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Membrane Protein Structure pp 249–267Cite as

Nuclear Magnetic Resonance Approaches to Membrane Protein Structure

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Part of the book series: Methods in Physiology Series ((METHPHYS))

Abstract

To understand the functions of membrane proteins requires the same high level of structural analysis that is now almost routinely applied to globular proteins by integrating results from the experimental methods of structural biology such as atomic resolution, x-ray crystallography, and multidimensional solution nuclear magnetic resonance (NMR) spectroscopy with those from molecular dynamics simulations and other calculations. Unfortunately, membrane proteins are problematic for the experimental and theoretical methods of structural biology, largely because these methods were developed with globular proteins in mind; as a result, both the breadth and depth of the structural analysis of membrane proteins lag far behind those of globular proteins. Structure determination by x-ray diffraction requires high-quality single crystals, and proteins associated with membranes are much more resistant to crystallization than water-soluble globular proteins; the multidimensional NMR methods that are so successful in determining the structures of globular proteins in solution are severely limited by the slow reorientation rates of proteins complexed with lipids; and molecular dynamics calculations of proteins were originally used with globular proteins in vacuum—including the effects of both lipid and solvent molecules in these calculations is an even more daunting task than for solvent molecules alone.

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References

  • Abragam, A. (1961) The Principles of Nuclear Magnetism. Oxford: Oxford University Press.

    Google Scholar 

  • Bechinger, B., Kim, Y., Chirlian, L. E., Gesell, J., Neumann, J., Montai, M., Tomich, J., Zasloff, M., and Opella S. J. (1991) Orientations of amphipathic helical peptides in membrane bilayers deter-mined by solid-state NMR spectroscopy. J. Biomol. NMR 1: 167–173.

    Article  PubMed  CAS  Google Scholar 

  • Bechinger, B., and Opella, S. J. (1991) Flat coil probe for NMR spectroscopy of oriented membrane samples. J. Magn. Reson. 95: 585–588.

    Google Scholar 

  • Bevins, C. and Zasloff, M. (1990) Peptides from Frog skin. Annu. Rev. Biochem. 59: 395–414.

    Article  PubMed  CAS  Google Scholar 

  • Blazyk, J., Hing, A., Schaefer, J., and Ferguson, M. C. (1991) Rotational-echo double-resonance (REDOR) NMR spectroscopy of the antimicrobial peptide magainin 2. J. Cell Biol. Suppl. 15G, 73.

    Google Scholar 

  • Bogusky, M. J., Schiksnis, R. A., Leo, G. C., and Opella, S. J. (1987) Protein backbone dynamics by solid state and solution 15N NMR spectroscopy. J. Magn. Reson. 72: 186–190.

    CAS  Google Scholar 

  • Bogusky, M. J., Leo, G. C., and Opella, S. J. (1988) Comparison of the dynamics of the membrane bound form of fd coat protein in micelles and in bilayers. Proteins Struct. Fund. Genet. 4: 123130.

    Google Scholar 

  • Boman, H. (1991) Developmental abnormalities in transgenic mice expressing a sialic acid-specific 9–0acetylesterase. Cell 65: 205.

    Article  PubMed  CAS  Google Scholar 

  • Borgias, B., and James, T. (1988) COMATOSE, a method for constrained refinement of macromolecular structure based on two-dimensional nuclear Overhauser effect spectra. J. Magn. Reson. 79: 493512.

    Google Scholar 

  • Braun, W. (1987) Distance geometry and related materials for protein structure determination from NMR data. Q. Rev. Biophys. 19: 115–157.

    Article  PubMed  CAS  Google Scholar 

  • Braun, W., Wilder, G., Lee, K., and Wuthrich, K. (1983) Conformation of glucagon in lipid-water interphase by 1H nuclear magnetic resonance. J. Mol. Biol. 169: 921–948.

    Article  PubMed  CAS  Google Scholar 

  • Brown, L. (1979) Use of fully deuterated micelles for conformational studies of membrane proteins by high resolution 1H nuclear magnetic resonance. Biochim. Biophys. Acta 557: 135–148.

    Article  PubMed  CAS  Google Scholar 

  • Brown, L., Braun, W., Kumar, A., and Wuthrich, K. (1982) High resolution nuclear magnetic resonance studies of the conformation and orientation of melittin bound to a lipid-water interface. Biophys. J. 37: 319–328.

    Article  PubMed  CAS  Google Scholar 

  • Bruch, M., Mcknight, C., and Gierasch, L. (1989) Helix formation and stability in a signal sequence. Biochemistry 28: 8554–8561.

