N‐3 PUFA deficiency disrupts oligodendrocyte maturation and myelin integrity during brain development
Quentin Leyrolle
(1)
,
Fanny Decoeur
(1)
,
Cyril Dejean
(2)
,
Marie-Galadriel Briere
(3)
,
Stephane Leon
(1)
,
Ioannis Bakogiannis
(1)
,
Emilie Baroux
(1)
,
Tony‐lee Sterley
(4)
,
Clémentine Bosch-Bouju
(1)
,
Lydie Morel
(1)
,
Camille Amadieu
(1)
,
Cynthia Lecours
(5, 6)
,
Marie‐kim St‐pierre
(5, 6)
,
Maude Bordeleau
(5, 6, 7)
,
Veronique de Smedt-Peyrusse
(1)
,
Alexandra Sere
(1)
,
Leslie Schwendimann
(8)
,
Stéphane Grégoire
(9, 10)
,
Lionel Brétillon
(9, 10)
,
Niyazi Acar
(9, 10)
,
Corinne Joffre
(1)
,
Guillaume Ferreira
(1)
,
Raluca Uricaru
(3)
,
Patricia Thebault
(3)
,
Pierre Gressens
(8)
,
Marie‐eve Tremblay
(5, 6, 7, 11)
,
Sophie Layé
(1)
,
Agnes Nadjar
(1)
1
NutriNeuro -
Nutrition et Neurobiologie intégrée
2 U1215 Inserm - UB - Neurocentre Magendie : Physiopathologie de la Plasticité Neuronale
3 LaBRI - Laboratoire Bordelais de Recherche en Informatique
4 University of Calgary
5 ULaval - Université Laval [Québec]
6 UVIC - University of Victoria [Canada]
7 UQAM - Université du Québec à Montréal = University of Québec in Montréal
8 NeuroDiderot (UMR_S_1141 / U1141) - Maladies neurodéveloppementales et neurovasculaires
9 CSGA - Centre des Sciences du Goût et de l'Alimentation [Dijon]
10 UBFC - Université Bourgogne Franche-Comté [COMUE]
11 UNBC - University of Northern British Columbia [Prince George]
2 U1215 Inserm - UB - Neurocentre Magendie : Physiopathologie de la Plasticité Neuronale
3 LaBRI - Laboratoire Bordelais de Recherche en Informatique
4 University of Calgary
5 ULaval - Université Laval [Québec]
6 UVIC - University of Victoria [Canada]
7 UQAM - Université du Québec à Montréal = University of Québec in Montréal
8 NeuroDiderot (UMR_S_1141 / U1141) - Maladies neurodéveloppementales et neurovasculaires
9 CSGA - Centre des Sciences du Goût et de l'Alimentation [Dijon]
10 UBFC - Université Bourgogne Franche-Comté [COMUE]
11 UNBC - University of Northern British Columbia [Prince George]
Cyril Dejean
- Fonction : Auteur
- PersonId : 1375772
- ORCID : 0000-0002-2592-7502
Clémentine Bosch-Bouju
- Fonction : Auteur
- PersonId : 747607
- IdHAL : clemboschbouju
- ORCID : 0000-0001-8869-768X
Lionel Brétillon
- Fonction : Auteur
- PersonId : 735917
- IdHAL : lionel-bretillon
- ORCID : 0000-0002-6957-100X
- IdRef : 149670303
Niyazi Acar
- Fonction : Auteur
- PersonId : 1136622
- IdHAL : niyazi-acar
- ORCID : 0000-0002-3401-8079
- IdRef : 070519188
Corinne Joffre
- Fonction : Auteur
- PersonId : 747399
- IdHAL : corinne-joffre
- ORCID : 0000-0001-8327-3554
- IdRef : 12845606X
Guillaume Ferreira
- Fonction : Auteur
- PersonId : 804521
- IdHAL : guillaume-ferreira
- ORCID : 0000-0001-5984-8143
- IdRef : 136818978
Pierre Gressens
- Fonction : Auteur
- PersonId : 757208
- ORCID : 0000-0002-0909-4221
- IdRef : 066987458
Sophie Layé
- Fonction : Auteur
- PersonId : 747372
- IdHAL : sophie-laye
- ORCID : 0000-0002-3843-1012
- IdRef : 11366883X
Résumé
Westernization of dietary habits has led to a progressive reduction in dietary intake of n-3 polyunsaturated fatty acids (n-3 PUFAs). Low maternal intake of n-3 PUFAs has been linked to neurodevelopmental disorders, conditions in which myelination processes are abnormal, leading to defects in brain functional connectivity. Only little is known about the role of n-3 PUFAs in oligodendrocyte physiology and white matter development. Here, we show that lifelong n-3 PUFA deficiency disrupts oligodendrocytes maturation and myelination processes during the postnatal period in mice. This has long-term deleterious consequences on white matter organization and hippocampus-prefrontal functional connectivity in adults, associated with cognitive and emotional disorders. Promoting developmental myelination with clemastine, a first-generation histamine antagonist and enhancer of oligodendrocyte precursor cell differentiation, rescues memory deficits in n-3 PUFA deficient animals. Our findings identify a novel mechanism through which n-3 PUFA deficiency alters brain functions by disrupting oligodendrocyte maturation and brain myelination during the neurodevelopmental period.
