ZFIN ID: ZDB-PUB-100317-10
Non-Ca2+-conducting Ca2+ channels in fish skeletal muscle excitation-contraction coupling
Schredelseker, J., Shrivastav, M., Dayal, A., and Grabner, M.
Date: 2010
Source: Proceedings of the National Academy of Sciences of the United States of America   107(12): 5658-5663 (Journal)
Registered Authors: Dayal, Anamika, Grabner, Manfred, Schredelseker, Johann
Keywords: calcium conductivity, evolution, ion channels, slow and fast muscle, zebrafish
MeSH Terms:
  • Amino Acid Sequence
  • Animals
  • Calcium Channels, L-Type/chemistry
  • Calcium Channels, L-Type/genetics
  • Calcium Channels, L-Type/metabolism*
  • Evolution, Molecular
  • Excitation Contraction Coupling
  • Fishes/genetics
  • Fishes/physiology*
  • In Vitro Techniques
  • Molecular Sequence Data
  • Muscle Contraction/physiology
  • Muscle, Skeletal/physiology*
  • Patch-Clamp Techniques
  • Phylogeny
  • Protein Isoforms/chemistry
  • Protein Isoforms/genetics
  • Protein Isoforms/metabolism
  • Protein Subunits
  • Ryanodine Receptor Calcium Release Channel/chemistry
  • Ryanodine Receptor Calcium Release Channel/genetics
  • Ryanodine Receptor Calcium Release Channel/metabolism
  • Sequence Homology, Amino Acid
  • Species Specificity
  • Tissue Distribution
  • Zebrafish/genetics
  • Zebrafish/physiology*
  • Zebrafish Proteins/chemistry
  • Zebrafish Proteins/genetics
  • Zebrafish Proteins/metabolism*
PubMed: 20212109 Full text @ Proc. Natl. Acad. Sci. USA
ABSTRACT
During skeletal muscle excitation-contraction (EC) coupling, membrane depolarizations activate the sarcolemmal voltage-gated L-type Ca(2+) channel (Ca(V)1.1). Ca(V)1.1 in turn triggers opening of the sarcoplasmic Ca(2+) release channel (RyR1) via interchannel protein-protein interaction to release Ca(2+) for myofibril contraction. Simultaneously to this EC coupling process, a small and slowly activating Ca(2+) inward current through Ca(V)1.1 is found in mammalian skeletal myotubes. The role of this Ca(2+) influx, which is not immediately required for EC coupling, is still enigmatic. Interestingly, whole-cell patch clamp experiments on freshly dissociated skeletal muscle myotubes from zebrafish larvae revealed the lack of such Ca(2+) currents. We identified two distinct isoforms of the pore-forming Ca(V)1.1alpha(1S) subunit in zebrafish that are differentially expressed in superficial slow and deep fast musculature. Both do not conduct Ca(2+) but merely act as voltage sensors to trigger opening of two likewise tissue-specific isoforms of RyR1. We further show that non-Ca(2+) conductivity of both Ca(V)1.1alpha(1S) isoforms is a common trait of all higher teleosts. This non-Ca(2+) conductivity of Ca(V)1.1 positions teleosts at the most-derived position of an evolutionary trajectory. Though EC coupling in early chordate muscles is activated by the influx of extracellular Ca(2+), it evolved toward Ca(V)1.1-RyR1 protein-protein interaction with a relatively small and slow influx of external Ca(2+) in tetrapods. Finally, the Ca(V)1.1 Ca(2+) influx was completely eliminated in higher teleost fishes.
ADDITIONAL INFORMATION