ACS Publications. Most Trusted. Most Cited. Most Read
My Activity
CONTENT TYPES

NMR-Based Biosensing with Optimized Delivery of Polarized 129Xe to Solutions

View Author Information
Material Sciences and Physical Biosciences Divisions, Lawrence Berkeley National Laboratory, and Howard Hughes Medical Institute, Department of Molecular and Cell Biology, University of California, Berkeley, California 94720
Cite this: Anal. Chem. 2005, 77, 13, 4008–4012
Publication Date (Web):May 18, 2005
https://doi.org/10.1021/ac0500479
Copyright © 2005 American Chemical Society

    Article Views

    456

    Altmetric

    -

    Citations

    LEARN ABOUT THESE METRICS
    Other access options

    Abstract

    Laser-enhanced (LE) 129Xe nuclear magnetic resonance (NMR) is an exceptional tool for sensing extremely small physical and chemical changes; however, the difficult mechanics of bringing polarized xenon and samples of interest together have limited applications, particularly to biological molecules. Here we present a method for accomplishing solution 129Xe biosensing based on flow (bubbling) of LE 129Xe gas through a solution in situ in the NMR probe, with pauses for data acquisition. This overcomes fundamental limitations of conventional solution-state LE 129Xe NMR, e.g., the difficulty in transferring hydrophobic xenon into aqueous environments, and the need to handle the sample to refresh LE 129Xe after an observation pulse depletes polarization. With this new method, we gained a factor of >100 in sensitivity due to improved xenon transfer to the solution and the ability to signal average by renewing the polarized xenon. Polarized xenon in biosensors was detected at very low concentrations, ≤250 nanomolar, while retaining all the usual information from NMR. This approach can be used to simultaneously detect multiple sensors with different chemical shifts and is also capable of detecting signals from opaque, heterogeneous samples, which is a unique advantage over optical methods. This general approach is adaptable for sensing minute quantities of xenon in heterogeneous in vitro samples, in miniaturized devices and should be applicable to certain in-vivo environments.

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. You can change your affiliated institution below.

    *

     To whom correspondence should be addressed. Current address:  Department of Chemistry and Biochemistry, University of California Santa Barbara, CA 93106-9510. Phone:  805 893 4858. Fax:  805 893 4120. E-mail:  songi@ chem.ucsb.edu.

     Department of Chemistry, University of California, Berkeley.

     Material Sciences Division, Lawrence Berkeley National Laboratory.

    §

     Physical Biosciences Division, Lawrence Berkeley National Laboratory.

     Howard Hughes Medical Institute and Department of Molecular and Cell Biology.

    Cited By

    This article is cited by 49 publications.

