IGF-I stimulates protein synthesis in skeletal muscle through multiple signaling pathways during sepsis

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 290, Issue 2, 2006, Pages

  Vary, Thomas C ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

4E binding protein 1; Eukaryotic initiation factor 4E; Eukaryotic initiation factor 4G; Eukaryotic initiation factors; Gastrocnemius; Messenger ribonuclease; Ribosomal protein S6 kinase 1; Translation initiation

Indexed keywords

CARRIER PROTEIN; EIF4EBP1 PROTEIN, RAT; INITIATION FACTOR 4E; INITIATION FACTOR 4G; MAMMALIAN TARGET OF RAPAMYCIN; MUSCLE PROTEIN; PHOSPHOPROTEIN; PROTEIN KINASE; S6 KINASE; SOMATOMEDIN C;

ANIMAL; ARTICLE; BIOSYNTHESIS; DRUG EFFECT; MALE; METABOLISM; PHOSPHORYLATION; RAT; SEPSIS; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT;

ANIMALS; CARRIER PROTEINS; EUKARYOTIC INITIATION FACTOR-4E; EUKARYOTIC INITIATION FACTOR-4G; INSULIN-LIKE GROWTH FACTOR I; MALE; MUSCLE PROTEINS; MUSCLE, SKELETAL; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY; RIBOSOMAL PROTEIN S6 KINASES; SEPSIS;

EID: 33644864086     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00333.2005     Document Type: Article

References (64)

