Home / Publications / Parahydrogen-based NMR signal amplification by reversible exchange (SABRE): Recent advances and applications

Parahydrogen-based NMR signal amplification by reversible exchange (SABRE): Recent advances and applications

Oleg Georgievich Salnikov 1
Oleg Georgievich Salnikov
, 
Dudari Bairovna Burueva 1
Dudari Bairovna Burueva
, 
Ivan Vladimirovich Skovpin 1
Ivan Vladimirovich Skovpin
, 
Igor Valentinovich Koptyug 1
Igor Valentinovich Koptyug
1 International Tomography Center, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russian Federation
10.1016/j.mencom.2023.09.001
Published 2023-09-01
Communication , Volume 33, Issue 5, 583-596
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Salnikov O. G. et al. Parahydrogen-based NMR signal amplification by reversible exchange (SABRE): Recent advances and applications // Mendeleev Communications. 2023. Vol. 33. No. 5. pp. 583-596.
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Salnikov O. G., Burueva D. B., Skovpin I. V., Koptyug I. V. Parahydrogen-based NMR signal amplification by reversible exchange (SABRE): Recent advances and applications // Mendeleev Communications. 2023. Vol. 33. No. 5. pp. 583-596.
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TY - JOUR
DO - 10.1016/j.mencom.2023.09.001
UR - https://mendcomm.colab.ws/publications/10.1016/j.mencom.2023.09.001
TI - Parahydrogen-based NMR signal amplification by reversible exchange (SABRE): Recent advances and applications
T2 - Mendeleev Communications
AU - Salnikov, Oleg Georgievich
AU - Burueva, Dudari Bairovna
AU - Skovpin, Ivan Vladimirovich
AU - Koptyug, Igor Valentinovich
PY - 2023
DA - 2023/09/01
PB - Mendeleev Communications
SP - 583-596
IS - 5
VL - 33
ER -
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@article{2023_Salnikov,
author = {Oleg Georgievich Salnikov and Dudari Bairovna Burueva and Ivan Vladimirovich Skovpin and Igor Valentinovich Koptyug},
title = {Parahydrogen-based NMR signal amplification by reversible exchange (SABRE): Recent advances and applications},
journal = {Mendeleev Communications},
year = {2023},
volume = {33},
publisher = {Mendeleev Communications},
month = {Sep},
url = {https://mendcomm.colab.ws/publications/10.1016/j.mencom.2023.09.001},
number = {5},
pages = {583--596},
doi = {10.1016/j.mencom.2023.09.001}
}
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Salnikov, Oleg Georgievich, et al. “Parahydrogen-based NMR signal amplification by reversible exchange (SABRE): Recent advances and applications.” Mendeleev Communications, vol. 33, no. 5, Sep. 2023, pp. 583-596. https://mendcomm.colab.ws/publications/10.1016/j.mencom.2023.09.001.

Keywords

hyperpolarization
magnetic resonance.
NMR spectroscopy
parahydrogen
SABRE

Abstract

Signal amplification by reversible exchange (SABRE) is a rapidly developing nuclear magnetic resonance (NMR) hyperpolarization technique utilizing parahydrogen for dramatic increase of NMR sensitivity to benefit its biomedical and analytic applications. This mini-review covers the most important methodological advances of SABRE with the focus on recent developments. We discuss the mechanistic aspects of SABRE effects, hyperpolarization of protons and heteronuclei including the novel SABRE-Relay approach, the ongoing work to make SABRE biocompatible, the analytical applications, the advances in instrumentation and, finally, more exotic developments such as the low-field detection of SABRE and the SABRE-initiated radiofrequency amplification by stimulated emission of radiation (RASER) effects.

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Ligand effects of NHC–iridium catalysts for signal amplification by reversible exchange (SABRE)
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Catalysis Science and Technology, 2014
.
Transfer of SABRE-derived hyperpolarization to spin-1/2 heteronuclei
Pravdivtsev A.N., Yurkovskaya A.V., Zimmermann H., Vieth H., Ivanov K.L.
RSC Advances, 2015
.
NMR detection in biofluid extracts at sub-μM concentrations via para-H2 induced hyperpolarization
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The Analyst, 2016
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Quantitative description of the SABRE process: rigorous consideration of spin dynamics and chemical exchange
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Using signal amplification by reversible exchange (SABRE) to hyperpolarise 119Sn and 29Si NMR nuclei
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Chemical Communications, 2016
.
