From “sliding” to “winding” filaments theory: A narrative review of mechanisms behind skeletal muscle contraction
Keywords:
Muscle contraction, Actin, Myosin, TitinAbstract
The physiological mechanisms behind muscle contraction are a main concept in sport medicine and rehabilitation. The sarcomere is the functional unit of skeletal muscle and several proteins definite its complex structure. The most common theory to explain muscle contraction was proposed in the last 50’s and has become widely popular and accepted: the “sliding filaments” theory. Even if this hypothesis was able to justify some form of muscle contraction, other processes are not fully described by it. Eccentric contraction and some phenomena, like the “force enhancement during stretch” concept described in the 2002, are not explicable according to the sliding filament theory. Therefore, several hypotheses have been suggested over the years, such as the “popping sarcomeres” theory and the “winding filament” theory. Some other proteins, like titin, have gained a main role in the physiology of the sarcomere and should be relevant to explain mechanisms of eccentric contraction, where the sarcomere generates highest level of tension while it is lengthening. The aim of this review is to summarize the physiological theories of muscle contraction and to define concepts applicable in sport medicine and in rehabilitation areas.
Downloads
References
Abbott, B. C., & Aubert, X. M. (1952). The force exerted by active striated muscle during and after change of length. The Journal of Physiology, 117(1), 77-86.
Ackermann, M. A., & Kontrogianni-Konstantopoulos, A. (2013). Myosin binding protein-C slow: A multifaceted family of proteins with a complex expression profile in fast and slow twitch skeletal muscles. Frontiers in Physiology, 4 DEC. https://doi.org/10.3389/fphys.2013.00391
Astumian, R. (2015). Huxley's Model for Muscle Contraction Revisited: The Importance of Microscopic Reversibility. Topics in Current Chemistry, 369. https://doi.org/10.1007/128_2015_644
Bianco, P., Nagy, A., Kengyel, A., Szatmári, D., Mártonfalvi, Z., Huber, T., & Kellermayer, M. S. Z. (2007). Interaction forces between F-actin and titin PEVK domain measured with optical tweezers. Biophysical Journal, 93(6), 2102-2109. https://doi.org/10.1529/biophysj.107.106153
Cooke, R. (2004). The sliding filament model: 1972-2004. The Journal of General Physiology, 123(6), 643-656. https://doi.org/10.1085/jgp.200409089
Corrado, B, Albano, M., Caprio, M. G., Di Luise, C., Sansone, M., Servodidio, V., … Servodio Iammarrone, C. (2019). Usefulness of point shear wave elastography to assess the effects of extracorporeal shockwaves on spastic muscles in children with cerebral palsy: An uncontrolled experimental study. Muscles, Ligaments and Tendons Journal, 9(1), 124-130. https://doi.org/10.32098/mltj.01.2019.04
Corrado, Bruno, Ciardi, G., Fortunato, L., & Iammarrone, C. (2019). Burnout syndrome among Italian physiotherapists: a cross-sectional study. European Journal of Physiotherapy, 1-6. https://doi.org/10.1080/21679169.2018.1536765
Corrado, Bruno, Ciardi, G., & Iammarrone, C. S. (2019). Rehabilitation management of pompe disease, from childhood trough adulthood: A systematic review of the literature. Neurology International, 11(2), 7983. https://doi.org/10.4081/ni.2019.7983
Corrado, Bruno, Mazzuoccolo, G., Liguori, L., Chirico, V. A., Costanzo, M., Bonini, I., … Curci, L. (2019). Treatment of lateral epicondylitis with collagen injections: A pilot study. Muscles, Ligaments and Tendons Journal, 9(4), 584-589. https://doi.org/10.32098/mltj.04.2019.14
Croisier, J. L., & Crielaard, J. M. (2001). [Isokinetic exercise and sports injuries]. Revue medicale de Liege, 56(5), 360-368.
Davies, G., Riemann, B. L., & Manske, R. (2015). Current concepts of plyometric exercise. International Journal of Sports Physical Therapy, 10(6), 760-786.
Dewa, C. S., Loong, D., Bonato, S., Thanh, N. X., & Jacobs, P. (2014). How does burnout affect physician productivity? A systematic literature review. BMC Health Services Research, 14(1), 325. https://doi.org/10.1186/1472-6963-14-325
Exeter, D., & Connell, D. A. (2010). Skeletal muscle: Functional anatomy and pathophysiology. Seminars in Musculoskeletal Radiology, 14(2), 97-105. https://doi.org/10.1055/s-0030-1253154
Freiburg, A., & Gautel, M. (1996). A molecular map of the interactions between titin and myosin-binding protein C. Implications for sarcomeric assembly in familial hypertrophic cardiomyopathy. European Journal of Biochemistry, 235(1-2), 317-323. https://doi.org/10.1111/j.1432-1033.1996.00317.x
Frontera, W. R., & Ochala, J. (2015). Skeletal muscle: a brief review of structure and function. Calcified Tissue International, 96(3), 183-195. https://doi.org/10.1007/s00223-014-9915-y
Funatsu, T., Kono, E., Higuchi, H., Kimura, S., Ishiwata, S., Yoshioka, T., … Tsukita, S. (1993). Elastic filaments in situ in cardiac muscle: deep-etch replica analysis in combination with selective removal of actin and myosin filaments. The Journal of Cell Biology, 120(3), 711-724. https://doi.org/10.1083/jcb.120.3.711
Galińska-Rakoczy, A., Engel, P., Xu, C., Jung, H. S., Craig, R., Tobacman, L. S., & Lehman, W. (2008). Structural Basis for the Regulation of Muscle Contraction by Troponin and Tropomyosin. Journal of Molecular Biology, 379(5), 929-935. https://doi.org/10.1016/j.jmb.2008.04.062
Gash, M. C., & Varacallo, M. (2018). Physiology, Muscle Contraction. StatPearls. StatPearls Publishing.
Gilbert, R., Cohen, J. A., Pardo, S., Basu, A., & Fischman, D. A. (1999). Identification of the A-band localization domain of myosin binding proteins C and H (MyBP-C, MyBP-H) in skeletal muscle. Journal of Cell Science, 112 ( Pt 1, 69-79.
Gillies, A. R., & Lieber, R. L. (2011, September). Structure and function of the skeletal muscle extracellular matrix. Muscle and Nerve. NIH Public Access. https://doi.org/10.1002/mus.22094
Gokhin, D. S., Ochala, J., Domenighetti, A. A., & Fowler, V. M. (2015). Tropomodulin 1 directly controls thin filament length in both wild-type and tropomodulin 4-deficient skeletal muscle. Development (Cambridge, England), 142(24), 4351-4362. https://doi.org/10.1242/dev.129171
Gordon, A. M., Huxley, A. F., & Julian, F. J. (1966). The variation in isometric tension with sarcomere length in vertebrate muscle fibres. The Journal of Physiology, 184(1), 170-192. https://doi.org/10.1113/jphysiol.1966.sp007909
Grzelkowska-Kowalczyk, K. (2016). The Importance of Extracellular Matrix in Skeletal Muscle Development and Function. In Composition and Function of the Extracellular Matrix in the Human Body. InTech. https://doi.org/10.5772/62230
Gustafsson, H., DeFreese, J. D., & Madigan, D. J. (2017). Athlete burnout: review and recommendations. Current Opinion in Psychology, 16, 109-113. https://doi.org/10.1016/j.copsyc.2017.05.002
Hamid, M. S. A., Yusof, A., & Mohamed Ali, M. R. (2014). Platelet-rich plasma (PRP) for acute muscle injury: A systematic review. PLoS ONE, 9(2). https://doi.org/10.1371/journal.pone.0090538
Haycock, J. W., MacNeil, S., Jones, P., Harris, J. B., & Mantle, D. (1996). Oxidative damage to muscle protein in Duchenne muscular dystrophy. Neuroreport, 8(1), 357-361. https://doi.org/10.1097/00001756-199612200-00070
Herzog, W., & Leonard, T. R. (2002a). Force enhancement following stretching of skeletal muscle: a new mechanism. The Journal of Experimental Biology, 205(Pt 9), 1275-1283.
Herzog, W., & Leonard, T. R. (2002b). Force enhancement following stretching of skeletal muscle. Journal of Experimental Biology, 205(9), 1275 LP - 1283.
Horowits, R., Kempner, E. S., Bisher, M. E., & Podolsky, R. J. (1986). A physiological role for titin and nebulin in skeletal muscle. Nature, 323(6084), 160-164. https://doi.org/10.1038/323160a0
Humphrey, J. D., Dufresne, E. R., & Schwartz, M. A. (2014, December 11). Mechanotransduction and extracellular matrix homeostasis. Nature Reviews Molecular Cell Biology. Nature Publishing Group. https://doi.org/10.1038/nrm3896
Huxley, A. F. (1957). Muscle structure and theories of contraction. Progress in Biophysics and Biophysical Chemistry, 7, 255-318. https://doi.org/10.1016/S0096-4174(18)30128-8
Huxley, A. F., & Niedergerke, R. (1954). Structural changes in muscle during contraction: Interference microscopy of living muscle fibres. Nature, 173(4412), 971-973. https://doi.org/10.1038/173971a0
Huxley, H. E. (1957). The double array of filaments in cross-striated muscle. The Journal of Biophysical and Biochemical Cytology, 3(5), 631-648. https://doi.org/10.1083/jcb.3.5.631
Huxley, H., & Hanson, J. (1954). Changes in the Cross-striations of muscle during contraction and stretch and their structural interpretation. Nature, 173(4412), 973-976. https://doi.org/10.1038/173973a0
Jiménez-Reyes, P., Samozino, P., Brughelli, M., & Morin, J. B. (2017). Effectiveness of an individualized training based on force-velocity profiling during jumping. Frontiers in Physiology, 7(JAN), 677. https://doi.org/10.3389/fphys.2016.00677
Jones, D. A., & Rutherford, O. M. (1987). Human muscle strength training: the effects of three different regimens and the nature of the resultant changes. The Journal of Physiology, 391(1), 1-11. https://doi.org/10.1113/jphysiol.1987.sp016721
Lieber, R. L. (2009). Skeletal Muscle Structure, Function, and Plasticity: The Physiological Basis of Rehabilitation: Amazon.it: Lieber, Richard L.: Libri in altre lingue. (Wolters Kluwer Health - Lippincott Williams & Wilkins, Ed.) (3rd ed.).
Linke, W. A. (2018). Titin Gene and Protein Functions in Passive and Active Muscle. Annual Review of Physiology, 80(1), 389-411. https://doi.org/10.1146/annurev-physiol-021317-121234
Linke, W. A., Kulke, M., Li, H., Fujita-Becker, S., Neagoe, C., Manstein, D. J., … Fernandez, J. M. (2002). PEVK domain of titin: An entropic spring with actin-binding properties. In Journal of Structural Biology (Vol. 137, pp. 194-205). Academic Press Inc. https://doi.org/10.1006/jsbi.2002.4468
Loiacono, C., Palermi, S., Massa, B., Belviso, I., Romano, V., Gregorio, A. Di, … Sacco, A. M. (2019). Tendinopathy: Pathophysiology, Therapeutic Options, and Role of Nutraceutics. A Narrative Literature Review. Medicina (Kaunas, Lithuania), 55(8). https://doi.org/10.3390/medicina55080447
Lombardi, V., & Piazzesi, G. (1990). The contractile response during steady lengthening of stimulated frog muscle fibres. The Journal of Physiology, 431(1), 141-171. https://doi.org/10.1113/jphysiol.1990.sp018324
Mazzeo, F., Tafuri, D., & Montesano, P. (2020). Respiratory endurance, pulmonary drugs and sport performance: An analysis in a sample of amateur soccer athletes. Sport Science, 13(1), 11-16.
Montesano, P., Masala, D., Silvestro, M., Cipriani, G., Tafuri, D., & Mazzeo, F. (2020). Effects of combined training program, controlled diet and drugs on middle-distance amateur runners : A pilot study. Sport Science, 13(1), 17-22.
Montesano, P., Tafuri, D., & Mazzeo, F. (2013). Improvement of the motor performance difference in athletes of weelchair Basketball. Journal of Physical Education and Sport, 13, 362-370. https://doi.org/10.7752/jpes.2013.03058
Morgan, D. L. (1990). New insights into the behavior of muscle during active lengthening. Biophysical Journal, 57(2), 209-221. https://doi.org/10.1016/S0006-3495(90)82524-8
Morgan, David L, & Proske, U. (2004). Popping sarcomere hypothesis explains stretch-induced muscle damage. In Clinical and Experimental Pharmacology and Physiology (Vol. 31, pp. 541-545). https://doi.org/10.1111/j.1440-1681.2004.04029.x
Mukund, K., & Subramaniam, S. (2020, August 13). Skeletal muscle: A review of molecular structure and function, in health and disease. Wiley Interdisciplinary Reviews: Systems Biology and Medicine. Wiley-Blackwell. https://doi.org/10.1002/wsbm.1462
Naugle, K. M., Naugle, K. E., Fillingim, R. B., & Riley, J. L. (2014). Isometric exercise as a test of pain modulation: Effects of experimental pain test, psychological variables, and sex. Pain Medicine (United States), 15(4), 692-701. https://doi.org/10.1111/pme.12312
Nishikawa, K. C., Lindstedt, S. L., & LaStayo, P. C. (2018, July 1). Basic science and clinical use of eccentric contractions: History and uncertainties. Journal of Sport and Health Science. Elsevier B.V. https://doi.org/10.1016/j.jshs.2018.06.002
Nishikawa, K. C., Monroy, J. A., Uyeno, T. E., Yeo, S. H., Pai, D. K., & Lindstedt, S. L. (2012). Is titin a "winding filament"? A new twist on muscle contraction. Proceedings of the Royal Society B: Biological Sciences, 279(1730), 981-990. https://doi.org/10.1098/rspb.2011.1304
Nishikawa, K., Monroy, J., Uyeno, T., Yeo, S., Pai, D., & Lindstedt, S. (2011). Is titin a "winding filament"? A new twist on muscle contraction. Proceedings. Biological Sciences / The Royal Society, 279, 981-990. https://doi.org/10.1098/rspb.2011.1304
O'Neill, S., Watson, P. J., & Barry, S. (2015). Why are eccentric exercises effective for achilles tendinopathy? International Journal of Sports Physical Therapy, 10(4), 552-562.
Padulo, J., Laffaye, G., Chamari, K., & Concu, A. (2013, July). Concentric and Eccentric: Muscle Contraction or Exercise? Sports Health. SAGE Publications. https://doi.org/10.1177/1941738113491386
Palermi, S., Sacco, A. M., Belviso, I., Romano, V., Montesano, P., Corrado, B., & Sirico, F. (2020). Guidelines for physical activity-a cross-sectional study to assess their application in the general population. Have we achieved our goal? International Journal of Environmental Research and Public Health, 17(11), 1-14. https://doi.org/10.3390/ijerph17113980
Rice, D. A., McNair, P. J., Lewis, G. N., & Dalbeth, N. (2014). Quadriceps arthrogenic muscle inhibition: The effects of experimental knee joint effusion on motor cortex excitability. Arthritis Research and Therapy, 16(1). https://doi.org/10.1186/s13075-014-0502-4
Rio, E., Kidgell, D., Purdam, C., Gaida, J., Moseley, G. L., Pearce, A. J., & Cook, J. (2015). Isometric exercise induces analgesia and reduces inhibition in patellar tendinopathy. British Journal of Sports Medicine, 49(19), 1277-1283. https://doi.org/10.1136/bjsports-2014-094386
Servodio Iammarrone, C., Cadossi, M., Sambri, A., Grosso, E., Corrado, B., & Servodio Iammarrone, F. (2016). Is there a role of pulsed electromagnetic fields in management of patellofemoral pain syndrome? Randomized controlled study at one year follow-up. Bioelectromagnetics, 37(2), 81-88. https://doi.org/10.1002/bem.21953
Sirico, F., Ricca, F., DI Meglio, F., Nurzynska, D., Castaldo, C., Spera, R., & Montagnani, S. (2017). Local corticosteroid versus autologous blood injections in lateral epicondylitis: meta-analysis of randomized controlled trials. European Journal of Physical and Rehabilitation Medicine, 53(3), 483-491. https://doi.org/10.23736/S1973-9087.16.04252-0
Sonnery-Cottet, B., Saithna, A., Quelard, B., Daggett, M., Borade, A., Ouanezar, H., … Blakeney, W. G. (2019). Arthrogenic muscle inhibition after ACL reconstruction: a scoping review of the efficacy of interventions. British Journal of Sports Medicine, 53(5), 289 LP - 298. https://doi.org/10.1136/bjsports-2017-098401
Spera, R., Belviso, I., Sirico, F., Palermi, S., Massa, B., Mazzeo, F., & Montesano, P. (2019). Jump and balance test in judo athletes with or without visual impairments. Journal of Human Sport and Exercise, 14(Proc4), S937-S947. https://doi.org/10.14198/jhse.2019.14.Proc4.56
Sweeney, H. L., & Hammers, D. W. (2018). Muscle Contraction. Cold Spring Harbor Perspectives in Biology, 10(2). https://doi.org/10.1101/cshperspect.a023200
Tesch, P. A., Fernandez-Gonzalo, R., & Lundberg, T. R. (2017, April 27). Clinical applications of iso-inertial, eccentric-overload (YoYoTM) resistance exercise. Frontiers in Physiology. Frontiers Media S.A. https://doi.org/10.3389/fphys.2017.00241
