Ribosome Biogenesis: Emerging Evidence for a Central Role in the Regulation of Skeletal Muscle Mass

Journal of Cellular Physiology

Volumn 229, Issue 11, 2014, Pages 1584-1594

  Chaillou, Thomas ^a,b   Kirby, Tyler J ^a,b   Mccarthy, John J ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MYC PROTEIN; WNT PROTEIN;

ARTICLE; BIOGENESIS; BIOSYNTHESIS; CACHEXIA; CATABOLISM; HUMAN; MUSCLE ATROPHY; MUSCLE CONTRACTILITY; MUSCLE CONTRACTION; MUSCLE DENERVATION; MUSCLE MASS; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTEIN SYNTHESIS REGULATION; RIBOSOME; RNA TRANSLATION; SARCOPENIA; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ANIMALS; HUMANS; MUSCLE, SKELETAL; ORGAN SIZE; RIBOSOMES; SIGNAL TRANSDUCTION;

EID: 84904865507     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24604     Document Type: Article

References (125)

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-C1195.
2. Alawi F, Lee MN. 2007. DKC1 is a direct and conserved transcriptional target of c-MYC. Biochem Biophys Res Commun 362:893-898.
3. 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.
4. Armstrong DD, Esser KA. 2005. Wnt/beta-catenin signaling activates growth-control genes during overload-induced skeletal muscle hypertrophy. Am J Physiol Cell Physiol 289:C853-C859.
5. Armstrong DD, Wong VL, Esser KA. 2006. Expression of beta-catenin is necessary for physiological growth of adult skeletal muscle. Am J Physiol Cell Physiol 291:C185-C188.
6. Aschenbach WG, Ho RC, Sakamoto K, Fujii N, Li Y, Kim YB, Hirshman MF, Goodyear LJ. 2006. Regulation of dishevelled and beta-catenin in rat skeletal muscle: An alternative exercise-induced GSK-3beta signaling pathway. Am J Physiol Endocrinol Metab 291:E152-E158.
7. Baar K, Esser K. 1999. Phosphorylation of p70(S6k) correlates with increased skeletal muscle mass following resistance exercise. Am J Physiol 276:C120-C127.
8. Babij P, Booth FW. 1988. Alpha-actin and cytochrome c mRNAs in atrophied adult rat skeletal muscle. Am J Physiol 254:C651-C656.
9. Ben-Ze'ev A, Shtutman M, Zhurinsky J. 2000. The integration of cell adhesion with gene expression: The role of beta-catenin. Exp Cell Res 261:75-82.
10. Bentzinger CF, Lin S, Romanino K, Castets P, Guridi M, Summermatter S, Handschin C, Tintignac LA, Hall MN, Ruegg MA. 2013. Differential response of skeletal muscles to mTORC1 signaling during atrophy and hypertrophy. Skelet Muscle 3:6.
11. Bickel CS, Slade JM, Haddad F, Adams GR, Dudley GA. 2003. Acute molecular responses of skeletal muscle to resistance exercise in able-bodied and spinal cord-injured subjects. J Appl Physiol 94:2255-2262.
12. Boisvert FM, van Koningsbruggen S, Navascues J, Lamond AI. 2007. The multifunctional nucleolus. Nat Rev Mol Cell Biol 8:574-585.
13. Chaillou T, Koulmann N, Simler N, Meunier A, Serrurier B, Chapot R, Peinnequin A, Beaudry M, Bigard X. 2012. Hypoxia transiently affects skeletal muscle hypertrophy in a functional overload model. Am J Physiol Regul Integr Comp Physiol 302:R643-R654.
14. Chaillou T, Lee JD, England JH, Esser KA, McCarthy JJ. 2013. Time course of gene expression during mouse skeletal muscle hypertrophy. J Appl Physiol 115:1065-1074.
15. Chen Y, Sood S, Biada J, Roth R, Rabkin R. 2008. Increased workload fully activates the blunted IRS-1/PI3-kinase/Akt signaling pathway in atrophied uremic muscle. Kidney Int 73:848-855.
