Orthophosphate increases the efficiency of slow muscle-myosin isoform in the presence of omecamtiv mecarbil.
Adenosine Triphosphatases
/ metabolism
Animals
Calcium
/ metabolism
Cardiac Myosins
/ drug effects
Drug Synergism
Male
Muscle, Skeletal
/ metabolism
Myocardial Contraction
/ drug effects
Myosins
/ metabolism
Phosphates
/ pharmacology
Rabbits
Sarcomeres
/ metabolism
Stress, Mechanical
Urea
/ analogs & derivatives
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
07 07 2020
07 07 2020
Historique:
received:
25
09
2019
accepted:
26
05
2020
entrez:
9
7
2020
pubmed:
9
7
2020
medline:
9
9
2020
Statut:
epublish
Résumé
Omecamtiv mecarbil (OM) is a putative positive inotropic tool for treatment of systolic heart dysfunction, based on the finding that in vivo it increases the ejection fraction and in vitro it prolongs the actin-bond life time of the cardiac and slow-skeletal muscle isoforms of myosin. OM action in situ, however, is still poorly understood as the enhanced Ca
Identifiants
pubmed: 32636378
doi: 10.1038/s41467-020-17143-2
pii: 10.1038/s41467-020-17143-2
pmc: PMC7341760
doi:
Substances chimiques
Phosphates
0
omecamtiv mecarbil
2M19539ERK
Urea
8W8T17847W
Adenosine Triphosphatases
EC 3.6.1.-
Cardiac Myosins
EC 3.6.1.-
Myosins
EC 3.6.4.1
Calcium
SY7Q814VUP
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3405Références
Spudich, J. A. Hypertrophic and dilated cardiomyopathy: four decades of basic research on muscle lead to potential therapeutic approaches to these devastating genetic diseases. Biophys. J. 106, 1236–1249 (2014).
pubmed: 24655499
pmcid: 3985504
Malik, F. I. et al. Cardiac myosin activation: a potential therapeutic approach for systolic heart failure. Science 331, 1439–1443 (2011).
pubmed: 21415352
pmcid: 4090309
Cleland, J. G. et al. The effects of the cardiac myosin activator, omecamtiv mecarbil, on cardiac function in systolic heart failure: a double-blind, placebo-controlled, crossover, dose-ranging phase 2 trial. Lancet 378, 676–683 (2011).
pubmed: 21856481
Teerlink, J. R. et al. Dose-dependent augmentation of cardiac systolic function with the selective cardiac myosin activator, omecamtiv mecarbil: a first-in-man study. Lancet 378, 667–675 (2011).
pubmed: 21856480
Teerlink, J. R. et al. Acute treatment with omecamtiv mecarbil to increase contractility in acute heart failure: The ATOMIC-AHF Study. J. Am. Coll. Cardiol. 67, 1444–1455 (2016).
pubmed: 27012405
Morgan, B. P. et al. Discovery of omecamtiv mecarbil the first, selective, small molecule activator of cardiac Myosin. ACS Med. Chem. Lett. 1, 472–477 (2010).
pubmed: 24900233
pmcid: 4007828
Kaplinsky, E. & Mallarkey, G. Cardiac myosin activators for heart failure therapy: focus on omecamtiv mecarbil. Drugs Context 7, 212518 (2018).
pubmed: 29707029
pmcid: 5916097
Nagy, L. et al. The novel cardiac myosin activator omecamtiv mecarbil increases the calcium sensitivity of force production in isolated cardiomyocytes and skeletal muscle fibres of the rat. Br. J. Pharmacol. 172, 4506–4518 (2015).
pubmed: 26140433
pmcid: 4562511
Woody, M. S. et al. Positive cardiac inotrope omecamtiv mecarbil activates muscle despite suppressing the myosin working stroke. Nat. Commun. 9, 3838 (2018).
pubmed: 30242219
pmcid: 6155018
Schiaffino, S. & Reggiani, C. Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol. Rev. 76, 371–423 (1996).
pubmed: 8618961
van Rooij, E. et al. A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Developmental Cell 17, 662–673 (2009).
pubmed: 19922871
pmcid: 2796371
Chikuni, K., Muroya, S., Tanabe R-i & Nakajima, I. Comparative sequence analysis of four myosin heavy chain isoforms expressed in porcine skeletal muscles: Sequencing and characterization of the porcine myosin heavy chain slow isoform. Anim. Sci. J. 73, 257–262 (2002).
