Programming A Molecular Relay for Ultrasensitive Biodetection through 129 Xe NMR

Wang, Yanfei; Roose, Benjamin W.; Philbin, John P.; Doman, Jordan L.; Dmochowski, Ivan J.

doi:10.1002/anie.201508990

Programming A Molecular Relay for Ultrasensitive Biodetection through ¹²⁹ Xe NMR

Journal Article · Mon Dec 21 00:00:00 EST 2015 · Angewandte Chemie (International Edition)

DOI:https://doi.org/10.1002/anie.201508990· OSTI ID:1260842

^[1]; ^[1]; Philbin, John P. ^[1]; Doman, Jordan L. ^[1]; ^[1]

Univ. of Pennsylvania, Philadelphia, PA (United States)

We reported a supramolecular strategy for detecting specific proteins in complex media by using hyperpolarized ¹²⁹Xe NMR. A cucurbit[6]uril (CB[6])-based molecular relay was programmed for three sequential equilibrium conditions by designing a two-faced guest (TFG) that initially binds CB[6] and blocks the CB[6]–Xe interaction. Moreover, the protein analyte recruits the TFG and frees CB[6] for Xe binding. TFGs containing CB[6]- and carbonic anhydrase II (CAII)-binding domains were synthesized in one or two steps. X-ray crystallography confirmed TFG binding to Zn²⁺ in the deep CAII active-site cleft, which precludes simultaneous CB[6] binding. The molecular relay was reprogrammed to detect avidin by using a different TFG. Finally, Xe binding by CB[6] was detected in buffer and in E. coli cultures expressing CAII through ultrasensitive ¹²⁹Xe NMR spectroscopy.

View Accepted Manuscript (DOE)

Research Organization:: Advanced Photon Source (APS), Argonne National Laboratory (ANL), Argonne, IL (US)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE

OSTI ID:: 1260842

Journal Information:: Angewandte Chemie (International Edition), Journal Name: Angewandte Chemie (International Edition) Journal Issue: 5 Vol. 55; ISSN 1433-7851

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (37)

