The abundance and activation of mTORC1 regulators in skeletal muscle of neonatal pigs are modulated by insulin, amino acids, and age

Journal of Applied Physiology

Volumn 109, Issue 5, 2010, Pages 1448-1454

  Suryawan, Agus ^a   Davis, Teresa A ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Amino acid signaling; Insulin signaling; PLD1; Protein synthesis; RagB

Indexed keywords

AMINO ACID; FK 506 BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; MAMMALIAN TARGET OF RAPAMYCIN; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; MULTIPROTEIN COMPLEX; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE D; PHOSPHOLIPASE D1; PHOSPHOPROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

AGE; ANIMAL; ARTICLE; GLUCOSE CLAMP TECHNIQUE; METABOLISM; NEWBORN; PHOSPHORYLATION; POSTPRANDIAL STATE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SWINE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AGE FACTORS; AMINO ACIDS; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANIMALS, NEWBORN; CLASS III PHOSPHATIDYLINOSITOL 3-KINASES; GLUCOSE CLAMP TECHNIQUE; GTP-BINDING PROTEIN BETA SUBUNITS; INSULIN; MONOMERIC GTP-BINDING PROTEINS; MULTIPROTEIN COMPLEXES; MUSCLE, SKELETAL; PHOSPHOLIPASE D; PHOSPHOPROTEINS; PHOSPHORYLATION; POSTPRANDIAL PERIOD; SIGNAL TRANSDUCTION; SWINE; TACROLIMUS BINDING PROTEINS; TOR SERINE-THREONINE KINASES;

EID: 78549288864     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00428.2010     Document Type: Article

References (51)