1. American College of Chest Physician, and Society of Critical Care Medicine Consensus Conference. Definitions for sepsis and organ failure and guidelines for use of innovative therapies in sepsis. Crit Care Med 20: 864-875, 1992.
2. Avruch J. Insulin signal transduction through protein kinase cascades. Mol Cell Biochem 182: 31-42, 1998.
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. Bylund-Fellenius AC, Ojamaa KM, Flaim KE, Li JB, Wassner SJ, and Jefferson LS. Protein synthesis versus energy state in contracting muscle of perfused rat hindlimb. Am J Physiol Endocrinol Metab 246: E297-E305, 1984.
5. Cooney R, Owens E, Jurasinski C, Gray K, Vannice J, and Vary T. Interleukin-1 receptor antagonist prevents sepsis-induced inhibition of protein synthesis. Am J Physiol Endocrinol Metab 267: E636-E641, 1994.
6. Cooney RN, Kimball SR, and Vary TC. Regulation of skeletal muscle protein turnover during sepsis: mechanisms and mediators. Shock 7: 1-16, 1998.
7. Dardevet D, Sornet C, Attaix D, Baracos VE, and Grizard J. Insulin-like growth factor-I and insulin resistance in skeletal muscle of adult and old rats. Endocrinology 134: 1475-1484, 1994.
8. Dickerson RN, Manzo CB, Charland SL, Settle RG, Kuhl DA, and Rajter JJ. The effects of insulin-like growth factor-1 on protein metabolism and hepatic response to endotoxin in parenterally fed rats. J Surg Res 58: 260-266, 1995.
9. Drnevich D and Vary TC. Analysis of physiological amino acids using dabsyl derivatization and reverse-phase liquid chromatography. J Chromatogr A 613: 137-144, 1993.
10. Farrari S and Thomas G. S6 phosphorylation and the p70(s6k)/p85(s6k). Crit Rev Biochem Mol Biol 29: 385-413, 1994.
11. Gingras AC, Gygi SP, and Raught B. Regulation of 4E-BP1 phosphorylation: a novel 2-step mechanism. Genes Dev 13: 1422-1437, 1999.
12. Gingras AC, Raught B, and Sonenberg N. Regulation of translation initiation by FRAP/TOR. Genes Dev 15: 807-826, 2001.
13. Haghihat A, Maderr S, Pause A, and Sonenberg N. Repression of cap-dependent translation by 4E-binding protein I: competition with p220 for binding to eukaryotic initiation factor-4E. EMBO J 14: 5701-5709, 1995.
14. Jefferson LS, Vary TC, and Kimball SR. Regulation of protein metabolism in muscle. In: Handbook of Physiology, edited by Jefferson LS and Cherrington AD. New York: Oxford University Press, 2001, p. 529-552.
15. Jurasinski CV, Gray K, and Vary TC. Modulation of skeletal muscle protein synthesis by amino acids and insulin during sepsis. Metabolism 44: 1130-1138, 1995.
16. Jurasinski CV, Kilpatrick L, and Vary TC. Amrinone prevents muscle protein wasting during chronic sepsis. Am J Physiol Endocrinol Metab 268: E491-E500, 1995.
17. Jurasinski CV and Vary TC. Insulin-like growth factor-I accelerates protein synthesis during sepsis. Am J Physiol Endocrinol Metab 269: E977-E981, 1995.
18. Kimball S, Jefferson L, Fadden P, Haystead T, and Lawrence J Jr. Insulin and diabetes cause reciprocal changes in the association of eIF-4E and PHAS-I in rat skeletal muscle. Am J Physiol Cell Physiol 270: C705-C709, 1996.
19. Kimball S, Jurasinski C, Lawrence J Jr, and Jefferson L. Insulin stimulates protein synthesis in skeletal muscle by enhancing the association of eIF-4E and eIF-4G. Am J Physiol Cell Physiol 272: C754-C759, 1997.
20. Kozma SC and Thomas G. p70s6k/p85s6k: mechanism of activation and role in mitogenesis. Cancer Biol 5: 255-266, 1994.
21. Lamphear BJ, Kirchweger JR, Skern T, and Rhoads RE. Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF-4G) with pircoviral proteases. Implication for cap-dependent and cap-independent translation initiation. J Biol Chem 270: 21975-21983, 1995.
22. 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.
23. 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.
24. Lang CH, Frost RA, Svanberg E, and Vary TC. IGF-I/IGFBP-3 ameliorates alterations in protein synthesis, eIF4E availability, and myostatin in alcohol-fed rats. Am J Physiol Endocrinol Metab 286: E916-E926, 2004.
25. Lang CH, Fan J, Cooney R, and Vary TC. IL-1 receptor antagonist attenuates sepsis-induced alterations in IGF system and protein synthesis. Am J Physiol Endocrinol Metab 270: E430-E437, 1996.
26. Lin T, Kong X, Haystead T, Pause A, Belsham G, Sonnenberg N, and Lawrence J. PHAS-I as a link between mitogen activated protein kinase and translation initiation. Science 266: 653-656, 1994.
27. Mader S, Lee H, Pause A, and Sonnenberg N. The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4 gamma and the translational repressors 4E-binding proteins. Mol Cell Biol 15: 4900-4907, 1995.
28. Morley SJ and Traugh JA. Differential stimulation of phosphorylation of initiation factors eIF-4F, eIF-4B, eIF-3 and ribosomal protein S6 by insulin and phorbol esters. J Biol Chem 265: 10611-10616, 1990.
29. Nakatani T, Sato T, Marzella L, Hirai F, Trump FB, and Siegel JH. Hepatic and systemic metabolic response to aerobic and anaerobic intra-abdominal abscess in a highly reproducible chronic rat model. Circ Shock 73: 2271-2294, 1984.
30. Pause A, Belsham GJ, Gingras AC, Donze O, Lin TA, Lawrence JC Jr, and Sonenberg N. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′ -cap function. Nature 371: 762-767, 1994.
31. Peterson RT, Beal PA, Comb MJ, and Schreiber SL. FKBP12-rapamycin- associated protein (FRAP) autophosphorylates at serine 2481 under translationally repressive conditions. J Biol Chem 275: 7416-7423, 2000.
32. Plank LD, Connolly AB, and Hill AG. Sequential changes in the metabolic response in severely septic patients during the first 23 days after onset of peritonitis. Ann Surg 228: 146-158, 1998.
