Lippincott Williams & Wilkins
Supplemental dataFigure e-1. Representative radiological and pathological images of patients identified using targeted amplicon sequencing(A) Pre-op and post-op brain MR T2 weight images from patients identified using targeted amplicon sequencing. For EPI44, mMCD13 and EPI340, T2 weighted images demonstrate no remarkable findings in the brain parenchyma, including the temporal lobe. For EPI147, T2 weighted image showed diffuse cortical dysplasia in the Rt. frontal lobe. Yellow arrowhead: putative regions of epileptic focus. (B) Histopathologic images from H & E staining and immunohistochemical (IHC) staining. Scale bars, 40 ?m in H & E staining (upper panels) and 200 ?m in IHC staining of NeuN, neuronal marker (lower panels). (C) Capture image from Integrative Genomic Viewer (IGV) (upper panels) showing the validation results of site-specific amplicon sequencing in matched brain and peripheral blood samples. Schematic tables (lower panels) showing the number of sequence reads counted as mutated or reference sequences, as well as VAF of mutated alleles. Mut: mutation, Ref: reference.Figure e-2. The schematic figure of targeted amplicon sequencing(A) Schematic figure showing how to design sequencing primers. (B) Sequence of primers used in targeted amplicon sequencing. Figure e-3. Schematic diagram of the bioinformatics pipeline to analyze all sequencing dataData for the raw read qualified with FastQC were mapped from Fastq files to the GRCh37 assembly of the human genome reference sequence using BWA-MEM. We utilized MuTect and Strelka for analyzing matched brain and peripheral sample sequencing data sets (left). We applied in-house filtering criteria to exclude 1) read depth < 100, 2) registered mutations in a public database (common dbSNP147); 3) mutations with a putative low snpEFF impact score; 4) mutations with a PolyPhen & SIFT ≠ Damaging, phastCons score <0.9; 5) mutations with an allele frequency in the ExAC database for minor allele frequency (MAF) and East Asian populations > 0.01%; and 6) EB score < 5.099. After filtering process, we manually investigated mutations using Integrative Genomics Viewer (IGV) according to the following exclusion criteria; 1) adjacent alterations, not germline mutation, were found only in reads with target mutation; 2) target mutation detected in the read in one direction; 3) one or more biological similar sequence regions calculated by BLAST (). For germline variants analysis, we used GATK haplotype caller (right). We extracted variants in genes potentially associated with epilepsy. All extracted variants were applied same in-house filtering criteria.Figure e-4. Immunohistochemical studies to examine mTOR pathway activity(A) Representative immunohistochemical staining of phosphorylated S6 and NeuN in patients brain samples. FCD254: subject carrying mTOR p.A1459D mutation. mMCD013 and LGS150: subjects carrying mutations in SLC35A2. Compared with FCD254, mMCD016 and LGS150 samples show decreased percentages of cells with positive staining for phosphorylated S6 (P-S6) and NeuN, a neuronal marker. Scale bars, 50 ?m. (B) Quantification of P-S6 positive cells from three randomly selected representative cortical areas per case. * P < 0.05 (relative to FCD254 samples, one-way ANOVA with Bonferroni posttest). Error bars represent mean ± s.e.m.Table e-1. Clinical information of individuals enrolled in this studyType of sequencingIDILAE epilepsy classificationSyndromeSexAgeat surgeryAgeat diagnosisMRI report (3 tesla)PathologicdiagnosisWESEPI28FocalM8.34.8No abnormal lesion in brain