Proton-detected 15N-1H dipolar coupling/1H chemical shift correlation experiment for the measurement of NH distances in biological solids under fast MAS solid-state NMR

Nehra, Ekta; Sehrawat, Neelam; Kobayashi, Takeshi; Nishiyama, Yusuke; Pandey, Manoj Kumar

doi:10.1016/j.jmro.2021.100028

Title: Proton-detected ¹⁵N-₁H dipolar coupling/₁H chemical shift correlation experiment for the measurement of NH distances in biological solids under fast MAS solid-state NMR

Journal Article · Tue Dec 28 00:00:00 EST 2021 · Journal of Magnetic Resonance Open

DOI:https://doi.org/10.1016/j.jmro.2021.100028· OSTI ID:1837758

Nehra, Ekta ^[1]; Sehrawat, Neelam ^[1]; Kobayashi, Takeshi ^[2]; Nishiyama, Yusuke ^[3]; Pandey, Manoj Kumar ^[1]

Indian Inst. of Technology (IIT), Rupnagar (India)
Ames Lab., and Iowa State Univ., Ames, IA (United States)
Institute of Physical and Chemical Research (RIKEN), Yokohama (Japan). RIKEN-JEOL Collaboration Center; JEOL RESONANCE Inc., Tokyo (Japan)

Measurement of distances from dipolar couplings is essential for structural characterization, refinement and validation using the solid-state nuclear magnetic resonance (ssNMR) spectroscopy. Particularly, knowledge about NH dipolar interactions in biological solids is important for understanding the hydrogen (H)-bonding interactions, molecular geometry and spin dynamics. In this regard, we have proposed a proton-detected two-dimensional (2D) ¹⁵N-¹H dipolar coupling/¹H chemical shift correlation experiment using the C-symmetry based windowless recoupling of chemical shift anisotropy (ROCSA) in combination with the DIPSHIFT pulse-based method for the measurement of short NH distances in the isotopically labeled and naturally abundant biological solids at fast magic angle spinning (MAS) rates (40–70 kHz). Our proposed method results in undistorted recoupled ¹⁵N-¹H dipolar coupling powder lineshapes that are free from the recoupled ¹H CSA contributions under the ¹⁵N evolution, a feature that is essential for the measurement of NH distances with improved accuracy (± 500 Hz in terms of the NH dipolar couplings). The pulse sequence developed in the present study is also insensitive to the 1H–1H homonuclear dipolar interactions, relaxation effects owing to its constant-time implementation, and t1-noise from the fluctuations in the MAS.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Ames Lab., Ames, IA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Materials Sciences & Engineering Division; JSPS KAKENHI; Science and Engineering Research Board (SERB)

Grant/Contract Number:: AC02-07CH11358; ECR/2017/000713; 20K05483; JPMJMI17A2

OSTI ID:: 1837758

Report Number(s):: IS-J-10,681

Journal Information:: Journal of Magnetic Resonance Open, Vol. 10-11; ISSN 2666-4410

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (59)

