Effect of dietary n-3 PUFA supplementation on the muscle transcriptome in older adults

Physiological Reports

Volumn 4, Issue 11, 2016, Pages

  Yoshino, Jun ^a   Smith, Gordon I ^a   Kelly, Shannon C ^a   Julliand, Sophie ^a   Reeds, Dominic N ^a   Mittendorfer, Bettina ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; fish oil; gene expression; hypertrophy; sarcopenia

Indexed keywords

OMEGA 3 FATTY ACID; TRANSCRIPTOME;

AGED; CONTROLLED STUDY; DIETARY SUPPLEMENT; DRUG EFFECTS; FEMALE; GENE EXPRESSION PROFILING; HUMAN; MALE; METABOLISM; MUSCLE MITOCHONDRION; MUSCLE STRENGTH; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL; SKELETAL MUSCLE; TREATMENT OUTCOME;

AGED; DIETARY SUPPLEMENTS; FATTY ACIDS, OMEGA-3; FEMALE; GENE EXPRESSION PROFILING; HUMANS; MALE; MITOCHONDRIA, MUSCLE; MUSCLE STRENGTH; MUSCLE, SKELETAL; TRANSCRIPTOME; TREATMENT OUTCOME;

EID: 84974853411     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12785     Document Type: Article

References (49)

