Mechanisms of altered protein turnover in chronic diseases: A review of human kinetic studies

Current Opinion in Clinical Nutrition and Metabolic Care

Volumn 6, Issue 1, 2003, Pages 55-63

  Biolo, Gianni ^a,b   Antonione, Raffaella ^a   Barazzoni, Rocco ^a   Zanetti, Michela ^a   Guarnieri, Gianfranco ^a  

^a UNIVERSITY OF TRIESTE   (Italy)

^b UNIVERSITY OF TRIESTE   (Italy)

Author keywords

Chronic inflammation; Insulin; Protein synthesis; Proteolysis; Tissue perfusion

Indexed keywords

AMINO ACID; CYTOKINE; GAMMA INTERFERON; INSULIN; INTERLEUKIN 1; INTERLEUKIN 6; INTERLEUKIN 8; PROTEIN; SOMATOMEDIN C; TUMOR NECROSIS FACTOR ALPHA; HORMONE;

ACID BASE BALANCE; AEROBIC METABOLISM; CACHEXIA; CHRONIC DISEASE; HORMONE ACTION; HUMAN; HYDRATION; HYPERINSULINEMIA; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; NITROGEN BALANCE; NUTRIENT; PHYSICAL ACTIVITY; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; REVIEW; TISSUE OXYGENATION; TISSUE PERFUSION; UREMIA; EATING; EDITORIAL; ENERGY METABOLISM; KINETICS; METABOLISM; PHYSIOLOGY; PROTEIN INTAKE;

CHRONIC DISEASE; CYTOKINES; DIETARY PROTEINS; EATING; ENERGY METABOLISM; HORMONES; HUMANS; KINETICS; PROTEIN BIOSYNTHESIS; PROTEINS;

EID: 1842833243     PISSN: 13631950     EISSN: None     Source Type: Journal    
DOI: 10.1097/00075197-200301000-00009     Document Type: Review

References (100)

