Department of Biochemistry University of Oxford Department of Biochemistry
University of Oxford
South Parks Road
Oxford OX1 3QU

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OUBSU Publications : 1990-1999

Scientific papers 1995-9, Scientific papers 1990-4 and Reviews
1995 - 1999
  • Ulrich,A.S., Wallat, I., Heyn, M.P. & Watts, A. (1995) Re-orientation of the retinal chromophore in the M-photointermediate of bacteriorhodopsin. Nature Structural Biology, 2, 190-192.
  • Middleton, D.A., Reid, D.G. & Watts, A. (1995) The conformations of a functional spin-labelled derivative of gastric H/K-ATPase investigated by EPR spectroscopy. Biochemistry, 34, 7420-7429.
  • Pinheiro, T.J.T., Elöve, G.A., Roder, H., de Jongh, H.H.J., de Kruijff, B. & Watts, A. (1995) Lipid-mediate folding of apocytochrome c . Proceedings of the Meeting "Perspectives on Protein Engingeering and Complementary Technologies".
  • Venien-Bryan, C., Davies, A., Langmack, K., Baverstock, J., Watts, A., Marsh, D., & Saibil, H. (1995) Effect of the C-terminal proline repeats on ordered packing of squid rhodopsin and its mobility in membranes. FEBS Lett. 359, 45-49.
  • Watts, A., Sternberg, B., Ulrich, A.S., Whiteway, C.A., Seifert, G., Sami, M., Fisher, P., Heyn, M. & Wallat, I. (1995) Bacteriorhodopsin: the effect of bilayer thickness on 2D array formation, and the structural re-alignment of retinal through the photocycle. Biophysical Chemistry, 56, 41-46.
  • Boulter, J.M., Taylor, A.M. & Watts, A. (1996) Asymmetric and functional reconstitution of band 3 into pre-formed phosphatidylcholine vesicles. Biochim. Biophys. Acta 1280, 265-271
  • Albert, A.D., Boesze-Battaglia, K., Paw, Z., Watts, A., Epand, R.M. (1996) Effect of cholesterol on rhodopsin stability in disk membranes. Biochim. Biophys. Acta. 1297(1): 77-82
  • Biaggi, M.H., Pinheiro, T.J.T., Watts, A., Lamy-Freund, M.T. (1996) Spin label and 2H-NMR studies on the interaction of melanotropic peptides with lipid bilayers. Eur. Biophys. J. ; 24(4): 251-9
  • Cölfen, H., Harding, S.E., Boulter, J.M. & Watts, A. (1996) A hydrodynamic examination of the dimeric cytoplasmic domain of the human erythrocyte anion transporter, band 3. Biophysical J., 71, 1611-1615.
  • Pinheiro, T.J.T., Duer, M.J. & Watts, A. (1997) Phospholipid headgroup dynamics in DOPG-d5-cytochrome c complexes as revealed by 2H and 31P NMR: The effects of a peripheral protein on collective lipid fluctuations. Solid state NMR 8, 55-64.
  • Middleton, D.A., Robins, R., Feng, X., Levitt, M.H., Spiers, I.D., Schwalbe, C., Reid, D.G. & Watts, A. (1997) The conformation of an inhibitor bound to gastric proton pump. FEBS Letts. 410, 269-274.
  • Albert, A.D., Watts, A., Spooner, P.J.R., Grobner, G., Young, J. & Yeagle, P.L. (1997) A distance measurement between specific sites on the cytoplasmic surface of bovine rhodopsin in rod outer segment disk membranes. Biochim. Biophys. Acta 1328, 74-82.
  • Grobner, G., Choi, G., Burnett, I., Verdegem, P., Lugtenburg, J., Glaubitz, C. & Watts, A. (1997) Photoreceptor rhodopsin: A structural and conformational study of 11-cis retinal in rhodopsin in oriented membranes by deuterium solid state NMR. Biophys. J. 72, A114.
