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Regulation of ubiquitin proteasome pathway molecular markers in response to endurance and resistance exercise and training

  • Muscle physiology
  • Published:
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Abstract

Knowledge on the effects of divergent exercise on ostensibly protein degradation pathways may be valuable for counteracting muscle wasting and for understanding muscle remodelling. This study examined mRNA and/or protein levels of molecular markers of the ubiquitin proteasome pathway (UPP), including FBXO32 (atrogin-1), MURF-1, FBXO40, FOXO1 and FOXO3. Protein substrates of atrogin-1—including EIF3F, MYOG and MYOD1—and of MURF-1—including PKM and MHC—were also measured. Subjects completed 10 weeks of endurance training (ET) or resistance training (RT) followed by a single-bout of endurance exercise (EE) or resistance exercise (RE). Following training, atrogin-1, FBXO40, FOXO1 and FOXO3 mRNA increased independently of exercise mode, whereas MURF-1 mRNA and FOXO3 protein increased following ET only. No change in other target proteins occurred post-training. In the trained state, single-bout EE, but not RE, increased atrogin-1, MURF-1, FBXO40, FOXO1, FOXO3 mRNA and FOXO3 protein. In contrast to EE, FBXO40 mRNA and protein decreased following single-bout RE. MURF-1 and FOXO1 protein levels as well as the protein substrates of atrogin-1 and MURF-1 were unchanged following training and single-bout exercise. This study demonstrates that the intracellular signals elicited by ET and RT result in an upregulation of UPP molecular markers, with a greater increase following ET. However, in the trained state, the expression levels of UPP molecular markers are increased following single-bout EE, but are less responsive to single-bout RE. This suggests that adaptations following endurance exercise training are more reliant on protein UPP degradation processes than adaptations following resistance exercise training.

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References

  1. Andersen LB (1995) A maximal cycle exercise protocol to predict maximal oxygen uptake. Scand J Med Sci Sports 5(3):143–146. doi:10.1111/j.1600-0838.1995.tb00027.x

    Article  CAS  PubMed  Google Scholar 

  2. Andersen JL, Aagaard P (2000) Myosin heavy chain IIX overshoot in human skeletal muscle. Muscle Nerve 23(7):1095–1104

    Article  CAS  PubMed  Google Scholar 

  3. Andersen LL, Tufekovic G, Zebis MK, Crameri RM, Verlaan G, Kjaer M, Suetta C, Magnusson P, Aagaard P (2005) The effect of resistance training combined with timed ingestion of protein on muscle fiber size and muscle strength. Metabolism 54(2):151–156. doi:10.1016/j.metabol.2004.07.012

    Article  CAS  PubMed  Google Scholar 

  4. Biolo G, Maggi SP, Williams BD, Tipton KD, Wolfe RR (1995) Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans. Am J Physiol 268(3 Pt 1):E514–E520

    CAS  PubMed  Google Scholar 

  5. Biolo G, Williams BD, Fleming RY, Wolfe RR (1999) Insulin action on muscle protein kinetics and amino acid transport during recovery after resistance exercise. Diabetes 48(5):949–957. doi:10.2337/diabetes.48.5.949

    Article  CAS  PubMed  Google Scholar 

  6. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294(5547):1704–1708. doi:10.1126/science.1065874

    Article  CAS  PubMed  Google Scholar 

  7. Borgenvik M, Apro W, Blomstrand E (2012) Intake of branched-chain amino acids influences the levels of MAFbx mRNA and MuRF-1 total protein in resting and exercising human muscle. Am J Physiol Endocrinol Metab 302(5):E510–E521. doi:10.1152/ajpendo.00353.2011

    Article  CAS  PubMed  Google Scholar 

  8. Brooke MH, Kaiser KK (1970) Muscle fiber types: how many and what kind? Arch Neurol 23(4):369–379. doi:10.1001/archneur.1970.00480280083010

    Article  CAS  PubMed  Google Scholar 

  9. Brzycki M (1993) Strength testing: predicting a one-rep max from a reps-to-fatigue. J Phys Educ Recreat Dance 64(1):88–90

