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Structure Determination of Membrane Peptides and Proteins by Solid-State NMR

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Experimental Approaches of NMR Spectroscopy

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Abstract

Solid-state nuclear magnetic resonance (NMR) spectroscopy provides useful information on the structure, topology, and orientation of peptides and proteins bound to lipid bilayers. The structure and orientation of membrane-associated peptides and proteins can be elucidated by analyzing structural constraints obtained from anisotropic chemical-shift interactions, nuclear dipolar interactions, or a combination of these interactions. Detailed structures of various peptides and proteins in their membrane-bound states can be studied by analyzing anisotropic chemical-shift interactions by, for example, chemical-shift oscillation analysis, and nuclear dipolar interactions using techniques such as polarity index slant angle wheel analysis. Magic-angle spinning (MAS) experiments coupled with cross-polarization (CP) and high-power decoupling (CP-MAS) techniques provide high-resolution 13C and 15N NMR signals for selectively or uniformly labeled membrane-bound peptides and proteins in solid-state NMR. Furthermore, homonuclear and heteronuclear dipolar interactions can be recoupled using various spin manipulation pulse sequences under MAS conditions. These experiments enable the correlation of 13C–13C and 13C–15N signals, allowing their assignment to specific amino acid residues and ultimately determination of the high-resolution structure of membrane-bound peptides and proteins.

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References

  1. Opella, S.J., Marassi, F.M.: Structure determination of membrane proteins by NMR spectroscopy. Chem. Rev. 104, 3587–3606 (2004)

    Article  CAS  Google Scholar 

  2. Watts, A., Straus, S.K., Grage, S.L., Kamihira, M., Lam, Y.H., Zhao, X.: Membrane protein structure determination using solid-state NMR. In: Downing, A.K. (ed.) Protein NMR. Techniques, methods in molecular biology, vol. 278, pp. 403–473. Humana Press, Totowa (2004)

    Chapter  Google Scholar 

  3. Saitô, H., Ando, I., Naito, A.: NMR constraints for determination of secondary structure. In: Solid state NMR spectroscopy for biopolymers. Principles and Applications, pp. 127–199. Springer, Berlin (2006)

    Google Scholar 

  4. Naito, A.: Structure elucidation of membrane-associated peptides and proteins in oriented bilayers by solid-state NMR spectroscopy. Solid State Nucl. Magn. Reson. 36, 67–76 (2009)

    Article  CAS  Google Scholar 

  5. Opella, S.J., Das, B.B.: Determination of the equivalence of solid-state NMR orientational constraints from magnetic and rotational alignment of the coat protein in a filamentous bacteriophage. In: Separopvic, F., Naito, A. (eds.) Advances in Biological Solid State NMR: Protein and Membrane-Active Peptides, pp. 53–70. Royal Society of Chemistry, Cambridge (2014)

    Chapter  Google Scholar 

  6. Naito, A., Kawamura, I., Javkhlantugs, N.: Recent Solid-state NMR studies of membrane-bound peptides and proteins. Annu. Rev. NMR Spectrosc. 86, 333–411 (2015)

    Article  CAS  Google Scholar 

  7. Toraya, S., Nishimura, K., Naito, A.: Dynamic structure of vesicle-bound melittin in a variety of lipid chain lengths by solid-state NMR. Biophys. J. 87, 3323–3335 (2004)

    Article  CAS  Google Scholar 

  8. Marassi, F.M., Ramamoorthy, A., Opella, S.J.: Complete resolution of the solid-state NMR spectrum of a uniformly 15N-labeled membrane protein in phospholipid bilayers. Proc. Natl. Acad. Sci. 94, 8551–8556 (1997)

    Article  CAS  Google Scholar 

  9. Opella, S.J.: Solid-state NMR and membrane ptoteins. J. Magn. Reson. 253, 129–137 (2015)

    Article  CAS  Google Scholar 

  10. Weingarth, M., Buldus, M.: Introduction to Biological Solid-State NMR: Protein and Membrane Active Peptides, pp. 1–17. Royal Society of Chemistry, Cambridge (2014)

    Book  Google Scholar 

  11. Ward, M.E., Brown, L.S., Ladizhansky, V.: Advanced solid-state NMR techniques for characterization of membrane protein structure and dynamics: application to anabaena sensory rhodopsin. J. Magn. Reson. 253, 119–128 (2015)

    Article  CAS  Google Scholar 

  12. Naito, A., Nagao, T., Norisada, K., Mizuno, T., Tuzi, S., Saitô, H.: Conformation and dynamics of melittin bound to magnetically oriented lipid bilayers by solid-state 31P and 13 C NMR spectroscopy. Biophys. J. 78, 2405–2417 (2000)

