The DOI matches its Crossref record; 87 of the 91 references it cites were found in a registry or an index.
Prior Stressor Exposure Sensitizes LPS-Induced Cytokine Production
Abstract
Exposure to stressors often alters the subsequent responsiveness of many systems. The present study tested whether prior exposure to inescapable tailshock (IS) alters the interleukin (IL)-1beta, tumor necrosis factor (TNF)-alpha, or IL-6 response to an injection of bacterial endotoxin (lipopolysaccharide; LPS). Rats were exposed to IS or remained as home cage controls (HCC); 24 h later animals were injected i.p. with either 10 microg/kg LPS or equilvolume sterile saline. IS significantly increased plasma TNF-alpha, IL-1beta, and pituitary, hypothalamus, hippocampus, cerebellum IL-1beta 1 h, but not 2 h, after LPS, compared to controls. Additional animals were injected with LPS or saline 4, 10, or 21 days after exposure to IS and tail vein blood was collected and assayed for IL-1beta. An enhanced plasma IL-1beta response occurred 4 days after IS, but was gone by 10 days. These results suggest that exposure to IS sensitizes the innate immune response to LPS by resulting in either a larger or a more rapid induction of proinflammatory cytokines.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Stress and depression can permanently alter the responsiveness of the immune system (41-44).”
From Chronic stress and age-related increases in the proinflammatory cytokine IL-6. (2003) · cites this paper as [41]
In the citing paper
“For example, prior stressor exposure appears to prime proinflammatory cytokine responses, such that subsequent exposure to a bacterial endotoxin, lipopolysaccharide, resulted in a larger or more rapid induction of proinflammatory cytokines in stressed rats compared with nonstressed controls (41).”
From Chronic stress and age-related increases in the proinflammatory cytokine IL-6. (2003) · cites this paper as [41]
In the citing paper
“serum concentrations of lipocalin-type PGD synthase, which catalyzes the conversion from PGH2 to PGD2, have been reported to vary throughout the day, with highest levels at night (sleep period) and lowest levels in the afternoon. Total sleep deprivation blunted the nocturnal increase at night and elevated levels during the daytime (275)”
From The Sleep-Immune Crosstalk in Health and Disease (2019) · cites this paper as [275]
In the citing paper
“For example, acute stress 24 hr prior to lipopolysaccharide (LPS) treatment augments LPS-induced increases in plasma levels of IL-1β, TNF-α, and IL-6 (Johnson et al., 2002).”
From The Stressed CNS: When Glucocorticoids Aggravate Inflammation (2009) · cites this paper as Johnson et al., 2002
In the citing paper
“For instance, acute stressors such as inescapable tailshocks (IS) were demonstrated to potentiate the expression of pro-inflammatory mediators in specific regions of the brain following the peripheral administration of LPS in rodents (140–142).”
From The HPA – Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain (2014) · cites this paper as [141]
In the citing paper
“As a matter of act, both types of stress elicit an HPA response and were shown to exacerbate salient features of inflammation in the CNS provided that they occur prior to peripheral or cerebral immune insults.”
From The HPA – Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain (2014) · cites this paper as [141]
In the citing paper
“GR signaling was thus proposed to be essential for the cross-sensitization between stress and the inflammatory response to LPS.”
From The HPA – Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain (2014) · cites this paper as [141]
In the citing paper
“Interestingly, in these studies the priming effects of stress (regardless of its chronicity) on the ensuing immune response could be abated with RU486 or by experimentally maintaining plasma GCs to basal levels in adrenalectomized animals.”
