Skip to main content
SpringerLink
Log in
Book cover

Protein NMR pp 55–66Cite as

Afterglow Solid-State NMR Spectroscopy

  • Protocol
  • First Online:

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1688))

Abstract

Biomolecular solid-state NMR experiments have traditionally been collected through detection of 13C or 15N nuclei. Since these nuclei have relatively low sensitivity stemming from their smaller gyromagnetic ratios relative to 1H, the time required to collect multi-dimensional datasets serves as a limitation to resonance assignment and structure determination. One improvement in the field has been to employ simultaneous or parallel acquisition techniques with the goal of acquiring more than one dataset at a time and therefore speeding up the overall data collection process. Central to these experiments is the cross-polarization (CP) element, which serves as a way to transfer magnetization between nuclei via magnetic dipolar couplings. In this chapter, we show how residual signal remaining after CP is a polarization source that can be used to acquire additional datasets. The setup of this class of experiments, referred to as Afterglow spectroscopy, is described and demonstrated using a membrane protein transporter involved in multidrug resistance.

This is a preview of subscription content, log in via an institution.

Protocol
USD   49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Springer Nature is developing a new tool to find and evaluate Protocols. Learn more

References

  1. Gutmann T, Grünberg A, Rothermel N et al (2013) Solid-state NMR concepts for the investigation of supported transition metal catalysts and nanoparticles. Solid State Nucl Magn Reson 55:1–11

    Article  PubMed  Google Scholar 

  2. Heise H, Hoyer W, Becker S et al (2005) Molecular-level secondary structure, polymorphism, and dynamics of full-length a-synuclein fibrils studied by solid-state NMR. Proc Natl Acad Sci USA 102:15871–15876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Opella SJ, Marassi FM (2004) Structure determination of membrane proteins by NMR spectroscopy. Chem Rev 104:3587–3606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Hong M, Zhang Y, Hu F (2012) Membrane protein structure and dynamics from NMR spectroscopy. Annu Rev Phys Chem 63:1–24

    Article  CAS  PubMed  Google Scholar 

  5. Wylie BJ, Do HQ, Borcik CG, Hardy EP (2016) Advances in solid-state NMR of membrane proteins. Mol Phys 114(24):3598–3609

    Article  CAS  Google Scholar 

  6. Quinn CM, Lu M, Suiter CL et al (2015) Magic angle spinning NMR of viruses. Prog Nucl Magn Reson Spectrosc 86:21–40

    Article  PubMed  Google Scholar 

  7. Takahashi H, Ayala I, Bardet M et al (2013) Solid-state NMR on bacterial cells: selective cell wall signal enhancement and resolution improvement using dynamic nuclear polarization. J Am Chem Soc 135:5105–5110

    Article  CAS  PubMed  Google Scholar 

  8. Andrew ER, Bradbury A, Eades GR (1958) Nuclear magnetic resonance spectra from a crystal rotated at high speed. Nature 182:1659–1659

    Article  CAS  Google Scholar 

  9. Lowe IJ (1959) Free induction decays of rotating solids. Phys Rev Lett 2:285–287

    Article  CAS  Google Scholar 

  10. Hong M (1999) Determination of multiple φ-torsion angles in proteins by selective and extensive 13C labeling and two-dimensional solid-state NMR. J Magn Reson 139:389–401

    Article  CAS  PubMed  Google Scholar 

  11. Zhou DH, Shah G, Cormos M et al (2007) Proton-detected solid-state NMR spectroscopy of fully protonated proteins at 40 kHz magic-angle spinning. J Am Chem Soc 129:11791–11801

    Article  CAS  PubMed  Google Scholar 

  12. Loquet A, Sgourakis NG, Gupta R et al (2012) Atomic model of the type III secretion system needle. Nature 486:276–279

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Wang S, Munro RA, Shi L et al (2013) Solid-state NMR spectroscopy structure determination of a lipid-embedded heptahelical membrane protein. Nat Methods 10:1007–1012

