Skip to main content
SpringerLink
Log in

Characterization of fast-twitch and slow-twitch skeletal muscles of calsequestrin 2 (CASQ2)-knock out mice: unexpected adaptive changes of fast-twitch muscles only

  • Published:
Journal of Muscle Research and Cell Motility Aims and scope Submit manuscript

Abstract

This study investigates the functional role of calsequestrin 2 (CASQ2) in both fast-twitch and slow-twitch skeletal muscles by using CASQ2−/− mice; CASQ2 is expressed throughout life in slow-twitch muscles, but only in the developmental and neonatal stages in fast-twitch muscles. CASQ2−/− causes increase in calsequestrin 1 (CASQ1) expression, but without functional changes in both muscle types. CASQ2−/− mice have ultrastructural changes in fast-twitch muscles only, i.e., formation of pentads and stacks in the sarcoplasmic reticulum.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

CRT:

Calreticulin

CASQ1:

Calsequestrin 1

CASQ2:

Calsequestrin 2

KO:

CASQ2−/−

CPVT:

Catecholaminergic polymorphic ventricular tachycardia

ER:

Endoplasmic reticulum

ECCE:

Excitation-coupled calcium entry

EDL:

Extensor digitorum longus

FDB:

Flexor digitorum longus

GRP78:

Glucose related protein 78

GRP94:

Glucose-related protein 94

LSR:

Longitudinal SR

SR:

Sarcoplasmic reticulum

SOL:

Soleus

TC:

Terminal cisternae

T-tubules:

Transverse tubules

WT:

Wild type

DD:

Days

References

  • Amoasii L, Hnia K, Chicanne G, Brech A, Cowling BS, Müller MM, Schwab Y, Koebel P, Ferry A, Payrastre B, Laporte J (2013) Myotubularin and PtdIns3P remodel the sarcoplasmic reticulum in muscle in vivo. J Cell Sci 126:1806–1819

    Article  CAS  PubMed  Google Scholar 

  • Arai M, Otsu K, MacLennan DH, Periasamy M (1992) Regulation of sarcoplasmic reticulum gene expression during cardiac and skeletal development. Am J Physiol 262:C614–C620

    CAS  PubMed  Google Scholar 

  • Biral D, Volpe P, Damiani E, Margreth A (1992) Coexistence of two calsequestrin isoforms in slow-twitch skeletal muscle fibers. FEBS Lett 299:175–178

    Article  CAS  PubMed  Google Scholar 

  • Boncompagni S, Thomas M, Lopez JR, Allen PD, Yuan Q, Kranias EG, Franzini-Armstrong C, Perez CF (2012) Triadin/Junctin double null mouse reveals a differential role for triadin and junctin in anchoring CASQ to the jSR and regulating Ca2+ homeostasis. PLoS One 7:1–12

  • Damiani E, Volpe P, Margreth A (1990) Coexpression of two isoforms of calsequestrin in rabbit slow-twitch muscle. J Muscle Res Cell Motil 11:522–530

    Article  CAS  PubMed  Google Scholar 

  • Denegri M, Cruz JEE, Boncompagni S, De Simone S, Auricchio A, Villani L, Volpe P, Protasi F, Napolitano C, Priori SG (2012) Viral gene transfer rescues arrhythmogenic phenotype and ultrastructural abnormalities in adult calsequestrin-null mice with inherited arrhythmias. Circ Res 110:663–668

    Article  CAS  PubMed  Google Scholar 

  • Engel AG (1994) Ultrastructural changes in diseased muscles. In: Engel AG, Franzini-Armstrong C (eds) Myology, 3rd edn. McGraw-Hill, NY, 749–888

    Google Scholar 

  • Ferretti R, Marques MJ, Pertille A, Santo Neto H (2009) Sarcoplasmic-endoplasmic-reticulum Ca2+-ATPase and calsequestrin are overexpressed in spared intrinsic laryngeal muscles of dystrophin-deficient mdx mice. Muscle Nerve 39:609–615

    Article  CAS  PubMed  Google Scholar 

  • Franzini-Armstrong C (1991) Simultaneous maturation of transverse tubule and sarcoplasmic reticulum during muscle differentiation in the mouse. Dev Biol 146:353–363

    Article  CAS  PubMed  Google Scholar 

  • Franzini-Armstrong C (2012) Junctophilins and SR docking in muscle. FASEB J 26:1774

    Article  CAS  PubMed  Google Scholar 

  • Franzini-Armstrong C, Jorgensen AO (1994) Structure and development of E-C coupling units in skeletal muscle. Annu Rev Physiol 56:509–534