From The HPA – Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain (2014) · cites this paper as [141]
Citations
Cites
Immunobiology: the immune system in health and disease
(1995) · Choice Reviews Online · doi:10.5860/choice.32-3876 · Cited by 4,111
Biological basis of the behavior of sick animals
Hart, B. L. (1988) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(88)80004-6 · Cited by 2,223
The psychology and neurobiology of addiction: an incentive–sensitization view
Robinson, T. E., & Berridge, K. C. (2000) · Addiction · doi:10.1046/j.1360-0443.95.8s2.19.x · Cited by 1,507
Interleukin-1 stimulates the secretion of hypothalamic corticotropin-releasing factor
Sapolsky, R., Rivier, C., Yamamoto, G., Plotsky, P., & Vale, W. (1987) · Science · doi:10.1126/science.2821621 · Cited by 1,504
Fever: Role of Pyrogens and Cryogens
Kluger, M. J. (1991) · Physiological Reviews · doi:10.1152/physrev.1991.71.1.93 · Cited by 1,220
Sickness behavior as a new target for drug development
Kent, S., Bluthé, R.-M., Kelley, K. W., & Dantzer, R. (1992) · Trends in Pharmacological Sciences · doi:10.1016/0165-6147(92)90012-u · Cited by 867
The role of stress in drug self-administration
Piazza, P. V., & Moal, M. L. (1998) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(97)01115-2 · Cited by 674
Interchangeability of Stress and Amphetamine in Sensitization
Antelman, S. M., Eichler, A. J., Black, C. A., & Kocan, D. J. (1980) · Science · doi:10.1126/science.7188649 · Cited by 562
The immune system as a sensory organ.
Blalock, J. E. (1984) · The Journal of Immunology · doi:10.4049/jimmunol.132.3.1067 · Cited by 551
Stress and immunity: An integrated view of relationships between the brain and the immune system
Dantzer, R., & Kelley, K. W. (1989) · Life Sciences · doi:10.1016/0024-3205(89)90345-7 · Cited by 534
Cited by
Sorted by citations
Items 201–268 of 268
Expression of JP-8–Induced Inflammatory Genes in AEII Cells Is Mediated by NF-κB and PARP-1
Espinoza, L. A., Tenzin, F., Cecchi, A. O., Chen, Z., Witten, M. L., & Smulson, M. E. (2006) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2006-0059oc · Cited by 13
Vichaya, E. G., Young, E. E., Frazier, M. A., Cook, J. L., Welsh, C. J., & Meagher, M. W. (2011) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2011.08.006 · Cited by 11
Stress, Negative Emotions, and Inflammation
Gouin, J., Hantsoo, L. V., & Kiecolt‐Glaser, J. K. (2011) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780195342161.013.0054 · Cited by 14
Nowacka-Chmielewska, M. M., Liśkiewicz, D., Paul-Samojedny, M., Bielecka, A., Barski, J. J., Małecki, A., & Obuchowicz, E. (2017) · Pharmacological Reports · doi:10.1016/j.pharep.2017.01.004 · Cited by 10
Psychological Influences on Neuroendocrine and Immune Outcomes
Christian, L. M., Deichert, N. T., Gouin, J., Graham‐Engeland, J. E., & Kiecolt‐Glaser, J. K. (2009) · Wiley eBooks · doi:10.1002/9780470478509.neubb002064 · Cited by 10
Kamisoglu, K., Sleight, K. E., Nguyen, T. T., Calvano, S. E., Coyle, S. M., Corbett, S., & Androulakis, I. P. (2013) · Innate Immunity · doi:10.1177/1753425913508458 · Cited by 10
Gano, A., Pautassi, R. M., Doremus‐Fitzwater, T. L., Barney, T. M., Vore, A. S., & Terrence Deak, B. (2019) · Experimental Biology and Medicine · doi:10.1177/1535370219831709 · Cited by 9
