Advertisement

Physiological and biochemical characteristics of skeletal muscles in sedentary and active rats

  • Hongyang Xu
  • Xiaoyu Ren
  • Graham D. Lamb
  • Robyn M. Murphy
Article
  • 158 Downloads

Abstract

Laboratory rats are sedentary if housed in conditions where activity is limited. Changes in muscle characteristics with chronic inactivity were investigated by comparing sedentary rats with rats undertaking voluntary wheel running for either 6 or 12 weeks. EDL (type II fibers) and soleus (SOL) muscles (predominantly type I fibers) were examined. When measured within 1–2 h post-running, calcium sensitivity of the contractile apparatus was increased, but only in type II fibers. This increase disappeared when fibers were treated with DTT, indicative of oxidative regulation of the contractile apparatus, and was absent in fibers from rats that had ceased running 24 h prior to experiments. Specific force production was ~ 10 to 25% lower in muscle fibers of sedentary compared to active rats, and excitability of skinned fibers was decreased. Muscle glycogen content was ~ 30% lower and glycogen synthase content ~ 50% higher in SOL of sedentary rats, and in EDL glycogenin was 30% lower. Na+, K+-ATPase α1 subunit density was ~ 20% lower in both EDL and SOL in sedentary rats, and GAPDH content in SOL ~ 35% higher. There were no changes in content of the calcium handling proteins calsequestrin and SERCA, but the content of CSQ-like protein was increased in active rats (by ~ 20% in EDL and 60% in SOL). These findings show that voluntary exercise elicits an acute oxidation-induced increase in Ca2+ sensitivity in type II fibers, and also that there are substantial changes in skeletal muscle characteristics and biochemical processes in sedentary rats.

Keywords

Chronic inactivity Voluntary wheel running Single muscle fibers Ca2+-sensitivity Glutathionylation Glycogen MHC composition 

Notes

Acknowledgements

This was supported by a National Health and Medical Research Council (Australia) Grant (APP1085331) to GDL and RMM.

