Activated protein synthesis and suppressed protein breakdown signaling in skeletal muscle of critically ill patients

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Jespersen, Jakob G ^a   Nedergaard, Anders ^a   Reitelseder, Søren ^a   Mikkelsen, Ulla R ^a   Dideriksen, Kasper J ^a   Agergaard, Jakob ^a   Kreiner, Frederik ^b   Pott, Frank C ^c   Schjerling, Peter ^a   Kjaer, Michael ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Rigshospitalet   (Denmark)

^c BISPEBJERG HOSPITAL   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ATROGIN 1; BRANCHED CHAIN AMINO ACID; C REACTIVE PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; HYDROCORTISONE; INITIATION FACTOR 4E BINDING PROTEIN 1; INSULIN; INTERLEUKIN 6; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MUSCLE PROTEIN; MUSCLE RING FINGER 1 PROTEIN; MYOSTATIN; PREDNISOLONE; PROTEIN KINASE B; S6 KINASE; SOMATOMEDIN C; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR FOXO; TRANSCRIPTION FACTOR FOXO 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ABDOMINAL ABSCESS; ADULT; AGED; AMINO ACID BLOOD LEVEL; ARTICLE; BLOOD ANALYSIS; BLOOD SAMPLING; CLINICAL ARTICLE; CONTROLLED STUDY; CRITICALLY ILL PATIENT; DEATH; FEMALE; HEART ARREST; HEPATIC COMA; HUMAN; HUMAN TISSUE; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN INFUSION; INTENSIVE CARE UNIT; INTESTINE NECROSIS; INTESTINE PERFORATION; MALE; MUSCLE BIOPSY; NON INSULIN DEPENDENT DIABETES MELLITUS; OUTCOME ASSESSMENT; PERITONITIS; PNEUMONIA; PROTEIN BLOOD LEVEL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RESPIRATORY FAILURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEPSIS; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; THORAX INJURY; ULCER PERFORATION; WESTERN BLOTTING; CASE CONTROL STUDY; CRITICAL ILLNESS; GENETICS; METABOLISM; MIDDLE AGED; PHYSIOLOGY;

EUKARYOTA; MAMMALIA;

ADULT; AGED; BLOTTING, WESTERN; CASE-CONTROL STUDIES; CRITICAL ILLNESS; FEMALE; HUMANS; MALE; MIDDLE AGED; MUSCLE PROTEINS; MUSCLE, SKELETAL; PROTEIN BIOSYNTHESIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 79953299011     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018090     Document Type: Article

References (83)

1. Janssen I, Heymsfield SB, Wang ZM, Ross R, (2000) Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. J Appl Physiol 89: 81-88.
2. Schols AM, Broekhuizen R, Weling-Scheepers CA, Wouters EF, (2005) Body composition and mortality in chronic obstructive pulmonary disease. Am J Clin Nutr 82: 53-59.
3. Evans WJ, Morley JE, Argiles J, Bales C, Baracos V, et al. (2008) Cachexia: a new definition. Clin Nutr 27: 793-799.
4. Plank LD, Hill GL, (2000) Similarity of changes in body composition in intensive care patients following severe sepsis or major blunt injury. Ann NY Acad Sci 904: 592-602.
5. Helliwell TR, Wilkinson A, Griffiths RD, McClelland P, Palmer TE, et al. (1998) Muscle fibre atrophy in critically ill patients is associated with the loss of myosin filaments and the presence of lysosomal enzymes and ubiquitin. Neuropathol Appl Neurobiol 24: 507-517.
6. Helliwell TR, Coakley JH, Wagenmakers AJ, Griffiths RD, Campbell IT, et al. (1991) Necrotizing myopathy in critically-ill patients. J Pathol 164: 307-314.
7. Gruther W, Benesch T, Zorn C, Paternostro-Sluga T, Quittan M, et al. (2008) Muscle wasting in intensive care patients: ultrasound observation of the M. quadriceps femoris muscle layer. J Rehabil Med 40: 185-189.
