Tissue-specific regulation of protein synthesis by insulin and free fatty acids

American Journal of Physiology - Endocrinology and Metabolism

Volumn 285, Issue 4 48-4, 2003, Pages

  Crozier, Stephen J ^a   Anthony, Joshua C ^a   Schworer, Charles M ^a   Reiter, Ali K ^a   Anthony, Tracy G ^a   Kimball, Scot R ^a   Jefferson, Leonard S ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

AMP activated protein kinase; Energy status; Pyridine dinucleotides; Translation initiation

Indexed keywords

FATTY ACID; GUANINE NUCLEOTIDE EXCHANGE FACTOR; INSULIN; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ENERGY; CONTROLLED STUDY; DIABETES MELLITUS; GASTROCNEMIUS MUSCLE; GENE ACTIVITY; HEART; HORMONE ACTION; HYPOINSULINEMIA; HYPOLIPEMIA; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; REDUCTION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TRANSLATION REGULATION;

EID: 0141727765     PISSN: 01931849     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpendo.00063.2003     Document Type: Article

References (42)

1. Anthony JC, Reiter AK, Anthony TG, Crozier SJ, Lang CH, MacLean DA, Kimball SR, and Jefferson LS. Orally administered leucine enhances protein synthesis in skeletal muscle of diabetic rats in the absence of increases in 4E-BP1 or S6K1 phosphorylation. Diabetes 51: 928-936, 2002.
2. Bolster DR, Crozier SJ, Kimball SR, and Jefferson LS. AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through downregulated mTOR signaling. J Biol Chem 277: 23977-23980, 2002.
3. Brown EJ, Beal PA, Keith CT, Chen J, Shin TB, and Schreiber SL. Control of p70 S6 kinase by kinase activity of FRAP in vivo. Nature 377: 441-446, 1995.
4. Brunn GJ, Hudson C, Sekulic A, Williams JM, Hosoi H, Houghton PJ, Lawrence JC, and Abraham RT. Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. Science 277: 99-101, 1997.
5. Clemens MJ, Galpine AR, Austin SA, Pollard JW, Jefferey IW, Kelly FJ, and Pain VM. The role of phosphorylation of eIF-2α in translational regulation in nonerythroid cells. In: Current Communications in Molecular Biology, edited by Mathews MB. Cold Spring Harbor, NY: Cold Spring Harbor, 1986, p. 63-69.
6. Crozier SJ, Bolster DR, Reiter AK, Kimball SR, and Jefferson LS. β-Oxidation of free fatty acids is required for maintenance of translational control of protein synthesis in heart. Am J Physiol Endocrinol Metab 283: E1144-E1150, 2002.
7. Dennis P, Jaeschke A, Saitoh M, Fowler B, Kozma S, and Thomas G. Mammalian TOR: a homeostatic ATP sensor. Science 294: 1102-1105, 2001.
8. Dholakia JN, Mueser TC, Woodley CL, Parkhurst LJ, and Wahba AJ. The association of NADPH with the guanine nucleotide exchange factor from rabbit reticulocytes: a role of pyridine dinucleotides in eukaryotic polypeptide chain initiation. Proc Natl Acad Sci USA 83: 6746-6750, 1986.
9. Flaim KE, Copenhaver ME, and Jefferson LS. Effects of diabetes on protein synthesis in fast- and slow-twitch rat skeletal muscle. Am J Physiol Endocrinol Metab 239: E88-E95, 1980.
10. Garlick PJ, McNurlan MA, and Preedy VR. A rapid and convenient technique for measuring the rate of protein synthesis in postabsorptive rats. Biochem J 192: 719-723, 1980.
11. Gautsch T, Kandl S, Donovan S, and Layman D. Growth hormone promotes somatic and skeletal muscle growth in rats following chronic protein-energy malnutrition. J Nutr 129: 828-837, 1999.
12. Gautsch TA, Anthony JC, Kimball SR, Paul GL, Layman DK, and Jefferson LS. Eukaryotic initiation factor 4E availability regulates skeletal muscle protein synthesis during recovery from exercise. Am J Physiol Cell Physiol 274: C406-C414, 1998.
13. Hardie DG, Carling D, and Carlson M. The AMP-activated/SNF1 protein kinase subfamily: metabolic sensor of the eukaryotic cell? Annu Rev Biochem 67: 821-855, 1998.
14. Hardie DG, Salt IP, Hawley SA, and Davies SP. AMP-activated protein kinase: an ultrasensitive system for monitoring cellular energy charge. Biochem J 338: 717-722, 1999.
15. Harding HP, Zhang Y, and Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274, 1999.
16. Jefferey IW, Kelly FJ, Duncan R, Hershey JWB, and Pain VM. Effect of starvation and diabetes on the activity of the eukaryotic initiation factor eIF-2 in rat skeletal muscle. Biochimie 72: 751-757, 1990.
17. Jefferson LS, Rannels DE, Munger BL, and Morgan HE. Insulin in the regulation of protein turnover in heart and skeletal muscle. Fed Proc 33: 1098-1104, 1974.