  • Gröbner, G., Taylor, A., Williamson, P.T.F., Choi, G., Glaubitz, C., Watts, J.A., de Grip, W.J. & Watts, A. (1997) Macroscopic orientation of natural and model membranes for structural studies. Analytical Biochemistry, 254,132-136.
  • Pinheiro, T.J.T., Elöve, G.A., Watts, A. & Roder, H. (1997) Structural and kinetic description of cytochrome c unfolding induced by the interaction with lipid vesicles. Biochemistry, 36, 13122-13132
  • Watts, A. and Sabra, M. (1997) Not all integral proteins are freely diffusing in a fluid mosaic: how lipids can promote protein array formation. Biol. Skr. Dan. Vid. Selsk, 49, 123-126.
  • Arêas, J.A.G., Gröbner, G.J., Pellacani, L.B., Glaubitz, C. & Watts, A. (1997) Use of solid state 2H NMR for studying protein-lipid interactions at emulsion interfaces. Mag. Res. in Chemistry 35: S119-S124.
  • Glaubitz, C. and Watts, A. (1998) Magic angle oriented sample spinning (MAOSS): A new approach towards biomembrane studies. J. Mag. Res. 130, 305-316.
  • Addy, V.L., Covington, A.D. and Watts, A. (1998) Enzyme degreasing of animal skins: a biochemical and microscopical study. Proceeding of IULTCS Congress.
  • Grobner, G., Choi, G., Burnett, I., Glaubitz, C. & Watts, A. (1998) Photoreceptor rhodopsin: Structural and conformational study of its chromophore 11-cis retinal in oriented membranes by deuterium solid state NMR. FEBS Lett, 422, 201-204.
  • Duralski, A.A., Spooner, P.J.R., Rankin, S.E. & Watts, A. (1998) Synthesis of isotopically labelled cardiolipins. Tetrahedron Letts., 39, 1607-1610.
  • Arêas, J.A.G., Gröbner, G.J., Glaubitz, C. & Watts, A. (1998) Interaction of a type II myosin with biological membranes studied by 2H solid state NMR. Biochemistry, 37, 5582-5588.
  • Williamson, P.T.F., Gröbner, G., Spooner, P.J.R., Miller, K.W. & Watts, A. (1998) Probing the agonist binding pocket on the nicotinic acetylcholine receptor: a high resolution solid state NMR approach. Biochemistry, 37, 10854-10859.
  • Cölfen, H., Boulter, J., Harding, S.E. and Watts, A. (1998) Ultracentrifugation studies on the transmembrane domain of the human erythrocyte anion transporter Band 3 in the detergent C12E8. Eur. Biophys. J. 27, 651-655.
  • Watts, A., Burnett, I.J., Glaubitz, C., Gröbner, G., Middleton, D.A., Spooner, P.J.R. & Williamson, P.T.F. (1998) Structural descriptions of ligands in their binding site of integral membrane proteins at near physiological conditions. Eur. Biophys. J. 28, 84-90.
  • Rankin, S.E., Watts, A. & Pinheiro, T.J.T. (1998) Electrostatic and hydrophobic contributions to the folding mechanism of apocytochrome c driven by the interaction with lipid. Biochemistry, 37, 12588-12595.
  • Sabra, M.C., Uitdehaag, J.C.M. & Watts, A. (1998) General model for lipid-mediated 2D array formation of membrane proteins. Application to bacteriorhodopsin. Biophys. J., 75, 1180-1188
  • Spooner, P.J.R., O'Reilly, W.J., Homans, S.W., Rutherford, N.G., Henderson, P.J.F. & Watts, A. (1998) Weak substrate binding to transport proteins studied by NMR. Biophys. J. 2794-2800.
  • Rankin, S.E., Watts, A., Roder, H. & Pinheiro, T.J.T. (1999) Folding of apolcytochrome c induced by the interaction with negatively charged lipid micelles proceeds via a collapsed intermediate state. Protein Science, 8, 381-393.