Solid-State NMR of a Paramagnetic DIAD-Fe ^II Catalyst: Sensitivity, Resolution Enhancement, and Structure-Based Assignments Kervern, Gwendal; Pintacuda, Guido; Zhang, Yong Journal of the American Chemical Society, Vol. 128, Issue 41 https://doi.org/10.1021/ja063510n	journal	October 2006
Rotary Resonance Recoupling in Heteronuclear Spin Pair Systems Levitt, Malcolm H.; Oas, Terrence G.; Griffin, Robert G. Israel Journal of Chemistry, Vol. 28, Issue 4 https://doi.org/10.1002/ijch.198800039	journal	January 1988
Heteronuclear dipolar modulated chemical shift spectra for geometrical information in polycrystalline solids Stoll, M. E.; Vega, A. J.; Vaughan, R. W. The Journal of Chemical Physics, Vol. 65, Issue 10 https://doi.org/10.1063/1.432863	journal	November 1976
Improving dipolar recoupling for site-specific structural and dynamics studies in biosolids NMR: windowed RN-symmetry sequences Lu, Xingyu; Zhang, Huilan; Lu, Manman Physical Chemistry Chemical Physics, Vol. 18, Issue 5 https://doi.org/10.1039/C5CP07818K	journal	January 2016
Measurement of 13C–1H dipolar couplings in solids by using ultra-fast magic-angle spinning NMR spectroscopy with symmetry-based sequences Wang, Qiang; Lu, Xingyu; Lafon, Olivier Physical Chemistry Chemical Physics, Vol. 13, Issue 13 https://doi.org/10.1039/c0cp01907k	journal	January 2011
Magic angle spinning NMR methods for internuclear distance measurements Smith, Steven O. Current Opinion in Structural Biology, Vol. 3, Issue 5 https://doi.org/10.1016/0959-440X(93)90060-X	journal	October 1993
Detailed analysis of the S-RESPDOR solid-state NMR method for inter-nuclear distance measurement between spin-1/2 and quadrupolar nuclei Lu, Xingyu; Lafon, Olivier; Trébosc, Julien Journal of Magnetic Resonance, Vol. 215 https://doi.org/10.1016/j.jmr.2011.12.009	journal	February 2012
Composite-180° pulse-based symmetry sequences to recouple proton chemical shift anisotropy tensors under ultrafast MAS solid-state NMR spectroscopy Pandey, Manoj Kumar; Malon, Michal; Ramamoorthy, Ayyalusamy Journal of Magnetic Resonance, Vol. 250 https://doi.org/10.1016/j.jmr.2014.11.002	journal	January 2015
Sensitivity and Resolution Enhanced Solid-State NMR for Paramagnetic Systems and Biomolecules under Very Fast Magic Angle Spinning Parthasarathy, Sudhakar; Nishiyama, Yusuke; Ishii, Yoshitaka Accounts of Chemical Research, Vol. 46, Issue 9 https://doi.org/10.1021/ar4000482	journal	June 2013
¹ H– ¹³ C/ ¹ H– ¹⁵ N Heteronuclear Dipolar Recoupling by R-Symmetry Sequences Under Fast Magic Angle Spinning for Dynamics Analysis of Biological and Organic Solids Hou, Guangjin; Byeon, In-Ja L.; Ahn, Jinwoo Journal of the American Chemical Society, Vol. 133, Issue 46 https://doi.org/10.1021/ja203771a	journal	November 2011
Structure Solution of Nano-Crystalline Small Molecules Using MicroED and Solid-State NMR Dipolar-Based Experiments Duong, Nghia Tuan; Aoyama, Yoshitaka; Kawamoto, Katsumi Molecules, Vol. 26, Issue 15 https://doi.org/10.3390/molecules26154652	journal	July 2021
NMR in rotating solids Maricq, M. Matti; Waugh, J. S. The Journal of Chemical Physics, Vol. 70, Issue 7 https://doi.org/10.1063/1.437915	journal	April 1979
Cross polarization under fast magic angle spinning: thermodynamical considerations Meier, B. H. Chemical Physics Letters, Vol. 188, Issue 3-4 https://doi.org/10.1016/0009-2614(92)90009-C	journal	January 1992
Neutron diffraction study of L-histidine hydrochloride monohydrate Fuess, H.; Hohlwein, D.; Mason, S. A. Acta Crystallographica Section B Structural Crystallography and Crystal Chemistry, Vol. 33, Issue 3 https://doi.org/10.1107/S0567740877004415	journal	March 1977