1. Zhang XJ, Chinkes DL, Wolfe RR. Measurement of muscle protein fractional synthesis and breakdown rates from a pulse tracer injection. Am J Physiol Endocrinol Metab 2002; 283:E753-E764. This study describes a novel approach to determine protein kinetics in human skeletal muscle.
2. Morrison WL, Gibson JN, Scrimgeour C, Rennie MJ. Muscle wasting in emphysema. Clin Sci 1988; 75:415-420.
3. Morrison WL, Bouchier IA, Gibson JN, Rennie MJ. Skeletal muscle and whole body protein turnover in cirrhosis. Clin Sci Colch 1990; 78:613-619.
4. Castellino P, Solini A, Luzi L, et al. Glucose and amino acid metabolism in chronic renal failure: effect of insulin and amino acids. Am J Physiol 1992; 262:F168-F176.
5. Ferrando AA, Lane HW, Stuart CA, et al. Prolonged bed rest decreases skeletal muscle and whole body protein synthesis. Am J Physiol 1996; 270:E627-E633.
6. Lim VS, Wolfson M, Yarasheski KE, et al. Leucine turnover in patients with nephrotic syndrome: evidence suggesting body protein conservation. J Am Soc Nephrol 1998; 9:1067-1073.
7. Adey D, Kumar R, McCarthy JT, Nair KS. Reduced synthesis of muscle proteins in chronic renal failure. Am J Physiol Endocrinol Metab 2000; 278:E219-E225.
8. Wolfe RR, Goodenough RD, Burke JF, Wolfe MH. Response of protein and urea kinetics in burn patients to different levels of protein intake. Ann Surg 1983; 197:163-171.
9. Ikizler TA, Pupim LB, Brouillette JR, et al. Hemodialysis stimulates muscle and whole body protein loss and alters substrate oxidation. Am J Physiol Endocrinol Metab 2002; 282:E107-E116. This study highlights for the first time the acute catabolic effect of dialysis.
10. Biolo G, Maggi SP, Williams BD, et al. Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans. Am J Physiol 1995; 268:E514-E520.
11. Moller-Loswick AC, Zachrisson H, Hyltander A, et al. Insulin selectively attenuates breakdown of nonmyofibrillar proteins in peripheral tissues of normal men. Am J Physiol 1994; 266:E645-E652.
12. Biolo G, Fleming RY, Maggi SP, et al. Inverse regulation of protein turnover and amino acid transport in skeletal muscle of hypercatabolic patients. J Clin Endocrinol Metab 2002; 87:3378-3384. This paper clearly supports the evidence that in-vivo changes in protein synthesis and degradation are strictly related.
13. Tessari P, Inchiostro S, Biolo G, et al. Differential effects of hyperinsulinemia and hyperaminoacidemia on leucine-carbon metabolism in vivo. Evidence for distinct mechanisms in regulation of net amino acid deposition. J Clin Invest 1987; 79:1062-1069.
14. Sakurai Y, Aarsland A, Herndon DN, et al. Stimulation of muscle protein synthesis by long-term insulin infusion in severely burned patients. Ann Surg 1995; 222:283-294.
15. Vandenburgh HH, Karlisch P, Shansky J, Feldstein R. Insulin and IGF-I induce pronounced hypertrophy of skeletal myofibers in tissue culture. Am J Physiol 1991; 260:C475-C484.
16. De Feo P, Volpi E, Lucidi P, et al. Physiological increments in plasma insulin concentrations have selective and different effects on synthesis of hepatic proteins in humans. Diabetes 1992; 42:995-1002.
17. Caso G, Ford GC, Nair KS, et al. Aminoacyl-tRNA enrichment after a flood of labeled phenylalanine: insulin effect on muscle protein synthesis. Am J Physiol Endocrinol Metab 2002; 282:E1029-E1038.
18. Boirie Y, Short KR, Ahlman B, et al. Tissue-specific regulation of mitochondrial and cytoplasmic protein synthesis rates by insulin. Diabetes 2001; 50:2652-2658. An elegant study in vivo of insulin effects at the molecular level.
19. Wing SS, Banville D. 14-kDa-ubiquitin-conjugating enzyme: structure of the rat gene and regulation upon fasting and by insulin. Am J Physiol 1994; 267:E39-E48.
20. 2+-dependent and ubiquitin/proteasome-dependent proteolytic pathways in fast-twitch and slow-twitch rat muscle following hyperinsulinaemia. Clin Sci (Lond) 2001; 101:551-558. A comprehensive assessment of the insulin effects on proteolytic systems.
21. Biolo G, Declan Fleming RY, Wolfe RR. Physiologic hyperinsulinemia stimulates protein synthesis and enhances transport of selected amino acids in human skeletal muscle. J Clin Invest 1995; 95:811-819.
22. Hillier TA, Fryburg DA, Jahn LA, Barrett EJ. Extreme hyperinsulinemia unmasks insulin's effect to stimulate protein synthesis in the human forearm. Am J Physiol 1998; 274:E1067-E1074.
23. Fryburg DA, Jahn LA, Hill SA, et al. Insulin and insulin-like growth factor-I enhance human skeletal muscle protein anabolism during hyperaminoacidemia by different mechanisms. J Clin Invest 1995; 96:1722-1729.
