Quantitative effects of thermal injury and insulin on the metabolism of the skeletal muscle using the perfused rat hindquarter 'preparation

Biotechnology and Bioengineering

Volumn 88, Issue 5, 2004, Pages 613-629

  Banta, Scott ^a   Yokoyama, Tadaaki ^a   Berthiaume, François ^a   Yarmush, Martin L ^a  

^a SHRINERS HOSPITALS FOR CHILDREN   (United States)

Author keywords

Hindquarter perfusion; Metabolic flux analysis; Muscle wasting; Proteolysis; Skeletal muscle metabolism

Indexed keywords

AMINES; CELLS; FLUXES; GLUCOSE; INSULIN; METABOLISM; METABOLITES; MUSCLE; NITROGEN;

EXPERIMENTAL MODELS; METABOLIC FLUX ANALYSIS (MFA); PENTOSE PHOSPHATE; THERMAL INJURY;

MEDICAL PROBLEMS;

ALANINE; GLUTAMINE; INSULIN; LEUCINE; NITROGEN;

ANALYTIC METHOD; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BURN; CATABOLISM; CONTROLLED STUDY; HINDLIMB; HYPERMETABOLISM; MALE; METABOLIC FLUX; METABOLIC FLUX ANALYSIS; METABOLIC RATE; MUSCLE ATROPHY; MUSCLE MASS; MUSCLE METABOLISM; NITROGEN BALANCE; NONHUMAN; PROTEIN DEGRADATION; QUANTITATIVE ANALYSIS; RAT; SKELETAL MUSCLE; THERMAL INJURY;

ANIMALS; BURNS; COMPUTER SIMULATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENERGY METABOLISM; HINDLIMB; INSULIN; MALE; MODELS, BIOLOGICAL; MUSCLE PROTEINS; MUSCLE, SKELETAL; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY;

EID: 10644251624     PISSN: 00063592     EISSN: None     Source Type: Journal    
DOI: 10.1002/bit.20258     Document Type: Article

References (74)

