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Lessons from calsequestrin-1 ablation in vivo: much more than a Ca2+ buffer after all

  • EMC2011 special issue
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Abstract

Calsequestrin type-1 (CASQ1), the main sarcoplasmic reticulum (SR) Ca2+ binding protein, plays a dual role in skeletal fibers: a) it provides a large pool of rapidly-releasable Ca2+ during excitation–contraction (EC) coupling; and b) it modulates the activity of ryanodine receptors (RYRs), the SR Ca2+ release channels. We have generated a mouse lacking CASQ1 in order to further characterize the role of CASQ1 in skeletal muscle. Contrary to initial expectations, CASQ1 ablation is compatible with normal motor activity, in spite of moderate muscle atrophy. However, CASQ1 deficiency results in profound remodeling of the EC coupling apparatus: shrinkage of junctional SR lumen; proliferation of SR/transverse-tubule contacts; and increased density of RYRs. While force development during a twitch is preserved, it is nevertheless characterized by a prolonged time course, likely reflecting impaired Ca2+ re-uptake by the SR. Finally, lack of CASQ1 also results in increased rate of SR Ca2+ depletion and inability of muscle to sustain tension during a prolonged tetani. All modifications are more pronounced (or only found) in fast-twitch extensor digitorum longus muscle compared to slow-twitch soleus muscle, likely because the latter expresses higher amounts of calsequestrin type-2 (CASQ2). Surprisingly, male CASQ1-null mice also exhibit a marked increased rate of spontaneous mortality suggestive of a stress-induced phenotype. Consistent with this idea, CASQ1-null mice exhibit an increased susceptibility to undergo a hypermetabolic syndrome characterized by whole body contractures, rhabdomyolysis, hyperthermia and sudden death in response to halothane- and heat-exposure, a phenotype remarkably similar to human malignant hyperthermia and environmental heat-stroke. The latter findings validate the CASQ1 gene as a candidate for linkage analysis in human muscle disorders.

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Abbreviations

Ca2+ :

Calcium ions

CASQ1 and CASQ2:

Skeletal and cardiac isoform of calsequestrin

CPVT:

Catecholaminergic polymorphic ventricular tachycardia

CRUs:

Calcium release units

EC coupling:

Excitation–contraction coupling

EDL:

Extensor digitorum longus

EHS:

Environmental heat-stroke

EM:

Electron microscopy

FDB:

Flexor digitorum brevis

MH:

Malignant hyperthermia

MHC:

Myosin heavy-chain

RYR1:

Ryanodine receptor type-1

SERCA:

Sarco-endoplasmic reticulum Ca2+ ATP-ase

SOCE:

Store-operated Ca2+ entry

SR:

Sarcoplasmic reticulum

TnC:

Troponin-C

T-tubule:

Transverse tubule

WT:

Wild type

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Acknowledgments

This study was supported by Research Grant # GGP08153 from the Italian Telethon ONLUS Foundation to FP and CR. We also thank Drs. P.D. Allen, P. Volpe, A. Nori, and R.T. Dirksen for the collaboration provided in generating mice and in crucial experiments (see Paolini et al. 2007; Dainese et al. 2009; Paolini et al. 2011b).

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  1. IIM – Interuniversitary Institute of Myology http://www.coram-iim.it/iim/index.asp

    Feliciano Protasi, Cecilia Paolini, Marta Canato, Carlo Reggiani & Marco Quarta

  2. CeSI-Center for Research on Ageing & DNI-Department of Neuroscience and Imaging, University Gabriele d’Annunzio of Chieti, Via Colle dell’Ara, 66100, Chieti, Italy

    Feliciano Protasi & Cecilia Paolini

  3. Department of Anatomy and Physiology, University of Padova, 35131, Padua, Italy

    Marta Canato, Carlo Reggiani & Marco Quarta

  4. Department of Neurology and Neurological Sciences, Stanford University, Palo Alto, CA, 94304, USA

    Marco Quarta

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  1. Feliciano Protasi
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  2. Cecilia Paolini
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  3. Marta Canato
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  4. Carlo Reggiani
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  5. Marco Quarta
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Correspondence to Feliciano Protasi.

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Protasi, F., Paolini, C., Canato, M. et al. Lessons from calsequestrin-1 ablation in vivo: much more than a Ca2+ buffer after all. J Muscle Res Cell Motil 32, 257–270 (2011). https://doi.org/10.1007/s10974-011-9277-2

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  • DOI: https://doi.org/10.1007/s10974-011-9277-2

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