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Nuclear Magnetic Resonance

  • Milan Zachrdla
  • Zuzana Jaseňáková
  • Lukáš Žídek
Chapter

Abstract

Application of nuclear magnetic resonance (NMR) in protein studies is briefly described. The basic physical principles of the method are introduced, and relation of NMR spectra to chemical structure is explained. The basic technique of isotope labeling is presented, and recommendations for sample preparations are reviewed. The methods used for assignment of NMR spectra, structure determinations, investigation of intermolecular interactions, and monitoring molecular motions are discussed.

Notes

Acknowledgment

Financial contribution made by the Ministry of Education, Youths, and Sports of the Czech Republic within special support paid from the National Programme for Sustainability II funds, project CEITEC 2020 (LQ1601), is gratefully acknowledged.

References

  1. Anglister J, Srivastava G, Naider F (2016) Detection of intermolecular NOE interactions in large protein complexes. Prog Nucl Magn Reson Spectrosc 97:40–56CrossRefPubMedGoogle Scholar
  2. Bhattacharya A, Tejero R, Montelione GT (2007) Evaluating protein structures determined by structural genomics consortia. Proteins 66(4):778–795CrossRefPubMedGoogle Scholar
  3. Briggman KB, Tolman JR (2003) De novo determination of bond orientations and order parameters from residual dipolar couplings with high accuracy. J Am Chem Soc 125(34):10164–10165CrossRefPubMedGoogle Scholar
  4. Brunger AT, Adams PD, Clore GM, Gros P, Grosse-Kunstleve RW, Jiang J, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Crystallography & NMR system (CNS), a new software suite for macromolecular structure determination. Acta Cryst D54:905–921Google Scholar
  5. Buevich AV, Baum J (1999) Dynamics of unfolded proteins: incorporation of distributions of correlation times in the model free analysis of NMR relaxation data. J Am Chem Soc 121:8671–8672Google Scholar
  6. Camilloni C, De Simone A, Vranken WF, Vendruscolo M (2012) Determination of secondary structure populations in disordered states of proteins using nuclear magnetic resonance chemical shifts. Biochemistry 51(11):2224–2231CrossRefPubMedGoogle Scholar
  7. Cavanagh J, Skelton NJ, Fairbrother WJ, Rance M, Palmer AG (2007) Protein NMR spectroscopy: principles and practice, 2nd edn. Academic Press, CambridgeGoogle Scholar
  8. Cheung M, Maguire ML, Stevens TJ, Broadhurst RW (2010) DANGLE: a Bayesian inferential method for predicting protein backbone dihedral angles and secondary structure. J Magn Reson 202(2):223–233CrossRefPubMedGoogle Scholar
  9. Coggins BE, Werner-Allen JW, Yan A, Zhou P (2012) Rapid protein global fold determination using Ultrasparse sampling, high-dynamic range artifact suppression, and time-shared NOESY. J Am Chem Soc 134:18619–18630CrossRefPubMedPubMedCentralGoogle Scholar
  10. Crespi HL, Rosenberg RM, Katz JL (1968) Proton magnetic resonance of proteins fully deuterated except for H-leucine side chains. Science 161:795–796CrossRefPubMedGoogle Scholar
  11. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6:277–293CrossRefPubMedGoogle Scholar
  12. Dodevski I, Nucci NV, Valentine KG, Sidhu GK, O’Brien ES, Pardi A, Wand AJ (2014) Optimized reverse micelle surfactant system for high-resolution NMR spectroscopy of encapsulated proteins and nucleic acids dissolved in low viscosity fluids. J Am Chem Soc 136(9):3465–3474CrossRefPubMedPubMedCentralGoogle Scholar
  13. Doreleijers JF, Sousa da Silva AW, Krieger E, Nabuurs SB, Spronk CA, Stevens TJ, Vranken WF, Vriend G, Vuister GW (2012) CING: an integrated residue-based structure validation program suite. J Biomol NMR 54(3):267–283CrossRefPubMedPubMedCentralGoogle Scholar
  14. Engelke J, Rüterjans H (1999) Recent developments in studying the dynamics of protein structures from and 15N and 13C relaxation time measurements. In: Krishna NR, Berliner L (eds) Structure computation and dynamics in protein NMR. Kluwer Academic/Plenum, New YorkGoogle Scholar
  15. Ernst RR, Bodenhausen G, Wokaun A (1987) Principles of nuclear magnetic resonance in one and two dimensions. Oxford University Press, OxfordGoogle Scholar
  16. Fiaux J, Bertelsen EB, Horwich AL, Wüthrich K (2002) NMR analysis of a 900K GroEL–GroES complex. Nature 418:207–211CrossRefPubMedGoogle Scholar