    1. Praveena D. Garimella, Tyler Meldrum, Leah S. Witus, Monica Smith, Vikram S. Bajaj, David E. Wemmer, Matthew B. Francis, and Alexander Pines . Hyperpolarized Xenon-Based Molecular Sensors for Label-Free Detection of analytes. Journal of the American Chemical Society 2014, 136 (1) , 164-168. https://doi.org/10.1021/ja406760r
    2. Johannes F. Teichert, Dmitry Mazunin, and Jeffrey W. Bode . Chemical Sensing of Polyols with Shapeshifting Boronic Acids As a Self-Contained Sensor Array. Journal of the American Chemical Society 2013, 135 (30) , 11314-11321. https://doi.org/10.1021/ja404981q
    3. Zackary I. Cleveland, Harald E. Möller, Laurence W. Hedlund and Bastiaan Driehuys . Continuously Infusing Hyperpolarized 129Xe into Flowing Aqueous Solutions Using Hydrophobic Gas Exchange Membranes. The Journal of Physical Chemistry B 2009, 113 (37) , 12489-12499. https://doi.org/10.1021/jp9049582
    4. Thierry Brotin and Jean-Pierre Dutasta. Cryptophanes and Their Complexes—Present and Future. Chemical Reviews 2009, 109 (1) , 88-130. https://doi.org/10.1021/cr0680437
    5. Heather A. Fogarty,, Patrick Berthault,, Thierry Brotin,, Gaspard Huber,, Hervé Desvaux, and, Jean-Pierre Dutasta. A Cryptophane Core Optimized for Xenon Encapsulation. Journal of the American Chemical Society 2007, 129 (34) , 10332-10333. https://doi.org/10.1021/ja073771c
    6. Julia Schulte-Hermann, Jing Yang, Andrea C. Hurtado Rivera, Jan G. Korvink, Neil MacKinnon, Jürgen J. Brandner. Integrating Micro Process Chemistry into an NMR Spectrometer. Chemie Ingenieur Technik 2024, 96 (3) , 257-278. https://doi.org/10.1002/cite.202300103
    7. Eric S. McLamore, Evangelyn Alocilja, Carmen Gomes, Sundaram Gunasekaran, Daniel Jenkins, Shoumen P.A. Datta, Yanbin Li, Yu (Jessie) Mao, Sam R. Nugen, José I. Reyes-De-Corcuera, Paul Takhistov, Olga Tsyusko, Jarad P. Cochran, Tzuen-Rong (Jeremy) Tzeng, Jeong-Yeol Yoon, Chenxu Yu, Anhong Zhou. FEAST of biosensors: Food, environmental and agricultural sensing technologies (FEAST) in North America. Biosensors and Bioelectronics 2021, 178 , 113011. https://doi.org/10.1016/j.bios.2021.113011
    8. Joseph W. Plummer, Kiarash Emami, Andrew Dummer, Jason C. Woods, Laura L. Walkup, Zackary I. Cleveland. A semi-empirical model to optimize continuous-flow hyperpolarized 129Xe production under practical cryogenic-accumulation conditions. Journal of Magnetic Resonance 2020, 320 , 106845. https://doi.org/10.1016/j.jmr.2020.106845
    9. Jabadurai Jayapaul, Leif Schröder. Molecular Sensing with Host Systems for Hyperpolarized 129Xe. Molecules 2020, 25 (20) , 4627. https://doi.org/10.3390/molecules25204627
    10. Sebastian Kiss, Lorenzo Bordonali, Jan G. Korvink, Neil MacKinnon. Microscale Hyperpolarization. 2018, 297-351. https://doi.org/10.1002/9783527697281.ch11
    11. Alexey S. Kiryutin, Grit Sauer, Sara Hadjiali, Alexandra V. Yurkovskaya, Hergen Breitzke, Gerd Buntkowsky. A highly versatile automatized setup for quantitative measurements of PHIP enhancements. Journal of Magnetic Resonance 2017, 285 , 26-36. https://doi.org/10.1016/j.jmr.2017.10.007
    12. Leif Schr ¨ oder. Chapter 8 HyperCEST Imaging. 2017, 121-158. https://doi.org/10.1201/9781315364421-9
    13. L. Schröder. Xenon Biosensor HyperCEST MRI. 2017, 263-277. https://doi.org/10.1016/B978-0-12-803675-4.00017-8