    Article  Google Scholar 

  10. Camera DM, Edge J, Short MJ, Hawley JA, Coffey VG (2010) Early time course of Akt phosphorylation after endurance and resistance exercise. Med Sci Sports Exerc 42(10):1843–1852. doi:10.1249/MSS.0b013e3181d964e4

    Article  CAS  PubMed  Google Scholar 

  11. Carraro F, Stuart CA, Hartl WH, Rosenblatt J, Wolfe RR (1990) Effect of exercise and recovery on muscle protein synthesis in human subjects. Am J Physiol 259(4 Pt 1):E470–E476

    CAS  PubMed  Google Scholar 

  12. Centner T, Yano J, Kimura E, McElhinny AS, Pelin K, Witt CC, Bang ML, Trombitas K, Granzier H, Gregorio CC, Sorimachi H, Labeit S (2001) Identification of muscle specific ring finger proteins as potential regulators of the titin kinase domain. J Mol Biol 306(4):717–726. doi:10.1006/jmbi.2001.4448

    Article  CAS  PubMed  Google Scholar 

  13. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162(1):156–159. doi:10.1006/abio.1987.9999

    Article  CAS  PubMed  Google Scholar 

  14. Churchley EG, Coffey VG, Pedersen DJ, Shield A, Carey KA, Cameron-Smith D, Hawley JA (2007) Influence of preexercise muscle glycogen content on transcriptional activity of metabolic and myogenic genes in well-trained humans. J Appl Physiol 102(4):1604–1611. doi:10.1152/japplphysiol.01260.2006

    Article  CAS  PubMed  Google Scholar 

  15. Clarke BA, Drujan D, Willis MS, Murphy LO, Corpina RA, Burova E, Rakhilin SV, Stitt TN, Patterson C, Latres E, Glass DJ (2007) The E3 Ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab 6(5):376–385. doi:10.1016/j.cmet.2007.09.009

    Article  CAS  PubMed  Google Scholar 

  16. Coffey VG, Shield A, Canny BJ, Carey KA, Cameron-Smith D, Hawley JA (2006) Interaction of contractile activity and training history on mRNA abundance in skeletal muscle from trained athletes. Am J Physiol Endocrinol Metab 290(5):E849–E855. doi:10.1152/ajpendo.00299.2005

    Article  CAS  PubMed  Google Scholar 

  17. Cohen S, Brault JJ, Gygi SP, Glass DJ, Valenzuela DM, Gartner C, Latres E, Goldberg AL (2009) During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation. J Cell Biol 185(6):1083–1095. doi:10.1083/jcb.200901052

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Cunha TF, Moreira JB, Paixao NA, Campos JC, Monteiro AW, Bacurau AV, Bueno CR Jr, Ferreira JC, Brum PC (2012) Aerobic exercise training upregulates skeletal muscle calpain and ubiquitin-proteasome systems in healthy mice. J Appl Physiol 112(11):1839–1846. doi:10.1152/japplphysiol.00346.2011

    Article  CAS  PubMed  Google Scholar 

  19. Dalbo VJ, Roberts MD, Hassell S, Kerksick CM (2013) Effects of pre-exercise feeding on serum hormone concentrations and biomarkers of myostatin and ubiquitin proteasome pathway activity. Eur J Nutr 52(2):477–487. doi:10.1007/s00394-012-0349-x

    Article  CAS  PubMed  Google Scholar 

  20. Deldicque L, Atherton P, Patel R, Theisen D, Nielens H, Rennie MJ, Francaux M (2008) Effects of resistance exercise with and without creatine supplementation on gene expression and cell signaling in human skeletal muscle. J Appl Physiol 104(2):371–378. doi:10.1152/japplphysiol.00873.2007

    Article  CAS  PubMed  Google Scholar 

  21. Farup J, Kjolhede T, Sorensen H, Dalgas U, Moller AB, Vestergaard PF, Ringgaard S, Bojsen-Moller J, Vissing K (2012) Muscle morphological and strength adaptations to endurance vs. resistance training. J Strength Cond Res 26(2):398–407. doi:10.1519/JSC.0b013e318225a26f