24. Fryburg DA, Gelfand RA, Barrett EJ. Growth hormone acutely stimulates forearm muscle protein synthesis in normal humans. Am J Physiol 1991; 260:E499-E504.
25. Butterfield GE, Thompson J, Rennie MJ, et al. Effect of rhGH and rhIGF-I treatment on protein utilization in elderly women. Am J Physiol 1997; 272:E94-E99.
26. Biolo G, Iscra F, Bosutti A, et al. Growth hormone decreases muscle glutamine production and stimulates protein synthesis in hypercatabolic patients. Am J Physiol 2000; 279:E323-E332.
27. Norrelund H, Nair KS, Jorgensen JO, et al. The protein-retaining effects of growth hormone during fasting involve inhibition of muscle-protein breakdown. Diabetes 2001; 50:96-104. A well-designed clinical study assessing growth hormone action in vivo.
28. Hermann M, Berger P. Hormonal changes in aging men: a therapeutic indication? Exp Gerontol 2001; 36:1075-1082.
29. Urban RJ, Bodenburg YH, Gilkison C, et al. Testosterone administration to elderly men increases skeletal muscle strength and protein synthesis. Am J Physiol 1995; 269:E820-E826.
30. Morrison WL, Gibson JN, Jung RT, Rennie MJ. Skeletal muscle and whole body protein turnover in thyroid disease. Eur J Clin Invest 1988; 18:62-68.
31. Rochon C, Tauveron I, Dejax C, et al. Response of leucine metabolism to hyperinsulinemia in hypothyroid patients before and after thyroxine replacement. J Clin Endocrinol Metab 2000; 85:697-706.
32. Short KR, Nygren J, Barazzoni R, et al. T3 increases mitochondrial ATP production in oxidative but not glycolytic muscle despite increased expression of UCP-2 and -3. Am J Physiol Endocrinol Metab 2001; 280:E761-E766.
33. Brillon DJ, Zheng B, Campbell RG, Matthews DE. Effect of cortisol on energy expenditure and amino acid metabolism in humans. Am J Physiol 1995; 268:E501-E513.
34. Ferrando AA, Stuart CA, Sheffield-Moore M, Wolfe RR. Inactivity amplifies the catabolic response of skeletal muscle to cortisol. J Clin Endocrinol Metab 1999; 84:3515-3521.
35. Hesketh JE, Campbell GP, Lobley GE, et al. Stimulation of actin and myosin synthesis in rat gastrocnemius muscle by clenbuterol; evidence for translational control. Comp Biochem Physiol C 1992; 102:23-27.
36. Fryburg DA, Gelfand RA, Jahn LA, et al. Effects of epinephrine on human muscle glucose and protein metabolism. Am J Physiol 1995; 268:E55-E59.
37. Navegantes LC, Resano NM, Migliorini RH, Kettelhut IC. Catecholamines inhibit Ca(2+)-dependent proteolysis in rat skeletal muscle through beta(2)-adrenoceptors and cAMP. Am J Physiol Endocrinol Metab 2001; 281:E449-E454.
38. Herndon DN, Hart DW, Wolf SE, et al. Reversal of catabolism by beta-blockade after severe burns. N Engl J Med 2001; 345:1223-1229. An unexpected result from a well-designed clinical study.
39. Kaysen GA. The microinflammatory state in uremia: causes and potential consequences. J Am Soc Nephrol 2001; 12:1549-1557. Excellent synthesis and discussion of the current understanding on the consequences of a chronic low-grade inflammatory state.
40. Frost RA, Lang CH, Gelato MC. Transient exposure of human myoblasts to tumor necrosis factor alpha inhibits serum and insulin-like growth factor-I stimulated protein synthesis. Endocrinology 1997; 138:4153-4159.
41. Lang CH, Nystrom GJ, Frost RA. Tissue-specific regulation of IGF-I and IGF-binding proteins in response to TNFalpha. Growth Horm IGF Res 2001; 11:250-260.
42. Sakurai Y, Zhang XJ, Wolfe R. TNF directly stimulates glucose uptake and leucine oxidation and inhibits FFA flux in conscious dogs. Am J Physiol 1996; 270:864-872.
43. Charters Y, Grimble RF. Effects of recombinant human tumor necrosis factor-alpha on protein synthesis in liver, skeletal muscle and skin of rats. Biochem J 1989; 258:493-497.
44. Llovera M, Garcia-Martinez C, Agell N, et al. TNF can directly induce the expression of ubiquitin-dependent proteolytic system in rat soleus muscles. Biochem Biophys Res Commun 1997; 230:238-241.
45. Du J, Mitch WE, Wang X, Price SR. Glucocorticoids induce proteasome C3 subunit expression in L6 muscle cells by opposing the suppression of its transcription by NF-kappa B. J Biol Chem 2000; 275:19661-19666.
46. Combaret L, Tilignac T, Claustre A, et al. Torbafylline (HWA 448) inhibits enhanced skeletal muscle ubiquitin-proteasome-dependent proteolysis in cancer and septic rats. Biochem J 2002; 361:185-192.
47. Biolo G, Ciocchi B, Bosutti A, et al. Pentoxifylline acutely reduces protein catabolism in chronically uremic patients. Am J Kidney Dis; in press.
