Ribosome biogenesis adaptation in resistance training-induced human skeletal muscle hypertrophy

American Journal of Physiology - Endocrinology and Metabolism

Volumn 309, Issue 1, 2015, Pages E72-E83

  Figueiredo, Vandre C ^a   Caldow, Marissa K ^b   Massie, Vivien ^c   Markworth, James F ^a   Cameron Smith, David ^a   Blazevich, Anthony J ^c  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c EDITH COWAN UNIVERSITY   (Australia)

Author keywords

Cyclin D1; Ribosomal RNA; Transcription initiation factor 1A; Upstream binding protein

Indexed keywords

BINDING PROTEIN; CYCLIN D1; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE INTERACTING KINASE 1; POLYMERASE RNA I POLYPEPTIDE B; RIBOSOME PROTEIN; RIBOSOME RNA; RNA POLYMERASE; S6 KINASE; S6 RIBOSOMAL PROTEIN 1; TRANSCRIPTION FACTOR; TRANSCRIPTION INITIATION FACTOR 1A; UNCLASSIFIED DRUG; UPSTREAM BINDING PROTEIN;

ADAPTATION; ADULT; ARTICLE; BIOGENESIS; BODY COMPOSITION; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; DUAL ENERGY X RAY ABSORPTIOMETRY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; MALE; MUSCLE HYPERTROPHY; MUSCLE LEVEL; NORMAL HUMAN; PRIORITY JOURNAL; QUADRICEPS FEMORIS MUSCLE; REAL TIME POLYMERASE CHAIN REACTION; RESISTANCE TRAINING; RIBOSOME; RIBOSOME SUBUNIT; TRANSLATION INITIATION; ADOLESCENT; ENERGY METABOLISM; HYPERTROPHY; METABOLISM; PATHOLOGY; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL; REST; RNA TRANSLATION; SKELETAL MUSCLE; YOUNG ADULT;

ADAPTATION, PHYSIOLOGICAL; ADOLESCENT; ADULT; ENERGY METABOLISM; HUMANS; HYPERTROPHY; MALE; METABOLIC NETWORKS AND PATHWAYS; MUSCLE, SKELETAL; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; RESISTANCE TRAINING; REST; RIBOSOMES; YOUNG ADULT;

EID: 84935488816     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00050.2015     Document Type: Article

References (45)