33. Ptushkina M, von der Harr T, Karim MM, Hughes JM, and McCarthy JE. Repressor binding to a dual regulatory site traps human eIF4E in a high cap-affinity state. EMBO J 18: 4068-4075, 1999.
34. Pyronnet SE, Dotsie J, and Sonnenberg N. Suppression of cap-dependent translation in mitosis. Genes Dev 15: 2083-2093, 2001.
35. Raught B, Gingras AC, and Sonenberg N. The target of rapamycin (TOR) proteins. Proc Natl Acad Sci USA 98: 7037-7044, 2001.
36. Raught B and Gingras AC. eIF4E activity is regulated at multiple levels. Int J Biochem Cell Biol 31: 43-57, 1999.
37. Raught B, Gingras AC, Gygi SP, Imaataka H, Morino S, Gradi A, Aebersold R, and Sonenberg N. Serum-stimulated, rapamycin-sensitive phosphorylation sites in eukaryotic translation initiation factor 4GI. EMBO J 19: 434-444, 2000.
38. Rhoads RE. Regulation of eukaryotic protein synthesis by initiation factors. J Biol Chem 268: 3017-3020, 1993.
39. Rhoads RE, Joshi-Barve S, and Minich WB. Participation of initiation factors in recruitment of mRNA to ribosomes. Biochimie 76: 831-838, 1994.
40. Shen WH, Boyle DW, PW, Bade A, and Liechty EA. Insulin and IGF-I stimulate the formation of the eukaryotic initiation factor 4F complex and protein synthesis in C2C12 myotubes independent of availability of external amino acids. J Endocrinol 185: 275-289, 2005.
41. Shen W, Mallon D, Boyle BW, and Liechty EA. IGF-I and insulin regulate eIF4F formation by different mechanisms in muscle and liver in ovine fetus. Am J Physiol Endocrinol Metab 283: E593-E603, 2002.
42. Sonenberg N. Regulation of translation and cell growth by eIF-4E. Biochimie 76: 839-846, 1994.
43. Svanberg E, Frost RA, Lang CH, Isgaard J, Jefferson LS, Kimball SR, and Vary TC. IGF-I/IGFBP-3 binary complex modulates sepsis induced inhibition of protein synthesis in skeletal muscle. Am J Physiol Endocrinol Metab 279: E1145-E1158, 2000.
44. Tsukiyama-Kohara K, Vidal SM, Gingras AC, Glover TW, Hanash SM, Heng H, and Sonenberg N. Tissue distribution, genomic structure, and chromosome mapping of mouse and human eukaryotic initiation factor 4E-binding proteins 1 and 2. Genomics 38: 353-356, 1996.
45. Vary T, Dardevet D, Grizard J, Voisin L, Buffiere C, Denis P, Brueille D, and Obled C. Differential regulation of skeletal muscle protein turnover by insulin and IGF-I following bacteremia. Am J Physiol Endocrinol Metab 275: E584-E593, 1998.
46. Vary TC. Interorgan protein and carbohydrate metabolic relationships during sepsis: necessary evils or uncanny coincidences? Curr Opin Clin Nutr Metabol Care 2: 235-242, 1999.
47. Vary TC. Regulation of skeletal muscle protein turnover in sepsis. Curr Opin Clin Nutr Metab Care 1: 217-224, 1998.
48. Vary TC and Deiter G. Long-term alcohol administration inhibits synthesis of both myofibrillar and sarcoplasmic proteins. Metabolism 54: 212-219, 2005.
49. Vary TC, Deiter G, and Goodman SA. Acute alcohol intoxication enhances myocardial eIF4G phosphorylation despite reducing mTOR signaling. Am J Physiol Heart Circ Physiol 288: H121-H128, 2005.
50. Vary TC, Jefferson LS, and Kimball SR. Amino acid-induced stimulation of translation initiation in rat skeletal muscle. Am J Physiol Endocrinol Metab 277: E1077-E1086, 1999.
51. Vary TC, Jefferson LS, and Kimball SR. Insulin fails to stimulate muscle protein synthesis in sepsis despite unimpaired signaling to 4E-BP1 and S6K1. Am J Physiol Endocrinol Metab 281: E1045-E1053, 2001.
52. Vary TC, Jefferson LS, and Kimball SR. Role of eIF4E in stimulation of protein synthesis by IGF-I in perfused skeletal muscle. Am J Physiol Endocrinol Metab 278: E58-E64, 2000.
53. Vary TC, Jurasinski CV, and Kimball SR. Reduced 40S initiation complex formation in skeletal muscle during sepsis. Mol Cell Biochem 178: 81-86, 1998.
54. Vary TC and Kimball SR. Effect of sepsis on eIF4E availability in skeletal muscle. Am J Physiol Endocrinol Metab 279: E1178-E1184, 2000.
55. Vary TC and Kimball SR. Sepsis-induced changes in protein synthesis: differential effects on fast- and slow-twitch muscles. Am J Physiol Cell Physiol 262: C1513-C1519, 1992.
56. Vary TC, Lynch CJ, and Lang CH. Effects of chronic alcohol consumption on regulation of myocardial protein synthesis. Am J Physiol Heart Circ Physiol 281: H1242-H1251, 2001.
57. Vary TC, Siegel JH, Tall BD, and Morris JG. Role of anaerobic bacteria in intra-abdominal septic abscesses in mediating septic control of skeletal muscle glucose oxidation and lactic acidemia. J Trauma 29: 1003-1014, 1989.
58. Vary TC, Voisin L, and Cooney RN. Regulation of peptide-chain initiation during sepsis by interleukin-1 receptor antagonist. Am J Physiol Endocrinol Metab 271: E309-E316, 1996.
59. Voisin L, Gray K, Flowers KM, Kimball SR, Jefferson LS, and Vary TC. Altered expression of eukaryotic initiation factor 2B in skeletal muscle during sepsis. Am J Physiol Endocrinol Metab 270: E43-E50, 1996.
60. Waskiewicz AJ, Flynn A, Proud CG, and Cooper JA. Mitogenactivated protein kinases activate the serine/threonine kinases MNK1 and MNK2. EMBO J 16: 1909-1920, 1997.
61. Wells SE, Hillner PE, Vale RD, and Sachs AB. Circularization of mRNA by eukaryotic translation initiation factors. Mol Cell 2: 135-140, 1998.
62. Weng QP, Anadrabi K, Kozlowski MT, Grove JR, and Avruch J. Multiple independent inputs are required for activation of the p70 S6 kinase. Mol Cell Biol 15: 2333-2340, 1998.
63. Weng QP, Kozlowski M, Belham C, Zhang A, Comb MJ, and Avruch J. Regulation of the p70 S6 kinase by phosphorylation in vivo: Analysis using site-specific anti-phosphopeptide antibodies. J Biol Chem 273: 16621-16629, 1998.
64. Wilmore DW. Metabolic response to severe surgical illness: overview. World J Surg 24: 705-711, 2000.