Hydrophobic boundaries calculated with detergent solvation parameters (Table 1 Methods). This is consistant with spin-labeling studies of rhodopsin in dodecyl-maltoside (red -- water-accessible residues; blue -- lipid-accessible residues).

References

Chemical modification studies

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Davison M.D. and Findlay J.B.C. (1986a) Modification of ovine opsin with the photosensitive hydrophobic probe 1-azido-4-[125]-iodobenzene. Biochem. J. 234: 413-420.

Davison M.D. and Findlay J.B.C. (1986b) Identification of the sites in opsin modified by photoactivated azido[125]iodobenzene. Biochem. J. 236: 389-395.

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Venkatesan P., Hu Y.L., and Kaback H.R. (2000) Site-directed sulfhydryl labeling of the lactose permease of Escherichia coli: Helix X. Biochemistry 39: 10656-10661.

Zhang W., Hu Y.L., and Kaback H.R. (2003) Site-directed sulfhydryl labeling of helix IX in the lactose permease of Escherichia coli. Biochemistry 42 (17): 4904-4908.

Studies in detergents

Altenbach C., Cai K.W., Khorana H.G., Hubbell W.L. (1999) Structural features and light-dependent changes in the sequence 306-322 extending from helix VII to the palmitoylation sites in rhodopsin: A site-directed spin-labeling study. Biochemistry 38: 7931-7937.

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Roth, M., Lewit-Bentley, M.H., Deisenhofer, J., Huber, R., and Oesterhelt, D. 1989. Detergent structure in crystals of a bacterial photosynthetic reaction center. Nature 340: 659-662.

Roth, M., Arnoux, B., Ducruix, A., and Reiss-Husson, F. 1991. Structure of the detergent phase and protein-detergent interactions in crystals of the wild-type (strain Y) Rhodobacter sphaeroides photochemical reaction center. Biochemistry 30: 9403-9413.

Snijder, H.J., Timmins, P.A., Kalk, K.H., and Dijkstra, B.W. 2003. Detergent organization in crystals of monomeric outer membrane phospholipase A. J. Struct. Biol. 141: 122-131.

Spin-labeling of bacteiorhodopsin, sensory rhodopsin, mechanosensitive channel, potassium channel, lactose permease, transporter BtuB, receptor FepA, Na+/H+ antiporter, and peripheral C2 domains.

Altenbach C., Marti T., Khorana H.G., Hubbell W.L. (1990) Transmembrane protein structure: spin labeling of bacteriorhodopsin mutants. Science 248: 1088-1092.

Altenbach C., Greenhalgh DA., Khorana H.G., Hubbell W.L. (1994) A collision gradient method to determine the immersion dept of nitroxides in lipid bilayers: application ro spin-labeled mutants of bacteiorhdopsin. Proc. Nat. Acad. Sci. USA91: 1667-1671.

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Fanucci G.E., Cadieux N., Piedmont C.A., Kadner R.J., and Cafiso D.S. (2002) Structure and dynamics of the beta-barrel of the membrane by site-directed spin labeling. Biochemistry 41: 11543-11551.

Frazier A.A., Roller C.R., Havelka J.J., Hinderliter A., and Cafiso D.S. (2003) Membrane-bound orientation and position of the synaptotagmin IC2A domain by site-directed spin labeling Biochemistry 42: 96-105.

Greenhalgh, D.A., Altenbach, C., Hubbell, W.L., and Khorana, H.G. 1991. Locations of Arg-82, Asp-85 and Asp-96 in helix C of bacteriorhodopsin relative to the aqueous boundaries. Proc. Natl. Acad. Sci. USA 88: 8626-8630.

Gross A. and Hubbell W.L. (2002) Identification of protein side chains near the membrane-aqueous interface: A site-directed spin labeling study of KcsA. Biochemistry 41: 1123-1128.

Gross A., Columbus L., Hideg K., Altenbach C., and Hubbell W.L.  (1999) Structure of the KcsA potassium channel from Streptomyces lividans: A site-directed spin labeling study of the second transmembrane segment. Biochemistry 38: 10324-10335.

Hilger D., Jung H., Padan E., Wegener C., Vogel K.P., Steinhoff H.J., and Jeschke G. (2005) Assessing oligomerization of membrane proteins by four-pulse DEER: pH-dependent dimerization of NhaA Na+/H+ antiporter of E. coli. Biophys. J. 89: 1328-1338.

Klug C.S., Su W.Y., and Feix J.B. (1997) Mapping of the residues involved in a proposed beta-strand located in the ferric enterobactin receptor FepA using site-directed spin-labeling. Biochemistry 36: 13027-13033.

Kohout S.C., Corbalan-Garcia S., Gomez-Fernandez J.C., and Falke J.J. (2003) C2 domain of protein kinase C alpha: Elucidation of the membrane docking surface by site-directed fluorescence and spin labeling. Biochemistry42: 1254-1265.

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Malmberg N.J. and Falke J.J. (2005) Use of EPR power saturation to analyze the membrane-docking geometries of peripheral proteins: A applications to C2 domains. Ann. Rev. Biophys Biomol. Struct. 34: 71-90.

Perozo E., Cortes D.M., and Cuello L.G. (1998) Three-dimensional architecture and gating mechanism of a K+ channel studied by EPR spectroscopy Nature Struct. Biol.  5 (6): 459-469.

