Acute resistance exercise activates rapamycin-sensitive and -insensitive mechanisms that control translational activity and capacity in skeletal muscle

Journal of Physiology

Volumn 594, Issue 2, 2016, Pages 453-468

  West, Daniel W D ^a   Baehr, Leslie M ^a   Marcotte, George R ^a   Chason, Courtney M ^b   Tolento, Luis ^b   Gomes, Aldrin V ^a,b   Bodine, Sue C ^a,b,c   Baar, Keith ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VA NORTHERN CALIFORNIA HEALTH CARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; ELONGATION FACTOR 2; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MUSCLE PROTEIN; MYOSTATIN; PROTEASOME; PROTEIN S6; RAPAMYCIN; S6 KINASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; UPSTREAM BINDING FACTOR; MYC PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROSTIMULATION; ENZYME PHOSPHORYLATION; EXERCISE RECOVERY; FEMALE; GENE; GENE EXPRESSION; GENE FUNCTION; IN VITRO STUDY; MIGHTY GENE; NERVE STIMULATION; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN HOMEOSTASIS; PROTEIN SYNTHESIS; RAT; RESISTANCE TRAINING; RIBOSOME; RIBOSOME BIOGENESIS; RNA TRANSLATION; SCIATIC NERVE; SKELETAL MUSCLE; TIBIALIS ANTERIOR MUSCLE; ANIMAL; CELL LINE; DRUG EFFECTS; FISCHER 344 RAT; METABOLISM; MOUSE; MUSCLE CONTRACTION; PHYSIOLOGY;

ANIMALS; CELL LINE; FEMALE; MICE; MUSCLE CONTRACTION; MUSCLE, SKELETAL; PHYSICAL CONDITIONING, ANIMAL; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BIOSYNTHESIS; PROTO-ONCOGENE PROTEINS C-MYC; RATS; RATS, INBRED F344; RIBOSOMES; SIROLIMUS;

EID: 84956748341     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP271365     Document Type: Article

References (71)

