A neuronal MCT2 knockdown in the rat somatosensory cortex reduces both the NMR lactate signal and the BOLD response during whisker stimulation
Open accessAbstract
Although several in vitro and ex vivo evidence support the existence of lactate exchange between astrocytes and neurons, a direct demonstration in vivo is still lacking. In the present study, a lentiviral vector carrying a short hairpin RNA (shRNA) was used to downregulate the expression of the monocarboxylate transporter type 2 (MCT2) in neurons of the rat somatosensory cortex (called S1BF) by ~ 25%. After one hour of whisker stimulation, HRMAS 1H-NMR spectroscopy analysis of S1BF perchloric acid extracts showed that while an increase in lactate content is observed in both uninjected and shRNA-control injected extracts, such an effect was abrogated in shMCT2 injected rats. A 13C-incorporation analysis following [1-13C]glucose infusion during the stimulation confirmed that the elevated lactate observed during activation originates from newly synthesized [3-13C]lactate, with blood-derived [1-13C]glucose being the precursor. Moreover, the analysis of the 13C-labeling of glutamate in position C3 and C4 indicates that upon activation, there is an increase in TCA cycle velocity for control rats while a decrease is observed for MCT2 knockdown animals. Using in vivo localized 1H-NMR spectroscopy, an increase in lactate levels is observed in the S1BF area upon whisker stimulation for shRNA-control injected rats but not for MCT2 knockdown animals. Finally, while a robust BOLD fMRI response was evidenced in control rats, it was absent in MCT2 knockdown rats. These data not only demonstrate that glucose-derived lactate is locally produced following neuronal activation but also suggest that its use by neurons via MCT2 is probably essential to maintain synaptic activity within the barrel cortex.
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Multiple studies exhibit net production of lactate from glucose in activated brain, arguing that glycolysis without oxidative phosphorylation constitutes a component of the reduced OGI.
“Nevertheless, multiple studies exhibit net production of lactate from glucose in activated brain, arguing that glycolysis without oxphos constitutes a component of the reduced OGI (Korf and de Boer, 1990; Hu and Wilson, 1997; Mazuel et al., 2017).”
From Fueling thought: Management of glycolysis and oxidative phosphorylation in neuronal metabolism (2018) · cites this paper as Mazuel et al., 2017
Local brain lactate levels are elevated with stimulation.
“This is supported by measurements showing local elevation of brain lactate levels with stimulation (Korf and de Boer, 1990; Hu and Wilson, 1997; Mazuel et al., 2017) and even lactate export from the brain (e.g., Duffy et al., 1975, with stronger stimuli such as epileptic seizures).”
From Fueling thought: Management of glycolysis and oxidative phosphorylation in neuronal metabolism (2018) · cites this paper as Mazuel et al., 2017
Chronic disruption of MCT, LDH, or glycogenolysis in astrocytes can affect neuronal function.
“If an ANLS operates at rest, it could also explain why chronic disruption of MCT, LDH, or glycogenolysis in astrocytes can affect neuronal function (Suzuki et al., 2011; Zhang et al., 2016; Mazuel et al., 2017); these and similar results showing that MCT and lactate transport contribute to neuronal health and function provide evidence for some critical biological role for lactate uptake, but do”
From Fueling thought: Management of glycolysis and oxidative phosphorylation in neuronal metabolism (2018) · cites this paper as Mazuel et al., 2017
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“This is supported by measurements showing local elevation of brain lactate levels with stimulation (Korf and de Boer, 1990; Hu and Wilson, 1997; Mazuel et al., 2017) and even lactate export from the brain (e.”
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Mächler, P., Broggini, T., Matéo, C., Thunemann, M., Fomin-Thunemann, N., Doran, P. R., Şencan, İ., Kılıç, K., Desjardins, M., Uhlířová, H., et al. (2021) · Current Opinion in Biomedical Engineering · doi:10.1016/j.cobme.2021.100273 · Cited by 7 · see citing works
Resistance training boosts lactate transporters and synaptic proteins in insulin-resistance mice
Bian, X., Li, M., & Lou, S. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e34425 · Cited by 5 · see citing works
Outilaft, H., Bund, C., Piotto, M., & Namer, I. J. (2022) · Analytical Chemistry · doi:10.1021/acs.analchem.2c00214 · Cited by 4 · see citing works
Functional Magnetic Resonance Spectroscopy at 7 T in the Rat Barrel Cortex During Whisker Activation
Blanc, J., Roumes, H., Mazuel, L., Massot, P., Raffard, G., Biran, M., & Bouzier‐Sore, A. (2019) · Journal of Visualized Experiments · doi:10.3791/58912 · Cited by 4 · see citing works
Effet neuroprotecteur du lactate dans l’hypoxie-ischémie cérébrale néonatale
Roumes, H., Pellerin, L., & Bouzier‐Sore, A. (2020) · médecine/sciences · doi:10.1051/medsci/2020179 · Cited by 3 · see citing works
Hyppönen, V., Rosa, J., & Kettunen, M. I. (2024) · NMR in Biomedicine · doi:10.1002/nbm.5108 · Cited by 2 · see citing works
Disruption of Lactate Metabolism in the Peripheral Nervous System Leads to Motor‐Selective Deficits
Bloom, A. J., Tendulkar, S., Hackett, A. R., Strickland, A. M., Yamada, Y., Yuan, L., Dong, W., Ippolito, J. E., Schmidt, R. E., Sasaki, Y., et al. (2026) · Glia · doi:10.1002/glia.70245
- Authors
- Mazuel, L., Blanc, J., Repond, C., Bouchaud, V., Raffard, G., Déglon, N., Bonvento, G., Pellerin, L., & Bouzier-Sore, A.-K.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Centre Hospitalier Universitaire Vaudois (CH)
- Université Paris-Sud (FR)
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2017-04-07
- Volume
- 12
- Issue
- 4
- Pages
- e0174990
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC5384673
- OpenAlex
- W2605202107
- Cited by
- 44
- References
- 56
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 3 · 2022: 3 · 2021: 11 · 2020: 8 · 2019: 7 · 2018: 7 · 2017: 1
- FWCI
- 4.83
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- SERVAL (Université de Lausanne) (publishedVersion, other-oa)
- IRIS (submittedVersion)
- HAL (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Oskar-Bordeaux (Universite de Bordeaux) (submittedVersion)
- Funders
- Agence Nationale de la Recherche (ANR-10-LABX-57, ANR-15-CE37-0012)
- Fonds National Suisse (310030E-164271)
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Keywords
- MCT2, somatosensory cortex, whisker stimulation, barrel cortex, BOLD signal, 13C-labeled glucose, TCA cycle, synaptic activity, shRNA knockdown
- MeSH terms
- Animals, Female, Genetic Vectors, Magnetic Resonance Imaging, Neurons, Somatosensory Cortex, Vibrissae, Lentivirus, Rats, Wistar, Lactic Acid, Monocarboxylic Acid Transporters, Rats, Gene Knockdown Techniques, Carbon-13 Magnetic Resonance Spectroscopy, Proton Magnetic Resonance Spectroscopy
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