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

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Self-extinguishing relay waves enable homeostatic control of human neutrophil swarming
Developmental Cell ( IF 10.7 ) Pub Date : 2024-07-05 , DOI: 10.1016/j.devcel.2024.06.003
Evelyn Strickland ₁ , Deng Pan ₂ , Christian Godfrey ₃ , Julia S Kim ₄ , Alex Hopke ₅ , Wencheng Ji ₆ , Maureen Degrange ₇ , Bryant Villavicencio ₈ , Michael K Mansour ₉ , Christa S Zerbe ₁₀ , Daniel Irimia ₅ , Ariel Amir ₁₁ , Orion D Weiner ₁

Affiliation

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.

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.

中文翻译：

自熄灭中继波可实现对人中性粒细胞群的稳态控制

中性粒细胞集体迁移到损伤和感染部位。目前尚不清楚这些群体如何协调以确保适当的招募水平。使用感染的离体模型，我们表明人类中性粒细胞群是由多个脉冲趋化波组织的。这些波通过主动中继传播，其中受刺激的嗜中性粒细胞触发其邻居释放额外的蜂群线索。与规范的有源中继不同，我们发现这些波是自终止的，限制了细胞募集的空间范围。我们确定了这种自终止行为所需的基于 NADPH 氧化酶的负反馈回路。我们在广泛的起始条件下观察到中性粒细胞募集的水平几乎恒定，揭示了蜂群过程中令人惊讶的稳健性。这种稳态控制是通过在较低细胞密度下更大、更多的蜂群波来实现的。在人类慢性肉芽肿病的背景下，我们将有缺陷的波终止与破损的募集稳态联系起来。

更新日期：2024-07-05

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