    Article  CAS  Google Scholar 

  13. Wu, C.H., Ramamoorth, A., Opella, S.J.: High-resolution heteronuclear dipolar solid-state NMR spectroscopy. J. Magn. Reson. A109, 270–272 (1994)

    Article  Google Scholar 

  14. Ramamoorthy, A., Wei, Y., Lee, D.-K.: PISEMA solid-state NMR spectroscopy. Annu. Rep. NMR Spectrosc. 52, 1–52 (2004)

    Article  CAS  Google Scholar 

  15. Lee, D.K., Narasimhaswamy, T., Ramamoorthy, A.: PITANSEMA, a low-power PISEMA solid-state NMR experiment. Chem. Phys. Lett. 399, 359–362 (2004)

    Article  CAS  Google Scholar 

  16. Nishimura, K., Naito, A.: Dramatic reduction of the RF power for attenuation of sample heating in 2D-separated local field solid-state NMR spectroscopy. Chem. Phys. Lett. 402, 245–250 (2005)

    Article  CAS  Google Scholar 

  17. Nishimura, K., Naito, A.: Remarkable reduction of rf power by ATANSEMA and DATANSEMA separated local field in solid-state NMR spectroscopy. Chem. Phys. Lett. 419, 120–124 (2006)

    Article  CAS  Google Scholar 

  18. Gor’kov, P.L., Chekmenev, E.Y., Li, C., Cotton, M., Butfy, J.J., Traasch, N.J., Veglia, G., Brey, W.W.: Using low-E resonance to reduce RF heating in biological samples for static solid-state NMR up to 900 MHz. J. Magn. Reson. 185, 77–93 (2007)

    Article  CAS  Google Scholar 

  19. Yamamoto, K., Lee, D.K., Ramamoorthy, A.: Spectroscopy, broadband-PISEMA solid-state NMR spectroscopy. Chem. Phys. Lett. 407, 289–293 (2005)

    Article  CAS  Google Scholar 

  20. Marassi, F.M., Opella, S.J.: A solid-state NMR index of helical membrane protein structure and topology. J. Magn. Reson. 144, 150–155 (2000)

    Article  CAS  Google Scholar 

  21. Marrasi, F.M., Ma, C., Gesel, J.J., Opella, S.J.: Three-dimensional solid-state NMR spectroscopy is essential for resolution of resonances from in-plane residues in uniformly 15N-labeled helical membrane proteins in oriented lipid bilayers. J. Magn. Reson. 144, 156–161 (2000)

    Article  CAS  Google Scholar 

  22. Wang, J., Denny, J., Tian, C., Kim, S., Mo, Y., Kovacs, F., Song, Z., Nishimura, K., Gan, Z., Fu, R., Quine, J.R., Cross, T.A.: Imaging membrane protein helical wheels. J. Magn. Reson. 144, 162–167 (2000)

    Article  CAS  Google Scholar 

  23. Gullion, T., Schaefer, J.: Rotational-echo double-resonance. J. Magn. Reson. 81, 196–200 (1989)

    CAS  Google Scholar 

  24. Naito, A., Nishimura, K., Kimura, S., Tuzi, S., Aida, M., Yasuoka, N., Saitô, H.: Determination of the three-dimensional structure of a new crystalline form of N-acetyl-Pro-Gly-Phe as revealed by 13C REDOR, X-ray diffraction, and molecular dynamics calculation. J. Phys. Chem. 100, 14995–15004 (1996)

    Article  CAS  Google Scholar 

  25. Naito, A., Nishimura, K., Tuzi, S., Saitô, H.: Inter- and intra-molecular contributions of neighboring dipolar pairs to the precise determination of interatomic distances in a simple [13C, 15N]-peptide by 13C, 15N-REDOR NMR spectroscopy. Chem. Phys. Lett. 229, 506–511 (1994)

    Google Scholar 

  26. Jaroniec, C.P., Tounge, B.T., Rienstra, C.M., Herzfeld, J., Griffin, R.G.: Recoupling of heteronuclear dipolar interactions with rotational-echo double-resonance at high magic-angle spinning frequencies. J. Magn. Reson. 146, 132–139 (2000)

    Article  CAS  Google Scholar 

  27. Gullion, T., Schaefer, J.: Elimination of resonance offset effects in rotational-echo double resonance NMR. J. Magn. Reson. 92, 439–442 (1991)

    CAS  Google Scholar 

  28. Pan, Y., Gullion, T., Schaefer, J.: Determination of C-N internuclear distances by rotational-echo double-resonance NMR of solids. J. Magn. Reson. 90, 330–340 (1990)

    CAS  Google Scholar 

  29. Garbow, J.R., McWherter, C.A.: Determination of the molecular conformation of melanostatin using 13C, 15N-REDOR NMR spectroscopy. J. Am. Chem. Soc. 115, 238–244 (1993)

    Article  CAS  Google Scholar 

  30. Suwelack, D., Rothwell, W.P., Waugh, J.S.: Slow molecular motion detecting in the NMR spectra of rotating solids. J. Chem. Phys. 74, 2559–2569 (1980)

    Article  Google Scholar 

  31. Rothwell, W.P., Waugh, J.S.: Transverse relaxation of dipolar coupled spin systems under rf irradiation. J. Chem. Phys. 74, 2721–2732 (1981)

    Article  CAS  Google Scholar 

  32. Naito, A., Fukutani, A., Uitdehaag, M., Tuzi, S., Saitô, H.: Backbone dynamics of polycrystalline peptides studied by measurements of 15N NMR lineshapes and 13C transverse relaxation times. J. Mol. Struct. 441, 231–241 (1998)

    Article  CAS  Google Scholar 

  33. Kamihira, M., Naito, A., Nishimura, K., Tuzi, S., Saitô, H.: A high-resolution solid-state 13C and 15N NMR study on crystalline Leu- and Met-enkephalins: Distinction of polymorphs, backbone dynamics and local conformational rearrangements induced by dehydration or freezing of motion of bound solvent molecules. J. Phys. Chem. B 102, 2826–2834 (1998)

    Article  CAS  Google Scholar 

  34. Peersen, O.B., Groesbeek, M., Aimoto, S., Smith, S.O.: Analysis of rotational resonance magnetization exchange curves from crystalline peptides. J. Am. Chem. Soc. 117, 7228–7237 (1995)

    Article  CAS  Google Scholar 

  35. Andrew, E.R.: The narrowing of NMR spectra of solids by high-speed specimen rotation and resolution of chemical shift and spin multiplet structure for solids. Prog. Nucl. Magn. Reson. Spectrosc. 8, 1–39 (1971)

    Article  CAS  Google Scholar 

  36. Hartmann, S.R., Hahn, E.L.: Nuclear double resonance in the rotating frame. Phys. Rev. 128, 2042–2053 (1962)

    Article  CAS  Google Scholar 

  37. Pines, A., Gibby, M.G., Waugh, J.S.: Proton-enhanced NMR of dilute spins in solids. J. Chem. Phys. 59, 569–590 (1973)

    Article  CAS  Google Scholar 

  38. Schaefer, J., Stejeskal, E.O.: Carbon-13 nuclear magnetic resonance of polymers spinning at magic angle. J. Am. Chem. Soc. 98, 1031–1032 (1976)

    Article  CAS  Google Scholar 

  39. Baldus, M., Petokova, A.T., Herzfeld, J., Griffin, R.G.: Cross polarization in the tilted frame assignment and spectral simplification in heteronuclear spin system. Mol. Phys. 95, 1197–1207 (1998)

    Article  CAS  Google Scholar 

  40. Lewandowski, J.R., Paep, G.D., Griffin, R.G.: Proton assisted insensitive nuclei cross polarization. J. Am. Chem. Soc. 129, 728–729 (2007)

    Article  CAS  Google Scholar 

  41. Paep, G.D., Lewandowski, J.R., Loquet, A., Bockmann, A., Griffin, R.G.: Proton assisted recoupling and protein structure determination. J. Chem. Phys. 129, 245101 (2008)

    Article  CAS  Google Scholar 

  42. Grommek, A., Meier, B.H., Ernst, M.: Distance information from proton-driven spin diffusion under MAS. Chem. Phys. Lett. 427, 631–637 (2006)

    Article  CAS  Google Scholar 

  43. Takegoshi, K., Nakamura, S., Terao, T.: 13C–1H dipolar-assisted rotational resonance in magic-angle spinning NMR. Chem. Phys. Lett. 344, 631–637 (2001)

    Article  CAS  Google Scholar 

  44. Takegoshi, K., Nakamura, S., Terao, T.: 13C–1H dipolar-driven 13C–13C recoupling without 13C rf irradiation in nuclear magnetic resonance of rotating solids. J. Chem. Phys. 118, 2325–2341 (2003)

    Article  CAS  Google Scholar 

  45. Weingarth, M., Demaco, D.E., Bodenhausen, G., Tekely, P.: Improved magnetization transfer in solid-state NMR with fast magic angle spinning. Chem. Phys. Lett. 469, 342–348 (2009)

    Article  CAS  Google Scholar 

  46. Scholz, I., Huber, M., Manolikas, T., Meier, B.H., Ernst, M.: MIRROR recoupling and its application to spin diffusion under fast magic-angle spinning. Chem. Phys. Lett. 460, 278–283 (2008)

    Article  CAS  Google Scholar 

  47. Weigarth, M., Masuda, Y., Takegoshi, K., Bodenhausen, G., Tekely, P.: Sensitive 13C–13C correlation spectra of amyloid fibrils at very high spinning frequencies and magnetic fields. J. Biomol. NMR 50, 129–136 (2011)

