MuRF-1 is Involved in Laryngeal Muscle Denervation Atrophy by Regulating G-Actin Ubiquitination.
F-actin
G-actin
internal laryngeal muscle denervated atrophy
muscle RING-finger protein-1
ubiquitination
Journal
The Laryngoscope
ISSN: 1531-4995
Titre abrégé: Laryngoscope
Pays: United States
ID NLM: 8607378
Informations de publication
Date de publication:
02 Sep 2023
02 Sep 2023
Historique:
revised:
05
08
2023
received:
09
05
2023
accepted:
16
08
2023
medline:
2
9
2023
pubmed:
2
9
2023
entrez:
2
9
2023
Statut:
aheadofprint
Résumé
Muscle RING-finger protein-1 (MuRF-1), an E3 ubiquitin ligase, has been reported to aggravate skeletal muscle denervated atrophy by mediating the ubiquitination degradation of multiple proteins, whereas the molecular mechanism underlying MuRF-1-mediated internal laryngeal muscle denervated atrophy remains unknown. A rat unilateral recurrent laryngeal nerve (RLN) transection model was established to evaluate denervated muscle atrophy of the larynx. The expression of MuRF-1, G- and F-actin in thyroarytenoid muscle (TA) myocytes before and after RLN injury was analyzed by immunofluorescence and Western blotting. Coimmunoprecipitation experiments detected molecular interactions between MuRF-1 and G-actin. Immunoprecipitation tested MuRF-1-mediated ubiquitination of G-actin in denervated and innervated TA muscle tissues. The shRNA-MuRF-1 AAV was used to suppress MuRF-1 expression in denervated TA muscles in vivo. First, MuRF-1 expression was significantly elevated in denervated TA muscle compared to innervated TA muscle (p < 0.001). Second, there was a progressive increase in the G/F-actin ratio in TA myocytes from day 3 to 14 after RLNI (p < 0.01). Furthermore, colocalization of MuRF-1 and G-actin in denervated TA myocytes was observed. Moreover, the upregulation of MuRF-1 was closely associated with the ubiquitination of G-actin in denervated TA myocytes and muscle tissues. Knockdown of MuRF-1 decelerated the degree of TA muscle atrophy compared with that in the Blank and NC groups (p < 0.001) but seemed to promote the compensatory movement of the healthy side. Collectively, we illustrate a novel molecular mechanism underlying MuRF-1-mediated internal laryngeal muscle denervated atrophy in that MuRF-1 could promote disequilibrium of the G/F-actin ratio by regulating G-actin ubiquitination. N/A Laryngoscope, 2023.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Beijing Tongren Hospital Intra-Hospital Fund for the Young Reserve Talent
ID : ynkywh1
Organisme : Beijing Municipal Natural Science Foundation
ID : 7172051
Organisme : Capital Medical University Research Nurturing Fund (Natural Science Category)
ID : PYZ21099
Organisme : National Natural Science Foundation of China
ID : 82201267
Informations de copyright
© 2023 The American Laryngological, Rhinological and Otological Society, Inc.
Références
Mattei A, Desuter G, Roux M, et al. International consensus (ICON) on basic voice assessment for unilateral vocal fold paralysis. Eur Ann Otorhinolaryngol Head Neck Dis. 2018;135:S11-S15.
Wang H, Wang H, Li X, Xu W. Characteristics of early internal laryngeal muscle atrophy after recurrent laryngeal nerve injuries in rats. Laryngoscope. 2021;131:E1256-E1264.
Taillandier D, Polge C. Skeletal muscle atrogenes: from rodent models to human pathologies. Biochimie. 2019;166:251-269.
Sei H, Taguchi A, Nishida N, Hato N, Gyo K. Expression of atrophy-related transcription factors in the process of intrinsic laryngeal muscle atrophy after denervation. Eur Arch Otorhinolaryngol. 2015;272:137-141.
Lang F, Aravamudhan S, Nolte H, et al. Dynamic changes in the mouse skeletal muscle proteome during denervation-induced atrophy. Dis Model Mech. 2017;10:881-896.
Olie CS, van der Wal E, Cikes D, et al. Author correction: cytoskeletal disorganization underlies PABPN1-mediated myogenic disability. Sci Rep. 2021;11:6429.
Becker EW. The roles of ATP in the dynamics of the Actin filaments of the cytoskeleton. Biol Chem. 2006;387:401-406.
Nguyen T, Bowen TS, Augstein A, et al. Expression of MuRF1 or MuRF2 is essential for the induction of skeletal muscle atrophy and dysfunction in a murine pulmonary hypertension model. Skelet Muscle. 2020;10:12.
Clarke BA, Drujan D, Willis MS, et al. The E3 ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab. 2007;6:376-385.
Franke B, Gasch A, Rodriguez D, et al. Molecular basis for the fold organization and sarcomeric targeting of the muscle atrogin MuRF1. Open Biol. 2014;4:130172.
Khan MM, Strack S, Wild F, et al. Role of autophagy, SQSTM1, SH3GLB1, and TRIM63 in the turnover of nicotinic acetylcholine receptors. Autophagy. 2014;10:123-136.
Baehr LM, Hughes DC, Lynch SA, et al. Identification of the MuRF1 skeletal muscle Ubiquitylome through quantitative proteomics. Function. 2021;2:zqab029.
Polge C, Heng AE, Jarzaguet M, et al. Muscle Actin is polyubiquitinylated in vitro and in vivo and targeted for breakdown by the E3 ligase MuRF1. FASEB J. 2011;25:3790-3802.
Cohen S, Brault JJ, Gygi SP, et al. During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation. J Cell Biol. 2009;185:1083-1095.
