An Activity-Based Methionine Bioconjugation Approach To Developing Proximity-Activated Imaging Reporters

Ohata, Jun; Krishnamoorthy, Lakshmi; Gonzalez, Monica A.; Xiao, Tong; Iovan, Diana A.; Toste, F. Dean; Miller, Evan W.; Chang, Christopher J.

doi:10.1021/acscentsci.9b01038

Title: An Activity-Based Methionine Bioconjugation Approach To Developing Proximity-Activated Imaging Reporters

Journal Article · 06 January 2020 · ACS Central Science

DOI: https://doi.org/10.1021/acscentsci.9b01038 · OSTI ID:1603592

^[1];

^[1]; Gonzalez, Monica A. ^[1];

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^[1]

Univ. of California, Berkeley, CA (United States)

Chemical probes that report on protein activity, rather than protein abundance, with spatial and temporal resolution can enable studies of their native function in biological contexts as well as provide opportunities for developing new types of biochemical reporters. Here we present a sensing platform, termed proximity-activated imaging reporter (PAIR), which combines activity-based methionine bioconjugation and antibody labeling with proximity-dependent oligonucleotide-based amplification to monitor dynamic changes of a given analyte in cells and animals through context-dependent methionine labeling of specific protein targets. We establish this PAIR method to develop sensors for imaging reactive oxygen species (ROS) and calcium ions through oxaziridine-directed labeling of reactive methionine residues on β-actin and calmodulin (CaM), respectively, where the extent of methionine bioconjugation on these protein targets can serve as an indicator of oxidative stress or calcium status. In particular, application of PAIR to activity-based CaM detection provides a method for imaging integrated calcium activity in both in vitro cell and in vivo zebrafish models. By relying on native protein biochemistry, PAIR enables redox and metal imaging without introduction of external small molecules or genetically encoded indicators that can potentially buffer the natural/existing pools. This approach can be potentially generalized to target a broader range of analytes by pairing appropriate activity-based protein probes with protein detection reagents in a proximity-driven manner, providing a starting point not only for designing new sensors but also for monitoring endogenous activity of specific protein targets in biological specimens with spatial and temporal fidelity.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1603592

Journal Information:: ACS Central Science, Journal Name: ACS Central Science Journal Issue: 1 Vol. 6; ISSN 2374-7943

