Improvement of calcium handling and changes in calcium-release properties after mini- or full-length dystrophin forced expression in cultured skeletal myotubes

Marchand, Éric; Constantin, Bruno; Balghi, Haouaria; Claudepierre, Marie-Christine; Cantereau, Anne; Magaud, Christophe; Mouzou, Aklesso; Raymond, Guy; Braun, Serge; Cognard, Christian

doi:10.1016/j.yexcr.2004.02.032

Cited by 24 publications

(46 citation statements)

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“…This mini-dystrophin-forced expression allows readdressing of members of the DAP complex and recovery of intracellular Ca 2ϩ levels similar to those observed in myotubes from mouse primary cell culture (33). Furthermore, this model allows the physiological exploration of two cellular systems (4,5,47) with the only difference being the transfection-induced presence (or not) of mini-dystrophin and has also been used to demonstrate the restoration of sarcolemmal store-dependent channels with forced expression of mini-dystrophin (46).…”

Section: Discussionmentioning

confidence: 63%

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Negative modulation of inositol 1,4,5-trisphosphate type 1 receptor expression prevents dystrophin-deficient muscle cells death

Mondin

Balghi

Constantin

et al. 2009

American Journal of Physiology-Cell Physiology

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Evidence for a modulatory effect of cyclosporin A (CsA) on calcium signaling and cell survival in dystrophin-deficient cells is presented. Our previous works strongly supported the hypothesis of an overactivation of Ca 2ϩ release via inositol 1,4,5-trisphosphate (IP3) receptors (IP3R) in dystrophindeficient cells, both during membrane depolarization and at rest, through spontaneous Ca 2ϩ release events. Forced expression of minidystrophin in these cells contributed, during stimulation and in resting condition, to the recovery of a controlled calcium homeostasis. In the present work, we demonstrate that CsA exposure displayed a dualmodulator effect on calcium signaling in dystrophin-deficient cells. Short-time incubation induced a decrease of IP3-dependent calcium release, leading to patterns of release similar to those observed in myotubes expressing mini-dystrophin, whereas long-time incubation reduced the expression of the type I of IP3 receptors (IP3R-1) RNA levels. Moreover, both IP3R-1 knockdown and blockade through 2-aminoethoxydiphenyle borate or CsA induced improved survival of dystrophin-deficient myotubes, demonstrating the cell death dependence on the IP3-dependent calcium signaling as well as the protective effect of CsA. Inhibition of the IP3 pathway could be a very interesting approach for reducing the natural cell death of dystrophindeficient cells in development. calcium regulation; cyclosporin A; muscular dystrophy DUCHENNE MUSCULAR DYSTROPHY (DMD) is a severe X-linked recessive, progressive muscle-wasting disease affecting 1/3,500 male births. A milder form of the disease, Becker muscular dystrophy (BMD), has a later onset and a much longer survival. Both disorders are caused by mutations in the DMD gene that encodes a 427-kDa cytoskeletal protein dystrophin expressed at the inner surface of the sarcolemma of muscle fibers (26). The vast majority of DMD mutations results in the absence of dystrophin in all muscle fibers, apart from the sporadic "revertant" fibers (49), whereas the presence of a low level of a 229-kDa truncated protein mini-dystrophin is seen in BMD patients (20).Perturbations in intracellular calcium homeostasis are thought to come with DMD. Indications suggesting such calcium alterations were discovered early before dystrophin protein was identified (16), and it was then proposed that the absence of dystrophin leads to increased levels of intracellular calcium (11), contributing to muscle degeneration through activation of calcium-dependent proteases. Further data progressively reinforced such a hypothesis. Elevated subsarcolemmal calcium levels were found in mdx muscle cells using direct measurements (6) and as well as the exploration of calciumactivated K ϩ -channels activities (32). It has been also hypothesized that calcium entry due to increased microdisruptions in dystrophic muscle cells results in an alteration of calcium leak channels. First, a local exocytotic response induced by calcium influx from a membrane wound could increase the amount of calcium leak channels (...

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Section: Discussionmentioning

confidence: 63%

“…The method for obtaining cell lines [SolC1(Ϫ) and SolD(ϩ)] was described elsewhere (33). In brief, after several steps of cloning, a dystrophin-deficient cell line was obtained, named SolC1(Ϫ).…”

Section: Cell Linesmentioning

confidence: 99%

Negative modulation of inositol 1,4,5-trisphosphate type 1 receptor expression prevents dystrophin-deficient muscle cells death

Mondin

Balghi

Constantin

et al. 2009

American Journal of Physiology-Cell Physiology

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“…Our group also showed an abnormal increase in storeoperated calcium entry (SOCE) in dystrophin-deficient mouse myotubes corrected by a stable tranfection with minidystrophin (41,58). The regulation of SOCE involves the subsarcolemmal scaffolding protein ␣ 1 -syntrophin, which is capable of correcting the abnormal increase of SOCE in dystrophin-deficient mouse myotubes (50,59).…”

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confidence: 69%

Involvement of TRPV2 and SOCE in calcium influx disorder in DMD primary human myotubes with a specific contribution of α₁-syntrophin and PLC/PKC in SOCE regulation