  • Taylor, A.M. & Watts, A. (1999) Spin-label studies of lipid-protein interactions with reconstituted Band 3, the human erythrocyte chloride/bicarbonate exchanger. J. Biochem & Cell Biol. 76(5), 815-22.
  • Taylor, A.M., Boulter, J., Harding, S.E. & Watts, A. (1999) Hydrodynamic properties of human erythrocyte Band 3 solubilized in reduced Triton X-100. Biophys. J. 76, 2043-2055.
  • Glaubitz, C., Burnett, I., Gröbner, G., Mason, J. & Watts, A. (1999) Deuterium-MAS NMR spectroscopy on oriented membrane proteins: Application to photointermediates of bacteriorhodopsin. J. Am. Chem. Soc. 121, 5787-5794.
  • Spooner, P.J.R., Veenhoff, L., Watts, A. & Poolman, B. (1999) Structural information on a membrane transport protein from NMR using sequence-selective nitroxide labelling. Biochemistry, 38, 9634-9639.
  • Bryson, E.A., Rankin, S.E., Carey, M., Watts, A. & Pinheiro, T.J.T. (1999) Folding of apocytochrome c in lipid micelles: Formation of a-helix precedes membrane insertion. Biochemistry, 38, 9758 -9767
  • Taylor, A.M., Gröbner, G., Williamson, P.T.F. & Watts, A. (1999) Binding properties of the stilbene disulfonate sites on human erythrocyte AE1: kinetic, thermodynamic and solid state deuterium NMR analyses. Biochemistry, 38, 11172-11179.
  • Gröbner, G, Glaubitz, C and Watts, A. (1999) Probing membrane surfaces and the location of membrane embedded peptides by 13C MAS NMR using lanthanide ions. J. Mag. Res. 141, 335-339.

1990 - 1994
  • Fraser, D., Louro, S., Horvath, L.I., Miller, K. and Watts, A. (1990) A study of the effect of general anesthetics on lipid-protein interactions in acetylcholine receptor enriched membranes from Torpedo nobiliana using nitroxide spin-labels. Biochemistry, 29, 2664-2669.
  • Ulrich, A.S., Volke, F. and Watts, A. (1990) The dependence of phospholipid head- group mobility on hydration as studied by deuterium-NMR spin-lattice relaxation time measurements. Chem. Phys. Lipids 55 61-66
  • Ulrich, A.S., Poile, T.W. and Watts, A. (1990) Deuterium NMR to study the surface of phospholipid bilayers. Bull. Mag. Res. 12, 80-83.
  • van Gorkom, L., Horvath, L.I., Hemminga, M.A., Sternberg, B. and Watts, A. (1990) Identification of trapped and boundary lipid binding sites in M13 coat protein-lipid complexes by deuterium NMR spectroscopy. Biochemistry, 29, 3828-3834..
  • Spooner, P.J.R. , Van Gorkom, L.C.M. and Watts, A. (1990) Moderating the heating of biological samples during magic-angle spinning experiments. J. Mag. Res. 90, 584-588.
  • Sanders, J.C., Poile, T.W., Spruijt, R.B., Van Nuland, N.A.J., Watts, A. and Hemminga, M.A. (1991) A NMR investigation on the interactions of the a-oligomeric form of the M13 coat protein with lipids which mimic the Escherichia coli inner membrane. Biochim. Biophys. Acta, 1066, 102-108.
  • Gale, P. & Watts, A. (1991) Characterization of phospholipid compositions and physical properties of DMPC/Bacteriorhodopsin vesicles produced by a detergent-free method. Biochem. Biophys. Res. Comm. 180, 939-944.
  • Fraser, D.M., Van Gorkom, L.C.M. and Watts, A. (1991) Partitioning behaviour of 1- hexanol into lipid membranes as studied by deuterium NMR spectroscopy. Biochim. Biophys. Acta, 1069, 53-60.