8. Poulsen JB, Moller K, Jensen CV, Weisdorf S, Kehlet H, et al. (2010) Effect of transcutaneous electrical muscle stimulation on muscle volume in patients with septic shock. Crit Care Med. In press.
9. Sandri M, (2008) Signaling in muscle atrophy and hypertrophy. Physiology (Bethesda) 23: 160-170.
10. Lang CH, Frost RA, Vary TC, (2007) Regulation of muscle protein synthesis during sepsis and inflammation. Am J Physiol Endocrinol Metab 293: E453-459.
11. Glass DJ, (2005) Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol 37: 1974-1984.
12. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, et al. (2004) Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117: 399-412.
13. Zhao J, Brault JJ, Schild A, Cao P, Sandri M, et al. (2007) FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 6: 472-483.
14. Senf SM, Dodd SL, Judge AR, (2010) FOXO signaling is required for disuse muscle atrophy and is directly regulated by Hsp70. Am J Physiol Cell Physiol 298: C38-45.
15. Brault JJ, Jespersen JG, Goldberg AL, (2010) Peroxisome proliferator-activated receptor gamma coactivator 1alpha or 1beta overexpression inhibits muscle protein degradation, induction of ubiquitin ligases, and disuse atrophy. J Biol Chem 285: 19460-19471.
16. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, et al. (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708.
17. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, et al. (2004) Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18: 39-51.
18. Jespersen J, Kjaer M, Schjerling P, (2006) The possible role of myostatin in skeletal muscle atrophy and cachexia. Scand J Med Sci Sports 16: 74-82.
19. Jespersen JG, Nedergaard A, Andersen LL, Schjerling P, Andersen JL, (2009) Myostatin expression during human muscle hypertrophy and subsequent atrophy: increased myostatin with detraining. Scand J Med Sci Sports. In press.
20. Lee SJ, (2004) Regulation of muscle mass by myostatin. Annu Rev Cell Dev Biol 20: 61-86.
21. Sugita H, Kaneki M, Sugita M, Yasukawa T, Yasuhara S, et al. (2004) Burn injury impairs insulin-stimulated Akt/PKB activation in skeletal muscle. Am J Physiol Endocrinol Metab 288: E585-591.
22. Crossland H, Constantin-Teodosiu D, Gardiner SM, Constantin D, Greenhaff PL, (2008) A potential role for Akt/FOXO signalling in both protein loss and the impairment of muscle carbohydrate oxidation during sepsis in rodent skeletal muscle. J Physiol 586: 5589-5600.
23. Fredriksson K, Tjader I, Keller P, Petrovic N, Ahlman B, et al. (2008) Dysregulation of mitochondrial dynamics and the muscle transcriptome in ICU patients suffering from sepsis induced multiple organ failure. PloS ONE 3: e3686.
24. Van den Berghe G, Wilmer A, Hermans G, Meersseman W, Wouters PJ, et al. (2006) Intensive insulin therapy in the medical ICU. N Engl J Med 354: 449-461.
25. van den Berghe G, Wouters P, Weekers F, Verwaest C, Bruyninckx F, et al. (2001) Intensive insulin therapy in the critically ill patients. N Engl J Med 345: 1359-1367.
26. Reitelseder S, Agergaard J, Doessing S, Helmark IC, Lund P, et al. (2011) Whey and casein labeled with L-[1-13C]leucine and muscle protein synthesis: effect of resistance exercise and protein ingestion. Am J Physiol Endocrinol Metab 300: E231-242.
27. Frystyk J, Dinesen B, Orskov H, (1995) Non-competitive time-resolved immunofluorometric assays for determination of human insulin-like growth factor I and II. Growth Regul 5: 169-176.