16. Chen Y, Sood S, McIntire K, Roth R, Rabkin R. 2011. Leucine-stimulated mTOR signaling is partly attenuated in skeletal muscle of chronically uremic rats. Am J Physiol Endocrinol Metab 301:E873-E881.
17. Coller HA, Grandori C, Tamayo P, Colbert T, Lander ES, Eisenman RN, Golub TR. 2000. Expression analysis with oligonucleotide microarrays reveals that MYC regulates genes involved in growth, cell cycle, signaling, and adhesion. Proc Natl Acad Sci USA 97:3260-3265.
18. Constantin D, McCullough J, Mahajan RP, Greenhaff PL. 2011. Novel events in the molecular regulation of muscle mass in critically ill patients. J Physiol 589:3883-3895.
19. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA. 1995. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378:785-789.
20. Csibi A, Cornille K, Leibovitch MP, Poupon A, Tintignac LA, Sanchez AM, Leibovitch SA. 2010. The translation regulatory subunit eIF3f controls the kinase-dependent mTOR signaling required for muscle differentiation and hypertrophy in mouse. PLoS ONE 5:e8994.
21. Dapp C, Schmutz S, Hoppeler H, Fluck M. 2004. Transcriptional reprogramming and ultrastructure during atrophy and recovery of mouse soleus muscle. Physiol Genomics 20:97-107.
22. de Boer MD, Selby A, Atherton P, Smith K, Seynnes OR, Maganaris CN, Maffulli N, Movin T, Narici MV, Rennie MJ. 2007. The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. J Physiol 585:241-251.
23. Drummond MJ, Dickinson JM, Fry CS, Walker DK, Gundermann DM, Reidy PT, Timmerman KL, Markofski MM, Paddon-Jones D, Rasmussen BB, Volpi E. 2012. Bed rest impairs skeletal muscle amino acid transporter expression, mTORC1 signaling, and protein synthesis in response to essential amino acids in older adults. Am J Physiol Endocrinol Metab 302:E1113-E1122.
24. Farnfield MM, Breen L, Carey KA, Garnham A, Cameron-Smith D. 2012. Activation of mTOR signalling in young and old human skeletal muscle in response to combined resistance exercise and whey protein ingestion. Applied physiology, nutrition, and metabolism = Physiologie appliquee. Nutr Metab 37:21-30.
25. Favier FB, Costes F, Defour A, Bonnefoy R, Lefai E, Bauge S, Peinnequin A, Benoit H, Freyssenet D. 2010. Downregulation of Akt/mammalian target of rapamycin pathway in skeletal muscle is associated with increased REDD1 expression in response to chronic hypoxia. Am J Physiol Regul Integr Comp Physiol 298:R1659-R1666.
26. Fry CS, Drummond MJ, Glynn EL, Dickinson JM, Gundermann DM, Timmerman KL, Walker DK, Dhanani S, Volpi E, Rasmussen BB. 2011. Aging impairs contraction-induced human skeletal muscle mTORC1 signaling and protein synthesis. Skelet Muscle 1:11.
27. Gamrin L, Berg HE, Essen P, Tesch PA, Hultman E, Garlick PJ, McNurlan MA, Wernerman J. 1998. The effect of unloading on protein synthesis in human skeletal muscle. Acta Physiol Scand 163:369-377.
28. Gebauer F, Hentze MW. 2004. Molecular mechanisms of translational control. Nat Rev Mol Cell Biol 5:827-835.
29. Gibson JN, Halliday D, Morrison WL, Stoward PJ, Hornsby GA, Watt PW, Murdoch G, Rennie MJ. 1987. Decrease in human quadriceps muscle protein turnover consequent upon leg immobilization. Clin Sci (Lond) 72:503-509.
30. Gibson JN, Smith K, Rennie MJ. 1988. Prevention of disuse muscle atrophy by means of electrical stimulation: Maintenance of protein synthesis. Lancet 2:767-770.
