Skip to main content
SpringerLink
Log in

Efficient 18.8 T MAS-DNP NMR reveals hidden side chains in amyloid fibrils

  • Article
  • Published:
Journal of Biomolecular NMR Aims and scope Submit manuscript

Abstract

Amyloid fibrils are large and insoluble protein assemblies composed of a rigid core associated with a cross-β arrangement rich in β-sheet structural elements. It has been widely observed in solid-state NMR experiments that semi-rigid protein segments or side chains do not yield easily observable NMR signals at room temperature. The reasons for the missing peaks may be due to the presence of unfavorable dynamics that interfere with NMR experiments, which result in very weak or unobservable NMR signals. Therefore, for amyloid fibrils, semi-rigid and dynamically disordered segments flanking the amyloid core are very challenging to study. Here, we show that high-field dynamic nuclear polarization (DNP), an NMR hyperpolarization technique typically performed at low temperatures, can circumvent this issue because (i) the low-temperature environment (~ 100 K) slows down the protein dynamics to escape unfavorable detection regime, (ii) DNP improves the overall NMR sensitivity including those of flexible side chains, and (iii) efficient cross-effect DNP biradicals (SNAPol-1) optimized for high-field DNP (≥ 18.8 T) are employed to offer high sensitivity and resolution suitable for biomolecular NMR applications. By combining these factors, we have successfully established an impressive enhancement factor of ε ~ 50 on amyloid fibrils using an 18.8 T/ 800 MHz magnet. We have compared the DNP efficiencies of M-TinyPol, NATriPol-3, and SNAPol-1 biradicals on amyloid fibrils. We found that SNAPol-1 (with ε ~ 50) outperformed the other two radicals. The MAS DNP experiments revealed signals of flexible side chains previously inaccessible at conventional room-temperature experiments. These results demonstrate the potential of MAS-DNP NMR as a valuable tool for structural investigations of amyloid fibrils, particularly for side chains and dynamically disordered segments otherwise hidden at room temperature.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Akbey Ü, Linden AH, Oschkinat H (2012) High-temperature dynamic nuclear polarization enhanced magic-angle-spinning NMR. Appl Magn Reson 43:81–90

    Article  Google Scholar 

  • Bahri S et al (2022) H detection and dynamic nuclear polarization—enhanced NMR of Aβ 1–42 fibrils.

  • Bajaj VS, Mak-Jurkauskas ML, Belenky M, Herzfeld J, Griffin RG (2010) DNP enhanced frequency-selective TEDOR experiments in bacteriorhodopsin. J Magn Reson 202:9–13

    Article  ADS  Google Scholar 

  • Barnes AB et al (2009) Cryogenic sample exchange NMR probe for magic angle spinning dynamic nuclear polarization. J Magn Reson 198:261–270

    Article  ADS  Google Scholar 

  • Barnes AB et al (2010) Resolution and polarization distribution in cryogenic DNP/MAS experiments. Phys Chem Chem Phys 12:5861

    Article  Google Scholar 

  • Bauer T et al (2017) Line-broadening in low-temperature solid-State NMR spectra of fibrils. J Biomol NMR 67:51–61

  • Bayro MJ et al (2011) Intermolecular structure determination of amyloid fibrils with magic-angle spinning and dynamic nuclear polarization NMR. J Am Chem Soc 133:13967–13974

    Article  Google Scholar 

  • Berruyer P (2020) Dynamic nuclear polarization enhancement of 200 at 21.15 T enabled by 65 kHz magic angle spinning. J Phys Chem Lett 11:8386–8391.

  • Biedenbänder T, Aladin V, Saeidpour S, Corzilius B (2022) Dynamic nuclear polarization for sensitivity enhancement in NMR. Chem Rev.

    Article  Google Scholar 

  • Björklund S, Nowacka A, Bouwstra JA, Sparr E, Topgaard D (2013) Characterization of stratum corneum molecular dynamics by natural-abundance 13C solid-state NMR. PLoS ONE.

