Maternal heme-enriched diet promotes a gut pro-oxidative status associated with microbiota alteration, gut leakiness and glucose intolerance in mice offspring.


Journal

Redox biology
ISSN: 2213-2317
Titre abrégé: Redox Biol
Pays: Netherlands
ID NLM: 101605639

Informations de publication

Date de publication:
07 2022
Historique:
received: 22 04 2022
revised: 06 05 2022
accepted: 06 05 2022
pubmed: 20 5 2022
medline: 9 6 2022
entrez: 19 5 2022
Statut: ppublish

Résumé

Maternal environment, including nutrition and microbiota, plays a critical role in determining offspring's risk of chronic diseases such as diabetes later in life. Heme iron requirement is amplified during pregnancy and lactation, while excessive dietary heme iron intake, compared to non-heme iron, has shown to trigger acute oxidative stress in the gut resulting from reactive aldehyde formation in conjunction with microbiota reshape. Given the immaturity of the antioxidant defense system in early life, we investigated the extent to which a maternal diet enriched with heme iron may have a lasting impact on gut homeostasis and glucose metabolism in 60-day-old C3H/HeN mice offspring. As hypothesized, the form of iron added to the maternal diet differentially governed the offspring's microbiota establishment despite identical fecal iron status in the offspring. Importantly, despite female offspring was unaffected, oxidative stress markers were however higher in the gut of male offspring from heme enriched-fed mothers, and were accompanied by increases in fecal lipocalin-2, intestinal para-cellular permeability and TNF-α expression. In addition, male mice displayed blood glucose intolerance resulting from impaired insulin secretion following oral glucose challenge. Using an integrated approach including an aldehydomic analysis, this male-specific phenotype was further characterized and revealed close covariations between unidentified putative reactive aldehydes and bacterial communities belonging to Bacteroidales and Lachnospirales orders. Our work highlights how the form of dietary iron in the maternal diet can dictate the oxidative status in gut offspring in a sex-dependent manner, and how a gut microbiota-driven oxidative challenge in early life can be associated with gut barrier defects and glucose metabolism disorders that may be predictive of diabetes development.

Identifiants

pubmed: 35588638
pii: S2213-2317(22)00105-7
doi: 10.1016/j.redox.2022.102333
pmc: PMC9119830
pii:
doi:

Substances chimiques

Heme 42VZT0U6YR
Iron E1UOL152H7

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

102333

Informations de copyright

Copyright © 2022 The Authors. Published by Elsevier B.V. All rights reserved.

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Auteurs

Anaïs Mazenc (A)

Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, France.

Loïc Mervant (L)

Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, France; Metatoul-AXIOM Plaform, National Infrastructure for Metabolomics and Fluxomics, MetaboHUB, Toulouse, France.

Claire Maslo (C)

Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, France.

Corinne Lencina (C)

Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, France.

Valérie Bézirard (V)

Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, France.

Mathilde Levêque (M)

Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, France.

Ingrid Ahn (I)

Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, France.

Valérie Alquier-Bacquié (V)

Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, France.

Nathalie Naud (N)

Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, France.

Cécile Héliès-Toussaint (C)

Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, France.

Laurent Debrauwer (L)

Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, France; Metatoul-AXIOM Plaform, National Infrastructure for Metabolomics and Fluxomics, MetaboHUB, Toulouse, France.

Sylvie Chevolleau (S)

Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, France; Metatoul-AXIOM Plaform, National Infrastructure for Metabolomics and Fluxomics, MetaboHUB, Toulouse, France.

Françoise Guéraud (F)

Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, France.

Fabrice H F Pierre (FHF)

Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, France.

Vassilia Théodorou (V)

Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, France.

Maïwenn Olier (M)

Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, France. Electronic address: maiwenn.olier@inrae.fr.

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