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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Direct Redox Regulation of F-Actin Assembly and Disassembly by Mical Hung, R. -J.; Pak, C. W.; Terman, J. R. Science, Vol. 334, Issue 6063 https://doi.org/10.1126/science.1211956	journal	November 2011
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Redox-based reagents for chemoselective methionine bioconjugation Lin, Shixian; Yang, Xiaoyu; Jia, Shang Science, Vol. 355, Issue 6325 https://doi.org/10.1126/science.aal3316	journal	February 2017
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Genetically encoded optical sensors for monitoring of intracellular chloride and chloride-selective channels activity Bregestovski, Piotr Frontiers in Molecular Neuroscience, Vol. 2 https://doi.org/10.3389/neuro.02.015.2009	journal	January 2009
ATP sensing in living plant cells reveals tissue gradients and stress dynamics of energy physiology De Col, Valentina; Fuchs, Philippe; Nietzel, Thomas eLife, Vol. 6 https://doi.org/10.7554/elife.26770	journal	July 2017
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Chemoproteomic Method for Profiling Inhibitor-Bound Kinase Complexes Fang, Linglan; Chakraborty, Sujata; Dieter, Emily M. Journal of the American Chemical Society, Vol. 141, Issue 30 https://doi.org/10.1021/jacs.9b02963	journal	June 2019
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Low concentrations of tetrodotoxin interact with tetrodotoxin-resistant voltage-gated sodium channels Farmer, C. E.; Smith, K. J.; Docherty, R. J. British Journal of Pharmacology, Vol. 155, Issue 1 https://doi.org/10.1038/bjp.2008.235	journal	September 2008
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A light- and calcium-gated transcription factor for imaging and manipulating activated neurons Wang, Wenjing; Wildes, Craig P.; Pattarabanjird, Tanyaporn Nature Biotechnology, Vol. 35, Issue 9 https://doi.org/10.1038/nbt.3909	journal	June 2017
Assay to visualize specific protein oxidation reveals spatio-temporal regulation of SHP2 Tsutsumi, Ryouhei; Harizanova, Jana; Stockert, Rabea Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00503-w	journal	September 2017
An activity-dependent proximity ligation platform for spatially resolved quantification of active enzymes in single cells Li, Gang; Montgomery, Jeffrey E.; Eckert, Mark A. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01854-0	journal	November 2017
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Calcium signalling in T cells Trebak, Mohamed; Kinet, Jean-Pierre Nature Reviews Immunology, Vol. 19, Issue 3 https://doi.org/10.1038/s41577-018-0110-7	journal	January 2019
Molecular tools for imaging and recording neuronal activity Wang, Wenjing; Kim, Christina K.; Ting, Alice Y. Nature Chemical Biology, Vol. 15, Issue 2 https://doi.org/10.1038/s41589-018-0207-0	journal	January 2019
Optical measurement of synaptic glutamate spillover and reuptake by linker optimized glutamate-sensitive fluorescent reporters Hires, S. A.; Zhu, Y.; Tsien, R. Y. Proceedings of the National Academy of Sciences, Vol. 105, Issue 11 https://doi.org/10.1073/pnas.0712008105	journal	March 2008
Chemoselective tarantula toxins report voltage activation of wild-type ion channels in live cells Tilley, D. C.; Eum, K. S.; Fletcher-Taylor, S. Proceedings of the National Academy of Sciences, Vol. 111, Issue 44 https://doi.org/10.1073/pnas.1406876111	journal	October 2014
Antibody detection by agglutination–PCR (ADAP) enables early diagnosis of HIV infection by oral fluid analysis Tsai, Cheng-ting; Robinson, Peter V.; Cortez, Felipe de Jesus Proceedings of the National Academy of Sciences, Vol. 115, Issue 6 https://doi.org/10.1073/pnas.1711004115	journal	January 2018
Evaluation of Calcium Influx Factors from Stimulated Jurkat T-lymphocytes by Microinjection into Xenopus Oocytes Thomas, David; Hanley, Michael R. Journal of Biological Chemistry, Vol. 270, Issue 12 https://doi.org/10.1074/jbc.270.12.6429	journal	March 1995
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Imaging calcium signalsin vivo: a powerful tool in physiology and pharmacology Russell, James T. British Journal of Pharmacology, Vol. 163, Issue 8 https://doi.org/10.1111/j.1476-5381.2010.00988.x	journal	July 2011
Direct Redox Regulation of F-Actin Assembly and Disassembly by Mical Hung, R. -J.; Pak, C. W.; Terman, J. R. Science, Vol. 334, Issue 6063 https://doi.org/10.1126/science.1211956	journal	November 2011
Labeling of active neural circuits in vivo with designed calcium integrators Fosque, Benjamin F.; Sun, Yi; Dana, Hod Science, Vol. 347, Issue 6223 https://doi.org/10.1126/science.1260922	journal	February 2015
Redox-based reagents for chemoselective methionine bioconjugation Lin, Shixian; Yang, Xiaoyu; Jia, Shang Science, Vol. 355, Issue 6325 https://doi.org/10.1126/science.aal3316	journal	February 2017
CD3/CD28 Costimulation-Induced NF-κB Activation Is Mediated by Recruitment of Protein Kinase C-θ, Bcl10, and IκB Kinase β to the Immunological Synapse through CARMA1 Wang, Donghai; Matsumoto, Reiko; You, Yun Molecular and Cellular Biology, Vol. 24, Issue 1 https://doi.org/10.1128/MCB.24.1.164-171.2003	journal	January 2004
Calmodulin: an introduction Stevens, Frits C. Canadian Journal of Biochemistry and Cell Biology, Vol. 61, Issue 8 https://doi.org/10.1139/o83-115	journal	August 1983
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Developmental and architectural principles of the lateral-line neural map Pujol-Martí, Jesús; López-Schier, Hernán Frontiers in Neural Circuits, Vol. 7 https://doi.org/10.3389/fncir.2013.00047	journal	January 2013
Genetically encoded optical sensors for monitoring of intracellular chloride and chloride-selective channels activity Bregestovski, Piotr Frontiers in Molecular Neuroscience, Vol. 2 https://doi.org/10.3389/neuro.02.015.2009	journal	January 2009
ATP sensing in living plant cells reveals tissue gradients and stress dynamics of energy physiology De Col, Valentina; Fuchs, Philippe; Nietzel, Thomas eLife, Vol. 6 https://doi.org/10.7554/eLife.26770	journal	July 2017
Semisynthetic biosensors for mapping cellular concentrations of nicotinamide adenine dinucleotides Sallin, Olivier; Reymond, Luc; Gondrand, Corentin eLife, Vol. 7 https://doi.org/10.7554/eLife.32638	journal	May 2018

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