Rohde, J. A., Thomas, D. D. & Muretta, J. M. Heart failure drug changes the mechanoenzymology of the cardiac myosin powerstroke. Proc. Natl Acad. Sci. USA 114, E1796–E1804 (2017).
pubmed: 28223517
Planelles-Herrero, V. J., Hartman, J. J., Robert-Paganin, J., Malik, F. I. & Houdusse, A. Mechanistic and structural basis for activation of cardiac myosin force production by omecamtiv mecarbil. Nat. Commun. 8, 190 (2017).
pubmed: 28775348
pmcid: 5543065
Liu, Y., White, H. D., Belknap, B., Winkelmann, D. A. & Forgacs, E. Omecamtiv Mecarbil modulates the kinetic and motile properties of porcine beta-cardiac myosin. Biochemistry 54, 1963–1975 (2015).
pubmed: 25680381
Aksel, T., Choe, Yu. E., Sutton, S., Ruppel, K. M. & Spudich, J. A. Ensemble force changes that result from human cardiac myosin mutations and a small-molecule effector. Cell Rep. 11, 910–920 (2015).
pubmed: 25937279
pmcid: 4431957
Winkelmann, D. A., Forgacs, E., Miller, M. T. & Stock, A. M. Structural basis for drug-induced allosteric changes to human beta-cardiac myosin motor activity. Nat. Commun. 6, 7974 (2015).
pubmed: 26246073
pmcid: 4918383
Linari, M., Caremani, M., Piperio, C., Brandt, P. & Lombardi, V. Stiffness and fraction of Myosin motors responsible for active force in permeabilized muscle fibers from rabbit psoas. Biophys. J. 92, 2476–2490 (2007).
pubmed: 17237201
pmcid: 1864836
Percario, V. et al. Mechanical parameters of the molecular motor myosin II determined in permeabilised fibres from slow and fast skeletal muscles of the rabbit. J. Physiol. 596, 1243–1257 (2018).
pubmed: 29148051
pmcid: 5878222
Caremani, M. et al. Size and speed of the working stroke of cardiac myosin in situ. Proc. Natl Acad. Sci. USA 113, 3675–3680 (2016).
pubmed: 26984499
Pinzauti, F. et al. The force and stiffness of myosin motors in the isometric twitch of a cardiac trabecula and the effect of the extracellular calcium concentration. J. Physiol. 596, 2581–2596 (2018).
pubmed: 29714038
pmcid: 6023834
Allen, D. G., Morris, P. G., Orchard, C. H. & Pirolo, J. S. A nuclear magnetic resonance study of metabolism in the ferret heart during hypoxia and inhibition of glycolysis. J. Physiol. 361, 185–204 (1985).
pubmed: 3989725
pmcid: 1192854
Kentish, J. C. The effects of inorganic phosphate and creatine phosphate on force production in skinned muscles from rat ventricle. J. Physiol. 370, 585–604 (1986).
pubmed: 3958986
pmcid: 1192698
Morris P. G., Allen D. G. & Orchard C. H. High-time-resolution 31P NMR studies of the perfused ferret heart. In: Advances in Myocardiology (eds Harris, P. & Poole-Wilson, P.A.) (Springer US, 1985).
Meyer, R. A., Brown, T. R. & Kushmerick, M. J. Phosphorus nuclear magnetic resonance of fast- and slow-twitch muscle. Am. J. Physiol. 248, C279–C287 (1985).
pubmed: 3976878
Bevington, A. et al. A study of intracellular orthophosphate concentration in human muscle and erythrocytes by 31P nuclear magnetic resonance spectroscopy and selective chemical assay. Clin. Sci. 71, 729–735 (1986).
pubmed: 3024899
Elliott, A. C., Smith, G. L. & Allen, D. G. The metabolic consequences of an increase in the frequency of stimulation in isolated ferret hearts. J. Physiol. 474, 147–159 (1994).
pubmed: 8014891
pmcid: 1160302
Eijgelshoven, M. H. et al. Cardiac high-energy phosphates adapt faster than oxygen consumption to changes in heart rate. Circ. Res. 75, 751–759 (1994).
pubmed: 7923620
Kampourakis, T., Zhang, X., Sun, Y. B. & Irving, M. Omecamtiv mercabil and blebbistatin modulate cardiac contractility by perturbing the regulatory state of the myosin filament. J. Physiol. 596, 31–46 (2018).
pubmed: 29052230
Kieu, T. T., Awinda, P. O. & Tanner, B. C. W. Omecamtiv mecarbil slows myosin kinetics in skinned rat myocardium at physiological temperature. Biophys. J. 116, 2149–2160 (2019).
pubmed: 31103235
pmcid: 6554472
Pate, E. & Cooke, R. A model of crossbridge action: the effects of ATP, ADP and Pi. J. Muscle Res. Cell Motil. 10, 181–196 (1989).
