PUBLICATION
A mechano- and heat-gated two-pore domain K+ channel controls excitability in adult zebrafish skeletal muscle
- Authors
- Idoux, R., Exbrayat-Héritier, C., Sohm, F., Jaque-Fernandez, F., Vaganay, E., Berthier, C., Bretaud, S., Jacquemond, V., Ruggiero, F., Allard, B.
- ID
- ZDB-PUB-231031-53
- Date
- 2023
- Source
- Proceedings of the National Academy of Sciences of the United States of America 120: e2305959120e2305959120 (Journal)
- Registered Authors
- Bretaud, Sandrine, Ruggiero, Florence, Sohm, Frédéric, Vaganay, Elisabeth
- Keywords
- K+ channel, single-channel recording, skeletal muscle fiber, voltage-clamp, zebrafish
- MeSH Terms
-
- Animals
- COS Cells
- Chlorocebus aethiops
- Hot Temperature*
- Mice
- Muscle Fibers, Skeletal/physiology
- Muscle, Skeletal
- Zebrafish*/genetics
- PubMed
- 37903280 Full text @ Proc. Natl. Acad. Sci. USA
Citation
Idoux, R., Exbrayat-Héritier, C., Sohm, F., Jaque-Fernandez, F., Vaganay, E., Berthier, C., Bretaud, S., Jacquemond, V., Ruggiero, F., Allard, B. (2023) A mechano- and heat-gated two-pore domain K+ channel controls excitability in adult zebrafish skeletal muscle. Proceedings of the National Academy of Sciences of the United States of America. 120:e2305959120e2305959120.
Abstract
TRAAK channels are mechano-gated two-pore-domain K+ channels. Up to now, activity of these channels has been reported in neurons but not in skeletal muscle, yet an archetype of tissue challenged by mechanical stress. Using patch clamp methods on isolated skeletal muscle fibers from adult zebrafish, we show here that single channels sharing properties of TRAAK channels, i.e., selective to K+ ions, of 56 pS unitary conductance in the presence of 5 mM external K+, activated by membrane stretch, heat, arachidonic acid, and internal alkaline pH, are present in enzymatically isolated fast skeletal muscle fibers from adult zebrafish. The kcnk4b transcript encoding for TRAAK channels was cloned and found, concomitantly with activity of mechano-gated K+ channels, to be absent in zebrafish fast skeletal muscles at the larval stage but arising around 1 mo of age. The transfer of the kcnk4b gene in HEK cells and in the adult mouse muscle, that do not express functional TRAAK channels, led to expression and activity of mechano-gated K+ channels displaying properties comparable to native zebrafish TRAAK channels. In whole-cell voltage-clamp and current-clamp conditions, membrane stretch and heat led to activation of macroscopic K+ currents and to acceleration of the repolarization phase of action potentials respectively, suggesting that heat production and membrane deformation associated with skeletal muscle activity can control muscle excitability through TRAAK channel activation. TRAAK channels may represent a teleost-specific evolutionary product contributing to improve swimming performance for escaping predators and capturing prey at a critical stage of development.
Genes / Markers
Expression
Phenotype
Mutations / Transgenics
Human Disease / Model
Sequence Targeting Reagents
Fish
Orthology
Engineered Foreign Genes
Mapping