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Progress of membrane protein structural studies

  • School of Life Science, University of Science and Technology of China, Hefei 230027, China

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  • Corresponding author: TIAN Chang-lin, E-mail: cltian@ustc.edu.cn
  • Received Date: 28 June 2008
  • Rev Recd Date: 10 July 2008
  • Publish Date: 31 August 2008
    Abstract

  • Abstract

    Membrane proteins play vital roles in maintaining cells proper function, but structural studies of membrane proteins lag far behind water soluble proteins. Because it is unnecessary to prepare crystals of membrane proteins, nuclear magnetic resonance (NMR) is coming to play an increasingly important role in membrane protein structural studies. Several NMR methods can be applied for different states of membrane protein samples. Solution NMR is used to study membrane protein in detergent micelles or in low q bicelles, and several membrane proteins structures have been solved using solution NMR. Static oriented solid state NMR can be applied for uniformly oriented membrane proteins in high q bicelles or in lipid bilayers. Methods of magic angle spinning (MAS) solid state NMR are also under development to solve membrane protein structures in lipid bilayers.

    Abstract

    Membrane proteins play vital roles in maintaining cells proper function, but structural studies of membrane proteins lag far behind water soluble proteins. Because it is unnecessary to prepare crystals of membrane proteins, nuclear magnetic resonance (NMR) is coming to play an increasingly important role in membrane protein structural studies. Several NMR methods can be applied for different states of membrane protein samples. Solution NMR is used to study membrane protein in detergent micelles or in low q bicelles, and several membrane proteins structures have been solved using solution NMR. Static oriented solid state NMR can be applied for uniformly oriented membrane proteins in high q bicelles or in lipid bilayers. Methods of magic angle spinning (MAS) solid state NMR are also under development to solve membrane protein structures in lipid bilayers.
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    • References(51)
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    Tian C, Karra M D, Ellis C D, et al. Membrane protein preparation for TROSY NMR screening[J]. Methods Enzymol, 2005, 321-334.
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    Tian C, Vanoye C G, Kang C, et al. Preparation, functional characterization, and NMR studies of human KCNE1, a voltage-gated potassium channel accessory subunit associated with deafness and long QT syndrome[J]. Biochemistry, 2007, 41: 11 459-11 472.
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    Sanders C R, Oxenoid K. Customizing model membranes and samples for NMR spectroscopic studies of complex membrane proteins[J]. Biochim Biophys Acta, 2000, 1-2: 129-145.
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    Angrand M, Briolay A, Ronzon F, et al. Detergent-mediated reconstitution of a glycosyl-phosphatidylinositol-protein into liposomes[J]. Eur J Biochem, 1997, 1: 168-176.
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    Voehler M W, Collier G, Young J K, et al. Performance of cryogenic probes as a function of ionic strength and sample tube geometry[J]. J Magn Reson, 2006, 1: 102-109.
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    Kelly A E, Ou H D, Withers R, et al. Low-conductivity buffers for high-sensitivity NMR measurements[J]. J Am Chem Soc, 2002, 40: 12 013-12 019.
    [27]
    Sanders C R, Sonnichsen F. Solution NMR of membrane proteins: practice and challenges[J]. Magn Reson Chem, 2006, S24-40.
    [28]
    Dosset P, Hus J C, Marion D, et al. A novel interactive tool for rigid-body modeling of multi-domain macromolecules using residual dipolar couplings[J]. J Biomol NMR, 2001, 3: 223-231.
    [29]
    Valafar H, Prestegard J H. REDCAT: a residual dipolar coupling analysis tool[J]. J Magn Reson, 2004, 2: 228-241.
    [30]
    Battiste J L, Wagner G. Utilization of site-directed spin labeling and high-resolution heteronuclear nuclear magnetic resonance for global fold determination of large proteins with limited nuclear overhauser effect data[J]. Biochemistry, 2000, 18: 5 355-5 365.
    [31]
    Tugarinov V, Kay L E. An isotope labeling strategy for methyl TROSY spectroscopy[J]. J Biomol NMR, 2004, 2: 165-172.
    [32]
    Tugarinov V, Kay L E. Ile, Leu, and Val methyl assignments of the 723-residue malate synthase G using a new labeling strategy and novel NMR methods[J]. J Am Chem Soc, 2003, 45: 13 868-13 878.
    [33]
    Li C, Mo Y, Hu J, et al. Analysis of RF heating and sample stability in aligned static solid-state NMR spectroscopy[J]. J Magn Reson, 2006, 1: 51-57.
    [34]
    Gorkov P L, Chekmenev E Y, Fu R, et al. A large volume flat coil probe for oriented membrane proteins[J]. J Magn Reson, 2006, 1: 9-20.