References

  1. Adams GR, Caiozzo VJ, Baldwin KM (2003) Skeletal muscle unweighting: spaceflight and ground-based models. J Appl Physiol (1985) 95:2185–2201CrossRefGoogle Scholar
  2. Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88:287–332CrossRefGoogle Scholar
  3. Bortolotto SK, Cellini M, Stephenson DG, Stephenson GM (2000) MHC isoform composition and Ca(2+)- or Sr(2+)-activation properties of rat skeletal muscle fibers. Am J Physiol Cell Physiol 279:C1564-1577CrossRefGoogle Scholar
  4. Brocca L, Longa E, Cannavino J, Seynnes O, de Vito G, McPhee J, Narici M, Pellegrino MA, Bottinelli R (2015) Human skeletal muscle fibre contractile properties and proteomic profile: adaptations to 3 weeks of unilateral lower limb suspension and active recovery. J Physiol 593:5361–5385CrossRefPubMedPubMedCentralGoogle Scholar
  5. Broch-Lips M, de Paoli F, Pedersen TH, Overgaard K, Nielsen OB (2011) Effects of 8 wk of voluntary unloaded wheel running on K+ tolerance and excitability of soleus muscles in rat. J Appl Physiol (1985) 111:212–220CrossRefGoogle Scholar
  6. Cala SE, Scott BT, Jones LR (1990) Intralumenal sarcoplasmic reticulum Ca(2+)-binding proteins. Semin Cell Biol 1:265–275PubMedGoogle Scholar
  7. Chevessier F, Marty I, Paturneau-Jouas M, Hantai D, Verdiere-Sahuque M (2004) Tubular aggregates are from whole sarcoplasmic reticulum origin: alterations in calcium binding protein expression in mouse skeletal muscle during aging. Neuromuscul Disord 14:208–216CrossRefGoogle Scholar
  8. Christ-Roberts CY, Pratipanawatr T, Pratipanawatr W, Berria R, Belfort R, Kashyap S, Mandarino LJ (2004) Exercise training increases glycogen synthase activity and GLUT4 expression but not insulin signaling in overweight nondiabetic and type 2 diabetic subjects. Metab Clin Exp 53:1233–1242CrossRefGoogle Scholar
  9. Chua M, Dulhunty AF (1988) Inactivation of excitation-contraction coupling in rat extensor digitorum longus and soleus muscles. J Gen Physiol 91:737–757CrossRefGoogle Scholar
  10. Culligan K, Banville N, Dowling P, Ohlendieck K (2002) Drastic reduction of calsequestrin-like proteins and impaired calcium binding in dystrophic mdx muscle. J Appl Physiol 92:435–445CrossRefGoogle Scholar
  11. Desplanches D, Mayet MH, Sempore B, Flandrois R (1987) Structural and functional responses to prolonged hindlimb suspension in rat muscle. J Appl Physiol (1985) 63:558–563CrossRefGoogle Scholar
  12. Dutka TL, Mollica JP, Lamboley CR, Weerakkody VC, Greening DW, Posterino GS, Murphy RM, Lamb GD (2017) S-nitrosylation and S-glutathionylation of Cys134 on troponin I have opposing competitive actions on Ca2+ sensitivity in rat fast-twitch muscle fibers. Am J Physiol Cell Physiol 312:C316-c327CrossRefGoogle Scholar
  13. Ebashi S (1972) Calcium ions and muscle contraction. Nature 240:217–218CrossRefGoogle Scholar
  14. Fitts RH, Metzger JM, Riley DA, Unsworth BR (1986) Models of disuse: a comparison of hindlimb suspension and immobilization. J Appl Physiol (1985) 60:1946–1953CrossRefGoogle Scholar
  15. Froemming GR, Ohlendieck K (2001) The role of ion-regulatory membrane proteins of excitation-contraction coupling and relaxation in inherited muscle diseases. Front Biosci 6:D65–D74CrossRefGoogle Scholar
  16. Froemming GR, Murray BE, Harmon S, Pette D, Ohlendieck K (2000) Comparative analysis of the isoform expression pattern of Ca(2+)-regulatory membrane proteins in fast-twitch, slow-twitch, cardiac, neonatal and chronic low-frequency stimulated muscle fibers. Biochim Biophys Acta 1466:151–168CrossRefGoogle Scholar
  17. Gallo M, Gordon T, Syrotuik D, Shu Y, Tyreman N, MacLean I, Kenwell Z, Putman CT (2006) Effects of long-term creatine feeding and running on isometric functional measures and myosin heavy chain content of rat skeletal muscles. Pflugers Arch 452:744–755CrossRefGoogle Scholar
  18. Garvey SM, Russ DW, Skelding MB, Dugle JE, Edens NK (2015) Molecular and metabolomic effects of voluntary running wheel activity on skeletal muscle in late middle-aged rats. Physiol Rep 3:E12319Google Scholar
