Molecular Signatures of Resilience to Alzheimer’s Disease in Neocortical Layer 4 Neurons
Cite
Dharshini, S.A.P., Sanz-Ros, J., Pan, J., Tang, W., Vallejo, K., Otero-Garcia, M. and Cobos, I., 2024. Molecular Signatures of Resilience to Alzheimer's Disease in Neocortical Layer 4 Neurons. bioRxiv, pp.2024-11. https://doi.org/10.1101/2024.11.03.621787
Abstract
Single-cell omics is advancing our understanding of selective neuronal vulnerability in Alzheimer’s disease (AD), revealing specific subtypes that are either susceptible or resilient to neurodegeneration. Using single-nucleus and spatial transcriptomics to compare neocortical regions affected early (prefrontal cortex and precuneus) or late (primary visual cortex) in AD, we identified a resilient excitatory population in layer 4 of the primary visual cortex expressing RORB, CUX2, and EYA4. Layer 4 neurons in association neocortex also remained relatively preserved as AD progressed and shared overlapping molecular signatures of resilience. Early in the disease, resilient neurons upregulated genes associated with synapse maintenance, synaptic plasticity, calcium homeostasis, and neuroprotective factors, including GRIN2A, RORA, NRXN1, NLGN1, NCAM2, FGF14, NRG3, NEGR1, and CSMD1. We also identified KCNIP4, which encodes a voltage-gated potassium (Kv) channel-interacting protein that interacts with Kv4.2 channels and presenilins, as a key factor linked to resilience. KCNIP4 was consistently upregulated in the early stages of pathology. Furthermore, AAV-mediated overexpression of Kcnip4 in a humanized AD mouse model reduced the expression of the activity-dependent genes Arc and c-Fos, suggesting compensatory mechanisms against neuronal hyperexcitability. Our dataset provides a valuable resource for investigating mechanisms underlying resilience to neurodegeneration.
Datasets
APOE class
Brain region
SORT
Braak stage
Disease group
Amyloid
Postmortem interval (hours)
Race
Age (years)
RNA integrity number
Subject ID
Age group
Postmortem interval group
RNA integrity number group
Major cell type
Cell type
NP diagonis
Assay
Disease
Sex
Tissue
Ethnicity
Sample preservation method
Leiden clustering
L4 clusters across brain region
Frontal Cx (BA9)288030 cells Precuneous (BA7)72088 cells Primary Visual Cx (BA17)64410 cells 10 to 15 hours93284 cells 15.2 to 19.5 hours92648 cells 5 to 9.3 hours80803 cells 1 to 4.5 hours77529 cells More than 20 hours63777 cells Oligodendrocytes36589 cells Ex1:[CUX2-SERPINE2-LAMP5]65152 cells Ex2:[CUX2-RORB-GLIS3-LRRC2]42034 cells Oligodendrocyte-OPALIN35839 cells Ex5:[RORB-CUX2-EYA4-LAMA3]27918 cells Ex12:[THEMIS-PRRX1]21756 cells Ex7:[RORB-GABRG1]21065 cells In1:[LHX6-PVALB-CLMN]19009 cells Ex9:[RORB-TLL1-PCP4-MID1]17264 cells Ex16:[FEZF2-SYT6]12579 cells Ex8:[RORB-TLL1-TMTC4]11805 cells Ex3:[CUX2-RORB-GLIS3-SV2C]10258 cells Ex10:[RORB-TLL1-PCP4-TYR]8436 cells Ex17:[FEZF2-ZFHX3-SEMA3D]8071 cells In2:[LHX6-PVALB-MEPE]7465 cells In11:[ADARB2-LAMP5-KIT]7163 cells Ex11:[RORB-ADGRL4]6726 cells Ex4:[CUX2-RORB-COL5A2-CLMN]6316 cells Ex14:|FEZF2-HTR2C]6229 cells Ex13:[THEMIS-POSTN]5974 cells In6:[LHX6-SST-SLC9A2]5687 cells Astrocyte-SLC1A2-WIF15246 cells In10:[LHX6-ADARB2-LAMP5-HCRTR2]4232 cells In19:[ADARB2-CALB2-SCML4]4183 cells In17:[ADARB2-VIP-ABI3BP]4177 cells Astrocyte-SLC1A2-SMTN4155 cells In18:[ADARB2-VIP-EXPH5]4131 cells Ex18:[FEZF2-ZFHX3-SCUBE1]3193 cells In14:[ADARB2-SEMA3C]3074 cells Microglia-Reactive-CD1633001 cells In7:[LHX6-SST-B3GAT2]2982 cells Astrocyte-GFAP-VCAN2937 cells In16:[ADARB2-VIP-TAC3-NRP1]2845 cells In4:[LHX6-SST-MSR1]2733 cells In5:[LHX6-SST-SPON1]2369 cells Astrocyte-GFAP-OSMR2353 cells In3:[LHX6-PVALB-COL15A1]2117 cells In15:[ADARB2-VIP-DACH2]1888 cells In13:[ADARB2-SYT6]1858 cells In12:[ADARB2-LAMP5-NDNF]1819 cells