Solid-State NMR Spectroscopic Approaches to Investigate Dynamics, Secondary Structure and Topology of Membrane Proteins

Abstract

Solid-state NMR spectroscopy is routinely used to determine the structural and dynamic properties of both membrane proteins and peptides in phospholipid bilayers [1-26]. From the perspective of the perpetuated lipids, 2H solid-state NMR spectroscopy can be used to probe the effect of embedded proteins on the order and dynamics of the acyl chains of phospholipid bilayers [8-13]. Moreover, 31P solid-state NMR spectroscopy can be used to investigate the interaction of peptides, proteins and drugs with phospholipid head groups [11-14]. The secondary structure of 13C = O site-specific isotopically labeled peptides or proteins inserted into lipid bilayers can be probed utilizing 13C CPMAS solid-state NMR spectroscopy [15-18]. Also, solid-state NMR spectroscopic studies can be utilized to ascertain pertinent informa- tion on the backbone and side-chain dynamics of 2H- and 15N-labeled proteins, respectively, in phospholipid bilayers [19-26]. Finally, specific 15N-labeled amide sites on a protein embedded inside oriented bilayers can be used to probe the alignment of the helices with respect to the bilayer normal [2]. A brief summary of all these solid-state NMR ap- proaches are provided in this minireview.

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S. Abu-Baker and G. Lorigan, "Solid-State NMR Spectroscopic Approaches to Investigate Dynamics, Secondary Structure and Topology of Membrane Proteins," Open Journal of Biophysics, Vol. 2 No. 4, 2012, pp. 109-116. doi: 10.4236/ojbiphy.2012.24014.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] T. A. Cross, “Solid-State Nuclear Magnetic Resonance Characterization of Gramicidin Channel Structure,” Methods in Enzymology, Vol. 289, 1997, pp. 672-696.
[2] T. A. Cross and S. J. Opella, “Solid-State NMR Structural Studies of peptides and Proteins in Membranes,” Current Opinion in Structural Biology, Vol. 4, No. 4, 1994, pp. 574-581. doi:10.1016/S0959-440X(94)90220-8
[3] J. R. Long, , W. J. Shaw, P. S. Stayton and G. P. Drobny, “Structure and Dynamics of Hydrated Staherin on Hydroxyapatite as Determined by Solid-State NMR,” Biochemistry, Vol. 40, No. 51, 2001, pp. 15451-15455.
[4] R. Mani, J. J. Buffy, A. J. Waring, R. I. Lehrer and M. Hong, “Solid-State NMR Investigation of the Selective Disruption of Lipid Membranes by Protegrin-1,” Biochemistry, Vol. 43, No. 43, 2004, pp. 13839-13848. doi:10.1021/bi048650t
[5] I. Marcotte, E. J. Dufourc, M. Ouellet and M. Auger, “Interaction of the Neuropeptide Met-Enkephalin with Zwitterionic And Negatively Charged Bicelles as Viewed by 31P and 2H Solid-State NMR,” Biophysical Journal, Vol. 85, No. 1, 2003, pp. 328-339.
[6] Y. Nakazawa and T. Asakura, “Structure Determination of a Peptide Model of the Repeated Helical Dmoain in Samia Cynthia Ricini Silk Fibroin before Spinning by a Combination of Advanced Solid-State NMR Methods,” Journal of the American Chemical Society, Vol. 125, No. 24, 2003, pp. 7230-7237.
[7] A. Watts, “Solid-State NMR Approaches for Studying the Interaction of Peptides and Proteins with Membranes,” Biochim Biophys Acta, Vol. 37, No. 2, 1998, pp. 297-318.
[8] B. W. Koenig, J. A. Ferritti and K. Gawrisch, “Site-Specific Deuterium Order Parameters and Membrane-Bound Behavior of a Peptide Fragment from the Intracellular Domain of HIV-1 gp-41,” Biochemistry, Vol. 38, No. 19, 1999, pp. 6327-6334.
[9] G. Laroche, E. J. Dufourc, M. Pezolet and J. Dufourcq, “Coupled Changes between Lipid Order and Polypeptide Conformation at the Membrane-Surface: A 2H NMR and Raman-Study of Polylysine Phosphatidic-Acid Systems,” Biochemistry, Vol. 29, No. 27, 1990, pp. 6460-6465. doi:10.1021/bi00479a018
[10] S. Yamaguchi, D. Huster, A. Waring, R. I. Lehrer, W. Kearney, B. F. Tack and M. Hong, “Orientation and Dynamics of an antimicrobial Peptide in the Lipid Bilayer by Solid-State NMR Spectroscopy,” Biophysical Journal, Vol. 81, No. 4, 2001, pp. 2203-2214. doi:10.1016/S0006-3495(01)75868-7
[11] S. Abu-Baker, X. Qi, J. Newstadt and G. A. Lorigan, “Structural Changes in a Binary Mixed Phospholipid Bilayer of DOPG and DOPS upon Sap C Interaction at Acidic pH Utilizing 31P and 2H solid-State NMR Spectroscopy,” Biochimica et Biophysica Acta, Vol. 17, No. 1, 2005, pp. 58-66.