  19. Hayes A, Williams DA (1996) Beneficial effects of voluntary wheel running on the properties of dystrophic mouse muscle. J Appl Physiol (1985) 80:670–679CrossRefGoogle Scholar
  20. Heinemeier KM, Olesen JL, Schjerling P, Haddad F, Langberg H, Baldwin KM, Kjaer M (2007) Short-term strength training and the expression of myostatin and IGF-I isoforms in rat muscle and tendon: differential effects of specific contraction types. J Appl Physiol 102:573–581CrossRefPubMedPubMedCentralGoogle Scholar
  21. Henriksen EJ, Halseth AE (1995) Adaptive responses of GLUT-4 and citrate synthase in fast-twitch muscle of voluntary running rats. Am J Physiol 268:R130-134Google Scholar
  22. Ishihara A, Roy RR, Ohira Y, Ibata Y, Edgerton VR (1998) Hypertrophy of rat plantaris muscle fibers after voluntary running with increasing loads. J Appl Physiol (1985) 84:2183–2189CrossRefGoogle Scholar
  23. Kariya F, Yamauchi H, Kobayashi K, Narusawa M, Nakahara Y (2004) Effects of prolonged voluntary wheel-running on muscle structure and function in rat skeletal muscle. Eur J Appl Physiol 92:90–97CrossRefGoogle Scholar
  24. Kim JH, Thompson LV (2013) Inactivity, age, and exercise: single-muscle fiber power generation. J Appl Physiol (1985) 114:90–98CrossRefGoogle Scholar
  25. Kriketos AD, Pan DA, Sutton JR, Hoh JF, Baur LA, Cooney GJ, Jenkins AB, Storlien LH (1995) Relationships between muscle membrane lipids, fiber type, and enzyme activities in sedentary and exercised rats. Am J Physiol Regul Integr Comp Physiol 269:R1154–R1162CrossRefGoogle Scholar
  26. Lamb GD (2002) Excitation-contraction coupling and fatigue mechanisms in skeletal muscle: studies with mechanically skinned fibres. J Muscle Res Cell Motil 23:81–91CrossRefGoogle Scholar
  27. Lamb GD, Stephenson DG (1990) Calcium release in skinned muscle fibres of the toad by transverse tubule depolarization or by direct stimulation. J Physiol 423:495–517CrossRefPubMedPubMedCentralGoogle Scholar
  28. Lamb GD, Stephenson DG (1994) Effects of intracellular pH and [Mg2+] on excitation-contraction coupling in skeletal muscle fibres of the rat. J Physiol 478(Pt 2):331–339CrossRefPubMedPubMedCentralGoogle Scholar
  29. Lamboley CR, Wyckelsma VL, Dutka TL, McKenna MJ, Murphy RM, Lamb GD (2015) Contractile properties and sarcoplasmic reticulum calcium content in type I and type II skeletal muscle fibres in active aged humans. J Physiol 593:2499–2514CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lamboley CR, Wyckelsma VL, Perry BD, McKenna MJ, Lamb GD (2016) Effect of 23-day muscle disuse on sarcoplasmic reticulum Ca2+ properties and contractility in human type I and type II skeletal muscle fibers. J Appl Physiol (1985) 121:483–492CrossRefGoogle Scholar
  31. Larsen S, Nielsen J, Hansen CN, Nielsen LB, Wibrand F, Stride N, Schroder HD, Boushel R, Helge JW, Dela F, Hey-Mogensen M (2012) Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J Physiol 590:3349–3360CrossRefPubMedPubMedCentralGoogle Scholar
  32. Larsson L, Li X, Berg HE, Frontera WR (1996) Effects of removal of weight-bearing function on contractility and myosin isoform composition in single human skeletal muscle cells. Pflugers Arch 432:320–328CrossRefGoogle Scholar
  33. Mollica JP, Dutka TL, Merry TL, Lamboley CR, McConell GK, McKenna MJ, Murphy RM, Lamb GD (2012) S-glutathionylation of troponin I (fast) increases contractile apparatus Ca2+ sensitivity in fast-twitch muscle fibres of rats and humans. J Physiol 590:1443–1463CrossRefPubMedPubMedCentralGoogle Scholar
  34. Mondon CE, Dolkas CB, Sims C, Reaven GM (1985) Spontaneous running activity in male rats: effect of age. J Appl Physiol (1985) 58:1553–1557CrossRefGoogle Scholar
  35. Murphy RM, Lamb GD (2013) Important considerations for protein analyses using antibody based techniques: down-sizing Western blotting up-sizes outcomes. J Physiol Lond 591:5823–5831CrossRefPubMedPubMedCentralGoogle Scholar
  36. Murphy RM, Watt KK, Cameron-Smith D, Gibbons CJ, Snow RJ (2003) Effects of creatine supplementation on housekeeping genes in human skeletal muscle using real-time RT-PCR. Physiol Genom 12:163–174CrossRefGoogle Scholar
