Central presynaptic terminals are enriched in ATP but the majority lack mitochondria
Open accessAbstract
Synaptic neurotransmission is known to be an energy demanding process. At the presynapse, ATP is required for loading neurotransmitters into synaptic vesicles, for priming synaptic vesicles before release, and as a substrate for various kinases and ATPases. Although it is assumed that presynaptic sites usually harbor local mitochondria, which may serve as energy powerhouse to generate ATP as well as a presynaptic calcium depot, a clear role of presynaptic mitochondria in biochemical functioning of the presynapse is not well-defined. Besides a few synaptic subtypes like the mossy fibers and the Calyx of Held, most central presynaptic sites are either en passant or tiny axonal terminals that have little space to accommodate a large mitochondrion. Here, we have used imaging studies to demonstrate that mitochondrial antigens poorly co-localize with the synaptic vesicle clusters and active zone marker in the cerebral cortex, hippocampus and the cerebellum. Confocal imaging analysis on neuronal cultures revealed that most neuronal mitochondria are either somatic or distributed in the proximal part of major dendrites. A large number of synapses in culture are devoid of any mitochondria. Electron micrographs from neuronal cultures further confirm our finding that the majority of presynapses may not harbor resident mitochondria. We corroborated our ultrastructural findings using serial block face scanning electron microscopy (SBFSEM) and found that more than 60% of the presynaptic terminals lacked discernible mitochondria in the wild-type mice hippocampus. Biochemical fractionation of crude synaptosomes into mitochondria and pure synaptosomes also revealed a sparse presence of mitochondrial antigen at the presynaptic boutons. Despite a low abundance of mitochondria, the synaptosomal membranes were found to be highly enriched in ATP suggesting that the presynapse may possess alternative mechanism/s for concentrating ATP for its function. The potential mechanisms including local glycolysis and the possible roles of ATP-binding synaptic proteins such as synapsins, are discussed.
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Many synaptic sites in brain lack mitochondria.
“Many synaptic sites in brain have been shown to lack mitochondria (Chavan et al., 2015)”
From Fueling thought: Management of glycolysis and oxidative phosphorylation in neuronal metabolism (2018) · cites this paper as Chavan et al., 2015
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Riboul, D. V., Crill, S., Oliva, C. D., Restifo, M. G., Joseph, R., Joseph, K., Nguyen, K. C. Q., Hall, D. H., Fily, Y., & Macleod, G. T. (2024) · The Journal of Comparative Neurology · doi:10.1002/cne.70002 · Cited by 2 · see citing works
Correction: Central Presynaptic Terminals Are Enriched in ATP but the Majority Lack Mitochondria
Chavan, V., Willis, J., Walker, S. K., Clark, H. R., Liu, X., Fox, M. A., Srivastava, S., & Mukherjee, K. (2017) · PLoS ONE · doi:10.1371/journal.pone.0181140 · Cited by 2 · see citing works
Self-citationIn situ proximity labeling reveals the proteome and signaling landscape of presynaptic boutons
Nakazawa, K., Taoufiq, Z., Kakuda, N., Goda, Y., & Takamori, S. (2026) · Neuroscience Research · doi:10.1016/j.neures.2026.105070 · Cited by 1 · see citing works
Bioenergetic signature of Synaptic mitochondriaPreprint
Faria‐Pereira, A., & Morais, V. A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.28.625855 · Cited by 1 · see citing works
Mitochondrial adaptation at the neuronal presynapse
Lange, F. (2021) · doi:10.53846/goediss-8959
The Dynamic Organization of Proteins in the Synaptic Bouton
Reshetniak, S. (2022) · doi:10.53846/goediss-9435
Santos‐Silva, T. (2023) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.17.2023.tde-10112023-160657
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- Authors
- Chavan, V., Willis, J., Walker, S. K., Clark, H. R., Liu, X., Fox, M. A., Srivastava, S., & Mukherjee, K.
- Affiliations
- Virginia Tech (US)
- Yale University (US)
- Corresponding author
- Srivastava, Sarika
- Mukherjee, Konark
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2015-04-30
- Volume
- 10
- Issue
- 4
- Pages
- e0125185
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC4416033
- OpenAlex
- W2157007777
- Cited by
- 52
- References
- 56
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 5 · 2023: 4 · 2022: 3 · 2021: 3 · 2020: 3 · 2019: 4 · 2018: 9 · 2017: 10 · 2016: 7 · 2015: 2
- FWCI
- 4.35
- Type
- journal article
- Language
- en
- Update notices
- correction (2017-07-10)
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- VTechWorks (Virginia Tech) (submittedVersion, cc-by)
- Funders
- National Eye Institute (R01EY021222)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Keywords
- presynaptic terminals, ATP, presynaptic mitochondria, synaptic vesicles, synaptosomes, synaptic ultrastructure, synapsin, hippocampus, cerebral cortex, cerebellum, neuronal culture
- MeSH terms
- Adenosine Triphosphate, Animals, Cells, Cultured, Mice, Inbred C57BL, Microscopy, Electron, Scanning, Mitochondria, Synaptosomes, Presynaptic Terminals, Mice
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