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Title: Caged luciferins for bioluminescent activity-based sensing

Abstract

Bioluminescence imaging is a powerful modality for in vivo imaging owing to its low background and high signal-to-noise ratio. Because bioluminescent emission occurs only upon the catalytic reaction between the luciferase enzyme and its luciferin substrate, caging luciferins with analyte-reactive triggers offers a general approach for activity-based sensing of specific biochemical processes in living systems across cell, tissue, and animal models. In this review, we summarize recent efforts in the development of synthetic caged luciferins for tracking enzyme, small molecule, and metal ion activity and their contributions to physiological and pathological processes.

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Chemistry
  2. Univ. of California, Berkeley, CA (United States). Dept. of Chemistry, Dept. of Molecular and Cell Biology, Helen Willis Neuroscience Institute, and Howard Hughes Medical Institute
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Institutes of Health (NIH)
OSTI Identifier:
1559227
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Current Opinion in Biotechnology
Additional Journal Information:
Journal Volume: 60; Journal Issue: C; Journal ID: ISSN 0958-1669
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Su, Timothy A., Bruemmer, Kevin J., and Chang, Christopher J. Caged luciferins for bioluminescent activity-based sensing. United States: N. p., 2019. Web. doi:10.1016/j.copbio.2019.05.002.
Su, Timothy A., Bruemmer, Kevin J., & Chang, Christopher J. Caged luciferins for bioluminescent activity-based sensing. United States. https://doi.org/10.1016/j.copbio.2019.05.002
Su, Timothy A., Bruemmer, Kevin J., and Chang, Christopher J. Tue . "Caged luciferins for bioluminescent activity-based sensing". United States. https://doi.org/10.1016/j.copbio.2019.05.002. https://www.osti.gov/servlets/purl/1559227.
@article{osti_1559227,
title = {Caged luciferins for bioluminescent activity-based sensing},
author = {Su, Timothy A. and Bruemmer, Kevin J. and Chang, Christopher J.},
abstractNote = {Bioluminescence imaging is a powerful modality for in vivo imaging owing to its low background and high signal-to-noise ratio. Because bioluminescent emission occurs only upon the catalytic reaction between the luciferase enzyme and its luciferin substrate, caging luciferins with analyte-reactive triggers offers a general approach for activity-based sensing of specific biochemical processes in living systems across cell, tissue, and animal models. In this review, we summarize recent efforts in the development of synthetic caged luciferins for tracking enzyme, small molecule, and metal ion activity and their contributions to physiological and pathological processes.},
doi = {10.1016/j.copbio.2019.05.002},
journal = {Current Opinion in Biotechnology},
number = C,
volume = 60,
place = {United States},
year = {Tue Jun 11 00:00:00 EDT 2019},
month = {Tue Jun 11 00:00:00 EDT 2019}
}

Works referenced in this record:

Imaging in the era of molecular oncology
journal, April 2008


Molecular imaging in living subjects: seeing fundamental biological processes in a new light
journal, March 2003


Reaction-based small-molecule fluorescent probes for chemoselective bioimaging
journal, November 2012

  • Chan, Jefferson; Dodani, Sheel C.; Chang, Christopher J.
  • Nature Chemistry, Vol. 4, Issue 12
  • DOI: 10.1038/nchem.1500

Fluorometric chemodosimetry. Mercury(II) and silver(I) indication in water via enhanced fluorescence signaling
journal, November 1992

  • Chae, Mi Young; Czarnik, Anthony W.
  • Journal of the American Chemical Society, Vol. 114, Issue 24
  • DOI: 10.1021/ja00050a085

Detection and Imaging of Nitric Oxide with Novel Fluorescent Indicators:  Diaminofluoresceins
journal, July 1998

  • Kojima, Hirotatsu; Nakatsubo, Naoki; Kikuchi, Kazuya
  • Analytical Chemistry, Vol. 70, Issue 13
  • DOI: 10.1021/ac9801723

A Selective, Cell-Permeable Optical Probe for Hydrogen Peroxide in Living Cells
journal, December 2004

  • Chang, Michelle C. Y.; Pralle, Arnd; Isacoff, Ehud Y.
  • Journal of the American Chemical Society, Vol. 126, Issue 47
  • DOI: 10.1021/ja0441716

A synthetic luciferin improves bioluminescence imaging in live mice
journal, February 2014

