Sarcomere. The structural unit of the myofibrillar complex of typical cardiomyocytes. Isometric aspects of sarcomere organization

Authors

DOI:

https://doi.org/10.26641/1997-9665.2024.1.83-88

Keywords:

sarcomere, actin and myosin, contraction, cardiomyocyte, electron microscopy.

Abstract

Background. The complexity of understanding the structure and function of cardiomyocytes in the myocardium is a fundamental problem in the field of heart morphology. Sarcomeres are the main structural and functional units of myofibrils. Understanding the organization and dynamics of sarcomeres in cardiomyocytes is crucial for establishing the mechanisms responsible for the process of forming the contractile system of cardiomyocytes. Objective. The main purpose of this study is a review of literary sources that complement and expand the essential findings about the construction of myofibrils and their components when studied by effective methods of microscopic techniques. Materials. Literature review databases, systematic search of primary sources related to the research topic. Methods of visual examination of the components of sarcomeres and elements of their organization. Results. Transmission electron microscopy provides high-resolution imaging of sarcomeres, which is necessary for detailed analysis of their ultrastructure, including visualization of sarcomere components such as Z-discs, M-lines, thick and thin filaments. Morphometric methods are crucial for studying the compaction and orientation of myofibrils in cardiomyocytes. Conclusion. Morphometric methods provide valuable information about the structural remodeling of myofibrils in response to physiological stimuli or pathological conditions. These techniques are needed to improve our understanding of the mechanisms underlying muscle contraction and to develop methods to study cardiac remodeling processes in response to the adaptive response.