SABRE hyperpolarisation of vitamin B3 as a function of pH
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Chemical Science, 2017
.
Direct and indirect hyperpolarisation of amines using parahydrogen
Iali W., Rayner P.J., Alshehri A., Holmes A.J., Ruddlesden A.J., Duckett S.B.
Chemical Science, 2018
.
Parahydrogen induced hyperpolarization provides a tool for NMR metabolomics at nanomolar concentrations
Sellies L., Reile I., Aspers R.L., Feiters M.C., Rutjes F.P., Tessari M.
Chemical Communications, 2019
.
Relayed hyperpolarization from para-hydrogen improves the NMR detectability of alcohols
Rayner P.J., Tickner B.J., Iali W., Fekete M., Robinson A.D., Duckett S.B.
Chemical Science, 2019
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Rapid13C NMR hyperpolarization delivered frompara-hydrogen enables the low concentration detection and quantification of sugars
Richardson P.M., Iali W., Roy S.S., Rayner P.J., Halse M.E., Duckett S.B.
Chemical Science, 2019
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Understanding substrate substituent effects to improve catalytic efficiency in the SABRE hyperpolarisation process
Stanbury E.V., Richardson P.M., Duckett S.B.
Catalysis Science and Technology, 2019
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Parahydrogen based NMR hyperpolarisation goes micro: an alveolus for small molecule chemosensing
Bordonali L., Nordin N., Fuhrer E., MacKinnon N., Korvink J.G.
Lab on a Chip, 2019
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Quantifying the effects of quadrupolar sinks via15N relaxation dynamics in metronidazoles hyperpolarized via SABRE-SHEATH
Birchall J.R., Kabir M.S., Salnikov O.G., Chukanov N.V., Svyatova A., Kovtunov K.V., Koptyug I.V., Gelovani J.G., Goodson B.M., Pham W., Chekmenev E.Y.
Chemical Communications, 2020
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Characterization of protein–ligand interactions by SABRE
Mandal R., Pham P., Hilty C.
Chemical Science, 2021
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SABRE enhancement with oscillating pulse sequences
Li X., Lindale J.R., Eriksson S.L., Warren W.S.
Physical Chemistry Chemical Physics, 2022
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Tuning of pH enables carbon-13 hyperpolarization of oxalates by SABRE
Roy S.S., Iali W., Moustafa G.A., Levitt M.H.
Chemical Communications, 2022
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Recent advances in the application of parahydrogen in catalysis and biochemistry
Buntkowsky G., Theiss F., Lins J., Miloslavina Y.A., Wienands L., Kiryutin A., Yurkovskaya A.
RSC Advances, 2022
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Micron-Scale NV-NMR Spectroscopy with Signal Amplification by Reversible Exchange
Arunkumar N., Bucher D.B., Turner M.J., TomHon P., Glenn D., Lehmkuhl S., Lukin M.D., Park H., Rosen M.S., Theis T., Walsworth R.L.
PRX Quantum, 2021
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NMR Imaging of Catalytic Hydrogenation in Microreactors with the Use of para-Hydrogen
Bouchard L., Burt S.R., Anwar M.S., Kovtunov K.V., Koptyug I.V., Pines A.
Science, 2008
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Infinite-order perturbative treatment for quantum evolution with exchange
Lindale J.R., Eriksson S.L., Tanner C.P., Warren W.S.
Science advances, 2020
.
Relayed hyperpolarization for zero-field nuclear magnetic resonance
Van Dyke E.T., Eills J., Picazo-Frutos R., Sheberstov K.F., Hu Y., Budker D., Barskiy D.A.
Science advances, 2022
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RASER MRI: Magnetic resonance images formed spontaneously exploiting cooperative nonlinear interaction
Lehmkuhl S., Fleischer S., Lohmann L., Rosen M.S., Chekmenev E.Y., Adams A., Theis T., Appelt S.
Science advances, 2022
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Direct and cost-efficient hyperpolarization of long-lived nuclear spin states on universal 15 N 2 -diazirine molecular tags
Theis T., Ortiz G.X., Logan A.W., Claytor K.E., Feng Y., Huhn W.P., Blum V., Malcolmson S.J., Chekmenev E.Y., Wang Q., Warren W.S.