  • Spooner, P.J.R. and Watts, A. (1991) Reversible unfolding of cytochrome c upon interaction with cardiolipin bilayers. 1. Evidence from deuterium NMR measurements. Biochemistry, 30, 3871-3879.
  • Spooner, P.J.R. and Watts, A. (1991) Reversible unfolding of cytochrome c upon interaction with cardiolipin bilayers. 2. Evidence from phosphorus-31 NMR measurements. Biochemistry, 30, 3880-3885.
  • Spooner, P.J.R. and Watts, A. (1992) Cytochrome c interactions with cardiolipin in bilayers: A multinuclear magic-angle spinning NMR study Biochemistry, 31, 10129-10138.
  • Gale, P. & Watts, A. (1992) Effect of bacteriorhodopsin on the orientation of the headgroup of 1,2-dimyristoyl-sn-glycero-3-phosphocholine in bilayers - a 31P and 2H- NMR study Biochim. Biophys. Acta, 1106, 317-324.
  • Ulrich, A.S., Wallat, I., Heyn, M.P. and Watts, A. (1992) Evidence for a curved retinal in BR from solid-state 2H-NMR. In: Structures and Functions of Retinal Proteins (J.- L. Rigaud, ed.) Colloque INSERM/John Libbey Eurotext Ltd., 221, 247-249.
  • Ulrich, A.S. & Watts, A. (1992) Membrane protein structure determination by deuterium-NMR. Case study: Retinal in bacteriorhodopsin. NATO ASI, 63, 243-249.
  • Fajer, P., Watts, A. and Marsh, D. (1992) Saturation transfer, continuous wave saturation, and saturation recovery electron spin resonance studies of chain-spin labeled phosphatidylcholines in the low temperature phases of dipalmitoyl phosphatidylcholine bilayers: Effects of rotational dynamics and spin-spin interaction. Biophys. J., 61, 879-891.
  • Sami, M., Malik, S. & Watts, A. (1992) Structural stability of the erythrocyte anion transporter, band 3, in native membranes and in detergent micelles. Biochim. Biophys. Acta, 1105, 148-154.
  • Ulrich, A.S., Heyn, M.P. and Watts, A. (1992) Structure determination of the cyclohexene-ring of retinal in bacteriorhodopsin by solid-state deuterium-NMR. Biochemistry, 31, 10390-10399.
  • Sternberg, B., L'Hostis, C., Whiteway, C.A. and Watts, A. (1992) The essential role of Halobacterium halobium lipids in 2D-array formation of bacteriorhodopsin. Biochim. Biophys. Acta, 1108, 21-30.
  • Duralski, A.A. and Watts, A. (1992) Synthesis of isotopically labelled ubiquinones. Tetrahedron Letts, 33, 4983-4984.
  • Areas, J.A.G. and Watts, A. (1993) Interaction of myosin with charged membranes is affected by ATP. Biochemical Society Transactions, 21, 80S.
  • Ulrich, A.S. and Watts, A. (1993) 2H NMR lineshapes of immobilized uniaxially oriented membrane proteins Solid State NMR 2, 21-36.
  • Abadji, V.C., Raines, D.E., Watts, A. and Miller, K.W. (1993) The effect of general anaesthetics on the dynamics of phosphatidylcholine-acetylcholine receptor interactions in reconstituted vesicles. Biochim. Biophys. Acta, 1147, 143-153.
  • Pinheiro, T.J.T., Bratt, P.J., Davis, I.H., Doetschman, D.C. and Watts, A. (1993) Spin- lattice relaxation times of phospholipid aminoxyl spin labels in cardiolipin-cytochrome c bilayers: a pulse saturation-recovery EPR study. J. Chemical Society, Perkin Transactions 2 p.2113-2117
  • Spooner, P.J.R., Duralski, A.A., Rankin, S.E., Pinheiro, T.J.T. and Watts, A. (1993) Dynamics in a protein-lipid complex: NMR measurements of the headgroup of cardiolipin when bound to cytochrome c. Biophysical Journal , 65, 106-112.
