Development aggravates the severity of skeletal muscle catabolism induced by endotoxemia in neonatal pigs

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 302, Issue 6, 2012, Pages 682-690

  Orellana, Renán A ^a,b   Suryawan, Agus ^a   Wilson, Fiona A ^a   Gazzaneo, María C ^a,b   Fiorotto, Marta L ^a   Nguyen, Hanh V ^a   Davis, Teresa A ^a  

^a CHILDREN S NUTRITION RESEARCH CENTER   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Adenosine 5= monophospate kinase; Muscle wasting; Plasma actin

Indexed keywords

3 METHYLHISTIDINE; ALPHA ACTIN; AMINO ACID; ATROGIN 1; CASPASE 3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; MUSCLE PROTEIN; PROCASPASE 3; TRANSCRIPTION FACTOR FOXC1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOTOXEMIA; MUSCLE METABOLISM; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; SKELETAL MUSCLE; SWINE;

ACTINS; AMINO ACIDS; ANIMALS; ANIMALS, NEWBORN; CASPASE 3; DISEASE MODELS, ANIMAL; ENDOTOXEMIA; ENDOTOXINS; ESCHERICHIA COLI INFECTIONS; INSULIN; METABOLISM; MUSCLE PROTEINS; MUSCLE, SKELETAL; NF-KAPPA B; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SEVERITY OF ILLNESS INDEX; SWINE;

EID: 84858213242     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00259.2011     Document Type: Article

References (44)

