Skip to main content
Top
Published in: Diabetologia 1/2016

01-01-2016 | Meta-Analysis

Role of insulin in the regulation of human skeletal muscle protein synthesis and breakdown: a systematic review and meta-analysis

Authors: Haitham Abdulla, Kenneth Smith, Philip J. Atherton, Iskandar Idris

Published in: Diabetologia | Issue 1/2016

Login to get access

Abstract

Aims/hypothesis

We aimed to investigate the role of insulin in regulating human skeletal muscle metabolism in health and diabetes.

Methods

We conducted a systematic review and meta-analysis of published data that examined changes in skeletal muscle protein synthesis (MPS) and/or muscle protein breakdown (MPB) in response to insulin infusion. Random-effects models were used to calculate weighted mean differences (WMDs), 95% CIs and corresponding p values. Both MPS and MPB are reported in units of nmol (100 ml leg vol.)−1 min−1.

Results

A total of 104 articles were examined in detail. Of these, 44 and 25 studies (including a total of 173 individuals) were included in the systematic review and meta-analysis, respectively. In the overall estimate, insulin did not affect MPS (WMD 3.90 [95% CI −0.74, 8.55], p = 0.71), but significantly reduced MPB (WMD −15.46 [95% CI −19.74, −11.18], p < 0.001). Overall, insulin significantly increased net balance protein acquisition (WMD 20.09 [95% CI 15.93, 24.26], p < 0.001). Subgroup analysis of the effect of insulin on MPS according to amino acid (AA) delivery was performed using meta-regression analysis. The estimate size (WMD) was significantly different between subgroups based on AA availability (p = 0.001). An increase in MPS was observed when AA availability increased (WMD 13.44 [95% CI 4.07, 22.81], p < 0.01), but not when AA availability was reduced or unchanged. In individuals with diabetes and in the presence of maintained delivery of AA, there was a significant reduction in MPS in response to insulin (WMD −6.67 [95% CI −12.29, −0.66], p < 0.05).

Conclusions/interpretation

This study demonstrates the complex role of insulin in regulating skeletal muscle metabolism. Insulin appears to have a permissive role in MPS in the presence of elevated AAs, and plays a clear role in reducing MPB independent of AA availability.
Appendix
Available only for authorised users
Literature
1.
go back to reference Bier DM (1989) Intrinsically difficult problems: the kinetics of body proteins and amino acids in man. Diabetes Metab Rev 5:111–132CrossRefPubMed Bier DM (1989) Intrinsically difficult problems: the kinetics of body proteins and amino acids in man. Diabetes Metab Rev 5:111–132CrossRefPubMed
2.
go back to reference Prod’homme M, Rieu I, Balage M, Dardevet D, Grizard J (2004) Insulin and amino acids both strongly participate to the regulation of protein metabolism. Curr Opin Clin Nutr Metab Care 7:71–77CrossRefPubMed Prod’homme M, Rieu I, Balage M, Dardevet D, Grizard J (2004) Insulin and amino acids both strongly participate to the regulation of protein metabolism. Curr Opin Clin Nutr Metab Care 7:71–77CrossRefPubMed
3.
go back to reference McNurlan MA, Garlick PJ (1989) Influence of nutrient intake on protein turnover. Diabetes Metab Rev 5:165–189CrossRefPubMed McNurlan MA, Garlick PJ (1989) Influence of nutrient intake on protein turnover. Diabetes Metab Rev 5:165–189CrossRefPubMed
4.
go back to reference Cruz-Jentoft AJ, Landi F, Schneider SM et al (2014) Prevalence and intervention for sarcopenia in ageing adults: a systematic review. Report of the International Sarcopenia Initiative (EWGSOP and IWGS). Age Ageing 43:748–759PubMedCentralCrossRefPubMed Cruz-Jentoft AJ, Landi F, Schneider SM et al (2014) Prevalence and intervention for sarcopenia in ageing adults: a systematic review. Report of the International Sarcopenia Initiative (EWGSOP and IWGS). Age Ageing 43:748–759PubMedCentralCrossRefPubMed
5.
go back to reference Atherton PJ, Etheridge T, Watt PW et al (2010) Muscle full effect after oral protein: time-dependent concordance and discordance between human muscle protein synthesis and mTORC1 signaling. Am J Clin Nutr 92:1080–1088CrossRefPubMed Atherton PJ, Etheridge T, Watt PW et al (2010) Muscle full effect after oral protein: time-dependent concordance and discordance between human muscle protein synthesis and mTORC1 signaling. Am J Clin Nutr 92:1080–1088CrossRefPubMed
6.
go back to reference Wolfson L, Judge J, Whipple R, King M (1995) Strength is a major factor in balance, gait, and the occurrence of falls. J Gerontol A Biol Sci Med Sci 50:64–67PubMed Wolfson L, Judge J, Whipple R, King M (1995) Strength is a major factor in balance, gait, and the occurrence of falls. J Gerontol A Biol Sci Med Sci 50:64–67PubMed
7.
go back to reference Tinetti ME, Williams CS (1997) Falls, injuries due to falls, and the risk of admission to a nursing home. N Engl J Med 337:1279–1284CrossRefPubMed Tinetti ME, Williams CS (1997) Falls, injuries due to falls, and the risk of admission to a nursing home. N Engl J Med 337:1279–1284CrossRefPubMed
8.
9.
go back to reference Mavros Y, Kay S, Anderberg KA et al (2013) Changes in insulin resistance and HbA1c are related to exercise-mediated changes in body composition in older adults with type 2 diabetes: interim outcomes from the GREAT2DO trial. Diabetes Care 36:2372–2379PubMedCentralCrossRefPubMed Mavros Y, Kay S, Anderberg KA et al (2013) Changes in insulin resistance and HbA1c are related to exercise-mediated changes in body composition in older adults with type 2 diabetes: interim outcomes from the GREAT2DO trial. Diabetes Care 36:2372–2379PubMedCentralCrossRefPubMed
10.
go back to reference Prospective UK (1995) Diabetes Study Group. UK Prospective Diabetes Study 16. Overview of 6 years’ therapy of type II diabetes: a progressive disease. Diabetes 44:1249–1258CrossRef Prospective UK (1995) Diabetes Study Group. UK Prospective Diabetes Study 16. Overview of 6 years’ therapy of type II diabetes: a progressive disease. Diabetes 44:1249–1258CrossRef
11.
go back to reference Koro CE, Bowlin SJ, Bourgeois N, Fedder DO (2004) Glycemic control from 1988 to 2000 among U.S. adults diagnosed with type 2 diabetes: a preliminary report. Diabetes Care 27:17–20CrossRefPubMed Koro CE, Bowlin SJ, Bourgeois N, Fedder DO (2004) Glycemic control from 1988 to 2000 among U.S. adults diagnosed with type 2 diabetes: a preliminary report. Diabetes Care 27:17–20CrossRefPubMed
12.
go back to reference Biesenbach G, Raml A, Alsaraji N (2006) Weight gain and insulin requirement in type 2 diabetic patients during the first year after initiating insulin therapy dependent on baseline BMI. Diabetes Obes Metab 8:669–673CrossRefPubMed Biesenbach G, Raml A, Alsaraji N (2006) Weight gain and insulin requirement in type 2 diabetic patients during the first year after initiating insulin therapy dependent on baseline BMI. Diabetes Obes Metab 8:669–673CrossRefPubMed
13.
go back to reference Packianathan IC, Fuller NJ, Peterson DB, Wright A, Coward WA, Finer N (2005) Use of a reference four-component model to define the effects of insulin treatment on body composition in type 2 diabetes: the ‘Darwin study’. Diabetologia 48:222–229CrossRefPubMed Packianathan IC, Fuller NJ, Peterson DB, Wright A, Coward WA, Finer N (2005) Use of a reference four-component model to define the effects of insulin treatment on body composition in type 2 diabetes: the ‘Darwin study’. Diabetologia 48:222–229CrossRefPubMed
14.
go back to reference Pain VM, Albertse EC, Garlick PJ (1983) Protein metabolism in skeletal muscle, diaphragm, and heart of diabetic rats. Am J Physiol 245:E604–E610PubMed Pain VM, Albertse EC, Garlick PJ (1983) Protein metabolism in skeletal muscle, diaphragm, and heart of diabetic rats. Am J Physiol 245:E604–E610PubMed
15.
go back to reference 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 254:579–584PubMedCentralCrossRefPubMed 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 254:579–584PubMedCentralCrossRefPubMed
16.
17.
go back to reference Pacy PJ, Nair KS, Ford C, Halliday D (1989) Failure of insulin infusion to stimulate fractional muscle protein synthesis in type I diabetic patients; anabolic effect of insulin and decreased proteolysis 38:612–624 Pacy PJ, Nair KS, Ford C, Halliday D (1989) Failure of insulin infusion to stimulate fractional muscle protein synthesis in type I diabetic patients; anabolic effect of insulin and decreased proteolysis 38:612–624
18.
go back to reference Denne SC, Liechty EA, Liu YM, Brechtel G, Baron AD (1991) Proteolysis in skeletal muscle and whole body in response to euglycemic hyperinsulinemia in normal adults. Am J Physiol 261:E809–E814PubMed Denne SC, Liechty EA, Liu YM, Brechtel G, Baron AD (1991) Proteolysis in skeletal muscle and whole body in response to euglycemic hyperinsulinemia in normal adults. Am J Physiol 261:E809–E814PubMed
19.
go back to reference Louard RJ, Fryburg DA, Gelfand RA, Barrett EJ (1992) Insulin sensitivity of protein and glucose metabolism in human forearm skeletal muscle. J Clin Invest 90:2348–2354PubMedCentralCrossRefPubMed Louard RJ, Fryburg DA, Gelfand RA, Barrett EJ (1992) Insulin sensitivity of protein and glucose metabolism in human forearm skeletal muscle. J Clin Invest 90:2348–2354PubMedCentralCrossRefPubMed
20.
go back to reference Bell JA, Volpi E, Fujita S et al (2006) Skeletal muscle protein anabolic response to increased energy and insulin is preserved in poorly controlled type 2 diabetes. J Nutr 136:1249–1255PubMedCentralPubMed Bell JA, Volpi E, Fujita S et al (2006) Skeletal muscle protein anabolic response to increased energy and insulin is preserved in poorly controlled type 2 diabetes. J Nutr 136:1249–1255PubMedCentralPubMed
21.
go back to reference Fujita S, Rasmussen BB, Cadenas JG et al (2007) Aerobic exercise overcomes the age-related insulin resistance of muscle protein metabolism by improving endothelial function and Akt/mammalian target of rapamycin signaling. Diabetes 56:1615–1622PubMedCentralCrossRefPubMed Fujita S, Rasmussen BB, Cadenas JG et al (2007) Aerobic exercise overcomes the age-related insulin resistance of muscle protein metabolism by improving endothelial function and Akt/mammalian target of rapamycin signaling. Diabetes 56:1615–1622PubMedCentralCrossRefPubMed
22.
go back to reference Biolo G, Fleming RY, Maggi SP, Wolfe RR (1995) Transmembrane transport and intracellular kinetics of amino acids in human skeletal muscle. Am J Physiol 268:E75–E84PubMed Biolo G, Fleming RY, Maggi SP, Wolfe RR (1995) Transmembrane transport and intracellular kinetics of amino acids in human skeletal muscle. Am J Physiol 268:E75–E84PubMed
24.
go back to reference Newman E, Heslin MJ, Wolf RF, Pisters PW, Brennan MF (1994) The effect of systemic hyperinsulinemia with concomitant amino acid infusion on skeletal muscle protein turnover in the human forearm. Metabolism 43:70–78CrossRefPubMed Newman E, Heslin MJ, Wolf RF, Pisters PW, Brennan MF (1994) The effect of systemic hyperinsulinemia with concomitant amino acid infusion on skeletal muscle protein turnover in the human forearm. Metabolism 43:70–78CrossRefPubMed
25.
go back to reference Biolo G, Declan Fleming RY, Wolfe RR (1995) Physiologic hyperinsulinemia stimulates protein synthesis and enhances transport of selected amino acids in human skeletal muscle. J Clin Invest 95:811–819PubMedCentralCrossRefPubMed Biolo G, Declan Fleming RY, Wolfe RR (1995) Physiologic hyperinsulinemia stimulates protein synthesis and enhances transport of selected amino acids in human skeletal muscle. J Clin Invest 95:811–819PubMedCentralCrossRefPubMed
26.
go back to reference Fryburg DA, Jahn LA, Hill SA, Oliveras DM, Barrett EJ (1995) Insulin and insulin-like growth factor-I enhance human skeletal muscle protein anabolism during hyperaminoacidemia by different mechanisms. J Clin Invest 96:1722–1729PubMedCentralCrossRefPubMed Fryburg DA, Jahn LA, Hill SA, Oliveras DM, Barrett EJ (1995) Insulin and insulin-like growth factor-I enhance human skeletal muscle protein anabolism during hyperaminoacidemia by different mechanisms. J Clin Invest 96:1722–1729PubMedCentralCrossRefPubMed
27.
go back to reference Luzi L, Piceni Sereni L, Spessot M et al (2000) Postabsorptive muscle protein metabolism in type 1 diabetic patients after pancreas transplantation. Acta Diabetol 37:219–224CrossRefPubMed Luzi L, Piceni Sereni L, Spessot M et al (2000) Postabsorptive muscle protein metabolism in type 1 diabetic patients after pancreas transplantation. Acta Diabetol 37:219–224CrossRefPubMed
28.
go back to reference Rasmussen BB, Fujita S, Wolfe RR et al (2006) Insulin resistance of muscle protein metabolism in aging. FASEB J 20:768–769PubMedCentralPubMed Rasmussen BB, Fujita S, Wolfe RR et al (2006) Insulin resistance of muscle protein metabolism in aging. FASEB J 20:768–769PubMedCentralPubMed
29.
go back to reference Fujita S, Rasmussen BB, Cadenas JG, Grady JJ, Volpi E (2006) Effect of insulin on human skeletal muscle protein synthesis is modulated by insulin-induced changes in muscle blood flow and amino acid availability. Am J Physiol Endocrinol Metab 291:E745–E754PubMedCentralCrossRefPubMed Fujita S, Rasmussen BB, Cadenas JG, Grady JJ, Volpi E (2006) Effect of insulin on human skeletal muscle protein synthesis is modulated by insulin-induced changes in muscle blood flow and amino acid availability. Am J Physiol Endocrinol Metab 291:E745–E754PubMedCentralCrossRefPubMed
30.
go back to reference Fujita S, Glynn EL, Timmerman KL, Rasmussen BB, Volpi E (2009) Supraphysiological hyperinsulinaemia is necessary to stimulate skeletal muscle protein anabolism in older adults: evidence of a true age-related insulin resistance of muscle protein metabolism. Diabetologia 52:1889–1898PubMedCentralCrossRefPubMed Fujita S, Glynn EL, Timmerman KL, Rasmussen BB, Volpi E (2009) Supraphysiological hyperinsulinaemia is necessary to stimulate skeletal muscle protein anabolism in older adults: evidence of a true age-related insulin resistance of muscle protein metabolism. Diabetologia 52:1889–1898PubMedCentralCrossRefPubMed
31.
go back to reference Timmerman KL, Lee JL, Fujita S et al (2010) Pharmacological vasodilation improves insulin-stimulated muscle protein anabolism but not glucose utilization in older adults. Diabetes 59:2764–2771PubMedCentralCrossRefPubMed Timmerman KL, Lee JL, Fujita S et al (2010) Pharmacological vasodilation improves insulin-stimulated muscle protein anabolism but not glucose utilization in older adults. Diabetes 59:2764–2771PubMedCentralCrossRefPubMed
32.
go back to reference Timmerman KL, Lee JL, Dreyer HC 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 95:3848–3857PubMedCentralCrossRefPubMed Timmerman KL, Lee JL, Dreyer HC 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 95:3848–3857PubMedCentralCrossRefPubMed
33.
go back to reference Gore DC, Herndon DN, Wolfe RR (2005) Comparison of peripheral metabolic effects of insulin and metformin following severe burn injury. J Trauma Inj Infect Crit Care 59:316–323CrossRef Gore DC, Herndon DN, Wolfe RR (2005) Comparison of peripheral metabolic effects of insulin and metformin following severe burn injury. J Trauma Inj Infect Crit Care 59:316–323CrossRef
34.
go back to reference Biolo G, Williams BD, Fleming RY, Wolfe RR (1999) Insulin action on muscle protein kinetics and amino acid transport during recovery after resistance exercise. Diabetes 48:949–957CrossRefPubMed Biolo G, Williams BD, Fleming RY, Wolfe RR (1999) Insulin action on muscle protein kinetics and amino acid transport during recovery after resistance exercise. Diabetes 48:949–957CrossRefPubMed
35.
go back to reference 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 229:11–18PubMedCentralCrossRefPubMed 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 229:11–18PubMedCentralCrossRefPubMed
36.
go back to reference Hillier TA, Fryburg DA, Jahn LA, Barrett EJ, Teresa A (1998) Extreme hyperinsulinemia unmasks insulin’s effect to stimulate protein synthesis in the human forearm. Am J Physiol Endocrinol Metab 247:E1067–E1074 Hillier TA, Fryburg DA, Jahn LA, Barrett EJ, Teresa A (1998) Extreme hyperinsulinemia unmasks insulin’s effect to stimulate protein synthesis in the human forearm. Am J Physiol Endocrinol Metab 247:E1067–E1074
37.
go back to reference Nygren J, Nair KS (2003) Differential regulation of protein dynamics in splanchnic and skeletal muscle beds by insulin and amino acids in healthy human subjects. Diabetes 52:1377–1385CrossRefPubMed Nygren J, Nair KS (2003) Differential regulation of protein dynamics in splanchnic and skeletal muscle beds by insulin and amino acids in healthy human subjects. Diabetes 52:1377–1385CrossRefPubMed
38.
go back to reference Guillet C, Prod'homme M, Balage M et al (2004) Impaired anabolic response of muscle protein synthesis is associated with S6K1 dysregulation in elderly humans. FASEB J 18:1586–1587PubMed Guillet C, Prod'homme M, Balage M et al (2004) Impaired anabolic response of muscle protein synthesis is associated with S6K1 dysregulation in elderly humans. FASEB J 18:1586–1587PubMed
39.
go back to reference Greenhaff PL, Karagounis LG, Peirce N 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 295:595–604CrossRef Greenhaff PL, Karagounis LG, Peirce N 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 295:595–604CrossRef
40.
go back to reference Guillet C, Delcourt I, Rance M et al (2009) Changes in basal and insulin and amino acid response of whole body and skeletal muscle proteins in obese men. J Clin Endocrinol Metab 94:3044–3050CrossRefPubMed Guillet C, Delcourt I, Rance M et al (2009) Changes in basal and insulin and amino acid response of whole body and skeletal muscle proteins in obese men. J Clin Endocrinol Metab 94:3044–3050CrossRefPubMed
41.
go back to reference Smith GI, Atherton P, Reed DN et al (2009) No major sex differences in muscle protein synthesis rates in the postabsorptive state and during hyperinsulinemia-hyperaminoacidemia in middle-aged adults. J Appl Physiol 107:1308–1315PubMedCentralCrossRefPubMed Smith GI, Atherton P, Reed DN et al (2009) No major sex differences in muscle protein synthesis rates in the postabsorptive state and during hyperinsulinemia-hyperaminoacidemia in middle-aged adults. J Appl Physiol 107:1308–1315PubMedCentralCrossRefPubMed
42.
go back to reference Toth MJ, LeWinter MM, Ades PA, Matthews DE (2010) Impaired muscle protein anabolic response to insulin and amino acids in heart failure patients: relationship with markers of immune activation. Clin Sci (Lond) 119:467–476 Toth MJ, LeWinter MM, Ades PA, Matthews DE (2010) Impaired muscle protein anabolic response to insulin and amino acids in heart failure patients: relationship with markers of immune activation. Clin Sci (Lond) 119:467–476
43.
go back to reference 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:E911–E918PubMed 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:E911–E918PubMed
44.