1. Adams GR, Caiozzo VJ, Haddad F & Baldwin KM (2002). Cellular and molecular responses to increased skeletal muscle loading after irradiation. Am J Physiol Cell Physiol 283, C1182-1195.
2. Akiho M, Nakashima H, Sakata M, Yamasa Y, Yamaguchi A & Sakuma K (2010). Expression profile of Notch-1 in mechanically overloaded plantaris muscle of mice. Life Sci 86, 59-65.
3. Al-Khalili L, de Castro Barbosa T, Ostling J, Massart J, Cuesta PG, Osler ME, Katayama M, Nystrom AC, Oscarsson J & Zierath JR (2014). Proteasome inhibition in skeletal muscle cells unmasks metabolic derangements in type 2 diabetes. Am J Physiol Cell Physiol 307, C774-787.
4. Altman DG, Gore SM, Gardner MJ & Pocock SJ (1983). Statistical guidelines for contributors to medical journals. Br Med J 286, 1489-1493.
5. Arabi A, Wu S, Ridderstrale K, Bierhoff H, Shiue C, Fatyol K, Fahlen S, Hydbring P, Soderberg O, Grummt I, Larsson LG & Wright AP (2005). c-Myc associates with ribosomal DNA and activates RNA polymerase I transcription. Nat Cell Biol 7, 303-310.
6. Atherton PJ & Smith K (2012). Muscle protein synthesis in response to nutrition and exercise. J Physiol 590, 1049-1057.
7. Baar K & Esser K (1999). Phosphorylation of p70(S6k) correlates with increased skeletal muscle mass following resistance exercise. Am J Physiol 276, C120-127.
8. Baehr LM, Tunzi M & Bodine SC (2014). Muscle hypertrophy is associated with increases in proteasome activity that is independent of MuRF1 and MAFbx expression. Front Physiol 5, 69.
9. Bickel CS, Slade J, Mahoney E, Haddad F, Dudley GA & Adams GR (2005). Time course of molecular responses of human skeletal muscle to acute bouts of resistance exercise. J Appl Physiol 98, 482-488.
10. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ & Yancopoulos GD (2001). Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3, 1014-1019.
11. Boon K, Caron HN, van Asperen R, Valentijn L, Hermus MC, van Sluis P, Roobeek I, Weis I, Voute PA, Schwab M & Versteeg R (2001). N-myc enhances the expression of a large set of genes functioning in ribosome biogenesis and protein synthesis. EMBO J 20, 1383-1393.
12. Brook MS, Wilkinson DJ, Mitchell WK, Lund JN, Szewczyk NJ, Greenhaff PL, Smith K & Atherton PJ (2015). Skeletal muscle hypertrophy adaptations predominate in the early stages of resistance exercise training, matching deuterium oxide-derived measures of muscle protein synthesis and mechanistic target of rapamycin complex 1 signaling. FASEB J 29, 4485-4496.
13. Carlson ME, Hsu M & Conboy IM (2008). Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature 454, 528-532.
14. Chaillou T, Kirby TJ & McCarthy JJ (2014). Ribosome biogenesis: emerging evidence for a central role in the regulation of skeletal muscle mass. J Cell Physiol 33, 474-483.
15. Chauvin C, Koka V, Nouschi A, Mieulet V, Hoareau-Aveilla C, Dreazen A, Cagnard N, Carpentier W, Kiss T, Meyuhas O & Pende M (2014). Ribosomal protein S6 kinase activity controls the ribosome biogenesis transcriptional program. Oncogene 229, 1584-1594.
16. Chesley A, MacDougall JD, Tarnopolsky MA, Atkinson SA & Smith K (1992). Changes in human muscle protein synthesis after resistance exercise. J Appl Physiol 73, 1383-1388.
17. Drummond MJ, Fry CS, Glynn EL, Dreyer HC, Dhanani S, Timmerman KL, Volpi E & Rasmussen BB (2009). Rapamycin administration in humans blocks the contraction-induced increase in skeletal muscle protein synthesis. J Physiol 587, 1535-1546.
18. Figueiredo VC, Caldow MK, Massie V, Markworth JF, Cameron-Smith D & Blazevich AJ (2015). Ribosome biogenesis adaptation in resistance training-induced human skeletal muscle hypertrophy. Am J. Physiol Endocrinol Metab 309, E72-82.
19. Fluckey JD, Vary TC, Jefferson LS & Farrell PA (1996). Augmented insulin action on rates of protein synthesis after resistance exercise in rats. Am J Physiol 270, E313-319.
20. Glover EI, Oates BR, Tang JE, Moore DR, Tarnopolsky MA & Phillips SM (2008). Resistance exercise decreases eIF2Bepsilon phosphorylation and potentiates the feeding-induced stimulation of p70S6K1 and rpS6 in young men. Am J Physiol Regul Integr Comp Physiol 295, R604-610.
21. 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, R533-540.
22. Gomes AV, Waddell DS, Siu R, Stein M, Dewey S, Furlow JD & Bodine SC (2012). Upregulation of proteasome activity in muscle RING finger 1-null mice following denervation. FASEB J 26, 2986-2999.
23. Goodman CA, Mabrey DM, Frey JW, Miu MH, Schmidt EK, Pierre P & Hornberger TA (2011). Novel insights into the regulation of skeletal muscle protein synthesis as revealed by a new nonradioactive in vivo technique. FASEB J 25, 1028-1039.
