The muscle protein synthetic response to food ingestion

Meat Science

Volumn 109, Issue , 2015, Pages 96-100

  Gorissen, Stefan H M ^a   Rémond, Didier ^b,c   van Loon, Luc J C ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b INRA and University of Auvergne   (France)

^c UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

Aging; Meat; Muscle mass maintenance; Muscle protein synthesis; Protein digestion and absorption

Indexed keywords

AGING OF MATERIALS; AMINO ACIDS; BIOSYNTHESIS; FEEDING; FOOD PRODUCTS; MEATS; MUSCLE; NUTRITION;

AMINO ACID UPTAKE; DIETARY PROTEINS; FUNCTIONAL CAPACITY; INSULIN RELEASE; MUSCLE MASS; MUSCLE PROTEINS; PHYSICAL ACTIVITY; PROTEIN DIGESTION;

PROTEINS;

MUSCLE PROTEIN; PROTEIN INTAKE;

ANIMAL; BIOSYNTHESIS; CALORIC INTAKE; DAIRY PRODUCT; EATING; GROWTH, DEVELOPMENT AND AGING; HUMAN; MEAT; METABOLISM; PHARMACOLOGY; POSTPRANDIAL STATE; PROTEIN INTAKE; PROTEIN SYNTHESIS; SKELETAL MUSCLE;

ANIMALS; DAIRY PRODUCTS; DIETARY PROTEINS; EATING; ENERGY INTAKE; HUMANS; MEAT; MUSCLE PROTEINS; MUSCLE, SKELETAL; POSTPRANDIAL PERIOD; PROTEIN BIOSYNTHESIS;

EID: 84937163888     PISSN: 03091740     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.meatsci.2015.05.009     Document Type: Review

References (66)

