IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-55302-x.html
   My bibliography  Save this article

A family of NADPH/NADP+ biosensors reveals in vivo dynamics of central redox metabolism across eukaryotes

Author

Listed:
  • Marie Scherschel

    (Saarland University)

  • Jan-Ole Niemeier

    (Schlossplatz 8)

  • Lianne J. H. C. Jacobs

    (University of Cologne)

  • Markus D. A. Hoffmann

    (Saarland University)

  • Anika Diederich

    (Saarland University)

  • Christopher Bell

    (Schlossplatz 8)

  • Pascal Höhne

    (Saarland University
    Schlossplatz 8)

  • Sonja Raetz

    (Schlossplatz 8)

  • Johanna B. Kroll

    (Schlossplatz 8)

  • Janina Steinbeck

    (Schlossplatz 8)

  • Sophie Lichtenauer

    (Schlossplatz 8)

  • Jan Multhoff

    (Schlossplatz 8)

  • Jannik Zimmermann

    (Saarland University)

  • Tanmay Sadhanasatish

    (Schlossplatz 5)

  • R. Alexander Rothemann

    (University of Cologne)

  • Carsten Grashoff

    (Schlossplatz 5)

  • Joris Messens

    (Vlaams Instituut voor Biotechnologie
    Vrije Universiteit Brussel
    Vrije Universiteit Brussel)

  • Emmanuel Ampofo

    (Saarland University)

  • Matthias W. Laschke

    (Saarland University)

  • Jan Riemer

    (University of Cologne
    University of Cologne)

  • Leticia Prates Roma

    (Saarland University)

  • Markus Schwarzländer

    (Schlossplatz 8)

  • Bruce Morgan

    (Saarland University)

Abstract

The NADPH/NADP+ redox couple is central to metabolism and redox signalling. NADP redox state is differentially regulated by distinct enzymatic machineries at the subcellular compartment level. Nonetheless, a detailed understanding of subcellular NADP redox dynamics is limited by the availability of appropriate tools. Here, we introduce NAPstars, a family of genetically encoded, fluorescent protein-based NADP redox state biosensors. NAPstars offer real-time, specific measurements, across a broad-range of NADP redox states, with subcellular resolution. NAPstar measurements in yeast, plants, and mammalian cell models, reveal a conserved robustness of cytosolic NADP redox homoeostasis. NAPstars uncover cell cycle-linked NADP redox oscillations in yeast and illumination- and hypoxia-dependent NADP redox changes in plant leaves. By applying NAPstars in combination with selective impairment of the glutathione and thioredoxin antioxidative pathways under acute oxidative challenge, we find an unexpected and conserved role for the glutathione system as the primary mediator of antioxidative electron flux.

Suggested Citation

  • Marie Scherschel & Jan-Ole Niemeier & Lianne J. H. C. Jacobs & Markus D. A. Hoffmann & Anika Diederich & Christopher Bell & Pascal Höhne & Sonja Raetz & Johanna B. Kroll & Janina Steinbeck & Sophie Li, 2024. "A family of NADPH/NADP+ biosensors reveals in vivo dynamics of central redox metabolism across eukaryotes," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-55302-x
    DOI: 10.1038/s41467-024-55302-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-55302-x
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-55302-x?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Jinhong Liu & Shey-Li Lim & Jia Yi Zhong & Boon Leong Lim, 2022. "Bioenergetics of pollen tube growth in Arabidopsis thaliana revealed by ratiometric genetically encoded biosensors," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    2. Linda Liedgens & Jannik Zimmermann & Lucas Wäschenbach & Fabian Geissel & Hugo Laporte & Holger Gohlke & Bruce Morgan & Marcel Deponte, 2020. "Quantitative assessment of the determinant structural differences between redox-active and inactive glutaredoxins," Nature Communications, Nature, vol. 11(1), pages 1-18, December.
    3. Pamela E. Molinari & Adriana R. Krapp & Andrea Weiner & Hannes M. Beyer & Arun Kumar Kondadi & Tim Blomeier & Melina López & Pilar Bustos-Sanmamed & Evelyn Tevere & Wilfried Weber & Andreas S. Reicher, 2023. "NERNST: a genetically-encoded ratiometric non-destructive sensing tool to estimate NADP(H) redox status in bacterial, plant and animal systems," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Elizabeth M. Corteselli & Mona Sharafi & Robert Hondal & Maximilian MacPherson & Sheryl White & Ying-Wai Lam & Clarissa Gold & Allison M. Manuel & Albert Vliet & Severin T. Schneebeli & Vikas Anathy &, 2023. "Structural and functional fine mapping of cysteines in mammalian glutaredoxin reveal their differential oxidation susceptibility," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Pascal Mrozek & Stephan Grunewald & Katrin Treffon & Gereon Poschmann & Fabian Rabe von Pappenheim & Kai Tittmann & Christiane Gatz, 2025. "Molecular basis for the enzymatic inactivity of class III glutaredoxin ROXY9 on standard glutathionylated substrates," Nature Communications, Nature, vol. 16(1), pages 1-15, December.
    3. Fabian Geissel & Lukas Lang & Britta Husemann & Bruce Morgan & Marcel Deponte, 2024. "Deciphering the mechanism of glutaredoxin-catalyzed roGFP2 redox sensing reveals a ternary complex with glutathione for protein disulfide reduction," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-55302-x. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.