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Myofibrillar function differs markedly between denervated and dexamethasone-treated rat skeletal muscles: Role of mechanical load


Autoři: Takashi Yamada aff001;  Yuki Ashida aff001;  Daisuke Tatebayashi aff001;  Koichi Himori aff001
Působiště autorů: Graduate School of Health Sciences, Sapporo Medical University, Sapporo, Japan aff001;  Research Fellow of Japan Society for the Promotion of Science, Tokyo, Japan aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0223551

Souhrn

Although there is good evidence to indicate a major role of intrinsic impairment of the contractile apparatus in muscle weakness seen in several pathophysiological conditions, the factors responsible for control of myofibrillar function are not fully understood. To investigate the role of mechanical load in myofibrillar function, we compared the skinned fiber force between denervated (DEN) and dexamethasone-treated (DEX) rat skeletal muscles with or without neuromuscular electrical stimulation (ES) training. DEN and DEX were induced by cutting the sciatic nerve and daily injection of dexamethasone (5 mg/kg/day) for 7 days, respectively. For ES training, plantarflexor muscles were electrically stimulated to produce four sets of five isometric contractions each day. In situ maximum torque was markedly depressed in the DEN muscles compared to the DEX muscles (-74% vs. -10%), whereas there was not much difference in the degree of atrophy in gastrocnemius muscles between DEN and DEX groups (-24% vs. -17%). Similar results were obtained in the skinned fiber preparation, with a greater reduction in maximum Ca2+-activated force in the DEN than in the DEX group (-53% vs. -16%). Moreover, there was a parallel decline in myosin heavy chain (MyHC) and actin content per muscle volume in DEN muscles, but not in DEX muscles, which was associated with upregulation of NADPH oxidase (NOX) 2, neuronal nitric oxide synthase (nNOS), and endothelial NOS expression, translocation of nNOS from the membrane to the cytosol, and augmentation of mRNA levels of muscle RING finger protein 1 (MuRF-1) and atrogin-1. Importantly, mechanical load evoked by ES protects against DEN- and DEX-induced myofibrillar dysfunction and these molecular alterations. Our findings provide novel insights regarding the difference in intrinsic contractile properties between DEN and DEX and suggest an important role of mechanical load in preserving myofibrillar function in skeletal muscle.

Klíčová slova:

Gene expression – Skeletal muscles – Functional electrical stimulation – Torque – Actins – Atrophy – Myosins – Muscle proteins


Zdroje

1. Reid MB, Moylan JS. Beyond atrophy: redox mechanisms of muscle dysfunction in chronic inflammatory disease. J Physiol. 2011;589:2171–9. doi: 10.1113/jphysiol.2010.203356 21320886; PubMed Central PMCID: PMC3098696.

2. Friedrich O, Reid MB, Van den Berghe G, Vanhorebeek I, Hermans G, Rich MM, et al. The Sick and the Weak: Neuropathies/Myopathies in the Critically Ill. Physiol Rev. 2015;95:1025–109. Epub 2015/07/03. doi: 10.1152/physrev.00028.2014 26133937; PubMed Central PMCID: PMC4491544.

3. Germinario E, Esposito A, Megighian A, Midrio M, Biral D, Betto R, et al. Early changes of type 2B fibers after denervation of rat EDL skeletal muscle. J Appl Physiol. 2002;92:2045–52. doi: 10.1152/japplphysiol.00673.2001 11960956

4. Alamdari N, Toraldo G, Aversa Z, Smith I, Castillero E, Renaud G, et al. Loss of muscle strength during sepsis is in part regulated by glucocorticoids and is associated with reduced muscle fiber stiffness. Am J Physiol Regul Integr Comp Physiol. 2012;303:R1090–9. Epub 2012/09/29. doi: 10.1152/ajpregu.00636.2011 23019215; PubMed Central PMCID: PMC3517670.

5. Eason JM, Dodd SL, Powers SK, Martin AD. Detrimental effects of short-term glucocorticoid use on the rat diaphragm. Phys Ther. 2000;80:160–7. Epub 2000/02/02. 10654062.

6. Dodd SL, Powers SK, Vrabas IS, Eason JM. Interaction of glucocorticoids and activity patterns affect muscle function. Muscle Nerve. 1995;18:190–5. Epub 1995/02/01. doi: 10.1002/mus.880180207 7823977.

