Cited by 374IL-33, ST2, and ILC PathwaysT-cell and B-cell ImmunologyBirth, Development, and Health

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Maternal retinoids control type 3 innate lymphoid cells and set the offspring immunity

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van de Pavert, Serge A., Ferreira, Manuela, Domingues, Rita G., Ribeiro, Hélder, Molenaar, Rosalie, Moreira-Santos, Lara, Almeida, Francisca F., Ibiza, Sales, Barbosa, Inês, Goverse, Gera, Labão-Almeida, Carlos, Godinho-Silva, Cristina, Konijn, Tanja, Schooneman, Dennis, O’Toole, Tom, Mizee, Mark R., Habani, Yasmin, Haak, Esther, Santori, Fabio R., Littman, Dan R., Schulte-Merker, Stefan, Dzierzak, Elaine, Simas, J. Pedro, Mebius, Reina E., Veiga-Fernandes, Henrique·2014·Nature

DOI 10.1038/nature13158PMC PMC4932833

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Abstract

The impact of nutritional status during fetal life on the overall health of adults has been recognized; however, dietary effects on the developing immune system are largely unknown. Development of secondary lymphoid organs occurs during embryogenesis and is considered to be developmentally programmed. Secondary lymphoid organ formation depends on a subset of type 3 innate lymphoid cells (ILC3) named lymphoid tissue inducer (LTi) cells. Here we show that mouse fetal ILC3s are controlled by cell-autonomous retinoic acid (RA) signalling in utero, which pre-sets the immune fitness in adulthood. We found that embryonic lymphoid organs contain ILC progenitors that differentiate locally into mature LTi cells. Local LTi cell differentiation was controlled by maternal retinoid intake and fetal RA signalling acting in a haematopoietic cell-autonomous manner. RA controlled LTi cell maturation upstream of the transcription factor RORγt. Accordingly, enforced expression of Rorgt restored maturation of LTi cells with impaired RA signalling, whereas RA receptors directly regulated the Rorgt locus. Finally, we established that maternal levels of dietary retinoids control the size of secondary lymphoid organs and the efficiency of immune responses in the adult offspring. Our results reveal a molecular link between maternal nutrients and the formation of immune structures required for resistance to infection in the offspring.

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Authors: van de Pavert, S. A., Ferreira, M., Domingues, R. G., Ribeiro, H., Molenaar, R., Moreira-Santos, L., Almeida, F. F., Ibiza, S., Barbosa, I., Goverse, G., Labão-Almeida, C., Godinho-Silva, C., Konijn, T., Schooneman, D., O’Toole, T., Mizee, M. R., Habani, Y., Haak, E., Santori, F. R., Littman, D. R., Schulte-Merker, S., Dzierzak, E., Simas, J. P., Mebius, R. E., & Veiga-Fernandes, H.
Affiliations: Instituto de Medicina Molecular João Lobo Antunes (PT)
University of Lisbon (PT)
Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
Erasmus MC (NL)
Howard Hughes Medical Institute (US)
ORCID: Ferreira, Manuela
Domingues, Rita G.
Ribeiro, Hélder
Almeida, Francisca F.
Ibiza, Sales
Barbosa, Inês
Mizee, Mark R.
Haak, Esther
Santori, Fabio R.
Littman, Dan R.
Dzierzak, Elaine
Simas, J. Pedro
Mebius, Reina E.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2014-03-19
Volume: 508
Issue: 7494
Pages: 123-127
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature13158
PMC: PMC4932833
OpenAlex: W2076363780
Cited by: 374
References: 42
Citations by year: 2026: 11 · 2025: 20 · 2024: 15 · 2023: 25 · 2022: 26 · 2021: 21 · 2020: 33 · 2019: 34 · 2018: 48 · 2017: 24 · 2016: 39 · 2015: 47 · 2014: 30
FWCI: 21.33
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
PubMed Central (acceptedVersion)
EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Minerva Access (University of Melbourne) (submittedVersion)
Pure Amsterdam UMC (submittedVersion)
KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (submittedVersion)
Funders: Howard Hughes Medical Institute
Crohn's and Colitis Foundation (313089)
National Institute of Allergy and Infectious Diseases (R01AI080885)
Topics: Life Sciences › Immunology and Microbiology › Immunology › IL-33, ST2, and ILC Pathways
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Keywords: retinoic acid, ILC3, lymphoid tissue inducer cells, fetal immune development, RORγt, retinoic acid receptor, maternal nutrition
MeSH terms: Animals, Cell Differentiation, Diet, Female, Fetus, Immunity, Innate, Lymphoid Tissue, Mice, Inbred C57BL, Pregnancy, Prenatal Exposure Delayed Effects, Stem Cells, Tretinoin, Signal Transduction, Receptors, Retinoic Acid, Mice

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Maternal retinoids control type 3 innate lymphoid cells and set the offspring immunity

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