Maternal high-fat diet-induced microbiota changes are associated with alterations in embryonic brain metabolites and adolescent behaviour

Autores
Ratsika, Anna; Codagnone, Martín Gabriel; Bastiaanssen, Thomaz F.S.; Hoffmann Sarda, Fabiana A.; Lynch, Caoimhe M.K.; Ventura Silva, Ana Paula; Rosell Cardona, Cristina; Caputi, Valentina; Stanton, Catherine; Fülling, Christine; Clarke, Gerard; Cryan, John F.
Año de publicación
2024
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The developing central nervous system is highly sensitive to nutrient changes during the perinatal period, emphasising the potential impact of alterations of maternal diet on offspring brain development and behaviour. A growing body of research implicates the gut microbiota in neurodevelopment and behaviour. Maternal overweight and obesity during the perinatal period has been linked to changes in neurodevelopment, plasticity and affective disorders in the offspring, with implications for microbial signals from the maternal gut. Here we investigate the impact of maternal high-fat diet (mHFD)-induced changes in microbial signals on offspring brain development, and neuroimmune signals, and the enduring effects on behaviour into adolescence. We first demonstrate that maternal caecal microbiota composition at term pregnancy (embryonic day 18: E18) differs significantly in response to maternal diet. Moreover, mHFD resulted in the upregulation of microbial genes in the maternal intestinal tissue linked to alterations in quinolinic acid synthesis and elevated kynurenine levels in the maternal plasma, both neuronal plasticity mediators related to glutamate metabolism. Metabolomics of mHFD embryonic brains at E18 also detected molecules linked to glutamate-glutamine cycle, including glutamic acid, glutathione disulphide, and kynurenine. During adolescence, the mHFD offspring exhibited increased locomotor activity and anxiety-like behaviour in a sex-dependent manner, along with upregulation of glutamate-related genes compared to controls. Overall, our results demonstrate that maternal exposure to high-fat diet results in microbiota changes, behavioural imprinting, altered brain metabolism, and glutamate signalling during critical developmental windows during the perinatal period.
Fil: Ratsika, Anna. University College Cork; Irlanda
Fil: Codagnone, Martín Gabriel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Biología Celular y Neurociencia "Prof. Eduardo de Robertis". Universidad de Buenos Aires. Facultad de Medicina. Instituto de Biología Celular y Neurociencia; Argentina
Fil: Bastiaanssen, Thomaz F.S.. University College Cork; Irlanda
Fil: Hoffmann Sarda, Fabiana A.. University College Cork; Irlanda
Fil: Lynch, Caoimhe M.K.. University College Cork; Irlanda
Fil: Ventura Silva, Ana Paula. University College Cork; Irlanda
Fil: Rosell Cardona, Cristina. University College Cork; Irlanda
Fil: Caputi, Valentina. University College Cork; Irlanda
Fil: Stanton, Catherine. University College Cork; Irlanda
Fil: Fülling, Christine. University College Cork; Irlanda
Fil: Clarke, Gerard. University College Cork; Irlanda
Fil: Cryan, John F.. University College Cork; Irlanda
Materia
MICROBIOTA-GUT-BRAIN-AXIS
NEURODEVELOPMENT
GLUTAMATE
MATERNAL-OBESITY
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/267671
Acceder
id CONICETDig_1fcea67fc3e712c92635fc2d30b2ce56
oai_identifier_str oai:ri.conicet.gov.ar:11336/267671
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Maternal high-fat diet-induced microbiota changes are associated with alterations in embryonic brain metabolites and adolescent behaviourRatsika, AnnaCodagnone, Martín GabrielBastiaanssen, Thomaz F.S.Hoffmann Sarda, Fabiana A.Lynch, Caoimhe M.K.Ventura Silva, Ana PaulaRosell Cardona, CristinaCaputi, ValentinaStanton, CatherineFülling, ChristineClarke, GerardCryan, John F.MICROBIOTA-GUT-BRAIN-AXISNEURODEVELOPMENTGLUTAMATEMATERNAL-OBESITYhttps://purl.org/becyt/ford/3.1https://purl.org/becyt/ford/3The developing central nervous system is highly sensitive to nutrient changes during the perinatal period, emphasising the potential impact of alterations of maternal diet on offspring brain development and behaviour. A growing body of research implicates the gut microbiota in neurodevelopment and behaviour. Maternal overweight and obesity during the perinatal period has been linked to changes in neurodevelopment, plasticity and affective disorders in the offspring, with