Soluble Factors Associated with Denervation-induced Skeletal Muscle
Atrophy

Marianny   Portal   Rodríguez; Claudio      Cabello-Verrugio
Abstract

Skeletal muscle tissue has the critical function of mechanical support protecting the body. In addition, its functions are strongly influenced by the balanced synthesis and degradation processes of structural and regulatory proteins. The inhibition of protein synthesis and/or the activation of catabolism generally determines a pathological state or condition called muscle atrophy, a reduction in muscle mass that results in partial or total loss of function. It has been established that many pathophysiological conditions can cause a decrease in muscle mass. Skeletal muscle innervation involves stable and functional neural interactions with muscles via neuromuscular junctions and is essential for maintaining normal muscle structure and function. Loss of motor innervation induces rapid skeletal muscle fiber degeneration with activation of atrophy-related signaling and subsequent disassembly of sarcomeres, altering normal muscle function. After denervation, an inflammation stage is characterized by the increased expression of pro-inflammatory cytokines that determine muscle atrophy. In this review, we highlighted the impact of some soluble factors on the development of muscle atrophy by denervation.
Graphical Abstract

[1]
Yin, L.; Li, N.; Jia, W.; Wang, N.; Liang, M.; Yang, X.; Du, G. Skeletal muscle atrophy: From mechanisms to treatments. Pharmacol. Res.,  2021, 172, 105807.
 [http://dx.doi.org/10.1016/j.phrs.2021.105807] [PMID: 34389456]

[2]
Chemello, F.; Bean, C.; Cancellara, P.; Laveder, P.; Reggiani, C.; Lanfranchi, G. Microgenomic analysis in skeletal muscle: Expression signatures of individual fast and slow myofibers. PLoS One,  2011, 6(2), e16807.
 [http://dx.doi.org/10.1371/journal.pone.0016807] [PMID: 21364935]

[3]
Marzuca-Nassr, G.N. , 2019. 

[4]
Sharlo, K.; Tyganov, S.A.; Tomilovskaya, E.; Popov, D.V.; Saveko, A.A.; Shenkman, B.S. Effects of various muscle disuse states and countermeasures on muscle molecular signaling. Int. J. Mol. Sci.,  2021, 23(1), 468.
 [http://dx.doi.org/10.3390/ijms23010468] [PMID: 35008893]

[5]
Ramírez, Ramírez, C. Una visión desde la biología molecular a una deficiencia comúnmente encontrada en la práctica del fisioterapeuta: la atrofia muscular. Revista de la Universidad Industrial de Santander Salud.,  2012, 44(3), 31-39.

[6]
Iyer, S.R.; Shah, S.B.; Lovering, R.M. The neuromuscular junction: Roles in aging and neuromuscular disease. Int. J. Mol. Sci.,  2021, 22(15), 8058.
 [http://dx.doi.org/10.3390/ijms22158058] [PMID: 34360831]

[7]
Kostrominova, T.Y. Skeletal Muscle Denervation: Past, Present and Future; MDPI, 2022, p. 7489.

[8]
Burns, T.M.; Graham, C.D.; Rose, M.R.; Simmons, Z. Quality of life and measures of quality of life in patients with neuromuscular disorders. Muscle Nerve,  2012, 46(1), 9-25.
 [http://dx.doi.org/10.1002/mus.23245] [PMID: 22644588]

[9]
Ware, F., Jr; Bennett, A.L.; McIntyre, A.R. Membrane resting potential of denervated mammalian skeletal muscle measured in vivo. Am. J. Physiol.,  1954, 177(1), 115-118.
 [http://dx.doi.org/10.1152/ajplegacy.1954.177.1.115] [PMID: 13148353]

[10]
Ehmsen, J.T.; Höke, A. Cellular and molecular features of neurogenic skeletal muscle atrophy. Exp. Neurol.,  2020, 331, 113379.
 [http://dx.doi.org/10.1016/j.expneurol.2020.113379] [PMID: 32533969]

[11]
Shen, Y.; Zhang, R.; Xu, L.; Wan, Q.; Zhu, J.; Gu, J.; Huang, Z.; Ma, W.; Shen, M.; Ding, F.; Sun, H. Microarray analysis of gene expression provides new insights into denervation-induced skeletal muscle atrophy. Front. Physiol.,  2019, 10, 1298.
 [http://dx.doi.org/10.3389/fphys.2019.01298] [PMID: 31681010]

