Dual-Channel Fluorescent Probe for the Simultaneous Monitoring of Peroxynitrite and Adenosine-5′-triphosphate in Cellular Applications

Luling Wu; Jihong Liu; Xue Tian; Robin R. Groleau; Beidou Feng; Yonggang Yang; Adam C. Sedgwick; Hai Hao Han; Yang Wang; Han Min Wang; Fang Huang; Steven D. Bull; Hua Zhang; Chusen Huang; Yi Zang; Jia Li; Xiao Peng He; Ping Li; Bo Tang; Tony D. James; Jonathan L. Sessler

doi:10.1021/jacs.1c07954

Dual-Channel Fluorescent Probe for the Simultaneous Monitoring of Peroxynitrite and Adenosine-5′-triphosphate in Cellular Applications

Luling Wu, Jihong Liu, Xue Tian, Robin R. Groleau, Beidou Feng, Yonggang Yang, Adam C. Sedgwick, Hai Hao Han, Yang Wang, Han Min Wang, Fang Huang, Steven D. Bull, Hua Zhang, Chusen Huang, Yi Zang, Jia Li, Xiao Peng He, Ping Li, Bo Tang, Tony D. JamesJonathan L. Sessler

Research output: Contribution to journal › Article › peer-review

134 Citations (SciVal)

Abstract

Changes in adenosine triphosphate (ATP) and peroxynitrite (ONOO-) concentrations have been correlated in a number of diseases including ischemia-reperfusion injury and drug-induced liver injury. Herein, we report the development of a fluorescent probe ATP-LW, which enables the simultaneous detection of ONOO- and ATP. ONOO- selectively oxidizes the boronate pinacol ester of ATP-LW to afford the fluorescent 4-hydroxy-1,8-naphthalimide product NA-OH (λex = 450 nm, λem = 562 nm or λex = 488 nm, λem = 568 nm). In contrast, the binding of ATP to ATP-LW induces the spirolactam ring opening of rhodamine to afford a highly emissive product (λex = 520 nm, λem = 587 nm). Due to the differences in emission between the ONOO- and ATP products, ATP-LW allows ONOO- levels to be monitored in the green channel (λex = 488 nm, λem = 500-575 nm) and ATP concentrations in the red channel (λex = 514 nm, λem = 575-650 nm). The use of ATP-LW as a combined ONOO- and ATP probe was demonstrated using hepatocytes (HL-7702 cells) in cellular imaging experiments. Treatment of HL-7702 cells with oligomycin A (an inhibitor of ATP synthase) resulted in a reduction of signal intensity in the red channel and an increase in that of the green channel as expected for a reduction in ATP concentrations. Similar fluorescence changes were seen in the presence of SIN-1 (an exogenous ONOO- donor).

Original language	English
Pages (from-to)	174-183
Number of pages	10
Journal	Journal of the American Chemical Society
Volume	144
Issue number	1
Early online date	21 Dec 2021
DOIs	https://doi.org/10.1021/jacs.1c07954
Publication status	Published - 12 Jan 2022

Bibliographical note

Funding Information:
L.W. wishes to thank China Scholarship Council and the University of Bath for supporting his Ph.D. in the UK. R.R.G. wishes to thank the EPSRC Centre for Doctoral Training in Catalysis (EP/L016443/1). We would like to thank the EPSRC and the University of Bath for funding. T.D.J. wishes to thank the Royal Society for a Wolfson Research Merit Award and the Open Research Fund of the School of Chemistry and Chemical Engineering, Henan Normal University, for support (2020ZD01). P.L. and B.T. thank the National Natural Science Foundation of China (21927811, 22074083), the Key Research and Development Program of Shandong Province (2018YFJH0502), and the National Science Foundation of Shandong Province of China (ZR2020ZD17). C.H. thanks the National Natural Science Foundation of China (Grants 21672150, 21302125), Alexander von Humboldt Foundation (AvH), Shanghai Rising-Star Program (19QA1406400), and the Shanghai Government (18DZ2254200). H.-H.H. would like to thank the Project funded by China Postdoctoral Science Foundation (No. 2020M681196). X.-P.H. thanks the National Natural Science Foundation (No. 91853201), the Shanghai Municipal Science and Technology Major Project (2018SHZDZX03), the National Key Sci-Tech Special Projects of Infection Diseases of China (2018ZX10732202), and the International Cooperation Program of Shanghai Science and Technology Committee (17520750100). H.Z. thanks the National Natural Science Foundation of China (21722501, 11974103), the Zhongyuan High Level Talents Special Support Plan─Science and Technology Innovation Leading Talents (204200510006), and Program for Science Technology Innovation Talents in Universities of Henan Province (21HASTIT019). J.L.S. thanks the Robert A. Welch Foundation (F-0018) for support. NMR spectroscopic and mass spectrometric services were provided by the Material and Chemical Characterisation Facility (MC) at the University of Bath ( http://go.bath.ac.uk/mc2 ), and we would like to thank Dr. John Lowe for his support with characterization. We are also grateful to Feng-Ming Liu, Yao Li, and Yang Yu from the National Facility for Protein Science in Shanghai (NFPS) for their kind discussions on preliminary bioimaging experiments. 2

