Midbrain gene screening identifies a new mesoaccumbal glutamatergic pathway and a marker for dopamine cells neuroprotected in Parkinson's disease
Open accessAbstract
The ventral tegmental area (VTA) and substantia nigra pars compacta (SNc) of the midbrain are associated with Parkinson's disease (PD), schizophrenia, mood disorders and addiction. Based on the recently unraveled heterogeneity within the VTA and SNc, where glutamate, GABA and co-releasing neurons have been found to co-exist with the classical dopamine neurons, there is a compelling need for identification of gene expression patterns that represent this heterogeneity and that are of value for development of human therapies. Here, several unique gene expression patterns were identified in the mouse midbrain of which NeuroD6 and Grp were expressed within different dopaminergic subpopulations of the VTA, and TrpV1 within a small heterogeneous population. Optogenetics-coupled in vivo amperometry revealed a previously unknown glutamatergic mesoaccumbal pathway characterized by TrpV1-Cre-expression. Human GRP was strongly detected in non-melanized dopaminergic neurons within the SNc of both control and PD brains, suggesting GRP as a marker for neuroprotected neurons in PD. This study thus unravels markers for distinct subpopulations of neurons within the mouse and human midbrain, defines unique anatomical subregions within the VTA and exposes an entirely new glutamatergic pathway. Finally, both TRPV1 and GRP are implied in midbrain physiology of importance to neurological and neuropsychiatric disorders.
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Otx2+, Aldh1a1+ dopamine neurons are located in the ventromedial ventral tegmental area.
“Otx2+, Aldh1a1+ DA neurons in the ventromedial VTA”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [34]
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“Based on our identification of their expression in the newborn mouse (Viereckel et al., 2016), these markers were next selected for analysis at E11.”
BackgroundResultInfluentialBimpisidis, Z., König, N., Stagkourakis, S., Zell, V., Vlcek, B., Dumas, S., Giros, B., Broberger, C., Hnasko, T. S., & Wallén-Mackenzie, Å. (2019) · eNeuro · doi:10.1523/eneuro.0066-19.2019 · Cited by 36 · see citing works
“In contrast, another study found that photostimulation of Vglut2-Cre neurons in VTA induced modest real time place preference and self-stimulation (Wang et al., 2015).”
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“Although it had been identified in the periphery, evidence has accumulated suggesting its expression and function in the central nervous system, in various encephalic regions (Mezey et al., 2000; Kauer and Gibson, 2009; Viereckel et al., 2016).”
BackgroundConrad, W. S., Oriol, L., Kollman, G. J., Faget, L. C., & Hnasko, T. S. (2024) · Addiction Neuroscience · doi:10.1016/j.addicn.2024.100183 · Cited by 33 · see citing works
“Our findings also align well with scRNAseq studies that revealed an abundance of GABA and glutamate neurons, and identified subtypes of SNc and VTA neurons that go well beyond neurotransmitter markers [1,53,55,73,78].”
Kramer, D. J., Aisenberg, E. E., Kosillo, P., Friedmann, D., Stafford, D. A., Lee, A. Y.-F., Luo, L., Hockemeyer, D. F., Ngai, J., & Bateup, H. S. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109123 · Cited by 28 · see citing works
“Intersectional labeling of Neurod6-expressing DA neurons Previous studies have revealed that DA neurons are composed of genetically distinct subclasses (La Manno et al., 2016; Kramer et al., 2018; Hook et al., 2018; Poulin et al., 2014; Viereckel et al., 2016).”
Shiying, L., Qu, X., Guanghua, J., Feng, N., Liu, F., Shu-mei, C., & Hu, F. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.07.058 · Cited by 27 · see citing works
Mongrédien, R., Erdozain, A. M., Dumas, S., Cutando, L., Nuñez-delMoral, A., Puighermanal, E., Amin, S. R., Bruno Giros, A., Valjent, E., Meana, J. J., et al. (2019) · Brain Structure and Function · doi:10.1007/s00429-019-01831-x · Cited by 27 · see citing works
Olusakin, J., Moutkine, I., Dumas, S., Ponimaskin, E. G., Païzanis, E., Soiza‐Reilly, M., & Gaspar, P. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0775-z · Cited by 24 · see citing works
“Colorimetric ISH was carried out as described previously [32], using a 5-HTR7 DIG-labeled probe, phosphatase-coupled anti-DIG antibodies (1:1000), and developed with NBT/BCIP.”
MethodIdentification of hub genes and construction of diagnostic nomogram model in schizophrenia
Zhang, C., Dong, N., Xu, S., Ma, H., & Cheng, M. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.1032917 · Cited by 21 · see citing works
“NEUROD6 may also improve cellular resistance to oxidative stress, which is important in neurodegenerative illness prevention including Parkinson’s disease and autism spectrum disorder (Viereckel et al., 2016).”
