Integrated Myofibrillar Protein Synthesis in Recovery From Unaccustomed and Accustomed Resistance Exercise With and Without Multi-ingredient Supplementation in Overweight Older Men

Kirsten E Bell, Matthew S Brook, Tim Snijders, Dinesh Kumbhare, Gianni Parise, Ken Smith, Philip J Atherton, Stuart M Phillips, Kirsten E Bell, Matthew S Brook, Tim Snijders, Dinesh Kumbhare, Gianni Parise, Ken Smith, Philip J Atherton, Stuart M Phillips

Abstract

Background: We previously showed that daily consumption of a multi-ingredient nutritional supplement increased lean mass in older men, but did not enhance lean tissue gains during a high-intensity interval training (HIIT) plus resistance exercise training (RET) program. Here, we aimed to determine whether these divergent observations aligned with the myofibrillar protein synthesis (MyoPS) response to acute unaccustomed and accustomed resistance exercise. Methods: A sub-sample of our participants were randomly allocated (n = 15; age: 72 ± 7 years; BMI: 26.9 ± 3.1 kg/m2 [mean ± SD]) to ingest an experimental supplement (SUPP, n = 8: containing whey protein, creatine, vitamin D, and n-3 PUFA) or control beverage (CON, n = 7: 22 g maltodextrin) twice per day for 21 weeks. After 7 weeks of consuming the beverage alone (Phase 1: SUPP/CON only), subjects completed 12 weeks of RET (twice per week) + HIIT (once per week) (Phase 2: SUPP/CON + EX). Orally administered deuterated water was used to measure integrated rates of MyoPS over 48 h following a single session of resistance exercise pre- (unaccustomed) and post-training (accustomed). Results: Following an acute bout of accustomed resistance exercise, 0-24 h MyoPS was 30% higher than rest in the SUPP group (effect size: 0.86); however, in the CON group, 0-24 h MyoPS was 0% higher than rest (effect size: 0.04). Nonetheless, no within or between group changes in MyoPS were statistically significant. When collapsed across group, rates of MyoPS in recovery from acute unaccustomed resistance exercise were positively correlated with training-induced gains in whole body lean mass (r = 0.63, p = 0.01). Conclusion: There were no significant between-group differences in MyoPS pre- or post-training. Integrated rates of MyoPS post-acute exercise in the untrained state were positively correlated with training-induced gains in whole body lean mass. Our finding that supplementation did not alter 0-48 h MyoPS following 12 weeks of training suggests a possible adaptive response to longer-term increased protein intake and warrants further investigation. This study was registered at ClinicalTrials.gov. Clinical Trial Registration: www.ClinicalTrials.gov, identifier: NCT02281331.

Keywords: creatine; deuterated water; fractional synthesis rate; high-intensity interval training; n-3 PUFA; resistance exercise training; vitamin D; whey protein.

Figures

Figure 1
Figure 1
Overall study schematic (A) and acute MyoPS response protocol (B). (A) Participants were randomly assigned to consume a multi-ingredient supplement (SUPP, n = 8) or control (CON, n = 7) beverage twice per day for 21 weeks. Between weeks 8 and 19, inclusive, participants completed a 12 weeks combined RET (twice per week) + HIIT (once per week) exercise training program. Lean tissue mass (DXA) and strength (1RM) were assessed at baseline (week 0), as well as pre- (week 7; Phase 1: SUPP/CON) and post-training (week 20; Phase 2: SUPP/CON + EX). The integrated MyoPS response to acute resistance exercise was assessed during participants' initial RET session (UT, untrained; week 8) and 10 days following their last RET session (TR, trained; week 21). (B) Following a baseline saliva sample, participants consumed 150 mL 70% deuterated water (D2O; Day 0). On Days 2–4, we obtained a fasting muscle sample from the vastus lateralis. Immediately after their muscle biopsy on Day 2, participants completed a session of resistance exercise at 65% 1RM. Saliva samples were collected regularly throughout each acute response period to assess deuterium (2H) enrichment of total body water. Eight weeks prior to the untrained acute response (–8 weeks), we obtained an unenriched, fasted muscle sample for the measurement of resting FSR. SUPP, supplement; CON, control; RET, resistance exercise training; HIIT, high-intensity interval training; DXA, dual-energy x-ray absorptiometry; 1RM, one repetition maximum; MyoPS, myofibrillar protein synthesis; 2H, deuterium; D2O, deuterated water; UT, untrained; TR, trained; FSR, fractional synthesis rate.
Figure 2
Figure 2
Integrated day-to-day (A) and cumulative (B) myofibrillar protein synthesis in response to acute resistance exercise pre- and post-training. Individual day-to-day (i.e., temporal) data are presented on the inset line graph in (A). The SUPP group is presented in black; the CON group is presented in white. SUPP, supplement; CON, control; UT, untrained; TR, trained; FSR, fractional synthetic rate.
Figure 3
Figure 3
Correlation analysis. FSR 0–24 h after unaccustomed acute resistance exercise was positively associated with the change in (A) whole body and (B) leg fat- and bone-free (i.e., lean) mass during 12 weeks of multimodal (RET + HIIT) exercise training (Phase 2). Linear regression lines of best fit are shown in black. Dotted lines indicate 95% confidence intervals. UT, untrained; TR, trained; FSR, fractional synthesis rate; RET, resistance exercise training; HIIT, high-intensity interval training.