Science advances, 2016
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Delivering strong 1 H nuclear hyperpolarization levels and long magnetic lifetimes through signal amplification by reversible exchange
Rayner P.J., Burns M.J., Olaru A.M., Norcott P., Fekete M., Green G.G., Highton L.A., Mewis R.E., Duckett S.B.
Proceedings of the National Academy of Sciences of the United States of America, 2017
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Catalyst-Free Aqueous Hyperpolarized [1-13C]Pyruvate Obtained by Re-Dissolution Signal Amplification by Reversible Exchange
Schmidt A.B., de Maissin H., Adelabu I., Nantogma S., Ettedgui J., TomHon P., Goodson B.M., Theis T., Chekmenev E.Y.
ACS Sensors, 2022
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Hyperpolarization via dissolution dynamic nuclear polarization: new technological and methodological advances
Pinon A.C., Capozzi A., Ardenkjær-Larsen J.H.
Magnetic Resonance Materials in Physics, Biology, and Medicine, 2020
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Unveiling coherently driven hyperpolarization dynamics in signal amplification by reversible exchange
Lindale J.R., Eriksson S.L., Tanner C.P., Zhou Z., Colell J.F., Zhang G., Bae J., Chekmenev E.Y., Theis T., Warren W.S.
Nature Communications, 2019
.
Para-hydrogen raser delivers sub-millihertz resolution in nuclear magnetic resonance
Suefke M., Lehmkuhl S., Liebisch A., Blümich B., Appelt S.
Nature Physics, 2017
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SQUID-based detection of ultra-low-field multinuclear NMR of substances hyperpolarized using signal amplification by reversible exchange
Buckenmaier K., Rudolph M., Back C., Misztal T., Bommerich U., Fehling P., Koelle D., Kleiner R., Mayer H.A., Scheffler K., Bernarding J., Plaumann M.
Scientific Reports, 2017
.
Proton-Only Sensing of Hyperpolarized [1,2-13C2]Pyruvate
Mandzhieva I., Adelabu I., Chekmenev E.Y., Theis T.
ACS Sensors, 2022
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A theoretical basis for spontaneous polarization transfer in non-hydrogenative parahydrogen-induced polarization.
Adams R.W., Duckett S.B., Green R.A., Williamson D.C., Green G.G.
Journal of Chemical Physics, 2009
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Heterogeneous solution NMR signal amplification by reversible exchange.
Shi F., Coffey A.M., Waddell K.W., Chekmenev E.Y., Goodson B.M.
Angewandte Chemie - International Edition, 2014
.
Spin polarization transfer mechanisms of SABRE: A magnetic field dependent study.
Pravdivtsev A.N., Ivanov K.L., Yurkovskaya A.V., Petrov P.A., Limbach H., Kaptein R., Vieth H.
Journal of Magnetic Resonance, 2015
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Interplay of Near-Zero-Field Dephasing, Rephasing, and Relaxation Dynamics and [1-13C]Pyruvate Polarization Transfer Efficiency in Pulsed SABRE-SHEATH
Nantogma S., Eriksson S.L., Adelabu I., Mandzhieva I., Browning A., TomHon P., Warren W.S., Theis T., Goodson B.M., Chekmenev E.Y.
Journal of Physical Chemistry A, 2022
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External high-quality-factor resonator tunes up nuclear magnetic resonance
Suefke M., Liebisch A., Blümich B., Appelt S.
Nature Physics, 2015
.
Analysis of the SABRE (Signal Amplification by Reversible Exchange) Effect at High Magnetic Fields
Pravdivtsev A.N., Yurkovskaya A.V., Petrov P.A., Vieth H., Ivanov K.L.
Applied Magnetic Resonance, 2016
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Selective hyperpolarization of heteronuclear singlet states via pulsed microtesla SABRE
Tanner C.P., Lindale J.R., Eriksson S.L., Zhou Z., Colell J.F., Theis T., Warren W.S.
Journal of Chemical Physics, 2019
.
Theoretical description of hyperpolarization formation in the SABRE-relay method
Knecht S., Barskiy D.A., Buntkowsky G., Ivanov K.L.
Journal of Chemical Physics, 2020
.