BackgroundBimpisidis, Z., & Wallén‐Mackenzie, Å. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8111887 · Cited by 19 · see citing works
Spatial Transcriptome Profiling of Mouse Hippocampal Single Cell Microzone in Parkinson’s Disease
Jia, E., Sheng, Y., Shi, H., Wang, Y., Zhou, Y. Y., Liu, Z., Qi, T., Pan, M., Bai, Y., Zhao, X., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24031810 · Cited by 18 · see citing works
König, N., Bimpisidis, Z., Dumas, S., & Wallén‐Mackenzie, Å. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.578443 · Cited by 15 · see citing works
“In the midbrain dopamine system of rodents and primates, some, but far from all, dopamine neurons of the VTA and SNc are positive for Calb2 gene expression (Rogers, 1992; Isaacs and Jacobowitz, 1994; Mouatt-Prigent et al., 1994; Fortin and Parent, 1996; Liang et al., 1996; McRitchie et al., 1996; Nemoto et al., 1999;…”
BackgroundMethodInfluentialMidbrain Dopamine Neurons Defined by TrpV1 Modulate Psychomotor Behavior
Serra, G. P., Guillaumin, A., Dumas, S., Vlcek, B., & Wallén‐Mackenzie, Å. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.726893 · Cited by 15 · see citing works
Fujita, A., Zhong, L., Antony, M. S., Chamiec-Case, E., Mickelsen, L. E., Kanoski, S. E., Flynn, W. F., & Jackson, A. C. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2600-20.2021 · Cited by 14 · see citing works
Immenschuh, J., Thalhammer, S. B., Poromaa, I. S., Biegon, A. R., Dumas, S., & Comasco, E. (2023) · Biology of Sex Differences · doi:10.1186/s13293-023-00541-8 · Cited by 15 · see citing works
“Single FISH FISH was used to determine Cyp19a1-expressing cells, as described previously [18, 19].”
MethodViereckel, T., Konradsson‐Geuken, Å., & Wallén‐Mackenzie, Å. (2018) · Journal of Neurochemistry · doi:10.1111/jnc.14288 · Cited by 12 · see citing works
Chazalon, M., Dumas, S., Bernard, J., Sahly, I., Tronche, F., d’Exaerde, A. D. K., Hamon, M., Adrien, J., Fabre, V., & Bonnavion, P. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.06.014 · Cited by 12 · see citing works
Fakira, A. K., Peck, E. G., Liu, Y., Lueptow, L. M., Trimbake, N. A., Han, M., Calipari, E. S., & Devi, L. A. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107666 · Cited by 13 · see citing works
“Although this was unexpected based on the GPR83 ISH analysis in the Allen Brain Developing Mouse brain, it is supported by studies showing GPR83 expression in dopamine neurons using several methods including single-cell RNAseq analysis, laser capture microdissection and microarray analysis (Chung et al., 2005; Kramer…”
BackgroundMorishita, Y., Fuentes, I., González-Salinas, S., Favate, J. S., Mejaes, J. I., Zushida, K., Nishi, A., Hevi, C., Goldsmith, N., Buyske, S. G., et al. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02843-8 · Cited by 11 · see citing works
Butler, C. R., Boychuk, J. A., Pomerleau, F., Alcala, R., Huettl, P. F., Ai, Y., Jakobsson, J., Whiteheart, S. W., Gerhardt, G. A., Smith, B. N., et al. (2019) · Epilepsy Research · doi:10.1016/j.eplepsyres.2019.106244 · Cited by 9 · see citing works
Erdozain, A. M., Gois, S. D., Bernard, V., Gorgievski, V., Pietrancosta, N., Dumas, S., de Macedo, C. E. A., Vanhoutte, P., Ortega, J. E., Meana, J. J., et al. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.217 · Cited by 9 · see citing works
“Double Labeling Fluorescent In-Situ Hybridization Hybridization was performed as described (Viereckel et al, 2016).”
MethodJain, V., Behl, T., Sehgal, A., Singh, S., Sharma, N., Makeen, H. A., Albratty, M., Meraya, A. M., & Najmi, A. (2022) · Neurotoxicity Research · doi:10.1007/s12640-022-00619-y · Cited by 8 · see citing works
“Agonists and antagonists of the CB1 receptor have been suggested as potential therapies for this ailment, either alone or in tandem, with the goal of alleviating specific motor symptoms or halting the disease from progressing (Van der Stelt and Marzo 2003; Viereckel et al. 2016) (Fig.”
BackgroundTimonidis, N., Llera, A., & Tiesinga, P. H. E. (2021) · Neuroinformatics · doi:10.1007/s12021-021-09511-0 · Cited by 5 · see citing works
Recinto, S. J., Premachandran, S., Mukherjee, S., Allot, A., MacDonald, A., Yaqubi, M., Gruenheid, S., Trudeau, L., & Stratton, J. A. (2024) · European Journal of Neuroscience · doi:10.1111/ejn.16307 · Cited by 4 · see citing works
“This subtype also expressed genes found in disparate classes of CNS DA neurons, such as Grp , Sst , and Calcb (Kramer et al., 2018; La Manno et al., 2016; Poulin et al., 2014; Viereckel et al., 2016).”