[12]
Tomasi, M.L.; Ramani, K.; Ryoo, M.; Cossu, C.; Floris, A.; Murray, B.J.; Iglesias-Ara, A.; Spissu, Y.; Mavila, N. SUMOylation regulates cytochrome P450 2E1 expression and activity in alcoholic liver disease. FASEB J.,  2018, 32(6), 3278-3288.
 [http://dx.doi.org/10.1096/fj.201701124R] [PMID: 29401608]

[13]
Costamagna, D; Costelli, P; Sampaolesi, M; Penna, F, 2015, Role of inflammation in muscle homeostasis and myogenesis. Mediators Inflamm.,  2015, 2015-805172.
 [http://dx.doi.org/10.1155/2015/805172]

[14]
Wu, C.; Tang, L.; Ni, X.; Xu, T.; Fang, Q.; Xu, L.; Ma, W.; Yang, X.; Sun, H. Salidroside attenuates denervation-induced skeletal muscle atrophy through negative regulation of pro-inflammatory cytokine. Front. Physiol.,  2019, 10, 665.
 [http://dx.doi.org/10.3389/fphys.2019.00665] [PMID: 31293430]

[15]
Yamauchi, Y.; Ferdousi, F.; Fukumitsu, S.; Isoda, H. Maslinic acid attenuates denervation-induced loss of skeletal muscle mass and strength. Nutrients,  2021, 13(9), 2950.
 [http://dx.doi.org/10.3390/nu13092950] [PMID: 34578826]

[16]
Chen, X.; Li, M.; Chen, B.; Wang, W.; Zhang, L.; Ji, Y.; Chen, Z.; Ni, X.; Shen, Y.; Sun, H. Transcriptome sequencing and analysis reveals the molecular mechanism of skeletal muscle atrophy induced by denervation. Ann. Transl. Med.,  2021, 9(8), 697.
 [http://dx.doi.org/10.21037/atm-21-1230] [PMID: 33987395]

[17]
Bodine, S.C.; Latres, E.; Baumhueter, S.; Lai, V.K.M.; Nunez, L.; Clarke, B.A.; Poueymirou, W.T.; Panaro, F.J.; Na, E.; Dharmarajan, K.; Pan, Z.Q.; Valenzuela, D.M.; DeChiara, T.M.; Stitt, T.N.; Yancopoulos, G.D.; Glass, D.J. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science,  2001, 294(5547), 1704-1708.
 [http://dx.doi.org/10.1126/science.1065874] [PMID: 11679633]

[18]
Boutari, C.; Mantzoros, C.S. Decreasing lean body mass with age: Challenges and opportunities for novel therapies. Endocrinol. Metab. (Seoul),  2017, 32(4), 422-425.
 [http://dx.doi.org/10.3803/EnM.2017.32.4.422] [PMID: 29271616]

[19]
Raso, V.; Greve, JMDA.; Polito, MD. Pollock: Fisiologia clínica do exercício (2013) 2017. Available From: https://repositorio.usp.br/item/002683087

[20]
Draznin, B. Molecular mechanisms of insulin resistance. Insulin resistance. Springer,  2020, 55-66.

[21]
Cai, D.; Frantz, J.D.; Tawa, N.E., Jr; Melendez, P.A.; Oh, B.C.; Lidov, H.G.W.; Hasselgren, P.O.; Frontera, W.R.; Lee, J.; Glass, D.J.; Shoelson, S.E. IKKbeta/NF-kappaB activation causes severe muscle wasting in mice. Cell,  2004, 119(2), 285-298.
 [http://dx.doi.org/10.1016/j.cell.2004.09.027] [PMID: 15479644]

[22]
Cadena, S.M.; Zhang, Y.; Fang, J.; Brachat, S.; Kuss, P.; Giorgetti, E.; Stodieck, L.S.; Kneissel, M.; Glass, D.J. Skeletal muscle in MuRF1 null mice is not spared in low-gravity conditions, indicating atrophy proceeds by unique mechanisms in space. Sci. Rep.,  2019, 9(1), 9397.
 [http://dx.doi.org/10.1038/s41598-019-45821-9] [PMID: 31253821]

[23]
Paul, P.K.; Bhatnagar, S.; Mishra, V.; Srivastava, S.; Darnay, B.G.; Choi, Y.; Kumar, A. The E3 ubiquitin ligase TRAF6 intercedes in starvation-induced skeletal muscle atrophy through multiple mechanisms. Mol. Cell. Biol.,  2012, 32(7), 1248-1259.
 [http://dx.doi.org/10.1128/MCB.06351-11] [PMID: 22290431]

