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Actin nano-architecture of phagocytic podosomes

Author

Listed:
  • J. Cody Herron

    (University of North Carolina at Chapel Hill
    University of North Carolina at Chapel Hill)

  • Shiqiong Hu

    (University of North Carolina at Chapel Hill)

  • Takashi Watanabe

    (University of North Carolina at Chapel Hill
    Fujita Health University)

  • Ana T. Nogueira

    (University of North Carolina at Chapel Hill)

  • Bei Liu

    (University of North Carolina at Chapel Hill)

  • Megan E. Kern

    (University of North Carolina at Chapel Hill)

  • Jesse Aaron

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Aaron Taylor

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Michael Pablo

    (University of North Carolina at Chapel Hill
    University of North Carolina at Chapel Hill)

  • Teng-Leong Chew

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Timothy C. Elston

    (University of North Carolina at Chapel Hill
    University of North Carolina at Chapel Hill
    University of North Carolina at Chapel Hill)

  • Klaus M. Hahn

    (University of North Carolina at Chapel Hill
    University of North Carolina at Chapel Hill)

Abstract

Podosomes are actin-enriched adhesion structures important for multiple cellular processes, including migration, bone remodeling, and phagocytosis. Here, we characterize the structure and organization of phagocytic podosomes using interferometric photoactivated localization microscopy, a super-resolution microscopy technique capable of 15–20 nm resolution, together with structured illumination microscopy and localization-based super-resolution microscopy. Phagocytic podosomes are observed during frustrated phagocytosis, a model in which cells attempt to engulf micropatterned IgG antibodies. For circular patterns, this results in regular arrays of podosomes with well-defined geometry. Using persistent homology, we develop a pipeline for semi-automatic identification and measurement of podosome features. These studies reveal an hourglass shape of the podosome actin core, a protruding knob at the bottom of the core, and two actin networks extending from the core. Additionally, the distributions of paxillin, talin, myosin II, α-actinin, cortactin, and microtubules relative to actin are characterized.

Suggested Citation

  • J. Cody Herron & Shiqiong Hu & Takashi Watanabe & Ana T. Nogueira & Bei Liu & Megan E. Kern & Jesse Aaron & Aaron Taylor & Michael Pablo & Teng-Leong Chew & Timothy C. Elston & Klaus M. Hahn, 2022. "Actin nano-architecture of phagocytic podosomes," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32038-0
    DOI: 10.1038/s41467-022-32038-0
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    References listed on IDEAS

    as
    1. Cai Huang & Zenon Rajfur & Christoph Borchers & Michael D. Schaller & Ken Jacobson, 2003. "JNK phosphorylates paxillin and regulates cell migration," Nature, Nature, vol. 424(6945), pages 219-223, July.
    2. Koen van den Dries & Leila Nahidiazar & Johan A. Slotman & Marjolein B. M. Meddens & Elvis Pandzic & Ben Joosten & Marleen Ansems & Joost Schouwstra & Anke Meijer & Raymond Steen & Mietske Wijers & Ja, 2019. "Modular actin nano-architecture enables podosome protrusion and mechanosensing," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    3. Pakorn Kanchanawong & Gleb Shtengel & Ana M. Pasapera & Ericka B. Ramko & Michael W. Davidson & Harald F. Hess & Clare M. Waterman, 2010. "Nanoscale architecture of integrin-based cell adhesions," Nature, Nature, vol. 468(7323), pages 580-584, November.
    4. Anna Labernadie & Anaïs Bouissou & Patrick Delobelle & Stéphanie Balor & Raphael Voituriez & Amsha Proag & Isabelle Fourquaux & Christophe Thibault & Christophe Vieu & Renaud Poincloux & Guillaume M. , 2014. "Protrusion force microscopy reveals oscillatory force generation and mechanosensing activity of human macrophage podosomes," Nature Communications, Nature, vol. 5(1), pages 1-10, December.
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