1. Atherton PJ, Smith K. Muscle protein synthesis in response to nutrition and exercise. J Physiol 590: 1049–1057, 2012.
2. Bianchini A, Loiarro M, Bielli P, Busa R, Paronetto MP, Loreni F, Geremia R, Sette C. Phosphorylation of eIF4E by MNKs supports protein synthesis, cell cycle progression and proliferation in prostate cancer cells. Carcinogenesis 29: 2279–2288, 2008.
3. Blattner C, Jennebach S, Herzog F, Mayer A, Cheung AC, Witte G, Lorenzen K, Hopfner KP, Heck AJ, Aebersold R, Cramer P. Molecular basis of Rrn3-regulated RNA polymerase I initiation and cell growth. Genes Dev 25: 2093–2105, 2011.
4. Chamousset D, Mamane S, Boisvert FM, Trinkle-Mulcahy L. Efficient extraction of nucleolar proteins for interactome analyses. Proteomics 10: 3045–3050, 2010.
5. Coffey VG, Zhong Z, Shield A, Canny BJ, Chibalin AV, Zierath JR, Hawley JA. Early signaling responses to divergent exercise stimuli in skeletal muscle from well-trained humans. FASEB J 20: 190–192, 2006.
6. Drummond MJ, Dreyer HC, Fry CS, Glynn EL, Rasmussen BB. Nutritional and contractile regulation of human skeletal muscle protein synthesis and mTORC1 signaling. J Appl Physiol (1985) 106: 1374–1384, 2009.
7. Drygin D, Rice WG, Grummt I. The RNA polymerase I transcription machinery: an emerging target for the treatment of cancer. Annu Rev Pharmacol Toxicol 50: 131–156, 2010.
8. Gelinas JN, Banko JL, Hou L, Sonenberg N, Weeber EJ, Klann E, Nguyen PV. ERK and mTOR signaling couple beta-adrenergic receptors to translation initiation machinery to gate induction of protein synthesis-dependent long-term potentiation. J Biol Chem 282: 27527–27535, 2007.
9. Goodman CA, Frey JW, Mabrey DM, Jacobs BL, Lincoln HC, You JS, Hornberger TA. The role of skeletal muscle mTOR in the regulation of mechanical load-induced growth. J Physiol 589: 5485–5501, 2011.
10. Grummt I. Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev 17: 1691–1702, 2003.
11. Guo Y, Stacey DW, Hitomi M. Post-transcriptional regulation of cyclin D1 expression during G2 phase. Oncogene 21: 7545–7556, 2002.
12. Iadevaia V, Liu R, Proud CG. mTORC1 signaling controls multiple steps in ribosome biogenesis. Semin Cell Dev Biol 36: 113–120, 2014.
13. Iijima Y, Laser M, Shiraishi H, Willey CD, Sundaravadivel B, Xu L, McDermott PJ, Kuppuswamy D. c-Raf/MEK/ERK pathway controls protein kinase C-mediated p70S6K activation in adult cardiac muscle cells. J Biol Chem 277: 23065–23075, 2002.
14. Kim PL, Staron RS, Phillips SM. Fasted-state skeletal muscle protein synthesis after resistance exercise is altered with training. J Physiol 568: 283–290, 2005.
15. Kiyatkin A, Aksamitiene E. Multistrip western blotting to increase quantitative data output. Methods Mol Biol 536: 149–161, 2009.
16. Knudsen KE, Diehl JA, Haiman CA, Knudsen ES. Cyclin D1: polymorphism, aberrant splicing and cancer risk. Oncogene 25: 1620–1628, 2006.
17. Kopp K, Gasiorowski JZ, Chen D, Gilmore R, Norton JT, Wang C, Leary DJ, Chan EK, Dean DA, Huang S. Pol I transcription and pre-rRNA processing are coordinated in a transcription-dependent manner in mammalian cells. Mol Biol Cell 18: 394–403, 2007.
18. Mane VP, Heuer MA, Hillyer P, Navarro MB, Rabin RL. Systematic method for determining an ideal housekeeping gene for real-time PCR analysis. J Biomol Tech 19: 342–347, 2008.
19. McCarthy JJ, Esser KA. Anabolic and catabolic pathways regulating skeletal muscle mass. Curr Opin Clin Nutr Metab Care 13: 230–235, 2010.
20. Miller G, Panov KI, Friedrich JK, Trinkle-Mulcahy L, Lamond AI, Zomerdijk JC. hRRN3 is essential in the SL1-mediated recruitment of RNA Polymerase I to rRNA gene promoters. EMBO J 20: 1373–1382, 2001.
21. Moss T, Langlois F, Gagnon-Kugler T, Stefanovsky V. A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis. Cell Mol Life Sci 64: 29–49, 2007.
22. Muise-Helmericks RC, Grimes HL, Bellacosa A, Malstrom SE, Tsi-chlis PN, Rosen N. Cyclin D expression is controlled post-transcription-ally via a phosphatidylinositol 3-kinase/Akt-dependent pathway. J Biol Chem 273: 29864–29872, 1998.
23. Mullineux ST, Lafontaine DL. Mapping the cleavage sites on mammalian pre-rRNAs: where do we stand? Biochimie 94: 1521–1532, 2012.
