Abstracts

Somatic Mutations Activating Ras/Raf/MAPK Signaling in Mesial Temporal Lobe Epilepsy

Abstract number : 3.46
Submission category : 12. Genetics / 12A. Human Studies
Year : 2022
Submission ID : 2232851
Source : www.aesnet.org
Presentation date : 12/5/2022 12:00:00 PM
Published date : Nov 22, 2022, 05:28 AM

Authors :
Sattar Khoshkhoo, MD – Brigham and Women's Hospital; Yilan Wang, BS – Boston Children's Hospital; Yasmine Chahine, BS – Boston Children's Hospital; Stephanie Robert, MD, PhD – Yale School of Medicine; August Yue Huang, PhD – Boston Children's Hospital; Edward Stronge, BS – Boston Children's Hospital; H. Westley Phillips, MD – Boston Children's Hospital; Brian Chhouk, BS – Boston Children's Hospital; Sara Bizzotto, PhD – Sorbonne University, Paris Brain Institute (ICM); Thiuni Adikari, BMSc (Hons) – University of Melbourne; Zimeng Ye, MS – University of Melbourne; Tom Witkowski, BSc (Hons) – University of Melbourne; Dulcie Lai, PharmD, PhD – University of North Carolina, Chapel Hill; Nadine Lee, . – Boston Children's Hospital; Julie Lokan, MBBS – Austin Health; Ingrid Scheffer, MBBS, PhD – University of Melbourne; Samuel Berkovic, MD – University of Melbourne; Michael Hildebrand, PhD – University of Melbourne; Edward Yang, MD, PhD – Boston Children's Hospital; Ingmar Blümcke, MD – University Hospitals Erlangen; Sanda Alexandrescu, MD – Boston Children's Hospital; Anita Huttner, MD – Yale School of Medicine; Erin Heinzen, PharmD, PhD – University of North Carolina, Chapel Hill; Annapurna Poduri, MD, MPH – Boston Children's Hospital; Dennis Spencer, MD – Yale School of Medicine; Eunjung Lee, PhD – Boston Children's Hospital; Christopher Walsh, MD, PhD – Boston Children's Hospital/HHMI; Kristopher Kahle, MD, PhD – Massachusetts General Hospital

This is a Late Breaking abstract

Rationale: Mesial temporal lobe epilepsy (MTLE), characterized by seizures arising from the hippocampus, is the most common focal epilepsy subtype and often refractory to anti-seizure medications. Large-cohort whole-exome sequencing (WES) studies of blood-derived DNA have established the important role of rare, damaging de novo and inherited (i.e., germline) variants in developmental and epileptic encephalopathies. However, with few exceptions, this approach has proven far less successful in identifying genetic determinants of focal epilepsies like MTLE. Recently, post-zygotic (i.e., somatic) variants have emerged as a major cause of pediatric focal epilepsies like focal cortical dysplasia. In this study we set out to test the hypothesis that somatic variants in the hippocampus are an important pathogenic mechanism underlying drug-resistant MTLE.

Methods: We performed high-coverage whole-exome and gene-panel sequencing (depth > 500X) of DNA derived from hippocampal tissue, and paired temporal neocortex and blood, when available, of 105 surgically-treated MTLE patients and 30 neurotypical individuals. Candidate somatic variants were validated with amplicon sequencing and/or droplet digital Polymerase Chain Reaction (ddPCR). A subset of the novel MTLE-associated somatic variants were evaluated experimentally using cellular and molecular assays.

Results: We detected ten pathogenic variants in PTPN11, SOS1, KRAS, BRAF, and NF1, all predicted to constitutively activate Ras/Raf/MAPK signaling, in patients with MTLE and none in the neurotypical controls. In five of these patients, mesial temporal sclerosis was the only finding on clinical imaging and histopathology. Immunohistochemical studies of hippocampal tissue harboring pathogenic somatic variants demonstrated increased phosphorylation of Erk1/2, confirming Ras/Raf/MAPK overactivation, predominantly in glial cells. Molecular assays showed abnormal liquid-liquid phase separation for the PTPN11 variants which suggested a gain-of-function mechanism, similar to Noonan syndrome.

Conclusions: Somatic variants activating Ras/Raf/MAPK signaling likely cause MTLE in a significant subset of patients with sporadic, medically-refractory disease, even in the absence of other pathology. Our findings provide a novel genetic mechanism for MTLE and highlight new therapeutic targets for this common form of epilepsy.

Funding: This work was supported by the NIH grants R25-NS065743, K08-NS128272, R01-NS109358, R01-NS111029, R01-NS117609, and R01-NS035129. CAW is an investigator of the Howard Hughes Medical Institute.
Genetics