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Decoding transcriptomic signatures of cysteine string protein alpha-mediated synapse maintenance.

Na Wang^1,2, Biqing Zhu^3,4, Mary Alice Allnutt^1,2,5

¹Department of Neurology, Yale University, New Haven, CT 06510.

Proceedings of the National Academy of Sciences of the United States of America

|June 4, 2024

Summary

Synapse maintenance is crucial for brain function and neuroprotection. This study reveals how Cysteine string protein alpha (CSPα) deficiency impacts gene expression and cell communication, offering insights into neurodegenerative disease mechanisms.

Keywords:

Neurexin1–Neuroligin 1 autophagosome chaperone synapse loss

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Area of Science:

Neuroscience
Molecular Biology
Genetics

Background:

Synapse maintenance is vital for neural circuit function and is impaired in neurodegenerative diseases.
Cysteine string protein alpha (CSPα), a synaptic vesicle chaperone, is essential for synapse maintenance and implicated in neurodegeneration.
Understanding in vivo synapse maintenance mechanisms, particularly transcriptional changes, remains limited.

Purpose of the Study:

To investigate the transcriptional alterations in the brain associated with impaired synapse maintenance.
To elucidate the roles of neurons and glial cells in response to CSPα deficiency.
To identify molecular mechanisms underlying synapse maintenance and neurodegeneration.

Main Methods:

Single-nucleus RNA sequencing (snRNA-seq) was performed on the cortex of young CSPα knockout (KO) mice and controls.
Differential gene expression and gene ontology analyses were conducted to identify transcriptional signatures.
Electron microscopy was used to visualize synapses and autophagosomes.
Cell-cell interaction analysis was employed to infer communication patterns.

Main Results:

CSPα KO brains showed distinct transcriptional signatures in both neuronal and glial cells.
Neurons exhibited repression of synaptic pathways and upregulation of autophagy-related genes.
Electron microscopy confirmed alterations in synapses and increased autophagosomes, particularly at inhibitory synapses.
Microglia showed signs of activation, and neuron-glia interactions, mediated by synaptogenic adhesion molecules like Neurexin1-Neuroligin 1, were increased.

Conclusions:

CSPα deficiency leads to significant transcriptional changes in neurons and glia, impacting synaptic pathways and autophagy.
Enhanced neuron-glia communication, potentially as a compensatory mechanism, is observed in CSPα KO mice.
This study provides a comprehensive dataset of transcriptional changes and sheds light on the molecular underpinnings of synapse maintenance and neurodegeneration.