Immune-mediated impairment of tonic immobility defensive behavior in an experimental model of colonic inflammation

Ulcerative colitis has been associated with psychological distress and an aberrant immune response. The immunomodulatory role of systemic cytokines produced during experimental intestinal inflammation in tonic immobility (TI) defensive behavior remains unknown. The present study characterized the TI...

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Bibliographic Details
Published in:	Pflügers Archiv Vol. 476; no. 11; pp. 1743 - 1760
Main Authors:	Menescal-de-Oliveira, Leda, Brentegani, Mariulza Rocha, Teixeira, Fernanda Pincelli, Giusti, Humberto, Saia, Rafael Simone
Format:	Journal Article
Language:	English
Published:	Berlin/Heidelberg Springer Berlin Heidelberg 01-11-2024 Springer Nature B.V
Subjects:	Acetic acid Animals Biomedical and Life Sciences Biomedicine c-Fos protein Cell Biology Colitis - chemically induced Colitis - immunology Colitis - metabolism Cyclooxygenase 2 - metabolism Cyclooxygenase-2 Cytokines - metabolism Defensive behavior Dexamethasone Dexamethasone - pharmacology Disease Models, Animal Guinea Pigs Human Physiology Immobility Response, Tonic Immune response Immunomodulation Immunoreactivity Inflammatory bowel disease Inflammatory bowel diseases Infliximab Infliximab - pharmacology Infliximab - therapeutic use Interleukin 10 Interleukin 8 Intestine Male Molecular Medicine Monoclonal antibodies Neuroscience Neurosciences Periaqueductal Gray - metabolism Periaqueductal gray area Prostaglandin endoperoxide synthase Prostaglandins Proto-Oncogene Proteins c-fos - metabolism Receptors Substantia grisea Tonic immobility Tumor necrosis factor-TNF Tumor necrosis factor-α Ulcerative colitis Periaqueductal gray matter Infliximab Cytokines Tumor necrosis factor Interleukin Inflammatory response Cyclooxygenase-2 Colitis Microglia Neuronal activation
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Summary:	Ulcerative colitis has been associated with psychological distress and an aberrant immune response. The immunomodulatory role of systemic cytokines produced during experimental intestinal inflammation in tonic immobility (TI) defensive behavior remains unknown. The present study characterized the TI defensive behavior of guinea pigs subjected to colitis induction at the acute stage and after recovery from intestinal mucosa injury. Moreover, we investigated whether inflammatory mediators (tumor necrosis factor (TNF)-α, interleukin (IL)-1β, IL-8, IL-10, and prostaglandins) act on the mesencephalic nucleus, periaqueductal gray matter (PAG). Colitis was induced in guinea pigs by intrarectal administration of acetic acid. The TI defensive behavior, histology, cytokine production, and expression of c-FOS, IBA-1, and cyclooxygenase (COX)-2 in PAG were evaluated. Colitis reduced the duration of TI episodes from the first day, persisting throughout the 7-day experimental period. Neuronal c-FOS immunoreactivity was augmented in both columns of the PAG (ventrolateral (vlPAG) and dorsal), but there were no changes in IBA-1 expression. Dexamethasone, infliximab, and parecoxib treatments increased the duration of TI episodes, suggesting a modulatory role of peripheral inflammatory mediators in this behavior. Immunoneutralization of TNF-α, IL-1β, and IL-8 in the vlPAG reversed all effects produced by colitis. In contrast, IL-10 neutralization further reduced the duration of TI episodes. Our results reveal that peripherally produced inflammatory mediators during colitis may modulate neuronal functioning in mesencephalic structures such as vlPAG.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23
ISSN:	0031-6768 1432-2013 1432-2013
DOI:	10.1007/s00424-024-03011-1