Structural and functional impact of troponin C-mediated Ca2+ sensitization on myofilament lattice spacing and cross-bridge mechanics in mouse cardiac muscle

Gonzalez-Martinez, David; Johnston, Jamie R.; Landim-Vieira, Maicon; Ma, Weikang; Antipova, Olga; Awan, Omar; Irving, Thomas C.; Bryant Chase, P.; Pinto, J. Renato

doi:10.1016/j.yjmcc.2018.08.015

Structural and functional impact of troponin C-mediated Ca²⁺ sensitization on myofilament lattice spacing and cross-bridge mechanics in mouse cardiac muscle

Journal Article · Mon Oct 01 00:00:00 EDT 2018 · Journal of Molecular and Cellular Cardiology

DOI:https://doi.org/10.1016/j.yjmcc.2018.08.015· OSTI ID:1505173

Gonzalez-Martinez, David ^[1]; Johnston, Jamie R. ^[1]; Landim-Vieira, Maicon ^[1]; Ma, Weikang ^[2]; Antipova, Olga ^[3]; Awan, Omar ^[1]; Irving, Thomas C. ^[2]; ^[4]; ^[1]

Florida State Univ., Tallahassee, FL (United States). Dept. of Biomedical Sciences
Illinois Inst. of Technology, Chicago, IL (United States). Dept. of Biological Sciences
Illinois Inst. of Technology, Chicago, IL (United States). Dept. of Biological Sciences; Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS), X-Ray Science Division
Florida State Univ., Tallahassee, FL (United States). Dept. of Biological Science

Acto-myosin cross-bridge kinetics are important for beat-to-beat regulation of cardiac contractility; however, physiological and pathophysiological mechanisms for regulation of contractile kinetics are incompletely understood. Here we explored whether thin filament-mediated Ca²⁺ sensitization influences cross-bridge kinetics in permeabilized, osmotically compressed cardiac muscle preparations. We used a murine model of hypertrophic cardiomyopathy (HCM) harboring a cardiac troponin C (cTnC) Ca²⁺-sensitizing mutation, Ala8Val in the regulatory N-domain. We also treated wild-type murine muscle with bepridil, a cTnC-targeting Ca²⁺ sensitizer. Our findings suggest that both methods of increasing myofilament Ca²⁺ sensitivity increase cross-bridge cycling rate measured by the rate of tension redevelopment (k_TR); force per cross-bridge was also enhanced as measured by sinusoidal stiffness and I_1,1-1/I_1,0 ratio from X-ray diffraction. Computational modeling suggests that Ca²⁺ sensitization through this cTnC mutation or bepridil accelerates k_TR primarily by promoting faster cross-bridge detachment. To elucidate if myofilament structural rearrangements are associated with changes in k(TR), we used small angle X-ray diffraction to simultaneously measure myofilament lattice spacing and isometric force during steady-state Ca²⁺ activations. Within in vivo lattice dimensions, lattice spacing and steady-state isometric force increased significantly at submaximal activation. We conclude that the cTnC N-domain controls force by modulating both the number and rate of cycling cross-bridges, and that the both methods of Ca²⁺ sensitization may act through stabilization of cTnC's D-helix. Furthermore, we propose that the transient expansion of the myofilament lattice during Ca²⁺ activation may be an additional factor that could increase the rate of cross-bridge cycling in cardiac muscle. These findings may have implications for the pathophysiology of HCM.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1505173

Alternate ID(s):: OSTI ID: 1691653
OSTI ID: 1478093

Journal Information:: Journal of Molecular and Cellular Cardiology, Journal Name: Journal of Molecular and Cellular Cardiology Journal Issue: C Vol. 123; ISSN 0022-2828

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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The intrinsically disordered C terminus of troponin T binds to troponin C to modulate myocardial force generation Johnston, Jamie R.; Landim-Vieira, Maicon; Marques, Mayra A. Journal of Biological Chemistry, Vol. 294, Issue 52 https://doi.org/10.1074/jbc.ra119.011177	journal	November 2019

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Related Subjects

60 APPLIED LIFE SCIENCES
Ca2+ sensitivity
bepridil
cardiac thin filament
hypertrophic cardiomyopathy
kinetics of tension redevelopment
myofilament lattice spacing
sinusoidal stiffness
small-angle x-ray diffraction
thin filament
troponin C