    Article  PubMed  Google Scholar 

  22. Glynn EL, Fry CS, Drummond MJ, Dreyer HC, Dhanani S, Volpi E, Rasmussen BB (2010) Muscle protein breakdown has a minor role in the protein anabolic response to essential amino acid and carbohydrate intake following resistance exercise. Am J Physiol Regul Integr Comp Physiol 299(2):R533–R540. doi:10.1152/ajpregu.00077.2010

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL (2001) Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci U S A 98(25):14440–14445. doi:10.1073/pnas.251541198

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Green H, Goreham C, Ouyang J, Ball-Burnett M, Ranney D (1999) Regulation of fiber size, oxidative potential, and capillarization in human muscle by resistance exercise. Am J Physiol 276:R591–R596

    CAS  PubMed  Google Scholar 

  25. Hirner S, Krohne C, Schuster A, Hoffmann S, Witt S, Erber R, Sticht C, Gasch A, Labeit S, Labeit D (2008) MuRF1-dependent regulation of systemic carbohydrate metabolism as revealed from transgenic mouse studies. J Mol Biol 379(4):666–677. doi:10.1016/j.jmb.2008.03.049

    Article  CAS  PubMed  Google Scholar 

  26. Holloszy JO, Coyle EF (1984) Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol 56:831–838

    CAS  PubMed  Google Scholar 

  27. Hood DA, Terjung RL (1987) Leucine metabolism in perfused rat skeletal muscle during contractions. Am J Physiol 253(6 Pt 1):E636–E647

    CAS  PubMed  Google Scholar 

  28. Hulmi JJ, Kovanen V, Selanne H, Kraemer WJ, Hakkinen K, Mero AA (2009) Acute and long-term effects of resistance exercise with or without protein ingestion on muscle hypertrophy and gene expression. Amino Acids 37(2):297–308. doi:10.1007/s00726-008-0150-6

    Article  CAS  PubMed  Google Scholar 

  29. Jogo M, Shiraishi S, Tamura TA (2009) Identification of MAFbx as a myogenin-engaged F-box protein in SCF ubiquitin ligase. FEBS Lett 583(17):2715–2719. doi:10.1016/j.febslet.2009.07.033

    Article  CAS  PubMed  Google Scholar 

  30. Kedar V, McDonough H, Arya R, Li HH, Rockman HA, Patterson C (2004) Muscle-specific RING finger 1 is a bona fide ubiquitin ligase that degrades cardiac troponin I. Proc Natl Acad Sci U S A 101(52):18135–18140. doi:10.1073/pnas.0404341102

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Kim PL, Staron RS, Phillips SM (2005) Fasted-state skeletal muscle protein synthesis after resistance exercise is altered with training. J Physiol 568(Pt 1):283–290. doi:10.1113/jphysiol.2005.093708

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Kostek MC, Chen YW, Cuthbertson DJ, Shi R, Fedele MJ, Esser KA, Rennie MJ (2007) Gene expression responses over 24 h to lengthening and shortening contractions in human muscle: major changes in CSRP3, MUSTN1, SIX1, and FBXO32. Physiol Genomics 31(1):42–52. doi:10.1152/physiolgenomics.00151.2006

    Article  CAS  PubMed  Google Scholar 

  33. Lagirand-Cantaloube J, Offner N, Csibi A, Leibovitch MP, Batonnet-Pichon S, Tintignac LA, Segura CT, Leibovitch SA (2008) The initiation factor eIF3-f is a major target for atrogin1/MAFbx function in skeletal muscle atrophy. EMBO J 27(8):1266–1276. doi:10.1038/emboj.2008.52

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Lamon S, Wallace MA, Stefanetti RJ, Rahbek SK, Vendelbo MH, Russell AP, Vissing K (2013) Regulation of the STARS signaling pathway in response to endurance and resistance exercise and training. Pflugers Arch - Eur J Physiol. doi:10.1007/s00424-013-1265-5

    Google Scholar 

  35. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, Price SR, Mitch WE, Goldberg AL (2004) Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18(1):39–51. doi:10.1096/fj.03-0610com

