Enhanced Protein Translation Underlies Improved Metabolic and Physical Adaptations to Different Exercise Training Modes in Young and Old Humans

Cell Metabolism

Volumn 25, Issue 3, 2017, Pages 581-592

  Robinson, Matthew M ^a   Dasari, Surendra ^a   Konopka, Adam R ^a   Johnson, Matthew L ^a   Manjunatha, S ^a   Esponda, Raul Ruiz ^a   Carter, Rickey E ^a   Lanza, Ian R ^a   Nair, K Sreekumaran ^a  

^a MAYO CLINIC   (United States)

Author keywords

aging; exercise; human; insulin clamp; interval; methylation; proteome; skeletal muscle; tracer; transcriptome

Indexed keywords

ANGIOTENSINOGEN; ARGININE TRANSFER RNA; FIBROBLAST GROWTH FACTOR; GLUCOSE; GLYCINE TRANSFER RNA; INSULIN; INTERLEUKIN 10 RECEPTOR; LEUCINE TRANSFER RNA; MESSENGER RNA; METHIONINE TRANSFER RNA; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE; VALINE TRANSFER RNA; VASCULOTROPIN; MUSCLE PROTEIN; PROTEOME;

ADULT; AEROBIC CAPACITY; AEROBIC EXERCISE; AGED; ARTICLE; CARDIORESPIRATORY FITNESS; CLINICAL ARTICLE; CONTROLLED STUDY; DNA METHYLATION; ENERGY EXPENDITURE; EXERCISE INTENSITY; FAT FREE MASS; FEMALE; GENETIC TRANSCRIPTION; GLUCOSE BLOOD LEVEL; GROUPS BY AGE; HUMAN; HUMAN CELL; INSULIN BLOOD LEVEL; INSULIN SENSITIVITY; LEAN BODY WEIGHT; LUNG GAS EXCHANGE; MALE; MITOCHONDRIAL RESPIRATION; MUSCLE MASS; MUSCLE MITOCHONDRION; MUSCLE STRENGTH; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROSPECTIVE STUDY; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; RANDOMIZED CONTROLLED TRIAL; RESISTANCE TRAINING; RNA SEQUENCE; SKELETAL MUSCLE; UPREGULATION; ADAPTATION; ADOLESCENT; AGING; CLINICAL TRIAL; DOWN REGULATION; EXERCISE; FITNESS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHYLATION; MIDDLE AGED; MITOCHONDRION; PHYSIOLOGY; VERY ELDERLY; YOUNG ADULT;

ADAPTATION, PHYSIOLOGICAL; ADOLESCENT; AGED; AGED, 80 AND OVER; AGING; DOWN-REGULATION; EXERCISE; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MALE; METABOLISM; METHYLATION; MIDDLE AGED; MITOCHONDRIA; MUSCLE PROTEINS; MUSCLE, SKELETAL; PHYSICAL FITNESS; PROTEIN BIOSYNTHESIS; PROTEOME; YOUNG ADULT;

EID: 85014576938     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2017.02.009     Document Type: Article

References (33)