    14. Erika Weiland, Marie-Anne Springuel-Huet, Andrei Nossov, Antoine Gédéon. 129Xenon NMR: Review of recent insights into porous materials. Microporous and Mesoporous Materials 2016, 225 , 41-65. https://doi.org/10.1016/j.micromeso.2015.11.025
    15. A. Causier, G. Carret, C. Boutin, T. Berthelot, P. Berthault. 3D-printed system optimizing dissolution of hyperpolarized gaseous species for micro-sized NMR. Lab on a Chip 2015, 15 (9) , 2049-2054. https://doi.org/10.1039/C5LC00193E
    16. Kai Ruppert. Biomedical imaging with hyperpolarized noble gases. Reports on Progress in Physics 2014, 77 (11) , 116701. https://doi.org/10.1088/0034-4885/77/11/116701
    17. Yuning Zhang, Pei Che Soon, Alexej Jerschow, James W. Canary. Long‐Lived 1 H Nuclear Spin Singlet in Dimethyl Maleate Revealed by Addition of Thiols. Angewandte Chemie 2014, 126 (13) , 3464-3467. https://doi.org/10.1002/ange.201310284
    18. Yuning Zhang, Pei Che Soon, Alexej Jerschow, James W. Canary. Long‐Lived 1 H Nuclear Spin Singlet in Dimethyl Maleate Revealed by Addition of Thiols. Angewandte Chemie International Edition 2014, 53 (13) , 3396-3399. https://doi.org/10.1002/anie.201310284
    19. C. Witte, M. Kunth, F. Rossella, L. Schröder. Observing and preventing rubidium runaway in a direct-infusion xenon-spin hyperpolarizer optimized for high-resolution hyper-CEST (chemical exchange saturation transfer using hyperpolarized nuclei) NMR. The Journal of Chemical Physics 2014, 140 (8) https://doi.org/10.1063/1.4865944
    20. Krishnan K. Palaniappan, Matthew B. Francis, Alexander Pines, David E. Wemmer. Molecular Sensing Using Hyperpolarized Xenon NMR Spectroscopy. Israel Journal of Chemistry 2014, 54 (1-2) , 104-112. https://doi.org/10.1002/ijch.201300128
    21. J. Yang, M. Palla, F. G. Bosco, M. S. Schmidt, T. Rindzevicius, A. Boisen, J. Ju, Q. Lin. A microfluidic surface enhanced Raman spectroscopic biosensor using aptamer functionalized nanopillars. 2013, 1799-1802. https://doi.org/10.1109/Transducers.2013.6627138
    22. Krishnan K. Palaniappan, R. Matthew Ramirez, Vikram S. Bajaj, David E. Wemmer, Alexander Pines, Matthew B. Francis. Molecular Imaging of Cancer Cells Using a Bacteriophage‐Based 129 Xe NMR Biosensor. Angewandte Chemie International Edition 2013, 52 (18) , 4849-4853. https://doi.org/10.1002/anie.201300170
    23. Krishnan K. Palaniappan, R. Matthew Ramirez, Vikram S. Bajaj, David E. Wemmer, Alexander Pines, Matthew B. Francis. Molecular Imaging of Cancer Cells Using a Bacteriophage‐Based 129 Xe NMR Biosensor. Angewandte Chemie 2013, 125 (18) , 4949-4953. https://doi.org/10.1002/ange.201300170
    24. Leif Schröder. Xenon for NMR biosensing – Inert but alert. Physica Medica 2013, 29 (1) , 3-16. https://doi.org/10.1016/j.ejmp.2011.11.001
    25. Francesca Gruppi, Xiang Xu, Boyang Zhang, Joel A. Tang, Alexej Jerschow, James W. Canary. Peptide Hydrogenation and Labeling with Parahydrogen. Angewandte Chemie International Edition 2012, 51 (47) , 11787-11790. https://doi.org/10.1002/anie.201204403
    26. Francesca Gruppi, Xiang Xu, Boyang Zhang, Joel A. Tang, Alexej Jerschow, James W. Canary. Peptide Hydrogenation and Labeling with Parahydrogen. Angewandte Chemie 2012, 124 (47) , 11957-11960. https://doi.org/10.1002/ange.201204403