31. Gilbert WV. 2011. Functional specialization of ribosomes?. Trends Biochem Sci 36:127-132.
32. Glover EI, Oates BR, Tang JE, Moore DR, Tarnopolsky MA, Phillips SM. 2008a. 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-R610.
33. Glover EI, Phillips SM, Oates BR, Tang JE, Tarnopolsky MA, Selby A, Smith K, Rennie MJ. 2008b. Immobilization induces anabolic resistance in human myofibrillar protein synthesis with low and high dose amino acid infusion. J Physiol 586:6049-6061.
34. Goldspink DF. 1976. The effects of denervation on protein turnover of rat skeletal muscle. Biochem J 156:71-80.
35. Gomez-Roman N, Grandori C, Eisenman RN, White RJ. 2003. Direct activation of RNA polymerase III transcription by c-Myc. Nature 421:290-294.
36. Gomez-Roman N, Felton-Edkins ZA, Kenneth NS, Goodfellow SJ, Athineos D, Zhang J, Ramsbottom BA, Innes F, Kantidakis T, Kerr ER, Brodie J, Grandori C, White RJ. 2006. Activation by c-Myc of transcription by RNA polymerases I, II and III. Biochem Soc Symp 73:141-154.
37. Goodfellow SJ, Innes F, Derblay LE, MacLellan WR, Scott PH, White RJ. 2006. Regulation of RNA polymerase III transcription during hypertrophic growth. EMBO J 25:1522-1533.
38. Goodman CA, Frey JW, Mabrey DM, Jacobs BL, Lincoln HC, You JS, Hornberger TA. 2011. The role of skeletal muscle mTOR in the regulation of mechanical load-induced growth. J Physiol 589:5485-5501.
39. Gordon BS, Kelleher AR, Kimball SR. 2013. Regulation of muscle protein synthesis and the effects of catabolic states. Int J Biochem Cell Biol 45:2147-2157.
40. 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.
41. Granneman S, Tollervey D. 2007. Building ribosomes: Even more expensive than expected?. Curr Biol 17:R415-R417.
42. Haddad F, Adams GR. 2006. Aging-sensitive cellular and molecular mechanisms associated with skeletal muscle hypertrophy. J Appl Physiol 100:1188-1203.
43. Haddad F, Roy RR, Zhong H, Edgerton VR, Baldwin KM. 2003. Atrophy responses to muscle inactivity. I. Cellular markers of protein deficits. J Appl Physiol 95:781-790.
44. Haddad F, Baldwin KM, Tesch PA. 2005. Pretranslational markers of contractile protein expression in human skeletal muscle: Effect of limb unloading plus resistance exercise. J Appl Physiol 98:46-52.
45. Hannan RD, Luyken J, Rothblum LI. 1996. Regulation of ribosomal DNA transcription during contraction-induced hypertrophy of neonatal cardiomyocytes. J Biol Chem 271:3213-3220.
46. 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.
47. Harrington D, Anker SD, Chua TP, Webb-Peploe KM, Ponikowski PP, Poole-Wilson PA, Coats AJ. 1997. Skeletal muscle function and its relation to exercise tolerance in chronic heart failure. J Am Coll Cardiol 30:1758-1764.
48. Heinemeier KM, Olesen JL, Haddad F, Schjerling P, Baldwin KM, Kjaer M. 2009. Effect of unloading followed by reloading on expression of collagen and related growth factors in rat tendon and muscle. J Appl Physiol 106:178-186.
49. Held WA, Mizushima S, Nomura M. 1973. Reconstitution of Escherichia coli 30 S ribosomal subunits from purified molecular components. J Biol Chem 248:5720-5730.
50. Henras AK, Soudet J, Gerus M, Lebaron S, Caizergues-Ferrer M, Mougin A, Henry Y. 2008. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell Mol Life Sci 65:2334-2359.
51. Hinoi T, Yamamoto H, Kishida M, Takada S, Kishida S, Kikuchi A. 2000. Complex formation of adenomatous polyposis coli gene product and axin facilitates glycogen synthase kinase-3 beta-dependent phosphorylation of beta-catenin and down-regulates beta-catenin. J Biol Chem 275:34399-34406.
52. Hulmi JJ, Tannerstedt J, Selanne H, Kainulainen H, Kovanen V, Mero AA. 2009. Resistance exercise with whey protein ingestion affects mTOR signaling pathway and myostatin in men. J Appl Physiol 106:1720-1729.
53. Hwee DT, Bodine SC. 2009. Age-related deficit in load-induced skeletal muscle growth. J Gerontol Ser A 64:618-628.
54. Iadevaia V, Huo Y, Zhang Z, Foster LJ, Proud CG. 2012. Roles of the mammalian target of rapamycin, mTOR, in controlling ribosome biogenesis and protein synthesis. Biochem Soc Trans 40:168-172.
55. Jefferies HB, Reinhard C, Kozma SC, Thomas G. 1994. Rapamycin selectively represses translation of the "polypyrimidine tract" mRNA family. Proc Natl Acad Sci USA 91:4441-4445.
56. Jefferies HB, Fumagalli S, Dennis PB, Reinhard C, Pearson RB, Thomas G. 1997. Rapamycin suppresses 5′TOP mRNA translation through inhibition of p70s6k. EMBO J 16:3693-3704.
57. Kantidakis T, Ramsbottom BA, Birch JL, Dowding SN, White RJ. 2010. MTOR associates with TFIIIC, is found at tRNA and 5S rRNA genes, and targets their repressor Maf1. Proc Natl Acad Sci USA 107:11823-11828.
58. Kapp LD, Lorsch JR. 2004. The molecular mechanics of eukaryotic translation. Annu Rev Biochem 73:657-704.
59. Kelleher AR, Kimball SR, Dennis MD, Schilder RJ, Jefferson LS. 2013. The mTORC1 signaling repressors REDD1/2 are rapidly induced and activation of p70S6K1 by leucine is defective in skeletal muscle of an immobilized rat hindlimb. Am J Physiol Endocrinol Metab 304:E229-E236.
60. Kim S, Li Q, Dang CV, Lee LA. 2000. Induction of ribosomal genes and hepatocyte hypertrophy by adenovirus-mediated expression of c-Myc in vivo. Proc Natl Acad Sci USA 97:11198-11202.
61. Kirn-Safran CB, Oristian DS, Focht RJ, Parker SG, Vivian JL, Carson DD. 2007. Global growth deficiencies in mice lacking the ribosomal protein HIP/RPL29. Dev Dyn 236:447-460.
62. Kondrashov N, Pusic A, Stumpf CR, Shimizu K, Hsieh AC, Xue S, Ishijima J, Shiroishi T, Barna M. 2011. Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell 145:383-397.
63. Kumar V, Selby A, Rankin D, Patel R, Atherton P, Hildebrandt W, Williams J, Smith K, Seynnes O, Hiscock N, Rennie MJ. 2009. Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. J Physiol 587:211-217.
64. Lang CH, Frost RA, Vary TC. 2007. Regulation of muscle protein synthesis during sepsis and inflammation. Am J Physiol Endocrinol Metab 293:E453-E459.
65. Lang SM, Kazi AA, Hong-Brown L, Lang CH. 2012. Delayed recovery of skeletal muscle mass following hindlimb immobilization in mTOR heterozygous mice. PLoS ONE 7:e38910.
66. 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 18:39-51.
67. Li L, Yuan H, Weaver CD, Mao J, Farr GH, III, Sussman DJ, Jonkers J, Kimelman D, Wu D. 1999. Axin and Frat1 interact with dvl and GSK, bridging Dvl to GSK in Wnt-mediated regulation of LEF-1. EMBO J 18:4233-4240.
68. Lindstrom MS. 2009. Emerging functions of ribosomal proteins in gene-specific transcription and translation. Biochem Biophys Res Commun 379:167-170.