48. Tisdale MJ. Loss of skeletal muscle in cancer: biochemical mechanisms. Front Biosci 2001; 6:D164-D174.
49. Cederholm T, Wretlind B, Hellstrom K, et al. Enhanced generation of interleukins 1beta and 6 may contribute to the cachexia of chronic disease. Am J Clin Nutr 1997; 65:876-882.
50. Fryburg DA, Barrett EJ, Louard RJ, Gelfand RA. Effect of starvation on human muscle protein metabolism and its response to insulin. Am J Physiol 1990; 259:E477-E482.
51. Gougeon R, Hoffer LJ, Pencharz PB, Marliss EB. Protein metabolism in obese subjects during a very-low-energy diet. Am J Clin Nutr 1992; 56 (suppl):249S-254S.
52. Essen P, McNurlan MA, Wernerman J, et al. Short-term starvation decreases skeletal muscle protein synthesis rate in man. Clin Physiol 1992; 12:287-299.
53. Lee CK, Klopp RG, Weindruch R, Prolla TA. Gene expression profile of aging and its retardation by caloric restriction. Science 1999; 285:1390-1393.
54. Dhahbi JM, Mote PL, Wingo J, et al. Caloric restriction alters the feeding response of key metabolic enzyme genes. Mech Ageing Dev 2001; 122:1033-1048.
55. Merker K, Stolzing A, Grune T. Proteolysis, caloric restriction and aging. Mech Ageing Dev 2001; 122:595-615.
56. Weindruch R, Kayo T, Lee CK, Prolla TA. Microarray profiling of gene expression in aging and its alteration by caloric restriction in mice. J Nutr 2001; 131 (suppl):918S-923S. In this study a novel technique is used to assess protein turnover in vivo.
57. Tavernarakis N, Driscoll M. Caloric restriction and lifespan: a role for protein turnover? Mech Ageing Dev 2002; 123:215-229.
58. Biolo G, Tipton KD, Klein S, Wolfe RR. An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. Am J Physiol 1997; 273:E122-E129.
59. Borsheim E, Tipton KD, Wolf SE, Wolfe RR. Essential amino acids and muscle protein recovery from resistance exercise. Am J Physiol Endocrinol Metab 2002; 283:E648-E657.
60. Blomstrand E, Saltin B. BCAA intake affects protein metabolism in muscle after but not during exercise in humans. Am J Physiol Endocrinol Metab 2001; 281:E365-E374.
61. Bevington A, Brown J, Walls J. Leucine suppresses acid-induced protein wasting in L6 rat muscle cells. Eur J Clin Invest 2001; 31:497-503.
62. Gore DC, Wolf SE, Herndon DN, Wolfe RR. Relative influence of glucose and insulin on peripheral amino acid metabolism in severely burned patients. J Parenter Enter Nutr 2002; 26:271-277.
63. Plauth M, Egberts EH, Abele R, et al. Characteristic pattern of free amino acids in plasma and skeletal muscle in stable hepatic cirrhosis. Hepatogastroenterology 1990; 37:135-139.
64. Engelen MP, Wouters EF, Deutz NE, et al. Factors contributing to alterations in skeletal muscle and plasma amino acid profiles in patients with chronic obstructive pulmonary disease. Am J Clin Nutr 2000; 72:1480-1487.
65. Tessari P, Deferrari G, Robaudo C, et al. Phenylalanine hydroxylation across the kidney in humans. Kidney Int 1999; 56:2168-2172.
66. Moller N, Meek S, Bigelow M, et al. The kidney is an important site for in vivo phenylalanine-to-tyrosine conversion in adult humans: a metabolic role of the kidney. Proc Natl Acad Sci U S A 2000; 97:1242-1246.
67. Biolo G, Ciocchi G, Toigo G, et al. Sensitivity of whole body protein synthesis to amino acid administration during short-term bed rest. Proceedings of the symposium on life in space for life on earth. 2-7th June 2002, Stockholm, Sweden pp. 365-354.
68. Warnholtz A, Mollnau H, Oelze M, et al. Antioxidants and endothelial dysfunction in hyperlipidemia. Curr Hypertens Rep 2001; 3:53-60.
69. Booth G, Stalker TJ, Lefer AM, Scalia R. Mechanisms of amelioration of glucose-induced endothelial dysfunction following inhibition of protein kinase C in vivo. Diabetes 2002; 51:1556-1564.
70. Taddei S, Salvetti A. Endothelial dysfunction in essential hypertension: clinical implications. J Hypertens 2002; 20:1671-1674.
71. Williams IL, Wheatcroft SB, Shah AM, Kearney MT. Obesity, atherosclerosis and the vascular endothelium: mechanisms of reduced nitric oxide bioavailability in obese humans. Int J Obes Relat Metab Disord 2002; 26:754-764.
72. Hossmann KA. Ischemia-mediated neuronal injury. Resuscitation 1993; 26:225-235.
73. Fryburg DA. NG-monomethyl-I-arginine inhibits the blood flow but not the insulin-like response of forearm muscle to IGF-I: possible role of nitric oxide in muscle protein synthesis. J Clin Invest 1996; 97:1319-1328.
74. Straumann E, Keller U, Kury D, et al. Effect of acute acidosis and alkalosis on leucine kinetics in man. Clin Physiol 1992; 12:39-51.
