Activity-Based Sensing for Chemistry-Enabled Biology: Illuminating Principles, Probes, and Prospects for Boronate Reagents for Studying Hydrogen Peroxide

Overview

Journal ACS Bio Med Chem Au

Publisher American Chemical Society

Specialty Biochemistry

Date 2022 Dec 27

PMID 36573097

Authors

Marco S Messina

Gianluca Quargnali

Christopher J Chang

Affiliations

Soon will be listed here.

Abstract

Activity-based sensing (ABS) offers a general approach that exploits chemical reactivity as a method for selective detection and manipulation of biological analytes. Here, we illustrate the value of this chemical platform to enable new biological discovery through a case study in the design and application of ABS reagents for studying hydrogen peroxide (HO), a major type of reactive oxygen species (ROS) that regulates a diverse array of vital cellular signaling processes to sustain life. Specifically, we summarize advances in the use of activity-based boronate probes for the detection of HO featuring high molecular selectivity over other ROS, with an emphasis on tailoring designs in chemical structure to promote new biological principles of redox signaling.

Citing Articles

Difunctional oxidatively cleavable alkenyl boronates: application to cellular peroxide sensing from a fluorophore-quencher pair.

Klootwyk B, Fleury G, Albright S, Deiters A, Floreancig P Chem Commun (Camb). 2025; 61(16):3375-3378.

PMID: 39887215 PMC: 11784462. DOI: 10.1039/d5cc00090d.

Activatable Porphyrin-Based Sensors, Photosensitizers and Combination Therapeutics.

Bandyopadhyay S, Forzano J, Dirak M, Chan J JACS Au. 2025; 5(1):42-54.

PMID: 39886600 PMC: 11775669. DOI: 10.1021/jacsau.4c01108.

Sub-organellar mitochondrial hydrogen peroxide observed using a SNAP tag targeted coumarin-based fluorescent reporter.

Eaglesfield R, Fernandez-Vizarra E, Lacko E, Caldwell S, Sloan N, Siciarz D Redox Biol. 2025; 80:103502.

PMID: 39864323 PMC: 11802384. DOI: 10.1016/j.redox.2025.103502.

Molecular Determinants of Optical Modulation in ssDNA-Carbon Nanotube Biosensors.

Krasley A, Chakraborty S, Vukovic L, Beyene A ACS Nano. 2025; 19(8):7804-7820.

PMID: 39817860 PMC: 11887485. DOI: 10.1021/acsnano.4c13814.

Xanthene-Based Dyes for Photoacoustic Imaging and their Use as Analyte-Responsive Probes.

Brondsted F, Stains C Chemistry. 2024; 30(37):e202400598.

PMID: 38662806 PMC: 11219268. DOI: 10.1002/chem.202400598.

References

Chen X, Ren X, Zhang L, Liu Z, Hai Z . Mitochondria-Targeted Fluorescent and Photoacoustic Imaging of Hydrogen Peroxide in Inflammation. Anal Chem. 2020; 92(20):14244-14250. DOI: 10.1021/acs.analchem.0c03506. View

Green O, Eilon T, Hananya N, Gutkin S, Bauer C, Shabat D . Opening a Gateway for Chemiluminescence Cell Imaging: Distinctive Methodology for Design of Bright Chemiluminescent Dioxetane Probes. ACS Cent Sci. 2017; 3(4):349-358. PMC: 5408346. DOI: 10.1021/acscentsci.7b00058. View

Brewer T, Garcia F, Onak C, Carroll K, Chang C . Chemical approaches to discovery and study of sources and targets of hydrogen peroxide redox signaling through NADPH oxidase proteins. Annu Rev Biochem. 2015; 84:765-90. PMC: 6063359. DOI: 10.1146/annurev-biochem-060614-034018. View

OShea J, Gadina M, Kanno Y . Cytokine signaling: birth of a pathway. J Immunol. 2011; 187(11):5475-8. PMC: 3226779. DOI: 10.4049/jimmunol.1102913. View

