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Self-extinguishing relay waves enable homeostatic control of human neutrophil swarming

  1. Author:
    Strickland, Evelyn
    Pan, Deng
    Godfrey, Christian
    Kim, Julia S
    Hopke, Alex
    Ji, Wencheng
    Degrange,Maureen
    Villavicencio, Bryant
    Mansour, Michael K
    Zerbe, Christa S
    Irimia, Daniel
    Amir, Ariel
    Weiner, Orion D

  2. Author Address

    Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA, USA; Cardiovascular Research Institute, University of California, San Francisco, San Francisco, CA, USA., John A. Paulson School of Engineering and Applied Sciences, Harvard University, Cambridge, MA, USA., Center for Engineering in Medicine and Surgery, Department of Surgery, Massachusetts General Hospital, Boston, MA, USA; Harvard Medical School, Boston, MA, USA., Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA, USA., Center for Engineering in Medicine and Surgery, Department of Surgery, Massachusetts General Hospital, Boston, MA, USA; Harvard Medical School, Boston, MA, USA; Shriners Burns Hospital, Boston, MA 02114, USA., Department of Physics of Complex Systems, The Weizmann Institute of Science, Rehovot 7610001, Israel., Leidos Biomedical Research, Inc., Frederick National Laboratory for Cancer Research, Frederick, MD 21702, USA., Kelly Government Services, Bethesda, MD, USA., Harvard Medical School, Boston, MA, USA; Division of Infectious Diseases, Massachusetts General Hospital, Boston, MA, USA., Laboratory of Clinical Immunology and Microbiology (LCIM), National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD, USA., John A. Paulson School of Engineering and Applied Sciences, Harvard University, Cambridge, MA, USA; Department of Physics of Complex Systems, The Weizmann Institute of Science, Rehovot 7610001, Israel., Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA, USA; Cardiovascular Research Institute, University of California, San Francisco, San Francisco, CA, USA. Electronic address: orion.weiner@ucsf.edu.,
    1. Year: 2024
    2. Date: Oct 7
    3. Epub Date: 2024 07 02
  2. Journal: Developmental Cell
    1. 59
    2. 19
    3. Pages: 2659-2671
  4. Type of Article: Article
  1. Abstract:

    Neutrophils collectively migrate to sites of injury and infection. How these swarms are coordinated to ensure the proper level of recruitment is unknown. Using an ex vivo model of infection, we show that human neutrophil swarming is organized by multiple pulsatile chemoattractant waves. These waves propagate through active relay in which stimulated neutrophils trigger their neighbors to release additional swarming cues. Unlike canonical active relays, we find these waves to be self-terminating, limiting the spatial range of cell recruitment. We identify an NADPH-oxidase-based negative feedback loop that is needed for this self-terminating behavior. We observe near-constant levels of neutrophil recruitment over a wide range of starting conditions, revealing surprising robustness in the swarming process. This homeostatic control is achieved by larger and more numerous swarming waves at lower cell densities. We link defective wave termination to a broken recruitment homeostat in the context of human chronic granulomatous disease. Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved.

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External Sources

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  2. DOI: 10.1016/j.devcel.2024.06.003
  3. PMID: 38971157
  4. PMCID: PMC11461132
  5. View record in Web of Science®
  6. WOS: 001333939400001
  7. PII : S1534-5807(24)00381-2

Library Notes

  1. Fiscal Year: FY2024-2025
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