Endogenous Extracellular Hsp72 Release Is an Adaptive Feature of the Acute Stress Response
Fleshner, M., Sharkey, C. M., Nickerson, M., & JOHNSON, J. D. (2007) · Elsevier eBooks · doi:10.1016/b978-012088576-3/50055-1 · Cited by 9
Self-citationGavrilov, 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
Periodontal Innate Immune Mechanisms Relevant to Atherosclerosis
Amar, S., & Al‐Hashemi, J. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-801078-5.00007-8 · Cited by 8
Yan, J., Bai, J., Gao, C., Liang, Y., Zhao, B., & Bian, Y. (2017) · Neuroscience Letters · doi:10.1016/j.neulet.2017.02.070 · Cited by 9
Autism Spectrum Disorders and Aluminum Vaccine Adjuvants
Tomljenovic, L., Blaylock, R. L., & Shaw, C. A. (2013) · Springer eBooks · doi:10.1007/978-1-4614-4788-7_89 · Cited by 8
Mehrzad, J., Shajari, M., Saleh-moghaddam, M., & Mohammad, S. N. (2015) · International Immunopharmacology · doi:10.1016/j.intimp.2015.05.041 · Cited by 7
Hasan, Z. W., Nguyen, V. T., & Ashley, N. T. (2024) · PeerJ · doi:10.7717/peerj.17539 · Cited by 7
Natarajan, R., Mitchell, C. M., Harless, N., & Yamamoto, B. K. (2018) · Scientific Reports · doi:10.1038/s41598-018-28970-1 · Cited by 7
Szteroidok: A glükokortikoidok élettani és gyógyszertani hatásai
Zelena, D., & Makara, B. G. (2015) · Orvosi Hetilap · doi:10.1556/650.2015.30248 · Cited by 6
Shahane, A. D., Fagundes, C. P., & Denny, B. T. (2018) · Bereavement Care · doi:10.1080/02682621.2018.1493640 · Cited by 6
Grizzell, J. A., Clarity, T. T., Rodriguez, R. M., Marshall, Z. Q., & Cooper, M. A. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.08.043 · Cited by 5
Chanyalew, M., Abebe, M., Endale, B., Girma, S., Tasew, G., van Zandbergen, G., Ritter, U., Gadisa, E., Aseffa, A., & Laskay, T. (2020) · Cytokine · doi:10.1016/j.cyto.2020.155289 · Cited by 5
The Inflammatory Hypothesis of Depression
Soskin, D. P., Cassiello-Robbins, C. F., Isacoff, O. K., & D, M. F. M. (2012) · FOCUS The Journal of Lifelong Learning in Psychiatry · doi:10.1176/appi.focus.10.4.413 · Cited by 5
Brennan, F. X., & Tieder, J. B. (2006) · Brain Research · doi:10.1016/j.brainres.2006.06.040 · Cited by 5
Social Conflict Exacerbates an Animal Model of Multiple Sclerosis
Meagher, M. W., Johnson, R. R., Vichaya, E. G., Young, E. E., Lunt, S., & Welsh, C. J. (2007) · Trauma Violence & Abuse · doi:10.1177/1524838007303506 · Cited by 5
Social disruption alters pain and cognition in an animal model of multiple sclerosis
Linsenbardt, H. R., Cook, J. L., Young, E. E., Vichaya, E. G., Young, C. R., Reusser, N. M., Storts, R. W., Welsh, C. J., & Meagher, M. W. (2015) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2015.09.005 · Cited by 4
Li, B., Shi, X., Chen, E., & Wu, X. (2023) · Food Science and Biotechnology · doi:10.1007/s10068-023-01441-8 · Cited by 5
Relación de los mecanismos inmunológicos del asma y la contaminación ambiental
Falcón-Rodríguez, C. I., Rosas‐Pérez, I., & Segura-Medina, P. (2017) · Revista de la Facultad de Medicina · doi:10.15446/revfacmed.v65n2.59954 · Cited by 3
(2006) · doi:10.1016/b978-012088576-3/50060-5 · Cited by 3
Social Stress Alters the Severity of an Animal Model of Multiple Sclerosis
Meagher, M. W., Johnson, R. R., Vichaya, E. G., & Welsh, C. J. (2007) · Springer eBooks · doi:10.1007/978-0-387-48334-4_11 · Cited by 3
Chronic sleep loss alters the inflammatory response and BDNF expression in C57BL/6J mice
