Adding protein to a carbohydrate supplement provided after endurance exercise enhances 4E-BP1 and RPS6 signaling in skeletal muscle

Journal of Applied Physiology

Volumn 104, Issue 4, 2008, Pages 1029-1036

  Morrison, Paul J ^a   Hara, Daisuke ^a   Ding, Zhenping ^a   Ivy, John L ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Amino acids; Carbohydrates; Insulin; Mammalian target of rapamycin; Signal transduction

Indexed keywords

AMINO ACID; CARBOHYDRATE; INITIATION FACTOR 4E BINDING PROTEIN 1; INSULIN; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; PLACEBO; S6 KINASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE INTAKE; CONTROLLED STUDY; ENDURANCE; ENZYME PHOSPHORYLATION; EXERCISE; GLUCOSE BLOOD LEVEL; IMMUNOBLOTTING; INSULIN BLOOD LEVEL; MALE; NONHUMAN; NUTRITION; PRIORITY JOURNAL; PROTEIN INTAKE; RAT; RNA TRANSLATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; STATISTICAL ANALYSIS; SWIMMING;

ANIMALS; BLOOD GLUCOSE; CARRIER PROTEINS; DIETARY CARBOHYDRATES; DIETARY PROTEINS; GLUCOSE; HYPOGLYCEMIC AGENTS; INSULIN; MALE; MUSCLE, SKELETAL; PHOSPHOPROTEINS; PHOSPHORYLATION; PHYSICAL CONDITIONING, ANIMAL; PHYSICAL ENDURANCE; PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY; RIBOSOMAL PROTEIN S6 KINASES; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; RNA, MESSENGER; SIGNAL TRANSDUCTION; SWIMMING;

EID: 41949089334     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01173.2007     Document Type: Article

References (41)