  17. Gossert AD, Jahnke W (2016) NMR in drug discovery: a practical guide to identification and validation of ligands interacting with biological macromolecules. Prog NMR Spectrosc 97:82–125CrossRefGoogle Scholar
  18. Gottstein D, Kirchner DK, Güntert P (2012) Simultaneous single-structure and bundle representation of protein NMR structures in torsion angle space. J Biomol NMR 52(4):351–364CrossRefPubMedGoogle Scholar
  19. Güntert P, Buchner L (2015) Combined automated NOE assignment and structure calculation with CYANA. J Biomol NMR 62:453–471CrossRefPubMedGoogle Scholar
  20. Hafsa NE, Arndt D, Wishart DS (2015) CSI 3.0: a web server for identifying secondary and super-secondary structure in proteins using NMR chemical shifts. Nucleic Acids Res 43(W1):W370–W377CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hagn F, Etzkorn M, Raschle T, Wagner G (2013) Optimized phospholipid bilayer Nanodiscs facilitate high-resolution structure determination of membrane proteins. J Am Chem Soc 135(5):1919–1925CrossRefPubMedPubMedCentralGoogle Scholar
  22. Herrmann T, Güntert P, Wüthrich K (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J Mol Biol 319(1):209–227CrossRefPubMedGoogle Scholar
  23. Hus JC, Salmon L, Bouvignies G, Lotze J, Blackledge M, Brüschweiler R (2008) 16-fold degeneracy of peptide plane orientations from residual dipolar couplings: analytical treatment and implications for protein structure determination. J Am Chem Soc 130(47):15927–15937CrossRefPubMedPubMedCentralGoogle Scholar
  24. Hyberts SG, Milbradt AG, Wagner AB, Arthanari H, Wagner G (2012) Application of iterative soft thresholding for fast reconstruction of NMR data non-uniformly sampled with multidimensional Poisson gap scheduling. J Biomol NMR 52(4):315–327CrossRefPubMedPubMedCentralGoogle Scholar
  25. Ishima R, Nagayama K (1995) Protein backbone dynamics revealed by quasi spectral density function analysis of amide N-15 nuclei. Biochemistry 34:31623171CrossRefGoogle Scholar
  26. Kainosho M, Torizawa T, Iwashita Y, Terauchi T, Ono AM, Güntert P (2006) Optimal isotope labelling for NMR protein structure determinations. Nature 440:52–57CrossRefPubMedGoogle Scholar
  27. Keeler J (2010) Understanding NMR spectroscopy, 2nd edn. Wiley, ChichesterGoogle Scholar
  28. Kirkpatrick S, Gelatt CD, Vecchi MP (1983) Optimization by simulated annealing. Science 220(4598):671–680CrossRefGoogle Scholar
  29. Korzhnev DM, Billeter M, Arseniev AS, Orekhov VY (2001) NMR studies of Brownian tumbling and internal motions in proteins. Prog NMR Spectrosc 38(3):197–266CrossRefGoogle Scholar
  30. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8(4):477–486CrossRefPubMedGoogle Scholar
  31. Levitt MH (2008) Spin dynamics: basics of nuclear magnetic resonance, 2nd edn. Wiley, ChichesterGoogle Scholar
  32. Marsh JA, Singh VK, Jia Z, Forman-Kay JD (2006) Sensitivity of secondary structure propensities to sequence differences between alpha- and gamma-synuclein: implications for fibrillation. Protein Sci 15(12):2795–2804CrossRefPubMedPubMedCentralGoogle Scholar
  33. Meirovitch E, Shapiro YE, Polimeno A, Freed JH (2010) Structural dynamics of biomacromolecules by NMR: the slowly relaxing local structure approach. Prog Nucl Magn Reson Spectrosc 56:360405CrossRefGoogle Scholar
  34. Nováček J, Žídek L, Sklenář V (2014) Toward optimal-resolution NMR of intrinsically disordered proteins. J Magn Reson 241:41–52CrossRefPubMedGoogle Scholar
  35. Ohki S, Takeuchi M, Mori M (2011) The NMR structure of stomagen reveals the basis of stomatal density regulation by plant peptide hormones. Nature Communications 2:512. https://doi.org/10.1038/ncomms150
  36. Orekhov VY, Jaravine VA (2011) Analysis of non-uniformly sampled spectra with MultiDimensional decomposition. Prog Nucl Magn Reson Spectrosc 59:271–292CrossRefPubMedGoogle Scholar
  37. Pervushin K, Riek R, Wider G, Wüthrich K (1997) Attenuated T 2 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. Proc Natl Acad Sci U S A 94:12366–12371CrossRefPubMedPubMedCentralGoogle Scholar
  38. Primrose WU (1993) Sample preparation. In: Roberts GCK (ed) NMR of macromolecules, a practical approach. Oxford University Press, OxfordGoogle Scholar
  39. Putter I, Barreto A, Markley JL, Jardetzky O (1969) Nuclear magnetic resonance studies of the structure and binding sites of enzymes, X. preparation of selectively deuterated analogs of staphylococcal nuclease. Biochemistry 64:1396–1403Google Scholar
