MTOR signaling and ubiquitin-proteosome gene expression in the preservation of fat free mass following high protein, calorie restricted weight loss

Nutrition and Metabolism

Volumn 9, Issue , 2012, Pages

  McIver, Cassandra M ^a   Wycherley, Thomas P ^b   Clifton, Peter M ^a,c  

^a CSIRO   (Australia)

^b UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^c BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

Author keywords

Caloric restriction; Fat free mass; High protein diet; MTORC1; MuRF 1; Skeletal muscle

Indexed keywords

ATROGIN 1; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MUSCLE RING FINGER 1 PROTEIN; PROTEASOME; UBIQUITIN PROTEASOME; UNCLASSIFIED DRUG;

BIOSYNTHESIS; CALORIC RESTRICTION; FAT FREE MASS; GENE EXPRESSION; HUMAN; PROTEIN DEGRADATION; PROTEIN DIET; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; WEIGHT REDUCTION; WEIGHT, MASS AND SIZE;

EID: 84866181985     PISSN: None     EISSN: 17437075     Source Type: Journal    
DOI: 10.1186/1743-7075-9-83     Document Type: Review

References (99)

1. Brinkworth GD, Noakes M, Clifton PM, Buckley JD, Effects of a Low Carbohydrate Weight Loss Diet on Exercise Capacity and Tolerance in Obese Subjects Obesity (Silver Spring). 2009
2. Diet-induced weight loss is associated with an improvement in beta-cell function in older men. Utzschneider KM, Carr DB, Barsness SM, Kahn SE, Schwartz RS, J Clin Endocrinol Metab 2004 89 2704 2710 10.1210/jc.2003-031827 15181045 (Pubitemid 38766353)
3. Lifestyle, diabetes, and cardiovascular risk factors 10years after bariatric surgery. Sjostrom L, Lindroos AK, Peltonen M, Torgerson J, Bouchard C, Carlsson B, Dahlgren S, Larsson B, Narbro K, Sjostrom CD, Sullivan M, Wedel H, N Engl J Med 2004 351 2683 2693 10.1056/NEJMoa035622 15616203 (Pubitemid 39665322)
4. Adipose tissue transcriptome reflects variations between subjects with continued weight loss and subjects regaining weight 6 mo after caloric restriction independent of energy intake. Marquez-Quinones A, Mutch DM, Debard C, Wang P, Combes M, Roussel B, Holst C, Martinez JA, Handjieva-Darlenska T, Kalouskova P, Jebb S, Babalis D, Pfeiffer AF, Larsen TM, Astrup A, Saris WH, Mariman E, Clement K, Vidal H, Langin D, Viguerie N, Am J Clin Nutr 2010 92 975 984 10.3945/ajcn.2010.29808 20739421
5. The role of diet and exercise for the maintenance of fat-free mass and resting metabolic rate during weight loss. Stiegler P, Cunliffe A, Sports Med 2006 36 239 262 10.2165/00007256-200636030-00005 16526835
6. The Muscle Protein Synthetic Response to Carbohydrate and Protein Ingestion Is Not Impaired in Men with Longstanding Type 2 Diabetes. Manders RJ, Koopman R, Beelen M, Gijsen AP, Wodzig WK, Saris WH, van Loon LJ, J Nutr 2008 138 1079 1085 18492837 (Pubitemid 351769132)
7. The underappreciated role of muscle in health and disease. Wolfe RR, Am J Clin Nutr 2006 84 475 482 16960159 (Pubitemid 44713395)
8. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P, Wackerhage H, Taylor PM, Rennie MJ, FASEB J 2005 19 422 424 15596483 (Pubitemid 40316537)
9. Latency and duration of stimulation of human muscle protein synthesis during continuous infusion of amino acids. Bohe J, Low JF, Wolfe RR, Rennie MJ, J Physiol 2001 532 575 579 10.1111/j.1469-7793.2001.0575f.x 11306673 (Pubitemid 32390411)
10. Dietary protein to support anabolism with resistance exercise in young men. Phillips SM, Hartman JW, Wilkinson SB, J Am Coll Nutr 2005 24 134S 139S 15798080 (Pubitemid 40489659)
11. mTOR signaling in growth control and disease. Laplante M, Sabatini DM, Cell 2012 149 274 293 10.1016/j.cell.2012.03.017 22500797
12. Insulin resistance due to nutrient excess: Is it a consequence of AMPK downregulation? Saha AK, Xu XJ, Balon TW, Brandon A, Kraegen EW, Ruderman NB, Cell Cycle 2011 10 3447 3451 10.4161/cc.10.20.17886 22067655
13. Influence of dietary protein intake on whole-body protein turnover in humans. Garlick PJ, McNurlan MA, Ballmer PE, Diabetes Care 1991 14 1189 1198 10.2337/diacare.14.12.1189 1773704
14. Villareal DT, Smith GI, Shah K, Mittendorfer B, Effect of Weight Loss on the Rate of Muscle Protein Synthesis During Fasted and Fed Conditions in Obese Older Adults Obesity (Silver Spring). 2011
15. Excess leucine intake enhances muscle anabolic signaling but not net protein anabolism in young men and women. Glynn EL, Fry CS, Drummond MJ, Timmerman KL, Dhanani S, Volpi E, Rasmussen BB, J Nutr 2010 140 1970 1976 10.3945/jn.110.127647 20844186
16. Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. Moore DL, Robinson MJ, Fry JL, Tang JE, Glover EI, Wilkinson S, Prior T, Tarnopolsky MA, Phillips SM, Am J Clin Nutr 2009 89 161 168 19056590
17. Nutrition guidelines for strength sports: sprinting, weightlifting, throwing events, and bodybuilding. Slater G, Phillips SM, J Sports Sci 2011 29 Suppl 1 67 77 21660839
18. Ingestion of whey hydrolysate, casein, or soy protein isolate: effects on mixed muscle protein synthesis at rest and following resistance exercise in young men. Tang JE, Moore DR, Kujbida GW, Tarnopolsky MA, Phillips SM, J Appl Physiol 2009 107 987 992 10.1152/japplphysiol.00076.2009 19589961
19. Maximizing muscle protein anabolism: the role of protein quality. Tang JE, Phillips SM, Curr Opin Clin Nutr Metab Care 2009 12 66 71 10.1097/MCO.0b013e32831cef75 19057190
20. High protein vs high carbohydrate hypoenergetic diet for the treatment of obese hyperinsulinemic subjects. Baba NH, Sawaya S, Torbay N, Habbal Z, Azar S, Hashim SA, Int J Obes Relat Metab Disord 1999 23 1202 1206 10.1038/sj.ijo. 0801064 10578211
21. Reduced body weight and adiposity with a high-protein diet improves functional status, lipid profiles, glycemic control, and quality of life in patients with heart failure: a feasibility study. Evangelista LS, Heber D, Li Z, Bowerman S, Hamilton MA, Fonarow GC, J Cardiovasc Nurs 2009 24 207 215 19390338
22. Enhanced weight loss with protein-enriched meal replacements in subjects with the metabolic syndrome. Flechtner-Mors M, Boehm BO, Wittmann R, Thoma U, Ditschuneit HH, Diabetes Metab Res Rev 2010 26 393 405 10.1002/dmrr.1097 20578205
23. Effects of protein vs. carbohydrate-rich diets on fuel utilisation in obese women during weight loss. Labayen I, Diez N, Gonzalez A, Parra D, Martinez JA, Forum Nutr 2003 56 168 170 15806847
24. Moderate carbohydrate, moderate protein weight loss diet reduces cardiovascular disease risk compared to high carbohydrate, low protein diet in obese adults: a randomized clinical trial. Lasker DA, Evans EM, Layman DK, Nutr Metab (Lond) 2008 5 30 10.1186/1743-7075-5-30