69. Machida M, Takeda K, Yokono H, Ikemune S, Taniguchi Y, Kiyosawa H, Takemasa T. 2012. Reduction of ribosome biogenesis with activation of the mTOR pathway in denervated atrophic muscle. J Cell Physiol 227:1569-1576.
70. Magnusson C, Svensson A, Christerson U, Tagerud S. 2005. Denervation-induced alterations in gene expression in mouse skeletal muscle. Eur J Neurosci 21:577-580.
71. Mauro VP, Edelman GM. 2007. The ribosome filter redux. Cell Cycle 6:2246-2251.
72. Mayer C, Zhao J, Yuan X, Grummt I. 2004. MTOR-dependent activation of the transcription factor TIF-IA links rRNA synthesis to nutrient availability. Genes Dev 18:423-434.
73. 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.
74. Meyer N, Penn LZ. 2008. Reflecting on 25 years with MYC. Nat Rev Cancer 8:976-990.
75. Miyazaki M, McCarthy JJ, Fedele MJ, Esser KA. 2011. Early activation of mTORC1 signalling in response to mechanical overload is independent of phosphoinositide 3-kinase/Akt signalling. J Physiol 589:1831-1846.
76. Montanaro L, Trere D, Derenzini M. 2012. Changes in ribosome biogenesis may induce cancer by down-regulating the cell tumor suppressor potential. Biochim Biophys Acta 1825:101-110.
77. Moss T, Stefanovsky VY. 1995. Promotion and regulation of ribosomal transcription in eukaryotes by RNA polymerase I. Prog Nucleic Acid Res Mol Biol 50:25-66.
78. Moss T, Langlois F, Gagnon-Kugler T, Stefanovsky V. 2007. A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis. Cell Mol Life Sci 64:29-49.
79. 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-C1465.
80. Nader GA, von Walden F, Liu C, Lindvall J, Gutmann L, Pistilli EE, Gordon PM. 2014. Resistance exercise training modulates acute gene expression during human skeletal muscle hypertrophy. J Appl Physiol.
81. Nierhaus KH, Dohme F. 1974. Total reconstitution of functionally active 50S ribosomal subunits from Escherichia coli. Proc Natl Acad Sci USA 71:4713-4717.
82. Novak A, Dedhar S. 1999. Signaling through beta-catenin and Lef/Tcf. Cell Mol Life Sci 56:523-537.
83. Olson AK, Ledee D, Iwamoto K, Kajimoto M, O'Kelly Priddy C, Isern N, Portman MA. 2013. C-Myc induced compensated cardiac hypertrophy increases free fatty acid utilization for the citric acid cycle. J Mol Cell Cardiol 55:156-164.
84. Orellana RA, Wilson FA, Gazzaneo MC, Suryawan A, Davis TA, Nguyen HV. 2011. Sepsis and development impede muscle protein synthesis in neonatal pigs by different ribosomal mechanisms. Pediatr Res 69:473-478.
85. Pehme A, Alev K, Kaasik P, Seene T. 2004. Age-related changes in skeletal-muscle myosin heavy-chain composition: Effect of mechanical loading. J Aging Phys Act 12:29-44.
86. Pende M, Um SH, Mieulet V, Sticker M, Goss VL, Mestan J, Mueller M, Fumagalli S, Kozma SC, Thomas G. 2004. S6K1(-/-)/S6K2(-/-) mice exhibit perinatal lethality and rapamycin-sensitive 5′-terminal oligopyrimidine mRNA translation and reveal a mitogen-activated protein kinase-dependent S6 kinase pathway. Mol Cell Biol 24:3112-3124.
87. Petersson B, Wernerman J, Waller SO, von der Decken A, Vinnars E. 1990. Elective abdominal surgery depresses muscle protein synthesis and increases subjective fatigue: Effects lasting more than 30 days. Br J Surg 77:796-800.
88. Phillips SM, Glover EI, Rennie MJ. 2009. Alterations of protein turnover underlying disuse atrophy in human skeletal muscle. J Appl Physiol 107:645-654.
89. 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 Genet 9:e1003389.