Perozo E., Kloda A., Cortes D.M., and Martinac B. (2001) Site-directed spin-labeling analysis of reconstituted MscL in the closed state. J. Gen. Physiol. 118: 193-205.

Rufener E., Frazier A.A., Wieser C.M., Hinderliter A., and Cafiso D.S. (2005) Membrane-bound orientation and position of the synaptotagmin C2B domain determined by site-directed spin labeling. Biochemistry 44: 18-28.

Wegener A.A., Chizhov I., Engelhard M., and Steinhoff H.J. (2000) Time-resolved detection of transient movement of helix F in spin-labelled pharaonis sensory rhodopsin II. J. Mol. Biol. 301: 881-891.

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Zhao M., Zen K.C., Hernandez-Borrell J., Altenbach C., Hubbell W.L., and Kaback H.R. (1999) Nitroxide scanning electron paramagnetic resonance of helices IV and V and the intervening loop in the lactose permease of Escherichia coli. Biochemistry 38: 15970-15977.

Fluorescence studies of mechanosensitive channel, OmpA porin, a-hemolysin, and acetylcholine receptor.

Chattopadhyay A. and McNamee M.G. (1991) Average membrane penetration depth of tryptophan residues of the nicotinic acetylcholine receptor by the parallax method. Biochemistry 30: 7159-7164.

Kleinschmidt, J.H., and Tamm, L.K. 1999. Time-resolved distance determination by tryptophan fluorescence quenching: Probing intermediates in membrane protein folding. Biochemistry38: 4996-5005.

Powl A.M., East J.M., and Lee A.G. (2003) Lipid-protein interactions studied by introduction of a tryptophan residue: The mechanosensitive channel MscL. Biochemistry 42: 14306-14317.

Powl A.M., Wright J.N., East J.M., and Lee A.G. (2005) Identification of the hydrophobic thickness of a membrane protein using fluorescence spectroscopy: Studies with the mechanosensitive channel MscL. Biochemistry 44: 5713-5721.

Raja S.M., Rawat S.S., Chattopadhyay A., and Lala A.K. (1999) Localization and environment of tryptophans in soluble and membrane-bound states of a pore-forming toxin from Staphylococcus aureus. Biophys. J. 76: 1469-1479.

Rodionova N.A., Tatulian S.A., Surrey T.S., Jahnig F., and Tamm L.K. (1995) Characterization of two membrane-bound forms of OmpA. Biochemistry 34: 1921-1929.

ATR FTIR and solid-state NMR studies of gramicidin A, potassium channel, lactose permease, OmpA, FhuA, bacteriorhodopsin, and phospholamban.

Andersen O.S., Koeppe R.E., and Roux B. (2005) Gramicidin channels. IEEE Transact. Nanobiosci. 4: 10-20.

Andronesi O.C., Pfeifer J.R., Al-Momani L., Ozdirekcan S., Rijkers D.T.S., Angerstein B., Luca S., Koert U., Killian J.A., and Baldus M. (2004) Probing membrane protein orientation and structure using fast magic-angle-spinning solid-state NMR. J. Biomol. NMR 30: 253-265.

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Kamihira M., Vosegaard T., Mason A.J., Straus S.K., Nielsen N.C., and Watts A. (2005) Structural and orientational constraints of bacteriorhodopsin in purple membranes determined by oriented-sample solid-state NMR spectroscopy. J. Struct. Biol. 149: 7-16.

Kota Z., Pali T., and Marsh D. (2004) Orientation and lipid-peptide interactions of gramicidin A in lipid membranes: Polarized attenuated total reflection infrared spectroscopy and spin-label electron spin resonance. Biophys. J. 86: 1521-1531.

Le Coutre J., Narasimhan L.R., Patel C.K.N., and Kaback H.R. (1997) The lipid bilayer determines helical tilt angle and function in lactose permease of Escherichia coli. Proc. Nat. Acad. Sci. USA94: 10167-10171.

Le Coutre J., Kaback H.R., Patel C.K.N., Heginbotham L., and Miller C. (1998) Fourier transform infrared spectroscopy reveals a rigid alpha-helical assembly for the tetrameric Streptomyces lividans K+ channel. Proc. Natl. Acad. Sci. USA 95: 6114-6117.

Nabedryk, E., Gingold, M.P., and Breton, J. 1982. Orientation of gramicidin A transmembrane channel. Infrared dichroism study of gramicidin in vesicles. Biophys J. 38: 243-249.

Ramakrishnan M., Qu J., Pocanschi C.L., Kleinschmidt J.H., and Marsh D. (2005) Orientation of beta-barrel proteins OmpA and FhuA in lipid membranes. Chain length dependence from infrared dichroism. Biochemistry 44: 3515-3523.

Electron cryo-microsopy

Vonck, J., von Nidda, T.K., Meier, T., Matthey, U., Mills, D.J., Kuhlbrandt, W., and Dimroth, P. 2002. Molecular architecture of the undecameric rotor of a bacterial Na+-ATP synthase. J. Mol. Biol.321: 307-316.

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Krebs, A., Edwards, P.C., Villa, C., Li, J.D., and Schertler, G.F.X. 2003. The three-dimensional structure of bovine rhodopsin determined by electron cryomicroscopy. J. Biol. Chem. 278: 50217-50225.