Differential presynaptic ATP supply for basal and high-demand transmission
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The relative contributions of glycolysis and oxidative phosphorylation to neuronal presynaptic energy demands are unclear. In rat hippocampal neurons, ATP production by either glycolysis or oxidative phosphorylation alone sustained basal evoked synaptic transmission for up to 20 min. However, combined inhibition of both ATP sources abolished evoked transmission. Neither action potential propagation failure nor depressed Ca 2+ influx explained loss of evoked synaptic transmission. Rather, inhibition of ATP synthesis caused massive spontaneous vesicle exocytosis, followed by arrested endocytosis, accounting for the disappearance of evoked postsynaptic currents. In contrast to its weak effects on basal transmission, inhibition of oxidative phosphorylation alone depressed recovery from vesicle depletion. Local astrocytic lactate shuttling was not required. Instead, either ambient monocarboxylates or neuronal glycolysis was sufficient to supply requisite substrate. In summary, basal transmission can be sustained by glycolysis, but strong presynaptic demands are met preferentially by oxidative phosphorylation, which can be maintained by bulk but not local monocarboxylates or by neuronal glycolysis. SIGNIFICANCE STATEMENT Neuronal energy levels are critical for proper CNS function, but the relative roles for the two main sources of ATP production, glycolysis and oxidative phosphorylation, in fueling presynaptic function in unclear. Either glycolysis or oxidative phosphorylation can fuel low-frequency synaptic function and inhibiting both underlies loss of synaptic transmission via massive vesicle release and subsequent failure to endocytose lost vesicles. Oxidative phosphorylation, fueled by either glycolysis or endogenously released monocarboxylates, can fuel more metabolically demanding tasks such as vesicle recovery after depletion. Our work demonstrates the flexible nature of fueling presynaptic function to maintain synaptic function.
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In presynaptic terminals, both glycolysis and oxphos appear important for managing intense activity.
“In presynaptic terminals, both glycolysis and oxphos appear important for managing intense activity (Rangaraju et al., 2014; Sobieski et al., 2017).”
From Fueling thought: Management of glycolysis and oxidative phosphorylation in neuronal metabolism (2018) · cites this paper as Sobieski et al., 2017
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Cites
Interplay between Cortical Spreading Depolarization and Seizures
Kramer, D. R., Fujii, T., Ohiorhenuan, I. E., & Liu, C. Y. (2017) · Stereotactic and Functional Neurosurgery · doi:10.1159/000452841 · Cited by 3,718 · see citing works
An Energy Budget for Signaling in the Grey Matter of the Brain
Attwell, D., & Laughlin, S. B. (2001) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-200110000-00001 · Cited by 3,543 · see citing works
Pellerin, L., & Magistretti, P. J. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.22.10625 · Cited by 2,927 · cited 2× · see citing works
“The importance of oxidative phosphorylation for EPSC recovery after a strong presynaptic stimulus could implicate the astrocyte–neuron lactate shuttle (Pellerin and Magistretti, 1994; Takahashi et al., 1995; Bittner et al., 2010).”
BackgroundSynaptic Energy Use and Supply
Harris, J. J., Jolivet, R., & Attwell, D. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.019 · Cited by 1,747 · see citing works
Cooperation and Competition in the Evolution of ATP-Producing Pathways
Pfeiffer, T., Schuster, S., & Bonhoeffer, S. (2001) · Science · doi:10.1126/science.1058079 · Cited by 1,365 · see citing works
Definition of the readily releasable pool of vesicles at hippocampal synapses.
Rosenmund, C., & Stevens, C. (1996) · Neuron · doi:10.1016/s0896-6273(00)80146-4 · Cited by 1,084 · see citing works
Verstreken, P., Ly, C. V., Venken, K. J. T., Koh, T.-W., Zhou, Y., & Bellen, H. J. (2005) · Neuron · doi:10.1016/j.neuron.2005.06.018 · Cited by 841 · see citing works
Activity-driven local ATP synthesis is required for synaptic function
Rangaraju, V., Calloway, N., & Ryan, T. A. (2014) · Cell · doi:10.1016/j.cell.2013.12.042 · Cited by 836 · see citing works
Pellerin, L., & Magistretti, P. J. (2011) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2011.149 · Cited by 726 · see citing works
Kang, J.-S., Tian, J.-H., Pan, P.-Y., Zald, P., Li, C., Deng, C., & Sheng, Z.-H. (2008) · Cell · doi:10.1016/j.cell.2007.11.024 · Cited by 598 · see citing works
Lactate-supported synaptic function in the rat hippocampal slice preparation.