pubmed: 2527246
Millar, N. C. & Homsher, E. Kinetics of force generation and phosphate release in skinned rabbit soleus muscle fibers. Am. J. Physiol. 262, C1239–C1245 (1992).
pubmed: 1590362
Tesi, C., Colomo, F., Piroddi, N. & Poggesi, C. Characterization of the cross-bridge force-generating step using inorganic phosphate and BDM in myofibrils from rabbit skeletal muscles. J. Physiol. 541, 187–199 (2002).
pubmed: 12015429
pmcid: 2315793
Caremani, M., Dantzig, J., Goldman, Y. E., Lombardi, V. & Linari, M. Effect of inorganic phosphate on the force and number of myosin cross-bridges during the isometric contraction of permeabilized muscle fibers from rabbit psoas. Biophys. J. 95, 5798–5808 (2008).
pubmed: 18835889
pmcid: 2599836
Swenson, A. M. et al. Omecamtiv mecarbil enhances the duty ratio of human beta-cardiac myosin resulting in increased calcium sensitivity and slowed force development in cardiac muscle. J. Biol. Chem. 292, 3768–3778 (2017).
pubmed: 28082673
pmcid: 5339759
Potma, E. J., van Graas, I. A. & Stienen, G. J. Effects of pH on myofibrillar ATPase activity in fast and slow skeletal muscle fibers of the rabbit. Biophys. J. 67, 2404–2410 (1994).
pubmed: 7696480
pmcid: 1225625
Linari, M., Caremani, M. & Lombardi, V. A kinetic model that explains the effect of inorganic phosphate on the mechanics and energetics of isometric contraction of fast skeletal muscle. Proc. Biol. Sci. 277, 19–27 (2010).
pubmed: 19812088
Johnson, C. A. et al. The ATPase cycle of human muscle myosin II isoforms: Adaptation of a single mechanochemical cycle for different physiological roles. J. Biol. Chem. 294, 14267–14278 (2019).
pubmed: 31387944
Potma, E. J., van Graas, I. A. & Stienen, G. J. Influence of inorganic phosphate and pH on ATP utilization in fast and slow skeletal muscle fibers. Biophys. J. 69, 2580–2589 (1995).
pubmed: 8599665
pmcid: 1236496
Bowater, R. & Sleep, J. Demembranated muscle fibers catalyze a more rapid exchange between phosphate and adenosine triphosphate than actomyosin subfragment 1. Biochemistry 27, 5314–5323 (1988).
pubmed: 3167048
Millar, N. C. & Homsher, E. The effect of phosphate and calcium on force generation in glycerinated rabbit skeletal muscle fibers. A steady-state and transient kinetic study. J. Biol. Chem. 265, 20234–20240 (1990).
pubmed: 2243087
Dantzig, J. A., Goldman, Y. E., Millar, N. C., Lacktis, J. & Homsher, E. Reversal of the cross-bridge force-generating transition by photogeneration of phosphate in rabbit psoas muscle fibres. J. Physiol. 451, 247–278 (1992).
pubmed: 1403812
pmcid: 1176160
Caremani, M., Melli, L., Dolfi, M., Lombardi, V. & Linari, M. The working stroke of the myosin II motor in muscle is not tightly coupled to release of orthophosphate from its active site. J. Physiol. 591, 5187–5205 (2013).
pubmed: 23878374
pmcid: 3810818
Caremani, M., Melli, L., Dolfi, M., Lombardi, V. & Linari, M. Force and number of myosin motors during muscle shortening and the coupling with the release of the ATP hydrolysis products. J. Physiol. 593, 3313–3332 (2015).
pubmed: 26041599
pmcid: 4553055
McKillop, D. F. & Geeves, M. A. Regulation of the interaction between actin and myosin subfragment 1: evidence for three states of the thin filament. Biophys. J. 65, 693–701 (1993).
pubmed: 8218897
pmcid: 1225772
Vu, T. et al. Population pharmacokinetic-pharmacodynamic modeling of omecamtiv mecarbil, a cardiac myosin activator, in healthy volunteers and patients with stable heart failure. J. Clin. Pharmacol. 55, 1236–1247 (2015).
pubmed: 25951506
Dantzig, J. A., Hibberd, M. G., Trentham, D. R. & Goldman, Y. E. Cross-bridge kinetics in the presence of MgADP investigated by photolysis of caged ATP in rabbit psoas muscle fibres. J. Physiol. 432, 639–680 (1991).
