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Bordey, A.

Publications and source records attributed to Bordey, A..

2 recordsLinked to original sources

Genetic expression of 4E-BP1 in juvenile mice alleviates mTOR-induced neuronal dysfunction and epilepsy

Hyperactivation of mTOR signaling during fetal neurodevelopment alters neuron structure and function, leading to focal malformation of cortical development (FMCD) and intractable epilepsy. Recent evidence suggests increased cap-dependent translation downstream of mTOR contributes to FMCD formation and seizures. However, whether reducing overactive translation once the developmental pathologies are established reverses neuronal abnormalities and seizures is unknown. Here, we found that the translational repressor 4E-BP1, which is inactivated by mTOR-mediated phosphorylation, is hyperphosphorylated in patient FMCD tissue and in a mouse model of FMCD. Expressing constitutive active 4E-BP1 to repress aberrant translation in juvenile mice with FMCD reduced neuronal cytomegaly and corrected several electrophysiological alterations, including depolarized resting membrane potential, irregular firing pattern, and aberrant HCN4 channel expression. This was accompanied by improved cortical spectral activity and decreased seizures. Although mTOR controls multiple pathways, our study shows that targeting 4E-BP1-mediated translation alone is sufficient to alleviate neuronal dysfunction and ongoing epilepsy.

neuroscience↗

Ectopic HCN4 expression drives mTOR-dependent epilepsy

The causative link between focal cortical malformations (FCM) and epilepsy is well-accepted, especially among patients with focal cortical dysplasia type II (FCDII) and tuberous sclerosis complex (TSC). However, the mechanisms underlying seizures remain unclear. Using a mouse model of TSC- and FCDII-associated FCM, we show that FCM neurons are responsible for seizure activity via their unexpected abnormal expression of the hyperpolarization-activated cyclic nucleotide-gated potassium channel isoform 4 (HCN4), which is normally not present in cortical pyramidal neurons after birth. Increasing intracellular cAMP levels, which preferentially affects HCN4 gating relative to the other isoforms, drove repetitive firing of FCM neurons but not that of control pyramidal neurons. Ectopic HCN4 expression was mTOR-dependent, preceded the onset of seizures, and was also found in diseased neurons in tissue resected for epilepsy treatment from TSC and FCDII patients. Finally, blocking HCN4 channel activity in FCM neurons prevented epilepsy in mice. These findings that demonstrate HCN4 acquisition as seizure-genic, identify a novel cAMP-dependent seizure mechanism in TSC and FCDII. Furthermore, the unique expression of HCN4 exclusively in FCM neurons provides opportunities for using HCN4 as a gene therapy target to treat epilepsy in individuals with FCDII or TSC. One Sentence SummaryOur data provide a novel cAMP-dependent mechanism of seizure initiation in focal cortical dysplasia and tuberous sclerosis complex due to the unexpected ectopic expression of HCN4 channels only in diseased neurons. HCN4 channels are thus promising candidates for gene therapy to treat epilepsy generated by mTOR-driven focal malformations.

neuroscience↗