  • Heyer-Hartl, M., Brophy, P.J., Marsh, D. and Watts, A. (1993) Interaction of two complementary fragments of the bovine spinal cord myelin basic protein with phosphatidyglclycerol bilayers, studied by 2H and 31P NMR spectroscopy. Biochemistry 32, 9709-9713.
  • Sternberg, B., Watts, A. and Cejka, Z. (1993) Lipid induced modulation of the protein packing in two-dimensional crystals of bacteriorhodopsin. J. Struct. Biology, 110, 196-204.
  • Malik, S., Sami, M. and Watts, A. (1993) A role for Band 4.2 in Human erythrocyte band 3 mediated anion transport. Biochemistry, 32, 10078-10084.
  • Yeagle, P.L., Dentino, A.R., Frazer Smith, T., Spooner, P. and Watts, A. (1993) The anti-viral peptide carbobenzoxy-D-phenylalanine-L-phenylalanine-glycine changes the average conformation of phospholipids in membranes. Biochemistry, 32, 12197- 12202.
  • Ulrich, A.S. and Watts, A. (1994) Lipid headgroup hydration by 2H-NMR: a link between spectroscopy and thermodynamics. Biophysical Chemistry, 49, 39- 50.
  • Renfrey, S. & Watts, A. (1994) Morphological and biochemical characterization of influenza vaccines commercially available in the United Kingdom. Vaccine, 12, 747-751.
  • Pinheiro, T.J.T. and Watts, A. (1994) Lipid specificity in the interaction of cytochrome c with anionic phospholipid bilayers revealed by solid-state 31P NMR. Biochemistry, 33, 2451-2458.
  • Pinheiro, T.J.T. and Watts, A. (1994) Resolution of individual lipids in mixed phospholipid membranes and specific lipid-cytochrome c interactions by magic angle spinning solid-state phosphorus-31 NMR. Biochemistry, 33, 2459-2467.
  • Pinheiro, T.J.T., Duralski, A.J. and Watts, A. (1994) Phospholipid headgroup- headgroup electrostatic interactions in mixed bilayers of cardiolipin with phosphatidylcholines studied by 2H NMR. Biochemistry, 33, 4896-4902.
  • Spooner, P.J.R., Rutherford, N., Watts, A. and Henderson, P.J.F. (1994) NMR observation of substrate in the binding site of an active sugar H+ symport protein in native membranes. PNAS. 91, 3877-3881.
  • Bradshaw, J.P., Dempsey, C.E. and Watts, A. (1994) A combined X-ray and neutron diffraction study of selectively deuterated melittin in phospholipid bilayers: the effect of pH. Mol. Membrane Biol. 11, 79-86.
  • Calder, P.C., Yaqoob, P., Harvey, D.J., Watts, A. and Newsholme, E.A. (1994) Incorporation of fatty acids by concanavalin A-stimulated lymphocytes and the effect on fatty acid composition and membrane fluidity. Biochem. J., 300, 509-518
  • Ulrich, A.S. & Watts, A. (1994) Molecular response of the lipid headgroup to bilayer hydration as monitored by 2H-NMR. Biophysical J., 66, 1441- 1449.
  • Ulrich, A.S., Sami, M. and Watts, A. (1994) Hydration of DOPC bilayers by DSC. Biochim. Biophys. Acta, 1191, 225-230.
  • Ulrich, A.S., Watts, A., Wallat, I. & Heyn, M.P. (1994) Distorted structure of retinal chromophore in bacteriorhodopsin resolved by 2H-NMR. Biochemistry, 33, 5370-5375.


