Publication Cover
Stress
The International Journal on the Biology of Stress
Volume 18, 2015 - Issue 6
794
Views
23
CrossRef citations to date
0
Altmetric
Original Research Report

Glucocorticoids retard skeletal muscle development and myoblast protein synthesis through a mechanistic target of rapamycin (mTOR)-signaling pathway in broilers (Gallus gallus domesticus)

, , , &
Pages 686-698 | Received 15 Apr 2015, Accepted 12 Aug 2015, Published online: 21 Aug 2015

References

  • Anthony JC, Anthony TG, Kimball SR, Jefferson LS. (2001). Signaling pathways involved in translational control of protein synthesis in skeletal muscle by leucine. J Nutr 13:856S–60
  • Aoki M, Blazek E, Vogt PK. (2001). A role of the kinase mTOR in cellular transformation induced by the oncoproteins PI3k and Akt. Proc Natl Acad Sci USA 98:136–41
  • Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, et al. (2001). Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3:1014–19
  • Bolster DR, Jefferson LS, Kimball SR. (2004). Regulation of protein synthesis associated with skeletal muscle hypertrophy by insulin-, amino acid-and exercise-induced signaling. Proc Nutr Soc 63:351–6
  • Browne GJ, Finn SG, Proud CG. (2004). Stimulation of the AMP-activated protein kinase leads to activation of eukaryotic elongation factor 2 kinase and to its phosphorylation at a novel site, serine 398. J Biol Chem 279:12220–31
  • Cheng SW, Fryer LG, Carling D, Shepherd PR. (2004). Thr2446 is a novel mammalian target of rapamycin (mTOR) phosphorylation site regulated by nutrient status. J Biol Chem 2004;279:15719–22
  • Close B, Banister K, Baumans V, Bernoth EM, Bromage N, Bunyan J, Erhardt W, et al. (1997). Recommendations for euthanasia of experimental animals: part 2. DGXT of the European Commission. Lab Anim 31:1–32
  • Crozier SJ, Kimball SR, Emmert SW, Anthony JC, Jefferson LS. (2005). Oral leucine administration stimulates protein synthesis in rat skeletal muscle. J Nutr 135:376–82
  • Deldicque L, Theisen D, Francaux M. (2005). Regulation of mTOR by amino acids and resistance exercise in skeletal muscle. Eur J Appl Physiol 94:1–10
  • Dennis PB, Fumagalli S, Thomas G. (1999). Target of Rapamycin (TOR): balancing the opposing forces of protein synthesis and degradation. Curr Opin Genet Dev 9:49–54
  • Dong H, Lin H, Jiao HC, Song ZG, Zhao JP, Jiang KJ. (2007). Altered development and protein metabolism in skeletal muscle of broiler chichens (Gallus gallus domesticus) by corticosterone. Comp Biochem Physiol A Mol Integr Physiol 147:A189–95
  • Deng D, Yao K, Chu WY, Li TJ, Huang RL, Yin YL, Liu HQ, et al. (2009). Impaired translation initiation activation and reduced protein synthesis in weaned piglets fed a low-protein diet. J Nutr Biochem 20:544–52
  • Duan Y, Li F, Liu H, Li Y, Liu Y, Kong X, Zhang Y, et al. (2015). Nutritional and regulatory roles of leucine in muscle growth and fat reduction. Front Biosci (Landmark Ed) 20:796–813
  • Duchêne S, Métayer S, Audouin E, Bigot K, Dupont J, Tesseraud S. (2008). Refeeding and insulin activate the AKT/p70S6 kinase pathway without affecting IRS1 tyrosine phosphorylation in chicken muscle. Domest Anim Endocrinol 34:1–13
  • Dupont J, Dagou C, Derouet M, Simon J, Taouis M. (2004). Early steps of insulin receptor signaling in chicken and rat: apparent refractoriness in chicken muscle. Domest Anim Endocrinol 26:127–42
  • Dupont J, Tesseraud S, Derouet M, Collin A, Rideau N, Crochet S, Godet E, et al. (2008). Insulin immuno-neutralization in chicken: effects on insulin signaling and gene expression in liver and muscle. J Endocrinol 197:531–42
  • Fingar DC, Richardson CJ, Tee AR, Cheatham L, Tsou C, Blenis J. (2004). mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E. Mol Cell Biol 24:200–16
