Cited by 233Vagus Nerve Stimulation ResearchInflammatory Bowel DiseaseGastrointestinal motility and disorders

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Impaired parasympathetic function increases susceptibility to inflammatory bowel disease in a mouse model of depression

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Ghia, Jean-Eric, Blennerhassett, Patricia, Collins, Stephen M.·2008·Journal of Clinical Investigation

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Abstract

Clinical and experimental evidence indicates that intestinal inflammatory conditions can be exacerbated by behavioral conditions such as depression. The recent demonstration of a tonic counterinflammatory influence mediated by the vagus nerve in experimental colitis provides a potential link between behavior and gut inflammation. Here we show that experimental conditions that induced depressive-like behaviors in mice increased susceptibility to intestinal inflammation by interfering with the tonic vagal inhibition of proinflammatory macrophages and that tricyclic antidepressants restored vagal function and reduced intestinal inflammation. These results show that reserpine-induced monoamine depletion and maternal separation, 2 models for depression, produced a vulnerability to colitis by a mechanism involving parasympathetic transmission and the presence of gut macrophages. The tricyclic antidepressant desmethylimipramine protected against this vulnerability by a vagal-dependent mechanism. Together these results illustrate the critical role of the vagus in both the vulnerability to inflammation induced by depressive-like conditions and the protection afforded by tricyclic antidepressants and rationalize a clinical evaluation of both parasympathomimetics and tricyclic antidepressants in treatment of inflammatory bowel disease.