1. Baillie, R. A., R. Takada, M. Nakamura, and S. D. Clarke. 1999. Coordinate induction of peroxisomal acyl-CoA oxidase and UCP-3 by dietary fish oil: a mechanism for decreased body fat deposition. Prostaglandins Leukot. Essent. Fatty Acids 60:351–356.
2. Barbieri, E., D. Agostini, E. Polidori, L. Potenza, M. Guescini, F. Lucertini, et al. 2015. The pleiotropic effect of physical exercise on mitochondrial dynamics in aging skeletal muscle. Oxid. Med. Cell Longev. 2015:917085.
3. ten Broek, R. W., S. Grefte, and J. W. von den Hoff. 2010. Regulatory factors and cell populations involved in skeletal muscle regeneration. J. Cell. Physiol. 224:7–16.
4. Broekhuizen, R., E. F. Wouters, E. C. Creutzberg, C. A. Weling-Scheepers, and A. M. Schols. 2005. Polyunsaturated fatty acids improve exercise capacity in chronic obstructive pulmonary disease. Thorax 60:376–382.
5. Brown, M., D. R. Sinacore, E. F. Binder, and W. M. Kohrt. 2000. Physical and performance measures for the identification of mild to moderate frailty. J. Gerontol. A Biol. Sci. Med. Sci. 55:M350–M355.
6. Castillero, E., A. I. Martin, M. Lopez-Menduina, M. A. Villanua, and A. Lopez-Calderon. 2009. Eicosapentaenoic acid attenuates arthritis-induced muscle wasting acting on atrogin-1 and on myogenic regulatory factors. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297:R1322–R1331.
7. Cros, N., A. V. Tkatchenko, D. F. Pisani, L. Leclerc, J. J. Leger, J. F. Marini, et al. 2001. Analysis of altered gene expression in rat soleus muscle atrophied by disuse. J. Cell. Biochem. 83:508–519.
8. Dahiya, S., S. Bhatnagar, S. M. Hindi, C. Jiang, P. K. Paul, S. Kuang, et al. 2011. Elevated levels of active matrix metalloproteinase-9 cause hypertrophy in skeletal muscle of normal and dystrophin-deficient mdx mice. Hum. Mol. Genet. 20:4345–4359.
9. Fabbrini, E., J. Yoshino, M. Yoshino, F. Magkos, C. Tiemann Luecking, D. Samovski, et al. 2015. Metabolically normal obese people are protected from adverse effects following weight gain. J. Clin. Invest. 125:787–795.
10. Folch, J., M. Lees, and G. H. Sloane Stanley. 1957. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226:497–509.
11. Hagopian, K., K. L. Weber, D. T. Hwee, A. L. van Eenennaam, G. Lopez-Lluch, J. M. Villalba, et al. 2010. Complex I-associated hydrogen peroxide production is decreased and electron transport chain enzyme activities are altered in n-3 enriched fat-1 mice. PLoS ONE 5:e12696.
12. Hepple, R. T. 2014. Mitochondrial involvement and impact in aging skeletal muscle. Front. Aging Neurosci. 6:211.
13. Herbst, E. A., S. Paglialunga, C. Gerling, J. Whitfield, K. Mukai, A. Chabowski, et al. 2014. Omega-3 supplementation alters mitochondrial membrane composition and respiration kinetics in human skeletal muscle. J. Physiol. 592:1341–1352.
14. Hinds, S., W. Bian, R. G. Dennis, and N. Bursac. 2011. The role of extracellular matrix composition in structure and function of bioengineered skeletal muscle. Biomaterials 32:3575–3583.
15. Hiona, A., and C. Leeuwenburgh. 2008. The role of mitochondrial DNA mutations in aging and sarcopenia: implications for the mitochondrial vicious cycle theory of aging. Exp. Gerontol. 43:24–33.
16. Huang, F., H. Wei, H. Luo, S. Jiang, and J. Peng. 2011. EPA inhibits the inhibitor of kappaBalpha (IkappaBalpha)/NF-kappaB/muscle RING finger 1 pathway in C2C12 myotubes in a PPARgamma-dependent manner. Br. J. Nutr. 105:348–356.
17. Hyldahl, R. D., B. Nelson, L. Xin, T. Welling, L. Groscost, M. J. Hubal, et al. 2015. Extracellular matrix remodeling and its contribution to protective adaptation following lengthening contractions in human muscle. FASEB J. 29:2894–2904.
18. Ibebunjo, C., J. M. Chick, T. Kendall, J. K. Eash, C. Li, Y. Zhang, et al. 2013. Genomic and proteomic profiling reveals reduced mitochondrial function and disruption of the neuromuscular junction driving rat sarcopenia. Mol. Cell. Biol. 33:194–212.
19. Johnson, M. L., A. Z. Lalia, S. Dasari, M. Pallauf, M. Fitch, M. K. Hellerstein, et al. 2015. Eicosapentaenoic acid but not docosahexaenoic acid restores skeletal muscle mitochondrial oxidative capacity in old mice. Aging Cell 14:734–743.
20. Kawabata, F., M. Neya, K. Hamazaki, Y. Watanabe, S. Kobayashi, and T. Tsuji. 2014. Supplementation with eicosapentaenoic acid-rich fish oil improves exercise economy and reduces perceived exertion during submaximal steady-state exercise in normal healthy untrained men. Biosci. Biotechnol. Biochem. 78:2081–2088.
21. Kim, S. Y., and D. J. Volsky. 2005. PAGE: parametric analysis of gene set enrichment. BMC Bioinformatics 6:144.
22. Lanza, I. R., A. Blachnio-Zabielska, M. L. Johnson, J. M. Schimke, D. R. Jakaitis, N. K. Lebrasseur, et al. 2013. Influence of fish oil on skeletal muscle mitochondrial energetics and lipid metabolites during high-fat diet. Am. J. Physiol. Endocrinol. Metab. 304:E1391–E1403.
23. Lecker, S. H., R. T. Jagoe, A. Gilbert, M. Gomes, V. Baracos, J. Bailey, et al. 2004. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 18:39–51.
24. Liu, Y., F. Chen, J. Odle, X. Lin, H. Zhu, H. Shi, et al. 2013. Fish oil increases muscle protein mass and modulates Akt/FOXO, TLR4, and NOD signaling in weanling piglets after lipopolysaccharide challenge. J. Nutr. 143:1331–1339.