Funding

L.W. wishes to thank China Scholarship Council and the University of Bath for supporting his Ph.D. in the UK. R.R.G. wishes to thank the EPSRC Centre for Doctoral Training in Catalysis (EP/L016443/1). We would like to thank the EPSRC and the University of Bath for funding. T.D.J. wishes to thank the Royal Society for a Wolfson Research Merit Award and the Open Research Fund of the School of Chemistry and Chemical Engineering, Henan Normal University, for support (2020ZD01). P.L. and B.T. thank the National Natural Science Foundation of China (21927811, 22074083), the Key Research and Development Program of Shandong Province (2018YFJH0502), and the National Science Foundation of Shandong Province of China (ZR2020ZD17). C.H. thanks the National Natural Science Foundation of China (Grants 21672150, 21302125), Alexander von Humboldt Foundation (AvH), Shanghai Rising-Star Program (19QA1406400), and the Shanghai Government (18DZ2254200). H.-H.H. would like to thank the Project funded by China Postdoctoral Science Foundation (No. 2020M681196). X.-P.H. thanks the National Natural Science Foundation (No. 91853201), the Shanghai Municipal Science and Technology Major Project (2018SHZDZX03), the National Key Sci-Tech Special Projects of Infection Diseases of China (2018ZX10732202), and the International Cooperation Program of Shanghai Science and Technology Committee (17520750100). H.Z. thanks the National Natural Science Foundation of China (21722501, 11974103), the Zhongyuan High Level Talents Special Support Plan─Science and Technology Innovation Leading Talents (204200510006), and Program for Science Technology Innovation Talents in Universities of Henan Province (21HASTIT019). J.L.S. thanks the Robert A. Welch Foundation (F-0018) for support. NMR spectroscopic and mass spectrometric services were provided by the Material and Chemical Characterisation Facility (MC) at the University of Bath ( http://go.bath.ac.uk/mc2 ), and we would like to thank Dr. John Lowe for his support with characterization. We are also grateful to Feng-Ming Liu, Yao Li, and Yang Yu from the National Facility for Protein Science in Shanghai (NFPS) for their kind discussions on preliminary bioimaging experiments. 2

ASJC Scopus subject areas

Catalysis
General Chemistry
Biochemistry
Colloid and Surface Chemistry

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Cite this

Wu, L., Liu, J., Tian, X., Groleau, R. R., Feng, B., Yang, Y., Sedgwick, A. C., Han, H. H., Wang, Y., Wang, H. M., Huang, F., Bull, S. D., Zhang, H., Huang, C., Zang, Y., Li, J., He, X. P., Li, P., Tang, B., ... Sessler, J. L. (2022). Dual-Channel Fluorescent Probe for the Simultaneous Monitoring of Peroxynitrite and Adenosine-5′-triphosphate in Cellular Applications. Journal of the American Chemical Society, 144(1), 174-183. https://doi.org/10.1021/jacs.1c07954

Wu, L, Liu, J, Tian, X , Groleau, RR, Feng, B, Yang, Y, Sedgwick, AC, Han, HH, Wang, Y, Wang, HM, Huang, F, Bull, SD, Zhang, H, Huang, C, Zang, Y, Li, J, He, XP, Li, P, Tang, B, James, TD & Sessler, JL 2022, 'Dual-Channel Fluorescent Probe for the Simultaneous Monitoring of Peroxynitrite and Adenosine-5′-triphosphate in Cellular Applications', Journal of the American Chemical Society, vol. 144, no. 1, pp. 174-183. https://doi.org/10.1021/jacs.1c07954

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title = "Dual-Channel Fluorescent Probe for the Simultaneous Monitoring of Peroxynitrite and Adenosine-5′-triphosphate in Cellular Applications",