  • Gao X, Zhang Y, Arrazola P, Hino O, Kobayashi T, Yeung RS, Ru B, Pan D. (2002). Tsc tumour suppressor proteins antagonize amino-acid-TOR signalling. Nat Cell Biol 4:699–704
  • Goodman CA, Mabrey DM, Frey JW, Miu MH, Schmidt EK, Pierre P. (2011). Novel insights into the regulation of skeletal muscle protein synthesis as revealed by a new nonradioactive in vivo technique. FASEB J 25:1028–39
  • Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ. (2008). AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30:214–26
  • Halevy O, Geyra A, Barak M, Uni Z, Sklan D. (2000). Early posthatch starvation decreases statellite cell proliferation and skeletal muscle growth in chicks. J Nutr 130:858–64
  • Hawley SA, Pan DA, Mustard KJ, Ross L, Bain J, Edelman AM, Frenguelli BG, Hardie DG. (2005). Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab 2:9–19
  • Inoki K, Corradetti MN, Guan KL. (2005). Dysregulation of the TSC-mTOR pathway in human disease. Nat Genet 37:19–24
  • Kimball SR, Jefferson LS. (2006). Signaling pathways and molecular mechanisms through which branched-chain amino acids mediate translational control of protein synthesis. J Nutr 136:227S–31
  • Kimball SR, Shantz LM, Horetsky RL, Jefferson LS. (1999). Leucine regulates translation of specific mRNAs in L6 myoblasts through mTOR-mediated changes in Availability of eIF4E and phosphorylation of ribosomal protein S6. J Biol Chem 274:11647–52
  • Kimura N, Tokunaga C, Dalal S, Richardson C, Yoshino K, Hara K, Kemp BE, et al. (2003). A possible linkage between AMP-activated protein kinase (AMPK) and mammalian target of rapamycin (mTOR) signalling pathway. Genes Cells 1:65–79
  • Kong X, Wang X, Yin Y, Li X, Gao H, Bazer FW, Wu G. (2014). Putrescine stimulates the mTOR signaling pathway and protein synthesis in porcine trophectoderm cells. Biol Reprod 91:106
  • Laemmli UK. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–5
  • Li F, Yin Y, Tan B, Kong X, Wu G. (2011). Leucine nutrition in animals and humans: mTOR signaling and beyond. Amino Acids 41:1185–93
  • Lin H, Decuypere E, Buyse J. (2004a). Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus) 1. Chronic exposure. Comp Biochem Physiol B Biochem Mol Biol 139:B737–44
  • Lin H, Decuypere E, Buyse J. (2004b). Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus) 2. Short-term effect. Comp Biochem Physiol B Biochem Mol Biol 139:B745–51
  • Lin H, Sui SJ, Jiao HC, Buyse J, Decuypere E. (2006). Impaired development of broiler chickens by stress mimicked by corticosterone exposure. Comp Biochem Physiol A Mol Integr Physiol 143:A400–5
  • Livak KJ, Schmittgen TD. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delta][Delta]CT method. Methods 25:402–8
  • Long W, Wei L, Barrett EJ. (2001). Dexamethasone inhibits the stimulation of muscle protein synthesis and PHAS-I and p70S6-kinase phosphorylation. Am J Physiol Endocrinol Metab 280:E570–5
  • Matteri RL, Carroll JA, Dyer CJ. (2000). Neuroendocrine responses to stress. The biology of animal stress. Wallingford, Oxon, UK: CAB International. p 43–56
  • Mayer C, Grummt I. (2006). Ribosome biogenesis and cell growth: mTOR coordinates transcription by all three classes of nuclear RNA polymerases. Oncogene 25:6384–91
  • Munck A, Guyre PM, Holbrook NJ. (1984). Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr Rev 5:25–44
  • Nakano K, Hara H. (1979). Measurement of the protein-synthetic activity in vivo of various tissues in rats by using [3H] Puromycin. Biochem J 184:663–8
  • Post J, Rebel JM, ter Huurne AA. (2003). Physiological effects of elevated plasma corticosterone concentrations in broiler chickens, an alternative means by which to assess the physiological effects of stress. Poult Sci 82:1313–18
  • Price SR, Du J, Bailey JL, Mitch WE. (2001). Molecular mechanisms regulating protein turnover in muscle. Am J Kidney Dis 37:S112–14