25. Lukashev, M. E., and Z. Werb. 1998. ECM signalling: orchestrating cell behaviour and misbehaviour. Trends Cell Biol. 8:437–441.
26. Mizunoya, W., Y. Iwamoto, B. Shirouchi, M. Sato, Y. Komiya, F. R. Razin, et al. 2013. Dietary fat influences the expression of contractile and metabolic genes in rat skeletal muscle. PLoS ONE 8:e80152.
27. Ogasawara, R., K. Nakazato, K. Sato, M. D. Boppart, and S. Fujita. 2014. Resistance exercise increases active MMP and beta1-integrin protein expression in skeletal muscle. Physiol. Rep. 2:e12212.
28. Osses, N., and E. Brandan. 2002. ECM is required for skeletal muscle differentiation independently of muscle regulatory factor expression. Am. J. Physiol. Cell Physiol. 282:C383–C394.
29. Peoples, G. E., and P. L. McLennan. 2010. Dietary fish oil reduces skeletal muscle oxygen consumption, provides fatigue resistance and improves contractile recovery in the rat in vivo hindlimb. Br. J. Nutr. 104:1771–1779.
30. Peoples, G. E., and P. L. McLennan. 2014. Long-chain n-3 DHA reduces the extent of skeletal muscle fatigue in the rat in vivo hindlimb model. Br. J. Nutr. 111:996–1003.
31. Peoples, G. E., P. L. McLennan, P. R. Howe, and H. Groeller. 2008. Fish oil reduces heart rate and oxygen consumption during exercise. J. Cardiovasc. Pharmacol. 52:540–547.
32. Philp, L. K., L. K. Hellborn, A. Janovska, and G. A. Wittert. 2015. Dietary enrichment with fish oil prevents high fat-induced metabolic dysfunction in skeletal muscle in mice. PLoS ONE 10:e0117494.
33. Rodacki, C. L., A. L. Rodacki, G. Pereira, K. Naliwaiko, I. Coelho, D. Pequito, et al. 2012. Fish-oil supplementation enhances the effects of strength training in elderly women. Am. J. Clin. Nutr. 95:428–436.
34. Smith, H. J., S. M. Wyke, and M. J. Tisdale. 2004. Mechanism of the attenuation of proteolysis-inducing factor stimulated protein degradation in muscle by beta-hydroxy-beta-methylbutyrate. Cancer Res. 64:8731–8735.
35. Smith, H. J., J. Khal, and M. J. Tisdale. 2005. Downregulation of ubiquitin-dependent protein degradation in murine myotubes during hyperthermia by eicosapentaenoic acid. Biochem. Biophys. Res. Commun. 332:83–88.
36. Smith, G. I., P. Atherton, D. N. Reeds, B. S. Mohammed, D. Rankin, M. J. Rennie, et al. 2011a. Dietary omega-3 fatty acid supplementation increases the rate of muscle protein synthesis in older adults: a randomized controlled trial. Am. J. Clin. Nutr. 93:402–412.
37. Smith, G. I., P. Atherton, D. N. Reeds, B. S. Mohammed, D. Rankin, M. J. Rennie, et al. 2011b. 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. 121:267–278.
38. Smith, G. I., J. Yoshino, D. N. Reeds, D. Bradley, R. E. Burrows, H. D. Heisey, et al. 2014. Testosterone and progesterone, but not estradiol, stimulate muscle protein synthesis in postmenopausal women. J. Clin. Endocrinol. Metab. 99:256–265.
39. Smith, G. I., S. Julliand, D. N. Reeds, D. R. Sinacore, S. Klein, and B. Mittendorfer. 2015. Fish oil-derived n-3 PUFA therapy increases muscle mass and function in healthy older adults. Am. J. Clin. Nutr. 102:115–122.
40. Supinski, G. S., J. Vanags, and L. A. Callahan. 2010. Eicosapentaenoic acid preserves diaphragm force generation following endotoxin administration. Crit. Care 14:R35.
41. Thomas, K., A. J. Engler, and G. A. Meyer. 2015. Extracellular matrix regulation in the muscle satellite cell niche. Connect. Tissue Res. 56:1–8.
42. Urso, M. L., A. G. Scrimgeour, Y. W. Chen, P. D. Thompson, and P. M. Clarkson. 2006. Analysis of human skeletal muscle after 48 h immobilization reveals alterations in mRNA and protein for extracellular matrix components. J. Appl. Physiol. 101:1136–1148.
43. Vaughan, R. A., R. Garcia-Smith, M. Bisoffi, C. A. Conn, and K. A. Trujillo. 2012. Conjugated linoleic acid or omega 3 fatty acids increase mitochondrial biosynthesis and metabolism in skeletal muscle cells. Lipids Health Dis. 11:142.
44. Whitehouse, A. S., and M. J. Tisdale. 2001. Downregulation of ubiquitin-dependent proteolysis by eicosapentaenoic acid in acute starvation. Biochem. Biophys. Res. Commun. 285:598–602.
45. Whitehouse, A. S., H. J. Smith, J. L. Drake, and M. J. Tisdale. 2001. Mechanism of attenuation of skeletal muscle protein catabolism in cancer cachexia by eicosapentaenoic acid. Cancer Res. 61:3604–3609.
46. Whitehouse, A. S., J. Khal, and M. J. Tisdale. 2003. Induction of protein catabolism in myotubes by 15(S)-hydroxyeicosatetraenoic acid through increased expression of the ubiquitin-proteasome pathway. Br. J. Cancer 89:737–745.
47. Yoshino, J., K. F. Mills, M. J. Yoon, and S. Imai. 2011. Nicotinamide mononucleotide, a key NAD(+) intermediate, treats the pathophysiology of diet- and age-induced diabetes in mice. Cell Metab. 14:528–536.
48. Yoshino, J., P. Almeda-Valdes, B. W. Patterson, A. L. Okunade, S. Imai, B. Mittendorfer, et al. 2014. Diurnal variation in insulin sensitivity of glucose metabolism is associated with diurnal variations in whole-body and cellular fatty acid metabolism in metabolically normal women. J. Clin. Endocrinol. Metab. 99:E1666–E1670.
49. Zhang, Q., S. K. Joshi, D. H. Lovett, B. Zhang, S. Bodine, H. T. Kim, et al. 2015. Matrix metalloproteinase-2 plays a critical role in overload induced skeletal muscle hypertrophy. Muscles Ligaments Tendons J. 4:446–454.