Endurance Training Attenuates Catabolic Signals Induced by TNF-alpha in Muscle of Mice.

Animals; Cytokines/metabolism; Female; Mice, Inbred C57BL; Microfilament Proteins/metabolism; Muscle, Skeletal/drug effects/metabolism; Physical Conditioning, Animal; Physical Endurance/physiology; RNA, Messenger/metabolism; Signal Transduction; TOR Serine-Threonine Kinases/metabolism; Tumor Necrosis Factor-alpha/administration & dosage

Abstract :

[en] PURPOSE: To determine whether endurance training attenuates the negative effects induced by an acute injection of tumor necrosis factor-alpha (TNF-alpha) in skeletal muscle of mice. METHODS: Trained (6 wk of endurance training at 60% of maximal velocity) and untrained mice were injected with TNF-alpha or vehicle and killed 6 h after. Tibialis anterior muscles were analyzed using Western blot and qRT-PCR for markers of inflammation and protein synthesis/degradation. RESULTS: Independently of training, TNF-alpha increased the mRNA of cytokines and downregulated signals linked to protein synthesis. The phosphorylation of IKKalpha/beta and IkappaBalpha induced by TNF-alpha was blunted in trained mice, suggesting altered NF-kappaB activation. This was associated with lower induction of several markers of protein degradation (FoxO1, MURF1, MAFbx, myostatin, Gabarapl1, and LC3BII/LC3BI ratio). CONCLUSIONS: Endurance training protects skeletal muscle against the activation of protein degradation signaling pathways induced by TNF-alpha.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Rodriguez, Julie

Fernandez-Verdejo, Rodrigo

Pierre, Nicolas ; Université de Liège - ULiège > Département des sciences cliniques > Hépato-gastroentérologie

Priem, Fabian

Francaux, Marc

Language :

English

Title :

Endurance Training Attenuates Catabolic Signals Induced by TNF-alpha in Muscle of Mice.

Publication date :

2016

Journal title :

Medicine and Science in Sports and Exercise

ISSN :

0195-9131

eISSN :

1530-0315

Publisher :

Lippincott Williams & Wilkins, United States - Maryland

Volume :

Issue :

Pages :

227-34

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 18 June 2019

Statistics

Number of views

50 (0 by ULiège)