Vola, E. A., Albano, M., Di Luise, C., Servodidio, V., Sansone, M., Russo, S., … Vallone, G. (2018). Use of ultrasound shear wave to measure muscle stiffness in children with cerebral palsy. Journal of Ultrasound, 21(3), 241-247. https://doi.org/10.1007/s40477-018-0313-6
Wang, K., McClure, J., & Tu, A. (1979). Titin: Major myofibrillar components of striated muscle. Proceedings of the National Academy of Sciences of the United States of America, 76(8), 3698-3702. https://doi.org/10.1073/pnas.76.8.3698
Yamasaki, R., Berri, M., Wu, Y., Trombitás, K., McNabb, M., Kellermayer, M. S., … Granzier, H. (2001). Titin-actin interaction in mouse myocardium: passive tension modulation and its regulation by calcium/S100A1. Biophysical Journal, 81(4), 2297-2313. https://doi.org/10.1016/S0006-3495(01)75876-6
Zot, A. S., & Potter, J. D. (1987). Structural aspects of troponin-tropomyosin regulation of skeletal muscle contraction. Annual Review of Biophysics and Biophysical Chemistry. Annu Rev Biophys Biophys Chem. https://doi.org/10.1146/annurev.bb.16.060187.002535
Published
How to Cite
Issue
Section
License
Copyright (c) 2020 Journal of Human Sport and Exercise
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Each author warrants that his or her submission to the Work is original and that he or she has full power to enter into this agreement. Neither this Work nor a similar work has been published elsewhere in any language nor shall be submitted for publication elsewhere while under consideration by JHSE. Each author also accepts that the JHSE will not be held legally responsible for any claims of compensation.
Authors wishing to include figures or text passages that have already been published elsewhere are required to obtain permission from the copyright holder(s) and to include evidence that such permission has been granted when submitting their papers. Any material received without such evidence will be assumed to originate from the authors.
Please include at the end of the acknowledgements a declaration that the experiments comply with the current laws of the country in which they were performed. The editors reserve the right to reject manuscripts that do not comply with the abovementioned requirements. The author(s) will be held responsible for false statements or failure to fulfill the above-mentioned requirements.
This title is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International license (CC BY-NC-ND 4.0).
You are free to share, copy and redistribute the material in any medium or format. The licensor cannot revoke these freedoms as long as you follow the license terms under the following terms:
Attribution — You must give appropriate credit, provide a link to the license, and indicate if changes were made. You may do so in any reasonable manner, but not in any way that suggests the licensor endorses you or your use.
NonCommercial — You may not use the material for commercial purposes.
NoDerivatives — If you remix, transform, or build upon the material, you may not distribute the modified material.
No additional restrictions — You may not apply legal terms or technological measures that legally restrict others from doing anything the license permits.
Notices:
You do not have to comply with the license for elements of the material in the public domain or where your use is permitted by an applicable exception or limitation.
No warranties are given. The license may not give you all of the permissions necessary for your intended use. For example, other rights such as publicity, privacy, or moral rights may limit how you use the material.
Transfer of Copyright
In consideration of JHSE’s publication of the Work, the authors hereby transfer, assign, and otherwise convey all copyright ownership worldwide, in all languages, and in all forms of media now or hereafter known, including electronic media such as CD-ROM, Internet, and Intranet, to JHSE. If JHSE should decide for any reason not to publish an author’s submission to the Work, JHSE shall give prompt notice of its decision to the corresponding author, this agreement shall terminate, and neither the author nor JHSE shall be under any further liability or obligation.
Each author certifies that he or she has no commercial associations (e.g., consultancies, stock ownership, equity interest, patent/licensing arrangements, etc.) that might pose a conflict of interest in connection with the submitted article, except as disclosed on a separate attachment. All funding sources supporting the Work and all institutional or corporate affiliations of the authors are acknowledged in a footnote in the Work.
Each author certifies that his or her institution has approved the protocol for any investigation involving humans or animals and that all experimentation was conducted in conformity with ethical and humane principles of research.
Competing Interests
Biomedical journals typically require authors and reviewers to declare if they have any competing interests with regard to their research.
JHSE require authors to agree to Copyright Notice as part of the submission process.