[12] P. C. Dave, E. K. Tiburu, K. Damodaran and G. A. Lorigan, “31P and 2H Solid-State NMR Spectroscopic Studies of the Transmembrane Domain of the Membrane-Bound Protein Phospholamban,” Biophysical Journal, Vol. 86, 2004, pp. 1564-1573.
[13] J. Lu, K. Damodaran, J. Blazyk and G. A. Lorigan, “Solid-State Nuclear Magnetic Resonance Relaxation Studies of the Interaction Mechanism of Antimicrobial Peptides with Phospholipid Bilayer Membranes,” Biochemistry, Vol. 44, No. 30, 2005, pp. 10208-10217.
[14] J. S. Santos, D. K. Lee and A. Ramamoorthy, “Effects of Antidepressants on the Conformation of Phospholipid Headgroups Studied by Solid-State NMR,” Magnetic Resonance in Chemistry, Vol. 42, No. 2, 2004, pp. 105-114.
[15] D. J. Hirsh, J. Hammer, W. L. Maloy, J. Blazyk and J. Schaefer, “Secondary Structure and Location of a Magainin Analogue in Synthetic Phospholipid Bilayers,” Biochemistry, Vol. 35, No. 39, 1996, pp. 12733-12741. doi:10.1021/bi961468a
[16] S. Kimura, A. Naito, S. Tuzi and H. Saito, “Dynamics and Orietation of Transmembrane Peptide from Bacteriorhodopsin Incorporated into Lipid Bilayer as Revealed by Solid State 31P and 13C NMR Spectroscopy,” Biopolymers, Vol. 63, No. 2, 2002, pp. 122-131.
[17] S. Tuzi, A. Naito and H. Saito, “A High-Resolusion Solid-State 13C-NMR Study on [1-13C]Ala and [3-13C] Ala and [1-13C]Leu and Val-Labelled Bacteriorhodopsin: Conformation and Dynamics of Transmembrane Helics, Loops and Termini, and Hydration-Induced Conformational Changes,” European Journal of Biochemistry, Vol. 218, No. 3, 1993, pp. 837-844.
[18] S. Yamaguchi, K. Shimono, Y. Sudo, S. Tuzi, A. Naito and N. Kamo, “Conformation and Dynamics of the [3-13C]Ala, [1-13C]Val-Labeled Truncated Pharaonis Transducer, pHtrII(1-159), as Revealed by Site-Directed 13C Solid-State NMR: Changes Due to Association with Phoborhodopsin (Sensory Rhodopsin II),” Biophysical Journal, Vol. 86, No. 5, 2004, pp. 3131-3140.
[19] L. S. Batchelder, C. E. Sullivan, L. W. Jelinski and D. A. Trochia, “Characterization of Leucine Side-Chain Reorientation in Collagen-Fibrils by Solid-State Deuterium NMR,” Proceedings of the National Academy of Sciences of the USA, Vol. 79, No. 2, 1982, pp. 386-389.
[20] K. Beshah, E. T. Olejniczak and R. G. Griffin, “Deuterium NMR Study of Methyl Dynamics in L-Alanine,” Journal of Chemical Physics, Vol. 86, No. 9, 1987, pp. 4730-4736.
[21] M. A. Keniry, A. Kintanar, R. L. Smith, H. S. Gutowsky and E. Oldfield, “Nuclear Magnetic Resonance Relaxation of Deuteriomethyl-Labeled Amino Acids Crystals and in Halobacterium Halobium and E. coli Cell Membranes,” Biochemsitry, Vol. 23, 1984, pp. 288-298.
[22] R. A.vKinsey, A. Kintanar and E. Oldfield, “Dynamics of Amino Acid Side-Chains in Membrane Proteins by High Field Solid-State Deuterium Nuclear Magnetic Resonance Spectroscopy,” The Journal of Biological Chemistry, Vol. 256, No. 17, 1981, pp. 9028-9036.