  • Evans, Melanie S.; Chaurette, Joanna P.; Adams, Spencer T.
  • Nature Methods, Vol. 11, Issue 4
  • DOI: 10.1038/nmeth.2839

Advances in In Vivo Bioluminescence Imaging of Gene Expression
journal, August 2002


Lessons Learned from Luminous Luciferins and Latent Luciferases
journal, February 2018


Bioluminescent Probes for Imaging Biology beyond the Culture Dish
journal, July 2017


Cage the firefly luciferin! – a strategy for developing bioluminescent probes
journal, January 2013

  • Li, Jing; Chen, Laizhong; Du, Lupei
  • Chem. Soc. Rev., Vol. 42, Issue 2
  • DOI: 10.1039/C2CS35249D

In Vivo Molecular Bioluminescence Imaging: New Tools and Applications
journal, July 2017


A New Ultrasensitive Bioluminogenic Enzyme Substrate for β -Galactosidase
journal, January 1992


Synthesis and Characterization of a Bioluminogenic Substrate for α-Chymotrypsin
journal, September 1994


New Bioluminogenic Substrates for Monoamine Oxidase Assays
journal, March 2006

  • Zhou, Wenhui; Valley, Michael P.; Shultz, John
  • Journal of the American Chemical Society, Vol. 128, Issue 10
  • DOI: 10.1021/ja058519o

Electrophilic aromatic substituted luciferins as bioluminescent probes for glutathione S-transferase assays
journal, January 2006

  • Zhou, Wenhui; Shultz, John W.; Murphy, Nancy
  • Chemical Communications, Issue 44
  • DOI: 10.1039/b610682j

Proluciferin Acetals as Bioluminogenic Substrates for Cytochrome P450 Activity and Probes for CYP3A Inhibition
journal, September 2011

  • Meisenheimer, Poncho L.; Uyeda, H. Tetsuo; Ma, Dongping
  • Drug Metabolism and Disposition, Vol. 39, Issue 12
  • DOI: 10.1124/dmd.111.041541

Homogeneous, Bioluminescent Protease Assays: Caspase-3 as a Model
journal, March 2005

  • O’Brien, Martha A.; Daily, William J.; Hesselberth, P. Eric
  • Journal of Biomolecular Screening, Vol. 10, Issue 2
  • DOI: 10.1177/1087057104271865

A bioluminescence assay for aldehyde dehydrogenase activity
journal, March 2013

  • Duellman, Sarah J.; Valley, Michael P.; Kotraiah, Vinayaka
  • Analytical Biochemistry, Vol. 434, Issue 2
  • DOI: 10.1016/j.ab.2012.11.016

In vivo imaging of S-TRAIL-mediated tumor regression and apoptosis
journal, June 2005


Development of a Bioluminescent Nitroreductase Probe for Preclinical Imaging
journal, June 2015


In Vivo Bioluminescence Imaging of Furin Activity in Breast Cancer Cells Using Bioluminogenic Substrates
journal, July 2009

  • Dragulescu-Andrasi, Anca; Liang, Gaolin; Rao, Jianghong
  • Bioconjugate Chemistry, Vol. 20, Issue 8
  • DOI: 10.1021/bc9002508

A Bioluminogenic Substrate for In Vivo Imaging of β-Lactamase Activity
journal, September 2007

  • Yao, Hequan; So, Min-kyung; Rao, Jianghong
  • Angewandte Chemie International Edition, Vol. 46, Issue 37
  • DOI: 10.1002/anie.200701931

Visualizing cellular interactions with a generalized proximity reporter
journal, May 2013

  • Sellmyer, M. A.; Bronsart, L.; Imoto, H.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 21
  • DOI: 10.1073/pnas.1218336110

Luciferin Amides Enable in Vivo Bioluminescence Detection of Endogenous Fatty Acid Amide Hydrolase Activity
journal, July 2015

  • Mofford, David M.; Adams, Spencer T.; Reddy, G. S. Kiran Kumar
  • Journal of the American Chemical Society, Vol. 137, Issue 27
  • DOI: 10.1021/jacs.5b04357

Real-time analysis of uptake and bioactivatable cleavage of luciferin-transporter conjugates in transgenic reporter mice
journal, June 2007

  • Wender, P. A.; Goun, E. A.; Jones, L. R.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 25
  • DOI: 10.1073/pnas.0703919104

