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Lineage tracing and differential expression analysis of single nuclei RNA-sequencing data from human neocortex identifies novel genes and pathways involved in progression of Alzheimer’s disease

Anatoly Buchin

Cajal Neuroscience, Human Multi-Omics Team

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GWAS provides information about AD risk genes

Bellenguez et al 2022

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What happens during the course of disease development?

Goedert et al 2015

A-beta and tau have a stereotypical progression

A-beta

Tau

Extract hidden structure in gene expression data

Correlation with

Braak stage,

Thal phase,

Cognitive decline

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Human cortical data

Tissue processing

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Analysis of snRNA-seq data of patients with different stages of disease development evaluated by Braak score

1.2 M cells

84 donors

Middle Temporal Gyrus (MTG)

MTG

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Pseudotime analysis of gene expression: single nuclei RNA-seq

Haghverdi et al 2016

Pseudotime

gene x

gene y

gene z

Braak stage

Correlation

Start: healthy

End: diseased

Hidden structure

Cetti et al 2019

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Transcripts correlated with pseudotime: microglia PVM-1

Upregulated genes

Pseudotime

Trajectory

start

corr 0.51

pval 7.014 E-107

corr -0.39

pval 8.24 E-60

Correlation

(pseudotime, expression)

COLEC12

F13A1

Down-regulated genes

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Analysis of microglial subclusters

Microglia subclusters

Braak stage

Microglia-PVM_1

Pseudotime

Braak stage

Trajectory

start

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Analysis of microglial subclusters

Microglia subclusters

Braak stage

Microglia-PVM_1

Pseudotime

Trajectory

start

Micro-PVM_1 corr 0.173 pval 0.0

Micro-PVM_1_1 corr 0.217 pval 0.0

Micro-PVM_2 corr 0.169 pval 0.0

Micro-PVM_2_1 corr 0.154 pval 0.009

Micro-PVM_2_2 corr 0.105 pval 0.002

Micro-PVM_2_3 corr 0.15 pval 0.0

Micro-PVM_3 corr 0.227 pval 0.0

Micro-PVM_4 corr 0.566 pval 0.0

Braak stage and pseudotime correlations

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Enrichment analysis of microglia

Enrichment terms

Microglia subtypes

Upregulated genes

Replication pathways

Immune pathways

Response to bacterium: PDE4B, AHR, IL10RA, IL15, C3, IL7R, IL15, … (155 genes)

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Analysis of astrocyte subclusters

Pseudotime

Braak stage

Astrocyte subclusters

Braak stage

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Analysis of astrocyte subclusters

Braak stage and pseudotime correlations

Astro_1 corr 0.11 pval 0.0

Astro_2 corr 0.16 pval 0.0

Astro_3 corr 0.12 pval 0.0

Astro_4 corr 0.55 pval 0.0

Astro_5 corr 0.10 pval 0.0

Astro_6 corr 0.12 pval 0.0

Pseudotime

Astrocyte subclusters

Braak stage

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Enrichment analysis of astrocytes

Enrichment terms

Astrocyte subtypes

Downregulated genes

Cholesterol / Translation pathways

Synaptic

pathways

Cellular respiration

pathways

Cholesterol pathway: GPAM, APOE, PGP, ALOX12, ACSS1, ACOT2, CYP4V2, … (46 genes)

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Pathways affected by Alzheimer’s disease

Murdock and Tsai 2022

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Conclusions

  • Trajectory inference methods allow to extract disease-relevant cell-type specific changes in cells transcriptome state during the course of disease progression

  • Microglia 3 subpopulation shows an activation of immune pathways and bacterial infection pathways in later Braak stages

  • Astrocytes 5 subpopulation has decreased APOE transcript levels in later Braak stages.

Trajectory

start

Microglia

Astrocytes

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Plan for the presentation

-Problem statement: many different genes affect idiopathic Alzheimer’s disease (Bellenguez graph). How could we go from genes to cellular mechanisms?

-Recent work on single cell identified many different genes involved in disease development

-Disease development: Tau staging by Braak and brain regions. Figure from paper

-Novel method of gene expression analysis: general method idea

-Analysis of cortical data: more about MTG dataset

-Analysis of excitatory cells, inhibitory cells, microglia, astrocytes. More about MTG, then ETX, SFG and PFC

-On the analysis of specific pathway: show the specific cell type

-Common pathways across cortical areas and cell types. Microglia, Oligodendrocytes

-

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The logic behind pseudotime analysis

Neurons

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Pseudotime analysis of gene expression: single nuclei RNA-seq

Cells

Braak score

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Enrichment analysis of microglia

Enrichment terms

Microglia subtypes

Downregulated genes

Immune pathways 1

Immune pathways 2

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Analysis of excitatory subclusters

Excitatory subclusters

Braak stage

Pseudotime

Braak stage

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Analysis of excitatory subclusters

Excitatory subclusters

Braak stage

Pseudotime

L2/3 IT_1 corr 0.143 pval 0.0

L2/3 IT_10 corr 0.296 pval 0.0

L2/3 IT_12 corr 0.323 pval 0.0

L2/3 IT_13 corr 0.28 pval 0.0

L2/3 IT_2 corr 0.146 pval 0.0

L2/3 IT_3 corr 0.274 pval 0.0

L2/3 IT_5 corr 0.175 pval 0.0

L2/3 IT_6 corr 0.189 pval 0.0

L2/3 IT_7 corr 0.27 pval 0.0

L2/3 IT_8 corr 0.264 pval 0.0

Braak stage and pseudotime correlations

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Enrichment analysis of excitatory cells

Enrichment terms

Excitatory subtypes

Upregulated genes

Stress / ubiquitin / viral pathways

Mitochondrial / synapse pathways

Neuron projection: NTNG1, PTPRD, GRIN2B, APP, NRG3, ZNF804A, … (151 gene)