    Article  CAS  PubMed  Google Scholar 

  • Kinnunen S, Mänttäri S (2012) Specific effects of endurance and sprint training on protein expression of calsequestrin and SERCA in mouse skeletal muscle. J Muscle Res Cell Motil 33:123–130

    Article  CAS  PubMed  Google Scholar 

  • Knollmann BC, Chopra N, Hlaing T, Akin B, Yang T, Ettensohn K, Knollmann BE, Horton KD, Weissman NJ, Holinstat I, Zhang W, Roden DM, Jones LR, Franzini-Armstrong C, Pfeifer K (2006) Casq2 deletion causes sarcoplasmic reticulum volume increase, premature Ca2+ release, and catecholaminergic polymorphic ventricular tachycardia. J Clin Invest 116:2510–2520

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ko JK, Choi KH, Zhao X, Komazaki S, Pan Z, Weisleder N, Ma J (2011) A versatile single-plasmid system for tissue-specific and inducible control of gene expression in transgenic mice. FASEB J 25:2638–2649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lahat H, Pras E, Olender T, Avidan N, Ben-Asher E, Man O, Levy-Nissenbaum E, Khoury A, Lorber A, Goldman B, Lancet D, Eldar M (2001) A missense mutation in a highly conserved region of CASQ2 is associated with autosomal recessive catecholamine-induced polymorphic ventricular tachycardia in Bedouin families from Israel. Am J Hum Genet 69:1378–1384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamboley CR, Murphy RM, McKenna MJ, Lamb GD (2013) Endogenous and maximal sarcoplasmic reticulum calcium content and calsequestrin expression in type I and type II human skeletal muscle fibres. J Physiol 591:6053–6068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leberer E, Pette D (1986) Immunochemical quantification of sarcoplasmic reticulum Ca-ATPase, of calsequestrin and of parvalbumin in rabbit skeletal muscles of defined fiber composition. Eur J Biochem 156:489–496

    Article  CAS  PubMed  Google Scholar 

  • Lehotský J, Bezáková G, Kaplán P, Raeymaekers L (1993) Distribution of Ca2+ modulating proteins in sarcoplasmic reticulum membranes after denervation. Gen Physiol Biophys 12:339–348

    PubMed  Google Scholar 

  • Mosca B, Eckhardt J, Bergamelli L, Treves S, Bongianino R, De Negri M, Priori SG, Protasi F, Zorzato F (2016) Role of the JP45-calsequestrin complex on calcium entry in slow twitch skeletal muscles. J Biol Chem 291: 4555–4565

    Google Scholar 

  • Murphy RM, Larkins NT, Mollica JP, Beard NA, Lamb GD (2009) Calsequestrin content and SERCA determine normal and maximal Ca2+ storage levels in sarcoplasmic reticulum of fast- and slow-twitch fibres of rat. J Physiol 587:443–460

    Article  CAS  PubMed  Google Scholar 

  • Paolini C, Quarta M, Nori A, Boncompagni S, Canato M, Volpe P, Allen PD, Reggiani C, Protasi F (2007) Re-organized stores and impaired calcium handling in skeletal muscle of mice lacking calsequestrin-1. J Physiol 583:767–784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pellegrino MA, Canepari M, Rossi R, D’Antona G, Reggiani C, Bottinelli R (2003) Orthologous myosin isoforms and scaling of shortening velocity with body size in mouse, rat, rabbit and human muscles. J Physiol 546:677–689

    Article  CAS  PubMed  Google Scholar 

  • Raffaele di Barletta M, Viatcheko-Karpinski S, Nori A, Memmi M, Terentyev D, Turcato F, Valle G, Rizzi N, Napolitano C, Gyorke S, Volpe P, Priori SG (2006) Clinical phenotype and functional characterization of CASQ2 mutations associated with catecholaminergic polymorphic ventricular tachycardia. Circulation 114:1012–1019

    Article  Google Scholar 

  • Rizzi N, Liu N, Napolitano C, Nori A, Turcato F, Colombi B, Bicciato S, Arcelli D, Spedito A, Scelsi M, Villani L, Esposito G, Boncompagni S, Protasi F, Volpe P, Priori SG (2008) Unexpected structural and functional consequences of the R33Q homozygous mutation in cardiac calsequestrin. A complex arrhythmogenic cascade in a knock in mouse model. Circ Res 103:298–306

    Article  CAS  PubMed  Google Scholar 

  • Sacchetto R, Volpe P, Damiani E, Margreth A (1993) Postnatal development of rabbit fast-twitch skeletal muscle: accumulation, isoform transition and fiber distribution of calsequestrin. J Muscle Res Cell Motil 14:646–653

    Article  CAS  PubMed  Google Scholar 

  • Salvatori S, Damiani E, Zorzato F, Volpe P, Pierobon S, Quaglino D, Salviati G, Margreth A (1988) Denervation-induced proliferative changes of triads in rabbit skeletal muscle. Muscle Nerve 11:1246–1259

    Article  CAS  PubMed  Google Scholar 

  • Schiaffino S (2012) Tubular aggregates in skeletal muscle: just a special type of protein aggregates? Neuromuscul Disord 22:199–207

    Article  PubMed  Google Scholar 

  • Slupsky JR, Ohnishi M, Carpenter MR, Reithmeier RA (1987) Characterization of cardiac calsequestrin. Biochemistry 26:6539–6544

    CAS  Google Scholar 

  • Song L, Alcalai R, Arad M, Wolf CM, Toka O, Conner DA, Berul CI, Eldar M, Seidman CE, Seidman JG (2007) Calsequestrin 2 (CASQ2) mutations increase expression of calreticulin and ryanodine receptors, causing catecholaminergic polymorphic ventricular tachycardia. J Clin Invest 117:1814–1823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki S, Nagayoshi H, Ishino K, Hino N, Sugi H (2003) Ultrastructural organization of the transverse tubules and the sarcoplasmic reticulum in a fish sound-producing muscle. J Electron Microsc (Tokyo) 52:337–347

    Article  Google Scholar 

  • Takekura H, Kasuga N, Kitada K, Yoshioka T (1996) Morphological changes in the triads and sarcoplasmic reticulum of rat slow and fast muscle fibres following denervation and immobilization. J Muscle Res Cell Motil 17:391–400

    Article  CAS  PubMed  Google Scholar 

  • Valle G, Boncompagni S, Sacchetto R, Protasi F, Volpe P (2014) Post-natal adaptation in a knock-in mouse model of calsequestrin 2-linked recessive catecholaminergic polymorphic ventricular tachycardia. Exp Cell Res 321:178–189

    Article  CAS  PubMed  Google Scholar 

  • Villa A, Podini P, Nori A, Panzeri MC, Martini A, Meldolesi J, Volpe P (1993) The endoplasmic reticulum-sarcoplasmic reticulum connection. II. Postnatal differentiation of the sarcoplasmic reticulum in skeletal muscle fibers. Exp Cell Res 209:140–148

    Article  CAS  PubMed  Google Scholar 

  • Woo JS, Cho CH, Lee KJ, Kim DH, Ma J, Lee EH (2012) Hypertrophy in skeletal myotubes induced by junctophilin-2 mutant, Y141H, involves an increase in store-operated Ca2+ entry via Orai1. J Biol Chem 287:14336–14348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank Silvia G. Priori, Barbara Mosca and Francesco Zorzato for their keen interest in preliminary stages of the work. Funds have been provided by Telethon (Grant GGP11141) and MIUR (Grant 2010BWY8E9) to PV.

Author information

Authors and Affiliations

  1. Dipartimento di Scienze Biomediche dell’Università di Padova, Istituto Interuniversitario di Miologia, Viale G. Colombo 3, 35121, Padova, Italy

    Giorgia Valle, Carlo Reggiani, Edith De Rosa, Alessandra Nori & Pompeo Volpe

  2. Consorzio MIA (Microscopy Image Analysis), Università di Milano-Bicocca, 20052, Monza, Italy

    Barbara Vergani & Antonello Villa

  3. Dipartimento di Biomedicina Comparata ed Alimentazione dell’Università di Padova, Padova, Italy

    Roberta Sacchetto & Lisa Maccatrozzo

Authors
  1. Giorgia Valle
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Barbara Vergani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Roberta Sacchetto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carlo Reggiani
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Edith De Rosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lisa Maccatrozzo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alessandra Nori
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Antonello Villa
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Pompeo Volpe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pompeo Volpe.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Valle, G., Vergani, B., Sacchetto, R. et al. Characterization of fast-twitch and slow-twitch skeletal muscles of calsequestrin 2 (CASQ2)-knock out mice: unexpected adaptive changes of fast-twitch muscles only. J Muscle Res Cell Motil 37, 225–233 (2016). https://doi.org/10.1007/s10974-016-9463-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10974-016-9463-3

Keywords

Search

Navigation