References

  1. Lehman SJ, Crocini C, Leinwand LA. Targeting the sarcomere in inherited cardiomyopathies. Nat Rev Cardiol. 2022;19(6):353-63. doi: 10.1038/s41569-022-00682-0. Epub 2022 Mar 18. PMID: 35304599; PMCID: PMC9119933.
  2. Pettinato AM, Ladha FA, Hinson JT. The Cardiac Sarcomere and Cell Cycle. Curr Cardiol Rep. 2022;24(6):623-30. doi: 10.1007/s11886-022-01682-9. Epub 2022 Apr 5. PMID: 35380383.
  3. Wang Z, Grange M, Wagner T, Kho AL, Gautel M, Raunser S. The molecular basis for sarcomere organization in vertebrate skeletal muscle. Cell. 2021;184(8):2135-50. doi: 10.1016/j.cell.2021.02.047. Epub 2021 Mar 24. PMID: 33765442; PMCID: PMC8054911.
  4. Tsukamoto O. Direct Sarcomere Modulators Are Promising New Treatments for Cardiomyopathies. Int J Mol Sci. 2019;21(1):226. doi: 10.3390/ijms21010226. PMID: 31905684; PMCID: PMC6982115.
  5. Nayak A, Amrute-Nayak M. SUMO system - a key regulator in sarcomere organization. FEBS J. 2020;287(11):2176-90. doi: 10.1111/febs.15263. Epub 2020 Mar 13. PMID: 32096922.
  6. Watkins H. Time to Think Differently About Sarcomere-Negative Hypertrophic Cardiomyopathy. Circulation. 2021;143(25):2415-17. doi: 10.1161/CIRCULATIONAHA.121.053527. Epub 2021 Jun 21. PMID: 34152793.
  7. Henderson CA, Gomez CG, Novak SM, Mi-Mi L, Gregorio CC. Overview of the Muscle Cytoskeleton. Compr Physiol. 2017;7(3):891-944. doi: 10.1002/cphy.c160033. PMID: 28640448; PMCID: PMC5890934.
  8. Toepfer CN, Garfinkel AC, Venturini G, Wakimoto H, Repetti G, Alamo L, Sharma A, Agarwal R, Ewoldt JK, Cloonan P, Letendre J, Lun M, Olivotto I, Colan S, Ashley E, Jacoby D, Michels M, Redwood CS, Watkins HC, Day SM, Staples JF, Padrón R, Chopra A, Ho CY, Chen CS, Pereira AC, Seidman JG, Seidman CE. Myosin Sequestration Regulates Sarcomere Function, Cardiomyocyte Energetics, and Metabolism, Informing the Pathogenesis of Hypertrophic Cardiomyopathy. Circulation. 2020;141(10):828-42. doi: 10.1161/CIRCULATIONAHA.119.042339. Epub 2020 Jan 27. Erratum in: Circulation. 2020 Mar 10;141(10):e645. PMID: 31983222; PMCID: PMC7077965.
  9. Li J, Sundnes J, Hou Y, Laasmaa M, Ruud M, Unger A, Kolstad TR, Frisk M, Norseng PA, Yang L, Setterberg IE, Alves ES, Kalakoutis M, Sejersted OM, Lanner JT, Linke WA, Lunde IG, de Tombe PP, Louch WE. Stretch Harmonizes Sarcomere Strain Across the Cardiomyocyte. Circ Res. 2023;133(3):255-70. doi: 10.1161/CIRCRESAHA.123.322588. Epub 2023 Jul 4. PMID: 37401464; PMCID: PMC10355805.
  10. Nguyen PD, Gooijers I, Campostrini G, Verkerk AO, Honkoop H, Bouwman M, de Bakker DEM, Koopmans T, Vink A, Lamers GEM, Shakked A, Mars J, Mulder AA, Chocron S, Bartscherer K, Tzahor E, Mummery CL, de Boer TP, Bellin M, Bakkers J. Interplay between calcium and sarcomeres directs cardiomyocyte maturation during regeneration. Science. 2023;380(6646):758-64. doi: 10.1126/science.abo6718. Epub 2023 May 18. PMID: 37200435.
  11. Pettinato AM, Ladha FA, Hinson JT. The Cardiac Sarcomere and Cell Cycle. Curr Cardiol Rep. 2022;24(6):623-30. doi: 10.1007/s11886-022-01682-9. Epub 2022 Apr 5. PMID: 35380383.
  12. Lookin O, de Tombe P, Boulali N, Gergely C, Cloitre T, Cazorla O. Cardiomyocyte sarcomere length variability: Membrane fluorescence versus second harmonic generation myosin imaging. J Gen Physiol. 2023;155(4):e202213289. doi: 10.1085/jgp.202213289. Epub 2023 Jan 25. PMID: 36695814; PMCID: PMC9930136.
  13. Ahmed RE, Tokuyama T, Anzai T, Chanthra N, Uosaki H. Sarcomere maturation: function acquisition, molecular mechanism, and interplay with other organelles. Philos Trans R Soc Lond B Biol Sci. 2022;377(1864):20210325. doi: 10.1098/rstb.2021.0325. Epub 2022 Oct 3. PMID: 36189811; PMCID: PMC9527934.
  14. Gerdes AM. How to improve the overall quality of cardiac morphometric data. Am J Physiol Heart Circ Physiol. 2015;309(1):9-14. doi: 10.1152/ajpheart.00232.2015. Epub 2015 May 8. PMID: 25957219.
  15. Sjöström M, Angquist KA, Bylund AC, Fridén J, Gustavsson L, Scherstén T. Morphometric analyses of human muscle fiber types. Muscle Nerve. 1982;5(7):538-53. doi: 10.1002/mus.880050708. PMID: 6292711.
  16. Cury DP, Dias FJ, Sosthenes MC, Dos Santos Haemmerle CA, Ogawa K, Da Silva MC, Mardegan Issa JP, Iyomasa MM, Watanabe IS. Morphometric, quantitative, and three-dimensional analysis of the heart muscle fibers of old rats: transmission electron microscopy and high-resolution scanning electron microscopy methods. Microsc Res Tech. 2013;76(2):184-95. doi: 10.1002/jemt.22151. Epub 2012 Nov 24. PMID: 23180425.
