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SUN1/2 controls macrophage polarization via modulating nuclear size and stiffness

Author

Listed:
  • Shi Jiao

    (Fudan University)

  • Chuanchuan Li

    (University of Chinese Academy of Sciences
    Memorial Sloan Kettering Cancer Center)

  • Fenghua Guo

    (Fudan University Shanghai Medical College)

  • Jinjin Zhang

    (Chinese Academy of Sciences)

  • Hui Zhang

    (Fudan University)

  • Zhifa Cao

    (Tongji University School of Medicine)

  • Wenjia Wang

    (Fudan University)

  • Wenbo Bu

    (Fudan University)

  • Mobin Lin

    (Tongji University School of Medicine)

  • Junhong Lü

    (Chinese Academy of Sciences
    Binzhou Medical University)

  • Zhaocai Zhou

    (Fudan University
    Tongji University School of Medicine
    Nanjing Medical University)

Abstract

Alteration of the size and stiffness of the nucleus triggered by environmental cues are thought to be important for eukaryotic cell fate and function. However, it remains unclear how context-dependent nuclear remodeling occurs and reprograms gene expression. Here we identify the nuclear envelope proteins SUN1/2 as mechano-regulators of the nucleus during M1 polarization of the macrophage. Specifically, we show that LPS treatment decreases the protein levels of SUN1/2 in a CK2-βTrCP-dependent manner to shrink and soften the nucleus, therefore altering the chromatin accessibility for M1-associated gene expression. Notably, the transmembrane helix of SUN1/2 is solely required and sufficient for the nuclear mechano-remodeling. Consistently, SUN1/2 depletion in macrophages facilitates their phagocytosis, tissue infiltration, and proinflammatory cytokine production, thereby boosting the antitumor immunity in mice. Thus, our study demonstrates that, in response to inflammatory cues, SUN1/2 proteins act as mechano-regulators to remodel the nucleus and chromatin for M1 polarization of the macrophage.

Suggested Citation

  • Shi Jiao & Chuanchuan Li & Fenghua Guo & Jinjin Zhang & Hui Zhang & Zhifa Cao & Wenjia Wang & Wenbo Bu & Mobin Lin & Junhong Lü & Zhaocai Zhou, 2023. "SUN1/2 controls macrophage polarization via modulating nuclear size and stiffness," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42187-5
    DOI: 10.1038/s41467-023-42187-5
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    References listed on IDEAS

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    1. Maili Zimmermann & Francisco Bianchetto Aguilera & Monica Castellucci & Marzia Rossato & Sara Costa & Claudio Lunardi & Renato Ostuni & Giampiero Girolomoni & Gioacchino Natoli & Flavia Bazzoni & Nico, 2015. "Chromatin remodelling and autocrine TNFα are required for optimal interleukin-6 expression in activated human neutrophils," Nature Communications, Nature, vol. 6(1), pages 1-14, May.
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