    Article  CAS  Google Scholar 

  48. Egawa, A., Fujiwara, T., Mizoguchi, T., Kakitani, Y., Koyama, Y., Akutsu, H.: Structure of the light-harvesting bacteriochlorophyll c assembly in chlorosomes from Chlorobium limicola determined by solid-state NMR. Proc. Natl. Acad. Sci. 104, 790–795 (2007)

    Article  CAS  Google Scholar 

  49. Dumez, J.L., Emsley, L.: A master-equation approach to the description of proton-driven spin diffusion from crystal geometry using simulated zero-quantum lineshapes. Phys. Chem. Chem. Phys. 13, 7363–7370 (2011)

    Article  CAS  Google Scholar 

  50. Kubo, A., McDowell, C.A.: Spectral spin diffusion in polycrystalline solids under magic angle spinning. Chem. Soc. Faraday Trans. I 84, 3713–3730 (1988)

    Article  CAS  Google Scholar 

  51. Kubo, A., McDowell, C.A.: 31P spectral spin diffusion in crystalline solids. J. Chem. Phys. 89, 63–70 (1988)

    Article  CAS  Google Scholar 

  52. Grommek, A., Meier, B.H., Ernst, M.: Distance information from proton-driven spin diffusion under MAS. Chem. Phys. Lett. 427, 404–409 (2006)

    Article  CAS  Google Scholar 

  53. Toraya, S., Nagao, T., Norisada, K., Tuzi, S., Saitô, H., Izumi, S., Naito, A.: Morphological behavior of lipid bilayers induced by melittin near the phase transition temperature. Biophys. J. 89, 3214–3222 (2005)

    Article  CAS  Google Scholar 

  54. Norisada, K., Javkhlantugs, N., Mishima, D., Kawamura, I., Saitô, H., Ueda, K., Naito, A.: Dynamic structure and orientation of melittin bound to acidic lipid bilayers, as revealed by solid-state NMR and molecular dynamics simulation. J. Phys. Chem. B 121, 1802–1811 (2017)

    Article  CAS  Google Scholar 

  55. Uezono, T., Toraya, S., Obata, M., Nishimura, K., Tuzi, S., Saitô, H., Naito, A.: Structure and orientation of dynorphin bound to lipid bilayers by 13C solid-state NMR. J. Mol. Struct. 749, 13–19 (2005)

    Article  CAS  Google Scholar 

  56. Toraya, S., Javkhlantugs, N., Mishima, D., Nishimura, K., Ueda, K., Naito, A.: Dynamic structure of bombolitin II bound to lipid bilayers as revealed by solid-state NMR and molecular-dynamics simulation. Biophys. J. 99, 3282–3289 (2010)

    Article  CAS  Google Scholar 

  57. Tsutsumi, A., Javkhlantugs, N., Kira, A., Umeyama, M., Kawamura, I., Nishimura, K., Ueda, K., Naito, A.: Structure and orientation of bovine lactroferrampin in the mimetic bacterial membrane as revealed by solid-state NMR and molecular dynamic simulation. Biophys. J. 103, 1735–1743 (2012)

    Article  CAS  Google Scholar 

  58. Kira, A., Javkhlantugs, N., Miyamori, T., Sasaki, Y., Eguchi, M., Kawamura, I., Ueda, K., Naito, A.: Interaction of extracellular loop II of k-opioid receptor (196–228) with opioid peptide dynorphin in membrane environments as revealed by solid state nuclear magnetic resonance, quartz crystal microbalance and molecular dynamics simulation. J. Phys. Chem. B 2014(118), 9604–9612 (2014)

    Article  CAS  Google Scholar 

  59. Nagao, T., Mishima, D., Javkhlantugs, N., Wang, J., Ishioka, D., Yokota, K., Norisada, K., Kawamura, I., Ueda, K., Naito, A.: Structure and orientation of antibiotic peptide alamethicin in phospholipid bilayers as revealed by chemical shift oscillation analysis of solid state nuclear magnetic resonance and molecular dynamics simulation. Biochim. Biophys. Acta 2015(1848), 2789–2798 (2015)

    Article  CAS  Google Scholar 

  60. Habermann, E., Jentsc, J.: Sequence analysis of melittin from tryptic and peptic degradation and products. Hoppe-Seyler’s Z. Phys. Chem. 348, 37–50 (1967)

    Article  CAS  Google Scholar 

  61. Sessa, G., Free, J.H., Colacicco, G., Weissmann, G.: Interaction of a lytic polypeptide, melittin, with lipid membrane systems. J. Biol. Chem. 244, 3575–3582 (1969)