    [35]
    Wang J, Denny J, Tian C, et al. Imaging membrane protein helical wheels[J]. J Magn Reson, 2000, 1: 162-167.
    [36]
    Mesleh M F, Veglia G, DeSilva T M, et al. Dipolar waves as NMR maps of protein structure[J]. J Am Chem Soc, 2002, 16: 4 206-4 207.
    [37]
    Mesleh M F, Opella S J. Dipolar Waves as NMR maps of helices in proteins[J]. J Magn Reson, 2003, 2: 288-299.
    [38]
    Schaefer J. REDOR-determined distances from heterospins to clusters of 13C labels[J]. J Magn Reson, 1999, 1: 272-275.
    [39]
    Castellani F, van Rossum B, Diehl A, et al. Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy[J]. Nature, 2002, 6 911: 98-102.
    [40]
    Li Y, Kijac A Z, Sligar S G, et al. Structural analysis of nanoscale self-assembled discoidal lipid bilayers by solid-state NMR spectroscopy[J]. Biophys J, 2006, 10: 3 819-3 828.
    [41]
    Lorch M, Fahem S, Kaiser C, et al. How to prepare membrane proteins for solid-state NMR: A case study on the alpha-helical integral membrane protein diacylglycerol kinase from E[J]. coli. Chembiochem, 2005, 9: 1 693-1 700.
    [42]
    Bechinger B, Aisenbrey C, Bertani P. The alignment, structure and dynamics of membrane-associated polypeptides by solid-state NMR spectroscopy[J]. Biochim Biophys Acta, 2004, 1-2: 190-204.
    [43]
    Shimba N, Kovacs H, Stern A S, et al. Optimization of 13C direct detection NMR methods[J]. J Biomol NMR, 2004, 2: 175-179.
    [44]
    Bertini I, Felli I C, Kummerle R, et al. 13C-13C NOESY: A constructive use of 13C-13C spin-diffusion[J]. J Biomol NMR, 2004, 3: 245-251.
    [45]
    Tugarinov V, Kay L E, Ibraghimov I, et al. High-resolution four-dimensional 1H-13C NOE spectroscopy using methyl-TROSY, sparse data acquisition, and multidimensional decomposition[J]. J Am Chem Soc, 2005, 8: 2 767-2 775.
    [46]
    Shen Y, Lange O, Delaglio F, et al. Consistent blind protein structure generation from NMR chemical shift data[J]. Proc Natl Acad Sci U S A, 2008, 12: 4 685-4 690.
    [47]
    Morcombe C R, Paulson E K, Gaponenko V, et al. 1H-15N correlation spectroscopy of nanocrystalline proteins[J]. J Biomol NMR, 2005, 3: 217-230.
    [48]
    Lefman J, Zhang P, Hirai T, et al. Three-dimensional electron microscopic imaging of membrane invaginations in Escherichia coli overproducing the chemotaxis receptor Tsr[J]. J Bacteriol, 2004, 15: 5 052-5 061.
    [49]
    Elmes M L, Scraba D G, Weiner J H. Isolation and characterization of the tubular organelles induced by fumarate reductase overproduction in Escherichia coli[J]. J Gen Microbiol, 1986, 1 429-1 439.
    [50]
    Reif B, Griffin R G. 1H detected 1H,15N correlation spectroscopy in rotating solids[J]. J Magn Reson, 2003,1: 78-83.
    [51]
    Zhou D H, Shah G, Cormos M, et al. Proton-detected solid-state NMR spectroscopy of fully protonated proteins at 40 kHz magic-angle spinning[J]. J Am Chem Soc, 2007,38: 11 791-11 801.
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    [1]
    Wallin E, von Heijne G. Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms[J]. Protein Sci, 1998, 4: 1 029-1 038.
    [2]
    Chou J J, Kaufman J D, Stahl S J, et al. Micelle-induced curvature in a water-insoluble HIV-1 Env peptide revealed by NMR dipolar coupling measurement in stretched polyacrylamide gel[J]. J Am Chem Soc, 2002, 11: 2 450-2 451.
    [3]
    Al-Hashimi H M, Valafar H, Terrell M, et al. Variation of molecular alignment as a means of resolving orientational ambiguities in protein structures from dipolar couplings[J]. J Magn Reson, 2000, 2: 402-406.
    [4]
    Ottiger M, Bax A. Characterization of magnetically oriented phospholipid micelles for measurement of dipolar couplings in macromolecules[J]. J Biomol NMR, 1998, 3: 361-372.
    [5]
    Opella S J, Marassi F M. Structure determination of membrane proteins by NMR spectroscopy[J]. Chem Rev, 2004, 8: 3 587-3 606.
    [6]
    Nicholson L K, Moll F, Mixon T E, et al. Solid-state 15N NMR of oriented lipid bilayer bound gramicidin A[J]. Biochemistry, 1987, 21: 6 621-6 626.
