Literature DB >> 30778519

Stretching single titin molecules from failing human hearts reveals titin's role in blunting cardiac kinetic reserve.

Mei-Pian Chen1,2, Salome A Kiduko1,2, Nancy S Saad1,2,3, Benjamin D Canan1,2, Ahmet Kilic4, Peter J Mohler1,2,5, Paul M L Janssen1,2,5.   

Abstract

AIMS: Heart failure (HF) patients commonly experience symptoms primarily during elevated heart rates, as a result of physical activities or stress. A main determinant of diastolic passive tension, the elastic sarcomeric protein titin, has been shown to be associated with HF, with unresolved involvement regarding its role at different heart rates. To determine whether titin is playing a role in the heart rate (frequency-) dependent acceleration of relaxation (FDAR). W, we studied the FDAR responses in live human left ventricular cardiomyocytes and the corresponding titin-based passive tension (TPT) from failing and non-failing human hearts. METHODS AND
RESULTS: Using atomic force, we developed a novel single-molecule force spectroscopy approach to detect TPT based on the frequency-modulated cardiac cycle. Mean TPT reduced upon an increased heart rate in non-failing human hearts, while this reduction was significantly blunted in failing human hearts. These mechanical changes in the titin distal Ig domain significantly correlated with the frequency-dependent relaxation kinetics of human cardiomyocytes obtained from the corresponding hearts. Furthermore, the data suggested that the higher the TPT, the faster the cardiomyocytes relaxed, but the lower the potential of myocytes to speed up relaxation at a higher heart rate. Such poorer FDAR response was also associated with a lesser reduction or a bigger increase in TPT upon elevated heart rate.
CONCLUSIONS: Our study established a novel approach in detecting dynamic heart rate relevant tension changes physiologically on native titin domains. Using this approach, the data suggested that the regulation of kinetic reserve in cardiac relaxation and its pathological changes were associated with the intensity and dynamic changes of passive tension by titin. Published on behalf of the European Society of Cardiology. All rights reserved.
© The Author(s) 2019. For permissions, please email: journals.permissions@oup.com.

Entities:  

Keywords:  Atomic force microscopy; Frequency-dependent acceleration of relaxation; Heart failure; Single-molecule force spectroscopy; Titin

Mesh:

Substances:

Year:  2020        PMID: 30778519      PMCID: PMC6918063          DOI: 10.1093/cvr/cvz043

Source DB:  PubMed          Journal:  Cardiovasc Res        ISSN: 0008-6363            Impact factor:   10.787


  65 in total

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Journal:  Circulation       Date:  1992-05       Impact factor: 29.690

2.  Lack of diastolic reserve in patients with heart failure and normal ejection fraction.

Authors:  Sudipta Chattopadhyay; Mohammed F Alamgir; Nikolay P Nikitin; Alan S Rigby; Andrew L Clark; John G F Cleland
Journal:  Circ Heart Fail       Date:  2009-10-22       Impact factor: 8.790

3.  Molecular dissection of N2B cardiac titin's extensibility.

Authors:  K Trombitás; A Freiburg; T Centner; S Labeit; H Granzier
Journal:  Biophys J       Date:  1999-12       Impact factor: 4.033

4.  Elasticity and unfolding of single molecules of the giant muscle protein titin.

Authors:  L Tskhovrebova; J Trinick; J A Sleep; R M Simmons
Journal:  Nature       Date:  1997-05-15       Impact factor: 49.962

5.  Heart failure with preserved ejection fraction is characterized by dynamic impairment of active relaxation and contraction of the left ventricle on exercise and associated with myocardial energy deficiency.

Authors:  Thanh T Phan; Khalid Abozguia; Ganesh Nallur Shivu; Gnanadevan Mahadevan; Ibrar Ahmed; Lynne Williams; Girish Dwivedi; Kiran Patel; Paul Steendijk; Houman Ashrafian; Anke Henning; Michael Frenneaux
Journal:  J Am Coll Cardiol       Date:  2009-07-28       Impact factor: 24.094

6.  Differential changes in titin domain phosphorylation increase myofilament stiffness in failing human hearts.

Authors:  Sebastian Kötter; Laurence Gout; Marion Von Frieling-Salewsky; Anna Eliane Müller; Stefan Helling; Katrin Marcus; Cristobal Dos Remedios; Wolfgang A Linke; Martina Krüger
Journal:  Cardiovasc Res       Date:  2013-06-13       Impact factor: 10.787

7.  Deleting titin's I-band/A-band junction reveals critical roles for titin in biomechanical sensing and cardiac function.

Authors:  Henk L Granzier; Kirk R Hutchinson; Paola Tonino; Mei Methawasin; Frank W Li; Rebecca E Slater; Mathew M Bull; Chandra Saripalli; Christopher T Pappas; Carol C Gregorio; John E Smith
Journal:  Proc Natl Acad Sci U S A       Date:  2014-09-22       Impact factor: 11.205

8.  Blunted frequency-dependent upregulation of cardiac output is related to impaired relaxation in diastolic heart failure.

Authors:  Rolf Wachter; Stephan Schmidt-Schweda; Dirk Westermann; Heiner Post; Frank Edelmann; Mario Kasner; Claus Lüers; Paul Steendijk; Gerd Hasenfuss; Carsten Tschöpe; Burkert Pieske
Journal:  Eur Heart J       Date:  2009-12       Impact factor: 29.983

9.  Titin determines the Frank-Starling relation in early diastole.

Authors:  Michiel Helmes; Chee Chew Lim; Ronglih Liao; Ajit Bharti; Lei Cui; Douglas B Sawyer
Journal:  J Gen Physiol       Date:  2003-02       Impact factor: 4.086

10.  The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunoelectron microscopy: a map of ten nonrepetitive epitopes starting at the Z line extends close to the M line.

Authors:  D O Fürst; M Osborn; R Nave; K Weber
Journal:  J Cell Biol       Date:  1988-05       Impact factor: 10.539

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