    CAS  Google Scholar 

  62. Tosteson, M.T., Tosteson, D.C.: The sting melittin forms channels in lipid bilayers. Biophys. J. 36, 109–116 (1981)

    Article  CAS  Google Scholar 

  63. Dempsey, C.E.: The action of melittin on membrane. Biochim. Biophys. Acta 1031, 143–161 (1990)

    Article  CAS  Google Scholar 

  64. Dufourcq, J., Faucon, J.-F., Fourche, G., Dasseux, J.L., Le Maire, M., Gulik-Krywicki, T.: Morphological change of phosphatidylcholine bilayers induced by melittin: vesicularization, fusion, discoidal particles. Biochim. Biophys. Acta 859, 33–48 (1986)

    Article  CAS  Google Scholar 

  65. Saitô, H.: Conformation-dependent 13C chemical shifts: a new means of conformation characterization as obtained by high-resolution solid-state 13C NMR. Magn. Reson. Chem. 24, 835–852 (1986)

    Article  Google Scholar 

  66. Saitô, H., Ando, I.: High-resolution solid-state NMR studies of synthetic and biological macromolecules. Annu. Rep. NMR Spectrosc. 21, 209–290 (1989)

    Article  Google Scholar 

  67. Naito, A., Saitô, H.: Limit of accuracy of internuclear distances measured by REDOR. Encycl. Nucl. Magn. Reson. 9, 191–283 (2002)

    Google Scholar 

  68. Meyer, C.E., Reusser, F.: A polypeptide antibacterial agent isolated from Trichoderma viride. Experientia 23, 85–86 (1967)

    Article  CAS  Google Scholar 

  69. Balasubramanian, T.M., Kendrick, N.C.E., Taylor, M., Marshall, G.R., Hall, J.E., Vodyanoy, J., Reusser, F.: Synthesis and characterization of the major component of alamethicin. J. Am. Chem. Soc. 103, 6127–6132 (1981)

    Article  CAS  Google Scholar 

  70. Vedovato, N., Baldhini, C., Toniolo, C., Rispoli, G.: Pore-forming properties of alamethicin F50/5 inserted in a biological membrane. Chem. Biodivers. 4, 1338–1346 (2007)

    Article  CAS  Google Scholar 

  71. Mueller, P., Rudin, D.O.: Action potentials induced in biomolecular lipid membranes. Nature 217, 713–719 (1068)

    Article  Google Scholar 

  72. Dave, P.C., Billington, E., Pan, Y.-L., Straus, S.K.: Interaction of alamethicin with ether-linked phospholipid bilayers: oriented circular dichroism, 31P solid-state NMR, and differential scanning calorimetry studies. Biophys. J. 89, 2434–2442 (2005)

    Article  CAS  Google Scholar 

  73. Tieleman, D.P., Berendsen, H.J.C., Sanson, M.S.P.: Voltage-dependent insertion of alamethicin at phospholipid/water and octane/water interfaces. Biophys. J. 80, 331–346 (2001)

    Article  CAS  Google Scholar 

  74. Fox Jr., R.O., Richards, F.M.: A voltage-gated ion channel model inferred from the crystal structure of alamethicin at 1.5-Å resolution. Nature 300, 325–330 (1982)

    Article  CAS  Google Scholar 

  75. Pan, P., Tristram-Nagle, S., Nagle, J.F.: Alamethicin aggregation in lipid membranes. J. Membr. Biol. 231, 11–27 (2009)

    Article  CAS  Google Scholar 

  76. Sansom, M.S.: Alamethicin and related peptaibols—model ion channels. Eur. Biophys. J. 22, 105–124 (1993)

    Article  CAS  Google Scholar 

  77. Saitô, H., Tabeta, R., Formaggio, F., Crisma, M., Toniolo, C.: High-resolution solid-state 13C-NMR of peptides: A study of chain-length dependence for 310-helix formation. Biopolymers 27, 1607–1617 (1988)

    Article  Google Scholar 

  78. Nagao, T., Naito, A., Tuzi, S., Saitô, H.: Conformation and orientation of biologically active peptide alamethicin in phospholipid bilayer by high-resolution solid state NMR spectroscopy. Pept. Sci. 1988, 341–344 (1988)

    Google Scholar 

  79. Bak, M., Bywater, R.P., Hohwy, M., Thomsen, J.K., Adelhorst, K., Jakobsen, H.J., Søronsen, O.W., Nielsen, N.C.: Conformation of alamethicin in oriented phospholipid bilayers determined by 15N solid-state nuclear magnetic resonance. Biophys. J. 81, 1684–1698 (2001)