parenchymaVentricular system normalGliosis onlyWESEPI41FocalF9.9No abnormal lesion in brain parenchymaVentricular system normalGliosis onlyWESEPI58FocalM7.66No abnormal lesion in brain parenchymaVentricular system normalGliosis onlyWESEPI148Combined generalized and focalLGSM14.310No abnormal lesion in brain parenchymaVentricular system normalGliosis onlyWESEPI150Combined generalized and focalLGSfrom ISM5.20.4No abnormal lesion in brain parenchymaVentricular system normalNeurons in white matter, consistent with mMCDWESEPI165FocalM15.010No abnormal lesion in brain parenchymaVentricular system normalGliosis onlyWESEPI166FocalM9.04No abnormal lesion in brain parenchymaVentricular system normalGliosis onlyWESEPI182Combined generalized and focalLGSM14.24No abnormal lesion in brain parenchymaVentricular system normalGliosis onlyWESEPI219Combined generalized and focalLGSfrom ISM3.50.3No abnormal lesion in brain parenchymaVentricular system normalNeurons in white matter, consistent with mMCDWESEPI225Combined generalized and focalISM0.60.5No abnormal lesion in brain parenchymaVentricular system normalGliosis onlyWESEPI227Combined generalized and focalLGSM2.91.9No abnormal lesion in brain parenchymaVentricular system normalGliosis onlyWESEPI362FocalF4.71.5No abnormal lesion in brain parenchymaVentricular system normalGliosis onlyWESEPI383Combined generalized and focalLGSM14.77No abnormal lesion in brain parenchymaVentricular system normalGliosis onlyTargetedEPI147Combined generalized and focalLGSF4.00.4Diffuse cortical dysplasia, Rt frontal lobeMinimal gliosisTargetedEPI212Combined generalized and focalLGSM1.91.3No abnormal lesion in brain parenchymaVentricular system normalGliosis onlyTargetedEPI218FocalM7.12.7S/P Lt. anterior temporal lobectomy.No other remarkable findings in the brain parenchyma and ventricular systemGliosis onlyTargetedEPI223Combined generalized and focalLGSM7.24No abnormal lesion in brain parenchymaVentricular system normalGliosis onlyTargetedEPI334Combined generalized and focalIS, later LGSF1.20.3Suspicion of slightly decreased volume of bilateral periventricular WM.Minimal gliosisTargetedEPI340Combined generalized and focalLGSM4.23No abnormal lesion in brain parenchymaVentricular system normalNeurons in white matter, consistent with mMCDTargetedEPI352Combined generalized and focalLGSM10.35No abnormal lesion in brain parenchymaVentricular system normalGliosis onlyTargetedEPI379Combined generalized and focalISM0.70.1Suspicious for polymicrogyriaGliosis onlyTargetedEPI44Combined generalized and focalLGSfrom ISM2.70.5No abnormal lesion in brain parenchymaVentricular system normalGliosis onlyTargetedEPI48FocalM15.69Cortical dysplasia, Lt temporal pole. Lesion affected Lt amygdala and hippocampal head.DDx. low grade gliomaGliosis onlyTargetedmMCD10Combined generalized and focalLGSfrom ISM11.20.5No abnormal lesion in brain parenchymaVentricular system normalNeurons in white matter, consistent with mMCDTargetedmMCD11Combined generalized and focalISF0.70.1MCD involving left frontoparietal lobe.Neurons in white matter, consistent with mMCDTargetedmMCD13Combined generalized and focalLGSfrom ISF5.11.1No abnormal lesion in brain parenchymaVentricular system normalNeurons in white matter, consistent with mMCDTargetedmMCD14Combined generalized and focalLGSfrom ISM5.90.2White matter signal increase at Rt temporo-parieto-occipital lobe with blurring margin from gray matter.Diffuse cortical dysplasia should be suspected.Neurons in white matter, consistent with mild MCDTargetedmMCD16FocalM12.15communicating hydrocephalus,no newly developed lesionNeurons in