1. Arsham AM, Howell JJ, Simon MC. A novel hypoxia-inducible factorindependent hypoxic response regulating mammalian target of rapamycin and its targets. J Biol Chem 278: 29655-29660, 2003.
2. Avruch J, Lin Y, Long X, Murthy S, Ortiz-Vega S. Recent advances in the regulation of the TOR pathway by insulin and nutrients. Curr Opin Clin Nutr Metab Care 8: 67-72, 2005.
3. Backer JM. The regulation and function of Class III PI3Ks: novel roles for Vps34. Biochem J 410: 1-17, 2008.
4. Bai X, Ma D, Liu A, Shen X, Wang QJ, Liu Y, Jiang Y. Rheb activates mTOR by antagonizing its endogenous inhibitor, FKBP38. Science 318: 977-980, 2007.
5. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
6. Byfield MP, Murray JT, Backer JM. hVps34 is a nutrient-regulated lipid kinase required for activation of p70 S6 kinase. J Biol Chem 280: 33076-33082, 2005.
7. Corradetti MN, Guan KL. Upstream of the mammalian target of rapamycin: do all roads pass through mTOR? Oncogene 25: 6347-6360, 2006.
8. Davis TA, Burrin DG, Fiorotto ML, Nguyen HV. Protein synthesis in skeletal muscle and jejunum is more responsive to feeding in 7-than in 26-day-old pigs. Am J Physiol Endocrinol Metab 270: E802-E809, 1996.
9. Davis TA, Fiorotto ML. Regulation of muscle growth in neonates. Curr Opin Clin Nutr Metab Care 12: 78-85, 2009.
10. Davis TA, Fiorotto ML, Burrin DG, Reeds PJ, Nguyen HV, Beckett PR, Vann RC, O'Connor PM. Stimulation of protein synthesis by bothinsulin and amino acids is unique to skeletal muscle in neonatal pigs. Am J Physiol Endocrinol Metab 282: E880-E890, 2002.
11. Davis TA, Fiorotto ML, Nguyen HV, Reeds PJ. Protein turnover in skeletal muscle of suckling rats. Am J Physiol Regul Integr Comp Physiol 257: R1141-R1146, 1989.
12. Davis TA, Nguyen HV, Suryawan A, Bush JA, Jefferson LS, Kimball SR. Developmental changes in the feeding-induced stimulation of translation initiation in muscle of neonatal pigs. Am J Physiol Endocrinol Metab 279: E1226-E1234, 2000.
13. Denne SC, Kalhan SC. Leucine metabolism in human newborns. Am J Physiol Endocrinol Metab 253: E608-E615, 1987.
14. Fonseca BD, Smith EM, Lee VH, MacKintosh C, Proud CG. PRAS40 is a target for mammalian target of rapamycin complex 1 and is required for signaling downstream of this complex. J Biol Chem 282: 24514-24524, 2007.
15. Formisano P, Oriente F, Fiory F, Caruso M, Miele C, Maitan MA, Andreozzi F, Vigliotta G, Condorelli G, Beguinot F. Insulin-activated protein kinase Cbeta bypasses Ras and stimulates mitogen-activated protein kinase activity and cell proliferation in muscle cells. Mol Cell Biol 20: 6323-6333, 2000.
16. Guertin DA, Stevens DM, Thoreen CC, Burds AA, Kalaany NY, Moffat J, Brown M, Fitzgerald KJ, Sabatini DM. Ablation in mice of the mTORC components raptor, rictor, or mLST8 reveals that mTORC2 is required for signaling to Akt-FOXO and PKCalpha, but not S6K1. Dev Cell 11: 859-871, 2006.
17. Gulati P, Gaspers LD, Dann SG, Joaquin M, Nobukuni T, Natt F, Kozma SC, Thomas AP, Thomas G. Amino acids activate mTOR complex 1 via Ca2-/CaM signaling to hVps34. Cell Metab 7: 456-465, 2008.
18. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30: 214-226, 2008.
19. Hara K, Maruki Y, Long X, Yoshino K, Oshiro N, Hidayat S, Tokunaga C, Avruch J, Yonezawa K. Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 110: 177-189, 2002.
20. Jeyapalan AS, Orellana RA, Suryawan A, O'Connor PM, Nguyen HV, Escobar J, Frank JW, Davis TA. Glucose stimulates protein synthesis in skeletal muscle of neonatal pigs through an. Am J Physiol Endocrinol Metab 293: E595-E603, 2007.
21. Juhasz G, Hill JH, Yan Y, Sass M, Baehrecke EH, Backer JM, Neufeld TP. The class III PI(3)K Vps34 promotes autophagy and endocytosis but not TOR signaling in Drosophila. J Cell Biol 181: 655-666, 2008.
22. Kim E, Goraksha-Hicks P, Li L, Neufeld TP, Guan KL. Regulation of TORC1 by Rag GTPases in nutrient response. Nat Cell Biol 10: 935-945, 2008.
23. Kim Y, Han JM, Park JB, Lee SD, Oh YS, Chung C, Lee TG, Kim JH, Park SK, Yoo JS, Suh PG, Ryu SH. Phosphorylation and activation of phospholipase D1 by protein kinase C in vivo: determination of multiple phosphorylation sites. Biochemistry 38: 10344-10351, 1999.
24. Long X, Lin Y, Ortiz-Vega S, Busch S, Avruch J. The Rheb switch 2 segment is critical for signaling to target of rapamycin complex 1. J Biol Chem 282: 18542-18551, 2007.
25. Long X, Ortiz-Vega S, Lin Y, Avruch J. Rheb binding to mammalian target of rapamycin (mTOR) is regulated by amino acid sufficiency. J Biol Chem 280: 23433-23436, 2005.
