Alcohol Intoxication Following Muscle Contraction in Mice Decreases Muscle Protein Synthesis But Not mTOR Signal Transduction

Alcoholism: Clinical and Experimental Research

Volumn 39, Issue 1, 2015, Pages 1-10

  Steiner, Jennifer L ^a   Lang, Charles H ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Anabolic Signaling; Electrical Stimulation; Ethanol; S6K1; Skeletal Muscle Metabolism

Indexed keywords

ALCOHOL; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MITOGEN ACTIVATED PROTEIN KINASE; MUSCLE PROTEIN; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; TARGET OF RAPAMYCIN KINASE;

ALCOHOL INTOXICATION; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINGE DRINKING; CONTROLLED STUDY; ELECTROSTIMULATION; GASTROCNEMIUS MUSCLE; MALE; MOUSE; MUSCLE CONTRACTION; MUSCLE METABOLISM; NONHUMAN; PLANTARIS MUSCLE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RNA TRANSLATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; ANIMAL; BIOSYNTHESIS; DRUG EFFECTS; METABOLISM; PHYSIOLOGY;

MAMMALIA; MUS;

ALCOHOLIC INTOXICATION; ANIMALS; ELECTRIC STIMULATION; MALE; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; MULTIPROTEIN COMPLEXES; MUSCLE CONTRACTION; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84921458936     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/acer.12600     Document Type: Article

References (40)