28. Bergstrom J, (1962) Muscle electrolytes in man. Scand J Clin Lab Invest 68: 1-110.
29. Chomczynski P, Sacchi N, (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159.
30. Engelman JA, Luo J, Cantley LC, (2006) The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet 7: 606-619.
31. Lang CH, Frost RA, (2007) Sepsis-induced suppression of skeletal muscle translation initiation mediated by tumor necrosis factor alpha. Metabolism 56: 49-57.
32. Lang CH, Frost RA, (2005) Endotoxin disrupts the leucine-signaling pathway involving phosphorylation of mTOR, 4E-BP1, and S6K1 in skeletal muscle. J Cell Physiol 203: 144-155.
33. Fang CH, Li B, James JH, Yahya A, Kadeer N, et al. (2007) GSK-3beta activity is increased in skeletal muscle after burn injury in rats. Am J Physiol Regul Integr Comp Physiol 293: R1545-1551.
34. Langouche L, Vander Perre S, Wouters PJ, D'Hoore A, Hansen TK, et al. (2007) Effect of intensive insulin therapy on insulin sensitivity in the critically ill. J Clin Endocrinol Metab 92: 3890-3897.
35. Saberi F, Heyland D, Lam M, Rapson D, Jeejeebhoy K, (2008) Prevalence, incidence, and clinical resolution of insulin resistance in critically ill patients: an observational study. JPEN J Parenter Enteral Nutr 32: 227-235.
36. Biolo G, De Cicco M, Lorenzon S, Dal Mas V, Fantin D, et al. (2008) Treating hyperglycemia improves skeletal muscle protein metabolism in cancer patients after major surgery. Crit Care Med 36: 1768-1775.
37. Gore DC, Wolf SE, Sanford AP, Herndon DN, Wolfe RR, (2004) Extremity hyperinsulinemia stimulates muscle protein synthesis in severely injured patients. Am J Physiol Endocrinol Metab 286: E529-534.
38. Biolo G, Fleming RY, Maggi SP, Nguyen TT, Herndon DN, et al. (2002) Inverse regulation of protein turnover and amino acid transport in skeletal muscle of hypercatabolic patients. J Clin Endocrinol Metab 87: 3378-3384.
39. Kimball SR, Jefferson LS, (2006) New functions for amino acids: effects on gene transcription and translation. Am J Clin Nutr 83: 500S-507S.
40. Anthony JC, Reiter AK, Anthony TG, Crozier SJ, Lang CH, et al. (2002) 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.
41. Lang CH, Frost RA, (2004) Differential effect of sepsis on ability of leucine and IGF-I to stimulate muscle translation initiation. Am J Physiol Endocrinol Metab 287: E721-730.
42. Druml W, Heinzel G, Kleinberger G, (2001) Amino acid kinetics in patients with sepsis. Am J Clin Nutr 73: 908-913.
43. Roth E, Zoch G, Schulz F, Karner J, Muhlbacher F, et al. (1985) Amino acid concentrations in plasma and skeletal muscle of patients with acute hemorrhagic necrotizing pancreatitis. Clin Chem 31: 1305-1309.
44. Doucet M, Russell AP, Leger B, Debigare R, Joanisse DR, et al. (2007) Muscle atrophy and hypertrophy signaling in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 176: 261-269.
45. Tjader I, Rooyackers O, Forsberg AM, Vesali RF, Garlick PJ, et al. (2004) Effects on skeletal muscle of intravenous glutamine supplementation to ICU patients. Intensive Care Med 30: 266-275.
46. Fluck M, Mund SI, Schittny JC, Klossner S, Durieux AC, et al. (2008) Mechano-regulated tenascin-C orchestrates muscle repair. Proc Natl Acad Sci U S A 105: 13662-13667.
47. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, et al. (2007) FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6: 458-471.
48. Furuyama T, Kitayama K, Yamashita H, Mori N, (2003) Forkhead transcription factor FOXO1 (FKHR)-dependent induction of PDK4 gene expression in skeletal muscle during energy deprivation. Biochem J 375: 365-371.