Number of downloads

2 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Adams V, Mangner N, Gasch A, Induction of MuRF1 is essential for TNF-alpha-induced loss of muscle function in mice. J Mol Biol. 2008; 384 (1): 48-59
Ahmad S, Karlstad MD, Choudhry MA, Sayeed MM,. Sepsis-induced myofibrillar protein catabolism in rat skeletal muscle. Life Sci. 1994; 55 (18): 1383-91
Akerstrom TC, Krogh-Madsen R, Petersen AM, Pedersen BK,. Glucose ingestion during endurance training in men attenuates expression of myokine receptor. Exp Physiol. 2009; 94 (11): 1124-31
Argilés JM, López-Soriano FJ,. The role of cytokines in cancer cachexia. Med Res Rev. 1999; 19 (3): 223-48
Costelli P, Muscaritoli M, Bonetto A, Muscle myostatin signalling is enhanced in experimental cancer cachexia. Eur J Clin Invest. 2008; 38 (7): 531-8
De Alvaro C, Teruel T, Hernandez R, Lorenzo M,. Tumor necrosis factor alpha produces insulin resistance in skeletal muscle by activation of inhibitor kappaB kinase in a p38 MAPK-dependent manner. J Biol Chem. 2004; 279 (17): 17070-8
Deldicque L, Cani PD, Delzenne NM, Baar K, Francaux M,. Endurance training in mice increases the unfolded protein response induced by a high-fat diet. J Physiol Biochem. 2013; 69 (2): 215-25
Dempsey PW, Doyle SE, He JQ, Cheng G,. The signaling adaptors and pathways activated by TNF superfamily. Cytokine Growth Factor Rev. 2003; 14 (3-4): 193-209
Flores EA, Bistrian BR, Pomposelli JJ, Dinarello CA, Blackburn GL, Istfan NW,. Infusion of tumor necrosis factor/cachectin promotes muscle catabolism in the rat. A synergistic effect with interleukin 1. J Clin Invest. 1989; 83 (5): 1614-22
García-Martínez C, Agell N, Llovera M, López-Soriano FJ, Argilés JM,. Tumour necrosis factor-alpha increases the ubiquitinization of rat skeletal muscle proteins. FEBS Lett. 1993; 323 (3): 211-4
García-Martínez C, Llovera M, Agell N, López-Soriano FJ, Argilés JM,. Ubiquitin gene expression in skeletal muscle is increased by tumour necrosis factor-alpha. Biochem Biophys Res Commun. 1994; 201 (2): 682-6
García-Martínez C, López-Soriano FJ, Argilés JM,. Acute treatment with tumour necrosis factor-alpha induces changes in protein metabolism in rat skeletal muscle. Mol Cell Biochem. 1993; 125 (1): 11-8
Glass DJ,. Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol. 2005; 37 (10): 1974-84
Gleeson M, Bishop NC, Stensel DJ, Lindley MR, Mastana SS, Nimmo MA,. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol. 2011; 11 (9): 607-15
Gleeson M, McFarlin B, Flynn M,. Exercise and Toll-like receptors. Exerc Immunol Rev. 2006; 12: 34-53
Goodman MN,. Tumor necrosis factor induces skeletal muscle protein breakdown in rats. Am J Physiol. 1991; 260 (5 Pt 1): E727-30
Hanada T, Noda NN, Satomi Y, The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J Biol Chem. 2007; 282 (52): 37298-302
Keller C, Keller P, Giralt M, Hidalgo J, Pedersen BK,. Exercise normalises overexpression of TNF-alpha in knockout mice. Biochem Biophys Res Commun. 2004; 321 (1): 179-82
Lambert CP, Wright NR, Finck BN, Villareal DT,. Exercise but not diet-induced weight loss decreases skeletal muscle inflammatory gene expression in frail obese elderly persons. J Appl Physiol (1985). 2008; 105 (2): 473-8
Lancaster GI, Febbraio MA,. The immunomodulating role of exercise in metabolic disease. Trends Immunol. 2014; 35 (6): 262-9
Lang CH, Frost RA,. Sepsis-induced suppression of skeletal muscle translation initiation mediated by tumor necrosis factor alpha. Metabolism. 2007; 56 (1): 49-57
Lang CH, Frost RA, Nairn AC, MacLean DA, Vary TC,. TNF-alpha impairs heart and skeletal muscle protein synthesis by altering translation initiation. Am J Physiol Endocrinol Metab. 2002; 282 (2): E336-47
Li YP, Chen Y, John J, TNF-alpha acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin1/MAFbx in skeletal muscle. FASEB J. 2005; 19 (3): 362-70
Li YP, Schwartz RJ, Waddell ID, Holloway BR, Reid MB,. Skeletal muscle myocytes undergo protein loss and reactive oxygen-mediated NF-kappaB activation in response to tumor necrosis factor alpha. FASEB J. 1998; 12 (10): 871-80
Llovera M, García-Martínez C, Agell N, López-Soriano FJ, Argilés JM,. TNF can directly induce the expression of ubiquitin-dependent proteolytic system in rat soleus muscles. Biochem Biophys Res Commun. 1997; 230 (2): 238-41
Llovera M, García-Martínez C, López-Soriano J, Role of TNF receptor 1 in protein turnover during cancer cachexia using gene knockout mice. Mol Cell Endocrinol. 1998; 142 (1-2): 183-9
Naudé PJ, den Boer JA, Luiten PG, Eisel UL,. Tumor necrosis factor receptor cross-Talk. FEBS J. 2011; 278 (6): 888-98
Paul PK, Kumar A,. TRAF6 coordinates the activation of autophagy and ubiquitin-proteasome systems in atrophying skeletal muscle. Autophagy. 2011; 7 (5): 555-6
Pedersen BK,. The diseasome of physical inactivity-and the role of myokines in muscle-fat cross talk. J Physiol. 2009; 587 (Pt 23): 5559-68
Renard P, Raes M,. The proinflammatory transcription factor NFkappaB: a potential target for novel therapeutical strategies. Cell Biol Toxicol. 1999; 15 (6): 341-4
Rodriguez J, Vernus B, Chelh I, Myostatin and the skeletal muscle atrophy and hypertrophy signaling pathways. Cell Mol Life Sci. 2014; 71 (22): 4361-71
Sakurai T, Ogasawara J, Kizaki T, The effects of exercise training on obesity-induced dysregulated expression of adipokines in white adipose tissue. Int J Endocrinol. 2013; 2013: 801743
Sandri M, Sandri C, Gilbert A, Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell. 2004; 117 (3): 399-412
Schindler JF, Monahan JB, Smith WG,. p38 pathway kinases as anti-inflammatory drug targets. J Dent Res. 2007; 86 (9): 800-11
Sishi BJ, Engelbrecht AM,. Tumor necrosis factor alpha (TNF-α) inactivates the PI3-kinase/PKB pathway and induces atrophy and apoptosis in L6 myotubes. Cytokine. 2011; 54 (2): 173-84
Souza RW, Piedade WP, Soares LC, Aerobic exercise training prevents heart failure-induced skeletal muscle atrophy by anti-catabolic, but not anabolic actions. PLoS One. 2014; 9 (10): e110020
Starkie R, Ostrowski SR, Jauffred S, Febbraio M, Pedersen BK,. Exercise and IL-6 infusion inhibit endotoxin-induced TNF-alpha production in humans. FASEB J. 2003; 17 (8): 884-6
Steensberg A, Fischer CP, Keller C, Møller K, Pedersen BK,. IL-6 enhances plasma IL-1ra, IL-10, and cortisol in humans. Am J Physiol Endocrinol Metab. 2003; 285 (2): E433-7
Van Hall G,. Cytokines: muscle protein and amino acid metabolism. Curr Opin Clin Nutr Metab Care. 2012; 15 (1): 85-91
Zhao J, Brault JJ, Schild A, FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 2007; 6 (6): 472-83