  17. Fanin M, Nascimbeni AC, Angelini C. Muscle atrophy in Limb Girdle Muscular Dystrophy 2A: a morphometric and molecular study. Neuropathol Appl Neurobiol. 2013;39(7):762-71. doi: 10.1111/nan.12034. PMID: 23414389.
  18. Squire J. Special Issue: The Actin-Myosin Interaction in Muscle: Background and Overview. Int J Mol Sci. 2019;20(22):5715. doi: 10.3390/ijms20225715. PMID: 31739584; PMCID: PMC6887992.
  19. Dittloff KT, Spanghero E, Solís C, Banach K, Russell B. Transthyretin deposition alters cardiomyocyte sarcomeric architecture, calcium transients, and contractile force. Physiol Rep. 2022;10(5):15207. doi: 10.14814/phy2.15207. PMID: 35262277; PMCID: PMC8906053.
  20. Pasqualin C, Gannier F, Yu A, Malécot CO, Bredeloux P, Maupoil V. SarConfoCal: simultaneous sarcomere length and cytoplasmic calcium measurements for laser scanning confocal microscopy images. Bioinformatics. 2017;33(5):789-90. doi: 10.1093/bioinformatics/btw754. PMID: 28011776.
  21. Wang J, Fan Y, Sanger JM, Sanger JW. Nonmuscle myosin II in cardiac and skeletal muscle cells. Cytoskeleton (Hoboken). 2018;75(8):339-51. doi: 10.1002/cm.21454. PMID: 29781105; PMCID: PMC6249054.
  22. Nicolas JD, Bernhardt M, Schlick SF, Tiburcy M, Zimmermann WH, Khan A, Markus A, Alves F, Toischer K, Salditt T. X-ray diffraction imaging of cardiac cells and tissue. Prog Biophys Mol Biol. 2019;144:151-65. doi: 10.1016/j.pbiomolbio.2018.05.012. Epub 2018 Jun 18. PMID: 29914693.
  23. Usukura E, Narita A, Yagi A, Sakai N, Uekusa Y, Imaoka Y, Ito S, Usukura J. A Cryosectioning Technique for the Observation of Intracellular Structures and Immunocytochemistry of Tissues in Atomic Force Microscopy (AFM). Sci Rep. 2017;7(1):6462. doi: 10.1038/s41598-017-06942-1. PMID: 28743939; PMCID: PMC5526917.
  24. Camors EM, Roth AH, Alef JR, Sullivan RD, Johnson JN, Purevjav E, Towbin JA. Progressive Reduction in Right Ventricular Contractile Function Attributable to Altered Actin Expression in an Aging Mouse Model of Arrhythmogenic Cardiomyopathy. Circulation. 2022;145(21):1609-24. doi: 10.1161/CIRCULATIONAHA.120.049261. Epub 2022 Apr 19. PMID: 35437032; PMCID: PMC9133220.
  25. Bradshaw M, Paul DM. After the revolution: how is Cryo-EM contributing to muscle research? J Muscle Res Cell Motil. 2019;40(2):93-98. doi: 10.1007/s10974-019-09537-7. Epub 2019 Jul 13. PMID: 31302812; PMCID: PMC6726666.
  26. Dadson K, Hauck L, Billia F. Molecular mechanisms in cardiomyopathy. Clin Sci (Lond). 2017;131(13):1375-92. doi: 10.1042/CS20160170. PMID: 28645928.
  27. Mouton J, Loos B, Moolman-Smook JC, Kinnear CJ. Ascribing novel functions to the sarcomeric protein, myosin binding protein H (MyBPH) in cardiac sarcomere contraction. Exp Cell Res. 2015;331(2):338-51. doi: 10.1016/j.yexcr.2014.11.006. Epub 2014 Nov 18. PMID: 25449695.
  28. Poole DC, Batra S, Mathieu-Costello O, Rakusan K. Capillary geometrical changes with fiber shortening in rat myocardium. Circ Res. 1992;70(4):697-706. doi: 10.1161/01.res.70.4.697. PMID: 1551196.
  29. Cury DP, Dias FJ, Sosthenes MC, Dos Santos Haemmerle CA, Ogawa K, Da Silva MC, Mardegan Issa JP, Iyomasa MM, Watanabe IS. Morphometric, quantitative, and three-dimensional analysis of the heart muscle fibers of old rats: transmission electron microscopy and high-resolution scanning electron microscopy methods. Microsc Res Tech. 2013;76(2):184-95. doi: 10.1002/jemt.22151. Epub 2012 Nov 24. PMID: 23180425.
  30. Telley IA, Denoth J. Sarcomere dynamics during muscular contraction and their implications to muscle function. J Muscle Res Cell Motil. 2007;28(1):89-104. doi: 10.1007/s10974-007-9107-8. Epub 2007 May 26. PMID: 17530424.
  31. Burbaum L, Schneider J, Scholze S, Böttcher RT, Baumeister W, Schwille P, Plitzko JM, Jasnin M. Molecular-scale visualization of sarcomere contraction within native cardiomyocytes. Nat Commun. 2021;12(1):4086. doi: 10.1038/s41467-021-24049-0. PMID: 34215727; PMCID: PMC8253822.
  32. Lange S, Pinotsis N, Agarkova I, Ehler E. The M-band: The underestimated part of the sarcomere. Biochim Biophys Acta Mol Cell Res. 2020;1867(3):118440. doi: 10.1016/j.bbamcr.2019.02.003. Epub 2019 Feb 7. PMID: 30738787; PMCID: PMC7023976.
  33. De Souza Leite F, Rassier DE. Sarcomere Length Nonuniformity and Force Regulation in Myofibrils and Sarcomeres. Biophys J. 2020;119(12):2372-7. doi: 10.1016/j.bpj.2020.11.005. Epub 2020 Nov 18. PMID: 33217382; PMCID: PMC7822744.