implications for microbial signals from the maternal gut. Here we investigate the impact of maternal high-fat diet (mHFD)-induced changes in microbial signals on offspring brain development, and neuroimmune signals, and the enduring effects on behaviour into adolescence. We first demonstrate that maternal caecal microbiota composition at term pregnancy (embryonic day 18: E18) differs significantly in response to maternal diet. Moreover, mHFD resulted in the upregulation of microbial genes in the maternal intestinal tissue linked to alterations in quinolinic acid synthesis and elevated kynurenine levels in the maternal plasma, both neuronal plasticity mediators related to glutamate metabolism. Metabolomics of mHFD embryonic brains at E18 also detected molecules linked to glutamate-glutamine cycle, including glutamic acid, glutathione disulphide, and kynurenine. During adolescence, the mHFD offspring exhibited increased locomotor activity and anxiety-like behaviour in a sex-dependent manner, along with upregulation of glutamate-related genes compared to controls. Overall, our results demonstrate that maternal exposure to high-fat diet results in microbiota changes, behavioural imprinting, altered brain metabolism, and glutamate signalling during critical developmental windows during the perinatal period.Fil: Ratsika, Anna. University College Cork; IrlandaFil: Codagnone, Martín Gabriel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Biología Celular y Neurociencia "Prof. Eduardo de Robertis". Universidad de Buenos Aires. Facultad de Medicina. Instituto de Biología Celular y Neurociencia; ArgentinaFil: Bastiaanssen, Thomaz F.S.. University College Cork; IrlandaFil: Hoffmann Sarda, Fabiana A.. University College Cork; IrlandaFil: Lynch, Caoimhe M.K.. University College Cork; IrlandaFil: Ventura Silva, Ana Paula. University College Cork; IrlandaFil: Rosell Cardona, Cristina. University College Cork; IrlandaFil: Caputi, Valentina. University College Cork; IrlandaFil: Stanton, Catherine. University College Cork; IrlandaFil: Fülling, Christine. University College Cork; IrlandaFil: Clarke, Gerard. University College Cork; IrlandaFil: Cryan, John F.. University College Cork; IrlandaAcademic Press Inc Elsevier Science2024-10info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/267671Ratsika, Anna; Codagnone, Martín Gabriel; Bastiaanssen, Thomaz F.S.; Hoffmann Sarda, Fabiana A.; Lynch, Caoimhe M.K.; et al.; Maternal high-fat diet-induced microbiota changes are associated with alterations in embryonic brain metabolites and adolescent behaviour; Academic Press Inc Elsevier Science; Brain Behavior And Immunity; 121; 10-2024; 317-3300889-1591CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://linkinghub.elsevier.com/retrieve/pii/S0889159124004896info:eu-repo/semantics/altIdentifier/doi/10.1016/j.bbi.2024.07.020info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:59:21Zoai:ri.conicet.gov.ar:11336/267671instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-03 09:59:21.721CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Maternal high-fat diet-induced microbiota changes are associated with alterations in embryonic brain metabolites and adolescent behaviour
title Maternal high-fat diet-induced microbiota changes are associated with alterations in embryonic brain metabolites and adolescent behaviour
spellingShingle Maternal high-fat diet-induced microbiota changes are associated with alterations in embryonic brain metabolites and adolescent behaviour
Ratsika, Anna
MICROBIOTA-GUT-BRAIN-AXIS
NEURODEVELOPMENT
GLUTAMATE
MATERNAL-OBESITY
title_short Maternal high-fat diet-induced microbiota changes are associated with alterations in embryonic brain metabolites and adolescent behaviour
title_full Maternal high-fat diet-induced microbiota changes are associated with alterations in embryonic brain metabolites and adolescent behaviour
title_fullStr Maternal high-fat diet-induced microbiota changes are associated with alterations in embryonic brain metabolites and adolescent behaviour
title_full_unstemmed Maternal high-fat diet-induced microbiota changes are associated with alterations in embryonic brain metabolites and adolescent behaviour
title_sort Maternal high-fat diet-induced microbiota changes are associated with alterations in embryonic brain metabolites and adolescent behaviour
dc.creator.none.fl_str_mv Ratsika, Anna
Codagnone, Martín Gabriel
Bastiaanssen, Thomaz F.S.