24. Nader GA, von Walden F, Liu C, Lindvall J, Gutmann L, Pistilli EE, Gordon PM. Resistance exercise training modulates acute gene expression during human skeletal muscle hypertrophy. J Appl Physiol (1985) 116: 693–702, 2014.
25. Ogasawara R, Kobayashi K, Tsutaki A, Lee K, Abe T, Fujita S, Nakazato K, Ishii N. mTOR signaling response to resistance exercise is altered by chronic resistance training and detraining in skeletal muscle. J Appl Physiol 114: 934–940, 2013.
26. O’Mahony DJ, Smith SD, Xie W, Rothblum LI. Analysis of the phosphorylation, DNA-binding and dimerization properties of the RNA polymerase I transcription factors UBF1 and UBF2. Nucleic Acids Res 20: 1301–1308, 1992.
27. O’Sullivan AC, Sullivan GJ, McStay B. UBF binding in vivo is not restricted to regulatory sequences within the vertebrate ribosomal DNA repeat. Mol Cell Biol 22: 657–668, 2002.
28. Phillips SM. A brief review of critical processes in exercise-induced muscular hypertrophy. Sports Med 44, Suppl 1: S71–S77, 2014.
29. Rosenwald IB, Lazaris-Karatzas A, Sonenberg N, Schmidt EV. Elevated levels of cyclin D1 protein in response to increased expression of eukaryotic initiation factor 4E. Mol Cell Biol 13: 7358–7363, 1993.
30. Roux PP, Shahbazian D, Vu H, Holz MK, Cohen MS, Taunton J, Sonenberg N, Blenis J. RAS/ERK signaling promotes site-specific ribo-somal protein S6 phosphorylation via RSK and stimulates cap-dependent translation. J Biol Chem 282: 14056–14064, 2007.
31. 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. UBF levels determine the number of active ribosomal RNA genes in mammals. J Cell Biol 183: 1259–1274, 2008.
32. Stepanchick A, Zhi H, Cavanaugh AH, Rothblum K, Schneider DA, Rothblum LI. DNA binding by the ribosomal DNA transcription factor rrn3 is essential for ribosomal DNA transcription. J Biol Chem 288: 9135–9144, 2013.
33. Strandberg S, Wretling ML, Wredmark T, Shalabi A. Reliability of computed tomography measurements in assessment of thigh muscle cross-sectional area and attenuation. BMC Med Imaging 10: 18, 2010.
34. Thoreen CC, Chantranupong L, Keys HR, Wang T, Gray NS, Saba-tini DM. A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 485: 109–113, 2012.
35. Topisirovic I, Ruiz-Gutierrez M, Borden KL. Phosphorylation of the eukaryotic translation initiation factor eIF4E contributes to its transformation and mRNA transport activities. Cancer Res 64: 8639–8642, 2004.
36. Voit R, Grummt I. 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, 2001.
37. Voit R, Hoffmann M, Grummt I. Phosphorylation by G1-specific cdk-cyclin complexes activates the nucleolar transcription factor UBF. EMBO J 18: 1891–1899, 1999.
38. von Walden F, Casagrande V, Östlund Farrants AK, Nader GA. 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, 2012.
39. Wang X, Proud CG. The mTOR pathway in the control of protein synthesis. Physiology (Bethesda) 21: 362–369, 2006.
40. Wilkinson SB, Phillips SM, Atherton PJ, Patel R, Yarasheski KE, Tarnopolsky MA, Rennie MJ. Differential effects of resistance and endurance exercise in the fed state on signalling molecule phosphorylation and protein synthesis in human muscle. J Physiol 586: 3701–3717, 2008.
41. Wilson DN, Doudna Cate JH. The structure and function of the eukary-otic ribosome. Cold Spring Harb Perspect Biol 4: pii: a011536, 2012.
42. Yang W, Xu Y, Wu J, Zeng W, Shi Y. Solution structure and DNA binding property of the fifth HMG box domain compared with the first HMG box domain in human upstream binding factor. Biochemistry 42: 1930–1938, 2003.
43. Young VR. The role of skeletal and cardiac muscle in the regulation of protein metabolism. In: Mammalian Protein Metabolism, edited by Munro HN. New York: Academic, 1970, p. 585–674.
44. Zhang Z, Liu R, Townsend PA, Proud CG. 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, 2013.
45. Zhao J, Yuan X, Frodin M, Grummt I. ERK-dependent phosphorylation of the transcription initiation factor TIF-IA is required for RNA polymer-ase I transcription and cell growth. Mol Cell 11: 405–413, 2003.