90. Quy PN, Kuma A, Pierre P, Mizushima N. 2013. Proteasome-dependent activation of mammalian target of rapamycin complex 1 (mTORC1) is essential for autophagy suppression and muscle remodeling following denervation. J Biol Chem 288:1125-1134.
91. Reiter AK, Bolster DR, Crozier SJ, Kimball SR, Jefferson LS. 2008. AMPK represses TOP mRNA translation but not global protein synthesis in liver. Biochem Biophys Res Commun 374:345-350.
92. Rodnina MV, Wintermeyer W. 2009. Recent mechanistic insights into eukaryotic ribosomes. Curr Opin Cell Biol 21:435-443.
93. Ruvinsky I, Sharon N, Lerer T, Cohen H, Stolovich-Rain M, Nir T, Dor Y, Zisman P, Meyuhas O. 2005. Ribosomal protein S6 phosphorylation is a determinant of cell size and glucose homeostasis. Genes Dev 19:2199-2211.
94. Ruvinsky I, Katz M, Dreazen A, Gielchinsky Y, Saada A, Freedman N, Mishani E, Zimmerman G, Kasir J, Meyuhas O. 2009. Mice deficient in ribosomal protein S6 phosphorylation suffer from muscle weakness that reflects a growth defect and energy deficit. PLoS ONE 4:e5618.
95. Schakman O, Kalista S, Bertrand L, Lause P, Verniers J, Ketelslegers JM, Thissen JP. 2008. Role of Akt/GSK-3beta/beta-catenin transduction pathway in the muscle anti-atrophy action of insulin-like growth factor-I in glucocorticoid-treated rats. Endocrinology 149:3900-3908.
96. Schiaffino S, Dyar KA, Ciciliot S, Blaauw B, Sandri M. 2013. Mechanisms regulating skeletal muscle growth and atrophy. FEBS J 280:4294-4314.
97. Schlosser I, Holzel M, Murnseer M, Burtscher H, Weidle UH, Eick D. 2003. A role for c-Myc in the regulation of ribosomal RNA processing. Nucleic Acids Res 31:6148-6156.
98. Schols AM, Broekhuizen R, Weling-Scheepers CA, Wouters EF. 2005. Body composition and mortality in chronic obstructive pulmonary disease. Am J Clin Nutr 82:53-59.
99. Schuhmacher M, Staege MS, Pajic A, Polack A, Weidle UH, Bornkamm GW, Eick D, Kohlhuber F. 1999. Control of cell growth by c-Myc in the absence of cell division. Curr Biol 9:1255-1258.
100. Shor B, Wu J, Shakey Q, Toral-Barza L, Shi C, Follettie M, Yu K. 2010. Requirement of the mTOR kinase for the regulation of Maf1 phosphorylation and control of RNA polymerase III-dependent transcription in cancer cells. J Biol Chem 285:15380-15392.
101. Sions JM, Tyrell CM, Knarr BA, Jancosko A, Binder-Macleod SA. 2012. Age- and stroke-related skeletal muscle changes: A review for the geriatric clinician. J Geriatr Phys Ther 35:155-161.
102. Siu PM, Alway SE. 2005. Mitochondria-associated apoptotic signalling in denervated rat skeletal muscle. J Physiol 565:309-323.
103. Sun H, Li M, Gong L, Liu M, Ding F, Gu X. 2012. ITRAQ-coupled 2D LC-MS/MS analysis on differentially expressed proteins in denervated tibialis anterior muscle of Rattus norvegicus. Mol Cell Biochem 364:193-207.
104. Teng T, Thomas G, Mercer CA. 2013. Growth control and ribosomopathies. Curr Opin Genet Dev 23:63-71.
105. Thomas GM, Frame S, Goedert M, Nathke I, Polakis P, Cohen P. 1999. A GSK3-binding peptide from FRAT1 selectively inhibits the GSK3-catalysed phosphorylation of axin and beta-catenin. FEBS Lett 458:247-251.