Microglia-Homeostatic-CX3CR11390 cells In8:[LHX6-SST-SEL1L3]1225 cells Ex15:[FEZF2-ADRA1A]1120 cells Oligodendrocyte-COL18A1750 cells Microglia-Reactive-AIF1352 cells In9:[LHX6-SST-NPY]337 cells Microglia-Reactive-CACNA1B328 cells 10x 3' v3, single nuclear230350 cells Drop-seq, single nuclear132305 cells 10x 3' v2, single nuclear61873 cells Alzheimer disease310773 cells prefrontal cortex, Brodmann (1909) area 9, B9288030 cells precuneus , Brodmann (1909) area 7, B772088 cells primary visual cortex, Brodmann (1909) area 17, B1764410 cells African American35877 cells Hispanic or Latin American4367 cells fresh-frozen, stored at −80°C424528 cells APOE class
Brain region
SORT
Braak stage
Disease group
Amyloid
Postmortem interval (hours)
Race
Age (years)
RNA integrity number
Age group
Postmortem interval group
RNA integrity number group
Major cell type
Cell type
NP diagonis
Assay
Disease
Sex
Tissue
Ethnicity
Sample preservation method
Leiden clustering
L4 clusters across brain region
Frontal Cx (BA9)182140 cells Primary Visual Cx (BA17)51520 cells Precuneous (BA7)49270 cells 10 to 15 hours66240 cells 15.2 to 19.5 hours62672 cells 5 to 9.3 hours50296 cells 1 to 4.5 hours47913 cells More than 20 hours45529 cells Ex1:[CUX2-SERPINE2-LAMP5]65152 cells Ex2:[CUX2-RORB-GLIS3-LRRC2]42034 cells Ex5:[RORB-CUX2-EYA4-LAMA3]27918 cells Ex12:[THEMIS-PRRX1]21756 cells Ex7:[RORB-GABRG1]21065 cells Ex9:[RORB-TLL1-PCP4-MID1]17264 cells Ex16:[FEZF2-SYT6]12579 cells Ex8:[RORB-TLL1-TMTC4]11805 cells Ex3:[CUX2-RORB-GLIS3-SV2C]10258 cells Ex10:[RORB-TLL1-PCP4-TYR]8436 cells Ex17:[FEZF2-ZFHX3-SEMA3D]8071 cells Ex11:[RORB-ADGRL4]6726 cells Ex4:[CUX2-RORB-COL5A2-CLMN]6316 cells Ex14:|FEZF2-HTR2C]6229 cells Ex13:[THEMIS-POSTN]5974 cells Ex18:[FEZF2-ZFHX3-SCUBE1]3193 cells Ex15:[FEZF2-ADRA1A]1120 cells 10x 3' v3, single nuclear146712 cells Drop-seq, single nuclear98040 cells 10x 3' v2, single nuclear38178 cells Alzheimer disease207990 cells prefrontal cortex, Brodmann (1909) area 9, B9182140 cells primary visual cortex, Brodmann (1909) area 17, B1751520 cells precuneus , Brodmann (1909) area 7, B749270 cells African American24969 cells Hispanic or Latin American3276 cells fresh-frozen, stored at −80°C282930 cells APOE class
Brain region
SORT
Braak stage
Disease group
Amyloid
Postmortem interval (hours)
Race
Age (years)
RNA integrity number
Age group
Postmortem interval group
RNA integrity number group
Major cell type
Cell type
NP diagonis
Assay
Disease
Sex
Tissue
Ethnicity
Sample preservation method
Leiden clustering
Frontal Cx (BA9)58379 cells Precuneous (BA7)13351 cells Primary Visual Cx (BA17)7564 cells 10 to 15 hours16864 cells 15.2 to 19.5 hours16539 cells 5 to 9.3 hours15994 cells 1 to 4.5 hours14760 cells More than 20 hours11923 cells In1:[LHX6-PVALB-CLMN]19009 cells In2:[LHX6-PVALB-MEPE]7465 cells In11:[ADARB2-LAMP5-KIT]7163 cells In6:[LHX6-SST-SLC9A2]5687 cells In10:[LHX6-ADARB2-LAMP5-HCRTR2]4232 cells In19:[ADARB2-CALB2-SCML4]4183 cells In17:[ADARB2-VIP-ABI3BP]4177 cells In18:[ADARB2-VIP-EXPH5]4131 cells In14:[ADARB2-SEMA3C]3074 cells In7:[LHX6-SST-B3GAT2]2982 cells In16:[ADARB2-VIP-TAC3-NRP1]2845 cells In4:[LHX6-SST-MSR1]2733 cells In5:[LHX6-SST-SPON1]2369 cells In3:[LHX6-PVALB-COL15A1]2117 cells In15:[ADARB2-VIP-DACH2]1888 cells In13:[ADARB2-SYT6]1858 cells In12:[ADARB2-LAMP5-NDNF]1819 cells In8:[LHX6-SST-SEL1L3]1225 cells In9:[LHX6-SST-NPY]337 cells 10x 3' v3, single nuclear44666 cells Drop-seq, single nuclear22397 cells 10x 3' v2, single nuclear12231 cells Alzheimer disease54479 cells prefrontal cortex, Brodmann (1909) area 9, B958379 cells precuneus , Brodmann (1909) area 7, B713351 cells primary visual cortex, Brodmann (1909) area 17, B177564 cells African American6871 cells Hispanic or Latin American785 cells fresh-frozen, stored at −80°C79294 cells