Brice, K. N., Braden-Kuhle, P. N., Miller, S. K., Regan, A., Lacy, V. A., Chumley, M. J., & Boehm, G. W. (2024) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2024.578462 · Cited by 2
Gutiérrez‐Coronado, O., Villalobos‐Gutiérrez, P. T., Villaseñor-Garcı́a, M. M., Paredes, J. M. V., & Puebla‐Pérez, A. M. (2015) · European Scientific Journal ESJ · Cited by 2
Matsumoto, T., Komori, T., Yamamoto, M., Shimada, Y., Nakagawa, M., Shiroyama, T., Inui, K., & Okazaki, Y. (2006) · Neuropsychobiology · doi:10.1159/000099946 · Cited by 2
Effects of Lipopolysaccharide Induced Inflammatory Response on Early Embryo Survival in Ewes
Graham, M. R. (2014) · doi:10.33915/etd.232 · Cited by 2
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
Self-citationLeón‐Rodríguez, A., Fernández‐Arjona, M. D. M., Pedraza, C., López‐Aranda, M. F., Visser, R., & López-Ávalos, M. D. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1828445 · Cited by 1
STRESS AND INFLAMMATION: A DETRIMENTAL COMBINATION IN THE DEVELOPMENT OF NEURODEGENERATIVE DISEASE.
de Pablos, R. M., Espinosa‐Oliva, A. M., Soto, M. S., & Venero, J. L. (2014) · Inflammation and Cell Signaling · doi:10.14800/ics.182 · Cited by 1
Kohman, R. A., Tarr, A. J., McLinden, K. A., & Boehm, G. W. (2008) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2008.04.098 · Cited by 1
Stress, aging, and inflammation
Matovic, S., Rummel, C. D., Feldotto, M., & Gouin, J. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-817558-3.00004-4 · Cited by 1
Neural Functions of Hematopoietic‐derived Cells
Derecki, N. C., & Kipnis, J. (2013) · Wiley eBooks · doi:10.1002/9781118314814.ch6 · Cited by 1
Vallès, A. (2003) · TDX (Tesis Doctorals en Xarxa) · Cited by 1
Examining an Animal Model of Depression with Recurrent Depression-like Episodes
Lebedeva, K. A. (2017) · University Library - University of Saskatchewan (University of Saskatchewan) · Cited by 1
O’Loughlin, A. (2011) · Maynooth University ePrints and eTheses Archive (Maynooth University) · Cited by 1
Martin, S. A. (2013) · Illinois Digital Environment for Access to Learning and Scholarship (University of Illinois at Urbana-Champaign)
Temporal Mapping of Acute Stress-Induced Central and Circulating Cytokine Production
Vecchiarelli, H. A. (2014) · Libraries and Cultural Resources (University of Calgary) · doi:10.11575/prism/27994
The Effect of Lipoposaccharide on Depressive-like Behavior Induced by Forced Swim Stress
Pan, Y., Lin, W., Dong-Lin, W. A. N. G., & Han, S. U. N. (2013) · Acta Psychologica Sinica · doi:10.3724/sp.j.1041.2012.00322
Un sustrato biológico para los trastornos somatomorfos
Dimsdale, J. E., & Dantzer, R. (2010) · Elsevier eBooks · doi:10.1016/b978-84-458-2037-7.00006-3
dos Santos, N. B. (2017) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.42.2017.tde-12072017-160810
DWiN, R. (2017) · www.diakonie-in-niedersachsen.de
Early-life stress and inflammatory cytokines in psychoses: from bench to community-based research
Zuelli, F. M. D. G. C. (2020) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/d.17.2020.tde-26072019-154034
Duque, É. D. A. (2019) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.42.2019.tde-15102019-100704
Cytokines and Stressors: Implications for Cancer Immunotherapy
Kusnecov, A. W., & Anisman, H. (2010) · Springer eBooks · doi:10.1007/978-90-481-3725-1_1