white matter, consistent with mMCDTargetedmMCD210FocalF2.70.3No abnormal lesion in brain parenchymaVentricular system normalNeurons in white matter, consistent with mMCDTargetedmMCD216Combined generalized and focalLGSfrom ISF1.90.3No abnormal lesion in brain parenchymaVentricular system normalNeurons in white matter, consistent with mMCDTargetedmMCD294FocalM17.915No abnormal lesion in brain parenchymaVentricular system normalNeurons in white matter, consistent with mMCDAbbreviation: WES: Whole Exome Sequencing; LGS: Lenox-gastaut syndrome; IS: Infantile syndrome; MCD: malformation of cortical development; FCD: focal cortical dysplasia; mMCD: mild malformation of cortical development; ILAE: International league against epilepsy; S/P: status post; WM: white matter; DDx: differential diagnosis Table e-2. Summary of deep whole exome sequencing fastq dataIDTotal ReadsTotal BasesMean depth (X)GC_RateQ30Q20CPS41-BL-135568156235923837762482 48.25%91.48%95.58%CPS41-BL-237842717438221144574513 48.23%91.47%95.57%CPS41-Br-134008602434348688424461 52.53%90.33%95.01%CPS41-Br-236018907636379096676488 52.62%90.24%94.96%CPS58-BL-134814858835163007388472 48.09%90.92%95.16%CPS58-BL-235658957436015546974483 48.19%90.34%94.83%CPS58-Br-133673118634009849786456 48.28%90.97%95.31%CPS58-Br-237306383637679447436506 48.17%90.84%95.25%EPI148-BL-131822292232140515122431 47.41%91.57%95.62%EPI148-BL-235966709036326376090488 47.21%90.74%95.06%EPI148-Br-139573086239968817062536 49.01%92.18%96.01%EPI148-Br-235370965635724675256479 48.85%91.71%95.72%EPI165-BL-136146226636507688866490 48.28%90.76%95.08%EPI165-BL-233774862034112610620458 48.15%88.79%94.03%EPI165-Br-137561099837936710798509 50.43%91.89%95.86%EPI165-Br-231960756232280363762433 50.20%91.49%95.62%EPI219-BL-134965778635315436386474 47.91%89.14%94.25%EPI219-BL-236826578037194843780499 48.00%89.08%94.20%EPI219-Br-129590654429886560944401 48.34%92.18%96.04%EPI219-Br-239477398239872172182535 48.06%90.69%95.13%EPI225-BL-137047083637417554436502 48.11%89.15%94.23%EPI225-BL-235995178036355129780488 48.39%88.51%93.85%EPI225-Br-132471453832796168338440 47.98%90.29%94.87%EPI225-Br-233078024033408804240448 48.12%90.20%94.84%EPI362-BL-133144167033475608670449 47.93%89.62%94.50%EPI362-BL-235114519835465664998476 47.93%89.33%94.32%EPI362-Br-133705928434042987684457 48.83%89.87%94.65%EPI362-Br-235419810235774008302480 48.77%90.45%94.99%FLE166-BL-135115118235466269382476 47.90%89.09%94.15%FLE166-BL-235823958036182197580486 47.92%90.98%95.24%FLE166-Br-132742374833069798548444 48.13%90.30%94.89%FLE166-Br-236610191236976293112496 48.14%90.58%95.04%FLE28-BL-136191878436553797184491 47.48%89.38%94.34%FLE28-BL-236132287636493610476490 47.38%89.64%94.49%FLE28-Br-135524402635879646626482 48.15%90.63%95.07%FLE28-Br-234608738234954825582469 47.95%90.42%94.97%LGS150-BL-135894512436253457524487 47.94%91.61%95.63%LGS150-BL-231673600831990336808429 47.94%91.78%95.74%LGS150-Br-134728489835075774698471 48.24%90.51%95.01%LGS150-Br-231051504831362019848421 48.03%91.58%95.58%LGS182-BL-131565993431881653334428 48.20%91.49%95.56%LGS182-BL-233969691634309388516460 48.31%91.53%95.58%LGS182-Br-134657624635004200846470 48.30%91.57%95.60%LGS182-Br-232596688232922655082442 48.23%91.69%95.65%LGS227-BL-133834090634172431506459 48.06%89.74%94.63%LGS227-BL-236687832837054711128497 47.98%89.85%94.70%LGS227-Br-133645812433982270524456 48.48%91.74%95.69%LGS227-Br-230424278030728520780412 48.47%91.42%95.55%LGS228-BL-137306226837679289068506 48.41%89.80%94.69%LGS228-BL-238875717439264474574527 48.26%89.55%94.54%LGS228-Br-130248096030550576960410 