24. Grandori C, Gomez-Roman N, Felton-Edkins ZA, Ngouenet C, Galloway DA, Eisenman RN & White RJ (2005). c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nat Cell Biol 7, 311-318.
25. 3 regulation in controlling skeletal muscle mass in response to resistance exercise. PloS one 5, e11624.
26. Hamosch M, Lesch M, Baron J & Kaufman S (1967). Enhanced protein synthesis in a cell-free system from hypertrophied skeletal muscle. Science 157, 935-937.
27. Hannan KM, Brandenburger Y, Jenkins A, Sharkey K, Cavanaugh A, Rothblum L, Moss T, Poortinga G, McArthur GA, Pearson RB & Hannan RD (2003). mTOR-dependent regulation of ribosomal gene transcription requires S6K1 and is mediated by phosphorylation of the carboxy-terminal activation domain of the nucleolar transcription factor UBF. Mol Cell Biol 23, 8862-8877.
28. Hernandez-Verdun D (2006). The nucleolus: a model for the organization of nuclear functions. Histochem Cell Biol 126, 135-148.
29. Holz MK, Ballif BA, Gygi SP & Blenis J (2005). mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 123, 569-580.
30. Hornberger TA & Chien S (2006). Mechanical stimuli and nutrients regulate rapamycin-sensitive signaling through distinct mechanisms in skeletal muscle. J Cell Biochem 97, 1207-1216.
31. Hornberger TA, Stuppard R, Conley KE, Fedele MJ, Fiorotto ML, Chin ER & Esser KA (2004). Mechanical stimuli regulate rapamycin-sensitive signalling by a phosphoinositide 3-kinase-, protein kinase B- and growth factor-independent mechanism. Biochem J 380, 795-804.
32. Huang MJ, Cheng YC, Liu CR, Lin S & Liu HE (2006). A small-molecule c-Myc inhibitor, 10058-F4, induces cell-cycle arrest, apoptosis, and myeloid differentiation of human acute myeloid leukemia. Exp Hematol 34, 1480-1489.
33. Hwee DT, Baehr LM, Philp A, Baar K & Bodine SC (2014). Maintenance of muscle mass and load-induced growth in Muscle RING Finger 1 null mice with age. Aging Cell 13, 92-101.
34. Jager S, Groll M, Huber R, Wolf DH & Heinemeyer W (1999). Proteasome beta-type subunits: unequal roles of propeptides in core particle maturation and a hierarchy of active site function. J Mol Biol 291, 997-1013.
35. Jastrzebski K, Hannan KM, Tchoubrieva EB, Hannan RD & Pearson RB (2007). Coordinate regulation of ribosome biogenesis and function by the ribosomal protein S6 kinase, a key mediator of mTOR function. Growth Factors 25, 209-226.
36. Kang SA, Pacold ME, Cervantes CL, Lim D, Lou HJ, Ottina K, Gray NS, Turk BE, Yaffe MB & Sabatini DM (2013). mTORC1 phosphorylation sites encode their sensitivity to starvation and rapamycin. Science 341, 1236566.
37. Kimball SR & Jefferson LS (2010). Control of translation initiation through integration of signals generated by hormones, nutrients, and exercise. J Biol Chem 285, 29027-29032.
38. Kubica N, Bolster DR, Farrell PA, Kimball SR & Jefferson LS (2005). Resistance exercise increases muscle protein synthesis and translation of eukaryotic initiation factor 2Bε mRNA in a mammalian target of rapamycin-dependent manner. J Biol Chem 280, 7570-7580.
39. Kwon H & Green MR (1994). The RNA polymerase I transcription factor, upstream binding factor, interacts directly with the TATA box-binding protein. J Biol Chem 269, 30140-30146.
40. Lee SJ (2004). Regulation of muscle mass by myostatin. Ann Rev Cell Devel Biol 20, 61-86.
41. Lee SJ (2010). Extracellular regulation of myostatin: a molecular rheostat for muscle mass. Immunol Endocr Metab Agents Med Chem 10, 183-194.
42. Li Z & Hann SR (2013). Nucleophosmin is essential for c-Myc nucleolar localization and c-Myc-mediated rDNA transcription. Oncogene 32, 1988-1994.
43. T Method. Methods 25, 402-408.
44. MacKenzie MG, Hamilton DL, Pepin M, Patton A & Baar K (2013). Inhibition of myostatin signaling through Notch activation following acute resistance exercise. PloS one 8, e68743.
45. Maggi LB, Jr, Kuchenruether M, Dadey DY, Schwope RM, Grisendi S, Townsend RR, Pandolfi PP & Weber JD (2008). Nucleophosmin serves as a rate-limiting nuclear export chaperone for the mammalian ribosome. Mol Cell Biol 28, 7050-7065.
46. Marshall A, Salerno MS, Thomas M, Davies T, Berry C, Dyer K, Bracegirdle J, Watson T, Dziadek M, Kambadur R, Bower R & Sharma M (2008). Mighty is a novel promyogenic factor in skeletal myogenesis. Exp Cell Res 314, 1013-1029.
47. Mayhew DL, Hornberger TA, Lincoln HC & Bamman MM (2011). Eukaryotic initiation factor 2B epsilon induces cap-dependent translation and skeletal muscle hypertrophy. J Physiol 589, 3023-3037.