    Article  PubMed  CAS  Google Scholar 

  • Chang, C., Blobel, G., and Model, P. (1978) Detection of prokaryotic signal peptidase in an Escherichia coli membrane fraction: endoproteolytic cleavage of nascent fl precoat protein. Proc. Natl. Acad. Sci. USA 75: 361–365.

    Article  PubMed  CAS  Google Scholar 

  • Chirlian, L. E., and Opella, S. J. (1990) Molecular structure by solid-state NMR spectroscopy. Adv. Magn. Reson. (W. Warren, ed.), Acad. Press, NY, NY, 14: 183–202.

    Google Scholar 

  • Clore, G., and Gronenborn, A. (1989) Determination of three-dimensional structures of proteins and nucleic acids in solution by nuclear magnetic resonance spectroscopy, CRC Crit. Rev. Biochem. Mol. Biol. 24: 479–564.

    Article  CAS  Google Scholar 

  • Cross, T. A., Frey, M. H., and Opella, S. J. (1983) 15N spin exchange in a protein. J. Am. Chem. Soc. 105: 7741–7743.

    Google Scholar 

  • Cross, T. A., and Opella, S. J. (1980) Structural properties of fd coat protein in sodium dodecyl sulfate micelles. Biochem. Biophys. Res. Commun. 92: 478–484.

    Article  PubMed  CAS  Google Scholar 

  • Cross, T. A., and Opella, S. J. (1983) Protein structure by solid state NMR. J. Am. Chem. Soc. 105: 306308.

    Google Scholar 

  • Deisenhofer, J., Epp, O., Miki, K., Huber, R., and Michel, H. (1985) Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3A resolution. Nature 318: 618.

    Article  PubMed  CAS  Google Scholar 

  • Dohlman, H., Thorner, J., Caron, M., and Lefkowitz, R. (1991) Model systems for the study of seventransmembrane-segment receptors. Annu. Rev. Biochem. 60: 653–688.

    Article  PubMed  CAS  Google Scholar 

  • Dunker, A., Fodor, S., and Williams, R. (1982) Lipid-dependent structural changes of an amphomorphic membrane protein. Biophys. J. 37: 201–203.

    Article  PubMed  CAS  Google Scholar 

  • Dyson, H., and Wright, P. (1991) Defining solution conformations of small linear peptides. Annu. Rev. Biophys. Biophys. Chem. 20: 519–538.

    Article  PubMed  CAS  Google Scholar 

  • Frey, M. H., and Opella, S. J. (1984) “C Spin exchange in amino acids and peptides. J. Am. Chem. Soc. 106: 4942–4945.

    Google Scholar 

  • Gullion, T., and Schaefer, J. (1989) Rotational-echo double-resonance NMR. J. Magn. Reson. 81: 196200.

    Google Scholar 

  • Glucksman, M., Bhattacharjee, S., and Makowski, L. (1992) Three-dimensional structure of a cloning vector. J. Mol. Biol. 226: 455–470.

    Article  PubMed  CAS  Google Scholar 

  • Griffin, R. (1981) Solid state nuclear magnetic resonance of lipid bilayers. Methods Enzymol. 72: 108173.

    Google Scholar 

  • Harbison, G., Jelinski, L., Stark, R., Torchia, D., Herzfeld, J., and Griffin, R. (1984) 15N chemical shift and 15N–13C dipolar tensors for the peptide bond in [1–13C]Clycyl[15N]glycine hydrochloride monohydrate. J. Magn. Reson. 60: 79–82.

    Google Scholar 

  • Hagen, D., Weiner, J., and Sykes, B. (1978) Fluorotyrosine M13 coat protein: fluorine-19 nuclear magnetic resonance study of the motional properties of an integral membrane protein in phospholipid vesicles. Biochemistry 17: 3860–3866.

    Article  PubMed  CAS  Google Scholar 

  • Hartzell, C., Whitfield, M., Oas, T., and Drobny, G. (1987) Determination of the 15N and 13C chemical shift tensors of L-[13C]Alanyl-L-[15N]alanine from the dipole-coupled powder patterns. J. Am. Chem. Soc. 109: 5966–5969.

    Article  CAS  Google Scholar 

  • Havel, T. (1990) The sampling properties of some distance geometry algorithms applied to unconstrained polypeptide chains: a study of 1830 independently computed conformations. Biopolymers 29: 1565–1585.

    Article  PubMed  CAS  Google Scholar 

  • Henderson, R., Baldwin, J., Cesko, T., Zemlin, F., Beckmann, E., and Downing, K. (1990) Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J. Mol. Biol. 213: 899–929.

