Cardiac myosin filaments are directly regulated by calcium

Ma, Weikang; Nag, Suman; Gong, Henry; Qi, Lin; Irving, ThomasC.

doi:10.1085/jgp.202213213

Title: Cardiac myosin filaments are directly regulated by calcium

Journal Article · 01 December 2022 · J. Gen. Physiol.

DOI:https://doi.org/10.1085/jgp.202213213· OSTI ID:1901179

Ma, Weikang; Nag, Suman; Gong, Henry; Qi, Lin; Irving, ThomasC.

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: DOE - Office Of Science; NIGMS; National Institutes of Health (NIH)

OSTI ID:: 1901179

Journal Information:: J. Gen. Physiol., Vol. 154, Issue (12)

Country of Publication:: United States

Language:: ENGLISH

References (50)

Titin strain contributes to the Frank–Starling law of the heart by structural rearrangements of both thin- and thick-filament proteins Ait-Mou, Younss; Hsu, Karen; Farman, Gerrie P. Proceedings of the National Academy of Sciences, Vol. 113, Issue 8 https://doi.org/10.1073/pnas.1516732113	journal	February 2016
Small Molecules Acting on Myofilaments as Treatments for Heart and Skeletal Muscle Diseases Alsulami, Khulud; Marston, Steven International Journal of Molecular Sciences, Vol. 21, Issue 24 https://doi.org/10.3390/ijms21249599	journal	December 2020
Deciphering the super relaxed state of human β-cardiac myosin and the mode of action of mavacamten from myosin molecules to muscle fibers Anderson, Robert L.; Trivedi, Darshan V.; Sarkar, Saswata S. Proceedings of the National Academy of Sciences, Vol. 115, Issue 35 https://doi.org/10.1073/pnas.1809540115	journal	August 2018
Intracellular Ca2+ Sensing: Its Role in Calcium Homeostasis and Signaling Bagur, Rafaela; Hajnóczky, György Molecular Cell, Vol. 66, Issue 6 https://doi.org/10.1016/j.molcel.2017.05.028	journal	June 2017
Inotropic interventions do not change the resting state of myosin motors during cardiac diastole Caremani, Marco; Pinzauti, Francesca; Powers, Joseph D. The Journal of General Physiology, Vol. 151, Issue 1 https://doi.org/10.1085/jgp.201812196	journal	December 2018
The role of the myosin ATPase activity in adaptive thermogenesis by skeletal muscle Cooke, Roger Biophysical Reviews, Vol. 3, Issue 1 https://doi.org/10.1007/s12551-011-0044-9	journal	March 2011
Structural basis of the super- and hyper-relaxed states of myosin II Craig, Roger; Padrón, Raúl Journal of General Physiology, Vol. 154, Issue 1 https://doi.org/10.1085/jgp.202113012	journal	December 2021
Calcium and Excitation-Contraction Coupling in the Heart Eisner, David A.; Caldwell, Jessica L.; Kistamás, Kornél Circulation Research, Vol. 121, Issue 2 https://doi.org/10.1161/CIRCRESAHA.117.310230	journal	July 2017
The Ins and Outs of Mitochondrial Calcium Finkel, Toren; Menazza, Sara; Holmström, Kira M. Circulation Research, Vol. 116, Issue 11 https://doi.org/10.1161/CIRCRESAHA.116.305484	journal	May 2015
The BioCAT undulator beamline 18ID: a facility for biological non-crystalline diffraction and X-ray absorption spectroscopy at the Advanced Photon Source Fischetti, R.; Stepanov, S.; Rosenbaum, G. Journal of Synchrotron Radiation, Vol. 11, Issue 5 https://doi.org/10.1107/S0909049504016760	journal	August 2004