25. Effect of an energy-restricted, high-protein, low-fat diet relative to a conventional high-carbohydrate, low-fat diet on weight loss, body composition, nutritional status, and markers of cardiovascular health in obese women. Noakes M, Keogh JB, Foster PR, Clifton PM, Am J Clin Nutr 2005 81 1298 1306 15941879 (Pubitemid 41710230)
26. High protein diets decrease total and abdominal fat and improve CVD risk profile in overweight and obese men and women with elevated triacylglycerol. Clifton PM, Bastiaans K, Keogh JB, Nutr Metab Cardiovasc Dis 2009 19 548 554 10.1016/j.numecd.2008.10.006 19179060
27. Separate effects of reduced carbohydrate intake and weight loss on atherogenic dyslipidemia. Krauss RM, Blanche PJ, Rawlings RS, Fernstrom HS, Williams PT, Am J Clin Nutr 2006 83 1025 1031 quiz 1205 16685042 (Pubitemid 44713100)
28. Effect of a high-protein, energy-restricted diet on body composition, glycemic control, and lipid concentrations in overweight and obese hyperinsulinemic men and women. Farnsworth E, Luscombe ND, Noakes M, Wittert G, Argyiou E, Clifton PM, Am J Clin Nutr 2003 78 31 39 12816768 (Pubitemid 39655245)
29. A reduced ratio of dietary carbohydrate to protein improves body composition and blood lipid profiles during weight loss in adult women. Layman DK, Boileau RA, Erickson DJ, Painter JE, Shiue H, Sather C, Christou DD, J Nutr 2003 133 411 417 12566476 (Pubitemid 36172892)
30. Higher protein intake preserves lean mass and satiety with weight loss in pre-obese and obese women. Leidy HJ, Carnell NS, Mattes RD, Campbell WW, Obesity (Silver Spring) 2007 15 421 429 10.1038/oby.2007.531 (Pubitemid 46407324)
31. Hypocaloric high-protein diet improves glucose oxidation and spares lean body mass: comparison to hypocaloric high-carbohydrate diet. Piatti PM, Monti F, Fermo I, Baruffaldi L, Nasser R, Santambrogio G, Librenti MC, Galli-Kienle M, Pontiroli AE, Pozza G, Metabolism 1994 43 1481 1487 10.1016/0026-0495(94)90005-1 7990700 (Pubitemid 24382697)
32. Effects of an 8-week high-protein or high-carbohydrate diet in adults with hyperinsulinemia. Kleiner RE, Hutchins AM, Johnston CS, Swan PD, MedGenMed 2006 8 39 17415320
33. Effect of a high-protein, energy-restricted diet on weight loss and energy expenditure after weight stabilization in hyperinsulinemic subjects. Luscombe ND, Clifton PM, Noakes M, Farnsworth E, Wittert G, Int J Obes Relat Metab Disord 2003 27 582 590 10.1038/sj.ijo.0802270 12704402 (Pubitemid 36561015)
34. A randomized trial of the effects of two types of short-term hypocaloric diets on weight loss in women with polycystic ovary syndrome. Stamets K, Taylor DS, Kunselman A, Demers LM, Pelkman CL, Legro RS, Fertil Steril 2004 81 630 637 10.1016/j.fertnstert.2003.08.023 15037413 (Pubitemid 38376121)
35. Effects of protein versus simple sugar intake on weight loss in polycystic ovary syndrome (according to the National Institutes of Health criteria). Kasim-Karakas SE, Almario RU, Cunningham W, Fertil Steril 2009 92 262 270 10.1016/j.fertnstert.2008.05.065 18691705
36. Effect of a high-protein, high-monounsaturated fat weight loss diet on glycemic control and lipid levels in type 2 diabetes. Parker B, Noakes M, Luscombe N, Clifton P, Diabetes Care 2002 25 425 430 10.2337/diacare.25.3.425 11874925 (Pubitemid 41103331)
37. A controlled trial of protein enrichment of meal replacements for weight reduction with retention of lean body mass. Treyzon L, Chen S, Hong K, Yan E, Carpenter CL, Thames G, Bowerman S, Wang HJ, Elashoff R, Li Z, Nutr J 2008 7 23 10.1186/1475-2891-7-23 18752682