48.55%91.79%95.80%LGS228-Br-230749558031057053580417 48.71%91.90%95.82%Table e-3. Annotations for all stop-gained mutations after filtering process.IDChrPOSREFALTEBTotal read DepthAltered readDepthVariant allelefrequencyGeneSnpEff effectNucleotidechangesProteinchangesSIFTPolyphenHDIVPolyphenHVARPhastconCADDEPI219X48762597GA601754023%SLC35A2stop_gainedc.589C>Tp.Gln197*NANANANANALGS150X48762426CA602734316%SLC35A2stop_gainedc.760G>Tp.Glu254*NANANANANAmMCD13X48762483TGNA1690991905610.12%SLC35A2missensec.703T>Gp.Asn235GlnNA11120.3EPI340X48762684GANA197579298117.50%SLC35A2stop-gainedc.502G>Ap.Gln168*NANANA122.2EPI147X48762633GANA123511972235.89%SLC35A2stop-gainedc.553G>Ap.Gln185*NANANA0.99418.69EPI044X48763821CANA9909452995.07%SLC35A2splice-acceptorNANANANANA121.4Abbreviation: NA: Non-availableAll identified variants annotated based on NM_005660.1Table e-4. 10 known mTOR pathway genes screened in this study.GeneNo. of targeted regionsCoverageReferenceAKT32293.03%Lee et al., Nat Genet 2012PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5MZWU8L0F1dGhvcj48WWVhcj4yMDEyPC9ZZWFyPjxSZWNO
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ADDIN EN.CITE.DATA 5AKT3Signaling protein, upstream regulator of mTORLee et al., Nat Genet 2012PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5MZWU8L0F1dGhvcj48WWVhcj4yMDEyPC9ZZWFyPjxSZWNO
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ADDIN EN.CITE.DATA 9STRADASignaling protein, upstream regulator of mTORCrino, Trends Mol Med 2011PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5DcmlubzwvQXV0aG9yPjxZZWFyPjIwMTE8L1llYXI+PFJl
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ADDIN EN.CITE.DATA 17TUBB2BEncoding subunit of tubulin related to cortical laminationBarkovich et al., Brain 2012 ADDIN EN.CITE <EndNote><Cite><Author>Barkovich</Author><Year>2012</Year><RecNum>35</RecNum><DisplayText><style face="superscript">21</style></DisplayText><record><rec-number>35</rec-number><foreign-keys><key app="EN" db-id="0dr0f2rs49rv21ezer5v9f92daeexrxasdwt" timestamp="1510560272">35</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Barkovich, A. J.</author><author>Guerrini, R.</author><author>Kuzniecky, R. I.</author><author>Jackson, G. D.</author><author>Dobyns, W. B.</author></authors></contributors><auth-address>Neuroradiology, University of California at San Francisco, 505 Parnassus Avenue, San Francisco, CA 94913-0628, USA. james.barkovich@ucsf.edu</auth-address><titles><title>A developmental and genetic classification for malformations of cortical development: update 2012</title><secondary-title>Brain</secondary-title></titles><periodical><full-title>Brain</full-title></periodical><pages>1348-69</pages><volume>135</volume><number>Pt 5</number><keywords><keyword>Cell Movement/physiology</keyword><keyword>*Cerebral Cortex/abnormalities/growth & development/pathology</keyword><keyword>Developmental Disabilities/etiology</keyword><keyword>Diagnostic Imaging</keyword><keyword>Epilepsy/etiology</keyword><keyword>History, 21st Century</keyword><keyword>Humans</keyword><keyword>*Malformations of Cortical Development/classification/complications/genetics</keyword><keyword>Molecular Biology</keyword><keyword>Mutation/*genetics</keyword></keywords><dates><year>2012</year><pub-dates><date>May</date></pub-dates></dates><isbn>1460-2156 (Electronic)
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ADDIN EN.CITE.DATA 23EZH2Encoding histone methyltrasferaseKobow et al., Acta Neuropahtol 2013PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Lb2JvdzwvQXV0aG9yPjxZZWFyPjIwMTM8L1llYXI+PFJl