Synthetic thick filaments: A new avenue for better understanding the myosin super-relaxed state in healthy, diseased, and mavacamten-treated cardiac systems Gollapudi, Sampath K.; Yu, Ming; Gan, Qing-Fen Journal of Biological Chemistry, Vol. 296 https://doi.org/10.1074/jbc.RA120.016506	journal	January 2021
A small-molecule inhibitor of sarcomere contractility suppresses hypertrophic cardiomyopathy in mice Green, E. M.; Wakimoto, H.; Anderson, R. L. Science, Vol. 351, Issue 6273 https://doi.org/10.1126/science.aad3456	journal	February 2016
Structural Basis of the Cross-Striations in Muscle Hanson, Jean; Huxley, Hugh E. Nature, Vol. 172, Issue 4377 https://doi.org/10.1038/172530b0	journal	September 1953
X-ray evidence for radial cross-bridge movement and for the sliding filament model in actively contracting skeletal muscle Haselgrove, J. C.; Huxley, H. E. Journal of Molecular Biology, Vol. 77, Issue 4 https://doi.org/10.1016/0022-2836(73)90222-2	journal	July 1973
X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle Huxley, H. E.; Stewart, A.; Sosa, H. Biophysical Journal, Vol. 67, Issue 6 https://doi.org/10.1016/S0006-3495(94)80728-3	journal	December 1994
A small-molecule modulator of cardiac myosin acts on multiple stages of the myosin chemomechanical cycle Kawas, Raja F.; Anderson, Robert L.; Ingle, Sadie R. Bartholomew Journal of Biological Chemistry, Vol. 292, Issue 40 https://doi.org/10.1074/jbc.M117.776815	journal	August 2017
Nebulin stiffens the thin filament and augments cross-bridge interaction in skeletal muscle Kiss, Balázs; Lee, Eun-Jeong; Ma, Weikang Proceedings of the National Academy of Sciences, Vol. 115, Issue 41 https://doi.org/10.1073/pnas.1804726115	journal	September 2018
Calcium-dependent molecular spring elements in the giant protein titin Labeit, D.; Watanabe, K.; Witt, C. Proceedings of the National Academy of Sciences, Vol. 100, Issue 23 https://doi.org/10.1073/pnas.2235652100	journal	October 2003
Ca2+-induced tropomyosin movement in Limulus thin filaments revealed by three-dimensional reconstruction Lehman, William; Craig, Roger; Vibert, Peter Nature, Vol. 368, Issue 6466 https://doi.org/10.1038/368065a0	journal	March 1994
Force generation by skeletal muscle is controlled by mechanosensing in myosin filaments Linari, Marco; Brunello, Elisabetta; Reconditi, Massimo Nature, Vol. 528, Issue 7581 https://doi.org/10.1038/nature15727	journal	November 2015
Myosin dynamics during relaxation in mouse soleus muscle and modulation by 2′‐deoxy‐ATP Ma, Weikang; Childers, Matthew; Murray, Jason The Journal of Physiology, Vol. 598, Issue 22 https://doi.org/10.1113/JP280402	journal	September 2020
Myosin Head Configurations in Resting and Contracting Murine Skeletal Muscle Ma, Weikang; Gong, Henry; Irving, Thomas International Journal of Molecular Sciences, Vol. 19, Issue 9 https://doi.org/10.3390/ijms19092643	journal	September 2018
Myofibril orientation as a metric for characterizing heart disease Ma, Weikang; Gong, Henry; Jani, Vivek Biophysical Journal, Vol. 121, Issue 4 https://doi.org/10.1016/j.bpj.2022.01.009	journal	February 2022
Thick-Filament Extensibility in Intact Skeletal Muscle Ma, Weikang; Gong, Henry; Kiss, Balázs Biophysical Journal, Vol. 115, Issue 8 https://doi.org/10.1016/j.bpj.2018.08.038	journal	October 2018
Response to: Thick Filament Length Changes in Muscle Have Both Elastic and Structural Components Ma, Weikang; Gong, Henry; Kiss, Balazs Biophysical Journal, Vol. 116, Issue 6 https://doi.org/10.1016/j.bpj.2019.02.010	journal	March 2019
