AAV‐delivered diacylglycerol kinase DGKk achieves long‐term rescue of fragile X syndrome mouse model

Abstract Fragile X syndrome (FXS) is the most frequent form of familial intellectual disability. FXS results from the lack of the RNA‐binding protein FMRP and is associated with the deregulation of signaling pathways downstream of mGluRI receptors and upstream of mRNA translation. We previously foun...

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Main Authors: Karima Habbas, Oktay Cakil, Boglárka Zámbó, Ricardos Tabet, Fabrice Riet, Doulaye Dembele, Jean‐Louis Mandel, Michaël Hocquemiller, Ralph Laufer, Françoise Piguet, Hervé Moine
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Language:English
Published: Springer Nature 2022-04-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.202114649
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author Karima Habbas
Oktay Cakil
Boglárka Zámbó
Ricardos Tabet
Fabrice Riet
Doulaye Dembele
Jean‐Louis Mandel
Michaël Hocquemiller
Ralph Laufer
Françoise Piguet
Hervé Moine
author_facet Karima Habbas
Oktay Cakil
Boglárka Zámbó
Ricardos Tabet
Fabrice Riet
Doulaye Dembele
Jean‐Louis Mandel
Michaël Hocquemiller
Ralph Laufer
Françoise Piguet
Hervé Moine
author_sort Karima Habbas
collection DOAJ
description Abstract Fragile X syndrome (FXS) is the most frequent form of familial intellectual disability. FXS results from the lack of the RNA‐binding protein FMRP and is associated with the deregulation of signaling pathways downstream of mGluRI receptors and upstream of mRNA translation. We previously found that diacylglycerol kinase kappa (DGKk), a main mRNA target of FMRP in cortical neurons and a master regulator of lipid signaling, is downregulated in the absence of FMRP in the brain of Fmr1‐KO mouse model. Here we show that adeno‐associated viral vector delivery of a modified and FMRP‐independent form of DGKk corrects abnormal cerebral diacylglycerol/phosphatidic acid homeostasis and FXS‐relevant behavioral phenotypes in the Fmr1‐KO mouse. Our data suggest that DGKk is an important factor in FXS pathogenesis and provide preclinical proof of concept that its replacement could be a viable therapeutic strategy in FXS.
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spelling doaj-art-f6fe6fea1bab4023b24b4f87b67b81312025-08-20T03:46:13ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842022-04-0114511510.15252/emmm.202114649AAV‐delivered diacylglycerol kinase DGKk achieves long‐term rescue of fragile X syndrome mouse modelKarima Habbas0Oktay Cakil1Boglárka Zámbó2Ricardos Tabet3Fabrice Riet4Doulaye Dembele5Jean‐Louis Mandel6Michaël Hocquemiller7Ralph Laufer8Françoise Piguet9Hervé Moine10Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Département de Médecine Translationelle et Neurogénétique, Centre National de la Recherche Scientifique (CNRS UMR7104), Institut National de la Santé et de la Recherche Médicale (INSERM U1258), Université de StrasbourgInstitut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Département de Médecine Translationelle et Neurogénétique, Centre National de la Recherche Scientifique (CNRS UMR7104), Institut National de la Santé et de la Recherche Médicale (INSERM U1258), Université de StrasbourgInstitut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Département de Médecine Translationelle et Neurogénétique, Centre National de la Recherche Scientifique (CNRS UMR7104), Institut National de la Santé et de la Recherche Médicale (INSERM U1258), Université de StrasbourgInstitut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Département de Médecine Translationelle et Neurogénétique, Centre National de la Recherche Scientifique (CNRS UMR7104), Institut National de la Santé et de la Recherche Médicale (INSERM U1258), Université de StrasbourgInstitut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), PHENOMIN‐ICS, Centre National de la Recherche Scientifique (CNRS UMR7104), Institut National de la Santé et de la Recherche Médicale (INSERM U1258), Université de StrasbourgInstitut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Département de Médecine Translationelle et Neurogénétique, Centre National de la Recherche Scientifique (CNRS UMR7104), Institut National de la Santé et de la Recherche Médicale (INSERM U1258), Université de StrasbourgInstitut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Département de Médecine Translationelle et Neurogénétique, Centre National de la Recherche Scientifique (CNRS UMR7104), Institut National de la Santé et de la Recherche Médicale (INSERM U1258), Université de StrasbourgLysogeneLysogeneNeuroGenCell, INSERM U1127, Paris Brain Institute (ICM), Sorbonne University, CNRS, AP‐HP, University Hospital Pitié‐SalpêtrièreInstitut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Département de Médecine Translationelle et Neurogénétique, Centre National de la Recherche Scientifique (CNRS UMR7104), Institut National de la Santé et de la Recherche Médicale (INSERM U1258), Université de StrasbourgAbstract Fragile X syndrome (FXS) is the most frequent form of familial intellectual disability. FXS results from the lack of the RNA‐binding protein FMRP and is associated with the deregulation of signaling pathways downstream of mGluRI receptors and upstream of mRNA translation. We previously found that diacylglycerol kinase kappa (DGKk), a main mRNA target of FMRP in cortical neurons and a master regulator of lipid signaling, is downregulated in the absence of FMRP in the brain of Fmr1‐KO mouse model. Here we show that adeno‐associated viral vector delivery of a modified and FMRP‐independent form of DGKk corrects abnormal cerebral diacylglycerol/phosphatidic acid homeostasis and FXS‐relevant behavioral phenotypes in the Fmr1‐KO mouse. Our data suggest that DGKk is an important factor in FXS pathogenesis and provide preclinical proof of concept that its replacement could be a viable therapeutic strategy in FXS.https://doi.org/10.15252/emmm.202114649AAVdiacylglycerol kinaseFmr1‐KOFMRPFragile X syndrome
spellingShingle Karima Habbas
Oktay Cakil
Boglárka Zámbó
Ricardos Tabet
Fabrice Riet
Doulaye Dembele
Jean‐Louis Mandel
Michaël Hocquemiller
Ralph Laufer
Françoise Piguet
Hervé Moine
AAV‐delivered diacylglycerol kinase DGKk achieves long‐term rescue of fragile X syndrome mouse model
EMBO Molecular Medicine
AAV
diacylglycerol kinase
Fmr1‐KO
FMRP
Fragile X syndrome
title AAV‐delivered diacylglycerol kinase DGKk achieves long‐term rescue of fragile X syndrome mouse model
title_full AAV‐delivered diacylglycerol kinase DGKk achieves long‐term rescue of fragile X syndrome mouse model
title_fullStr AAV‐delivered diacylglycerol kinase DGKk achieves long‐term rescue of fragile X syndrome mouse model
title_full_unstemmed AAV‐delivered diacylglycerol kinase DGKk achieves long‐term rescue of fragile X syndrome mouse model
title_short AAV‐delivered diacylglycerol kinase DGKk achieves long‐term rescue of fragile X syndrome mouse model
title_sort aav delivered diacylglycerol kinase dgkk achieves long term rescue of fragile x syndrome mouse model
topic AAV
diacylglycerol kinase
Fmr1‐KO
FMRP
Fragile X syndrome
url https://doi.org/10.15252/emmm.202114649
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