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Park, J.-Y., & Namgung, U. (2018) · Journal of Inflammation Research · doi:10.2147/jir.s141198 · Cited by 67
“25 It should however be noted that the connectivity between the terminals of autonomic fiber and the target immune cells has not been clearly demonstrated in several organs.”
99th Dahlem Conference on Infection, Inflammation and Chronic Inflammatory Disorders: Psycho-neuroimmunology and the intestinal microbiota: clinical observations and basic mechanisms
Bienenstock, J., & Collins, S. M. (2010) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2010.04124.x · Cited by 59
Self-citation
Vagotomy and insights into the microbiota-gut-brain axis
Liu, Y., & Forsythe, P. (2021) · Neuroscience Research · doi:10.1016/j.neures.2021.04.001 · Cited by 67
Management of stress in inflammatory bowel disease: a therapeutic option?
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5‐HT3 receptors promote colonic inflammation via activation of substance P/neurokinin‐1 receptors in dextran sulphate sodium‐induced murine colitis
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“Assessment of disease activity index The disease activity index (DAI) was expressed as the sum of the scores assigned to reflect the following: body weight loss (0 = <5%, 1 = 5–10%, 2 = 10–15%, 3 = 15–20% and 4 = >20%), stool consistency (0 = normal, 1 = soft but still formed, 2 = very soft, 3 = diarrhoea and 4 = seve…”
BackgroundMethod
Diagnosis and management of functional symptoms in inflammatory bowel disease in remission
Teruel, C. (2016) · World Journal of Gastrointestinal Pharmacology and Therapeutics · doi:10.4292/wjgpt.v7.i1.78 · Cited by 47
Sexual development of mouse germ cells: Nanos2 promotes the male germ cell fate by suppressing the female pathway
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Vagus nerve cholinergic circuitry to the liver and the gastrointestinal tract in the neuroimmune communicatome
Metz, C. N., & Pavlov, V. A. (2018) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00195.2018 · Cited by 61
“An intriguing positive correlation between impaired vagus nerve cholinergic control of macrophage activation and proinflammatory function and enhanced susceptibility to intestinal inflammation and colitis has been demonstrated in mice with depressive-like behavior (20).”
Background
Evaluation of chemical mediators and cellular response during acute and chronic gut inflammatory response induced by dextran sodium sulfate in mice.
Bento, A., Leite, D. F., Marcon, R., Claudino, R., Dutra, R., Cola, M., Martini, A. C., & Calixto, J. (2012) · Biochemical Pharmacology · doi:10.1016/j.bcp.2012.09.007 · Cited by 54
Efficacy of duloxetine add on in treatment of inflammatory bowel disease patients: A double-blind controlled study
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“[3,4] There is an important pathophysiological relations and common pathways between some psychiatric disorders such as anxiety or depression and IBD, which is related to impaired function of immunoregulatory circuits.[5,6,7,8] Clinical studies shows that many of the patients experience depression and anxiety that is…”
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Self-citation
Early life adversity in piglets induces long-term upregulation of the enteric cholinergic nervous system and heightened, sex-specific secretomotor neuron responses
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Cholinergic Modulation of Type 2 Immune Responses
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Effects on neuroendocrinoimmune network of Lizhong Pill in the reserpine induced rats with spleen deficiency in traditional Chinese medicine.
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“…2005; Martinez-Olivares et al., 2006; Sreemantula et al., 2004; Verheij and Cools, 2007), and as a result, reserpine administration in rats can induce depressive behavior (Ghia et al., 2008) and a marked hypothermia (Bill et al., 1989) which are accompanied by impaired parasympathetic function.”
Background
Vagal Modulation of the Inflammatory Response in Sepsis
Wang, D., Yin, Y., & Yao, Y.-M. (2016) · International Reviews of Immunology · doi:10.3109/08830185.2015.1127369 · Cited by 57
“Tricyclic antidepressants reduced intestinal inflammation via a vagal-dependent mechanism [61].”
Background
Behavioral despair associated with a mouse model of Crohn's disease: Role of nitric oxide pathway
Heydarpour, P., Rahimian, R., Fakhfouri, G., Khoshkish, S., Fakhraei, N., Salehi-Sadaghiani, M., Wang, H., Abbasi, A., Dehpour, A. R., & Ghia, J. (2015) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2015.08.004 · Cited by 49
“We have previously shown that vagal nerve integrity is an important protective factor in experimental colitis (Ghia et al. , 2007, 2008).”
Self-citation
Clinical and experimental evidence of sympathetic neural dysfunction during inflammatory bowel disease
Lomax, L. B., Chisholm, S. P., Lukewich, M. K., & Lomax, A. E. (2009) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2009.05242.x · Cited by 46
Vagotomy Affects the Development of Oral Tolerance and Increases Susceptibility to Develop Colitis Independently of α-7 Nicotinic Receptor
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Autonomic Effects of Music in Health and Crohn's Disease: The Impact of Isochronicity, Emotional Valence, and Tempo
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“Specifically, parasympathetic activity is taken to protect against intestinal inflammation [88,89], whereas sympathetic activity appears to worsen intestinal inflammation [90].”
Background
Activation of sirtuin 1 by catalpol-induced down-regulation of microRNA-132 attenuates endoplasmic reticulum stress in colitis
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Salvianolic Acid B Restored Impaired Barrier Function via Downregulation of MLCK by microRNA-1 in Rat Colitis Model
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“According to the morphological criteria described previously, routine hematoxylin and eosin (HE)-stained colon section was measured to represent the degree of inflammation (Cooper et al., 1993; Ghia et al., 2008; Schwanke et al., 2013).”
Method
The vagus nerve as a modulator of intestinal inflammation
van der Zanden, E. P., Boeckxstaens, G. E., & de Jonge, W. J. (2008) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2008.01252.x · Cited by 155
“Nevertheless, vagus nerve activity can regulate disease in animal models 10 , possibly clarified by the role of the spleen in exerting the anti-inflammatory effect of vagus nerve signaling or by changes in autonomic (para)sympathetic balance 96,97 .”
Salicylates Ameliorate Intestinal Inflammation by Activating Macrophage AMPK.
Banskota, S., Wang, H.-Q., Kwon, Y. H., Gautam, J., Gurung, P., Haq, S., Hassan, F. M. N., Bowdish, D., Kim, J.-A., Carling, D., et al. (2020) · Inflammatory Bowel Diseases · doi:10.1093/ibd/izaa305 · Cited by 41
Psychiatric illnesses in inflammatory bowel diseases – psychiatric comorbidity and biological underpinnings
Nowakowski, J., Chrobak, A. A., & Dudek, D. (2016) · Psychiatria Polska · doi:10.12740/pp/62382 · Cited by 50