1. Anjum R, Blenis J (2008) The RSK family of kinases: emerging roles in cellular signalling. Nat Rev Mol Cell Biol 9:747-758.
2. Areta JL, Burke LM, Ross ML, Camera DM, West DW, Broad EM, Jeacocke NA, Moore DR, Stellingwerff T, Phillips SM, Hawley JA, Coffey VG (2013) Timing and distribution of protein ingestion during prolonged recovery from resistance exercise alters myofibrillar protein synthesis. J Physiol 591:2319-2331.
3. Atherton PJ, Babraj J, Smith K, Singh J, Rennie MJ, Wackerhage H (2005) Selective activation of AMPK-PGC-1alpha or PKB-TSC2-mTOR signaling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimulation. FASEB J 19:786-788.
4. Baar K, Esser K (1999) Phosphorylation of p70(S6k) correlates with increased skeletal muscle mass following resistance exercise. Am J Physiol 276:C120-C127.
5. 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.
6. Browne GJ, Proud CG (2002) Regulation of peptide-chain elongation in mammalian cells. Eur J Biochem 269:5360-5368.
7. Carrière A, Cargnello M, Julien LA, Gao H, Bonneil E, Thibault P, Roux PP (2008) Oncogenic MAPK signaling stimulates mTORC1 activity by promoting RSK-mediated raptor phosphorylation. Curr Biol 18:1269-1277.
8. Chen MM, Palmer JL, Ippolito JA, Curtis BJ, Choudhry MA, Kovacs EJ (2013) Intoxication by intraperitoneal injection or oral gavage equally potentiates postburn organ damage and inflammation. Mediators Inflamm 2013:971481.
9. Doig J, Griffiths LA, Peberdy D, Dharmasaroja P, Vera M, Davies FJ, Newbery HJ, Brownstein D, Abbott CM (2013) In vivo characterization of the role of tissue-specific translation elongation factor 1A2 in protein synthesis reveals insights into muscle atrophy. FEBS J 280:6528-6540.
10. 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.
11. Gingras AC, Raught B, Gygi SP, Niedzwiecka A, Miron M, Burley SK, Polakiewicz RD, Wyslouch-Cieszynska A, Aebersold R, Sonenberg N (2001) Hierarchical phosphorylation of the translation inhibitor 4E-BP1. Genes Dev 15:2852-2864.
12. 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.
13. Hong-Brown LQ, Brown CR, Huber DS, Lang CH (2007) Alcohol regulates eukaryotic elongation factor 2 phosphorylation via an AMP-activated protein kinase-dependent mechanism in C2C12 skeletal myocytes. J Biol Chem 282:3702-3712.
14. 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.
15. Jensen CJ, Buch MB, Krag TO, Hemmings BA, Gammeltoft S, Frödin M (1999) 90-kDa ribosomal S6 kinase is phosphorylated and activated by 3-phosphoinositide-dependent protein kinase-1. J Biol Chem 274:27168-27176.
16. Jørgensen R, Merrill AR, Andersen GR (2006) The life and death of translation elongation factor 2. Biochem Soc Trans 34:1-6.
17. Kubica N, Bolster DR, Farrell PA, Kimball SR, Jefferson LS (2005) Resistance exercise increases muscle protein synthesis and translation of eukaryotic initiation factor 2Bepsilon mRNA in a mammalian target of rapamycin-dependent manner. J Biol Chem 280:7570-7580.
18. Kumar V, Frost RA, Lang CH (2002) Alcohol impairs insulin and IGF-I stimulation of S6K1 but not 4E-BP1 in skeletal muscle. Am J Physiol Endocrinol Metab 283:E917-E928.
19. Lang CH, Frost RA (2006) Glucocorticoids and TNFalpha interact cooperatively to mediate sepsis-induced leucine resistance in skeletal muscle. Mol Med 12:291-299.
20. Lang CH, Frost RA, Deshpande N, Kumar V, Vary TC, Jefferson LS, Kimball SR (2003) Alcohol impairs leucine-mediated phosphorylation of 4E-BP1, S6K1, eIF4G, and mTOR in skeletal muscle. Am J Physiol Endocrinol Metab 285:E1205-E1215.
21. Lang CH, Frost RA, Kumar V, Wu D, Vary TC (2000) Impaired protein synthesis induced by acute alcohol intoxication is associated with changes in eIF4E in muscle and eIF2B in liver. Alcohol Clin Exp Res 24:322-331.
22. Lang CH, Kimball SR, Frost RA, Vary TC (2001) Alcohol myopathy: impairment of protein synthesis and translation initiation. Int J Biochem Cell Biol 33:457-473.
23. Lang CH, Lynch CJ, Vary TC (2010a) Alcohol-induced IGF-I resistance is ameliorated in mice deficient for mitochondrial branched-chain aminotransferase. J Nutr 140:932-938.
24. Lang CH, Lynch CJ, Vary TC (2010b) BCATm deficiency ameliorates endotoxin-induced decrease in muscle protein synthesis and improves survival in septic mice. Am J Physiol Regul Integr Comp Physiol 299:R935-R944.
25. Lang CH, Pruznak AM, Deshpande N, Palopoli MM, Frost RA, Vary TC (2004) Alcohol intoxication impairs phosphorylation of S6K1 and S6 in skeletal muscle independently of ethanol metabolism. Alcohol Clin Exp Res 28:1758-1767.
26. Lang CH, Pruznak AM, Nystrom GJ, Vary TC (2009) Alcohol-induced decrease in muscle protein synthesis associated with increased binding of mTOR and raptor: comparable effects in young and mature rats. Nutr Metab (Lond) 6:4.
27. 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.
28. Magnuson B, Ekim B, Fingar DC (2012) Regulation and function of ribosomal protein S6 kinase (S6K) within mTOR signalling networks. Biochem J 441:1-21.
29. Mothe-Satney I, Brunn GJ, McMahon LP, Capaldo CT, Abraham RT, Lawrence JC (2000) Mammalian target of rapamycin-dependent phosphorylation of PHAS-I in four (S/T)P sites detected by phospho-specific antibodies. J Biol Chem 275:33836-33843.
30. Parr EB, Camera DM, Areta JL, Burke LM, Phillips SM, Hawley JA, Coffey VG (2014) Alcohol ingestion impairs maximal post-exercise rates of myofibrillar protein synthesis following a single bout of concurrent training. PLoS ONE 9:e88384.
31. Roux PP, Ballif BA, Anjum R, Gygi SP, Blenis J (2004) Tumor-promoting phorbol esters and activated Ras inactivate the tuberous sclerosis tumor suppressor complex via p90 ribosomal S6 kinase. Proc Natl Acad Sci U S A 101:13489-13494.
32. Roux PP, Shahbazian D, Vu H, Holz MK, Cohen MS, Taunton J, Sonenberg N, Blenis J (2007) RAS/ERK signaling promotes site-specific ribosomal protein S6 phosphorylation via RSK and stimulates cap-dependent translation. J Biol Chem 282:14056-14064.
33. Ryder JW, Fahlman R, Wallberg-Henriksson H, Alessi DR, Krook A, Zierath JR (2000) Effect of contraction on mitogen-activated protein kinase signal transduction in skeletal muscle. Involvement of the mitogen- and stress-activated protein kinase 1. J Biol Chem 275:1457-1462.
34. Shahbazian D, Roux PP, Mieulet V, Cohen MS, Raught B, Taunton J, Hershey JW, Blenis J, Pende M, Sonenberg N (2006) The mTOR/PI3K and MAPK pathways converge on eIF4B to control its phosphorylation and activity. EMBO J 25:2781-2791.
35. Sneddon AA, Koll M, Wallace MC, Jones J, Miell JP, Garlick PJ, Preedy VR (2003) Acute alcohol administration inhibits the refeeding response after starvation in rat skeletal muscle. Am J Physiol Endocrinol Metab 284:E874-E882.
36. Sutherland C, Campbell DG, Cohen P (1993) Identification of insulin-stimulated protein kinase-1 as the rabbit equivalent of rskmo-2. Identification of two threonines phosphorylated during activation by mitogen-activated protein kinase. Eur J Biochem 212:581-588.
37. Vary TC, Lang CH (2008) Differential phosphorylation of translation initiation regulators 4EBP1, S6k1, and Erk 1/2 following inhibition of alcohol metabolism in mouse heart. Cardiovasc Toxicol 8:23-32.
38. 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.
39. Widegren U, Ryder JW, Zierath JR (2001) Mitogen-activated protein kinase signal transduction in skeletal muscle: effects of exercise and muscle contraction. Acta Physiol Scand 172:227-238.
40. Zaru R, Ronkina N, Gaestel M, Arthur JS, Watts C (2007) The MAPK-activated kinase Rsk controls an acute Toll-like receptor signaling response in dendritic cells and is activated through two distinct pathways. Nat Immunol 8:1227-1235.