Endotoxin induces differential regulation of mTOR-dependent signaling in skeletal muscle and liver of neonatal pigs

American Journal of Physiology - Endocrinology and Metabolism

Volumn 285, Issue 3 48-3, 2003, Pages

  Kimball, Scot R ^a   Orellana, Renán A ^b   O'Connor, Pamela M J ^b   Suryawan, Agus ^b   Bush, Jill A ^b   Nguyen, Hanh V ^b   Thivierge, M Carole ^b   Jefferson, Leonard S ^a   Davis, Teresa A ^b  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Eukaryotic initiation factor 2B; Eukaryotic initiation factor 4E; Eukaryotic initiation factor 4G; Lipopolysaccharide

Indexed keywords

ENDOTOXIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; LIPOPOLYSACCHARIDE; MESSENGER RNA; RAPAMYCIN; REGULATOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; LIVER; MUSCLE METABOLISM; NEWBORN; NEWBORN INFECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; RNA BINDING; SEPSIS; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SWINE; TRANSLATION INITIATION;

EID: 0042967444     PISSN: 01931849     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpendo.00340.2002     Document Type: Article

References (50)

1. Aloni R, Peleg D, and Meyuhas O. Selective translational control and nonspecific posttranscriptional regulation of ribosomal protein gene expression during development and regeneration of rat liver. Mol Cell Biol 12: 2203-2212, 1992.
2. Anthony JC, Yoshizawa F, Anthony TG, Vary TC, Jefferson LS, and Kimball SR. Leucine stimulates translation initiation in skeletal muscle of post-absorptive rats via a rapamycin-sensitive pathway. J Nutr 130: 2413-2419, 2000.
3. Burnett PE, Barrow RK, Cohen NA, Snyder SH, and Sabatini DM. RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc Natl Acad Sci USA 95: 1432-1437, 1998.
4. Cooney RN, Kimball SR, Maish G, Shumate M, and Vary TC. Effects of tumor necrosis factor-binding protein on hepatic protein synthesis during chronic sepsis. J Surg Res 93: 257-264, 2000.
5. Davis TA, Burrin DG, Fiorotto ML, and 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.
6. Davis TA, Fiorotto ML, Beckett PR, Burrin DG, Reeds PJ, Wray-Cahen D, and Nguyen HV. Differential effects of insulin on peripheral and visceral protein synthesis in neonatal pigs. Am J Physiol Endocrinol Metab 280: E770-E779, 2001.
7. Davis TA, Fiorotto ML, Burrin DG, Reeds PJ, Nguyen HV, Beckett PR, Vann R, and O'Connor PMJ. Stimulation of protein synthesis by both insulin and amino acids is unique to skeletal muscle in neonatal pigs. Am J Physiol Endocrinol Metab 282: E880-E890, 2002.
8. Davis TA, Fiorotto ML, Nguyen HV, and Reeds PJ. Enhanced response of muscle protein synthesis and plasma insulin to food intake in suckled rats. Am J Physiol Regul Integr Comp Physiol 265: R334-R340, 1993.
9. Davis TA, Fiorotto ML, Ngyuen HV, and Reeds PJ. Protein turnover in skeletal muscle of suckling rats. Am J Physiol Regul Integr Comp Physiol 257: R1141-Rll46, 1989.
10. De Benedetti A and Harris AL. eIF4E expression in tumors: its possible role in progression of malignancies. Int J Biochem Cell Biol 31: 59-72, 1999.
11. Denne SC, Rossi EM, and Kalhan SC. Leucine kinetics during feeding in normal newborns. Pediatr Res 30: 23-27, 1991.
12. Geyer PK, Meyuhas O, Perry RP, and Johnson LF. Regulation of ribosomal protein mRNA content and translation in growth-stimulated mouse fibroblasts. Mol Cell Biol 2: 685-693, 1982.
13. Gingras A-C, Raught B, and Sonenberg N. Regulation of translation initiation by FRAP/mTOR. Genes Dev 15: 807-826, 2001.