BackgroundBimpisidis, Z., Serra, G. P., König, N., & Wallén‐Mackenzie, Å. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1069834 · Cited by 2 · see citing works
“org heterogeneity of DA neurons within the midbrain, in terms of gene expression, projection patterns and behavioral role (Chung et al., 2005; Greene et al., 2005; Lammel et al., 2008, 2011, 2012; Poulin et al., 2014, 2018; Viereckel et al., 2016; Bimpisidis et al., 2019; Heymann et al., 2020; König et al., 2020; Serr…”
BackgroundMethodInfluentialKoltun, M., Cichewicz, K., Gibbs, J. T., Darvas, M., & Hirsh, J. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/468330 · Cited by 2 · see citing works
Vlcek, B., Dumas, S., Ekmark‐Lewén, S., Rubino, E., Ingelsson, M., & Wallén‐Mackenzie, Å. (2023) · Exploration of Neuroprotective Therapy · doi:10.37349/ent.2023.00053 · Cited by 1 · see citing works
Impact of 5-Lipoxygenase Deficiency on Dopamine-Mediated Behavioral Responses
Issy, A. C., Pedrazzi, J. F. C., Nascimento, G. C., Faccioli, L. H., & Bel, E. A. D. (2024) · Neurotoxicity Research · doi:10.1007/s12640-024-00720-4 · Cited by 1 · see citing works
“These neurons co-express both dopamine and glutamate markers (Viereckel et al. 2016; Serra et al. 2021).”
Aisenberg, E. E., Li, T. L., Wang, H., Sahagun, A., Tu, E. M., & Bateup, H. S. (2025) · Nature Communications · doi:10.1038/s41467-025-64373-3 · Cited by 2 · see citing works
“GRP -expressing DA neurons have also been observed in post-mortem human brains and are suggested to be relatively resistant to degeneration in Parkinson ’ s disease 16 .”
The gastrin-releasing peptide regulates stress-enhanced fear and dopamine signalingPreprint
Morishita, Y., Fuentes, I., Favate, J. S., Zushida, K., Nishi, A., Hevi, C., Goldsmith, N. K., Buyske, S. G., Sillivan, S. E., Miller, C. A., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.31.424996 · Cited by 1 · see citing works
“Other work also showed that the Grp mRNA is a selective marker for dopaminergic subpopulations in the VTA and substantia nigra pars compacta (SNc) of the midbrain, both in mice and humans (Kramer, Risso, Kosillo, Ngai, & Bateup, 2018; Viereckel et al., 2016).”
BackgroundExploring the heterogeneity of the ventral tegmental area in Parkinson’s disease
McLeod, R. (2019) · KTH Publication Database DiVA (KTH Royal Institute of Technology)
Immenschuh, J., Thalhammer, S. B., Poromaa, I. S., Biegon, A., Dumas, S., & Comasco, E. (2023) · Figshare · doi:10.6084/m9.figshare.24076920
Régulation du sommeil et de l’anxiété par VGLUT3, le transporteur vésiculaire du glutamate de type 3
Henderson, F. (2019) · theses.fr (ABES) · doi:10.70675/72ea7d04ze3b3z4768zab1fz66b684e1ed22
- Authors
- Viereckel, T., Dumas, S., Smith-Anttila, C. J. A., Vlcek, B., Bimpisidis, Z., Lagerström, M. C., Konradsson-Geuken, Å., & Wallén-Mackenzie, Å.
- Affiliations
- Uppsala University (SE)
- Venue
- Scientific Reports
- Published
- 2016-10-20
- Volume
- 6
- Issue
- 1
- Pages
- 35203-35203
- ISSN
- 2045-2322 (ISSN-L)
- PMC
- PMC5071886
- OpenAlex
- W2533973296
- Cited by
- 45
- References
- 72
- Citations by year
- 2025: 1 · 2024: 4 · 2023: 6 · 2022: 3 · 2021: 6 · 2020: 4 · 2019: 10 · 2018: 9 · 2017: 2
- FWCI
- 5.26
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Scientific Reports (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Uppsala University Publications (Uppsala University) (submittedVersion, other-oa)
- Minerva Access (University of Melbourne) (submittedVersion, cc-by)
- Funders
- Hjärnfonden
- Karolinska Institutet
- Vetenskapsrådet (2013-04657, 2014-03804)
- Universidad Autónoma de San Luis Potosí
- Bertil Hållstens Forskningsstiftelse
- Uppsala Universitet
- Parkinsonfonden
- Topics
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- Parkinson's disease, midbrain, ventral tegmental area, substantia nigra pars compacta, dopaminergic neurons, NeuroD6, GRP, TRPV1, gene expression patterns, neuronal heterogeneity, neuroprotection, optogenetics, amperometry
- MeSH terms
- Animals, Dopamine, gamma-Aminobutyric Acid, Gene Expression Regulation, Humans, Mice, Transgenic, Nerve Tissue Proteins, Synaptic Transmission, Parkinson Disease, Ventral Tegmental Area, Glutamic Acid, Gastrin-Releasing Peptide, TRPV Cation Channels, Mice, Basic Helix-Loop-Helix Proteins, Dopaminergic Neurons, GABAergic Neurons, Optogenetics, Pars Compacta
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