Real-Time Noninvasive Imaging of Fatty Acid Uptake in Vivo
journal, August 2012

  • Henkin, Amy H.; Cohen, Allison S.; Dubikovskaya, Elena A.
  • ACS Chemical Biology, Vol. 7, Issue 11
  • DOI: 10.1021/cb300194b

A branched-chain amino acid metabolite drives vascular fatty acid transport and causes insulin resistance
journal, March 2016

  • Jang, Cholsoon; Oh, Sungwhan F.; Wada, Shogo
  • Nature Medicine, Vol. 22, Issue 4
  • DOI: 10.1038/nm.4057

Chemistry and biology of reactive oxygen species in signaling or stress responses
journal, July 2011

  • Dickinson, Bryan C.; Chang, Christopher J.
  • Nature Chemical Biology, Vol. 7, Issue 8
  • DOI: 10.1038/nchembio.607

Searching for harmony in transition-metal signaling
journal, September 2015


Real-Time Bioluminescence Imaging of Glycans on Live Cells
journal, June 2010

  • Cohen, Allison S.; Dubikovskaya, Elena A.; Rush, Jason S.
  • Journal of the American Chemical Society, Vol. 132, Issue 25
  • DOI: 10.1021/ja101766r

In vivo imaging of hydrogen peroxide production in a murine tumor model with a chemoselective bioluminescent reporter
journal, November 2010

  • Van de Bittner, G. C.; Dubikovskaya, E. A.; Bertozzi, C. R.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 50
  • DOI: 10.1073/pnas.1012864107

Strategy for Dual-Analyte Luciferin Imaging: In Vivo Bioluminescence Detection of Hydrogen Peroxide and Caspase Activity in a Murine Model of Acute Inflammation
journal, January 2013

  • Van de Bittner, Genevieve C.; Bertozzi, Carolyn R.; Chang, Christopher J.
  • Journal of the American Chemical Society, Vol. 135, Issue 5
  • DOI: 10.1021/ja309078t

Acinetobacter baumannii OxyR Regulates the Transcriptional Response to Hydrogen Peroxide
journal, January 2019

  • Juttukonda, Lillian J.; Green, Erin R.; Lonergan, Zachery R.
  • Infection and Immunity, Vol. 87, Issue 1
  • DOI: 10.1128/IAI.00413-18

Development of a Sensitive Bioluminogenic Probe for Imaging Highly Reactive Oxygen Species in Living Rats
journal, October 2015

  • Kojima, Ryosuke; Takakura, Hideo; Kamiya, Mako
  • Angewandte Chemie International Edition, Vol. 54, Issue 49
  • DOI: 10.1002/anie.201507530

Visualization of in Vivo Hydrogen Sulfide Production by a Bioluminescence Probe in Cancer Cells and Nude Mice
journal, October 2015


A Bioluminescent Probe for Imaging Endogenous Peroxynitrite in Living Cells and Mice
journal, February 2018


Developing drugs targeting transition metal homeostasis
journal, April 2017


Metals, Toxicity and Oxidative Stress
journal, May 2005


In vivo bioluminescence imaging reveals copper deficiency in a murine model of nonalcoholic fatty liver disease
journal, November 2016

  • Heffern, Marie C.; Park, Hyo Min; Au-Yeung, Ho Yu
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 50
  • DOI: 10.1073/pnas.1613628113

A Modular Ionophore Platform for Liver-Directed Copper Supplementation in Cells and Animals
journal, September 2018

  • Su, Timothy A.; Shihadih, Diyala S.; Cao, Wendy
  • Journal of the American Chemical Society, Vol. 140, Issue 42
  • DOI: 10.1021/jacs.8b08014

In vivo bioluminescence imaging of labile iron accumulation in a murine model of Acinetobacter baumannii infection
journal, November 2017

  • Aron, Allegra T.; Heffern, Marie C.; Lonergan, Zachery R.
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 48
  • DOI: 10.1073/pnas.1708747114

A selective reaction-based fluorescent probe for detecting cobalt in living cells
journal, January 2012

  • Au-Yeung, Ho Yu; New, Elizabeth J.; Chang, Christopher J.
  • Chemical Communications, Vol. 48, Issue 43
  • DOI: 10.1039/c2cc31681a

In Vivo Bioluminescence Imaging of Cobalt Accumulation in a Mouse Model
journal, March 2018


Visualization of mercury( ii ) accumulation in vivo using bioluminescence imaging with a highly selective probe
journal, January 2018

