RSU-1 Regulates the Integrity of Dense Bodies in Muscle Cells of Aging

Overview

Journal iScience

Publisher Cell Press

Date 2024 May 24

PMID 38784006

Authors

Ling Jiang

Xinyan Wang

Dandan Zhang

Karen Wing Yee Yuen

Yu Chung Tse

Affiliations

Soon will be listed here.

Abstract

Muscle contraction is vital for animal survival, and the sarcomere is the fundamental unit for this process. However, the functions of many conserved sarcomere proteins remain unknown, as their mutants do not exhibit obvious defects. To address this, was utilized as a model organism to investigate RSU-1 function in the body wall muscle. RSU-1 is found to colocalize with UNC-97 at the dense body and M-line, and it is particularly crucial for regulating locomotion in aging worms, rather than in young worms. This suggests that RSU-1 has a specific function in maintaining muscle function during aging. Furthermore, the interaction between RSU-1 and UNC-97/PINCH is essential for RSU-1 to modulate locomotion, preserve filament structure, and sustain the M-line and dense body throughout aging. Overall, these findings highlight the significant contribution of RSU-1, through its interaction with UNC-97, in maintaining proper muscle cell function in aging worms.

References

Lim J, Frontera W . Single skeletal muscle fiber mechanical properties: a muscle quality biomarker of human aging. Eur J Appl Physiol. 2022; 122(6):1383-1395. DOI: 10.1007/s00421-022-04924-4. View

Qadota H, Moody J, Lesanpezeshki L, Moncrief T, Kitzler D, Bhat P . A Region of UNC-89 (Obscurin) Lying between Two Protein Kinase Domains Is a Highly Elastic Spring Required for Proper Sarcomere Organization. J Mol Biol. 2020; 432(17):4799-4814. PMC: 9549344. DOI: 10.1016/j.jmb.2020.06.024. View

Wang X, Huang S, Zheng C, Ge W, Wu C, Tse Y . RSU-1 Maintains Integrity of Vulval Muscles by Regulating α-Actinin. G3 (Bethesda). 2020; 10(7):2507-2517. PMC: 7341117. DOI: 10.1534/g3.120.401185. View

Garcia G, Homentcovschi S, Kelet N, Higuchi-Sanabria R . Imaging of Actin Cytoskeletal Integrity During Aging in C. elegans. Methods Mol Biol. 2021; 2364:101-137. DOI: 10.1007/978-1-0716-1661-1_5. View

Yin J, Gao G, Liu X, Hao Z, Li K, Kang X . Genetic variation in glia-neuron signalling modulates ageing rate. Nature. 2017; 551(7679):198-203. DOI: 10.1038/nature24463. View

Wang Z, Grange M, Wagner T, Kho A, Gautel M, Raunser S . The molecular basis for sarcomere organization in vertebrate skeletal muscle. Cell. 2021; 184(8):2135-2150.e13. PMC: 8054911. DOI: 10.1016/j.cell.2021.02.047. View

Qadota H, Mayans O, Matsunaga Y, McMurry J, Wilson K, Kwon G . The SH3 domain of UNC-89 (obscurin) interacts with paramyosin, a coiled-coil protein, in Caenorhabditis elegans muscle. Mol Biol Cell. 2016; 27(10):1606-20. PMC: 4865318. DOI: 10.1091/mbc.E15-09-0675. View

Ono S, Lewis M, Ono K . Mutual dependence between tropomodulin and tropomyosin in the regulation of sarcomeric actin assembly in Caenorhabditis elegans striated muscle. Eur J Cell Biol. 2022; 101(2):151215. PMC: 9081161. DOI: 10.1016/j.ejcb.2022.151215. View

Benian G, Tinley T, Tang X, Borodovsky M . The Caenorhabditis elegans gene unc-89, required fpr muscle M-line assembly, encodes a giant modular protein composed of Ig and signal transduction domains. J Cell Biol. 1996; 132(5):835-48. PMC: 2120741. DOI: 10.1083/jcb.132.5.835. View

10.

Dougherty G, Chopp T, Qi S, Cutler M . The Ras suppressor Rsu-1 binds to the LIM 5 domain of the adaptor protein PINCH1 and participates in adhesion-related functions. Exp Cell Res. 2005; 306(1):168-79. DOI: 10.1016/j.yexcr.2005.01.025. View

11.

Timmons L, Fire A . Specific interference by ingested dsRNA. Nature. 1998; 395(6705):854. DOI: 10.1038/27579. View

12.

Moerman D, Williams B . Sarcomere assembly in C. elegans muscle. WormBook. 2007; :1-16. PMC: 4781162. DOI: 10.1895/wormbook.1.81.1. View

13.

Lecuit T, Lenne P, Munro E . Force generation, transmission, and integration during cell and tissue morphogenesis. Annu Rev Cell Dev Biol. 2011; 27:157-84. DOI: 10.1146/annurev-cellbio-100109-104027. View

14.

Gaiser A, Kaiser C, Haslbeck V, Richter K . Downregulation of the Hsp90 system causes defects in muscle cells of Caenorhabditis elegans. PLoS One. 2011; 6(9):e25485. PMC: 3182237. DOI: 10.1371/journal.pone.0025485. View

15.

Wu J, Ding P, Wu H, Yang P, Guo H, Tian Y . Sarcopenia: Molecular regulatory network for loss of muscle mass and function. Front Nutr. 2023; 10:1037200. PMC: 9932270. DOI: 10.3389/fnut.2023.1037200. View

16.

Zhang S, Li F, Zhou T, Wang G, Li Z . as a Useful Model for Studying Aging Mutations. Front Endocrinol (Lausanne). 2020; 11:554994. PMC: 7570440. DOI: 10.3389/fendo.2020.554994. View

17.

Dridi H, Forrester F, Umanskaya A, Xie W, Reiken S, Lacampagne A . Role of oxidation of excitation-contraction coupling machinery in age-dependent loss of muscle function in . Elife. 2022; 11. PMC: 9113742. DOI: 10.7554/eLife.75529. View

18.

Lecroisey C, Segalat L, Gieseler K . The C. elegans dense body: anchoring and signaling structure of the muscle. J Muscle Res Cell Motil. 2007; 28(1):79-87. DOI: 10.1007/s10974-007-9104-y. View

19.

Wilson K, Qadota H, Benian G . Immunofluorescent localization of proteins in Caenorhabditis elegans muscle. Methods Mol Biol. 2011; 798:171-81. PMC: 3731740. DOI: 10.1007/978-1-61779-343-1_10. View

20.

Sweeney H, Hammers D . Muscle Contraction. Cold Spring Harb Perspect Biol. 2018; 10(2). PMC: 5793755. DOI: 10.1101/cshperspect.a023200. View