7. Patterson MF, Stephenson GM, Stephenson DG. Denervation produces different single fiber phenotypes in fast- and slow-twitch hindlimb muscles of the rat. Am J Physiol Cell Physiol. 2006;291:C518–28. doi: 10.1152/ajpcell.00013.2006 16611740

8. Geiger PC, Cody MJ, Macken RL, Bayrd ME, Sieck GC. Effect of unilateral denervation on maximum specific force in rat diaphragm muscle fibers. J Appl Physiol (1985). 2001;90:1196–204. Epub 2001/03/15. doi: 10.1152/jappl.2001.90.4.1196 11247914.

9. Minetto MA, Qaisar R, Agoni V, Motta G, Longa E, Miotti D, et al. Quantitative and qualitative adaptations of muscle fibers to glucocorticoids. Muscle Nerve. 2015;52:631–9. Epub 2015/01/17. doi: 10.1002/mus.24572 25594832.

10. Laszewski B, Ruff RL. Effects of glucocorticoid treatment on excitation-contraction coupling. Am J Physiol. 1985;248:E363–9. Epub 1985/03/01. doi: 10.1152/ajpendo.1985.248.3.E363 3976885.

11. Mozaffar T, Haddad F, Zeng M, Zhang LY, Adams GR, Baldwin KM. Molecular and cellular defects of skeletal muscle in an animal model of acute quadriplegic myopathy. Muscle Nerve. 2007;35:55–65. Epub 2006/09/13. doi: 10.1002/mus.20647 16967495.

12. Cohen S, Brault JJ, Gygi SP, Glass DJ, Valenzuela DM, Gartner C, et al. During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation. J Cell Biol. 2009;185:1083–95. Epub 2009/06/10. doi: 10.1083/jcb.200901052 19506036; PubMed Central PMCID: PMC2711608.

13. Clarke BA, Drujan D, Willis MS, Murphy LO, Corpina RA, Burova E, et al. The E3 Ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab. 2007;6:376–85. doi: 10.1016/j.cmet.2007.09.009 17983583

14. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, et al. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science. 2001;294:1704–8. doi: 10.1126/science.1065874 11679633.

15. Ochala J, Gustafson AM, Diez ML, Renaud G, Li M, Aare S, et al. Preferential skeletal muscle myosin loss in response to mechanical silencing in a novel rat intensive care unit model: underlying mechanisms. J Physiol. 2011;589:2007–26. Epub 2011/02/16. doi: 10.1113/jphysiol.2010.202044 21320889; PubMed Central PMCID: PMC3090600.

16. Corpeno Kalamgi R, Salah H, Gastaldello S, Martinez-Redondo V, Ruas JL, Fury W, et al. Mechano-signalling pathways in an experimental intensive critical illness myopathy model. J Physiol. 2016;594:4371–88. Epub 2016/03/19. doi: 10.1113/JP271973 26990577.

17. Friedrich O, Diermeier S, Larsson L. Weak by the machines: muscle motor protein dysfunction—a side effect of intensive care unit treatment. Acta Physiol (Oxf). 2018;222. Epub 2017/04/08. doi: 10.1111/apha.12885 28387014.

18. Suzuki N, Motohashi N, Uezumi A, Fukada S, Yoshimura T, Itoyama Y, et al. NO production results in suspension-induced muscle atrophy through dislocation of neuronal NOS. J Clin Invest. 2007;117:2468–76. doi: 10.1172/JCI30654 17786240.

19. Bhattacharya A, Hamilton R, Jernigan A, Zhang Y, Sabia M, Rahman MM, et al. Genetic ablation of 12/15-lipoxygenase but not 5-lipoxygenase protects against denervation-induced muscle atrophy. Free Radic Biol Med. 2014;67:30–40. Epub 2013/10/15. doi: 10.1016/j.freeradbiomed.2013.10.002 24121057.

20. Konno S. Hydroxyl radical formation in skeletal muscle of rats with glucocorticoid-induced myopathy. Neurochem Res. 2005;30:669–75. Epub 2005/09/24. doi: 10.1007/s11064-005-2755-4 16176071.

21. Lawler JM, Kunst M, Hord JM, Lee Y, Joshi K, Botchlett RE, et al. EUK-134 ameliorates nNOSmu translocation and skeletal muscle fiber atrophy during short-term mechanical unloading. Am J Physiol Regul Integr Comp Physiol. 2014;306:R470–82. Epub 2014/01/31. doi: 10.1152/ajpregu.00371.2013 24477538; PubMed Central PMCID: PMC3962621.