    Article  CAS  PubMed  Google Scholar 

  36. Lecker SH, Goldberg AL, Mitch WE (2006) Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. J Am Soc Nephrol 17(7):1807–1819. doi:10.1681/ASN.2006010083

    Article  CAS  PubMed  Google Scholar 

  37. Leger B, Cartoni R, Praz M, Lamon S, Deriaz O, Crettenand A, Gobelet C, Rohmer P, Konzelmann M, Luthi F, Russell AP (2006) Akt signalling through GSK-3beta, mTOR and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy. J Physiol 576(Pt 3):923–933. doi:10.1113/jphysiol.2006.116715

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Louis E, Raue U, Yang Y, Jemiolo B, Trappe S (2007) Time course of proteolytic, cytokine, and myostatin gene expression after acute exercise in human skeletal muscle. J Appl Physiol 103(5):1744–1751. doi:10.1152/japplphysiol.00679.2007

    Article  CAS  PubMed  Google Scholar 

  39. Mahoney DJ, Parise G, Melov S, Safdar A, Tarnopolsky MA (2005) Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise. FASEB J 19(11):1498–1500. doi:10.1096/fj.04-3149fje

    CAS  PubMed  Google Scholar 

  40. Mascher H, Andersson H, Nilsson PA, Ekblom B, Blomstrand E (2007) Changes in signalling pathways regulating protein synthesis in human muscle in the recovery period after endurance exercise. Acta Physiol (Oxf) 191(1):67–75. doi:10.1111/j.1748-1716.2007.01712.x

    Article  CAS  Google Scholar 

  41. Mascher H, Tannerstedt J, Brink-Elfegoun T, Ekblom B, Gustafsson T, Blomstrand E (2008) Repeated resistance exercise training induces different changes in mRNA expression of MAFbx and MuRF-1 in human skeletal muscle. Am J Physiol Endocrinol Metab 294(1):E43–E51. doi:10.1152/ajpendo.00504.2007

    Article  CAS  PubMed  Google Scholar 

  42. Nedergaard A, Vissing K, Overgaard K, Kjaer M, Schjerling P (2007) Expression patterns of atrogenic and ubiquitin proteasome component genes with exercise: effect of different loading patterns and repeated exercise bouts. J Appl Physiol 103(5):1513–1522. doi:10.1152/japplphysiol.01445.2006

    Article  CAS  PubMed  Google Scholar 

  43. Pasiakos SM, McClung HL, McClung JP, Urso ML, Pikosky MA, Cloutier GJ, Fielding RA, Young AJ (2010) Molecular responses to moderate endurance exercise in skeletal muscle. Int J Sport Nutr Exerc Metab 20(4):282–290

    CAS  PubMed  Google Scholar 

  44. Peserico A, Chiacchiera F, Grossi V, Matrone A, Latorre D, Simonatto M, Fusella A, Ryall JG, Finley LW, Haigis MC, Villani G, Puri PL, Sartorelli V, Simone C (2013) A novel AMPK-dependent FoxO3A-SIRT3 intramitochondrial complex sensing glucose levels. Cell Mol Life Sci: CMLS 70(11):2015–2029. doi:10.1007/s00018-012-1244-6

    Article  CAS  PubMed  Google Scholar 

  45. Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR (1997) Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am J Physiol 273(1 Pt 1):E99–E107. doi:10.1097/00005768-199705001-01319

    CAS  PubMed  Google Scholar 

  46. Phillips SM, Tipton KD, Ferrando AA, Wolfe RR (1999) Resistance training reduces the acute exercise-induced increase in muscle protein turnover. Am J Physiol 276(1 Pt 1):E118–E124

    CAS  PubMed  Google Scholar 

  47. Raue U, Slivka D, Jemiolo B, Hollon C, Trappe S (2007) Proteolytic gene expression differs at rest and after resistance exercise between young and old women. J Gerontol A Biol Sci Med Sci 62(12):1407–1412

    Article  PubMed  Google Scholar 

  48. Rauramaa R, Kuusela P, Hietanen E (1980) Adipose, muscle and lung tissue lipoprotein lipase activities in young streptozotocin treated rats. Horm Metab Res Hormon Stoffwechs Hormon Metab 12(11):591–595. doi:10.1055/s-2007-999207

    Article  CAS  Google Scholar 

  49. Reitelseder S, Agergaard J, Doessing S, Helmark IC, Schjerling P, van Hall G, Kjaer M, Holm L (2013) Positive muscle protein net balance and differential regulation of atrogene expression after resistance exercise and milk protein supplementation. Eur J Nutr. doi:10.1007/s00394-013-0530-x

    PubMed  Google Scholar 

  50. Russell AP (2010) Molecular regulation of skeletal muscle mass. Clin Exp Pharmacol Physiol 37(3):378–384. doi:10.1111/j.1440-1681.2009.05265.x

    Article  CAS  PubMed  Google Scholar 

  51. Sacheck JM, Hyatt JP, Raffaello A, Jagoe RT, Roy RR, Edgerton VR, Lecker SH, Goldberg AL (2007) Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB J 21(1):140–155. doi:10.1096/fj.06-6604com

    Article  CAS  PubMed  Google Scholar 

  52. Sale D, MacDougall D (1981) Specificity in strength training: a review for the coach and athlete. Can J Appl Sport Sci J Can Sci Appl Sport 6(2):87–92

    CAS  Google Scholar 

  53. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL (2004) Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117(3):399–412. doi:10.1016/S0092-8674(04)00400-3

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. Sandri M, Barberi L, Bijlsma AY, Blaauw B, Dyar KA, Milan G, Mammucari C, Meskers CG, Pallafacchina G, Paoli A, Pion D, Roceri M, Romanello V, Serrano AL, Toniolo L, Larsson L, Maier AB, Munoz-Canoves P, Musaro A, Pende M, Reggiani C, Rizzuto R, Schiaffino S (2013) Signalling pathways regulating muscle mass in ageing skeletal muscle. The role of the IGF1-Akt-mTOR-FoxO pathway. Biogerontology 14(3):303–323. doi:10.1007/s10522-013-9432-9

    Article  CAS  PubMed  Google Scholar 

  55. Shi J, Luo L, Eash J, Ibebunjo C, Glass DJ (2011) The SCF-Fbxo40 complex induces IRS1 ubiquitination in skeletal muscle, limiting IGF1 signaling. Dev Cell 21(5):835–847. doi:10.1016/j.devcel.2011.09.011

    Article  PubMed  Google Scholar 

  56. Stefanetti RJ, Lamon S, Rahbek SK, Farup J, Zacharewicz E, Wallace MA, Vendelbo MH, Russell AP, Vissing K (2014) Influence of divergent exercise contraction mode and whey protein supplementation on atrogin-1, MuRF1 and FOXO1/3A in human skeletal muscle. J Appl Physiol. doi:10.1152/japplphysiol.00136.2013

    PubMed  Google Scholar 

  57. Stefanetti RJ, Zacharewicz E, Della Gatta P, Garnham A, Russell AP, Lamon S (2014) Ageing has no effect on the regulation of the ubiquitin proteasome-related genes and proteins following resistance exercise. Front Physiol 5:30. doi:10.3389/fphys.2014.00030

    Article  PubMed Central  PubMed  Google Scholar 

  58. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD, Glass DJ (2004) The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14(3):395–403. doi:10.1016/S1097-2765(04)00211-4

    Article  CAS  PubMed  Google Scholar 

  59. Tintignac LA, Lagirand J, Batonnet S, Sirri V, Leibovitch MP, Leibovitch SA (2005) Degradation of MyoD mediated by the SCF (MAFbx) ubiquitin ligase. J Biol Chem 280(4):2847–2856. doi:10.1074/jbc.M411346200

    Article  CAS  PubMed  Google Scholar 

  60. Toth MJ, Tchernof A (2006) Effect of age on skeletal muscle myofibrillar mRNA abundance: relationship to myosin heavy chain protein synthesis rate. Exp Gerontol 41(11):1195–1200. doi:10.1016/j.exger.2006.08.005