Magnitudes and Orientations of the Principal Elements of the ¹ H Chemical Shift, ¹ H− ¹⁵ N Dipolar Coupling, and ¹⁵ N Chemical Shift Interaction Tensors in ¹⁵ N _ε1 -Tryptophan and ¹⁵ N _π -Histidine Side Chains Determined by Three-Dimensional Solid-State NMR Spectroscopy of Polycrystalline Samples Ramamoorthy, A.; Wu, C. H.; Opella, S. J. Journal of the American Chemical Society, Vol. 119, Issue 43 https://doi.org/10.1021/ja9632670	journal	October 1997
Two-dimensional rotational spin-echo nuclear magnetic resonance in solids: correlation of chemical shift and dipolar interactions Munowitz, M. G.; Griffin, R. G.; Bodenhausen, G. Journal of the American Chemical Society, Vol. 103, Issue 10 https://doi.org/10.1021/ja00400a007	journal	May 1981
Recoupling of chemical shift anisotropies in solid-state NMR under high-speed magic-angle spinning and in uniformly 13C-labeled systems Chan, Jerry C. C.; Tycko, Robert The Journal of Chemical Physics, Vol. 118, Issue 18 https://doi.org/10.1063/1.1565109	journal	May 2003
Two‐dimensional nuclear magnetic resonance in rotating solids: Time reversal effects in chemical shift‐dipolar spectra Munowitz, M. G.; Griffin, R. G. The Journal of Chemical Physics, Vol. 78, Issue 2 https://doi.org/10.1063/1.444816	journal	January 1983
REPULSION, A Novel Approach to Efficient Powder Averaging in Solid-State NMR Bak, Mads; Nielsen, Niels Chr Journal of Magnetic Resonance, Vol. 125, Issue 1 https://doi.org/10.1006/jmre.1996.1087	journal	March 1997
Protein NMR Spectroscopy at 150 kHz Magic‐Angle Spinning Continues To Improve Resolution and Mass Sensitivity Schledorn, Maarten; Malär, Alexander A.; Torosyan, Anahit ChemBioChem, Vol. 21, Issue 17 https://doi.org/10.1002/cbic.202000341	journal	July 2020
Unraveling multi-spin effects in rotational resonance nuclear magnetic resonance using effective reduced density matrix theory SivaRanjan, Uppala; Ramachandran, Ramesh The Journal of Chemical Physics, Vol. 140, Issue 5 https://doi.org/10.1063/1.4863212	journal	February 2014
Coherent Averaging Effects in Magnetic Resonance Haeberlen, U.; Waugh, J. S. Physical Review, Vol. 175, Issue 2 https://doi.org/10.1103/PhysRev.175.453	journal	November 1968
Intermediate motions as studied by solid-state separated local field NMR experiments deAzevedo, Eduardo Ribeiro; Saalwachter, Kay; Pascui, Ovidiu The Journal of Chemical Physics, Vol. 128, Issue 10 https://doi.org/10.1063/1.2831798	journal	March 2008
Proton-detected 3D 1H anisotropic/14N/1H isotropic chemical shifts correlation NMR under fast magic angle spinning on solid samples without isotopic enrichment Pandey, Manoj Kumar; Damron, Joshua T.; Ramamoorthy, Ayyalusamy Solid State Nuclear Magnetic Resonance, Vol. 97 https://doi.org/10.1016/j.ssnmr.2018.12.002	journal	February 2019
De Novo 3D Structure Determination from Sub-milligram Protein Samples by Solid-State 100 kHz MAS NMR Spectroscopy Agarwal, Vipin; Penzel, Susanne; Szekely, Kathrin Angewandte Chemie International Edition, Vol. 53, Issue 45 https://doi.org/10.1002/anie.201405730	journal	September 2014
Quantitative ¹ H– ¹ H Distances in Protonated Solids by Frequency-Selective Recoupling at Fast Magic Angle Spinning NMR Duong, Nghia Tuan; Raran-Kurussi, Sreejith; Nishiyama, Yusuke The Journal of Physical Chemistry Letters, Vol. 9, Issue 20 https://doi.org/10.1021/acs.jpclett.8b02189	journal	September 2018
Progress in proton-detected solid-state NMR (SSNMR): Super-fast 2D SSNMR collection for nano-mole-scale proteins Ishii, Yoshitaka; Wickramasinghe, Ayesha; Matsuda, Isamu Journal of Magnetic Resonance, Vol. 286 https://doi.org/10.1016/j.jmr.2017.11.011	journal	January 2018
Theoretical study of CP-VC: A simple, robust and accurate MAS NMR method for analysis of dipolar C–H interactions under rotation speeds faster than ca. 60kHz Paluch, P.; Trébosc, J.; Nishiyama, Y. Journal of Magnetic Resonance, Vol. 252 https://doi.org/10.1016/j.jmr.2015.01.002	journal	March 2015