22. Lechado ITA, Vitadello M, Traini L, Namuduri AV, Gastaldello S, Gorza L. Sarcolemmal loss of active nNOS (Nos1) is an oxidative stress-dependent, early event driving disuse atrophy. J Pathol. 2018;246:433–46. Epub 2018/08/02. doi: 10.1002/path.5149 30066461.

23. Tiago T, Simao S, Aureliano M, Martin-Romero FJ, Gutierrez-Merino C. Inhibition of skeletal muscle S1-myosin ATPase by peroxynitrite. Biochemistry. 2006;45:3794–804. doi: 10.1021/bi0518500 16533063

24. Tiago T, Ramos S, Aureliano M, Gutierrez-Merino C. Peroxynitrite induces F-actin depolymerization and blockade of myosin ATPase stimulation. Biochem Biophys Res Commun. 2006;342:44–9. doi: 10.1016/j.bbrc.2006.01.112 16480685.

25. Smuder AJ, Kavazis AN, Hudson MB, Nelson WB, Powers SK. Oxidation enhances myofibrillar protein degradation via calpain and caspase-3. Free Radic Biol Med. 2010;49:1152–60. doi: 10.1016/j.freeradbiomed.2010.06.025 20600829

26. Grune T, Merker K, Sandig G, Davies KJ. Selective degradation of oxidatively modified protein substrates by the proteasome. Biochem Biophys Res Commun. 2003;305:709–18. Epub 2003/05/24. doi: 10.1016/s0006-291x(03)00809-x 12763051.

27. Powers SK, Morton AB, Ahn B, Smuder AJ. Redox control of skeletal muscle atrophy. Free Radic Biol Med. 2016;98:208–17. Epub 2016/02/26. doi: 10.1016/j.freeradbiomed.2016.02.021 26912035; PubMed Central PMCID: PMC5006677.

28. Yamada T, Himori K, Tatebayashi D, Yamada R, Ashida Y, Imai T, et al. Electrical Stimulation Prevents Preferential Skeletal Muscle Myosin Loss in Steroid-Denervation Rats. Front Physiol. 2018;9:1111. Epub 2018/08/28. doi: 10.3389/fphys.2018.01111 30147660; PubMed Central PMCID: PMC6097132.

29. Allen DG, Kurihara S. The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. J Physiol. 1982;327:79–94. Epub 1982/06/01. doi: 10.1113/jphysiol.1982.sp014221 7120151; PubMed Central PMCID: PMC1225098.

30. Watanabe D, Wada M. Predominant cause of prolonged low-frequency force depression changes during recovery after in situ fatiguing stimulation of rat fast-twitch muscle. Am J Physiol Regul Integr Comp Physiol. 2016;311:R919–R29. Epub 2016/11/03. doi: 10.1152/ajpregu.00046.2016 27654397.

31. Moisescu DG, Thieleczek R. Calcium and strontium concentration changes within skinned muscle preparations following a change in the external bathing solution. J Physiol. 1978;275:241–62. Epub 1978/02/01. doi: 10.1113/jphysiol.1978.sp012188 24736; PubMed Central PMCID: PMC1282543.

32. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–54. doi: 10.1006/abio.1976.9999 942051

33. Kuczmarski JM, Hord JM, Lee Y, Guzzoni V, Rodriguez D, Lawler MS, et al. Effect of Eukarion-134 on Akt-mTOR signalling in the rat soleus during 7 days of mechanical unloading. Exp Physiol. 2018;103:545–58. Epub 2018/01/10. doi: 10.1113/EP086649 29315934.

34. Kanzaki K, Kuratani M, Matsunaga S, Yanaka N, Wada M. Three calpain isoforms are autolyzed in rat fast-twitch muscle after eccentric contractions. J Muscle Res Cell Motil. 2014;35:179–89. Epub 2014/02/22. doi: 10.1007/s10974-014-9378-9 24557809.

35. Goll DE, Thompson VF, Li H, Wei W, Cong J. The calpain system. Physiol Rev. 2003;83:731–801. Epub 2003/07/05. doi: 10.1152/physrev.00029.2002 12843408.

36. Renaud G, Llano-Diez M, Ravara B, Gorza L, Feng HZ, Jin JP, et al. Sparing of muscle mass and function by passive loading in an experimental intensive care unit model. J Physiol. 2013;591:1385–402. Epub 2012/12/26. doi: 10.1113/jphysiol.2012.248724 23266938; PubMed Central PMCID: PMC3607878.