  • Proszkowiec-Weglarz M, Richards MP, Ramachandran R, McMurtry JP. (2006). Characterization of the AMP-activated protein kinase pathway in chickens. Comp Biochem Physiol B Biochem Mol Biol 143:B92–106
  • Rannels DE, Rannels SR, Li JB, Pegg AE, Morgan HE, Jefferson LS. (1980). Effects of glucocorticoids on peptide chain initiation in heart and skeletal muscle. Adv Myocardiol 1:493–501
  • Schmidt EK, Clavarino G, Ceppi M, Pierre P. (2009). SUnSET, a nonradioactive method to monitor protein synthesis. Nat Methods 6:275–7
  • Shah OJ, Anthony JC, Kimball SR, Jefferson LS. (2000a). Glucocorticoids oppose translational control by leucine in skeletal muscle. Am J Physiol Endocrinol Metab 279:E1185–90
  • Shah OJ, Kimball SR, Jefferson LS. (2000b). Acute attenuation of translation initiation and protein synthesis by glucocorticoids in skeletal muscle. Am J Physiol Endocrinol Metab 278:E76–82
  • Shah OJ, Kimball SR, Jefferson LS. (2000c). Glucocorticoids abate p70(S6k) and eIF4E function in L6 skeletal myoblasts. Am J Physiol Endocrinol Metab 279:E74–82
  • Shah OJ, Kimball SR, Jefferson LS. (2000d). Among translational effecters, p70(S6k) is uniquely sensitive to inhibition by glucocorticoids. Biochem J 347:389–97
  • Shimizu N, Yoshikawa N, Ito N, Maruyama T, Suzuki Y, Takeda S, Nakae J, et al. (2011). Crosstalk between glucocorticoid receptor and nutritional sensor mTOR in skeletal muscle. Cell Metab 13:170–82
  • Southorn BG, Palmer RM, Garlick PJ. (1990). Acute effects of corticosterone on tissue protein synthesis and insulin sensitivity in rats in vivo. Biochem J 272:187–91
  • Tsiotra PC, Tsigos C. (2006). Stress, the endoplasmic reticulum, and insulin resistance. Ann N Y Acad Sci 1083:63–76
  • Wang H, Kubica N, Ellisen LW, Jefferson LS, Kimball SR. (2006). Dexametasone represses signaling through the mammalian target of rapamycin in muscle cells by enhancing expression of REDD1. J Biol Chem 282:25604–12
  • Wang XJ, Song ZG, Jiao HC, Lin H. (2012a). Skeletal muscle fatty acids shift from oxidation to storage upon dexamethasone treatment in chickens. Gen Comp Endocrinol 179:319–30
  • Wang XJ, Song ZG, Jiao HC, Lin H. (2012b). Dexamethasone facilitates lipid accumulation in chicken skeletal muscle. Stress 15:443–56
  • Wang XJ, Wei DL, Song ZG, Jiao HC, Lin H. (2012c). Effects of fatty acid treatments on the dexamethasone-induced intramuscular lipid accumulation in chickens. PLoS One 7:e36663
  • Woods A, Dickerson K, Heath R, Hong SP, Momcilovic M, Johnstone SR, Carlson M, Carling D. (2005). Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2:21–33
  • Yablonka-Reuveni Z, Nameroff M. (1987). Skeletal muscle cell populations. Separation and partial characterization of fibroblast-like cells from embryonic tissue using density centrifugation. Histochemistry 87:27–38
  • Yang H, Yin Y. (2012). Chemerin regulates proliferation and differentiation of myoblast cells via ERK1/2 and mTOR signaling pathways. Cytokine 60:646–52
  • Yao K, Yin YL, Chu WY, Liu ZQ, Dun D, Li TJ, Huang RL, et al. (2008). Dietary arginine supplementation increases mTOR signaling activity in skeletal muscle of neonatal Pigs. J Nutr 138:867–72
  • Yin J, Liu M, Ren W, Duan J, Yang G, Zhao Y, Fang R, et al. (2015). Effects of dietary supplementation with glutamate and aspartate on diquat-induced oxidative stress in piglets. PLoS One 10:e0122893
  • Yin YL, Yao K, Liu ZJ, Gong M, Ruan Z, Deng D, Tan BE, et al. (2010). Supplementing L-leucine to a low-protein diet increases tissue protein synthesis in weanling pigs. Amino Acids 39:1477–86
  • Zhao JP, Lin H, Jiao HC, Song ZG. (2009). Corticosterone suppresses insulin-and NO-stimulated muscle glucose uptake in broiler chickens (Gallus gallus domesticus). Comp Biochem Physiol C Toxicol Pharmacol 49:448–54

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.