14. Gressner AM and Wool IG. The phosphorylation of liver ribosomal proteins in vivo. Evidence that only a single small subunit protein (S6) is phosphorylated. J Biol Chem 249: 6917-6925, 1974.
15. Haystead TAJ, Haystead CMM, Hu C, Lin T-A, and Lawrence JC. Phosphorylation of PHAS-I by mitogen-activated protein (MAP) kinase. Identification of a site phosphorylated by MAP kinase in vitro and in response to insulin in rat adipocytes. J Biol Chem 269: 23185-23191, 1994.
16. Hershey JWB and Merrick WC. The pathway and mechanism of initiation of protein synthesis. In: Translational Control of Gene Expression, edited by Sonenberg N, Hershey JWB, and Mathews MB. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 2000, p. 33-88.
17. Hinnebusch AG. Mechanism and regulation of initiator methionyl-tRNA binding to ribosomes. In: Translational Control of Gene Expression, edited by Sonenberg N, Hershey JWB, and Mathews MB. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 2000, p. 185-243.
18. Hornstein E, Git A, Braunstein I, Avni D, and Meyuhas O. The expression of poly(A)-binding protein gene is translationally regulated in a growth dependent fashion through a 5′-terminal oligopyrimidine tract motif. J Biol Chem 274: 1708-1714, 1999.
19. Jefferies HB, Fumagalli S, Dennis PB, Reinhard C, Pearson RB, and Thomas G. Rapamycin suppresses 5′TOP mRNA translation through inhibition of p70s6k. EMBO J 16: 3693-3704, 1997.
20. S6k defines its role in protein synthesis and rapamycin sensitivity. Proc Natl Acad Sci USA 95: 5033-5038, 1998.
21. Kimball SR, Horetsky RL, and Jefferson LS. Implication of eIF2B rather than eIF4E in the regulation of global protein synthesis by amino acids in L6 myoblasts. J Biol Chem 273: 30945-30953, 1998.
22. Kimball SR and Jefferson LS. Mechanism of inhibition of peptide chain initiation by amino acid deprivation in perfused rat liver. Regulation involving inhibition of eukaryotic initiation factor 2α phosphatase activity. J Biol Chem 266: 1969-1976, 1991.
23. Kimball SR, Jefferson LS, and Davis TA. Feeding stimulates protein synthesis in muscle and liver of neonatal pigs through an mTOR-dependent process. Am J Physiol Endocrinol Metab 279: E1080-E1087, 2000.
24. Kimball SR, Shantz LM, Horetsky RL, and 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.
25. Lang CH, Frost RA, Jefferson LS, Kimball SR, and Vary TC. Endotoxin-induced decrease in muscle protein synthesis is associated with changes in eIF2B, eIF4E, and IGF-I. Am J Physiol Endocrinol Metab 278: E1133-E1143, 2000.
26. Lang CH, Frost RA, Nairn AC, MacLean DA, and Vary TC. TNF-α impairs heart and skeletal muscle protein synthesis by altering translation initiation. Am J Physiol Endocrinol Metab 282: E336-E347, 2002.
27. Lawrence JC and Abraham RT. PHAS/4E-BPs as regulators of mRNA translation and cell proliferation. Trends Biochem Sci 22:345-349, 1997.
28. Loreni F, Francesconi A, and Amaldi F. Coordinate translational regulation in the synthesis of elongation factor 1α nd ribosomal proteins in Xenopus laevis. Nucleic Acids Res 21: 4721-4725, 1993.
29. Meyuhas O and Hornstein E. Translational control of TOP mRNAs. In: Translational Control of Gene Expression, edited by Sonenberg N, Hershey JWB, and Mathews MB. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 2000, p. 671-693.
30. Montagne J, Stewart MJ, Stocker H, Hafen E, Kozma SC, and Thomas G. Drosophila S6 kinase: a regulator of cell size. Science 285: 2126-2129, 1999.
31. 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.
