Impact of resistance exercise on ribosome biogenesis is acutely regulated by post-exercise recovery strategies

Physiological Reports

Volumn 4, Issue 2, 2016, Pages

  Figueiredo, Vandré C ^a   Roberts, Llion A ^b,c   Markworth, James F ^a   Barnett, Matthew P G ^d   Coombes, Jeff S ^b   Raastad, Truls ^e   Peake, Jonathan M ^c,f   Cameron Smith, David ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c QUEENSLAND ACADEMY OF SPORT   (Australia)

^d AGRESEARCH GRASSLANDS   (New Zealand)

^e NORWEGIAN SCHOOL OF SPORT SCIENCES   (Norway)

^f QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

Cyclin D1; Hypertrophy; Pre rRNA; Ribosomal RNA; Skeletal muscle; Upstream binding factor

Indexed keywords

CYCLIN D1; INITIATION FACTOR 1A; INITIATION FACTOR 4E; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; MYC PROTEIN; PROTEIN KINASE B; RIBOSOME RNA; RNA 18S; RNA 28S; RNA 5.8S; RNA POLYMERASE;

ADULT; ARTICLE; BIOGENESIS; CONTROLLED STUDY; CYCLING; EXERCISE RECOVERY; GENE EXPRESSION; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; MALE; MUSCLE BIOPSY; MUSCLE GROWTH; NORMAL HUMAN; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RESISTANCE TRAINING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RIBOSOME; RNA SYNTHESIS; TRANSCRIPTION REGULATION; WATER IMMERSION; WESTERN BLOTTING; YOUNG ADULT; COLD; CROSSOVER PROCEDURE; METABOLISM; PROCEDURES; RANDOMIZED CONTROLLED TRIAL; SKELETAL MUSCLE;

BLOTTING, WESTERN; COLD TEMPERATURE; CROSS-OVER STUDIES; HUMANS; MALE; MUSCLE, SKELETAL; RESISTANCE TRAINING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBOSOMES; YOUNG ADULT;

EID: 85004010215     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12670     Document Type: Article

References (39)

