Brain motor and fear circuits regulate leukocytes during acute stress
Open accessAbstract
The nervous and immune systems are intricately linked 1. Although psychological stress is known to modulate immune function, mechanistic pathways linking stress networks in the brain to peripheral leukocytes remain poorly understood 2. 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.
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Stressed mice are more susceptible to infections by pathogens such as Escherichia coli, influenza, and SARS-CoV-2, similar to humans with MDD.
“Similar to humans with MDD, stressed mice are also more susceptible to infections by pathogens such as Escherichia coli, influenza and SARS-CoV-269,150,151.”
From Central regulation of stress-evoked peripheral immune responses (2023) · cites this paper as [69]
The Article section reports that acutely stressed mice had higher SARS-CoV-2 viral titres and mortality, and higher influenza viral loads and more severe pathology. Our copy does not establish increased susceptibility to Escherichia coli or the comparison with humans with MDD. (LLM, conf=0.87)
Experimental — accuracy not yet measuredThe effect of PVH CRH+ neuron manipulation on leukocyte retention depends on the HPA axis, since adrenalectomy prevents the changes.
“Further, this effect was found to be HPA axis-dependent, as adrenalectomy prevented these changes69.”
From Central regulation of stress-evoked peripheral immune responses (2023) · cites this paper as [69]
Stimulating CRH+ neurons in the PVH raises plasma corticosterone and causes T cells, B cells and monocytes to be retained in bone marrow, lowering their circulating numbers.
“The authors found that stimulating corticotropin-releasing hormone-expressing (CRH+) neurons in the PVH, which increases plasma corticosterone concentrations, leads to the retention of T cells, B cells and monocytes in the bone marrow, thereby reducing their numbers in circulation”
From Central regulation of stress-evoked peripheral immune responses (2023) · cites this paper as [69]
Ablating CRH expression in the PVH prevents the fall in blood T cells, B cells and monocytes after acute restraint stress, as does inhibiting CXCR4.
“conversely ablating CRH expression in the PVH prevented the decrease in T cells, B cells, and monocytes in the blood following acute restraint stress, as did inhibiting CXCR4, the receptor for CXCL1269.”
From Central regulation of stress-evoked peripheral immune responses (2023) · cites this paper as [69]
Optogenetic stimulation of motor cortex or medulla causes skeletal muscle CXCL1 expression, and ablating or inhibiting these regions reduces restraint stress-induced neutrophilia.
“Stimulation of the motor cortex or medulla using optogenetics led to skeletal muscle expression of CXCL1, a chemokine for neutrophils71, while ablating or inhibiting these regions ameliorated the restraint stress-induced neutrophilia69.”
From Central regulation of stress-evoked peripheral immune responses (2023) · cites this paper as [69]
Acute restraint stress induces neutrophilia, and this is regulated by brain regions different from those controlling monocyte and lymphocyte mobilization.
“Interestingly, acute restraint stress was also shown to induce neutrophilia and this was found to be regulated by different brain regions than those regulating monocyte and lymphocyte mobilization.”
From Central regulation of stress-evoked peripheral immune responses (2023) · cites this paper as [69]
Restraint-stressed mice have high pulmonary viral loads, and ablating PVH CRH+ neurons ameliorates stress-induced immunosuppression.
“Similarly, high pulmonary viral loads were observed in restraint-stressed mice; however, ablating PVH CRH+ neurons ameliorated the immunosuppression brought upon by stress69.”
From Central regulation of stress-evoked peripheral immune responses (2023) · cites this paper as [69]
Excitation of CRH+ neurons in the PVH prevents pulmonary clearance of influenza A virus, implicating the HPA axis.
“For example, excitation of CRH+ neurons in the PVH prevented pulmonary clearance of influenza A virus, implicating the HPA axis in this response69.”
From Central regulation of stress-evoked peripheral immune responses (2023) · cites this paper as [69]
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- Authors
- Poller, W. C., Downey, J., Mooslechner, A. A., Khan, N., Li, L., Chan, C. T., McAlpine, C. S., Xu, C., Kahles, F., He, S., Janssen, H., Mindur, J. E., Singh, S., Kiss, M. G., Alonso-Herranz, L., Iwamoto, Y., Kohler, R. H., Wong, L. P., Chetal, K., Russo, S. J., Sadreyev, R. I., Weissleder, R., Nahrendorf, M., Frenette, P. S., Divangahi, M., & Swirski, F. K.
- Affiliations
- Harvard University (US)
- McGill University Health Centre (CA)
- Icahn School of Medicine at Mount Sinai (US)
- Albert Einstein College of Medicine (US)
- Corresponding author
- Poller, Wolfram C.
- ORCID
- Poller, Wolfram C.
- Downey, Jeffrey
- Mooslechner, Agnes A.
- Khan, Nargis
- Li, Long
- Chan, Christopher T.
- McAlpine, Cameron S.
- Xu, Chunliang
- Kahles, Florian
- He, Shun
- Janssen, Henrike
- Mindur, John E.
- Singh, Sumnima
- Kiss, Máté G.
- Alonso-Herranz, Laura
- Iwamoto, Yoshiko
- Kohler, Rainer H.
- Wong, Lai Ping
- Chetal, Kashish
- Russo, Scott J.
- Sadreyev, Ruslan I.
- Weissleder, Ralph
- Nahrendorf, Matthias
- Frenette, Paul S.
- Divangahi, Maziar
- Swirski, Filip K.
- Venue
- Nature
- Published
- 2022-05-30
- Volume
- 607
- Issue
- 7919
- Pages
- 578-584
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC9798885
- OpenAlex
- W4281752653
- Cited by
- 234
- References
- 47
- Citations by year
- 2026: 48 · 2025: 57 · 2024: 64 · 2023: 52 · 2022: 13
- FWCI
- 27.34
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Massachusetts General Hospital
- Icahn School of Medicine at Mount Sinai
- Dana-Farber/Harvard Cancer Center
- Marshallplan-Jubiläumsstiftung
- McGill University
- Deutsche Forschungsgemeinschaft (398190272)
- Austrian Science Fund (W1241, FWF W1241)
- National Institutes of Health (HL142494)
- Canadian Institutes of Health Research (174910_1)
- National Heart, Lung, and Blood Institute (R35HL135752, K99HL151750, R00HL151750, P01HL131478, P01HL142494, R01HL158534)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Psychiatry and Mental health › Cancer, Stress, Anesthesia, and Immune Response
- Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
- Keywords
- acute stress, leukocyte mobilization, neutrophil mobilization, lymphocyte egress, paraventricular hypothalamus, glucocorticoid signaling, corticotropin-releasing factor, neutrophil reprogramming, autoimmunity, SARS-CoV-2 susceptibility, influenza susceptibility, innate immunity, fear circuit, motor circuits
- MeSH terms
- COVID-19, SARS-CoV-2, Animals, Bone Marrow Cells, Brain, Disease Susceptibility, Fear, Glucocorticoids, Humans, Leukocytes, Lymphocytes, Lymphoid Tissue, Monocytes, Motor Neurons, Neural Pathways, Neutrophils, Orthomyxoviridae Infections, Paraventricular Hypothalamic Nucleus, Stress, Psychological, Chemokines, Mice, Optogenetics
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