go back to reference Wilkes EA, Selby AL, Atherton PJ et al (2009) Blunting of insulin inhibition of proteolysis in legs of older subjects may contribute to age-related sarcopenia. Am J Clin Nutr 90:1343–1350CrossRefPubMed Wilkes EA, Selby AL, Atherton PJ et al (2009) Blunting of insulin inhibition of proteolysis in legs of older subjects may contribute to age-related sarcopenia. Am J Clin Nutr 90:1343–1350CrossRefPubMed
45.
go back to reference 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:E46–E52PubMed 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:E46–E52PubMed
46.
go back to reference Barazzoni R, Short KR, Asmann Y, Coenen-Schimke JM, Robinson MM, Nair KS (2012) Insulin fails to enhance mTOR phosphorylation, mitochondrial protein synthesis, and ATP production in human skeletal muscle without amino acid replacement. Am J Physiol Endocrinol Metab 303:E1117–E1125PubMedCentralCrossRefPubMed Barazzoni R, Short KR, Asmann Y, Coenen-Schimke JM, Robinson MM, Nair KS (2012) Insulin fails to enhance mTOR phosphorylation, mitochondrial protein synthesis, and ATP production in human skeletal muscle without amino acid replacement. Am J Physiol Endocrinol Metab 303:E1117–E1125PubMedCentralCrossRefPubMed
47.
go back to reference Wolf RF, Heslin MJ, Newman E, Pearlstone DB, Gonenne A, Brennan MF (1992) Growth hormone and insulin combine to improve whole-body and skeletal muscle protein kinetics. Surgery 112:284–291, discussion 291–292PubMed Wolf RF, Heslin MJ, Newman E, Pearlstone DB, Gonenne A, Brennan MF (1992) Growth hormone and insulin combine to improve whole-body and skeletal muscle protein kinetics. Surgery 112:284–291, discussion 291–292PubMed
48.
go back to reference Bell JA, Fujita S, Volpi E, Cadenas JG, Rasmussen BB (2005) Short-term insulin and nutritional energy provision do not stimulate muscle protein synthesis if blood amino acid availability decreases. Am J Physiol Endocrinol Metab 289:E999–E1006PubMedCentralCrossRefPubMed Bell JA, Fujita S, Volpi E, Cadenas JG, Rasmussen BB (2005) Short-term insulin and nutritional energy provision do not stimulate muscle protein synthesis if blood amino acid availability decreases. Am J Physiol Endocrinol Metab 289:E999–E1006PubMedCentralCrossRefPubMed
49.
go back to reference Charlton MR, Balagopal P, Nair KS (1997) Skeletal muscle myosin heavy chain synthesis in type 1 diabetes. Diabetes 46:1336–1340CrossRefPubMed Charlton MR, Balagopal P, Nair KS (1997) Skeletal muscle myosin heavy chain synthesis in type 1 diabetes. Diabetes 46:1336–1340CrossRefPubMed
50.
go back to reference Halvatsiotis P, Short KR, Bigelow M, Nair KS (2002) Synthesis rate of muscle proteins, muscle functions, and amino acid kinetics in type 2 diabetes. Diabetes 51:2395–2404CrossRefPubMed Halvatsiotis P, Short KR, Bigelow M, Nair KS (2002) Synthesis rate of muscle proteins, muscle functions, and amino acid kinetics in type 2 diabetes. Diabetes 51:2395–2404CrossRefPubMed
51.
go back to reference Sakurai Y, Aarsland A, Herndon DN et al (1995) Stimulation of muscle protein synthesis by long-term insulin infusion in severely burned patients. Ann Surg 222:283–297PubMedCentralCrossRefPubMed Sakurai Y, Aarsland A, Herndon DN et al (1995) Stimulation of muscle protein synthesis by long-term insulin infusion in severely burned patients. Ann Surg 222:283–297PubMedCentralCrossRefPubMed
52.
go back to reference Wang C, Mamza J, Idris I (2015) Biphasic vs basal bolus insulin regimen in type 2 diabetes: a systematic review and meta-analysis of randomized controlled trials. Diabet Med 32:585–594CrossRefPubMed Wang C, Mamza J, Idris I (2015) Biphasic vs basal bolus insulin regimen in type 2 diabetes: a systematic review and meta-analysis of randomized controlled trials. Diabet Med 32:585–594CrossRefPubMed
Metadata
Title
Role of insulin in the regulation of human skeletal muscle protein synthesis and breakdown: a systematic review and meta-analysis
Authors
Haitham Abdulla
Kenneth Smith
Philip J. Atherton
Iskandar Idris
Publication date
01-01-2016
Publisher
Springer Berlin Heidelberg
Published in
Diabetologia / Issue 1/2016
Print ISSN: 0012-186X
Electronic ISSN: 1432-0428
DOI
https://doi.org/10.1007/s00125-015-3751-0

Other articles of this Issue 1/2016

Diabetologia 1/2016 Go to the issue

Editorial

A new chapter