[24]
Beehler, B.C.; Sleph, P.G.; Benmassaoud, L.; Grover, G.J. Reduction of skeletal muscle atrophy by a proteasome inhibitor in a rat model of denervation. Exp. Biol. Med. (Maywood),  2006, 231(3), 335-341.
 [http://dx.doi.org/10.1177/153537020623100315] [PMID: 16514182]

[25]
Kimura, N.; Kumamoto, T.; Oniki, T.; Nomura, M.; Nakamura, K.; Abe, Y.; Hazama, Y.; Ueyama, H. Role of ubiquitin-proteasome proteolysis in muscle fiber destruction in experimental chloroquine-induced myopathy. Muscle Nerve,  2009, 39(4), 521-528.
 [http://dx.doi.org/10.1002/mus.21223] [PMID: 19296457]

[26]
McGrath, M.J.; Eramo, M.J.; Gurung, R.; Sriratana, A.; Gehrig, S.M.; Lynch, G.S.; Lourdes, S.R.; Koentgen, F.; Feeney, S.J.; Lazarou, M.; McLean, C.A.; Mitchell, C.A. Defective lysosome reformation during autophagy causes skeletal muscle disease. J. Clin. Invest.,  2021, 131(1), e135124.
 [http://dx.doi.org/10.1172/JCI135124] [PMID: 33119550]

[27]
Masiero, E.; Agatea, L.; Mammucari, C.; Blaauw, B.; Loro, E.; Komatsu, M.; Metzger, D.; Reggiani, C.; Schiaffino, S.; Sandri, M. Autophagy is required to maintain muscle mass. Cell Metab.,  2009, 10(6), 507-515.
 [http://dx.doi.org/10.1016/j.cmet.2009.10.008] [PMID: 19945408]

[28]
Zhao, J.; Brault, J.J.; Schild, A.; Cao, P.; Sandri, M.; Schiaffino, S.; Lecker, S.H.; Goldberg, A.L. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab.,  2007, 6(6), 472-483.
 [http://dx.doi.org/10.1016/j.cmet.2007.11.004] [PMID: 18054316]

[29]
Mammucari, C.; Milan, G.; Romanello, V.; Masiero, E.; Rudolf, R.; Del Piccolo, P.; Burden, S.J.; Di Lisi, R.; Sandri, C.; Zhao, J.; Goldberg, A.L.; Schiaffino, S.; Sandri, M. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab.,  2007, 6(6), 458-471.
 [http://dx.doi.org/10.1016/j.cmet.2007.11.001] [PMID: 18054315]

[30]
Ganassi, M.; Zammit, P.S. Involvement of muscle satellite cell dysfunction in neuromuscular disorders: Expanding the portfolio of satellite cell-opathies. Eur. J. Transl. Myol.,  2022, 32(1), 10064.
 [http://dx.doi.org/10.4081/ejtm.2022.10064] [PMID: 35302338]

[31]
Seddon, H.J. A Classification of Nerve Injuries. BMJ,  1942, 2(4260), 237-239.
 [http://dx.doi.org/10.1136/bmj.2.4260.237] [PMID: 20784403]

[32]
Aydin, M.A.; Mackinnon, S.E.; Gu, X.M.; Kobayashi, J.; Kuzon, W.M., Jr. Force deficits in skeletal muscle after delayed reinnervation. Plast. Reconstr. Surg.,  2004, 113(6), 1712-1718.
 [http://dx.doi.org/10.1097/01.PRS.0000118049.93654.CA] [PMID: 15114133]

[33]
Wong, A.; Pomerantz, J.H. The role of muscle stem cells in regeneration and recovery after denervation: A review. Plast. Reconstr. Surg.,  2019, 143(3), 779-788.
 [http://dx.doi.org/10.1097/PRS.0000000000005370] [PMID: 30817650]

[34]
Carraro, U.; Boncompagni, S.; Gobbo, V.; Rossini, K.; Zampieri, S.; Mosole, S.; Ravara, B.; Nori, A.; Stramare, R.; Ambrosio, F.; Piccione, F.; Masiero, S.; Vindigni, V.; Gargiulo, P.; Protasi, F.; Kern, H.; Pond, A.; Marcante, A. Persistent muscle fiber regeneration in long term denervation. Past, present, future. Eur. J. Transl. Myol.,  2015, 25(2), 77.
 [http://dx.doi.org/10.4081/bam.2015.2.77] [PMID: 26913148]

