Journal Article

FZJ-2020-01276

http://join2-wiki.gsi.de/foswiki/pub/Main/Artwork/join2_logo100x88.png Relation between activity‐induced intracellular sodium transients and ATP dynamics in mouse hippocampal neurons

Gerkau, N. J. ; Lerchundi, R. ; Nelson, J. S. E. ; Lantermann, M. ; Meyer, J.FZJ* ; Hirrlinger, J. ; Rose, C. R. (Corresponding author)Extern*

2019
Wiley-Blackwell Hoboken, NJ

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Please use a persistent id in citations: http://hdl.handle.net/2128/24403  doi:10.1113/JP278658

Abstract: Excitatory neuronal activity results in the influx of Na+ through voltage‐ and ligand‐gated channels. Recovery from accompanying increases in intracellular Na+ concentrations ([Na+]i) is mainly mediated by the Na+/K+‐ATPase (NKA) and is one of the major energy‐consuming processes in the brain. Here, we analysed the relation between different patterns of activity‐induced [Na+]i signalling and ATP in mouse hippocampal CA1 pyramidal neurons by Na+ imaging with sodium‐binding benzofurane isophthalate (SBFI) and employing the genetically encoded nanosensor ATeam1.03YEMK (ATeam). In situ calibrations demonstrated a sigmoidal dependence of the ATeam Förster resonance energy transfer ratio on the intracellular ATP concentration ([ATP]i) with an apparent KD of 2.6 mm, indicating its suitability for [ATP]i measurement. Induction of recurrent network activity resulted in global [Na+]i oscillations with amplitudes of ∼10 mm, encompassing somata and dendrites. These were accompanied by a steady decline in [ATP]i by 0.3–0.4 mm in both compartments. Global [Na+]i transients, induced by afferent fibre stimulation or bath application of glutamate, caused delayed, transient decreases in [ATP]i as well. Brief focal glutamate application that evoked transient local Na+ influx into a dendrite, however, did not result in a measurable reduction in [ATP]i. Our results suggest that ATP consumption by the NKA following global [Na+]i transients temporarily overrides its availability, causing a decrease in [ATP]i. Locally restricted Na+ transients, however, do not result in detectable changes in local [ATP]i, suggesting that ATP production, together with rapid intracellular diffusion of both ATP and Na+ from and to unstimulated neighbouring regions, counteracts a local energy shortage under these conditions.

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Contributing Institute(s):

1. International Helmholtz Research School of Biophysics and Soft Matter (IHRS-BioSoft)
2. Zelluläre Biophysik (ICS-4)

Research Program(s):

1. 553 - Physical Basis of Diseases (POF3-553) (POF3-553)
2. IHRS-BioSoft - International Helmholtz Research School of Biophysics and Soft Matter (IHRS-BioSoft-20061101) (IHRS-BioSoft-20061101)

Appears in the scientific report 2020

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