Domaines
Neurosciences [q-bio.NC]Format du dépôt | Notice |
---|---|
Type de dépôt | Article dans une revue |
Titre |
en
N‐3 PUFA deficiency disrupts oligodendrocyte maturation and myelin integrity during brain development
|
Résumé |
en
Westernization of dietary habits has led to a progressive reduction in dietary intake of n-3 polyunsaturated fatty acids (n-3 PUFAs). Low maternal intake of n-3 PUFAs has been linked to neurodevelopmental disorders, conditions in which myelination processes are abnormal, leading to defects in brain functional connectivity. Only little is known about the role of n-3 PUFAs in oligodendrocyte physiology and white matter development. Here, we show that lifelong n-3 PUFA deficiency disrupts oligodendrocytes maturation and myelination processes during the postnatal period in mice. This has long-term deleterious consequences on white matter organization and hippocampus-prefrontal functional connectivity in adults, associated with cognitive and emotional disorders. Promoting developmental myelination with clemastine, a first-generation histamine antagonist and enhancer of oligodendrocyte precursor cell differentiation, rescues memory deficits in n-3 PUFA deficient animals. Our findings identify a novel mechanism through which n-3 PUFA deficiency alters brain functions by disrupting oligodendrocyte maturation and brain myelination during the neurodevelopmental period.
|
Auteur(s) |
Quentin Leyrolle
1
, Fanny Decoeur
1
, Cyril Dejean
2
, Marie-Galadriel Briere
3
, Stephane Leon
1
, Ioannis Bakogiannis
1
, Emilie Baroux
1
, Tony‐lee Sterley
4
, Clémentine Bosch-Bouju
1
, Lydie Morel
1
, Camille Amadieu
1
, Cynthia Lecours
5, 6
, Marie‐kim St‐pierre
5, 6
, Maude Bordeleau
5, 6, 7
, Veronique de Smedt-Peyrusse
1
, Alexandra Sere
1
, Leslie Schwendimann
8
, Stéphane Grégoire
9, 10
, Lionel Brétillon
9, 10
, Niyazi Acar
9, 10
, Corinne Joffre
1
, Guillaume Ferreira
1
, Raluca Uricaru
3
, Patricia Thebault
3
, Pierre Gressens
8
, Marie‐eve Tremblay
5, 6, 7, 11
, Sophie Layé
1
, Agnes Nadjar
1
1
NutriNeuro -
Nutrition et Neurobiologie intégrée
( 1002390 )
- Laboratoire NutriNeurO
UMR INRAE 1286 - Université de Bordeaux - Bordeaux INP
Bâtiment UFR Pharmacie - 2ème Tranche - 2ème Etage – CC34
Université de Bordeaux, site de Carreire
146 rue Léo Saignat
33076 BORDEAUX Cedex - FRANCE
- France
2
U1215 Inserm - UB -
Neurocentre Magendie : Physiopathologie de la Plasticité Neuronale
( 1067841 )
- 146, rue Léo Saignat
33077 Bordeaux cedex
- France
3
LaBRI -
Laboratoire Bordelais de Recherche en Informatique
( 3102 )
- Domaine Universitaire 351, cours de la Libération 33405 Talence Cedex
- France
4
University of Calgary
( 106219 )
- 2500 University Dr NW Calgary, Alberta, T2N 1N4
- Canada
5
ULaval -
Université Laval [Québec]
( 93488 )
- 2325, rue de l'Université Québec G1V 0A6
- Canada
6
UVIC -
University of Victoria [Canada]
( 15325 )
- University of Victoria
3800 Finnerty Road
Victoria BC V8P 5C2
Canada
- Canada
7
UQAM -
Université du Québec à Montréal = University of Québec in Montréal
( 360045 )
- Université du Québec à Montréal CP 8888, succursale Centre-ville Montréal (Québec) H3C 3P8
- Canada
8
NeuroDiderot (UMR_S_1141 / U1141) -
Maladies neurodéveloppementales et neurovasculaires
( 1005068 )
- Hôpital Robert Debré
48 Bd Serurier
75019 Paris
- France
9
CSGA -
Centre des Sciences du Goût et de l'Alimentation [Dijon]
( 1002225 )
- Université de Bourgogne - Bât. CSG - 9E Bd Jeanne d'Arc - 21000 Dijon
- France
10
UBFC -
Université Bourgogne Franche-Comté [COMUE]
( 426438 )
- 32, avenue de l’observatoire
25000 BESANCON
- France
11
UNBC -
University of Northern British Columbia [Prince George]
( 316431 )
- Prince George, BC, Canada V2N 4Z9
- Canada
|
Langue du document |
Anglais
|
Nom de la revue |
|
Comité de lecture |
Oui
|
Vulgarisation |
Non
|
Audience |
Internationale
|
Date de publication électronique |
2021-09-14
|
URL éditeur |
https://onlinelibrary.wiley.com/doi/10.1002/glia.24088
|
Public visé |
Scientifique
|
Sous-type de document pour les Articles |
Research article
|
Date de publication |
2022
|
Volume |
70
|
Numéro |
1
|
Page/Identifiant |
50-70
|
Domaine(s) |
|
Financement |
|
Mots-clés |
en
Clemastine, Cognition, Hippocampus, Myelin, N-3 PUFA, Neurodevelopement, Oligodendrocyte, Omega-3, Prefrontal cortex
|
DOI | 10.1002/glia.24088 |
Pubmed Id | 34519378 |
UT key WOS | 000695519900001 |
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