Literature DB >> 26224864

Probiotics Improve Inflammation-Associated Sickness Behavior by Altering Communication between the Peripheral Immune System and the Brain.

Charlotte D'Mello1, Natalie Ronaghan2, Raza Zaheer2, Michael Dicay2, Tai Le1, Wallace K MacNaughton2, Michael G Surrette3, Mark G Swain4.   

Abstract

Patients with systemic inflammatory diseases (e.g., rheumatoid arthritis, inflammatory bowel disease, chronic liver disease) commonly develop debilitating symptoms (i.e., sickness behaviors) that arise from changes in brain function. The microbiota-gut-brain axis alters brain function and probiotic ingestion can influence behavior. However, how probiotics do this remains unclear. We have previously described a novel periphery-to-brain communication pathway in the setting of peripheral organ inflammation whereby monocytes are recruited to the brain in response to systemic TNF-α signaling, leading to microglial activation and subsequently driving sickness behavior development. Therefore, we investigated whether probiotic ingestion (i.e., probiotic mixture VSL#3) alters this periphery-to-brain communication pathway, thereby reducing subsequent sickness behavior development. Using a well characterized mouse model of liver inflammation, we now show that probiotic (VSL#3) treatment attenuates sickness behavior development in mice with liver inflammation without affecting disease severity, gut microbiota composition, or gut permeability. Attenuation of sickness behavior development was associated with reductions in microglial activation and cerebral monocyte infiltration. These events were paralleled by changes in markers of systemic immune activation, including decreased circulating TNF-α levels. Our observations highlight a novel pathway through which probiotics mediate cerebral changes and alter behavior. These findings allow for the potential development of novel therapeutic interventions targeted at the gut microbiome to treat inflammation-associated sickness behaviors in patients with systemic inflammatory diseases. SIGNIFICANCE STATEMENT: This research shows that probiotics, when eaten, can improve the abnormal behaviors (including social withdrawal and immobility) that are commonly associated with inflammation. Probiotics are able to cause this effect within the body by changing how the immune system signals the brain to alter brain function. These findings broaden our understanding of how probiotics may beneficially affect brain function in the context of inflammation occurring within the body and may open potential new therapeutic alternatives for the treatment of these alterations in behavior that can greatly affect patient quality of life.
Copyright © 2015 the authors 0270-6474/15/3510822-10$15.00/0.

Entities:  

Keywords:  TNF-alpha; cerebral intravital microscopy; microglia; monocytes

Mesh:

Year:  2015        PMID: 26224864      PMCID: PMC6605112          DOI: 10.1523/JNEUROSCI.0575-15.2015

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  42 in total

1.  TNF-alpha-secreting monocytes are recruited into the brain of cholestatic mice.

Authors:  Steven M Kerfoot; Charlotte D'Mello; Henry Nguyen; Maureen N Ajuebor; Paul Kubes; Tai Le; Mark G Swain
Journal:  Hepatology       Date:  2006-01       Impact factor: 17.425

2.  Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system.

Authors:  J D Sedgwick; S Schwender; H Imrich; R Dörries; G W Butcher; V ter Meulen
Journal:  Proc Natl Acad Sci U S A       Date:  1991-08-15       Impact factor: 11.205

3.  Effects of insulin-like growth factor-I on cytokine-induced sickness behavior in mice.

Authors:  Rose-Marie Bluthé; Keith W Kelley; Robert Dantzer
Journal:  Brain Behav Immun       Date:  2006-01       Impact factor: 7.217

4.  Lactobacillus and bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles.

Authors:  Liam O'Mahony; Jane McCarthy; Peter Kelly; George Hurley; Fangyi Luo; Kersang Chen; Gerald C O'Sullivan; Barry Kiely; J Kevin Collins; Fergus Shanahan; Eamonn M M Quigley
Journal:  Gastroenterology       Date:  2005-03       Impact factor: 22.682

5.  Beneficial effects of a probiotic VSL#3 on parameters of liver dysfunction in chronic liver diseases.

Authors:  Carmela Loguercio; Alessandro Federico; Concetta Tuccillo; Fulvia Terracciano; Mauro Valeriano D'Auria; Claudio De Simone; Camillo Del Vecchio Blanco
Journal:  J Clin Gastroenterol       Date:  2005-07       Impact factor: 3.062

6.  Selective activation of STAT3 in human monocytes stimulated by G-CSF: implication in inhibition of LPS-induced TNF-alpha production.

Authors:  Saori Nishiki; Fumihiko Hato; Noriko Kamata; Erina Sakamoto; Taro Hasegawa; Akiko Kimura-Eto; Masayuki Hino; Seiichi Kitagawa
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Review 8.  From inflammation to sickness and depression: when the immune system subjugates the brain.

Authors:  Robert Dantzer; Jason C O'Connor; Gregory G Freund; Rodney W Johnson; Keith W Kelley
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9.  Downregulated hypothalamic 5-HT3 receptor expression and enhanced 5-HT3 receptor antagonist-mediated improvement in fatigue-like behaviour in cholestatic rats.

Authors:  H Nguyen; H Wang; T le; W Ho; K A Sharkey; M G Swain
Journal:  Neurogastroenterol Motil       Date:  2007-09-27       Impact factor: 3.598

10.  Actin-binding proteins coronin-1a and IBA-1 are effective microglial markers for immunohistochemistry.

Authors:  Zeshan Ahmed; Gerry Shaw; Ved P Sharma; Cui Yang; Eileen McGowan; Dennis W Dickson
Journal:  J Histochem Cytochem       Date:  2007-03-06       Impact factor: 2.479

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Journal:  Pharmacol Ther       Date:  2015-11-26       Impact factor: 12.310

2.  Perspective: Neuroregenerative Nutrition.

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Review 3.  Role and effective therapeutic target of gut microbiota in NAFLD/NASH.

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4.  Putative modulation of the gut microbiome by probiotics enhances preference for novelty in a preliminary double-blind placebo-controlled study in ferrets.

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Journal:  Neurosci Biobehav Rev       Date:  2018-11-22       Impact factor: 8.989

Review 6.  Interactions between the microbiota, immune and nervous systems in health and disease.

Authors:  Thomas C Fung; Christine A Olson; Elaine Y Hsiao
Journal:  Nat Neurosci       Date:  2017-01-16       Impact factor: 24.884

Review 7.  Inflammation Effects on Motivation and Motor Activity: Role of Dopamine.

Authors:  Jennifer C Felger; Michael T Treadway
Journal:  Neuropsychopharmacology       Date:  2016-08-02       Impact factor: 7.853

Review 8.  Contact-Dependent Growth Inhibition (CDI) and CdiB/CdiA Two-Partner Secretion Proteins.

Authors:  Julia L E Willett; Zachary C Ruhe; Celia W Goulding; David A Low; Christopher S Hayes
Journal:  J Mol Biol       Date:  2015-09-24       Impact factor: 5.469

9.  Targeting inflammatory monocytes in sepsis-associated encephalopathy and long-term cognitive impairment.

Authors:  Graciela Andonegui; Erin L Zelinski; Courtney L Schubert; Derrice Knight; Laura A Craig; Brent W Winston; Simon C Spanswick; Björn Petri; Craig N Jenne; Janice C Sutherland; Rita Nguyen; Natalie Jayawardena; Margaret M Kelly; Christopher J Doig; Robert J Sutherland; Paul Kubes
Journal:  JCI Insight       Date:  2018-05-03

10.  Gut Microbiota Dysbiosis Enhances Migraine-Like Pain Via TNFα Upregulation.

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Journal:  Mol Neurobiol       Date:  2019-08-04       Impact factor: 5.590

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