The DOI matches its Crossref record; 61 of the 61 references it cites were found in a registry or an index.
Stress induces the translocation of cutaneous and gastrointestinal microflora to secondary lymphoid organs of C57BL/6 mice
Abstract
Mammals are colonized by a vast array of bacteria that reside as part of the host's microflora. Despite their enormous levels, these microorganisms tend to be restricted to cutaneous and mucosal surfaces. In the current experiment, only a small percentage of non-stressed mice exhibited detectable levels of bacteria in their inguinal lymph nodes (ILN), spleen, liver, or mesenteric lymph nodes (MLN). However, after experiencing repeated social disruption (SDR), a significant increase in the number of animals having bacteria in their ILN and MLN was found. Since SDR involves fighting in which bite wounds on the skin could provide a portal of entry into the host, it was determined whether experimental wounding (full-thickness skin biopsy), chronic restraint (which is a potent stressor that does not disrupt the skin barrier), or wounding combined with restraint would increase the occurrence of bacteria in secondary lymphoid tissues and liver. Wounding did not significantly increase the prevalence of bacteria in the ILN, MLN, or liver. Interestingly, a larger percentage of restrained and restrained plus wounded mice, in comparison to controls, had bacteria in the ILN, MLN, and liver. Although the stressors increased the number of animals that became colonized, the levels of bacteria in the stressed mice were similar to the levels found in the few non-stressed mice that did become colonized. Our results indicate that psychological components of social stress facilitate the translocation of indigenous bacteria into the host, thus identifying an additional facet through which stressors may impact health.
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“Increased intestinal permeability caused by stress allows microbiota to cross the gut epithelial barrier to trigger the mucosal immune reactions (42) and then transfer to secondary lymphoid organs (46) to activate the innate immune system.”
From Stress triggers flare of inflammatory bowel disease in children and adults (2019) · cites this paper as [46]
In the citing paper
“Stress can also break the established tolerance and augments immune responses in chronic intestinal inflammation.”
From Stress triggers flare of inflammatory bowel disease in children and adults (2019) · cites this paper as [46]
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InfluentialMicrobial endocrinology: Host-bacteria communication within the gut microbiome
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Belei, O., Basaca, D.-G., Olariu, L., Pantea, M., Bozgan, D., Nanu, A.-M., Sîrbu, I., Mărginean, O., & Enătescu, I. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13051361 · Cited by 30
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BackgroundCampisi, J., Sharkey, C. M., Johnson, J. D., Asea, A. A. A., Maslanik, T., Bernstein-Hanley, I., & Fleshner, M. (2012) · Stress · doi:10.3109/10253890.2011.653596 · Cited by 25
“…translocation from the gut (Deitch and Berg 1987; Horton 1994; Katafuchi et al. 2003; Nettelbladt et al. 2003; Nazli et al. 2004; Velin et al. 2004; Bailey et al. 2006), has led us to speculate that perhaps some or all of the endogenous Hsp72 released by acute stress into the blood may be…”
Role of the Intestinal Microbiota in Host Responses to Stressor Exposure
Mackos, A. R., Varaljay, V. A., Maltz, R. M., Gur, T., & Bailey, M. T. (2016) · International review of neurobiology · doi:10.1016/bs.irn.2016.08.002 · Cited by 25
Self-citationSteinberger, K. J., Bailey, M. T., Gross, A. C., Sumner, L. A., Voorhees, J. L., Crouser, N. J., Curry, J. M., Wang, Y., DeVries, A. C., Marsh, C. B., et al. (2020) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-19-0370 · Cited by 21
“For example, social disruption promotes a proinflammatory phenotype characterized by elevated levels of IL6 and IL10 (27), enhanced macrophage activity (10), diminished inflammatory responsiveness to glucocorticoids (11), and splenomegaly stemming from a large increase in the number of splenic CD11bþ myeloid cells, as…”
BackgroundSelf-citationZaytsoff, S. J. M., Uwiera, R. R. E., & Inglis, G. D. (2020) · Microorganisms · doi:10.3390/microorganisms8101518 · Cited by 21
“A study investigating the impacts of a social stressor in mice showed that bacteria could translocate to secondary lymphoid tissue under conditions of stress [35].”