1. Adechian S., Balage M., Remond D., Migne C., Quignard-Boulange A., Marset-Baglieri A., et al. Protein feeding pattern, casein feeding, or milk-soluble protein feeding did not change the evolution of body composition during a short-term weight loss program. American Journal of Physiology - Endocrinology and Metabolism 2012, 303(8):E973-E982. 10.1152/ajpendo.00285.2012.
2. Areta J.L., Burke L.M., Ross M.L., Camera D.M., West D.W., Broad E.M., et al. Timing and distribution of protein ingestion during prolonged recovery from resistance exercise alters myofibrillar protein synthesis. The Journal of Physiology 2013, 591(Pt 9):2319-2331. 10.1113/jphysiol.2012.244897.
3. Arnal M.A., Mosoni L., Boirie Y., Gachon P., Genest M., Bayle G., et al. Protein turnover modifications induced by the protein feeding pattern still persist after the end of the diets. American Journal of Physiology - Endocrinology and Metabolism 2000, 278(5):E902-E909.
4. Arnal M.A., Mosoni L., Boirie Y., Houlier M.L., Morin L., Verdier E., et al. Protein pulse feeding improves protein retention in elderly women. The American Journal of Clinical Nutrition 1999, 69(6):1202-1208.
5. Arnal M.A., Mosoni L., Boirie Y., Houlier M.L., Morin L., Verdier E., et al. Protein feeding pattern does not affect protein retention in young women. The Journal of Nutrition 2000, 130(7):1700-1704.
6. Barbe F., Menard O., Le Gouar Y., Buffiere C., Famelart M.H., Laroche B., et al. The heat treatment and the gelation are strong determinants of the kinetics of milk proteins digestion and of the peripheral availability of amino acids. Food Chemistry 2013, 136(3-4):1203-1212. 10.1016/j.foodchem.2012.09.022.
7. Barbe F., Menard O., Le Gouar Y., Buffiere C., Famelart M.H., Laroche B., et al. Acid and rennet gels exhibit strong differences in the kinetics of milk protein digestion and amino acid bioavailability. Food Chemistry 2014, 143:1-8. 10.1016/j.foodchem.2013.07.100.
8. Bax M.L., Aubry L., Ferreira C., Daudin J.D., Gatellier P., Remond D., et al. Cooking temperature is a key determinant of in vitro meat protein digestion rate: Investigation of underlying mechanisms. Journal of Agricultural and Food Chemistry 2012, 60(10):2569-2576. 10.1021/jf205280y.
9. Bax M.L., Buffiere C., Hafnaoui N., Gaudichon C., Savary-Auzeloux I., Dardevet D., et al. Effects of meat cooking, and of ingested amount, on protein digestion speed and entry of residual proteins into the colon: a study in minipigs. PLoS ONE 2013, 8(4):e61252. 10.1371/journal.pone.0061252.
10. Boirie Y., Dangin M., Gachon P., Vasson M.P., Maubois J.L., Beaufrere B. Slow and fast dietary proteins differently modulate postprandial protein accretion. Proceedings of the National Academy of Sciences of the United States of America 1997, 94(26):14930-14935.
11. Boirie Y., Gachon P., Beaufrere B. Splanchnic and whole-body leucine kinetics in young and elderly men. The American Journal of Clinical Nutrition 1997, 65(2):489-495.
12. Bouillanne O., Curis E., Hamon-Vilcot B., Nicolis I., Chretien P., Schauer N., et al. Impact of protein pulse feeding on lean mass in malnourished and at-risk hospitalized elderly patients: A randomized controlled trial. Clinical Nutrition 2013, 32(2):186-192. 10.1016/j.clnu.2012.08.015.
13. Bouillanne O., Neveux N., Nicolis I., Curis E., Cynober L., Aussel C. Long-lasting improved amino acid bioavailability associated with protein pulse feeding in hospitalized elderly patients: A randomized controlled trial. Nutrition 2014, 30(5):544-550. 10.1016/j.nut.2013.10.006.
14. Burd N.A., Gorissen S.H., van Loon L.J. Anabolic resistance of muscle protein synthesis with aging. Exercise and Sport Sciences Reviews 2013, 41(3):169-173. 10.1097/JES.0b013e318292f3d5.
15. Burd N.A., Tang J.E., Moore D.R., Phillips S.M. Exercise training and protein metabolism: influences of contraction, protein intake, and sex-based differences. Journal of Applied Physiology 2009, 106(5):1692-1701. 10.1152/japplphysiol.91351.2008.
16. Burd N.A., West D.W., Moore D.R., Atherton P.J., Staples A.W., Prior T., et al. Enhanced amino acid sensitivity of myofibrillar protein synthesis persists for up to 24h after resistance exercise in young men. The Journal of Nutrition 2011, 141(4):568-573. 10.3945/jn.110.135038.
17. Cuthbertson D., Smith K., Babraj J., Leese G., Waddell T., Atherton P., et al. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB Journal 2005, 19(3):422-424. 10.1096/fj.04-2640fje.
