Manipulation of gut microbiota blunts the ventilatory response to hypercapnia in adult rats.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Jun 2019
Historique:
received: 10 12 2018
revised: 08 03 2019
accepted: 11 03 2019
pubmed: 23 3 2019
medline: 18 12 2019
entrez: 23 3 2019
Statut: ppublish

Résumé

It is increasingly evident that perturbations to the diversity and composition of the gut microbiota have significant consequences for the regulation of integrative physiological systems. There is growing interest in the potential contribution of microbiota-gut-brain signalling to cardiorespiratory control in health and disease. In adult male rats, we sought to determine the cardiorespiratory effects of manipulation of the gut microbiota following a 4-week administration of a cocktail of antibiotics. We subsequently explored the effects of administration of faecal microbiota from pooled control (vehicle) rat faeces, given by gavage to vehicle- and antibiotic-treated rats. Antibiotic intervention depressed the ventilatory response to hypercapnic stress in conscious animals, owing to a reduction in the respiratory frequency response to carbon dioxide. Baseline frequency, respiratory timing variability, and the expression of apnoeas and sighs were normal. Microbiota-depleted rats had decreased systolic blood pressure. Faecal microbiota transfer to vehicle- and antibiotic-treated animals also disrupted the gut microbiota composition, associated with depressed ventilatory responsiveness to hypercapnia. Chronic antibiotic intervention or faecal microbiota transfer both caused significant disruptions to brainstem monoamine neurochemistry, with increased homovanillic acid:dopamine ratio indicative of increased dopamine turnover, which correlated with the abundance of several bacteria of six different phyla. Chronic antibiotic administration and faecal microbiota transfer disrupt gut microbiota, brainstem monoamine concentrations and the ventilatory response to hypercapnia. We suggest that aberrant microbiota-gut-brain axis signalling has a modulatory influence on respiratory behaviour during hypercapnic stress. FUND: Department of Physiology and APC Microbiome Ireland, University College Cork, Ireland.

Sections du résumé

BACKGROUND BACKGROUND
It is increasingly evident that perturbations to the diversity and composition of the gut microbiota have significant consequences for the regulation of integrative physiological systems. There is growing interest in the potential contribution of microbiota-gut-brain signalling to cardiorespiratory control in health and disease.
METHODS METHODS
In adult male rats, we sought to determine the cardiorespiratory effects of manipulation of the gut microbiota following a 4-week administration of a cocktail of antibiotics. We subsequently explored the effects of administration of faecal microbiota from pooled control (vehicle) rat faeces, given by gavage to vehicle- and antibiotic-treated rats.
FINDINGS RESULTS
Antibiotic intervention depressed the ventilatory response to hypercapnic stress in conscious animals, owing to a reduction in the respiratory frequency response to carbon dioxide. Baseline frequency, respiratory timing variability, and the expression of apnoeas and sighs were normal. Microbiota-depleted rats had decreased systolic blood pressure. Faecal microbiota transfer to vehicle- and antibiotic-treated animals also disrupted the gut microbiota composition, associated with depressed ventilatory responsiveness to hypercapnia. Chronic antibiotic intervention or faecal microbiota transfer both caused significant disruptions to brainstem monoamine neurochemistry, with increased homovanillic acid:dopamine ratio indicative of increased dopamine turnover, which correlated with the abundance of several bacteria of six different phyla.
INTERPRETATION CONCLUSIONS
Chronic antibiotic administration and faecal microbiota transfer disrupt gut microbiota, brainstem monoamine concentrations and the ventilatory response to hypercapnia. We suggest that aberrant microbiota-gut-brain axis signalling has a modulatory influence on respiratory behaviour during hypercapnic stress. FUND: Department of Physiology and APC Microbiome Ireland, University College Cork, Ireland.

Identifiants

pubmed: 30898652
pii: S2352-3964(19)30169-0
doi: 10.1016/j.ebiom.2019.03.029
pmc: PMC6606895
pii:
doi:

Substances chimiques

Anti-Bacterial Agents 0
Biomarkers 0
Receptors, Serotonin, 5-HT3 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

618-638

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2019. Published by Elsevier B.V.

Auteurs

Karen M O'Connor (KM)

Department of Physiology, School of Medicine, College of Medicine & Health, University College Cork, Cork, Ireland; Department of Anatomy & Neuroscience, School of Medicine, College of Medicine & Health, University College Cork, Cork, Ireland; APC Microbiome Ireland, University College Cork, Cork, Ireland.

Eric F Lucking (EF)

Department of Physiology, School of Medicine, College of Medicine & Health, University College Cork, Cork, Ireland.

Anna V Golubeva (AV)

APC Microbiome Ireland, University College Cork, Cork, Ireland.

Conall R Strain (CR)

Teagasc Food Research Centre, Moorepark, Fermoy, County Cork, Ireland.

Fiona Fouhy (F)

APC Microbiome Ireland, University College Cork, Cork, Ireland; Teagasc Food Research Centre, Moorepark, Fermoy, County Cork, Ireland.

María C Cenit (MC)

Department of Anatomy & Neuroscience, School of Medicine, College of Medicine & Health, University College Cork, Cork, Ireland; Institute of Agrochemistry and Food Technology (IATA), National Council for Scientific Research (CSIC), Valencia, Spain.

Pardeep Dhaliwal (P)

Department of Physiology, School of Medicine, College of Medicine & Health, University College Cork, Cork, Ireland.

Thomaz F S Bastiaanssen (TFS)

Department of Anatomy & Neuroscience, School of Medicine, College of Medicine & Health, University College Cork, Cork, Ireland; APC Microbiome Ireland, University College Cork, Cork, Ireland.

David P Burns (DP)

Department of Physiology, School of Medicine, College of Medicine & Health, University College Cork, Cork, Ireland.

Catherine Stanton (C)

APC Microbiome Ireland, University College Cork, Cork, Ireland; Teagasc Food Research Centre, Moorepark, Fermoy, County Cork, Ireland.

Gerard Clarke (G)

APC Microbiome Ireland, University College Cork, Cork, Ireland; Department of Psychiatry and Neurobehavioural Science, School of Medicine, College of Medicine & Health, University College Cork, Cork, Ireland.

John F Cryan (JF)

Department of Anatomy & Neuroscience, School of Medicine, College of Medicine & Health, University College Cork, Cork, Ireland; APC Microbiome Ireland, University College Cork, Cork, Ireland.

Ken D O'Halloran (KD)

Department of Physiology, School of Medicine, College of Medicine & Health, University College Cork, Cork, Ireland; APC Microbiome Ireland, University College Cork, Cork, Ireland. Electronic address: k.ohalloran@ucc.ie.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH