Thick filament activation is different in fast- and slow-twitch skeletal muscle

Gong, Henry M.; Ma, Weikang; Regnier, Michael; Irving, Thomas C.

doi:10.1113/jp283574

Thick filament activation is different in fast- and slow-twitch skeletal muscle

Journal Article · Wed Nov 23 00:00:00 EST 2022 · Journal of Physiology

DOI:https://doi.org/10.1113/jp283574· OSTI ID:2423708

Gong, Henry M. ^[1]; ^[1]; Regnier, Michael ^[2]; Irving, Thomas C. ^[1]

Illinois Institute of Technology, Chicago, IL (United States)
Univ. of Washington, Seattle, WA (United States)

The contractile properties of fast-twitch and slow-twitch skeletal muscles are primarily determined by the myosin isoform content and modulated by a variety of sarcomere proteins. X-ray diffraction studies of regulatory mechanisms in muscle contraction have focused predominately on fast- or mixed-fibre muscle with slow muscle being much less studied. Here, we used time-resolved X-ray diffraction to investigate the dynamic behaviour of the myofilament proteins in relatively pure slow-twitch-fibre rat soleus (SOL) and pure fast-twitch-fibre rat extensor digitorum longus (EDL) muscle during twitch and tetanic contractions at optimal length. During twitch contractions the diffraction signatures indicating a transition in the myosin heads from ordered OFF states, where heads are held close to the thick filament backbone, to disordered ON states, where heads are free to bind to thin filaments, were found in EDL and not in SOL muscle. During tetanic contraction, changes in the disposition of myosin heads as active tension develops is a quasi-stepwise process in EDL muscle whereas in SOL muscle this relationship appears to be linear. The observed reduced extensibility of the thick filaments in SOL muscle as compared to EDL muscles indicates a molecular basis for this behaviour. These data indicate that for the EDL, thick filament activation is a cooperative strain-induced mechano-sensing mechanism, whereas for the SOL, thick filament activation has a more graded response. Further, these different approaches to thick filament regulation in fast- and slow-twitch muscles may be adaptations for short-duration, strong contractions versus sustained, finely controlled contractions, respectively.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH); USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 2423708

Journal Information:: Journal of Physiology, Journal Name: Journal of Physiology Journal Issue: 24 Vol. 600; ISSN 0022-3751

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (68)

Comprehensive analysis of titin protein isoform and alternative splicing in normal and mutant rats Li, Shijun; Guo, Wei; Schmitt, Benjamin M. Journal of Cellular Biochemistry, Vol. 113, Issue 4 https://doi.org/10.1002/jcb.23459	journal	February 2012
Fiber-type proportions in mammalian soleus muscle during postnatal development Wigston, Donald J.; English, Arthur Wm. Journal of Neurobiology, Vol. 23, Issue 1 https://doi.org/10.1002/neu.480230107	journal	February 1992
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
Cross-bridge movement in rat slow skeletal muscle as a function of calcium concentration Honda, Hideyuki; Koiwa, Yoshiro; Yagi, Naoto Pflügers Archiv - European Journal of Physiology, Vol. 432, Issue 5 https://doi.org/10.1007/s004240050201	journal	September 1996
Structural difference between resting and rigor muscle; Evidence from intensity changes in the low-angle equatorial X-ray diagram Huxley, H. E. Journal of Molecular Biology, Vol. 37, Issue 3 https://doi.org/10.1016/0022-2836(68)90118-6	journal	November 1968
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 evidence for conformational changes in the myosin filaments of vertebrate striated muscle Haselgrove, J. C. Journal of Molecular Biology, Vol. 92, Issue 1 https://doi.org/10.1016/0022-2836(75)90094-7	journal	February 1975
Time-resolved X-ray diffraction studies of the myosin layer-line reflections during muscle contraction Huxley, H. E.; Faruqi, A. R.; Kress, M. Journal of Molecular Biology, Vol. 158, Issue 4 https://doi.org/10.1016/0022-2836(82)90253-4	journal	July 1982
Equatorial x-ray diffraction from single skinned rabbit psoas fibers at various degrees of activation. Changes in intensities and lattice spacing Brenner, B.; Yu, L. C. Biophysical Journal, Vol. 48, Issue 5 https://doi.org/10.1016/S0006-3495(85)83841-8	journal	November 1985
Time-resolved changes in equatorial x-ray diffraction and stiffness during rise of tetanic tension in intact length-clamped single muscle fibers Cecchi, G.; Griffiths, P. J.; Bagni, M. A. Biophysical Journal, Vol. 59, Issue 6 https://doi.org/10.1016/S0006-3495(91)82342-6	journal	June 1991
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
X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction Wakabayashi, K.; Sugimoto, Y.; Tanaka, H. Biophysical Journal, Vol. 67, Issue 6 https://doi.org/10.1016/S0006-3495(94)80729-5	journal	December 1994
Extensibility and Symmetry of Actin Filaments in Contracting Muscles Bordas, J.; Svensson, A.; Rothery, M. Biophysical Journal, Vol. 77, Issue 6 https://doi.org/10.1016/S0006-3495(99)77150-X	journal	December 1999
Interaction between series compliance and sarcomere kinetics determines internal sarcomere shortening during fixed-end contraction Kawakami, Yasuo; Lieber, Richard L. Journal of Biomechanics, Vol. 33, Issue 10 https://doi.org/10.1016/S0021-9290(00)00095-6	journal	October 2000
An X-ray and light-diffraction study of the filament lattice of striated muscle in the living state and in rigor Elliott, G. F.; Lowy, J.; Worthington, C. R. Journal of Molecular Biology, Vol. 6, Issue 4 https://doi.org/10.1016/S0022-2836(63)80090-X	journal	April 1963
The low-angle X-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor Huxley, H. E.; Brown, W. Journal of Molecular Biology, Vol. 30, Issue 2 https://doi.org/10.1016/S0022-2836(67)80046-9	journal	December 1967
Dynamics of Thin-Filament Activation in Rabbit Skeletal Muscle Fibers Examined by Time-Resolved X-Ray Diffraction Tamura, Takumi; Wakayama, Jun'ichi; Inoue, Katsuaki Biophysical Journal, Vol. 96, Issue 3 https://doi.org/10.1016/j.bpj.2008.09.022	journal	February 2009
Tuning Passive Mechanics through Differential Splicing of Titin during Skeletal Muscle Development Ottenheijm, Coen A. C.; Knottnerus, Anna M.; Buck, Danielle Biophysical Journal, Vol. 97, Issue 8 https://doi.org/10.1016/j.bpj.2009.07.041	journal	October 2009
The Fraction of Myosin Motors That Participate in Isometric Contraction of Rabbit Muscle Fibers at Near-Physiological Temperature Tsaturyan, Andrey K.; Bershitsky, Sergey Y.; Koubassova, Natalia A. Biophysical Journal, Vol. 101, Issue 2 https://doi.org/10.1016/j.bpj.2011.06.008	journal	July 2011
Regulation of Contraction by the Thick Filaments in Skeletal Muscle Irving, Malcolm Biophysical Journal, Vol. 113, Issue 12 https://doi.org/10.1016/j.bpj.2017.09.037	journal	December 2017
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
Density and hydration of fresh and fixed human skeletal muscle Ward, Samuel R.; Lieber, Richard L. Journal of Biomechanics, Vol. 38, Issue 11 https://doi.org/10.1016/j.jbiomech.2004.10.001	journal	November 2005
Impacts of prolonged chlorpyrifos exposure on locomotion and slow-and fast- twitch skeletal muscles contractility in rats Hallal, Nancy; El Khayat El Sabbouri, Hiba; Salami, Ali Toxicology Reports, Vol. 6 https://doi.org/10.1016/j.toxrep.2019.06.006	journal	January 2019
Influence of Temperature on Isometric Contractions of Rat Skeletal Muscles Close, R.; Hoh, J. F. Y. Nature, Vol. 217, Issue 5134 https://doi.org/10.1038/2171179a0	journal	March 1968
F-actin is a helix with a random variable twist Egelman, E. H.; Francis, N.; DeRosier, D. J. Nature, Vol. 298, Issue 5870 https://doi.org/10.1038/298131a0	journal	July 1982
Why animals have different muscle fibre types Rome, Lawrence C.; Funke, Roel P.; Alexander, R. McNeill Nature, Vol. 335, Issue 6193 https://doi.org/10.1038/335824a0	journal	October 1988
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
Thick filament mechano-sensing is a calcium-independent regulatory mechanism in skeletal muscle Fusi, L.; Brunello, E.; Yan, Z. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13281	journal	October 2016
Polymorphism of myofibrillar proteins of rabbit skeletal-muscle fibres. An electrophoretic study of single fibres Salviati, G.; Betto, R.; Danieli Betto, D. Biochemical Journal, Vol. 207, Issue 2 https://doi.org/10.1042/bj2070261	journal	November 1982
Motion of myosin head domains during activation and force development in skeletal muscle Reconditi, M.; Brunello, E.; Linari, M. Proceedings of the National Academy of Sciences, Vol. 108, Issue 17 https://doi.org/10.1073/pnas.1018330108	journal	April 2011
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
Skeletal MyBP-C isoforms tune the molecular contractility of divergent skeletal muscle systems Li, Amy; Nelson, Shane R.; Rahmanseresht, Sheema Proceedings of the National Academy of Sciences, Vol. 116, Issue 43 https://doi.org/10.1073/pnas.1910549116	journal	October 2019
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
Interference fine structure and sarcomere length dependence of the axial x-ray pattern from active single muscle fibers Linari, M.; Piazzesi, G.; Dobbie, I. Proceedings of the National Academy of Sciences, Vol. 97, Issue 13 https://doi.org/10.1073/pnas.97.13.7226	journal	June 2000
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
Low temperature traps myosin motors of mammalian muscle in a refractory state that prevents activation Caremani, Marco; Brunello, Elisabetta; Linari, Marco Journal of General Physiology, Vol. 151, Issue 11 https://doi.org/10.1085/jgp.201912424	journal	September 2019
Lattice arrangement of myosin filaments correlates with fiber type in rat skeletal muscle Ma, Weikang; Lee, Kyoung Hwan; Yang, Shixin Journal of General Physiology, Vol. 151, Issue 12 https://doi.org/10.1085/jgp.201912460	journal	November 2019
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
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
Recent X–ray diffraction studies of muscle contraction and their implications Holmes, K. C.; Trentham, D. R.; Simmons, R. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 359, Issue 1452 https://doi.org/10.1098/rstb.2004.1556	journal	December 2004
Structural Changes in the Actin- and Myosin-eontaining Filaments during Contraction Huxley, H. E. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 37, Issue 0 https://doi.org/10.1101/SQB.1973.037.01.046	journal	January 1973
Fityk : a general-purpose peak fitting program Wojdyr, Marcin Journal of Applied Crystallography, Vol. 43, Issue 5 https://doi.org/10.1107/S0021889810030499	journal	September 2010
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
Changes in conformation of myosin heads during the development of isometric contraction and rapid shortening in single frog muscle fibres Piazzesi, Gabriella; Reconditi, Massimo; Dobbie, Ian The Journal of Physiology, Vol. 514, Issue 2 https://doi.org/10.1111/j.1469-7793.1999.305ae.x	journal	January 1999
Principles and standards for reporting animal experiments in The Journal of Physiology and Experimental Physiology: Editorial Grundy, David The Journal of Physiology, Vol. 593, Issue 12 https://doi.org/10.1113/JP270818	journal	June 2015
Mechanical parameters of the molecular motor myosin II determined in permeabilised fibres from slow and fast skeletal muscles of the rabbit Percario, Valentina; Boncompagni, Simona; Protasi, Feliciano The Journal of Physiology, Vol. 596, Issue 7 https://doi.org/10.1113/JP275404	journal	January 2018
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
Dynamic properties of fast and slow skeletal muscles of the rat during development Close, R. The Journal of Physiology, Vol. 173, Issue 1 https://doi.org/10.1113/jphysiol.1964.sp007444	journal	August 1964
The contributions of filaments and cross-bridges to sarcomere compliance in skeletal muscle: Myofilament and cross-bridge compliance Brunello, Elisabetta; Caremani, Marco; Melli, Luca The Journal of Physiology, Vol. 592, Issue 17 https://doi.org/10.1113/jphysiol.2014.276196	journal	September 2014
Actin Structure and Function Dominguez, Roberto; Holmes, Kenneth C. Annual Review of Biophysics, Vol. 40, Issue 1 https://doi.org/10.1146/annurev-biophys-042910-155359	journal	June 2011
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
Force development of fast and slow skeletal muscle at different muscle lengths Wallinga-de Jonge, W.; Boom, H. B.; Boon, K. L. American Journal of Physiology-Cell Physiology, Vol. 239, Issue 3 https://doi.org/10.1152/ajpcell.1980.239.3.C98	journal	September 1980
Skeletal muscle fatigue in vitro is temperature dependent Segal, S. S.; Faulkner, J. A.; White, T. P. Journal of Applied Physiology, Vol. 61, Issue 2 https://doi.org/10.1152/jappl.1986.61.2.660	journal	August 1986
Passive tension of rat skeletal soleus muscle fibers: effects of unloading conditions Toursel, Thierry; Stevens, Laurence; Granzier, Henk Journal of Applied Physiology, Vol. 92, Issue 4 https://doi.org/10.1152/japplphysiol.00621.2001	journal	April 2002
Fiber Types in Mammalian Skeletal Muscles Schiaffino, Stefano; Reggiani, Carlo Physiological Reviews, Vol. 91, Issue 4 https://doi.org/10.1152/physrev.00031.2010	journal	October 2011
Dynamic properties of mammalian skeletal muscles. Close, R. I. Physiological Reviews, Vol. 52, Issue 1 https://doi.org/10.1152/physrev.1972.52.1.129	journal	January 1972
The Filament Lattice of Striated Muscle Millman, Barry M. Physiological Reviews, Vol. 78, Issue 2 https://doi.org/10.1152/physrev.1998.78.2.359	journal	April 1998
Regulation of Contraction in Striated Muscle Gordon, A. M.; Homsher, E.; Regnier, M. Physiological Reviews, Vol. 80, Issue 2 https://doi.org/10.1152/physrev.2000.80.2.853	journal	January 2000
The mechanism for vertebrate striated muscle contraction. Julian, F. J.; Moss, R. L.; Sollins, M. R. Circulation Research, Vol. 42, Issue 1 https://doi.org/10.1161/01.RES.42.1.2	journal	January 1978
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
The histochemical profiles of fast fiber types IIB, IID, and IIA in skeletal muscles of mouse, rat, and rabbit. Hämäläinen, N.; Pette, D. Journal of Histochemistry & Cytochemistry, Vol. 41, Issue 5 https://doi.org/10.1177/41.5.8468455	journal	May 1993
Scaling of muscle architecture and fiber types in the rat hindlimb Eng, C. M.; Smallwood, L. H.; Rainiero, M. P. Journal of Experimental Biology, Vol. 211, Issue 14 https://doi.org/10.1242/jeb.017640	journal	July 2008
Effects of elimination of activity on contractile and histochemical properties of rat soleus muscle Spector, Sa The Journal of Neuroscience, Vol. 5, Issue 8 https://doi.org/10.1523/JNEUROSCI.05-08-02177.1985	journal	August 1985
Sarcomere Lengths Become More Uniform Over Time in Intact Muscle-Tendon Unit During Isometric Contractions Moo, Eng Kuan; Herzog, Walter Frontiers in Physiology, Vol. 11 https://doi.org/10.3389/fphys.2020.00448	journal	May 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
Estimation of Forces on Actin Filaments in Living Muscle from X-ray Diffraction Patterns and Mechanical Data Mijailovich, Srboljub M.; Prodanovic, Momcilo; Irving, Thomas C. International Journal of Molecular Sciences, Vol. 20, Issue 23 https://doi.org/10.3390/ijms20236044	journal	November 2019
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
Myosin-based regulation of twitch and tetanic contractions in mammalian skeletal muscle Hill, Cameron; Brunello, Elisabetta; Fusi, Luca eLife, Vol. 10 https://doi.org/10.7554/eLife.68211	journal	June 2021

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59 BASIC BIOLOGICAL SCIENCES
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Thick filament activation is different in fast- and slow-twitch skeletal muscle

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