37. Bowen TS, Eisenkolb S, Drobner J, Fischer T, Werner S, Linke A, et al. High-intensity interval training prevents oxidant-mediated diaphragm muscle weakness in hypertensive mice. FASEB J. 2017;31:60–71. Epub 2016/09/22. doi: 10.1096/fj.201600672R 27650398.

38. Cunha TF, Bacurau AV, Moreira JB, Paixao NA, Campos JC, Ferreira JC, et al. Exercise training prevents oxidative stress and ubiquitin-proteasome system overactivity and reverse skeletal muscle atrophy in heart failure. PLoS One. 2012;7:e41701. doi: 10.1371/journal.pone.0041701 22870245

39. Acharyya S, Ladner KJ, Nelsen LL, Damrauer J, Reiser PJ, Swoap S, et al. Cancer cachexia is regulated by selective targeting of skeletal muscle gene products. J Clin Invest. 2004;114:370–8. Epub 2004/08/03. doi: 10.1172/JCI20174 15286803; PubMed Central PMCID: PMC484974.

40. Ochala J, Larsson L. Effects of a preferential myosin loss on Ca2+ activation of force generation in single human skeletal muscle fibres. Exp Physiol. 2008;93:486–95. doi: 10.1113/expphysiol.2007.041798 18245202.

41. Ottenheijm CA, Heunks LM, Sieck GC, Zhan WZ, Jansen SM, Degens H, et al. Diaphragm dysfunction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2005;172:200–5. Epub 2005/04/26. doi: 10.1164/rccm.200502-262OC 15849324; PubMed Central PMCID: PMC2718467.

42. Yamada T, Place N, Kosterina N, Östberg T, Zhang SJ, Grundtman C, et al. Impaired myofibrillar function in the soleus muscle of mice with collagen-induced arthritis. Arthritis Rheum. 2009;60:3280–9. doi: 10.1002/art.24907 19877058.

43. D'Antona G, Pellegrino MA, Adami R, Rossi R, Carlizzi CN, Canepari M, et al. The effect of ageing and immobilization on structure and function of human skeletal muscle fibres. J Physiol. 2003;552:499–511. doi: 10.1113/jphysiol.2003.046276 14561832

44. Supinski GS, Callahan LA. Free radical-mediated skeletal muscle dysfunction in inflammatory conditions. J Appl Physiol. 2007;102:2056–63. doi: 10.1152/japplphysiol.01138.2006 17218425.

45. Goldberg AL. Protein turnover in skeletal muscle. II. Effects of denervation and cortisone on protein catabolism in skeletal muscle. J Biol Chem. 1969;244:3223–9. Epub 1969/06/25. 5792658.

46. Furlow JD, Watson ML, Waddell DS, Neff ES, Baehr LM, Ross AP, et al. Altered gene expression patterns in muscle ring finger 1 null mice during denervation- and dexamethasone-induced muscle atrophy. Physiol Genomics. 2013;45:1168–85. Epub 2013/10/17. doi: 10.1152/physiolgenomics.00022.2013 24130153; PubMed Central PMCID: PMC3882710.

47. Rudnick J, Puttmann B, Tesch PA, Alkner B, Schoser BG, Salanova M, et al. Differential expression of nitric oxide synthases (NOS 1–3) in human skeletal muscle following exercise countermeasure during 12 weeks of bed rest. FASEB J. 2004;18:1228–30. Epub 2004/06/08. doi: 10.1096/fj.03-0792fje 15180967.

48. Argadine HM, Hellyer NJ, Mantilla CB, Zhan WZ, Sieck GC. The effect of denervation on protein synthesis and degradation in adult rat diaphragm muscle. J Appl Physiol (1985). 2009;107:438–44. Epub 2009/06/13. doi: 10.1152/japplphysiol.91247.2008 19520837; PubMed Central PMCID: PMC2724326.

49. Quy PN, Kuma A, Pierre P, Mizushima N. Proteasome-dependent activation of mammalian target of rapamycin complex 1 (mTORC1) is essential for autophagy suppression and muscle remodeling following denervation. J Biol Chem. 2013;288:1125–34. Epub 2012/12/05. doi: 10.1074/jbc.M112.399949 23209294; PubMed Central PMCID: PMC3542997.

50. Schakman O, Gilson H, Thissen JP. Mechanisms of glucocorticoid-induced myopathy. J Endocrinol. 2008;197:1–10. Epub 2008/03/29. doi: 10.1677/JOE-07-0606 18372227.


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