Cited by 106Stress Responses and CortisolNeuroinflammation and Neurodegeneration MechanismsTryptophan and brain disorders

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Stress Downregulates Lipopolysaccharide-Induced Expression of Proinflammatory Cytokines in the Spleen, Pituitary, and Brain of Mice

Goujon, E., Parnet, P., Laye, S., Combe, C., Kelley, K.W., Dantzer, R.·1995·Brain Behavior and Immunity

DOI 10.1006/brbi.1995.1028

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Abstract

Mice injected with LPS (10 mu g/mouse, sc) or saline were submitted to a 15-min restraint stress and sacrificed 1 or 2 h later to assess the effect of stress on the induction of interleukin-1beta (IL-1beta) and other proinflammatory cytokines (IL-1alpha, IL-1ra, IL-6, and tumor necrosis factor-alpha) in the spleen, pituitary, hypothalamus, hippocampus, and striatum. LPS-induced cytokine gene expression, as determined by comparative RT-PCR, was lower in stressed than in nonstressed mice. LPS increased plasma and tissue levels of IL-1beta, as determined by ELISA, but this effect was less marked in stressed than in nonstressed mice. These results are discussed in relation to the modulatory effects of glucocorticoids on cytokine production.

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Paoletta, A., Arnaldi, G., Papa, R., Boscaro, M., & Tirabassi, G. (2010) · Pituitary · doi:10.1007/s11102-010-0285-9 · Cited by 15
“In particular, cytokines seem to play an important role in regulating the hypothalamic–pituitary–adrenal axis function [3] and in turn can be influenced by it [4–8].”
Background
Chapter 11 Immunological and neuroendocrine modulation of fever in stress
Roth, J. (1998) · Progress in brain research · doi:10.1016/s0079-6123(08)62036-1 · Cited by 15
The Impact of Social and Physical Peer Victimization on Systemic Inflammation in Adolescents
Araña, A. A., Boyd, E. Q., Guarneri-White, M. E., Iyer‐Eimerbrink, P. A., Dougall, A. L., & Jensen‐Campbell, L. A. (2018) · Merrill-palmer Quarterly · doi:10.13110/merrpalmquar1982.64.1.0012 · Cited by 15
“These results are particularly difficult to reconcile, as this is the first study to date to evaluate the unique effects of physical peer victimization on inflammatory biomarkers and one of very few to report an inverse relationship between stress and inflammation (see Goujon et al., 1995).”
Result
Chronic restraint stress impairs voluntary wheel running but has no effect on food-motivated behavior in mice
Scott, K. A., Phan, T., Boukelmoune, N., Heijnen, C. J., & Dantzer, R. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.10.017 · Cited by 13
Self-citation
Intracellular expression of c-Fos protein in various structures of the hypothalamus in electrical pain stimulation and administration of antigens
Gavrilov, Y. V., Перекрест, С. В., & Novikova, N. S. (2007) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-008-0012-4 · Cited by 13
“Many clinical experiments have demonstrated [8, 9, 11, 16 , 18] that immune system responses change on the background of stress reactions, though the central mechanisms of these effects have received virtually no study; they are of significant interest for basic and applied medicine.”
Background
Chromatin organization as an indicator of glucocorticoid induced natural killer cell dysfunction
Misale, M. S., Janusek, L. W., Tell, D., & Mathews, H. L. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.09.004 · Cited by 11
Systemic administration of betamethasone delays endotoxin-induced preterm labor in the murine model
Schwartz, W. J., Christensen, H. D., Carey, J. C., Rayburn, W. F., & Gonzalez, C. L. (2003) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2003.72 · Cited by 11
Increased resistance of immobilized-stressed mice to infection: Correlation with behavioral alterations
Mahanti, S., Majhi, A., Chongdar, S., Kundu, K., Dutta, K., Basu, A., & Bishayi, B. (2012) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2012.11.001 · Cited by 10
“It is well known that bacterial endotoxin is a potent stimulator for the synthesis and release of proinflammatory cytokines such as IL-6, TNF-a, IFN-c, but acute stress has been shown to downregulate these LPS-induced responses (Goujon et al., 1995) IL-6 is essential for activation of HPA axis during immunological cha…”
Liver vs. spleen: Time course of organ-dependent immune gene expression in an LPS-stimulated toad (Rhinella diptycha)
Floreste, F. R., Titon, B., Titon, S. C. M., Muxel, S. M., de Figueiredo, A. C., Gomes, F. R., & Assis, V. R. (2022) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2022.110784 · Cited by 9
Epstein–Barr virus (EBV)-encoded dUTPase and chronic restraint induce impaired learning and memory and sickness responses
Aubrecht, T. G., Weil, Z. M., Ariza, M. E., Williams, M., Reader, B. F., Glaser, R., Sheridan, J. F., & Nelson, R. J. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.07.001 · Cited by 9
“Therefore, short periods of restraint stress, which increase glucocorticoids, can decrease proinflammatory cytokine expression even in response to LPS injections [18].”
Background
Stress-induced changes in cellular responses in hypothalamic structures to administration of an antigen (lipopolysaccharide) (in terms of c-Fos protein expression)