[35]
Faroni, A.; Mobasseri, S.A.; Kingham, P.J.; Reid, A.J. Peripheral nerve regeneration: Experimental strategies and future perspectives. Adv. Drug Deliv. Rev.,  2015, 82-83, 160-167.
 [http://dx.doi.org/10.1016/j.addr.2014.11.010] [PMID: 25446133]

[36]
Huang, X.; Jiang, J.; Xu, J. Denervation-related neuromuscular junction changes: From degeneration to regeneration. Front. Mol. Neurosci.,  2022, 14, 810919.
 [http://dx.doi.org/10.3389/fnmol.2021.810919] [PMID: 35282655]

[37]
Lu, D.X.; Huang, S.K.; Carlson, B.M. Electron microscopic study of long-term denervated rat skeletal muscle. Anat. Rec.,  1997, 248(3), 355-365.
 [http://dx.doi.org/10.1002/(SICI)1097-0185(199707)248:3<355::AID-AR8>3.0.CO;2-O] [PMID: 9214553]

[38]
Chang, H.; Hwang, S.; Lim, S.; Eo, S.; Minn, K.W.; Hong, K.Y. Long-term fate of denervated skeletal muscle after microvascular flap transfer. Ann. Plast. Surg.,  2018, 80(6), 644-647.
 [http://dx.doi.org/10.1097/SAP.0000000000001397] [PMID: 29553977]

[39]
Rebolledo, DL; González, D; Faundez-Contreras, J; Contreras, O; Vio, CP; Murphy-Ullrich, JE Denervation-induced skeletal muscle fibrosis is mediated by CTGF/CCN2 independently of TGF-β. Matrix Biol.,  2019, 82, 20-37.

[40]
Lieber, R.L.; Ward, S.R. Cellular Mechanisms of Tissue Fibrosis. 4. Structural and functional consequences of skeletal muscle fibrosis. Am. J. Physiol. Cell Physiol.,  2013, 305(3), C241-C252.
 [http://dx.doi.org/10.1152/ajpcell.00173.2013] [PMID: 23761627]

[41]
Das, D.K.; Graham, Z.A.; Cardozo, C.P. Myokines in skeletal muscle physiology and metabolism: Recent advances and future perspectives. Acta Physiol. (Oxf.),  2020, 228(2), e13367.
 [http://dx.doi.org/10.1111/apha.13367] [PMID: 31442362]

[42]
Sharma, M.; McFarlane, C.; Kambadur, R.; Kukreti, H.; Bonala, S.; Srinivasan, S. Myostatin: Expanding horizons. IUBMB Life,  2015, 67(8), 589-600.
 [http://dx.doi.org/10.1002/iub.1392] [PMID: 26305594]

[43]
Lee, S.J.; McPherron, A.C. Regulation of myostatin activity and muscle growth. Proc. Natl. Acad. Sci. USA,  2001, 98(16), 9306-9311.
 [http://dx.doi.org/10.1073/pnas.151270098] [PMID: 11459935]

[44]
Han, H.Q.; Zhou, X.; Mitch, W.E.; Goldberg, A.L. Myostatin/activin pathway antagonism: Molecular basis and therapeutic potential. Int. J. Biochem. Cell Biol.,  2013, 45(10), 2333-2347.
 [http://dx.doi.org/10.1016/j.biocel.2013.05.019] [PMID: 23721881]

[45]
Sartori, R.; Milan, G.; Patron, M.; Mammucari, C.; Blaauw, B.; Abraham, R.; Sandri, M. Smad2 and 3 transcription factors control muscle mass in adulthood. Am. J. Physiol. Cell Physiol.,  2009, 296(6), C1248-C1257.
 [http://dx.doi.org/10.1152/ajpcell.00104.2009] [PMID: 19357234]

[46]
Lee, S.J.; Reed, L.A.; Davies, M.V.; Girgenrath, S.; Goad, M.E.P.; Tomkinson, K.N.; Wright, J.F.; Barker, C.; Ehrmantraut, G.; Holmstrom, J.; Trowell, B.; Gertz, B.; Jiang, M.S.; Sebald, S.M.; Matzuk, M.; Li, E.; Liang, L.; Quattlebaum, E.; Stotish, R.L.; Wolfman, N.M. Regulation of muscle growth by multiple ligands signaling through activin type II receptors. Proc. Natl. Acad. Sci. USA,  2005, 102(50), 18117-18122.
 [http://dx.doi.org/10.1073/pnas.0505996102] [PMID: 16330774]