Schurr, A., West, C. A., & Rigor, B. (1988) · Science · doi:10.1126/science.3375817 · Cited by 594 · see citing works
Bekkers, J. M., & Stevens, C. F. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.17.7834 · Cited by 568 · see citing works
Hall, C. N., Klein-Flugge, M. C., Howarth, C., & Attwell, D. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0026-12.2012 · Cited by 451 · see citing works
In Vivo Evidence for Lactate as a Neuronal Energy Source
Wyss, M. T., Jolivet, R., Buck, A., Magistretti, P. J., & Weber, B. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0415-11.2011 · Cited by 438 · see citing works
The glutamate‐glutamine cycle is not stoichiometric: Fates of glutamate in brain
McKenna, M. C. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21444 · Cited by 385 · see citing works
Edmond, J., Robbins, R., Bergstrom, J. D., Cole, R. A., & de Vellis, J. (1987) · Journal of Neuroscience Research · doi:10.1002/jnr.490180407 · Cited by 357 · see citing works
Lactate-mediated glia-neuronal signalling in the mammalian brain
Tang, F., Lane, S., KORSAK, A. S., Paton, J. F. R., Gourine, A. V., Kasparov, S., & Teschemacher, A. G. (2014) · Nature Communications · doi:10.1038/ncomms4284 · Cited by 340 · see citing works
The Role of Mitochondrially Derived ATP in Synaptic Vesicle Recycling
Pathak, D., Shields, L. Y., Mendelsohn, B. A., Haddad, D., Lin, W., Gerencser, A. A., Kim, H., Brand, M. D., Edwards, R. H., & Nakamura, K. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.656405 · Cited by 311 · see citing works
Schurr, A., Miller, J. J., Payne, R. S., & Rigor, B. M. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-01-00034.1999 · Cited by 295 · see citing works
The relative metabolic demand of inhibition and excitation
Waldvogel, D., van Gelderen, P., Muellbacher, W., Ziemann, U., Immisch, I., & Hallett, M. (2000) · Nature · doi:10.1038/35023171 · Cited by 271 · see citing works
Glycolytic enzymes localize to synapses under energy stress to support synaptic function
Jang, S., Nelson, J. C., Bend, E. G., Rodríguez-Laureano, L., Tueros, F. G., Cartagenova, L., Underwood, K., Jorgensen, E. M., & Colón-Ramos, D. A. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.011 · Cited by 270 · see citing works
Motile axonal mitochondria contribute to the variability of presynaptic strength
Sun, T., Qiao, H., Pan, P.-Y., Chen, Y., & Sheng, Z.-H. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.06.040 · Cited by 263 · see citing works
Fatty Acid Oxidation and Ketogenesis by Astrocytes in Primary Culture
Auestad, N., Korsak, R. A., Morrow, J. W., & Edmond, J. (1991) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1991.tb11435.x · Cited by 245 · see citing works
Choi, H. B., Gordon, G. R., Zhou, N., Tai, C., Rungta, R. L., Martinez, J., Milner, T. A., Ryu, J. K., McLarnon, J. G., Tresguerres, M., et al. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.032 · Cited by 242 · see citing works
Lipton, P., & Whittingham, T. S. (1982) · The Journal of Physiology · doi:10.1113/jphysiol.1982.sp014135 · Cited by 208 · see citing works
Gallagher, C., Carpenter, K. L. H., Grice, P., Howe, D. J., Mason, A., Timofeev, I. S., Menon, D. K., Kirkpatrick, P. J., Pickard, J. D., Sutherland, G. R., et al. (2009) · Brain · doi:10.1093/brain/awp202 · Cited by 201 · see citing works
Glycolysis and Glutamate Accumulation into Synaptic Vesicles
Ikemoto, A., Bole, D. G., & Ueda, T. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211617200 · Cited by 193 · see citing works
Role of sodium and potassium ions in regulation of glucose metabolism in cultured astroglia.