BackgroundGlucocorticoid induced group 2 innate lymphoid cell overactivation exacerbates experimental colitis
Feng, B., Lin, L., Li, L., Xin, L., Liu, C., Zhao, Z., Li, S., & Li, Y. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.863034 · Cited by 18
The impact of acute-stressor exposure on splenic innate immunity: A gene expression analysis
Maslanik, T., Bernstein-Hanley, I., Helwig, B. G., & Fleshner, M. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.08.006 · Cited by 18
“Acute stressor exposure, for example, can increase bacterial clearance (Bailey et al., 2006, 2007), proliferation of splenic macrophages (Bailey et al., 2007; Salman et al., 1999), and increase antimicrobial responses from splenocytes (Bailey et al., 2004; Campisi et al., 2002), decrease viral…”
From gut to brain: understanding the role of microbiota in inflammatory bowel disease
Wang, S., Zhou, S., Han, Z., Yu, B., Xu, Y., Lin, Y., Chen, Y., Jin, Z., Li, Y., Cao, Q., et al. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1384270 · Cited by 17
Sharaff, F., & Freestone, P. P. E. (2011) · Open Life Sciences · doi:10.2478/s11535-011-0067-z · Cited by 17
Social Isolation and Breast Cancer
Hilakivi-Clarke, L. A., & Andrade, F. D. O. (2023) · Endocrinology · doi:10.1210/endocr/bqad126 · Cited by 22
Extracellular Hsp 72: A Double-Edged Sword for Host Defense
Fleshner, M., Johnson, J. D., & Friedman, J. (2007) · Springer eBooks · doi:10.1007/978-1-4020-5585-0_15 · Cited by 15
“, 2003), social disruption (Bailey et al., 2006), water avoidance stress (Velin et al.”
BackgroundMartins, A. S. D. P., Campos, S. B. G., Goulart, M. O. F., Fabiana, & Moura, F. A. (2021) · Biocell · doi:10.32604/biocell.2021.014332 · Cited by 13
Ngwai, Y. B., Iliyasu, H., Young, E., & Owuna, G. (2012) · Jundishapur Journal of Microbiology · doi:10.5812/kowsar.20083645.2372 · Cited by 13
Pneumonia as a long-term consequence of chronic psychological stress in BALB/c mice
Kiank, C., Daeschlein, G., & Schuett, C. (2008) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2008.05.003 · Cited by 13
Beyond the neuro-immune interplay in depression: Could gut microbes be the missing link?
Audet, M. (2021) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2021.100308 · Cited by 12
“…al., 2014; Menard et al., 2017; Szyszkowicz et al., 2017), stressors induced damages to the intestinal barrier and allowed the passage of bacterial fragments from the intestinal lumen to the bloodstream in male rodents and in humans (Bailey et al., 2006; Karl et al., 2017; S€oderholm et al., 2002).”
BackgroundThe gut microbiota: A new player in the innate immune stress response?
Fleshner, M. (2010) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2010.12.007 · Cited by 11
“Gut microbiota also provide a natural defensive barrier against patho- genic bacterial infection (O’Hara and Shanahan, 2006) and can be impacted by stressors (Bailey et al., 2006).”
BackgroundMaltz, R. M., Marte-Ortiz, P., Rajasekera, T. A., Loman, B. R., Gur, T., & Bailey, M. T. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23042000 · Cited by 10
Self-citationJaggers, R. M., DiSabato, D. J., Loman, B. R., Kontic, D., Spencer, K. D., Allen, J. M., Godbout, J. P., Quan, N., Gur, T. L., & Bailey, M. T. (2022) · Journal of Inflammation Research · doi:10.2147/jir.s332793 · Cited by 11
“Interestingly, we have observed changes in microbial composition, as well as increases in bacterial translocation, in mice exposed to a prolonged restraint stressor.(15) However, this type of chronic, physical restraint leads to suppressed inflammatory responses rather than enhanced responses.”
BackgroundSelf-citationPredictive tools for the evaluation of microbial effects on drugs during gastrointestinal passage
Pieper, I., & Bertau, M. (2010) · Expert Opinion on Drug Metabolism & Toxicology · doi:10.1517/17425251003769859 · Cited by 12
“Even emotions and stress have been reported to affect both gut flora composition and microbial metabolism [33].”
BackgroundSlevin, M. C., Houtz, J. L., Vitousek, M. N., Baldassarre, D. T., & Anderson, R. C. (2024) · Oikos · doi:10.1111/oik.10905 · Cited by 7
Wang, Y., Wang, W., Zhang, Y., Zhao, X., & Yang, D. (2010) · Journal of Huazhong University of Science and Technology [Medical Sciences] · doi:10.1007/s11596-010-0445-1 · Cited by 7
“The main pathway of enteric bacterial translocation during cirrhosis is via the mesenteric lymph nodes [ 18 ] . In addition, the immunological injury caused by intestinal pro-inflammatory factor MPO might also contribute to the development of HPS.”
BackgroundStevens, M. P. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-20215-0_6 · Cited by 8
Serum myoglobin, but not lipopolysaccharides, is predictive of AMPH-induced striatal neurotoxicity
Levi, M. S., Patton, R. E., Hanig, J. P., Tranter, K. M., George, N. I., James, L. P., Davis, K. J., & Bowyer, J. F. (2013) · NeuroToxicology · doi:10.1016/j.neuro.2013.04.003 · Cited by 6
Gut Microbiome-Brain Communications Regulate Host Physiology and Behavior
Serre, C. B. D. L. (2015) · Journal of Nutritional Health & Food Science · doi:10.15226/jnhfs.2015.00141 · Cited by 6
“In their previous study, the authors also showed that the secondary lymphoid organs were involved in the stress-induced increase in bacterial translocation [119].”
