Cited by 124Tryptophan and brain disordersInflammatory Bowel DiseaseNeuroinflammation and Neurodegeneration Mechanisms

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Neuroinflammation as an etiological trigger for depression comorbid with inflammatory bowel disease

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Craig, Colin F., Filippone, Rhiannon T., Stavely, Rhian, Bornstein, Joel C., Apostolopoulos, Vasso, Nurgali, Kulmira·2022·Journal of Neuroinflammation

DOI 10.1186/s12974-021-02354-1PMC PMC8729103

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Abstract

Patients with inflammatory bowel disease (IBD) suffer from depression at higher rates than the general population. An etiological trigger of depressive symptoms is theorised to be inflammation within the central nervous system. It is believed that heightened intestinal inflammation and dysfunction of the enteric nervous system (ENS) contribute to impaired intestinal permeability, which facilitates the translocation of intestinal enterotoxins into the blood circulation. Consequently, these may compromise the immunological and physiological functioning of distant non-intestinal tissues such as the brain. In vivo models of colitis provide evidence of increased blood–brain barrier permeability and enhanced central nervous system (CNS) immune activity triggered by intestinal enterotoxins and blood-borne inflammatory mediators. Understanding the immunological, physiological, and structural changes associated with IBD and neuroinflammation may aid in the development of more tailored and suitable pharmaceutical treatment for IBD-associated depression.

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Fig. 1 Schematic overview of the mechanisms underlying intestinal barrier dysfunction commonly seen in human IBD and animal models of colitis. Impaired mucous production and composition and/or impaired tight junction protein localisation and production result in luminal microbiota and toxin paracellularly translocating into the intestinal lamina propria layer. Immune cells in this region interacting with antigens trigger the production of inflammatory mediators, which facilitate the recruitment of other leukocytes and lymphocytes. Inflammatory mediators enter peripheral circulation whereby they may trigger distant immunological activation. FADD Fas-associated protein with death domain; IFN Interferon; IL Interleukin; MLC myosin light chain; MLCK myosin light-chain kinase; MMP metalloproteinase, P phosphate; PI3K phosphoinositide 3-kinase; ROCK Rho associated protein kinase; TJ tight junction; TLR toll-like receptor; TNF tumour necrosis factor; ZO zonula occludensCC BY · PubMed Central

Fig. 2 Schematic diagram of neuroinflammatory changes seen in and postulated in human and animals with intestinal inflammation. Circulating inflammatory mediators enter into brain parenchyma through the suggested mechanisms whereby they may modulate local glia populations such as the microglia. Microglia can impact the various neurobiological correlates of depression including neurodegeneration, serotonin biosynthesis, and hippocampal neurogenesis. 5-HT 5-hydroxytryptamine (serotonin); BDNF brain-derived neurotrophic factor; CCL2 chemokine (C–C motif) ligand 2; CNS central nervous system; COX cyclooxygenase; CVO circumventricular organ; EC endothelial cells; Glu glutamate; IDO indoleamine-pyrrole 2,3-dioxygenase; IL interleukin; NO nitric oxide; NOS nitric oxide synthase; PGE2 prostaglandin E2; PVN perivascular macrophages; QA quinolinic acid; ROS reactive oxygen species; TJ tight junction; TNF tumour necrosis factor; TNFR1 tumour necrosis factor receptor-1; TRP tryptophanCC BY · PubMed Central

Fig. 3 Schematic representation of neuroinflammatory-induced impairment of the HPA axis functioning. Resultant neuroinflammation associated with animal models of colitis may induce damage or neurobiological alteration in important regions associated with inhibition of the HPA axis. This may trigger the aberrant secretion of hippocampal, pituitary, or adrenal hormones triggering worsening of intestinal and cortical inflammation and depressive symptoms. ACTH adrenal corticotrophin-releasing hormone; CA1 cornu ammonis 1; CNS, central nervous system; CRH corticotrophin releasing hormone; HPA hypothalamic–pituitary–adrenal; PVN paraventricular nucleusCC BY · PubMed Central

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Authors: Craig, C. F., Filippone, R. T., Stavely, R., Bornstein, J. C., Apostolopoulos, V., & Nurgali, K.
Affiliations: Sunshine Hospital (AU)
Harvard University (US)
The University of Melbourne (AU)
Australian Institute for Musculoskeletal Science (AU)
Corresponding author: Nurgali, Kulmira
ORCID: Craig, Colin F.
Stavely, Rhian
Bornstein, Joel C.
Apostolopoulos, Vasso
Nurgali, Kulmira
Venue: Journal of Neuroinflammation
Publisher: Springer Science and Business Media LLC
Published: 2022-01-04
Volume: 19
Issue: 1
Pages: 4-4
ISSN: 1742-2094 (ISSN-L)
DOI: 10.1186/s12974-021-02354-1
PMC: PMC8729103
OpenAlex: W4206422593
Cited by: 124
References: 373
Citations by year: 2026: 26 · 2025: 39 · 2024: 30 · 2023: 20 · 2022: 9
FWCI: 1.85
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
creativecommons.org/licenses/by/4.0 (vor)
Locations: Journal of Neuroinflammation (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Victoria University Research Repository (Victoria University) (submittedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Minerva Access (University of Melbourne) (submittedVersion, cc-by)
Funders: Victoria University
National Health and Medical Research Council (1158952)
Topics: Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Health Sciences › Medicine › Gastroenterology › Inflammatory Bowel Disease
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: neuroinflammation, depression, inflammatory bowel disease, intestinal permeability, enterotoxin, blood-brain barrier permeability, enteric nervous system, colitis, gut-brain axis
MeSH terms: Brain-Gut Axis, Neuroinflammatory Diseases, Depression, Humans, Inflammatory Bowel Diseases

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Neuroinflammation as an etiological trigger for depression comorbid with inflammatory bowel disease

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