The intrinsically disordered C terminus of troponin T binds to troponin C to modulate myocardial force generation

Aberrant regulation of myocardial force production represents an early biomechanical defect associated with sarcomeric cardiomyopathies, but the molecular mechanisms remain poorly defined. Here, we evaluated the pathogenicity of a previously unreported sarcomeric gene variant identified in a pediatr...

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Detalles Bibliográficos
Autores: Jamie R. Johnston, Einat Birk, Nili Zucker, Jerson Lima da Silva, P. Bryant Chase, Jose Renato Pinto, Maicon Landim-vieira, Mayra de Amorim Marques, Guilherme A. P. de Oliveira, David Gonzalez-martinez, Adolfo Henrique de Moraes Silva, Huan he, Anwar Iqbal, Yael Wilnai
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2019
País:Brasil
Institución:Universidade Federal de Minas Gerais (UFMG)
Repositorio:Repositório Institucional da UFMG
Idioma:inglés
OAI Identifier:oai:repositorio.ufmg.br:1843/46345
Acceso en línea:https://doi.org/10.1074/jbc.RA119.011177
http://hdl.handle.net/1843/46345
https://orcid.org/0000-0002-6696-8888
https://orcid.org/0000-0002-0063-5888
https://orcid.org/0000-0001-9523-9441
https://orcid.org/0000-0001-9701-561X
https://orcid.org/0000-0001-9092-4976
https://orcid.org/0000-0002-4131-4634
Access Level:acceso abierto
Palabra clave:Cardiac muscle contractile
Contractile protein
Protein dynamic
Structure–function
Cardiovascular disease
Cardiomyopathy
Cross-bridges
NMR
Troponin
Espectroscopia de ressonância nuclear
Ressonância magnética nuclear
Miocárdio
Doenças
Descripción
Sumario:Aberrant regulation of myocardial force production represents an early biomechanical defect associated with sarcomeric cardiomyopathies, but the molecular mechanisms remain poorly defined. Here, we evaluated the pathogenicity of a previously unreported sarcomeric gene variant identified in a pediatric patient with sporadic dilated cardiomyopathy, and we determined a molecular mechanism. Trio whole-exome sequencing revealed a de novo missense variant in TNNC1 that encodes a p.I4M substitution in the N-terminal helix of cardiac troponin C (cTnC). Reconstitution of this human cTnC variant into permeabilized porcine cardiac muscle preparations significantly decreases the magnitude and rate of isometric force generation at physiological Ca2+-activation levels. Computational modeling suggests that this inhibitory effect can be explained by a decrease in the rates of cross-bridge attachment and detachment. For the first time, we show that cardiac troponin T (cTnT), in part through its intrinsically disordered C terminus, directly binds to WT cTnC, and we find that this cardiomyopathic variant displays tighter binding to cTnT. Steady-state fluorescence and NMR spectroscopy studies suggest that this variant propagates perturbations in cTnC structural dynamics to distal regions of the molecule. We propose that the intrinsically disordered C terminus of cTnT directly interacts with the regulatory N-domain of cTnC to allosterically modulate Ca2+ activation of force, perhaps by controlling the troponin I switching mechanism of striated muscle contraction. Alterations in cTnC–cTnT binding may compromise contractile performance and trigger pathological remodeling of the myocardium.