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Background
IBS-like symptoms in patients with ulcerative colitis
Gracie, D. J., & Ford, A. C. (2015) · Clinical and Experimental Gastroenterology · doi:10.2147/ceg.s58153 · Cited by 42
“Studies have demonstrated that in murine models of quiescent colitis, the induction of depression can reactivate inflammation of the colonic mucosa,(63) which can be attenuated by the administration of antidepressant drugs, and that this is mediated via interference with the inhibition of proinflammatory macrophage ac…”
The Gut's Little Brain in Control of Intestinal Immunity.
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“Acetylcholine Nicotinic acetylcholine receptors Muscarinic acetylcholine receptors Multiple Vagotomy ameliorates colitis [68] Variable outcomes of nicotinic agonists on the course of colitis [51] Vagal nerve stimulation ameliorates intestinal inflammation: Postoperative ileus, [69] septic ileus Intestinal barrier brea…”
Background
Potential of Electrical Neuromodulation for Inflammatory Bowel Disease
Cheng, J., Shen, H., Chowdhury, R., Abdi, T., Selaru, F. M., & Chen, J. D. Z. (2019) · Inflammatory Bowel Diseases · doi:10.1093/ibd/izz289 · Cited by 42
The Cholinergic Anti-Inflammatory Pathway as a Conceptual Framework to Treat Inflammation-Mediated Renal Injury
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The Versatile Role of the Vagus Nerve in the Gastrointestinal Tract
Stakenborg, N., Giovangiulio, M. D., Boeckxstaens, G., & Matteoli, G. (2013) · EMJ Gastroenterology · doi:10.33590/emjgastroenterol/10314603 · Cited by 36
Interleukin-17A Increases Neurite Outgrowth from Adult Postganglionic Sympathetic Neurons
Chisholm, S. P., Cervi, A. L., Nagpal, S., & Lomax, A. E. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5343-11.2012 · Cited by 37
Adoptive transfer of macrophage from mice with depression‐like behavior enhances susceptibility to colitis
Ghia, J., Park, A. J., Blennerhassett, P., Khan, W., & Collins, S. (2011) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21531 · Cited by 35
“2%) or reserpine solution (1 lg/day for 14 days) and were placed as previously described.(21) The same day vagotomy and pyloroplasty (VXP) was performed, ventral and dorsal truncal branches of the subdiaphragmatic vagus were cut (1 cm above gastroesophageal junction).”
MethodResultSelf-citation
The role of antidepressants in the management of inflammatory bowel disease (IBD): A short report on a clinical case-note audit
Mikocka-Walus, A. A., Gordon, A. L., Stewart, B. J., & Andrews, J. M. (2012) · Journal of Psychosomatic Research · doi:10.1016/j.jpsychores.2011.06.006 · Cited by 34
“[1] have shown that inducing depression inmice increased their susceptibility to spontaneous intestinal inflammation by interfering with tonic vagal inhibition of pro-inflammatory macrophages.”
Background
Effect of 2 Psychotherapies on Depression and Disease Activity in Pediatric Crohnʼs Disease
Szigethy, E., Youk, A. O., Gonzalez-Heydrich, J., Bujoreanu, S. I., Weisz, J., Fairclough, D., Ducharme, P., Jones, N., Lotrich, F., Keljo, D., et al. (2015) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000358 · Cited by 34
Review article: bugs, inflammation and mood—a microbiota‐based approach to psychiatric symptoms in inflammatory bowel diseases
Thomann, A., Mak, J. W. Y., Zhang, J., Wüstenberg, T., Ebert, M. P., Sung, J. J. �., Bernstein, C. N., Reindl, W., & Ng, S. C. (2020) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.15787 · Cited by 44
Cholinergic receptor activation on epithelia protects against cytokine‐induced barrier dysfunction
Dhawan, S., Hiemstra, I., Verseijden, C., Hilbers, F., Velde, A. T., Willemsen, L., Stap, J., den Haan, J. D., & de Jonge, W. (2015) · Acta Physiologica · doi:10.1111/apha.12469 · Cited by 34
“Third, muscarinic receptors are involved in colitis pathogenesis (Hirota & McKay 2006a, Hirota & Mckay 2006b), where the role of nicotinic receptors in mediating colitis disease course (Ghia et al. 2008) likely involves central activation of muscarinic receptors (Martelli et al.”
Background
Gpr174 Knockout Alleviates DSS-Induced Colitis via Regulating the Immune Function of Dendritic Cells
Wei, W., Mu, S., Han, Y., Chen, Y., Kuang, Z.-S., Wu, X.-Y., Luo, Y., Tong, C.-Y., Zhang, Y., Yang, Y.-L., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.841254 · Cited by 33
“The health condition was monitored daily, and the disease activity index (DAI), including weight loss, stool consistency, and stool bleeding, was scored as described (14).”
Background
Inhibition of Epithelial TNF-α Receptors by Purified Fruit Bromelain Ameliorates Intestinal Inflammation and Barrier Dysfunction in Colitis
Zhou, Z.-J., Wang, L., Feng, P., Yin, L., Wang, C., Zhi, S., Dong, J., Wang, J.-Y., Lin, Y., Chen, D.-P., et al. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01468 · Cited by 33
Exacerbation of DSS ‐induced colitis in mice lacking kinin B 1 receptors through compensatory up‐regulation of kinin B 2 receptors: the role of tight junctions and intestinal homeostasis
Marcon, R., Claudino, R., Dutra, R. C., Bento, A., Schmidt, E., Bouzon, Z., Sordi, R., Morais, R., Pesquero, J. B., & Calixto, J. Β. (2012) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2012.02136.x · Cited by 30
“All animals were examined once a day and the disease activity index (DAI) was assessed as previously described (Ghia et al., 2008).”
Method
Evidence for the role of the brain–gut axis in inflammatory bowel disease: depression as cause and effect?
Taché, Y., & Bernstein, C. N. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.04.032 · Cited by 32
Psychiatric Comorbidities of Inflammatory Bowel Disease: It Is a Matter of Microglia’s Gut Feeling
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“In a pioneer study, Ghia et al. reported that impaired vagal nerve (VN) function increases susceptibility to IBD in a murine model of depression [24].”
Background
Cholinergic Receptors Modulate Immune Complex–Induced Inflammation In Vitro and In Vivo
Vukelic, M., Qing, X., Redecha, P. B., Koo, G. C., & Salmon, J. E. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1203467 · Cited by 29
A magic pill? A qualitative analysis of patients’ views on the role of antidepressant therapy in inflammatory bowel disease (IBD)
Mikocka‐Walus, A. A., Gordon, A. L., Stewart, B. J., & Andrews, J. M. (2012) · BMC Gastroenterology · doi:10.1186/1471-230x-12-93 · Cited by 29
“Moreover, in animal models antidepressant therapy has now been documented to ameliorate visible GI inflammation [22,23].”
Background
Relationship between social support and autonomic function during a stress protocol in ulcerative colitis patients in remission
Maunder, R., Nolan, R. P., Hunter, J., Lancee, W. J., Steinhart, A. H., & Greenberg, G. R. (2011) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21794 · Cited by 31
“Nonetheless, a common psychophysiological relationship may have particular importance in an inflammatory disease, because of the evidence that parasympathetic function downregulates inflammation.(13,18,47) Preliminary observations from our group indicate that fluctuations in HRV markers of parasympathetic function ove…”
Result