38. High protein vs high carbohydrate hypoenergetic diet in treatment of obese normoinsulinemic and hyperinsulinemic subjects. Torbay N, Baba NH, Sawaya S, Bajjani R, Habbal Z, Azar S, Hashim SA, Nutr Res 2002 22 587 598 10.1016/S0271-5317(02)00359-7 (Pubitemid 34556344)
39. Thermodynamics and metabolic advantage of weight loss diets. Feinman RD, Fine EJ, Metab Syndr Relat Disord 2003 1 209 219 10.1089/154041903322716688 18370664
40. Gluconeogenesis and energy expenditure after a high-protein, carbohydrate-free diet. Veldhorst MA, Westerterp-Plantenga MS, Westerterp KR, Am J Clin Nutr 2009 90 519 526 10.3945/ajcn.2009.27834 19640952
41. Changes in body fat percentage during body weight stable conditions of increased daily protein intake vs. control. Soenen S, Westerterp-Plantenga MS, Physiol Behav 2010 101 635 638 10.1016/j.physbeh.2010.09.014 20887742
42. Effect of dietary protein intake on insulin secretion and glucose metabolism in insulin-dependent diabetes mellitus. Linn T, Geyer R, Prassek S, Laube H, J Clin Endocrinol Metab 1996 81 3938 3943 10.1210/jc.81.11.3938 8923841 (Pubitemid 26380399)
43. Effect of long-term dietary protein intake on glucose metabolism in humans. Linn T, Santosa B, Gronemeyer D, Aygen S, Scholz N, Busch M, Bretzel RG, Diabetologia 2000 43 1257 1265 10.1007/s001250051521 11079744
44. Changes in fat-free mass during significant weight loss: a systematic review. Chaston TB, Dixon JB, O'Brien PE, Int J Obes (Lond) 2007 31 743 750 (Pubitemid 46663819)
45. Reduced Rate of Energy-Expenditure as a Risk Factor for Body-Weight Gain. Ravussin E, Lillioja S, Knowler WC, Christin L, Freymond D, Abbott WGH, Boyce V, Howard BV, Bogardus C, 1988 318 467 472
46. High protein intake sustains weight maintenance after body weight loss in humans. Westerterp-Plantenga MS, Lejeune MP, Nijs I, van Ooijen M, Kovacs EM, Int J Obes Relat Metab Disord 2004 28 57 64 10.1038/sj.ijo.0802461 14710168 (Pubitemid 38141991)
47. Effect of exercise training on long-term weight maintenance in weight-reduced men. Pasman WJ, Saris WH, Muls E, Vansant G, Westerterp-Plantenga MS, Metabolism 1999 48 15 21 10.1016/S0026-0495(99)90004-5 9920139 (Pubitemid 29035555)
48. Is lost lean mass from intentional weight loss recovered during weight regain in postmenopausal women. Beavers KM, Lyles MF, Davis CC, Wang X, Beavers DP, Nicklas BJ, Am J Clin Nutr 94 767 774
49. Muscle weakness in women occurs at an earlier age than in men, but strength is preserved by hormone replacement therapy. Phillips SK, Rook KM, Siddle NC, Bruce SA, Woledge RC, Clin Sci (Lond) 1993 84 95 98 (Pubitemid 23023845)
50. The danger of weight loss in the elderly. Miller SL, Wolfe RR, J Nutr Health Aging 2008 12 487 491 10.1007/BF02982710 18615231
51. Muscle atrophy in cachexia: can dietary protein tip the balance. Op den Kamp CM, Langen RC, Haegens A, Schols AM, Curr Opin Clin Nutr Metab Care 2009 12 611 616 10.1097/MCO.0b013e3283319399 19741519
52. Additional protein intake limits weight regain after weight loss in humans. Lejeune MP, Kovacs EM, Westerterp-Plantenga MS, Br J Nutr 2005 93 281 289 10.1079/BJN20041305 15788122