    Article  PubMed  CAS  Google Scholar 

  • Henry, G., and Sykes, B. (1990) Hydrogen exchange kinetics in a membrane protein determined by 15N NMR spectroscopy: use of the INEPT experiment to follow individual amides in detergent-solubilized M13 coat protein. Biochemistry 29: 6303–6313.

    Article  PubMed  CAS  Google Scholar 

  • Holak, T., Engstrom, A., Kraulis, P., Lindeberg, G., Bennich, H., Jones, T., Gronenborn, A., and Core, G. (1988) The solution conformation of the antibacterial peptide cecropin A: a nuclear magnetic resonance and dynamical simulated annealing study. Biochemistry 27: 7620–7629.

    Article  PubMed  CAS  Google Scholar 

  • Ikura, M., Kay, L., and Bax A. (1990) A novel approach for sequential assignment of 1H, 13C and t5N spectra of larger proteins: heteronuclear triple-resonance three-dimensional NMR spectroscopy. Application to calmodulin. Biochemistry 29: 4659–4667.

    Article  PubMed  CAS  Google Scholar 

  • Inagaki, F., Shimada, I., Kawaguchi, K., Hirano, M., Terasawa, I., Ikura, T., and Go, N. (1989) Structure of melittin bound to perdeuterated dodecylphosphocholine micelles as studied by two-dimensional NMR and distance geometry calculations. Biochemistry 28: 5985–5991.

    Article  CAS  Google Scholar 

  • Keniry, M., Gutowsky, H., and Oldfield, E. (1984) Surface dynamics of the integral membrane protein bacteriorhodopsin. Nature 307: 383–386.

    Article  PubMed  CAS  Google Scholar 

  • Kersh, J., Tomich, J., and Montai, M. (1989) The M25 transmembrane domain of the nicotinic cholinergic receptor forms ion channels in human erythrocyte membranes. Biochem. Biophys. Res. Commun. 162: 352–356.

    Article  PubMed  CAS  Google Scholar 

  • Kühlbrandt, W., Wang, D. N., and Fujiyoshi, Y. (1994) Atomic model of plant light-harvesting complex by electronic crystallography. Nature 367: 614–621.

    Article  PubMed  Google Scholar 

  • Lauterwein, J., Bosch, C., Brown, L., and Wuthrich, K. (1979) Physiochemical studies of the protein-lipid interactions in melittin-containing micelles. Biochim. Biophys. Acta 556: 244–264.

    Article  PubMed  CAS  Google Scholar 

  • Lee, K., Fitton, J., and Wuthrich, K. (1987) Nuclear magnetic resonance investigation of the conformation of d-haemolysin bound to dodecylphosphocholine micelles. Biochim. Biophys. Acta. 911: 144–153.

    Article  PubMed  CAS  Google Scholar 

  • Leo, G. C., Conago, L. A., Valentine, K. G., and Opella, S. J. (1987) Dynamics of fd coat protein in lipid bilayers. Biochemistry 26: 854–862.

    Article  PubMed  CAS  Google Scholar 

  • Lewis, B., Harbison, G., Herzfeld, J., and Griffin, R. (1985) NMR structural analysis of a membrane protein: bacteriorhodopsin peptide backbone orientation and motion. Biochemistry 24: 46714679.

    Google Scholar 

  • Makowski, L. (1984) Structural diversity in filamentous bacteriophages. In: Biological Macromolecules and Assemblies, edited by A. McPherson. New York: Wiley, p. 202.

    Google Scholar 

  • Marion, D., Ikura, M., Tshudin, R., and A. Bax (1989) Rapid recording of 2D NMR spectra without phase cycling. Application to the study of hydrogen exchange in proteins. J. Magn. Reson. 85: 393399.

    Google Scholar 

  • Marvin, D., and Hohn, B. (1969) Filamentous bacterial viruses. Bacterial Rev. 33: 172–209.

    CAS  Google Scholar 

  • Marvin, D., and Wachtel, E. (1975) Structure and assembly of filamentous bacterial viruses. Nature 253: 19–23.

    Article  PubMed  CAS  Google Scholar 

  • McDermott, A., Thompson, L., Winklel, C., Farrar, M., Pelletier, S., Lugtenburg, J., Herzfeld, J., and Griffin, R. (1991) Mechanism of proton pumping in bacteriorhodopsin by solid-state NMR: the protonation state of tyrosine in the light-adapted and M states. Biochemistry 30: 8366–8371.

    Article  PubMed  CAS  Google Scholar 

  • McLaughlin, A., Cullis, P., Hemminga, M., Hoult, D., Redda, G., Ritchie, G., Seeley, P., and Richards, R. (1975) Application of 31P NMR to model and biological membrane systems. FEBS Lett. 57: 213–218.

