Sexual dimorphism in skeletal muscle protein turnover

Journal of Applied Physiology

Volumn 120, Issue 6, 2016, Pages 674-682

  Smith, Gordon I ^a   Mittendorfer, Bettina ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Hypertrophy; Muscle protein; Protein turnover

Indexed keywords

MUSCLE PROTEIN;

BODY COMPOSITION; HUMAN; METABOLISM; PHYSIOLOGY; SEXUAL DEVELOPMENT; SEXUAL MATURATION; SKELETAL MUSCLE;

BODY COMPOSITION; HUMANS; MUSCLE PROTEINS; MUSCLE, SKELETAL; SEX CHARACTERISTICS; SEXUAL MATURATION;

EID: 84984710656     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00625.2015     Document Type: Review

References (129)

1. Abe T, DeHoyos DV, Pollock ML, Garzarella L. Time course for strength and muscle thickness changes following upper and lower body resistance training in men and women. Eur J Appl Physiol 81: 174-180, 2000.
2. Ahtiainen JP, Pakarinen A, Alen M, Kraemer WJ, Hakkinen K. Short vs long rest period between the sets in hypertrophic resistance training: influence on muscle strength, size, and hormonal adaptations in trained men. J Strength Cond Res 19: 572-582, 2005.
3. Aloia JF, McGowan DM, Vaswani AN, Ross P, Cohn SH. Relationship of menopause to skeletal and muscle mass. Am J Clin Nutr 53: 1378-1383, 1991.
4. Arden NK, Spector TD. Genetic influences on muscle strength, lean body mass, and bone mineral density: a twin study. J Bone Miner Res 12: 2076-2081, 1997.
5. Areta JL, Burke LM, Camera DM, West DW, Crawshay S, Moore DR, Stellingwerff T, Phillips SM, Hawley JA, Coffey VG. Reduced resting skeletal muscle protein synthesis is rescued by resistance exercise and protein ingestion following short-term energy deficit. Am J Physiol Endocrinol Metab 306: E989-E997, 2014.
6. Areta JL, Burke LM, Ross ML, Camera DM, West DW, Broad EM, Jeacocke NA, Moore DR, Stellingwerff T, Phillips SM, Hawley JA, Coffey VG. Timing and distribution of protein ingestion during prolonged recovery from resistance exercise alters myofibrillar protein synthesis. J Physiol 591: 2319-2331, 2013.
7. Atherton PJ, Etheridge T, Watt PW, Wilkinson D, Selby A, Rankin D, Smith K, Rennie MJ. Muscle full effect after oral protein: timedependent concordance and discordance between human muscle protein synthesis and mTORC1 signaling. Am J Clin Nutr 92: 1080-1088, 2010.
8. Babraj JA, Cuthbertson DJ, Smith K, Langberg H, Miller B, Krogsgaard MR, Kjaer M, Rennie MJ. Collagen synthesis in human musculoskeletal tissues and skin. Am J Physiol Endocrinol Metab 289: E864-E869, 2005.
9. Baer DJ, Stote KS, Paul DR, Harris GK, Rumpler WV, Clevidence BA. Whey protein but not soy protein supplementation alters body weight and composition in free-living overweight and obese adults. J Nutr 141: 1489-1494, 2011.
10. Bamman MM, Hill VJ, Adams GR, Haddad F, Wetzstein CJ, Gower BA, Ahmed A, Hunter GR. Gender differences in resistance-traininginduced myofiber hypertrophy among older adults. J Gerontol A Biol Sci Med Sci 58: 108-116, 2003.
11. Bohe J, Low A, Wolfe RR, Rennie MJ. Human muscle protein synthesis is modulated by extracellular, not intramuscular amino acid availability: a dose-response study. J Physiol 552: 315-324, 2003.
12. Bohe J, Low JF, Wolfe RR, Rennie MJ. Latency and duration of stimulation of human muscle protein synthesis during continuous infusion of amino acids. J Physiol 532: 575-579, 2001.
13. Bray GA, Smith SR, de Jonge L, Xie H, Rood J, Martin CK, Most M, Brock C, Mancuso S, Redman LM. Effect of dietary protein content on weight gain, energy expenditure, and body composition during overeating: a randomized controlled trial. JAMA 307: 47-55, 2012.
