Postmortem brain transcriptomes in Dup15q and idiopathic autism. T Grant Belgard, DPhil Dan Geschwind s Lab UCLA Neuropsychiatric Institute
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1 Postmortem brain transcriptomes in Dup15q and idiopathic autism T Grant Belgard, DPhil Dan Geschwind s Lab UCLA Neuropsychiatric Institute
2 Many genetic causes of autism, none particularly dominant Is there molecular convergence? (for understanding & translation)
3 Sequence RNA from frontal & temporal cortex 8 Dup15q, 37 idiopathic cases, and 30 controls from two brain banks (University of Maryland & Autism Tissue Program) Dissected grey matter from frontal cortex (ba9) and temporal cortex (ba 41/42/22) RNA-seq using rrna-depleted RNA to an average depth of 50M read pairs (50 nt from each end) Removed non-expressed genes, normalized, removed outliers, etc. Penalized cubic splines regression to remove effects of RIN and differential white matter contribution Linear mixed-effects model with age and sex as covariates
4 Expression differences across the 15q region Some changes are unique to Dup15q Others are shared with idiopathic autism Some genes have lower expression in Dup15q/idiopathic ASD
5 15q region expression: breakpoints 1-2 Dup15q + autism idiopathic autism control Differentially expressed in 15q vs idiopathic + control
6 15q region expression: breakpoints 2-3 Dup15q + autism idiopathic autism control
7 15q region expression: breakpoints 3-5 Dup15q + autism idiopathic autism control Differentially expressed in 15q vs idiopathic + control, but significantly more so in 15q
8 Global expression differences: most changes outside the 15q region Characteristic gene expression signature in idiopathic autism This signature is even stronger in Dup15q Uncorrelated with seizures Activated glial genes up; synaptic genes down
9 Idiopathic autism gene expression signature replicates requiring p<0.005 in at least one comparison rho = 0.65; N=382 t=16.7 p tiny
10 Also replicates across platforms Chi-squared 279; p incalculably tiny 3.6 fold enrichment (Chi-squared) Voineagu et al. brains on arrays new brains with RNA- seq Both circles FDR 5% and fold change > 1.3
11 Dup15q shares this same gene expression signature 2158 genes overlap All at FDR 5%
12 These gene sets are inversely correlated in individual samples Neelroop Parikshak
13 Signature is stronger in Dup15q than in idiopathic autism 5 We get the slope for each sample like this 4 3 slope 2 1 Control Idiopathic 15q Dup
14 Gene expression changes are unrelated to seizures Correlation, t test & F test not close to significant Presumably not seizure medications No apparent relationship with age or cause of death Other medications?
15 Synaptic & activity- related genes go down PVALB is the most downregulated in this overlap down by half GABA production: GAD1 (34% lower), GAD2 (35% lower) Top 5: Synapse part, synaptic transmission, neurotransmitter transport, synapse, neuron projection (Z>9; 5% for all) Glutamate secretion: CPLX1 GLS GLS2 SNAP25 STX1A STXBP1 SYT1 GABA receptor activity: GABBR2 GABRA1 GABRB2 GABRD GABRG2 Ion transport: ATP1A1 ATP1A3 ATP1B1 ATP5A1 ATP5B ATP5G1 ATP6AP1 ATP6V0A1 ATP6V0D1 ATP6V1A ATP6V1B2 ATP6V1C1 ATP6V1E1 ATP6V1G2 HCN1 KCNA1 KCNA2 KCNAB1 KCNAB3 KCNB2 KCNC2 KCND2 KCNH1 KCNIP4 KCNJ11 KCNJ3 KCNJ9 KCNK1 KCNK9 KCNS1 KCNS2 KCTD1 NSF SCN1A SCN1B SCN2A SCN2B SCN4B SCN8A SLC12A5 SLC24A2 SLC32A1 SLC36A1 SLC38A1 SLC4A10 SLC4A8 SLC8A1 SLC8A2 SLC9A6 SLC9B2 Ionotropic glutamate receptor: APP ATP1A3 GRIK1 GRIN2A
16 Activated glial and immune/ inflammation markers go up Top gene is S100A9, a marker of activated microglia in Alzheimer s Disease (and apparently also one of the most upregulated genes in Matt Anderson s Ube3a duplication mouse model), 2.5 fold higher Also PSEN1, APOE, SOCS3, ICAM1, CDKN1A, SERPINH1, NFKB1, NFKB2, NFKBIA, BCL3, CD44, IL4R, IL6R, AQP4, PTN Other interesting players: COMT, MAOA, GLUD1 & GLUD2, ALDH9A1, SLC1A3, GABRG1, SAT1, NEAT1, EMX2, PAX6, HDAC1
17 What might be happening? Microglial pruning hypothesis Enlarged, putatively active microglia in postmortem autism DLPFC (Morgan et al Biol Psychiatry) Microglia 20% more dense in autism cerebral cortex (Tetreault et al J Autism Dev Disord) Microglia closer to neurons in autism DLPFC (Morgan et al Brain Res) Kefenmann et al. Neuron 2013
18 One possible model for autism pathogenesis?* Genetic variation Environmental insult Synaptic dysfunction: activity- dependent protein synthesis or breakdown, cell adhesion Excitatory/ inhibitory imbalance Altered brain growth trajectory Seizures Impaired systems- level connectivity or physiology *speculation! Microglial inflammation & synaptic pruning? Fewer or less active synapses Autism Causal Consistent with gene expression in Dup15q
19 Could one intervene retrospectively in Dup15q?* X Genetic variation Correct the synaptic dysfunction Restore excitatory/ inhibitory balance Seizures X Altered brain growth trajectory Impaired systems- level connectivity or physiology *speculation! Reduce microglial activation and pruning? Boost synapse activity or promote new synapse formation Autism
20 Conclusions and future directions Idiopathic autism and especially Dup15q are characterized by two highly anticorrelated sets of genes in frontal and temporal cortex o Immune/microglial genes up o Synaptic genes down This signature is uncorrelated to seizures Need to determine exactly what these changes reflect and if there might be a pharmacological pressure point therein
21 Acknowledgements Dan Geschwind Neelroop Parikshak Irina Voineagu Vivek Swarup Jing Ou Joe DeYoung Claire Orosco Jason Stein Yuan Tian The families of the deceased Autism Tissue Program University of Maryland Brain Bank
22 Questions, comments, suggestions?
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