    Article  PubMed  CAS  Google Scholar 

  • Montal, M. (1990) Molecular anatomy and molecular design of channel proteins. FASEB J. 9: 26232635.

    Google Scholar 

  • Mulvey, D., King, G., Cooke, R., Doak, D., Harvey, T., and Campbell, I. (1989) High resolution 1H NMR study of the solution structure of the S4 segment of the sodium channel protein. FEBS Lett. 257: 113–117.

    Article  PubMed  CAS  Google Scholar 

  • Nambudripad, R., Stark, W., Opella, S. J., and Makowski, L. (1991) Membrane mediated assembly of filamentous bacteriophage Pfl. Science 252: 1305–1308.

    Article  PubMed  CAS  Google Scholar 

  • Oiki, S., Danho, W., Madison, V., and Montal, M. (1988) M25, a candidate for the structure lining the ionic channel of the nicotinic cholinergic receptor. Proc. Natl. Acad. Sci. USA 85: 8703–8707.

    Article  PubMed  CAS  Google Scholar 

  • Oldfield, E., Kinsey, R., and Kintanar, A. (1982) Recent advances in the study of bacteriorhodopsin dynamic structure using high-field solid-state nuclear magnetic resonance spectroscopy. Methods Enzymol. 88: 310–325.

    Article  CAS  Google Scholar 

  • Opella, S. J. (1982) Solid state NMR of biological systems. Annu. Rev. Phys. Chem. 33: 533–549.

    Article  CAS  Google Scholar 

  • Opella, S. J. (1985) Protein dynamics by solid state NMR. Methods Enzymol. 17: 327–361.

    Google Scholar 

  • Opella, S. J., and Stewart, P. (1989) Solid-state nuclear magnetic resonance structural studies of proteins. Method Enzymol. 176: 242–275.

    Article  CAS  Google Scholar 

  • Opella, S. J., Stewart, P., and Valentine, K. (1987) Protein structure by solid-state NMR spectroscopy. Q. Rev. Biophys. 19: 7–49.

    Article  PubMed  CAS  Google Scholar 

  • Opella, S. J., and Waugh, J. (1977) Two-dimensional 13C NMR of highly oriented polyethylene. J. Chem. Phys. 66: 4919–4924.

    Article  CAS  Google Scholar 

  • Pake, G. (1948) Nuclear resonance absorption in hydrated crystals: fine structure of the proton line. J. Chem. Phys. 16: 327–339.

    Article  CAS  Google Scholar 

  • Pervushin, K., Arsenieu, A., Kozhich, A. and Ivanov, U. (1991) Two-dimensional NMR study of the conformation of (34–65) bacterioopsin polypeptide in SDS micelles. J. Biomol. NMR 1: 313–322.

    Article  PubMed  CAS  Google Scholar 

  • Raleigh, D., Levitt, M., and Griffin, R. (1988) Rotational resonance in solid state NMR. Chem. Phys. Lett. 146: 71–76.

    Article  CAS  Google Scholar 

  • Rees, D., Komiga, H., Yeates, T., Allen, J., and Feher, G. (1989) The bacterial photosynthetic reaction center as a model for membrane proteins. Annu. Rev. Biochem. 58: 607–633.

    Article  PubMed  CAS  Google Scholar 

  • Rice, D., Blume, A., Herzfeld, J., Wittebort, R., Huangi, T., Das Gupta, S., and Griffin, R. (1981) Solid state NMR investigations of lipid bilayers, peptides and proteins. Biomol. Stereodynam. II: 271.

    Google Scholar 

  • Sanders, J., van Nuland, N., Edholm, O., and Hemminga, M. (1991) Conformation and aggregation of M13 coat protein studied by molecular dynamics. Biophys. Chem. 41: 193–202.

    Article  PubMed  CAS  Google Scholar 

  • Schiksnis, R. A., Bogusky, M. J., Tsang, P., and Opella, S. J. (1987) Structure and dynamics of the Pfl filamentous bacteriophage coat protein in micelles. Biochemistry 26: 1373–1381.

    Article  PubMed  CAS  Google Scholar 

  • Seelig, J., and Niederberger, W. (1974) Deuterium-labeled lipids as structural probes in liquid crystalline bilayers. A deuterium magnetic resonance study. J. Am. Chem. Soc. 96: 2069–2072.

    Article  CAS  Google Scholar 

  • Shon, K., and Opella, S. J. (1989) Detection of 1H homonuclear NOE between amide sites in proteins with 1H/15N heteronuclear correlation spectroscopy. J. Magn. Reson. 82: 193–197.

