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Mitochondrial function provides instructive signals for activation-induced B-cell fates

Author

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  • Kyoung-Jin Jang

    (Institute for Advancement of Clinical and Translational Science, Kyoto University Hospital)

  • Hiroto Mano

    (Institute for Advancement of Clinical and Translational Science, Kyoto University Hospital)

  • Koji Aoki

    (School of Medicine, University of Fukui)

  • Tatsunari Hayashi

    (Institute for Advancement of Clinical and Translational Science, Kyoto University Hospital)

  • Akihiko Muto

    (Tohoku University Graduate School of Medicine
    CREST, Japan Science and Technology Agency)

  • Yukiko Nambu

    (Institute for Advancement of Clinical and Translational Science, Kyoto University Hospital
    Present address: Bioprocessing Technology Institute, A*STAR20 Biopolis Way #06-01 Centros, Singapore 138668, Singapore)

  • Katsu Takahashi

    (Kyoto University Hospital)

  • Katsuhiko Itoh

    (Graduate School of Medicine, Kyoto University)

  • Shigeru Taketani

    (Kyoto Institute of Technology)

  • Stephen L. Nutt

    (The Walter and Eliza Hall Institute of Medical Research
    University of Melbourne)

  • Kazuhiko Igarashi

    (Tohoku University Graduate School of Medicine
    CREST, Japan Science and Technology Agency)

  • Akira Shimizu

    (Institute for Advancement of Clinical and Translational Science, Kyoto University Hospital)

  • Manabu Sugai

    (Institute for Advancement of Clinical and Translational Science, Kyoto University Hospital
    School of Medicine, University of Fukui)

Abstract

During immune reactions, functionally distinct B-cell subsets are generated by stochastic processes, including class-switch recombination (CSR) and plasma cell differentiation (PCD). In this study, we show a strong association between individual B-cell fates and mitochondrial functions. CSR occurs specifically in activated B cells with increased mitochondrial mass and membrane potential, which augment mitochondrial reactive oxygen species (mROS), whereas PCD occurs in cells with decreased mitochondrial mass and potential. These events are consequences of initial slight changes in mROS in mitochondriahigh B-cell populations. In CSR-committed cells, mROS attenuates haeme synthesis by inhibiting ferrous ion addition to protoporphyrin IX, thereby maintaining Bach2 function. Reduced mROS then promotes PCD by increasing haeme synthesis. In PCD-committed cells, Blimp1 reduces mitochondrial mass, thereby reducing mROS levels. Identifying mROS as a haeme synthesis regulator increases the understanding of mechanisms regulating haeme homeostasis and cell fate determination after B-cell activation.

Suggested Citation

  • Kyoung-Jin Jang & Hiroto Mano & Koji Aoki & Tatsunari Hayashi & Akihiko Muto & Yukiko Nambu & Katsu Takahashi & Katsuhiko Itoh & Shigeru Taketani & Stephen L. Nutt & Kazuhiko Igarashi & Akira Shimizu , 2015. "Mitochondrial function provides instructive signals for activation-induced B-cell fates," Nature Communications, Nature, vol. 6(1), pages 1-13, November.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms7750
    DOI: 10.1038/ncomms7750
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    Cited by:

    1. Sophie Hillion & Anjelica Miranda & Christelle Dantec & Marina Boudigou & Laëtitia Pottier & Divi Cornec & Raul M. Torres & Roberta Pelanda, 2024. "Maf expression in B cells restricts reactive plasmablast and germinal center B cell expansion," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Marta Iborra-Pernichi & Jonathan Ruiz García & María Velasco de la Esperanza & Belén S. Estrada & Elena R. Bovolenta & Claudia Cifuentes & Cristina Prieto Carro & Tamara González Martínez & José Garcí, 2024. "Defective mitochondria remodelling in B cells leads to an aged immune response," Nature Communications, Nature, vol. 15(1), pages 1-20, December.

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