49. Cho JE, Fournier M, Da X, Lewis MI, (2009) Time Course Expression of Foxo Transcription Factors in Skeletal Muscle Following Corticosteroid Administration. J Appl Physiol 108: 137-145.
50. Nystrom GJ, Lang CH, (2008) Sepsis and AMPK Activation by AICAR Differentially Regulate FoxO-1,-3 and-4 mRNA in Striated Muscle. Int J Clin Exp Med 1: 50-63.
51. Smith IJ, Alamdari N, O'Neal P, Gonnella P, Aversa Z, et al. (2010) Sepsis increases the expression and activity of the transcription factor Forkhead Box O 1 (FOXO1) in skeletal muscle by a glucocorticoid-dependent mechanism. Int J Biochem Cell Biol 42: 701-711.
52. Greer EL, Oskoui PR, Banko MR, Maniar JM, Gygi MP, et al. (2007) The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J Biol Chem 282: 30107-30119.
53. Nakae J, Kitamura T, Silver DL, Accili D, (2001) The forkhead transcription factor Foxo1 (Fkhr) confers insulin sensitivity onto glucose-6-phosphatase expression. J Clin Invest 108: 1359-1367.
54. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, et al. (2004) The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14: 395-403.
55. Kamei Y, Miura S, Suzuki M, Kai Y, Mizukami J, et al. (2004) Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, down-regulated Type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J Biol Chem 279: 41114-41123.
56. McLoughlin TJ, Smith SM, DeLong AD, Wang H, Unterman TG, et al. (2009) FoxO1 induces apoptosis in skeletal myotubes in a DNA-binding-dependent manner. Am J Physiol Cell Physiol 297: C548-555.
57. Sacheck JM, Ohtsuka A, McLary SC, Goldberg AL, (2004) IGF-I stimulates muscle growth by suppressing protein breakdown and expression of atrophy-related ubiquitin ligases, atrogin-1 and MuRF1. Am J Physiol Endocrinol Metab 287: E591-601.
58. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, et al. (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3: 1014-1019.
59. Mikura M, Yamaoka I, Doi M, Kawano Y, Nakayama M, et al. (2009) Glucose infusion suppresses surgery-induced muscle protein breakdown by inhibiting ubiquitin-proteasome pathway in rats. Anesthesiology 110: 81-88.
60. Krogh-Madsen R, Plomgaard P, Keller P, Keller C, Pedersen BK, (2004) Insulin stimulates interleukin-6 and tumor necrosis factor-alpha gene expression in human subcutaneous adipose tissue. Am J Physiol Endocrinol Metab 286: E234-238.
61. Greenhaff PL, Karagounis LG, Peirce N, Simpson EJ, Hazell M, et al. (2008) Disassociation between the effects of amino acids and insulin on signaling, ubiquitin ligases, and protein turnover in human muscle. Am J Physiol Endocrinol Metab 295: E595-604.
62. Timmerman KL, Lee JL, Dreyer HC, Dhanani S, Glynn EL, et al. (2010) Insulin stimulates human skeletal muscle protein synthesis via an indirect mechanism involving endothelial-dependent vasodilation and mammalian target of rapamycin complex 1 signaling. J Clin Endocrinol Metab 95: 3848-3857.
63. Hasselgren PO, Warner BW, James JH, Takehara H, Fischer JE, (1987) Effect of insulin on amino acid uptake and protein turnover in skeletal muscle from septic rats. Evidence for insulin resistance of protein breakdown. Arch Surg 122: 228-233.
64. Vary TC, Dardevet D, Grizard J, Voisin L, Buffiere C, et al. (1998) Differential regulation of skeletal muscle protein turnover by insulin and IGF-I after bacteremia. Am J Physiol 275: E584-593.
65. Tischler ME, Fagan JM, (1983) Response to trauma of protein, amino acid, and carbohydrate metabolism in injured and uninjured rat skeletal muscles. Metabolism 32: 853-868.