  • Blank M, Borchard P, Cauffman S, Felch K, Rosay M (2016) Development of high-frequency cw gyrotrons for DNP/NMR applications. Terahertz Sci Technol 9:177–186

    Google Scholar 

  • Cai X et al (2021) Highly efficient trityl-nitroxide biradicals for biomolecular high-field dynamic nuclear polarization. Chemisty A 27:12758–12762

    Google Scholar 

  • Chapman MR et al (2002) Role of Escherichia coli curli operons in directing amyloid fiber formation. Science (80-) 295:851–855

    Article  ADS  Google Scholar 

  • Colvin MT et al (2015) High resolution structural characterization of Aβ42 amyloid fibrils by magic angle spinning NMR. J Am Chem Soc 137:7509–7518

    Article  Google Scholar 

  • Colvin MT et al (2016) Atomic resolution structure of monomorphic Aβ 42 amyloid fibrils. J Am Chem Soc 138:9663–9674

    Article  Google Scholar 

  • Conroy DW et al (2022) Probing Watson-Crick and Hoogsteen base pairing in duplex DNA using dynamic nuclear polarization solid-state NMR spectroscopy. Proc Natl Acad Sci USA

  • Corzilius B, Andreas LB, Smith AA, Ni QZ, Griffin RG (2014) Paramagnet induced signal quenching in MAS-DNP experiments in frozen homogeneous solutions. J Magn Reson 240:113–123

    Article  ADS  Google Scholar 

  • Daskalov A et al (2015) Signal transduction by a fungal NOD-like receptor based on propagation of a prion amyloid fold. PLoS Biol 13:1–26

    Article  Google Scholar 

  • Daskalov A et al (2020) Structural and molecular basis of cross-seeding barriers in amyloids. Proc Natl Acad Sci USA 118:1–8

    Google Scholar 

  • Daskalov A et al (2021) Structures of pathological and functional amyloids and prions, a solid-state NMR perspective. Front Mol Neurosci 14:1–18

    Article  Google Scholar 

  • David G et al (2018) Structural studies of self-assembled subviral particles: combining cell-free expression with 110 kHz MAS NMR spectroscopy. Angew Chem Int Ed 57:4787–4791

    Article  Google Scholar 

  • De Paëpe G et al (2011) Heteronuclear proton assisted recoupling. J Chem Phys 134:1–18

    Article  Google Scholar 

  • Debelouchina GT et al (2013) Higher order amyloid fibril structure by MAS NMR and DNP spectroscopy. J Am Chem Soc 135:19237–19247

    Article  Google Scholar 

  • Delage-Laurin L et al (2021) Overhauser dynamic nuclear polarization with selectively deuterated BDPA radicals. J Am Chem Soc 143:20281–20290

    Article  Google Scholar 

  • Deo T, Cheng Q, Paul S, Qiang W, Potapov A (2021) Application of DNP-enhanced solid-state NMR to studies of amyloid-β peptide interaction with lipid membranes. Chem Phys Lipids 236:105071

    Article  Google Scholar 

  • Dobson CM, Knowles TPJ, Vendruscolo M (2020) The amyloid phenomenon and its significance in biology and medicine. Cold Spring Harb Perspect Biol 12

  • Donovan KJ, Jain SK, Silvers R, Linse S, Griffin RG (2017a) Proton-assisted recoupling (PAR) in peptides and proteins. J Phys Chem B 121:10804–10817

    Article  Google Scholar 

  • Donovan KJ, Silvers R, Linse S, Griffin RG (2017b) 3D MAS NMR experiment utilizing through-space 15 N– 15 N correlations. J Am Chem Soc 139:6518–6521

    Article  Google Scholar 

  • Felch K et al (2013) First tests of a 527 GHz gyrotron for dynamic nuclear polarization. In 2013 IEEE 14th international vacuum electronics conference (IVEC) 1–2 (IEEE, 2013).