Authors: Ghia, J.-E., Blennerhassett, P., & Collins, S. M.
Affiliations: McMaster University (CA)
Corresponding author: Collins, Stephen M.
ORCID: Ghia, Jean-Eric
Collins, Stephen M.
Venue: Journal of Clinical Investigation
Publisher: American Society for Clinical Investigation
Published: 2008-05-01
Volume: 118
Issue: 6
Pages: 2209-18
ISSN: 0021-9738 (ISSN-L)
DOI: 10.1172/jci32849
PMC: PMC2350428
OpenAlex: W2169338224
Cited by: 233
References: 0
Citations by year: 2026: 2 · 2025: 10 · 2024: 13 · 2023: 14 · 2022: 16 · 2021: 10 · 2020: 13 · 2019: 9 · 2018: 12 · 2017: 10 · 2016: 23 · 2015: 16 · 2014: 15 · 2013: 19 · 2012: 10
FWCI: 9.02
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Clinical Investigation (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Institut de France
McMaster University
Crohn's and Colitis Foundation
Crohn's and Colitis Foundation of Canada
Canadian Association of Gastroenterology
Topics: Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
Health Sciences › Medicine › Gastroenterology › Inflammatory Bowel Disease
Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Keywords: depression, inflammatory bowel disease, vagus nerve, parasympathetic nervous system, colitis, tricyclic antidepressants, desmethylimipramine, reserpine, maternal separation, monoamine depletion, gut-brain axis, neuroimmune regulation
MeSH terms: Animals, Antidepressive Agents, Brain, Colitis, Depressive Disorder, Disease Models, Animal, Female, Macrophages, Male, Mice, Inbred C57BL, Parasympathetic Nervous System, Reserpine, Serotonin, Inflammatory Bowel Diseases, Serotonin Agents, Genetic Predisposition to Disease, Mice

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Impaired parasympathetic function increases susceptibility to inflammatory bowel disease in a mouse model of depression

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