Chronic Stress-Induced Depression and Anxiety Priming Modulated by Gut-Brain-Axis Immunity

Chronic stress manifests as depressive- and anxiety-like behavior while recurrent stress elicits disproportionate behavioral impairments linked to stress-induced immunological priming. The gut-brain-microbiota-axis is a promising therapeutic target for stress-induced behavioral impairments as it sim...

Full description

Bibliographic Details
Main Authors: Susan Westfall, Francesca Caracci, Molly Estill, Tal Frolinger, Li Shen, Giulio M. Pasinetti
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-06-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2021.670500/full
_version_ 1818589063603552256
author Susan Westfall
Francesca Caracci
Molly Estill
Tal Frolinger
Li Shen
Giulio M. Pasinetti
Giulio M. Pasinetti
author_facet Susan Westfall
Francesca Caracci
Molly Estill
Tal Frolinger
Li Shen
Giulio M. Pasinetti
Giulio M. Pasinetti
author_sort Susan Westfall
collection DOAJ
description Chronic stress manifests as depressive- and anxiety-like behavior while recurrent stress elicits disproportionate behavioral impairments linked to stress-induced immunological priming. The gut-brain-microbiota-axis is a promising therapeutic target for stress-induced behavioral impairments as it simultaneously modulates peripheral and brain immunological landscapes. In this study, a combination of probiotics and prebiotics, known as a synbiotic, promoted behavioral resilience to chronic and recurrent stress by normalizing gut microbiota populations and promoting regulatory T cell (Treg) expansion through modulation of ileal innate lymphoid cell (ILC)3 activity, an impact reflecting behavioral responses better than limbic brain region neuroinflammation. Supporting this conclusion, a multivariate machine learning model correlatively predicted a cross-tissue immunological signature of stress-induced behavioral impairment where the ileal Treg/T helper17 cell ratio associated to hippocampal chemotactic chemokine and prefrontal cortex IL-1β production in the context of stress-induced behavioral deficits. In conclusion, stress-induced behavioral impairments depend on the gut-brain-microbiota-axis and through ileal immune regulation, synbiotics attenuate the associated depressive- and anxiety-like behavior.
first_indexed 2024-12-16T09:34:42Z
format Article
id doaj.art-b381a3a05d3641478a5f87fff0d38d19
institution Directory Open Access Journal
issn 1664-3224
language English
last_indexed 2024-12-16T09:34:42Z
publishDate 2021-06-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Immunology
spelling doaj.art-b381a3a05d3641478a5f87fff0d38d192022-12-21T22:36:26ZengFrontiers Media S.A.Frontiers in Immunology1664-32242021-06-011210.3389/fimmu.2021.670500670500Chronic Stress-Induced Depression and Anxiety Priming Modulated by Gut-Brain-Axis ImmunitySusan Westfall0Francesca Caracci1Molly Estill2Tal Frolinger3Li Shen4Giulio M. Pasinetti5Giulio M. Pasinetti6Department of Neurology, Icahn School of Medicine at Mount Sinai, New York, NY, United StatesDepartment of Neurology, Icahn School of Medicine at Mount Sinai, New York, NY, United StatesDepartment of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY, United StatesDepartment of Neurology, Icahn School of Medicine at Mount Sinai, New York, NY, United StatesDepartment of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY, United StatesDepartment of Neurology, Icahn School of Medicine at Mount Sinai, New York, NY, United StatesGeriatric Research, Education and Clinical Center, James J. Peters Veterans Affairs Medical Center, Bronx, NY, United StatesChronic stress manifests as depressive- and anxiety-like behavior while recurrent stress elicits disproportionate behavioral impairments linked to stress-induced immunological priming. The gut-brain-microbiota-axis is a promising therapeutic target for stress-induced behavioral impairments as it simultaneously modulates peripheral and brain immunological landscapes. In this study, a combination of probiotics and prebiotics, known as a synbiotic, promoted behavioral resilience to chronic and recurrent stress by normalizing gut microbiota populations and promoting regulatory T cell (Treg) expansion through modulation of ileal innate lymphoid cell (ILC)3 activity, an impact reflecting behavioral responses better than limbic brain region neuroinflammation. Supporting this conclusion, a multivariate machine learning model correlatively predicted a cross-tissue immunological signature of stress-induced behavioral impairment where the ileal Treg/T helper17 cell ratio associated to hippocampal chemotactic chemokine and prefrontal cortex IL-1β production in the context of stress-induced behavioral deficits. In conclusion, stress-induced behavioral impairments depend on the gut-brain-microbiota-axis and through ileal immune regulation, synbiotics attenuate the associated depressive- and anxiety-like behavior.https://www.frontiersin.org/articles/10.3389/fimmu.2021.670500/fullprobioticnutraceuticalinnate lymphocyte cellspsychiatrymicrobiota
spellingShingle Susan Westfall
Francesca Caracci
Molly Estill
Tal Frolinger
Li Shen
Giulio M. Pasinetti
Giulio M. Pasinetti
Chronic Stress-Induced Depression and Anxiety Priming Modulated by Gut-Brain-Axis Immunity
Frontiers in Immunology
probiotic
nutraceutical
innate lymphocyte cells
psychiatry
microbiota
title Chronic Stress-Induced Depression and Anxiety Priming Modulated by Gut-Brain-Axis Immunity
title_full Chronic Stress-Induced Depression and Anxiety Priming Modulated by Gut-Brain-Axis Immunity
title_fullStr Chronic Stress-Induced Depression and Anxiety Priming Modulated by Gut-Brain-Axis Immunity
title_full_unstemmed Chronic Stress-Induced Depression and Anxiety Priming Modulated by Gut-Brain-Axis Immunity
title_short Chronic Stress-Induced Depression and Anxiety Priming Modulated by Gut-Brain-Axis Immunity
title_sort chronic stress induced depression and anxiety priming modulated by gut brain axis immunity
topic probiotic
nutraceutical
innate lymphocyte cells
psychiatry
microbiota
url https://www.frontiersin.org/articles/10.3389/fimmu.2021.670500/full
work_keys_str_mv AT susanwestfall chronicstressinduceddepressionandanxietyprimingmodulatedbygutbrainaxisimmunity
AT francescacaracci chronicstressinduceddepressionandanxietyprimingmodulatedbygutbrainaxisimmunity
AT mollyestill chronicstressinduceddepressionandanxietyprimingmodulatedbygutbrainaxisimmunity
AT talfrolinger chronicstressinduceddepressionandanxietyprimingmodulatedbygutbrainaxisimmunity
AT lishen chronicstressinduceddepressionandanxietyprimingmodulatedbygutbrainaxisimmunity
AT giuliompasinetti chronicstressinduceddepressionandanxietyprimingmodulatedbygutbrainaxisimmunity
AT giuliompasinetti chronicstressinduceddepressionandanxietyprimingmodulatedbygutbrainaxisimmunity