14. Brodsky IG, Balagopal P, Nair KS. Effects of testosterone replacement on muscle mass and muscle protein synthesis in hypogonadal men-a clinical research center study. J Clin Endocrinol Metab 81: 3469-3475, 1996.
15. Brose A, Parise G, Tarnopolsky MA. Creatine supplementation enhances isometric strength and body composition improvements following strength exercise training in older adults. J Gerontol A Biol Sci Med Sci 58: 11-19, 2003.
16. Brown M, Foley A, Ferreria JA. Ovariectomy, hindlimb unweighting, and recovery effects on skeletal muscle in adult rats. Aviat Space Environ Med 76: 1012-1018, 2005.
17. Buford TW, Anton SD, Judge AR, Marzetti E, Wohlgemuth SE, Carter CS, Leeuwenburgh C, Pahor M, Manini TM. Models of accelerated sarcopenia: critical pieces for solving the puzzle of agerelated muscle atrophy. Ageing Res Rev 9: 369-383, 2010.
18. Bukhari SS, Phillips BE, Wilkinson DJ, Limb MC, Rankin D, Mitchell WK, Kobayashi H, Greenhaff PL, Smith K, Atherton PJ. Intake of low-dose leucine-rich essential amino acids stimulates muscle anabolism equivalently to bolus whey protein in older women at rest and after exercise. Am J Physiol Endocrinol Metab 308: E1056-E1065, 2015.
19. Burd NA, Yang Y, Moore DR, Tang JE, Tarnopolsky MA, Phillips SM. Greater stimulation of myofibrillar protein synthesis with ingestion of whey protein isolate v. micellar casein at rest and after resistance exercise in elderly men. Br J Nutr 108: 958-962, 2012.
20. Callahan DM, Tourville TW, Miller MS, Hackett SB, Sharma H, Cruickshank NC, Slauterbeck JR, Savage PD, Ades PA, Maughan DW, Beynnon BD, Toth MJ. Chronic disuse and skeletal muscle structure in older adults: sex-specific differences and relationships to contractile function. Am J Physiol Cell Physiol 308: C932-C943, 2015.
21. Castaneda C, Charnley JM, Evans WJ, Crim MC. Elderly women accommodate to a low-protein diet with losses of body cell mass, muscle function, and immune response. Am J Clin Nutr 62: 30-39, 1995.
22. Castaneda C, Gordon PL, Fielding RA, Evans WJ, Crim MC. Marginal protein intake results in reduced plasma IGF-I levels and skeletal muscle fiber atrophy in elderly women. J Nutr Health Aging 4: 85-90, 2000.
23. Chevalier S, Goulet ED, Burgos SA, Wykes LJ, Morais JA. Protein anabolic responses to a fed steady state in healthy aging. J Gerontol A Biol Sci Med Sci 66: 681-688, 2011.
24. Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P, Wackerhage H, Taylor PM, Rennie MJ. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J 19: 422-424, 2005.
25. de Boer MD, Selby A, Atherton P, Smith K, Seynnes OR, Maganaris CN, Maffulli N, Movin T, Narici MV, Rennie MJ. The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. J Physiol 585: 241-251, 2007.
26. Dieli-Conwright CM, Spektor TM, Rice JC, Sattler FR, Schroeder ET. Influence of hormone replacement therapy on eccentric exercise induced myogenic gene expression in postmenopausal women. J Appl Physiol 107: 1381-1388, 2009.
27. Dreyer HC, Fujita S, Glynn EL, Drummond MJ, Volpi E, Rasmussen BB. Resistance exercise increases leg muscle protein synthesis and mTOR signalling independent of sex. Acta Physiol (Oxf) 199: 71-81, 2010.
28. 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.
29. Drummond MJ, Miyazaki M, Dreyer HC, Pennings B, Dhanani S, Volpi E, Esser KA, Rasmussen BB. Expression of growth-related genes in young and older human skeletal muscle following an acute stimulation of protein synthesis. J Appl Physiol 106: 1403-1411, 2009.
30. Enns DL, Iqbal S, Tiidus PM. Oestrogen receptors mediate oestrogeninduced increases in post-exercise rat skeletal muscle satellite cells. Acta Physiol (Oxf) 194: 81-93, 2008.
31. Enns DL, Tiidus PM. Estrogen influences satellite cell activation and proliferation following downhill running in rats. J Appl Physiol 104: 347-353, 2008.
32. Evans WJ, Ivy JL. Effects of testosterone propionate on hindlimbimmobilized rats. J Appl Physiol Respir Environ Exerc Physiol 52: 1643-1647, 1982.
33. Faulkner JA, Larkin LM, Claflin DR, Brooks SV. Age-related changes in the structure and function of skeletal muscles. Clin Exp Pharmacol Physiol 34: 1091-1096, 2007.
34. Ferrando AA, Sheffield-Moore M, Paddon-Jones D, Wolfe RR, Urban RJ. Differential anabolic effects of testosterone and amino acid feeding in older men. J Clin Endocrinol Metab 88: 358-362, 2003.
35. Fonseca H, Powers SK, Goncalves D, Santos A, Mota MP, Duarte JA. Physical inactivity is a major contributor to ovariectomy-induced sarcopenia. Int J Sports Med 33: 268-278, 2012.
36. Forbes GB. The effect of anabolic steroids on lean body mass: the dose response curve. Metabolism 34: 571-573, 1985.
37. Forbes GB, Reina JC. Adult lean body mass declines with age: some longitudinal observations. Metabolism 19: 653-663, 1970.
38. Ford LE, Detterline AJ, Ho KK, Cao W. Gender-and height-related limits of muscle strength in world weightlifting champions. J Appl Physiol 89: 1061-1064, 2000.
39. Frontera WR, Hughes VA, Fielding RA, Fiatarone MA, Evans WJ, Roubenoff R. Aging of skeletal muscle: a 12-yr longitudinal study. J Appl Physiol 88: 1321-1326, 2000.
40. Frontera WR, Hughes VA, Lutz KJ, Evans WJ. A cross-sectional study of muscle strength and mass in 45-to 78-yr-old men and women. J Appl Physiol 71: 644-650, 1991.
41. Fujita S, Rasmussen BB, Bell JA, Cadenas JG, Volpi E. Basal muscle intracellular amino acid kinetics in women and men. Am J Physiol Endocrinol Metab 292: E77-E83, 2007.
42. Glover EI, Phillips SM, Oates BR, Tang JE, Tarnopolsky MA, Selby A, Smith K, Rennie MJ. Immobilization induces anabolic resistance in human myofibrillar protein synthesis with low and high dose amino acid infusion. J Physiol 586: 6049-6061, 2008.
43. Greenhaff PL, Karagounis LG, Peirce N, Simpson EJ, Hazell M, Layfield R, Wackerhage H, Smith K, Atherton P, Selby A, Rennie MJ. 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: E595-E604, 2008.
44. Greising SM, Carey RS, Blackford JE, Dalton LE, Kosir AM, Lowe DA. Estradiol treatment, physical activity, and muscle function in ovarian-senescent mice. Exp Gerontol 46: 685-693, 2011.
45. Griggs RC, Kingston W, Jozefowicz RF, Herr BE, Forbes G, Halliday D. Effect of testosterone on muscle mass and muscle protein synthesis. J Appl Physiol 66: 498-503, 1989.
46. Hansen M, Kongsgaard M, Holm L, Skovgaard D, Magnusson SP, Qvortrup K, Larsen JO, Aagaard P, Dahl M, Serup A, Frystyk J, Flyvbjerg A, Langberg H, Kjaer M. Effect of estrogen on tendon collagen synthesis, tendon structural characteristics, and biomechanical properties in postmenopausal women. J Appl Physiol 106: 1385-1393, 2009.
47. Hansen M, Langberg H, Holm L, Miller BF, Petersen SG, Doessing S, Skovgaard D, Trappe T, Kjaer M. Effect of administration of oral contraceptives on the synthesis and breakdown of myofibrillar proteins in young women. Scand J Med Sci Sports 21: 62-72, 2011.
48. Hansen M, Miller BF, Holm L, Doessing S, Petersen SG, Skovgaard D, Frystyk J, Flyvbjerg A, Koskinen S, Pingel J, Kjaer M, Langberg H. Effect of administration of oral contraceptives in vivo on collagen synthesis in tendon and muscle connective tissue in young women. J Appl Physiol 106: 1435-1443, 2009.
49. Hansen M, Skovgaard D, Reitelseder S, Holm L, Langbjerg H, Kjaer M. Effects of estrogen replacement and lower androgen status on skeletal muscle collagen and myofibrillar protein synthesis in postmenopausal women. J Gerontol A Biol Sci Med Sci 67: 1005-1013, 2012.
50. Harjola VP, Jankala H, Harkonen M. The effect of androgen status on skeletal muscle myosin heavy chain mRNA and protein levels in rats recovering from immobilization. Eur J Appl Physiol 83: 427-433, 2000.
51. Harman SM, Metter EJ, Tobin JD, Pearson J, Blackman MR. Longitudinal effects of aging on serum total and free testosterone levels in healthy men. Baltimore Longitudinal Study of Aging. J Clin Endocrinol Metab 86: 724-731, 2001.
52. Haymond MW, Karl IE, Clarke WL, Pagliara AS, Santiago JV. Differences in circulating gluconeogenic substrates during short-term fasting in men, women, and children. Metabolism 31: 33-42, 1982.
53. Henderson GC, Dhatariya K, Ford GC, Klaus KA, Basu R, Rizza RA, Jensen MD, Khosla S, O'Brien P, Nair KS. Higher muscle protein synthesis in women than men across the lifespan, and failure of androgen administration to amend age-related decrements. FASEB J 23: 631-641, 2009.
54. Hubal MJ, Gordish-Dressman H, Thompson PD, Price TB, Hoffman EP, Angelopoulos TJ, Gordon PM, Moyna NM, Pescatello LS, Visich PS, Zoeller RF, Seip RL, Clarkson PM. Variability in muscle size and strength gain after unilateral resistance training. Med Sci Sports Exerc 37: 964-972, 2005.
55. Isidori AM, Giannetta E, Greco EA, Gianfrilli D, Bonifacio V, Isidori A, Lenzi A, Fabbri A. Effects of testosterone on body composition, bone metabolism and serum lipid profile in middle-aged men: a meta-analysis. Clin Endocrinol (Oxf) 63: 280-293, 2005.
56. Jackson JM, Blaine D, Powell-Tuck J, Korbonits M, Carey A, Elia M. Macro-and micronutrient losses and nutritional status resulting from 44 days of total fasting in a non-obese man. Nutrition 22: 889-897, 2006.
57. Jahn LA, Barrett EJ, Genco ML, Wei L, Spraggins TA, Fryburg DA. Tissue composition affects measures of postabsorptive human skeletal muscle metabolism: comparison across genders. J Clin Endocrinol Metab 84: 1007-1010, 1999.
58. Katznelson L, Finkelstein JS, Schoenfeld DA, Rosenthal Di, Anderson EJ, Klibanski A. Increase in bone density and lean body mass during testosterone administration in men with acquired hypogonadism. J Clin Endocrinol Metab 81: 4358-4365, 1996.
59. Kim JS, Kosek DJ, Petrella JK, Cross JM, Bamman MM. Resting and load-induced levels of myogenic gene transcripts differ between older adults with demonstrable sarcopenia and young men and women. J Appl Physiol 99: 2149-2158, 2005.
60. Koopman R, van Loon LJ. Aging, exercise, and muscle protein metabolism. J Appl Physiol 106: 2040-2048, 2009.
61. Kumar V, Selby A, Rankin D, Patel R, Atherton P, Hildebrandt W, Williams J, Smith K, Seynnes O, Hiscock N, Rennie MJ. Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. J Physiol 587: 211-217, 2009.
62. Kyle UG, Genton L, Hans D, Karsegard L, Slosman DO, Pichard C. Age-related differences in fat-free mass, skeletal muscle, body cell mass and fat mass between 18 and 94 years. Eur J Clin Nutr 55: 663-672, 2001.
63. Kyle UG, Genton L, Slosman DO, Pichard C. Fat-free and fat mass percentiles in 5225 healthy subjects aged 15 to 98 years. Nutrition 17: 534-541, 2001.
64. La Favor JD, Kraus RM, Carrithers JA, Roseno SL, Gavin TP, Hickner RC. Sex differences with aging in nutritive skeletal muscle blood flow: impact of exercise training, nitric oxide, and alpha-adrenergic-mediated mechanisms. Am J Physiol Heart Circ Physiol 307: H524-H532, 2014.
65. Lee SJ, Janssen I, Heymsfield SB, Ross R. Relation between wholebody and regional measures of human skeletal muscle. Am J Clin Nutr 80: 1215-1221, 2004.
66. Loos R, Thomis M, Maes HH, Beunen G, Claessens AL, Derom C, Legius E, Derom R, Vlietinck R. Gender-specific regional changes in genetic structure of muscularity in early adolescence. J Appl Physiol 82: 1802-1810, 1997.
67. Lynch NA, Metter EJ, Lindle RS, Fozard JL, Tobin JD, Roy TA, Fleg JL, Hurley BF. Muscle quality. I. Age-associated differences between arm and leg muscle groups. J Appl Physiol 86: 188-194, 1999.
68. Mamerow MM, Mettler JA, English KL, Casperson SL, Arentson-Lantz E, Sheffield-Moore M, Layman DK, Paddon-Jones D. Dietary protein distribution positively influences 24-h muscle protein synthesis in healthy adults. J Nutr 144: 876-880, 2014.
69. Markofski MM, Dickinson JM, Drummond MJ, Fry CS, Fujita S, Gundermann DM, Glynn EL, Jennings K, Paddon-Jones D, Reidy PT, Sheffield-Moore M, Timmerman KL, Rasmussen BB, Volpi E. Effect of age on basal muscle protein synthesis and mTORC1 signaling in a large cohort of young and older men and women. Exp Gerontol 65: 1-7, 2015.
70. McCall GE, Byrnes WC, Dickinson A, Pattany PM, Fleck SJ. Muscle fiber hypertrophy, hyperplasia, and capillary density in college men after resistance training. J Appl Physiol 81: 2004-2012, 1996.
71. McClung JM, Davis JM, Wilson MA, Goldsmith EC, Carson JA. Estrogen status and skeletal muscle recovery from disuse atrophy. J Appl Physiol 100: 2012-2023, 2006.
72. McGregor RA, Cameron-Smith D, Poppitt SD. It is not just muscle mass: a review of muscle quality, composition and metabolism during ageing as determinants of muscle function and mobility in later life. Longev Healthspan 3: 9, 2014.
73. Miller AE, MacDougall JD, Tarnopolsky MA, Sale DG. Gender differences in strength and muscle fiber characteristics. Eur J Appl Physiol Occup Physiol 66: 254-262, 1993.
74. Miller BF, Hansen M, Olesen JL, Flyvbjerg A, Schwarz P, Babraj JA, Smith K, Rennie MJ, Kjaer M. No effect of menstrual cycle on myofibrillar and connective tissue protein synthesis in contracting skeletal muscle. Am J Physiol Endocrinol Metab 290: E163-E168, 2006.
75. Miller BF, Hansen M, Olesen JL, Schwarz P, Babraj JA, Smith K, Rennie MJ, Kjaer M. Tendon collagen synthesis at rest and after exercise in women. J Appl Physiol 102: 541-546, 2007.
76. Miller BF, Olesen JL, Hansen M, Dossing S, Crameri RM, Welling RJ, Langberg H, Flyvbjerg A, Kjaer M, Babraj JA, Smith K, Rennie MJ. Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. J Physiol 567: 1021-1033, 2005.
77. Millward DJ, Garlick PJ, James WP, Nnanyelugo DO, Ryatt JS. Relationship between protein synthesis and RNA content in skeletal muscle. Nature 241: 204-205, 1973.
78. Mingrone G, Marino S, DeGaetano A, Capristo E, Heymsfield SB, Gasbarrini G, Greco AV. Different limit to the body's ability of increasing fat-free mass. Metabolism 50: 1004-1007, 2001.
79. Mittendorfer B, Andersen JL, Plomgaard P, Saltin B, Babraj JA, Smith K, Rennie MJ. Protein synthesis rates in human muscles: neither anatomical location nor fibre-type composition are major determinants. J Physiol 563: 203-211, 2005.
80. Moore DR, Churchward-Venne TA, Witard O, Breen L, Burd NA, Tipton KD, Phillips SM. Protein ingestion to stimulate myofibrillar protein synthesis requires greater relative protein intakes in healthy older versus younger men. J Gerontol A Biol Sci Med Sci 70: 57-62, 2015.
81. Moore DR, Phillips SM, Babraj JA, Smith K, Rennie MJ. Myofibrillar and collagen protein synthesis in human skeletal muscle in young men after maximal shortening and lengthening contractions. Am J Physiol Endocrinol Metab 288: E1153-E1159, 2005.
82. Moore DR, Robinson MJ, Fry JL, Tang JE, Glover EI, Wilkinson SB, Prior T, Tarnopolsky MA, Phillips SM. Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. Am J Clin Nutr 89: 161-168, 2009.
83. Morton RW, McGlory C, Phillips SM. Nutritional interventions to augment resistance training-induced skeletal muscle hypertrophy. Front Physiol 6: 245, 2015.
84. Narici MV, Roi GS, Landoni L, Minetti AE, Cerretelli P. Changes in force, cross-sectional area and neural activation during strength training and detraining of the human quadriceps. Eur J Appl Physiol Occup Physiol 59: 310-319, 1989.
85. Nguyen TV, Howard GM, Kelly PJ, Eisman JA. Bone mass, lean mass, and fat mass: same genes or same environments? Am J Epidemiol 147: 3-16, 1998.
86. Parise G, Mihic S, MacLennan D, Yarasheski KE, Tarnopolsky MA. Effects of acute creatine monohydrate supplementation on leucine kinetics and mixed-muscle protein synthesis. J Appl Physiol 91: 1041-1047, 2001.
87. Parker BA, Smithmyer SL, Pelberg JA, Mishkin AD, Proctor DN. Sex-specific influence of aging on exercising leg blood flow. J Appl Physiol 104: 655-664, 2008.
88. Pearson SJ, Young A, Macaluso A, Devito G, Nimmo MA, Cobbold M, Harridge SD. Muscle function in elite master weightlifters. Med Sci Sports Exerc 34: 1199-1206, 2002.
89. Pingel J, Langberg H, Skovgard D, Koskinen S, Flyvbjerg A, Frystyk J, Kjaer M, Hansen M. Effects of transdermal estrogen on collagen turnover at rest and in response to exercise in postmenopausal women. J Appl Physiol 113: 1040-1047, 2012.
90. Pollanen E, Ronkainen PH, Suominen H, Takala T, Koskinen S, Puolakka J, Sipila S, Kovanen V. Muscular transcriptome in postmenopausal women with or without hormone replacement. Rejuvenation Res 10: 485-500, 2007.
91. Raue U, Slivka D, Jemiolo B, Hollon C, Trappe S. Myogenic gene expression at rest and after a bout of resistance exercise in young (18-30 yr) and old (80-89 yr) women. J Appl Physiol 101: 53-59, 2006.
92. Rennie MJ, Wackerhage H, Spangenburg EE, Booth FW. Control of the size of the human muscle mass. Annu Rev Physiol 66: 799-828, 2004.
93. Roth SM, Ivey FM, Martel GF, Lemmer JT, Hurlbut DE, Siegel EL, Metter EJ, Fleg JL, Fozard JL, Kostek MC, Wernick DM, Hurley BF. Muscle size responses to strength training in young and older men and women. J Am Geriatr Soc 49: 1428-1433, 2001.
94. Sarwar G, Botting HG, Collins M. A comparison of fasting serum amino acid profiles of young and elderly subjects. J Am Coll Nutr 10: 668-674, 1991.
95. Scalzo RL, Peltonen GL, Binns SE, Shankaran M, Giordano GR, Hartley DA, Klochak AL, Lonac MC, Paris HL, Szallar SE, Wood LM, Peelor FF 3rd, Holmes WE, Hellerstein MK, Bell C, Hamilton KL, Miller BF. Greater muscle protein synthesis and mitochondrial biogenesis in males compared with females during sprint interval training. FASEB J 28: 2705-2714, 2014.
96. Seeman E, Hopper JL, Young NR, Formica C, Goss P, Tsalamandris C. Do genetic factors explain associations between muscle strength, lean mass, and bone density? A twin study. Am J Physiol Endocrinol Metab 270: E320-E327, 1996.