Peris-Moreno D, Malige M, Claustre A, et al. UBE2L3, A partner of MuRF1/TRIM63, is involved in the degradation of myofibrillar Actin and myosin. Cell. 2021;10:10.
Huang Z, Zhong L, Zhu J, et al. Inhibition of IL-6/JAK/STAT3 pathway rescues denervation-induced skeletal muscle atrophy. Ann Transl Med. 2020;8:1681.
Wang J, Tierney L, Wilson C, et al. Carboxyl-terminal modulator protein (CTMP) deficiency mitigates denervation-induced skeletal muscle atrophy. Biochem Biophys Res Commun. 2023;644:155-161.
Bedard N, Jammoul S, Moore T, et al. Inactivation of the ubiquitin-specific protease 19 deubiquitinating enzyme protects against muscle wasting. FASEB J. 2015;29:3889-3898.
Yang X, Xue P, Liu Z, Li W, Li C, Chen Z. SESN2 prevents the slow-to-fast myofiber shift in denervated atrophy via AMPK/PGC-1alpha pathway. Cell Mol Biol Lett. 2022;27:66.
Ribeiro F, Alves PKN, Bechara LRG, Ferreira JCB, Labeit S, Moriscot AS. Small-molecule inhibition of MuRF1 prevents early disuse-induced diaphragmatic dysfunction and atrophy. Int J Mol Sci. 2023;24(4):3637;1-17.
Peris-Moreno D, Taillandier D, Polge C. MuRF1/TRIM63, master regulator of muscle mass. Int J Mol Sci. 2020;21(18):6663;1-39.
Peris-Moreno D, Cussonneau L, Combaret L, Polge C, Taillandier D. Ubiquitin ligases at the heart of skeletal muscle atrophy control. Molecules. 2021;26(2):407;1-36.
Rudolf R, Bogomolovas J, Strack S, et al. Regulation of nicotinic acetylcholine receptor turnover by MuRF1 connects muscle activity to endo/lysosomal and atrophy pathways. Age. 2013;35:1663-1674.
Hooijman PE, Beishuizen A, Witt CC, et al. Diaphragm muscle fiber weakness and ubiquitin-proteasome activation in critically ill patients. Am J Respir Crit Care Med. 2015;191:1126-1138.
Cracknell T, Mannsverk S, Nichols A, Dowle A, Blanco G. Proteomic resolution of IGFN1 complexes reveals a functional interaction with the Actin nucleating protein COBL. Exp Cell Res. 2020;395:112179.
Domsch K, Acs A, Obermeier C, Nguyen HT, Reim I. Identification of the essential protein domains for Mib2 function during the development of the drosophila larval musculature and adult flight muscles. PloS One. 2017;12:e0173733.
Pollard TD. Actin and actin-binding proteins. Cold Spring Harb Perspect Biol. 2016;8(8):a018226.
Eddins MJ, Marblestone JG, Suresh Kumar KG, et al. Targeting the ubiquitin E3 ligase MuRF1 to inhibit muscle atrophy. Cell Biochem Biophys. 2011;60:113-118.
Adams V, Gussen V, Zozulya S, et al. Small-molecule chemical knockdown of MuRF1 in melanoma bearing mice attenuates tumor cachexia associated myopathy. Cell. 2020;9:9.
Bowen TS, Adams V, Werner S, et al. Small-molecule inhibition of MuRF1 attenuates skeletal muscle atrophy and dysfunction in cardiac cachexia. J Cachexia Sarcopenia Muscle. 2017;8:939-953.
Wan Q, Zhang L, Huang Z, et al. Aspirin alleviates denervation-induced muscle atrophy via regulating the Sirt1/PGC-1alpha axis and STAT3 signaling. Ann Transl Med. 2020;8:1524.
Hong Y, Lee JH, Jeong KW, Choi CS, Jun HS. Amelioration of muscle wasting by glucagon-like peptide-1 receptor agonist in muscle atrophy. J Cachexia Sarcopenia Muscle. 2019;10:903-918.
Liu Q, Yuan W, Yan Y, et al. Identification of a novel small-molecule inhibitor of miR-29b attenuates muscle atrophy. Mol Ther Nucleic Acids. 2023;31:527-540.
Xu X, Zhuang P, Wilson A, Jiang JJ. Compensatory movement of contralateral vocal folds in patients with unilateral vocal fold paralysis. J Voice. 2021;35:328 e323-e328.
Morales L, Gambhir Y, Bennett J, Stedman HH. Broader implications of progressive liver dysfunction and lethal sepsis in two boys following systemic high-dose AAV. Mol Ther. 2020;28:1753-1755.
High-dose AAV gene therapy deaths. Nat Biotechnol. 2020;38:910.
Bonnemann CG. Designer AAV muscle up. Cell. 2021;184:4845-4847.
Weinmann J, Weis S, Sippel J, et al. Identification of a myotropic AAV by massively parallel in vivo evaluation of barcoded capsid variants. Nat Commun. 2020;11:5432.
Tabebordbar M, Lagerborg KA, Stanton A, et al. Directed evolution of a family of AAV capsid variants enabling potent muscle-directed gene delivery across species. Cell. 2021;184:4919-4938 e4922.
Kishimoto TK, Samulski RJ. Addressing high dose AAV toxicity - 'one and done' or 'slower and lower'? Expert Opin Biol Ther. 2022;22:1067-1071.
Levy JM, Yeh WH, Pendse N, et al. Cytosine and adenine base editing of the brain, liver, retina, heart and skeletal muscle of mice via adeno-associated viruses. Nat Biomed Eng. 2020;4:97-110.
Wilson JM, Flotte TR. Moving forward after two deaths in a gene therapy trial of myotubular myopathy. Hum Gene Ther. 2020;31:695-696.