  • Fitzpatrick AWP et al (2013) Atomic structure and hierarchical assembly of a cross-β amyloid fibril. Proc Natl Acad Sci USA 110:5468–5473

    Article  ADS  Google Scholar 

  • Fitzpatrick AW, Saibil HR (2019) Cryo-EM of amyloid fibrils and cellular aggregates. Curr Opin Struct Biol 58:34–42

    Article  Google Scholar 

  • Frederick KK et al (2017) Combining DNP NMR with segmental and specific labeling to study a yeast prion protein strain that is not parallel in-register. Proc Natl Acad Sci USA 114:3642–3647

    Article  ADS  Google Scholar 

  • Fricke P, Demers JP, Becker S, Lange A (2014) Studies on the MxiH protein in T3SS needles using DNP-enhanced ssNMR spectroscopy. ChemPhysChem 15:57–60

    Article  Google Scholar 

  • Fricke P et al (2016) High resolution observed in 800 MHz DNP spectra of extremely rigid type III secretion needles. J Biomol NMR 65:121–126

    Article  Google Scholar 

  • Gath J et al (2014) Yet another polymorph of α-synuclein: solid-state sequential assignments. Biomol NMR Assign 8:395–404

    Article  Google Scholar 

  • Gauto DF et al (2019) Aromatic ring dynamics, thermal activation, and transient conformations of a 468 kDa enzyme by specific 1H–13C labeling and fast magic-angle spinning NMR. J Am Chem Soc 141:11183–11195

    Article  Google Scholar 

  • Gauto D, Dakhlaoui O, Marin-Montesinos I, Hediger S, De Paëpe G (2021) Targeted DNP for biomolecular solid-state NMR. Chem Sci 12:6223–6237

    Article  Google Scholar 

  • Halbritter T, Harrabi R, Paul S, Tol JV, Lee D, Sigurdsson ST, Mentink-Vigier F, De Paëpe G (2022) PyrroTriPol: a Semi-rigid trityl-nitroxide for high field dynamic nuclear polarization. Chem. Sci.

    Article  Google Scholar 

  • Heise H et al (2008) Solid-state NMR reveals structural differences between fibrils of wild-type and disease-related A53T mutant α-synuclein. J Mol Biol 380:444–450

    Article  Google Scholar 

  • Henstra A, Dirksen P, Schmidt J, Wenckebach WT (1988) Nuclear spin orientation via electron spin locking (NOVEL). J Magn Reson 77:389–393

    ADS  Google Scholar 

  • Jaroniec CP (2019) Two decades of progress in structural and dynamic studies of amyloids by solid-state NMR. J Magn Reson 306:42–47

    Article  ADS  Google Scholar 

  • Jaudzems K et al (2018) Dynamic nuclear polarization-enhanced biomolecular NMR spectroscopy at high magnetic field with fast magic-angle spinning. Angew Chem Int Ed 7458–7462.

  • Jaudzems K, Polenova T, Pintacuda G, Oschkinat H, Lesage A (2019) DNP NMR of biomolecular assemblies. J Struct Biol 206:90–98

    Article  Google Scholar 

  • Jirasko V et al (2021) Dimer organization of membrane-associated NS5A of hepatitis C virus as determined by highly sensitive 1H-detected solid-state NMR. Angew Chem Int Ed 60:5339–5347

    Article  Google Scholar 

  • Ke PC et al (2020) Half a century of amyloids: past, present and future. Chem Soc Rev 49:5473–5509

    Article  Google Scholar 

  • Kubicki DJ et al (2014) Amplifying dynamic nuclear polarization of frozen solutions by incorporating dielectric particles. J Am Chem Soc 136:15711–15718

    Article  Google Scholar 

  • Lewandowski JR, De Paëpe G, Griffin RG (2007) Proton assisted insensitive nuclei cross polarization. J Am Chem Soc 129:728–729

    Article  Google Scholar 

  • Li Y et al (2021) Solid-state MAS NMR at ultra low temperature of hydrated alanine doped with DNP radicals. J Magn Reson 333:107090

    Article  Google Scholar 

  • Lopez del Amo J-M, Schneider D, Loquet A, Lange A, Reif B (2013) Cryogenic solid state NMR studies of fibrils of the Alzheimer’s disease amyloid-β peptide: perspectives for DNP. J Biomol NMR 56:359–363