97. Shifren JL, Desindes S, McIlwain M, Doros G, Mazer NA. A randomized, open-label, crossover study comparing the effects of oral versus transdermal estrogen therapy on serum androgens, thyroid hormones, and adrenal hormones in naturally menopausal women. Menopause 14: 985-994, 2007.
98. Sitnick M, Foley AM, Brown M, Spangenburg EE. Ovariectomy prevents the recovery of atrophied gastrocnemius skeletal muscle mass. J Appl Physiol 100: 286-293, 2006.
99. Smith GI, Atherton P, Reeds DN, Mohammed BS, Jaffery H, Rankin D, Rennie MJ, Mittendorfer B. 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: 1308-1315, 2009.
100. Smith GI, Atherton P, Villareal DT, Frimel TN, Rankin D, Rennie MJ, Mittendorfer B. Differences in muscle protein synthesis and anabolic signaling in the postabsorptive state and in response to food in 65-80 year old men and women. PLoS One 3: e1875, 2008.
101. Smith GI, Reeds DN, Hall AM, Chambers KT, Finck BN, Mittendorfer B. Sexually dimorphic effect of aging on skeletal muscle protein synthesis. Biol Sex Differ 3: 11, 2012.
102. Smith GI, Villareal DT, Sinacore DR, Shah K, Mittendorfer B. Muscle protein synthesis response to exercise training in obese, older men and women. Med Sci Sports Exerc 44: 1259-1266, 2012.
103. Smith GI, Yoshino J, Reeds DN, Bradley D, Burrows RE, Heisey HD, Moseley AC, Mittendorfer B. Testosterone and progesterone, but not estradiol, stimulate muscle protein synthesis in postmenopausal women. J Clin Endocrinol Metab 99: 256-265, 2014.
104. Sonnet E, Lacut K, Roudaut N, Mottier D, Kerlan V, Oger E. Effects of the route of oestrogen administration on IGF-1 and IGFBP-3 in healthy postmenopausal women: results from a randomized placebocontrolled study. Clin Endocrinol (Oxf) 66: 626-631, 2007.
105. Sugiura T, Ito N, Goto K, Naito H, Yoshioka T, Powers SK. Estrogen administration attenuates immobilization-induced skeletal muscle atrophy in male rats. J Physiol Sci 56: 393-399, 2006.
106. Svensson J, Movérare-Skrtic S, Windahl S, Swanson C, Sjögren K. Stimulation of both estrogen and androgen receptors maintains skeletal muscle mass in gonadectomized male mice but mainly via different pathways. J Mol Endocrinol 45: 45-57, 2010.
107. Tesch PA, von Walden F, Gustafsson T, Linnehan RM, Trappe TA. Skeletal muscle proteolysis in response to short-term unloading in humans. J Appl Physiol 105: 902-906, 2008.
108. Thomis MA, Van Leemputte M, Maes HH, Blimkie CJ, Claessens AL, Marchal G, Willems E, Vlietinck RF, Beunen GP. Multivariate genetic analysis of maximal isometric muscle force at different elbow angles. J Appl Physiol 82: 959-967, 1997.
109. Tonson A, Ratel S, Le Fur Y, Cozzone P, Bendahan D. Effect of maturation on the relationship between muscle size and force production. Med Sci Sports Exerc 40: 918-925, 2008.
110. Toth MJ, Poehlman ET, Matthews DE, Tchernof A, MacCoss MJ. Effects of estradiol and progesterone on body composition, protein synthesis, and lipoprotein lipase in rats. Am J Physiol Endocrinol Metab 280: E496-E501, 2001.
111. Trappe T. Influence of aging and long-term unloading on the structure and function of human skeletal muscle. Appl Physiol Nutr Metab 34: 459-464, 2009.
112. Tsai WJ, McCormick KM, Brazeau DA, Brazeau GA. Estrogen effects on skeletal muscle insulin-like growth factor 1 and myostatin in ovariectomized rats. Exp Biol Med (Maywood) 232: 1314-1325, 2007.
113. Urban RJ, Bodenburg YH, Gilkison C, Foxworth J, Coggan AR, Wolfe RR, Ferrando A. Testosterone administration to elderly men increases skeletal muscle strength and protein synthesis. Am J Physiol Endocrinol Metab 269: E820-E826, 1995.