26. Ma D, Bai X, Guo S, Jiang Y. The switch I region of Rheb is critical for its interaction with FKBP38. J Biol Chem 283: 25963-25970, 2008.
27. MacKenzie MG, Hamilton DL, Murray JT, Taylor PM, Baar K. mVps34 is activated following high-resistance contractions. J Physiol 587: 253-260, 2009.
28. Mothe-Satney I, Gautier N, Hinault C, Lawrence JC Jr, Van OE. In rat hepatocytes glucagon increases mammalian target of rapamycin phosphorylation on serine 2448 but antagonizes the phosphorylation of its downstream targets induced by insulin and amino acids. J Biol Chem 279: 42628-42637, 2004.
29. Oshiro N, Takahashi R, Yoshino K, Tanimura K, Nakashima A, Eguchi S, Miyamoto T, Hara K, Takehana K, Avruch J, Kikkawa U, Yonezawa K. The proline-rich Akt substrate of 40 kDa (PRAS40) is a physiological substrate of mammalian target of rapamycin complex 1. J Biol Chem 282: 20329-20339, 2007.
30. Oshiro N, Yoshino K, Hidayat S, Tokunaga C, Hara K, Eguchi S, Avruch J, Yonezawa K. Dissociation of raptor from mTOR is a mechanism of rapamycin-induced inhibition of mTOR function. Genes Cells 9: 359-366, 2004.
31. Proud CG. Regulation of mammalian translation factors by nutrients. Eur J Biochem 269: 5338-5349, 2002.
32. Proud CG. Amino acids and mTOR signalling in anabolic function. Biochem Soc Trans 35: 1187-1190, 2007.
33. Proud CG. Cell signaling. mTOR, unleashed. Science 318: 926-927, 2007.
34. Sabatini DM. mTOR and cancer: insights into a complex relationship. Nat Rev Cancer 6: 729-734, 2006.
35. Sancak Y, Peterson TR, Shaul YD, Lindquist RA, Thoreen CC, Bar-Peled L, Sabatini DM. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320: 1496-1501, 2008.
36. Sanchez Canedo C, Demeulder B, Ginion A, Bayascas JR, Balligand JL, Alessi DR, Vanoverschelde JL, Beauloye C, Hue L, Bertrand L. Activation of the cardiac mTOR/p70S6K pathway by leucine requires PDK1 and correlates with PRAS40 phosphorylation. Am J Physiol Endocrinol Metab 298: E761-E769, 2010.
37. Shaw RJ. mTOR signaling: RAG GTPases transmit the amino acid signal. Trends Biochem Sci 33: 565-568, 2008.
38. Sun Y, Chen J. mTOR signaling: PLD takes center stage. Cell Cycle 7: 3118-3123, 2008.
39. Sun Y, Fang Y, Yoon MS, Zhang C, Roccio M, Zwartkruis FJ, Armstrong M, Brown HA, Chen J. Phospholipase D1 is an effector of Rheb in the mTOR pathway. Proc Natl Acad Sci USA 105: 8286-8291, 2008.
40. Suryawan A, Jeyapalan AS, Orellana RA, Wilson FA, Nguyen HV, Davis TA. Leucine stimulates protein synthesis in skeletal muscle of neonatal pigs by enhancing mTORC1 activation. Am J Physiol Endocrinol Metab 295: E868-E875, 2008.
41. Suryawan A, Nguyen HV, Bush JA, Davis TA. Developmental changes in the feeding-induced activation of the insulin-signaling pathway in neonatal pigs. Am J Physiol Endocrinol Metab 281: E908-E915, 2001.
42. Suryawan A, O'Connor PM, Kimball SR, Bush JA, Nguyen HV, Jefferson LS, Davis TA. Amino acids do not alter the insulin-induced activation of the insulin signaling pathway in neonatal pigs. J Nutr 134: 24-30, 2004.
43. Suryawan A, Orellana RA, Nguyen HV, Jeyapalan AS, Fleming JR, Davis TA. Activation by insulin and amino acids of signaling components leading to translation initiation in skeletal muscle of neonatal pigs is developmentally regulated. Am J Physiol Endocrinol Metab 293: E1597-E1605, 2007.
44. Tokunaga C, Yoshino K, Yonezawa K. mTOR integrates amino acidand energy-sensing pathways. Biochem Biophys Res Commun 313: 443-446, 2004.
45. Uhlenbrock K, Weiwad M, Wetzker R, Fischer G, Wittinghofer A, Rubio I. Reassessment of the role of FKBP38 in the Rheb/mTORC1 pathway. FEBS Lett 583: 965-970, 2009.
46. Vander HE, Lee SI, Bandhakavi S, Griffin TJ, Kim DH. Insulin signalling to mTOR mediated by the Akt/PKB substrate PRAS40. Nat Cell Biol 9: 316-323, 2007.
47. Wang L, Harris TE, Lawrence JC Jr. Regulation of proline-rich Akt substrate of 40 kDa (PRAS40) function by mammalian target of rapamycin complex 1 (mTORC1)-mediated phosphorylation. J Biol Chem 283: 15619-15627, 2008.
48. Wang X, Fonseca BD, Tang H, Liu R, Elia A, Clemens MJ, Bommer UA, Proud CG. Re-evaluating the roles of proposed modulators of mammalian target of rapamycin complex 1 (mTORC1) signaling. J Biol Chem 283: 30482-30492, 2008.
49. Yan Y, Backer JM. Regulation of class III (Vps34) PI3Ks. Biochem Soc Trans 35: 239-241, 2007. (Pubitemid 46596478)
50. Yang X, Yang C, Farberman A, Rideout TC, de Lange CF, France J, Fan MZ. The mTOR-signaling pathway in regulating metabolism and growth. J Anim Sci 86, Suppl 14: :E36-E50, 2008.
51. Yonezawa K, Tokunaga C, Oshiro N, Yoshino K. Raptor, a binding partner of target of rapamycin. Biochem Biophys Res Commun 313: 437-441, 2004.