Takahashi, S., Driscoll, B. F., Law, M. J., & Sokoloff, L. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.10.4616 · Cited by 184 · see citing works
Chatton, J., Pellerin, L., & Magistretti, P. J. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2132096100 · Cited by 180 · see citing works
Mennerick, S. J., & Zorumski, C. F. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp020948 · Cited by 171 · see citing works
Self-citationIzumi, Y., Benz, A. M., Katsuki, H., & Zorumski, C. F. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-24-09448.1997 · Cited by 166 · see citing works
Chung, C., Baryłko, B., Leitz, J., Liu, X., & Kavalali, E. T. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3427-09.2010 · Cited by 154 · see citing works
High resolution measurement of the glycolytic rate
Bittner, C. X. (2010) · Frontiers in Neuroenergetics · doi:10.3389/fnene.2010.00026 · Cited by 151 · see citing works
Sara, Y., Mozhayeva, M. G., Liu, X., & Kavalali, E. T. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-05-01608.2002 · Cited by 133 · see citing works
Effects of lactate and pyruvate on glucose deprivation in rat hippocampal slices
Izumi, Y., Benz, A. M., Zorumski, C. F., & Olney, J. W. (1994) · Neuroreport · doi:10.1097/00001756-199401000-00021 · Cited by 132 · see citing works
Allen, N. J., Rossi, D. J., & Attwell, D. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5539-03.2004 · Cited by 129 · see citing works
Energy metabolism in glutamatergic neurons, GABAergic neurons and astrocytes in primary cultures
Hertz, L., Drejer, J., & Schousboe, A. (1988) · Neurochemical Research · doi:10.1007/bf00973275 · Cited by 126 · see citing works
Erlichman, J. S., Hewitt, A. J., Damon, T., Hart, M. P., Kurascz, J., Li, A., & Leiter, J. C. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5430-07.2008 · Cited by 121 · see citing works
Selective Depression of Low–Release Probability Excitatory Synapses by Sodium Channel Blockers
Prakriya, M., & Mennerick, S. J. (2000) · Neuron · doi:10.1016/s0896-6273(00)81203-9 · Cited by 108 · see citing works
Self-citationMeeks, J. P., & Mennerick, S. J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4845-03.2004 · Cited by 102 · see citing works
Self-citationIzumi, Y., Ishii, K., Katsuki, H., Benz, A. M., & Zorumski, C. F. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1009 · Cited by 95 · see citing works
Association of glycolytic enzymes with particulate fractions from nerve endings
Knull, H. R. (1978) · Biochimica et Biophysica Acta (BBA) - Enzymology · doi:10.1016/0005-2744(78)90316-9 · Cited by 92 · see citing works
Rapid manifestation of reactive astrogliosis in acute hippocampal brain slices
Takano, T., He, W. J., Han, X., Wang, F., Xu, Q., Wang, X., Bush, N. A. O., Cruz, N. F., Dienel, G. A., & Nedergaard, M. (2013) · Glia · doi:10.1002/glia.22588 · Cited by 88 · see citing works
Molecular Underpinnings of Synaptic Vesicle Pool Heterogeneity
Crawford, D. C., & Kavalali, E. T. (2015) · Traffic · doi:10.1111/tra.12262 · Cited by 84 · see citing works
McKenna, M. C. (2012) · Neurochemical Research · doi:10.1007/s11064-012-0901-3 · Cited by 84 · see citing works
Controlling synaptotagmin activity by electrostatic screening
Park, Y., Hernández, J. M., van den Bogaart, G., Ahmed, S., Holt, M., Riedel, D., & Jahn, R. (2012) · Nature Structural &Molecular Biology · doi:10.1038/nsmb.2375 · Cited by 79 · see citing works
Fujimoto, S., Katsuki, H., Kume, T., Kaneko, S., & Akaike, A. (2004) · Neuroscience Research · doi:10.1016/j.neures.2004.06.013 · Cited by 68 · see citing works