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ADDIN EN.CITE PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Lb2JvdzwvQXV0aG9yPjxZZWFyPjIwMTM8L1llYXI+PFJl
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ADDIN EN.CITE.DATA 24HNRNPUEncoding nuclear ribonucleoproteinEpi 4KC et al., Nature 2013PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5FcGk8L0F1dGhvcj48WWVhcj4yMDEzPC9ZZWFyPjxSZWNO
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ADDIN EN.CITE.DATA 16RYR3Encoding ryanodine receptorEuro E-RESC et al., 2014 ADDIN EN.CITE <EndNote><Cite><Author>Euro</Author><Year>2014</Year><RecNum>29</RecNum><DisplayText><style face="superscript">25</style></DisplayText><record><rec-number>29</rec-number><foreign-keys><key app="EN" db-id="0dr0f2rs49rv21ezer5v9f92daeexrxasdwt" timestamp="1510559766">29</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Euro, Epinomics- R. E. S. Consortium</author><author>Epilepsy Phenome/Genome, Project</author><author>Epi, K. Consortium</author></authors></contributors><titles><title>De novo mutations in synaptic transmission genes including DNM1 cause epileptic encephalopathies</title><secondary-title>Am J Hum Genet</secondary-title></titles><periodical><full-title>Am J Hum Genet</full-title></periodical><pages>360-70</pages><volume>95</volume><number>4</number><keywords><keyword>Cohort Studies</keyword><keyword>Dynamin I/*genetics</keyword><keyword>Exome/genetics</keyword><keyword>Fatty Acid Synthase, Type I/genetics</keyword><keyword>Female</keyword><keyword>Gene Regulatory Networks</keyword><keyword>Humans</keyword><keyword>Infant, Newborn</keyword><keyword>Lennox Gastaut Syndrome/*genetics</keyword><keyword>Male</keyword><keyword>Mutation/*genetics</keyword><keyword>Protein Interaction Maps</keyword><keyword>Receptors, GABA-B/genetics</keyword><keyword>Ryanodine Receptor Calcium Release Channel/genetics</keyword><keyword>Spasms, Infantile/*genetics</keyword><keyword>Synaptic Transmission/*genetics</keyword></keywords><dates><year>2014</year><pub-dates><date>Oct 02</date></pub-dates></dates><isbn>1537-6605 (Electronic)
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ADDIN EN.CITE.DATA 16Table e-6. Summary of targeted hybrid capture sequencingIDTotal BasesMean depth (X)% Coverage of target regions more than10x50x100x200x300x400x500xLGS013-BL1613342061621.32100938474696662LGS013-Br1751651291760.311001009998959391LGS044-BL1558940291566.651001009998969492LGS044-Br1533698671541.2810010010099999896LGS147-Br1636221451644.311001009999979593LGS147-BL1801374751810.2810010010099989796LGS340-BL1332895151339.49100999997949188LGS340-Br1407323901414.281001009998969389Table e-7. Probability values for amplicon sequencing of matched peripheral samplesIDTotal DepthRefAltVAFp-valueEPI219103589GA0.03%0.78547LGS150958719CA0.16%0.077007mMCD132096201TG0.02%0.488391EPI3403544147GA0.08%0.543417EPI1471636503GA0.07%0.619817EPI0441889823CA0.08%0.268407 ADDIN EN.REFLIST 1.Lee JH, Huynh M, Silhavy JL, et al. De novo somatic mutations in components of the PI3K-AKT3-mTOR pathway cause hemimegalencephaly. Nat Genet 2012;44:941-945.2.Poduri A, Evrony GD, Cai X, et al. Somatic activation of AKT3 causes hemispheric developmental brain malformations. Neuron 2012;74:41-48.3.Lal D, Reinthaler EM, Schubert J, et al. DEPDC5 mutations in genetic focal epilepsies of childhood. Ann Neurol 2014;75:788-792.4.Scheffer IE, Heron SE, Regan BM, et al. Mutations in mammalian target of rapamycin regulator DEPDC5 cause focal epilepsy with brain malformations. Ann Neurol 2014;75:782-787.5.Lim JS, Kim WI, Kang HC, et al. Brain somatic mutations in MTOR cause focal cortical dysplasia type II