    [7]
    Ketchem R, Roux B, Cross T. High-resolution polypeptide structure in a lamellar phase lipid environment from solid state NMR derived orientational constraints[J]. Structure, 1997, 12: 1 655-1 669.
    [8]
    Quine J R, Brenneman M T, Cross T A. Protein structural analysis from solid-state NMR-derived orientational constraints[J]. Biophys J, 1997, 5: 2 342-2 348.
    [9]
    Poget S F, Girvin M E. Solution NMR of membrane proteins in bilayer mimics: small is beautiful, but sometimes bigger is better[J]. Biochim Biophys Acta, 2007, 12: 3 098-3 106.
    [10]
    Poget S F, Cahill S M, Girvin M E. Isotropic bicelles stabilize the functional form of a small multidrug-resistance pump for NMR structural studies[J]. J Am Chem Soc, 2007,129(9):2 432-2 433.
    [11]
    Tucker J, Grisshammer R. Purification of a rat neurotensin receptor expressed in Escherichia coli[J]. Biochem J, 1996, 891-899.
    [12]
    Tian C, Karra M D, Ellis C D, et al. Membrane protein preparation for TROSY NMR screening[J]. Methods Enzymol, 2005, 321-334.
    [13]
    Tian C, Vanoye C G, Kang C, et al. Preparation, functional characterization, and NMR studies of human KCNE1, a voltage-gated potassium channel accessory subunit associated with deafness and long QT syndrome[J]. Biochemistry, 2007, 41: 11 459-11 472.
    [14]
    Tian C, Breyer R M, Kim H J, et al. Solution NMR spectroscopy of the human vasopressin V2 receptor, a G protein-coupled receptor[J]. J Am Chem Soc, 2005, 22: 8 010-8 011.
    [15]
    Sanders C R, Oxenoid K. Customizing model membranes and samples for NMR spectroscopic studies of complex membrane proteins[J]. Biochim Biophys Acta, 2000, 1-2: 129-145.
    [16]
    Rigaud J L, Pitard B, Levy D. Reconstitution of membrane proteins into liposomes: application to energy-transducing membrane proteins[J]. Biochim Biophys Acta, 1995, 3: 223-246.
    [17]
    Angrand M, Briolay A, Ronzon F, et al. Detergent-mediated reconstitution of a glycosyl-phosphatidylinositol-protein into liposomes[J]. Eur J Biochem, 1997, 1: 168-176.
    [18]
    Knol J, Sjollema K, Poolman B. Detergent-mediated reconstitution of membrane proteins[J]. Biochemistry, 1998, 46: 16 410-16 415.
    [19]
    Moll F, 3rd Cross T A. Optimizing and characterizing alignment of oriented lipid bilayers containing gramicidin D[J]. Biophys J, 1990, 2: 351-362.
    [20]
    LoGrasso P V, Moll F, 3rd Cross T A. Solvent history dependence of gramicidin A conformations in hydrated lipid bilayers[J]. Biophys J, 1988, 2: 259-267.
    [21]
    Tian C, Tobler K, Lamb R A, et al. Expression and initial structural insights from solid-state NMR of the M2 proton channel from influenza A virus[J]. Biochemistry, 2002, 37: 11 294-11 300.
    [22]
    Quine J R, Cross T A. Protein Structure in Anisotropic Environments: Unique Structural Fold from Orientational Constrains[J]. Concepts in Magnetic Resonance, 2000, 2: 71-82.
    [23]
    Quine J R, Cross T A, Chapman M S, et al. Mathematical aspects of protein structure determination with NMR orientational restraints[J]. Bull Math Biol, 2004, 6: 1 705-1 730.
    [24]
    Pervushin K, Riek R, Wider G, et al. Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution[J]. Proc Natl Acad Sci U S A, 1997, 23: 12 366-12 371.
    [25]
    Voehler M W, Collier G, Young J K, et al. Performance of cryogenic probes as a function of ionic strength and sample tube geometry[J]. J Magn Reson, 2006, 1: 102-109.
    [26]
    Kelly A E, Ou H D, Withers R, et al. Low-conductivity buffers for high-sensitivity NMR measurements[J]. J Am Chem Soc, 2002, 40: 12 013-12 019.
    [27]
    Sanders C R, Sonnichsen F. Solution NMR of membrane proteins: practice and challenges[J]. Magn Reson Chem, 2006, S24-40.
    [28]
    Dosset P, Hus J C, Marion D, et al. A novel interactive tool for rigid-body modeling of multi-domain macromolecules using residual dipolar couplings[J]. J Biomol NMR, 2001, 3: 223-231.
    [29]
    Valafar H, Prestegard J H. REDCAT: a residual dipolar coupling analysis tool[J]. J Magn Reson, 2004, 2: 228-241.