1990 - 1999
  • Watts, A. (1990) Protein-lipid interactions at membrane surfaces. In: Biophysics of the cell surface (Glazer, R. and Gingell, D. eds) Springer -Verlag, Berlin-Heidelberg. pp 23-50.
  • Watts, A. (1991) Magnetic Resonance Studies of Lipid-Protein Interfaces and Lipophilic Molecule Partitioning In: Molecular and cellular mechanisms of alcohol and anesthetics (E. Rubin, K.W. Miller and S.H. Roth, eds.) Annals of the New York Academy of Science, 625, 653-669.
  • Watts, A. & Spooner, P.J.R. (1991) Phospholipid phase transitions as revealed by NMR. Chem. Phys. Lipids 57, 195-211
  • Watts, A. & Van Gorkom, L.C.M. (1991) Surface organization of lipid bilayers. In: The Structure of Biological Membranes (P. Yeagle ed.) C.R.C. Press Inc., pp.307- 377.
  • Watts, A. (1993) Magnetic resonance studies of phospholipid-protein interactions in bilayers In: Phospholipids Handbook (G. Cevc, ed.) 687-740, Marcel Dekker, New York
  • 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: Protein Lipid Interactions, New Comprehensive Biochemistry series (ed. A. Watts), 351- 370, Elsevier, Amsterdam
  • Watts, A. (1994) Magnetic resonance studies of protein-lipid interactions. In: Biological Membranes: Structure, biogenesis and dynamics (ed. J.A.F. Op den Kamp) NATO ASI Series, H82, 79-92.
  • Watts, A. (1994) Non-crystallographic methods to study membrane proteins. In: Biological Membranes: Structure, biogenesis and dynamics (ed. J.A.F. Op den Kamp) NATO ASI Series, H82, 131-138.
  • Watts, A. (1994) High resolution, non-crystallographic structural studies of large integral membrane proteins. Biochemical Society Transactions, 22, 801-805
  • Watts, A. (1994) Red Heat on salted hides. BCL Journal, 37, 130- 133.
  • Watts, A. (1994) Bacteriorhodopsin: The mechanism of 2D-array formation and the structure of the retinal in the protein. Biophysical Chemistry, 55, 137-151.
  • Watts, A., Ulrich, A.S. & Middleton, D.A. (1995) Membrane protein structure: the contribution and potential of novel solid state NMR approaches. Mol. Membrane Biol., 12, 233-246
  • Watts, A. (1995) Biophysics of the membrane interface. Biochemical Society Transactions, 23, 959-965.
  • Watts, A. (1997) Structural and functional consequence of long-chain polyunsaturation in biomembranes. Prenat. Neonat. Med. 2, 1-11.
  • Watts, A. & Pinheiro, T.J.T. (1998) Biophysics of the membrane interface. In: Membrane protein insertion and translocation. (ed. D. Phoenix), 1-17, Pub. Portland Press.
  • Watts, A. (1998) Solid state NMR approaches for studying the interaction of peptides and proteins with membranes. Biochem. Biophys. Acta, 1376, 297-318.
  • Watts, A. (1999) NMR of drugs and ligands bound to membrane receptors. Current Opinion in Biotechnology, 10, 48-53.
  • Watts, A. (1999) Structural resolution of ligand-receptor interactions in functional, membrane-embedded receptors and proteins using novel, non-perturbing solid state NMR methods. Pharmacy & Pharmacology Communications, 5, 7-13.
  • Watts, A. & Middleton, D. (1999) Biological solid state NMR comes of age: NMR to study non-crystalline, heterogeneous biological complexes with no size of molecular weight limit. The Biochemist, 19, 11-17.
  • Watts, A., Burnett, I.J., Glaubitz, C.,Gröbner, G., Middleton, D.A., Spooner, P.J.R., Watts, J.A. & Williamson, P.T.F. (1999) Membrane protein structure determination by solid state NMR. Natural Product Reports, 16, 419-423.



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