53. How nutrition and exercise maintain the human musculoskeletal mass. Wackerhage H, Rennie MJ, J Anat 2006 208 451 458 10.1111/j.1469-7580.2006.00544. x 16637871
54. Skeletal muscle hypertrophy and atrophy signaling pathways. Glass DJ, Int J Biochem Cell Biol 2005 37 1974 1984 10.1016/j.biocel.2005.04.018 16087388 (Pubitemid 41206815)
55. mTOR's role in ageing: protein synthesis or autophagy? Hands SL, Proud CG, Wyttenbach A, Aging (Albany NY) 2009 1 586 597
56. The role of mTOR in the adaptation and failure of beta-cells in type 2 diabetes. Leibowitz G, Cerasi E, Ketzinel-Gilad M, Diabetes Obes Metab 2008 10 Suppl 4 157 169 18834443
57. In vivo activation of ROCK1 by insulin is impaired in skeletal muscle of humans with type 2 diabetes. Chun KH, Choi KD, Lee DH, Jung Y, Henry RR, Ciaraldi TP, Kim YB, Am J Physiol Endocrinol Metab 2011 300 536 542 10.1152/ajpendo.00538.2010 21189360
58. A novel regulation of IRS1 (insulin receptor substrate-1) expression following short term insulin administration. Ruiz-Alcaraz AJ, Liu HK, Cuthbertson DJ, McManus EJ, Akhtar S, Lipina C, Morris AD, Petrie JR, Hundal HS, Sutherland C, Biochem J 2005 392 345 352 10.1042/BJ20051194 16128672 (Pubitemid 41796523)
59. Control of translation initiation through integration of signals generated by hormones, nutrients, and exercise. Kimball SR, Jefferson LS, J Biol Chem 2010 285 29027 29032 10.1074/jbc.R110.137208 20576612
60. Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. Kumar V, Selby A, Rankin D, Patel R, Atherton P, Hildebrandt W, Williams J, Smith K, Seynnes O, Hiscock N, Rennie MJ, J Physiol 2009 587 211 217 10.1113/jphysiol.2008.164483 19001042
61. Nutritional and contractile regulation of human skeletal muscle protein synthesis and mTORC1 signaling. Drummond MJ, Dreyer HC, Fry CS, Glynn EL, Rasmussen BB, J Appl Physiol 2009 106 1374 1384 10.1152/japplphysiol.91397.2008 19150856
62. Calorie restriction: decelerating mTOR-driven aging from cells to organisms (including humans). Blagosklonny MV, Cell Cycle 2010 9 683 688 10.4161/cc.9.4.10766 20139716
63. Skeletal muscle protein anabolic response to resistance exercise and essential amino acids is delayed with aging. Drummond MJ, Dreyer HC, Pennings B, Fry CS, Dhanani S, Dillon EL, Sheffield-Moore M, Volpi E, Rasmussen BB, J Appl Physiol 2008 104 1452 1461 10.1152/japplphysiol.00021.2008 18323467
64. Gran P, Anabolic signalling in skeletal muscle: impact of diet and disease In School of Exercise and Nutrition Sciences, Deakin University 2011
65. Carbohydrate-restricted diets high in either monounsaturated fat or protein are equally effective at promoting fat loss and improving blood lipids. Luscombe-Marsh ND, Noakes M, Wittert GA, Keogh JB, Foster P, Clifton PM, Am J Clin Nutr 2005 81 762 772 15817850 (Pubitemid 41724981)
66. Molecular signaling pathways regulating muscle proteolysis during atrophy. Franch HA, Price SR, Curr Opin Clin Nutr Metab Care 2005 8 271 275 10.1097/01.mco.0000165005.01331.45 15809529 (Pubitemid 40586185)
67. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Glickman MH, Ciechanover A, Physiol Rev 2002 82 373 428 11917093 (Pubitemid 34654457)
68. Importance of the ATP-ubiquitin-proteasome pathway in the degradation of soluble and myofibrillar proteins in rabbit muscle extracts. Solomon V, Goldberg AL, J Biol Chem 1996 271 26690 26697 10.1074/jbc.271.43.26690 8900146 (Pubitemid 26359075)
69. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, Lecker SH, Goldberg AL, Cell Metab 2007 6 472 483 10.1016/j.cmet.2007.11.004 18054316 (Pubitemid 350163056)
70. Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. Lecker SH, Goldberg AL, Mitch WE, J Am Soc Nephrol 2006 17 1807 1819 10.1681/ASN.2006010083 16738015 (Pubitemid 44036165)
71. IGF-I stimulates muscle growth by suppressing protein breakdown and expression of atrophy-related ubiquitin ligases, atrogin-1 and MuRF1. Sacheck JM, Ohtsuka A, McLary SC, Goldberg AL, Am J Physiol Endocrinol Metab 2004 287 591 601 10.1152/ajpendo.00073.2004 15100091 (Pubitemid 39242684)
72. Endoplasmic reticulum stress markers and ubiquitin-proteasome pathway activity in response to a 200-km run. Kim HJ, Jamart C, Deldicque L, An GL, Lee YH, Kim CK, Raymackers JM, Francaux M, Med Sci Sports Exerc 2011 43 18 25 20473228
73. Ubiquitin-proteasome pathway is compromised in CD45RO+and CD45RA+T lymphocyte subsets during aging. Ponnappan U, Exp Gerontol 2002 37 359 367 10.1016/S0531-5565(01)00203-0 11772523 (Pubitemid 34073554)
74. Skeletal muscle autophagy and apoptosis during aging: effects of calorie restriction and life-long exercise. Wohlgemuth SE, Seo AY, Marzetti E, Lees HA, Leeuwenburgh C, Exp Gerontol 2010 45 138 148 10.1016/j.exger.2009.11.002 19903516
75. Life long calorie restriction increases heat shock proteins and proteasome activity in soleus muscles of Fisher 344 rats. Selsby JT, Judge AR, Yimlamai T, Leeuwenburgh C, Dodd SL, Exp Gerontol 2005 40 37 42 10.1016/j.exger.2004.08.012 15664730 (Pubitemid 40138744)
76. Caloric restriction optimizes the proteasome pathway with aging in rat plantaris muscle: implications for sarcopenia. Hepple RT, Qin M, Nakamoto H, Goto S, Am J Physiol Regul Integr Comp Physiol 2008 295 1231 1237 10.1152/ajpregu.90478.2008 18703409
77. Patterns of gene expression in atrophying skeletal muscles: response to food deprivation. Jagoe RT, Lecker SH, Gomes M, Goldberg AL, FASEB J 2002 16 1697 1712 10.1096/fj.02-0312com 12409312 (Pubitemid 35345118)
78. Long-term effects of calorie or protein restriction on serum IGF-1 and IGFBP-3 concentration in humans. Fontana L, Weiss EP, Villareal DT, Klein S, Holloszy JO, Aging Cell 2008 7 681 687 10.1111/j.1474-9726.2008.00417.x 18843793
79. Caloric restriction. Speakman JR, Mitchell SE, Mol Aspects Med 2011 32 159 221 10.1016/j.mam.2011.07.001 21840335
80. Moderate energy restriction-induced weight loss affects circulating IGF levels independent of dietary composition. Belobrajdic DP, Frystyk J, Jeyaratnaganthan N, Espelund U, Flyvbjerg A, Clifton PM, Noakes M, Eur J Endocrinol 2010 162 1075 1082 10.1530/EJE-10-0062 20212016
81. The effects of a two-year randomized, controlled trial of whey protein supplementation on bone structure, IGF-1, and urinary calcium excretion in older postmenopausal women. Zhu K, Meng X, Kerr DA, Devine A, Solah V, Binns CW, Prince RL, J Bone Miner Res 2011 26 2298 2306 10.1002/jbmr.429 21590739
82. Insulin-induced phosphorylation of FKHR (Foxo1) targets to proteasomal degradation. Matsuzaki H, Daitoku H, Hatta M, Tanaka K, Fukamizu A, Proc Natl Acad Sci USA 2003 100 11285 11290 10.1073/pnas.1934283100 13679577 (Pubitemid 37205927)
83. Ubiquitin ligases MuRF1 and MAFbx in human skeletal muscle atrophy. de Palma L, Marinelli M, Pavan M, Orazi A, Joint Bone Spine 2008 75 53 57 10.1016/j.jbspin.2007.04.019 17977773