18. Karinch AM, Kimball SR, Vary TC, and Jefferson LS. Regulation of eukaryotic initiation factor-2B activity in muscle of diabetic animals. Am J Physiol Endocrinol Metab 264: E101-E108, 1993.
19. Kaufman RJ. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational control. Genes Dev 1211-1233, 1999.
20. Kimball SR, Antonetti DA, Brawley RM, and Jefferson LS. Mechanisms of inhibition of peptide chain initiation by amino acid deprivation in perfued rat liver. Regulation involving inhibition of eukaryotic initiation factor 2α phosphatase activity. J Biol Chem 266: 1969-1976, 1991.
21. Kimball SR and Jefferson LS. Effect of diabetes on guanine nucleotide exchange factor activity in skeletal muscle and heart. Biochem Biophys Res Commun 156: 706-711, 1988.
22. Kimball SR, Jurasinski CV, Lawrence JC, and Jefferson LS. Insulin stimulates protein synthesis in skeletal muscle by enhancing the association of eIF4E and eIF4G. Am J Physiol Cell Physiol 272: C754-C759, 1997.
23. Kimball SR, Vary TC, and Jefferson LS. Age-dependent decrease in the amount of eukaryotic initiation factor 2 in various tissues. Biochem J 286: 263-268, 1992.
24. Kimura N, Tokunaga C, Dalal S, Richardson C, Yoshino K, Hara K, Kemp BE, Witters LA, Mimura O, and Yonezawa K. A possible linkage between AMP-activated protein kinase (AMPK) and mammalian target of rapamycin (mTOR) signalling pathway. Genes Cells 8: 65-79, 2003.
25. Lowell BB and Goodman MN. Protein sparing in skeletal muscle during prolonged starvation: dependence on lipid fuel availability. Diabetes 36: 14-19, 1987.
26. McGarry JD. Dysregulation of fatty acid metabolism in the etiology of type 2 diabetes. Diabetes 51: 7-18, 2002.
27. Merrick WC. Eukaryotic protein synthesis: an in vitro analysis. Biochimie 76: 822-830, 1994.
28. Mothe-Satney I, Brunn GJ, McMahon LP, Capaldo CT, Abraham RT, and Lawrence JC. 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, 2000.
29. Munro HN and Fleck A. Analysis of Tissue and Body Fluids for Nitrogenous Constituents. New York: Academic, 1969.
30. Nave BT, Ouwens DM, Withers DJ, Alessi DR, and Shepherd PR. Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem J 344: 427-431, 1999.
31. Ochoa S. Regulation of protein synthesis initiation in eukaryotes. Arch Biochem Biophys 223: 325-349, 1983.
32. Pain VM. Initiation of protein synthesis in mammalian cells. Biochem J 235: 625-637, 1986.
33. Pain VM, Albertse EC, and Garlick PJ. Protein metabolism in skeletal muscle, diaphragm, and heart of diabetic rats. Am J Physiol Endocrinol Metab 245: E605-E610, 1983.
34. Pain VM and Garlick PJ. Effect of streptozotocin diabetes and insulin treatment on the rate of protein synthesis in tissues of the rat in vivo. J Biol Chem 249: 4510-4514, 1974.
35. Proud CG, Wang X, Patel JV, Campbell LE, Kleijn M, Li W, and Browne GJ. Interplay between insulin and nutrients in the regulation of translation factors. Biochem Soc Trans 29: 541-547, 2001.
36. Rannels DE, Hjarlmarson AC, and Morgan HE. Effects of noncarbohydrate substrates on protein synthesis in muscle. Am J Physiol 226: 528-539, 1974.
37. Rannels DE, Jefferson LS, Hjalmarson AC, Wolpert EB, and Morgan HE. Maintenance of protein synthesis in hearts of diabetic animals. Biochem Biophys Res Commun 40: 1110-1116, 1970.
38. Rannels DE, Pegg AE, Rannels SR, and Jefferson LS. Effect of starvation on initiation of protein synthesis in skeletal muscle and heart. Am J Physiol Endocrinol Metab Gastrointest Physiol 235: E126-E133, 1978.
39. Sekulic A, Hudson CC, Homme JL, Peng Y, Otterness DM, Karnitz LM, and Abraham RT. A direct linkage between the phosphoinositide 3-kinase-akt signaling pathway and the mammalian target of rapamycin in mitogen-stimulated and transformed cells. Cancer Res 60: 3504-3513, 2000.
40. Shah OJ, Anthony JC, Kimball SR, and Jefferson LS. 4E-BP1 and S6K1: translational integration sites for nutritional and hormonal information in muscle. Am J Physiol Endocrinol Metab 279: E715-E729, 2000.
41. Stein DT, Esser V, Stevenson BE, Lane KE, Whiteside JH, Daniels MB, Chen S, and McGarry JM. Essentiality of circulating fatty acids for glucose-stimulated insulin secretion in the fasted rat. J Clin Invest 97: 2728-2735, 1996.
42. Weng QP, Andrabi K, Kozlowski MT, Grove JR, and Avruch J. Multiple independent inputs are required for activation of p70 S6 kinase. Mol Cell Biol 15: 2333-2340, 1995.