Literature DB >> 29532476

Effect of resistance training and protein intake pattern on myofibrillar protein synthesis and proteome kinetics in older men in energy restriction.

Caoileann H Murphy1, Mahalakshmi Shankaran2,3, Tyler A Churchward-Venne1, Cameron J Mitchell1, Nathan M Kolar1, Louise M Burke4, John A Hawley5,6, Amira Kassis7, Leonidas G Karagounis7, Kelvin Li2,3, Chelsea King2, Marc Hellerstein2,3, Stuart M Phillips1.   

Abstract

KEY POINTS: Strategies to enhance the loss of fat while preserving muscle mass during energy restriction are of great importance to prevent sarcopenia in overweight older adults. We show for the first time that the integrated rate of synthesis of numerous individual contractile, cytosolic and mitochondrial skeletal muscle proteins was increased by resistance training (RT) and unaffected by dietary protein intake pattern during energy restriction in free-living, obese older men. We observed a correlation between the synthetic rates of skeletal muscle-derived proteins obtained in serum (creatine kinase M-type, carbonic anhydrase 3) and the synthetic rates of proteins obtained via muscle sampling; and that the synthesis rates of these proteins in serum revealed the stimulatory effects of RT. These results have ramifications for understanding the influence of RT on skeletal muscle and are consistent with the role of RT in maintaining muscle protein synthesis and potentially supporting muscle mass preservation during weight loss. ABSTRACT: We determined how the pattern of protein intake and resistance training (RT) influenced longer-term (2 weeks) integrated myofibrillar protein synthesis (MyoPS) during energy restriction (ER). MyoPS and proteome kinetics were measured during 2 weeks of ER alone and 2 weeks of ER plus RT (ER + RT) in overweight/obese older men. Participants were randomized to consume dietary protein in a balanced (BAL: 25% daily protein per meal × 4 meals) or skewed (SKEW: 7:17:72:4% daily protein per meal) pattern (n = 10 per group). Participants ingested deuterated water during the consecutive 2-week periods, and skeletal muscle biopsies and serum were obtained at the beginning and conclusion of ER and ER + RT. Bulk MyoPS (i.e. synthesis of the myofibrillar protein sub-fraction) and the synthetic rates of numerous individual skeletal muscle proteins were quantified. Bulk MyoPS was not affected by protein distribution during ER or ER + RT (ER: BAL = 1.24 ± 0.31%/day, SKEW = 1.26 ± 0.37%/day; ER + RT: BAL = 1.64 ± 0.48%/day, SKEW = 1.52 ± 0.66%/day) but was ∼26% higher during ER + RT than during ER (P = 0.023). The synthetic rates of 175 of 190 contractile, cytosolic and mitochondrial skeletal muscle proteins, as well as synthesis of muscle-derived proteins measured in serum, creatine kinase M-type (CK-M) and carbonic anhydrase 3 (CA-3), were higher during ER + RT than during ER (P < 0.05). In addition, the synthetic rates of CK-M and CA-3 measured in serum correlated with the synthetic rates of proteins obtained via muscle sampling (P < 0.05). This study provides novel data on the skeletal muscle adaptations to RT and dietary protein distribution.
© 2018 The Authors. The Journal of Physiology © 2018 The Physiological Society.

Entities:  

Keywords:  aging; muscle protein synthesis; proteome dynamics

Mesh:

Substances:

Year:  2018        PMID: 29532476      PMCID: PMC5983154          DOI: 10.1113/JP275246

Source DB:  PubMed          Journal:  J Physiol        ISSN: 0022-3751            Impact factor:   5.182


  42 in total

1.  Measurement of protein turnover rates by heavy water labeling of nonessential amino acids.

Authors:  Robert Busch; Yoo-Kyeong Kim; Richard A Neese; Valerie Schade-Serin; Michelle Collins; Mohamad Awada; James L Gardner; Carine Beysen; Michael E Marino; Lisa M Misell; Marc K Hellerstein
Journal:  Biochim Biophys Acta       Date:  2006-01-24

2.  Effect of intake of different dietary protein sources on plasma amino acid profiles at rest and after exercise.

Authors:  Louise M Burke; Julie A Winter; David Cameron-Smith; Marc Enslen; Michelle Farnfield; Jacques Decombaz
Journal:  Int J Sport Nutr Exerc Metab       Date:  2012-07-04       Impact factor: 4.599

3.  Dynamic proteome profiling of individual proteins in human skeletal muscle after a high-fat diet and resistance exercise.

Authors:  Donny M Camera; Jatin G Burniston; Mark A Pogson; William J Smiles; John A Hawley
Journal:  FASEB J       Date:  2017-08-30       Impact factor: 5.191

4.  Measurement of human plasma proteome dynamics with (2)H(2)O and liquid chromatography tandem mass spectrometry.

Authors:  John C Price; William E Holmes; Kelvin W Li; Nicholas A Floreani; Richard A Neese; Scott M Turner; Marc K Hellerstein
Journal:  Anal Biochem       Date:  2011-09-14       Impact factor: 3.365

5.  Effect of food form on postprandial plasma amino acid concentrations in older adults.

Authors:  Travis B Conley; John W Apolzan; Heather J Leidy; Kathryn A Greaves; Eunjung Lim; Wayne W Campbell
Journal:  Br J Nutr       Date:  2011-07       Impact factor: 3.718

6.  Sarcopenic obesity predicts instrumental activities of daily living disability in the elderly.

Authors:  Richard N Baumgartner; Sharon J Wayne; Debra L Waters; Ian Janssen; Dympna Gallagher; John E Morley
Journal:  Obes Res       Date:  2004-12

Review 7.  Weight loss in obese adults 65years and older: a review of the controversy.

