Assessment of the aggregation state of integral membrane proteins in reconstituted phospholipid vesicles using small angle neutron scattering

Journal of Molecular Biology

Volumn 273, Issue 5, 1997, Pages 1004-1019

  Hunt, John F ^a,d   McCrea, Pierre D ^a,e   Zaccaï, Giuseppe ^b,c   Engelman, Donald M ^a  

^a YALE UNIVERSITY   (United States)

^b CEA GRENOBLE   (France)

^c INSTITUT LAUE LANGEVIN   (France)

^d Columbia University ^*  (United States)

^e UNIVERSITY OF TEXAS   (United States)

Author keywords

Aggregation state; Bacteriorhodopsin; Membrane proteins; Phospholipid vesicles; Small angle neutron scattering

Indexed keywords

BACTERIORHODOPSIN; MEMBRANE PROTEIN;

ARTICLE; LIPID BILAYER; MOLECULAR WEIGHT; NEUTRON SCATTERING; PHOSPHOLIPID VESICLE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN STRUCTURE;

EID: 0031567785     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1330     Document Type: Article

References (58)

1. Bendzko, P. I., Pfeil, W. A., Privalov, P. L. & Tiktopulo, E. I. (1988). Temperature-induced phase transitions in proteins and lipids. Volume and heat capacity effects. Biophys. Chem. 29, 301-307.
2. Bormann, B. J. & Engelman, D. M. (1992). Intramembrane helix-helix association in oligomerization and transmembrane signaling. Annu. Rev. Biophys. Biomol. Struct. 21, 223-242.
3. Büldt, G., Gally, H. U., Seelig, A., Seelig, J. & Zaccaï, G. (1978). Neutron diffraction studies on selectively deuterated phospholipid bilayers. Nature, 271, 182-184.
4. Büldt, G., Gally, H. U., Seelig, J. & Zaccaï, G. (1979). Neutron diffraction studies on phosphatidylcholine model membranes. I. Head group conformation. J. Mol. Biol. 134, 673-691.
5. Capel, M. S., Engelman, D. M., Freeborn, B. R., Kjeldgaard, M., Langer, J. A., Ramakrishnan, V., Schindler, D. G., Schneider, D. K., Schoenborn, B. P. & Sillers, I. Y., et al. (1987). A complete mapping of the proteins in the small ribosomal subunit of Escherichia coli. Science, 238, 1403-1406.
6. Carraway, K. L. & Cerione, R. A. (1991). Comparison of epidermal growth factor (EGF) receptor-receptor interactions in intact A431 cells and isolated plasma membranes. Large scale receptor micro-aggregation is not detected during EGF-stimulated early events. J. Biol. Chem. 266, 8899-8906.
7. Carraway, K. L., Koland, J. G. & Cerione, R. A. (1989). Visualization of epidermal growth factor (EGF) receptor aggregation in plasma membranes by fluorescence resonance energy transfer. Correlation of receptor activation with aggregation. J. Biol. Chem. 264, 8699-8707.
8. Casey, J. R. & Reithmeier, R. A. (1991). Analysis of the oligomeric state of Band 3, the anion transport protein of the human erythrocyte membrane, by size exclusion high performance liquid chromatography. Oligomeric stability and origin of heterogeneity. J. Biol. Chem. 266, 15726-15737.
9. Cherry, R. J., Moøller, U., Henderson, R. & Heyn, M. P. (1978). Temperature-dependent aggregation of bacteriorhodopsin in dipalmitoyl and dimyristoylphosphatidylcholine vesicles. J. Mol. Biol. 121, 283-298.
10. Cochet, C., Kashles, O., Chambaz, E. M., Borrello, I., King, C. R. & Schlessinger, J. (1988). Demonstration of epidermal growth factor-induced receptor dimerization in living cells using a chemical covalent cross-linking agent. J. Biol. Chem. 263, 3290-3295.
11. Curmi, P. M., Stone, D. B., Schneider, D. K., Spudich, J. A. & Mendelson, R. A. (1988). Comparison of the structure of myosin subfragment 1 bound to actin and free in solution. A neutron scattering study using actin made "invisible" by deuteration. J. Mol. Biol. 203, 781-798.
12. de Vos, A. M., Ultsch, M. & Kossiakoff, A. A. (1992). Human growth hormone and extracellular domain of its receptor: crystal structure of the complex. Science, 255, 306-312.