Fast magic-angle sample spinning solid-state NMR at 60–100 kHz for natural abundance samples Nishiyama, Yusuke Solid State Nuclear Magnetic Resonance, Vol. 78 https://doi.org/10.1016/j.ssnmr.2016.06.002	journal	September 2016
Computer-intensive simulation of solid-state NMR experiments using SIMPSON Tošner, Zdeněk; Andersen, Rasmus; Stevensson, Baltzar Journal of Magnetic Resonance, Vol. 246 https://doi.org/10.1016/j.jmr.2014.07.002	journal	September 2014
13C- and 1H-detection under fast MAS for the study of poorly available proteins: application to sub-milligram quantities of a 7 trans-membrane protein Dannatt, Hugh R. W.; Taylor, Garrick F.; Varga, Krisztina Journal of Biomolecular NMR, Vol. 62, Issue 1 https://doi.org/10.1007/s10858-015-9911-1	journal	February 2015
Recent progress in dipolar recoupling techniques under fast MAS in solid-state NMR spectroscopy Ji, Yi; Liang, Lixin; Bao, Xinhe Solid State Nuclear Magnetic Resonance, Vol. 112 https://doi.org/10.1016/j.ssnmr.2020.101711	journal	April 2021
Accurate measurement of heteronuclear dipolar couplings by phase-alternating R-symmetry (PARS) sequences in magic angle spinning NMR spectroscopy Hou, Guangjin; Lu, Xingyu; Vega, Alexander J. The Journal of Chemical Physics, Vol. 141, Issue 10 https://doi.org/10.1063/1.4894226	journal	September 2014
Dipolar Recoupling in Magic Angle Spinning Solid-State Nuclear Magnetic Resonance De Paëpe, Gaël Annual Review of Physical Chemistry, Vol. 63, Issue 1 https://doi.org/10.1146/annurev-physchem-032511-143726	journal	May 2012
Accurate heteronuclear distance measurements at all magic-angle spinning frequencies in solid-state NMR spectroscopy Liang, Lixin; Ji, Yi; Zhao, Zhenchao Chemical Science, Vol. 12, Issue 34 https://doi.org/10.1039/D1SC03194E	journal	January 2021
Broadband dipolar recoupling in rotating solids: a numerical comparison of some pulse schemes Baldus, M.; Geurts, D. G.; Meier, B. H. Solid State Nuclear Magnetic Resonance, Vol. 11, Issue 3-4 https://doi.org/10.1016/S0926-2040(98)00036-8	journal	June 1998
Measurement of hetero-nuclear distances using a symmetry-based pulse sequence in solid-state NMR Chen, Lei; Wang, Qiang; Hu, Bingwen Physical Chemistry Chemical Physics, Vol. 12, Issue 32 https://doi.org/10.1039/b926546e	journal	January 2010
SIMPSON: A General Simulation Program for Solid-State NMR Spectroscopy Bak, Mads; Rasmussen, Jimmy T.; Nielsen, Niels Chr Journal of Magnetic Resonance, Vol. 147, Issue 2 https://doi.org/10.1006/jmre.2000.2179	journal	December 2000
Dipolar Recoupling in MAS NMR: A Probe for Segmental Order in Lipid Bilayers Gross, John D.; Warschawski, Dror E.; Griffin, Robert G. Journal of the American Chemical Society, Vol. 119, Issue 4 https://doi.org/10.1021/ja962951b	journal	January 1997
Is protein deuteration beneficial for proton detected solid-state NMR at and above 100 kHz magic-angle spinning? Cala-De Paepe, Diane; Stanek, Jan; Jaudzems, Kristaps Solid State Nuclear Magnetic Resonance, Vol. 87 https://doi.org/10.1016/j.ssnmr.2017.07.004	journal	October 2017
Accurate 1H-14N distance measurements by phase-modulated RESPDOR at ultra-fast MAS Duong, Nghia Tuan; Rossi, Federica; Makrinich, Maria Journal of Magnetic Resonance, Vol. 308 https://doi.org/10.1016/j.jmr.2019.07.046	journal	November 2019
Selective 1H-14N Distance Measurements by 14N Overtone Solid-State NMR Spectroscopy at Fast MAS Duong, Nghia Tuan; Gan, Zhehong; Nishiyama, Yusuke Frontiers in Molecular Biosciences, Vol. 8 https://doi.org/10.3389/fmolb.2021.645347	journal	April 2021
Measurements of motionally averaged heteronuclear dipolar couplings in MAS NMR using R-type recoupling Dvinskikh, Sergey V.; Zimmermann, Herbert; Maliniak, Arnold Journal of Magnetic Resonance, Vol. 168, Issue 2 https://doi.org/10.1016/j.jmr.2004.03.001	journal	June 2004