Downloads

Published

2024-04-29

How to Cite

Kobeza, P. (2024). Sarcomere. The structural unit of the myofibrillar complex of typical cardiomyocytes. Isometric aspects of sarcomere organization. Морфологія / Morphologia / Morfologìâ, 18(1), 83–88. https://doi.org/10.26641/1997-9665.2024.1.83-88

Issue

Vol. 18 No. 1 (2024)

Section

Статті

License

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

 The authors reserve the right to authorship of their work and transfer to the Journal the right to the first publication of this work under the terms of a license Creative commons Attribution 4.0 International (CC BY 4.0), which allows other people to freely distribute the published work with a mandatory reference to the authors of the original work and the first publication of the work in this journal.
        By submitting a manuscript to the editorial office of the Journal ‘Morphologia’ authors agree to transfer the rights to protect and use the manuscript (all supplemental materials, particularly protected objects such as photos, drawings, diagrams, tables, etc.), including the reproduction in the press and distribution via the Internet; translation of the manuscript into any language; export and import of journal copies with the Authors’ article in order to make it available for public. Authors convey the rights mentioned above to the editorial office without any temporal or territorial limitation all over the world. 
        The Authors guarantee that they have the exclusive rights to use the material transferred to editorial office. Editors are not responsible to third parties for contraventions of warranty given by the Authors. The considered rights are transferred to the editorial office since the moment when the current issue is signed for publishing. Reproduction of materials published in the Journal by other individuals and legal entities is possible only with the consent of Editorial office, with the obligatory indication of the full bibliographic reference of the primary publication. The Authors reserve the right to use the published material, its fragments and parts for teaching materials, oral presentations, dissertation thesis prepararion with obligatory bibliographic citation of the original paper. Electron copy of the published article, downloaded from official journal web-site in .pdf format may be put by authors on the official web-site of their institutions, any other official resources with open access.