  40. Riek R, Wider G, Pervushin K, Wüthrich K (1999) Polarization transfer by cross-correlated relaxation in solution NMR with very large molecules. Proc Natl Acad Sci U S A 96(9):4918–4923CrossRefPubMedPubMedCentralGoogle Scholar
  41. Rieping W, Habeck M, Bardiaux B, Bernard A, Malliavin TE, Nilges M (2007) ARIA2: automated NOE assignment and data integration in NMR structure calculation. Bioinformatics 23:381–382CrossRefPubMedGoogle Scholar
  42. Rule GS, Hitchens TK (2006) Fundamentals of protein NMR spectroscopy. Springer, DordrechtGoogle Scholar
  43. Sattler M, Schleucher J, Griesinger C (1999) Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog Nucl Magn Reson Spectrosc 34:93–158CrossRefGoogle Scholar
  44. Schwieters CD, Kuszewski J, Tjandra N, Clore GM (2003) The Xplor-NIH NMR molecular structure determination package. J Magn Reson 160:66–74CrossRefGoogle Scholar
  45. Shen Y, Bax A (2013) Protein backbone and sidechain torsion angles predicted from NMR chemical shifts using artificial neural networks. J Biomol NMR 56:227–241CrossRefPubMedPubMedCentralGoogle Scholar
  46. Shen Y, Lange O, Delaglio F, Rossi P, Aramini JM, Liu G, Eletsky A, Wu Y, Singarapu KK, Lemak A, Ignatchenko A, Arrowsmith CH, Szyperski T, Montelione GT, Baker D, Bax A (2008) Consistent blind protein structure generation from NMR chemical shift data. Proc Natl Acad Sci U S A 105(12):4685–4690CrossRefPubMedPubMedCentralGoogle Scholar
  47. Stanek J, Koźmiński W (2010) Iterative algorithm of discrete Fourier transform for processing randomly sampled NMR data sets. J Biomol NMR 47(1):65–77CrossRefPubMedGoogle Scholar
  48. Sun S, Gill M, Li Y, Huang M, Byrd RA (2015) Efficient and generalized processing of multidimensional NUS NMR data: the NESTA algorithm and comparison of regularization terms. J Biomol NMR 62(1):105–117CrossRefPubMedPubMedCentralGoogle Scholar
  49. Tugarinov V, Kay LE (2003) Ile, Leu, and Val methyl assignments of the 723-residue malate synthase G using a new labeling strategy and novel NMR methods. J Am Chem Soc 125(45):13868–13878CrossRefPubMedGoogle Scholar
  50. Vallurupalli P, Bouvignies G, Kay LE (2012) Studying “invisible” excited protein states in slow exchange with a major state conformation. J Am Chem Soc 134(19):8148–8161CrossRefPubMedGoogle Scholar
  51. Vriend G (1990) WHAT IF: a molecular modeling and drug design program. J Mol Graph 8(1):52–56. 29CrossRefPubMedGoogle Scholar
  52. Wand AJ, Ehrhardt MR, Flynn PF (1998) High-resolution NMR of encapsulated proteins dissolved in low-viscosity fluids. Proc Natl Acad Sci U S A 95(26):15299–15302CrossRefPubMedPubMedCentralGoogle Scholar
  53. Williamson MP, Havel TF, Wüthrich K (1985) Solution conformation of proteinase inhibitor IIA from bull seminal plasma by 1H nuclear magnetic resonance and distance geometry. J Mol Biol 182(2):295–315CrossRefPubMedGoogle Scholar
  54. Wishart DS, Sykes BD, Richards FM (1991) Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J Mol Biol 222(2):311–333CrossRefPubMedGoogle Scholar
  55. Worley B (2016) Convex accelerated maximum entropy reconstruction. J Magn Reson 265:90–98CrossRefPubMedPubMedCentralGoogle Scholar
  56. Wüthrich K (1986) NMR of proteins and nucleic acids. Wiley, New YorkGoogle Scholar
  57. Yadav DK, Lukavsky PJ (2016) NMR solution structure determination of large RNA-protein complexes. Prog Nucl Magn Reson Spectrosc 97:57–81CrossRefGoogle Scholar
  58. Yao J, Dyson HJ, Wright PE (1997) Chemical shift dispersion and secondary structure prediction in unfolded and partly folded proteins. FEBS Lett 419(2–3):285–289CrossRefPubMedGoogle Scholar
  59. Ying J, Delaglio F, Torchia DA, Bax A (2016) Sparse multidimensional iterative Lineshape-enhanced (SMILE) reconstruction of both non-uniformly sampled and conventional NMR data. J Biomol NMR 68(2):101–118CrossRefPubMedPubMedCentralGoogle Scholar
  60. Zhang HY, van Ingen H (2016) Isotope-labeling strategies for solution NMR studies of macromolecular assemblies. Curr Opin Struct Biol 38:75–82CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Milan Zachrdla
    • 1
  • Zuzana Jaseňáková
    • 1
  • Lukáš Žídek
    • 1
  1. 1.Central European Institute of TechnologyMasaryk UniversityBrnoCzech Republic

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