Choi N, Lee J, Park E, Lee J, Lee J . Recent Advances in Organelle-Targeted Fluorescent Probes. Molecules. 2021; 26(1). PMC: 7795030. DOI: 10.3390/molecules26010217. View

Li J, Dong Y, Wei R, Jiang G, Yao C, Lv M . Stable, Bright, and Long-Fluorescence-Lifetime Dyes for Deep-Near-Infrared Bioimaging. J Am Chem Soc. 2022; 144(31):14351-14362. DOI: 10.1021/jacs.2c05826. View

Srikun D, Miller E, Domaille D, Chang C . An ICT-based approach to ratiometric fluorescence imaging of hydrogen peroxide produced in living cells. J Am Chem Soc. 2008; 130(14):4596-7. DOI: 10.1021/ja711480f. View

Wang W, Jiang W, Mao G, Tan Z, Tan M, Li C . A novel near-infrared theranostic probe for accurate cancer chemotherapy by a dual activation strategy. Chem Commun (Camb). 2021; 57(100):13768-13771. DOI: 10.1039/d1cc05864a. View

Cravatt B, Wright A, Kozarich J . Activity-based protein profiling: from enzyme chemistry to proteomic chemistry. Annu Rev Biochem. 2008; 77:383-414. DOI: 10.1146/annurev.biochem.75.101304.124125. View

10.

Sies H, Jones D . Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nat Rev Mol Cell Biol. 2020; 21(7):363-383. DOI: 10.1038/s41580-020-0230-3. View

11.

Masanta G, Heo C, Lim C, Bae S, Cho B, Kim H . A mitochondria-localized two-photon fluorescent probe for ratiometric imaging of hydrogen peroxide in live tissue. Chem Commun (Camb). 2012; 48(29):3518-20. DOI: 10.1039/c2cc00034b. View

12.

Carroll V, Michel B, Blecha J, VanBrocklin H, Keshari K, Wilson D . A boronate-caged [¹⁸F]FLT probe for hydrogen peroxide detection using positron emission tomography. J Am Chem Soc. 2014; 136(42):14742-5. PMC: 4210116. DOI: 10.1021/ja509198w. View

13.

Li J, Xie X . Recent advance in dual-functional luminescent probes for reactive species and common biological ions. Anal Bioanal Chem. 2022; 414(18):5087-5103. DOI: 10.1007/s00216-021-03792-9. View

14.

Niethammer P, Grabher C, Look A, Mitchison T . A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature. 2009; 459(7249):996-9. PMC: 2803098. DOI: 10.1038/nature08119. View

15.

Miller E, Dickinson B, Chang C . Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc Natl Acad Sci U S A. 2010; 107(36):15681-6. PMC: 2936599. DOI: 10.1073/pnas.1005776107. View

16.

Miki T, Awa M, Nishikawa Y, Kiyonaka S, Wakabayashi M, Ishihama Y . A conditional proteomics approach to identify proteins involved in zinc homeostasis. Nat Methods. 2016; 13(11):931-937. DOI: 10.1038/nmeth.3998. View

17.

Albers A, Okreglak V, Chang C . A FRET-based approach to ratiometric fluorescence detection of hydrogen peroxide. J Am Chem Soc. 2006; 128(30):9640-1. DOI: 10.1021/ja063308k. View

18.

Xiao H, Li P, Hu X, Shi X, Zhang W, Tang B . Simultaneous fluorescence imaging of hydrogen peroxide in mitochondria and endoplasmic reticulum during apoptosis. Chem Sci. 2018; 7(9):6153-6159. PMC: 6024174. DOI: 10.1039/c6sc01793b. View

19.

Forman H, Zhang H . Targeting oxidative stress in disease: promise and limitations of antioxidant therapy. Nat Rev Drug Discov. 2021; 20(9):689-709. PMC: 8243062. DOI: 10.1038/s41573-021-00233-1. View

20.

Iovan D, Jia S, Chang C . Inorganic Chemistry Approaches to Activity-Based Sensing: From Metal Sensors to Bioorthogonal Metal Chemistry. Inorg Chem. 2019; 58(20):13546-13560. PMC: 8544879. DOI: 10.1021/acs.inorgchem.9b01221. View