18. Dangin M., Boirie Y., Garcia-Rodenas C., Gachon P., Fauquant J., Callier P., et al. The digestion rate of protein is an independent regulating factor of postprandial protein retention. American Journal of Physiology - Endocrinology and Metabolism 2001, 280(2):E340-E348.
19. Drummond M.J., Glynn E.L., Fry C.S., Timmerman K.L., Volpi E., Rasmussen B.B. An increase in essential amino acid availability upregulates amino acid transporter expression in human skeletal muscle. American Journal of Physiology - Endocrinology and Metabolism 2010, 298(5):E1011-E1018. 10.1152/ajpendo.00690.2009.
20. Elliot T.A., Cree M.G., Sanford A.P., Wolfe R.R., Tipton K.D. Milk ingestion stimulates net muscle protein synthesis following resistance exercise. Medicine and Science in Sports and Exercise 2006, 38(4):667-674. 10.1249/01.mss.0000210190.64458.25.
21. Fouillet H., Mariotti F., Gaudichon C., Bos C., Tome D. Peripheral and splanchnic metabolism of dietary nitrogen are differently affected by the protein source in humans as assessed by compartmental modeling. The Journal of Nutrition 2002, 132(1):125-133.
22. Fujita S., Glynn E.L., Timmerman K.L., Rasmussen B.B., Volpi E. 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 2009, 52(9):1889-1898. 10.1007/s00125-009-1430-8.
23. Glynn E.L., Fry C.S., Drummond M.J., Dreyer H.C., Dhanani S., Volpi E., et al. Muscle protein breakdown has a minor role in the protein anabolic response to essential amino acid and carbohydrate intake following resistance exercise. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2010, 299(2):R533-R540. 10.1152/ajpregu.00077.2010.
24. Glynn E.L., Fry C.S., Timmerman K.L., Drummond M.J., Volpi E., Rasmussen B.B. Addition of carbohydrate or alanine to an essential amino acid mixture does not enhance human skeletal muscle protein anabolism. The Journal of Nutrition 2013, 143(3):307-314. 10.3945/jn.112.168203.
25. Gorissen S.H., Burd N.A., Hamer H.M., Gijsen A.P., Groen B.B., van Loon L.J. Carbohydrate coingestion delays dietary protein digestion and absorption but does not modulate postprandial muscle protein accretion. The Journal of Clinical Endocrinology and Metabolism 2014, 99(6):2250-2258. 10.1210/jc.2013-3970.
26. Greenhaff P.L., Karagounis L.G., Peirce N., Simpson E.J., Hazell M., Layfield R., et al. Disassociation between the effects of amino acids and insulin on signaling, ubiquitin ligases, and protein turnover in human muscle. American Journal of Physiology - Endocrinology and Metabolism 2008, 295(3):E595-E604. 10.1152/ajpendo.90411.2008.
27. Groen B.B., Res P.T., Pennings B., Hertle E., Senden J.M., Saris W.H., et al. Intragastric protein administration stimulates overnight muscle protein synthesis in elderly men. American Journal of Physiology - Endocrinology and Metabolism 2012, 302(1):E52-E60. 10.1152/ajpendo.00321.2011.
28. Guillet C., Prod'homme M., Balage M., Gachon P., Giraudet C., Morin L., et al. Impaired anabolic response of muscle protein synthesis is associated with S6K1 dysregulation in elderly humans. FASEB Journal 2004, 18(13):1586-1587. 10.1096/fj.03-1341fje.
29. Hamer H.M., Wall B.T., Kiskini A., de Lange A., Groen B.B., Bakker J.A., et al. Carbohydrate co-ingestion with protein does not further augment post-prandial muscle protein accretion in older men. Nutrition & Metabolism (London) 2013, 10(1):15. 10.1186/1743-7075-10-15.
30. Katsanos C.S., Kobayashi H., Sheffield-Moore M., Aarsland A., Wolfe R.R. Aging is associated with diminished accretion of muscle proteins after the ingestion of a small bolus of essential amino acids. The American Journal of Clinical Nutrition 2005, 82(5):1065-1073.
31. Katsanos C.S., Kobayashi H., Sheffield-Moore M., Aarsland A., Wolfe R.R. A high proportion of leucine is required for optimal stimulation of the rate of muscle protein synthesis by essential amino acids in the elderly. American Journal of Physiology - Endocrinology and Metabolism 2006, 291(2):E381-E387. 10.1152/ajpendo.00488.2005.
32. Kim I.Y., Schutzler S., Schrader A., Spencer H., Kortebein P., Deutz N.E., et al. Quantity of dietary protein intake, but not pattern of intake, affects net protein balance primarily through differences in protein synthesis in older adults. American Journal of Physiology - Endocrinology and Metabolism 2015, 308(1):E21-E28. 10.1152/ajpendo.00382.2014.
33. Koopman R., Beelen M., Stellingwerff T., Pennings B., Saris W.H., Kies A.K., et al. Coingestion of carbohydrate with protein does not further augment postexercise muscle protein synthesis. American Journal of Physiology - Endocrinology and Metabolism 2007, 293(3):E833-E842. 10.1152/ajpendo.00135.2007.