1. Cai D, Frantz JD, Tawa NE Jr, Melendez PA, Oh BC, Lidov HG, Hasselgren PO, Frontera WR, Lee J, Glass DJ and Shoelson SE. IKKβ/NF-κB activation causes severe muscle wasting in mice. Cell 119: 285-298, 2004.
2. Cooney RN, Owens E, Slaymaker D, Vary TC. Prevention of skeletal muscle catabolism in sepsis does not impair visceral protein metabolism. Am J Physiol Endocrinol Metab 270: E621-E626, 1996.
3. Davis TA, Fiorotto ML. Regulation of muscle growth in neonates. Curr Opin Clin Nutr Metab Care 12: 78-85, 2009.
4. Davis TA, Suryawan A, Orellana RA, Nguyen HV, Fiorotto ML. Postnatal ontogeny of skeletal muscle protein synthesis in pigs. J Anim Sci 86: E13-E18, 2008.
5. Doucet M, Russell AP, Leger B, Debigare R, Joanisse DR, Caron MA, LeBlanc P, Maltais F. Muscle atrophy and hypertrophy signaling in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 176: 261-269, 2007.
6. Drummond MJ, Dreyer HC, Pennings B, Fry CS, Dhanani S, Dillon EL, Sheffield-Moore M, Volpi E, Rasmussen BB. Skeletal muscle protein anabolic response to resistance exercise and essential amino acids is delayed with aging. J Appl Physiol 104: 1452-1461, 2008.
7. Evans WJ, Morley JE, Argiles J, Bales C, Baracos V, Guttridge D, Jatoi A, Kalantar-Zadeh K, Lochs H, Mantovani G, Marks D, Mitch WE, Muscaritoli M, Najand A, Ponikowski P, Rossi FF, Schambelan M, Schols A, Schuster M, Thomas D, Wolfe R, Anker SD. Cachexia: a new definition. Clin Nutr 27: 793-799, 2008.
8. Gao Y, Ordas R, Klein JD, Price SR. Regulation of caspase-3 activity by insulin in skeletal muscle cells involves both PI3-kinase and MEK-1/2. J Appl Physiol 105: 1772-1778, 2008.
9. Glass DJ. Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol 37: 1974-1984, 2005.
10. Hasselgren PO, Fischer JE. Sepsis: stimulation of energy-dependent protein breakdown resulting in protein loss in skeletal muscle. World J Surg 22: 203-208, 1998.
11. Hasselgren PO, Pedersen P, Sax HC, Warner BW, Fischer JE. Current concepts of protein turnover and amino acid transport in liver and skeletal muscle during sepsis. Arch Surg 123: 992-999, 1988.
12. Jurasinski C, Gray K, Vary TC. Modulation of skeletal muscle protein synthesis by amino acids and insulin during sepsis. Metabolism 44: 1130-1138, 1995.
13. Krawiec BJ, Nystrom GJ, Frost RA, Jefferson LS, Lang CH. AMPactivated protein kinase agonists increase mRNA content of the musclespecific ubiquitin ligases MAFbx and MuRF1 in C2C12 cells. Am J Physiol Endocrinol Metab 292: E1555-E1567, 2007.
14. Lang CH. Sepsis-induced changes in pancreatic hormone secretion. In: Handbook of Physiology, edited by Jefferson LS and Cherrington AD. Oxford, UK: Oxford University Press, 2001, p. 999-1013.
15. Lang CH, Frost RA, Vary TC. Regulation of muscle protein synthesis during sepsis and inflammation. Am J Physiol Endocrinol Metab 293: E453-E459, 2007.
16. Levine S, Nguyen T, Taylor N, Friscia ME, Budak MT, Rothenberg P, Zhu J, Sachdeva R, Sonnad S, Kaiser LR, Rubinstein NA, Powers SK, Shrager JB. Rapid disuse atrophy of diaphragm fibers in mechanically ventilated humans. N Engl J Med 358: 1327-1335, 2008.
17. Li YP, Chen Y, John J, Moylan J, Jin B, Mann DL, Reid MB. TNF-alpha acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin1/MAFbx in skeletal muscle. FASEB J 19: 362-370, 2005.
18. Martinez-Amat A, Boulaiz H, Prados J, Marchal JA, Padial PP, Caba O, Rodriguez-Serrano F, Aranega A. Release of alpha-actin into serum after skeletal muscle damage. Br J Sports Med 39: 830-834, 2005.
19. McKinnell IW, Rudnicki MA. Molecular mechanisms of muscle atrophy. Cell 119: 907-910, 2004.
20. Michie HR. Metabolism of sepsis and multiple organ failure. World J Surg 20: 460-464, 1996.
21. Moylan JS, Smith JD, Chambers MA, McLoughlin TJ, Reid MB. TNF induction of atrogin-1/MAFbx mRNA depends on Foxo4 expression but not AKT-Foxo1/3 signaling. Am J Physiol Cell Physiol 295: C986-C993, 2008.
22. Nader GA. Molecular determinants of skeletal muscle mass: getting the "AKT" together. Int J Biochem Cell Biol 37: 1985-1996, 2005.
23. Nystrom GJ, Lang CH. 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, 2008.
24. O'Connor PM, Kimball SR, Suryawan A, Bush JA, Nguyen HV, Jefferson LS, Davis TA. Regulation of translation initiation by insulin and amino acids in skeletal muscle of neonatal pigs. Am J Physiol Endocrinol Metab 285: E40-E53, 2003.
25. O'Connor PMJ, Kimball SR, Suryawan A, Bush JA, Nguyen HV, Jefferson LS, Davis TA. Regulation of neonatal liver protein synthesis by insulin and amino acids in pigs. Am J Physiol Endocrinol Metab 286: E994-E1003, 2004.
26. Orellana RA, Jeyapalan A, Escobar J, Frank JW, Nguyen HV, Suryawan A, Davis TA. Amino acids augment muscle protein synthesis in neonatal pigs during acute endotoxemia by stimulating mTOR-dependent translation initiation. Am J Physiol Endocrinol Metab 293: E1416-E1425, 2007.
27. Orellana RA, O'Connor PM, Bush JA, Suryawan A, Thivierge MC, Nguyen HV, Fiorotto ML, Davis TA. Modulation of muscle protein synthesis by insulin is maintained during neonatal endotoxemia. Am J Physiol Endocrinol Metab 291: E159-E166, 2006.
28. Orellana RA, O'Connor PM, Nguyen HV, Bush JA, Suryawan A, Thivierge MC, Fiorotto ML, Davis TA. Endotoxemia reduces skeletal muscle protein synthesis in neonates. Am J Physiol Endocrinol Metab 283: E909-E916, 2002.
29. Orellana RA, Wilson FA, Gazzaneo MC, Suryawan A, Davis TA, Nguyen HV. Sepsis and development impede muscle protein synthesis in neonatal pigs by different ribosomal mechanisms. Pediatr Res 69: 473-478, 2011.
30. Powers SK, Duarte J, Kavazis AN, Talbert EE. Reactive oxygen species are signalling molecules for skeletal muscle adaptation. Exp Physiol 95: 1-9, 2010.
31. Pruznak AM, Kazi AA, Frost RA, Vary TC, Lang CH. Activation of AMP-activated protein kinase by 5-aminoimidazole-4-carboxamide-1-beta- D-ribonucleoside prevents leucine-stimulated protein synthesis in rat skeletal muscle. J Nutr 138: 1887-1894, 2008.
32. Rabuel C, Renaud E, Brealey D, Ratajczak P, Damy T, Alves A, Habib A, Singer M, Payen D, Mebazaa A. Human septic myopathy: induction of cyclooxygenase, heme oxygenase and activation of the ubiquitin proteolytic pathway. Anesthesiology 101: 583-590, 2004.
33. Rathmacher JA, Nissen SL. Development and application of a compartmental model of 3-methylhistidine metabolism in humans and domestic animals. Adv Exp Med Biol 445: 303-324, 1998.
34. Rathmacher JA, Nissen SL, Paxton RE, Anderson DB. Estimation of 3-methylhistidine production in pigs by compartmental analysis. J Anim Sci 74: 46-56, 1996.
35. Smith IJ, Lecker SH, Hasselgren PO. Calpain activity and muscle wasting in sepsis. Am J Physiol Endocrinol Metab 295: E762-E771, 2008.
36. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC. Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76-85, 1985.
37. Steinberg GR, Watt MJ, Febbraio MA. Cytokine regulation of AMPK signalling. Front Biosci 14: 1902-1916, 2009.
38. Thivierge MC, Bush JA, Suryawan A, Nguyen HV, Orellana RA, Burrin DG, Jahoor F, Davis TA. Positive net movements of amino acids in the hindlimb after overnight food deprivation contribute to sustaining the elevated anabolism of neonatal pigs. J Appl Physiol 105: 1959-1966, 2008.
39. van den Hemel-Grooten HN, Koohmaraie M, Yen JT, Arbona JR, Rathmacher JA, Nissen SL, Fiorotto ML, Garssen GJ, and Verstegen MW. Comparison between 3-methylhistidine production and proteinase activity as measures of skeletal muscle break down in protein-deficient growing barrows. J Anim Sci 73: 2272-2281, 1995.
40. Vesali RF, Klaude M, Rooyackers O, Wernerman J. Amino acid metabolism in leg muscle after an endotoxin injection in healthy volunteers. Am J Physiol Endocrinol Metab 288: E360-E364, 2005.
41. Vesali RF, Klaude M, Thunblad L, Rooyackers OE, Wernerman J. Contractile protein breakdown in human leg skeletal muscle as estimated by [2H3]-3-methylhistidine: a new method. Metabolism 53: 1076-1080, 2004.
42. von HS, Genth-Zotz S, Anker SD, Volk HD. Cachexia: a therapeutic approach beyond cytokine antagonism. Int J Cardiol 85: 173-183, 2002.
43. Wolfe RR. Regulation of skeletal muscle protein metabolism in catabolic states. Curr Opin Clin Nutr Metab Care 8: 61-65, 2005.
44. Workeneh BT, Mitch WE. Review of muscle wasting associated with chronic kidney disease. Am J Clin Nutr 91:1128S-1132S, 2010.