Harisseh

Chatelier

Magaud

et al. 2013

American Journal of Physiology-Cell Physiology

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Harisseh R, Chatelier A, Magaud C, Déliot N, Constantin B. Involvement of TRPV2 and SOCE in calcium influx disorder in DMD primary human myotubes with a specific contribution of ␣ 1-syntrophin and PLC/PKC in SOCE regulation. Am J Physiol Cell Physiol 304: C881-C894, 2013. First published February 20, 2013 doi:10.1152/ajpcell.00182.2012.-Calcium homeostasis is critical for several vital functions in excitable and nonexcitable cells and has been shown to be impaired in many pathologies including Duchenne muscular dystrophy (DMD). Various studies using murine models showed the implication of calcium entry in the dystrophic phenotype. However, alteration of store-operated calcium entry (SOCE) and transient receptor potential vanilloid 2 (TRPV2)-dependant cation entry has not been investigated yet in human skeletal muscle cells. We pharmacologically characterized basal and storeoperated cation entries in primary cultures of myotubes prepared from muscle of normal and DMD patients and found, for the first time, an increased SOCE in DMD myotubes. Moreover, this increase cannot be explained by an over expression of the well-known SOCE actors: TRPC1/4, Orai1, and stromal interaction molecule 1 (STIM1) mRNA and proteins. Thus we investigated the modes of regulation of this cation entry. We firstly demonstrated the important role of the scaffolding protein ␣ 1-syntrophin, which regulates SOCE in primary human myotubes through its PDZ domain. We also studied the implication of phospholipase C (PLC) and protein kinase C (PKC) in SOCE and showed that their inhibition restores normal levels of SOCE in DMD human myotubes. In addition, the involvement of TRPV2 in calcium deregulation in DMD human myotubes was explored. We showed an abnormal elevation of TRPV2-dependant cation entry in dystrophic primary human myotubes compared with normal ones. These findings show that calcium homeostasis mishandling in DMD myotubes depends on SOCE under the influence of Ca 2ϩ /PLC/PKC pathway and ␣1-syntrophin regulation as well as on TRPV2-dependant cation influx. DMD; human primary myotubes; Ca 2ϩ /PLC/PKC; ␣1-syntrophin; TRPV2; SOCE CALCIUM HOMEOSTASIS IS BASED on strictly cohesive and regulated communication between internal and plasma membrane calcium channels and pumps and has been shown to be altered in several pathologies and particularly in dystrophinopathies including Duchenne muscular dystrophy (DMD; Ref. 5). DMD is characterized by an abnormally high concentration of intracellular ionized calcium (7), which is thought to contribute to the final muscle necrosis. DMD is an X-linked recessive genetic disorder that affects 1 male birth over 3,500 in the world. This disease is caused by mutations on the locus Xp21.2 of the gene encoding the subsarcolemmal dystrophin, resulting in the loss of this protein (57). In the absence of dystrophin, the transmembrane dystrophin glycoprotein complex components lose their localization at costamers. This disorganization is thought to be responsible for membrane instability and muscle damage and for ...

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“…Dystrophin, which links the intracellular cytoskeleton to the extracellular matrix [Blake et al, 2002], appears to be important for the maintenance of Ca 2+ concentration in muscle, thus providing a link between the cytoskeleton and Ca 2+ signaling [Marchand et al, 2004]. Also, while there are some signaling differences between mouse skeletal and diaphragm muscle [Lang et al, 2004], the functional importance of dystrophin has been shown in diaphragm muscle where differences in stretch-related signaling and the infl uence of Ca 2+ were shown between normal muscle cells and those lacking dystrophin [Kumar et al, 2004].…”

Section: Sarcomeric and Cytoskeletal Proteinsmentioning

confidence: 99%

Understanding Muscle Architectural Adaptation: Macro- and Micro-Level Research

Blazevich

Sharp²

2005

Cells Tissues Organs

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Recent research using muscle-imaging techniques has revealed a remarkable plasticity of human muscle architecture where significant changes in fascicle lengths and angles have resulted from the chronic performance, or cessation, of strong muscle contractions. However, there is a paucity of data describing architectural adaptations to chronic stretching, disuse and immobilization, illness, and aging, and those data that are available are equivocal. Understanding their impact is important in order that effective interventions for illness/injury management and rehabilitation, and programs to improve the physical capacity of workers, the aged and athletes can be determined. Nonetheless, recent advances in myocellular research could provide a framework allowing the prediction of architectural changes in these understudied areas. Examination of the site-specific response to mechanical stress of calpain-dependent ubiquitin-proteasome proteolysis, or of the cellular response to stress after the knockout (or incapacitation) of sarcomeric and cytoskeletal proteins involved in cellular signal transduction, provides an exciting paradigm by which myocellular adaptation can be described. Such research might contribute to the understanding of macro-level changes in muscle architecture.

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Improvement of calcium handling and changes in calcium-release properties after mini- or full-length dystrophin forced expression in cultured skeletal myotubes

Cited by 24 publications

References 55 publications

Negative modulation of inositol 1,4,5-trisphosphate type 1 receptor expression prevents dystrophin-deficient muscle cells death

Negative modulation of inositol 1,4,5-trisphosphate type 1 receptor expression prevents dystrophin-deficient muscle cells death

Involvement of TRPV2 and SOCE in calcium influx disorder in DMD primary human myotubes with a specific contribution of α₁-syntrophin and PLC/PKC in SOCE regulation

Understanding Muscle Architectural Adaptation: Macro- and Micro-Level Research

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Improvement of calcium handling and changes in calcium-release properties after mini- or full-length dystrophin forced expression in cultured skeletal myotubes

Cited by 24 publications

References 55 publications

Negative modulation of inositol 1,4,5-trisphosphate type 1 receptor expression prevents dystrophin-deficient muscle cells death

Negative modulation of inositol 1,4,5-trisphosphate type 1 receptor expression prevents dystrophin-deficient muscle cells death

Involvement of TRPV2 and SOCE in calcium influx disorder in DMD primary human myotubes with a specific contribution of α1-syntrophin and PLC/PKC in SOCE regulation

Understanding Muscle Architectural Adaptation: Macro- and Micro-Level Research

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Involvement of TRPV2 and SOCE in calcium influx disorder in DMD primary human myotubes with a specific contribution of α₁-syntrophin and PLC/PKC in SOCE regulation