Hoffmann Sarda, Fabiana A.
Lynch, Caoimhe M.K.
Ventura Silva, Ana Paula
Rosell Cardona, Cristina
Caputi, Valentina
Stanton, Catherine
Fülling, Christine
Clarke, Gerard
Cryan, John F.
author Ratsika, Anna
author_facet Ratsika, Anna
Codagnone, Martín Gabriel
Bastiaanssen, Thomaz F.S.
Hoffmann Sarda, Fabiana A.
Lynch, Caoimhe M.K.
Ventura Silva, Ana Paula
Rosell Cardona, Cristina
Caputi, Valentina
Stanton, Catherine
Fülling, Christine
Clarke, Gerard
Cryan, John F.
author_role author
author2 Codagnone, Martín Gabriel
Bastiaanssen, Thomaz F.S.
Hoffmann Sarda, Fabiana A.
Lynch, Caoimhe M.K.
Ventura Silva, Ana Paula
Rosell Cardona, Cristina
Caputi, Valentina
Stanton, Catherine
Fülling, Christine
Clarke, Gerard
Cryan, John F.
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv MICROBIOTA-GUT-BRAIN-AXIS
NEURODEVELOPMENT
GLUTAMATE
MATERNAL-OBESITY
topic MICROBIOTA-GUT-BRAIN-AXIS
NEURODEVELOPMENT
GLUTAMATE
MATERNAL-OBESITY
purl_subject.fl_str_mv https://purl.org/becyt/ford/3.1
https://purl.org/becyt/ford/3
dc.description.none.fl_txt_mv The developing central nervous system is highly sensitive to nutrient changes during the perinatal period, emphasising the potential impact of alterations of maternal diet on offspring brain development and behaviour. A growing body of research implicates the gut microbiota in neurodevelopment and behaviour. Maternal overweight and obesity during the perinatal period has been linked to changes in neurodevelopment, plasticity and affective disorders in the offspring, with implications for microbial signals from the maternal gut. Here we investigate the impact of maternal high-fat diet (mHFD)-induced changes in microbial signals on offspring brain development, and neuroimmune signals, and the enduring effects on behaviour into adolescence. We first demonstrate that maternal caecal microbiota composition at term pregnancy (embryonic day 18: E18) differs significantly in response to maternal diet. Moreover, mHFD resulted in the upregulation of microbial genes in the maternal intestinal tissue linked to alterations in quinolinic acid synthesis and elevated kynurenine levels in the maternal plasma, both neuronal plasticity mediators related to glutamate metabolism. Metabolomics of mHFD embryonic brains at E18 also detected molecules linked to glutamate-glutamine cycle, including glutamic acid, glutathione disulphide, and kynurenine. During adolescence, the mHFD offspring exhibited increased locomotor activity and anxiety-like behaviour in a sex-dependent manner, along with upregulation of glutamate-related genes compared to controls. Overall, our results demonstrate that maternal exposure to high-fat diet results in microbiota changes, behavioural imprinting, altered brain metabolism, and glutamate signalling during critical developmental windows during the perinatal period.
