Direct in vivo monitoring of sarcoplasmic reticulum Ca2+ and cytosolic cAMP dynamics in mouse skeletal muscle

Skeletal muscle contraction depends on the release of Ca2+ from the sarcoplasmic reticulum (SR), but the dynamics of the SR free Ca2+ concentration ([Ca2+]SR), its modulation by physiological stimuli such as catecholamines, and the concomitant changes in cAMP handling have never been directly determined. We used two-photon microscopy imaging of GFP-based probes expressed in mouse skeletal muscles to monitor, for the first time in a live animal, the dynamics of [Ca2+]SR and cAMP. Our data, which were obtained in highly physiological conditions, suggest that free [Ca2+]SR decreases by ∼50 μM during single twitches elicited through nerve stimulation. We also demonstrate that cAMP levels rise upon β-adrenergic stimulation, leading to an increased efficacy of the Ca2+ release/reuptake cycle during motor nerve stimulation.

• Publication year

  2006

• Venue

  Journal of Cell Biology

• Publication date

  2006-04-24

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1083/jcb.200601160PMID 16618815PMCID 2063810
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

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• Fluorescent indicators for Ca2+based on green fluorescent proteins and calmodulin

  1997cited by this paper
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• Ca2+ release from the sarcoplasmic reticulum compared in amphibian and mammalian skeletal muscle

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• Cardiac troponin I phosphorylation increases the rate of cardiac muscle relaxation.

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• Local ATP regeneration is important for sarcoplasmic reticulum Ca2+ pump function.

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• Beta-adrenergic potentiation of E-C coupling increases force in rat skeletal muscle.

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• Phosphorylation of ryanodine receptors in rat myocytes during beta-adrenergic stimulation.

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• Beta-adrenergic modulation of calcium channels in frog ventricular heart cells.

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  1981influential reference
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