abstract = "Changes in adenosine triphosphate (ATP) and peroxynitrite (ONOO-) concentrations have been correlated in a number of diseases including ischemia-reperfusion injury and drug-induced liver injury. Herein, we report the development of a fluorescent probe ATP-LW, which enables the simultaneous detection of ONOO- and ATP. ONOO- selectively oxidizes the boronate pinacol ester of ATP-LW to afford the fluorescent 4-hydroxy-1,8-naphthalimide product NA-OH (λex = 450 nm, λem = 562 nm or λex = 488 nm, λem = 568 nm). In contrast, the binding of ATP to ATP-LW induces the spirolactam ring opening of rhodamine to afford a highly emissive product (λex = 520 nm, λem = 587 nm). Due to the differences in emission between the ONOO- and ATP products, ATP-LW allows ONOO- levels to be monitored in the green channel (λex = 488 nm, λem = 500-575 nm) and ATP concentrations in the red channel (λex = 514 nm, λem = 575-650 nm). The use of ATP-LW as a combined ONOO- and ATP probe was demonstrated using hepatocytes (HL-7702 cells) in cellular imaging experiments. Treatment of HL-7702 cells with oligomycin A (an inhibitor of ATP synthase) resulted in a reduction of signal intensity in the red channel and an increase in that of the green channel as expected for a reduction in ATP concentrations. Similar fluorescence changes were seen in the presence of SIN-1 (an exogenous ONOO- donor). ",

author = "Luling Wu and Jihong Liu and Xue Tian and Groleau, {Robin R.} and Beidou Feng and Yonggang Yang and Sedgwick, {Adam C.} and Han, {Hai Hao} and Yang Wang and Wang, {Han Min} and Fang Huang and Bull, {Steven D.} and Hua Zhang and Chusen Huang and Yi Zang and Jia Li and He, {Xiao Peng} and Ping Li and Bo Tang and James, {Tony D.} and Sessler, {Jonathan L.}",

note = "Funding Information: L.W. wishes to thank China Scholarship Council and the University of Bath for supporting his Ph.D. in the UK. R.R.G. wishes to thank the EPSRC Centre for Doctoral Training in Catalysis (EP/L016443/1). We would like to thank the EPSRC and the University of Bath for funding. T.D.J. wishes to thank the Royal Society for a Wolfson Research Merit Award and the Open Research Fund of the School of Chemistry and Chemical Engineering, Henan Normal University, for support (2020ZD01). P.L. and B.T. thank the National Natural Science Foundation of China (21927811, 22074083), the Key Research and Development Program of Shandong Province (2018YFJH0502), and the National Science Foundation of Shandong Province of China (ZR2020ZD17). C.H. thanks the National Natural Science Foundation of China (Grants 21672150, 21302125), Alexander von Humboldt Foundation (AvH), Shanghai Rising-Star Program (19QA1406400), and the Shanghai Government (18DZ2254200). H.-H.H. would like to thank the Project funded by China Postdoctoral Science Foundation (No. 2020M681196). X.-P.H. thanks the National Natural Science Foundation (No. 91853201), the Shanghai Municipal Science and Technology Major Project (2018SHZDZX03), the National Key Sci-Tech Special Projects of Infection Diseases of China (2018ZX10732202), and the International Cooperation Program of Shanghai Science and Technology Committee (17520750100). H.Z. thanks the National Natural Science Foundation of China (21722501, 11974103), the Zhongyuan High Level Talents Special Support Plan─Science and Technology Innovation Leading Talents (204200510006), and Program for Science Technology Innovation Talents in Universities of Henan Province (21HASTIT019). J.L.S. thanks the Robert A. Welch Foundation (F-0018) for support. NMR spectroscopic and mass spectrometric services were provided by the Material and Chemical Characterisation Facility (MC) at the University of Bath ( http://go.bath.ac.uk/mc2 ), and we would like to thank Dr. John Lowe for his support with characterization. We are also grateful to Feng-Ming Liu, Yao Li, and Yang Yu from the National Facility for Protein Science in Shanghai (NFPS) for their kind discussions on preliminary bioimaging experiments. 2 ",

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T1 - Dual-Channel Fluorescent Probe for the Simultaneous Monitoring of Peroxynitrite and Adenosine-5′-triphosphate in Cellular Applications

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AU - Liu, Jihong

AU - Tian, Xue

AU - Groleau, Robin R.

AU - Feng, Beidou

AU - Yang, Yonggang

AU - Sedgwick, Adam C.

AU - Han, Hai Hao

AU - Wang, Yang

AU - Wang, Han Min

AU - Huang, Fang

AU - Bull, Steven D.

AU - Zhang, Hua

AU - Huang, Chusen

AU - Zang, Yi

AU - Li, Jia

AU - He, Xiao Peng

AU - Li, Ping

AU - Tang, Bo

AU - James, Tony D.

AU - Sessler, Jonathan L.