    Article  Google Scholar 

  • Loquet A, Saupe SJ (2017) Diversity of amyloid motifs in NLR signaling in fungi. Biomolecules 7:1–10

    Article  Google Scholar 

  • Loquet A et al (2012) Atomic model of the type III secretion system needle. Nature 486:276–279

    Article  ADS  Google Scholar 

  • Loquet A, Saupe SJ, Romero D (2018a) Functional amyloids in health and disease. J Mol Biol 430:3629–3630

    Article  Google Scholar 

  • Loquet A et al (2018b) 3D structure determination of amyloid fibrils using solid-state NMR spectroscopy. Methods.

    Article  Google Scholar 

  • Lund A et al (2020) TinyPols: a family of water-soluble binitroxides tailored for dynamic nuclear polarization enhanced NMR spectroscopy at 18.8 and 21.1 T. Chem Sci 68:42–61.

  • Maciejko J et al (2015) Visualizing specific cross-protomer interactions in the homo-oligomeric membrane protein proteorhodopsin by dynamic-nuclear-polarization-enhanced solid-state NMR. J Am Chem Soc 137:9032–9043

    Article  Google Scholar 

  • Maji SK et al (2009) Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science (80-) 325:328–332

    Article  ADS  Google Scholar 

  • Marin-Montesinos I et al (2019) Selective high-resolution DNP-enhanced NMR of biomolecular binding sites. Chem Sci 10:3366–3374

    Article  Google Scholar 

  • Mathies G et al (2015) Efficient dynamic nuclear polarization at 800 MHz/527 GHz with trityl-nitroxide biradicals. Angew Chemie - Int Ed 54:11770–11774

    Article  Google Scholar 

  • Matsuki Y, Idehara T, Fukazawa J, Fujiwara T (2016) Advanced instrumentation for DNP-enhanced MAS NMR for higher magnetic fields and lower temperatures. J Magn Reson 264:107–115

    Article  ADS  Google Scholar 

  • Maus DC et al (1996) A solid-state NMR study of tungsten methyl group dynamics in [W(η 5-C 5Me 5)Me 4][PF 6]. J Am Chem Soc 118:5665–5671

    Article  Google Scholar 

  • Meier BH, Böckmann A (2015) The structure of fibrils from ‘misfolded’ proteins. Curr Opin Struct Biol 30:43–49

    Article  Google Scholar 

  • Menzildjian G et al (2021) Efficient dynamic nuclear polarization up to 230 K with hybrid BDPA-nitroxide radicals at a high magnetic field. J Phys Chem B 125:13329–13338

    Article  Google Scholar 

  • Nagaraj M et al (2016) Surface binding of TOTAPOL assists structural investigations of amyloid fibrils by dynamic nuclear polarization NMR spectroscopy. ChemBioChem.

    Article  Google Scholar 

  • Ni QZ et al (2017) Peptide and protein dynamics and low-temperature/DNP magic angle spinning NMR. J Phys Chem B (2017). https://doi.org/10.1021/acs.jpcb.7b02066

  • Potapov A, Yau W, Ghirlando R, Thurber KR, Tycko R (2015) Successive stages of amyloid-β self-assembly characterized by solid-state nuclear magnetic resonance with dynamic nuclear polarization. J Am Chem Soc 137:8294–8307

    Article  Google Scholar 

  • Purea A et al (2019) Improved waveguide coupling for 1.3mm MAS DNP probes at 263 GHz. J Magn Reson 302:43–49

  • Rankin A, Trébosc J, Pourpoint F, Amoureux J-P, Lafon O (2019) Recent developments in MAS DNP-NMR of materials. Solid State Nucl Magn Reson.