34. Koopman R., Crombach N., Gijsen A.P., Walrand S., Fauquant J., Kies A.K., et al. Ingestion of a protein hydrolysate is accompanied by an accelerated in vivo digestion and absorption rate when compared with its intact protein. The American Journal of Clinical Nutrition 2009, 90(1):106-115. 10.3945/ajcn.2009.27474.
35. Koopman R., Walrand S., Beelen M., Gijsen A.P., Kies A.K., Boirie Y., et al. Dietary protein digestion and absorption rates and the subsequent postprandial muscle protein synthetic response do not differ between young and elderly men. The Journal of Nutrition 2009, 139(9):1707-1713. 10.3945/jn.109.109173.
36. Mahe S., Roos N., Benamouzig R., Davin L., Luengo C., Gagnon L., et al. Gastrojejunal kinetics and the digestion of [15N]beta-lactoglobulin and casein in humans: The influence of the nature and quantity of the protein. The American Journal of Clinical Nutrition 1996, 63(4):546-552.
37. Mamerow M.M., Mettler J.A., English K.L., Casperson S.L., Arentson-Lantz E., Sheffield-Moore M., et al. Dietary protein distribution positively influences 24-h muscle protein synthesis in healthy adults. The Journal of Nutrition 2014, 144(6):876-880. 10.3945/jn.113.185280.
38. Moore D.R., Areta J., Coffey V.G., Stellingwerff T., Phillips S.M., Burke L.M., et al. Daytime pattern of post-exercise protein intake affects whole-body protein turnover in resistance-trained males. Nutrition & Metabolism (London) 2012, 9(1):91. 10.1186/1743-7075-9-91.
39. Moore D.R., Robinson M.J., Fry J.L., Tang J.E., Glover E.I., Wilkinson S.B., et al. Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. The American Journal of Clinical Nutrition 2009, 89(1):161-168. 10.3945/ajcn.2008.26401.
40. Pennings B., Boirie Y., Senden J.M., Gijsen A.P., Kuipers H., van Loon L.J. Whey protein stimulates postprandial muscle protein accretion more effectively than do casein and casein hydrolysate in older men. The American Journal of Clinical Nutrition 2011, 93(5):997-1005. 10.3945/ajcn.110.008102.
41. Pennings B., Groen B., de Lange A., Gijsen A.P., Zorenc A.H., Senden J.M., et al. Amino acid absorption and subsequent muscle protein accretion following graded intakes of whey protein in elderly men. American Journal of Physiology - Endocrinology and Metabolism 2012, 302(8):E992-E999. 10.1152/ajpendo.00517.2011.
42. Pennings B., Groen B.B., van Dijk J.W., de Lange A., Kiskini A., Kuklinski M., et al. Minced beef is more rapidly digested and absorbed than beef steak, resulting in greater postprandial protein retention in older men. The American Journal of Clinical Nutrition 2013, 98(1):121-128. 10.3945/ajcn.112.051201.
43. Pennings B., Koopman R., Beelen M., Senden J.M., Saris W.H., van Loon L.J. Exercising before protein intake allows for greater use of dietary protein-derived amino acids for de novo muscle protein synthesis in both young and elderly men. The American Journal of Clinical Nutrition 2011, 93(2):322-331. 10.3945/ajcn.2010.29649.
44. Phillips S.M. Insulin and muscle protein turnover in humans: Stimulatory, permissive, inhibitory, or all of the above?. American Journal of Physiology - Endocrinology and Metabolism 2008, 295(4):E731. 10.1152/ajpendo.90569.2008.
45. Rasmussen B.B., Fujita S., Wolfe R.R., Mittendorfer B., Roy M., Rowe V.L., et al. Insulin resistance of muscle protein metabolism in aging. FASEB Journal 2006, 20(6):768-769. 10.1096/fj.05-4607fje.
46. Remond D., Machebeuf M., Yven C., Buffiere C., Mioche L., Mosoni L., et al. Postprandial whole-body protein metabolism after a meat meal is influenced by chewing efficiency in elderly subjects. The American Journal of Clinical Nutrition 2007, 85(5):1286-1292.
47. Rennie M.J. Anabolic resistance: The effects of aging, sexual dimorphism, and immobilization on human muscle protein turnover. Applied Physiology, Nutrition and Metabolism 2009, 34(3):377-381. 10.1139/h09-012.
48. Res P.T., Groen B., Pennings B., Beelen M., Wallis G.A., Gijsen A.P., et al. Protein ingestion before sleep improves postexercise overnight recovery. Medicine and Science in Sports and Exercise 2012, 44(8):1560-1569. 10.1249/MSS.0b013e31824cc363.
49. Rieu I., Balage M., Sornet C., Giraudet C., Pujos E., Grizard J., et al. Leucine supplementation improves muscle protein synthesis in elderly men independently of hyperaminoacidaemia. The Journal of Physiology 2006, 575(Pt 1):305-315. 10.1113/jphysiol.2006.110742.
50. Robinson M.J., Burd N.A., Breen L., Rerecich T., Yang Y., Hector A.J., et al. Dose-dependent responses of myofibrillar protein synthesis with beef ingestion are enhanced with resistance exercise in middle-aged men. Applied Physiology, Nutrition and Metabolism 2013, 38(2):120-125. 10.1139/apnm-2012-0092.