  • Ke, Bowen; Chen, Hui; Ma, Lin
  • Organic & Biomolecular Chemistry, Vol. 16, Issue 14
  • DOI: 10.1039/C8OB00398J

Robust Light Emission from Cyclic Alkylaminoluciferin Substrates for Firefly Luciferase
journal, October 2010

  • Reddy, Gadarla Randheer; Thompson, Walter C.; Miller, Stephen C.
  • Journal of the American Chemical Society, Vol. 132, Issue 39
  • DOI: 10.1021/ja104525m

Development of simple firefly luciferin analogs emitting blue, green, red, and near-infrared biological window light
journal, May 2013


Parallel Screening for Rapid Identification of Orthogonal Bioluminescent Tools
journal, November 2017

  • Rathbun, Colin M.; Porterfield, William B.; Jones, Krysten A.
  • ACS Central Science, Vol. 3, Issue 12
  • DOI: 10.1021/acscentsci.7b00394

Luciferase Activity of Insect Fatty Acyl-CoA Synthetases with Synthetic Luciferins
journal, November 2017

  • Mofford, David M.; Liebmann, Kate L.; Sankaran, Ganapathy Subramanian
  • ACS Chemical Biology, Vol. 12, Issue 12
  • DOI: 10.1021/acschembio.7b00813

Statistical Coupling Analysis-Guided Library Design for the Discovery of Mutant Luciferases
journal, December 2017


Firefly Luciferase Mutants Allow Substrate-Selective Bioluminescence Imaging in the Mouse Brain
journal, March 2016

  • Adams, Spencer T.; Mofford, David M.; Reddy, G. S. Kiran Kumar
  • Angewandte Chemie International Edition, Vol. 55, Issue 16
  • DOI: 10.1002/anie.201511350

A Glowing Trajectory between Bio- and Chemiluminescence: From Luciferin-Based Probes to Triggerable Dioxetanes
journal, December 2017

  • Hananya, Nir; Shabat, Doron
  • Angewandte Chemie International Edition, Vol. 56, Issue 52
  • DOI: 10.1002/anie.201706969

Unlocking the Potential of Chemiluminescence Imaging
journal, March 2017


In Vivo Chemiluminescent Imaging Agents for Nitroreductase and Tissue Oxygenation
journal, April 2016


Unprecedented Sensitivity in a Probe for Monitoring Cathepsin B: Chemiluminescence Microscopy Cell-Imaging of a Natively Expressed Enzyme
journal, November 2017

  • Roth-Konforti, Michal E.; Bauer, Christoph R.; Shabat, Doron
  • Angewandte Chemie International Edition, Vol. 56, Issue 49
  • DOI: 10.1002/anie.201709347

Near-Infrared Dioxetane Luminophores with Direct Chemiluminescence Emission Mode
journal, September 2017

  • Green, Ori; Gnaim, Samer; Blau, Rachel
  • Journal of the American Chemical Society, Vol. 139, Issue 37
  • DOI: 10.1021/jacs.7b08446

Chemiluminescent Probes for Activity-Based Sensing of Formaldehyde Released from Folate Degradation in Living Mice
journal, April 2018

  • Bruemmer, Kevin J.; Green, Ori; Su, Timothy A.
  • Angewandte Chemie International Edition, Vol. 57, Issue 25
  • DOI: 10.1002/anie.201802143

A chemiluminescent probe for cellular peroxynitrite using a self-immolative oxidative decarbonylation reaction
journal, January 2018

  • Cao, Jian; An, Weiwei; Reeves, Audrey G.
  • Chemical Science, Vol. 9, Issue 9
  • DOI: 10.1039/C7SC05087A

Works referencing / citing this record:

Bioluminescence imaging of carbon monoxide in living cells based on a selective deiodination reaction
journal, January 2020


An Activity‐Based Sensing Approach for the Detection of Cyclooxygenase‐2 in Live Cells
journal, February 2020

  • Yadav, Anuj K.; Reinhardt, Christopher J.; Arango, Andres S.
  • Angewandte Chemie International Edition, Vol. 59, Issue 8
  • DOI: 10.1002/anie.201914845

An Activity‐Based Sensing Approach for the Detection of Cyclooxygenase‐2 in Live Cells
journal, January 2020

  • Yadav, Anuj K.; Reinhardt, Christopher J.; Arango, Andres S.
  • Angewandte Chemie, Vol. 132, Issue 8
  • DOI: 10.1002/ange.201914845