Eicosapentaenoic acid but not docosahexaenoic acid restores skeletal muscle mitochondrial oxidative capacity in old mice

Aging Cell

Volumn 14, Issue 5, 2015, Pages 734-743

  Johnson, Matthew L ^a   Lalia, Antigoni Z ^a   Dasari, Surendra ^a   Pallauf, Maximilian ^a   Fitch, Mark ^b   Hellerstein, Marc K ^b   Lanza, Ian R ^a  

^a Mayo Clinic   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aging; Docosahexaenoic acid; Eicosapentaenoic acid; Mitochondria; Omega 3; Proteomics; Sarcopenia

Indexed keywords

DOCOSAHEXAENOIC ACID; ICOSAPENTAENOIC ACID; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); RETINOID X RECEPTOR; SUCCINATE DEHYDROGENASE (UBIQUINONE);

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTICOAGULATION; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BIOGENESIS; CARBAMOYLATION; CONTROLLED STUDY; DEAMINATION; DIET SUPPLEMENTATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MOUSE; MUSCLE MITOCHONDRION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; PROTEOMICS; QUADRICEPS FEMORIS MUSCLE; RNA SEQUENCE; AGING; ANIMAL; C57BL MOUSE; CYTOLOGY; DRUG EFFECTS; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; SKELETAL MUSCLE;

AGING; ANIMALS; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUSCLE, SKELETAL; OXIDATION-REDUCTION;

EID: 84940897515     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12352     Document Type: Article

References (44)