    Article  Google Scholar 

  • Ravotti F et al (2016) Solid-state NMR sequential assignment of an Amyloid-β(1–42) fibril polymorph. Biomol NMR Assign 10:269–276

    Article  Google Scholar 

  • Redrouthu VS, Mathies G (2022) Efficient pulsed dynamic nuclear polarization with the X-Inverse-X sequence. J Am Chem Soc 144:1513–1516

    Article  Google Scholar 

  • Sauvée C et al (2013) Highly efficient, water-soluble polarizing agents for dynamic nuclear polarization at high frequency. Angew Chem 52:10858–10861

    Article  Google Scholar 

  • Sesti EL et al (2018) Magic angle spinning NMR below 6 K with a computational fluid dynamics analysis of fluid flow and temperature gradients. J Magn Reson 286:1–9

    Article  ADS  Google Scholar 

  • Siemer AB (2020) Advances in studying protein disorder with solid-state NMR. Solid State Nucl Magn Reson 106:101643

    Article  Google Scholar 

  • Siemer AB, Ritter C, Ernst M, Riek R, Meier BH (2005) High-resolution solid-state NMR spectroscopy of the prion protein HET-s in its amyloid conformation. Angew Chem 44:2441–2444

    Article  Google Scholar 

  • Siemer AB et al (2006) Observation of highly flexible residues in amyloid fibrils of the HET-s prion. J Am Chem Soc 128:13224–13228

    Article  Google Scholar 

  • Su Y, Andreas L, Griffin RG (2015) Magic angle spinning NMR of proteins: high-frequency dynamic nuclear polarization and (1)H detection. Annu Rev Biochem 84:465–497

    Article  Google Scholar 

  • Takahashi H, Hediger S, De Paëpe G (2013) Matrix-free dynamic nuclear polarization enables solid-state NMR 13C–13C correlation spectroscopy of proteins at natural isotopic abundance. Chem Commun 49:9479–9481

    Article  Google Scholar 

  • Tan KO, Jawla S, Temkin RJ, Griffin RG (2019a) Pulsed dynamic nuclear polarization. eMagRes 339–352.

  • Tan KO, Yang C, Weber RT, Mathies G, Griffin RG (2019b) Time-optimized pulsed dynamic nuclear polarization. Sci Adv 5:eaav6909

  • Tan KO et al (2022) Observing nearby nuclei on paramagnetic trityls and MOFs via DNP and electron decoupling. Chem. Eur. J.

  • Thankamony AS, Wittmann JJ, Kaushik M, Corzilius B (2017) Dynamic nuclear polarization for sensitivity enhancement in modern solid-state NMR. Prog Nucl Magn Reson Spectrosc 102–103:120–195

  • Thurber K, Tycko R (2016) Low-temperature dynamic nuclear polarization with helium-cooled samples and nitrogen-driven magic-angle spinning. J Magn Reson 264:99–106

    Article  ADS  Google Scholar 

  • Thurber K, Yau W, Tycko R (2010) Low-temperature dynamic nuclear polarization at 9.4 T with a 30 mW microwave source. J Magn Reson 204:303–313

    Article  ADS  Google Scholar 

  • Tycko R (2014) Physical and structural basis for polymorphism in amyloid fibrils. Protein Sci 23:1528–1539

    Article  Google Scholar 

  • van der Wel PCA (2017) Insights into protein misfolding and aggregation enabled by solid-state NMR spectroscopy. Solid State Nucl Magn Reson 88:1–14

    Article  ADS  Google Scholar 

  • Van Melckebeke H et al (2010) Atomic-resolution three-dimensional structure of HET-s(218–289) amyloid fibrils by solid-state NMR spectroscopy. J Am Chem Soc 132:13765–13775

    Article  Google Scholar 

  • Van Melckebeke H et al (2011) Probing water accessibility in HET-s(218–289) amyloid fibrils by solid-state NMR. J Mol Biol 405:765–772

    Article  Google Scholar 

  • Vranken WF et al (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins Struct Funct Genet 59:687–696

    Article  Google Scholar 

  • Wasmer C et al (2008) Amyloid fibrils of the HET-s(218–289) prion form a beta solenoid with a triangular hydrophobic core. Science 319:1523–1526

