Sarcomere Maturation: Function Acquisition, Molecular Mechanism, and Interplay with Other Organelles

Overview

Journal Philos Trans R Soc Lond B Biol Sci

Specialty Biology

Date 2022 Oct 3

PMID 36189811

Authors

Razan E Ahmed

Takeshi Tokuyama

Tatsuya Anzai

Nawin Chanthra

Hideki Uosaki

Affiliations

Soon will be listed here.

Abstract

During postnatal cardiac development, cardiomyocytes mature and turn into adult ones. Hence, all cellular properties, including morphology, structure, physiology and metabolism, are changed. One of the most important aspects is the contractile apparatus, of which the minimum unit is known as a sarcomere. Sarcomere maturation is evident by enhanced sarcomere alignment, ultrastructural organization and myofibrillar isoform switching. Any maturation process failure may result in cardiomyopathy. Sarcomere function is intricately related to other organelles, and the growing evidence suggests reciprocal regulation of sarcomere and mitochondria on their maturation. Herein, we summarize the molecular mechanism that regulates sarcomere maturation and the interplay between sarcomere and other organelles in cardiomyocyte maturation. This article is part of the theme issue 'The cardiomyocyte: new revelations on the interplay between architecture and function in growth, health, and disease'.

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References

Uosaki H, Cahan P, Lee D, Wang S, Miyamoto M, Fernandez L . Transcriptional Landscape of Cardiomyocyte Maturation. Cell Rep. 2015; 13(8):1705-16. PMC: 4662925. DOI: 10.1016/j.celrep.2015.10.032. View

Zhang T, Lin Y, Liu J, Zhang Z, Fu W, Guo L . Rbm24 Regulates Alternative Splicing Switch in Embryonic Stem Cell Cardiac Lineage Differentiation. Stem Cells. 2016; 34(7):1776-89. DOI: 10.1002/stem.2366. View

Heffler J, Shah P, Robison P, Phyo S, Veliz K, Uchida K . A Balance Between Intermediate Filaments and Microtubules Maintains Nuclear Architecture in the Cardiomyocyte. Circ Res. 2019; 126(3):e10-e26. PMC: 7029779. DOI: 10.1161/CIRCRESAHA.119.315582. View

Homma S, Iwasaki M, Shelton G, Engvall E, Reed J, Takayama S . BAG3 deficiency results in fulminant myopathy and early lethality. Am J Pathol. 2006; 169(3):761-73. PMC: 1698816. DOI: 10.2353/ajpath.2006.060250. View

Reza N, Garg A, Merrill S, Chowns J, Rao S, Owens A . ACTA1 Novel Likely Pathogenic Variant in a Family With Dilated Cardiomyopathy. Circ Genom Precis Med. 2018; 11(10):e002243. PMC: 6208136. DOI: 10.1161/CIRCGEN.118.002243. View

Chanthra N, Abe T, Miyamoto M, Sekiguchi K, Kwon C, Hanazono Y . A Novel Fluorescent Reporter System Identifies Laminin-511/521 as Potent Regulators of Cardiomyocyte Maturation. Sci Rep. 2020; 10(1):4249. PMC: 7060274. DOI: 10.1038/s41598-020-61163-3. View

Dabiri G, Turnacioglu K, Sanger J, Sanger J . Myofibrillogenesis visualized in living embryonic cardiomyocytes. Proc Natl Acad Sci U S A. 1997; 94(17):9493-8. PMC: 23235. DOI: 10.1073/pnas.94.17.9493. View

Takeda S, Yamashita A, Maeda K, Maeda Y . Structure of the core domain of human cardiac troponin in the Ca(2+)-saturated form. Nature. 2003; 424(6944):35-41. DOI: 10.1038/nature01780. View

Agarkova I, Ehler E, Lange S, Schoenauer R, Perriard J . M-band: a safeguard for sarcomere stability?. J Muscle Res Cell Motil. 2003; 24(2-3):191-203. DOI: 10.1023/a:1026094924677. View

10.

Favaro G, Romanello V, Varanita T, Desbats M, Morbidoni V, Tezze C . DRP1-mediated mitochondrial shape controls calcium homeostasis and muscle mass. Nat Commun. 2019; 10(1):2576. PMC: 6561930. DOI: 10.1038/s41467-019-10226-9. View

11.

Clark K, McElhinny A, Beckerle M, Gregorio C . Striated muscle cytoarchitecture: an intricate web of form and function. Annu Rev Cell Dev Biol. 2002; 18:637-706. DOI: 10.1146/annurev.cellbio.18.012502.105840. View

12.

Fukuda R, Gunawan F, Ramadass R, Beisaw A, Konzer A, Mullapudi S . Mechanical Forces Regulate Cardiomyocyte Myofilament Maturation via the VCL-SSH1-CFL Axis. Dev Cell. 2019; 51(1):62-77.e5. DOI: 10.1016/j.devcel.2019.08.006. View

13.

Lahmers S, Wu Y, Call D, Labeit S, Granzier H . Developmental control of titin isoform expression and passive stiffness in fetal and neonatal myocardium. Circ Res. 2004; 94(4):505-13. DOI: 10.1161/01.RES.0000115522.52554.86. View

14.

Spinozzi S, Liu C, Chen Z, Feng W, Zhang L, Ouyang K . Nexilin Is Necessary for Maintaining the Transverse-Axial Tubular System in Adult Cardiomyocytes. Circ Heart Fail. 2020; 13(7):e006935. PMC: 7583668. DOI: 10.1161/CIRCHEARTFAILURE.120.006935. View

15.

Katzemich A, Kreiskother N, Alexandrovich A, Elliott C, Schock F, Leonard K . The function of the M-line protein obscurin in controlling the symmetry of the sarcomere in the flight muscle of Drosophila. J Cell Sci. 2012; 125(Pt 14):3367-79. PMC: 3516378. DOI: 10.1242/jcs.097345. View

16.

Lee E, Marcucci M, Daniell L, Pypaert M, Weisz O, Farsad K . Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science. 2002; 297(5584):1193-6. DOI: 10.1126/science.1071362. View

17.

Murphy S, Miyamoto M, Kervadec A, Kannan S, Tampakakis E, Kambhampati S . PGC1/PPAR drive cardiomyocyte maturation at single cell level via YAP1 and SF3B2. Nat Commun. 2021; 12(1):1648. PMC: 7955035. DOI: 10.1038/s41467-021-21957-z. View

18.

Gregorio C, Antin P . To the heart of myofibril assembly. Trends Cell Biol. 2000; 10(9):355-62. DOI: 10.1016/s0962-8924(00)01793-1. View

19.

Takayama S, Bimston D, Matsuzawa S, Freeman B, Aime-Sempe C, Xie Z . BAG-1 modulates the chaperone activity of Hsp70/Hsc70. EMBO J. 1997; 16(16):4887-96. PMC: 1170124. DOI: 10.1093/emboj/16.16.4887. View

20.

Franzini-Armstrong C, Landmesser L, PILAR G . Size and shape of transverse tubule openings in frog twitch muscle fibers. J Cell Biol. 1975; 64(2):493-7. PMC: 2109503. DOI: 10.1083/jcb.64.2.493. View