48. McPherron AC & Lee SJ (1997). Double muscling in cattle due to mutations in the myostatin gene. Proc Natl Acad Sci USA 94, 12457-12461.
49. Morton CC, Brown JA, Holmes WM, Nance WE & Wolf B (1983). Stain intensity of human nucleolus organizer region reflects incorporation of uridine into mature ribosomal RNA. Exp Cell Res 145, 405-413.
50. I68, a subunit of TIF-IB/SL1, activates RNA polymerase I transcription. EMBO J 20, 1353-1362.
51. Nader GA, McLoughlin TJ & Esser KA (2005). mTOR function in skeletal muscle hypertrophy: increased ribosomal RNA via cell cycle regulators. Am J Physiol Cell Physiol 289, C1457-1465.
52. Olivier J, Johnson WD & Marshall GD (2008). The logarithmic transformation and the geometric mean in reporting experimental IgE results: what are they and when and why to use them? Ann Allergy Asthma Immunol 100, 333-337.
53. Osmulski PA & Gaczynska M (2013). Rapamycin allosterically inhibits the proteasome. Mol Pharmacol 84, 104-113.
54. Phillips BE, Williams JP, Gustafsson T, Bouchard C, Rankinen T, Knudsen S, Smith K, Timmons JA & Atherton PJ (2013). Molecular networks of human muscle adaptation to exercise and age. PLoS genetics 9, e1003389.
55. 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, E99-107.
56. Ploton D, Menager M, Jeannesson P, Himber G, Pigeon F & Adnet JJ (1986). Improvement in the staining and in the visualization of the argyrophilic proteins of the nucleolar organizer region at the optical level. Histochem J 18, 5-14.
57. Rock KL, Gramm C, Rothstein L, Clark K, Stein R, Dick L, Hwang D & Goldberg AL (1994). Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78, 761-771.
58. Rodriguez KA, Dodds SG, Strong R, Galvan V, Sharp ZD & Buffenstein R (2014). Divergent tissue and sex effects of rapamycin on the proteasome-chaperone network of old mice. Front Mol Neurosci 7, 83.
59. Sanij E, Poortinga G, Sharkey K, Hung S, Holloway TP, Quin J, Robb E, Wong LH, Thomas WG, Stefanovsky V, Moss T, Rothblum L, Hannan KM, McArthur GA, Pearson RB & Hannan RD (2008). UBF levels determine the number of active ribosomal RNA genes in mammals. J Cell Biol 183, 1259-1274.
60. Stefanovsky VY, Pelletier G, Hannan R, Gagnon-Kugler T, Rothblum LI & Moss T (2001). An immediate response of ribosomal transcription to growth factor stimulation in mammals is mediated by ERK phosphorylation of UBF. Mol Cell 8, 1063-1073.
61. Thoreen CC, Chantranupong L, Keys HR, Wang T, Gray NS & Sabatini DM (2012). A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 485, 109-113.
62. Trere D (2000). AgNOR staining and quantification. Micron 31, 127-131.
63. Voit R & Grummt I (2001). Phosphorylation of UBF at serine 388 is required for interaction with RNA polymerase I and activation of rDNA transcription. Proc Natl Acad Sci USA 98, 13631-13636.
64. Voit R, Kuhn A, Sander EE & Grummt I (1995). Activation of mammalian ribosomal gene transcription requires phosphorylation of the nucleolar transcription factor UBF. Nucleic Acids Res 23, 2593-2599.
65. Voit R, Schnapp A, Kuhn A, Rosenbauer H, Hirschmann P, Stunnenberg HG & Grummt I (1992). The nucleolar transcription factor mUBF is phosphorylated by casein kinase II in the C-terminal hyperacidic tail which is essential for transactivation. EMBO J 11, 2211-2218.
66. von Walden F, Casagrande V, Ostlund Farrants AK & Nader GA (2012). Mechanical loading induces the expression of a Pol I regulon at the onset of skeletal muscle hypertrophy. Am J Physiol Cell Physiol 302, C1523-1530.
67. Wang X, Li W, Williams M, Terada N, Alessi DR & Proud CG (2001). Regulation of elongation factor 2 kinase by p90(RSK1) and p70 S6 kinase. EMBO J 20, 4370-4379.
68. West DW, Kujbida GW, Moore DR, Atherton P, Burd NA, Padzik JP, De Lisio M, Tang JE, Parise G, Rennie MJ, Baker SK & Phillips SM (2009). Resistance exercise-induced increases in putative anabolic hormones do not enhance muscle protein synthesis or intracellular signalling in young men. J Physiol 587, 5239-5247.
69. Wong TS & Booth FW (1990a). Protein metabolism in rat gastrocnemius muscle after stimulated chronic concentric exercise. J Appl Physiol 69, 1709-1717.
70. Wong TS & Booth FW (1990b). Protein metabolism in rat tibialis anterior muscle after stimulated chronic eccentric exercise. J Appl Physiol 69, 1718-1724.
71. Young VR (1970). The role of skeletal and cardiac muscle in the regulation of protein metabolism. In Mammalian Protein Metabolism, ed. Munro HN, pp. 586-657. Academic Press, New York.