    Article  CAS  PubMed  Google Scholar 

  61. van Wessel T, de Haan A, van der Laarse WJ, Jaspers RT (2010) The muscle fiber type-fiber size paradox: hypertrophy or oxidative metabolism? Eur J Appl Physiol 110(4):665–694. doi:10.1007/s00421-010-1545-0

    Article  PubMed Central  PubMed  Google Scholar 

  62. Vissing K, Brink M, Lonbro S, Sorensen H, Overgaard K, Danborg K, Mortensen J, Elstrom O, Rosenhoj N, Ringgaard S, Andersen JL, Aagaard P (2008) Muscle adaptations to plyometric vs. resistance training in untrained young men. J Strength Cond Res 22(6):1799–1810. doi:10.1519/JSC.0b013e318185f673

    Article  PubMed  Google Scholar 

  63. Vissing K, McGee SL, Roepstorff C, Schjerling P, Hargreaves M, Kiens B (2008) Effect of sex differences on human MEF2 regulation during endurance exercise. Am J Physiol Endocrinol Metab 294(2):E408–E415. doi:10.1152/ajpendo.00403.2007

    Article  CAS  PubMed  Google Scholar 

  64. Vissing K, McGee SL, Farup J, Kjolhede T, Vendelbo MH, Jessen N (2011) Differentiated mTOR but not AMPK signaling after strength vs endurance exercise in training-accustomed individuals. Scand J Med Sci Sports. doi:10.1111/j.1600-0838.2011.01395.x

    PubMed  Google Scholar 

  65. Wakshlag JJ, Kallfelz FA, Barr SC, Ordway G, Haley NJ, Flaherty CE, Kelley RL, Altom EK, Lepine AJ, Davenport GM (2002) Effects of exercise on canine skeletal muscle proteolysis: an investigation of the ubiquitin-proteasome pathway and other metabolic markers. Vet Ther: Res Appl Vet Med 3(3):215–225

    Google Scholar 

  66. Yan Z, Lira VA, Greene NP (2012) Exercise training-induced regulation of mitochondrial quality. Exerc Sport Sci Rev 40(3):159–164. doi:10.1097/JES.0b013e3182575599

    PubMed Central  PubMed  Google Scholar 

  67. Yang Y, Jemiolo B, Trappe S (2006) Proteolytic mRNA expression in response to acute resistance exercise in human single skeletal muscle fibers. J Appl Physiol 101(5):1442–1450. doi:10.1152/japplphysiol.00438.2006

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The sarcomeric myosin (MF 20) hybridoma antibody developed by Donald A. Fischman was obtained from the Developmental Studies Hybridoma Bank developed under the auspices of the NICHD and maintained by The University of Iowa, Department of Biology, Iowa City, IA 52242. We thank the subjects for their participation in the project. Jean Farup, Tue Kjølhede, Andreas Buch Møller and Poul Vestergaard are thanked for the assistance with training and testing of the subjects. Séverine Lamon was supported by an Alfred Deakin Postdoctoral fellowship from Deakin University. Kristian Vissing was supported by the Novo Nordisk Foundation. The study complied with the current laws of Region Midtjylland, Denmark.

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Authors and Affiliations

  1. Centre for Physical Activity and Nutrition, School of Exercise and Nutrition Sciences, Deakin University, Burwood, 3125, Australia

    Renae J. Stefanetti, Séverine Lamon, Marita Wallace & Aaron P. Russell

  2. Section of Sport Science, Department of Public Health, Aarhus University, Dalgas Avenue 4, Aarhus C, 8000, Aarhus, Denmark

    Kristian Vissing

  3. Department of Internal Medicine and Endocrinology, Aarhus University Hospital, 8000, Aarhus, Denmark

    Mikkel H. Vendelbo

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  1. Renae J. Stefanetti
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Correspondence to Kristian Vissing.

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Stefanetti, R.J., Lamon, S., Wallace, M. et al. Regulation of ubiquitin proteasome pathway molecular markers in response to endurance and resistance exercise and training. Pflugers Arch - Eur J Physiol 467, 1523–1537 (2015). https://doi.org/10.1007/s00424-014-1587-y

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