References

    1. Marzetti E, Calvani R, Tosato M, Cesari M, Di Bari M, Cherubini A, et al. . Sarcopenia: an overview. Aging Clin Exp Res. (2017). 29:11–7. 10.1007/s40520-016-0704-5
    1. Kumar V, Selby A, Rankin D, Patel R, Atherton P, Hildebrandt W, et al. . Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. J Physiol. (2009) 587:211–7. 10.1113/jphysiol.2008.164483
    1. Yang Y, Breen L, Burd NA, Hector AJ, Churchward-Venne TA, Josse AR, et al. . Resistance exercise enhances myofibrillar protein synthesis with graded intakes of whey protein in older men. Br J Nutr. (2012) 108:1780–8. 10.1017/S0007114511007422
    1. Morton RW, Murphy KT, McKellar SR, Schoenfeld BJ, Henselmans M, Helms E, et al. . A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training-induced gains in muscle mass and strength in healthy adults. Br J Sports Med. (2018) 52:376–84. 10.1136/bjsports-2017-097608
    1. O'Bryan KR, Doering TM, Morton RW, Coffey VG, Phillips SM, Cox GR. Do multi-ingredient protein supplements augment resistance training-induced gains in skeletal muscle mass and strength? A systematic review and meta-analysis of 35 trials. Br J Sports Med. (2019). 10.1136/bjsports-2018-099889 [Epub ahead of print].
    1. Bell KE, Snijders T, Zulyniak M, Kumbhare D, Parise G, Chabowski A, et al. . A whey protein-based multi-ingredient nutritional supplement stimulates gains in lean body mass and strength in healthy older men: a randomized controlled trial. PLoS ONE. (2017) 12:e0181387. 10.1371/journal.pone.0181387
    1. Rondanelli M, Klersy C, Terracol G, Talluri J, Maugeri R, Guido D, et al. . Whey protein, amino acids, and vitamin D supplementation with physical activity increases fat-free mass and strength, functionality, and quality of life and decreases inflammation in sarcopenic elderly. Am J Clin Nutr. (2016) 103:830–40. 10.3945/ajcn.115.113357
    1. Verreijen AM, Verlaan S, Engberink MF, Swinkels S, de Vogel-van den Bosch J, Weijs PJ. A high whey protein-, leucine-, and vitamin D-enriched supplement preserves muscle mass during intentional weight loss in obese older adults: a double-blind randomized controlled trial. Am J Clin Nutr. (2015) 101:279–86. 10.3945/ajcn.114.090290
    1. Candow DG, Little JP, Chilibeck PD, Abeysekara S, Zello GA, Kazachkov M, et al. . Low-dose creatine combined with protein during resistance training in older men. Med Sci Sports Exerc. (2008) 40:1645–52. 10.1249/MSS.0b013e318176b310
    1. Bell KE, Snijders T, Zulyniak MA, Kumbhare D, Parise G, Chabowski A, et al. . A multi-ingredient nutritional supplement enhances exercise training-related reductions in markers of systemic inflammation in healthy older men. Appl Physiol Nutr Metab. (2018) 43:299–302. 10.1139/apnm-2017-0533
    1. West DW, Phillips SM. Associations of exercise-induced hormone profiles and gains in strength and hypertrophy in a large cohort after weight training. Eur J Appl Physiol. (2012) 112:2693–702. 10.1007/s00421-011-2246-z
    1. Damas F, Phillips SM, Libardi CA, Vechin FC, Lixandrao ME, Jannig PR, et al. . Resistance training-induced changes in integrated myofibrillar protein synthesis are related to hypertrophy only after attenuation of muscle damage. J Physiol. (2016) 594:5209–22. 10.1113/JP272472
    1. Diabetes Canada Clinical Practice Guidelines Expert Committee Diabetes Canada 2018 clinical practice guidelines for the prevention and management of diabetes in Canada. Can J Diabetes. (2018) 42(Suppl. 1):S1–S325. Available online at:
    1. Snijders T, Bell KE, Nederveen JP, Saddler NI, Mazara N, Kumbhare DA, et al. Ingestion of a multi-ingredient supplement does not alter exercise-induced satellite cell responses in older men. J Nutr. (2018) 148:891–9. 10.1093/jn/nxy063