1. Abcouwer SF, Lohmann R, Bode BP, Lustig RJ, Souba WW. 1997. Induction of glutamine synthetase expression after major burn injury is tissue specific and temporally variable. J Trauma 42(3):421-428.
2. Aragon JJ, Lowenstein JM. 1980. The purine-nucleotide cycle. Comparison of the levels of citric acid cycle intermediates with the operation of the purine nucleotide cycle in rat skeletal muscle during exercise and recovery from exercise. Eur J Biochem 110(2):371-377.
3. Arai K, Lee K, Berthiaume F, Tompkins RG, Yarmush ML. 2001. Intrahepatic amino acid and glucose metabolism in a D-galactosamine-induced rat liver failure model. Hepatology 34(2):360-371.
4. Ardawi MS. 1988. Skeletal muscle glutamine production in thermally injured rats. Clin Sci (Lond) 74(2):165-172.
5. Arfvidsson B, Zachrisson H, Moller-Loswick AC, Hyltander A, Sandstrom R, Lundholm K. 1991. Effect of systemic hyperinsulinemia on amino acid flux across human legs in postabsorptive state. Am J Physiol 260(1, Pt 1):E46-52.
6. Baron AD, Clark MG. 1997. Role of blood flow in the regulation of muscle glucose uptake. Annu Rev Nutr 17:487-499.
7. Berger M, Hagg S, Ruderman NB. 1975. Glucose metabolism in perfused skeletal muscle. Interaction of insulin and exercise on glucose uptake. Biochem J 146(1):231-238.
8. Berger M, Hagg SA, Goodman MN, Ruderman NB. 1976. Glucose metabolism in perfused skeletal muscle. Effects of starvation, diabetes, fatty acids, acetoacetate, insulin and exercise on glucose uptake and disposition. Biochem J 158(2):191-202.
9. Biolo G, Fleming RY, Maggi SP, Nguyen TT, Herndon DN, Wolfe RR. 2000a. Inhibition of muscle glutamine formation in hypercatabolic patients. Clin Sci (Lond) 99(3):189-194.
10. Biolo G, Fleming RY, Maggi SP, Nguyen TT, Herndon DN, Wolfe RR. 2002. Inverse regulation of protein turnover and amino acid transport in skeletal muscle of hypercatabolic patients. J Clin Endocrinol Metab 87(7):3378-3384.
11. Biolo G, Iscra F, Bosutti A, Toigo G, Ciocchi B, Geatti O, Gullo A, Guarnieri G. 2000b. Growth hormone decreases muscle glutamine production and stimulates protein synthesis in hypercatabolic patients. Am J Physiol Endocrinol Metab 279(2):E323-332.
12. Bonen A, Clark MG, Henriksen EJ. 1994. Experimental approaches in muscle metabolism: hindlimb perfusion and isolated muscle incubations. Am J Physiol 266(1, Pt 1):E1-16.
13. Brooks DC, Bessey PQ, Black PR, Aoki TT, Wilmore DW. 1986. Insulin stimulates branched chain amino acid uptake and diminishes nitrogen flux from skeletal muscle of injured patients. J Surg Res 40(4):395-405.
14. Cabezas H, Raposo RR, Melendez-Hevia E. 1999. Activity and metabolic roles of the pentose phosphate cycle in several rat tissues. Mol Cell Biochem 201(1-2):57-63.
15. Carter EA, Tompkins RG, Babich JW, Correia J, Bailey EM, Fischman AJ. 1996. Thermal injury in rats alters glucose utilization by skin, wound, and small intestine, but not by skeletal muscle. Metabolism 45(9): 1161-1167.
16. Clark AS, Kelly RA, Mitch WE. 1984. Systemic response to thermal injury in rats. Accelerated protein degradation and altered glucose utilization in muscle. J Clin Invest 74(3):888-897.
17. Clerk LH, Vincent MA, Lindner JR, Clark MG, Rattigan S, Barrett EJ. 2004. The vasodilatory actions of insulin on resistance and terminal arterioles and their impact on muscle glucose uptake. Diabetes Metab Res Rev 20(1):3-12.
18. Davis EJ, Gibson DM. 1969. Regulation of the metabolism of rabbit liver mitochondria by long chain fatty acids and other uncouplers of oxidative phosphorylation. J Biol Chem 244(1):161-170.
19. Davis EJ, Lee SH. 1985. Amino acid metabolism by perfused rat hindquarter. Effects of insulin, leucine and 2-chloro-4-methylvalerate. Biochem J 229(1):19-29.
20. Demling RH, Seigne P. 2000. Metabolic management of patients with severe burns. World J Surg 24(6):673-80.
21. Fagan JM, Ganguly M, Stockman H, Ferland LH, Toner M. 1999. Posttranslational modifications of cardiac and skeletal muscle proteins by reactive oxygen species after burn injury in the rat. Ann Surg 229(1):106-114.
22. Feng B, Banner C, Max SR. 1990. Effect of diabetes on glutamine synthetase expression in rat skeletal muscles. Am J Physiol 258(5, Pt 1): E762-6.
23. Ferrando AA, Chinkes DL, Wolf SE, Matin S, Herndon DN, Wolfe RR. 1999. A submaximal dose of insulin promotes net skeletal muscle protein synthesis in patients with severe burns. Ann Surg 229(1): 11-18.
