Trametinib alters contractility of paediatric Noonan syndrome‐associated hypertrophic myocardial tissue slices

Abstract Aims No curative treatment is available for RASopathy‐associated childhood‐onset hypertrophic cardiomyopathy (RAS‐CM). Preclinical data and individual reports suggest a beneficial effect of small molecules targeting the RAS–mitogen‐activated protein (MAP) kinase (MAPK) pathway in severely a...

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Main Authors: Jules Hamers, Payel Sen, Sarala Raj Murthi, Laura Papanakli, Maria vonStumm, Francesca Baessato, Julie Cleuziou, Christian Meierhofer, Peter Ewert, Andreas Dendorfer, Daphne Merkus, Cordula M. Wolf
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Language:English
Published: Wiley 2025-06-01
Series:ESC Heart Failure
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Online Access:https://doi.org/10.1002/ehf2.15173
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author Jules Hamers
Payel Sen
Sarala Raj Murthi
Laura Papanakli
Maria vonStumm
Francesca Baessato
Julie Cleuziou
Christian Meierhofer
Peter Ewert
Andreas Dendorfer
Daphne Merkus
Cordula M. Wolf
author_facet Jules Hamers
Payel Sen
Sarala Raj Murthi
Laura Papanakli
Maria vonStumm
Francesca Baessato
Julie Cleuziou
Christian Meierhofer
Peter Ewert
Andreas Dendorfer
Daphne Merkus
Cordula M. Wolf
author_sort Jules Hamers
collection DOAJ
description Abstract Aims No curative treatment is available for RASopathy‐associated childhood‐onset hypertrophic cardiomyopathy (RAS‐CM). Preclinical data and individual reports suggest a beneficial effect of small molecules targeting the RAS–mitogen‐activated protein (MAP) kinase (MAPK) pathway in severely affected RAS‐CM patients. The aim of this study was to evaluate the biophysical effects of trametinib, rapamycin and dasatinib on cultivated myocardial tissue slices of a paediatric RAS‐CM patient using biomimetic cultivation chambers (BMCCs) and to correlate the findings with clinical data. Methods Contracting right ventricular (RV) tissue slices were prepared from resected myocardium, cultivated in BMCCs and treated with distinct molecules directly and indirectly targeting the RAS–MAPK pathway (trametinib, rapamycin and dasatinib) or dimethyl sulfoxide (DMSO). Tissue biophysical properties were assessed using electrical stimulation protocols. Contractile function, force–frequency relationship and post‐pause potentiation were compared before and after treatment. These parameters correlated to L‐type Ca2+ channel function and sarcoplasmic Ca2+ loading. Results In vivo, off‐label treatment with MAPK kinase (MEK) inhibitor trametinib of a child with severe RAS‐CM resulted in a modest reduction of RV outflow tract (RVOT) obstruction (RVOT 151 to 122 mmHg after 11 weeks) and improved diastolic function (E/A 0.68 to 1.09 after 11 weeks) and myocardial strain [RV global radial strain (RV‐GRS) 25.94 to 42.76; RV global circumferential strain (RV‐GCS) −15.26 to −18.61; and RV global longitudinal strain (RV‐GLS) −10.31 to −16.78 at 11 weeks], as determined by echocardiography and cardiac magnetic resonance tomography. In cultivated RV myocardial tissue slices, contraction force decreased after addition of trametinib and rapamycin but not after addition of DMSO and dasatinib. Improvement of Ca2+ handling, as depicted by a more positive force–frequency relationship and enhanced post‐pause potentiation (31.2%), was noted in the trametinib‐treated slice. The increase in post‐pause potentiation was less pronounced in rapamycin‐treated (26%) and absent in dasatinib‐treated (<1%) slices. Conclusions Ex vivo analysis of cultivated and electrically stimulated RV myocardial tissue slices of a patient with RAS‐CM showed decreased contractility and improved sarcoplasmic reticulum function after addition of trametinib and in part after addition of rapamycin, but not after addition of dasatinib.