leading to intractable epilepsy. Nat Med 2015;21:395-400.6.Jansen LA, Mirzaa GM, Ishak GE, et al. PI3K/AKT pathway mutations cause a spectrum of brain malformations from megalencephaly to focal cortical dysplasia. Brain 2015;138:1613-1628.7.Riviere JB, Mirzaa GM, O'Roak BJ, et al. De novo germline and postzygotic mutations in AKT3, PIK3R2 and PIK3CA cause a spectrum of related megalencephaly syndromes. Nat Genet 2012;44:934-940.8.Luchman HA, Stechishin OD, Nguyen SA, Lun XQ, Cairncross JG, Weiss S. Dual mTORC1/2 blockade inhibits glioblastoma brain tumor initiating cells in vitro and in vivo and synergizes with temozolomide to increase orthotopic xenograft survival. Clin Cancer Res 2014;20:5756-5767.9.Zhou J, Blundell J, Ogawa S, et al. Pharmacological inhibition of mTORC1 suppresses anatomical, cellular, and behavioral abnormalities in neural-specific Pten knock-out mice. J Neurosci 2009;29:1773-1783.10.Crino PB. mTOR: A pathogenic signaling pathway in developmental brain malformations. Trends Mol Med 2011;17:734-742.11.Marin-Valencia I, Guerrini R, Gleeson JG. Pathogenetic mechanisms of focal cortical dysplasia. Epilepsia 2014;55:970-978.12.Parker WE, Orlova KA, Parker WH, et al. Rapamycin prevents seizures after depletion of STRADA in a rare neurodevelopmental disorder. Sci Transl Med 2013;5:182ra153.13.Alfaiz AA, Micale L, Mandriani B, et al. TBC1D7 mutations are associated with intellectual disability, macrocrania, patellar dislocation, and celiac disease. Hum Mutat 2014;35:447-451.14.Lim JS, Gopalappa R, Kim SH, et al. Somatic Mutations in TSC1 and TSC2 Cause Focal Cortical Dysplasia. Am J Hum Genet 2017;100:454-472.15.Tyburczy ME, Dies KA, Glass J, et al. Mosaic and Intronic Mutations in TSC1/TSC2 Explain the Majority of TSC Patients with No Mutation Identified by Conventional Testing. PLoS Genet 2015;11:e1005637.16.Epi KC, Epilepsy Phenome/Genome P, Allen AS, et al. De novo mutations in epileptic encephalopathies. Nature 2013;501:217-221.17.Guerrini R. Genetic malformations of the cerebral cortex and epilepsy. Epilepsia 2005;46 Suppl 1:32-37.18.Shen T, Ji F, Yuan Z, Jiao J. CHD2 is Required for Embryonic Neurogenesis in the Developing Cerebral Cortex. Stem Cells 2015;33:1794-1806.19.Poirier K, Lebrun N, Broix L, et al. Mutations in TUBG1, DYNC1H1, KIF5C and KIF2A cause malformations of cortical development and microcephaly. Nat Genet 2013;45:639-647.20.Bi W, Sapir T, Shchelochkov OA, et al. Increased LIS1 expression affects human and mouse brain development. Nat Genet 2009;41:168-177.21.Barkovich AJ, Guerrini R, Kuzniecky RI, Jackson GD, Dobyns WB. A developmental and genetic classification for malformations of cortical development: update 2012. Brain 2012;135:1348-1369.22.Cushion TD, Dobyns WB, Mullins JG, et al. Overlapping cortical malformations and mutations in TUBB2B and TUBA1A. Brain 2013;136:536-548.23.Marucci G, de Biase D, Visani M, et al. Mutant BRAF in low-grade epilepsy-associated tumors and focal cortical dysplasia. Ann Clin Transl Neurol 2014;1:130-134.24.Kobow K, Kaspi A, Harikrishnan KN, et al. Deep sequencing reveals increased DNA methylation in chronic rat epilepsy. Acta Neuropathol 2013;126:741-756.25.Euro E-RESC, Epilepsy Phenome/Genome P, Epi KC. De novo mutations in synaptic transmission genes including DNM1 cause epileptic encephalopathies. Am J Hum Genet 2014;95:360-370.26.Lehnart SE, Mongillo M, Bellinger A, et al. Leaky Ca2+ release channel/ryanodine receptor 2 causes seizures and sudden cardiac death in mice. J Clin Invest 2008;118:2230-2245. ................
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