    1. Snijders T, Nederveen JP, Bell KE, Lau SW, Mazara N, Kumbhare DA, et al. . Prolonged exercise training improves the acute type II muscle fibre satellite cell response in healthy older men. J Physiol. (2019) 597:105–19. 10.1113/JP276260
    1. Burd NA, West DW, Staples AW, Atherton PJ, Baker JM, Moore DR, et al. . Low-load high volume resistance exercise stimulates muscle protein synthesis more than high-load low volume resistance exercise in young men. PLoS ONE. (2010) 5:e12033. 10.1371/journal.pone.0012033
    1. Wilkinson DJ, Franchi MV, Brook MS, Narici MV, Williams JP, Mitchell WK, et al. . A validation of the application of D(2)O stable isotope tracer techniques for monitoring day-to-day changes in muscle protein subfraction synthesis in humans. Am J Physiol Endocrinol Metab. (2014) 306:E571–9. 10.1152/ajpendo.00650.2013
    1. Brook MS, Wilkinson DJ, Mitchell WK, Lund JN, Phillips BE, Szewczyk NJ, et al. . Synchronous deficits in cumulative muscle protein synthesis and ribosomal biogenesis underlie age-related anabolic resistance to exercise in humans. J Physiol. (2016) 594:7399–417. 10.1113/JP272857
    1. MacDonald AJ, Small AC, Greig CA, Husi H, Ross JA, Stephens NA, et al. . A novel oral tracer procedure for measurement of habitual myofibrillar protein synthesis. Rapid Commun Mass Spectrom. (2013) 27:1769–77. 10.1002/rcm.6622
    1. 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. (2012) 108:958–62. 10.1017/S0007114511006271
    1. Smith GI, Atherton P, Reeds DN, Mohammed BS, Rankin D, Rennie MJ, et al. . Dietary omega-3 fatty acid supplementation increases the rate of muscle protein synthesis in older adults: a randomized controlled trial. Am J Clin Nutr. (2011) 93:402–12. 10.3945/ajcn.110.005611
    1. Smith GI, Atherton P, Reeds DN, Mohammed BS, Rankin D, Rennie MJ, et al. . Omega-3 polyunsaturated fatty acids augment the muscle protein anabolic response to hyperinsulinaemia-hyperaminoacidaemia in healthy young and middle-aged men and women. Clin Sci. (2011) 121:267–78. 10.1042/CS20100597
    1. Chanet A, Verlaan S, Salles J, Giraudet C, Patrac V, Pidou V, et al. . Supplementing breakfast with a vitamin D and leucine-enriched whey protein medical nutrition drink enhances postprandial muscle protein synthesis and muscle mass in healthy older men. J Nutr. (2017) 147:2262–71. 10.3945/jn.117.252510
    1. Hector AJ, Marcotte GR, Churchward-Venne TA, Murphy CH, Breen L, von Allmen M, et al. . Whey protein supplementation preserves postprandial myofibrillar protein synthesis during short-term energy restriction in overweight and obese adults. J Nutr. (2015) 145:246–52. 10.3945/jn.114.200832
    1. Murphy CH, Churchward-Venne TA, Mitchell CJ, Kolar NM, Kassis A, Karagounis LG, et al. . Hypoenergetic diet-induced reductions in myofibrillar protein synthesis are restored with resistance training and balanced daily protein ingestion in older men. Am J Physiol Endocrinol Metab. (2015) 308:E734–43. 10.1152/ajpendo.00550.2014
    1. Pasiakos SM, Cao JJ, Margolis LM, Sauter ER, Whigham LD, McClung JP, et al. . Effects of high-protein diets on fat-free mass and muscle protein synthesis following weight loss: a randomized controlled trial. FASEB J. (2013) 27:3837–47. 10.1096/fj.13-230227
    1. Gorissen SH, Horstman AM, Franssen R, Kouw IW, Wall BT, Burd NA, et al. Habituation to low or high protein intake does not modulate basal or postprandial muscle protein synthesis rates: a randomized trial. Am J Clin Nutr. (2017) 105:332–42. 10.3945/ajcn.115.129924
    1. Hursel R, Martens EA, Gonnissen HK, Hamer HM, Senden JM, van Loon LJ, et al. Prolonged adaptation to a low or high protein diet does not modulate basal muscle protein synthesis rates - a substudy. PLoS ONE. (2015) 10:e0137183 10.1371/journal.pone.0137183