[23] G. C. Leo, L. A. Colnago, K. G. Valentine and S. J. Opella, “Dynamics of fd Coat Protein in Lipid Bilayers,” Biochemistry, Vol. 26, No. 3, 1987, pp. 854-862. doi:10.1021/bi00377a029
[24] W. Ying, S. E. Irvine, R. A. Beekman, D. J. Siminovitch and S. O. Smith, “Deuterium NMR Reveals Helix Packing Interactions in Phospholamban,” Journal of the American Chemical Society, Vol. 122, No. 45, 2000, pp. 11125-11128.
[25] E. K. Tiburu, P. C. Dave, K. Damodaran and G. A. Lorigan, “Investigating Leucine Side-Chain Dynamics and Backbone Conformations of Phospholamban Incorporated in Phospholipid Bilayers Utilizing 2H and 15N Solid-State NMR Spectroscopy,” Biochemistry, Vol. 43, No. 44, 2004, pp. 13899-13909. doi:10.1021/bi0490993
[26] L. A. Colnago, K. G. Valentine and S. J. Opella, “Dynamics of fd Coat Protein in Bacteriophage,” Biochemistry, Vol. 26, No. 5, 1987, pp. 847-854.
[27] W. L. Smith, R. M. Garavito and S. Fergusson-Miller, “Membrane Protein Structural Biology Minireview Series,” The Journal of Biological Chemistry, Vol. 276, No. 35, 2001, pp. 32393-32394. doi:10.1074/jbc.R100044200
[28] D. A. Doyle, J. M. Cabral, R. A. Pfuetzner, A. L. Kuo, J. M. Gulbis, S. L. Cohen, B. T. Chait and R. MacKinnon, “The Structure of the Potassium Channel: Molecular Basis of K+ Conduction and Selectivity,” Science, Vol. 280, No. 5360, 1998, pp. 69-77. doi:10.1126/science.280.5360.69
[29] G. Chang, R. H. Spencer, A. T. Lee, M. T. Barclay and D. C. Rees, “Structure of the MscL Homolog from Mycobacterium Tuberculosis: A Gated Mechanosensitive Ion Channel,” Science, Vol. 282, No. 5397, 1998, pp. 2220-2226. doi:10.1126/science.282.5397.2220
[30] Y. X. Jiang, A. Lee, J. Y. Chen, V. Ruta, M. Cadene, B. T. Chait and R. MacKinnon, “X-Ray Structure of a Voltage-Dependent K+ Channel,” Nature , Vol. 423, No. 6935, 2003, pp. 33-41. doi:10.1038/nature01580
[31] Y. X. Jiang, A. Lee, J. Y. Chen, M. Cadene, B. T. Chait, and R. MacKinnon, “Crystal Structure and Mechanism of a Calcium-Gated Potassium Channel,” Nature, Vol. 417, No. 6888, 2002, pp. 515-522. doi:10.1038/417515a
[32] Y. X. Jiang, A. Lee, J. Y. Chen, M. Cadene, B. T. Chait, and R. MacKinnon, “The Open Pore Conformation of Potassium Channels,” Nature, Vol. 417, No. 6888, 2002, pp. 523-526. doi:10.1038/417523a
[33] R. MacKinnon, “Nothing Automatic about Ion-Channel Structures,” Nature, Vol. 416, No. 6878, 2002, pp. 261-262. doi:10.1038/416261b
[34] A. Ben-Shem and D. Fass, “Structural Basis for Intramembrane Proteolysis by Rhomboid Serine Protease,” Proceedings of the National Academy of Sciences of the USA, Vol. 102, No. 2, 2007, pp. 401-402.
[35] M. J. Lemieux, S. J. Fischer, M. M. Cherney, M. M. Bateman and M. N. James, “The Crystal Structure of Rhomboid Peptidase from Haemophilus Influenzae Provides Insight into Intramembrane Proteolysis,” Proceedings of the National Academy of Sciences of the USA, Vol. 104, No. 3, 2007, pp. 750-754. doi:10.1073/pnas.0609981104
[36] Stephen White laboratory official website, 2007. www.blanco.biomol.uci.edu/Membrane_proteins_xtal.html
[37] S. J. Opella and F. M. Marassi, “Structure Determination of Membrane Proteins by NMR Spectroscopy,” Chemical Reviews, Vol. 104, No. 8, 2004, pp. 3587-3606. doi:10.1021/cr0304121
[38] S. J. Opella, “NMR and Membrane Proteins,” Nature Structural & Molecular Biology, Vol. 4, 1997, pp. 845- 848.
[39] Avanti Company Official Website, 2006. http://www.avantilipids.com/TechnicalInformation.html
[40] S. Abu-Baker and G. A. Lorigan, “Phospholamban and Its Phosphorylated form Interact Differently with Lipid Bilayers: A 31P, 2H, and 13C Solid-State NMR Spectroscopic Study,” Biochemistry, Vol. 45, No. 44, 2006, pp. 13312-13322.