The Super-Relaxed State and Length Dependent Activation in Porcine Myocardium Ma, Weikang; Henze, Marcus; Anderson, Robert L. Circulation Research, Vol. 129, Issue 6 https://doi.org/10.1161/CIRCRESAHA.120.318647	journal	September 2021
Small Angle X-ray Diffraction as a Tool for Structural Characterization of Muscle Disease Ma, Weikang; Irving, Thomas C. International Journal of Molecular Sciences, Vol. 23, Issue 6 https://doi.org/10.3390/ijms23063052	journal	March 2022
Regulatory Light Chains in Cardiac Development and Disease Markandran, Kasturi; Poh, Jane Wenjin; Ferenczi, Michael A. International Journal of Molecular Sciences, Vol. 22, Issue 9 https://doi.org/10.3390/ijms22094351	journal	April 2021
X-Ray Diffraction Studies of the Heart Matsubara, I. Annual Review of Biophysics and Bioengineering, Vol. 9, Issue 1 https://doi.org/10.1146/annurev.bb.09.060180.000501	journal	June 1980
Myosin light chain 2 modulates calcium-sensitive cross-bridge transitions in vertebrate skeletal muscle Metzger, J. M.; Moss, R. L. Biophysical Journal, Vol. 63, Issue 2 https://doi.org/10.1016/S0006-3495(92)81614-4	journal	August 1992
Multiscale modeling of twitch contractions in cardiac trabeculae Mijailovich, Srboljub M.; Prodanovic, Momcilo; Poggesi, Corrado Journal of General Physiology, Vol. 153, Issue 3 https://doi.org/10.1085/jgp.202012604	journal	January 2021
Evidence for structural changes in vertebrate thick filaments induced by calcium Morimoto, Keisuke; Harrington, William F. Journal of Molecular Biology, Vol. 88, Issue 3 https://doi.org/10.1016/0022-2836(74)90417-3	journal	September 1974
To lie or not to lie: Super-relaxing with myosins Nag, Suman; Trivedi, Darshan V. eLife, Vol. 10 https://doi.org/10.7554/eLife.63703	journal	February 2021
The myosin mesa and the basis of hypercontractility caused by hypertrophic cardiomyopathy mutations Nag, Suman; Trivedi, Darshan V.; Sarkar, Saswata S. Nature Structural & Molecular Biology, Vol. 24, Issue 6 https://doi.org/10.1038/nsmb.3408	journal	May 2017
The myosin interacting-heads motif present in live tarantula muscle explains tetanic and posttetanic phosphorylation mechanisms Padrón, Raúl; Ma, Weikang; Duno-Miranda, Sebastian Proceedings of the National Academy of Sciences, Vol. 117, Issue 22 https://doi.org/10.1073/pnas.1921312117	journal	May 2020
Stress-dependent activation of myosin in the heart requires thin filament activation and thick filament mechanosensing Park-Holohan, So-Jin; Brunello, Elisabetta; Kampourakis, Thomas Proceedings of the National Academy of Sciences, Vol. 118, Issue 16 https://doi.org/10.1073/pnas.2023706118	journal	April 2021
Order-disorder structural transitions in synthetic filaments of fast and slow skeletal muscle myosins under relaxing and activating conditions. Podlubnaya, Z. A.; Malyshev, S. L.; Nieznański, K. Acta Biochimica Polonica, Vol. 47, Issue 4 https://doi.org/10.18388/abp.2000_3954	journal	December 2000
Recent improvements in small angle x-ray diffraction for the study of muscle physiology Reconditi, Massimo Reports on Progress in Physics, Vol. 69, Issue 10 https://doi.org/10.1088/0034-4885/69/10/R01	journal	September 2006