    1. Pennings B, Boirie Y, Senden JM, Gijsen AP, Kuipers H, van Loon LJ. Whey protein stimulates postprandial muscle protein accretion more effectively than do casein and casein hydrolysate in older men. Am J Clin Nutr. (2011) 93:997–1005. 10.3945/ajcn.110.008102
    1. Churchward-Venne TA, Murphy CH, Longland TM, Phillips SM. Role of protein and amino acids in promoting lean mass accretion with resistance exercise and attenuating lean mass loss during energy deficit in humans. Amino Acids. (2013) 45:231–40. 10.1007/s00726-013-1506-0
    1. Bell KE, Seguin C, Parise G, Baker SK, Phillips SM. Day-to-day changes in muscle protein synthesis in recovery from resistance, aerobic, and high-intensity interval exercise in older men. J Gerontol A Biol Sci Med Sci. (2015) 70:1024–9. 10.1093/gerona/glu313
    1. Murphy CH, Saddler NI, Devries MC, McGlory C, Baker SK, Phillips SM. Leucine supplementation enhances integrative myofibrillar protein synthesis in free-living older men consuming lower- and higher-protein diets: a parallel-group crossover study. Am J Clin Nutr. (2016) 104:1594–606. 10.3945/ajcn.116.136424
    1. Mayhew DL, Kim JS, Cross JM, Ferrando AA, Bamman MM. Translational signaling responses preceding resistance training-mediated myofiber hypertrophy in young and old humans. J Appl Physiol (1985). (2009) 107:1655–62. 10.1152/japplphysiol.91234.2008
    1. Dickinson JM, Gundermann DM, Walker DK, Reidy PT, Borack MS, Drummond MJ, et al. . Leucine-enriched amino acid ingestion after resistance exercise prolongs myofibrillar protein synthesis and amino acid transporter expression in older men. J Nutr. (2014) 144:1694–702. 10.3945/jn.114.198671
    1. Sheffield-Moore M, Paddon-Jones D, Sanford AP, Rosenblatt JI, Matlock AG, Cree MG, et al. . Mixed muscle and hepatic derived plasma protein metabolism is differentially regulated in older and younger men following resistance exercise. Am J Physiol Endocrinol Metab. (2005) 288:E922–9. 10.1152/ajpendo.00358.2004
    1. Beals JW, Skinner SK, McKenna CF, Poozhikunnel EG, Farooqi SA, van Vliet S, et al. . Altered anabolic signalling and reduced stimulation of myofibrillar protein synthesis after feeding and resistance exercise in people with obesity. J Physiol. (2018) 596:5119–33. 10.1113/JP276210
    1. Mitchell CJ, Churchward-Venne TA, Parise G, Bellamy L, Baker SK, Smith K, et al. Acute post-exercise myofibrillar protein synthesis is not correlated with resistance training-induced muscle hypertrophy in young men. PLoS ONE. (2014) 9:e89431 10.1371/journal.pone.0089431
    1. Peterson MD, Sen A, Gordon PM. Influence of resistance exercise on lean body mass in aging adults: a meta-analysis. Med Sci Sports Exerc. (2011) 43:249–58. 10.1249/MSS.0b013e3181eb6265
    1. Nana A, Slater GJ, Stewart AD, Burke LM. Methodology review: using dual-energy X-ray absorptiometry (DXA) for the assessment of body composition in athletes and active people. Int J Sport Nutr Exerc Metab. (2015) 25:198–215. 10.1123/ijsnem.2013-0228
    1. Mitchell CJ, Milan AM, Mitchell SM, Zeng N, Ramzan F, Sharma P, et al. . The effects of dietary protein intake on appendicular lean mass and muscle function in elderly men: a 10-wk randomized controlled trial. Am J Clin Nutr. (2017) 106:1375–83. 10.3945/ajcn.117.160325
    1. Fluharty FL, McClure KE. Effects of dietary energy intake and protein concentration on performance and visceral organ mass in lambs. J Amin Sci. (1997) 75:604–10. 10.2527/1997.753604x
    1. Hammond KA, Janes DN. The effects of increased protein intake on kidney size and function. J Exp Biol. (1998) 201:2081–90.

Source: PubMed

3
購読する