84. An exploratory analysis of the effects of a weight loss plus exercise program on cellular quality control mechanisms in older overweight women. Wohlgemuth SE, Lees HA, Marzetti E, Manini TM, Aranda JM, Daniels MJ, Pahor M, Perri MG, Leeuwenburgh C, Anton SD, Rejuvenation Res 2011 14 315 324 10.1089/rej.2010.1132 21631380
85. Functional impact of high protein intake on healthy elderly people. Walrand S, Short KR, Bigelow ML, Sweatt AJ, Hutson SM, Nair KS, Am J Physiol Endocrinol Metab 2008 295 921 928 10.1152/ajpendo.90536.2008 18697911
86. Protein quantity and quality at levels above the RDA improves adult weight loss. Layman DK, J Am Coll Nutr 2004 23 631S 636S 15640518 (Pubitemid 40096753)
87. Proposed role of calcium and dairy food components in weight management and metabolic health. Zemel MB, Phys Sportsmed 2009 37 29 39 20058398
88. The role of leucine in weight loss diets and glucose homeostasis. Layman DK, J Nutr 2003 133 261S 267S 12514305 (Pubitemid 36070614)
89. Signaling pathways involved in translational control of protein synthesis in skeletal muscle by leucine. Anthony JC, Anthony TG, Kimball SR, Jefferson LS, J Nutr 2001 131 856S 860S 11238774 (Pubitemid 32199159)
90. Signaling pathways and molecular mechanisms through which branched-chain amino acids mediate translational control of protein synthesis. Kimball SR, Jefferson LS, J Nutr 2006 136 227S 231S 16365087 (Pubitemid 43156513)
91. Oral leucine administration stimulates protein synthesis in rat skeletal muscle. Crozier SJ, Kimball SR, Emmert SW, Anthony JC, Jefferson LS, J Nutr 2005 135 376 382 15735066 (Pubitemid 40365191)
92. McDaniel ML: Branched-chain amino acids are essential in the regulation of PHAS-I and p70 S6 kinase by pancreatic beta-cells. A possible role in protein translation and mitogenic signaling. Xu G, Kwon G, Marshall CA, Lin TA, Lawrence JC Jr, J Biol Chem 1998 273 28178 28184 10.1074/jbc.273.43.28178 9774438 (Pubitemid 28496115)
93. The role of nutrition in stimulating muscle protein accretion at the molecular level. Kimball SR, Biochem Soc Trans 2007 35 1298 1301 17956335 (Pubitemid 350206484)
94. Rapid turnover of the mTOR complex 1 (mTORC1) repressor REDD1 and activation of mTORC1 signaling following inhibition of protein synthesis. Kimball SR, Do AN, Kutzler L, Cavener DR, Jefferson LS, J Biol Chem 2008 283 3465 3475 18070882
95. mTORC1 signaling in energy balance and metabolic disease. Catania C, Binder E, Cota D, Int J Obes (Lond) 2011 35 751 761 10.1038/ijo.2010.208
96. hVps34 is a nutrient-regulated lipid kinase required for activation of p70 S6 kinase. Byfield MP, Murray JT, Backer JM, J Biol Chem 2005 280 33076 33082 10.1074/jbc.M507201200 16049009 (Pubitemid 41368357)
97. Thomas G: hvps34, an ancient player, enters a growing game: mTOR Complex1/S6K1 signaling. Nobukuni T, Kozma SC, Curr Opin Cell Biol 2007 19 135 141 10.1016/j.ceb.2007.02.019 17321123 (Pubitemid 46386413)
98. Nutrient overload, insulin resistance, and ribosomal protein S6 kinase 1, S6K1. Um SH, D'Alessio D, Thomas G, Cell Metab 2006 3 393 402 10.1016/j.cmet.2006.05.003 16753575 (Pubitemid 43811780)
99. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD, Nat Cell Biol 2001 3 1014 1019 10.1038/ncb1101-1014 11715023 (Pubitemid 34428747)