Proton-Detected Solid-State NMR Spectroscopy at Aliphatic Sites: Application to Crystalline Systems Asami, Sam; Reif, Bernd Accounts of Chemical Research, Vol. 46, Issue 9 https://doi.org/10.1021/ar400063y	journal	June 2013
Homonuclear radio frequency-driven recoupling in rotating solids Bennett, Andrew E.; Rienstra, Chad M.; Griffiths, Janet M. The Journal of Chemical Physics, Vol. 108, Issue 22 https://doi.org/10.1063/1.476420	journal	June 1998
Accurate NMR determination of C–H or N–H distances for unlabeled molecules Nishiyama, Y.; Malon, M.; Potrzebowski, M. J. Solid State Nuclear Magnetic Resonance, Vol. 73 https://doi.org/10.1016/j.ssnmr.2015.06.005	journal	February 2016
Measuring proton shift tensors with ultrafast MAS NMR Miah, Habeeba K.; Bennett, David A.; Iuga, Dinu Journal of Magnetic Resonance, Vol. 235 https://doi.org/10.1016/j.jmr.2013.07.005	journal	October 2013
Dipolar recoupling in MAS spectra of biological solids Griffin, Robert Nature Structural Biology, Vol. 5, Issue 7 https://doi.org/10.1038/749	journal	July 1998
Determination of the chemical shift tensor anisotropy and asymmetry of strongly dipolar coupled protons under fast MAS Kobayashi, Takeshi; Perras, Frédéric A.; Nishiyama, Yusuke Solid State Nuclear Magnetic Resonance, Vol. 114 https://doi.org/10.1016/j.ssnmr.2021.101743	journal	August 2021
Free Induction Decays of Rotating Solids Lowe, I. J. Physical Review Letters, Vol. 2, Issue 7, p. 285-287 https://doi.org/10.1103/PhysRevLett.2.285	journal	April 1959
Separated Local Field Spectra in NMR: Determination of Structure of Solids Hester, R. K.; Ackerman, J. L.; Neff, B. L. Physical Review Letters, Vol. 36, Issue 18 https://doi.org/10.1103/PhysRevLett.36.1081	journal	May 1976
Multidimensional Magic Angle Spinning NMR Spectroscopy for Site-Resolved Measurement of Proton Chemical Shift Anisotropy in Biological Solids Hou, Guangjin; Paramasivam, Sivakumar; Yan, Si Journal of the American Chemical Society, Vol. 135, Issue 4 https://doi.org/10.1021/ja3084972	journal	January 2013
Removal of Dipolar Broadening of Nuclear Magnetic Resonance Spectra of Solids by Specimen Rotation Andrew, E. R.; Bradbury, A.; Eades, R. G. Nature, Vol. 183, Issue 4678 https://doi.org/10.1038/1831802a0	journal	June 1959
Molecular Characterization of Hexaoctyloxy-Rufigallol in the Solid and Columnar Phases: A Local Field NMR Study Dvinskikh, Sergey V.; Luz, Zeev; Zimmermann, Herbert The Journal of Physical Chemistry B, Vol. 107, Issue 9 https://doi.org/10.1021/jp0274381	journal	February 2003
Applications of NMR to membrane proteins Opella, Stanley J.; Marassi, Francesca M. Archives of Biochemistry and Biophysics, Vol. 628 https://doi.org/10.1016/j.abb.2017.05.011	journal	August 2017
Theory and simulation of vibrational effects on structural measurements by solid-state nuclear magnetic resonance Ishii, Yoshitaka; Terao, Takehiko; Hayashi, Soichi The Journal of Chemical Physics, Vol. 107, Issue 8 https://doi.org/10.1063/1.474633	journal	August 1997
Proton-Detected Solid-State NMR Spectroscopy of Fully Protonated Proteins at 40 kHz Magic-Angle Spinning Zhou, Donghua H.; Shah, Gautam; Cormos, Mircea Journal of the American Chemical Society, Vol. 129, Issue 38 https://doi.org/10.1021/ja073462m	journal	September 2007
Recoupling of heteronuclear dipolar interactions in solid-state NMR using symmetry-based pulse sequences Zhao, Xin; Edén, Mattias; Levitt, Malcolm H. Chemical Physics Letters, Vol. 342, Issue 3-4 https://doi.org/10.1016/S0009-2614(01)00593-0	journal	July 2001
Simple and accurate determination of X–H distances under ultra-fast MAS NMR Paluch, Piotr; Pawlak, Tomasz; Amoureux, Jean-Paul Journal of Magnetic Resonance, Vol. 233 https://doi.org/10.1016/j.jmr.2013.05.005	journal	August 2013