24. Frayn KN, Maycock PF. 1979. Regulation of protein metabolism by a physiological concentration of insulin in mouse soleus and extensor digitorum longus muscles. Effects of starvation and scald injury. Biochem J 184(2):323-330.
25. Fukagawa NK, Minaker KL, Rowe JW, Goodman MN, Matthews DE, Bier DM, Young VR. 1985. Insulin-mediated reduction of whole body protein breakdown. Dose-response effects on leucine metabolism in postabsorptive men. J Clin Invest 76(6):2306-2311.
26. Garlick PJ, Grant I. 1988. Amino acid infusion increases the sensitivity of muscle protein synthesis in vivo to insulin. Effect of branched-chain amino acids. Biochem J 254(2):579-584.
27. Gore DC, Jahoor F. 1994. Glutamine kinetics in burn patients. Comparison with hormonally induced stress in volunteers. Arch Surg 129(12): 1318-1323.
28. Graham TE, Gibala MJ. 1998. Anaplerosis of the tricarboxylic acid cycle in human skeletal muscle during exercise. Magnitude, sources, and potential physiological significance. Adv Exp Med Biol 441:271-286.
29. Greene SM, Fisher H. 1985. Differential response of muscle and gastric histidine decarboxylase to compound 48/80 and dietary calcium. Proc Soc Exp Biol Med 180(2):240-245.
30. Grubb B. 1976. De novo synthesis of alanine by the perfused rat hindlimb. Am J Physiol 230(5):1379-1384.
31. Hadley JS, Hinds CJ. 2002. Anabolic strategies in critical illness. Curr Opin Pharmacol 2(6):700-707.
32. Hasselgren PO. 2000. Catabolic response to stress and injury: Implications for regulation. World J Surg 24(12):1452-1459.
33. Hasselgren PO, Pedersen P, Sax HC, Warner BW, Fischer JE. 1988. Methods for studying protein synthesis and degradation in liver and skeletal muscle. J Surg Res 45(4):389-415.
34. Herndon DN, Wilmore DW, Mason AD Jr. 1978. Development and analysis of a small animal model simulating the human postburn hypermetabolic response. J Surg Res 25(5):394-403.
35. Herzfeld A, Mezl VA, Knox WE. 1977. Enzymes metabolizing delta 1-pyrroline-5-carboxylate in rat tissues. Biochem J 166(1): 95-103.
36. Heslin MJ, Newman E, Wolf RF, Pisters PW, Brennan MF. 1992. Effect of hyperinsulinemia on whole body and skeletal muscle leucine carbon kinetics in humans. Am J Physiol 262(6, Pt 1):E911-918.
37. Hutson SM, Cree TC, Harper AE. 1978. Regulation of leucine and alpha-ketoisocaproate metabolism in skeletal muscle. J Biol Chem 253 (22):8126-8133.
38. Hutson SM, Zapalowski C, Cree TC, Harper AE. 1980. Regulation of leucine and alpha-ketoisocaproic acid metabolism in skeletal muscle. Effects of starvation and insulin. J Biol Chem 255(6):2418-2426.
39. Jefferson LS, Li JB, Rannels SR. 1977. Regulation by insulin of amino acid release and protein turnover in the perfused rat hemicorpus. J Biol Chem 252(4):1476-1483.
40. Kikuchi G, Hiraga K, Yoshida T. 1980. Role of the glycine-cleavage system in glycine and serine metabolism in various organs. Biochem Soc Trans 8(5):504-506.
41. Lee K, Berthiaume F, Stephanopoulos GN, Yarmush DM, Yarmush ML. 2000. Metabolic flux analysis of postburn hepatic hypermetabolism. Metab Eng 2(4):312-327.
42. Lee K, Berthiaume F, Stephanopoulos GN, Yarmush ML. 1999. Metabolic flux analysis: A powerful tool for monitoring tissue function. Tissue Eng 5(4):347-368.
43. Lee SH, Davis EJ. 1979. Carboxylation and decarboxylation reactions. Anaplerotic flux and removal of citrate cycle intermediates in skeletal muscle. J Biol Chem 254(2):420-430.
44. Malmezat T, Breuille D, Capitan P, Mirand PP, Obled C. 2000. Glutathione turnover is increased during the acute phase of sepsis in rats. J Nutr 130(5):1239-1246.
45. McDermott JC, Hutber A, Tan MH, Bonen A. 1989. The use of a cell-free perfusate in the perfused rat hindquarter: methodological concerns. Can J Physiol Pharmacol 67(11):1450-1454.
46. Nguyen TT, Gilpin DA, Meyer NA, Herndon DN. 1996. Current treatment of severely burned patients. Ann Surg 223(1):14-25.
47. Noordenbos J, Hansbrough JF, Gutmacher H, Dore C, Hansbrough WB. 2000. Enteral nutritional support and wound excision and closure do not prevent postburn hypermetabolism as measured by continuous metabolic monitoring. J Trauma 49(4):667-672.
48. Odessey R, Parr B. 1982. Effect of insulin and leucine on protein turnover in rat soleus muscle after burn injury. Metabolism 31(1):82-87.
49. Pardridge WM, Duducgian-Vartavarian L, Casanello-Ertl D, Jones MR, Kopple JD. 1982. Arginine metabolism and urea synthesis in cultured rat skeletal muscle cells. Am J Physiol 242(2):E87-92.