Roles and Regulation of Ketogenesis in Cultured Astroglia and Neurons Under Hypoxia and Hypoglycemia
Takahashi, S., Iizumi, T., Mashima, K., Abe, T., & Suzuki, N. (2014) · ASN NEURO · doi:10.1177/1759091414550997 · Cited by 65 · see citing works
Vesicle Pool Heterogeneity at Hippocampal Glutamate and GABA Synapses
Moulder, K. L., Jiang, X., Taylor, A., Shin, W., Gillis, K. D., & Mennerick, S. J. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2803-07.2007 · Cited by 60 · see citing works
Self-citationMRS study of glutamate metabolism in cultured neurons/glia
Sonnewald, U., White, L. R., Ødegård, E., Westergaard, N., Bakken, I. J., Aasly, J. O., Unsgård, G., & Schousboe, A. (1996) · Neurochemical Research · doi:10.1007/bf02532408 · Cited by 58 · see citing works
Glycolysis selectively shapes the presynaptic action potential waveform
Lujan, B., Kushmerick, C., Banerjee, T. D., Dagda, R. K., & Renden, R. (2016) · Journal of Neurophysiology · doi:10.1152/jn.00629.2016 · Cited by 56 · see citing works
Ivanov, A., Mukhtarov, M. R., Bregestovski, P. D., & Zilberter, Y. (2011) · Frontiers in Neuroenergetics · doi:10.3389/fnene.2011.00002 · Cited by 55 · see citing works
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. (2015) · PLoS ONE · doi:10.1371/journal.pone.0125185 · Cited by 52 · see citing works
Comparison of glucose and lactate as substrates during NMDA-induced activation of hippocampal slices
Chih, C.-P., He, J., Sly, T. S., & Roberts, E. L. (2001) · Brain Research · doi:10.1016/s0006-8993(00)03306-0 · Cited by 30 · see citing works
Sobieski, C. A., Jiang, X., Crawford, D. C., & Mennerick, S. J. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1289-15.2015 · Cited by 20 · see citing works
Self-citationPresynaptically Silent Synapses Studied with Light Microscopy
Moulder, K. L., Jiang, X., Taylor, A., Benz, A. M., & Mennerick, S. J. (2010) · Journal of Visualized Experiments · doi:10.3791/1676 · Cited by 12 · see citing works
Self-citation
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Brain Glucose Metabolism: Integration of Energetics with Function.
Dienel, G. (2019) · Physiological Reviews · doi:10.1152/physrev.00062.2017 · Cited by 806 · see citing works
Fueling thought: Management of glycolysis and oxidative phosphorylation in neuronal metabolism
Yellen, G. (2018) · Journal of Cell Biology · doi:10.1083/jcb.201803152 · Cited by 371 · see citing works
“In presynaptic terminals, both glycolysis and oxphos appear important for managing intense activity (Rangaraju et al., 2014; Sobieski et al., 2017).”
BackgroundSynaptic, Mitochondrial, and Lysosomal Dysfunction in Parkinson’s Disease
Nguyen, M., Wong, Y. C., Ysselstein, D., Severino, A., & Krainc, D. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2018.11.001 · Cited by 323 · see citing works
Energy matters: presynaptic metabolism and the maintenance of synaptic transmission
Li, S., & Sheng, Z. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00535-8 · Cited by 273 · see citing works
Synapses: The Brain’s Energy-Demanding Sites
Faria‐Pereira, A., & Morais, V. A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23073627 · Cited by 145 · see citing works
Recent development of boronic acid-based fluorescent sensors
Fang, G., Wang, H., Bian, Z., Sun, J., Liu, A., Fang, H., Liu, B., Yao, Q., & Wu, Z. (2018) · RSC Advances · doi:10.1039/c8ra04503h · Cited by 132 · see citing works
Brain energetics during the sleep-wake cycle
DiNuzzo, M., & Nedergaard, M. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.09.010 · Cited by 130 · see citing works
Neuronal vulnerability in Parkinson disease: Should the focus be on axons and synaptic terminals?