    Article  PubMed  Google Scholar 

  14. Bertini I, Emsley L, Lelli M et al (2010) Ultrafast MAS solid-state NMR permits extensive 13C and 1H detection in paramagnetic metalloproteins. J Am Chem Soc 132:5558–5559

    Article  CAS  PubMed  Google Scholar 

  15. Paramasivam S, Suiter CL, Hou G et al (2012) Enhanced sensitivity by nonuniform sampling enables multidimensional MAS NMR spectroscopy of protein assemblies. J Phys Chem B 116:7416–7427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. McNeill SA, Gor’kov PL, Shetty K et al (2009) A low-E magic angle spinning probe for biological solid state NMR at 750 MHz. J Magn Reson 197:135–144

    Article  CAS  PubMed  Google Scholar 

  17. Kupče Ē (2011) NMR with multiple receivers. In: Mod. NMR Methodol. Springer, Berlin, pp 71–96

    Google Scholar 

  18. Kupče E, Kay LE, Freeman R (2010) Detecting the “afterglow” of 13C NMR in proteins using multiple receivers. J Am Chem Soc 132:18008–18011

    Article  PubMed  Google Scholar 

  19. Pines A, Gibby MG, Waugh JS (1973) Proton-enhanced NMR of dilute spins in solids. J Chem Phys 59:569–590

    Article  CAS  Google Scholar 

  20. Banigan JR, Traaseth NJ (2012) Utilizing afterglow magnetization from cross-polarization magic-angle-spinning solid-state NMR spectroscopy to obtain simultaneous Heteronuclear multidimensional spectra. J Phys Chem B 116:7138–7144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Gopinath T, Veglia G (2012) Dual acquisition magic-angle spinning solid-state NMR-spectroscopy: simultaneous acquisition of multidimensional spectra of biomacromolecules. Angew Chem Int Ed Engl 51:2731–2735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Gopinath T, Veglia G (2013) Orphan spin operators enable the acquisition of multiple 2D and 3D magic angle spinning solid-state NMR spectra. J Chem Phys 138:184201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Gopinath T, Veglia G (2016) Multiple acquisitions via sequential transfer of orphan spin polarization (MAeSTOSO): how far can we push residual spin polarization in solid-state NMR? J Magn Reson 267:1–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Mote KR, Gopinath T, Veglia G (2013) Determination of structural topology of a membrane protein in lipid bilayers using polarization optimized experiments (POE) for static and MAS solid state NMR spectroscopy. J Biomol NMR 57:91–102

    Article  CAS  PubMed  Google Scholar 

  25. Das BB, Opella SJ (2016) Simultaneous cross polarization to 13C and 15N with 1H detection at 60kHz MAS solid-state NMR. J Magn Reson 262:20–26

    Article  CAS  PubMed  Google Scholar 

  26. Akbey Ü, Camponeschi F, van Rossum B-J, Oschkinat H (2011) Triple resonance cross-polarization for more sensitive 13C MAS NMR spectroscopy of Deuterated proteins. ChemPhysChem 12:2092–2096

    Article  CAS  PubMed  Google Scholar 

  27. Banigan JR, Gayen A, Cho M-K, Traaseth NJ (2015) A structured loop modulates coupling between the substrate-binding and dimerization domains in the multidrug resistance transporter EmrE. J Biol Chem 290:805–814

    Article  CAS  PubMed  Google Scholar 

  28. Banigan JR, Gayen A, Traaseth NJ (2015) Correlating lipid bilayer fluidity with sensitivity and resolution of polytopic membrane protein spectra by solid-state NMR spectroscopy. Biochim Biophys Acta 1848:334–341

    Article  CAS  PubMed  Google Scholar 

  29. Delaglio F, Grzesiek S, Vuister GW et al (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6:277–293

    Article  CAS  PubMed  Google Scholar 

  30. Goddard TD, Kneller DG SPARKY 3. https://www.cgl.ucsf.edu/home/sparky/

  31. Stringer JA, Bronnimann CE, Mullen CG et al (2005) Reduction of RF-induced sample heating with a scroll coil resonator structure for solid-state NMR probes. J Magn Reson 173:40–48

