Maternal dietary omega-3 deficiency worsens the deleterious effects of prenatal inflammation on the gut-brain axis in the offspring across lifetime

Q Leyrolle; F Decoeur; G Briere; C Amadieu; A R A A Quadros; I Voytyuk; C Lacabanne; A Benmamar-Badel; J Bourel; A Aubert; A Sere; F Chain; L Schwendimann; B Matrot; T Bourgeois; S Grégoire; J G Leblanc; A De Moreno De Leblanc; P Langella; G R Fernandes; L Bretillon; C Joffre; R Uricaru; P Thebault; P Gressens; J M Chatel; S Layé; A Nadjar

doi:10.1038/s41386-020-00793-7

Maternal dietary omega-3 deficiency worsens the deleterious effects of prenatal inflammation on the gut-brain axis in the offspring across lifetime

Q Leyrolle, F Decoeur, G Briere, C Amadieu, A R A A Quadros, I Voytyuk, C Lacabanne, A Benmamar-Badel, J Bourel, A Aubert, A Sere, F Chain, L Schwendimann, B Matrot, T Bourgeois, S Grégoire, J G Leblanc, A De Moreno De Leblanc, P Langella, G R FernandesL Bretillon, C Joffre, R Uricaru, P Thebault, P Gressens, J M Chatel, S Layé, A Nadjar

Research output: Contribution to journal › Article › peer-review

15 Citations (Scopus)

Abstract

Maternal immune activation (MIA) and poor maternal nutritional habits are risk factors for the occurrence of neurodevelopmental disorders (NDD). Human studies show the deleterious impact of prenatal inflammation and low n-3 polyunsaturated fatty acid (PUFA) intake on neurodevelopment with long-lasting consequences on behavior. However, the mechanisms linking maternal nutritional status to MIA are still unclear, despite their relevance to the etiology of NDD. We demonstrate here that low maternal n-3 PUFA intake worsens MIA-induced early gut dysfunction, including modification of gut microbiota composition and higher local inflammatory reactivity. These deficits correlate with alterations of microglia-neuron crosstalk pathways and have long-lasting effects, both at transcriptional and behavioral levels. This work highlights the perinatal period as a critical time window, especially regarding the role of the gut-brain axis in neurodevelopment, elucidating the link between MIA, poor nutritional habits, and NDD.[Figure not available: see fulltext.][Figure not available: see fulltext.][Figure not available: see fulltext.][Figure not available: see fulltext.][Figure not available: see fulltext.].

Original language	English
Journal	Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology
DOIs	https://doi.org/10.1038/s41386-020-00793-7
Publication status	E-pub ahead of print - 11 Aug 2020

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Leyrolle, Q., Decoeur, F., Briere, G., Amadieu, C., Quadros, A. R. A. A., Voytyuk, I., Lacabanne, C., Benmamar-Badel, A., Bourel, J., Aubert, A., Sere, A., Chain, F., Schwendimann, L., Matrot, B., Bourgeois, T., Grégoire, S., Leblanc, J. G., De Moreno De Leblanc, A., Langella, P., ... Nadjar, A. (2020). Maternal dietary omega-3 deficiency worsens the deleterious effects of prenatal inflammation on the gut-brain axis in the offspring across lifetime. Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology. Advance online publication. https://doi.org/10.1038/s41386-020-00793-7

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title = "Maternal dietary omega-3 deficiency worsens the deleterious effects of prenatal inflammation on the gut-brain axis in the offspring across lifetime",

abstract = "Maternal immune activation (MIA) and poor maternal nutritional habits are risk factors for the occurrence of neurodevelopmental disorders (NDD). Human studies show the deleterious impact of prenatal inflammation and low n-3 polyunsaturated fatty acid (PUFA) intake on neurodevelopment with long-lasting consequences on behavior. However, the mechanisms linking maternal nutritional status to MIA are still unclear, despite their relevance to the etiology of NDD. We demonstrate here that low maternal n-3 PUFA intake worsens MIA-induced early gut dysfunction, including modification of gut microbiota composition and higher local inflammatory reactivity. These deficits correlate with alterations of microglia-neuron crosstalk pathways and have long-lasting effects, both at transcriptional and behavioral levels. This work highlights the perinatal period as a critical time window, especially regarding the role of the gut-brain axis in neurodevelopment, elucidating the link between MIA, poor nutritional habits, and NDD.[Figure not available: see fulltext.][Figure not available: see fulltext.][Figure not available: see fulltext.][Figure not available: see fulltext.][Figure not available: see fulltext.].",

author = "Q Leyrolle and F Decoeur and G Briere and C Amadieu and Quadros, {A R A A} and I Voytyuk and C Lacabanne and A Benmamar-Badel and J Bourel and A Aubert and A Sere and F Chain and L Schwendimann and B Matrot and T Bourgeois and S Gr{\'e}goire and Leblanc, {J G} and {De Moreno De Leblanc}, A and P Langella and Fernandes, {G R} and L Bretillon and C Joffre and R Uricaru and P Thebault and P Gressens and Chatel, {J M} and S Lay{\'e} and A Nadjar",

year = "2020",

month = aug,

day = "11",

doi = "10.1038/s41386-020-00793-7",

language = "English",

journal = "Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology",

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Leyrolle, Q, Decoeur, F, Briere, G, Amadieu, C, Quadros, ARAA, Voytyuk, I, Lacabanne, C, Benmamar-Badel, A, Bourel, J, Aubert, A, Sere, A, Chain, F, Schwendimann, L, Matrot, B, Bourgeois, T, Grégoire, S, Leblanc, JG, De Moreno De Leblanc, A, Langella, P, Fernandes, GR, Bretillon, L, Joffre, C, Uricaru, R, Thebault, P, Gressens, P, Chatel, JM, Layé, S & Nadjar, A 2020, 'Maternal dietary omega-3 deficiency worsens the deleterious effects of prenatal inflammation on the gut-brain axis in the offspring across lifetime', Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology. https://doi.org/10.1038/s41386-020-00793-7

Maternal dietary omega-3 deficiency worsens the deleterious effects of prenatal inflammation on the gut-brain axis in the offspring across lifetime. / Leyrolle, Q; Decoeur, F; Briere, G et al.
In: Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology, 11.08.2020.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - Maternal dietary omega-3 deficiency worsens the deleterious effects of prenatal inflammation on the gut-brain axis in the offspring across lifetime

AU - Leyrolle, Q

AU - Decoeur, F

AU - Briere, G

AU - Amadieu, C

AU - Quadros, A R A A

AU - Voytyuk, I

AU - Lacabanne, C

AU - Benmamar-Badel, A

AU - Bourel, J

AU - Aubert, A

AU - Sere, A

AU - Chain, F

AU - Schwendimann, L

AU - Matrot, B

AU - Bourgeois, T

AU - Grégoire, S

AU - Leblanc, J G

AU - De Moreno De Leblanc, A

AU - Langella, P

AU - Fernandes, G R

AU - Bretillon, L

AU - Joffre, C

AU - Uricaru, R

AU - Thebault, P

AU - Gressens, P

AU - Chatel, J M

AU - Layé, S

AU - Nadjar, A

PY - 2020/8/11

Y1 - 2020/8/11

N2 - Maternal immune activation (MIA) and poor maternal nutritional habits are risk factors for the occurrence of neurodevelopmental disorders (NDD). Human studies show the deleterious impact of prenatal inflammation and low n-3 polyunsaturated fatty acid (PUFA) intake on neurodevelopment with long-lasting consequences on behavior. However, the mechanisms linking maternal nutritional status to MIA are still unclear, despite their relevance to the etiology of NDD. We demonstrate here that low maternal n-3 PUFA intake worsens MIA-induced early gut dysfunction, including modification of gut microbiota composition and higher local inflammatory reactivity. These deficits correlate with alterations of microglia-neuron crosstalk pathways and have long-lasting effects, both at transcriptional and behavioral levels. This work highlights the perinatal period as a critical time window, especially regarding the role of the gut-brain axis in neurodevelopment, elucidating the link between MIA, poor nutritional habits, and NDD.[Figure not available: see fulltext.][Figure not available: see fulltext.][Figure not available: see fulltext.][Figure not available: see fulltext.][Figure not available: see fulltext.].

AB - Maternal immune activation (MIA) and poor maternal nutritional habits are risk factors for the occurrence of neurodevelopmental disorders (NDD). Human studies show the deleterious impact of prenatal inflammation and low n-3 polyunsaturated fatty acid (PUFA) intake on neurodevelopment with long-lasting consequences on behavior. However, the mechanisms linking maternal nutritional status to MIA are still unclear, despite their relevance to the etiology of NDD. We demonstrate here that low maternal n-3 PUFA intake worsens MIA-induced early gut dysfunction, including modification of gut microbiota composition and higher local inflammatory reactivity. These deficits correlate with alterations of microglia-neuron crosstalk pathways and have long-lasting effects, both at transcriptional and behavioral levels. This work highlights the perinatal period as a critical time window, especially regarding the role of the gut-brain axis in neurodevelopment, elucidating the link between MIA, poor nutritional habits, and NDD.[Figure not available: see fulltext.][Figure not available: see fulltext.][Figure not available: see fulltext.][Figure not available: see fulltext.][Figure not available: see fulltext.].

UR - http://www.scopus.com/inward/record.url?scp=85089290670&partnerID=8YFLogxK

U2 - 10.1038/s41386-020-00793-7

DO - 10.1038/s41386-020-00793-7

M3 - Article

C2 - 32781459

SN - 0893-133X

JO - Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology

JF - Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology

ER -

Leyrolle Q, Decoeur F, Briere G, Amadieu C, Quadros ARAA, Voytyuk I et al. Maternal dietary omega-3 deficiency worsens the deleterious effects of prenatal inflammation on the gut-brain axis in the offspring across lifetime. Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology. 2020 Aug 11. Epub 2020 Aug 11. doi: 10.1038/s41386-020-00793-7

Maternal dietary omega-3 deficiency worsens the deleterious effects of prenatal inflammation on the gut-brain axis in the offspring across lifetime

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