Efficient Fluorescence Enhancement and Cooperative Binding of an Organic Dye in a Supra-biomolecular Host–Protein Assembly Bhasikuttan, Achikanath C.; Mohanty, Jyotirmayee; Nau, Werner M. Angewandte Chemie, Vol. 119, Issue 22 https://doi.org/10.1002/ange.200604757	journal	May 2007
Efficient Fluorescence Enhancement and Cooperative Binding of an Organic Dye in a Supra-biomolecular Host–Protein Assembly Bhasikuttan, Achikanath C.; Mohanty, Jyotirmayee; Nau, Werner M. Angewandte Chemie International Edition, Vol. 46, Issue 22 https://doi.org/10.1002/anie.200604757	journal	May 2007
The Potential of Cucurbit[n]urils in Drug Delivery Walker, Shonagh; Oun, Rabbab; McInnes, Fiona J. Israel Journal of Chemistry, Vol. 51, Issue 5-6 https://doi.org/10.1002/ijch.201100033	journal	April 2011
Hyperpolarized ¹²⁹ Xe MRI of the human lung Mugler, John P.; Altes, Talissa A. Journal of Magnetic Resonance Imaging, Vol. 37, Issue 2 https://doi.org/10.1002/jmri.23844	journal	January 2013
129Xe NMR of xenon adsorbed on zeolites Demarquay, J.; Fraissard, J. Chemical Physics Letters, Vol. 136, Issue 3-4 https://doi.org/10.1016/0009-2614(87)80258-0	journal	May 1987
Cucurbituril Homologues and Derivatives: New Opportunities in Supramolecular Chemistry Lee, Jae Wook; Samal, S.; Selvapalam, N. Accounts of Chemical Research, Vol. 36, Issue 8 https://doi.org/10.1021/ar020254k	journal	August 2003
Cryptophanes and Their Complexes—Present and Future Brotin, Thierry; Dutasta, Jean-Pierre Chemical Reviews, Vol. 109, Issue 1 https://doi.org/10.1021/cr0680437	journal	January 2009
Dynamics of molecular recognition involving cucurbituril Mock, William L.; Shih, Neng Yang Journal of the American Chemical Society, Vol. 111, Issue 7 https://doi.org/10.1021/ja00189a053	journal	March 1989
Molecular Recognition of Insulin by a Synthetic Receptor Chinai, Jordan M.; Taylor, Alexander B.; Ryno, Lisa M. Journal of the American Chemical Society, Vol. 133, Issue 23 https://doi.org/10.1021/ja201581x	journal	June 2011
Nanoemulsion Contrast Agents with Sub-picomolar Sensitivity for Xenon NMR Stevens, Todd K.; Ramirez, R. Matthew; Pines, Alexander Journal of the American Chemical Society, Vol. 135, Issue 26 https://doi.org/10.1021/ja402885q	journal	June 2013
Cryptophane Xenon-129 Nuclear Magnetic Resonance Biosensors Targeting Human Carbonic Anhydrase Chambers, Jennifer M.; Hill, P. Aru; Aaron, Julie A. Journal of the American Chemical Society, Vol. 131, Issue 2 https://doi.org/10.1021/ja806092w	journal	January 2009
Biological Catalysis Regulated by Cucurbit[7]uril Molecular Containers Ghosh, Soumyadip; Isaacs, Lyle Journal of the American Chemical Society, Vol. 132, Issue 12 https://doi.org/10.1021/ja910915k	journal	March 2010
Structure-Based Design of a Sulfonamide Probe for Fluorescence Anisotropy Detection of Zinc with a Carbonic Anhydrase-Based Biosensor Elbaum, Daniel; Nair, Satish K.; Patchan, Marcia W. Journal of the American Chemical Society, Vol. 118, Issue 35 https://doi.org/10.1021/ja954102e	journal	January 1996
Increasing Binding Constants of Ligands to Carbonic Anhydrase by Using "Greasy Tails" Gao, Jinming; Qiao, Shuang; Whitesides, George M. Journal of Medicinal Chemistry, Vol. 38, Issue 13 https://doi.org/10.1021/jm00013a005	journal	June 1995
A Class of 4-Sulfamoylphenyl-ω-aminoalkyl Ethers with Effective Carbonic Anhydrase Inhibitory Action and Antiglaucoma Effects Bozdag, Murat; Pinard, Melissa; Carta, Fabrizio Journal of Medicinal Chemistry, Vol. 57, Issue 22 https://doi.org/10.1021/jm501497m	journal	October 2014
Structure and selectivity in host-guest complexes of cucurbituril Mock, William L.; Shih, Neng Yang The Journal of Organic Chemistry, Vol. 51, Issue 23 https://doi.org/10.1021/jo00373a018	journal	November 1986
Cesium Effect: High Chemoselectivity in Direct N-Alkylation of Amines Salvatore, Ralph Nicholas; Nagle, Advait S.; Jung, Kyung Woon The Journal of Organic Chemistry, Vol. 67, Issue 3 https://doi.org/10.1021/jo010643c	journal	February 2002
Multichannel MRI Labeling of Mammalian Cells by Switchable Nanocarriers for Hyperpolarized Xenon Klippel, Stefan; Freund, Christian; Schröder, Leif Nano Letters, Vol. 14, Issue 10 https://doi.org/10.1021/nl502498w	journal	September 2014
