Skeletal muscle protein synthesis and the abundance of the mRNA translation initiation repressor PDCD4 are inversely regulated by fasting and refeeding in rats

American Journal of Physiology - Endocrinology and Metabolism

Volumn 300, Issue 6, 2011, Pages

  Zargar, Sana ^a,b   Moreira, Tracy S ^a,b   Samimi Seisan, Helena ^a,b   Jeganathan, Senthure ^a,b   Kakade, Dhanshri ^a   Islam, Nushaba ^a   Campbell, Jonathan ^a   Adegoke, Olasunkanmi A J ^a,b  

^a YORK UNIVERSITY   (Canada)

^b YORK UNIVERSITY   (Canada)

Author keywords

Mammalian target of rapamycin complex 1; MRNA translation; Programmed cell death 4; Protein metabolism; Ribosomal protein s6 kinase

Indexed keywords

AMINO ACID; MUSCLE PROTEIN; PHENYLALANINE; PROTEIN PROGRAMMED CELL DEATH 4; S6 KINASE; SERINE; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL GROWTH; CONTROLLED STUDY; CULTURE MEDIUM; DIET RESTRICTION; FEEDING; MALE; MUSCLE; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS REGULATION; RAT; REFEEDING; RNA TRANSLATION; SKELETAL MUSCLE; TRANSLATION REGULATION;

AMINO ACIDS; AMINO ACIDS, BRANCHED-CHAIN; ANIMALS; APOPTOSIS REGULATORY PROTEINS; CELL COUNT; CELL LINE; EATING; FASTING; INSULIN; MALE; MUSCLE FIBERS, SKELETAL; MUSCLE PROTEINS; MUSCLE, SKELETAL; MYOBLASTS; PHENYLALANINE; RATS; RATS, SPRAGUE-DAWLEY; RNA INTERFERENCE; RNA, MESSENGER; TRANSCRIPTION FACTORS;

EID: 79957646819     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00642.2010     Document Type: Article

References (51)