SABRE polarized low field rare-spin spectroscopy
Lehmkuhl S., Suefke M., Kentner A., Yen Y., Blümich B., Rosen M.S., Appelt S., Theis T.
Journal of Chemical Physics, 2020
.
Subsecond Three-Dimensional Nitrogen-15 Magnetic Resonance Imaging Facilitated by Parahydrogen-Based Hyperpolarization
Trepakova A.I., Skovpin I.V., Chukanov N.V., Salnikov O.G., Chekmenev E.Y., Pravdivtsev A.N., Hövener J., Koptyug I.V.
Journal of Physical Chemistry Letters, 2022
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Characterization of Microfluidic Gas Reactors Using Remote-Detection MRI and Parahydrogen-Induced Polarization
Zhivonitko V.V., Telkki V., Koptyug I.V.
Angewandte Chemie - International Edition, 2012
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NMR Discrimination of d- and l-α-Amino Acids at Submicromolar Concentration via Parahydrogen-Induced Hyperpolarization
Dreisewerd L., Aspers R.L., Feiters M.C., Rutjes F.P., Tessari M.
Journal of the American Chemical Society, 2023
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Probing signal amplification by reversible exchange using an NMR flow system
Mewis R.E., Atkinson K.D., Cowley M.J., Duckett S.B., Green G.G., Green R.A., Highton L.A., Kilgour D., Lloyd L.S., Lohman J.A., Williamson D.C.
Magnetic Resonance in Chemistry, 2014
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Quantitative Trace Analysis of Complex Mixtures Using SABRE Hyperpolarization
Eshuis N., van Weerdenburg B.J., Feiters M.C., Rutjes F.P., Wijmenga S.S., Tessari M.
Angewandte Chemie - International Edition, 2014
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In Situ and Ex Situ Low-Field NMR Spectroscopy and MRI Endowed by SABRE Hyperpolarization
Barskiy D.A., Kovtunov K.V., Koptyug I.V., He P., Groome K.A., Best Q.A., Shi F., Goodson B.M., Shchepin R.V., Truong M.L., Coffey A.M., Waddell K.W., Chekmenev E.Y.
ChemPhysChem, 2014
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Parahydrogen-induced polarization in imaging: Subsecond13C angiography
Golman K., Axelsson O., Jóhannesson H., Månsson S., Olofsson C., Petersson J.S.
Magnetic Resonance in Medicine, 2001
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LIGHT-SABRE enables efficient in-magnet catalytic hyperpolarization
Theis T., Truong M., Coffey A.M., Chekmenev E.Y., Warren W.S.
Journal of Magnetic Resonance, 2014
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Spin Hyperpolarization in Modern Magnetic Resonance
Eills J., Budker D., Cavagnero S., Chekmenev E.Y., Elliott S.J., Jannin S., Lesage A., Matysik J., Meersmann T., Prisner T., Reimer J.A., Yang H., Koptyug I.V.
Chemical Reviews, 2023
.
Practical dissolution dynamic nuclear polarization
Elliott S.J., Stern Q., Ceillier M., El Daraï T., Cousin S.F., Cala O., Jannin S.
Progress in Nuclear Magnetic Resonance Spectroscopy, 2021
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An inexpensive apparatus for up to 97% continuous-flow parahydrogen enrichment using liquid helium
Du Y., Zhou R., Ferrer M., Chen M., Graham J., Malphurs B., Labbe G., Huang W., Bowers C.R.
Journal of Magnetic Resonance, 2020
.
Surface-Mediated Hyperpolarization of Liquid Water from Parahydrogen
Zhao E.W., Maligal-Ganesh R., Du Y., Zhao T.Y., Collins J., Ma T., Zhou L., Goh T., Huang W., Bowers C.R.
Chem, 2018
.
Towards large‐scale steady‐state enhanced nuclear magnetization with in situ detection
Blanchard J.W., Ripka B., Suslick B.A., Gelevski D., Wu T., Münnemann K., Barskiy D.A., Budker D.
Magnetic Resonance in Chemistry, 2021
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High-throughput continuous-flow system for SABRE hyperpolarization
Štěpánek P., Sanchez-Perez C., Telkki V., Zhivonitko V.V., Kantola A.M.
Journal of Magnetic Resonance, 2019
.