[47]
De la Torre Álamo, M.M. El papel de los microRNAs en la regeneración muscular. 2021. Available From: https://crea.ujaen.es/handle/10953.1/14539

[48]
Mikolajczyk, T.P.; Szczepaniak, P.; Vidler, F.; Maffia, P.; Graham, G.J.; Guzik, T.J. Role of inflammatory chemokines in hypertension. Pharmacol. Ther.,  2021, 223, 107799.
 [http://dx.doi.org/10.1016/j.pharmthera.2020.107799] [PMID: 33359600]

[49]
Wagner, K.R.; McPherron, A.C.; Winik, N.; Lee, S.J. Loss of myostatin attenuates severity of muscular dystrophy inmdx mice. Ann. Neurol.,  2002, 52(6), 832-836.
 [http://dx.doi.org/10.1002/ana.10385] [PMID: 12447939]

[50]
Crone, M.; Mah, J.K. Current and emerging therapies for duchenne muscular dystrophy. Curr. Treat. Options Neurol.,  2018, 20(8), 31.
 [http://dx.doi.org/10.1007/s11940-018-0513-6] [PMID: 29936551]

[51]
Cannon, J.G.; Fielding, R.A.; Fiatarone, M.A.; Orencole, S.F.; Dinarello, C.A.; Evans, W.J. Increased interleukin 1 beta in human skeletal muscle after exercise. Am. J. Physiol.,  1989, 257(2 Pt 2), R451-R455.
 [PMID: 2669532]

[52]
Aneas, I.; Decker, D.C.; Howard, C.L.; Sobreira, D.R. Asthma-associated genetic variants induce IL33 differential expression through an enhancer-blocking regulatory region. Nat. Commun.,  2021, 12(1), 6115.
 [http://dx.doi.org/10.1038/s41467-021-26347-z]

[53]
You, Z.; Huang, X.; Xiang, Y.; Dai, J.; Xu, L.; Jiang, J.; Xu, J. Ablation of NLRP3 inflammasome attenuates muscle atrophy via inhibiting pyroptosis, proteolysis and apoptosis following denervation. Theranostics,  2023, 13(1), 374-390.
 [http://dx.doi.org/10.7150/thno.74831] [PMID: 36593964]

[54]
Yi, X.; Tao, J.; Qian, Y.; Feng, F.; Hu, X.; Xu, T.; Jin, H.; Ruan, H.; Zheng, H.F.; Tong, P. Morroniside ameliorates inflammatory skeletal muscle atrophy via inhibiting canonical and non-canonical NF-κB and regulating protein synthesis/degradation. Front. Pharmacol.,  2022, 13, 1056460.
 [http://dx.doi.org/10.3389/fphar.2022.1056460] [PMID: 36618945]

[55]
Cayrol, C.; Girard, J.P. Interleukin-33 (IL-33): A critical review of its biology and the mechanisms involved in its release as a potent extracellular cytokine. Cytokine,  2022, 156, 155891.
 [http://dx.doi.org/10.1016/j.cyto.2022.155891] [PMID: 35640416]

[56]
Chaweewannakorn, C.; Tsuchiya, M. Roles of IL-1α/β in regeneration of cardiotoxin-injured muscle and satellite cell function. Am. J. Physiol. Regul. Integr. Comp. Physiol.,  2018, 315(1), R90-R103.

[57]
Cohen, T.V.; Many, G.M.; Fleming, B.D.; Gnocchi, V.F.; Ghimbovschi, S.; Mosser, D.M.; Hoffman, E.P.; Partridge, T.A. Upregulated IL-1β in dysferlin-deficient muscle attenuates regeneration by blunting the response to pro-inflammatory macrophages. Skelet. Muscle,  2015, 5(1), 24.
 [http://dx.doi.org/10.1186/s13395-015-0048-4] [PMID: 26251696]

[58]
Pedersen, B.; Febbraio, M. Músculos, ejercicio y obesidad: Músculo esquelético como órgano secretor. Nat. Rev. Endocrinol.,  2012, 8, 457-465.
 [http://dx.doi.org/10.1038/nrendo.2012.49] [PMID: 22473333]

[59]
Garneau, L.; Aguer, C. Role of myokines in the development of skeletal muscle insulin resistance and related metabolic defects in type 2 diabetes. Diabetes Metab.,  2019, 45(6), 505-516.
 [http://dx.doi.org/10.1016/j.diabet.2019.02.006] [PMID: 30844447]

[60]
Fischer, C.P. Interleukin-6 in acute exercise and training: What is the biological relevance? Exerc. Immunol. Rev.,  2006, 12, 6-33.
 [PMID: 17201070]

[61]
Pedersen, B.K.; Febbraio, M.A. Muscle as an endocrine organ: Focus on muscle-derived interleukin-6. Physiol. Rev.,  2008, 88(4), 1379-1406.
 [http://dx.doi.org/10.1152/physrev.90100.2007] [PMID: 18923185]

[62]
Forcina, L; Miano, C; Scicchitano, BM; Musarò, A Signals from the Niche: Insights into the Role of IGF-1 and IL-6 in Modulating Skeletal Muscle Fibrosis. Cells.,  2019, 8(3), 232.