Shorter Synthesis of Trifunctionalized Cryptophane-A Derivatives Taratula, Olena; Hill, P. Aru; Bai, Yubin Organic Letters, Vol. 13, Issue 6 https://doi.org/10.1021/ol200088f	journal	March 2011
Genetically encoded reporters for hyperpolarized xenon magnetic resonance imaging Shapiro, Mikhail G.; Ramirez, R. Matthew; Sperling, Lindsay J. Nature Chemistry, Vol. 6, Issue 7 https://doi.org/10.1038/nchem.1934	journal	April 2014
Crystallographic observation of 'induced fit' in a cryptophane host–guest model system Taratula, Olena; Hill, P. Aru; Khan, Najat S. Nature Communications, Vol. 1, Issue 1 https://doi.org/10.1038/ncomms1151	journal	December 2010
Label-free continuous enzyme assays with macrocycle-fluorescent dye complexes Hennig, Andreas; Bakirci, Hüseyin; Nau, Werner M. Nature Methods, Vol. 4, Issue 8 https://doi.org/10.1038/nmeth1064	journal	July 2007
Making molecular machines work Browne, Wesley R.; Feringa, Ben L. Nature Nanotechnology, Vol. 1, Issue 1 https://doi.org/10.1038/nnano.2006.45	journal	October 2006
An artificial molecular pump Cheng, Chuyang; McGonigal, Paul R.; Schneebeli, Severin T. Nature Nanotechnology, Vol. 10, Issue 6 https://doi.org/10.1038/nnano.2015.96	journal	May 2015
Carbonic anhydrases: novel therapeutic applications for inhibitors and activators Supuran, Claudiu T. Nature Reviews Drug Discovery, Vol. 7, Issue 2 https://doi.org/10.1038/nrd2467	journal	February 2008
Functionalized cucurbiturils and their applications Kim, Kimoon; Selvapalam, Narayanan; Ko, Young Ho Chemical Society Reviews, Vol. 36, Issue 2, p. 267-279 https://doi.org/10.1039/B603088M	journal	January 2007
Cucurbit[n]urils: from mechanism to structure and function Isaacs, Lyle Chem. Commun., Issue 6 https://doi.org/10.1039/B814897J	journal	January 2009
Bacterial spore detection and analysis using hyperpolarized ¹²⁹ Xe chemical exchange saturation transfer (Hyper-CEST) NMR Bai, Yubin; Wang, Yanfei; Goulian, Mark Chem. Sci., Vol. 5, Issue 8 https://doi.org/10.1039/C4SC01190B	journal	January 2014
DNA–ligand interactions gained and lost: light-induced ligand redistribution in a supramolecular cascade Berdnikova, Daria V.; Aliyeu, Tseimur M.; Paululat, Thomas Chemical Communications, Vol. 51, Issue 23 https://doi.org/10.1039/C5CC01025J	journal	January 2015
Cucurbit[6]uril is an ultrasensitive ¹²⁹ Xe NMR contrast agent Wang, Yanfei; Dmochowski, Ivan J. Chemical Communications, Vol. 51, Issue 43 https://doi.org/10.1039/C5CC01826A	journal	January 2015
Identification, classification, and signal amplification capabilities of high-turnover gas binding hosts in ultra-sensitive NMR Kunth, Martin; Witte, Christopher; Hennig, Andreas Chemical Science, Vol. 6, Issue 11 https://doi.org/10.1039/C5SC01400J	journal	January 2015
Nanoporosity of an organo-clay shown by hyperpolarized xenon and 2D NMR spectroscopy Sozzani, Piero; Bracco, Silvia; Comotti, Angiolina Chemical Communications, Issue 18 https://doi.org/10.1039/b602040b	journal	January 2006
Highly symmetric columnar channels in metal-free cucurbit[n]uril hydrate crystals (n = 6, 8) Bardelang, David; Udachin, Konstantin A.; Leek, Donald M. CrystEngComm, Vol. 9, Issue 11 https://doi.org/10.1039/b711285h	journal	January 2007
Water soluble cucurbit[6]uril derivative as a potential Xe carrier for 129Xe NMR-based biosensors Kim, Byoung Soo; Ko, Young Ho; Kim, Youngkook Chemical Communications, Issue 24 https://doi.org/10.1039/b805724a	journal	January 2008
Avidin. 1. the use of [14c]Biotin for Kinetic Studies and for Assay Green, Nm Biochemical Journal, Vol. 89, Issue 3 https://doi.org/10.1042/bj0890585	journal	December 1963
Self-Assembly at All Scales Whitesides, George M.; Grzybowski, Bartosz Science, Vol. 295, Issue 5564, p. 2418-2421 https://doi.org/10.1126/science.1070821	journal	March 2002
Molecular Imaging Using a Targeted Magnetic Resonance Hyperpolarized Biosensor Schroder, L.; Lowery, T. J.; Hilty, C. Science, Vol. 314, Issue 5798 https://doi.org/10.1126/science.1131847	journal	October 2006