Similar Records

Determination of the relative orientation between ¹⁵N-¹H dipolar coupling and ¹H chemical shift anisotropy tensors under fast MAS solid-state NMR

Journal Article · Wed Mar 29 00:00:00 EDT 2023 · Journal of Magnetic Resonance · OSTI ID:1837758

Sehrawat, Neelam; Nehra, Ekta; Kumar Rohilla, Ketan; +3 more

Accurate measurement of heteronuclear dipolar couplings by phase-alternating R-symmetry (PARS) sequences in magic angle spinning NMR spectroscopy

Journal Article · Sun Sep 14 00:00:00 EDT 2014 · Journal of Chemical Physics · OSTI ID:1837758

Hou, Guangjin; Lu, Xingyu; Polenova, Tatyana

Determination of statherin N-terminal peptide conformation on hydroxyapatite crystals

Journal Article · Wed Mar 01 00:00:00 EST 2000 · Journal of the American Chemical Society · OSTI ID:1837758

Shaw, W J; Long, J R; Dindot, J L; +3 more

Related Subjects

72 PHYSICS OF ELEMENTARY PARTICLES AND FIELDS
Solid-state NMR
ROCSA
DIPSHIFT
Dipolar couplings
Fast MAS

Title: Proton-detected 15N-1H dipolar coupling/1H chemical shift correlation experiment for the measurement of NH distances in biological solids under fast MAS solid-state NMR

Citation Formats

References (59)

Similar Records

Related Subjects

Title: Proton-detected ¹⁵N-₁H dipolar coupling/₁H chemical shift correlation experiment for the measurement of NH distances in biological solids under fast MAS solid-state NMR