13. Earnest, T. N., Herzfeld, J. & Rothschild, K. J. (1990). Polarized Fourier transform infrared spectroscopy of bacteriorhodopsin. Transmembrane alpha helices are resistant to hydrogen/deuterium exchange. Biophys. J. 58, 1539-1546.
14. Feigin, L. A. & Svergun, D. I. (1987). Structure Analysis by Small-Angle X-ray and Neutron Scattering, Plenum Press, New York.
15. Findlay, J. B., Donnelly, D., Bhogal, N., Hurrell, C. & Attwood, T. K. (1993). Structure of G-protein-linked receptors. Biochem. Soc. Trans. 21, 869-873.
16. Gaffney, B. J. (1985). Chemical and biochemical cross-linking of membrane components. Biochim. Biophys. Acta, 822, 289-317.
17. Gennis, R. B. (1989). Biomembranes: Molecular Structure and Function, Springer-Verlag, New York.
18. Ghosh, R. E. (1989). A Computing Guide for Small Angle Scattering Experiments, Institut Laue-Langevin, Grenoble, France.
19. Glatter, O. & Kratky, O. (1982). Small Angle X-ray Scattering, Academic Press, New York.
20. Grigorieff, N., Ceska, T. A., Downing, K. H., Baldwin, J. M. & Henderson, R. (1996). Electron-crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol. 259, 393-421.
21. Guinier, A. (1963). X-Ray Diffraction In Crystals, Imperfect Crystals, and Amorphous Bodies, W. H. Freeman, San Francisco.
22. 2+-ATPaSe, reconstituted with an excess of phospholipid. J. Biol. Chem. 265, 12020-12028.
23. Heldin, C. H. (1995). Dimerization of cell surface receptors in signal transduction. Cell, 80, 213-223.
24. Henderson, R., Baldwin, J. M., Ceska, T. A., Zemlin, F., Beckmann, E. & Downing, K. H. (1990). Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J. Mol. Biol. 213, 899-929.
25. Huang, K. S., Bayley, H. & Khorana, H. G. (1980). Delipidation of bacteriorhodopsin and reconstitution with exogenous phospholipid. Proc. Natl Acad. Sci. USA, 77, 323-327.
26. Hurtley, S. M. & Helenius, A. (1989). Protein oligomerization in the endoplasmic reticulum. Annu. Rev. Cell Biol. 5, 277-307.
27. Ibel, K. (1976). The small angle neutron scattering station D11 at the Institut Laue-Langevin. J. Appl. Crystallog. 9, 296-309.
28. Ibel, K. & Stuhrmann, H. B. (1975). Comparison of neutron and X-ray scattering of dilute myoglobin solutions. J. Mol. Biol. 93, 255-265.
29. Jacrot, B. (1976). The study of biological structures by neutron scattering from solution. Rep. Prog. Phys. 39, 911-953.
30. Jacrot, B. & Zaccaï, G. (1981). Determination of molecular weight by neutron scattering. Biopholymers, 20, 2414-2426.
31. Khorana, H. G. (1988). Bacteriorhodopsin, a membrane protein that uses light to translocate protons. J. Biol. Chem. 263, 7439-7442.
32. Knoll, W., Ibel, K. & Sackmann, E. (1981). Small-angle neutron scattering study of lipid phase diagrams by the contrast variation method. Biochemistry, 20, 6379-6383.
33. Lattman, E. E. (1989). Rapid calculation of the solution scattering profile from a macromolecule of known structure. Proteins: Struct. Funct. Genet. 5, 149-155.
34. Lehmann, N. S. & Zaccaï, G. (1984). Neutron small-angle scattering studies of ribonuclease in mixed aqueous solutions and determination of the preferentially bound water. Biochemistry, 23, 1939-1942.
35. le, Maire M. (1986). Protein-protein interactions in membranes: concepts and the example of calcium ATPase from the sarcoplasmic reticulum. Biochimie, 68, 395-400.
36. le Maire, M., Aggerbeck, L. P., Monteilhet, C., Andersen, J. P. & Møller, J. V. (1986). The use of high-performance liquid chromatography for the determination of size and molecular weight of proteins: a caution and a list of membrane proteins suitable as standards. Anal. Biochem. 154, 525-535.