Wong, Y. C., Luk, K. C., Purtell, K., Burke, S., Stoessl, A. J., Trudeau, L., Yue, Z., Krainc, D., Oertel, W. H., Obeso, J. A., et al. (2019) · Movement Disorders · doi:10.1002/mds.27823 · Cited by 123 · see citing works
Powerhouse of the mind: mitochondrial plasticity at the synapse
Rossi, M., & Pekkurnaz, G. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.02.001 · Cited by 110 · see citing works
Mechanisms for the maintenance and regulation of axonal energy supply
Chamberlain, K. A., & Sheng, Z. (2019) · Journal of Neuroscience Research · doi:10.1002/jnr.24411 · Cited by 105 · see citing works
Axonal energy metabolism, and the effects in aging and neurodegenerative diseases
Yang, S., Park, J. H., & Lu, H.-C. (2023) · Molecular Neurodegeneration · doi:10.1186/s13024-023-00634-3 · Cited by 94 · see citing works
Mitochondria in Neuronal Health: From Energy Metabolism to Parkinson's Disease
Mahadevan, H. M., Hashemiaghdam, A., Ashrafi, G., & Harbauer, A. B. (2021) · Advanced Biology · doi:10.1002/adbi.202100663 · Cited by 106 · see citing works
Mitochondrial fission drives neuronal metabolic burden to promote stress susceptibility in male mice
Dong, W.-T., Long, L.-H., Deng, Q., Liu, D., Wang, J.-L., Wang, F., & Chen, J.-G. (2023) · Nature Metabolism · doi:10.1038/s42255-023-00924-6 · Cited by 84 · see citing works
Mitochondrial calcium at the synapse
Datta, S., & Jaiswal, M. (2021) · Mitochondrion · doi:10.1016/j.mito.2021.04.006 · Cited by 73 · see citing works
Isoflurane disrupts excitatory neurotransmitter dynamics via inhibition of mitochondrial complex I
Zimin, P. I., Woods, C. B., Kayser, E. B., Ramirez, J. M., Morgan, P. G., & Sedensky, M. M. (2018) · British Journal of Anaesthesia · doi:10.1016/j.bja.2018.01.036 · Cited by 76 · see citing works
Dysregulation of Astrocyte Ion Homeostasis and Its Relevance for Stroke-Induced Brain Damage
van Putten, M. J. A. M., Fahlke, C. M., Kafitz, K. W., Hofmeijer, J., & Rose, C. R. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22115679 · Cited by 73 · see citing works
Energy metabolic pathways in neuronal development and function
Rumpf, S., Sanal, N., & Marzano, M. (2023) · Oxford Open Neuroscience · doi:10.1093/oons/kvad004 · Cited by 75 · see citing works
Reassessment of Pioglitazone for Alzheimer’s Disease
Saunders, A. M., Burns, D. K., & Gottschalk, W. K. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.666958 · Cited by 67 · see citing works
Scarnati, M. S., Kataria, R., Biswas, M., & Paradiso, K. G. (2018) · eLife · doi:10.7554/elife.36697 · Cited by 55 · see citing works
Presynaptic Mitochondrial Volume and Packing Density Scale with Presynaptic Power Demand
Justs, K. A., Lu, Z., Chouhan, A. K., Borycz, J. A., Lu, Z., Meinertzhagen, I. A., & Macleod, G. T. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1236-21.2021 · Cited by 52 · see citing works
Gerkau, N. J., Lerchundi, R., Nelson, J. S. E., Lantermann, M., Meyer, J., Hirrlinger, J., & Rose, C. R. (2019) · The Journal of Physiology · doi:10.1113/jp278658 · Cited by 50 · see citing works
Presynaptic Boutons That Contain Mitochondria Are More Stable
Lees, R. M., Johnson, J. D., & Ashby, M. C. (2020) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2019.00037 · Cited by 45 · see citing works
Kann, O. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.15867 · Cited by 44 · see citing works
Mitochondrial pyruvate transport regulates presynaptic metabolism and neurotransmission
Tiwari, A., Myeong, J., Hashemiaghdam, A., Zhang, H., Niu, X., Laramie, M. A., Stunault, M. I., Sponagel, J., Patti, G. J., Shriver, L. P., et al. (2024) · Science Advances · doi:10.1126/sciadv.adp7423 · Cited by 33 · see citing works