Myosin filament activation in the heart is tuned to the mechanical task Reconditi, Massimo; Caremani, Marco; Pinzauti, Francesca Proceedings of the National Academy of Sciences, Vol. 114, Issue 12 https://doi.org/10.1073/pnas.1619484114	journal	March 2017
Thick Filament Length Changes in Muscle Have Both Elastic and Structural Components Reconditi, Massimo; Fusi, Luca; Caremani, Marco Biophysical Journal, Vol. 116, Issue 6 https://doi.org/10.1016/j.bpj.2019.02.009	journal	March 2019
The structure of the native cardiac thin filament at systolic Ca ²⁺ levels Risi, Cristina M.; Pepper, Ian; Belknap, Betty Proceedings of the National Academy of Sciences, Vol. 118, Issue 13 https://doi.org/10.1073/pnas.2024288118	journal	March 2021
Systolic [Ca ²⁺ ] _i regulates diastolic levels in rat ventricular myocytes: Control of diastolic [Ca ²⁺ ] _i in heart Sankaranarayanan, Rajiv; Kistamás, Kornél; Greensmith, David J. The Journal of Physiology, Vol. 595, Issue 16 https://doi.org/10.1113/JP274366	journal	July 2017
Three perspectives on the molecular basis of hypercontractility caused by hypertrophic cardiomyopathy mutations Spudich, James A. Pflügers Archiv - European Journal of Physiology, Vol. 471, Issue 5 https://doi.org/10.1007/s00424-019-02259-2	journal	February 2019
Myosin ATP turnover rate is a mechanism involved in thermogenesis in resting skeletal muscle fibers Stewart, M. A.; Franks-Skiba, K.; Chen, S. Proceedings of the National Academy of Sciences, Vol. 107, Issue 1 https://doi.org/10.1073/pnas.0909468107	journal	December 2009
Myosin light chain kinase and the role of myosin light chain phosphorylation in skeletal muscle Stull, James T.; Kamm, Kristine E.; Vandenboom, Rene Archives of Biochemistry and Biophysics, Vol. 510, Issue 2 https://doi.org/10.1016/j.abb.2011.01.017	journal	June 2011
Regulation by Myosin: How Calcium Regulates Some Myosins, Past and Present Szent-Gyorgyi, Andrew G. Regulatory Mechanisms of Striated Muscle Contraction https://doi.org/10.1007/978-4-431-38453-3_21	book	January 2007
Thin Filament-Mediated Regulation of Cardiac Contraction Tobacman, L. S. Annual Review of Physiology, Vol. 58, Issue 1 https://doi.org/10.1146/annurev.ph.58.030196.002311	journal	October 1996
Analysing force–pCa curves Walker, John S.; Li, Xiaotao; Buttrick, Peter M. Journal of Muscle Research and Cell Motility, Vol. 31, Issue 1 https://doi.org/10.1007/s10974-010-9208-7	journal	May 2010
Calmodulin and the regulation of smooth muscle contraction Walsh, Michael P. Molecular and Cellular Biochemistry, Vol. 135, Issue 1 https://doi.org/10.1007/BF00925958	journal	January 1994
Molecular basis of force-pCa relation in MYL2 cardiomyopathy mice: Role of the super-relaxed state of myosin Yuan, Chen-Ching; Kazmierczak, Katarzyna; Liang, Jingsheng Proceedings of the National Academy of Sciences, Vol. 119, Issue 8 https://doi.org/10.1073/pnas.2110328119	journal	February 2022

Similar Records

Cardiac myosin filaments are directly regulated by calcium

Journal Article · 2022 · Journal of General Physiology · OSTI ID:1901179

Ma, Weikang; Nag, Suman; Gong, Henry; +2 more

Amino terminus of cardiac myosin binding protein-C regulates cardiac contractility

Journal Article · 2021 · J. Mol. Cell. Cardiol. · OSTI ID:1901179

Lynch IV, Thomas L .; Kumar, Mohit; McNamara, James W.; +22 more