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Membrane tension in swelling and shrinking molluscan neurons
J Dai1, M P Sheetz, X Wan
1Department of Cell Biology, Duke University Medical Center, Durham, North Carolina 27710, USA.
Summary
Neurons maintain surface area homeostasis by regulating membrane tension. Even when swelling or shrinking, membrane tension feedback loops help neurons survive mechanical stress, with calcium ions playing a role in this regulation.
Area of Science:
- Cell Biology
- Neuroscience
- Biophysics
Background:
- Neurons experience significant volume and shape changes.
- Maintaining cell surface area is crucial for neuronal function and survival.
- The membrane tension hypothesis proposes a feedback mechanism for surface area homeostasis.
Purpose of the Study:
- To investigate the role of membrane tension in neuronal surface area homeostasis.
- To test the membrane tension hypothesis during cell swelling and shrinking.
- To examine the influence of cytoplasmic calcium on membrane tension regulation.
Main Methods:
- Measuring apparent membrane tension of Lymnaea neurons using membrane tether forces.
- Inducing cell swelling and shrinking using hypotonic and isotonic media.
- Utilizing BAPTA to chelate cytoplasmic calcium (Ca2+).
- Measuring membrane capacitance changes in voltage-clamped neurons.
Main Results:
- Neuronal swelling increased membrane tension, but steady-state tension was only moderately elevated.
- Shrinking neurons exhibited reduced membrane tension and membrane invagination.
- BAPTA-induced calcium depletion led to large, non-lytic tension surges during swelling.
- Membrane capacitance increased during swelling, indicating an increase in membrane area.
- Neurons survived tension surges even without calcium signaling.
Conclusions:
- The membrane tension hypothesis provides a framework for neuronal surface area homeostasis.
- Feedback regulation of membrane tension helps buffer against mechanical stress.
- Cytoplasmic calcium influences the regulation of membrane tension during swelling.
- Neurons possess a tension-sensing mechanism for recruiting membrane stores to prevent rupture.