  37. Murphy RM, Larkins NT, Mollica JP, Beard NA, Lamb GD (2009a) Calsequestrin content and SERCA determine normal and maximal Ca2+ storage levels in sarcoplasmic reticulum of fast- and slow-twitch fibres of rat. J Physiol 587:443–460CrossRefPubMedPubMedCentralGoogle Scholar
  38. Murphy RM, Mollica JP, Lamb GD (2009b) Plasma membrane removal in rat skeletal muscle fibers reveals caveolin-3 hot-spots at the necks of transverse tubules. Exp Cell Res 315:1015–1028CrossRefPubMedPubMedCentralGoogle Scholar
  39. Murphy RM, Xu H, Latchman H, Larkins NT, Gooley PR, Stapleton DI (2012) Single fiber analyses of glycogen-related proteins reveal their differential association with glycogen in rat skeletal muscle. Am J Physiol Cell Physiol 303:C1146–C1155CrossRefGoogle Scholar
  40. Murray BE, Froemming GR, Maguire PB, Ohlendieck K (1998) Excitation-contraction-relaxation cycle: role of Ca2+-regulatory membrane proteins in normal, stimulated and pathological skeletal muscle (review). Int J Mol Med 1:677–687PubMedGoogle Scholar
  41. Nielsen J, Holmberg HC, Schroder HD, Saltin B, Ortenblad N (2011) Human skeletal muscle glycogen utilization in exhaustive exercise: role of subcellular localization and fibre type. J Physiol 589:2871–2885CrossRefPubMedPubMedCentralGoogle Scholar
  42. Parker GJ, Koay A, Gilbert-Wilson R, Waddington LJ, Stapleton D (2007) AMP-activated protein kinase does not associate with glycogen alpha-particles from rat liver. Biochem Biophys Res Commun 362:811–815CrossRefGoogle Scholar
  43. Pedersen TH, Nielsen OB, Lamb GD, Stephenson DG (2004) Intracellular acidosis enhances the excitability of working muscle. Science 305:1144–1147CrossRefGoogle Scholar
  44. Perry BD, Wyckelsma VL, Murphy RM, Steward CH, Anderson M, Levinger I, Petersen AC, McKenna MJ (2016) Dissociation between short-term unloading and resistance training effects on skeletal muscle Na+,K+-ATPase, muscle function, and fatigue in humans. J Appl Physiol (1985) 121:1074–1086CrossRefGoogle Scholar
  45. Posterino GS, Lamb GD (2003) Effect of sarcoplasmic reticulum Ca2+ content on action potential-induced Ca2+ release in rat skeletal muscle fibres. J Physiol 551:219–237CrossRefPubMedPubMedCentralGoogle Scholar
  46. Powers SK, Jackson MJ (2008) Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 88:1243–1276CrossRefPubMedPubMedCentralGoogle Scholar
  47. Prats C, Helge JW, Nordby P, Qvortrup K, Ploug T, Dela F, Wojtaszewski JF (2009) Dual regulation of muscle glycogen synthase during exercise by activation and compartmentalization. J Biol Chem 284:15692–15700CrossRefPubMedPubMedCentralGoogle Scholar
  48. Prats C, Gomez-Cabello A, Hansen AV (2011) Intracellular compartmentalization of skeletal muscle glycogen metabolism and insulin signalling. Exp Physiol 96:385–390CrossRefGoogle Scholar
  49. Rebbeck RT, Karunasekara Y, Board PG, Beard NA, Casarotto MG, Dulhunty AF (2014) Skeletal muscle excitation-contraction coupling: who are the dancing partners? Int J Biochem Cell Biol 48:28–38CrossRefGoogle Scholar
  50. Redl C, Gfoehler M, Pandy MG (2007) Sensitivity of muscle force estimates to variations in muscle-tendon properties. Hum Mov Sci 26:306–319CrossRefGoogle Scholar
  51. Ren JM, Semenkovich CF, Gulve EA, Gao J, Holloszy JO (1994) Exercise induces rapid increases in GLUT4 expression, glucose transport capacity, and insulin-stimulated glycogen storage in muscle. J Biol Chem 269:14396–14401PubMedGoogle Scholar
  52. Rockl KS, Hirshman MF, Brandauer J, Fujii N, Witters LA, Goodyear LJ (2007) Skeletal muscle adaptation to exercise training: AMP-activated protein kinase mediates muscle fiber type shift. Diabetes 56:2062–2069CrossRefGoogle Scholar
  53. Rodnick KJ, Reaven GM, Haskell WL, Sims CR, Mondon CE (1989) Variations in running activity and enzymatic adaptations in voluntary running rats. J Appl Physiol (1985) 66:1250–1257CrossRefGoogle Scholar
  54. Rodnick KJ, Henriksen EJ, James DE, Holloszy JO (1992) Exercise training, glucose transporters, and glucose transport in rat skeletal muscles. Am J Physiol 262:C9-14CrossRefGoogle Scholar