1. Anthony TG, McDaniel BJ, Knoll P, Bunpo P, Paul GL, McNurlan MA. Feeding meals containing soy or whey protein after exercise stimulates protein synthesis and translation initiation in the skeletal muscle of male rats. J Nutr 137: 357-362, 2007.
2. Biolo G, Fleming RY, Maggi SP, Wolfe RR. Transmembrane transport and intracellular kinetics of amino acids in human skeletal muscle. Am J Physiol Endocrinol Metab 268: E75-E84, 1995.
3. Biolo G, Maggi SP, Williams BD, Tipton KD, Wolfe RR. Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans. Am J Physiol Endocrinol Metab 268: E514-E520, 1995.
4. Biolo G, Tipton KD, Klein S, Wolfe RR. An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. Am J Physiol Endocrinol Metab 273: E122-E129, 1997.
5. Biolo G, Williams BD, Fleming RY, Wolfe RR. Insulin action on muscle protein kinetics and amino acid transport during recovery after resistance exercise. Diabetes 48: 949-957, 1999.
6. Blomstrand E, Eliasson J, Karlsson HK, Kohnke R. Branched-chain amino acids activate key enzymes in protein synthesis after physical exercise. J Nutr 136: 269-273, 2006.
7. Bolster DR, Kubica N, Crozier SJ, Williamson DL, Farrell PA, Kimball SR, Jefferson LS. Immediate response of mammalian target of rapamycin (mTOR)-mediated signaling following acute resistance exercise in rat skeletal muscle. J Physiol 553: 213-220, 2003.
8. Borsheim E, Cree MG, Tipton KD, Elliott TA, Aarsland A, Wolfe RR. Effect of carbohydrate intake on net muscle protein synthesis during recovery from resistance exercise. J Appl Physiol 96: 674-678, 2004.
9. Chesley A, MacDougall JD, Tarnopolsky MA, Atkinson SA, Smith K. Changes in human muscle protein synthesis after resistance exercise. J Appl Physiol 73: 1383-1388, 1992.
10. Crozier SJ, Kimball SR, Emmert SW, Anthony JC, Jefferson LS. Oral leucine administration stimulates protein synthesis in rat skeletal muscle. J Nutr 135: 376-382, 2005.
11. Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P, Wackerhage H, Taylor PM, Rennie MJ. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J 19: 422-424, 2005.
12. Deldicque L, Theisen D, Francaux M. Regulation of mTOR by amino acids and resistance exercise in skeletal muscle. Eur J Appl Physiol 94: 1-10, 2005.
13. Dreyer HC, Fujita S, Cadenas JG, Chinkes DL, Volpi E, Rasmussen BB. Resistance exercise increases AMPK activity and reduces 4E-BP1 phosphorylation and protein synthesis in human skeletal muscle. J Physiol 576: 613-624, 2006.
14. Eliasson J, Elfegoun T, Nilsson J, Kohnke R, Ekblom BT, Blomstrand E. Maximal lengthening contractions increase p70S6 kinase phosphorylation in human skeletal muscle in the absence of nutritional supply. Am J Physiol Endocrinol Metab 291: E1197-E1205, 2006.
15. Fedele MJ, Hernandez JM, Lang CH, Vary TC, Kimball SR, Jefferson LS, Farrell PA. Severe diabetes prohibits elevations in muscle protein synthesis after acute resistance exercise in rats. J Appl Physiol 88: 102-108, 2000.
16. Ferrari S, Bandi HR, Hofsteenge J, Bussian BM, Thomas G. Mitogen-activated 70KS6 kinase. Identification of in vitro 40S ribosomal S6 phosphorylation sites. J Biol Chem 266: 22770-22775, 1991.
17. Fingar DC, Richardson CJ, Tee AR, Cheatham L, Tsou C, Blenis J. mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E. Mol Cell Biol 24: 200-216, 2004.
18. Fluckey JD, Vary TC, Jefferson LS, Farrell PA. Augmented insulin action on rates of protein synthesis after resistance exercise in rats. Am J Physiol Endocrinol Metab 270: E313-E319, 1996.
19. Fujita S, Dreyer HC, Drummond MJ, Glynn EL, Cadenas JG, Yoshizawa F, Volpi E, Rasmussen BB. Nutrient signaling in the regulation of human muscle protein synthesis. J Physiol 582: 813-823, 2007.
20. Gautsch TA, Anthony JC, Kimball SR, Paul GL, Layman DK, Jefferson LS. Availability of eIF4E regulates skeletal muscle protein synthesis during recovery from exercise. Am J Physiol Cell Physiol 274: C406-C414, 1998.
21. Gingras AC, Gygi SP, Raught B, Polakiewicz RD, Abraham RT, Hoekstra MF, Aebersold R, Sonenberg N. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev 13: 1422-1437, 1999.
22. Hara K, Yonezawa K, Weng QP, Kozlowski MT, Belham C, Avruch J. Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF-4E BP1 through a common effector mechanism. J Biol Chem 273: 14484-14494, 1998.
23. Hood DA. Invited Review: contractile activity-induced mitochondrial biogenesis in skeletal muscle. J Appl Physiol 90: 1137-1157, 2001.
24. Karlsson HK, Nilsson PA, Nilsson J, Chibalin AV, Zierath JR, Blomstrand E. Branched-chain amino acids increase p70S6k phosphorylation in human skeletal muscle after resistance exercise. Am J Physiol Endocrinol Metab 287: E1-E7, 2004.
25. Kimball SR, Farrell PA, Jefferson LS. Invited Review: Role of insulin in translational control of protein synthesis in skeletal muscle by amino acids or exercise. J Appl Physiol 93: 1168-1180, 2002.
26. Kimball SR, Jefferson LS. Amino acids as regulators of gene expression. Nutr Metab 1: 3, 2004.
27. Kimball SR, Jefferson LS. Molecular mechanisms through which amino acids mediate signaling through the mammalian target of rapamycin. Curr Opin Clin Nutr Metab Care 7: 39-44, 2004.
28. Koopman R, Beelen M, Stellingwerff T, Pennings B, Saris WH, Kies AK, Kuipers H, van Loon LJ. Coingestion of carbohydrate with protein does not further augment post exercise muscle protein synthesis. Am J Physiol Endocrinol Metab 293: E833-E842, 2007.
29. Koopman R, Verdijk L, Manders RJ, Gijsen AP, Gorselink M, Pijpers E, Wagenmakers AJ, van Loon LJ. Co-ingestion of protein and leucine stimulates muscle protein synthesis rates to the same extent in young and elderly lean men. Am J Clin Nutr 84: 623-632, 2006.
30. Koopman R, Zorenc AH, Gransier RJ, Cameron-Smith D, van Loon LJ. Increase in S6K1 phosphorylation in human skeletal muscle following resistance exercise occurs mainly in type II muscle fibers. Am J Physiol Endocrinol Metab 290: E1245-E1252, 2006.
31. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685, 1970.
32. Liu Z, Wu Y, Nicklas EW, Jahn LA, Price WJ, Barrett EJ. Unlike insulin, amino acids stimulate p70S6K but not GSK-3 or glycogen synthase in human skeletal muscle. Am J Physiol Endocrinol Metab 286: E523-E528, 2004.
33. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275, 1951.
34. Mascher H, Andersson H, Nilsson PA, Ekblom B, Blomstrand E. Changes in signaling pathways regulating protein synthesis in human muscle in the recovery period after endurance exercise. Acta Physiol Scand 191: 67-75, 2007.
35. Miller SL, Tipton KD, Chinkes DL, Wolf SE, Wolfe RR. Independent and combined effects of amino acids and glucose after resistance exercise. Med Sci Sports Exerc 35: 449-455, 2003.
36. Pilegaard H, Saltin B, Neufer PD. Exercise induces transient transcriptional activation of the PGC-1alpha gene in human skeletal muscle. J Physiol 546: 851-858, 2003.
37. Raught B, Gingras AC. eIF4E activity is regulated at multiple levels. Int J Biochem Cell Biol 31: 43-57, 1999.
38. Rennie MJ, Bohe J, Smith K, Wackerhage H, Greenhaff P. Branchedchain amino acids as fuels and anabolic signals in human muscle. J Nutr 136: 264-268, 2006.
39. Roux PP, Blenis J. ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 68: 320-344, 2004.
40. Roy BD, Tarnopolsky MA, MacDougall JD, Fowles J, Yarasheski KE. Effect of glucose supplement timing on protein metabolism after resistance training. J Appl Physiol 82: 1882-1888, 1997.
41. Williamson DL, Kubica N, Kimball SR, Jefferson LS. Exercise-induced alterations in extracellular signal-regulated kinase 1/2 and mammalian target of rapamycin (mTOR) signaling to regulatory mechanisms of mRNA translation in mouse muscle. J Physiol 573: 497-510, 2006.