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Key Genes in Olfactory Disorder in Experimental Autoimmune Encephalomyelitis Identified by Transcriptomic Analysis of the Olfactory Bulbs

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Abstract

Experimental autoimmune encephalomyelitis (EAE) is an animal model of multiple sclerosis that shows demyelination in the central nervous system and functional deficits, including olfactory impairment. However, the genes related to olfactory impairment in EAE are unknown. We evaluated hub genes of the olfactory bulb in EAE mice. Differentially expressed genes (cut-offs, fold change > 2 and adjusted p < 0.05) and their related pathways in olfactory bulbs were subjected to gene ontology (GO) pathway analysis, gene set enrichment analysis (GSEA). Protein-protein interactions with selected genes were evaluated using the Search Tool for the Retrieval of Interacting Genes/Proteins. Gene regulatory networks (GRNs) which were constructed at the post-transcriptional level, including the genes-transcription factors (TFs) and gene-microRNAs (miRNAs) interaction networks. Twelve hub genes were found, three of which (Ctss, Itgb2, and Tlr2) were validated by RT-qPCR to be related to GO pathways such as immune response and regulation of immune response. GSEA showed that neuron-related genes—including Atp6v1g2, Egr1, and Gap43—and their pathways were significantly downregulated. GRNs analysis of six genes (Ctss, Itgb2, Tlr2, Atp6v1g2, Egr1, and Gap43) revealed 37 TFs and 84 miRNAs were identified as potential regulators of six genes, indicating significant interaction among six genes, TFs, and miRNAs. Collectively, these results suggest that transcriptomic analysis of the olfactory bulb of EAE mice can provide insight into olfactory dysfunction and reveal therapeutic targets for olfactory impairment.

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Data Availability

Data will be made available on request.

Abbreviations

BP:

Biological process

CC:

Cellular component

cDNA:

Complementary deoxyribonucleic acid

CNS:

Central nervous system

DEG:

Differentially expressed gene

EAE:

Experimental autoimmune encephalomyelitis

FDR:

False discovery rate

GAPDH:

Glyceraldehyde 3-phosphate dehydrogenase

GO:

Gene ontology

GSEA:

Gene set enrichment analysis

Iba1:

Ionized calcium-binding adapter molecule 1

KEGG:

Kyoto encyclopedia of genes and genomes

MCC:

Maximal clique centrality

MF:

Molecular function

MHC:

Major histocompatibility complex

MNC:

Maximum neighborhood component

MOG:

Myelin oligodendrocyte glycoprotein

MS:

Multiple sclerosis

MSigDB:

Molecular signatures database

NOM:

Nominal

PC:

Principal component

PCA:

Principal component analysis

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Author Contributions

Conceptualization, T.S. and C.M.; methodology, J.K., K.J., and M.A.; investigation, T.S., S.H., and J.K.; writing—original draft, S.H.; writing—review and editing, C.M., C.A., and P.S.Q.; funding acquisition, T.S.

Funding

This research was supported by the 2024 scientific promotion program funded by Jeju National University. The funders had no role in the design, analysis, write-up, or decision to submit for publication.

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Authors and Affiliations

  1. College of Veterinary Medicine and Veterinary Medical Research Institute, Jeju National University, 102 Jejudaehakno, Jeju, 63243, Republic of Korea

    Sungmoo Hong, Changhwan Ahn & Taekyun Shin

  2. Department of Anatomy, Kosin University College of Medicine, Busan, 49267, Republic of Korea

    Jeongtae Kim

  3. Department of Animal Science, College of Life Science, Sangji University, Wonju, 26339, Republic of Korea

    Meejung Ahn

  4. Functional Biomaterials Research Center, Korea Research Institute of Bioscience and Biotechnology, Jeongeup, 56212, Republic of Korea

    Kyungsook Jung

  5. Department of Veterinary Anatomy and Animal Behavior, College of Veterinary Medicine and BK21 Plus Project Team, Chonnam National University, Gwangju, 61186, Republic of Korea

    Changjong Moon

  6. Department of Anatomy, Animal Production and Clinical Veterinary Sciences, Faculty of Veterinary, University of Santiago de Compostela, Lugo, Spain

    Pablo Sanchez-Quinteiro

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  1. Sungmoo Hong
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Correspondence to Taekyun Shin.

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All experimental procedures were conducted in accordance with the Guidelines for the Care and Use of Laboratory Animals of Jeju National University (Nos. 2017-0019, 2022-0062). The animal protocols also conformed to the National Institutes of Health Guide for the Care and Use of Laboratory Animals (No. 85-23; 1985, rev. 1996).

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Hong, S., Kim, J., Ahn, M. et al. Key Genes in Olfactory Disorder in Experimental Autoimmune Encephalomyelitis Identified by Transcriptomic Analysis of the Olfactory Bulbs. Mol Neurobiol (2024). https://doi.org/10.1007/s12035-024-03923-0

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