  55. Ryu JH, Drain J, Kim JH, McGee S, Gray-Weale A, Waddington L, Parker GJ, Hargreaves M, Yoo SH, Stapleton D (2009) Comparative structural analyses of purified glycogen particles from rat liver, human skeletal muscle and commercial preparations. Int J Biol Macromol 45:478–482CrossRefGoogle Scholar
  56. Salanova M, Schiffl G, Gutsmann M, Felsenberg D, Furlan S, Volpe P, Clarke A, Blottner D (2013) Nitrosative stress in human skeletal muscle attenuated by exercise countermeasure after chronic disuse. Redox Biol 1:514–526CrossRefPubMedPubMedCentralGoogle Scholar
  57. Steffen JM, Musacchia XJ (1984) Effect of hypokinesia and hypodynamia on protein, RNA, and DNA in rat hindlimb muscles. Am J Physiol 247:R728-732Google Scholar
  58. Stephenson DG, Williams DA (1981) Calcium-activated force responses in fast-twitch and slow-twitch skinned muscle-fibers of the rat at different temperatures. J Physiol Lond 317:281–302CrossRefPubMedPubMedCentralGoogle Scholar
  59. Talmadge RJ, Roy RR, Caiozzo VJ, Edgerton VR (2002) Mechanical properties of rat soleus after long-term spinal cord transection. J Appl Physiol (1985) 93:1487–1497CrossRefGoogle Scholar
  60. Thomason DB, Herrick RE, Surdyka D, Baldwin KM (1987) Time course of soleus muscle myosin expression during hindlimb suspension and recovery. J Appl Physiol (1985) 63:130–137CrossRefGoogle Scholar
  61. Trappe S, Trappe T, Gallagher P, Harber M, Alkner B, Tesch P (2004) Human single muscle fibre function with 84 day bed-rest and resistance exercise. J Physiol 557:501–513CrossRefPubMedPubMedCentralGoogle Scholar
  62. Trinh HH, Lamb GD (2006) Matching of sarcoplasmic reticulum and contractile properties in rat fast- and slow-twitch muscle fibres. Clin Exp Pharmacol Physiol 33:591–600CrossRefPubMedPubMedCentralGoogle Scholar
  63. Tristan C, Shahani N, Sedlak TW, Sawa A (2011) The diverse functions of GAPDH: views from different subcellular compartments. Cell Signal 23:317–323CrossRefPubMedPubMedCentralGoogle Scholar
  64. Watanabe D, Kanzaki K, Kuratani M, Matsunaga S, Yanaka N, Wada M (2015) Contribution of impaired myofibril and ryanodine receptor function to prolonged low-frequency force depression after in situ stimulation in rat skeletal muscle. J Muscle Res Cell Motil 36:275–286CrossRefPubMedPubMedCentralGoogle Scholar
  65. Widrick JJ, Trappe SW, Romatowski JG, Riley DA, Costill DL, Fitts RH (2002) Unilateral lower limb suspension does not mimic bed rest or spaceflight effects on human muscle fiber function. J Appl Physiol 93:354–360CrossRefPubMedPubMedCentralGoogle Scholar
  66. Wyckelsma VL, McKenna MJ, Serpiello FR, Lamboley CR, Aughey RJ, Stepto NK, Bishop DJ, Murphy RM (2015) Single-fiber expression and fiber-specific adaptability to short-term intense exercise training of Na+-K+-ATPase alpha- and beta-isoforms in human skeletal muscle. J Appl Physiol (1985) 118:699–706CrossRefGoogle Scholar
  67. Wyckelsma VL, McKenna MJ, Levinger I, Petersen AC, Lamboley CR, Murphy RM (2016) Cell specific differences in the protein abundances of GAPDH and Na(+),K(+)-ATPase in skeletal muscle from aged individuals. Exp Gerontol 75:8–15CrossRefGoogle Scholar
  68. Xu H, Stapleton D, Murphy RM (2015) Rat skeletal muscle glycogen degradation pathways reveal differential association of glycogen-related proteins with glycogen granules. J Physiol Biochem 71:267–280CrossRefGoogle Scholar
  69. Xu H, Frankenberg NT, Lamb GD, Gooley PR, Stapleton DI, Murphy RM (2016) When phosphorylated at Thr148, the beta2-subunit of AMP-activated kinase does not associate with glycogen in skeletal muscle. Am J Physiol Cell Physiol 311:C35-42PubMedGoogle Scholar
  70. Xu H, Lamb GD, Murphy RM (2017) Changes in contractile and metabolic parameters of skeletal muscle as rats age from 3 to 12 months. J Muscle Res Cell Motil.  https://doi.org/10.1007/s10974-017-9484-6 CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biochemistry and Genetics, La Trobe Institute for Molecular ScienceLa Trobe UniversityMelbourneAustralia
  2. 2.Department of Physiology, Anatomy and MicrobiologyLa Trobe UniversityMelbourneAustralia

Personalised recommendations