1. Adegoke OA, Chevalier S, Morais JA, Gougeon R, Kimball SR, Jefferson LS, Wing SS, Marliss EB. Fed-state clamp stimulates cellular mechanisms of muscle protein anabolism and modulates glucose disposal in normal men. Am J Physiol Endocrinol Metab 296: E105-E113, 2009.
2. Adegoke OA, McBurney MI, Baracos VE. Jejunal mucosal protein synthesis: validation of luminal flooding dose method and effect of luminal osmolarity. Am J Physiol Gastrointest Liver Physiol 276: G14-G20, 1999.
3. Aguilar V, Alliouachene S, Sotiropoulos A, Sobering A, Athea Y, Djouadi F, Miraux S, Thiaudière E, Foretz M, Viollet B, Diolez P, Bastin J, Benit P, Rustin P, Carling D, Sandri M, Ventura-Clapier R, Pende M. S6 kinase deletion suppresses muscle growth adaptations to nutrient availability by activating AMP kinase. Cell Metab 5: 476-487, 2007.
4. Anthony JC, Lang CH, Crozier SJ, Anthony TG, MacLean DA, Kimball SR, Jefferson LS. Contribution of insulin to the translational control of protein synthesis in skeletal muscle by leucine. Am J Physiol Endocrinol Metab 282: E1092-E1101, 2002.
5. Anthony JC, Yoshizawa F, Anthony TG, Vary TC, Jefferson LS, Kimball SR. Leucine stimulates translation initiation in skeletal muscle of postabsorptive rats via a rapamycin-sensitive pathway. J Nutr 130: 2413-2419, 2000.
6. Bentzinger CF, Romanino K, Cloetta D, Lin S, Mascarenhas JB, Oliveri F, Xia J, Casanova E, Costa CF, Brink M, Zorzato F, Hall MN, Ruegg MA. Skeletal muscle-specific ablation of raptor, but not of rictor, causes metabolic changes and results in muscle dystrophy. Cell Metab 8: 411-424, 2008.
7. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3: 1014-1019, 2001.
8. Bolster DR, Jefferson LS, Kimball SR. Regulation of protein synthesis associated with skeletal muscle hypertrophy by insulin-, amino acid- and exercise-induced signalling. Proc Nutr Soc 63: 351-356, 2004.
9. Carnevalli LS, Masuda K, Frigerio F, Le Bacquer O, Um SH, Gandin V, Topisirovic I, Sonenberg N, Thomas G, Kozma SC. S6K1 plays a critical role in early adipocyte differentiation. Dev Cell 18: 763-774, 2010.
10. Chang JH, Cho YH, Sohn SY, Choi JM, Kim A, Kim YC, Jang SK, Cho Y. Crystal structure of the eIF4A-PDCD4 complex. Proc Natl Acad Sci USA 106: 3148-3153, 2009.
11. Chevalier S, Gougeon R, Kreisman SH, Cassis C, Morais JA. The hyperinsulinemic amino acid clamp increases whole-body protein synthesis in young subjects. Metabolism 53: 388-396, 2004.
12. 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.
13. Dancey JE. Inhibitors of the mammalian target of rapamycin. Expert Opin Investig Drugs 14: 313-328, 2005.
14. Davis TA, Reeds PJ. The roles of nutrition, development and hormone sensitivity in the regulation of protein metabolism: an overview. J Nutr 128: 340S-341S, 1998.
15. Dorrello NV, Peschiaroli A, Guardavaccaro D, Colburn NH, Sherman NE, Pagano M. S6K1- and betaTRCP-mediated degradation of PDCD4 promotes protein translation and cell growth. Science 314: 467-471, 2006.
16. Dowling RJ, Topisirovic I, Alain T, Bidinosti M, Fonseca BD, Petroulakis E, Wang X, Larsson O, Selvaraj A, Liu Y, Kozma SC, Thomas G, Sonenberg N. mTORC1-mediated cell proliferation, but not cell growth, controlled by the 4E-BPs. Science 328: 1172-1176, 2010.
17. Efeyan A, Sabatini DM. mTOR and cancer: many loops in one pathway. Curr Opin Cell Biol 22: 169-176, 2010.
18. Elliott NT, Yuan F. A review of three-dimensional in vitro tissue models for drug discovery and transport studies. J Pharm Sci 100: 59-74, 2010.
19. Escobar J, Frank JW, Suryawan A, Nguyen HV, Kimball SR, Jefferson LS, Davis TA. Physiological rise in plasma leucine stimulates muscle protein synthesis in neonatal pigs by enhancing translation initiation factor activation. Am J Physiol Endocrinol Metab 288: E914-E921, 2005.
20. Ferrari S, Pearson RB, Siegmann M, Kozma SC, Thomas G. The immunosuppressant rapamycin induces inactivation of p70s6k through dephosphorylation of a novel set of sites. J Biol Chem 268: 16091-16094, 1993.
21. Ferrucci L, Studenski S. Diabetes, muscles, and the myth of Ulysses' bow. Diabetes Care 32: 2136-2137, 2009.
22. Frank JW, Escobar J, Suryawan A, Kimball SR, Nguyen HV, Jefferson LS, Davis TA. Protein synthesis and translation initiation factor activation in neonatal pigs fed increasing levels of dietary protein. J Nutr 135: 1374-1381, 2005.
23. Garlick PJ, McNurlan MA, Preedy VR. A rapid and convenient technique for measuring the rate of protein synthesis in tissues by injection of [3H]phenylalanine. Biochem J 192: 719-723, 1980.
24. Giles JT, Ling SM, Ferrucci L, Bartlett SJ, Andersen RE, Towns M, Muller D, Fontaine KR, Bathon JM. Abnormal body composition phenotypes in older rheumatoid arthritis patients: association with disease characteristics and pharmacotherapies. Arthritis Rheum 59: 807-815, 2008.
25. Goke A, Goke R, Knolle A, Trusheim H, Schmidt H, Wilmen A, Carmody R, Goke B, Chen YH. DUG is a novel homologue of translation initiation factor 4G that binds eIF4A. Biochem Biophys Res Commun 297: 78-82, 2002.
