Essential omega-3 fatty acids tune microglial phagocytosis of synaptic elements in the mouse developing brain

C. Madore, Q. Leyrolle, L. Morel, M. Rossitto, A. D. Greenhalgh, J. C. Delpech, M. Martinat, C. Bosch-Bouju, J. Bourel, B. Rani, C. Lacabanne, A. Thomazeau, K. E. Hopperton, S. Beccari, A. Sere, A. Aubert, V. Smedt-Peyrusse, C. Lecours, K. Bisht, L. Fourgeaud, S. Gregoire, L. Bretillon, N. Acar, N. J. Grant, J. Badaut, P. Gressens, A. Sierra, O. Butovsky, M. E. Tremblay, R. P. Bazinet, C. Joffre, A. Nadjar () and S. Layé ()
Additional contact information
C. Madore: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286
Q. Leyrolle: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286
L. Morel: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286
M. Rossitto: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286
A. D. Greenhalgh: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286
J. C. Delpech: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286
M. Martinat: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286
C. Bosch-Bouju: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286
J. Bourel: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286
B. Rani: University of Florence
C. Lacabanne: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286
A. Thomazeau: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286
K. E. Hopperton: University of Toronto
S. Beccari: University of the Basque Country and Ikerbasque Foundation
A. Sere: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286
A. Aubert: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286
V. Smedt-Peyrusse: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286
C. Lecours: Neurosciences Axis, CRCHU de Québec-Université Laval
K. Bisht: Neurosciences Axis, CRCHU de Québec-Université Laval
L. Fourgeaud: The Salk Institute for Biological Studies
S. Gregoire: Univ. Bourgogne Franche-Comté
L. Bretillon: Univ. Bourgogne Franche-Comté
N. Acar: Univ. Bourgogne Franche-Comté
N. J. Grant: CNRS UPR3212, Institut des Neurosciences Cellulaires et Intégratives
J. Badaut: CNRS UMR5287, University of Bordeaux
P. Gressens: Université de Paris Diderot
A. Sierra: University of the Basque Country and Ikerbasque Foundation
O. Butovsky: Harvard Medical School
M. E. Tremblay: Neurosciences Axis, CRCHU de Québec-Université Laval
R. P. Bazinet: University of Toronto
C. Joffre: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286
A. Nadjar: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286
S. Layé: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeuro, UMR 1286

Nature Communications, 2020, vol. 11, issue 1, 1-19

Abstract: Abstract Omega-3 fatty acids (n-3 PUFAs) are essential for the functional maturation of the brain. Westernization of dietary habits in both developed and developing countries is accompanied by a progressive reduction in dietary intake of n-3 PUFAs. Low maternal intake of n-3 PUFAs has been linked to neurodevelopmental diseases in Humans. However, the n-3 PUFAs deficiency-mediated mechanisms affecting the development of the central nervous system are poorly understood. Active microglial engulfment of synapses regulates brain development. Impaired synaptic pruning is associated with several neurodevelopmental disorders. Here, we identify a molecular mechanism for detrimental effects of low maternal n-3 PUFA intake on hippocampal development in mice. Our results show that maternal dietary n-3 PUFA deficiency increases microglia-mediated phagocytosis of synaptic elements in the rodent developing hippocampus, partly through the activation of 12/15-lipoxygenase (LOX)/12-HETE signaling, altering neuronal morphology and affecting cognitive performance of the offspring. These findings provide a mechanistic insight into neurodevelopmental defects caused by maternal n-3 PUFAs dietary deficiency.

Date: 2020
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DOI: 10.1038/s41467-020-19861-z

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