37. le, Maire M., Thauvette, L., de Foresta, B., Viel, A., Beauregard, G. & Potier, M. (1990). Effects of ionizing radiations on proteins. Evidence of non-random fragmentations and a caution in the use of the method for determination of molecular mass. Biochem. J. 267, 431-439.
38. Livnah, O., Stura, E. A., Johnson, D. L., Middleton, S. A., Mulcahy, L. S., Wrighton, N. C., Dower, W. J., Jolliffe, L. K. & Wilson, I. A. (1996). Functional mimicry of a protein hormone by a peptide agonist: the EPO receptor complex at 2.8 angstroms. Science, 273, 464-471.
39. Malfois, M., Bonneté, F., Belloni, L. & Tardieu, A. (1996). A model of attractive interactions to account for fluid-fluid phase separation of protein solutions. J. Chem. Phys. 105, 3290-3300.
40. Manolios, N., Bonifacino, J. S. & Klausner, R. D. (1990). Transmembrane helical interactions and the assembly of the T cell receptor complex. Science, 249, 274-277.
41. Marsh, D. (1990). Handbook of Lipid Bilayers, CRC Press, Boca Raton, FL.
42. 2+-pump protein as monomers and defined oligomers. Methods Enzymol. 157, 261-270.
43. Oesterhelt, D. & Stoeckenius, W. (1971). Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nature New Biol. 233, 149-152.
44. Popot, J. L. & Engelman, D. M. (1990). Membrane protein folding and oligomerization: the two-stage model. Biochemistry, 29, 4031-4037.
45. Popot, J. L., Gerchman, S. E. & Engelman, D. M. (1987). Refolding of bacteriorhodopsin in lipid bilayers. A thermodynamically controlled two-stage process. J. Mol. Biol. 198, 655-676.
46. Racker, E., Violand, B., O'Neal, S., Alfonzo, M. & Telford, J. (1979). Reconstitution, a way of biochemical research; some new approaches to membrane-bound enzymes. Arch. Biochem. Biophys. 198, 470-477.
47. Tanford, C. & Reynolds, J. A. (1976). Characterization of membrane proteins in detergent solutions. Biochim. Biophys. Acta, 457, 133-170.
48. Tardieu, A., Veretout, F., Krop, B. & Slingsby, C. (1992). Protein interactions in the calf eye lens: interactions between β-crystallins are repulsive whereas in γ-crystallins they are attractive. Eur. Biophys. J. 21, 1-12.
49. Ullrich, A. & Schlessinger, J. (1990). Signal transduction by receptors with tyrosine kinase activity. Cell, 61, 203-212.
50. Veatch, W. & Stryer, L. (1977). The dimeric nature of the gramicidin A transmembrane channel: conductance and fluorescence energy transfer studies of hybrid channels. J. Mol. Biol. 113, 89-102.
51. Veretout, F., Delaye, M. & Tardieu, A. (1989). Molecular basis of eye lens transparency. Osmotic pressure and X-ray analysis of α-crystallin solutions. J. Mol. Biol. 205, 713-728.
52. Wells, J. A. (1994). Structural and functional basis for hormone binding and receptor oligomerization. Curr. Opin. Cell Biol. 6, 163-173.
53. Wiener, M. C. & White, S. H. (1992). Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of X-ray and neutron diffraction data. III. Complete structure. Biophys. J. 61, 437-447.
54. Zaccaï, G. (1986). Measurement of density and location of solvent associated with biomolecules by small-angle neutron scattering. Methods Enzymol. 127, 619-629.
55. Zaccaï, G., Büldt, G., Seelig, A. & Seelig, J. (1979). Neutron diffraction studies on phosphatidylcholine model membranes. II. Chain conformation and segmental disorder. J. Mol. Biol. 134, 693-706.
56. Zaccaï, G. & Jacrot, B. (1983). Small angle neutron scattering. Annu. Rev. Biophys. Bioeng. 12, 139-157.
57. Zaccaï, G., Wachtel, E. & Eisenberg, H. (1986). Solution structure of halophilic malate dehydrogenase from small-angle neutron and X-ray scattering and ultracentrifugation. J. Mol. Biol. 190, 97-106.
58. Zamyatnin, A. A. (1984). Amino acid, peptide, and protein volume in solution. Annu. Rev. Biophys. Bioeng. 13, 145-165.