Fil: Ratsika, Anna. University College Cork; Irlanda
Fil: Codagnone, Martín Gabriel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Biología Celular y Neurociencia "Prof. Eduardo de Robertis". Universidad de Buenos Aires. Facultad de Medicina. Instituto de Biología Celular y Neurociencia; Argentina
Fil: Bastiaanssen, Thomaz F.S.. University College Cork; Irlanda
Fil: Hoffmann Sarda, Fabiana A.. University College Cork; Irlanda
Fil: Lynch, Caoimhe M.K.. University College Cork; Irlanda
Fil: Ventura Silva, Ana Paula. University College Cork; Irlanda
Fil: Rosell Cardona, Cristina. University College Cork; Irlanda
Fil: Caputi, Valentina. University College Cork; Irlanda
Fil: Stanton, Catherine. University College Cork; Irlanda
Fil: Fülling, Christine. University College Cork; Irlanda
Fil: Clarke, Gerard. University College Cork; Irlanda
Fil: Cryan, John F.. University College Cork; Irlanda
description The developing central nervous system is highly sensitive to nutrient changes during the perinatal period, emphasising the potential impact of alterations of maternal diet on offspring brain development and behaviour. A growing body of research implicates the gut microbiota in neurodevelopment and behaviour. Maternal overweight and obesity during the perinatal period has been linked to changes in neurodevelopment, plasticity and affective disorders in the offspring, with implications for microbial signals from the maternal gut. Here we investigate the impact of maternal high-fat diet (mHFD)-induced changes in microbial signals on offspring brain development, and neuroimmune signals, and the enduring effects on behaviour into adolescence. We first demonstrate that maternal caecal microbiota composition at term pregnancy (embryonic day 18: E18) differs significantly in response to maternal diet. Moreover, mHFD resulted in the upregulation of microbial genes in the maternal intestinal tissue linked to alterations in quinolinic acid synthesis and elevated kynurenine levels in the maternal plasma, both neuronal plasticity mediators related to glutamate metabolism. Metabolomics of mHFD embryonic brains at E18 also detected molecules linked to glutamate-glutamine cycle, including glutamic acid, glutathione disulphide, and kynurenine. During adolescence, the mHFD offspring exhibited increased locomotor activity and anxiety-like behaviour in a sex-dependent manner, along with upregulation of glutamate-related genes compared to controls. Overall, our results demonstrate that maternal exposure to high-fat diet results in microbiota changes, behavioural imprinting, altered brain metabolism, and glutamate signalling during critical developmental windows during the perinatal period.
publishDate 2024
dc.date.none.fl_str_mv 2024-10
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/267671
Ratsika, Anna; Codagnone, Martín Gabriel; Bastiaanssen, Thomaz F.S.; Hoffmann Sarda, Fabiana A.; Lynch, Caoimhe M.K.; et al.; Maternal high-fat diet-induced microbiota changes are associated with alterations in embryonic brain metabolites and adolescent behaviour; Academic Press Inc Elsevier Science; Brain Behavior And Immunity; 121; 10-2024; 317-330
0889-1591
CONICET Digital
CONICET
url http://hdl.handle.net/11336/267671
identifier_str_mv Ratsika, Anna; Codagnone, Martín Gabriel; Bastiaanssen, Thomaz F.S.; Hoffmann Sarda, Fabiana A.; Lynch, Caoimhe M.K.; et al.; Maternal high-fat diet-induced microbiota changes are associated with alterations in embryonic brain metabolites and adolescent behaviour; Academic Press Inc Elsevier Science; Brain Behavior And Immunity; 121; 10-2024; 317-330
0889-1591
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://linkinghub.elsevier.com/retrieve/pii/S0889159124004896
info:eu-repo/semantics/altIdentifier/doi/10.1016/j.bbi.2024.07.020
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Academic Press Inc Elsevier Science
publisher.none.fl_str_mv Academic Press Inc Elsevier Science
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
_version_ 1842269577639100416
score 13.13397

Publicaciones similares