    Article  CAS  PubMed  Google Scholar 

  32. Morcombe CR, Zilm KW (2003) Chemical shift referencing in MAS solid state NMR. J Magn Reson 162:479–486

    Article  CAS  PubMed  Google Scholar 

  33. Oas TG, Griffin RG, Levitt MH (1988) Rotary resonance recoupling of dipolar interactions in solid-state nuclear magnetic resonance spectroscopy. J Chem Phys 89:692–695

    Article  CAS  Google Scholar 

  34. Gan Z (2006) Rotary resonance echo double resonance for measuring heteronuclear dipolar coupling under MAS. J Magn Reson 183:235–241

    Article  CAS  PubMed  Google Scholar 

  35. Schaefer J, McKay R, Stejskal E (1979) Double-cross-polarization NMR of solids. Academic Press, New York

    Google Scholar 

  36. Baldus M, Petkova AT, Herzfeld J, Griffin RG (1998) Cross polarization in the tilted frame: assignment and spectral simplification in heteronuclear spin systems. Mol Phys 95:1197–1207

    Article  CAS  Google Scholar 

  37. Ishii Y, Ashida J, Terao T (1995) 13C-1H dipolar recoupling dynamics in 13C multiple-pulse solid-state NMR. Chem Phys Lett 246:439–445

    Article  CAS  Google Scholar 

  38. Franks WT, Kloepper KD, Wylie BJ, Rienstra CM (2007) Four-dimensional heteronuclear correlation experiments for chemical shift assignment of solid proteins. J Biomol NMR 39:107–131

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  40. Morcombe CR, Gaponenko V, Byrd RA, Zilm KW (2004) Diluting abundant spins by isotope edited radio frequency field assisted diffusion. J Am Chem Soc 126:7196–7197

    Article  CAS  PubMed  Google Scholar 

  41. Banigan JR, Gayen A, Traaseth NJ (2013) Combination of 15N reverse labeling and afterglow spectroscopy for assigning membrane protein spectra by magic-angle-spinning solid-state NMR: application to the multidrug resistance protein EmrE. J Biomol NMR 55:391–399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Good D, Pham C, Jagas J et al. (2017) Solid-state NMR provides evidence for small-amplitude slow domain motions in a multispanning transmembrane α-Helical Protein. J Am Chem Soc 139(27):9246–9258.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Harris RK, Becker ED, Cabral de Menezes SM et al (2002) NMR nomenclature: nuclear spin properties and conventions for chemical shifts. IUPAC recommendations 2001. International Union of Pure and Applied Chemistry. Physical chemistry division. Commission on molecular structure and spectroscopy. Magn Reson Chem 40:489–505

    Article  CAS  Google Scholar 

  44. Siemer AB, Ritter C, Steinmetz MO et al (2006) 13C, 15N resonance assignment of parts of the HET-s prion protein in its amyloid form. J Biomol NMR 34:75–87

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by NSF (MCB1506420) and NIH (R01AI108889).

Author information

Authors and Affiliations

  1. Department of Chemistry, New York University, 100 Washington Square East, New York, NY, 10003, USA

    Gili Abramov & Nathaniel J. Traaseth

Authors
  1. Gili Abramov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nathaniel J. Traaseth
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nathaniel J. Traaseth .

Editor information

Editors and Affiliations

  1. Department of Chemistry and Biochemistry, The City College of New York, New York, New York, USA

    Ranajeet Ghose

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Science+Business Media LLC

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Abramov, G., Traaseth, N.J. (2018). Afterglow Solid-State NMR Spectroscopy. In: Ghose, R. (eds) Protein NMR. Methods in Molecular Biology, vol 1688. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7386-6_3

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-7386-6_3

  • Published:

  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-7385-9

  • Online ISBN: 978-1-4939-7386-6

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation