Literature DB >> 23508784

Perturbed length-dependent activation in human hypertrophic cardiomyopathy with missense sarcomeric gene mutations.

Vasco Sequeira1, Paul J M Wijnker, Louise L A M Nijenkamp, Diederik W D Kuster, Aref Najafi, E Rosalie Witjas-Paalberends, Jessica A Regan, Nicky Boontje, Folkert J Ten Cate, Tjeerd Germans, Lucie Carrier, Sakthivel Sadayappan, Marjon A van Slegtenhorst, Ruud Zaremba, D Brian Foster, Anne M Murphy, Corrado Poggesi, Cris Dos Remedios, Ger J M Stienen, Carolyn Y Ho, Michelle Michels, Jolanda van der Velden.   

Abstract

RATIONALE: High-myofilament Ca(2+) sensitivity has been proposed as a trigger of disease pathogenesis in familial hypertrophic cardiomyopathy (HCM) on the basis of in vitro and transgenic mice studies. However, myofilament Ca(2+) sensitivity depends on protein phosphorylation and muscle length, and at present, data in humans are scarce.
OBJECTIVE: To investigate whether high myofilament Ca(2+) sensitivity and perturbed length-dependent activation are characteristics for human HCM with mutations in thick and thin filament proteins. METHODS AND
RESULTS: Cardiac samples from patients with HCM harboring mutations in genes encoding thick (MYH7, MYBPC3) and thin (TNNT2, TNNI3, TPM1) filament proteins were compared with sarcomere mutation-negative HCM and nonfailing donors. Cardiomyocyte force measurements showed higher myofilament Ca(2+) sensitivity in all HCM samples and low phosphorylation of protein kinase A (PKA) targets compared with donors. After exogenous PKA treatment, myofilament Ca(2+) sensitivity was similar (MYBPC3mut, TPM1mut, sarcomere mutation-negative HCM), higher (MYH7mut, TNNT2mut), or even significantly lower (TNNI3mut) compared with donors. Length-dependent activation was significantly smaller in all HCM than in donor samples. PKA treatment increased phosphorylation of PKA-targets in HCM myocardium and normalized length-dependent activation to donor values in sarcomere mutation-negative HCM and HCM with truncating MYBPC3 mutations but not in HCM with missense mutations. Replacement of mutant by wild-type troponin in TNNT2mut and TNNI3mut corrected length-dependent activation to donor values.
CONCLUSIONS: High-myofilament Ca(2+) sensitivity is a common characteristic of human HCM and partly reflects hypophosphorylation of PKA targets compared with donors. Length-dependent sarcomere activation is perturbed by missense mutations, possibly via posttranslational modifications other than PKA hypophosphorylation or altered protein-protein interactions, and represents a common pathomechanism in HCM.

Entities:  

Keywords:  calcium; cardiomyopathy; contractility; hypertrophy; myocardium

Mesh:

Substances:

Year:  2013        PMID: 23508784      PMCID: PMC3675884          DOI: 10.1161/CIRCRESAHA.111.300436

Source DB:  PubMed          Journal:  Circ Res        ISSN: 0009-7330            Impact factor:   17.367


  70 in total

1.  Myofilament Ca sensitization increases cytosolic Ca binding affinity, alters intracellular Ca homeostasis, and causes pause-dependent Ca-triggered arrhythmia.

Authors:  Tilmann Schober; Sabine Huke; Raghav Venkataraman; Oleksiy Gryshchenko; Dmytro Kryshtal; Hyun Seok Hwang; Franz J Baudenbacher; Björn C Knollmann
Journal:  Circ Res       Date:  2012-05-29       Impact factor: 17.367

2.  Length dependence of Ca(2+)-tension relationship in aequorin-injected ferret papillary muscles.

Authors:  K Komukai; S Kurihara
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3.  Multiple reaction monitoring to identify site-specific troponin I phosphorylated residues in the failing human heart.

Authors:  Pingbo Zhang; Jonathan A Kirk; Weihua Ji; Cristobal G dos Remedios; David A Kass; Jennifer E Van Eyk; Anne M Murphy
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4.  Familial hypertrophic cardiomyopathy-linked mutant troponin T causes stress-induced ventricular tachycardia and Ca2+-dependent action potential remodeling.

Authors:  Björn C Knollmann; Paulus Kirchhof; Syevda G Sirenko; Hubertus Degen; Anne E Greene; Tilmann Schober; Jessica C Mackow; Larissa Fabritz; James D Potter; Martin Morad
Journal:  Circ Res       Date:  2003-02-06       Impact factor: 17.367

5.  Phosphorylation of tropomyosin extends cooperative binding of myosin beyond a single regulatory unit.

Authors:  Vijay S Rao; Ellisha N Marongelli; William H Guilford
Journal:  Cell Motil Cytoskeleton       Date:  2009-01

6.  Familial hypertrophic cardiomyopathy-related cardiac troponin C mutation L29Q affects Ca2+ binding and myofilament contractility.

Authors:  Bo Liang; Franca Chung; Yang Qu; Dmitri Pavlov; Todd E Gillis; Svetlana B Tikunova; Jonathan P Davis; Glen F Tibbits
Journal:  Physiol Genomics       Date:  2008-02-19       Impact factor: 3.107

7.  How do hypertrophic cardiomyopathy mutations affect myocardial function in carriers with normal wall thickness? Assessment with cardiovascular magnetic resonance.

Authors:  Tjeerd Germans; Iris K Rüssel; Marco J W Götte; Marieke D Spreeuwenberg; Pieter A Doevendans; Yigal M Pinto; Rob J van der Geest; Jolanda van der Velden; Arthur A M Wilde; Albert C van Rossum
Journal:  J Cardiovasc Magn Reson       Date:  2010-03-15       Impact factor: 5.364

8.  Effect of length and cross-bridge attachment on Ca2+ binding to cardiac troponin C.

Authors:  P A Hofmann; F Fuchs
Journal:  Am J Physiol       Date:  1987-07

9.  Structural interpretation of the mutations in the beta-cardiac myosin that have been implicated in familial hypertrophic cardiomyopathy.

Authors:  I Rayment; H M Holden; J R Sellers; L Fananapazir; N D Epstein
Journal:  Proc Natl Acad Sci U S A       Date:  1995-04-25       Impact factor: 11.205

10.  Increased myofilament Ca2+ sensitivity and diastolic dysfunction as early consequences of Mybpc3 mutation in heterozygous knock-in mice.

Authors:  Bodvaël Fraysse; Florian Weinberger; Sonya C Bardswell; Friederike Cuello; Nicolas Vignier; Birgit Geertz; Jutta Starbatty; Elisabeth Krämer; Catherine Coirault; Thomas Eschenhagen; Jonathan C Kentish; Metin Avkiran; Lucie Carrier
Journal:  J Mol Cell Cardiol       Date:  2012-03-23       Impact factor: 5.000

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  107 in total

1.  Rapid large-scale purification of myofilament proteins using a cleavable His6-tag.

Authors:  Mengjie Zhang; Jody L Martin; Mohit Kumar; Ramzi J Khairallah; Pieter P de Tombe
Journal:  Am J Physiol Heart Circ Physiol       Date:  2015-09-18       Impact factor: 4.733

2.  Cardiac Myosin-binding Protein C and Troponin-I Phosphorylation Independently Modulate Myofilament Length-dependent Activation.

Authors:  Mohit Kumar; Suresh Govindan; Mengjie Zhang; Ramzi J Khairallah; Jody L Martin; Sakthivel Sadayappan; Pieter P de Tombe
Journal:  J Biol Chem       Date:  2015-10-09       Impact factor: 5.157

Review 3.  Cardiac myosin-binding protein C: hypertrophic cardiomyopathy mutations and structure-function relationships.

Authors:  Vasco Sequeira; E Rosalie Witjas-Paalberends; Diederik W D Kuster; Jolanda van der Velden
Journal:  Pflugers Arch       Date:  2013-11-17       Impact factor: 3.657

Review 4.  Modelling sarcomeric cardiomyopathies with human cardiomyocytes derived from induced pluripotent stem cells.

Authors:  Lorenzo R Sewanan; Stuart G Campbell
Journal:  J Physiol       Date:  2019-02-06       Impact factor: 5.182

Review 5.  Phenotyping cardiomyopathy in adult zebrafish.

Authors:  Alexey V Dvornikov; Pieter P de Tombe; Xiaolei Xu
Journal:  Prog Biophys Mol Biol       Date:  2018-05-30       Impact factor: 3.667

6.  Length-dependent activation is modulated by cardiac troponin I bisphosphorylation at Ser23 and Ser24 but not by Thr143 phosphorylation.

Authors:  Paul J M Wijnker; Vasco Sequeira; D Brian Foster; Yuejin Li; Cristobal G Dos Remedios; Anne M Murphy; Ger J M Stienen; Jolanda van der Velden
Journal:  Am J Physiol Heart Circ Physiol       Date:  2014-02-28       Impact factor: 4.733

7.  Computationally efficient model of myocardial electromechanics for multiscale simulations.

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8.  Altered C10 domain in cardiac myosin binding protein-C results in hypertrophic cardiomyopathy.

Authors:  Diederik W D Kuster; Thomas L Lynch; David Y Barefield; Mayandi Sivaguru; Gina Kuffel; Michael J Zilliox; Kyoung Hwan Lee; Roger Craig; Rajasekaran Namakkal-Soorappan; Sakthivel Sadayappan
Journal:  Cardiovasc Res       Date:  2019-12-01       Impact factor: 10.787

9.  Phosphorylation of protein kinase C sites Ser42/44 decreases Ca(2+)-sensitivity and blunts enhanced length-dependent activation in response to protein kinase A in human cardiomyocytes.

Authors:  Paul J M Wijnker; Vasco Sequeira; E Rosalie Witjas-Paalberends; D Brian Foster; Cristobal G dos Remedios; Anne M Murphy; Ger J M Stienen; Jolanda van der Velden
Journal:  Arch Biochem Biophys       Date:  2014-05-09       Impact factor: 4.013

10.  Contractile dysfunction in a mouse model expressing a heterozygous MYBPC3 mutation associated with hypertrophic cardiomyopathy.

Authors:  David Barefield; Mohit Kumar; Pieter P de Tombe; Sakthivel Sadayappan
Journal:  Am J Physiol Heart Circ Physiol       Date:  2014-01-24       Impact factor: 4.733

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