[41] M. A. McCabe and S. R. Wassall, “Fast-Fourier-Transform Depaking,” Journal of Magnetic Resonance, Series B , Vol. 106, No. 1, 1995, pp. 80-82. doi:10.1006/jmrb.1995.1013
[42] M. A. McCabe and S. R. Wassall, “Rapid Deconvolution of NMR Powder Spectra by Weighted Fast Fourier Transformation,” Solid State Nuclear Magnetic Resonance, Vol 10, No. 1-2, 1997, pp. 53-61. doi:10.1016/S0926-2040(97)00024-6
[43] P. C. Dave E. K. Tiburu, K. Damodaran and G. A. Lorigan, “Investigating Structural Changes in the Lipid Bilayer upon Insertion of the Transmembrane Domain of the Membrane-Bound Protein Phospholamban Utilizing 31P and 2H Solid-State NMR Spectroscopy,” Biophysical Journal, Vol. 86, No. 3, 2004, pp. 1564-1573.
[44] P. C. Dave, E. K. Tiburu, N. A. Nusair and G. A. Lorigan, “Calculating Order Parameter Profiles Utilizing Magnetically Aligned Phospholipid Bilayers for 2H Solid-State NMR Studies,” Solid State Nuclear Magnetic Resonance, Vol. 24, No. 2-3, 2003, pp. 137-149. doi:10.1016/S0926-2040(03)00052-3
[45] D. Huster, X. Yao, K. Jakes and M. Hong, “Conformational Changes of Colicin Ia Channel-Forming Domain upon Membrane Binding: A Solid-State NMR Study,” Biochimica et Biophysica Acta, Vol. 1561, No. 2, 2002, pp. 159-170.
[46] D. Huster, K. Arnold and K. Garwrisch, “Influence of Docosahexaenoic Acid and Cholesterol on Lateral Lipid Organization,” Biochemistry, Vol. 37, No. 49, 1998, pp. 17299-17308.
[47] G. W. Stockson, C. F. Polnaszek, A. P. Tulloch, F. Hasan and I. C. P. Hasan, “Molecular Motion and Order in Single Bilayer Vesicles and Multilamellar Dispersions of Egg Lecithin and Lecithin-Cholesterol Moxtures. A Deuterium Nuclear Magnetic Resonance Study of Specifically Labeld Lipids,” Biochemistry, Vol. 15, 1976, pp. 954-966.
[48] J. Seelig, “31P Nuclear Magnetic Resonance and the Head Group Structure of Phospholipids in Membranes,” Biochimica et Biophysica Acta, Vol. 515, 1978, pp. 105-140.
[49] C. D. Pointer-Keenan, D. K. Lee, K. J. Hallock, A.Tan, R. Zand and A. Ramamoorthy, “Investigation of the Interaction of Myelin Basic Protein with phospholipid Bilayers Using Solid-State NMR Spectroscopy,” Chemistry and Physics of Lipids , Vol. 132, No. 1, 2004, pp. 47-54.
[50] S. Abu-Baker and G. A. Lorigan, “Phospholamban and Its Phosphorylated Form Interact Differently with Lipid Bilayers: A 31P, 2H, and 13C Solid-State NMR Spectroscopic Study,” Biochemistry, Vol. 45, No. 44, 2006, pp. 13312-13322. doi:10.1021/bi0614028
[51] J. W. Mack, D. A. Torchia and P. M. Steinert, “Solid-State NMR Studies of the Dynamics and Structure of Mouse Keratin Intermediate Filaments,” Biochemsitry, Vol. 27, No. 15, 1988, pp. 5418-5426.
[52] R. S. Prosser, S. I. Daleman and J. H. Davis, “The Structure of an Integral Membrane Peptide: A Deuterium NMR-Study of Gramicidin,” Biophysical Journal, Vol. 66, No. 5, 1994, pp. 1415-1428. doi:10.1016/S0006-3495(94)80932-4
[53] S. Sharpe, K. R. Barber, C. W. M. Grant and M. R. Morrow, “Evidence of a Tendancy of Self-Association of the Transmembrane Domain of ErbB-2 in Fluid Phospholipid Bilayers,” Biochemistry, Vol. 41, 2002, pp. 2341-2352.
[54] D. H. Jones, A. C. Rigby, K. R. Barber and W. M. Grant, “Oligoerization of EGF Receptor Transmembrane Domain: A 2H NMR Study in Lipid Bilayers,” Biochemsitry, Vol. 36, No. 41, 1997, pp. 12616-12624.