Maier, S. F., & Watkins, L. R. (2009) · Wiley eBooks · doi:10.1002/9780470478509.neubb001008
Self-citation(2018) · Elsevier eBooks · doi:10.1016/b978-0-12-811351-6.00026-7
Stressor and cytokine interactions : implications in depressive-like pathology
Gibb, J. (2011) · Carleton University's Institutional Repository (MacOdrum Library, Carleton University) · doi:10.22215/etd/2011-09658
Study on the Immunity Interventions A Deterrent Effect Against Pathogens
Manan, M. A., SHERAZI, M., NAEEM, A., & SHAFIQUE, L. (2022) · University of Sindh Journal of Animal Sciences (USJAS) · doi:10.57038/usjas.v6i03.5202
(2024) · Elsevier eBooks · doi:10.1016/b978-0-443-23565-8.09996-8
Stressor Processes and Effects on Neurobiological Functioning
Anisman, H., Hayley, S. P., & Kusnecov, A. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-23565-8.00018-1
Anisman, H., Hayley, S. P., & Kusnecov, A. W. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-23565-8.00007-7
Dr. Steven F. Maier: A fearless scientist, a rigorous mentor, and a legacy of excellence
Barrientos, R. M., Baratta, M. V., & Frank, M. G. (2025) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2025.04.021
De l’importance des médiateurs du stress dans le contrôle de l’immunité
Bacou, E. (2017) · theses.fr (ABES) · doi:10.70675/c3e20630z2e84z4f0ez9c4ez2ff5647f0f03
Janowski, A. J., Hayashi, K., Plumb, A. N., Lesnak, J. B., Smith, A. F., Rasmussen, L., Gross, E., Post, A. A., Berardi, G., Klein, M. E., et al. (2026) · Scientific Reports · doi:10.1038/s41598-026-62864-x
Huang, W., Lan, M., Liu, J., Ren, X., Xu, H., & Wang, H. (2026) · Psychiatry Research · doi:10.1016/j.psychres.2026.117347
A crosstalk between the immune system and obstructive sleep apnea
Ahmed, S., Gozal, D., Borthakur, A., & Khalyfa, A. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1963127
Schwierling, H. C., Sengupta, S., Noel, J. G., O’Connell, C. J., Potter, A. S., Adam, M., Robson, M. J., & Gardner, J. C. (2026) · The FASEB Journal · doi:10.1096/fj.202504681r
Urbach‐Ross, D. (2009) · Rutgers University Community Repository (Rutgers University) · doi:10.7282/t3rr1zf9
Metadata
- Authors
- Johnson, J. D., O'Connor, K. A., Deak, T., Stark, M., Watkins, L. R., & Maier, S. F.
- Affiliations
- University of Colorado Boulder (US)
- Venue
- Brain, Behavior, and Immunity
- Publisher
- Elsevier BV
- Published
- 2002-08
- Volume
- 16
- Issue
- 4
- Pages
- 461-476
- ISSN
- 0889-1591 (ISSN-L)
- OpenAlex
- W2148779404
- Cited by
- 270
- References
- 91
- Citations by year
- 2026: 5 · 2025: 1 · 2024: 8 · 2023: 5 · 2022: 3 · 2021: 5 · 2020: 6 · 2019: 12 · 2018: 14 · 2017: 17 · 2016: 12 · 2015: 21 · 2014: 20 · 2013: 14 · 2012: 12
- FWCI
- 4.81
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Behavior and Immunity (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (MH-0314, MH-5045, MH-1558, MH-5283)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- lipopolysaccharide, endotoxin, IL-1β, TNF-α, interleukin-6, inflammatory cytokines, innate immune response, stress-immune interaction, hippocampus, hypothalamus, pituitary gland, rats
- MeSH terms
- Animals, Brain, Electroshock, Interleukin-1, Lipopolysaccharides, Male, Stress, Physiological, Time Factors, Tumor Necrosis Factor-alpha, Interleukin-6, Cytokines, Rats, Sprague-Dawley, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