    CAS  Google Scholar 

  • Shon, K., Kim, Y., Colnago, L. A., and Opella, S. J. (1991a) NMR studies of the structure and dynamics of membrane bound bacteriophage Pfl coat protein. Science 252: 1303–1305.

    Article  PubMed  CAS  Google Scholar 

  • Shon, K, Schrader, P., Kim, Y., Bechinger, B., Zasloff, M., and Opella, S. J. (1991) NMR structural studies of membrane bound peptides and proteins. In: Biotechnology: Bridging Research and Applications, edited by D. Kamely, A. Chakrabarty, and S. Kornguth. Dodrecht, the Netherlands: Kluwer, p. 109–124.

    Chapter  Google Scholar 

  • Shon, K., Schrader, P., Opella, S. J., Richards, J., and Tomich, J. (1989) NMR spectra of synthetic membrane bound coat protein species. In: Frontiers of NMR in Molecular Biology: UCLA Symposia on Molecular and Cellular Biology, New Series, edited by D. Live, I. Armitage, and D. Patel. New York: Alan R. Liss, p. 109–118.

    Google Scholar 

  • Smith, S., and Griffin, R. (1988) High-resolution solid-state NMR of proteins. Annu. Rev. Phys. Chem. 39: 511–535.

    Article  PubMed  CAS  Google Scholar 

  • Sobol, A., Arsenieu, A., Abdulaeva, G., Musina, L., and Bystrov, V. (1992) Sequence-specific resonance assignment and secondary structure of (1–71) bacterioopsin. J. Biomol. NMR 2: 161–171.

    Article  PubMed  CAS  Google Scholar 

  • Spiess, H. (1982) Rotation of molecules and nuclear spin relaxation. In: NMR Basic Principles and Prog-ress, edited by P. Diehl, E. Fluck, and R. Kosfeld. New York: Wiley, p. 55–214.

    Google Scholar 

  • Spruijt, R., and Hemminga, M. (1991) The in situ aggregational and conformational state of the major coat protein of bacteriophage M13 in phospholipid bilayers mimicking the inner membrane of host Escherichia coli. Biochemistry 30: 11147–11154.

    CAS  Google Scholar 

  • Spruijt, R., Wolfs, C., and Hemminga, M. (1989) Aggregation-related conformational changes of the membrane-associated coat protein of bacteriophage M13. Biochemistry 28: 9158–9165.

    Article  PubMed  CAS  Google Scholar 

  • Teng, Q., and Cross, T. (1989) The in situ determination of the 15N chemical-shift tensor orientation in a polypeptide. J. Magn. Reson. 85: 439–447.

    CAS  Google Scholar 

  • Tobias, D., Klein, M., and Opella, S. J. (1993) Molecular dynamics simulation of Pf1 coat protein. Biophys. J. 64: 670–675.

    Article  PubMed  CAS  Google Scholar 

  • Torchia, D. (1984) Solid-state NMR studies of protein internal dynamics. Annu. Rev. Biophys. Bioeng. 13: 125–144.

    Article  PubMed  CAS  Google Scholar 

  • Weiss, M., Abele, U., Weckesser, J., Welte, W., Schultz, E., and Schulz, G. (1991) Molecular architecture and electrostatic properties of a bacterial porin. Science 254: 1627–1630.

    Article  PubMed  CAS  Google Scholar 

  • Wennerberg, A., Cooke, R., Carlquist, M., Rigler, R., and Campbell, J. (1990) A 1H NMR study of the solution conformation of the neuropeptide galanin. Biochem. Biophys. Res. Commun. 166: 11021109.

    Google Scholar 

  • Wuthrich, K. (1986) NMR of Proteins and Nucleic Acids. New York: Wiley.

    Google Scholar 

  • Zasloff, M. (1987) Magainins, a class of antimicrobial peptides from Xenopus skin: isolation, characterization of two active forms, and partial cDNA sequence of a precursor. Proc. Natl. Acad. Sci. USA 84: 5449–5453.

    Article  PubMed  CAS  Google Scholar 

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Authors
  1. Stanley J. Opella
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Editors and Affiliations

  1. College of Medicine, Department of Physiology and Biophysics, University of California, Irvine, Irvine, California, USA

    Stephen H. White Ph.D. (Professor of Physiology and Biophysics) (Professor of Physiology and Biophysics)

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© 1994 American Physiological Society

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Opella, S.J. (1994). Nuclear Magnetic Resonance Approaches to Membrane Protein Structure. In: White, S.H. (eds) Membrane Protein Structure. Methods in Physiology Series. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-7515-6_11

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  • DOI: https://doi.org/10.1007/978-1-4614-7515-6_11

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