66. Dehoux M, Gobier C, Lause P, Bertrand L, Ketelslegers JM, et al. (2007) IGF-I does not prevent myotube atrophy caused by proinflammatory cytokines despite activation of Akt/Foxo and GSK-3beta pathways and inhibition of atrogin-1 mRNA. Am J Physiol Endocrinol Metab 292: E145-150.
67. Sartori R, Milan G, Patron M, Mammucari C, Blaauw B, et al. (2009) Smad2 and 3 Transcription Factors Control Muscle Mass in Adulthood. Am J Physiol Cell Physiol 296: C1248-C1257.
68. Lee SJ, (2007) Quadrupling Muscle Mass in Mice by Targeting TGF-beta Signaling Pathways. PLoS ONE 2: e789.
69. Lee SJ, Reed LA, Davies MV, Girgenrath S, Goad ME, et al. (2005) Regulation of muscle growth by multiple ligands signaling through activin type II receptors. Proc Natl Acad Sci USA 102: 18117-18122.
70. McPherron AC, Huynh TV, Lee SJ, (2009) Redundancy of myostatin and growth/differentiation factor 11 function. BMC Dev Biol 9: 24.
71. Bassel-Duby R, Olson EN, (2006) Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem 75: 19-37.
72. Rabuel C, Renaud E, Brealey D, Ratajczak P, Damy T, et al. (2004) Human septic myopathy: induction of cyclooxygenase, heme oxygenase and activation of the ubiquitin proteolytic pathway. Anesthesiology 101: 583-590.
73. Grander W, Dunser M, Stollenwerk B, Siebert U, Dengg C, et al. (2010) C-reactive protein levels and post-ICU mortality in nonsurgical intensive care patients. Chest 138: 856-862.
74. Ho KM, Lee KY, Dobb GJ, Webb SA, (2008) C-reactive protein concentration as a predictor of in-hospital mortality after ICU discharge: a prospective cohort study. Intensive Care Med 34: 481-487.
75. Gamrin L, Essen P, Forsberg AM, Hultman E, Wernerman J, (1996) A descriptive study of skeletal muscle metabolism in critically ill patients: free amino acids, energy-rich phosphates, protein, nucleic acids, fat, water, and electrolytes. Crit Care Med 24: 575-583.
76. Plank LD, Hill GL, (2000) Sequential metabolic changes following induction of systemic inflammatory response in patients with severe sepsis or major blunt trauma. World J Surg 24: 630-638.
77. Lang CH, Frost RA, Summer AD, Vary TC, (2005) Molecular mechanisms responsible for alcohol-induced myopathy in skeletal muscle and heart. Int J Biochem Cell Biol 37: 2180-2195.
78. Lexell J, Taylor CC, Sjostrom M, (1988) What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 84: 275-294.
79. Song YH, Li Y, Du J, Mitch WE, Rosenthal N, et al. (2005) Muscle-specific expression of IGF-1 blocks angiotensin II-induced skeletal muscle wasting. J Clin Invest 115: 451-458.
80. Schulze PC, Fang J, Kassik KA, Gannon J, Cupesi M, et al. (2005) Transgenic overexpression of locally acting insulin-like growth factor-1 inhibits ubiquitin-mediated muscle atrophy in chronic left-ventricular dysfunction. Circ Res 97: 418-426.
81. Dehoux M, Van BR, Pasko N, Lause P, Verniers J, et al. (2004) Role of the insulin-like growth factor I decline in the induction of atrogin-1/MAFbx during fasting and diabetes. Endocrinology 145: 4806-4812.
82. Vogt PK, Jiang H, Aoki M, (2005) Triple layer control: phosphorylation, acetylation and ubiquitination of FOXO proteins. Cell Cycle 4: 908-913.
83. Finfer S, Chittock DR, Su SY, Blair D, Foster D, et al. (2009) Intensive versus conventional glucose control in critically ill patients. N Engl J Med 360: 1283-1297.