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Article

Single-Cell RNA-Seq Analysis of Olfactory Mucosal Cells of Alzheimer’s Disease Patients

by
Riikka Lampinen
1,†,
Mohammad Feroze Fazaludeen
1,†,
Simone Avesani
2,
Tiit Örd
1,
Elina Penttilä
3,
Juha-Matti Lehtola
4,5,
Toni Saari
4,
Sanna Hannonen
4,5,
Liudmila Saveleva
1,
Emma Kaartinen
1,
Francisco Fernández Acosta
1,
Marcela Cruz-Haces
1,
Heikki Löppönen
3,
Alan Mackay-Sim
6,
Minna U. Kaikkonen
1,
Anne M. Koivisto
4,5,7,
Tarja Malm
1,
Anthony R. White
8,
Rosalba Giugno
2,
Sweelin Chew
1 and
Katja M. Kanninen
1,*add Show full author list remove Hide full author list
1
A. I. Virtanen Institute for Molecular Sciences, University of Eastern Finland, 70210 Kuopio, Finland
2
Department of Computer Science, University of Verona, 37134 Verona, Italy
3
Department of Otorhinolaryngology, University of Eastern Finland, Kuopio University Hospital, 70210 Kuopio, Finland
4
Brain Research Unit, Department of Neurology, School of Medicine, University of Eastern Finland, 70210 Kuopio, Finland
5
Department of Neurology, Neuro Centre, Kuopio University Hospital, 70210 Kuopio, Finland
6
Griffith Institute for Drug Discovery, Griffith University, Nathan, QLD 4111, Australia
7
Department of Neurology and Geriatrics, Helsinki University Hospital and Neurosciences, Faculty of Medicine, University of Helsinki, 00014 Helsinki, Finland
8
Department of Cell and Molecular Biology, QIMR Berghofer, Medical Research Institute, Mental Health Program, Herston, QLD 4006, Australia
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Cells 2022, 11(4), 676; https://doi.org/10.3390/cells11040676
Submission received: 12 January 2022 / Revised: 10 February 2022 / Accepted: 11 February 2022 / Published: 15 February 2022
(This article belongs to the Special Issue Cellular and Molecular Mechanisms of Neurodegenerative Diseases)
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Abstract

Olfaction is orchestrated by olfactory mucosal cells located in the upper nasal cavity. Olfactory dysfunction manifests early in several neurodegenerative disorders including Alzheimer’s disease, however, disease-related alterations to the olfactory mucosal cells remain poorly described. The aim of this study was to evaluate the olfactory mucosa differences between cognitively healthy individuals and Alzheimer’s disease patients. We report increased amyloid-beta secretion in Alzheimer’s disease olfactory mucosal cells and detail cell-type-specific gene expression patterns, unveiling 240 differentially expressed disease-associated genes compared to the cognitively healthy controls, and five distinct cell populations. Overall, alterations of RNA and protein metabolism, inflammatory processes, and signal transduction were observed in multiple cell populations, suggesting their role in Alzheimer’s disease-related olfactory mucosa pathophysiology. Furthermore, the single-cell RNA-sequencing proposed alterations in gene expression of mitochondrially located genes in AD OM cells, which were verified by functional assays, demonstrating altered mitochondrial respiration and a reduction of ATP production. Our results reveal disease-related changes of olfactory mucosal cells in Alzheimer’s disease and demonstrate the utility of single-cell RNA sequencing data for investigating molecular and cellular mechanisms associated with the disease.
Keywords: Alzheimer’s disease; olfactory mucosa; amyloid beta; single-cell RNA-sequencing; mitochondria Alzheimer’s disease; olfactory mucosa; amyloid beta; single-cell RNA-sequencing; mitochondria
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MDPI and ACS Style

Lampinen, R.; Fazaludeen, M.F.; Avesani, S.; Örd, T.; Penttilä, E.; Lehtola, J.-M.; Saari, T.; Hannonen, S.; Saveleva, L.; Kaartinen, E.; et al. Single-Cell RNA-Seq Analysis of Olfactory Mucosal Cells of Alzheimer’s Disease Patients. Cells 2022, 11, 676. https://doi.org/10.3390/cells11040676

AMA Style

Lampinen R, Fazaludeen MF, Avesani S, Örd T, Penttilä E, Lehtola J-M, Saari T, Hannonen S, Saveleva L, Kaartinen E, et al. Single-Cell RNA-Seq Analysis of Olfactory Mucosal Cells of Alzheimer’s Disease Patients. Cells. 2022; 11(4):676. https://doi.org/10.3390/cells11040676

Chicago/Turabian Style

Lampinen, Riikka, Mohammad Feroze Fazaludeen, Simone Avesani, Tiit Örd, Elina Penttilä, Juha-Matti Lehtola, Toni Saari, Sanna Hannonen, Liudmila Saveleva, Emma Kaartinen, and et al. 2022. "Single-Cell RNA-Seq Analysis of Olfactory Mucosal Cells of Alzheimer’s Disease Patients" Cells 11, no. 4: 676. https://doi.org/10.3390/cells11040676

APA Style

Lampinen, R., Fazaludeen, M. F., Avesani, S., Örd, T., Penttilä, E., Lehtola, J.-M., Saari, T., Hannonen, S., Saveleva, L., Kaartinen, E., Fernández Acosta, F., Cruz-Haces, M., Löppönen, H., Mackay-Sim, A., Kaikkonen, M. U., Koivisto, A. M., Malm, T., White, A. R., Giugno, R., ... Kanninen, K. M. (2022). Single-Cell RNA-Seq Analysis of Olfactory Mucosal Cells of Alzheimer’s Disease Patients. Cells, 11(4), 676. https://doi.org/10.3390/cells11040676

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