75. Rooyackers OE, Adey DB, Ades PA, Nair KS. Effect of age in vivo synthesis rates of mitochondrial protein in human skeletal muscle. Proc Natl Acad Sci USA 1996; 93:15364-15369.
76. Barazzoni R, Short KR, Nair KS. Effects of aging on mitochondrial DNA copy number and cytochrome C oxidase gene expression in rat skeletal muscle, liver and heart. J Biol Chem 2000; 275:3343-3347.
77. Barazzoni R, Nair KS. Changes in uncoupling protein-2 and -3 expression in aging rat skeletal muscle, liver and heart. Am J Physiol Endocrinol Metab 2001; 280:E413-E419. An elegant study showing comparative changes in mitochondrial functions in different tissues of ageing rats.
78. Haussinger D, Roth E, Lang F, Gerok W. Cellular hydration state: an important determinant of protein catabolism in health and disease. Lancet 1993; 341:1330-1332.
79. Garibotto G, Russo R, Sofia A, et al. Skeletal muscle protein synthesis and degradation in patients with chronic renal failure. Kidney Int 1994; 45:1432-1439.
80. Garibotto G, Russo R, Sofia A, et al. Muscle protein turnover in chronic renal failure patients with metabolic acidosis or normal acid-base balance. Miner Electrolyte Metab 1996; 22:58-61.
81. Griggs RC, Jozefowicz R, Kingston W, et al. Mechanism of muscle wasting in myotonic dystrophy. Ann Neurol 1990; 27:505-512.
82. Tessari P, Biolo G, Inchiostro S, et al. Leucine and phenylalanine kinetics in compensated liver cirrhosis: effects of insulin. Gastroenterology 1993; 104:1712-1721.
83. Goodship TH, Lloyd S, Clague MB, et al. Whole body leucine turnover and nutritional status in continuous ambulatory peritoneal dialysis. Clin Sci 1987; 73:463-469.
84. 13C leucine. Am J Clin Nutr 1987; 46:778-783.
85. Tessari P, Zanetti M, Barazzoni R, et al. Response of phenylatanine and leucine kinetics to branched chain enriched amino acids and insulin in patients with cirrhosis. Gastroenterology 1996; 111:127-137.
86. Engelen MP, Deutz NE, Wouters EF, Schols AM. Enhanced levels of whole-body protein turnover in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2000; 162:1488-1492.
87. McCullough AJ, Mullen KD, Kalhan SC. Body cell mass and leucine metabolism in cirrhosis. Gastroenterology 1992; 102:1325-1333.
88. Tessari P, Inchiostro S, Barazzoni R, et al. Fasting and postprandial phenylalanine and leucine kinetics in liver cirrhosis. Am J Physiol 1994; 267:E140-E149.
89. Carmichael MJ, Clague MB, Keir MJ, Johnston ID. Whole body protein turnover, synthesis and breakdown in patients with colorectal carcinoma. Br J Surg 1980; 67:736-739.
90. Jeevanandam M, Horowitz GD, Lowry SF, Brennan MF. Cancer cachexia and protein metabolism. Lancet 1984; 30:1423-1426.
91. Melville S, McNurlan MA, Calder AG, Garlick PJ. Increased protein turnover despite normal energy metabolism and responses to feeding in patients with lung cancer. Cancer Res 1990; 50:1125-1131.
92. Dworzak F, Ferrari P, Gavazzi C, et al. Effects of cachexia due to cancer on whole body and skeletal muscle protein turnover. Cancer 1998; 82:42-48.
93. Salman EK, Haymond MW, Bayne E, et al. Protein and energy metabolism in prepubertal children with sickle cell anemia. Pediatr Res 1996; 40:34-40.
94. Thomas AG, Miller V, Taylor F, et al. Whole body protein turnover in childhood Crohn's disease. Gut 1992; 33:675-677.
95. Selberg O, Suttmann U, Melzer A, et al. Effect of increased protein intake and nutritional status on whole body protein metabolism of AIDS patients with weight loss. Metabolism 1995; 44:1159-1165.
96. Henderson RA, Talusan K, Hutton N, et al. Whole body protein turnover in children with human immunodeficiency virus (HIV) infection. Nutrition 1999; 15:189-194.
97. Messing B, Dutra SL, Thuillier F, et al. Whole body protein metabolism assessed by leucine and glutamine kinetics in adult patients with active celiac disease. Metabolism 1998; 47:1429-1433.
98. Morrison WL, Gibson JN, Rennie MJ. Skeletal muscle and whole body protein turnover in cardiac cachexia: influence of branched chain amino acid administration. Eur J Clin Invest 1988; 18:648-654.
99. Newsholme EA, Crabtree B. Substrate cycles in metabolic regulation and in heat generation. Biochem Soc Symp 1976; 41:61-109.
100. Spindler SR. Calorie restriction enhances the expression of key metabolic enzymes associated with protein renewal during aging. Ann NY Acad Sci 2001; 928:296-304. The author suggests the novel hypothesis that enhanced protein renewal may contribute to the extension of the lifespan associated with caloric restriction.