[63]
Muñoz-Cánoves, P.; Scheele, C.; Pedersen, B.K.; Serrano, A.L. Interleukin-6 myokine signaling in skeletal muscle: A double-edged sword? FEBS J.,  2013, 280(17), 4131-4148.
 [http://dx.doi.org/10.1111/febs.12338] [PMID: 23663276]

[64]
Grothe, C.; Heese, K.; Meisinger, C.; Wewetzer, K.; Kunz, D.; Cattini, P.; Otten, U. Expression of interleukin-6 and its receptor in the sciatic nerve and cultured Schwann cells: Relation to 18-kD fibroblast growth factor-2. Brain Res.,  2000, 885(2), 172-181.
 [http://dx.doi.org/10.1016/S0006-8993(00)02911-5] [PMID: 11102571]

[65]
Bolin, L.M.; Verity, A.N.; Silver, J.E.; Shooter, E.M.; Abrams, J.S. Interleukin-6 production by Schwann cells and induction in sciatic nerve injury. J. Neurochem.,  1995, 64(2), 850-858.
 [http://dx.doi.org/10.1046/j.1471-4159.1995.64020850.x] [PMID: 7830079]

[66]
Hoene, M.; Runge, H.; Häring, H.U.; Schleicher, E.D.; Weigert, C. Interleukin-6 promotes myogenic differentiation of mouse skeletal muscle cells: Role of the STAT3 pathway. Am. J. Physiol. Cell Physiol.,  2013, 304(2), C128-C136.
 [http://dx.doi.org/10.1152/ajpcell.00025.2012] [PMID: 23114963]

[67]
Baeza-Raja, B.; Muñoz-Cánoves, P. p38 MAPK-induced nuclear factor-kappaB activity is required for skeletal muscle differentiation: Role of interleukin-6. Mol. Biol. Cell,  2004, 15(4), 2013-2026.
 [http://dx.doi.org/10.1091/mbc.e03-08-0585] [PMID: 14767066]

[68]
Pelosi, M.; De Rossi, M.; Barberi, L.; Musarò, A. IL-6 impairs myogenic differentiation by downmodulation of p90RSK/eEF2 and mTOR/p70S6K axes, without affecting AKT activity. BioMed. Res. Int.,  2014, 2014, 1-12.
 [http://dx.doi.org/10.1155/2014/206026] [PMID: 24967341]

[69]
Llovera, M.; García-Martínez, C.; López-Soriano, J.; Agell, N.; López-Soriano, F.J.; Garcia, I.; Argilés, J.M. Protein turnover in skeletal muscle of tumour-bearing transgenic mice overexpressing the soluble TNF receptor-1. Cancer Lett.,  1998, 130(1-2), 19-27.
 [http://dx.doi.org/10.1016/S0304-3835(98)00137-2] [PMID: 9751252]

[70]
Xiang, Y.; Dai, J.; Xu, L.; Li, X.; Jiang, J.; Xu, J. Research progress in immune microenvironment regulation of muscle atrophy induced by peripheral nerve injury. Life Sci.,  2021, 287, 120117.
 [http://dx.doi.org/10.1016/j.lfs.2021.120117] [PMID: 34740577]

[71]
Komiya, Y; Kobayashi, C; Uchida, N; Otsu, S; Tanio, T; Yokoyama, I Effect of dietary fish oil intake on ubiquitin ligase expression during muscle atrophy induced by sciatic nerve denervation in mice. Animal Sci. J,  2019, 90(8), 1018-1025.
 [http://dx.doi.org/10.1111/asj.13224]

[72]
Ma, W.; Zhang, R.; Huang, Z.; Zhang, Q.; Xie, X.; Yang, X.; Zhang, Q.; Liu, H.; Ding, F.; Zhu, J.; Sun, H. PQQ ameliorates skeletal muscle atrophy, mitophagy and fiber type transition induced by denervation via inhibition of the inflammatory signaling pathways. Ann. Transl. Med.,  2019, 7(18), 440.
 [http://dx.doi.org/10.21037/atm.2019.08.101] [PMID: 31700876]

