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Vitamin A deficiency during the perinatal period induces changes in vitamin A metabolism in the offspring. The regulation of intestinal vitamin A metabolism via ISX occurs only in male rats severely vitamin A-deficient

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Abstract

Purpose

1) To test the hypothesis of the existence of a perinatal vitamin A (VA) programming of VA metabolism and to better understand the intestinal regulation of VA metabolism.

Methods

Offspring from rats reared on a control (C) or a VA-deficient (D) diet from 6 weeks before mating until offspring weaning, i.e., 7 weeks after mating, were themselves reared on a C or D diet for 19 weeks, resulting in the following groups: C–C (parents fed C—offspring fed C), D-C, C-D and D-D. VA concentrations were measured in plasma and liver. β-Carotene bioavailability and its intestinal conversion rate to VA, as well as vitamin D and E bioavailability, were assessed after gavages with these vitamins. Expression of genes involved in VA metabolism and transport was measured in intestine and liver.

Results

C–D and D–D had no detectable retinyl esters in their liver. Retinolemia, hepatic retinol concentrations and postprandial plasma retinol response to β-carotene gavage were higher in D–C than in C–C. Intestinal expression of Isx was abolished in C–D and D–D and this was concomitant with a higher expression of Bco1, Scarb1, Cd36 and Lrat in males receiving a D diet as compared to those receiving a C diet. β-Carotene, vitamin D and E bio-availabilities were lower in offspring receiving a D diet as compared to those receiving a C diet.

Conclusion

A VA-deficient diet during the perinatal period modifies the metabolism of this vitamin in the offspring. Isx-mediated regulation of Bco1 and Scarb1 expression exists only in males severely deficient in this vitamin. Severe VA deficiency impairs β-carotene and vitamin D and E bioavailability.

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Acknowledgements

The authors thank Benjamin Guillet for giving us access to the animal facility.

This project received funding from both the AlimH department of INRA (ANSSD 2016) and the G.L.N. (Groupe Lipides et Nutrition) in 2017.

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Author notes

  1. Romane Troadec—Co-first author.

Authors and Affiliations

  1. Center for CardioVascular and Nutrition Research (C2VN), Faculté de Médecine, INRAE, INSERM, Aix Marseille Univ, 27, boulevard Jean Moulin, 13005, Marseille, France

    Patrick Borel, Romane Troadec, Morgane Damiani, Charlotte Halimi, Marion Nowicki, Philippe Guichard, Charlene Couturier, Marielle Margier, Lourdes Mounien, Michel Grino, Emmanuelle Reboul, Jean-François Landrier & Charles Desmarchelier

  2. Institut Universitaire de France (IUF), Marseille, France

    Charles Desmarchelier

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Contributions

Patrick Borel: Conceptualization, Methodology, first interpretation of the results, Resources, Writing—Original Draft, Supervision, Project administration, Funding acquisition. Romane Troadec: HPLC analysis, gene expression, figures. Morgane Damiani: HPLC and gene expression analysis. Charlotte Halimi: HPLC analysis and preparation of β-carotene and vitamins D and E rich emulsions, tissue sampling. Marion Nowicki: gene expression, tissue sampling. Charlene Couturier: tissue sampling. Philippe Guichard: nutritional intervention on rats, rat gavages, blood sampling. Marielle Margier: tissue sampling. Lourdes Mounien: tissue sampling. Michel Grino: conceptualization, methodology, nutritional intervention on rats, rat gavages, blood sampling. Emmanuelle Reboul: conceptualization, tissue sampling, review and editing. Jean-François Landrier: conceptualization, gene expression validation, review and editing. Charles Desmarchelier: Statistics, interpretation of the results, Writing—Original Draft.

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Correspondence to Patrick Borel.

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Borel, P., Troadec, R., Damiani, M. et al. Vitamin A deficiency during the perinatal period induces changes in vitamin A metabolism in the offspring. The regulation of intestinal vitamin A metabolism via ISX occurs only in male rats severely vitamin A-deficient. Eur J Nutr 62, 633–646 (2023). https://doi.org/10.1007/s00394-022-03019-2

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