51. Staples A.W., Burd N.A., West D.W., Currie K.D., Atherton P.J., Moore D.R., et al. Carbohydrate does not augment exercise-induced protein accretion versus protein alone. Medicine and Science in Sports and Exercise 2011, 43(7):1154-1161. 10.1249/MSS.0b013e31820751cb.
52. Symons T.B., Schutzler S.E., Cocke T.L., Chinkes D.L., Wolfe R.R., Paddon-Jones D. Aging does not impair the anabolic response to a protein-rich meal. The American Journal of Clinical Nutrition 2007, 86(2):451-456.
53. Symons T.B., Sheffield-Moore M., Mamerow M.M., Wolfe R.R., Paddon-Jones D. The anabolic response to resistance exercise and a protein-rich meal is not diminished by age. The Journal of Nutrition, Health & Aging 2011, 15(5):376-381.
54. Symons T.B., Sheffield-Moore M., Wolfe R.R., Paddon-Jones D. A moderate serving of high-quality protein maximally stimulates skeletal muscle protein synthesis in young and elderly subjects. Journal of the American Dietetic Association 2009, 109(9):1582-1586. 10.1016/j.jada.2009.06.369.
55. Tang J.E., Moore D.R., Kujbida G.W., Tarnopolsky M.A., Phillips S.M. Ingestion of whey hydrolysate, casein, or soy protein isolate: Effects on mixed muscle protein synthesis at rest and following resistance exercise in young men. Journal of Applied Physiology 2009, 107(3):987-992. 10.1152/japplphysiol.00076.2009.
56. Tieland M., Borgonjen-Van den Berg K.J., van Loon L.J., de Groot L.C. Dietary protein intake in community-dwelling, frail, and institutionalized elderly people: Scope for improvement. European Journal of Nutrition 2012, 51(2):173-179. 10.1007/s00394-011-0203-6.
57. Timmerman K.L., Lee J.L., Dreyer H.C., Dhanani S., Glynn E.L., Fry C.S., et al. Insulin stimulates human skeletal muscle protein synthesis via an indirect mechanism involving endothelial-dependent vasodilation and mammalian target of rapamycin complex 1 signaling. The Journal of Clinical Endocrinology and Metabolism 2010, 95(8):3848-3857. 10.1210/jc.2009-2696.
58. Timmerman K.L., Lee J.L., Fujita S., Dhanani S., Dreyer H.C., Fry C.S., et al. Pharmacological vasodilation improves insulin-stimulated muscle protein anabolism but not glucose utilization in older adults. Diabetes 2010, 59(11):2764-2771. 10.2337/db10-0415.
59. Volpi E., Mittendorfer B., Rasmussen B.B., Wolfe R.R. The response of muscle protein anabolism to combined hyperaminoacidemia and glucose-induced hyperinsulinemia is impaired in the elderly. The Journal of Clinical Endocrinology and Metabolism 2000, 85(12):4481-4490. 10.1210/jcem.85.12.7021.
60. Volpi E., Mittendorfer B., Wolf S.E., Wolfe R.R. Oral amino acids stimulate muscle protein anabolism in the elderly despite higher first-pass splanchnic extraction. The American Journal of Physiology 1999, 277(3 Pt 1):E513-E520.
61. Volpi E., Sheffield-Moore M., Rasmussen B.B., Wolfe R.R. Basal muscle amino acid kinetics and protein synthesis in healthy young and older men. JAMA 2001, 286(10):1206-1212.
62. Wall B.T., Hamer H.M., de Lange A., Kiskini A., Groen B.B., Senden J.M., et al. Leucine co-ingestion improves post-prandial muscle protein accretion in elderly men. Clinical Nutrition 2013, 32(3):412-419. 10.1016/j.clnu.2012.09.002.
63. West D.W., Burd N.A., Coffey V.G., Baker S.K., Burke L.M., Hawley J.A., et al. Rapid aminoacidemia enhances myofibrillar protein synthesis and anabolic intramuscular signaling responses after resistance exercise. The American Journal of Clinical Nutrition 2011, 94(3):795-803. 10.3945/ajcn.111.013722.
64. Wilkinson S.B., Tarnopolsky M.A., Macdonald M.J., Macdonald J.R., Armstrong D., Phillips S.M. Consumption of fluid skim milk promotes greater muscle protein accretion after resistance exercise than does consumption of an isonitrogenous and isoenergetic soy-protein beverage. The American Journal of Clinical Nutrition 2007, 85(4):1031-1040.
65. Witard O.C., Jackman S.R., Breen L., Smith K., Selby A., Tipton K.D. Myofibrillar muscle protein synthesis rates subsequent to a meal in response to increasing doses of whey protein at rest and after resistance exercise. The American Journal of Clinical Nutrition 2014, 99(1):86-95. 10.3945/ajcn.112.055517.
66. Yang Y., Churchward-Venne T.A., Burd N.A., Breen L., Tarnopolsky M.A., Phillips S.M. Myofibrillar protein synthesis following ingestion of soy protein isolate at rest and after resistance exercise in elderly men. Nutrition & Metabolism (London) 2012, 9(1):57. 10.1186/1743-7075-9-57.