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Imaging of Intracellular ATP in Organotypic Tissue Slices of the Mouse Brain using the FRET-based Sensor ATeam1.03YEMK

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Activity-dependent citrate dynamics in neurons.

Paul C Rosen^1,2, Panhui Fu¹, Beatriz Ferrán^3,4,5

¹Department of Neurobiology, Harvard Medical School, Boston, MA 02115.

Proceedings of the National Academy of Sciences of the United States of America

|October 10, 2025

Summary

This summary is machine-generated.

Scientists developed new fluorescent biosensors to measure citrate levels in live neurons. They observed a rapid, transient decrease in citrate upon neuronal activation, crucial for understanding glycolysis control.

Keywords:

fluorescence lifetime genetically encoded fluorescent biosensor glycolytic regulation mitochondrial calcium uniporter

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Area of Science:

Neuroscience
Metabolic Biochemistry
Cellular Physiology

Background:

Glycolytic enzymes rapidly adapt cellular energy production in response to metabolic cues.
Measuring key glycolytic metabolites, like citrate, with spatiotemporal precision in live cells remains a significant challenge.
Neuronal depolarization activates glycolysis, highlighting the need to understand metabolite dynamics during neural activity.

Purpose of the Study:

To engineer advanced fluorescent biosensors for precise, real-time measurement of intracellular citrate levels.
To investigate the dynamic changes in cytosolic free citrate concentration in neurons during depolarization.
To elucidate the role of mitochondrial calcium transport in regulating citrate levels during neuronal activation.

Main Methods:

Development of novel quantitative fluorescent biosensors for citrate, optimized for affinity, pH, Mg2+, and temperature.
Utilized two-photon fluorescence lifetime imaging microscopy for high-resolution live-cell imaging.
Employing acute mouse brain slices to study neuronal responses in a physiologically relevant context.

Main Results:

Engineered biosensors successfully quantified citrate dynamics in live neurons.
Observed a rapid two-to-threefold decrease in cytosolic free citrate within seconds of neuronal activation.
Citrate levels returned to baseline over several minutes, with dependence on the mitochondrial calcium uniporter.

Conclusions:

The study presents a breakthrough in live-cell metabolite measurement, enabling real-time monitoring of glycolysis regulators.
Demonstrated a rapid, transient decrease in neuronal citrate upon activation, linked to mitochondrial calcium influx.
These findings provide critical insights into the fast, dynamic control of glycolysis in neurons.