Brain motor and fear circuits regulate leukocytes during acute stress

Wolfram C. Poller (), Jeffrey Downey, Agnes A. Mooslechner, Nargis Khan, Long Li, Christopher T. Chan, Cameron S. McAlpine, Chunliang Xu, Florian Kahles, Shun He, Henrike Janssen, John E. Mindur, Sumnima Singh, Máté G. Kiss, Laura Alonso-Herranz, Yoshiko Iwamoto, Rainer H. Kohler, Lai Ping Wong, Kashish Chetal, Scott J. Russo, Ruslan I. Sadreyev, Ralph Weissleder, Matthias Nahrendorf, Paul S. Frenette, Maziar Divangahi and Filip K. Swirski ()
Additional contact information
Wolfram C. Poller: Icahn School of Medicine at Mount Sinai
Jeffrey Downey: Icahn School of Medicine at Mount Sinai
Agnes A. Mooslechner: Massachusetts General Hospital and Harvard Medical School
Nargis Khan: McGill University
Long Li: Friedman Brain Institute, Icahn School of Medicine at Mount Sinai
Christopher T. Chan: Icahn School of Medicine at Mount Sinai
Cameron S. McAlpine: Icahn School of Medicine at Mount Sinai
Chunliang Xu: Albert Einstein College of Medicine
Florian Kahles: Massachusetts General Hospital and Harvard Medical School
Shun He: Massachusetts General Hospital and Harvard Medical School
Henrike Janssen: Icahn School of Medicine at Mount Sinai
John E. Mindur: Massachusetts General Hospital and Harvard Medical School
Sumnima Singh: Icahn School of Medicine at Mount Sinai
Máté G. Kiss: Icahn School of Medicine at Mount Sinai
Laura Alonso-Herranz: Massachusetts General Hospital and Harvard Medical School
Yoshiko Iwamoto: Massachusetts General Hospital and Harvard Medical School
Rainer H. Kohler: Massachusetts General Hospital and Harvard Medical School
Lai Ping Wong: Massachusetts General Hospital and Harvard Medical School
Kashish Chetal: Massachusetts General Hospital and Harvard Medical School
Scott J. Russo: Friedman Brain Institute, Icahn School of Medicine at Mount Sinai
Ruslan I. Sadreyev: Massachusetts General Hospital and Harvard Medical School
Ralph Weissleder: Massachusetts General Hospital and Harvard Medical School
Matthias Nahrendorf: Massachusetts General Hospital and Harvard Medical School
Paul S. Frenette: Albert Einstein College of Medicine
Maziar Divangahi: McGill University
Filip K. Swirski: Icahn School of Medicine at Mount Sinai

Nature, 2022, vol. 607, issue 7919, 578-584

Abstract: Abstract The nervous and immune systems are intricately linked1. Although psychological stress is known to modulate immune function, mechanistic pathways linking stress networks in the brain to peripheral leukocytes remain poorly understood2. Here we show that distinct brain regions shape leukocyte distribution and function throughout the body during acute stress in mice. Using optogenetics and chemogenetics, we demonstrate that motor circuits induce rapid neutrophil mobilization from the bone marrow to peripheral tissues through skeletal-muscle-derived neutrophil-attracting chemokines. Conversely, the paraventricular hypothalamus controls monocyte and lymphocyte egress from secondary lymphoid organs and blood to the bone marrow through direct, cell-intrinsic glucocorticoid signalling. These stress-induced, counter-directional, population-wide leukocyte shifts are associated with altered disease susceptibility. On the one hand, acute stress changes innate immunity by reprogramming neutrophils and directing their recruitment to sites of injury. On the other hand, corticotropin-releasing hormone neuron-mediated leukocyte shifts protect against the acquisition of autoimmunity, but impair immunity to SARS-CoV-2 and influenza infection. Collectively, these data show that distinct brain regions differentially and rapidly tailor the leukocyte landscape during psychological stress, therefore calibrating the ability of the immune system to respond to physical threats.

Date: 2022
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DOI: 10.1038/s41586-022-04890-z

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