1. Balagopal P, Rooyackers OE, Adey DB, Ades PA, Nair KS (1997) Effects of aging on in vivo synthesis of skeletal muscle myosin heavy-chain and sarcoplasmic protein in humans. Am. J. Physiol. 273, E790-E800.
2. Balagopal P, Schimke JC, Ades P, Adey D, Nair KS (2001) Age effect on transcript levels and synthesis rate of muscle MHC and response to resistance exercise. Am. J. Physiol. Endocrinol. Metab. 280, E203-E208.
3. Belcastro AN, Arthur GD, Albisser TA, Raj DA (1996) Heart, liver, and skeletal muscle myeloperoxidase activity during exercise. J. Appl. Physiol. Bethesda Md 1985 80, 1331-1335.
4. Coggan AR, Spina RJ, King DS, Rogers MA, Brown M, Nemeth PM, Holloszy JO (1992) Skeletal muscle adaptations to endurance training in 60- to 70-yr-old men and women. J. Appl. Physiol. Bethesda Md 1985 72, 1780-1786.
5. Conley KE, Jubrias SA, Esselman PC (2000) Oxidative capacity and ageing in human muscle. J. Physiol. 526, 203-210.
6. Desvergne B, Wahli W (1999) Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr. Rev. 20, 649-688.
7. Feng J, Xie H, Meany DL, Thompson LV, Arriaga EA, Griffin TJ (2008) Quantitative proteomic profiling of muscle type-dependent and age-dependent protein carbonylation in rat skeletal muscle mitochondria. J. Gerontol. A Biol. Sci. Med. Sci. 63, 1137-1152.
8. Flachs P, Horakova O, Brauner P, Rossmeisl M, Pecina P, Franssen-van Hal N, Ruzickova J, Sponarova J, Drahota Z, Vlcek C, Keijer J, Houstek J, Kopecky J (2005) Polyunsaturated fatty acids of marine origin upregulate mitochondrial biogenesis and induce beta-oxidation in white fat. Diabetologia 48, 2365-2375.
9. Franceschi C, Campisi J (2014) Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. J. Gerontol. A Biol. Sci. Med. Sci. 69(Suppl 1), S4-S9.
10. Fry CS, Drummond MJ, Glynn EL, Dickinson JM, Gundermann DM, Timmerman KL, Walker DK, Dhanani S, Volpi E, Rasmussen BB (2011) Aging impairs contraction-induced human skeletal muscle mTORC1 signaling and protein synthesis. Skelet Muscle 1, 11.
11. Gouspillou G, Sgarioto N, Kapchinsky S, Purves-Smith F, Norris B, Pion CH, Barbat-Artigas S, Lemieux F, Taivassalo T, Morais JA, Aubertin-Leheudre M, Hepple RT (2014) Increased sensitivity to mitochondrial permeability transition and myonuclear translocation of endonuclease G in atrophied muscle of physically active older humans. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 28, 1621-1633.
12. Hasten DL, Pak-Loduca J, Obert KA, Yarasheski KE (2000) Resistance exercise acutely increases MHC and mixed muscle protein synthesis rates in 78-84 and 23-32 yr olds. Am. J. Physiol. Endocrinol. Metab. 278, E620-E626.
13. Henderson GC, Dhatariya K, Ford GC, Klaus KA, Basu R, Rizza RA, Jensen MD, Khosla S, O'Brien P, Nair KS (2008) Higher muscle protein synthesis in women than men across the lifespan, and failure of androgen administration to amend age-related decrements. FASEB J. 23, 631-641.
14. Hepple RT, Qin M, Nakamoto H, Goto S (2008) Caloric restriction optimizes the proteasome pathway with aging in rat plantaris muscle: implications for sarcopenia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R1231-R1237.
15. Herbst EAF, Paglialunga S, Gerling C, Whitfield J, Mukai K, Chabowski A, Heigenhauser GJF, Spriet LL, Holloway GP (2014) Omega-3 supplementation alters mitochondrial membrane composition and respiration kinetics in human skeletal muscle. J. Physiol. 592, 1341-1352.
16. Hütter E, Skovbro M, Lener B, Prats C, Rabøl R, Dela F, Jansen-Dürr P (2007) Oxidative stress and mitochondrial impairment can be separated from lipofuscin accumulation in aged human skeletal muscle. Aging Cell 6, 245-256.
17. Jeng J-Y, Lee W-H, Tsai Y-H, Chen C-Y, Chao S-Y, Hsieh R-H (2009) Functional modulation of mitochondria by eicosapentaenoic acid provides protection against ceramide toxicity to C6 glioma cells. J. Agric. Food Chem. 57, 11455-11462.
18. Jubrias SA, Esselman PC, Price LB, Cress ME, Conley KE (2001) Large energetic adaptations of elderly muscle to resistance and endurance training. J. Appl. Physiol. Bethesda Md 1985 90, 1663-1670.
19. Kalari KR, Nair AA, Bhavsar JD, O'Brien DR, Davila JI, Bockol MA, Nie J, Tang X, Baheti S, Doughty JB, Middha S, Sicotte H, Thompson AE, Asmann YW, Kocher J-PA (2014) MAP-RSeq: mayo analysis pipeline for RNA sequencing. BMC Bioinformatics 15, 224.
20. Kamolrat T, Gray SR (2013) The effect of eicosapentaenoic and docosahexaenoic acid on protein synthesis and breakdown in murine C2C12 myotubes. Biochem. Biophys. Res. Commun. 432, 593-598.