Authors:  Debra L Waters; Aimee L Ward; Dennis T Villareal
Journal:  Exp Gerontol       Date:  2013-02-10       Impact factor: 4.032

Review 8.  Sarcopenic obesity: how do we treat it?

Authors:  Matthew F Bouchonville; Dennis T Villareal
Journal:  Curr Opin Endocrinol Diabetes Obes       Date:  2013-10       Impact factor: 3.243

9.  Two weeks of reduced activity decreases leg lean mass and induces "anabolic resistance" of myofibrillar protein synthesis in healthy elderly.

Authors:  Leigh Breen; Keith A Stokes; Tyler A Churchward-Venne; Daniel R Moore; Stephen K Baker; Kenneth Smith; Philip J Atherton; Stuart M Phillips
Journal:  J Clin Endocrinol Metab       Date:  2013-04-15       Impact factor: 5.958

10.  Internal comparison between deuterium oxide (D2O) and L-[ring-13C6] phenylalanine for acute measurement of muscle protein synthesis in humans.

Authors:  Daniel J Wilkinson; Jessica Cegielski; Bethan E Phillips; Catherine Boereboom; Jonathan N Lund; Philip J Atherton; Kenneth Smith
Journal:  Physiol Rep       Date:  2015-07
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  13 in total

Review 1.  The application of stable-isotope tracers to study human musculoskeletal protein turnover: a tale of bag filling and bag enlargement.

Authors:  D Joe Millward; Ken Smith
Journal:  J Physiol       Date:  2018-09-07       Impact factor: 5.182

2.  Recent Advances in the Characterization of Skeletal Muscle and Whole-Body Protein Responses to Dietary Protein and Exercise during Negative Energy Balance.

Authors:  John W Carbone; James P McClung; Stefan M Pasiakos
Journal:  Adv Nutr       Date:  2019-01-01       Impact factor: 8.701

Review 3.  Tracing metabolic flux in vivo: basic model structures of tracer methodology.

Authors:  Il-Young Kim; Sanghee Park; Yeongmin Kim; Hee-Joo Kim; Robert R Wolfe
Journal:  Exp Mol Med       Date:  2022-09-08       Impact factor: 12.153

4.  Mitochondrial ATP synthase β-subunit production rate and ATP synthase specific activity are reduced in skeletal muscle of humans with obesity.

Authors:  Lee Tran; Paul R Langlais; Nyssa Hoffman; Lori Roust; Christos S Katsanos
Journal:  Exp Physiol       Date:  2018-11-12       Impact factor: 2.969

Review 5.  The impact of exercise and nutrition on the regulation of skeletal muscle mass.

Authors:  Chris McGlory; Stephan van Vliet; Tanner Stokes; Bettina Mittendorfer; Stuart M Phillips
Journal:  J Physiol       Date:  2018-08-01       Impact factor: 5.182

6.  Fractional Synthesis Rates of Individual Proteins in Rat Soleus and Plantaris Muscles.

Authors:  Connor A Stead; Stuart J Hesketh; Samuel Bennett; Hazel Sutherland; Jonathan C Jarvis; Paulo J Lisboa; Jatin G Burniston
Journal:  Proteomes       Date:  2020-05-11

Review 7.  Protein Distribution and Muscle-Related Outcomes: Does the Evidence Support the Concept?

Authors:  Joshua L Hudson; Robert E Bergia Iii; Wayne W Campbell
Journal:  Nutrients       Date:  2020-05-16       Impact factor: 5.717

8.  Sex- and age-specific effects of energy intake and physical activity on sarcopenia.

Authors:  Yu Jin Cho; Youn-Hee Lim; Jae Moon Yun; Hyung-Jin Yoon; Minseon Park
Journal:  Sci Rep       Date:  2020-06-17       Impact factor: 4.379

Review 9.  Dietary Protein Requirements in Children: Methods for Consideration.

Authors:  Joshua L Hudson; Jamie I Baum; Eva C Diaz; Elisabet Børsheim
Journal:  Nutrients       Date:  2021-05-05       Impact factor: 5.717

10.  A mycoprotein-based high-protein vegan diet supports equivalent daily myofibrillar protein synthesis rates compared with an isonitrogenous omnivorous diet in older adults: a randomised controlled trial.

Authors:  Alistair J Monteyne; Mandy V Dunlop; David J Machin; Mariana O C Coelho; George F Pavis; Craig Porter; Andrew J Murton; Doaa R Abdelrahman; Marlou L Dirks; Francis B Stephens; Benjamin T Wall
Journal:  Br J Nutr       Date:  2020-11-11       Impact factor: 3.718

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