26. Gulve EA, Dice JF. Regulation of protein synthesis and degradation in L8 myotubes. Effects of serum, insulin and insulin-like growth factors. Biochem J 260: 377-387, 1989.
27. Han JW, Pearson RB, Dennis PB, Thomas G. Rapamycin, wortmannin, and the methylxanthine SQ20006 inactivate p70s6k by inducing dephosphorylation of the same subset of sites. J Biol Chem 270: 21396-21403, 1995.
28. Holz MK, Ballif BA, Gygi SP, Blenis J. mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 123: 569-580, 2005.
29. Jepson MM, Pell JM, Bates PC, Millward DJ. The effects of endotoxaemia on protein metabolism in skeletal muscle and liver of fed and fasted rats. Biochem J 235: 329-336, 1986.
30. Kang MJ, Ahn HS, Lee JY, Matsuhashi S, Park WY. Up-regulation of PDCD4 in senescent human diploid fibroblasts. Biochem Biophys Res Commun 293: 617-621, 2002.
31. Kimball SR, Jefferson LS. Control of translation initiation through integration of signals generated by hormones, nutrients, and exercise. J Biol Chem 285: 29027-29032, 2010.
32. Kimball SR, Shantz LM, Horetsky RL, Jefferson LS. 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: 11647-11652, 1999.
33. Krieg J, Hofsteenge J, Thomas G. Identification of the 40 S ribosomal protein S6 phosphorylation sites induced by cycloheximide. J Biol Chem 263: 11473-11477, 1988.
34. Lang CH, Frost RA, Vary TC. Regulation of muscle protein synthesis during sepsis and inflammation. Am J Physiol Endocrinol Metab 293: E453-E459, 2007.
35. Lankat-Buttgereit B, Goke R. The tumour suppressor Pdcd4: recent advances in the elucidation of function and regulation. Biol Cell 101: 309-317, 2009.
36. Loh PG, Yang HS, Walsh MA, Wang Q, Wang X, Cheng Z, Liu D, Song H. Structural basis for translational inhibition by the tumour suppressor Pdcd4. EMBO J 28: 274-285, 2009.
37. Mieulet V, Roceri M, Espeillac C, Sotiropoulos A, Ohanna M, Oorschot V, Klumperman J, Sandri M, Pende M. S6 kinase inactivation impairs growth and translational target phosphorylation in muscle cells maintaining proper regulation of protein turnover. Am J Physiol Cell Physiol 293: C712-C722, 2007.
38. Ohanna M, Sobering AK, Lapointe T, Lorenzo L, Praud C, Petroulakis E, Sonenberg N, Kelly PA, Sotiropoulos A, Pende M. Atrophy of S6K1(-/-) skeletal muscle cells reveals distinct mTOR effectors for cell cycle and size control. Nat Cell Biol 7: 286-294, 2005.
39. Onishi Y, Hashimoto S, Kizaki H. Cloning of the TIS gene suppressed by topoisomerase inhibitors. Gene 215: 453-459, 1998.
40. Pause A, Belsham GJ, Gingras AC, Donze O, Lin TA, Lawrence JC Jr, Sonenberg N. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5=-cap function. Nature 371: 762-767, 1994.
41. Prado CM, Lieffers JR, McCargar LJ, Reiman T, Sawyer MB, Martin L, Baracos VE. Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: a population-based study. Lancet Oncol 9: 629-635, 2008.
42. Risson V, Mazelin L, Roceri M, Sanchez H, Moncollin V, Corneloup C, Richard-Bulteau H, Vignaud A, Baas D, Defour A, Freyssenet D, Tanti JF, Le-Marchand-Brustel Y, Ferrier B, Conjard-Duplany A, Romanino K, Bauché S, Hantaï D, Mueller M, Kozma SC, Thomas G, Rüegg MA, Ferry A, Pende M, Bigard X, Koulmann N, Schaeffer L, Gangloff YG. Muscle inactivation of mTOR causes metabolic and dystrophin defects leading to severe myopathy. J Cell Biol 187: 859-874, 2009.
43. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD, Glass DJ. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat Cell Biol 3: 1009-1013, 2001.
44. Ruvinsky I, Meyuhas O. Ribosomal protein S6 phosphorylation: from protein synthesis to cell size. Trends Biochem Sci 31: 342-348, 2006.
45. Schmid T, Jansen AP, Baker AR, Hegamyer G, Hagan JP, Colburn NH. Translation inhibitor Pdcd4 is targeted for degradation during tumor promotion. Cancer Res 68: 1254-1260, 2008.
46. Shibahara K, Asano M, Ishida Y, Aoki T, Koike T, Honjo T. Isolation of a novel mouse gene MA-3 that is induced upon programmed cell death. Gene 166: 297-301, 1995.
47. Sonenberg N, Pause A. Signal transduction. Protein synthesis and oncogenesis meet again. Science 314: 428-429, 2006.
48. Tremblay F, Krebs M, Dombrowski L, Brehm A, Bernroider E, Roth E, Nowotny P, Waldhausl W, Marette A, Roden M. Overactivation of S6 kinase 1 as a cause of human insulin resistance during increased amino acid availability. Diabetes 54: 2674-2684, 2005.
49. Um SH, Frigerio F, Watanabe M, Picard F, Joaquin M, Sticker M, Fumagalli S, Allegrini PR, Kozma SC, Auwerx J, Thomas G. Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 431: 200-205, 2004.
50. Watford M. Net interorgan transport of L-glutamate in rats occurs via the plasma, not via erythrocytes. J Nutr 132: 952-956, 2002.
51. Yang HS, Jansen AP, Komar AA, Zheng X, Merrick WC, Costes S, Lockett SJ, Sonenberg N, Colburn NH. The transformation suppressor Pdcd4 is a novel eukaryotic translation initiation factor 4A binding protein that inhibits translation. Mol Cell Biol 23: 26-37, 2003.