    27. Rodolfo H. Acosta, Peter Blümler, Kerstin Münnemann, Hans-Wolfgang Spiess. Mixture and dissolution of laser polarized noble gases: Spectroscopic and imaging applications. Progress in Nuclear Magnetic Resonance Spectroscopy 2012, 66 , 40-69. https://doi.org/10.1016/j.pnmrs.2012.03.003
    28. Kimberly K. Larson, Maggie He, Johannes F. Teichert, Atsushi Naganawa, Jeffrey W. Bode. Chemical sensing with shapeshifting organic molecules. Chemical Science 2012, 3 (6) , 1825. https://doi.org/10.1039/c2sc20238g
    29. Vlad Badilita, Robert Ch. Meier, Nils Spengler, Ulrike Wallrabe, Marcel Utz, Jan G. Korvink. Microscale nuclear magnetic resonance: a tool for soft matter research. Soft Matter 2012, 8 (41) , 10583. https://doi.org/10.1039/c2sm26065d
    30. Tyler Meldrum, Vikram S. Bajaj, David E. Wemmer, Alexander Pines. Band-selective chemical exchange saturation transfer imaging with hyperpolarized xenon-based molecular sensors. Journal of Magnetic Resonance 2011, 213 (1) , 14-21. https://doi.org/10.1016/j.jmr.2011.06.027
    31. Franz Schilling, Leif Schröder, Krishnan K. Palaniappan, Sina Zapf, David E. Wemmer, Alexander Pines. MRI Thermometry Based on Encapsulated Hyperpolarized Xenon. ChemPhysChem 2010, 11 (16) , 3529-3533. https://doi.org/10.1002/cphc.201000507
    32. Tyler Meldrum, Leif Schröder, Philipp Denger, David E. Wemmer, Alexander Pines. Xenon-based molecular sensors in lipid suspensions. Journal of Magnetic Resonance 2010, 205 (2) , 242-246. https://doi.org/10.1016/j.jmr.2010.05.005
    33. Josef Granwehr, Rafal Panek, James Leggett, Walter Köckenberger. Quantifying the transfer and settling in NMR experiments with sample shuttling. The Journal of Chemical Physics 2010, 132 (24) https://doi.org/10.1063/1.3446804
    34. N. Amor, P.P. Zänker, P. Blümler, F.M. Meise, L.M. Schreiber, A. Scholz, J. Schmiedeskamp, H.W. Spiess, K. Münnemann. Magnetic resonance imaging of dissolved hyperpolarized 129Xe using a membrane-based continuous flow system. Journal of Magnetic Resonance 2009, 201 (1) , 93-99. https://doi.org/10.1016/j.jmr.2009.08.004
    35. Leif Schröder, Tyler Meldrum, Monica Smith, Thomas J. Lowery, David E. Wemmer, Alexander Pines. Temperature Response of Xe 129 Depolarization Transfer and Its Application for Ultrasensitive NMR Detection. Physical Review Letters 2008, 100 (25) https://doi.org/10.1103/PhysRevLett.100.257603
    36. Leif Schröder, Lana Chavez, Tyler Meldrum, Monica Smith, Thomas J. Lowery, David E. Wemmer, Alexander Pines. Temperature‐Controlled Molecular Depolarization Gates in Nuclear Magnetic Resonance. Angewandte Chemie International Edition 2008, 47 (23) , 4316-4320. https://doi.org/10.1002/anie.200800382
    37. Leif Schröder, Lana Chavez, Tyler Meldrum, Monica Smith, Thomas J. Lowery, David E. Wemmer, Alexander Pines. Molekulare Steuerelemente zur temperaturempfindlichen Depolarisierung in der kernmagnetischen Resonanz. Angewandte Chemie 2008, 120 (23) , 4388-4392. https://doi.org/10.1002/ange.200800382
    38. Byoung Soo Kim, Young Ho Ko, Youngkook Kim, Hyeong Ju Lee, N. Selvapalam, Hee Cheon Lee, Kimoon Kim. Water soluble cucurbit[6]uril derivative as a potential Xe carrier for 129Xe NMR-based biosensors. Chemical Communications 2008, 66 (24) , 2756. https://doi.org/10.1039/b805724a