BackgroundInfluentialStress and the Gastrointestinal System
Bonaz, B. L. (2016) · Springer eBooks · doi:10.1007/978-3-319-28609-9_7 · Cited by 6
In Vivo Tissue Source and Releasing Signal for Endogenous Extracellular Hsp72
Fleshner, M., Maslanik, T., & Beninson, L. A. (2009) · Heat shock proteins · doi:10.1007/978-90-481-3381-9_12 · Cited by 5
Radiation enteropathy‐related depression: A neglectable course of disease by gut bacterial dysbiosis
Liu, X. W., Li, Y., Gu, M., Xu, T., Wang, C., & Chang, P. (2024) · Cancer Medicine · doi:10.1002/cam4.6865 · Cited by 4
“99 Blood-entered LPS activates microglial TLR 4 in the brain, thus inducing depressive-like behaviors by eliciting excessive inflammatory responses.”
Investigating the Resistance of Escherichia coli Against Some Selected Antimicrobials in Bam
Ayatollahi, J., Vahidi, A., Shahcheraghi, S. H., Bagheripour, A., Lotfi, M., Lotfi, M., & Lotfi, S. R. (2013) · Jundishapur Journal of Microbiology · doi:10.5812/jjm.7407 · Cited by 5
“Based on the particular present strain, it can provide resistance against pathogenic organisms or can itself be pathogenic, causing diseases at intestinal and extra-intestinal sites (4).”
Prevention of Heat Stress Adverse Effects in Rats by Bacillus subtilis Strain
Sorokulova, I. B., Globa, L. P., Pustovyy, O. M., & Vodyanoy, V. J. (2016) · Journal of Visualized Experiments · doi:10.3791/54122 · Cited by 5
Mode of Action of Dietary Dexamethasone May Not Be Dependent Upon Microbial Mechanisms in Broilers
Duff, A. F., Baxter, M. F. A., Graham, D. B., Hargis, B. M., & Bielke, L. R. (2019) · Microorganisms · doi:10.3390/microorganisms7090346 · Cited by 5
The Effects of Psychological Stressors on the Intestinal Microbiota
Bailey, M. T. (2009) · Bioscience and Microflora · doi:10.12938/bifidus.28.125 · Cited by 3
Self-citationCan some microbes promote host stress and benefit evolutionarily from this strategy?
Aktipis, A., & Beltrán, D. G. (2020) · BioEssays · doi:10.1002/bies.202000188 · Cited by 4
“[35] In mice, social stress leads to greater microbial colonization of the lymph nodes and liver,[36] suggesting that the physiological changes that occur during stress may increase microbial colonization opportunities throughout the body.”
BackgroundStevens, M. P. (2010) · Springer eBooks · doi:10.1007/978-1-4419-5576-0_6 · Cited by 4
Development of an In Vitro Fermentation Model to Culture the Human Distal Gut Microbiota
McDonald, J. A. K. (2013) · The Atrium (University of Guelph) · Cited by 4
Metadata
- Authors
- Bailey, M. T., Engler, H., & Sheridan, J. F.
- Affiliations
- The Ohio State University (US)
- Corresponding author
- Bailey, Michael T.
- Venue
- Journal of Neuroimmunology
- Publisher
- Elsevier BV
- Published
- 2006-02
- Volume
- 171
- Issue
- 1-2
- Pages
- 29-37
- ISSN
- 0165-5728 (ISSN-L)
- OpenAlex
- W2038270610
- Cited by
- 133
- References
- 61
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 4 · 2023: 4 · 2022: 5 · 2021: 6 · 2020: 7 · 2019: 7 · 2018: 4 · 2017: 5 · 2016: 10 · 2015: 8 · 2014: 3 · 2013: 9 · 2012: 10
- FWCI
- 2.50
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neuroimmunology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (R01MH046801, R01-MH46801)
- National Institute of Dental and Craniofacial Research (T32 DE14320, T32DE014320)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Stress, Anesthesia, and Immune Response
- Keywords
- psychological stress, bacterial translocation, secondary lymphoid organs, gut microbiota, skin microbiome, social stress, social disruption, inguinal lymph nodes, mesenteric lymph nodes, spleen, liver colonization, C57BL/6 mice
- MeSH terms
- Animals, Biopsy, Cell Movement, Digestive System, Lymph Nodes, Male, Mice, Inbred C57BL, Random Allocation, Restraint, Physical, Skin, Specific Pathogen-Free Organisms, Stress, Physiological, Bacterial Translocation, Mice
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