Maternal heme-enriched diet promotes a gut pro-oxidative status associated with microbiota alteration, gut leakiness and glucose intolerance in mice offspring
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 i...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2022-07-01
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| Series: | Redox Biology |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213231722001057 |
| _version_ | 1811336484416913408 |
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| author | Anaïs Mazenc Loïc Mervant Claire Maslo Corinne Lencina Valérie Bézirard Mathilde Levêque Ingrid Ahn Valérie Alquier-Bacquié Nathalie Naud Cécile Héliès-Toussaint Laurent Debrauwer Sylvie Chevolleau Françoise Guéraud Fabrice H.F. Pierre Vassilia Théodorou Maïwenn Olier |
| author_facet | Anaïs Mazenc Loïc Mervant Claire Maslo Corinne Lencina Valérie Bézirard Mathilde Levêque Ingrid Ahn Valérie Alquier-Bacquié Nathalie Naud Cécile Héliès-Toussaint Laurent Debrauwer Sylvie Chevolleau Françoise Guéraud Fabrice H.F. Pierre Vassilia Théodorou Maïwenn Olier |
| author_sort | Anaïs Mazenc |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-13T17:41:05Z |
| format | Article |
| id | doaj.art-f6ff9ef0bac84898ba7a7f8342697768 |
| institution | Directory Open Access Journal |
| issn | 2213-2317 |
| language | English |
| last_indexed | 2024-04-13T17:41:05Z |
| publishDate | 2022-07-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Redox Biology |
| spelling | doaj.art-f6ff9ef0bac84898ba7a7f83426977682022-12-22T02:37:12ZengElsevierRedox Biology2213-23172022-07-0153102333Maternal heme-enriched diet promotes a gut pro-oxidative status associated with microbiota alteration, gut leakiness and glucose intolerance in mice offspringAnaïs Mazenc0Loïc Mervant1Claire Maslo2Corinne Lencina3Valérie Bézirard4Mathilde Levêque5Ingrid Ahn6Valérie Alquier-Bacquié7Nathalie Naud8Cécile Héliès-Toussaint9Laurent Debrauwer10Sylvie Chevolleau11Françoise Guéraud12Fabrice H.F. Pierre13Vassilia Théodorou14Maïwenn Olier15Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, FranceToxalim (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, FranceToxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, FranceToxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, FranceToxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, FranceToxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, FranceToxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, FranceToxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, FranceToxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, FranceToxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, FranceToxalim (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, FranceToxalim (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, FranceToxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, FranceToxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, FranceToxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, FranceToxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, Toulouse, France; Corresponding author. Toxalim, UMR 1331 INRAE, 180 chemin de Tournefeuille, BP93173, 31027, Toulouse cedex, France.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.http://www.sciencedirect.com/science/article/pii/S2213231722001057Heme ironEarly life nutritionLipoperoxidationRed meatGut barrierGut microbiota |
| spellingShingle | Anaïs Mazenc Loïc Mervant Claire Maslo Corinne Lencina Valérie Bézirard Mathilde Levêque Ingrid Ahn Valérie Alquier-Bacquié Nathalie Naud Cécile Héliès-Toussaint Laurent Debrauwer Sylvie Chevolleau Françoise Guéraud Fabrice H.F. Pierre Vassilia Théodorou Maïwenn Olier Maternal heme-enriched diet promotes a gut pro-oxidative status associated with microbiota alteration, gut leakiness and glucose intolerance in mice offspring Redox Biology Heme iron Early life nutrition Lipoperoxidation Red meat Gut barrier Gut microbiota |
| title | Maternal heme-enriched diet promotes a gut pro-oxidative status associated with microbiota alteration, gut leakiness and glucose intolerance in mice offspring |
| title_full | Maternal heme-enriched diet promotes a gut pro-oxidative status associated with microbiota alteration, gut leakiness and glucose intolerance in mice offspring |
| title_fullStr | Maternal heme-enriched diet promotes a gut pro-oxidative status associated with microbiota alteration, gut leakiness and glucose intolerance in mice offspring |
| title_full_unstemmed | Maternal heme-enriched diet promotes a gut pro-oxidative status associated with microbiota alteration, gut leakiness and glucose intolerance in mice offspring |
| title_short | Maternal heme-enriched diet promotes a gut pro-oxidative status associated with microbiota alteration, gut leakiness and glucose intolerance in mice offspring |
| title_sort | maternal heme enriched diet promotes a gut pro oxidative status associated with microbiota alteration gut leakiness and glucose intolerance in mice offspring |
| topic | Heme iron Early life nutrition Lipoperoxidation Red meat Gut barrier Gut microbiota |
| url | http://www.sciencedirect.com/science/article/pii/S2213231722001057 |
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