[73]
Langen, R.C.J.; Schols, A.M.W.J.; Kelders, M.C.J.M.; van der Velden, J.L.J.; Wouters, E.F.M.; Janssen-Heininger, Y.M.W. Tumor necrosis factor-α inhibits myogenesis through redox-dependent and -independent pathways. Am. J. Physiol. Cell Physiol.,  2002, 283(3), C714-C721.
 [http://dx.doi.org/10.1152/ajpcell.00418.2001] [PMID: 12176728]

[74]
Warren, G.L.; Hulderman, T.; Jensen, N.; McKinstry, M.; Mishra, M.; Luster, M.I.; Simeonova, P.P. Physiological role of tumor necrosis factor α in traumatic muscle injury. FASEB J.,  2002, 16(12), 1630-1632.
 [http://dx.doi.org/10.1096/fj.02-0187fje] [PMID: 12207010]

[75]
Chen, S.E.; Jin, B.; Li, Y.P. TNF-α regulates myogenesis and muscle regeneration by activating p38 MAPK. Am. J. Physiol. Cell Physiol.,  2007, 292(5), C1660-C1671.
 [http://dx.doi.org/10.1152/ajpcell.00486.2006] [PMID: 17151142]

[76]
Yeh, F.C.; Kao, C.F.; Kuo, P.H. Explore the features of brain-derived neurotrophic factor in mood disorders. PLoS One,  2015, 10(6), e0128605.
 [http://dx.doi.org/10.1371/journal.pone.0128605] [PMID: 26091093]

[77]
Clow, C.; Jasmin, B.J. Skeletal muscle-derived BDNF regulates satellite cell differentiation and muscle regeneration. Mol. Biol. Cell, 2010.
 [http://dx.doi.org/10.1091/mbc.e10-02-0154]

[78]
Chevrel, G.; Hohlfeld, R.; Sendtner, M. The role of neurotrophins in muscle under physiological and pathological conditions. Muscle Nerve,  2006, 33(4), 462-476.
 [http://dx.doi.org/10.1002/mus.20444] [PMID: 16228973]

[79]
Mousavi, K.; Parry, D.J.; Jasmin, B.J. BDNF rescues myosin heavy chain IIB muscle fibers after neonatal nerve injury. Am. J. Physiol. Cell Physiol.,  2004, 287(1), C22-C29.
 [http://dx.doi.org/10.1152/ajpcell.00583.2003] [PMID: 14973145]

[80]
Matthews, V.B.; Åström, M.B.; Chan, M.H.S.; Bruce, C.R.; Krabbe, K.S.; Prelovsek, O.; Åkerström, T.; Yfanti, C.; Broholm, C.; Mortensen, O.H.; Penkowa, M.; Hojman, P.; Zankari, A.; Watt, M.J.; Bruunsgaard, H.; Pedersen, B.K.; Febbraio, M.A. Brain-derived neurotrophic factor is produced by skeletal muscle cells in response to contraction and enhances fat oxidation via activation of AMP-activated protein kinase. Diabetologia,  2009, 52(7), 1409-1418.
 [http://dx.doi.org/10.1007/s00125-009-1364-1] [PMID: 19387610]

[81]
Aby, K.; Antony, R.; Eichholz, M.; Srinivasan, R.; Li, Y. Enhanced pro-BDNF-p75NTR pathway activity in denervated skeletal muscle. Life Sci.,  2021, 286, 120067.
 [http://dx.doi.org/10.1016/j.lfs.2021.120067] [PMID: 34678261]

[82]
Clow, C.; Jasmin, B.J. Brain-derived neurotrophic factor regulates satellite cell differentiation and skeltal muscle regeneration. Mol. Biol. Cell,  2010, 21(13), 2182-2190.
 [http://dx.doi.org/10.1091/mbc.e10-02-0154] [PMID: 20427568]

[83]
Akahori, H.; Karmali, V.; Polavarapu, R.; Lyle, A.N.; Weiss, D.; Shin, E.; Husain, A.; Naqvi, N.; Van Dam, R.; Habib, A.; Choi, C.U.; King, A.L.; Pachura, K.; Taylor, W.R.; Lefer, D.J.; Finn, A.V. CD163 interacts with TWEAK to regulate tissue regeneration after ischaemic injury. Nat. Commun.,  2015, 6(1), 7792.
 [http://dx.doi.org/10.1038/ncomms8792] [PMID: 26242746]