1. Anderson, E.J., Lustig, M.E., Boyle, K.E., Woodlief, T.L., Kane, D.A., Lin, C.T., Price, J.W. 3rd, Kang, L., Rabinovitch, P.S., Szeto, H.H., et al. Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J. Clin. Invest. 119 (2009), 573–581.
2. Balagopal, P., Schimke, J.C., Ades, P., Adey, D., Nair, K.S., Age effect on transcript levels and synthesis rate of muscle MHC and response to resistance exercise. Am. J. Physiol. Endocrinol. Metab. 280 (2001), E203–E208.
3. Barrès, R., Yan, J., Egan, B., Treebak, J.T., Rasmussen, M., Fritz, T., Caidahl, K., Krook, A., O'Gorman, D.J., Zierath, J.R., Acute exercise remodels promoter methylation in human skeletal muscle. Cell Metab. 15 (2012), 405–411.
4. Burgomaster, K.A., Howarth, K.R., Phillips, S.M., Rakobowchuk, M., Macdonald, M.J., McGee, S.L., Gibala, M.J., Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans. J. Physiol. 586 (2008), 151–160.
5. Delmonico, M.J., Harris, T.B., Visser, M., Park, S.W., Conroy, M.B., Velasquez-Mieyer, P., Boudreau, R., Manini, T.M., Nevitt, M., Newman, A.B., Goodpaster, B.H., Health, Aging, and Body. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am. J. Clin. Nutr. 90 (2009), 1579–1585.
6. Egan, B., Dowling, P., O'Connor, P.L., Henry, M., Meleady, P., Zierath, J.R., O'Gorman, D.J., 2-D DIGE analysis of the mitochondrial proteome from human skeletal muscle reveals time course-dependent remodelling in response to 14 consecutive days of endurance exercise training. Proteomics 11 (2011), 1413–1428.
7. Fry, C.S., Drummond, M.J., Glynn, E.L., Dickinson, J.M., Gundermann, D.M., Timmerman, K.L., Walker, D.K., Volpi, E., Rasmussen, B.B., Skeletal muscle autophagy and protein breakdown following resistance exercise are similar in younger and older adults. J. Gerontol. A Biol. Sci. Med. Sci. 68 (2013), 599–607.
8. Gillen, J.B., Martin, B.J., MacInnis, M.J., Skelly, L.E., Tarnopolsky, M.A., Gibala, M.J., Twelve weeks of sprint interval training improves indices of cardiometabolic health similar to traditional endurance training despite a five-fold lower exercise volume and time commitment. PLoS ONE, 11, 2016, e0154075.
9. Goodpaster, B.H., Park, S.W., Harris, T.B., Kritchevsky, S.B., Nevitt, M., Schwartz, A.V., Simonsick, E.M., Tylavsky, F.A., Visser, M., Newman, A.B., The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J. Gerontol. A Biol. Sci. Med. Sci. 61 (2006), 1059–1064.
10. Holloszy, J.O., Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J. Biol. Chem. 242 (1967), 2278–2282.
11. Irving, B.A., Short, K.R., Nair, K.S., Stump, C.S., Nine days of intensive exercise training improves mitochondrial function but not insulin action in adult offspring of mothers with type 2 diabetes. J. Clin. Endocrinol. Metab. 96 (2011), E1137–E1141.
12. Irving, B.A., Lanza, I.R., Henderson, G.C., Rao, R.R., Spiegelman, B.M., Nair, K.S., Combined training enhances skeletal muscle mitochondrial oxidative capacity independent of age. J. Clin. Endocrinol. Metab. 100 (2015), 1654–1663.
13. Karakelides, H., Irving, B.A., Short, K.R., O'Brien, P., Nair, K.S., Age, obesity, and sex effects on insulin sensitivity and skeletal muscle mitochondrial function. Diabetes 59 (2010), 89–97.
14. Konopka, A.R., Asante, A., Lanza, I.R., Robinson, M.M., Johnson, M.L., Dalla Man, C., Cobelli, C., Amols, M.H., Irving, B.A., Nair, K.S., Defects in mitochondrial efficiency and H2O2 emissions in obese women are restored to a lean phenotype with aerobic exercise training. Diabetes 64 (2015), 2104–2115.
15. Lalia, A.Z., Johnson, M.L., Jensen, M.D., Hames, K.C., Port, J.D., Lanza, I.R., Effects of dietary n-3 fatty acids on hepatic and peripheral insulin sensitivity in insulin-resistant humans. Diabetes Care 38 (2015), 1228–1237.
16. Lanza, I.R., Nair, K.S., Functional assessment of isolated mitochondria in vitro. Methods Enzymol. 457 (2009), 349–372.