    Article  CAS  Google Scholar 

  80. Bertelsen, K., Paaske, B., Thøgersen, L., Tajkhorshid, E., Schiøtt, B., Skrydstrup, T., Nielsen, N.C., Vosegaard, T.: Residue-specific information about the dynamics of antimicrobial peptides from 1H–15N and 2H solid-state NMR spectroscopy. J. Am. Chem. Soc. 131, 18335–18342 (2009)

    Article  CAS  Google Scholar 

  81. Bechinger, B., Skladnev, D.A., Ogrel, A., Li, X., Rogozhkina, E.V., Ovchinnikova, T.V., O’Neil, J.D.J., Raap, J.: 15N and 31P solid-state NMR investigations on the orientation of Zervamicin II and alamethicin in phosphatidylcholine membranes. Biochemistry 40, 9428–9437 (2001)

    Article  CAS  Google Scholar 

  82. Salnikov, E.S., Friedrich, H., Li, X., Bertani, P., Reissmann, S., Hertweck, C., O’Neil, J.D.J., Raap, J., Bechinger, B.: Structure and alignment of the membrane-associated peptaibols ampullosporin A and alamethicin by oriented 15N and 31P solid-state NMR spectroscopy. Biophys. J. 96, 86–100 (2009)

    Article  CAS  Google Scholar 

  83. van der Kraan, M.I.A., Groenink, J., Nazmi, K., Veeman, E.C.I., Bolscher, J.G.M., Amerongen, A.V.N.: Lactoferrampin: A novel antimicrobial peptide in the N1-domain of bovine lactoferrin. Peptides 25, 177–183 (2004)

    Article  CAS  Google Scholar 

  84. van der Kraan, M.I.A., van Marle, J., Nazmi, K., Groenink, J., van’t Hof, W., Veerman, E.C.I., Bolscher, J.G.M., Amerongen, A.V.N.: Ultrastructural effects of antimicrobial peptides from bovine lactoferrin on the membranes of Candida albicans and Escherichia coli. Peptides 26, 1537–1542 (2005)

    Article  CAS  Google Scholar 

  85. van der Kraan, M.I.A., Nazmi, K., Teeken, A., Groenink, J., van’t Hof, W., Veeman, E.C.I., Bolscher, J.M.G., Amerongen, A.V.N.: Lactoferrampin, an antimicrobial peptide of bovine lactoferrin, exerts its candidacidal activity by a cluster of positively charged residues at the C-terminus in combination with a helix-facilitating N-terminal part. Biol. Chem. 386, 137–142 (2005)

    Google Scholar 

  86. Haney, E.F., Lau, F., Vogel, H.J.: Solution structure and model membrane interactions of lactoferrampin, an antimicrobial peptide derived from bovine lactoferrin. Biochim. Biophys. Acta 1768, 2355–2364 (2007)

    Article  CAS  Google Scholar 

  87. Jenssen, H., Hamill, P., Hancock, R.E.W.: Peptide antimicrobial agents. Clin. Microbiol. Rev. 19, 491–511 (2006)

    Article  CAS  Google Scholar 

  88. Matsuzaki, K., Murase, O., Fujii, N., Miyajima, K.: An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation. Biochemistry 35, 11361–11368 (1996)

    Article  CAS  Google Scholar 

  89. Katherine, A., Wildman, H., Lee, D.-K., Ramamoorthy, A.: Mechanism of lipid bilayer disruption by the human antimicrobial peptide, LL-37. Biochemistry 42, 6545–6558 (2003)

    Article  CAS  Google Scholar 

  90. Steve, K.H., Ludtke, L., Worcester, D.L., Huang, H.W.: Neutron scattering in the plane of membranes: structure of alamethicin pores. Biophys. J. 1996(70), 2659–2666 (1996)

    Google Scholar 

  91. Pouny, Y., Rapaport, D., Mor, A., Nicolas, P., Shai, Y.: Interaction of antimicrobial dermaseptin and its fluorescently labeled analogues with phospholipid membranes. Biochemistry 31, 12416–12423 (1992)

    Article  CAS  Google Scholar 

  92. Umeyama, M., Kira, A., Nishimura, K., Naito, A.: Interaction of bovine lactoferricin with acidic phospholipid bilayers and its antimicrobial activity as studied by solid-state NMR. Biochim. Biophys. Acta 1758, 1523–1528 (2006)

    Article  CAS  Google Scholar 

  93. Park, S.H., Das, B.B., Casagrande, F., Tian, F.Y., Nothnagel, H.J., Chu, M., Kiefer, H., Maier, K., De Angelis, A.A., Marassi, F.M., Opella, S.J.: Structure of the chemokine receptor CXCR1 in phospholipid bilayers. Nature 491, 779–783 (2012)

    Article  CAS  Google Scholar 

  94. Shahid, S.A., Bardiaux, B., Franks, W.T., Krabben, L., Habeck, M., van Rossum, B.-J., Linke, D.: Membrane-protein structure determination by solid-state NMR spectroscopy of microcrystals. Nat. Methods 9, 1212–1217 (2012)