Hyperpolarized 13C MRI: Path to Clinical Translation in Oncology
Kurhanewicz J., Vigneron D.B., Ardenkjaer-Larsen J.H., Bankson J.A., Brindle K., Cunningham C.H., Gallagher F.A., Keshari K.R., Kjaer A., Laustsen C., Mankoff D.A., Merritt M.E., Nelson S.J., Pauly J.M., Lee P., et. al.
Neoplasia, 2019
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Optimization of SABRE for polarization of the tuberculosis drugs pyrazinamide and isoniazid
Zeng H., Xu J., Gillen J., McMahon M.T., Artemov D., Tyburn J., Lohman J.A., Mewis R.E., Atkinson K.D., Green G.G., Duckett S.B., van Zijl P.C.
Journal of Magnetic Resonance, 2013
.
Continuous hyperpolarization with parahydrogen in a membrane reactor
Lehmkuhl S., Wiese M., Schubert L., Held M., Küppers M., Wessling M., Blümich B.
Journal of Magnetic Resonance, 2018
.
From LASER physics to the para-hydrogen pumped RASER
Appelt S., Kentner A., Lehmkuhl S., Blümich B.
Progress in Nuclear Magnetic Resonance Spectroscopy, 2019
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Multiaxial fields improve SABRE efficiency by preserving hydride order
Eriksson S.L., Mammen M.W., Eriksson C.W., Lindale J.R., Warren W.S.
Journal of Magnetic Resonance, 2022
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parahydrogen Induced Polarization by Homogeneous Catalysis: Theory and Applications
Buljubasich L., Franzoni M.B., Münnemann K.
Topics in Current Chemistry, 2013
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SABRE Hyperpolarization with up to 200 bar Parahydrogen in Standard and Quickly Removable Solvents
Duchowny A., Denninger J., Lohmann L., Theis T., Lehmkuhl S., Adams A.
International Journal of Molecular Sciences, 2023
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Effect of the hydrogenation solvent in the PHIP-SAH hyperpolarization of [1-13C]pyruvate
Bondar O., Cavallari E., Carrera C., Aime S., Reineri F.
Catalysis Today, 2022
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Parahydrogen-Polarized Fumarate for Preclinical in Vivo Metabolic Magnetic Resonance Imaging
Gierse M., Nagel L., Keim M., Lucas S., Speidel T., Lobmeyer T., Winter G., Josten F., Karaali S., Fellermann M., Scheuer J., Müller C., van Heijster F., Skinner J., Löffler J., et. al.
Journal of the American Chemical Society, 2023
.
13 C and 15 N Benchtop NMR Detection of Metabolites via Relayed Hyperpolarization**
Alcicek S., Van Dyke E., Xu J., Pustelny S., Barskiy D.A.
Chemistry - Methods, 2023
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Parahydrogen in Reversible Exchange Induces Long-Lived 15N Hyperpolarization of Anticancer Drugs Anastrozole and Letrozole
MacCulloch K., Browning A., TomHon P., Lehmkuhl S., Chekmenev E.Y., Theis T.
Analytical Chemistry, 2023
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Efficient SABRE-SHEATH Hyperpolarization of Potent Branched-Chain-Amino-Acid Metabolic Probe [1-13C]ketoisocaproate
Adelabu I., Chowdhury M.R., Nantogma S., Oladun C., Ahmed F., Stilgenbauer L., Sadagurski M., Theis T., Goodson B.M., Chekmenev E.Y.
Metabolites, 2023
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Over 20% Carbon-13 Polarization of Perdeuterated Pyruvate Using Reversible Exchange with Parahydrogen and Spin-Lock Induced Crossing at 50 μT
Schmidt A.B., Eills J., Dagys L., Gierse M., Keim M., Lucas S., Bock M., Schwartz I., Zaitsev M., Chekmenev E.Y., Knecht S.
Journal of Physical Chemistry Letters, 2023
.
Detection of pyridine derivatives by SABRE hyperpolarization at zero field
Put P., Alcicek S., Bondar O., Bodek Ł., Duckett S., Pustelny S.
Communications Chemistry, 2023
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Hyperpolarisation of Mirfentanil by SABRE in the Presence of Heroin.
Robertson Thomas B R, Gilbert Nicolas, Sutcliffe Oliver B, Mewis Ryan E
ChemPhysChem