Gavrilov, Y. V., Перекрест, С. В., Novikova, N. S., & Korneva, E. A. (2008) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-008-0028-9 · Cited by 9
“A number of studies [ 16 , 19] have demonstrated decreases in interleukin-1 and tumor necrosis factor levels in the spleens of rats after administration of lipopolysaccharide on the background of electrical pain stimulation.”
Result
Immunophysiology: The Interaction of Hormones, Lymphohemopoietic Cytokines, and the Neuroimmune Axis
Arkins, S., Johnson, R. W., Minshall, C. T., Dantzer, R., & Kelley, K. W. (2000) · Comprehensive physiology · doi:10.1002/cphy.cp070421 · Cited by 9
“This induced expression of cytokine transcripts is transient, and is similar to the onset, maintenance, and cessation of overt symptoms of sickness (101).”
Self-citation
Stressed (acute) mice display neuroimmunodysregulation and defective innate immune response against coliform infection
Mehrzad, J., Shajari, M., Saleh-moghaddam, M., & Mohammad, S. N. (2015) · International Immunopharmacology · doi:10.1016/j.intimp.2015.05.041 · Cited by 7
Organ-specific changes in norepinephrine turnover against various stress conditions in thermoneutral mice.
Teramura, Y., Terao, A., Okada, Y., Tomida, J., Okamatsu‐Ogura, Y., & Kimura, K. (2014) · PubMed · doi:10.14943/jjvr.62.3.117 · Cited by 6
“LPS-induced cytokine production was reduced in the plasma and brain by immobilization [9].”
Background
Profound Effects of Burn and Ethanol on Proinflammatory Cytokines of the Reproductive Axis in the Male Mouse
Emanuele, N., LaPaglia, N., Kovacs, E. J., Gamelli, R. L., & Emanuele, M. A. (2008) · Journal of Burn Care & Research · doi:10.1097/bcr.0b013e3181711273 · Cited by 4
Immunomodulatory T cell death associated gene-8 (TDAG8) receptor in depression-associated behaviors
McMurray, K. M. J., Vollmer, L. L., Ahlbrand, R. A., Thomas, J. D., Winter, A. S., Lewkowich, I. P., & Sah, R. (2019) · Physiology & Behavior · doi:10.1016/j.physbeh.2019.112598 · Cited by 3
“Given contributions of the spleen in immune dysfunction associated with stress and depression-like behaviors, we next assessed cytokine levels within this tissue[46,47].”
Background
Stressors affect urocortin 1 and urocortin 2 gene expression in rat spleen: The role of glucocorticoids
Tillinger, A., Padová, A., Mravec, B., & Tomova, A. (2019) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2019.577030 · Cited by 3
Gut microbiota and immune response under chronic social stress in an LPS-induced inflammatory model
Petakh, P., Stravskyy, Y. S., Halabitska, I., Pavliuk, A., & Kamyshnyi, O. (2025) · Stress · doi:10.1080/10253890.2025.2595777 · Cited by 2
“Experimental studies in rodents have also demonstrated that prior exposure to acute or chronic stress can “prime” the innate immune system, resulting in exaggerated cytokine release upon subsequent inflammatory challenge (Frank et al., 2016; Goujon et al., 1995).”
Глюкокортикоиды в нейровоспалении гиппокампа: доктор Джекилл и мистер Хайд
Bolshakov, A. P., Третьякова, Л. В., Квичанский, А. А., & Гуляева, Н. В. (2021) · Biochemistry (Moscow) · doi:10.31857/s0320972521020044 · Cited by 2
Mechanisms of action of cytokines on the central nervous system. Interaction with glucocorticoids
Dantzer, R., Layé, S., Goujan, E., et al. (1997) · Springer eBooks · doi:10.1007/978-1-4471-0931-0_1 · Cited by 2
Self-citation
Depression and immunity: biological and behavioural mechanisms
Irwin, M. R. (2006) · Cambridge University Press eBooks · doi:10.1017/cbo9780511544293.015 · Cited by 2
Interactions between corticotropin releasing factor signaling and prophylactic antibiotics on measures of intestinal function in weaned and transported pigs
McConn, B. R., Kpodo, K. R., Rivier, J., Behan, D. P., Richert, B. T., Radcliffe, J. S., Lay, D. C., Jr., & Johnson, J. S. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1266409 · Cited by 1
Reciprocal Brain-Body Neuro-Endocrine-Immune Interactions: Role in Maintaining Pregnancy
Parker, V. J., Arck, P., & Douglas, A. J. (2011) · Advances in Neuroimmune Biology · doi:10.3233/nib-2011-020 · Cited by 1
Glucocorticoids: Immunity and Inflammation
Ronchetti, S., & Riccardi, C. (2018) · Springer eBooks · doi:10.1007/978-3-319-77658-3_12 · Cited by 1
Examination of the effect of weaning stress on the physiological and molecular regulation of immune function in circulating bovine leukocytes
O’Loughlin, A. (2011) · Maynooth University ePrints and eTheses Archive (Maynooth University) · Cited by 1
Brain Interleukin-1β Expression and Action in the Absence of Neuropathology
Chaskiel, L., & Konsman, J. P. (2008) · Neuroimmune biology · doi:10.1016/s1567-7443(07)10004-1
The immunomodulator OM-89 induces acth and glucocorticoid secretion in rats through an IL-1 dependent pathway
Mimouni, J., Farine, J. C., Melhaoui, A., et al. (1997) · International Journal of Immunopharmacology · doi:10.1016/s0192-0561(97)00051-9
Effects of voluntary wheel running and forced treadmill running on inflammation induced behavioral abnormalities in young and old mice
Martin, S. A. (2013) · Illinois Digital Environment for Access to Learning and Scholarship (University of Illinois at Urbana-Champaign)