17. Lanza, I.R., Short, D.K., Short, K.R., Raghavakaimal, S., Basu, R., Joyner, M.J., McConnell, J.P., Nair, K.S., Endurance exercise as a countermeasure for aging. Diabetes 57 (2008), 2933–2942.
18. Lanza, I.R., Zabielski, P., Klaus, K.A., Morse, D.M., Heppelmann, C.J., Bergen, H.R. 3rd, Dasari, S., Walrand, S., Short, K.R., Johnson, M.L., et al. Chronic caloric restriction preserves mitochondrial function in senescence without increasing mitochondrial biogenesis. Cell Metab. 16 (2012), 777–788.
19. Louis, E., Raue, U., Yang, Y., Jemiolo, B., Trappe, S., Time course of proteolytic, cytokine, and myostatin gene expression after acute exercise in human skeletal muscle. J. Appl. Physiol. 103 (2007), 1744–1751.
20. MacInnis, M.J., Zacharewicz, E., Martin, B.J., Haikalis, M.E., Skelly, L.E., Tarnopolsky, M.A., Murphy, R.M., Gibala, M.J., Superior mitochondrial adaptations in human skeletal muscle after interval compared to continuous single-leg cycling matched for total work. J. Physiol., 2016, 10.1113/JP272570 Published online July 11, 2016.
21. Martin, D.R., Dutta, P., Mahajan, S., Varma, S., Stevens, S.M. Jr., Structural and activity characterization of human PHPT1 after oxidative modification. Sci. Rep., 6, 2016, 23658.
22. Miller, B.F., Konopka, A.R., Hamilton, K.L., The rigorous study of exercise adaptations: why mRNA might not be enough. J. Appl. Physiol. 121 (2016), 594–596.
23. Myers, J., Prakash, M., Froelicher, V., Do, D., Partington, S., Atwood, J.E., Exercise capacity and mortality among men referred for exercise testing. N. Engl. J. Med. 346 (2002), 793–801.
24. Nair, K.S., Rizza, R.A., O'Brien, P., Dhatariya, K., Short, K.R., Nehra, A., Vittone, J.L., Klee, G.G., Basu, A., Basu, R., et al. DHEA in elderly women and DHEA or testosterone in elderly men. N. Engl. J. Med. 355 (2006), 1647–1659.
25. Neufer, P.D., Bamman, M.M., Muoio, D.M., Bouchard, C., Cooper, D.M., Goodpaster, B.H., Booth, F.W., Kohrt, W.M., Gerszten, R.E., Mattson, M.P., et al. Understanding the cellular and molecular mechanisms of physical activity-induced health benefits. Cell Metab. 22 (2015), 4–11.
26. Nitert, M.D., Dayeh, T., Volkov, P., Elgzyri, T., Hall, E., Nilsson, E., Yang, B.T., Lang, S., Parikh, H., Wessman, Y., et al. Impact of an exercise intervention on DNA methylation in skeletal muscle from first-degree relatives of patients with type 2 diabetes. Diabetes 61 (2012), 3322–3332.
27. Petersen, K.F., Befroy, D., Dufour, S., Dziura, J., Ariyan, C., Rothman, D.L., DiPietro, L., Cline, G.W., Shulman, G.I., Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 300 (2003), 1140–1142.
28. Rizza, R.A., Mandarino, L.J., Gerich, J.E., Dose-response characteristics for effects of insulin on production and utilization of glucose in man. Am. J. Physiol. 240 (1981), E630–E639.
29. Rooyackers, O.E., Adey, D.B., Ades, P.A., Nair, K.S., Effect of age on in vivo rates of mitochondrial protein synthesis in human skeletal muscle. Proc. Natl. Acad. Sci. USA 93 (1996), 15364–15369.
30. Ross, R., de Lannoy, L., Stotz, P.J., Separate effects of intensity and amount of exercise on interindividual cardiorespiratory fitness response. Mayo Clin. Proc. 90 (2015), 1506–1514.
31. Short, K.R., Vittone, J.L., Bigelow, M.L., Proctor, D.N., Rizza, R.A., Coenen-Schimke, J.M., Nair, K.S., Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity. Diabetes 52 (2003), 1888–1896.
32. Short, K.R., Bigelow, M.L., Kahl, J., Singh, R., Coenen-Schimke, J., Raghavakaimal, S., Nair, K.S., Decline in skeletal muscle mitochondrial function with aging in humans. Proc. Natl. Acad. Sci. USA 102 (2005), 5618–5623.
33. Simoneau, J.A., Kelley, D.E., Altered glycolytic and oxidative capacities of skeletal muscle contribute to insulin resistance in NIDDM. J. Appl. Physiol. 83 (1997), 166–171.