114. Velders M, Schleipen B, Fritzemeier KH, Zierau O, Diel P. Selective estrogen receptor-beta activation stimulates skeletal muscle growth and regeneration. FASEB J 26: 1909-1920, 2012.
115. Verdijk LB, Jonkers RA, Gleeson BG, Beelen M, Meijer K, Savelberg HH, Wodzig WK, Dendale P, van Loon LJ. Protein supplementation before and after exercise does not further augment skeletal muscle hypertrophy after resistance training in elderly men. Am J Clin Nutr 89: 608-616, 2009.
116. Volpi E, Sheffield-Moore M, Rasmussen BB, Wolfe RR. Basal muscle amino acid kinetics and protein synthesis in healthy young and older men. JAMA 286: 1206-1212, 2001.
117. Wall BT, Dirks ML, van Loon LJ. Skeletal muscle atrophy during short-term disuse: implications for age-related sarcopenia. Ageing Res Rev 12: 898-906, 2013.
118. Walts CT, Hanson ED, Delmonico MJ, Yao L, Wang MQ, Hurley BF. Do sex or race differences influence strength training effects on muscle or fat? Med Sci Sports Exerc 40: 669-676, 2008.
119. Welle S, Thornton C, Jozefowicz R, Statt M. Myofibrillar protein synthesis in young and old men. Am J Physiol Endocrinol Metab 264: E693-E698, 1993.
120. Wells JC. Sexual dimorphism of body composition. Best Pract Res Clin Endocrinol Metab 21: 415-430, 2007.
121. West DW, Burd NA, Churchward-Venne TA, Camera DM, Mitchell CJ, Baker SK, Hawley JA, Coffey VG, Phillips SM. Sex-based comparisons of myofibrillar protein synthesis after resistance exercise in the fed state. J Appl Physiol 112: 1805-1813, 2012.
122. Whitman SA, Wacker MJ, Richmond SR, Godard MP. Contributions of the ubiquitin-proteasome pathway and apoptosis to human skeletal muscle wasting with age. Pflugers Arch 450: 437-446, 2005.
123. Wilkes EA, Selby AL, Atherton PJ, Patel R, Rankin D, Smith K, Rennie MJ. Blunting of insulin inhibition of proteolysis in legs of older subjects may contribute to age-related sarcopenia. Am J Clin Nutr 90: 1343-1350, 2009.
124. Wimalawansa SM, Chapa MT, Wei JN, Westlund KN, Quast MJ, Wimalawansa SJ. Reversal of weightlessness-induced musculoskeletal losses with androgens: quantification by MRI. J Appl Physiol 86: 1841-1846, 1999.
125. Witard OC, Jackman SR, Breen L, Smith K, Selby A, Tipton KD. Myofibrillar muscle protein synthesis rates subsequent to a meal in response to increasing doses of whey protein at rest and after resistance exercise. Am J Clin Nutr 99: 86-95, 2014.
126. Yang Y, Breen L, Burd NA, Hector AJ, Churchward-Venne TA, Josse AR, Tarnopolsky MA, Phillips SM. Resistance exercise enhances myofibrillar protein synthesis with graded intakes of whey protein in older men. Br J Nutr 108: 1780-1788, 2012.
127. Yang Y, Churchward-Venne TA, Burd NA, Breen L, Tarnopolsky MA, Phillips SM. Myofibrillar protein synthesis following ingestion of soy protein isolate at rest and after resistance exercise in elderly men. Nutr Metab (Lond) 9: 57, 2012.
128. Yarrow JF, Conover CF, Beggs LA, Beck DT, Otzel DM, Balaez A, Combs SM, Miller JR, Ye F, Aguirre JI, Neuville KG, Williams AA, Conrad BP, Gregory CM, Wronski TJ, Bose PK, Borst SE. Testosterone dose dependently prevents bone and muscle loss in rodents after spinal cord injury. J Neurotrauma 31: 834-845, 2014.
129. Yasuda N, Glover EI, Phillips SM, Isfort RJ, Tarnopolsky MA. Sex-based differences in skeletal muscle function and morphology with short-term limb immobilization. J Appl Physiol 99: 1085-1092, 2005.