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Force-bearing phagocytic adhesion rings mediate the phagocytosis of surface-bound particles

Author

Listed:
  • Subhankar Kundu

    (University of Cincinnati)

  • Kaushik Pal

    (Indian Institute of Technology Tirupati)

  • Arghajit Pyne

    (University of Cincinnati)

  • Xuefeng Wang

    (University of Cincinnati)

Abstract

Many micro-particles including pathogens strongly adhere to hosts. It remains elusive how macrophages detach these surface-bound particles during phagocytosis. We show that, rather than binding directly to these particles, macrophages form unique β2 integrin-mediated adhesion structures at the cell-substrate interfaces, specifically encircling the surface-bound particles. These circular adhesion structures that we named phagocytic adhesion rings (PARs) serve as strongholds to support local ring-shaped actin structures constricting into the particle-substrate cleavages, thereby pinching off the particles from the substrate. During this process, integrins in PARs sustain tensions due to the reaction force of actin polymerization against the particles. Such tensions are critical for phagocytic efficiency of surface-bound particles. PARs were formed in all tested macrophages (mouse, human and fish) and micron-sized particles (microbeads and E. coli), demonstrating their conserved role in the phagocytosis. This study reveals a mechanism of PAR-mediated phagocytosis, specialized for the detachment and internalization of surface-bound particles.

Suggested Citation

  • Subhankar Kundu & Kaushik Pal & Arghajit Pyne & Xuefeng Wang, 2025. "Force-bearing phagocytic adhesion rings mediate the phagocytosis of surface-bound particles," Nature Communications, Nature, vol. 16(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-56404-w
    DOI: 10.1038/s41467-025-56404-w
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    1. Mingxi Yao & Benjamin T. Goult & Benjamin Klapholz & Xian Hu & Christopher P. Toseland & Yingjian Guo & Peiwen Cong & Michael P. Sheetz & Jie Yan, 2016. "The mechanical response of talin," Nature Communications, Nature, vol. 7(1), pages 1-11, September.
    2. Prakash Thangavel & Duckshin Park & Young-Chul Lee, 2022. "Recent Insights into Particulate Matter (PM 2.5 )-Mediated Toxicity in Humans: An Overview," IJERPH, MDPI, vol. 19(12), pages 1-22, June.
    3. 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.
    4. Masahiro Kitano & Michio Nakaya & Takeshi Nakamura & Shigekazu Nagata & Michiyuki Matsuda, 2008. "Imaging of Rab5 activity identifies essential regulators for phagosome maturation," Nature, Nature, vol. 453(7192), pages 241-245, May.
    5. 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.
    6. B. J. Nolen & N. Tomasevic & A. Russell & D. W. Pierce & Z. Jia & C. D. McCormick & J. Hartman & R. Sakowicz & T. D. Pollard, 2009. "Characterization of two classes of small molecule inhibitors of Arp2/3 complex," Nature, Nature, vol. 460(7258), pages 1031-1034, August.
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