[55] J. A. Killian, M. J. Taylor and R. E. Koeppe, “Orientation of Valine-1 Side-Chain of the Gramicidin Transmembrane Channel and Implications for Channel Functioning: A Deuterium NMR Study,” Biochemsitry , Vol. 31, No. 46, 1992, pp. 11283-11290.
[56] K. C. Lee, S. Huo and T. A. Cross, “Lipid-Peptide Interface: Valine Conformation and Dynamics in Gramicidin Channel in a Lipid Bilayer,” Biochemsitry, Vol. 34, 1995, pp. 857-867.
[57] P. C. A. Van der Wel, E. Strandberg, J. A. Killian and R. E. Koeppe, “Geometry and Intrinsic Tilt of a Trypto Phan-Anchored Transmembrane Alpha-Helix Determined by H-2 NMR,” Biophysical Journal, Vol. 83, No. 3, 2002, pp. 1479-1488. doi:10.1016/S0006-3495(02)73918-0
[58] L. S. Batchelder, C. H. Niu and D. A. Torchia, “Methyl Reorientation in Polycrystaline Amino Acids in Peptides,” Journal of the American Chemical Society, Vol. 105, No. 8, 1983, pp. 2228-2231.
[59] S. Abu-Baker, J. X. Lu, S.Chu, C. C. Brinn, C. A. Makaroff and G. A. Lorigan, “Side Chain and Backbone Dynamics of Phospholamban in Phospholipid Bilayers Utilizing 2H and 15N Solid-State NMR Spectroscopy,” Biochemistry , Vol. 46, No. 42, 2007, pp. 11695-11706. doi:10.1021/bi700749q
[60] J. Janin and S. Wodak, “Conformation of Amino Acid Side-Chain in Proteins,” Journal of Molecular Biology, Vol. 125, No. 3, 1978, pp. 357-386.
[61] A. C. Rigby, K. R. Barber, G. S. Shaw and C. W. M. Grant, “Transmembrane Region of the Epidermal Growth Factor Receptor: Behavior and Interactions Via 2H NMR,” Biochemistry, Vol. 35, 1996, pp. 12591-12601.
[62] W. J. Gibbons Jr., E. S. Krap, N. A. Cellar, R. E. Minto and G. A. Lorigan, “Solid-State NMR Studies of a Diverged Microsomal Amino-Proximate Delta12 Desaturase Peptide Reveal Causes of Stability in Bilayer: Tyrosine Anchoring and Arginine Snorkeling,” Biophysical Journal, Vol. 90, No. 4, 2006, pp. 1249-1259.
[63] M. S. Greenfield, A. D. Ronemus, R. L. Vold, R. R. Vold, P. D. Ellis and T. E. Raidy, “Deuterium Quadrupole-Echo NMR Spectroscoppy III. Practice Aspects of line Shape Calculations for Multiaxis Rotational Processes,” Journal of Magnetic Resonance, Vol. 72, No. 1, 1987, pp. 89-107.
[64] K. Oxenoid and J. J. Chou, “The Structure of Phospholamban Pentamer Reveals a Channel-Like Architecture in Membrane,” Proceedings of the National Academy of Sciences of the USA, Vol. 102, No. 31, 2005, pp. 10870-10875. doi:10.1073/pnas.0504920102
[65] H. K. B. Simmerman and L. R. Jones, “Phospholamban: Protein Structure, Mechanism of Action, and Role in Cardiac Function,” Physiological Reviews, Vol. 78, No. 4, 1998, pp. 921-947.
[66] J. Zamoon, F. Nitu, C. Karim, D. D. Thomas and G. Veglia, “Mapping the Interaction Surface of a Membrane Protein: Unveiling the Conformational Switch of Phospholamban in Calcium Pump Regulation,” Proceedings of the National Academy of Sciences of the USA, Vol. 102, No. 13, 2005, pp. 4747-4752. doi:10.1073/pnas.0406039102
[67] D. Massiot, F. Fayon, M. Capron, I. King, S. Lecalve, B. Alonso, J. O. Durand, , B. Bujoli, Z. Gan and G. Hoatson, “Modelling One-and Two-Dimensional Solid-State NMR Spectra,” Magnetic Resonance in Chemistry, Vol. 40, No. 1, 2002, pp. 70-76.
[68] S. Abu-Baker, J. X. Lu, S. Chu, K. K. Shetty, P. L. Gor’ kov and G. A. Lorigan, “The Structural Topology of Wild-Type Phospholamban in Oriented Lipid Bilayers Using 15N Solid-State NMR Spectroscopy,” Protein Science, Vol. 16, No. 11, 2007, pp. 2345-2349.

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