106. Thomason DB, Booth FW. 1990. Atrophy of the soleus muscle by hindlimb unweighting. J Appl Physiol 68:1-12.
107. Thomson DM, Gordon SE. 2006. Impaired overload-induced muscle growth is associated with diminished translational signalling in aged rat fast-twitch skeletal muscle. J Physiol 574:291-305.
108. Thomson E, Ferreira-Cerca S, Hurt E. 2013. Eukaryotic ribosome biogenesis at a glance. J Cell Sci 126:4815-4821.
109. Thorrez L, Van Deun K, Tranchevent LC, Van Lommel L, Engelen K, Marchal K, Moreau Y, Van Mechelen I, Schuit F. 2008. Using ribosomal protein genes as reference: a tale of caution. PLoS ONE 3:e1854.
110. Tsang CK, Liu H, Zheng XF. 2010. MTOR binds to the promoters of RNA polymerase I- and III-transcribed genes. Cell Cycle 9:953-957.
111. Upadhya R, Lee J, Willis IM. 2002. Maf1 is an essential mediator of diverse signals that repress RNA polymerase III transcription. Mol Cell 10:1489-1494.
112. van Riggelen J, Yetil A, Felsher DW. 2010. MYC as a regulator of ribosome biogenesis and protein synthesis. Nat Rev Cancer 10:301-309.
113. Volarevic S, Stewart MJ, Ledermann B, Zilberman F, Terracciano L, Montini E, Grompe M, Kozma SC, Thomas G. 2000. Proliferation, but not growth, blocked by conditional deletion of 40S ribosomal protein S6. Science 288:2045-2047.
114. von Maltzahn J, Bentzinger CF, Rudnicki MA. 2012. Wnt7a-Fzd7 signalling directly activates the Akt/mTOR anabolic growth pathway in skeletal muscle. Nat Cell Biol 14:186-191.
115. 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-C1530.
116. Warner JR. 1999. The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 24:437-440.
117. Wei Y, Zheng XF. 2009. Sch9 partially mediates TORC1 signaling to control ribosomal RNA synthesis. Cell Cycle 8:4085-4090.
118. White JP, Baynes JW, Welle SL, Kostek MC, Matesic LE, Sato S, Carson JA. 2011. The regulation of skeletal muscle protein turnover during the progression of cancer cachexia in the Apc(Min/+) mouse. PLoS ONE 6:e24650.
119. Williams JP, Phillips BE, Smith K, Atherton PJ, Rankin D, Selby AL, Liptrot S, Lund J, Larvin M, Rennie MJ. 2012. Effect of tumor burden and subsequent surgical resection on skeletal muscle mass and protein turnover in colorectal cancer patients. Am J Clin Nutr 96:1064-1070.
120. Woolford JL, Jr., Baserga SJ. 2013. Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics 195:643-681.
121. Wu CH, Sahoo D, Arvanitis C, Bradon N, Dill DL, Felsher DW. 2008. Combined analysis of murine and human microarrays and ChIP analysis reveals genes associated with the ability of MYC to maintain tumorigenesis. PLoS Genet 4:e1000090.
122. Xue S, Barna M. 2012. Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat Rev Mol Cell Biol 13:355-369.
123. Zeller KI, Zhao X, Lee CW, Chiu KP, Yao F, Yustein JT, Ooi HS, Orlov YL, Shahab A, Yong HC, Fu Y, Weng Z, Kuznetsov VA, Sung WK, Ruan Y, Dang CV, Wei CL. 2006. Global mapping of c-Myc binding sites and target gene networks in human B cells. Proc Natl Acad Sci USA 103:17834-17839.
124. Zhang Z, Liu R, Townsend PA, Proud CG. 2013. P90(RSK)s mediate the activation of ribosomal RNA synthesis by the hypertrophic agonist phenylephrine in adult cardiomyocytes. J Mol Cell Cardiol 59:139-147.
125. Zinzalla V, Stracka D, Oppliger W, Hall MN. 2011. Activation of mTORC2 by association with the ribosome. Cell 144:757-768.