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Single-molecule localization microscopy reveals the ultrastructural constitution of distal appendages in expanded mammalian centrioles

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  • Ting-Jui Ben Chang

    (National Taiwan University
    National Taiwan University
    Academia Sinica and National Taiwan University)

  • Jimmy Ching-Cheng Hsu

    (National Taiwan University)

  • T. Tony Yang

    (National Taiwan University
    National Taiwan University)

Abstract

Distal appendages (DAPs) are vital in cilia formation, mediating vesicular and ciliary docking to the plasma membrane during early ciliogenesis. Although numerous DAP proteins arranging a nine-fold symmetry have been studied using superresolution microscopy analyses, the extensive ultrastructural understanding of the DAP structure developing from the centriole wall remains elusive owing to insufficient resolution. Here, we proposed a pragmatic imaging strategy for two-color single-molecule localization microscopy of expanded mammalian DAP. Importantly, our imaging workflow enables us to push the resolution limit of a light microscope well close to a molecular level, thus achieving an unprecedented mapping resolution inside intact cells. Upon this workflow, we unravel the ultra-resolved higher-order protein complexes of the DAP and its associated proteins. Intriguingly, our images show that C2CD3, microtubule triplet, MNR, CEP90, OFD1, and ODF2 jointly constitute a unique molecular configuration at the DAP base. Moreover, our finding suggests that ODF2 plays an auxiliary role in coordinating and maintaining DAP nine-fold symmetry. Together, we develop an organelle-based drift correction protocol and a two-color solution with minimum crosstalk, allowing a robust localization microscopy imaging of expanded DAP structures deep into the gel-specimen composites.

Suggested Citation

  • Ting-Jui Ben Chang & Jimmy Ching-Cheng Hsu & T. Tony Yang, 2023. "Single-molecule localization microscopy reveals the ultrastructural constitution of distal appendages in expanded mammalian centrioles," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37342-x
    DOI: 10.1038/s41467-023-37342-x
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    References listed on IDEAS

    as
    1. T. Tony Yang & Weng Man Chong & Won-Jing Wang & Gregory Mazo & Barbara Tanos & Zhengmin Chen & Thi Minh Nguyet Tran & Yi-De Chen & Rueyhung Roc Weng & Chia-En Huang & Wann-Neng Jane & Meng-Fu Bryan Ts, 2018. "Super-resolution architecture of mammalian centriole distal appendages reveals distinct blade and matrix functional components," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    2. Qing Wei & Qingwen Xu & Yuxia Zhang & Yujie Li & Qing Zhang & Zeng Hu & Peter C. Harris & Vicente E. Torres & Kun Ling & Jinghua Hu, 2013. "Transition fibre protein FBF1 is required for the ciliary entry of assembled intraflagellar transport complexes," Nature Communications, Nature, vol. 4(1), pages 1-10, December.
    3. Mathew Bowler & Dong Kong & Shufeng Sun & Rashmi Nanjundappa & Lauren Evans & Veronica Farmer & Andrew Holland & Moe R. Mahjoub & Haixin Sui & Jadranka Loncarek, 2019. "High-resolution characterization of centriole distal appendage morphology and dynamics by correlative STORM and electron microscopy," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    4. Lei Wang & Marion Failler & Wenxiang Fu & Brian D. Dynlacht, 2018. "A distal centriolar protein network controls organelle maturation and asymmetry," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    5. Fabian U. Zwettler & Sebastian Reinhard & Davide Gambarotto & Toby D. M. Bell & Virginie Hamel & Paul Guichard & Markus Sauer, 2020. "Molecular resolution imaging by post-labeling expansion single-molecule localization microscopy (Ex-SMLM)," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
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