    [30]
    Battiste J L, Wagner G. Utilization of site-directed spin labeling and high-resolution heteronuclear nuclear magnetic resonance for global fold determination of large proteins with limited nuclear overhauser effect data[J]. Biochemistry, 2000, 18: 5 355-5 365.
    [31]
    Tugarinov V, Kay L E. An isotope labeling strategy for methyl TROSY spectroscopy[J]. J Biomol NMR, 2004, 2: 165-172.
    [32]
    Tugarinov V, Kay L E. Ile, Leu, and Val methyl assignments of the 723-residue malate synthase G using a new labeling strategy and novel NMR methods[J]. J Am Chem Soc, 2003, 45: 13 868-13 878.
    [33]
    Li C, Mo Y, Hu J, et al. Analysis of RF heating and sample stability in aligned static solid-state NMR spectroscopy[J]. J Magn Reson, 2006, 1: 51-57.
    [34]
    Gorkov P L, Chekmenev E Y, Fu R, et al. A large volume flat coil probe for oriented membrane proteins[J]. J Magn Reson, 2006, 1: 9-20.
    [35]
    Wang J, Denny J, Tian C, et al. Imaging membrane protein helical wheels[J]. J Magn Reson, 2000, 1: 162-167.
    [36]
    Mesleh M F, Veglia G, DeSilva T M, et al. Dipolar waves as NMR maps of protein structure[J]. J Am Chem Soc, 2002, 16: 4 206-4 207.
    [37]
    Mesleh M F, Opella S J. Dipolar Waves as NMR maps of helices in proteins[J]. J Magn Reson, 2003, 2: 288-299.
    [38]
    Schaefer J. REDOR-determined distances from heterospins to clusters of 13C labels[J]. J Magn Reson, 1999, 1: 272-275.
    [39]
    Castellani F, van Rossum B, Diehl A, et al. Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy[J]. Nature, 2002, 6 911: 98-102.
    [40]
    Li Y, Kijac A Z, Sligar S G, et al. Structural analysis of nanoscale self-assembled discoidal lipid bilayers by solid-state NMR spectroscopy[J]. Biophys J, 2006, 10: 3 819-3 828.
    [41]
    Lorch M, Fahem S, Kaiser C, et al. How to prepare membrane proteins for solid-state NMR: A case study on the alpha-helical integral membrane protein diacylglycerol kinase from E[J]. coli. Chembiochem, 2005, 9: 1 693-1 700.
    [42]
    Bechinger B, Aisenbrey C, Bertani P. The alignment, structure and dynamics of membrane-associated polypeptides by solid-state NMR spectroscopy[J]. Biochim Biophys Acta, 2004, 1-2: 190-204.
    [43]
    Shimba N, Kovacs H, Stern A S, et al. Optimization of 13C direct detection NMR methods[J]. J Biomol NMR, 2004, 2: 175-179.
    [44]
    Bertini I, Felli I C, Kummerle R, et al. 13C-13C NOESY: A constructive use of 13C-13C spin-diffusion[J]. J Biomol NMR, 2004, 3: 245-251.
    [45]
    Tugarinov V, Kay L E, Ibraghimov I, et al. High-resolution four-dimensional 1H-13C NOE spectroscopy using methyl-TROSY, sparse data acquisition, and multidimensional decomposition[J]. J Am Chem Soc, 2005, 8: 2 767-2 775.
    [46]
    Shen Y, Lange O, Delaglio F, et al. Consistent blind protein structure generation from NMR chemical shift data[J]. Proc Natl Acad Sci U S A, 2008, 12: 4 685-4 690.
    [47]
    Morcombe C R, Paulson E K, Gaponenko V, et al. 1H-15N correlation spectroscopy of nanocrystalline proteins[J]. J Biomol NMR, 2005, 3: 217-230.
    [48]
    Lefman J, Zhang P, Hirai T, et al. Three-dimensional electron microscopic imaging of membrane invaginations in Escherichia coli overproducing the chemotaxis receptor Tsr[J]. J Bacteriol, 2004, 15: 5 052-5 061.
    [49]
    Elmes M L, Scraba D G, Weiner J H. Isolation and characterization of the tubular organelles induced by fumarate reductase overproduction in Escherichia coli[J]. J Gen Microbiol, 1986, 1 429-1 439.
    [50]
    Reif B, Griffin R G. 1H detected 1H,15N correlation spectroscopy in rotating solids[J]. J Magn Reson, 2003,1: 78-83.
    [51]
    Zhou D H, Shah G, Cormos M, et al. Proton-detected solid-state NMR spectroscopy of fully protonated proteins at 40 kHz magic-angle spinning[J]. J Am Chem Soc, 2007,38: 11 791-11 801.
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