21. Khairallah RJ, Kim J, O'Shea KM, O'Connell KA, Brown BH, Galvao T, Daneault C, Des Rosiers C, Polster BM, Hoppel CL, Stanley WC (2012) Improved mitochondrial function with diet-induced increase in either docosahexaenoic acid or arachidonic acid in membrane phospholipids. PLoS ONE 7, e34402.
22. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36.
23. Kosek DJ, Kim J-S, Petrella JK, Cross JM, Bamman MM (2006) Efficacy of 3 days/wk resistance training on myofiber hypertrophy and myogenic mechanisms in young vs. older adults. J. Appl. Physiol. Bethesda Md 1985 101, 531-544.
24. Kumar V, Selby A, Rankin D, Patel R, Atherton P, Hildebrandt W, Williams J, Smith K, Seynnes O, Hiscock N, Rennie MJ (2009) Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. J. Physiol. 587, 211-217.
25. Lanza IR, Nair KS (2009) Functional assessment of isolated mitochondria in vitro. Methods Enzymol. 457, 349-372.
26. Lanza IR, Short DK, Short KR, Raghavakaimal S, Basu R, Joyner MJ, McConnell JP, Nair KS (2008) Endurance exercise as a countermeasure for aging. Diabetes 57, 2933-2942.
27. Lanza IR, Zabielski P, Klaus KA, Morse DM, Heppelmann CJ, Bergen HR 3rd, Dasari S, Walrand S, Short KR, Johnson ML, Robinson MM, Schimke JM, Jakaitis DR, Asmann YW, Sun Z, Nair KS (2012) Chronic caloric restriction preserves mitochondrial function in senescence without increasing mitochondrial biogenesis. Cell Metab. 16, 777-788.
28. Lanza IR, Blachnio-Zabielska A, Johnson ML, Schimke JM, Jakaitis DR, Lebrasseur NK, Jensen MD, Sreekumaran Nair K, Zabielski P (2013) Influence of fish oil on skeletal muscle mitochondrial energetics and lipid metabolites during high-fat diet. AJP Endocrinol. Metab. 304, E1391-E1403.
29. Leenders M, Verdijk LB, van der Hoeven L, van Kranenburg J, Nilwik R, van Loon LJC (2013) Elderly men and women benefit equally from prolonged resistance-type exercise training. J. Gerontol. A Biol. Sci. Med. Sci. 68, 769-779.
30. Menshikova EV, Ritov VB, Fairfull L, Ferrell RE, Kelley DE, Goodpaster BH (2006) Effects of exercise on mitochondrial content and function in aging human skeletal muscle. J. Gerontol. A Biol. Sci. Med. Sci. 61, 534-540.
31. Picard M, Ritchie D, Thomas MM, Wright KJ, Hepple RT (2011) Alterations in intrinsic mitochondrial function with aging are fiber type-specific and do not explain differential atrophy between muscles. Aging Cell 10, 1047-1055.
32. Proctor DN, Joyner MJ (1997) Skeletal muscle mass and the reduction of VO2max in trained older subjects. J. Appl. Physiol. Bethesda Md 1985 82, 1411-1415.
33. Rahman MM, Bhattacharya A, Fernandes G (2008) Docosahexaenoic acid is more potent inhibitor of osteoclast differentiation in RAW 264.7 cells than eicosapentaenoic acid. J. Cell. Physiol. 214, 201-209.
34. Richard D, Kefi K, Barbe U, Bausero P, Visioli F (2008) Polyunsaturated fatty acids as antioxidants. Pharmacol. Res. Off. J. Ital. Pharmacol. Soc. 57, 451-455.
35. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinforma. Oxf. Engl. 26, 139-140.
36. Short KR, Vittone JL, Bigelow ML, Proctor DN, Rizza RA, Coenen-Schimke JM, Nair KS (2003) Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity. Diabetes 52, 1888-1896.
37. Short KR, Bigelow ML, Kahl J, Singh R, Coenen-Schimke J, Raghavakaimal S, Nair KS (2005) Decline in skeletal muscle mitochondrial function with aging in humans. Proc. Natl Acad. Sci. U. S. A. 102, 5618-5623.
38. Siegel MP, Kruse SE, Percival JM, Goh J, White CC, Hopkins HC, Kavanagh TJ, Szeto HH, Rabinovitch PS, Marcinek DJ (2013) Mitochondrial-targeted peptide rapidly improves mitochondrial energetics and skeletal muscle performance in aged mice. Aging Cell 12, 763-771.
39. Smith GI, Atherton P, Reeds DN, Mohammed BS, Rankin D, Rennie MJ, Mittendorfer B (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.
40. Smith GI, Atherton P, Reeds DN, Mohammed BS, Rankin D, Rennie MJ, Mittendorfer B (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.
41. Tiidus PM, Bombardier E (1999) Oestrogen attenuates post-exercise myeloperoxidase activity in skeletal muscle of male rats. Acta Physiol. Scand. 166, 85-90.
42. Wang Z, Nicholls SJ, Rodriguez ER, Kummu O, Hörkkö S, Barnard J, Reynolds WF, Topol EJ, DiDonato JA, Hazen SL (2007) Protein carbamylation links inflammation, smoking, uremia and atherogenesis. Nat. Med. 13, 1176-1184.
43. Wang Y, Lin Q, Zheng P, Zhang J, Huang F (2013) DHA inhibits protein degradation more efficiently than EPA by regulating the PPARγ/NFκB pathway in C2C12 myotubes. BioMed Res. Int. 2013, 318981.
44. Yamaoka S, Urade R, Kito M (1988) Mitochondrial function in rats is affected by modification of membrane phospholipids with dietary sardine oil. J. Nutr. 118, 290-296.