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Regulation of meiotic telomere dynamics through membrane fluidity promoted by AdipoR2-ELOVL2

Author

Listed:
  • Jingjing Zhang

    (University of Gothenburg)

  • Mario Ruiz

    (University of Gothenburg)

  • Per-Olof Bergh

    (University of Gothenburg)

  • Marcus Henricsson

    (University of Gothenburg)

  • Nena Stojanović

    (University of Gothenburg)

  • Ranjan Devkota

    (University of Gothenburg)

  • Marius Henn

    (University of Würzburg)

  • Mohammad Bohlooly-Y

    (BioPharmaceuticals R&D, AstraZeneca)

  • Abrahan Hernández-Hernández

    (Karolinska Institutet
    Department of Cell and Molecular Biology, Karolinska Institute)

  • Manfred Alsheimer

    (University of Würzburg)

  • Jan Borén

    (University of Gothenburg)

  • Marc Pilon

    (University of Gothenburg)

  • Hiroki Shibuya

    (University of Gothenburg
    RIKEN Center for Biosystems Dynamics Research (BDR))

Abstract

The cellular membrane in male meiotic germ cells contains a unique class of phospholipids and sphingolipids that is required for male reproduction. Here, we show that a conserved membrane fluidity sensor, AdipoR2, regulates the meiosis-specific lipidome in mouse testes by promoting the synthesis of sphingolipids containing very-long-chain polyunsaturated fatty acids (VLC-PUFAs). AdipoR2 upregulates the expression of a fatty acid elongase, ELOVL2, both transcriptionally and post-transcriptionally, to synthesize VLC-PUFA. The depletion of VLC-PUFAs and subsequent accumulation of palmitic acid in AdipoR2 knockout testes stiffens the cellular membrane and causes the invagination of the nuclear envelope. This condition impairs the nuclear peripheral distribution of meiotic telomeres, leading to errors in homologous synapsis and recombination. Further, the stiffened membrane impairs the formation of intercellular bridges and the germ cell syncytium, which disrupts the orderly arrangement of cell types within the seminiferous tubules. According to our findings we propose a framework in which the highly-fluid membrane microenvironment shaped by AdipoR2-ELOVL2 underpins meiosis-specific chromosome dynamics in testes.

Suggested Citation

  • Jingjing Zhang & Mario Ruiz & Per-Olof Bergh & Marcus Henricsson & Nena Stojanović & Ranjan Devkota & Marius Henn & Mohammad Bohlooly-Y & Abrahan Hernández-Hernández & Manfred Alsheimer & Jan Borén &, 2024. "Regulation of meiotic telomere dynamics through membrane fluidity promoted by AdipoR2-ELOVL2," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46718-6
    DOI: 10.1038/s41467-024-46718-6
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    References listed on IDEAS

    as
    1. Mario Ruiz & Ranjan Devkota & Dimitra Panagaki & Per-Olof Bergh & Delaney Kaper & Marcus Henricsson & Ali Nik & Kasparas Petkevicius & Johanna L. Höög & Mohammad Bohlooly-Y & Peter Carlsson & Jan Boré, 2022. "Sphingosine 1-phosphate mediates adiponectin receptor signaling essential for lipid homeostasis and embryogenesis," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    2. Dennis S. Rice & Jorgelina M. Calandria & William C. Gordon & Bokkyoo Jun & Yongdong Zhou & Claire M. Gelfman & Songhua Li & Minghao Jin & Eric J. Knott & Bo Chang & Alex Abuin & Tawfik Issa & David P, 2015. "Correction: Corrigendum: Adiponectin receptor 1 conserves docosahexaenoic acid and promotes photoreceptor cell survival," Nature Communications, Nature, vol. 6(1), pages 1-1, November.
    3. Dennis S. Rice & Jorgelina M. Calandria & William C. Gordon & Bokkyoo Jun & Yongdong Zhou & Claire M. Gelfman & Songhua Li & Minghao Jin & Eric J. Knott & Bo Chang & Alex Abuin & Tawfik Issa & David P, 2015. "Adiponectin receptor 1 conserves docosahexaenoic acid and promotes photoreceptor cell survival," Nature Communications, Nature, vol. 6(1), pages 1-15, May.
    4. Jingjing Zhang & Yasuhiro Fujiwara & Shohei Yamamoto & Hiroki Shibuya, 2019. "Publisher Correction: A meiosis-specific BRCA2 binding protein recruits recombinases to DNA double-strand breaks to ensure homologous recombination," Nature Communications, Nature, vol. 10(1), pages 1-1, December.
    5. Jingjing Zhang & Yasuhiro Fujiwara & Shohei Yamamoto & Hiroki Shibuya, 2019. "A meiosis-specific BRCA2 binding protein recruits recombinases to DNA double-strand breaks to ensure homologous recombination," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
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