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spelling doaj-art-631b87093e034ed6865b48e925ce2d7a2025-08-20T03:11:21ZengWileyESC Heart Failure2055-58222025-06-011232321233410.1002/ehf2.15173Trametinib alters contractility of paediatric Noonan syndrome‐associated hypertrophic myocardial tissue slicesJules Hamers0Payel Sen1Sarala Raj Murthi2Laura Papanakli3Maria vonStumm4Francesca Baessato5Julie Cleuziou6Christian Meierhofer7Peter Ewert8Andreas Dendorfer9Daphne Merkus10Cordula M. Wolf11Institute of Surgical Research at the Walter Brendel Centre of Experimental Medicine University Hospital of Munich, LMU Munich Munich GermanyInstitute of Surgical Research at the Walter Brendel Centre of Experimental Medicine University Hospital of Munich, LMU Munich Munich GermanyDepartment of Congenital Heart Defects and Paediatric Cardiology German Heart Centre Munich, Technical University of Munich School of Medicine and Health Munich GermanyDepartment of Congenital Heart Defects and Paediatric Cardiology German Heart Centre Munich, Technical University of Munich School of Medicine and Health Munich GermanyDepartment of Congenital and Pediatric Heart Surgery German Heart Centre Munich, Technical University of Munich, School of Medicine and Health Munich GermanyDepartment of Congenital Heart Defects and Paediatric Cardiology German Heart Centre Munich, Technical University of Munich School of Medicine and Health Munich GermanyDepartment of Congenital and Pediatric Heart Surgery German Heart Centre Munich, Technical University of Munich, School of Medicine and Health Munich GermanyDepartment of Congenital Heart Defects and Paediatric Cardiology German Heart Centre Munich, Technical University of Munich School of Medicine and Health Munich GermanyGerman Centre for Cardiovascular Research (DZHK), Partner Site Munich, Munich Heart Alliance (MHA) Munich GermanyInstitute of Surgical Research at the Walter Brendel Centre of Experimental Medicine University Hospital of Munich, LMU Munich Munich GermanyInstitute of Surgical Research at the Walter Brendel Centre of Experimental Medicine University Hospital of Munich, LMU Munich Munich GermanyGerman Centre for Cardiovascular Research (DZHK), Partner Site Munich, Munich Heart Alliance (MHA) Munich GermanyAbstract Aims No curative treatment is available for RASopathy‐associated childhood‐onset hypertrophic cardiomyopathy (RAS‐CM). Preclinical data and individual reports suggest a beneficial effect of small molecules targeting the RAS–mitogen‐activated protein (MAP) kinase (MAPK) pathway in severely affected RAS‐CM patients. The aim of this study was to evaluate the biophysical effects of trametinib, rapamycin and dasatinib on cultivated myocardial tissue slices of a paediatric RAS‐CM patient using biomimetic cultivation chambers (BMCCs) and to correlate the findings with clinical data. Methods Contracting right ventricular (RV) tissue slices were prepared from resected myocardium, cultivated in BMCCs and treated with distinct molecules directly and indirectly targeting the RAS–MAPK pathway (trametinib, rapamycin and dasatinib) or dimethyl sulfoxide (DMSO). Tissue biophysical properties were assessed using electrical stimulation protocols. Contractile function, force–frequency relationship and post‐pause potentiation were compared before and after treatment. These parameters correlated to L‐type Ca2+ channel function and sarcoplasmic Ca2+ loading. Results In vivo, off‐label treatment with MAPK kinase (MEK) inhibitor trametinib of a child with severe RAS‐CM resulted in a modest reduction of RV outflow tract (RVOT) obstruction (RVOT 151 to 122 mmHg after 11 weeks) and improved diastolic function (E/A 0.68 to 1.09 after 11 weeks) and myocardial strain [RV global radial strain (RV‐GRS) 25.94 to 42.76; RV global circumferential strain (RV‐GCS) −15.26 to −18.61; and RV global longitudinal strain (RV‐GLS) −10.31 to −16.78 at 11 weeks], as determined by echocardiography and cardiac magnetic resonance tomography. In cultivated RV myocardial tissue slices, contraction force decreased after addition of trametinib and rapamycin but not after addition of DMSO and dasatinib. Improvement of Ca2+ handling, as depicted by a more positive force–frequency relationship and enhanced post‐pause potentiation (31.2%), was noted in the trametinib‐treated slice. The increase in post‐pause potentiation was less pronounced in rapamycin‐treated (26%) and absent in dasatinib‐treated (<1%) slices. Conclusions Ex vivo analysis of cultivated and electrically stimulated RV myocardial tissue slices of a patient with RAS‐CM showed decreased contractility and improved sarcoplasmic reticulum function after addition of trametinib and in part after addition of rapamycin, but not after addition of dasatinib.https://doi.org/10.1002/ehf2.15173cultivationmyocardial slicesNoonanRAF1trametinib
spellingShingle Jules Hamers
Payel Sen
Sarala Raj Murthi
Laura Papanakli
Maria vonStumm
Francesca Baessato
Julie Cleuziou
Christian Meierhofer
Peter Ewert
Andreas Dendorfer
Daphne Merkus
Cordula M. Wolf
Trametinib alters contractility of paediatric Noonan syndrome‐associated hypertrophic myocardial tissue slices
ESC Heart Failure
cultivation
myocardial slices
Noonan
RAF1
trametinib
title Trametinib alters contractility of paediatric Noonan syndrome‐associated hypertrophic myocardial tissue slices
title_full Trametinib alters contractility of paediatric Noonan syndrome‐associated hypertrophic myocardial tissue slices
title_fullStr Trametinib alters contractility of paediatric Noonan syndrome‐associated hypertrophic myocardial tissue slices
title_full_unstemmed Trametinib alters contractility of paediatric Noonan syndrome‐associated hypertrophic myocardial tissue slices
title_short Trametinib alters contractility of paediatric Noonan syndrome‐associated hypertrophic myocardial tissue slices
title_sort trametinib alters contractility of paediatric noonan syndrome associated hypertrophic myocardial tissue slices
topic cultivation
myocardial slices
Noonan
RAF1
trametinib
url https://doi.org/10.1002/ehf2.15173
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