[84]
Madrigal-Matute, J.; Fernandez-Laso, V.; Sastre, C.; Llamas-Granda, P.; Egido, J.; Martin-Ventura, J.L.; Zalba, G.; Blanco-Colio, L.M. TWEAK/Fn14 interaction promotes oxidative stress through NADPH oxidase activation in macrophages. Cardiovasc. Res.,  2015, 108(1), 139-147.
 [http://dx.doi.org/10.1093/cvr/cvv204] [PMID: 26224570]

[85]
Enwere, E.K.; Holbrook, J.; Lejmi-Mrad, R.; Vineham, J.; Timusk, K.; Sivaraj, B.; Isaac, M.; Uehling, D.; Al-awar, R.; LaCasse, E.; Korneluk, R.G. TWEAK and cIAP1 regulate myoblast fusion through the noncanonical NF-κB signaling pathway. Sci. Signal.,  2012, 5(246), ra75.
 [http://dx.doi.org/10.1126/scisignal.2003086] [PMID: 23074266]

[86]
Bowerman, M.; Salsac, C.; Coque, E.; Eiselt, E.; Deschaumes, R.G.; Brodovitch, A.; Burkly, L.C.; Scamps, F.; Raoul, C. Tweak regulates astrogliosis, microgliosis and skeletal muscle atrophy in a mouse model of amyotrophic lateral sclerosis. Hum. Mol. Genet.,  2015, 24(12), 3440-3456.
 [http://dx.doi.org/10.1093/hmg/ddv094] [PMID: 25765661]

[87]
Paul, P.K.; Gupta, S.K.; Bhatnagar, S.; Panguluri, S.K.; Darnay, B.G.; Choi, Y.; Kumar, A. Targeted ablation of TRAF6 inhibits skeletal muscle wasting in mice. J. Cell Biol.,  2010, 191(7), 1395-1411.
 [http://dx.doi.org/10.1083/jcb.201006098] [PMID: 21187332]

[88]
Morikawa, M.; Derynck, R.; Miyazono, K. TGF-β and the TGF-β family: Context-dependent roles in cell and tissue physiology. Cold Spring Harb. Perspect. Biol.,  2016, 8(5), a021873.
 [http://dx.doi.org/10.1101/cshperspect.a021873] [PMID: 27141051]

[89]
Lee, J.H.; Jun, H.S. Role of myokines in regulating skeletal muscle mass and function. Front. Physiol.,  2019, 10, 42.
 [http://dx.doi.org/10.3389/fphys.2019.00042] [PMID: 30761018]

[90]
Peng, D.; Fu, M.; Wang, M.; Wei, Y.; Wei, X. Targeting TGF-β signal transduction for fibrosis and cancer therapy. Mol. Cancer,  2022, 21(1), 104.
 [http://dx.doi.org/10.1186/s12943-022-01569-x] [PMID: 35461253]

[91]
Contreras, O.; Rebolledo, D.L.; Oyarzún, J.E.; Olguín, H.C.; Brandan, E. Connective tissue cells expressing fibro/adipogenic progenitor markers increase under chronic damage: Relevance in fibroblast-myofibroblast differentiation and skeletal muscle fibrosis. Cell Tissue Res.,  2016, 364(3), 647-660.
 [http://dx.doi.org/10.1007/s00441-015-2343-0] [PMID: 26742767]

[92]
Ugarte, G.; Brandan, E. Transforming growth factor beta (TGF-beta) signaling is regulated by electrical activity in skeletal muscle cells. TGF-beta type I receptor is transcriptionally regulated by myotube excitability. J. Biol. Chem.,  2006, 281(27), 18473-18481.
 [http://dx.doi.org/10.1074/jbc.M600918200] [PMID: 16682418]

[93]
Huang, Q.K.; Qiao, H.Y.; Fu, M.H.; Li, G.; Li, W.B.; Chen, Z.; Wei, J.; Liang, B.S. MiR-206 attenuates denervation-induced skeletal muscle atrophy in rats through regulation of satellite cell differentiation via TGF-β1, Smad3, and HDAC4 signaling. Med. Sci. Monit.,  2016, 22, 1161-1170.
 [http://dx.doi.org/10.12659/MSM.897909] [PMID: 27054781]
Cite As
Current Protein & Peptide Science

Soluble Factors Associated with Denervation-induced Skeletal Muscle Atrophy

Abstract

Graphical Abstract
