Desmin interacts with STIM1 and coordinates Ca2+ signaling in skeletal muscle

Zhang, Hengtao; Bryson, Victoria; Wang, Chaojian; Li, TianYu; Kerr, Jaclyn P.; Wilson, Rebecca J.; Muoio, Deborah M.; Bloch, Robert J.; Ward, Chris W.; Rosenberg, Paul B.

doi:10.1172/jci.insight.143472

Cited by 18 publications

(21 citation statements)

References 48 publications

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“…These small projections are an additional identifying feature of CEUs, since such frequent tethers are not present in other SR areas. Presence of STIM1 at sites where CEUs are preferentially located has been recently confirmed ( Zhang et al, 2021 ).…”

Section: Introductionmentioning

confidence: 82%

Ca2+ entry units in a superfast fish muscle

Kittelberger

Franzini‐Armstrong²,

Boncompagni³

2022

Front. Physiol.

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Over the past two decades, mounting evidence has demonstrated that a mechanism known as store-operated Ca2+ entry (SOCE) plays a crucial role in sustaining skeletal muscle contractility by facilitating Ca2+ influx from the extracellular space during sarcoplasmic reticulum (SR) Ca2+ depletion. We recently demonstrated that, in exercised fast-twitch muscle from mice, the incidence of Ca2+ entry units (CEUs), newly described intracellular junctions between dead-end longitudinal transverse tubular (T-tubule) extensions and stacks of sarcoplasmic reticulum (SR) flat cisternae, strictly correlate with both the capability of fibers to maintain contractions during fatigue and enhanced Ca2+ influx via SOCE. Here, we tested the broader relevance of this result across vertebrates by searching for the presence of CEUs in the vocal muscles of a teleost fish adapted for extended, high-frequency activity. Specifically, we examined active vs. inactive superfast sonic muscles of plainfin midshipman (Porichthys notatus). Interestingly, muscles from actively humming territorial males had a much higher incidence of CEU SR stacks relative to territorial males that were not actively vocalizing, strengthening the concept that assembly of these structures is dynamic and use-dependent, as recently described in exercised muscles from mice. Our results support the hypothesis that CEUs represent a conserved mechanism, across vertebrates, for enabling high levels of repetitive muscle activity, and also provide new insights into the adaptive mechanisms underlying the unique properties of superfast midshipman sonic muscles.

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Section: Introductionmentioning

confidence: 82%

Ca2+ entry units in a superfast fish muscle

Kittelberger

Franzini‐Armstrong²,

Boncompagni³

2022

Front. Physiol.

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“…Brennan and colleagues proposed that desmin intermediate filaments, making up the exosarcomeric cytoskeleton are responsible for the alignment of myofibrils (Brennan et al, 2005). Interestingly desmin activity seems to be regulated by calcium‐binding protein (Li et al, 1997; Zhang et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly desmin activity seems to be regulated by calciumbinding protein (Li et al, 1997;Zhang et al, 2021).…”

Section: Normal Alteredmentioning

confidence: 99%

Zebrafish dnm1a gene plays a role in the formation of axons and synapses in the nervous tissue

Bragato

Pistocchi

Bellipanni

et al. 2023

J of Neuroscience Research

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Classical dynamins (DNMs) are GTPase proteins engaged in endocytosis, a fundamental process for cargo internalization from the plasma membrane. In mammals, three DNM genes are present with different expression patterns. DNM1 is expressed at high levels in neurons, where it takes place in the recycling of synaptic vesicles; DNM2 is ubiquitously expressed, while DNM3 is found in the brain and in the testis. Due to the conservation of genes in comparison to mammals, we took advantage of a zebrafish model for functional characterization of dnm1a, ortholog of mammalian DNM1. Our data strongly demonstrated that dnm1a has a nervous tissue-specific expression pattern and plays a role in the formation of both axon and synapse. This is the first in vivo study that collects evidence about the effects of dnm1a loss of function in zebrafish, thus providing a new excellent model to be used in different scientific fields.

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“…The mechanism of activation of SOCE was first studied in non-excitable cells: Ca 2+ depletion of internal ER stores induces dimerization of STIM1 and its translocation towards the plasma membrane (PM), enabling in this way STIM1 to interact and activate Orai1 Ca 2+ channels [ 34 , 35 ]. In skeletal muscle, SOCE also relies on the concerted activity of STIM1 and Orai1 [ 25 , 30 , 36 , 37 , 38 ], as supported by the finding that SOCE is abolished in mice lacking STIM1 [ 39 ] and in muscle fibers from dominant-negative and muscle-specific Orai1-knockout mice [ 40 , 41 ]. The exact stoichiometry of the active SOCE complex is currently unclear [ 42 , 43 ].…”

Section: Introductionmentioning

confidence: 97%

Searching for Mechanisms Underlying the Assembly of Calcium Entry Units: The Role of Temperature and pH

Girolami

Serano

Fonso

et al. 2023

IJMS

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Store-operated Ca2+ entry (SOCE) is a mechanism that allows muscle fibers to recover external Ca2+, which first enters the cytoplasm andthen, via SERCA pump, also refills the depleted intracellular stores (i.e., the sarcoplasmic reticulum, SR). We recently discovered that SOCE is mediated by Calcium Entry Units (CEUs), intracellular junctions formed by: (i) SR stacks containing STIM1; and (ii) I-band extensions of the transverse tubule (TT) containing Orai1. The number and size of CEUs increase during prolonged muscle activity, though the mechanisms underlying exercise-dependent formation of new CEUs remain to be elucidated. Here, we first subjected isolated extensor digitorum longus (EDL) muscles from wild type mice to an exvivo exercise protocol and verified that functional CEUs can assemble alsoin the absence of blood supply and innervation. Then, we evaluated whetherparameters that are influenced by exercise, such as temperature and pH, may influence the assembly of CEUs. Results collected indicate that higher temperature (36 °C vs. 25 °C) and lower pH (7.2 vs. 7.4) increase the percentage of fibers containing SR stacks, the n. of SR stacks/area, and the elongation of TTs at the I band. Functionally, assembly of CEUs at higher temperature (36 °C) or at lower pH (7.2) correlates with increased fatigue resistance of EDL muscles in the presence of extracellular Ca2+. Taken together, these results indicate that CEUs can assemble in isolated EDL muscles and that temperature and pH are two of the possible regulators of CEU formation.

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Desmin interacts with STIM1 and coordinates Ca2+ signaling in skeletal muscle

Cited by 18 publications

References 48 publications

Ca2+ entry units in a superfast fish muscle

Ca2+ entry units in a superfast fish muscle

Zebrafish dnm1a gene plays a role in the formation of axons and synapses in the nervous tissue

Searching for Mechanisms Underlying the Assembly of Calcium Entry Units: The Role of Temperature and pH

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