N1 - Funding Information: L.W. wishes to thank China Scholarship Council and the University of Bath for supporting his Ph.D. in the UK. R.R.G. wishes to thank the EPSRC Centre for Doctoral Training in Catalysis (EP/L016443/1). We would like to thank the EPSRC and the University of Bath for funding. T.D.J. wishes to thank the Royal Society for a Wolfson Research Merit Award and the Open Research Fund of the School of Chemistry and Chemical Engineering, Henan Normal University, for support (2020ZD01). P.L. and B.T. thank the National Natural Science Foundation of China (21927811, 22074083), the Key Research and Development Program of Shandong Province (2018YFJH0502), and the National Science Foundation of Shandong Province of China (ZR2020ZD17). C.H. thanks the National Natural Science Foundation of China (Grants 21672150, 21302125), Alexander von Humboldt Foundation (AvH), Shanghai Rising-Star Program (19QA1406400), and the Shanghai Government (18DZ2254200). H.-H.H. would like to thank the Project funded by China Postdoctoral Science Foundation (No. 2020M681196). X.-P.H. thanks the National Natural Science Foundation (No. 91853201), the Shanghai Municipal Science and Technology Major Project (2018SHZDZX03), the National Key Sci-Tech Special Projects of Infection Diseases of China (2018ZX10732202), and the International Cooperation Program of Shanghai Science and Technology Committee (17520750100). H.Z. thanks the National Natural Science Foundation of China (21722501, 11974103), the Zhongyuan High Level Talents Special Support Plan─Science and Technology Innovation Leading Talents (204200510006), and Program for Science Technology Innovation Talents in Universities of Henan Province (21HASTIT019). J.L.S. thanks the Robert A. Welch Foundation (F-0018) for support. NMR spectroscopic and mass spectrometric services were provided by the Material and Chemical Characterisation Facility (MC) at the University of Bath ( http://go.bath.ac.uk/mc2 ), and we would like to thank Dr. John Lowe for his support with characterization. We are also grateful to Feng-Ming Liu, Yao Li, and Yang Yu from the National Facility for Protein Science in Shanghai (NFPS) for their kind discussions on preliminary bioimaging experiments. 2

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N2 - Changes in adenosine triphosphate (ATP) and peroxynitrite (ONOO-) concentrations have been correlated in a number of diseases including ischemia-reperfusion injury and drug-induced liver injury. Herein, we report the development of a fluorescent probe ATP-LW, which enables the simultaneous detection of ONOO- and ATP. ONOO- selectively oxidizes the boronate pinacol ester of ATP-LW to afford the fluorescent 4-hydroxy-1,8-naphthalimide product NA-OH (λex = 450 nm, λem = 562 nm or λex = 488 nm, λem = 568 nm). In contrast, the binding of ATP to ATP-LW induces the spirolactam ring opening of rhodamine to afford a highly emissive product (λex = 520 nm, λem = 587 nm). Due to the differences in emission between the ONOO- and ATP products, ATP-LW allows ONOO- levels to be monitored in the green channel (λex = 488 nm, λem = 500-575 nm) and ATP concentrations in the red channel (λex = 514 nm, λem = 575-650 nm). The use of ATP-LW as a combined ONOO- and ATP probe was demonstrated using hepatocytes (HL-7702 cells) in cellular imaging experiments. Treatment of HL-7702 cells with oligomycin A (an inhibitor of ATP synthase) resulted in a reduction of signal intensity in the red channel and an increase in that of the green channel as expected for a reduction in ATP concentrations. Similar fluorescence changes were seen in the presence of SIN-1 (an exogenous ONOO- donor).

AB - Changes in adenosine triphosphate (ATP) and peroxynitrite (ONOO-) concentrations have been correlated in a number of diseases including ischemia-reperfusion injury and drug-induced liver injury. Herein, we report the development of a fluorescent probe ATP-LW, which enables the simultaneous detection of ONOO- and ATP. ONOO- selectively oxidizes the boronate pinacol ester of ATP-LW to afford the fluorescent 4-hydroxy-1,8-naphthalimide product NA-OH (λex = 450 nm, λem = 562 nm or λex = 488 nm, λem = 568 nm). In contrast, the binding of ATP to ATP-LW induces the spirolactam ring opening of rhodamine to afford a highly emissive product (λex = 520 nm, λem = 587 nm). Due to the differences in emission between the ONOO- and ATP products, ATP-LW allows ONOO- levels to be monitored in the green channel (λex = 488 nm, λem = 500-575 nm) and ATP concentrations in the red channel (λex = 514 nm, λem = 575-650 nm). The use of ATP-LW as a combined ONOO- and ATP probe was demonstrated using hepatocytes (HL-7702 cells) in cellular imaging experiments. Treatment of HL-7702 cells with oligomycin A (an inhibitor of ATP synthase) resulted in a reduction of signal intensity in the red channel and an increase in that of the green channel as expected for a reduction in ATP concentrations. Similar fluorescence changes were seen in the presence of SIN-1 (an exogenous ONOO- donor).

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Dual-Channel Fluorescent Probe for the Simultaneous Monitoring of Peroxynitrite and Adenosine-5′-triphosphate in Cellular Applications

Abstract

Bibliographical note

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