pubmed: 1886072
pmcid: 1181346
Siemankowski, R. F., Wiseman, M. O. & White, H. D. ADP dissociation from actomyosin subfragment 1 is sufficiently slow to limit the unloaded shortening velocity in vertebrate muscle. Proc. Natl Acad. Sci. USA 82, 658–662 (1985).
pubmed: 3871943
Potma, E. J. & Stienen, G. J. Increase in ATP consumption during shortening in skinned fibres from rabbit psoas muscle: effects of inorganic phosphate. J. Physiol. 496(Pt 1), 1–12 (1996).
pubmed: 8910191
pmcid: 1160819
Gao, W. D., Atar, D., Backx, P. H. & Marban, E. Relationship between intracellular calcium and contractile force in stunned myocardium. Direct evidence for decreased myofilament Ca2+ responsiveness and altered diastolic function in intact ventricular muscle. Circ. Res. 76, 1036–1048 (1995).
pubmed: 7758158
Frampton, J. E., Orchard, C. H. & Boyett, M. R. Diastolic, systolic and sarcoplasmic reticulum [Ca2+] during inotropic interventions in isolated rat myocytes. J. Physiol. 437, 351–375 (1991).
pubmed: 1890639
pmcid: 1180052
Goldman, Y. E., Hibberd, M. G. & Trentham, D. R. Relaxation of rabbit psoas muscle fibres from rigor by photochemical generation of adenosine-5’-triphosphate. J. Physiol. 354, 577–604 (1984).
pubmed: 6481645
pmcid: 1193430
Brenner, B. & Yu, L. C. Characterization of radial force and radial stiffness in Ca(2+)-activated skinned fibres of the rabbit psoas muscle. J. Physiol. 441, 703–718 (1991).
pubmed: 1816390
pmcid: 1180221
Kawai, M., Wray, J. S. & Zhao, Y. The effect of lattice spacing change on cross-bridge kinetics in chemically skinned rabbit psoas muscle fibers. I. Proportionality between the lattice spacing and the fiber width. Biophys. J. 64, 187–196 (1993).
pubmed: 7679296
pmcid: 1262316
Matsubara, I. & Elliott, G. F. X-ray diffraction studies on skinned single fibres of frog skeletal muscle. J. Mol. Biol. 72, 657–669 (1972).
pubmed: 4540801
Maughan, D. W. & Godt, R. E. Stretch and radial compression studies on relaxed skinned muscle fibers of the frog. Biophys. J. 28, 391–402 (1979).
pubmed: 318072
pmcid: 1328645
Linari, M. et al. The stiffness of skeletal muscle in isometric contraction and rigor: the fraction of myosin heads bound to actin. Biophys. J. 74, 2459–2473 (1998).
pubmed: 9591672
pmcid: 1299588
Huxley, A. F., Lombardi, V. & Peachey, D. A system for fast recording of longitudinal displacement of a striated muscle fibre. J. Physiol. 317, 12–13 (1981).
Fusi, L., Brunello, E., Reconditi, M., Piazzesi, G. & Lombardi, V. The non-linear elasticity of the muscle sarcomere and the compliance of myosin motors. J. Physiol. 592, 1109–1118 (2014).
pubmed: 24344166
pmcid: 3948566
Glyn, H. & Sleep, J. Dependence of adenosine triphosphatase activity of rabbit psoas muscle fibres and myofibrils on substrate concentration. J. Physiol. 365, 259–276 (1985).
pubmed: 3162018
pmcid: 1193000
Potma, E. J., Stienen, G. J., Barends, J. P. & Elzinga, G. Myofibrillar ATPase activity and mechanical performance of skinned fibres from rabbit psoas muscle. J. Physiol. 474, 303–317 (1994).
pubmed: 8006817
pmcid: 1160319
White, H. D. & Taylor, E. W. Energetics and mechanism of actomyosin adenosine triphosphatase. Biochemistry 15, 5818–5826 (1976).
pubmed: 12793
Sleep, J. A. & Taylor, E. W. Intermediate states of actomyosin adenosine triphosphatase. Biochemistry 15, 5813–5817 (1976).
pubmed: 12792
Goldman, Y. E. Kinetics of the actomyosin ATPase in muscle fibers. Annu Rev. Physiol. 49, 637–654 (1987).
pubmed: 2952053
Kawai, M. & Halvorson, H. R. Two step mechanism of phosphate release and the mechanism of force generation in chemically skinned fibers of rabbit psoas muscle. Biophys. J. 59, 329–342 (1991).
pubmed: 2009356
pmcid: 1281150
Nyitrai, M. & Geeves, M. A. Adenosine diphosphate and strain sensitivity in myosin motors. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359, 1867–1877 (2004).
pubmed: 15647162
pmcid: 1693474