Dysregulated Glucose Metabolism as a Therapeutic Target to Reduce Post-traumatic Epilepsy
Koenig, J. B., & Dulla, C. G. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00350 · Cited by 31 · see citing works
Dromard, Y., Arango-Lievano, M., Fontanaud, P., Tricaud, N., & Jeanneteau, F. D. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100402 · Cited by 28 · see citing works
Chen, Y., & Zhang, J. (2021) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2021.648860 · Cited by 27 · see citing works
Photobiomodulation prevents PTSD-like memory impairments in rats
Li, Y., Dong, Y., Yang, L., Tucker, L. D., Zong, X., Brann, D. W., Hamblin, M. R., Vazdarjanova, A. I., & Zhang, Q. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01088-z · Cited by 28 · see citing works
Metabolic regulation of single synaptic vesicle exo- and endocytosis in hippocampal synapses
Myeong, J., Stunault, M. I., Klyachko, V. A., & Ashrafi, G. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114218 · Cited by 26 · see citing works
Lauric acid promotes neuronal maturation mediated by astrocytes in primary cortical cultures
Nakajima, S., & Kunugi, H. (2020) · Heliyon · doi:10.1016/j.heliyon.2020.e03892 · Cited by 25 · see citing works
Mitochondrial Ca2+ efflux controls neuronal metabolism and long-term memory across species
Vishwanath, A. A., Comyn, T., Mira, R. G., Brossier, C., Pascual-Caro, C., Faour, M., Boumendil, K., Chintaluri, C., Ramon‐Duaso, C., Fan, R., et al. (2026) · Nature Metabolism · doi:10.1038/s42255-026-01451-w · Cited by 24 · see citing works
Glucose metabolism impairment in major depressive disorder
Meng, F., Wang, J., Wang, L., & Zou, W. (2025) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2025.111191 · Cited by 23 · see citing works
Influences of Glaucoma on the Structure and Function of Synapses in the Visual System
Hook, M. J. V. (2022) · Antioxidants and Redox Signaling · doi:10.1089/ars.2021.0253 · Cited by 19 · see citing works
Regional knockdown of NDUFS4 implicates a thalamocortical circuit mediating anesthetic sensitivity
Ramadasan-Nair, R., Hui, J., Zimin, P. I., Itsara, L. S., Morgan, P. G., & Sedensky, M. M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0188087 · Cited by 22 · see citing works
McGuire, J. L., DePasquale, E. A. K., Watanabe, M., Anwar, F. N., Ngwenya, L. B., Atluri, G., Romick‐Rosendale, L. E., McCullumsmith, R. E., & Evanson, N. K. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-1276-5 · Cited by 22 · see citing works
Lujan, B., Singh, M., Singh, A., & Renden, R. (2021) · Journal of Neurophysiology · doi:10.1152/jn.00333.2021 · Cited by 21 · see citing works
Mitochondrial protein synthesis and the bioenergetic cost of neurodevelopment
Bülow, P., Patgiri, A., & Faúndez, V. (2022) · iScience · doi:10.1016/j.isci.2022.104920 · Cited by 20 · see citing works
Courtney, C. D., Sobieski, C. A., Ramakrishnan, C., Ingram, R. J., Wojnowski, N. M., DeFazio, R. A., Deisseroth, K. A., & Christian, C. A. (2023) · Hippocampus · doi:10.1002/hipo.23580 · Cited by 18 · see citing works
Self-citationAdams, S., Zubov, T., Bueschke, N., & Santin, J. M. (2020) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00209.2020 · Cited by 17 · see citing works
Energetic substrate availability regulates synchronous activity in an excitatory neural network
Tourigny, D. S., Karim, M. K. A., Echeveste, R., Kotter, M., & O'Neill, J. S. (2019) · PLoS ONE · doi:10.1371/journal.pone.0220937 · Cited by 15 · see citing works
Ye, Y., Fu, C., Li, Z., Sun, J., Li, X., Chai, S.-F., Li, S., Hou, M., Cai, H.-Y., Wang, Z., et al. (2024) · Experimental Neurology · doi:10.1016/j.expneurol.2024.114920 · Cited by 14 · see citing works
Limited distal organelles and synaptic function in extensive monoaminergic innervation