50. Pereira B, Rosa LF, Safi DA, Bechara EJ, Curi R. 1994. Superoxide dismutase, catalase and glutathione peroxidase activities in the lymphoid organs of diabetic rats. J Endocrinol 142(1):161-165.
51. Rooyackers OE, Wagenmakers AJ. 1996. Tracer kinetics are of limited value to measure in vivo protein synthesis and degradation rates in muscle of anesthesized rats. Metabolism 45(10):1279-1283.
52. Ruderman NB, Houghton CR, Hems R. 1971. Evaluation of the isolated perfused rat hindquarter for the study of muscle metabolism. Biochem J 124(3):639-651.
53. Sakurai Y, Aarsland A, Herndon DN, Chinkes DL, Pierre E, Nguyen TT, Patterson BW, Wolfe RR. 1995. Stimulation of muscle protein synthesis by long-term insulin infusion in severely burned patients. Ann Surg 222(3):283-297.
54. Schadewaldt P, Lammers E, Staib W. 1985. Influence of insulin and glucose on pyruvate catabolism in perfused rat hindlimbs. Biochem J 227(1):177-182.
55. Scharff R, Wool IG. 1966. Effect of diabetes on the concentration of amino acids in plasma and heart muscle of rats. Biochem J 99(1):173-178.
56. Scislowski PW, Davis EJ. 1986. Amino acid catabolism by perfused rat hindquarters: degradation of threonine and isoleucine. Arch Biochem Biophys 249(2):620-624.
57. Scislowski PW, Hokland BM, Davis-van Thienen WI, Bremer J, Davis EJ. 1987. Methionine metabolism by rat muscle and other tissues. Occurrence of a new carnitine intermediate. Biochem J 247(1):35-40.
58. Sheridan RL, Ryan CM, Yin LM, Hurley J, Tompkins RG. 1998. Death in the burn unit: Sterile multiple organ failure. Burns 24(4):307-311.
59. Shiota M, Sugano T. 1986. Characteristics of rat hindlimbs perfused with erythrocyte- and albumin-free medium. Am J Physiol 251(1, Pt 1): C78-84.
60. Shiozaki T, Tasaki O, Ohnishi M, Nishimura T, Hiraide A, Shimazu T, Yoshioka T, Sugimoto H. 1997. Paradoxical positive nitrogen balance in burn patients receiving high-dose administration of insulin for nutritional care. Surgery 122(3):527-533.
61. Snelling CF, Woolf LI, Groves AC, Moore JP, Duff JH. 1982. Amino acid metabolism in patients with severe burns. Surgery 91(4):474-481.
62. Solomon V, Madihally S, Mitchell RN, Yarmush M, Toner M. 2002. Antiproteolytic action of insulin in burn-injured rats. J Surg Res 105(2):234-242.
63. Tessari P, Inchiostro S, Biolo G, Vincenti E, Sabadin L. 1991. Effects of acute systemic hyperinsulinemia on forearm muscle proteolysis in healthy man. J Clin Invest 88(1):27-33.
64. Tredget EE, Yu YM. 1992. The metabolic effects of thermal injury. World J Surg 16(1):68-79.
65. van den Berghe G, Wouters P, Weekers F, Verwaest C, Bruyninckx F, Schetz M, Vlasselaers D, Ferdinande P, Lauwers P, Bouillon R. 2001. Intensive insulin therapy in the critically ill patients. N Engl J Med 345(19):1359-1367.
66. Wagenmakers AJ. 1998. Protein and amino acid metabolism in human muscle. Adv Exp Med Biol 441:307-319.
67. Wagle A, Jivraj S, Garlock GL, Stapleton SR. 1998. Insulin regulation of glucose-6-phosphate dehydrogenase gene expression is rapamycin-sensitive and requires phosphatidylinositol 3-kinase. J Biol Chem 273(24):14968-14974.
68. Wilmore DW. 2000. Metabolic response to severe surgical illness: Overview. World J Surg 24(6):705-711.
69. Wojtaszewski JF, Jakobsen AB, Ploug T, Richter EA. 1998. Perfused rat hindlimb is suitable for skeletal muscle glucose transport measurements. Am J Physiol 274(1, Pt 1):E184-191.
70. Xu J, Fei Z, Yu YM, Xu W, Rhodes A, Tompkins RG, Schulz JT. 2003. In vivo rabbit hindquarter model for assessment of regional burn hypermetabolism. J Appl Physiol 94(1):135-140.
71. Yamaguchi Y, Yu YM, Zupke C, Yarmush DM, Berthiaume F, Tompkins RG, Yarmush ML. 1997. Effect of burn injury on glucose and nitrogen metabolism in the liver: Preliminary studies in a perfused liver system. Surgery 121(3):295-303.
72. Yarmush ML, Banta S. 2003. Metabolic engineering: Advances in modeling and intervention in health and disease. Annu Rev Biomed Eng 5:349-381.
73. Zanetti M, Barazzoni R, Kiwanuka E, Tessari P. 1999. Effects of branched-chain-enriched amino acids and insulin on forearm leucine kinetics. Clin Sci (Lond) 97(4):437-448.
74. Zhang XJ, Chinkes DL, Wolf SE, Wolfe RR. 1999. Insulin but not growth hormone stimulates protein anabolism in skin wound and muscle. Am J Physiol 276(4, Pt 1):E712-720.