Authors: Goujon, E., Parnet, P., Laye, S., Combe, C., Kelley, K. W., & Dantzer, R.
Affiliations: Inserm (FR)
ORCID: Parnet, P.
Kelley, K.W.
Dantzer, R.
Venue: Brain Behavior and Immunity
Publisher: Elsevier BV
Published: 1995-12
Volume: 9
Issue: 4
Pages: 292-303
ISSN: 0889-1591 (ISSN-L)
DOI: 10.1006/brbi.1995.1028
OpenAlex: W2032191599
Cited by: 106
References: 0
Citations by year: 2025: 1 · 2023: 1 · 2022: 3 · 2021: 2 · 2020: 1 · 2019: 2 · 2018: 3 · 2017: 4 · 2015: 6 · 2014: 6 · 2013: 4 · 2012: 4
FWCI: 1.78
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Brain Behavior and Immunity (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Funders: National Institutes of Health (5r01dk049311-05)
National Institute of Mental Health (1RO1 MH51569-01A2, R01MH051569)
National Institute of Diabetes and Digestive and Kidney Diseases (1RO1 DK 49311)
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Keywords: restraint stress, lipopolysaccharide, inflammatory cytokines, IL-1β, interleukin-1 alpha, interleukin-1 receptor antagonist, interleukin-6, TNF-α, glucocorticoids, hypothalamic-pituitary-adrenal axis, spleen, pituitary gland, hippocampus, striatum, cytokine gene expression, neuroimmune interactions
MeSH terms: Animals, Brain, Corpus Striatum, Corticosterone, Gene Expression Regulation, Hippocampus, Hypothalamus, Interleukin-1, Lipopolysaccharides, Male, Mice, Inbred ICR, Pituitary Gland, Restraint, Physical, RNA, Messenger, Sialoglycoproteins, Spleen, Stress, Physiological, Tumor Necrosis Factor-alpha, Neuroimmunomodulation, Interleukin-6, Mice, Interleukin 1 Receptor Antagonist Protein

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Stress Downregulates Lipopolysaccharide-Induced Expression of Proinflammatory Cytokines in the Spleen, Pituitary, and Brain of Mice

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