Tao, J., Bulgari, D., Deitcher, D. L., & Levitan, E. S. (2017) · Journal of Cell Science · doi:10.1242/jcs.201111 · Cited by 12 · see citing works
Caspase inhibition rescues F1Fo ATP synthase dysfunction-mediated dendritic spine elimination
Chen, H. H., Tian, J., Guo, L., & Du, H. (2020) · Scientific Reports · doi:10.1038/s41598-020-74613-9 · Cited by 12 · see citing works
Synaptic modifications transform neural networks to function without oxygen
Amaral‐Silva, L., & Santin, J. M. (2023) · BMC Biology · doi:10.1186/s12915-023-01518-0 · Cited by 11 · see citing works
Ambient but not local lactate underlies neuronal tolerance to prolonged glucose deprivation
Sobieski, C. A., Warikoo, N., Shu, H., & Mennerick, S. J. (2018) · PLoS ONE · doi:10.1371/journal.pone.0195520 · Cited by 11 · see citing works
Self-citationOdaka, H., Numakawa, T., Soga, M., Kido, J., Matsumoto, S., Kajihara, R., Okumiya, T., Tani, N., Tanoue, Y., Fukuda, T., et al. (2021) · Neurobiology of Disease · doi:10.1016/j.nbd.2021.105279 · Cited by 11 · see citing works
Emerging roles for tubulin PTMs in neuronal function and neurodegenerative disease
Teoh, J. J., & Bartolini, F. (2025) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2025.102971 · Cited by 10 · see citing works
Regulated exocytosis from astrocytes: a matter of vesicles?
Calì, C. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1393165 · Cited by 9 · see citing works
Andreasen, M. M., & Nedergaard, S. (2020) · Brain Research · doi:10.1016/j.brainres.2020.147193 · Cited by 9 · see citing works
Zhao, B., Song, S., Zhao, W., Xu, H., Peng, K., Shan, X.-S., Chen, Q., Liu, H., Liu, H., & Ji, F. (2024) · Journal of Neurochemistry · doi:10.1111/jnc.16068 · Cited by 9 · see citing works
Mitochondrial specialization and signaling shape neuronal function
Tong, B. C., Gubinelli, F., Burbulla, L. F., & Harbauer, A. B. (2026) · Trends in Neurosciences · doi:10.1016/j.tins.2025.12.006 · Cited by 9 · see citing works
Sink or swim: Does a worm paralysis phenotype hold clues to neurodegenerative disease?
Rodriguez, P., & Blakely, R. (2023) · Journal of Cellular Physiology · doi:10.1002/jcp.31125 · Cited by 7 · see citing works
Yang, Y. Q., Zhou, D., Min, S., Liu, D., Zou, M., Yu, C., Chen, L., Huang, J., & Hong, R. (2024) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2024.173775 · Cited by 8 · see citing works
Targeting selective autophagy in CNS disorders by small-molecule compounds
Zheng, Y., Zhou, Z., Liu, M., & Chen, Z. (2024) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2024.108729 · Cited by 6 · see citing works
Dopamine Release Neuroenergetics in Mouse Striatal Slices
Msackyi, M., Chen, Y., Tsering, W., Wang, N., Zhao, J., & Zhang, H. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25094580 · Cited by 5 · see citing works
Hebda‐Bauer, E. K., Hagenauer, M. H., Munro, D. B., Blandino, P., Meng, F., Arakawa, K., Chitre, A. S., Ozel, A. B., Mohammadi, P., Watson, S. J., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.07.14.500129 · Cited by 4 · see citing works
Neuronal Synaptic Communication and Mitochondrial Energetics in Human Health and Disease
Glausier, J. R. (2025) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-89525-8_5 · Cited by 3 · see citing works
Hebda‐Bauer, E. K., Hagenauer, M. H., Munro, D. B., Blandino, P., Meng, F., Arakawa, K., Stead, J. D. H., Chitre, A. S., Ozel, A. B., Mohammadi, P., et al. (2025) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2025.1469467 · Cited by 2 · see citing works
Mechanisms of Nerve Injury in Diabetes: Dyslipidemia, Bioenergetics, and Oxidative Damage
Eid, S., Noureldein, M. H., Savelieff, M. G., & Feldman, E. L. (2023) · Contemporary diabetes · doi:10.1007/978-3-031-15613-7_16 · Cited by 2 · see citing works