32. Nemenoff R, Price D, Mendelsohn M, Carter E, and Avruch J. An S6 kinase activated during liver regeneration is related to the insulin-stimulated S6 kinase in H4 hepatoma cells. J Biol Chem 263: 19455-19460, 1988.
33. Nygard O and Nika H. Identification by RNA-protein cross-linking of ribosomal proteins located at the interface between the small and the large subunits of mammalian ribosomes. EMBO J 1:357-362, 1982.
34. Nygard O and Nilsson L. Translational dynamics. Interactions between the translational factors, tRNA and ribosomes during eukaryotic protein synthesis. Eur J Biochem 191: 1-17, 1990.
35. Orellana RA, O'Connor PMJ, Nguyen HV, Bush JA, Suryawan A, Thivierge MC, Fiorotto ML, and Davis TA. Endotoxemia reduces skeletal muscle protein synthesis in neonates. Am J Physiol Endocrinol Metab 283: E909-E916, 2002.
36. Pause A, Belsham GJ, Gingras A-C, Donze O, Lin T-A, Lawrence JC, and Sonenberg N. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5'-cap function. Nature 371: 762-767, 1994.
37. Raught B and Gingras A-C. eIF4E activity is regulated at multiple levels. Int J Biochem Cell Biol 31: 43-57, 1999.
38. Raught B, Gingras A-C, and Sonenberg N. Regulation of ribosomal recruitment in eukaryotes. In: Translational Control of Gene Expression, edited by Sonenberg N, Hershey JWB, and Mathews MB. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 2000, p. 245-293.
39. Ray BK, Brendler TG, Adya S, Daniels MS, Miller JK, Hershey JW, Grifo JA, Merrick WC, and Thach RE. Role of mRNA competition in regulating translation: further characterization of mRNA discriminatory initiation factors. Proc Natl Acad Sci USA 80: 663-667, 1983.
40. Reynolds TH, Bodine SC, and Lawrence JC. Control of Ser2448 phosphorylation in the mammalian target of rapamycin by insulin and skeletal muscle load. J Biol Chem 277: 17657-17662, 2002.
41. Sarkar G, Edery I, Gallo R, and Sonenberg N. Preferential stimulation of rabbit alpha globin mRNA translation by a cap-binding protein complex. Biochim Biophys Acta 783: 122-129, 1984.
42. Scott PH, Brunn GJ, Kohn AD, Roth RA, and Lawrence JC. Evidence of insulin-stimulated phosphorylation and activation of the mammalian target of rapamycin mediated by a protein kinase B signaling pathway. Proc Natl Acad Sci USA 95: 7772-7777, 1998.
43. Sekulic A, Hudson CC, Homme JL, Yin P, 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: 3504-3523, 2000.
44. Shima H, Pende M, Chen Y, Fumagalli S, Thomas G, and Kozma SC. Disruption of the p70(S6k)/p85(S6k) gene reveals a small mouse phenotype and a new functional S6 kinase. EMBO J 17: 6649-6659, 1998.
45. Sonenberg N, Trachsel H, Hecht S, and Shatkin AJ. Differential stimulation of capped mRNA translation in vitro by cap binding protein. Nature 285: 331-333, 1980.
46. Thomas G. An encore for ribosome biogenesis in the control of cell proliferation. Nat Cell Biol 2: E71-E72, 2000.
47. Vary TC. Interorgan protein and carbohydrate metabolic relationships during sepsis: necessary evils or uncanny coincidences? Curr Opin Clin Nutr Metab Care 2: 235-242, 1999.
48. Vary TC, Jurasinski CV, Karinch AM, and Kimball SR. Regulation of eukaryotic initiation factor 2 expression in sepsis. Am J Physiol Endocrinol Metab 266: E193-E201, 1994.
49. Vary TC and Kimball SR. Effect of sepsis on eIF4E availability in skeletal muscle. Am JPhysiol Endocrinol Metab 279: E1178-E1184, 2000.
50. Welsh GI, Miller CM, Loughlin AJ, Price NT, and Proud CG. Regulation of eukaryotic initiation factor eIF2B: glycogen synthase kinase-3 phosphorylates a conserved serine which undergoes dephosphorylation in response to insulin. FEBS Lett 421: 125-130, 1998.