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    Ratiometric NAD+ Sensors Reveal Subcellular NAD+ Modulators
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    • Liuqing Chen
      Liuqing Chen
      Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China
      Shenzhen Key Laboratory for the Intelligent Microbial Manufacturing of Medicines, Shenzhen 518055, China
      More by Liuqing Chen
      Orcidhttps://orcid.org/0000-0002-2104-3697
    • Meiting Chen
      Meiting Chen
      Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China
      More by Meiting Chen
    • Mupeng Luo
      Mupeng Luo
      Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China
      More by Mupeng Luo
      Orcidhttps://orcid.org/0000-0002-1222-7830
    • Yong Li
      Yong Li
      Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China
      More by Yong Li
    • Bagen Liao
      Bagen Liao
      Guangdong Provincial Key Laboratory of Physical Activity and Health Promotion, Guangzhou Sport University, Guangzhou 510150, China
      More by Bagen Liao
    • Min Hu*
      Min Hu
      Guangdong Provincial Key Laboratory of Physical Activity and Health Promotion, Guangzhou Sport University, Guangzhou 510150, China
      *Email: [email protected]
      More by Min Hu
    • Qiuliyang Yu*
      Qiuliyang Yu
      Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China
      Shenzhen Key Laboratory for the Intelligent Microbial Manufacturing of Medicines, Shenzhen 518055, China
      *Email: [email protected]
      More by Qiuliyang Yu
      Orcidhttps://orcid.org/0000-0001-5877-6547
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    ACS Sensors

    Cite this: ACS Sens. 2023, 8, 4, 1518–1528
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    https://doi.org/10.1021/acssensors.2c02565
    Published March 17, 2023
    Copyright © 2023 American Chemical Society
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    Abstract

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    Mapping NAD+ dynamics in live cells and human is essential for translating NAD+ interventions into effective therapies. Yet, genetically encoded NAD+ sensors with better specificity and pH resistance are still needed for the cost-effective monitoring of NAD+ in both subcellular compartments and clinical samples. Here, we introduce multicolor, resonance energy transfer-based NAD+ sensors covering nano- to millimolar concentration ranges for clinical NAD+ measurement and subcellular NAD+ visualization. The sensors captured the blood NAD+ increase induced by NMN supplementation and revealed the distinct subcellular effects of NAD+ precursors and modulators. The sensors then enabled high-throughput screenings for mitochondrial and nuclear NAD+ modulators and identified α-GPC, a cognition-related metabolite that induces NAD+ redistribution from mitochondria to the nucleus relative to the total adenine nucleotides, which was further confirmed by NAD+ FRET microscopy.

    Copyright © 2023 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acssensors.2c02565.

    • Amino acid sequence of sensors; structure analysis of EfLigA; performance of NS-Goji 1.0, NS-Olive, and NS-Grapefruit; emission spectra of NS-Goji 1.3; representative microscopic images of cells stably express NS-Olive; western blot analysis of whole cell lysates; calibration curves for HEK 293T cells that stably express NS-Olive; NS-Goji reports compartmentalized NAD+ metabolism in live cells; cellular performance of NS-Grapefruit; representative donor, acceptor, and ratio images of nuclear and mitochondrial FRET signals of NS-Grapefruit; cellular PARylation level detected by the PARP1cd sensor; variations of cellular ATP concentrations evaluated by the ARSeNL sensor after α-GPC treatment; summary of NAD+ sensor performance; top 20 compounds for increasing NAD+ in nucleus and mitochondria; comparison of known genetically encoded NAD+ sensors (PDF)

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    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

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    This article is cited by 7 publications.

    1. Anneliese M. M. Gest, Ayse Z. Sahan, Yanghao Zhong, Wei Lin, Sohum Mehta, Jin Zhang. Molecular Spies in Action: Genetically Encoded Fluorescent Biosensors Light up Cellular Signals. Chemical Reviews 2024, 124 (22) , 12573-12660. https://doi.org/10.1021/acs.chemrev.4c00293
    2. Wenfei Guo, Haiyuan Wang, Zhaoyang Wang, Fandi Wu, Yao He, Yuan Liu, Yan Deng, Tao Bing, Liping Qiu, Weihong Tan. DNA aptamer-based sensitive electrochemical biosensor for NAD(H) detection. Biosensors and Bioelectronics 2025, 271 , 116996. https://doi.org/10.1016/j.bios.2024.116996
    3. Lucy Wanjiru Njunge, Kaijing Liu, Chenghe Xiong, Liuqing Chen, Qifei He, Pei Wang, Guan Huang, Yong Li, Peace Osebhue Abhulimen, Wenxiang Cheng, Qiuliyang Yu. Deficient QPRT drives trans-Golgi NAD + hyperinflation and pathological protein secretion in rheumatoid arthritis. 2024https://doi.org/10.1101/2024.10.27.24316032
    4. Marie E. Migaud, Mathias Ziegler, Joseph A. Baur. Regulation of and challenges in targeting NAD+ metabolism. Nature Reviews Molecular Cell Biology 2024, 25 (10) , 822-840. https://doi.org/10.1038/s41580-024-00752-w
    5. Patryk Chudy, Jakub Kochan, Mateusz Wawro, Phu Nguyen, Monika Gorczyca, Aliaksandra Varanko, Aleksandra Retka, Swati Sweta Ghadei, Emilija Napieralska, Anna Grochot-Przęczek, Krzysztof Szade, Lea-Sophie Berendes, Julien Park, Grzegorz Sokołowski, Qiuliyang Yu, Alicja Józkowicz, Witold N. Nowak, Wojciech Krzeptowski. Heme oxygenase-1 protects cells from replication stress. Redox Biology 2024, 75 , 103247. https://doi.org/10.1016/j.redox.2024.103247
    6. Liuqing Chen, Pei Wang, Guan Huang, Wenxiang Cheng, Kaijing Liu, Qiuliyang Yu. Quantitative dynamics of intracellular NMN by genetically encoded biosensor. 2023https://doi.org/10.1101/2023.10.23.563573
    7. Pei Wang, Meiting Chen, Yaying Hou, Jun Luan, Ruili Liu, Liuqing Chen, Min Hu, Qiuliyang Yu. Fingerstick blood assay maps real‐world NAD + disparity across gender and age. Aging Cell 2023, 22 (10) https://doi.org/10.1111/acel.13965
    8. Lars Hellweg, Anna Edenhofer, Lucas Barck, Magnus-Carsten Huppertz, Michelle. S. Frei, Miroslaw Tarnawski, Andrea Bergner, Birgit Koch, Kai Johnsson, Julien Hiblot. A general method for the development of multicolor biosensors with large dynamic ranges. Nature Chemical Biology 2023, 19 (9) , 1147-1157. https://doi.org/10.1038/s41589-023-01350-1
    9. Scott N. Lyons, Xiaolu A. Cambronne. A chemical solution for FRET(ful) pairs. Nature Chemical Biology 2023, 19 (9) , 1048-1049. https://doi.org/10.1038/s41589-023-01403-5
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    ACS Sensors

    Cite this: ACS Sens. 2023, 8, 4, 1518–1528
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acssensors.2c02565
    Published March 17, 2023
    Copyright © 2023 American Chemical Society
    Request reuse permissions

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