    Article  CAS  Google Scholar 

  95. Wang, S., Munro, R.A., Shi, L., Kawamura, I., Okitsu, T., Wada, A., Kim, S.-Y., Jung, K.-H., Brown, L.S., Ladizhansky, V.: Solid-state NMR spectroscopy structure determination of a lipid-embedded heptahelical membrane protein. Nat. Methods 10, 1007–1012 (2013)

    Article  CAS  Google Scholar 

  96. Tang, M., Nesbill, A.E., Sperling, L.J., Berthold, D.A., Schwieters, C.D., Gennis, R.B., Rienstra, C.M.: Structure of the disulfide bond generating membrane protein DsbB in the lipid bilayer. J. Mol. Biol. 425, 1670–1682 (2013)

    Article  CAS  Google Scholar 

  97. Traaseth, N.J., Shi, L., Verardi, R., Mullen, D.G., Barany, G., Veglia, G.: Structure and topology of monomeric phospholamban in lipid membranes determined by a hybrid solution and solid-state NMR approach. Proc. Natl. Acad. Sci. USA 106, 10165–10170 (2009)

    Article  CAS  Google Scholar 

  98. Suter, D., Ernst, R.R.: Spin diffusion in resolved solid-state NMR spectra. Phys. Rev. 32, 5608–5627 (1985)

    Article  CAS  Google Scholar 

  99. Castellani, F., van Rossum, B., Diehl, A., Schubert, M., Rehbein, K., Oschkinat, H.: Structure of a protein determination by solid-state magic-angle-spinning NMR spectroscopy. Nature 420, 98–102 (2002)

    Article  CAS  Google Scholar 

  100. Crocker, E., Patel, A.B., Eilers, M., Jayaraman, S., Getmanova, E., Reeves, P.J., Ziliox, M., Khorana, H.G., Sheves, M., Smith, S.O.: Dipolar assisted rotational resonance NMR of tryptophan and tyrosine in rhodopsin. J. Biomol. NMR 29, 11–20 (2004)

    Article  CAS  Google Scholar 

  101. Marulanda, D., Tasayco, M.L., Cataldi, M., Arriaran, V., Polenova, Y.: Resonance assignments and secondary structure analysis of E. coli thioredoxin by magic spinning solid-state NMR spectroscopy. J. Phys. Chem. B 109, 18135–18145 (2005)

    Article  CAS  Google Scholar 

  102. Eilers, M., Goncalves, J.A., Ahuja, S., Kirkup, C., Hirshfeld, A., Simmerling, C., Reeves, P.J., Sheves, M., Smith, S.O.: Structural transitions of transmembrane helix 6 in the formation of metarhodopsin I. J. Phys. Chem. B 116, 10477–10489 (2012)

    Article  CAS  Google Scholar 

  103. Kimata, N., Pope, A., Eilers, M., Opefi, C.A., Ziliox, M., Hirshfeld, A., Zaitseva, E., Vogel, R., Sheves, M., Reeves, P.J., Smith, S.O.: Retinal orientation and interactions in rhodopsin reveal a two-stage trigger mechanism for activation. Nat. Commun. 7, 12683 (2016)

    Article  CAS  Google Scholar 

  104. Kato, H.E., Inoue, K., Abe-Yoshizumi, R., Kato, Y., Ono, H., Konno, M., Hososhima, S., Ishizuka, T., Hoque, M.R., Kunitomo, H., Ito, J., Yoshizawa, S., Yamashita, K., Takemoto, M., Nishizawa, T., Taniguchi, R., Kogure, K., Maturana, A.D., Iino, Y., Yawo, H., Ishitani, R., Kandori, H., Nureki, O.: Structural basis for Na+ transport mechanism by a light-driven Na+ pump. Nature 521, 48–53 (2015)

    Article  CAS  Google Scholar 

  105. Shigeta, A., Ito, S., Inoue, K., Okitsu, T., Wada, A., Kandori, K., Kawamura, I.: Solid-state nuclear magnetic resonance structural study of the retinal-binding pocket in sodium ion pump rhodopsin. Biochemistry 56, 543–550 (2017)

    Article  CAS  Google Scholar 

  106. Lange, A., Giller, K., Hornig, S., Martin-Eauclaire, M.-F., Pongs, O., Becker, S., Baldus, M.: Toxin-induced conformational changes in a potassium channel revealed by solid-state NMR. Nature 440, 959–962 (2006)

    Article  CAS  Google Scholar 

  107. Emami, S., Fan, Y., Munro, R., Ladizhansky, V., Brown, L.S.: Yeast-expressed human membrane protein aquaporin-1 yields excellent resolution of solid-state MAS NMR spectra. J. Biomol. NMR 55, 147–155 (2013)