    39. Vincent Roy, Thierry Brotin, Jean‐Pierre Dutasta, Marie‐Hélène Charles, Thierry Delair, François Mallet, Gaspard Huber, Hervé Desvaux, Yves Boulard, Patrick Berthault. A Cryptophane Biosensor for the Detection of Specific Nucleotide Targets through Xenon NMR Spectroscopy. ChemPhysChem 2007, 8 (14) , 2082-2085. https://doi.org/10.1002/cphc.200700384
    40. J. Granwehr. Multiplicative or t 1 Noise in NMR Spectroscopy. Applied Magnetic Resonance 2007, 32 (1-2) , 113-156. https://doi.org/10.1007/s00723-007-0006-3
    41. Sandra Garcia, Lana Chavez, Thomas J. Lowery, Song-I Han, David E. Wemmer, Alexander Pines. Sensitivity enhancement by exchange mediated magnetization transfer of the xenon biosensor signal. Journal of Magnetic Resonance 2007, 184 (1) , 72-77. https://doi.org/10.1016/j.jmr.2006.09.010
    42. Daniela Baumer, Eike Brunner, Peter Blümler, Paul Philipp Zänker, Hans Wolfgang Spiess. NMR Spectroscopy of Laser‐Polarized 129 Xe Under Continuous Flow: A Method To Study Aqueous Solutions of Biomolecules. Angewandte Chemie International Edition 2006, 45 (43) , 7282-7284. https://doi.org/10.1002/anie.200601008
    43. Daniela Baumer, Eike Brunner, Peter Blümler, Paul Philipp Zänker, Hans Wolfgang Spiess. NMR‐Spektroskopie von Laser‐polarisiertem 129 Xe unter kontinuierlichem Fluss: eine Methode zur Untersuchung von Biomolekülen in wässrigen Lösungen. Angewandte Chemie 2006, 118 (43) , 7440-7442. https://doi.org/10.1002/ange.200601008
    44. Leif Schröder, Thomas J. Lowery, Christian Hilty, David E. Wemmer, Alexander Pines. Molecular Imaging Using a Targeted Magnetic Resonance Hyperpolarized Biosensor. Science 2006, 314 (5798) , 446-449. https://doi.org/10.1126/science.1131847
    45. Elad Harel, Josef Granwehr, Juliette A. Seeley, Alex Pines. Multiphase imaging of gas flow in a nanoporous material using remote-detection NMR. Nature Materials 2006, 5 (4) , 321-327. https://doi.org/10.1038/nmat1598
    46. Thomas J. Lowery, Sandra Garcia, Lana Chavez, E. Janette Ruiz, Tom Wu, Thierry Brotin, Jean‐Pierre Dutasta, David S. King, Peter G. Schultz, Alex Pines, David E. Wemmer. Optimization of Xenon Biosensors for Detection of Protein Interactions. ChemBioChem 2006, 7 (1) , 65-73. https://doi.org/10.1002/cbic.200500327
    47. Christian Hilty, Thomas J. Lowery, David E. Wemmer, Alexander Pines. Spectrally Resolved Magnetic Resonance Imaging of a Xenon Biosensor. Angewandte Chemie International Edition 2006, 45 (1) , 70-73. https://doi.org/10.1002/anie.200502693
    48. Christian Hilty, Thomas J. Lowery, David E. Wemmer, Alexander Pines. Spectrally Resolved Magnetic Resonance Imaging of a Xenon Biosensor. Angewandte Chemie 2006, 118 (1) , 76-79. https://doi.org/10.1002/ange.200502693
    49. J. Granwehr, E. Harel, S. Han, S. Garcia, A. Pines, P. N. Sen, Y.-Q. Song. Time-of-Flight Flow Imaging Using NMR Remote Detection. Physical Review Letters 2005, 95 (7) https://doi.org/10.1103/PhysRevLett.95.075503

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    You’ve supercharged your research process with ACS and Mendeley!

    STEP 1:
    Click to create an ACS ID

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    MENDELEY PAIRING EXPIRED
    Your Mendeley pairing has expired. Please reconnect