    Article  ADS  Google Scholar 

  • Wiegand T et al (2016) Solid-state NMR sequential assignments of the N-terminal domain of HpDnaB helicase. Biomol NMR Assign 10:13–23

    Article  Google Scholar 

  • Wili N et al (2022) Designing broadband pulsed dynamic nuclear polarization sequences in static solids. Sci Adv 8:1–13

    Article  Google Scholar 

  • Wisser D et al (2018) BDPA-nitroxide biradicals tailored for efficient dynamic nuclear polarization enhanced solid-state NMR at magnetic fields up to 21.1 T. J Am Chem Soc 140:13340–13349

  • Zhai W et al (2020) Postmodification via thiol-click chemistry yields hydrophilic trityl-nitroxide biradicals for biomolecular high-field dynamic nuclear polarization. J Phys Chem B 124:9047–9060

    Article  Google Scholar 

  • Zhao W, Fernando LD, Kirui A, Deligey F, Wang T (2020) Solid-state NMR of plant and fungal cell walls: a critical review. Solid State Nucl Magn Reson 107:101660

    Article  Google Scholar 

Download references

Acknowledgements

A. Loquet acknowledges financial support from the European Research Council (ERC) under the European Unions Horizon 2020 research and innovation program (ERC-2015-StG GA No. 639020). A. Lends was supported by the Swiss National Science Foundation for the early postdoc mobility project (P2EZP2_184258). K.O.T is grateful for the fundings granted by the French National Research Agency: PulsedDNP (ANR-20-ERC9-0008) and HFPulsedDNP (ANR-21-CE29-0019). Financial support from the IR INFRANALYTICS FR2054 for conducting the research is gratefully acknowledged. Y.P.L. acknowledges the support from the National Natural Science Foundation of China (Nos. 22174099 and 21871210) and Science & Technology Projects of Tianjin (No. 20JCZDJC00050).

Funding

Funding was provided by European Research Council (639020), Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (P2EZP2_184258), Agence Nationale de la Recherche (ANR-20-ERC9-0008), National Natural Science Foundation of China (22174099), and Tianjin Science and Technology Program (20JCZDJC00050).

Author information

Authors and Affiliations

  1. CNRS, Chemistry and Biology of Membranes and Nanoobjects (CBMN), UMR 5348, Institut Europeen de Chimie et Biologie (IECB), University of Bordeaux, 33600, Pessac, France

    Alons Lends, Asen Daskalov, Jayakrishna Shenoy, Muhammed Bilal Abdul-Shukkoor, Mélanie Berbon & Antoine Loquet

  2. Laboratoire des Biomolécules, LBM, Département de Chimie, École Normale Supérieure, PSL University, Sorbonne Université, CNRS, 75005, Paris, France

    Nicolas Birlirakis, Fabien Ferrage & Kong Ooi Tan

  3. Tianjin Key Laboratory on Technologies Enabling Development of Clinical Therapeutics and Diagnostics, School of Pharmacy, Tianjin Medical University, Tianjin, 300070, China

    Xinyi Cai & Yangping Liu

Authors
  1. Alons Lends
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nicolas Birlirakis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xinyi Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Asen Daskalov
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jayakrishna Shenoy
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Muhammed Bilal Abdul-Shukkoor
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mélanie Berbon
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Fabien Ferrage
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yangping Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Antoine Loquet
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Kong Ooi Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

A. Lends, A. Loquet, and KOT designed the research. The NMR samples were prepared in Bordeaux, while the DNP experiments were performed at ENS. XC and YPL provided the radicals. A. Lends wrote the first draft of the manuscript. All authors prepared the figures, edited, and reviewed the manuscript.

Corresponding authors

Correspondence to Antoine Loquet or Kong Ooi Tan.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 333 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lends, A., Birlirakis, N., Cai, X. et al. Efficient 18.8 T MAS-DNP NMR reveals hidden side chains in amyloid fibrils. J Biomol NMR 77, 121–130 (2023). https://doi.org/10.1007/s10858-023-00416-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10858-023-00416-5

Keywords

Search

Navigation