1. Alao, J. P. 2007. The regulation of cyclin D1 degradation: roles in cancer development and the potential for therapeutic invention. Mol. Cancer. 6:24
2. Ayrault, O., L. Andrique, D. Fauvin, B. Eymin, S. Gazzeri, and P. Seite. 2006. Human tumor suppressor p14ARF negatively regulates rRNA transcription and inhibits UBF1 transcription factor phosphorylation. Oncogene 25:7577-7586
3. Bleakley, C., S. McDonough, E. Gardner, G. D. Baxter, J. T. Hopkins, and G. W. Davison. 2012. Cold-water immersion (cryotherapy) for preventing and treating muscle soreness after exercise. Cochrane Database Syst. Rev. 2:CD008262
4. Chan, J. C., K. M. Hannan, K. Riddell, P. Y. Ng, A. Peck, R. S. Lee, et al. 2011. AKT promotes rRNA synthesis and cooperates with c-MYC to stimulate ribosome biogenesis in cancer. Sci. Signal. 4:ra56
5. Coulthard, L. R., D. E. White, D. L. Jones, M. F. McDermott, and S. A. Burchill. 2009. p38(MAPK): stress responses from molecular mechanisms to therapeutics. Trends Mol. Med. 15:369-379
6. Drakas, R., X. Tu, and R. Baserga. 2004. Control of cell size through phosphorylation of upstream binding factor 1 by nuclear phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. U. S. A. 101:9272-9276
7. Eisenberg, E., and E. Y. Levanon. 2013. Human housekeeping genes, revisited. Trends Genet. 29:569-574
8. Figueiredo, V. C., M. K. Caldow, V. Massie, J. F. Markworth, D. Cameron-Smith, and A. J. Blazevich. 2015. Ribosome biogenesis adaptation in resistance training-induced human skeletal muscle hypertrophy. Am. J. Physiol. Endocrinol. Metab. 309:E72-E83
9. Henras, A. K., C. Plisson-Chastang, M. F. O’Donohue, A. Chakraborty, and P. E. Gleizes. 2015. An overview of preribosomal RNA processing in eukaryotes. Wiley Interdiscip. Rev. RNA 6:225-242
10. Hisatake, K., T. Nishimura, Y. Maeda, K. Hanada, C. Z. Song, and M. Muramatsu. 1991. Cloning and structural analysis of cDNA and the gene for mouse transcription factor UBF. Nucleic Acids Res. 19:4631-4637
11. Kirby, T. J., J. D. Lee, J. H. England, T. Chaillou, K. A. Esser, and J. J. McCarthy. 2015. Blunted hypertrophic response in aged skeletal muscle is associated with decreased ribosome biogenesis. J. Appl. Physiol. (1985) 119:321-327
12. Kuhn, A., R. Voit, V. Stefanovsky, R. Evers, M. Bianchi, and I. Grummt. 1994. Functional differences between the two splice variants of the nucleolar transcription factor UBF: the second HMG box determines specificity of DNA binding and transcriptional activity. EMBO J. 13:416-424
13. Kusnadi, E. P., K. M. Hannan, R. J. Hicks, R. D. Hannan, R. B. Pearson, and J. Kang. 2015. Regulation of rDNA transcription in response to growth factors, nutrients and energy. Gene 556:27-34
14. Landon, A. L., P. A. Muniandy, A. C. Shetty, E. Lehrmann, L. Volpon, S. Houng, et al. 2014. MNKs act as a regulatory switch for eIF4E1 and eIF4E3 driven mRNA translation in DLBCL. Nat. Commun. 5:5413
15. Mamane, Y., E. Petroulakis, L. Rong, K. Yoshida, L. W. Ler, and N. Sonenberg. 2004. eIF4E-from translation to transformation. Oncogene 23:3172-3179
16. Moore, S. F., R. W. Hunter, and I. Hers. 2011. mTORC2 protein complex-mediated Akt (Protein Kinase B) Serine 473 Phosphorylation is not required for Akt1 activity in human platelets [corrected. J. Biol. Chem. 286:24553-24560
17. Moss, T., F. Langlois, T. Gagnon-Kugler, and V. Stefanovsky. 2007. A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis. Cell. Mol. Life Sci. 64:29-49
18. Nader, G. A., F. von Walden, C. Liu, J. Lindvall, L. Gutmann, E. E. Pistilli, et al. 2014. Resistance exercise training modulates acute gene expression during human skeletal muscle hypertrophy. J. Appl. Physiol. (1985) 116:693-702.
19. Nguyen le, X. T., and B. S. Mitchell. 2013. Akt activation enhances ribosomal RNA synthesis through casein kinase II and TIF-IA. Proc. Natl. Acad. Sci. U. S. A. 110:20681-20686
20. Obata, T., G. E. Brown, and M. B. Yaffe. 2000. MAP kinase pathways activated by stress: the p38 MAPK pathway. Crit. Care Med. 28:N67-N77.
21. O’Mahony, D. J., and L. I. Rothblum. 1991. Identification of two forms of the RNA polymerase I transcription factor UBF. Proc. Natl. Acad. Sci. U. S. A. 88:3180-3184
22. O’Mahony, D. J., W. Q. Xie, S. D. Smith, H. A. Singer, and L. I. Rothblum. 1992. Differential phosphorylation and localization of the transcription factor UBF in vivo in response to serum deprivation. In vitro dephosphorylation of UBF reduces its transactivation properties. J. Biol. Chem. 267:35-38
23. Panov, K. I., J. K. Friedrich, and J. C. Zomerdijk. 2001. A step subsequent to preinitiation complex assembly at the ribosomal RNA gene promoter is rate limiting for human RNA polymerase I-dependent transcription. Mol. Cell. Biol. 21:2641-2649
24. Roberts, L. A., T. Raastad, J. F. Markworth, V. C. Figueiredo, I. M. Egner, A. Shield, et al. 2015. Post-exercise cold water immersion attenuates acute anabolic signalling and longterm adaptations in muscle to strength training. J. Physiol. 593:4285-4301
25. Rosenwald, I. B., A. Lazaris-Karatzas, N. Sonenberg, and E. V. Schmidt. 1993. Elevated levels of cyclin D1 protein in response to increased expression of eukaryotic initiation factor 4E. Mol. Cell. Biol. 13:7358-7363
26. Russell, J., and J. C. Zomerdijk. 2005. RNA-polymerase-Idirected rDNA transcription, life and works. Trends Biochem. Sci. 30:87-96
27. Stec, M. J., D. L. Mayhew, and M. M. Bamman. 2015. The effects of age and resistance loading on skeletal muscle ribosome biogenesis. J. Appl. Physiol. (1985) 119:851-857
28. Topisirovic, I., M. Ruiz-Gutierrez, and K. L. Borden. 2004. Phosphorylation of the eukaryotic translation initiation factor eIF4E contributes to its transformation and mRNA transport activities. Cancer Res. 64:8639-8642
29. Vander Haar, E., S. I. Lee, S. Bandhakavi, T. J. Griffin, and D. H. Kim. 2007. Insulin signalling to mTOR mediated by the Akt/PKB substrate PRAS40. Nat. Cell Biol. 9:316-323
30. Vandesompele, J., K. De Preter, F. Pattyn, B. Poppe, N. Van Roy, A. De Paepe, et al. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3: RESEARCH0034
31. Vincent, E. E., D. J. Elder, E. C. Thomas, L. Phillips, C. Morgan, J. Pawade, et al. 2011. Akt phosphorylation on Thr308 but not on Ser473 correlates with Akt protein kinase activity in human non-small cell lung cancer. Br. J. Cancer 104:1755-1761
32. Voit, R., and I. Grummt. 2001. Phosphorylation of UBF at serine 388 is required for interaction with RNA polymerase I and activation of rDNA transcription. Proc. Natl. Acad. Sci. U. S. A. 98:13631-13636
33. Voit, R., A. Kuhn, E. E. Sander, and I. Grummt. 1995. Activation of mammalian ribosomal gene transcription requires phosphorylation of the nucleolar transcription factor UBF. Nucleic Acids Res. 23:2593-2599
34. Voit, R., M. Hoffmann, and I. Grummt. 1999. Phosphorylation by G1-specific cdk-cyclin complexes activates the nucleolar transcription factor UBF. EMBO J. 18:1891-1899.
35. von Walden, F., V. Casagrande, A. K. Ostlund Farrants, and G. A. Nader. 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
36. White, R. J. 2005. RNA polymerases I and III, growth control and cancer. Nat. Rev. Mol. Cell Biol. 6:69-78
37. Yamane, M., N. Ohnishi, and T. Matsumoto. 2015. Does regular post-exercise cold application attenuate trained muscle adaptation? Int. J. Sports Med. 36:647-653
38. Yanagisawa, O., M. Niitsu, H. Takahashi, K. Goto, and Y. Itai. 2003. Evaluations of cooling exercised muscle with MR imaging and 31P MR spectroscopy. Med. Sci. Sports Exerc. 35:1517-1523
39. Zhao, J., X. Yuan, M. Frodin, and I. Grummt. 2003. ERKdependent phosphorylation of the transcription initiation factor TIF-IA is required for RNA polymerase I transcription and cell growth. Mol. Cell 11:405-413.