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An Expanded Palette of Xenon-129 NMR Biosensors Wang, Yanfei; Dmochowski, Ivan J. Accounts of Chemical Research, Vol. 49, Issue 10 https://doi.org/10.1021/acs.accounts.6b00309	journal	September 2016
Cyclodextrin-Based Pseudorotaxanes: Easily Conjugatable Scaffolds for Synthesizing Hyperpolarized Xenon-129 Magnetic Resonance Imaging Agents Hane, Francis T.; Fernando, Ashvin; Prete, Braedan R. J. ACS Omega, Vol. 3, Issue 1 https://doi.org/10.1021/acsomega.7b01744	journal	January 2018
In vivo detection of cucurbit[6]uril, a hyperpolarized xenon contrast agent for a xenon magnetic resonance imaging biosensor Hane, Francis T.; Li, Tao; Smylie, Peter Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep41027	journal	January 2017
Probing Reversible Guest Binding with Hyperpolarized 129Xe-NMR: Characteristics and Applications for Cucurbit[n]urils Jayapaul, Jabadurai; Schröder, Leif Molecules, Vol. 25, Issue 4 https://doi.org/10.3390/molecules25040957	journal	February 2020
A Genetically Encoded β-Lactamase Reporter for Ultrasensitive ¹²⁹ Xe NMR in Mammalian Cells Wang, Yanfei; Roose, Benjamin W.; Palovcak, Eugene J. Angewandte Chemie, Vol. 128, Issue 31 https://doi.org/10.1002/ange.201604055	journal	June 2016
Rotaxane Probes for the Detection of Hydrogen Peroxide by ¹²⁹ Xe HyperCEST NMR Spectroscopy Klass, Sarah H.; Truxal, Ashley E.; Fiala, Tahoe A. Angewandte Chemie, Vol. 131, Issue 29 https://doi.org/10.1002/ange.201903045	journal	June 2019
A Genetically Encoded β-Lactamase Reporter for Ultrasensitive ¹²⁹ Xe NMR in Mammalian Cells Wang, Yanfei; Roose, Benjamin W.; Palovcak, Eugene J. Angewandte Chemie International Edition, Vol. 55, Issue 31 https://doi.org/10.1002/anie.201604055	journal	June 2016
Rotaxane Probes for the Detection of Hydrogen Peroxide by ¹²⁹ Xe HyperCEST NMR Spectroscopy Klass, Sarah H.; Truxal, Ashley E.; Fiala, Tahoe A. Angewandte Chemie International Edition, Vol. 58, Issue 29 https://doi.org/10.1002/anie.201903045	journal	July 2019
Directly Functionalized Cucurbit[7]uril as a Biosensor for the Selective Detection of Protein Interactions by ¹²⁹ Xe hyperCEST NMR Truxal, Ashley E.; Cao, Liping; Isaacs, Lyle Chemistry – A European Journal, Vol. 25, Issue 24 https://doi.org/10.1002/chem.201900610	journal	February 2019
Quantitative Assessment of Xenon Exchange Kinetics with Cucurbit[6]uril in Physiological Saline Korchak, Sergey; Riemer, Thomas; Kilian, Wolfgang ChemPhysChem, Vol. 19, Issue 15 https://doi.org/10.1002/cphc.201800048	journal	June 2018
A Structural Basis for ¹²⁹ Xe Hyper-CEST Signal in TEM-1 β-Lactamase Roose, Benjamin W.; Zemerov, Serge D.; Wang, Yanfei ChemPhysChem, Vol. 20, Issue 2 https://doi.org/10.1002/cphc.201800624	journal	September 2018
Thermodynamic, kinetic, and structural parameterization of human carbonic anhydrase interactions toward enhanced inhibitor design Linkuvienė, Vaida; Zubrienė, Asta; Manakova, Elena Quarterly Reviews of Biophysics, Vol. 51 https://doi.org/10.1017/s0033583518000082	journal	January 2018
¹²⁹ Xe NMR-based sensors: biological applications and recent methods Mari, E.; Berthault, P. The Analyst, Vol. 142, Issue 18 https://doi.org/10.1039/c7an01088e	journal	January 2017
An intracellular diamine oxidase triggered hyperpolarized ¹²⁹ Xe magnetic resonance biosensor Zhang, Bin; Guo, Qianni; Luo, Qing Chemical Communications, Vol. 54, Issue 97 https://doi.org/10.1039/c8cc07822j	journal	January 2018
A supramolecular five-component relay switch that exposes the mechanistic competition of dissociative versus associative binding to cucurbiturils by ratiometric fluorescence monitoring Liu, Yan-Cen; Nau, Werner M.; Hennig, Andreas Chemical Communications, Vol. 55, Issue 94 https://doi.org/10.1039/c9cc07165b	journal	January 2019
Thermodynamic, kinetic, and structural parameterization of human carbonic anhydrase interactions toward enhanced inhibitor design Linkuvienė, Vaida; Zubrienė, Asta; Manakova, Elena Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2018-05504	text	January 2018

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Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
NMR spectroscopy
bioinorganic chemistry
biosensors
host–guest systems
molecular recognition