    Article  CAS  Google Scholar 

  108. Yang, J., Aslimovska, L., Glaubitz, C.: Molecular dynamics of proteorhodopsin in lipid bilayers by solid-state NMR. J. Am. Chem. Soc. 133, 4874–4881 (2011)

    Article  CAS  Google Scholar 

  109. Shi, L., Ahmed, M.A.M., Zhang, W., Whited, G., Brown, L.S., Ladizhansky, V.: Three-dimensional solid-state NMR study of a seven-helical integral membrane proton pump-structure insights. J. Mol. Biol. 386, 1078–1093 (2009)

    Article  CAS  Google Scholar 

  110. Etzkom, M., Seidel, K., Li, L., Martell, S., Geyer, M., Engelhard, M., Baldus, M.: Complex formation and light activation in membrane-embedded sensory rhodopsin II as seen by solid-state NMR spectroscopy. Structure 18, 293–300 (2010)

    Article  CAS  Google Scholar 

  111. Shen, Y., Delaglio, F., Cornilescua, G., Bax, Ad: TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR 44, 213–223 (2009)

    Article  CAS  Google Scholar 

  112. Jung, K.-H., Trivedi, V.D., Spudich, J.L: Demonstration of a sensory rhodopsin in eubacteria. Mol. Microbiol. 47, 1513–1522 (2003)

    Google Scholar 

  113. Shi, L., Kawamura, I., Jung, K.-H., Brown, L.S., Ladizhansky, V.: Conformation of a seven-helical transmembrane photosensor in the lipid environment. Angew. Chem. Int. Ed. 50, 1302–1305 (2011)

    Article  CAS  Google Scholar 

  114. Vogeley, L., Sineshchekov, O.A., Trivedi, V.D., Sasaki, J., Spudich, J.L., Luecke, H.: Anabaena sensory rhodopsin: a photochromic color sensor at 2.0 Å. Science 306, 1390–1393 (2004)

    Article  CAS  Google Scholar 

  115. Wang, S., Shi, L., Okitsu, T., Wada, A., Brown, L.S., Ladizhansky, V.: Solid-state NMR 13C and 15N resonance assignments of a seven-transmembrane helical protein Anabaena Sensory Rhodopsin. Biomol. NMR Assign 7, 253–256 (2013)

    Article  CAS  Google Scholar 

  116. Wang, S., Shi, L., Kawamura, I., Brown, L.S., Ladizhansky, V.: Site-specific solid-state NMR detection of hydrogen-deuterium exchange reveals conformational changes in a 7-helical transmembrane protein. Biophys. J. 101, L23–L25 (2011)

    Article  CAS  Google Scholar 

  117. Peng, X., Libich, D., Janik, R., Harauz, G., Ladizhansky, V.: Dipolar chemical shift correlation spectroscopy for homonuclear carbon distance measurements in proteins in the solid state: application to structure determination and refinement. J. Am. Chem. Soc. 130, 359–369 (2007)

    Article  CAS  Google Scholar 

  118. Lange, A., Luca, S., Baldus, M.: Structure constraints from protein-mediated rare-spin correlation spectroscopy in rotating solids. J. Am. Chem. Soc. 124, 9704–9705 (2002)

    Article  CAS  Google Scholar 

  119. Wang, S., Munro, R.A., Kim, S.Y., Jung, K.-H., Brown, L.S., Ladizhansky, V.: Paramagnetic relaxation enhancement reveals oligomerization interface of a membrane protein. J. Am. Chem. Soc. 134, 16995–16998 (2012)

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by grants-in-aid for Scientific Research in an Innovative Area (16H00756 to AN and 16H00828 to IK) and by a grant-in-aid for Scientific Research (C) (15K06963 to AN) and Research (B) (15H04336 to IK) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

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Authors and Affiliations

  1. Faculty of Engineering, Yokohama National University, 79-5 Hodogayaku Tokiwadai, Yokohama, 240-8501, Japan

    Izuru Kawamura & Akira Naito

  2. Graduate School of Engineering, Yokohama National University, 79-5 Hodogayaku Tokiwadai, Yokohama, 240-8501, Japan

    Kazushi Norisada

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  1. Izuru Kawamura
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  2. Kazushi Norisada
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  3. Akira Naito
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Correspondence to Izuru Kawamura .

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    The Nuclear Magnetic Resonance Society of Japan

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Kawamura, I., Norisada, K., Naito, A. (2018). Structure Determination of Membrane Peptides and Proteins by Solid-State NMR. In: The Nuclear Magnetic Resonance Society of Japan (eds) Experimental Approaches of NMR Spectroscopy. Springer, Singapore. https://doi.org/10.1007/978-981-10-5966-7_9

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