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Integrated Proteomics and Protein Co-expression Network Analysis Identifies Novel Epileptogenic Mechanism in Mesial Temporal Lobe Epilepsy

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Abstract

Over 50 million people worldwide are affected by epilepsy, a common neurological disorder that has a high rate of drug resistance and diverse comorbidities such as progressive cognitive and behavioural disorders, and increased mortality from direct or indirect effects of seizures and therapies. Despite extensive research with animal models and human studies, limited insights have been gained into the mechanisms underlying seizures and epileptogenesis, which has not translated into significant reductions in drug resistance, morbidities, or mortality. To better understand the molecular signaling networks associated with seizures in MTLE patients, we analyzed the proteome of brain samples from MTLE and control cases using an integrated approach that combines mass spectrometry-based quantitative proteomics, differential expression analysis, and co-expression network analysis. Our analyses of 20 human brain tissues from MTLE patients and 20 controls showed the organization of the brain proteome into a network of 9 biologically meaningful modules of co-expressed proteins. Of these, 6 modules are positively or negatively correlated to MTLE phenotypes with hub proteins that are altered in MTLE patients. Our study is the first to employ an integrated approach of proteomics and protein co-expression network analysis to study patients with MTLE. Our findings reveal a molecular blueprint of altered protein networks in MTLE brain and highlight dysregulated pathways and processes including altered cargo transport, neurotransmitter release from synaptic vesicles, synaptic plasticity, proteostasis, RNA homeostasis, ion transport and transmembrane transport, cytoskeleton disorganization, metabolic and mitochondrial dysfunction, blood micro-particle function, extracellular matrix organization, immune response, neuroinflammation, and cell signaling. These insights into MTLE pathogenesis suggest potential new candidates for future diagnostic and therapeutic development.

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Data Availability

The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD047201.

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Acknowledgements

The authors are indebted to all the patients and their family for participating in this study.

Funding

This work is funded by the MEG resource facility, funded by the Department of Biotechnology, Ministry of Science & Technology, Govt. of India (BT/MED/122/SP24580/2018), Faculty research program grant from the Institute of Eminence, University of Delhi, and MG grant from ACBR.

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Authors and Affiliations

  1. Department of Neurology, AIIMS, New Delhi, India

    Arpna Srivastava & Manjari Tripathi

  2. Dr B R Ambedkar Centre for Biomedical Research, University of Delhi, Delhi, India

    Priya Rajput & Aparna Banerjee Dixit

  3. Department of Neurosurgery, AIIMS, New Delhi, India

    Poodipedi Sarat Chandra & Ramesh Doddamani

  4. Department of Pathology, AIIMS, New Delhi, India

    Mehar Chand Sharma

  5. Department of Forensic Medicine & Toxicology, AIIMS, New Delhi, India

    Sanjeev Lalwani

  6. Department of Biophysics, AIIMS, New Delhi, India

    Jyotirmoy Banerjee

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  1. Arpna Srivastava
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  2. Priya Rajput
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Contributions

AS: conception and design; research, collection, and/or assembly of data; data analysis and interpretation; manuscript writing; and final approval of the manuscript. PR: conception and design; research, collection and/or assembly of data; and data analysis and interpretation. MT: conception and design; financial support; administrative support; manuscript writing; and final approval of the manuscript. PSC: conception and design; financial support; administrative support; provision of study material; and final approval of the manuscript. RD: data analysis and interpretation; manuscript writing; and final approval of the manuscript. MCS: histopathology of samples; data analysis and interpretation; and final approval of the manuscript. SL: conception and design; provision of study material (autopsy samples); and final approval of the manuscript. JB: conception and design; data analysis and interpretation; manuscript writing; and final approval of the manuscript. ABD: conception and design; financial support; administrative support; collection and/or assembly of data; data analysis and interpretation; manuscript writing; and final approval of the manuscript.

Corresponding authors

Correspondence to Jyotirmoy Banerjee or Aparna Banerjee Dixit.

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Ethics Approval

All studies were conducted in accordance with the Declaration of Helsinki and were approved by the Institute Ethics Committee, AIIMS, New Delhi & ACBR, University of Delhi (Ref. No. IEC-198/01.04.2016; ACBR/IHEC/AD-01/09–18).

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Informed and written consent was obtained from all patients, their parents, or legal representatives if patients were underage.

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Srivastava, A., Rajput, P., Tripathi, M. et al. Integrated Proteomics and Protein Co-expression Network Analysis Identifies Novel Epileptogenic Mechanism in Mesial Temporal Lobe Epilepsy. Mol Neurobiol (2024). https://doi.org/10.1007/s12035-024-04186-5

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