Chen, Z.-Y., Sheng, Q., Dong, X., Gao, C., Li, X., Hu, G.-P., Liu, J., & Wu, J. (2026) · Food Bioscience · doi:10.1016/j.fbio.2026.109330 · 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
Glucopuncture for Achilles Tendinopathy: A Descriptive Review
O'Byrne, A., & Kersschot, J. (2022) · World Journal of Advanced Research and Reviews · doi:10.30574/wjarr.2022.15.2.0824
Regulation of Synaptic Transmission through Mitochondrial Positioning and Metabolism
Li, S., & Sheng, Z. (2024) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780190932183.013.13
Additional file 2 of Synaptic modifications transform neural networks to function without oxygen
Amaral‐Silva, L., & Santin, J. M. (2023) · Figshare · doi:10.6084/m9.figshare.22622791
Additional file 4 of Synaptic modifications transform neural networks to function without oxygen
Amaral‐Silva, L., & Santin, J. M. (2023) · Figshare · doi:10.6084/m9.figshare.22622797
Additional file 5 of Synaptic modifications transform neural networks to function without oxygen
Amaral‐Silva, L., & Santin, J. M. (2023) · Figshare · doi:10.6084/m9.figshare.22622800
Additional file 1 of Synaptic modifications transform neural networks to function without oxygen
Amaral‐Silva, L., & Santin, J. M. (2023) · Figshare · doi:10.6084/m9.figshare.22622788
Additional file 3 of Synaptic modifications transform neural networks to function without oxygen
Amaral‐Silva, L., & Santin, J. M. (2023) · Figshare · doi:10.6084/m9.figshare.22622794
Morciano, G., Gorgoglione, R., Porcelli, V., Ahmed, A., Scarcia, P., Vozza, A., Lasorsa, F. M., Fiermonte, G., & Palmieri, L. (2026) · Biomolecules · doi:10.3390/biom16060842
Mohammad, S. I., Kareem, A. K., Rekha, M. M., Vasudevan, A., Jabir, M. S., Nayak, P. P., Abosaoda, M. K., Arora, V., Nanda, A., & Hsu, C. (2026) · Neurochemistry International · doi:10.1016/j.neuint.2026.106264
Liu, W., Wu, C., Tsai, P.-C., Gutkowska-Kawka, D., Fu, M., Tain, Y., Hsu, C., Hung, C., Chen, I.-C., Wu, K. L. H., et al. (2026) · Molecular Neurobiology · doi:10.1007/s12035-026-06181-4
Cunha, M. G. (2026) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2026.107007
Li, M., Ye, M., Xie, H., Gao, T., Kan, W., Chen, Y., Xia, Y., Zhao, Y., & Yuan, A.-H. (2026) · Frontiers in Endocrinology · doi:10.3389/fendo.2026.1991245
- Authors
- Sobieski, C., Fitzpatrick, M. J., & Mennerick, S. J.
- Affiliations
- Washington University in St. Louis (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2017-01-16
- Volume
- 37
- Issue
- 7
- Pages
- 1888-1899
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC5320616
- OpenAlex
- W2575996993
- Cited by
- 74
- References
- 56
- Citations by year
- 2026: 8 · 2025: 4 · 2024: 10 · 2023: 13 · 2022: 5 · 2021: 12 · 2020: 5 · 2019: 5 · 2018: 9 · 2017: 3
- FWCI
- 2.95
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Digital Commons@Becker (Washington University School of Medicine) (submittedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (F31MH106198, R21MH099658, R01MH078823, R21MH104506)
- 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
- glycolysis, oxidative phosphorylation, synaptic transmission, vesicle exocytosis, endocytosis, hippocampal neurons, neuronal energy metabolism
- MeSH terms
- Action Potentials, Adenosine Triphosphate, Animals, Animals, Newborn, Astrocytes, Cells, Cultured, Endocytosis, Enzyme Inhibitors, Glycolysis, Hippocampus, Synaptic Transmission, Neurons, Phosphorylation, Potassium Chloride, Synaptic Vesicles, Rats, Sprague-Dawley, Presynaptic Terminals, Neurotransmitter Agents, Patch-Clamp Techniques, Rats, Synaptic Potentials
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